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Critical Reviews in Biochemistry and Molecular Biology Volume 53, 2018 - Issue 6
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Review Article

Rab-dependent cellular trafficking and amyotrophic lateral sclerosis

S. ParakhFaculty of Medicine and Health Sciences, Department of Biomedical Sciences, Centre for MND Research, Macquarie University, Sydney, Australia; ;Department of Biochemistry and Genetics, La Trobe Institute for Molecular Science, La Trobe University, Melbourne, AustraliaView further author information
,
E. R. PerriFaculty of Medicine and Health Sciences, Department of Biomedical Sciences, Centre for MND Research, Macquarie University, Sydney, Australia; ;Department of Biochemistry and Genetics, La Trobe Institute for Molecular Science, La Trobe University, Melbourne, AustraliaView further author information
,
C. J. JagarajFaculty of Medicine and Health Sciences, Department of Biomedical Sciences, Centre for MND Research, Macquarie University, Sydney, Australia; View further author information
,
A. M. G. RagagninFaculty of Medicine and Health Sciences, Department of Biomedical Sciences, Centre for MND Research, Macquarie University, Sydney, Australia; View further author information
&
J. D. AtkinFaculty of Medicine and Health Sciences, Department of Biomedical Sciences, Centre for MND Research, Macquarie University, Sydney, Australia; ;Department of Biochemistry and Genetics, La Trobe Institute for Molecular Science, La Trobe University, Melbourne, AustraliaCorrespondence[email protected]
View further author information
Pages 623-651 | Received 26 Aug 2018, Accepted 27 Nov 2018, Published online: 11 Feb 2019

References

  • Al ‐Saif A, Al ‐Mohanna F, Bohlega S. 2011. A mutation in sigma‐1 receptor causes juvenile amyotrophic lateral sclerosis. Ann Neurol. 70:913–919.
  • Alami NH, Smith RB, Carrasco MA, Williams LA, Winborn CS, Han SSW, Kiskinis E, Winborn B, Freibaum BD, Kanagaraj A, et al. 2014. Axonal transport of TDP-43 mRNA granules is impaired by ALS-causing mutations. Neuron. 81:536–543.
  • Almanza A, Carlesso A, Chintha C, Creedican S, Doultsinos D, Leuzzi B, Luís A, McCarthy N, Montibeller L, More S. 2018. Endoplasmic reticulum stress signalling–from basic mechanisms to clinical applications. FEBS J.
  • Andersen PM, Sims KB, Xin WW, Kiely R, O'Neill G, Ravits J, Pioro E, Harati Y, Brower RD, Levine JS, et al. 2003. Sixteen novel mutations in the Cu/Zn superoxide dismutase gene in amyotrophic lateral sclerosis: a decade of discoveries, defects and disputes. Amyotroph Lateral Scl Other Motor Neuron Disord. 4:62–73.
  • Aoki Y, Manzano R, Lee Y, Dafinca R, Aoki M, Douglas AGL, Varela MA, Sathyaprakash C, Scaber J, Barbagallo P, et al. 2017. C9orf72 and RAB7L1 regulate vesicle trafficking in amyotrophic lateral sclerosis and frontotemporal dementia. Brain. 140:887–897.
  • Arai T, Hasegawa M, Akiyama H, Ikeda K, Nonaka T, Mori H, Mann D, Tsuchiya K, Yoshida M, Hashizume Y, et al. 2006. TDP-43 is a component of ubiquitin-positive tau-negative inclusions in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Biochem Biophys Res Commun. 351:602–611.
  • Aridor M. 2018. COPII gets in shape: lessons derived from morphological aspects of early secretion. Traffic. 19:823–839.
  • Arimura N, Kimura T, Nakamuta S, Taya S, Funahashi Y, Hattori A, Shimada A, Menager C, Kawabata S, Fujii K, et al. 2009. Anterograde transport of TrkB in axons is mediated by direct interaction with Slp1 and Rab27. Dev Cell. 16:675–686.
  • Atkin JD, Farg MA, Soo KY, Walker AK, Halloran M, Turner BJ, Nagley P, Horne MK. 2014. Mutant SOD 1 inhibits ER‐Golgi transport in amyotrophic lateral sclerosis. J Neurochem. 129:190–204.
  • Atsumi T. 1981. The ultrastructure of intramuscular nerves in amyotrophic lateral sclerosis. Acta neuropathologica. 55:193–198.
  • Bannwarth S, Ait-El-Mkadem S, Chaussenot A, Genin EC, Lacas-Gervais S, Fragaki K, Berg-Alonso L, Kageyama Y, Serre V, Moore DG, et al. 2014. A mitochondrial origin for frontotemporal dementia and amyotrophic lateral sclerosis through CHCHD10 involvement. Brain. 137:2329–2345.
  • Barmada SJ, Serio A, Arjun A, Bilican B, Daub A, Ando DM, Tsvetkov A, Pleiss M, Li X, Peisach D, et al. 2014. Autophagy induction enhances TDP43 turnover and survival in neuronal ALS models. Nat Chem Biol. 10:677.
  • Barr F, Lambright DG. 2010. Rab gefs and gaps. Curr Opin Cell Biol. 22:461–470.
  • Barrett EF, Barrett JN, David G. 2014. Dysfunctional mitochondrial Ca(2+) handling in mutant SOD1 mouse models of fALS: integration of findings from motor neuron somata and motor terminals. Front Cell Neurosci. 8:184.
  • Bartolome F, Wu H-C, Burchell VS, Preza E, Wray S, Mahoney CJ, Fox NC, Calvo A, Canosa A, Moglia C, et al. 2013. Pathogenic VCP mutations induce mitochondrial uncoupling and reduced ATP levels. Neuron. 78:57–64.
  • BasuRay S, Mukherjee S, Romero E, Wilson MC, Wandinger-Ness A. 2010. Rab7 mutants associated with Charcot-Marie-Tooth disease exhibit enhanced NGF-stimulated signaling. PLoS One. 5:e15351.
  • Bellouze S, Baillat G, Buttigieg D, de la Grange P, Rabouille C, Haase G. 2016. Stathmin 1/2-triggered microtubule loss mediates Golgi fragmentation in mutant SOD1 motor neurons. Mol Neurodegener. 11:43.
  • Belzil VV, Valdmanis PN, Dion PA, Daoud H, Kabashi E, Noreau A, Gauthier J, Hince P, Desjarlais A, Bouchard J-P, et al. 2009. Mutations in FUS cause FALS and SALS in French and French Canadian populations. Neurology. 73:1176–1179.
  • Bernard-Marissal N, Medard J-J, Azzedine H, Chrast R. 2015. Dysfunction in endoplasmic reticulum-mitochondria crosstalk underlies SIGMAR1 loss of function mediated motor neuron degeneration. Brain. 138:875–890.
  • Bhattacharya A, Bokov A, Muller FL, Jernigan AL, Maslin K, Diaz V, Richardson A, Van Remmen H. 2012. Dietary restriction but not rapamycin extends disease onset and survival of the H46R/H48Q mouse model of ALS. Neurobiol Aging. 33:1829–1832.
  • Bhuin T, Roy JK. 2014. Rab proteins: the key regulators of intracellular vesicle transport. Exp Cell Res. 328:1–19.
  • Bielli A, Thornqvist PO, Hendrick AG, Finn R, Fitzgerald K, McCaffrey MW. 2001. The small GTPase Rab4A interacts with the central region of cytoplasmic dynein light intermediate chain-1. Biochem Biophys Res Commun. 281:1141–1153.
  • Binotti B, Pavlos NJ, Riedel D, Wenzel D, Vorbrüggen G, Schalk AM, Kühnel K, Boyken J, Erck C, Martens H, et al. 2015. The GTPase Rab26 links synaptic vesicles to the autophagy pathway. Elife. 4:e05597.
  • Blair IP, Williams KL, Warraich ST, Durnall JC, Thoeng AD, Manavis J, Blumbergs PC, Vucic S, Kiernan MC, Nicholson GA. 2009. FUS mutations in amyotrophic lateral sclerosis: clinical, pathological, neurophysiological and genetic analysis. J Neurol Neurosurg Psychiatry. 2009:194399.
  • Boehringer A, Garcia-Mansfield K, Singh G, Bakkar N, Pirrotte P, Bowser R. 2017. ALS associated mutations in matrin 3 alter protein-protein interactions and impede mRNA nuclear export. Sci Rep. 7:14529.
  • Boncompain G, Weigel AV. 2018. Transport and sorting in the Golgi complex: multiple mechanisms sort diverse cargo. Curr Opin Cell Biol. 50:94–101.
  • Boopathy S, Silvas TV, Tischbein M, Jansen S, Shandilya SM, Zitzewitz JA, Landers JE, Goode BL, Schiffer CA, Bosco DA. 2015. Structural basis for mutation-induced destabilization of profilin 1 in ALS. Proc Natl Acad Sci USA. 112:7984–7989.
  • Borroni B, Archetti S, Del Bo R, Papetti A, Buratti E, Bonvicini C, Agosti C, Cosseddu M, Turla M, Di Lorenzo D, et al. 2010. TARDBP mutations in frontotemporal lobar degeneration: frequency, clinical features, and disease course. Rejuvenation Res. 13:509–517.
  • Bosco DA, Lemay N, Ko HK, Zhou H, Burke C, Kwiatkowski TJ, Jr Sapp P, McKenna-Yasek D, Brown RH, Jr, Hayward LJ. 2010. Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Hum Mol Genet. 19:4160–4175.
  • Boslem E, Weir JM, MacIntosh G, Sue N, Cantley J, Meikle PJ, Biden TJ. 2013. Alteration of endoplasmic reticulum lipid rafts contributes to lipotoxicity in pancreatic β-cells. J Biol Chem. 288:26569–26582.
  • Boylan K, Yang C, Crook J, Overstreet K, Heckman M, Wang Y, Borchelt D, Shaw G. 2009. Immunoreactivity of the phosphorylated axonal neurofilament H subunit (pNF-H) in blood of ALS model rodents and ALS patients: evaluation of blood pNF-H as a potential ALS biomarker. J Neurochem. 111:1182–1191.
  • Braak H, Neumann M, Ludolph A, Del Tredici K. 2017. Does sporadic amyotrophic lateral sclerosis spread via axonal connectivities?. Neurol Int Open. 1:E136–EE41.
  • Braakman I, Bulleid NJ. 2011. Protein folding and modification in the mammalian endoplasmic reticulum. Annu Rev Biochem. 80:71–99.
  • Bradshaw WJ, Rehman S, Pham TT, Thiyagarajan N, Lee RL, Subramanian V, Acharya KR. 2017. Structural insights into human angiogenin variants implicated in Parkinson's disease and Amyotrophic Lateral Sclerosis. Sci Rep. 7:41996.
  • Brenner D, Yilmaz R, Müller K, Grehl T, Petri S, Meyer T, Grosskreutz J, Weydt P, Ruf W, Neuwirth C, et al. 2018. Hot-spot KIF5A mutations cause familial ALS. Brain. 141:688–697.
  • Brettschneider J, Petzold A, Süssmuth S, Ludolph AC, Tumani H. 2006. Axonal damage markers in cerebrospinal fluid are increased in ALS. Neurology. 66:852–856.
  • Britt DJ, Farías GG, Guardia CM, Bonifacino JS. 2016. Mechanisms of polarized organelle distribution in neurons. Front Cell Neurosci. 10:88.
  • Bucci C, Alifano P, Cogli L. 2014. The role of rab proteins in neuronal cells and in the trafficking of neurotrophin receptors. Membranes. 4:642–677.
  • Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B. 2000. Rab7: a key to lysosome biogenesis. Mol Biol Cell. 11:467–480.
  • Bui M, Gilady SY, Fitzsimmons RE, Benson MD, Lynes EM, Gesson K, Alto NM, Strack S, Scott JD, Simmen T. 2010. Rab32 modulates apoptosis onset and mitochondria-associated membrane (MAM) properties. J Biol Chem. M110:101584.
  • Buratti E, Brindisi A, Giombi M, Tisminetzky S, Ayala YM, Baralle FE. 2005. TDP-43 binds heterogeneous nuclear ribonucleoprotein A/B through its C-terminal tail: an important region for the inhibition of cystic fibrosis transmembrane conductance regulator exon 9 splicing. J Biol Chem. 280:37572–37584.
  • Cai H, Reinisch K, Ferro-Novick S. 2007. Coats, tethers, Rabs, and SNAREs work together to mediate the intracellular destination of a transport vesicle. Dev Cell. 12:671–682.
  • Carlos Martín Zoppino F, Damián Militello R, Slavin I, Álvarez C, Colombo MI. 2010. Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites. Traffic. 11:1246–1261.
  • Carrì MT, D’Ambrosi N, Cozzolino M. 2017. Pathways to mitochondrial dysfunction in ALS pathogenesis. Biochem Biophys Res Commun. 483:1187–1193.
  • Castillo K, Nassif M, Valenzuela V, Rojas F, Matus S, Mercado G, Court FA, van Zundert B, Hetz C. 2013. Trehalose delays the progression of amyotrophic lateral sclerosis by enhancing autophagy in motoneurons. Autophagy. 9:1308–1320.
  • Chalasani ML, Swarup G, Balasubramanian D. 2009. Optineurin and its mutants: molecules associated with some forms of glaucoma. Ophthalmic Res. 42:176–184.
  • Chan C-C, Scoggin S, Wang D, Cherry S, Dembo T, Greenberg B, Jin EJ, Kuey C, Lopez A, Mehta SQ, et al. 2011. Systematic discovery of Rab GTPases with synaptic functions in Drosophila. Curr Biol. 21:1704–1715.
  • Chen Y, Sheng Z-H. 2013. Kinesin-1–syntaphilin coupling mediates activity-dependent regulation of axonal mitochondrial transport. J Cell Biol. 202:351–364.
  • Chen Y-Z, Bennett CL, Huynh HM, Blair IP, Puls I, Irobi J, Dierick I, Abel A, Kennerson ML, Rabin BA, et al. 2004. DNA/RNA helicase gene mutations in a form of juvenile amyotrophic lateral sclerosis (ALS4). Am J Hum Genet. 74:1128–1135.
  • Cheung AY, Chen CY-h, Glaven RH, De GBH, Vidali L, Hepler PK, Wu H-m. 2002. Rab2 GTPase regulates vesicle trafficking between the endoplasmic reticulum and the Golgi bodies and is important to pollen tube growth. Plant Cell. 14:945–962.
  • Chevalier-Larsen E, Holzbaur EL. 2006. Axonal transport and neurodegenerative disease. Biochim Biophys Acta Mol Basis Dis. 1762:1094–1108.
  • Chiò A, Restagno G, Brunetti M, Ossola I, Calvo A, Mora G, Sabatelli M, Monsurrò MR, Battistini S, Mandrioli J, et al. 2009. Two Italian kindreds with familial amyotrophic lateral sclerosis due to FUS mutation. Neurobiol Aging. 30:1272–1275.
  • Chou CC, Zhang Y, Umoh ME, Vaughan SW, Lorenzini I, Liu F, Sayegh M, Donlin-Asp PG, Chen YH, Duong DM, et al. 2018. TDP-43 pathology disrupts nuclear pore complexes and nucleocytoplasmic transport in ALS/FTD. Nat Neurosci. 21:228–239.
  • Chow CY, Landers JE, Bergren SK, Sapp PC, Grant AE, Jones JM, Everett L, Lenk GM, McKenna-Yasek DM, Weisman LS, et al. 2009. Deleterious variants of FIG4, a phosphoinositide phosphatase, in patients with ALS. Am J Hum Genet. 84:85–88.
  • Cirulli ET, Lasseigne BN, Petrovski S, Sapp PC, Dion PA, Leblond CS, Couthouis J, Lu Y-F, Wang Q, Krueger BJ, et al. 2015. Exome sequencing in amyotrophic lateral sclerosis identifies risk genes and pathways. Science. 347:1436–1441.
  • Clark LN, Poorkaj P, Wszolek Z, Geschwind DH, Nasreddine ZS, Miller B, Li D, Payami H, Awert F, Markopoulou K, et al. 1998. Pathogenic implications of mutations in the tau gene in pallido-ponto-nigral degeneration and related neurodegenerative disorders linked to chromosome 17. Proc Natl Acad Sci. 95:13103–13107.
  • Cogli L, Progida C, Lecci R, Bramato R, Krüttgen A, Bucci C. 2010. CMT2B-associated Rab7 mutants inhibit neurite outgrowth. Acta Neuropathol. 120:491–501.
  • Corbo M, Hays AP. 1992. Peripherin and neurofilament protein coexist in spinal spheroids of motor neuron disease. J Neuropathol Exp Neurol. 51:531–537.
  • Corcia P, Couratier P, Blasco H, Andres CR, Beltran S, Meininger V, Vourc’h P. 2017. Genetics of amyotrophic lateral sclerosis. Rev Neurol (Paris). 173:254–262.
  • Corrado L, Carlomagno Y, Falasco L, Mellone S, Godi M, Cova E, Cereda C, Testa L, Mazzini L, D'Alfonso S. 2011. A novel peripherin gene (PRPH) mutation identified in one sporadic amyotrophic lateral sclerosis patient. Neurobiol Aging. 32:552.e1–552.e6.
  • Cox LE, Ferraiuolo L, Goodall EF, Heath PR, Higginbottom A, Mortiboys H, Hollinger HC, Hartley JA, Brockington A, Burness CE, et al. 2010. Mutations in CHMP2B in lower motor neuron predominant amyotrophic lateral sclerosis (ALS). PloS One. 5:e9872.
  • Crippa V, Sau D, Rusmini P, Boncoraglio A, Onesto E, Bolzoni E, Galbiati M, Fontana E, Marino M, Carra S, et al. 2010. The small heat shock protein B8 (HspB8) promotes autophagic removal of misfolded proteins involved in amyotrophic lateral sclerosis (ALS). Human Mol Genet. 19:3440–3456.
  • D’Adamo P, Masetti M, Bianchi V, Morè L, Mignogna ML, Giannandrea M, Gatti S. 2014. RAB GTPases and RAB-interacting proteins and their role in the control of cognitive functions. Neurosci Biobehav Rev. 46:302–314.
  • Dafinca R, Scaber J, Ababneh N, Lalic T, Weir G, Christian H, Vowles J, Douglas AG, Fletcher ‐Jones A, Browne C. 2016. C9orf72 hexanucleotide expansions are associated with altered endoplasmic reticulum calcium homeostasis and stress granule formation in induced pluripotent stem cell‐derived neurons from patients with amyotrophic lateral sclerosis and frontotemporal dementia. Stem cells. 34:2063–2078.
  • Daoud H, Zhou S, Noreau A, Sabbagh M, Belzil V, Dionne-Laporte A, Tranchant C, Dion P, Rouleau GA. 2012. Exome sequencing reveals SPG11 mutations causing juvenile ALS. Neurobiol Aging. 33:839.e5–839.e9.
  • De Luca M, Cogli L, Progida C, Nisi V, Pascolutti R, Sigismund S, Di Fiore PP, Bucci C. 2014. RILP regulates vacuolar ATPase through interaction with the V1G1 subunit. J Cell Sci. 127:2697–2708.
  • De Vos KJ, Grierson AJ, Ackerley S, Miller CC. 2008. Role of axonal transport in neurodegenerative diseases. Annu Rev Neurosci. 31:151–173.
  • De Vos KJ, Hafezparast M. 2017. Neurobiology of axonal transport defects in motor neuron diseases: opportunities for translational research?. Neurobio Dis. 105:283–299.
  • De Vos KJ, Chapman AL, Tennant ME, Manser C, Tudor EL, Lau K-F, Brownlees J, Ackerley S, Shaw PJ, McLoughlin DM, et al. 2007. Familial amyotrophic lateral sclerosis-linked SOD1 mutants perturb fast axonal transport to reduce axonal mitochondria content. Human Mol Genet. 16:2720–2728.
  • de Wit H, Lichtenstein Y, Kelly RB, Geuze HJ, Klumperman J, van der Sluijs P. 2001. Rab4 regulates formation of synaptic-like microvesicles from early endosomes in PC12 cells. Mol Biol Cell. 12:3703–3715.
  • Deinhardt K, Salinas S, Verastegui C, Watson R, Worth D, Hanrahan S, Bucci C, Schiavo G. 2006. Rab5 and Rab7 control endocytic sorting along the axonal retrograde transport pathway. Neuron. 52:293–305.
  • DeJesus‐Hernandez M, Kocerha J, Finch N, Crook R, Baker M, Desaro P, Johnston A, Rutherford N, Wojtas A, Kennelly K. 2010. De novo truncating FUS gene mutation as a cause of sporadic amyotrophic lateral sclerosis. Hum Mutat. 31:E1377–E1E89.
  • DeJesus-Hernandez M, Desaro P, Johnston A, Ross O, Wszolek Z, Ertekin-Taner N, Graff-Radford N, Rademakers R, Boylan K. 2011. Novel p. Ile151Val mutation in VCP in a patient of African American descent with sporadic ALS. Neurology. 77:1102–1103.
  • DeJesus-Hernandez M, Mackenzie IR, Boeve BF, Boxer AL, Baker M, Rutherford NJ, Nicholson AM, Finch NA, Flynn H, Adamson J, et al. 2011. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron. 72:245–256.
  • Dejgaard SY, Murshid A, Erman A, Kizilay O, Verbich D, Lodge R, Dejgaard K, Ly-Hartig TBN, Pepperkok R, Simpson JC, et al. 2008. Rab18 and Rab43 have key roles in ER-Golgi trafficking. J Cell Sci. 121:2768–2781.
  • Deng Z, Sheehan P, Chen S, Yue Z. 2017. Is amyotrophic lateral sclerosis/frontotemporal dementia an autophagy disease?. Mol Neurodegener. 12:90.
  • Deng H-X, Chen W, Hong S-T, Boycott KM, Gorrie GH, Siddique N, Yang Y, Fecto F, Shi Y, Zhai H, et al. 2011. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature. 477:211.
  • Deshaies J-E, Shkreta L, Moszczynski AJ, Sidibé H, Semmler S, Fouillen A, Bennett ER, Bekenstein U, Destroismaisons L, Toutant J, et al. 2018. TDP-43 regulates the alternative splicing of hnRNP A1 to yield an aggregation-prone variant in amyotrophic lateral sclerosis. Brain. 141:1320–1333.
  • Deshpande M, Feiger Z, Shilton AK, Luo CC, Silverman E, Rodal AA. 2016. Role of BMP receptor traffic in synaptic growth defects in an ALS model. Mol Biol Cell. 27:2898–2910.
  • Devenney E, Hornberger M, Irish M, Mioshi E, Burrell J, Tan R, Kiernan MC, Hodges JR. 2014. Frontotemporal dementia associated with the C9ORF72 mutation: a unique clinical profile. JAMA Neurol. 71:331–339.
  • Dey S, Banker G, Ray K. 2017. Anterograde transport of Rab4-associated vesicles regulates synapse organization in Drosophila. Cell Rep. 18:2452–2463.
  • Dillen L, Van Langenhove T, Engelborghs S, Vandenbulcke M, Sarafov S, Tournev I, Merlin C, Cras P, Vandenberghe R, De Deyn PP. 2013. Explorative genetic study of UBQLN2 and PFN1 in an extended Flanders-Belgian cohort of frontotemporal lobar degeneration patients. Neurobiol Aging. 34:1711.e1–1711.e5.
  • Dols-Icardo O, Nebot I, Gorostidi A, Ortega-Cubero S, Hernández I, Rojas-García R, García-Redondo A, Povedano M, Lladó A, Álvarez V, et al. 2015. Analysis of the CHCHD10 gene in patients with frontotemporal dementia and amyotrophic lateral sclerosis from Spain. Brain. 138:e400.
  • Dormann D, Haass C. 2011. TDP-43 and FUS: a nuclear affair. Trends Neurosci. 34:339–348.
  • Dormann D, Rodde R, Edbauer D, Bentmann E, Fischer I, Hruscha A, Than ME, Mackenzie IR, Capell A, Schmid B, et al. 2010. ALS-associated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import. Embo J. 29:2841–2857.
  • Dorst J, Ludolph AC, Huebers A. 2018. Disease-modifying and symptomatic treatment of amyotrophic lateral sclerosis. Ther Adv Neurol Disord. 11:1756285617734734.
  • Duan W, Li X, Shi J, Guo Y, Li Z, Li C. 2010. Mutant TAR DNA-binding protein-43 induces oxidative injury in motor neuron-like cell. Neuroscience. 169:1621–1629.
  • Dulubova I, Lou X, Lu J, Huryeva I, Alam A, Schneggenburger R, Südhof TC, Rizo J. 2005. A Munc13/RIM/Rab3 tripartite complex: from priming to plasticity?. Embo J. 24:2839–2850.
  • Dupont N, Jiang S, Pilli M, Ornatowski W, Bhattacharya D, Deretic V. 2011. Autophagy‐based unconventional secretory pathway for extracellular delivery of IL‐1β. EMBO J. 30:4701–4711.
  • Echard A, Jollivet F, Martinez O, Lacapere JJ, Rousselet A, Janoueix-Lerosey I, Goud B. 1998. Interaction of a Golgi-associated kinesin-like protein with Rab6. Science (NY). 279:580–585.
  • Ederle H, Funk C, Abou-Ajram C, Hutten S, Funk EB, Kehlenbach RH, Bailer SM, Dormann D. 2018. Nuclear egress of TDP-43 and FUS occurs independently of Exportin-1/CRM1. Sci Rep. 8:7084.
  • Elden AC, Kim H-J, Hart MP, Chen-Plotkin AS, Johnson BS, Fang X, Armakola M, Geser F, Greene R, Lu MM, et al. 2010. Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature. 466:1069.
  • Ellgaard L, Helenius A. 2003. Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol. 4:181.
  • Eschbach J, Schwalenstöcker B, Soyal SM, Bayer H, Wiesner D, Akimoto C, Nilsson A-C, Birve A, Meyer T, Dupuis L, et al. 2013. PGC-1α is a male-specific disease modifier of human and experimental amyotrophic lateral sclerosis. Hum Mol Genet. 22:3477–3484.
  • Farg MA, Konopka A, Soo KY, Ito D, Atkin JD. 2017. The DNA damage response (DDR) is induced by the C9orf72 repeat expansion in amyotrophic lateral sclerosis. Human Mol Gen. 26:2882–2896.
  • Farg MA, Soo KY, Warraich ST, Sundaramoorthy V, Blair IP, Atkin JD. 2013. Ataxin-2 interacts with FUS and intermediate-length polyglutamine expansions enhance FUS-related pathology in amyotrophic lateral sclerosis. Hum Mol Genet. 22:717–728.
  • Farg MA, Sundaramoorthy V, Sultana JM, Yang S, Atkinson RAK, Levina V, Halloran MA, Gleeson PA, Blair IP, Soo KY, et al. 2014. C9ORF72, implicated in amytrophic lateral sclerosis and frontotemporal dementia, regulates endosomal trafficking. Hum Mol Genet. 23:3579–3595.
  • Fecto F, Yan J, Vemula SP, Liu E, Yang Y, Chen W, Zheng JG, Shi Y, Siddique N, Arrat H. 2011. SQSTM1 mutations in familial and sporadic amyotrophic lateral sclerosis. Archiv Neurol. 68:1440–1446.
  • Feit H, Silbergleit A, Schneider LB, Gutierrez JA, Fitoussi RP, Réyès C, Rouleau GA, Brais B, Jackson CE, Beckmann JS, Seboun E. 1998. Vocal cord and pharyngeal weakness with autosomal dominant distal myopathy: clinical description and gene localization to 5q31. Am J Hum Genet. 63:1732–1742.
  • Fernandes AC, Uytterhoeven V, Kuenen S, Wang YC, Slabbaert JR, Swerts J, Kasprowicz J, Aerts S, Verstreken P. 2014. Reduced synaptic vesicle protein degradation at lysosomes curbs TBC1D24/sky-induced neurodegeneration. J Cell Biol. 207:453–462.
  • Figlewicz DA, Krizus A, Martinoli MG, Meininger V, Dib M, Rouleau GA, Julien J-P. 1994. Variants of the heavy neurofilament subunit are associated with the development of amyotrophic lateral sclerosis. Hum Mol Genet. 3:1757–1761.
  • Figley MD, Bieri G, Kolaitis RM, Taylor JP, Gitler AD. 2014. Profilin 1 associates with stress granules and ALS-linked mutations alter stress granule dynamics. J Neurosci. 34:8083–8097.
  • Filimonenko M, Stuffers S, Raiborg C, Yamamoto A, Malerød L, Fisher EM, Isaacs A, Brech A, Stenmark H, Simonsen A. 2007. Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J Cell Biol. 179:485–500.
  • Fransson Å, Ruusala A, Aspenström P. 2006. The atypical Rho GTPases Miro-1 and Miro-2 have essential roles in mitochondrial trafficking. Biochem Biophys Res Commun. 344:500–510.
  • Frederick RL, McCaffery JM, Cunningham KW, Okamoto K, Shaw JM. 2004. Yeast Miro GTPase, Gem1p, regulates mitochondrial morphology via a novel pathway. J Cell Biol. 167:87–98.
  • Freibaum BD, Lu Y, Lopez-Gonzalez R, Kim NC, Almeida S, Lee K-H, Badders N, Valentine M, Miller BL, Wong PC, et al. 2015. GGGGCC repeat expansion in C9orf72 compromises nucleocytoplasmic transport. Nature. 525:129.
  • Freischmidt A, Wieland T, Richter B, Ruf W, Schaeffer V, Müller K, Marroquin N, Nordin F, Hübers A, Weydt P, et al. 2015. Haploinsufficiency of TBK1 causes familial ALS and fronto-temporal dementia. Nat Neurosci. 18:631.
  • Frick P, Sellier C, Mackenzie IR, Cheng C-Y, Tahraoui-Bories J, Martinat C, Pasterkamp RJ, Prudlo J, Edbauer D, Oulad-Abdelghani M. 2018. Novel antibodies reveal presynaptic localization of C9orf72 protein and reduced protein levels in C9orf72 mutation carriers. Acta Neuropathol Commun. 6:72.
  • Friedman JR, Webster BM, Mastronarde DN, Verhey KJ, Voeltz GK. 2010. ER sliding dynamics and ER-mitochondrial contacts occur on acetylated microtubules. J Cell Biol. 190:363–375.
  • Fujita Y, Mizuno Y, Takatama M, Okamoto K. 2008. Anterior horn cells with abnormal TDP-43 immunoreactivities show fragmentation of the Golgi apparatus in ALS. J Neurol Sci. 269:30–34.
  • Fujita Y, Okamoto K, Sakurai A, Gonatas NK, Hirano A. 2000. Fragmentation of the Golgi apparatus of the anterior horn cells in patients with familial amyotrophic lateral sclerosis with SOD1 mutations and posterior column involvement. J Neurol Sci. 174:137–140.
  • Gal J, Zhang J, Kwinter DM, Zhai J, Jia H, Jia J, Zhu H. 2011. Nuclear localization sequence of FUS and induction of stress granules by ALS mutants. Neurobiol Aging. 32:2323.e27–2323.e 23. e40
  • Gautam M, Jara JH, Sekerkova G, Yasvoina MV, Martina M, Özdinler PH. 2016. Absence of alsin function leads to corticospinal motor neuron vulnerability via novel disease mechanisms. Hum Mol Genet. 25:1074–1087.
  • Gerges NZ, Backos DS, Esteban JA. 2004. Local control of AMPA receptor trafficking at the postsynaptic terminal by a small GTPase of the Rab family. J Biol Chem. 279:43870–43878.
  • Gijselinck I, Van Mossevelde S, van der Zee J, Sieben A, Philtjens S, Heeman B, Engelborghs S, Vandenbulcke M, De Baets G, Bäumer V, et al. 2015. Loss of TBK1 is a frequent cause of frontotemporal dementia in a Belgian cohort. Neurology. 85:2116–2125.
  • Goldenring JR. 2013. A central role for vesicle trafficking in epithelial neoplasia: intracellular highways to carcinogenesis. Nat Rev Cancer. 13:813.
  • Goldstein LS, Das U. 2018. Neurodegenerative diseases and axonal transported. Michael S. Wolfe, editor. The molecular and cellular basis of neurodegenerative diseases. Lawrence, KS, United States: Elsevier; 345–367.
  • Gomez-Navarro N, Miller E. 2016. Protein sorting at the ER–Golgi interface. J Cell Biol. 201610031.
  • Gonatas NK, Stieber A, Gonatas JO. 2006. Fragmentation of the Golgi apparatus in neurodegenerative diseases and cell death. J Neurol Sci. 246:21–30.
  • Greenway MJ, Andersen PM, Russ C, Ennis S, Cashman S, Donaghy C, Patterson V, Swingler R, Kieran D, Prehn J, et al. 2006. ANG mutations segregate with familial and 'sporadic' amyotrophic lateral sclerosis. Nat Genet. 38:411.
  • Groen EJN, Fumoto K, Blokhuis AM, Engelen-Lee J, Zhou Y, van den Heuvel DMA, Koppers M, van Diggelen F, van Heest J, Demmers JAA, et al. 2013. ALS-associated mutations in FUS disrupt the axonal distribution and function of SMN. Hum Mol Genet. 22:3690–3704.
  • Gros-Louis F, Larivière R, Gowing G, Laurent S, Camu W, Bouchard J-P, Meininger V, Rouleau GA, Julien J-P. 2004. A frameshift deletion in peripherin gene associated with amyotrophic lateral sclerosis. J Biol Chem. 279:45951–45956.
  • Grosshans BL, Ortiz D, Novick P. 2006. Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci. 103:11821–11827.
  • Group U-LS. 2013. Lithium in patients with amyotrophic lateral sclerosis (LiCALS): a phase 3 multicentre, randomised, double-blind, placebo-controlled trial. Lancet Neurol. 12:339–345.
  • Guerra F, Bucci C. 2016. Multiple roles of the small GTPase Rab7. Cells. 5:34.
  • Gutierrez MG, Munafó DB, Berón W, Colombo MI. 2004. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci. 117:2687–2697.
  • Guven G, Lohmann E, Bras J, Gibbs JR, Gurvit H, Bilgic B, Hanagasi H, Rizzu P, Heutink P, Emre M, et al. 2016. Mutation frequency of the major frontotemporal dementia genes, MAPT, GRN and C9ORF72 in a Turkish cohort of dementia patients. PloS One. 11:e0162592.
  • Haas AK, Yoshimura S-i, Stephens DJ, Preisinger C, Fuchs E, Barr FA. 2007. Analysis of GTPase-activating proteins: Rab1 and Rab43 are key Rabs required to maintain a functional Golgi complex in human cells. J Cell Sci. 120:2997–3010.
  • Hadano S, Otomo A, Kunita R, Suzuki-Utsunomiya K, Akatsuka A, Koike M, Aoki M, Uchiyama Y, Itoyama Y, Ikeda J-E. 2010. Loss of ALS2/Alsin exacerbates motor dysfunction in a SOD1H46R-expressing mouse ALS model by disturbing endolysosomal trafficking. PloS One. 5:e9805.
  • Hadano S, Benn SC, Kakuta S, Otomo A, Sudo K, Kunita R, Suzuki-Utsunomiya K, Mizumura H, Shefner JM, Cox GA, et al. 2006. Mice deficient in the Rab5 guanine nucleotide exchange factor ALS2/alsin exhibit age-dependent neurological deficits and altered endosome trafficking. Hum Mol Genet. 15:233–250.
  • Hadano S, Hand CK, Osuga H, Yanagisawa Y, Otomo A, Devon RS, Miyamoto N, Showguchi-Miyata J, Okada Y, Singaraja R, et al. 2001. A gene encoding a putative GTPase regulator is mutated in familial amyotrophic lateral sclerosis 2. Nat Genet. 29:166.
  • Hand CK, Devon RS, Gros-Louis F, Rochefort D, Khoris J, Meininger V, Bouchard J-P, Camu W, Hayden MR, Rouleau GA. 2003. Mutation screening of the ALS2 gene in sporadic and familial amyotrophic lateral sclerosis. Arch Neurol. 60:1768–1771.
  • Henne WM, Buchkovich NJ, Emr SD. 2011. The ESCRT pathway. Dev Cell. 21:77–91.
  • Heo J-M, Ordureau A, Paulo JA, Rinehart J, Harper JW. 2015. The PINK1-PARKIN mitochondrial ubiquitylation pathway drives a program of OPTN/NDP52 recruitment and TBK1 activation to promote mitophagy. Mol Cell. 60:7–20.
  • Hetz C, Thielen P, Matus S, Nassif M, Kiffin R, Martinez G, Cuervo AM, Brown RH, Glimcher LH. 2009. XBP-1 deficiency in the nervous system protects against amyotrophic lateral sclerosis by increasing autophagy. Gene Dev.
  • Hirokawa N, Niwa S, Tanaka Y. 2010. Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron. 68:610–638.
  • Hong K, Li Y, Duan W, Guo Y, Jiang H, Li W, Li C. 2012. Full-length TDP-43 and its C-terminal fragments activate mitophagy in NSC34 cell line. Neurosci Lett. 530:144–149.
  • Horgan CP, McCaffrey MW. 2011. Rab GTPases and microtubule motors. Biochem Soc Trans. 39:1202–1206.
  • Horton AC, Rácz B, Monson EE, Lin AL, Weinberg RJ, Ehlers MD. 2005. Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron. 48:757–771.
  • Huang C, Tong J, Bi F, Wu Q, Huang B, Zhou H, Xia X-G. 2012. Entorhinal cortical neurons are the primary targets of FUS mislocalization and ubiquitin aggregation in FUS transgenic rats. Hum Mol Genet. 21:4602–4614.
  • Huang EJ, Zhang J, Geser F, Trojanowski JQ, Strober JB, Dickson DW, Brown J, Shapiro RH, Lomen BE, Hoerth C. 2010. Extensive FUS‐immunoreactive pathology in juvenile amyotrophic lateral sclerosis with basophilic inclusions. Brain Pathol. 20:1069–1076.
  • Hutagalung AH, Novick PJ. 2011. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev. 91:119–149.
  • Hutt DM, Balch WE. 2013. Expanding proteostasis by membrane trafficking networks. Cold Spring Harb Perspect Biol. a013383.
  • Hyttinen JM, Niittykoski M, Salminen A, Kaarniranta K. 2013. Maturation of autophagosomes and endosomes: a key role for Rab7. Biochim Biophys Acta. 1833:503–510.
  • Ito D, Seki M, Tsunoda Y, Uchiyama H, Suzuki N. 2011. Nuclear transport impairment of amyotrophic lateral sclerosis-linked mutations in FUS/TLS. Ann Neurol. 69:152–162.
  • Itoh T, Fujita N, Kanno E, Yamamoto A, Yoshimori T, Fukuda M. 2008. Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation. Mol Biol Cell. 19:2916–2925.
  • Ito H, Nakamura M, Komure O, Ayaki T, Wate R, Maruyama H, Nakamura Y, Fujita K, Kaneko S, Okamoto Y, et al. 2011. Clinicopathologic study on an ALS family with a heterozygous E478G optineurin mutation. Acta Neuropathologica. 122:223–229.
  • Iyer S, Subramanian V, Acharya KR. 2018. C9orf72, a protein associated with amyotrophic lateral sclerosis (ALS) is a guanine nucleotide exchange factor. PeerJ. 6:e5815.
  • Jackson CL. 2018. Membrane trafficking: a little flexibility helps vesicles get into shape. Curr Biol. 28:R706–RR09.
  • Jahreiss L, Menzies FM, Rubinsztein DC. 2008. The itinerary of autophagosomes: from peripheral formation to kiss-and-run fusion with lysosomes. Traffic. 9:574–587.
  • Jaiswal MK, Zech W-D, Goos M, Leutbecher C, Ferri A, Zippelius A, Carrì MT, Nau R, Keller BU. 2009. Impairment of mitochondrial calcium handling in a mtSOD1 cell culture model of motoneuron disease. BMC Neurosci. 10:64.
  • Jaiswal MK, Keller BU. 2008. Cu/Zn superoxide dismutase typical for familial amyotrophic lateral sclerosis increases the vulnerability of mitochondria and perturbed Ca2+ homeostasis in SOD1G93A mice. Mol Pharmacol.
  • Jiang J, Zhu Q, Gendron TF, Saberi S, McAlonis-Downes M, Seelman A, Stauffer JE, Jafar-Nejad P, Drenner K, Schulte D, et al. 2016. Gain of toxicity from ALS/FTD-linked repeat expansions in C9ORF72 is alleviated by antisense oligonucleotides targeting GGGGCC-containing RNAs. Neuron. 90:535–550.
  • Johnson JO, Glynn SM, Gibbs JR, Nalls MA, Sabatelli M, Restagno G, Drory VE, Chio A, Rogaeva E, Traynor BJ. 2014. Mutations in the CHCHD10 gene are a common cause of familial amyotrophic lateral sclerosis. Brain. 137:e311.
  • Johnson JO, Mandrioli J, Benatar M, Abramzon Y, Van Deerlin VM, Trojanowski JQ, Gibbs JR, Brunetti M, Gronka S, Wuu J, et al. 2010. Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron. 68:857–864.
  • Johnson JO, Pioro EP, Boehringer A, Chia R, Feit H, Renton AE, Pliner HA, Abramzon Y, Marangi G, Winborn BJ, et al. 2014. Mutations in the Matrin 3 gene cause familial amyotrophic lateral sclerosis. Nat Neurosci. 17:664.
  • Jordens I, Fernandez-Borja M, Marsman M, Dusseljee S, Janssen L, Calafat J, Janssen H, Wubbolts R, Neefjes J. 2001. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr Biol. 11:1680–1685.
  • Jovičić A, Mertens J, Boeynaems S, Bogaert E, Chai N, Yamada SB, Paul JW, Sun S, Herdy JR, Bieri G, et al. 2015. Modifiers of C9orf72 dipeptide repeat toxicity connect nucleocytoplasmic transport defects to FTD/ALS. Nat Neurosci. 18:1226.
  • Ju J-S, Fuentealba RA, Miller SE, Jackson E, Piwnica-Worms D, Baloh RH, Weihl CC. 2009. Valosin-containing protein (VCP) is required for autophagy and is disrupted in VCP disease. J Cell Biol. 187:875–888.
  • Kabashi E, El Oussini H, Bercier V, Gros-Louis F, Valdmanis PN, McDearmid J, Mejier IA, Dion PA, Dupre N, Hollinger D, et al. 2013. Investigating the contribution of VAPB/ALS8 loss of function in amyotrophic lateral sclerosis. Hum Mol Genet. 22:2350–2360.
  • Kabuta T, Kinugawa A, Tsuchiya Y, Kabuta C, Setsuie R, Tateno M, Araki T, Wada K. 2009. Familial amyotrophic lateral sclerosis-linked mutant SOD1 aberrantly interacts with tubulin. Biochem Biophys Res Commun. 387:121–126.
  • Kakuta S, Yamaguchi J, Suzuki C, Sasaki M, Kazuno S, Uchiyama Y. 2017. Small GTPase Rab1B is associated with ATG9A vesicles and regulates autophagosome formation. FASEB J. 31:3757–3773.
  • Kaneb HM, Folkmann AW, Belzil VV, Jao L-E, Leblond CS, Girard SL, Daoud H, Noreau A, Rochefort D, Hince P, et al. 2015. Deleterious mutations in the essential mRNA metabolism factor, hGle1, in amyotrophic lateral sclerosis. Hum Mol Genet. 24:1363–1373.
  • Khalil B, Morderer D, Price PL, Liu F, Rossoll W. 2018. mRNP assembly, axonal transport, and local translation in neurodegenerative diseases. Brain Res.
  • Kiernan MC, Vucic S, Cheah BC, Turner MR, Eisen A, Hardiman O, Burrell JR, Zoing MC. 2011. Amyotrophic lateral sclerosis. Lancet. 377:942–955.
  • Kim HJ, Taylor JP. 2017. Lost in transportation: nucleocytoplasmic transport defects in ALS and other neurodegenerative diseases. Neuron. 96:285–297.
  • Kim HJ, Kim NC, Wang Y-D, Scarborough EA, Moore J, Diaz Z, MacLea KS, Freibaum B, Li S, Molliex A, et al. 2013. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature. 495:467.
  • Kim H-J, Kwon M-J, Choi W-J, Oh K-W, Oh S-i, Ki C-S, Kim SH. 2014. Mutations in UBQLN2 and SIGMAR1 genes are rare in Korean patients with amyotrophic lateral sclerosis. Neurobiol Aging. 35:1957.e7–1957.e8.
  • Kimura S, Noda T, Yoshimori T. 2008. Dynein-dependent movement of autophagosomes mediates efficient encounters with lysosomes. Cell Struct Funct. 33:109–122.
  • Kino Y, Washizu C, Aquilanti E, Okuno M, Kurosawa M, Yamada M, Doi H, Nukina N. 2011. Intracellular localization and splicing regulation of FUS/TLS are variably affected by amyotrophic lateral sclerosis-linked mutations. Nucleic Acids Res. 39:2781–2798.
  • Kiral FR, Kohrs FE, Jin EJ, Hiesinger PR. 2018. Rab GTPases and membrane trafficking in neurodegeneration. Curr Biol. 28:R471–RR86.
  • Kirby J, Goodall EF, Smith W, Highley JR, Masanzu R, Hartley JA, Hibberd R, Hollinger HC, Wharton SB, Morrison KE, et al. 2010. Broad clinical phenotypes associated with TAR-DNA binding protein (TARDBP) mutations in amyotrophic lateral sclerosis. Neurogenetics. 11:217–225.
  • Kuijpers M, van Dis V, Haasdijk ED, Harterink M, Vocking K, Post JA, Scheper W, Hoogenraad CC, Jaarsma D. 2013. Amyotrophic lateral sclerosis (ALS)-associated VAPB-P56S inclusions represent an ER quality control compartment. Acta Neuropathol Commun. 1:24.
  • Kunita R, Otomo A, Mizumura H, Suzuki-Utsunomiya K, Hadano S, Ikeda J-E. 2007. The Rab5 activator ALS2/alsin acts as a novel Rac1 effector through Rac1-activated endocytosis. J Biol Chem.
  • Kwiatkowski TJ, Bosco DA, LeClerc AL, Tamrazian E, Vanderburg CR, Russ C, Davis A, Gilchrist J, Kasarskis EJ, Munsat T, et al. 2009. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science. 323:1205–1208.
  • Kwon I, Xiang S, Kato M, Wu L, Theodoropoulos P, Wang T, Kim J, Yun J, Xie Y, McKnight SL. 2014. Poly-dipeptides encoded by the C9orf72 repeats bind nucleoli, impede RNA biogenesis, and kill cells. Science. 345:1139–1145.
  • Laffita-Mesa JM, Rodríguez Pupo JM, Moreno Sera R, Vázquez Mojena Y, Kourí V, Laguna-Salvia L, Martínez-Godales M, Valdevila Figueira JA, Bauer PO, Rodríguez-Labrada R, et al. 2013. De novo mutations in ataxin-2 gene and ALS risk. PLoS One. 8:e70560.
  • Lai C, Xie C, Shim H, Chandran J, Howell BW, Cai H. 2009. Regulation of endosomal motility and degradation by amyotrophic lateral sclerosis 2/alsin. Mol Brain. 2:23.
  • Laird FM, Farah MH, Ackerley S, Hoke A, Maragakis N, Rothstein JD, Griffin J, Price DL, Martin LJ, Wong PC. 2008. Motor neuron disease occurring in a mutant dynactin mouse model is characterized by defects in vesicular trafficking. J Neurosci. 28:1997–2005.
  • Lai C, Xie C, McCormack SG, Chiang H-C, Michalak MK, Lin X, Chandran J, Shim H, Shimoji M, Cookson MR, et al. 2006. Amyotrophic lateral sclerosis 2-deficiency leads to neuronal degeneration in amyotrophic lateral sclerosis through altered AMPA receptor trafficking. J Neurosci. 26:11798–11806.
  • LaMonte BH, Wallace KE, Holloway BA, Shelly SS, Ascaño J, Tokito M, Van Winkle T, Howland DS, Holzbaur EL. 2002. Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron. 34:715–727.
  • Lattante S, Le Ber I, Camuzat A, Brice A, Kabashi E. 2013. Mutations in the PFN1 gene are not a common cause in patients with amyotrophic lateral sclerosis and frontotemporal lobar degeneration in France. Neurobiol Aging. 34:1709.e1–1709.e2.
  • Lazarou M, Sliter DA, Kane LA, Sarraf SA, Wang C, Burman JL, Sideris DP, Fogel AI, Youle RJ. 2015. The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy. Nature. 524:309.
  • Le Ber I, Camuzat A, Guerreiro R, Bouya-Ahmed K, Bras J, Nicolas G, Gabelle A, Didic M, De Septenville A, Millecamps S, et al. 2013. SQSTM1 mutations in French patients with frontotemporal dementia or frontotemporal dementia with amyotrophic lateral sclerosis. JAMA Neurol. 70:1403–1410.
  • Lee BJ, Cansizoglu AE, Süel KE, Louis TH, Zhang Z, Chook YM. 2006. Rules for nuclear localization sequence recognition by karyopherin beta 2. Cell. 126:543–558.
  • Lee JK, Shin JH, Lee JE, Choi E-J. 2015. Role of autophagy in the pathogenesis of amyotrophic lateral sclerosis. Biochim Biophys Acta Mol Basis Dis. 1852:2517–2524.
  • Lesage S, Bras J, Cormier-Dequaire F, Condroyer C, Nicolas A, Darwent L, Guerreiro R, Majounie E, Federoff M, Heutink P, et al. 2015. Loss-of-function mutations in RAB39B are associated with typical early-onset Parkinson disease. Neurol Genet. 1:e9.
  • Leung CL, He CZ, Kaufmann P, Chin SS, Naini A, Liem RK, Mitsumoto H, Hays AP. 2004. A pathogenic peripherin gene mutation in a patient with amyotrophic lateral sclerosis. Brain Pathol. 14:290–296.
  • Levine TP, Daniels RD, Gatta AT, Wong LH, Hayes MJ. 2013. The product of C9orf72, a gene strongly implicated in neurodegeneration, is structurally related to DENN Rab-GEFs. Bioinformatics. 29:499–503.
  • Levine B, Kroemer G. 2008. Autophagy in the pathogenesis of disease. Cell. 132:27–42.
  • Li Q, Spencer NY, Pantazis NJ, Engelhardt JF. 2011. Alsin and SOD1G93A proteins regulate endosomal reactive oxygen species production by glial cells and proinflammatory pathways responsible for neurotoxicity. J Biol Chem. 286:40151–40162.
  • Li L, Zhang X, Le W. 2008. Altered macroautophagy in the spinal cord of SOD1 mutant mice. Autophagy. 4:290–293.
  • Lin F. 2011. Ataxin-2 intermediate-length polyglutamine expansions in European ALS patients. Hum Mol Genet. 20:1697–1700.
  • Ling S-C, Polymenidou M, Cleveland DW. 2013. Converging mechanisms in ALS and FTD: disrupted RNA and protein homeostasis. Neuron. 79:416–438.
  • Liscic RM. 2017. Als and Ftd: insights into the disease mechanisms and therapeutic targets. Eur J Pharmacol. 817:2–6.
  • Liu J, Hu J, Ludlow AT, Pham JT, Shay JW, Rothstein JD, Corey DR. 2017. c9orf72 disease-related foci are each composed of one mutant expanded repeat RNA. Cell Chem Biol. 24:141–148.
  • Liu X, Yang L, Tang L, Chen L, Liu X, Fan D. 2017. DCTN1 gene analysis in Chinese patients with sporadic amyotrophic lateral sclerosis. PloS One. 12:e0182572.
  • Longatti A, Lamb CA, Razi M, Yoshimura S-i, Barr FA, Tooze SA. 2012. TBC1D14 regulates autophagosome formation via Rab11-and ULK1-positive recycling endosomes. J Cell Biol. 197:659–675.
  • Longatti A, Tooze S. 2009. Vesicular trafficking and autophagosome formation. Cell Death Differ. 16:956.
  • Lucocq J, Warren G, Pryde J. 1991. Okadaic acid induces Golgi apparatus fragmentation and arrest of intracellular transport. J Cell Sci. 100:753–759.
  • Ludolph AC, Brettschneider J, Weishaupt JH. 2012. Amyotrophic lateral sclerosis. Curr Opin neurol. 25:530–535.
  • Mackenzie IR, Neumann M. 2012. FET proteins in frontotemporal dementia and amyotrophic lateral sclerosis. Brain Res. 1462:40–43.
  • Mackenzie IR, Arzberger T, Kremmer E, Troost D, Lorenzl S, Mori K, Weng S-M, Haass C, Kretzschmar HA, Edbauer D, et al. 2013. Dipeptide repeat protein pathology in C9ORF72 mutation cases: clinico-pathological correlations. Acta Neuropathol. 126:859–879.
  • Maday S, Twelvetrees AE, Moughamian AJ, Holzbaur EL. 2014. Axonal transport: cargo-specific mechanisms of motility and regulation. Neuron. 84:292–309.
  • Mahipal A, Malafa M. 2016. Importins and exportins as therapeutic targets in cancer. Pharmacol Ther. 164:135–143.
  • Majounie E, Renton AE, Mok K, Dopper EGP, Waite A, Rollinson S, Chiò A, Restagno G, Nicolaou N, Simon-Sanchez J, et al. 2012. Frequency of the C9orf72 hexanucleotide repeat expansion in patients with amyotrophic lateral sclerosis and frontotemporal dementia: a cross-sectional study. Lancet Neurol. 11:323–330.
  • Marat AL, Ioannou MS, McPherson PS. 2012. Connecdenn 3/DENND1C binds actin linking Rab35 activation to the actin cytoskeleton. Mol Biol Cell. 23:163–175.
  • Marchesi C, Ciano C, Salsano E, Nanetti L, Milani M, Gellera C, Taroni F, Fabrizi GM, Uncini A, Pareyson D. 2011. Co-occurrence of amyotrophic lateral sclerosis and Charcot-Marie-Tooth disease type 2A in a patient with a novel mutation in the mitofusin-2 gene. Neuromuscular Disord. 21:129–131.
  • Martinez O, Antony C, Pehau-Arnaudet G, Berger EG, Salamero J, Goud B. 1997. GTP-bound forms of rab6 induce the redistribution of Golgi proteins into the endoplasmic reticulum. Proc Natl Acad Sci. 94:1828–1833.
  • Martinez O, Schmidt A, Salaméro J, Hoflack B, Roa M, Goud B. 1994. The small GTP-binding protein rab6 functions in intra-Golgi transport. J Cell Biol. 127:1575–1588.
  • Maruyama H, Morino H, Ito H, Izumi Y, Kato H, Watanabe Y, Kinoshita Y, Kamada M, Nodera H, Suzuki H, et al. 2010. Mutations of optineurin in amyotrophic lateral sclerosis. Nature. 465:223.
  • Mata IF, Jang Y, Kim C-H, Hanna DS, Dorschner MO, Samii A, Agarwal P, Roberts JW, Klepitskaya O, Shprecher DR. 2015. The RAB39B p. G192R mutation causes X-linked dominant Parkinson’s disease. Mol Neurodegener. 10:50.
  • Maximino JR, de Oliveira GP, Alves CJ, Chadi G. 2014. Deregulated expression of cytoskeleton related genes in the spinal cord and sciatic nerve of presymptomatic SOD1(G93A) Amyotrophic Lateral Sclerosis mouse model. Front Cell Neurosci. 8:148.
  • Mayor S, Pagano RE. 2007. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol. 8:603.
  • McCaughey J, Stephens DJ. 2018. COPII-dependent ER export in animal cells: adaptation and control for diverse cargo. Histochem Cell Biol. 1:13.
  • McCray BA, Skordalakes E, Taylor JP. 2010. Disease mutations in Rab7 result in unregulated nucleotide exchange and inappropriate activation. Human Mol Genet. 19:1033–1047.
  • McLauchlan H, Newell J, Morrice N, Osborne A, West M, Smythe E. 1998. A novel role for Rab5-GDI in ligand sequestration into clathrin-coated pits. Curr Biol. 8:34–45.
  • Meyer T, Schwan A, Dullinger JS, Brocke J, Hoffmann K-T, Nolte CH, Hopt A, Kopp U, Andersen P, Epplen JT, Linke P. 2005. Early-onset ALS with long-term survival associated with spastin gene mutation. Neurology. 65:141–143.
  • Michell RH, Heath VL, Lemmon MA, Dove SK. 2006. Phosphatidylinositol 3,5-bisphosphate: metabolism and cellular functions. Trends Biochem Sci. 31:52–63.
  • Mignogna ML, Giannandrea M, Gurgone A, Fanelli F, Raimondi F, Mapelli L, Bassani S, Fang H, Van Anken E, Alessio M. 2015. The intellectual disability protein RAB39B selectively regulates GluA2 trafficking to determine synaptic AMPAR composition. Nat Commun. 6:6504.
  • Millecamps S, Gentil BJ, Gros-Louis F, Rouleau G, Julien J-P. 2005. Alsin is partially associated with centrosome in human cells. Biochim Biophys Acta. 1745:84–100.
  • Millecamps S, Robertson J, Lariviere R, Mallet J, Julien JP. 2006. Defective axonal transport of neurofilament proteins in neurons overexpressing peripherin. J Neurochem. 98:926–938.
  • Millecamps S, Da Barroca S, Cazeneuve C, Salachas F, Pradat P-F, Danel-Brunaud V, Vandenberghe N, Lacomblez L, Le Forestier N, Bruneteau G, et al. 2010. Questioning on the role of D amino acid oxidase in familial amyotrophic lateral sclerosis. Proc Natl Acad Sci. 107:E107–EE07.
  • Mitchell J, Paul P, Chen H-J, Morris A, Payling M, Falchi M, Habgood J, Panoutsou S, Winkler S, Tisato V. 2010. Familial amyotrophic lateral sclerosis is associated with a mutation in D-amino acid oxidase. Proc Natl Acad Sci.
  • Mizusawa H, Matsumoto S, Yen S-H, Hirano A, Rojas-Corona R, Donnenfeld H. 1989. Focal accumulation of phosphorylated neurofilaments within anterior horn cell in familial amyotrophic lateral sclerosis. Acta Neuropathol. 79:37–43.
  • Mizushima N, Komatsu M. 2011. Autophagy: renovation of cells and tissues. Cell. 147:728–741.
  • Moller A, Bauer CS, Cohen RN, Webster CP, De Vos KJ. 2017. Amyotrophic lateral sclerosis-associated mutant SOD1 inhibits anterograde axonal transport of mitochondria by reducing Miro1 levels. Human Mol Genet. 26:4668–4679.
  • Momeni P, Rogaeva E, Van Deerlin V, Yuan W, Grafman J, Tierney M, Huey E, Bell J, Morris CM, Kalaria RN, et al. 2006. Genetic variability in CHMP2B and frontotemporal dementia. Neurodegen Dis. 3:129–133.
  • Mori Y, Fukuda M, Henley JM. 2014. Small GTPase Rab17 regulates the surface expression of kainate receptors but not α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors in hippocampal neurons via dendritic trafficking of syntaxin-4 protein. J Biol Chem. 289:20773–20787.
  • Morimoto N, Nagai M, Ohta Y, Miyazaki K, Kurata T, Morimoto M, Murakami T, Takehisa Y, Ikeda Y, Kamiya T, et al. 2007. Increased autophagy in transgenic mice with a G93A mutant SOD1 gene. Brain Res. 1167:112–117.
  • Mori K, Weng S-M, Arzberger T, May S, Rentzsch K, Kremmer E, Schmid B, Kretzschmar HA, Cruts M, Van Broeckhoven C, et al. 2013. The C9orf72 GGGGCC repeat is translated into aggregating dipeptide-repeat proteins in FTLD/ALS. Science. 339:1335–1338.
  • Morris DH, Yip CK, Shi Y, Chait BT, Wang QJ. 2015. Beclin 1-Vps34 complex architecture: Understanding the nuts and bolts of therapeutic targets. Front Biol (Beijing). 10:398–426.
  • Mourelatos Z, Gonatas NK, Stieber A, Gurney ME, Dal Canto MC. 1996. The Golgi apparatus of spinal cord motor neurons in transgenic mice expressing mutant Cu, Zn superoxide dismutase becomes fragmented in early, preclinical stages of the disease. Proc Natl Acad Sci. 93:5472–5477.
  • Müller TJ, Kraya T, Stoltenburg-Didinger G, Hanisch F, Kornhuber M, Stoevesandt D, Senderek J, Weis J, Baum P, Deschauer M, Zierz S. 2014. Phenotype of matrin‐3–related distal myopathy in 16 G erman patients. Ann Neurol. 76:669–680.
  • Münch C, Sedlmeier R, Meyer T, Homberg V, Sperfeld A, Kurt A, Prudlo J, Peraus G, Hanemann C, Stumm G. 2004. Point mutations of the p150 subunit of dynactin (DCTN1) gene in ALS. Neurology. 63:724–726.
  • Münch C, Rosenbohm A, Sperfeld A-D, Uttner I, Reske S, Krause BJ, Sedlmeier R, Meyer T, Hanemann CO, Stumm G, Ludolph AC. 2005. Heterozygous R1101K mutation of the DCTN1 gene in a family with ALS and FTD. Ann Neurol. 58:777–780.
  • Nagabhushana A, Chalasani ML, Jain N, Radha V, Rangaraj N, Balasubramanian D, Swarup G. 2010. Regulation of endocytic trafficking of transferrin receptor by optineurin and its impairment by a glaucoma-associated mutant. BMC Cell Biol. 11:4.
  • Nakagomi S, Barsoum MJ, Bossy-Wetzel E, Sütterlin C, Malhotra V, Lipton SA. 2008. A Golgi fragmentation pathway in neurodegeneration. Neurobiol Dis. 29:221–231.
  • Nakano I, Shibata T, Uesaka Y. 1993. On the possibility of autolysosomal processing of skein-like inclusions: electron microscopic observation in a case of amyotrophic lateral sclerosis. J Neurol Sci. 120:54–59.
  • Nalbandian A, Llewellyn KJ, Badadani M, Yin HZ, Nguyen C, Katheria V, Watts G, Mukherjee J, Vesa J, Caiozzo V. 2013. A progressive translational mouse model of human valosin‐containing protein disease: The VCPR155H/+ mouse. Muscle Nerve. 47:260–270.
  • Nascimbeni AC, Giordano F, Dupont N, Grasso D, Vaccaro MI, Codogno P, Morel E. 2017. ER–plasma membrane contact sites contribute to autophagosome biogenesis by regulation of local PI3P synthesis. EMBO J.
  • Neumann M, Rademakers R, Roeber S, Baker M, Kretzschmar HA, Mackenzie IR. 2009. A new subtype of frontotemporal lobar degeneration with FUS pathology. Brain. 132:2922–2931.
  • Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, Bruce J, Schuck T, Grossman M, Clark CM, et al. 2006. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science. 314:130–133.
  • Nishimura AL, Mitne-Neto M, Silva HCA, Richieri-Costa A, Middleton S, Cascio D, Kok F, Oliveira JRM, Gillingwater T, Webb J, et al. 2004. A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am J Human Genet. 75:822–831.
  • Niwa S, Tanaka Y, Hirokawa N. 2008. KIF1Bbeta- and KIF1A-mediated axonal transport of presynaptic regulator Rab3 occurs in a GTP-dependent manner through DENN/MADD. Nat Cell Biol. 10:1269–1279.
  • Ohbayashi N, Fukuda M, Kanaho Y. 2017. Rab32 subfamily small GTPases: pleiotropic Rabs in endosomal trafficking. J Biochem. 162:65–71.
  • Onesto E, Colombrita C, Gumina V, Borghi MO, Dusi S, Doretti A, Fagiolari G, Invernizzi F, Moggio M, Tiranti V, et al. 2016. Gene-specific mitochondria dysfunctions in human TARDBP and C9ORF72 fibroblasts. Acta Neuropathol Commun. 4:47.
  • Orlacchio A, Babalini C, Borreca A, Patrono C, Massa R, Basaran S, Munhoz RP, Rogaeva EA, St George-Hyslop PH, Bernardi G, et al. 2010. SPATACSIN mutations cause autosomal recessive juvenile amyotrophic lateral sclerosis. Brain. 133:591–598.
  • Otomo A, Kunita R, Suzuki-Utsunomiya K, Mizumura H, Onoe K, Osuga H, Hadano S, Ikeda J-E. 2008. ALS2/alsin deficiency in neurons leads to mild defects in macropinocytosis and axonal growth. Biochem Biophys Res Commun. 370:87–92.
  • Pakdel M, von Blume J. 2018. Exploring new routes for secretory protein export from the trans-Golgi network. Mol Biol Cell. 29:235–240.
  • Park M, Penick EC, Edwards JG, Kauer JA, Ehlers MD. 2004. Recycling endosomes supply AMPA receptors for LTP. Science. 305:1972–1975.
  • Parkinson N, Ince PG, Smith MO, Highley R, Skibinski G, Andersen PM, Morrison KE, Pall HS, Hardiman O, Collinge J, et al. 2006. ALS phenotypes with mutations in CHMP2B (charged multivesicular body protein 2B). Neurology. 67:1074–1077.
  • Pavlos NJ, Grønborg M, Riedel D, Chua JJ, Boyken J, Kloepper TH, Urlaub H, Rizzoli SO, Jahn R. 2010. Quantitative analysis of synaptic vesicle Rabs uncovers distinct yet overlapping roles for Rab3a and Rab27b in Ca2+-triggered exocytosis. J Neurosci. 30:13441–13453.
  • Pelletier S, Gingras S, Howell S, Vogel P, Ihle JN. 2012. An early onset progressive motor neuron disorder in Scyl1-deficient mice is associated with mislocalization of TDP-43. J Neurosci. 32:16560–16573.
  • Perera ND, Sheean RK, Lau CL, Shin YS, Beart PM, Horne MK, Turner BJ. 2018. Rilmenidine promotes MTOR-independent autophagy in the mutant SOD1 mouse model of amyotrophic lateral sclerosis without slowing disease progression. Autophagy. 14:534–551.
  • Perlson E, Maday S, Fu M-m, Moughamian AJ, Holzbaur EL. 2010. Retrograde axonal transport: pathways to cell death?. Trends Neurosci. 33:335–344.
  • Perrone F, Nguyen HP, Van Mossevelde S, Moisse M, Sieben A, Santens P, De Bleecker J, Vandenbulcke M, Engelborghs S, Baets J. 2017. Investigating the role of ALS genes CHCHD10 and TUBA4A in Belgian FTD-ALS spectrum patients. Neurobiol Aging. 51:177.e9–77.e16.
  • Pfeffer S, Aivazian D. 2004. Targeting Rab GTPases to distinct membrane compartments. Nat Rev Mol Cell Biol. 5:886.
  • Piccioni F, Pinton P, Simeoni S, Pozzi P, Fascio U, Vismara G, Martini L, Rizzuto R, Poletti A. 2002. Androgen receptor with elongated polyglutamine tract forms aggregates that alter axonal trafficking and mitochondrial distribution in motor neuronal processes. FASEB J. 16:1418–1420.
  • Pilli M, Arko-Mensah J, Ponpuak M, Roberts E, Master S, Mandell MA, Dupont N, Ornatowski W, Jiang S, Bradfute SB, et al. 2012. TBK-1 promotes autophagy-mediated antimicrobial defense by controlling autophagosome maturation. Immunity. 37:223–234.
  • Pinarbasi ES, Cağatay T, Fung HYJ, Li YC, Chook YM, Thomas PJ. 2018. Active nuclear import and passive nuclear export are the primary determinants of TDP-43 localization. Sci Rep. 8:7083.
  • Pizzasegola C, Caron I, Daleno C, Ronchi A, Minoia C, Carrì MT, Bendotti C. 2009. Treatment with lithium carbonate does not improve disease progression in two different strains of SOD1 mutant mice. Amyotroph Lateral Sc. 10:221–228.
  • Pottier C, Bieniek KF, Finch NCole, van de Vorst M, Baker M, Perkersen R, Brown P, Ravenscroft T, van Blitterswijk M, Nicholson AM, et al. 2015. Whole-genome sequencing reveals important role for TBK1 and OPTN mutations in frontotemporal lobar degeneration without motor neuron disease. Acta Neuropathol. 130:77–92.
  • Preston A, Gurisik E, Bartley C, Laybutt D, Biden T. 2009. Reduced endoplasmic reticulum (ER)-to-Golgi protein trafficking contributes to ER stress in lipotoxic mouse beta cells by promoting protein overload. Diabetologia. 52:2369–2373.
  • Puls I, Jonnakuty C, LaMonte BH, Holzbaur ELF, Tokito M, Mann E, Floeter MK, Bidus K, Drayna D, Oh SJ, et al. 2003. Mutant dynactin in motor neuron disease. Nat Genet. 33:455.
  • Rabouille C. 2017. Pathways of unconventional protein secretion. Trends Cell Biol. 27:230–240.
  • Ramesh N, Pandey UB. 2017. Autophagy dysregulation in ALS: when protein aggregates get out of hand. Front Mol Neurosci. 10:263.
  • Ramírez OA, Couve A. 2011. The endoplasmic reticulum and protein trafficking in dendrites and axons. Trends Cell Biol. 21:219–227.
  • Razi M, Chan EY, Tooze SA. 2009. Early endosomes and endosomal coatomer are required for autophagy. J Cell Biol. 185:305–321.
  • Reiterer V, Maier S, Sitte HH, Kriz A, Rüegg MA, Hauri H-P, Freissmuth M, Farhan H. 2008. Sec24- and ARFGAP1-dependent trafficking of GABA transporter-1 is a prerequisite for correct axonal targeting. J Neurosci. 28:12453–12464.
  • Renton AE, Majounie E, Waite A, Simón-Sánchez J, Rollinson S, Gibbs JR, Schymick JC, Laaksovirta H, van Swieten JC, Myllykangas L, et al. 2011. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron. 72:257–268.
  • Richter B, Sliter DA, Herhaus L, Stolz A, Wang C, Beli P, Zaffagnini G, Wild P, Martens S, Wagner SA, et al. 2016. Phosphorylation of OPTN by TBK1 enhances its binding to Ub chains and promotes selective autophagy of damaged mitochondria. Proc Natl Acad Sci. 113:4039. 44
  • Ritz D, Vuk M, Kirchner P, Bug M, Schütz S, Hayer A, Bremer S, Lusk C, Baloh RH, Lee H, et al. 2011. Endolysosomal sorting of ubiquitylated caveolin-1 is regulated by VCP and UBXD1 and impaired by VCP disease mutations. Nat Cell Biol. 13:1116.
  • Rohrer JD, Guerreiro R, Vandrovcova J, Uphill J, Reiman D, Beck J, Isaacs AM, Authier A, Ferrari R, Fox NC, et al. 2009. The heritability and genetics of frontotemporal lobar degeneration. Neurology. 73:1451–1456.
  • Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng H-X, et al. 1993. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature. 362:59–62.
  • Rubino E, Rainero I, Chiò A, Rogaeva E, Galimberti D, Fenoglio P, Grinberg Y, Isaia G, Calvo A, Gentile S, et al. 2012. SQSTM1 mutations in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Neurology. 79:1556–1562.
  • Rusten TE, Simonsen A. 2008. ESCRT functions in autophagy and associated disease. Cell Cycle. 7:1166–1172.
  • Rutherford NJ, Zhang Y-J, Baker M, Gass JM, Finch NA, Xu Y-F, Stewart H, Kelley BJ, Kuntz K, Crook RJP, et al. 2008. Novel mutations in TARDBP (TDP-43) in patients with familial amyotrophic lateral sclerosis. PLoS Genet. 4:e1000193.
  • Ryu H-H, Jun M-H, Min K-J, Jang D-J, Lee Y-S, Kim HK, Lee J-A. 2014. Autophagy regulates amyotrophic lateral sclerosis-linked fused in sarcoma-positive stress granules in neurons. Neurobiol Aging. 35:2822–2831.
  • Sahlender DA, Roberts RC, Arden SD, Spudich G, Taylor MJ, Luzio JP, Kendrick-Jones J, Buss F. 2005. Optineurin links myosin VI to the Golgi complex and is involved in Golgi organization and exocytosis. J Cell Biol. 169:285–295.
  • Saraste J. 2016. Spatial and functional aspects of ER-Golgi Rabs and tethers. Front Cell Dev Biol. 4:28.
  • Sasaki S. 2011. Autophagy in spinal cord motor neurons in sporadic amyotrophic lateral sclerosis. J Neuropathol Exp Neurol. 70:349–359.
  • Sasaki S, Iwata M. 2007. Mitochondrial alterations in the spinal cord of patients with sporadic amyotrophic lateral sclerosis. J Neuropathol Exp Neurol. 66:10–16.
  • Sasaki S, Maruyama S, Yamane K, Sakuma H, Takeishi M. 1990. Ultrastructure of swollen proximal axons of anterior horn neurons in motor neuron disease. J Neurol Sci. 97:233–240.
  • Sau D, Rusmini P, Crippa V, Onesto E, Bolzoni E, Ratti A, Poletti A. 2011. Dysregulation of axonal transport and motorneuron diseases. Biol Cell. 103:87–107.
  • Saxena S, Cabuy E, Caroni P. 2009. A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat Neurosci. 12:627.
  • Schlüter OM, Schmitz F, Jahn R, Rosenmund C, Südhof TC. 2004. A complete genetic analysis of neuronal Rab3 function. J Neurosci. 24:6629–6637.
  • Schmidt HB, Görlich D. 2016. Transport selectivity of nuclear pores, phase separation, and membraneless organelles. Trends Biochem Sci. 41:46–61.
  • Schonteich E, Wilson GM, Burden J, Hopkins CR, Anderson K, Goldenring JR, Prekeris R. 2008. The Rip11/Rab11-FIP5 and kinesin II complex regulates endocytic protein recycling. J Cell Sci. 121:3824–3833.
  • Schwenk BM, Hartmann H, Serdaroglu A, Schludi MH, Hornburg D, Meissner F, Orozco D, Colombo A, Tahirovic S, Michaelsen M. 2016. TDP‐43 loss of function inhibits endosomal trafficking and alters trophic signaling in neurons. EMBO J.
  • Scotter EL, Chen H-J, Shaw CE. 2015. TDP-43 proteinopathy and ALS: insights into disease mechanisms and therapeutic targets. Neurotherapeutics. 12:352–363.
  • Sellier C, Campanari M‐L, Julie Corbier C, Gaucherot A, Kolb‐Cheynel I, Oulad‐Abdelghani M, Ruffenach F, Page A, Ciura S, Kabashi E, et al. 2016. Loss of C9ORF72 impairs autophagy and synergizes with polyQ Ataxin‐2 to induce motor neuron dysfunction and cell death. EMBO J. 35:1276–1297.
  • Semerdjieva S, Shortt B, Maxwell E, Singh S, Fonarev P, Hansen J, Schiavo G, Grant BD, Smythe E. 2008. Coordinated regulation of AP2 uncoating from clathrin-coated vesicles by rab5 and hRME-6. J Cell Biol. 183:499–511.
  • Sephton CF, Cenik C, Kucukural A, Dammer EB, Cenik B, Han Y-H, Dewey CM, Roth FP, Herz J, Peng J. 2010. Identification of neuronal RNA targets of TDP-43-containing ribonucleoprotein complexes. J Biol Chem. M110:190884.
  • Sheehan P, Zhu M, Beskow A, Vollmer C, Waites CL. 2016. Activity-dependent degradation of synaptic vesicle proteins requires Rab35 and the ESCRT pathway. J Neurosci. 36:8668–8686.
  • Shi P, Gal J, Kwinter DM, Liu X, Zhu H. 2010. Mitochondrial dysfunction in amyotrophic lateral sclerosis. Biochim Biophys Acta Mol Basis Dis. 1802:45–51.
  • Shi Y, Lin S, Staats KA, Li Y, Chang W-H, Hung S-T, Hendricks E, Linares GR, Wang Y, Son EY, et al. 2018. Haploinsufficiency leads to neurodegeneration in C9ORF72 ALS/FTD human induced motor neurons. Nat Med. 24:313.
  • Shimizu H, Kawamura S, Ozaki K. 2003. An essential role of Rab5 in uniformity of synaptic vesicle size. J Cell Sci. 116:3583–3590.
  • Shi KY, Mori E, Nizami ZF, Lin Y, Kato M, Xiang S, Wu LC, Ding M, Yu Y, Gall JG, McKnight SL. 2017. Toxic PRn poly-dipeptides encoded by the C9orf72 repeat expansion block nuclear import and export. Proc Natl Acad Sci. 114:E1111–E1E17.
  • Shin N, Jeong H, Kwon J, Heo HY, Kwon JJ, Yun HJ, Kim C-H, Han BS, Tong Y, Shen J, et al. 2008. LRRK2 regulates synaptic vesicle endocytosis. Exp Cell Res. 314:2055–2065.
  • Simpson CL, Lemmens R, Miskiewicz K, Broom WJ, Hansen VK, van Vught PWJ, Landers JE, Sapp P, Van Den Bosch L, Knight J, et al. 2009. Variants of the elongator protein 3 (ELP3) gene are associated with motor neuron degeneration. Hum Mol Genet. 18:472–481.
  • Sivadasan R, Hornburg D, Drepper C, Frank N, Jablonka S, Hansel A, Lojewski X, Sterneckert J, Hermann A, Shaw PJ, et al. 2016. C9ORF72 interaction with cofilin modulates actin dynamics in motor neurons. Nat Neurosci. 19:1610–1618.
  • Skibinski G, Parkinson NJ, Brown JM, Chakrabarti L, Lloyd SL, Hummerich H, Nielsen JE, Hodges JR, Spillantini MG, Thusgaard T, et al. 2005. Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat Genet. 37:806.
  • Smith BN, Ticozzi N, Fallini C, Gkazi AS, Topp S, Kenna KP, Scotter EL, Kost J, Keagle P, Miller JW, et al. 2014. Exome-wide rare variant analysis identifies TUBA4A mutations associated with familial ALS. Neuron. 84:324–331.
  • Smith BN, Topp SD, Fallini C, Shibata H, Chen H-J, Troakes C, King A, Ticozzi N, Kenna KP, Soragia-Gkazi A, et al. 2017. Mutations in the vesicular trafficking protein annexin A11 are associated with amyotrophic lateral sclerosis. Sci Transl Med. 9:eaad9157.
  • Smith BN, Vance C, Scotter EL, Troakes C, Wong CH, Topp S, Maekawa S, King A, Mitchell JC, Lund K. 2014. Novel mutations support a role for Profilin1 in the pathogenesis of ALS. Neurobiol Aging. 36:e17–e27.
  • Soo K, Sultana J, King A, Atkinson R, Warraich S, Sundaramoorthy V, Blair I, Farg M, Atkin J. 2015. ALS-associated mutant FUS inhibits macroautophagy which is restored by overexpression of Rab1. Cell Death Discov. 1:15030.
  • Soo KY, Halloran M, Sundaramoorthy V, Parakh S, Toth RP, Southam KA, McLean CA, Lock P, King A, Farg MA, et al. 2015. Rab1-dependent ER-Golgi transport dysfunction is a common pathogenic mechanism in SOD1, TDP-43 and FUS-associated ALS. Acta Neuropathol. 130:679–697.
  • Spinosa MR, Progida C, De Luca A, Colucci AMR, Alifano P, Bucci C. 2008. Functional characterization of Rab7 mutant proteins associated with Charcot-Marie-Tooth type 2B disease. J Neurosci. 28:1640–1648.
  • Sreedharan J, Blair IP, Tripathi VB, Hu X, Vance C, Rogelj B, Ackerley S, Durnall JC, Williams KL, Buratti E, et al. 2008. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science. 319:1668–1672.
  • Štalekar M, Yin X, Rebolj K, Darovic S, Troakes C, Mayr M, Shaw C, Rogelj B. 2015. Proteomic analyses reveal that loss of TDP-43 affects RNA processing and intracellular transport. Neuroscience. 293:157–170.
  • Starr A, Sattler R. 2018. Synaptic dysfunction and altered excitability in C9ORF72 ALS/FTD. Brain Res. 1693:98–108.
  • Stenmark H. 2009. Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol. 10:513.
  • Stenmark H, Olkkonen VM. 2001. The rab gtpase family. Genome Biol. 2:Reviews3007.
  • Stoica R, De Vos KJ, Paillusson S, Mueller S, Sancho RM, Lau K-F, Vizcay-Barrena G, Lin W-L, Xu Y-F, Lewis J, et al. 2014. ER-mitochondria associations are regulated by the VAPB-PTPIP51 interaction and are disrupted by ALS/FTD-associated TDP-43. Nat Commun. 5:3996.
  • Stoica R, Paillusson S, Gomez-Suaga P, Mitchell JC, Lau DH, Gray EH, Sancho RM, Vizcay-Barrena G, De Vos KJ, Shaw CE, et al. 2016. ALS/FTD-associated FUS activates GSK-3β to disrupt the VAPB-PTPIP51 interaction and ER-mitochondria associations. EMBO Rep. 17:1326–1342.
  • Storrie B, White J, Röttger S, Stelzer EH, Suganuma T, Nilsson T. 1998. Recycling of Golgi-resident glycosyltransferases through the ER reveals a novel pathway and provides an explanation for nocodazole-induced Golgi scattering. J Cell Biol. 143:1505–1521.
  • Strong MJ. 2010. The evidence for altered RNA metabolism in amyotrophic lateral sclerosis (ALS). J Neurol Sci. 288:1–12.
  • Sundaramoorthy V, Sultana JM, Atkin JD. 2015. Golgi fragmentation in amyotrophic lateral sclerosis, an overview of possible triggers and consequences. Front Neurosci. 9:400.
  • Sundaramoorthy V, Walker AK, Tan V, Fifita JA, Mccann EP, Williams KL, Blair IP, Guillemin GJ, Farg MA, Atkin JD. 2015. Defects in optineurin- and myosin VI-mediated cellular trafficking in amyotrophic lateral sclerosis. Hum Mol Genet. 24:3830–3846.
  • Sundaramoorthy V, Walker AK, Yerbury J, Soo KY, Farg MA, Hoang V, Zeineddine R, Spencer D, Atkin JD. 2013. Extracellular wildtype and mutant SOD1 induces ER-Golgi pathology characteristic of amyotrophic lateral sclerosis in neuronal cells. Cell Mol Life Sci. 70:4181–4195.
  • Synofzik M, Maetzler W, Grehl T, Prudlo J, vom Hagen JM, Haack T, Rebassoo P, Munz M, Schöls L, Biskup S. 2012. Screening in ALS and FTD patients reveals 3 novel UBQLN2 mutations outside the PXX domain and a pure FTD phenotype. Neurobiol Aging. 33:2949.e13–2949.e17.
  • Szatmári Z, Kis V, Lippai M, Hegedus K, Faragó T, Lorincz P, Tanaka T, Juhász G, Sass M. 2014. Rab11 facilitates cross-talk between autophagy and endosomal pathway through regulation of Hook localization. Mol Biol Cell. 25:522–531.
  • Szodorai A, Kuan Y-H, Hunzelmann S, Engel U, Sakane A, Sasaki T, Takai Y, Kirsch J, Müller U, Beyreuther K, et al. 2009. APP anterograde transport requires Rab3A GTPase activity for assembly of the transport vesicle. J Neurosci. 29:14534–14544.
  • Takahashi Y, Fukuda Y, Yoshimura J, Toyoda A, Kurppa K, Moritoyo H, Belzil VV, Dion PA, Higasa K, Doi K, et al. 2013. ERBB4 mutations that disrupt the neuregulin-ErbB4 pathway cause amyotrophic lateral sclerosis type 19. Am J Hum Genet. 93:900–905.
  • Talaber G, Miklossy G, Oaks Z, Liu Y, Tooze SA, Chudakov DM, Banki K, Perl A. 2014. HRES-1/Rab4 promotes the formation of LC3(+) autophagosomes and the accumulation of mitochondria during autophagy. PLoS One. 9:e84392.
  • Tanaka Y, Nonaka T, Suzuki G, Kametani F, Hasegawa M. 2016. Gain-of-function profilin 1 mutations linked to familial amyotrophic lateral sclerosis cause seed-dependent intracellular TDP-43 aggregation. Hum Mol Genet. 25:1420–1433.
  • Teuling E, Ahmed S, Haasdijk E, Demmers J, Steinmetz MO, Akhmanova A, Jaarsma D, Hoogenraad CC. 2007. Motor neuron disease-associated mutant vesicle-associated membrane protein-associated protein (VAP) B recruits wild-type VAPs into endoplasmic reticulum-derived tubular aggregates. J Neurosci. 27:9801–9815.
  • Teyssou E, Chartier L, Lam R, Lautrette G, Nicol M, Machat S, Da Barroca S, Moigneu C, Mairey M, Larmonier T. 2017. Novel UBQLN2 mutations linked to amyotrophic lateral sclerosis and atypical hereditary spastic paraplegia phenotype through defective HSP70-mediated proteolysis. Neurobiol Aging. 58:239.e11–239.e20
  • Tian F, Morimoto N, Liu W, Ohta Y, Deguchi K, Miyazaki K, Abe K. 2011. In vivo optical imaging of motor neuron autophagy in a mouse model of amyotrophic lateral sclerosis. Autophagy. 7:985–992.
  • Ticozzi N, Vance C, LeClerc AL, Keagle P, Glass JD, McKenna-Yasek D, Sapp PC, Silani V, Bosco DA, Shaw CE, et al. 2011. Mutational analysis reveals the FUS homolog TAF15 as a candidate gene for familial amyotrophic lateral sclerosis. Am J Med Genet Part B Neuropsychiatr Genet. 156:285–290.
  • Tong J, Huang C, Bi F, Wu Q, Huang B, Zhou H. 2012. XBP1 depletion precedes ubiquitin aggregation and Golgi fragmentation in TDP-43 transgenic rats. J Neurochem. 123:406–416.
  • Toth RP, Atkin JD. 2018. Dysfunction of optineurin in amyotrophic lateral sclerosis and glaucoma. Front Immunol. 9:1017.
  • Touchot N, Chardin P, Tavitian A. 1987. Four additional members of the ras gene superfamily isolated by an oligonucleotide strategy: molecular cloning of YPT-related cDNAs from a rat brain library. Proc Natl Acad Sci. 84:8210–8214.
  • Tradewell ML, Yu Z, Tibshirani M, Boulanger M-C, Durham HD, Richard S. 2012. Arginine methylation by PRMT1 regulates nuclear-cytoplasmic localization and toxicity of FUS/TLS harbouring ALS-linked mutations. Hum Mol Genet. 21:136–149.
  • Tzeng H-T, Wang Y-C. 2016. Rab-mediated vesicle trafficking in cancer. J Biomed Sci. 23:70.
  • Urwin H, Authier A, Nielsen JE, Metcalf D, Powell C, Froud K, Malcolm DS, Holm I, Johannsen P, Brown J, et al. 2010. Disruption of endocytic trafficking in frontotemporal dementia with CHMP2B mutations. Hum Mol Genet. 19:2228–2238.
  • Uytterhoeven V, Kuenen S, Kasprowicz J, Miskiewicz K, Verstreken P. 2011. Loss of skywalker reveals synaptic endosomes as sorting stations for synaptic vesicle proteins. Cell. 145:117–132.
  • van der Zee J, Gijselinck I, Van Mossevelde S, Perrone F, Dillen L, Heeman B, Bäumer V, Engelborghs S, De Bleecker J, Baets J, et al. 2017. TBK1 mutation spectrum in an extended European patient cohort with frontotemporal dementia and amyotrophic lateral sclerosis. Hum Mutat. 38:297–309.
  • van Dis V, Kuijpers M, Haasdijk ED, Teuling E, Oakes SA, Hoogenraad CC, Jaarsma D. 2014. Golgi fragmentation precedes neuromuscular denervation and is associated with endosome abnormalities in SOD1-ALS mouse motor neurons. Acta Neuropathol Commun. 2:38.
  • Van Swieten JC, Heutink P. 2008. Mutations in progranulin (GRN) within the spectrum of clinical and pathological phenotypes of frontotemporal dementia. Lancet Neurol. 7:965–974.
  • van Vliet AR, Verfaillie T, Agostinis P. 2014. New functions of mitochondria associated membranes in cellular signaling. Biochim Biophys Acta. 1843:2253–2262.
  • Vance C, Rogelj B, Hortobagyi T, De Vos KJ, Nishimura AL, Sreedharan J, Hu X, Smith B, Ruddy D, Wright P, et al. 2009. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science. 323:1208–1211.
  • Veleri S, Punnakkal P, Dunbar GL, Maiti P. 2018. Molecular insights into the roles of Rab proteins in intracellular dynamics and neurodegenerative diseases. Neuromol Med. 20: 18–36. doi:10.1007/s12017-018-8479-9
  • Verstraete E, Veldink JH, Huisman MH, Draak T, Uijtendaal EV, van der Kooi AJ, Schelhaas HJ, de Visser M, van der Tweel I, van den Berg LH. 2012. Lithium lacks effect on survival in amyotrophic lateral sclerosis: a phase IIb randomised sequential trial. J Neurol Neurosurg Psychiatry. 83:557–564.
  • Vollrath JT, Sechi A, Dreser A, Katona I, Wiemuth D, Vervoorts J, Dohmen M, Chandrasekar A, Prause J, Brauers E, et al. 2014. Loss of function of the ALS protein SigR1 leads to ER pathology associated with defective autophagy and lipid raft disturbances. Cell Death Dis. 5:e1290.
  • von Mollard Fischer G, Stahl B, Walch-Solimena C, Takei K, Daniels L, Khoklatchev A, De PC, Südhof TC, Jahn R. 1994. Localization of Rab5 to synaptic vesicles identifies endosomal intermediate in synaptic vesicle recycling pathway. Eur J Cell Biol. 65:319–326.
  • Wang W, Li L, Lin W-L, Dickson DW, Petrucelli L, Zhang T, Wang X. 2013. The ALS disease-associated mutant TDP-43 impairs mitochondrial dynamics and function in motor neurons. Human Mol Genet. 22:4706–4719.
  • Wang T, Ming Z, Xiaochun W, Hong W. 2011. Rab7: role of its protein interaction cascades in endo-lysosomal traffic. Cell Signal. 23:516–521.
  • Ward ME, Taubes A, Chen R, Miller BL, Sephton CF, Gelfand JM, Minami S, Boscardin J, Martens LH, Seeley WW, et al. 2014. Early retinal neurodegeneration and impaired Ran-mediated nuclear import of TDP-43 in progranulin-deficient FTLD. J Exp Med. 211:1937–1945.
  • Watanabe S, Ilieva H, Tamada H, Nomura H, Komine O, Endo F, Jin S, Mancias P, Kiyama H, Yamanaka K. 2016. Mitochondria‐associated membrane collapse is a common pathomechanism in SIGMAR1‐and SOD1‐linked ALS. EMBO Mol Med. 8:1421–1437.
  • Webster CP, Smith EF, Bauer CS, Moller A, Hautbergue GM, Ferraiuolo L, Myszczynska MA, Higginbottom A, Walsh MJ, Whitworth AJ. 2016. The C9orf72 protein interacts with Rab1a and the ULK1 complex to regulate initiation of autophagy. EMBO J.
  • Weis K. 2003. Regulating access to the genome: nucleocytoplasmic transport throughout the cell cycle. Cell. 112:441–451.
  • Wen X, Tan W, Westergard T, Krishnamurthy K, Markandaiah SS, Shi Y, Lin S, Shneider NA, Monaghan J, Pandey UB, et al. 2014. Antisense proline-arginine RAN dipeptides linked to C9ORF72-ALS/FTD form toxic nuclear aggregates that initiate in vitro and in vivo neuronal death. Neuron. 84:1213–1225.
  • White J, Johannes L, Mallard F, Girod A, Grill S, Reinsch S, Keller P, Tzschaschel B, Echard A, Goud B, et al. 1999. Rab6 coordinates a novel Golgi to ER retrograde transport pathway in live cells. J Cell Biol. 147:743–760.
  • Williams KL, Topp S, Yang S, Smith B, Fifita JA, Warraich ST, Zhang KY, Farrawell N, Vance C, Hu X, et al. 2016. CCNF mutations in amyotrophic lateral sclerosis and frontotemporal dementia. Nat Commun. 7:11253.
  • Williams KL, Warraich ST, Yang S, Solski JA, Fernando R, Rouleau GA, Nicholson GA, Blair IP. 2012. UBQLN2/ubiquilin 2 mutation and pathology in familial amyotrophic lateral sclerosis. Neurobiol Aging. 33:2527.e3–2527.e10.
  • Wilson GR, Sim JCH, McLean C, Giannandrea M, Galea CA, Riseley JR, Stephenson SEM, Fitzpatrick E, Haas SA, Pope K, et al. 2014. Mutations in RAB39B cause X-linked intellectual disability and early-onset Parkinson disease with α-synuclein pathology. Am J Hum Genet. 95:729–735.
  • Woehlbier U, Colombo A, Saaranen MJ, Pérez V, Ojeda J, Bustos FJ, Andreu CI, Torres M, Valenzuela V, Medinas DB, et al. 2016. ALS-linked protein disulfide isomerase variants cause motor dysfunction . Embo J. 35:845–865.
  • Wu Y, Whiteus C, Xu CS, Hayworth KJ, Weinberg RJ, Hess HF, De Camilli P. 2017. Contacts between the endoplasmic reticulum and other membranes in neurons. Proc Natl Acad Sci. 114:E4859–E4E67.
  • Wu D, Yu WH, Kishikawa H, Folkerth RD, Iafrate AJ, Shen YP, Xin WM, Sims K, Hu GF. 2007. Angiogenin loss-of-function mutations in amyotrophic lateral sclerosis. Ann Neurol. 62:609–617.
  • Wucherpfennig T, Wilsch-Bräuninger M, González-Gaitán M. 2003. Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J Cell Biol. 161:609–624.
  • Wu C-H, Fallini C, Ticozzi N, Keagle PJ, Sapp PC, Piotrowska K, Lowe P, Koppers M, McKenna-Yasek D, Baron DM, et al. 2012. Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis. Nature. 488:499.
  • Xiao S, Tjostheim S, Sanelli T, McLean JR, Horne P, Fan Y, Ravits J, Strong MJ, Robertson J. 2008. An aggregate-inducing peripherin isoform generated through intron retention is upregulated in amyotrophic lateral sclerosis and associated with disease pathology. J Neurosci. 28:1833–1840.
  • Xie Z, Klionsky DJ. 2007. Autophagosome formation: core machinery and adaptations. Nat Cell Biol. 9:1102.
  • Yang X, Li X, Zhang Y, Rodriguez-Rodriguez L, Xiang M, Wang H-Y, Zheng XS. 2016. Rab1 in cell signaling, cancer and other diseases. Oncogene. 35:5699.
  • Yang Y, Hentati A, Deng H-X, Dabbagh O, Sasaki T, Hirano M, Hung W-Y, Ouahchi K, Yan J, Azim AC, et al. 2001. The gene encoding alsin, a protein with three guanine-nucleotide exchange factor domains, is mutated in a form of recessive amyotrophic lateral sclerosis. Nat Genet. 29:160.
  • Yin H, Nalbandian A, Hsu C, Li S, Llewellyn K, Mozaffar T, Kimonis V, Weiss J. 2012. Slow development of ALS-like spinal cord pathology in mutant valosin-containing protein gene knock-in mice. Cell Death Dis. 3:e374.
  • Ying H, Turturro S, Nguyen T, Shen X, Zelkha R, Johnson EC, Morrison JC, Yue BY. 2015. Induction of autophagy in rats upon overexpression of wild-type and mutant optineurin gene. BMC Cell Biol. 16:14.
  • Ylä-Anttila P, Mikkonen E, Happonen KE, Holland P, Ueno T, Simonsen A, Eskelinen E-L. 2015. RAB24 facilitates clearance of autophagic compartments during basal conditions. Autophagy. 11:1833–1848.
  • Yu C-E, Bird TD, Bekris LM, Montine TJ, Leverenz JB, Steinbart E, Galloway NM, Feldman H, Woltjer R, Miller CA. 2010. The spectrum of mutations in progranulin: a collaborative study screening 545 cases of neurodegeneration. Archiv Neurol. 67:161–170.
  • Zhang X, Chen S, Song L, Tang Y, Shen Y, Jia L, Le W. 2014. MTOR-independent, autophagic enhancer trehalose prolongs motor neuron survival and ameliorates the autophagic flux defect in a mouse model of amyotrophic lateral sclerosis. Autophagy. 10:588–602.
  • Zhang J, Fonovic M, Suyama K, Bogyo M, Scott MP. 2009. Rab35 controls actin bundling by recruiting fascin as an effector protein. Science (NY). 325:1250–1254.
  • Zhang X, Li L, Chen S, Yang D, Wang Y, Zhang X, Wang Z, Le W. 2011. Rapamycin treatment augments motor neuron degeneration in SOD1G93A mouse model of amyotrophic lateral sclerosis. Autophagy. 7:412–425.
  • Zhang K, Daigle JG, Cunningham KM, Coyne AN, Ruan K, Grima JC, Bowen KE, Wadhwa H, Yang P, Rigo F, et al. 2018. Stress granule assembly disrupts nucleocytoplasmic transport. Cell. 173:958–971.e17.
  • Zhang K, Donnelly CJ, Haeusler AR, Grima JC, Machamer JB, Steinwald P, Daley EL, Miller SJ, Cunningham KM, Vidensky S, et al. 2015. The C9orf72 repeat expansion disrupts nucleocytoplasmic transport. Nature. 525:56.
  • Zhang DL, Dubey J, Koushika SP, Rongo C. 2016. RAB-6.1 and RAB-6.2 Promote Retrograde Transport in C-elegans. Plos One. 11.
  • Zhang M, Xi Z, Zinman L, Bruni AC, Maletta RG, Curcio SAM, Rainero I, Rubino E, Pinessi L, Nacmias B, et al. 2015. Mutation analysis of CHCHD10 in different neurodegenerative diseases. Brain. 138:e380.
  • Zhen Y, Stenmark H. 2015. Cellular functions of Rab GTPases at a glance. J Cell Sci. 128:3171–3176.

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