759
Views
17
CrossRef citations to date
0
Altmetric
ORIGINAL ARTICLE

Human TDP-43 and FUS selectively affect motor neuron maturation and survival in a murine cell model of ALS by non-cell-autonomous mechanisms

, &
Pages 431-441 | Received 01 Jan 2015, Accepted 26 Apr 2015, Published online: 15 Jul 2015

References

  • Ludolph AC, Sperfeld AD. Preclinical trials: an update on translational research in ALS. Neuro-degenerative Diseases. 2005;2:215–9.
  • Johnston CA, Stanton BR, Turner MR, Gray R, Blunt AH, Butt D, et al. Amyotrophic lateral sclerosis in an urban setting: a population based study of inner city London. Journal of Neurology. 2006;253:1642–3.
  • Julien JP. ALS: astrocytes move in as deadly neighbours. Nature Neuroscience. 2007;10:535–7.
  • Rothstein JD. Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Annals of Neurology. 2009;65 (Suppl 1):S3–9.
  • Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature. 1993;362:59–62.
  • Di Giorgio FP, Carrasco MA, Siao MC, Maniatis T, Eggan K. Non-cell-autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nature Neuroscience. 2007;10:608–14.
  • Di Giorgio FP, Boulting GL, Bobrowicz S, Eggan KC. Human embryonic stem cell-derived motor neurons are sensitive to the toxic effect of glial cells carrying an ALS-causing mutation. Cell Stem Cell. 2008;3:637–48.
  • Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, et al. Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nature Neuroscience. 2007;10:615–22.
  • Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, Gutmann DH, et al. Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nature Neuroscience. 2008;11:251–3.
  • Mackenzie IR, Bigio EH, Ince PG, Geser F, Neumann M, Cairns NJ, et al. Pathological TDP-43 distinguishes sporadic amyotrophic lateral sclerosis from amyotrophic lateral sclerosis with SOD1 mutations. Annals of Neurology. 2007; 61:427–34.
  • Deng HX, Zhai H, Bigio EH, Yan J, Fecto F, Ajroud K, et al. FUS-immunoreactive inclusions are a common feature in sporadic and non-SOD1 familial amyotrophic lateral sclerosis. Annals of Neurology. 2010;67:739–48.
  • Lagier-Tourenne C, Polymenidou M, Cleveland DW. TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Human Molecular Genetics. 2010; 19:R46–64.
  • Strong MJ, Volkening K, Hammond R, Yang W, Strong W, Leystra-Lantz C, et al. TDP-43 is a human low molecular weight neurofilament (hNFL) mRNA-binding protein. Molecular and Cellular Neurosciences. 2007;35:320–7.
  • Sephton CF, Good SK, Atkin S, Dewey CM, Mayer P 3rd, Herz J, et al. TDP-43 is a developmentally regulated protein essential for early embryonic development. The Journal of Biological Chemistry. 2010;285:6826–34.
  • Han JH, Yu TH, Ryu HH, Jun MH, Ban BK, Jang DJ, et al. ALS/FTLD-linked TDP-43 regulates neurite morphology and cell survival in differentiated neurons. Experimental Cell Research. 2013;319:1998–2005.
  • Serio A, Bilican B, Barmada SJ, Ando DM, Zhao C, Siller R, et al. Astrocyte pathology and the absence of non-cell autonomy in an induced pluripotent stem cell model of TDP-43 proteinopathy. Proceedings of the National Academy of Sciences of the United States of America. 2013;110: 4697–702.
  • Winton MJ, Igaz LM, Wong MM, Kwong LK, Trojanowski JQ, Lee VM. Disturbance of nuclear and cytoplasmic TAR DNA-binding protein (TDP-43) induces disease-like redistribution, sequestration, and aggregate formation. The Journal of Biological Chemistry. 2008;283:13302–9.
  • Igaz LM, Kwong LK, Chen-Plotkin A, Winton MJ, Unger TL, Xu Y, et al. Expression of TDP-43 C-terminal Fragments In Vitro Recapitulates Pathological Features of TDP-43 Proteinopathies. The Journal of Biological Chemistry. 2009;284: 8516–24.
  • Ling SC, Albuquerque CP, Han JS, Lagier-Tourenne C, Tokunaga S, Zhou H, et al. ALS-associated mutations in TDP-43 increase its stability and promote TDP-43 complexes with FUS/TLS. Proceedings of the National Academy of Sciences of the United States of America. 2010;107: 13318–23.
  • Li Y, Ray P, Rao EJ, Shi C, Guo W, Chen X, et al. A Drosophila model for TDP-43 proteinopathy. Proceedings of the National Academy of Sciences of the United States of America. 2010;107:3169–74.
  • Estes PS, Boehringer A, Zwick R, Tang JE, Grigsby B, Zarnescu DC. Wild-type and A315T mutant TDP-43 exert differential neurotoxicity in a Drosophila model of ALS. Human Molecular Genetics. 2011;20:2308–21.
  • Barmada SJ, Skibinski G, Korb E, Rao EJ, Wu JY, Finkbeiner S. Cytoplasmic mislocalization of TDP-43 is toxic to neurons and enhanced by a mutation associated with familial amyotrophic lateral sclerosis. The Journal of Neuroscience: the official journal of the Society for Neuroscience. 2010;30:639–49.
  • Egawa N, Kitaoka S, Tsukita K, Naitoh M, Takahashi K, Yamamoto T, et al. Drug screening for ALS using patient-specific induced pluripotent stem cells. Science Translational Medicine. 2012;4:145ra04.
  • Hoing S, Rudhard Y, Reinhardt P, Glatza M, Stehling M, Wu G, et al. Discovery of inhibitors of microglial neurotoxicity acting through multiple mechanisms using a stem- cell-based phenotypic assay. Cell Stem Cell. 2012;11: 620–32.
  • Dimos JT, Rodolfa KT, Niakan KK, Weisenthal LM, Mitsumoto H, Chung W, et al. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science. 2008;321:1218–21.
  • Sotelo-Silveira JR, Lepanto P, Elizondo V, Horjales S, Palacios F, Martinez-Palma L, et al. Axonal mitochondrial clusters containing mutant SOD1 in transgenic models of ALS. Antioxidants and Redox Signaling. 2009;11:1535–45.
  • Wegorzewska I, Bell S, Cairns NJ, Miller TM, Baloh RH. TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proceedings of the National Academy of Sciences of the United States of America. 2009;106:18809–14.
  • Wils H, Kleinberger G, Janssens J, Pereson S, Joris G, Cuijt I, et al. TDP-43 transgenic mice develop spastic paralysis and neuronal inclusions characteristic of ALS and frontotemporal lobar degeneration. Proceedings of the National Academy of Sciences of the United States of America. 2010;107: 3858–63.
  • Xu YF, Gendron TF, Zhang YJ, Lin WL, D’Alton S, Sheng H, et al. Wild-type human TDP-43 expression causes TDP-43 phosphorylation, mitochondrial aggregation, motor deficits, and early mortality in transgenic mice. The Journal of Neuroscience : the official journal of the Society for Neuroscience. 2010;30:10851–9.
  • Igaz LM, Kwong LK, Lee EB, Chen-Plotkin A, Swanson E, Unger T, et al. Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice. The Journal of Clinical Investigation. 2011;121:726–38.
  • Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou TT, et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science. 2006;314:130–3.
  • Kwiatkowski TJ Jr, Bosco DA, Leclerc AL, Tamrazian E, Vanderburg CR, Russ C, et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science. 2009;323:1205–8.
  • Vance C, Rogelj B, Hortobagyi T, De Vos KJ, Nishimura AL, Sreedharan J, et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science. 2009;323:1208–11.
  • Halliday G, Bigio EH, Cairns NJ, Neumann M, Mackenzie IR, Mann DM. Mechanisms of disease in frontotemporal lobar degeneration: gain of function versus loss of function effects. Acta Neuropathologica. 2012;124:373–82.
  • Stallings NR, Puttaparthi K, Luther CM, Burns DK, Elliott JL. Progressive motor weakness in transgenic mice expressing human TDP-43. Neurobiology of Disease. 2010; 40:404–14.
  • Zhou H, Huang C, Chen H, Wang D, Landel CP, Xia PY, et al. Transgenic rat model of neurodegeneration caused by mutation in the TDP gene. PLoS Genet. 2010;6: e1000887.
  • Arnold ES, Ling SC, Huelga SC, Lagier-Tourenne C, Polymenidou M, Ditsworth D, et al. ALS-linked TDP-43 mutations produce aberrant RNA splicing and adult-onset motor neuron disease without aggregation or loss of nuclear TDP-43. Proceedings of the National Academy of Sciences of the United States of America. 2013;110:E736–45.
  • Haidet-Phillips AM, Gross SK, Williams T, Tuteja A, Sherman A, Ko M, et al. Altered astrocytic expression of TDP-43 does not influence motor neuron survival. Experimental Neurology. 2013;250:250–9.
  • Mitchell JC, McGoldrick P, Vance C, Hortobagyi T, Sreedharan J, Rogelj B, et al. Overexpression of human wild-type FUS causes progressive motor neuron degeneration in an age- and dose-dependent fashion. Acta Neuropathologica. 2013;125:273–88.
  • Huang C, Zhou H, Tong J, Chen H, Liu YJ, Wang D, et al. FUS transgenic rats develop the phenotypes of amyotrophic lateral sclerosis and frontotemporal lobar degeneration. PLoS Genet. 2011;7:e1002011.
  • Huang C, Xia PY, Zhou H. Sustained expression of TDP-43 and FUS in motor neurons in rodent’s lifetime. International Journal of Biological Sciences. 2010;6:396–406.
  • Wong M, Martin LJ. Skeletal muscle-restricted expression of human SOD1 causes motor neuron degeneration in transgenic mice. Human Molecular Genetics. 2010;19: 2284–302.
  • Grad LI, Yerbury JJ, Turner BJ, Guest WC, Pokrishevsky E, O’Neill MA, et al. Intercellular propagated misfolding of wild-type Cu/Zn superoxide dismutase occurs via exosome-dependent and -independent mechanisms. Proceedings of the National Academy of Sciences of the United States of America. 2014;111:3620–5.
  • Re DB, Le Verche V, Yu C, Amoroso MW, Politi KA, Phani S, et al. Necroptosis drives motor neuron death in models of both sporadic and familial ALS. Neuron. 2014;81:1001–8.
  • Wong M, Martin LJ. Skeletal muscle-restricted expression of human SOD1 causes motor neuron degeneration in transgenic mice. Hum Mol Genet. 2010;19:2284–302.
  • Cortes CJ, Ling SC, Guo LT, Hung G, Tsunemi T, Ly L, et al. Muscle expression of mutant androgen receptor accounts for systemic and motor neuron disease phenotypes in spinal and bulbar muscular atrophy. Neuron. 2014;82: 295–307.
  • Lieberman AP, Yu Z, Murray S, Peralta R, Low A, Guo S, et al. Peripheral androgen receptor gene suppression rescues disease in mouse models of spinal and bulbar muscular atrophy. Cell Reports. 2014;7:774–84.
  • Goswami A, Jesse CM, Chandrasekar A, Bushuven E, Vollrath JT, Dreser A, et al. Accumulation of STIM1 is associated with the degenerative muscle fibre phenotype in ALS and other neurogenic atrophies. Neuropathology and Applied Neurobiology. 2015;41:304–18.
  • Brettschneider J, Del Tredici K, Toledo JB, Robinson JL, Irwin DJ, Grossman M, et al. Stages of pTDP-43 pathology in amyotrophic lateral sclerosis. Annals of Neurology. 2013;74:20–38.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.