Autophagy and Its Comprehensive Impact on ALS

REFERENCES

• Rowland LP. Amyotrophic lateral sclerosis. Curr Opin Neurol. 1994;7:310–15.
   PubMed Web of Science ®Google Scholar
• Ciechanover A. The ubiquitin proteolytic system: from a vague idea, through basic mechanisms, and onto human diseases and drug targeting. Neurology. 2006;66:7–19.
   PubMed Web of Science ®Google Scholar
• Ferrucci M, Fulceri F, Toti L, Soldani P, Siciliano G, Paparelli A, Fornai F. Protein clearing pathways in ALS. Archives Italiennes de Biologie. 2011;149:121–49.
   PubMed Web of Science ®Google Scholar
• Tan JM, Wong ES, Kirkpatrick DS, Pletnikova O, Ko HS, Tay SP, Ho MW, Troncoso J, Gygi SP, Lee MK, Dawson VL, Dawson TM, Lim KL. Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum Mol Genet. 2008;17:431–9.
   PubMed Web of Science ®Google Scholar
• Ravikumar B, Vacher C, Berger Z, Davies JE, Luo S, Oroz LG, Scaravilli F, Easton DF, Duden R, O'Kane CJ, Rubinsztein DC. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet. 2004;36:585–95.
   PubMed Web of Science ®Google Scholar
• Tain LS, Mortiboys H, Tao RN, Ziviani E, Bandmann O, Whitworth AJ. Rapamycin activation of 4E-BP prevents parkinsonian dopaminergic neuron loss. Nat Neurosci. 2009;12:1129–35.
   PubMed Web of Science ®Google Scholar
• Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010;221:3–12.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science. 2000;290:1717–21.
   PubMed Web of Science ®Google Scholar
• Kirkin V, McEwan DG, Novak I, Dikic I. A role for ubiquitin in selective autophagy. Mol Cell. 2009;34:259–69.
   PubMed Web of Science ®Google Scholar
• Sarkar S, Ravikumar B, Rubinsztein DC. Autophagic clearance of aggregate-prone proteins associated with neurodegeneration. Methods Enzymol. 2009;453:83–110.
   PubMed Web of Science ®Google Scholar
• Komatsu M, Waguri S, Koike M, Sou YS, Ueno T, Hara T, Mizushima N, Iwata J, Ezaki J, Murata S, Hamazaki J, Nishito Y, Iemura S, Natsume T, Yanagawa T, Uwayama J, Warabi E, Yoshida H, Ishii T, Kobayashi A, Yamamoto M, Yue Z, Uchiyama Y, Kominami E, Tanaka K. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell. 2007;131:1149–63.
   PubMed Web of Science ®Google Scholar
• Zheng YT, Shahnazari S, Brech A, Lamark T, Johansen T, Brumell JH. The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway. J Immunol. 2009;183:5909–16.
   PubMed Web of Science ®Google Scholar
• Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H, Øvervatn A, Bjørkøy G, Johansen T. p62/SQSTM1 binds directly toAtg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem. 2007;282:24131–145.
   PubMed Web of Science ®Google Scholar
• Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol. 2009;10:458–67.
   PubMed Web of Science ®Google Scholar
• Nazarko VY, Nazarko TY, Farre JC, Stasyk OV, Warnecke D, Ulaszewski S, Cregg JM, Sibirny AA, Subramani S. Atg35, a micropexophagy-specific protein that regulates micropexophagic apparatus formation in Pichiapastoris. Autophagy. 2011;7:375–85.
   PubMed Web of Science ®Google Scholar
• Mizushima N. Autophagy: process and function. Genes Dev. 2007;21:2861–73.
   PubMed Web of Science ®Google Scholar
• Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000;19:5720–5728.
   PubMed Web of Science ®Google Scholar
• Eskelinen EL. Maturation of autophagic vacuoles in mammalian cells. Autophagy. 2005;1:1–10.
   PubMed Web of Science ®Google Scholar
• He C, Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet. 2009;43:67–93.
   PubMed Web of Science ®Google Scholar
• Cuervo, AM. Chaperone-mediated autophagy: selectivity pays off. Trends Endocrinol Metab. 2010;21:142–150.
   PubMed Web of Science ®Google Scholar
• Kon M, Cuervo AM. Chaperone-mediated autophagy in health and disease. FEBS Lett. 2010;584:1399–1404.
   PubMed Web of Science ®Google Scholar
• Díaz-Troya S, Pérez–Pérez ME, Florencio FJ, Crespo JL. The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy. 2008;4:851–65.
   PubMed Web of Science ®Google Scholar
• Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B, Wyss-Coray T. The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest. 2008;118(6):2190–99.
   PubMed Web of Science ®Google Scholar
• Shibata M, Lu T, Furuya T, Degterev A, Mizushima N, Yoshimori T, MacDonald M, Yankner B, Yuan J. Regulation of intracellular accumulation of mutant Huntingtin by Beclin 1. J Biol Chem. 2006;281:14474–85.
   PubMed Web of Science ®Google Scholar
• Erlich S, Shohami E, Pinkas-Kramarski R. Neurodegeneration induces upregulation of Beclin 1. Autophagy. 2006;2:49–51.
   PubMed Web of Science ®Google Scholar
• Petiot A, Ogier-Denis E, Blommaart EF, Meijer AJ, Condogno P. Distinct classes of phosphatidylinositol 30-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem. 2000;275:992–8.
   PubMed Web of Science ®Google Scholar
• Waterman-Storer CM, Karki SB, Kuznetsov SA, Tabb JS, Weiss DG, Langford GM, Holzbaur EL. The interaction between cytoplasmic dynein and dynactin is required for fast axonal transport. Proc Natl Acad Sci USA. 1997;94:12180–85.
   PubMed Web of Science ®Google Scholar
• Yamamoto M, Suzuki SO, Himeno M. The effects of dynein inhibition on the autophagic pathway in glioma cells. Neuropathology. 2010;30:1–6.
   PubMed Web of Science ®Google Scholar
• Cai Q, Lu L, Tian JH, Zhu YB, Qiao H, Sheng ZH. Snapin-regulated late endosomal transport is critical for efficient autophagy-lysosomal function in neurons. Neuron. 2010;68:73–86.
   PubMed Web of Science ®Google Scholar
• Shoichi Sasaki. Autophagy in Spinal Cord Motor Neurons in Sporadic Amyotrophic Lateral Sclerosis. J Neuropathol Exp Neurol. 2011;70(5):349–59.
   PubMed Web of Science ®Google Scholar
• Kroemer G, Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol. 2008;9:1004–10.
   PubMed Web of Science ®Google Scholar
• Sasaki Y, Vohra BP, Baloh RH, Milbrandt J. Transgenic mice expressing the Nmnat1 protein manifest robust delay in axonal degeneration in vivo. J Neurosci. 2009;29:6526–34.
   PubMed Web of Science ®Google Scholar
• Hetz C, Thielen P, Matus S, Nassif M, Court F, Kiffin R, Martinez G, Cuervo AM, Brown RH, Glimcher LH. XBP-1 deficiency in the nervous system protects against amyotrophic lateral sclerosis by increasing autophagy. Genes Dev. 2009;23:2294–3000.
   PubMed Web of Science ®Google Scholar
• Li L, Zhang X, Le W. Altered macroautophagy in the spinal cord of SOD1 mutant mice. Autophagy. 2008;4: 290–293.
   PubMed Web of Science ®Google Scholar
• Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A, Cuervo AM. Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J. Neuropathol. Exp. Neurol. 2005;64:113–22.
   PubMed Web of Science ®Google Scholar
• Webb JL, Ravikumar B, Atkins J. Alpha-Synuclein is degraded by both autophagy and the proteasome. J Biol Chem. 2003;278:25009–13.
   PubMed Web of Science ®Google Scholar
• Tellez-Nagel I, Johnson AB, Terry RD. Studies on brain biopsies of patients with Huntington's chorea. J Neuropathol. Exp Neurol. 1974;33:308–32.
   PubMed Web of Science ®Google Scholar
• Banerjee R, Beal MF, Thomas B. Autophgy in neurodegenerative disorders: pathogenic roles and therapeutic implications. Trends Neurosci. 2010;33(12):541–9.
   PubMed Web of Science ®Google Scholar
• Cheung ZH, Ip NY. Autophagy deregulation in neurodegenerative diseases—-recent advances and future perspectives. J Neurochem. 2011;118:317–25.
   PubMed Web of Science ®Google Scholar
• Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature. 2006;441:880–4.
   PubMed Web of Science ®Google Scholar
• Venkatachalam K, Long AA, Elsaesser R, Nikolaeva D, Broadie K, Montell C. Motor deficit in a Drosophila model of mucolipidosis type IV due to defective clearance of apoptotic cells. Cell. 2008;135:838–51.
   PubMed Web of Science ®Google Scholar
• Pasinelli P, Brown RH. Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nature Rev Neurosci. 2006;7:710–23.
   PubMed Web of Science ®Google Scholar
• Rosen DR. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature. 1993;362:59–62.
   PubMed Web of Science ®Google Scholar
• Hang F, Strom AL, Fukada K, Lee S, Hayward LJ, Zhu H. Interaction between familial amyotrophic lateral sclerosis (ALS)-linked SOD1 mutants and the dynein complex. J Biol Chem. 2007;282:16691–9.
   PubMed Web of Science ®Google Scholar
• Crippa V, Sau D, Rusmini P, Boncoraglio A, Onesto E, Bolzoni E Galbiati M, Fontana E, Marino M, Carra S, Bendotti C, De Biasi S, Poletti A. The small heat shock protein B8 (HspB8) promotes autophagic removal of misfolded proteins involved in amyotrophic lateral sclerosis (ALS). Hum Mol Genet. 2010;19:3440–56.
   PubMed Web of Science ®Google Scholar
• Kabuta T, Suzuki Y, Wada K. Degradation of amyotrophic lateral sclerosis-link mutant Cu/Zn-superoxide dismutase proteins by macroautophagy and the proteasome. J Biol Chem. 2006;281:30524–30533.
   PubMed Web of Science ®Google Scholar
• Hanson KA, Kim SH, Wassarman DA, Tibbetts RS. Tibbetts Ubiquilin modifies TDP-43 toxicity in a drosophila model of ALS. J Biol Chem. 2010;285(15):11068–72.
   PubMed Web of Science ®Google Scholar
• Filimonenko M, Stuffers S, Raiborg C, Yamamoto A, Malerød L, Fisher EM, Isaacs A, Brech A, Stenmark H, Simonsen A. Functional multivesicular bodies are required for autophagic clearance of protein aggregates associated with neurodegenerative disease. J Cell Biol. 2007;179:485–500.
   PubMed Web of Science ®Google Scholar
• Wang X, Fan H, Ying Z, Li B, Wang H, Wang G. Degradation of TDP-43 and its pathogenic form by autophagy and the ubiquitin-proteasome system. Neurosci Lett. 2010; 469(1):112–6.
   PubMed Web of Science ®Google Scholar
• Caccamo A, Majumder S, Deng JJ, Bai Y, Thornton FB, Oddo S. Rapamycin rescues TDP-43 mislocalization and the associated low molecular mass neurofilament instability. J Biol Chem. 2009;284:27416–24.
   PubMed Web of Science ®Google Scholar
• Gomes C, Escrevente C, Costa J. Mutant superoxide dismutase1 overexpression in NSC-34 cells: effect of trehalose on aggregation, TDP-43 localization and levels of co-expressed glycoproteins. Neurosci Lett. 2010;475:145–9.
   PubMed Web of Science ®Google Scholar
• Morimoto N, Nagai M, Ohta Y, Miyazaki K, Kurata T, Morimoto M, Murakami T, Takehisa Y, Ikeda Y, Kamiya T, Abe K. Increased autophagy in transgenic mice with a G93A mutant SOD1 gene. Brain Res. 2007;1167:112–7.
   PubMed Web of Science ®Google Scholar
• Zhang X, Li L, Chen S, Yang D, Wang Y, Zhang X, Wang Z, Le W. Rapamycin treatment augments motor neuron degeneration in SOD1G93A mouse model of amyotrophic lateral sclerosis. Autophagy. 2011;7:412–25.
   PubMed Web of Science ®Google Scholar
• Hadano S, Otomo A, Kunita R, Suzuki-Utsunomiya K, Akatsuka A, Koike M, Aoki M, Uchiyama Y, Itoyama Y, Ikeda JE. Loss of ALS2/Alsin exacerbates motor dysfunction in a SOD1H46R -expressing mouse ALS model by disturbing endolysosomal trafficking. PLoS ONE. 2011;5:e9805.
   Web of Science ®Google Scholar
• Nixon RA. Autophagy, amloidogenesis and Alzheimer disease. J Cell Sci. 2007;120:4081–91.
   PubMed Web of Science ®Google Scholar
• Kicran D, Hafezparast M, Bohnert S, Dick JR, Martin J, Schiavo G, Fisher EM, Greensmith L. A mutation in dynein rescues anxonal transport defects and extends the life span of ALS mice. J Cell Biol. 2005;169:561–7.
   PubMed Web of Science ®Google Scholar
• Tian F, Morimoto N, Liu W, Ohta Y, Deguchi K, Miyazaki K, Abe K. In vivi optical imaging of motor neuron autophagy in a mouse of amyotrophic lateral sclerosis. Autophagy. 2011;7:985–92.
   PubMed Web of Science ®Google Scholar
• Hadano S, Kunita R, Otomo A, Suzuki-Utsunomiya K, Ikeda JE. Molecular and cellular function of ALS2/alsin: implication of membrane dynamics in neuronal development and degeneration. Neurochem Int. 2007;51:74–84.
   PubMed Web of Science ®Google Scholar
• Babst M, Katzmann DJ, Estepa-Sabal EJ, Meerloo T, Emr SD. Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev Cell. 2002;3: 271–82.
   PubMed Web of Science ®Google Scholar
• Cox LE, Ferraiuolo L, Goodall EF, Heath PR, Higginbottom A, Mortiboys H, Hollinger HC, Hartley JA, Brockington A, Burness CE, Morrison KE, Wharton SB, Grierson AJ, Ince PG, Kirby J, Shaw PJ. Mutations in CHMP2B in Lower Motor Neuron Predominant Amyotrophic Lateral Sclerosis (ALS). PLoS ONE. 2010;5:e9872.
   PubMed Web of Science ®Google Scholar
• Deng HX, Chen W, Hong ST, Boycott KM, Gorrie GH, Siddique N, Yang Y, Fecto F, Shi Y, Zhai H, Jiang H, Hirano M, Rampersaud E, Jansen GH, Donkervoort S, Bigio EH, Brooks BR, Ajroud K, Sufit RL, Haines JL, Mugnaini E, Pericak-Vance MA, Siddique T. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS dementia. Nature. 2011;477:211–5.
   PubMed Web of Science ®Google Scholar
• Lindholm D, Wootz H, Korhonen L. ER stress and neurodegenerative diseases. Cell Death Differ. 2006;13:385–92.
   PubMed Web of Science ®Google Scholar
• Yamamoto K, Hamada H, Shinkai H, Kohno Y, Koseki H, Aoe T. The KDEL receptor modulates the endoplasmic reticulum stress response through mitogen-activated protein kinase signaling cascades. J Biol Chem. 2003;278:34525–32.
   PubMedGoogle Scholar
• Wang P, Li B, Zhou L, Fei E, Wang G. The KDEL receptor induces autophagy to promote the clearance of neurodegenerative disease-related proteins. Neuroscience. 2011;190:43–55.
   PubMed Web of Science ®Google Scholar
• Sarkar S, Krishna G, Imarisio S, Saiki S, O'Kane CJ, Rubinsztein DC. A rational mechanism for combination treatment of Huntington's disease using lithium and rapamycin. Hum Mol Genet. 2008;17:170–178.
   PubMed Web of Science ®Google Scholar
• Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, Miller RA. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature. 2009;460:392–5.
   PubMed Web of Science ®Google Scholar
• Malagelada C, Jin ZH, Jackson-Lewis V, Przedborski S, Greene LA. Rapamycin protects against neuron death in in vitro and in vivo models of Parkinson's disease. J Neurosci. 2010;30:1166–75.
   PubMed Web of Science ®Google Scholar
• Dehay B, Bové J, Rodríguez-Muela N, Perier C, Recasens A, Boya P, Vila M. Pathogenic lysosomal depletion in Parkinson's disease. J Neurosci. 2010;30:12535–44.
   PubMed Web of Science ®Google Scholar
• Caccamo A, Maldonado MA, Majumder S, Medina DX, Holbein W, Magrí A, Oddo S. Naturally secreted amyloid-β increases mammalian target of rapamycin (mTOR) activity via a PRAS40-mediated mechanism. J Biol Chem. 2011;286:8924–32.
   PubMed Web of Science ®Google Scholar
• Cherra SJ 3rd, Chu CT. Autophagy in neuroprotection and neurodegeneration: A question of balance. Future Neurol. 2008;3(3):309–23.
   PubMedGoogle Scholar
• Cheung ZH, Ip NY. The emerging role of autophagy in Parkinson's disease. Mol Brain. 2009;2:29.
   Google Scholar
• Scarlatti F, Granata R, Meijer AJ, Codogno P. Does autophagy have a license to kill mammalian cell? Cell Death Differ. 2009;16(1):12–20.
   PubMed Web of Science ®Google Scholar
• Wong AS, Lee RH, Cheung AY, Yeung PK, Chung SK, Cheung ZH, Ip NY. Cdk5-mediated phosphorylation of endophilin B1 is required for induced autophagy in models of Parkinson's disease. Nat Cell Biol. 2011;13:568–79.
   PubMed Web of Science ®Google Scholar
• Wong E, Cuervo AM. Autophagy gone awry in neurodegenerative diseases. Nat Neurosci. 2010;13:805–11.
   PubMed Web of Science ®Google Scholar
• Massey AC, Kaushik S, Sovak G, Kiffin R, Cuervo AM. Consequences of the selective blockage of chaperone-mediated autophagy. Proc Natl Acad Sci USA. 2006;103:5805–10.
   PubMed Web of Science ®Google Scholar
• Nishida Y, Arakawa S, Fujitani K, Yamaguchi H, Mizuta T, Kanaseki T, Komatsu M, Otsu K, Tsujimoto Y, Shimuzu S. Discovery of Atg5/Atg7-independent alternative macroautophagy. Nature. 2009;461:654–8.
   PubMed Web of Science ®Google Scholar
• Fornai F, Longone P, Cafaro L, Kastsiuchenka O, Ferrucci M, Manca ML, Lazzeri G, Spalloni A, Bellio N, Lenzi P, Modugno N, Siciliano G, Isidoro C, Murri L, Ruggieri S, Paparelli A. Lithium delays progression of amyotrophic lateral sclerosis. Proc Natl Acad Sci. 2008;105:2052–57.
   PubMed Web of Science ®Google Scholar
• Fornai F, Longone P, Ferrucci M, Lenzi P, Isidoro C, Ruggieri S, Paparelli A. Autophagy and amyotrophic lateral sclerosis: The multiple roles of lithium. Autophagy. 2008;4(4):527–30.
   PubMed Web of Science ®Google Scholar
• Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, Pasco M, Cook LJ, Rubinsztein DC. Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol 2005;170:1101–11.
   PubMed Web of Science ®Google Scholar
• Stambolic V, Ruel L, Woodgett JR. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr Biol. 1996;6:1664–68.
   PubMed Web of Science ®Google Scholar
• Pasquali L, Busceti CL, Fulceri F. Intracellular pathway underlying the effects of lithium. Behav Pharmacol. 2010;21(5-6):473–92.
   PubMed Web of Science ®Google Scholar
• Gill A, Kidd J, Vieira F, Thompson K Perrin S. No benefit from chronic lithium dosing in a sibling-matched, gender balanced, investigator-blinded trial using a standard mouse model of familial ALS. PLoS ONE. 2009;4:e6489.
   PubMedGoogle Scholar
• Chio A, Borghero G, Calvo A, Capasso M, Caponnetto C, Corbo M, Giannini F, Logroscino G, Mandrioli J, Marcello N, Mazzini L, Moglia C, Monsurrò MR, Mora G, Patti F, Perini M, Pietrini V, Pisano F, Pupillo E, Sabatelli M, Salvi F, Silani V, Simone IL, Sorarù G, Tola MR, Volanti P, Beghi E. LITALS Study Group. Lithium carbonate in amyotrophic lateral sclerosis: lack of efficacy in a dose-finding trial. Neurology. 2010;75:619–25.
   PubMed Web of Science ®Google Scholar
• Bové J, Martínez-Vicente M, Vila M. Fighting neurodegeneration with rapamycin: mechanistic insights. Nat Rev Neurosci. 2011;12:437–52.
   PubMed Web of Science ®Google Scholar