Rodent models of amyotrophic lateral sclerosis

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 9, 2013, Pages 1421-1436

  McGoldrick, Philip ^a   Joyce, Peter I ^b   Fisher, Elizabeth M C ^a   Greensmith, Linda ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b MRC MAMMALIAN GENETICS UNIT   (United Kingdom)

Author keywords

ALS; FUS; Models; SOD1; TDP 43; VCP

Indexed keywords

FUSED IN SARCOMA PROTEIN; TAR DNA BINDING PROTEIN; VALOSIN CONTAINING PROTEIN; BIOLOGICAL MARKER;

AMYOTROPHIC LATERAL SCLEROSIS; ARTIFICIAL CHROMOSOME; GENE INACTIVATION; NONHUMAN; PATHOPHYSIOLOGY; PRIMATE MODEL; PRION; PRIORITY JOURNAL; RAT MODEL; REVIEW; RODENT MODEL; TDP 43 PROTEINOPATHY; ANIMAL; DISEASE MODEL; GENE THERAPY; GENETICS; HUMAN; METABOLISM; PATHOLOGY; RODENT;

ANIMALIA; RODENTIA;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BIOLOGICAL MARKERS; DISEASE MODELS, ANIMAL; GENETIC THERAPY; HUMANS; RODENTIA;

MLCS; MLOWN;

EID: 84881226567     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.03.012     Document Type: Review

References (213)

1. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
2. Andersen P.M. Amyotrophic lateral sclerosis associated with mutations in the CuZn superoxide dismutase gene. Curr. Neurol. Neurosci. Rep. 2006, 6:37-46.
3. Neumann M., Sampathu D.M., Kwong L.K., Truax A.C., Micsenyi M.C., Chou T.T., Bruce J., Schuck T., Grossman M., Clark C.M., McCluskey L.F., Miller B.L., Masliah E., Mackenzie I.R., Feldman H., Feiden W., Kretzschmar H.A., Trojanowski J.Q., Lee V.M.-Y. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
4. Kabashi E., Valdmanis P.N., Dion P., Spiegelman D., McConkey B.J., Vande Velde C., Bouchard J.-P., Lacomblez L., Pochigaeva K., Salachas F., Pradat P.-F., Camu W., Meininger V., Dupre N., Rouleau G.A. TARDBP mutations in individuals with sporadic and familial amyotrophic lateral sclerosis. Nat. Genet. 2008, 40:572-574.
5. Sreedharan J., Blair I.P., Tripathi V.B., Hu X., Vance C., Rogelj B., Ackerley S., Durnall J.C., Williams K.L., Buratti E., Baralle F., de Belleroche J., Mitchell J.D., Leigh P.N., Al-Chalabi A., Miller C.C., Nicholson G., Shaw C.E. TDP-43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 2008, 319:1668-1672.
6. Chen Y.-Z., Bennett C.L., Huynh H.M., Blair I.P., Puls I., Irobi J., Dierick I., Abel A., Kennerson M.L., Rabin B.A., Nicholson G.A., Auer-Grumbach M., Wagner K., De Jonghe P., Griffin J.W., Fischbeck K.H., Timmerman V., Cornblath D.R., Chance P.F. DNA/RNA helicase gene mutations in a form of juvenile amyotrophic lateral sclerosis (ALS4). Am. J. Hum. Genet. 2004, 74:1128-1135.
7. Kwiatkowski T.J., Bosco D.A., Leclerc A.L., Tamrazian E., Vanderburg C.R., Russ C., Davis A., Gilchrist J., Kasarskis E.J., Munsat T., Valdmanis P., Rouleau G.A., Hosler B.A., Cortelli P., de Jong P.J., Yoshinaga Y., Haines J.L., Pericak-Vance M.A., Yan J., Ticozzi N., Siddique T., McKenna-Yasek D., Sapp P.C., Horvitz H.R., Landers J.E., Brown R.H. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009, 323:1205-1208.
8. Vance C., Rogelj B., Hortobágyi T., De Vos K.J., Nishimura A.L., Sreedharan J., Hu X., Smith B., Ruddy D., Wright P., Ganesalingam J., Williams K.L., Tripathi V., Al-Saraj S., Al-Chalabi A., Leigh P.N., Blair I.P., Nicholson G., de Belleroche J., Gallo J.-M., Miller C.C., Shaw C.E. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009, 323:1208-1211.
9. Yang Y., Hentati A., Deng H.X., Dabbagh O., Sasaki T., Hirano M., Hung W.Y., Ouahchi K., Yan J., Azim A.C., Cole N., Gascon G., Yagmour A., Ben-Hamida M., Pericak-Vance M., Hentati F., Siddique T. 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. 2001, 29:160-165.
10. Maruyama H., Morino H., Ito H., Izumi Y., Kato H., Watanabe Y., Kinoshita Y., Kamada M., Nodera H., Suzuki H., Komure O., Matsuura S., Kobatake K., Morimoto N., Abe K., Suzuki N., Aoki M., Kawata A., Hirai T., Kato T., Ogasawara K., Hirano A., Takumi T., Kusaka H., Hagiwara K., Kaji R., Kawakami H. Mutations of optineurin in amyotrophic lateral sclerosis. Nature 2010, 465:223-226.
11. Johnson J.O., Mandrioli J., Benatar M., Abramzon Y., Van Deerlin V.M., Trojanowski J.Q., Gibbs J.R., Brunetti M., Gronka S., Wuu J., Ding J., McCluskey L., Martinez-Lage M., Falcone D., Hernandez D.G., Arepalli S., Chong S., Schymick J.C., Rothstein J., Landi F., Wang Y.D., Calvo A., Mora G., Sabatelli M., Monsurro M.R., Battistini S., Salvo F., Spataro R., Sola P., Borghero G., ITALSGEN Consortium, Galassi G., Scholz S.W., Taylor J.P., Restagno G., Chio A., Traynor B.J. Exome sequencing reveals VCP mutations as a cause of familial ALS. Neuron 2010, 68:857-864.
12. Greenway M.J., Andersen P.M., Russ C., Ennis S., Cashman S., Donaghy C., Patterson V., Swingler R., Kieran D., Prehn J., Morrison K.E., Green A., Acharya K.R., Brown R.H., Hardiman O. ANG mutations segregate with familial and "sporadic" amyotrophic lateral sclerosis. Nat. Genet. 2006, 38:411-413.
13. Nishimura A.L., Mitne-Neto M., Silva H.C.A., Richieri-Costa A., Middleton S., Cascio D., Kok F., Oliveira J.R.M., Gillingwater T., Webb J., Skehel P., Zatz M. A mutation in the vesicle-trafficking protein VAPB causes late-onset spinal muscular atrophy and amyotrophic lateral sclerosis. Am. J. Hum. Genet. 2004, 75:822-831.
14. Deng H.-X., Chen W., Hong S.-T., Boycott K.M., Gorrie G.H., Siddique N., Yang Y., Fecto F., Shi Y., Zhai H., Jiang H., Hirano M., Rampersaud E., Jansen G.H., Donkervoort S., Bigio E.H., Brooks B.R., Ajroud K., Sufit R.L., Haines J.L., Mugnaini E., Peticak-Vance M.A., Siddique T. Mutations in UBQLN2 cause dominant X-linked juvenile and adult-onset ALS and ALS/dementia. Nature 2011, 477:211-215.
15. DeJesus-Hernandez M., Mackenzie I.R., Boeve B.F., Boxer A.L., Baker M., Rutherford N.J., Nicholson A.M., Finch N.A., Flynn H., Adamson J., Kouri N., Wojtas A., Sengdy P., Hsiung G.-Y.R., Karydas A., Seeley W.W., Josephs K.A., Coppola G., Geschwind D.H., Wszolek Z.K., Feldman H., Knopman D.S., Petersen R.C., Miller B.L., Dickson D.W., Boylan K.B., Graff-Radford N.R., Rademakers R. Expanded GGGGCC hexanucleotide repeat in noncoding region of C9ORF72 causes chromosome 9p-linked FTD and ALS. Neuron 2011, 72:245-256.
16. Renton A.E., Majounie E., Waite A., Simón-Sánchez J., Rollinson S., Gibbs J.R., Schymick J.C., Laaksovirta H., van Swieten J.C., Myllykangas L., Kalimo H., Paetau A., Abramzon Y., Remes A.M., Kaganovich A., Scholz S.W., Duckworth J., Ding J., Harmer D.W., Hernandez D.G., Johnson J.O., Mok K., Ryten M., Trabzuni D., Guerreiro R.J., Orrell R.Q., Neal J., Murray A., Pearson J., Jansen I.E., Sondervan D., Seelaar H., Blake D., Young K., Halliwell N., Callister J., Toulson G., Richardson A., Gerhard A., Snowden J., Mann D., Neary D., Nalis M.A., Peuralinna T., Jansson L., Isoviita V.-M., Kaivorinne A.-L., Holtta-Vuori M., Ikonen E., Sulkava R., Benatar M., Wuu J., Chio A., Restagno G., Borghero G., Sabatelli M., The ITALSGEN Consortium, Heckerman D., Rogaeva E., Zinman L., Rothstein J., Sendtner M., Drepper C., Eichler E.E., Alkan C., Abdullaev Z., Pack S.D., Dutra A., Pak E., Hardy J., Singleton A., Williams N.M., Heutink P., Pickering-Brown S., Morris H.R., Tienari P.J., Traynor B.J. A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 2011, 72:257-268.
17. Wu C.-H., Fallini C., Ticozzi N., Keagle P.J., Sapp P.C., Piotrowska K., Lowe P., Koppers M., McKenna-Yasek D., Baron D.M., Kost J.E., Gonzalez-Perez P., Fox A.D., Adams J., Taroni F., Tiloca C., Leclerc A.L., Chafe S.C., Mangroo D., Moore M.J., Zitzewitz J.A., Xu Z.S., van den Berg L.H., Glass J.D., Siciliano G., Cirulli E.T., Goldstein D.B., Salachas F., Meininger V., Rossoll W., Ratti A., Gellera C., Bosco D.A., Bassell G.J., Silani V., Drory V.E., Brown R.H., Landers J.E. Mutations in the profilin 1 gene cause familial amyotrophic lateral sclerosis. Nature 2012, 488:499-503.
18. Borchelt D.R., Guarnieri M., Wong P.C., Lee M.K., Slunt H.S., Xu Z.S., Sisodia S.S., Price D.L., Cleveland D.W. Superoxide dismutase 1 subunits with mutations linked to familial amyotrophic lateral sclerosis do not affect wild-type subunit function. J. Biol. Chem. 1995, 270:3234-3238.
19. Reaume A.G., Elliott J.L., Hoffman E.K., Kowall N.W., Ferrante R.J., Siwek D.F., Wilcox H.M., Flood D.G., Beal M.F., Brown R.H., Scott R.W., Snider W.D. Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. Nat. Genet. 1996, 13:43-47.
20. Fischer L.R., Igoudjil A., Magrané J., Li Y., Hansen J.M., Manfredi G., Glass J.D. SOD1 targeted to the mitochondrial intermembrane space prevents motor neuropathy in the Sod1 knockout mouse. Brain 2011, 134:196-209.
21. Flood D.G., Reaume A.G., Gruner J.A., Hoffman E.K., Hirsch J.D., Lin Y.G., Dorfman K.S., Scott R.W. Hindlimb motor neurons require Cu/Zn superoxide dismutase for maintenance of neuromuscular junctions. Am. J. Pathol. 1999, 155:663-672.
22. Jang Y.C., Lustgarten M.S., Liu Y., Muller F.L., Bhattacharya A., Liang H., Salmon A.B., Brooks S.V., Larkin L., Hayworth C.R., Richardson A., Van Remmen H. Increased superoxide in vivo accelerates age-associated muscle atrophy through mitochondrial dysfunction and neuromuscular junction degeneration. FASEB J. 2010, 24:1376-1390.
23. Shefner J.M., Reaume A.G., Flood D.G., Scott R.W., Kowall N.W., Ferrante R.J., Siwek D.F., Upton-Rice M., Brown R.H. Mice lacking cytosolic copper/zinc superoxide dismutase display a distinctive motor axonopathy. Neurology 1999, 53:1239-1246.
24. Gurney M.E., Pu H., Chiu A.Y., Dal Canto M.C., Polchow C.Y., Alexander D.D., Caliendo J., Hentati A., Kwon Y.W., Deng H.X. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 1994, 264:1772-1775.
25. Bruijn L.I., Becher M.W., Lee M.K., Anderson K.L., Jenkins N.A., Copeland N.G., Sisodia S.S., Rothstein J.D., Borchelt D.R., Price D.L., Cleveland D.W. ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 1997, 18:327-338.
26. Chang-Hong R., Wada M., Koyama S., Kimura H., Arawaka S., Kawanami T., Kurita K., Kadoya T., Aoki M., Itoyama Y., Kato T. Neuroprotective effect of oxidized galectin-1 in a transgenic mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 2005, 194:203-211.
27. Dal Canto M.C., Gurney M.E. A low expressor line of transgenic mice carrying a mutant human Cu, Zn superoxide dismutase (SOD1) gene develops pathological changes that most closely resemble those in human amyotrophic lateral sclerosis. Acta Neuropathol. 1997, 93:537-550.
28. Nagai M., Aoki M., Miyoshi I., Kato M., Pasinelli P., Kasai N., Brown R.H., Itoyama Y. Rats expressing human cytosolic copper-zinc superoxide dismutase transgenes with amyotrophic lateral sclerosis: associated mutations develop motor neuron disease. J. Neurosci. 2001, 21:9246-9254.
29. Ripps M.E., Huntley G.W., Hof P.R., Morrison J.H., Gordon J.W. Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:689-693.
30. Lino M.M., Schneider C., Caroni P. Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J. Neurosci. 2002, 22:4825-4832.
31. Jaarsma D., Teuling E., Haasdijk E.D., De Zeeuw C.I., Hoogenraad C.C. Neuron-specific expression of mutant superoxide dismutase is sufficient to induce amyotrophic lateral sclerosis in transgenic mice. J. Neurosci. 2008, 28:2075-2088.
32. Gong Y.H., Parsadanian A.S., Andreeva A., Snider W.D., Elliott J.L. Restricted expression of G86R Cu/Zn Superoxide dismutase in astrocytes results in astrocytosis but does not cause motoneuron degeneration. J. Neurosci. 2000, 20:660-665.
33. Aoki M., Kato S., Nagai M., Itoyama Y. Development of a rat model of amyotrophic lateral sclerosis expressing a human SOD1 transgene. Neuropathology 2005, 25:365-370.
34. Howland D.S., Liu J., She Y., Goad B., Maragakis N.J., Kim B., Erickson J., Kulik J., DeVito L., Psaltis G., DeGennaro L.J., Cleveland D.W., Rothstein J.D. Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc. Natl. Acad. Sci. U. S. A. 2002, 99:1604-1609.
35. Matsumoto A., Okada Y., Nakamichi M., Nakamura M., Toyama Y., Sobue G., Nagai M., Aoki M., Itoyama Y., Okano H. Disease progression of human SOD1 (G93A) transgenic ALS model rats. J. Neurosci. Res. 2006, 83:119-133.
36. Heiman-Patterson T.D., Sher R.B., Blankenhorn E.A., Alexander G., Deitch J.S., Kunst C.B., Maragakis N., Cox G. Effect of genetic background on phenotype variability in transgenic mouse models of amyotrophic lateral sclerosis: a window of opportunity in the search for genetic modifiers. Amyotroph Lateral Scler 2011, 12:79-86.
37. Mancuso R., Oliván S., Rando A., Casas C., Osta R., Navarro X. Sigma-1R agonist improves motor function and motoneuron survival in ALS mice. Neurotherapeutics 2012, 9:814-826.
38. Jaarsma D., Haasdijk E.D., Grashorn J.A., Hawkins R., van Duijn W., Verspaget H.W., London J., Holstege J.C. Human Cu/Zn superoxide dismutase (SOD1) overexpression in mice causes mitochondrial vacuolization, axonal degeneration, and premature motoneuron death and accelerates motoneuron disease in mice expressing a familial amyotrophic lateral sclerosis mutant SOD1. Neurobiol. Dis. 2000, 7:623-643.
39. Tu P.H., Raju P., Robinson K.A., Gurney M.E., Trojanowski J.Q., Lee V.M. Transgenic mice carrying a human mutant superoxide dismutase transgene develop neuronal cytoskeletal pathology resembling human amyotrophic lateral sclerosis lesions. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:3155-3160.
40. Jaarsma D. Swelling and vacuolisation of mitochondria in transgenic SOD1-ALS mice: a consequence of supranormal SOD1 expression?. Mitochondrion 2006, 6:48-49. (author reply 50-51).
41. Bosco D.A., Morfini G., Karabacak N.M., Song Y., Gros-Louis F., Pasinelli P., Goolsby H., Fontaine B.A., Lemay N., McKenna-Yasek D., Frosch M.P., Agar J.N., Julien J.-P., Brady S.T., Brown R.H. Wild-type and mutant SOD1 share an aberrant conformation and a common pathogenic pathway in ALS. Nat. Neurosci. 2010, 13:1396-1403.
42. Deng H.-X., Shi Y., Furukawa Y., Zhai H., Fu R., Liu E., Gorrie G.H., Khan M.S., Hung W.-Y., Bigio E.H., Lukas T., Dal Canto M.C., O'Halloran T.V., Siddique T. Conversion to the amyotrophic lateral sclerosis phenotype is associated with intermolecular linked insoluble aggregates of SOD1 in mitochondria. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:7142-7147.
43. Graffmo K.S., Forsberg K., Bergh J., Birve A., Zetterström P., Andersen P.M., Marklund S.L., Brännström T. Expression of wild-type human superoxide dismutase-1 in mice causes amyotrophic lateral sclerosis. Hum. Mol. Genet. 2012, 22:51-60.
44. Bento-Abreu A., Van Damme P., Van Den Bosch L., Robberecht W. The neurobiology of amyotrophic lateral sclerosis. Eur. J. Neurosci. 2010, 31:2247-2265.
45. Ou S.H., Wu F., Harrich D., García-Martínez L.F., Gaynor R.B. Cloning and characterization of a novel cellular protein, TDP-43, that binds to human immunodeficiency virus type 1 TAR DNA sequence motifs. J. Virol. 1995, 69:3584-3596.
46. Buratti E., Baralle F.E. Multiple roles of TDP-43 in gene expression, splicing regulation, and human disease. Front. Biosci. 2008, 13:867-878.
47. Sephton C.F., Good S.K., Atkin S., Dewey C.M., Mayer P., Herz J., Yu G. TDP-43 is a developmentally regulated protein essential for early embryonic development. J. Biol. Chem. 2010, 285:6826-6834.
48. Duan W., Guo Y., Jiang H., Yu X., Li C. MG132 enhances neurite outgrowth in neurons overexpressing mutant TAR DNA-binding protein-43 via increase of HO-1. Brain Res. 2011, 1397:1-9.
49. Fiesel F.C., Schurr C., Weber S.S., Kahle P.J. TDP-43 knockdown impairs neurite outgrowth dependent on its target histone deacetylase 6. Mol. Neurodegener. 2011, 6:64.
50. Wang I.-F., Wu L.-S., Chang H.-Y., Shen C.-K.J. TDP-43, the signature protein of FTLD-U, is a neuronal activity-responsive factor. J. Neurochem. 2008, 105:797-806.
51. Godena V.K., Romano G., Romano M., Appocher C., Klima R., Buratti E., Baralle F.E., Feiguin F. TDP-43 regulates Drosophila neuromuscular junctions growth by modulating Futsch/MAP1B levels and synaptic microtubules organization. PLoS One 2011, 6:e17808.
52. Lin M.-J., Cheng C.-W., Shen C.-K.J. Neuronal function and dysfunction of Drosophila dTDP. PLoS One 2011, 6:e20371.
53. Braun R.J., Sommer C., Carmona-Gutierrez D., Khoury C.M., Ring J., Büttner S., Madeo F. Neurotoxic 43-kDa TAR DNA-binding protein (TDP-43) triggers mitochondrion-dependent programmed cell death in yeast. J. Biol. Chem. 2011, 286:19958-19972.
54. Shan X., Chiang P.-M., Price D.L., Wong P.C. Altered distributions of Gemini of coiled bodies and mitochondria in motor neurons of TDP-43 transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:16325-16330.
55. Estes P.S., Boehringer A., Zwick R., Tang J.E., Grigsby B., Zarnescu D.C. Wild-type and A315T mutant TDP-43 exert differential neurotoxicity in a Drosophila model of ALS. Hum. Mol. Genet. 2011, 20:2308-2321.
56. Tsao W., Jeong Y.H., Lin S., Ling J., Price D.L., Chiang P.-M., Wong P.C. Rodent models of TDP-43: recent advances. Brain Res. 2012, 1462:26-39.
57. Wu L.-S., Cheng W.-C., Shen C.-K.J. Targeted depletion of TDP-43 expression in the spinal cord motor neurons leads to the development of amyotrophic lateral sclerosis-like phenotypes in mice. J. Biol. Chem. 2012, 287:27335-27344.
58. Wegorzewska I., Bell S., Cairns N.J., Miller T.M., Baloh R.H. TDP-43 mutant transgenic mice develop features of ALS and frontotemporal lobar degeneration. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:18809-18814.
59. Guo Y., Wang Q., Zhang K., An T., Shi P., Li Z., Duan W., Li C. HO-1 induction in motor cortex and intestinal dysfunction in TDP-43 A315T transgenic mice. Brain Res. 2012, 1460:88-95.
60. Xu Y.-F., Gendron T.F., Zhang Y.-J., Lin W.-L., D'Alton S., Sheng H., Casey M.C., Tong J., Knight J., Yu X., Rademakers R., Boylan K., Hutton M., McGowan E., Dickson D.W., Lewis J., Petrucelli L. Wild-type human TDP-43 expression causes TDP-43 phosphorylation, mitochondrial aggregation, motor deficits, and early mortality in transgenic mice. J. Neurosci. 2010, 30:10851-10859.
61. Xu Y.-F., Zhang Y.-J., Lin W.-L., Cao X., Stetler C., Dickson D.W., Lewis J., Petrucelli L. Expression of mutant TDP-43 induces neuronal dysfunction in transgenic mice. Mol. Neurodegener. 2011, 6:73.
62. Stallings N.R., Puttaparthi K., Luther C.M., Burns D.K., Elliott J.L. Progressive motor weakness in transgenic mice expressing human TDP-43. Neurobiol. Dis. 2010, 40:404-414.
63. Wils H., Kleinberger G., Janssens J., Pereson S., Joris G., Cuijt I., Smits V., Ceuterick-de Groote C., Van Broeckhoven C., Kumar-Singh S. TDP-43 transgenic mice develop spastic paralysis and neuronal inclusions characteristic of ALS and frontotemporal lobar degeneration. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3858-3863.
64. Caccamo A., Majumder S., Oddo S. Cognitive decline typical of frontotemporal lobar degeneration in transgenic mice expressing the 25-kDa C-terminal fragment of TDP-43. Am. J. Pathol. 2012, 180:293-302.
65. Tsai K.-J., Yang C.-H., Fang Y.-H., Cho K.-H., Chien W.-L., Wang W.-T., Wu T.-W., Lin C.-P., Fu W.-M., Shen C.-K.J. Elevated expression of TDP-43 in the forebrain of mice is sufficient to cause neurological and pathological phenotypes mimicking FTLD-U. J. Exp. Med. 2010, 207:1661-1673.
66. Igaz L.M., Kwong L.K., Lee E.B., Chen-Plotkin A., Swanson E., Unger T., Malunda J., Xu Y., Winton M.J., Trojanowski J.Q., Lee V.M.-Y. Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice. J. Clin. Invest. 2011, 121:726-738.
67. Cannon A., Yang B., Knight J., Farnham I.M., Zhang Y., Wuertzer C.A., D'Alton S., Lin W., Castanedes-Casey M., Rousseau L., Scott B., Jurasic M., Howard J., Yu X., Bailey R., Sarkisian M.R., Dickson D.W., Petrucelli L., Lewis J. Neuronal sensitivity to TDP-43 overexpression is dependent on timing of induction. Acta Neuropathol. 2012, 123:807-823.
68. Swarup V., Phaneuf D., Bareil C., Robertson J., Rouleau G.A., Kriz J., Julien J.-P. Pathological hallmarks of amyotrophic lateral sclerosis/frontotemporal lobar degeneration in transgenic mice produced with TDP-43 genomic fragments. Brain 2011, 134:2610-2626.
69. Zhou H., Huang C., Chen H., Wang D., Landel C.P., Xia P.Y., Bowser R., Liu Y.-J., Xia X.G. Transgenic rat model of neurodegeneration caused by mutation in the TDP gene. PLoS Genet. 2010, 6:e1000887.
70. Huang C., Tong J., Bi F., Zhou H., Xia X.-G. Mutant TDP-43 in motor neurons promotes the onset and progression of ALS in rats. J. Clin. Invest. 2012, 122:107-118.
71. Mitchell J.C., McGoldrick P., Vance C., Hortobagyi T., Sreedharan J., Rogelj B., Tudor E.L., Smith B.N., Klasen C., Miller C.C.J., Cooper J.D., Greensmith L., Shaw C.E. Overexpression of human wild-type FUS causes progressive motor neuron degeneration in an age- and dose-dependent fashion. Acta Neuropathol. 2012, 125:273-288.
72. Verbeeck C., Deng Q., Dejesus-Hernandez M., Taylor G., Ceballos-Diaz C., Kocerha J., Golde T.E., Das P., Rademakers R., Dickson D.W., Kukar T. Expression of Fused in sarcoma mutations in mice recapitulates the neuropathology of FUS proteinopathies and provides insight into disease pathogenesis. Mol. Neurodegener. 2012, 7:53.
73. Huang C., Zhou H., Tong J., Chen H., Liu Y.-J., Wang D., Wei X., Xia X.-G. FUS transgenic rats develop the phenotypes of amyotrophic lateral sclerosis and frontotemporal lobar degeneration. PLoS Genet. 2011, 7:e1002011.
74. Huang C., Tong J., Bi F., Wu Q., Huang B., Zhou H., Xia X.-G. Entorhinal cortical neurons are the primary targets of FUS mislocalization and ubiquitin aggregation in FUS transgenic rats. Hum. Mol. Genet. 2012, 21:4602-4614.
75. Chiang P.-M., Ling J., Jeong Y.H., Price D.L., Aja S.M., Wong P.C. Deletion of TDP-43 down-regulates Tbc1d1, a gene linked to obesity, and alters body fat metabolism. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:16320-16324.
76. Kraemer B.C., Schuck T., Wheeler J.M., Robinson L.C., Trojanowski J.Q., Lee V.M.Y., Schellenberg G.D. Loss of murine TDP-43 disrupts motor function and plays an essential role in embryogenesis. Acta Neuropathol. 2010, 119:409-419.
77. Wu L.-S., Cheng W.-C., Hou S.-C., Yan Y.-T., Jiang S.-T., Shen C.-K.J. TDP-43, a neuro-pathosignature factor, is essential for early mouse embryogenesis. Genesis 2010, 48:56-62.
78. Borchelt D.R., Davis J., Fischer M., Lee M.K., Slunt H.H., Ratovitsky T., Regard J., Copeland N.G., Jenkins N.A., Sisodia S.S., Price D.L. A vector for expressing foreign genes in the brains and hearts of transgenic mice. Genet. Anal. 1996, 13:159-163.
79. Wang I.-F., Guo B.-S., Liu Y.-C., Wu C.-C., Yang C.-H., Tsai K.-J., Shen C.-K.J. Autophagy activators rescue and alleviate pathogenesis of a mouse model with proteinopathies of the TAR DNA-binding protein 43. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:15024-15029.
80. Uchida A., Sasaguri H., Kimura N., Tajiri M., Ohkubo T., Ono F., Sakaue F., Kanai K., Hirai T., Sano T., Shibuya K., Kobayashi M., Yamamoto M., Yokota S., Kubodera T., Tomori M., Sakaki K., Enomoto M., Hirai Y., Kumagai J., Yasutomi Y., Mochizuki H., Kuwabara S., Uchihara T., Mizusawa H., Yokota T. Non-human primate model of amyotrophic lateral sclerosis with cytoplasmic mislocalization of TDP-43. Brain 2012, 135:833-846.
81. Lemon R.N. Descending pathways in motor control. Annu. Rev. Neurosci. 2008, 31:195-218.
82. Crozat A., Aman P., Mandahl N., Ron D. Fusion of CHOP to a novel RNA-binding protein in human myxoid liposarcoma. Nature 1993, 363:640-644.
83. Rabbitts T.H., Forster A., Larson R., Nathan P. Fusion of the dominant negative transcription regulator CHOP with a novel gene FUS by translocation t(12;16) in malignant liposarcoma. Nat. Genet. 1993, 4:175-180.
84. Prasad D.D., Ouchida M., Lee L., Rao V.N., Reddy E.S. TLS/FUS fusion domain of TLS/FUS-erg chimeric protein resulting from the t(16;21) chromosomal translocation in human myeloid leukemia functions as a transcriptional activation domain. Oncogene 1994, 9:3717-3729.
85. Udan M., Baloh R.H. Implications of the prion-related Q/N domains in TDP-43 and FUS. Prion 2011, 5:1-5.
86. Dormann D., Rodde R., Edbauer D., Bentmann E., Fischer I., Hruscha A., Than M.E., Mackenzie I.R.A., Capell A., Schmid B., Neumann M., Haass C. ALS-associated fused in sarcoma (FUS) mutations disrupt Transportin-mediated nuclear import. EMBO J. 2010, 29:2841-2857.
87. Huang C., Xia P.Y., Zhou H. Sustained expression of TDP-43 and FUS in motor neurons in rodent's lifetime. Int. J. Biol. Sci. 2010, 6:396-406.
88. Bosco D.A., Lemay N., Ko H.K., Zhou H., Burke C., Kwiatkowski T.J., Sapp P., McKenna-Yasek D., Brown R.H., Hayward L.J. Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Hum. Mol. Genet. 2010, 19:4160-4175.
89. Gal J., Zhang J., Kwinter D.M., Zhai J., Jia H., Jia J., Zhu H. Nuclear localization sequence of FUS and induction of stress granules by ALS mutants. Neurobiol. Aging 2011, 32:2323.e27-2323.e40.
90. Kabashi E., Bercier V., Lissouba A., Liao M., Brustein E., Rouleau G.A., Drapeau P. FUS and TARDBP but not SOD1 interact in genetic models of amyotrophic lateral sclerosis. PLoS Genet. 2011, 7:e1002214.
91. Hicks G.G., Singh N., Nashabi A., Mai S., Bozek G., Klewes L., Arapovic D., White E.K., Koury M.J., Oltz E.M., Van Kaer L., Ruley H.E. Fus deficiency in mice results in defective B-lymphocyte development and activation, high levels of chromosomal instability and perinatal death. Nat. Genet. 2000, 24:175-179.
92. Kuroda M., Sok J., Webb L., Baechtold H., Urano F., Yin Y., Chung P., de Rooij D.G., Akhmedov A., Ashley T., Ron D. Male sterility and enhanced radiation sensitivity in TLS(-/-) mice. EMBO J. 2000, 19:453-462.
93. Kimonis V.E., Fulchiero E., Vesa J., Watts G. VCP disease associated with myopathy, Paget disease of bone and frontotemporal dementia: review of a unique disorder. Biochim. Biophys. Acta 2008, 1782:744-748.
94. Badadani M., Nalbandian A., Watts G.D., Vesa J., Kitazawa M., Su H., Tanaja J., Dec E., Wallace D.C., Mukherjee J., Caiozzo V., Warman M., Kimonis V.E. VCP associated inclusion body myopathy and paget disease of bone knock-in mouse model exhibits tissue pathology typical of human disease. PLoS One 2010, 5.
95. Custer S.K., Neumann M., Lu H., Wright A.C., Taylor J.P. Transgenic mice expressing mutant forms VCP/p97 recapitulate the full spectrum of IBMPFD including degeneration in muscle, brain and bone. Hum. Mol. Genet. 2010, 19:1741-1755.
96. Meyer H., Bug M., Bremer S. Emerging functions of the VCP/p97 AAA-ATPase in the ubiquitin system. Nat. Cell Biol. 2012, 14:117-123.
97. Yamanaka K., Sasagawa Y., Ogura T. Recent advances in p97/VCP/Cdc48 cellular functions. Biochim. Biophys. Acta 2012, 1823:130-137.
98. Müller J.M.M., Deinhardt K., Rosewell I., Warren G., Shima D.T. Targeted deletion of p97 (VCP/CDC48) in mouse results in early embryonic lethality. Biochem. Biophys. Res. Commun. 2007, 354:459-465.
99. Yin H.Z., Nalbandian A., Hsu C.-I., Li S., Llewellyn K.J., Mozaffar T., Kimonis V.E., Weiss J.H. Slow development of ALS-like spinal cord pathology in mutant valosin-containing protein gene knock-in mice. Cell Death Dis. 2012, 3:e374.
100. Nalbandian A., Llewellyn K.J., Kitazawa M., Yin H.Z., Badadani M., Khanlou N., Edwards R., Nguyen C., Mukherjee J., Mozaffar T., Watts G., Weiss J., Kimonis V.E. The homozygote VCP(R155H/R155H) Mouse model exhibits accelerated human VCP-associated disease pathology. PLoS One 2012, 7:e46308.
101. Niu C., Zhang J., Gao F., Yang L., Jia M., Zhu H., Gong W. FUS-NLS/Transportin 1 complex structure provides insights into the nuclear targeting mechanism of FUS and the implications in ALS. PLoS ONE 2012, 7:e47056.
102. Zhang Z.C., Chook Y.M. Structural and energetic basis of ALS-causing mutations in the atypical proline-tyrosine nuclear localization signal of the Fused in Sarcoma protein (FUS). Proc. Natl. Acad. Sci. U. S. A. 2012, 109:12017-12021.
103. Joyce P.I., Fratta P., Fisher E.M.C., Acevedo-Arozena A. SOD1 and TDP-43 animal models of amyotrophic lateral sclerosis: recent advances in understanding disease toward the development of clinical treatments. Mamm. Genome 2011, 22:420-448.
104. Ghoddoussi F., Galloway M.P., Jambekar A., Bame M., Needleman R., Brusilow W.S.A. Methionine sulfoximine, an inhibitor of glutamine synthetase, lowers brain glutamine and glutamate in a mouse model of ALS. J. Neurol. Sci. 2010, 290:41-47.
105. Paizs M., Tortarolo M., Bendotti C., Engelhardt J.I., Siklós L. Talampanel reduces the level of motoneuronal calcium in transgenic mutant SOD1 mice only if applied presymptomatically. Amyotroph. Lateral Scler. 2011, 12:340-344.
106. 93A) mice. Neuroscience 2012, 220:26-31.
107. Takeuchi H., Mizoguchi H., Doi Y., Jin S., Noda M., Liang J., Li H., Zhou Y., Mori R., Yasuoka S., Li E., Parajuli B., Kawanokuchi J., Sonobe Y., Sato J., Yamanaka K., Sobue G., Mizuno T., Suzumura A. Blockade of gap junction hemichannel suppresses disease progression in mouse models of amyotrophic lateral sclerosis and Alzheimer's disease. PLoS One 2011, 6:e21108.
108. Thompson M., Marecki J.C., Marinesco S., Labrie V., Roder J.C., Barger S.W., Crow J.P. Paradoxical roles of serine racemase and D-serine in the G93A mSOD1 mouse model of amyotrophic lateral sclerosis. J. Neurochem. 2012, 120:598-610.
109. Amante D.J., Kim J., Carreiro S.T., Cooper A.C., Jones S.W., Li T., Moody J.P., Edgerly C.K., Bordiuk O.L., Cormier K., Smith K., Ferrante R.J., Rusche J. Uridine ameliorates the pathological phenotype in transgenic G93A-ALS mice. Amyotroph. Lateral Scler. 2010, 11:520-530.
110. Miquel E., Cassina A., Martínez-Palma L., Bolatto C., Trías E., Gandelman M., Radi R., Barbeito L., Cassina P. Modulation of astrocytic mitochondrial function by dichloroacetate improves survival and motor performance in inherited amyotrophic lateral sclerosis. PLoS One 2012, 7:e34776.
111. Kupershmidt L., Weinreb O., Amit T., Mandel S., Carri M.T., Youdim M.B.H. Neuroprotective and neuritogenic activities of novel multimodal iron-chelating drugs in motor-neuron-like NSC-34 cells and transgenic mouse model of amyotrophic lateral sclerosis. FASEB J. 2009, 23:3766-3779.
112. Shimojo Y., Kosaka K., Noda Y., Shimizu T., Shirasawa T. Effect of rosmarinic acid in motor dysfunction and life span in a mouse model of familial amyotrophic lateral sclerosis. J. Neurosci. Res. 2010, 88:896-904.
113. Hashimoto K., Hayashi Y., Watabe K., Inuzuka T., Hozumi I. Metallothionein-III prevents neuronal death and prolongs life span in amyotrophic lateral sclerosis model mice. Neuroscience 2011, 189:293-298.
114. Kaneb H.M., Sharp P.S., Rahmani-Kondori N., Wells D.J. Metformin treatment has no beneficial effect in a dose-response survival study in the SOD1(G93A) mouse model of ALS and is harmful in female mice. PLoS One 2011, 6:e24189.
115. Wang Q., Zhang X., Chen S., Zhang X., Zhang S., Youdium M., Le W. Prevention of motor neuron degeneration by novel iron chelators in SOD1(G93A) transgenic mice of amyotrophic lateral sclerosis. Neurodegener. Dis. 2011, 8:310-321.
116. Trumbull K.A., McAllister D., Gandelman M.M., Fung W.Y., Lew T., Brennan L., Lopez N., Morré J., Kalyanaraman B., Beckman J.S. Diapocynin and apocynin administration fails to significantly extend survival in G93A SOD1 ALS mice. Neurobiol. Dis. 2012, 45:137-144.
117. Soon C.P.W., Donnelly P.S., Turner B.J., Hung L.W., Crouch P.J., Sherratt N.A., Tan J.-L., Lim N.K.-H., Lam L., Bica L., Lim S., Hickey J.L., Morizzi J., Powell A., Finkelstein D.I., Culvenor J.G., Masters C.L., Duce J., White A.R., Barnham K.J., et al. Diacetylbis(N(4)-methylthiosemicarbazonato) copper(II) (CuII(atsm)) protects against peroxynitrite-induced nitrosative damage and prolongs survival in amyotrophic lateral sclerosis mouse model. J. Biol. Chem. 2011, 286:44035-44044.
118. Chian R.-J., Li J., Ay I., Celia S.A., Kashi B.B., Tamrazian E., Matthews J.C., Bronson R.T., Rossomando A., Pepinsky R.B., Fishman P.S., Brown R.H., Francis J.W. IGF-1:tetanus toxin fragment C fusion protein improves delivery of IGF-1 to spinal cord but fails to prolong survival of ALS mice. Brain Res. 2009, 1287:1-19.
119. Franz C.K., Federici T., Yang J., Backus C., Oh S.S., Teng Q., Carlton E., Bishop K.M., Gasmi M., Bartus R.T., Feldman E.L., Boulis N.M. Intraspinal cord delivery of IGF-I mediated by adeno-associated virus 2 is neuroprotective in a rat model of familial ALS. Neurobiol. Dis. 2009, 33:473-481.
120. Riddoch-Contreras J., Yang S.-Y., Dick J.R.T., Goldspink G., Orrell R.W., Greensmith L. Mechano-growth factor, an IGF-I splice variant, rescues motoneurons and improves muscle function in SOD1(G93A) mice. Exp. Neurol. 2009, 215:281-289.
121. Barbeito A.G., Martinez-Palma L., Vargas M.R., Pehar M., Mañay N., Beckman J.S., Barbeito L., Cassina P. Lead exposure stimulates VEGF expression in the spinal cord and extends survival in a mouse model of ALS. Neurobiol. Dis. 2010, 37:574-580.
122. Dodge J.C., Treleaven C.M., Fidler J.A., Hester M., Haidet A., Handy C., Rao M., Eagle A., Matthews J.C., Taksir T.V., Cheng S.H., Shihabuddin L.S., Kaspar B.K. AAV4-mediated expression of IGF-1 and VEGF within cellular components of the ventricular system improves survival outcome in familial ALS mice. Mol. Ther. 2010, 18:2075-2084.
123. Calvo A.C., Moreno-Igoa M., Mancuso R., Manzano R., Oliván S., Muñoz M.J., Penas C., Zaragoza P., Navarro X., Osta R. Lack of a synergistic effect of a non-viral ALS gene therapy based on BDNF and a TTC fusion molecule. Orphanet J. Rare Dis. 2011, 6:10.
124. Li Y., Chigurupati S., Holloway H.W., Mughal M., Tweedie D., Bruestle D.A., Mattson M.P., Wang Y., Harvey B.K., Ray B., Lahiri D.K., Greig N.H. Exendin-4 ameliorates motor neuron degeneration in cellular and animal models of amyotrophic lateral sclerosis. PLoS One 2012, 7:e32008.
125. Saenger S., Holtmann B., Nilges M.R., Schroeder S., Hoeflich A., Kletzl H., Spooren W., Ostrowitzki S., Hanania T., Sendtner M., Metzger F. Functional improvement in mouse models of familial amyotrophic lateral sclerosis by PEGylated insulin-like growth factor I treatment depends on disease severity. Amyotroph. Lateral Scler. 2012, 13:418-429.
126. Gros-Louis F., Soucy G., Larivière R., Julien J.-P. Intracerebroventricular infusion of monoclonal antibody or its derived Fab fragment against misfolded forms of SOD1 mutant delays mortality in a mouse model of ALS. J. Neurochem. 2010, 113:1188-1199.
127. Zhang X., Li L., Chen S., Yang D., Wang Y., Zhang X., Wang Z., Le W. Rapamycin treatment augments motor neuron degeneration in SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Autophagy 2011, 7:412-425.
128. Chen T., Benmohamed R., Kim J., Smith K., Amante D., Morimoto R.I., Kirsch D.R., Ferrante R.J., Silverman R.B. ADME-guided design and synthesis of aryloxanyl pyrazolone derivatives to block mutant superoxide dismutase 1 (SOD1) cytotoxicity and protein aggregation: potential application for the treatment of amyotrophic lateral sclerosis. J. Med. Chem. 2012, 55:515-527.
129. Han S., Choi J.-R., Soon Shin K., Kang S.J. Resveratrol upregulated heat shock proteins and extended the survival of G93A-SOD1 mice. Brain Res. 2012, 1483:112-117.
130. Gifondorwa D.J., Jimenz-Moreno R., Hayes C.D., Rouhani H., Robinson M.B., Strupe J.L., Caress J., Milligan C. Administration of recombinant heat shock protein 70 delays peripheral muscle denervation in the SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Neurol. Res. Int. 2012, 2012:170426.
131. Zhang Y., Benmohamed R., Zhang W., Kim J., Edgerly C.K., Zhu Y., Morimoto R.I., Ferrante R.J., Kirsch D.R., Silverman R.B. Chiral cyclohexane 1,3-diones as inhibitors of mutant SOD1-dependent protein aggregation for the treatment of ALS. ACS Med. Chem. Lett. 2012, 3:584-587.
132. Liu H.-N., Tjostheim S., Dasilva K., Taylor D., Zhao B., Rakhit R., Brown M., Chakrabartty A., McLaurin J., Robertson J. Targeting of monomer/misfolded SOD1 as a therapeutic strategy for amyotrophic lateral sclerosis. J. Neurosci. 2012, 32:8791-8799.
133. Lu C.-H., Petzold A., Kalmar B., Dick J., Malaspina A., Greensmith L. Plasma neurofilament heavy chain levels correlate to markers of late stage disease progression and treatment response in SOD1(G93A) mice that model ALS. PLoS One 2012, 7:e40998.
134. Takeuchi S., Fujiwara N., Ido A., Oono M., Takeuchi Y., Tateno M., Suzuki K., Takahashi R., Tooyama I., Taniguchi N., Julien J.-P., Urushitani M. Induction of protective immunity by vaccination with wild-type apo superoxide dismutase 1 in mutant SOD1 transgenic mice. J. Neuropathol. Exp. Neurol. 2010, 69:1044-1056.
135. Neymotin A., Petri S., Calingasan N.Y., Wille E., Schafer P., Stewart C., Hensley K., Beal M.F., Kiaei M. Lenalidomide (Revlimid) administration at symptom onset is neuroprotective in a mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 2009, 220:191-197.
136. Henriques A., Pitzer C., Dittgen T., Klugmann M., Dupuis L., Schneider A. CNS-targeted viral delivery of G-CSF in an animal model for ALS: improved efficacy and preservation of the neuromuscular unit. Mol. Ther. 2011, 19:284-292.
137. Lincecum J.M., Vieira F.G., Wang M.Z., Thompson K., De Zutter G.S., Kidd J., Moreno A., Sanchez R., Carrion I.J., Levine B.A., Al-Nakhala B.M., Sullivan S.M., Gill A., Perrin S. From transcriptome analysis to therapeutic anti-CD40L treatment in the SOD1 model of amyotrophic lateral sclerosis. Nat. Genet. 2010, 42:392-399.
138. Keller A.F., Gravel M., Kriz J. Treatment with minocycline after disease onset alters astrocyte reactivity and increases microgliosis in SOD1 mutant mice. Exp. Neurol. 2011, 228:69-79.
139. Naumenko N., Pollari E., Kurronen A., Giniatullina R., Shakirzyanova A., Magga J., Koistinaho J., Giniatullin R. Gender-specific mechanism of synaptic impairment and its prevention by GCSF in a mouse model of ALS. Front. Cell. Neurosci. 2011, 5:26.
140. Pollari E., Savchenko E., Jaronen M., Kanninen K., Malm T., Wojciechowski S., Ahtoniemi T., Goldsteins G., Giniatullina R., Giniatullin R., Koistinaho J., Magga J. Granulocyte colony stimulating factor attenuates inflammation in a mouse model of amyotrophic lateral sclerosis. J. Neuroinflammation 2011, 8:74.
141. Yang E.J., Kim S.H., Yang S.C., Lee S.M., Choi S.-M. Melittin restores proteasome function in an animal model of ALS. J. Neuroinflammation 2011, 8:69.
142. Butovsky O., Siddiqui S., Gabriely G., Lanser A.J., Dake B., Murugaiyan G., Doykan C.E., Wu P.M., Gali R.R., Iyer L.K., Lawson R., Berry J., Krichevsky A.M., Cudkowicz M.E., Weiner H.L. Modulating inflammatory monocytes with a unique microRNA gene signature ameliorates murine ALS. J. Clin. Invest. 2012, 122:3063-3087.
143. Fontanilla C.V., Wei X., Zhao L., Johnstone B., Pascuzzi R.M., Farlow M.R., Du Y. Caffeic acid phenethyl ester extends survival of a mouse model of amyotrophic lateral sclerosis. Neuroscience 2012, 205:185-193.
144. Gowing G., Lalancette-Hébert M., Audet J.-N., Dequen F., Julien J.-P. Macrophage colony stimulating factor (M-CSF) exacerbates ALS disease in a mouse model through altered responses of microglia expressing mutant superoxide dismutase. Exp. Neurol. 2009, 220:267-275.
145. Crochemore C., Virgili M., Bonamassa B., Canistro D., Pena-Altamira E., Paolini M., Contestabile A. Long-term dietary administration of valproic acid does not affect, while retinoic acid decreases, the lifespan of G93A mice, a model for amyotrophic lateral sclerosis. Muscle Nerve 2009, 39:548-552.
146. Lee J., Ryu H., Kowall N.W. Motor neuronal protection by l-arginine prolongs survival of mutant SOD1 (G93A) ALS mice. Biochem. Biophys. Res. Commun. 2009, 384:524-529.
147. Morrison B.M., Lachey J.L., Warsing L.C., Ting B.L., Pullen A.E., Underwood K.W., Kumar R., Sako D., Grinberg A., Wong V., Colantuoni E., Seehra J.S., Wagner K.R. A soluble activin type IIB receptor improves function in a mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 2009, 217:258-268.
148. Zhong Z., Ilieva H., Hallagan L., Bell R., Singh I., Paquette N., Thiyagarajan M., Deane R., Fernandez J.A., Lane S., Zlokovic A.B., Liu T., Griffin J.H., Chow N., Castellino F.J., Stojanovic K., Cleveland D.W., Zlokovic B.V. Activated protein C therapy slows ALS-like disease in mice by transcriptionally inhibiting SOD1 in motor neurons and microglia cells. J. Clin. Invest. 2009, 119:3437-3449.
149. Shimazawa M., Tanaka H., Ito Y., Morimoto N., Tsuruma K., Kadokura M., Tamura S., Inoue T., Yamada M., Takahashi H., Warita H., Aoki M., Hara H. An inducer of VGF protects cells against ER stress-induced cell death and prolongs survival in the mutant SOD1 animal models of familial ALS. PLoS One 2010, 5:e15307.
150. Suchy J., Lee S., Ahmed A., Shea T.B. Dietary supplementation with S-adenosyl methionine delays the onset of motor neuron pathology in a murine model of amyotrophic lateral sclerosis. Neuromolecular Med. 2010, 12:86-97.
151. Guo Y., Zhang K., Wang Q., Li Z., Yin Y., Xu Q., Duan W., Li C. Neuroprotective effects of diallyl trisulfide in SOD1-G93A transgenic mouse model of amyotrophic lateral sclerosis. Brain Res. 2011, 1374:110-115.
152. Neymotin A., Calingasan N.Y., Wille E., Naseri N., Petri S., Damiano M., Liby K.T., Risingsong R., Sporn M., Beal M.F., Kiaei M. Neuroprotective effect of Nrf2/ARE activators, CDDO ethylamide and CDDO trifluoroethylamide, in a mouse model of amyotrophic lateral sclerosis. Free Radic. Biol. Med. 2011, 51:88-96.
153. Seo J.-S., Baek I.-S., Leem Y.-H., Kim T.-K., Cho Y., Lee S.M., Park Y.H., Han P.-L. SK-PC-B70M alleviates neurologic symptoms in G93A-SOD1 amyotrophic lateral sclerosis mice. Brain Res. 2011, 1368:299-307.
154. Yoo Y.-E., Ko C.-P. Treatment with trichostatin A initiated after disease onset delays disease progression and increases survival in a mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 2011, 231:147-159.
155. Cappello V., Vezzoli E., Righi M., Fossati M., Mariotti R., Crespi A., Patruno M., Bentivoglio M., Pietrini G., Francolini M. Analysis of neuromuscular junctions and effects of anabolic steroid administration in the SOD1G93A mouse model of ALS. Mol. Cell. Neurosci. 2012, 51:12-21.
156. Eitan E., Tichon A., Gazit A., Gitler D., Slavin S., Priel E. Novel telomerase-increasing compound in mouse brain delays the onset of amyotrophic lateral sclerosis. EMBO Mol. Med. 2012, 4:313-329.
157. Hayes-Punzo A., Mulcrone P., Meyer M., McHugh J., Svendsen C.N., Suzuki M. Gonadectomy and dehydroepiandrosterone (DHEA) do not modulate disease progression in the G93A mutant SOD1 rat model of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2012, 13:311-314.
158. Jouroukhin Y., Ostritsky R., Gozes I. D-NAP prophylactic treatment in the SOD mutant mouse model of amyotrophic lateral sclerosis: review of discovery and treatment of tauopathy. J. Mol. Neurosci. 2012, 48:597-602.
159. Katsumata R., Ishigaki S., Katsuno M., Kawai K., Sone J., Huang Z., Adachi H., Tanaka F., Urano F., Sobue G. c-Abl inhibition delays motor neuron degeneration in the G93A Mouse, an animal model of amyotrophic lateral sclerosis. PLoS One 2012, 7:e46185.
160. Li J., Paulson J.M., Ye F.D., Sung M., Hollenberg A.N., Rutkove S.B. Reducing systemic hypermetabolism by inducing hypothyroidism does not prolong survival in the SOD1-G93A mouse. Amyotroph. Lateral Scler. 2012, 13:372-377.
161. Mancuso R., Oliván S., Mancera P., Pastén-Zamorano A., Manzano R., Casas C., Osta R., Navarro X. Effect of genetic background on onset and disease progression in the SOD1-G93A model of amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2012, 13:302-310.
162. Sunyach C., Michaud M., Arnoux T., Bernard-Marissal N., Aebischer J., Latyszenok V., Gouarné C., Raoul C., Pruss R.M., Bordet T., Pettmann B. Olesoxime delays muscle denervation, astrogliosis, microglial activation and motoneuron death in an ALS mouse model. Neuropharmacology 2012, 62:2346-2352.
163. Tesla R., Wolf H.P., Xu P., Drawbridge J., Estill S.J., Huntington P., McDaniel L., Knobbe W., Burket A., Tran S., Starwalt R., Morlock L., Naidoo J., Williams N.S., Ready J.M., McKnight S.L., Pieper A.A. Neuroprotective efficacy of aminopropyl carbazoles in a mouse model of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:17016-17021.
164. Yoo Y.-E., Ko C.-P. Dihydrotestosterone ameliorates degeneration in muscle, axons and motoneurons and improves motor function in amyotrophic lateral sclerosis model mice. PLoS One 2012, 7:e37258.
165. Tanaka K., Kanno T., Yanagisawa Y., Yasutake K., Hadano S., Yoshii F., Ikeda J.-E. Bromocriptine methylate suppresses glial inflammation and moderates disease progression in a mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 2011, 232:41-52.
166. Kanno T., Tanaka K., Yanagisawa Y., Yasutake K., Hadano S., Yoshii F., Hirayama N., Ikeda J.-E. A novel small molecule, N-(4-(2-pyridyl)(1,3-thiazol-2-yl))-2-(2,4,6-trimethylphenoxy) acetamide, selectively protects against oxidative stress-induced cell death by activating the Nrf2-ARE pathway: therapeutic implications for ALS. Free Radic. Biol. Med. 2012, 53:2028-2042.
167. 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.
168. Ferrucci M., Spalloni A., Bartalucci A., Cantafora E., Fulceri F., Nutini M., Longone P., Paparelli A., Fornai F. A systematic study of brainstem motor nuclei in a mouse model of ALS, the effects of lithium. Neurobiol. Dis. 2010, 37:370-383.
169. Solomon J.A., Gianforcaro A., Hamadeh M.J. Vitamin D3 deficiency differentially affects functional and disease outcomes in the G93A mouse model of amyotrophic lateral sclerosis. PLoS One 2011, 6:e29354.
170. Audet J.-N., Soucy G., Julien J.-P. Methylene blue administration fails to confer neuroprotection in two amyotrophic lateral sclerosis mouse models. Neuroscience 2012, 209:136-143.
171. Dibaj P., Zschüntzsch J., Steffens H., Scheffel J., Göricke B., Weishaupt J.H., Le Meur K., Kirchhoff F., Hanisch U.-K., Schomburg E.D., Neusch C. Influence of methylene blue on microglia-induced inflammation and motor neuron degeneration in the SOD1(G93A) model for ALS. PLoS One 2012, 7:e43963.
172. Feng X., Peng Y., Liu M., Cui L. DL-3-n-butylphthalide extends survival by attenuating glial activation in a mouse model of amyotrophic lateral sclerosis. Neuropharmacology 2012, 62:1004-1010.
173. Gianforcaro A., Hamadeh M.J. Dietary vitamin D3 supplementation at 10× the adequate intake improves functional capacity in the G93A transgenic mouse model of ALS, a pilot study. CNS Neurosci. Ther. 2012, 18:547-557.
174. Lougheed R., Turnbull J. Lack of effect of methylene blue in the SOD1 G93A mouse model of amyotrophic lateral sclerosis. PLoS One 2011, 6:e23141.
175. Li Q., Vande Velde C., Israelson A., Xie J., Bailey A.O., Dong M.-Q., Chun S.-J., Roy T., Winer L., Yates J.R., Capaldi R.A., Cleveland D.W., Miller T.M. ALS-linked mutant superoxide dismutase 1 (SOD1) alters mitochondrial protein composition and decreases protein import. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:21146-21151.
176. Israelson A., Arbel N., Da Cruz S., Ilieva H., Yamanaka K., Shoshan-Barmatz V., Cleveland D.W. Misfolded mutant SOD1 directly inhibits VDAC1 conductance in a mouse model of inherited ALS. Neuron 2010, 67:575-587.
177. Jung C., Higgins C.M.J., Xu Z. A quantitative histochemical assay for activities of mitochondrial electron transport chain complexes in mouse spinal cord sections. J. Neurosci. Methods 2002, 114:165-172.
178. Mattiazzi M., D'Aurelio M., Gajewski C.D., Martushova K., Kiaei M., Beal M.F., Manfredi G. Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice. J. Biol. Chem. 2002, 277:29626-29633.
179. Jaiswal M.K., Keller B.U. Cu/Zn superoxide dismutase typical for familial amyotrophic lateral sclerosis increases the vulnerability of mitochondria and perturbs Ca2+ homeostasis in SOD1G93A mice. Mol. Pharmacol. 2009, 75:478-489.
180. Gribkoff V.K., Bozik M.E. KNS-760704 [(6R)-4,5,6,7-tetrahydro-N6-propyl-2, 6-benzothiazole-diamine dihydrochloride monohydrate] for the treatment of amyotrophic lateral sclerosis. CNS Neurosci. Ther. 2008, 14:215-226.
181. Cudkowicz M., Bozik M.E., Ingersoll E.W., Miller R., Mitsumoto H., Shefner J., Moore D.H., Schoenfeld D., Mather J.L., Archibald D., Sullivan M., Amburgey C., Moritz J., Gribkoff V.K. The effects of dexpramipexole (KNS-760704) in individuals with amyotrophic lateral sclerosis. Nat. Med. 2011, 17:1652-1656.
182. http://www.biogenidec.com/PRESS_RELEASE_DETAILS.aspx?ID=5981&ReqId=1770780.
183. Pickles S., Vande Velde C. Misfolded SOD1 and ALS: zeroing in on mitochondria. Amyotroph. Lateral Scler. 2012, 13:333-340.
184. Barber S.C., Shaw P.J. Oxidative stress in ALS: key role in motor neuron injury and therapeutic target. Free Radic. Biol. Med. 2010, 48:629-641.
185. Ilieva H., Polymenidou M., Cleveland D.W. Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J. Cell Biol. 2009, 187:761-772.
186. Roberts K., Zeineddine R., Corcoran L., Li W., Campbell I.L., Yerbury J.J. Extracellular aggregated Cu/Zn superoxide dismutase activates microglia to give a cytotoxic phenotype. Glia 2013, 61:409-419.
187. McCombe P.A., Henderson R.D. The Role of immune and inflammatory mechanisms in ALS. Curr. Mol. Med. 2011, 11:246-254.
188. Papadimitriou D., Le Verche V., Jacquier A., Ikiz B., Przedborski S., Re D.B. Inflammation in ALS and SMA: sorting out the good from the evil. Neurobiol. Dis. 2010, 37:493-502.
189. Philips T., Robberecht W. Neuroinflammation in amyotrophic lateral sclerosis: role of glial activation in motor neuron disease. Lancet Neurol. 2011, 10:253-263.
190. Gordon P.H., Moore D.H., Miller R.G., Florence J.M., Verheijde J.L., Doorish C., Hilton J.F., Spitalny G.M., MacArthur R.B., Mitsumoto H., Neville H.E., Boylan K., Mozaffar T., Belsh J.M., Ravits J., Bedlack R.S., Graves M.C., McCluskey L.F., Barohn R.J., Tandan R. Efficacy of minocycline in patients with amyotrophic lateral sclerosis: a phase III randomised trial. Lancet Neurol. 2007, 6:1045-1053.
191. Stommel E.W., Cohen J.A., Fadul C.E., Cogbill C.H., Graber D.J., Kingman L., Mackenzie T., Channon Smith J.Y., Harris B.T. Efficacy of thalidomide for the treatment of amyotrophic lateral sclerosis: a phase II open label clinical trial. Amyotroph. Lateral Scler. 2009, 10:393-404.
192. Bellingham M.C. A review of the neural mechanisms of action and clinical efficiency of riluzole in treating amyotrophic lateral sclerosis: what have we learned in the last decade?. CNS Neurosci. Ther. 2011, 17:4-31.
193. Cheah B.C., Vucic S., Krishnan A.V., Kiernan M.C. Riluzole, neuroprotection and amyotrophic lateral sclerosis. Curr. Med. Chem. 2010, 17:1942-1959.
194. Miller R.G., Mitchell J.D., Moore D.H. Riluzole for amyotrophic lateral sclerosis (ALS)/motor neuron disease (MND). Cochrane Database Syst. Rev. 2012, 3:CD001447.
195. Rothstein J.D., Van Kammen M., Levey A.I., Martin L.J., Kuncl R.W. Selective loss of glial glutamate transporter GLT-1 in amyotrophic lateral sclerosis. Ann. Neurol. 1995, 38:73-84.
196. Rothstein J.D. Excitotoxicity and neurodegeneration in amyotrophic lateral sclerosis. Clin. Neurosci. 1995, 3:348-359.
197. http://www.nealsconsortium.org/news_ceftriaxone_announcement.php.
198. de Carvalho M., Pinto S., Costa J., Evangelista T., Ohana B., Pinto A. A randomized, placebo-controlled trial of memantine for functional disability in amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2010, 11:456-460.
199. Pascuzzi R.M., Shefner J., Chappell A.S., Bjerke J.S., Tamura R., Chaudhry V., Clawson L., Haas L., Rothstein J.D. A phase II trial of talampanel in subjects with amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2010, 11:266-271.
200. Sorenson E.J., Windbank A.J., Mandrekar J.N., Bamlet W.R., Appel S.H., Armon C., Barkhaus P.E., Bosch P., Boylan K., David W.S., Feldman E., Glass J., Gutmann L., Katz J., King W., Luciano C.A., McCluskey L.F., Nash S., Newman D.S., Pascuzzi R.M., Pioro E., Sams L.J., Sclesa S., Simpson E.P., Subramony S.H., Tiryaki E., Thornton C.A. Subcutaneous IGF-1 is not beneficial in 2-year ALS trial. Neurology 2008, 71:1770-1775.
201. De Vos K.J., Grierson A.J., Ackerley S., Miller C.C.J. Role of axonal transport in neurodegenerative diseases. Annu. Rev. Neurosci. 2008, 31:151-173.
202. Bilsland L.G., Sahai E., Kelly G., Golding M., Greensmith L., Schiavo G. Deficits in axonal transport precede ALS symptoms in vivo. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20523-20528.
203. Kieran D., Hafezparast M., Bohnert S., Dick J.R.T., Martin J., Schiavo G., Fisher E.M.C., Greensmith L. A mutation in dynein rescues axonal transport defects and extends the life span of ALS mice. J. Cell Biol. 2005, 169:561-567.
204. Ilieva H.S., Yamanaka K., Malkmus S., Kakinohana O., Yaksh T., Marsala M., Cleveland D.W. Mutant dynein (Loa) triggers proprioceptive axon loss that extends survival only in the SOD1 ALS model with highest motor neuron death. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:12599-12604.
205. Sobczak K., Wheeler T.M., Wang W., Thornton C.A. RNA interference targeting CUG repeats in a mouse model of myotonic dystrophy. Mol. Ther. 2013, 21:380-387.
206. Wheeler T.M., Leger A.J., Pandey S.K., MacLeod A.R., Nakamori M., Cheng S.H., Wentworth B.M., Bennett C.F., Thornton C.A. Targeting nuclear RNA for in vivo correction of myotonic dystrophy. Nature 2012, 488:111-115.
207. Benatar M. Lost in translation: treatment trials in the SOD1 mouse and in human ALS. Neurobiol. Dis. 2007, 26:1-13.
208. Rothstein J.D. Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann. Neurol. 2009, 65(Suppl. 1):S3-S9.
209. Acevedo-Arozena A., Kalmar B., Essa S., Ricketts T., Joyce P., Kent R., Rowe C., Parker A., Gray A., Hafezparast M., Thorpe J.R., Greensmith L., Fisher E.M.C. A comprehensive assessment of the SOD1G93A low-copy transgenic mouse, which models human amyotrophic lateral sclerosis. Dis. Model Mech. 2011, 4:686-700.
210. Devoy A., Bunton-Stasyshyn R.K.A., Tybulewicz V.L.J., Smith A.J.H., Fisher E.M.C. Genomically humanized mice: technologies and promises. Nat. Rev. Genet. 2012, 13:14-20.
211. Acevedo-Arozena A., Wells S., Potter P., Kelly M., Cox R.D., Brown S.D.M. ENU mutagenesis, a way forward to understand gene function. Annu. Rev. Genomics Hum. Genet. 2008, 9:49-69.
212. Hrabé de Angelis M.H., Flaswinkel H., Fuchs H., Rathkolb B., Soewarto D., Marschall S., Heffner S., Pargent W., Wuensch K., Jung M., Reis A., Richter T., Alessandrini F., Jakob T., Fuchs E., Kolb H., Kremmer E., Schaeble K., Rollinski B., Roscher A., Peters C., Meitinger T., Strom T., Steckler T., Holsboer F., Klopstock T., Gekeler F., Shindewolf C., Jung T., Avraham K., Behrendt H., Ring J., Zimmer A., Schughart K., Pfeffer K., Wolf E., Balling R. Genome-wide, large-scale production of mutant mice by ENU mutagenesis. Nat. Genet. 2000, 25:444-447.
213. Rathkolb B., Fuchs E., Kolb H.J., Renner-Müller I., Krebs O., Balling R., Hrabé de Angelis M., Wolf E. Large-scale N-ethyl-N-nitrosourea mutagenesis of mice-from phenotypes to genes. Exp. Physiol. 2000, 85:635-644.