Early gene expression changes in skeletal muscle from SOD1G93A amyotrophic lateral sclerosis animal model

Cellular and Molecular Neurobiology

Volumn 34, Issue 3, 2014, Pages 451-462

  De Oliveira, Gabriela P ^a   Maximino, Jessica R ^a   Maschietto, Mariana ^b   Zanoteli, Edmar ^a   Puga, Renato D ^a   Lima, Leandro ^b   Carraro, Dirce M ^b   Chadi, Gerson ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b A C CAMARGO CANCER CENTER   (Brazil)

Author keywords

ALS; Microarray; Presymptomatic; Protein protein network; Skeletal muscle; SOD1

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; PHOSPHATIDYLINOSITOL 3 KINASE; SOD1 G93A PROTEIN; SUPEROXIDE DISMUTASE;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; MOTONEURON; MOUSE; NERVE CELL DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SKELETAL MUSCLE; WESTERN BLOTTING; WNT SIGNALING PATHWAY; ANIMAL; BIOSYNTHESIS; CELL LINE; DISEASE MODEL; ENZYMOLOGY; GENE EXPRESSION REGULATION; HUMAN; MALE; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALIA; MUS;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; MALE; MICE; MICE, TRANSGENIC; MUSCLE, SKELETAL; SUPEROXIDE DISMUTASE;

EID: 84896488834     PISSN: 02724340     EISSN: 15736830     Source Type: Journal    
DOI: 10.1007/s10571-014-0029-x     Document Type: Article

References (102)

1. Alves CJ, de Santana LP, dos Santos AJ, de Oliveira GP, Duobles T, Scorisa JM, Martins RS, Maximino JR, Chadi G (2011) Early motor and electrophysiological changes in transgenic mouse model of amyotrophic lateral sclerosis and gender differences on clinical outcome. Brain Res 1394:90-104. doi:10.1016/j.brainres.2011.02.060
2. Azzouz M, Leclerc N, Gurney M, Warter JM, Poindron P, Borg J (1997) Progressive motor neuron impairment in an animal model of familial amyotrophic lateral sclerosis. Muscle Nerve 20(1):45-51. doi:10.1002/(SICI)1097-4598(199701) 20:1\45::AID- MUS6[3.0.CO;2-H
3. Barrallo-Gimeno A, Nieto MA(2005) The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132(14):3151-3161. doi:10.1242/dev.01907 (Pubitemid 41167144)
4. Berdeaux R, Goebel N, Banaszynski L, Takemori H, Wandless T, Shelton GD, Montminy M (2007) SIK1 is a class II HDAC kinase that promotes survival of skeletal myocytes. Nat Med 13(5):597-603. doi:10.1038/nm1573 (Pubitemid 46828484)
5. Bernardini C, Censi F, Lattanzi W, Barba M, Calcagnini G, Giuliani A, Tasca G, Sabatelli M, Ricci E, Michetti F (2013) Mitochondrial network genes in the skeletal muscle of amyotrophic lateral sclerosis patients. PLoS ONE 8(2):e57739. doi:10.1371/journal.pone.0057739
6. Boillee S, Vande Velde C, Cleveland DW (2006) ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52(1):39-59. doi:10.1016/j.neuron.2006.09.018 (Pubitemid 44466358)
7. Boyan BD, Chen J, Schwartz Z (2012) Mechanism of Pdia3-dependent 1alpha,25-dihydroxy vitamin D3 signaling in musculoskeletal cells. Steroids 77(10):892-896. doi:10.1016/j.steroids.2012.04.018
8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254. doi:S0003269776699996
9. Cai JJ, Borenstein E, Petrov DA (2010) Broker genes in human disease. Genome Biol Evol 2:815-825. doi:10.1093/gbe/evq064
10. Capitanio D, Vasso M, Ratti A, Grignaschi G, Volta M, Moriggi M, Daleno C, Bendotti C, Silani V, Gelfi C (2012) Molecular signatures of amyotrophic lateral sclerosis disease progression in hind and forelimb muscles of an SOD1(G93A) mouse model. Antioxid Redox Signal 17(10):1333-1350. doi:10.1089/ars2012.4524
11. Carlson ME, Hsu M, Conboy IM (2008) Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 454(7203):528-532. doi:10.1038/nature07034
12. Casey LM, Lyon HD, Olmsted JB (2003) Muscle-specific microtu-bule- associated protein 4 is expressed early in myogenesis and is not sufficient to induce microtubule reorganization. Cell Motil Cytoskeleton 54(4):317-336. doi:10.1002/cm.10105 (Pubitemid 36373671)
13. Castellani L, Reedy MC, Gauzzi MC, Provenzano C, Alema S, Falcone G (1995) Maintenance of the differentiated state in skeletal muscle: activation of v-Src disrupts sarcomeres in quail myotubes. J Cell Biol 130(4):871-885
14. Chen CM, Kraut N, Groudine M, Weintraub H (1996) I-mf, a novel myogenic repressor, interacts with members of the MyoD family. Cell 86(5):731-741. doi:10.1016/S0092-8674(00)80148-8 (Pubitemid 26303442)
15. Chen Y, Guan Y, Liu H, Wu X, Yu L, Wang S, Zhao C, Du H, Wang X (2012a) Activation of the Wnt/beta-catenin signaling pathway is associated with glial proliferation in the adult spinal cord of ALS transgenic mice. Biochem Biophys Res Commun 420(2):397-403. doi:10.1016/j.bbrc.2012.03.006
16. Chen Y, Guan Y, Zhang Z, Liu H, Wang S, Yu L, Wu X, Wang X (2012b) Wnt signaling pathway is involved in the pathogenesis of amyotrophic lateral sclerosis in adult transgenic mice. Neurol Res 34(4):390-399. doi:10.1179/1743132812Y.0000000027
17. Claycomb WC, Lanson NA Jr (1987) Proto-oncogene expression in proliferating and differentiating cardiac and skeletal muscle. Biochem J 247(3):701-706
18. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, Christmas R, Avila-Campilo I, Creech M, Gross B, Hanspers K, Isserlin R, Kelley R, Killcoyne S, Lotia S, Maere S, Morris J, Ono K, Pavlovic V, Pico AR, Vailaya A, Wang PL, Adler A, Conklin BR, Hood L, Kuiper M, Sander C, Schmulevich I, Schwikowski B, Warner GJ, Ideker T, Bader GD (2007) Integration of biological networks and gene expression data using Cytoscape. Nat Protoc 2(10):2366-2382. doi:10.1038/nprot.2007.324
19. Collins CA, Partridge TA (2005) Self-renewal of the adult skeletal muscle satellite cell. Cell Cycle 4(10):1338-1341. doi:2114
20. Conboy IM, Rando TA (2002) The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 3(3):397-409. doi:S153458070200254X
21. Conboy IM, Conboy MJ, Smythe GM, Rando TA (2003) Notch-mediated restoration of regenerative potential to aged muscle. Science 302(5650):1575-1577. doi:10.1126/science.1087573 (Pubitemid 37475703)
22. Dadon-Nachum M, Melamed E, Offen D (2011) The "dying-back" phenomenon of motor neurons in ALS. J Mol Neurosci 43(3):470-477. doi:10.1007/s12031-010-9467-1
23. Danisovic L, Varga I, Polak S, Ulicna M, Bohmer D, Vojtassak J (2008) Morphology of in vitro expanded human muscle-derived stem cells. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 152(2):235-238
24. De Craene B, van Roy F, Berx G (2005) Unraveling signalling cascades for the Snail family of transcription factors. Cell Signal 17(5):535-547. doi:10.1016/j.cellsig.2004.10.011 (Pubitemid 40430957)
25. Gonzalez de Aguilar JL, Niederhauser-Wiederkehr C, Halter B, De Tapia M, Di Scala F, Demougin P, Dupuis L, Primig M, Meininger V, Loeffler JP (2008) Gene profiling of skeletal muscle in an amyotrophic lateral sclerosis mouse model. Physiol Genomics 32(2):207-218. doi:10.1152/physiolgenomics.00017.2007 (Pubitemid 351186328)
26. de Oliveira GP, Alves CJ, Chadi G (2013) Early gene expression changes in spinal cord from SOD1 Amyotrophic Lateral Sclerosis animal model. Front Cell Neurosci 7:216. doi:10.3389/fncel.2013.00216
27. Delfini MC, De La Celle M, Gros J, Serralbo O, Marics I, Seux M, Scaal M, Marcelle C (2009) The timing of emergence of muscle progenitors is controlled by an FGF/ERK/SNAIL1 pathway. Dev Biol 333(2):229-237. doi:10.1016/j.ydbio.2009. 05.544
28. Dias P, Dilling M, Houghton P (1994) The molecular basis of skeletal muscle differentiation. Semin Diagn Pathol 11(1):3-14 (Pubitemid 24092131)
29. Dobrowolny G, Giacinti C, Pelosi L, Nicoletti C, Winn N, Barberi L, Molinaro M, Rosenthal N, Musaro A (2005) Muscle expression of a local Igf-1 isoform protects motor neurons in an ALS mouse model. J Cell Biol 168(2):193-199. doi:10.1083/jcb.200407021 (Pubitemid 40248217)
30. Dobrowolny G, Aucello M, Rizzuto E, Beccafico S, Mammucari C, Boncompagni S, Belia S, Wannenes F, Nicoletti C, Del Prete Z, Rosenthal N, Molinaro M, Protasi F, Fano G, Sandri M, Musaro A (2008) Skeletal muscle is a primary target of SOD1G93Amediated toxicity. Cell Metab 8(5):425-436. doi:10.1016/j.cmet. 2008.09.002
31. Drost J, Nonis D, Eich F, Leske O, Damrath E, Brunt ER, Lastres-Becker I, Heumann R, Nowock J, Auburger G (2013) Ataxin-2 modulates the levels of Grb2 and SRC but not ras signaling. J Mol Neurosci 51(1):68-81. doi:10.1007/s12031- 012-9949-4
32. Dupuis L, Oudart H, Rene F, Gonzalez de Aguilar JL, Loeffler JP (2004) Evidence for defective energy homeostasis in amyotrophic lateral sclerosis: benefit of a high-energy diet in a transgenic mouse model. Proc Natl Acad Sci USA 101(30):11159-11164. doi:10.1073/pnas.0402026101 (Pubitemid 38989600)
33. Eiraku M, Hirata Y, Takeshima H, Hirano T, Kengaku M (2002) Delta/notch-like epidermal growth factor (EGF)-related receptor, a novel EGF-like repeat-containing protein targeted to dendrites of developing and adult central nervous system neurons. J Biol Chem 277(28):25400-25407. doi:10.1074/jbc.M110793200 (Pubitemid 34951852)
34. Elden AC, Kim HJ, Hart MP, Chen-Plotkin AS, Johnson BS, Fang X, Armakola M, Geser F, Greene R, Lu MM, Padmanabhan A, Clay-Falcone D, McCluskey L, Elman L, Juhr D, Gruber PJ, Rub U, Auburger G, Trojanowski JQ, Lee VM, Van Deerlin VM, Bonini NM, Gitler AD (2010) Ataxin-2 intermediate-length polyglutamine expansions are associated with increased risk for ALS. Nature 466(7310):1069-1075. doi:10.1038/nature09320
35. Feldman I, Rzhetsky A, Vitkup D (2008) Network properties of genes harboring inherited disease mutations. Proc Natl Acad Sci USA 105(11):4323-4328. doi:10.1073/pnas.0701722105 (Pubitemid 351754379)
36. Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, Castellano-Sanchez A, Khan J, Polak MA, Glass JD (2004) Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 185(2):232-240. doi:S0014488603004795
37. Frey D, Schneider C, Xu L, Borg J, Spooren W, Caroni P (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J Neurosci 20(7):2534-2542 (Pubitemid 30220340)
38. Glass DJ (2010) PI3 kinase regulation of skeletal muscle hypertrophy and atrophy. Curr Top Microbiol Immunol 346:267-278. doi:10.1007/82-2010-78
39. Goh KI, Cusick ME, Valle D, Childs B, Vidal M, Barabasi AL (2007) The human disease network. Proc Natl Acad Sci USA 104(21):8685-8690. doi:10.1073/pnas.0701361104 (Pubitemid 47175372)
40. Goodman CA, Miu MH, Frey JW, Mabrey DM, Lincoln HC, Ge Y, Chen J, Hornberger TA (2010) A phosphatidylinositol 3-kinase/ protein kinase B-independent activation of mammalian target of rapamycin signaling is sufficient to induce skeletal muscle hypertrophy. Mol Biol Cell 21(18):3258-3268. doi:10.1091/mbc.E10-05-0454
41. Gordon MD, Nusse R (2006) Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem 281(32):22429-22433. doi:10.1074/jbc.R600015200
42. Gros J, Manceau M, Thome V, Marcelle C (2005) A common somitic origin for embryonic muscle progenitors and satellite cells. Nature 435(7044):954-958. doi:10.1038/nature03572 (Pubitemid 40896321)
43. Gurney ME (1994) Transgenic-mouse model of amyotrophic lateral sclerosis. N Engl J Med 331(25):1721-1722. doi:10.1056/NEJM199412223312516
44. Hagiwara H, Saito F, Masaki T, Ikeda M, Nakamura-Ohkuma A, Shimizu T, Matsumura K (2011) Histone deacetylase inhibitor trichostatin a enhances myogenesis by coordinating muscle regulatory factors and myogenic repressors. Biochem Biophys Res Commun 414(4):826-831. doi:10.1016/j.bbrc.2011.10.036
45. Harms MB, Sommerville RB, Allred P, Bell S, Ma D, Cooper P, Lopate G, Pestronk A, Weihl CC, Baloh RH (2012) Exome sequencing reveals DNAJB6 mutations in dominantly-inherited myopathy. Ann Neurol 71(3):407-416. doi:10.1002/ana. 22683
46. Hirayama E, Isobe A, Okamoto H, Nishioka M, Kim J (1997) Myogenin expression is necessary for commitment to differentiation and is closely related to src tyrosine kinase activity in quail myoblasts transformed with Rous sarcoma virus. Eur J Cell Biol 72(2):133-141 (Pubitemid 27095996)
47. Howland DS, Liu J, She Y, Goad B, Maragakis NJ, Kim B, Erickson J, Kulik J, DeVito L, Psaltis G, DeGennaro LJ, Cleveland DW, Rothstein JD (2002) Focal loss of the glutamate transporter EAAT2 in a transgenic rat model of SOD1 mutant-mediated amyotrophic lateral sclerosis (ALS). Proc Natl Acad Sci USA 99(3):1604-1609. doi:10.1073/pnas.032539299 (Pubitemid 34136539)
48. Hwang W, Cho YR, Zhang A, Ramanathan M (2006) A novel functional module detection algorithm for protein-protein interaction networks. Algorithms Mol Biol 1:24. doi:10.1186/1748- 7188-1-24
49. Jokic N, Gonzalez de Aguilar JL, Pradat PF, Dupuis L, Echaniz-Laguna A, Muller A, Dubourg O, Seilhean D, Hauw JJ, Loeffler JP, Meininger V (2005) Nogo expression in muscle correlates with amyotrophic lateral sclerosis severity. Ann Neurol 57(4):553-556. doi:10.1002/ana.20420 (Pubitemid 40471166)
50. Jonsson PA, Ernhill K, Andersen PM, Bergemalm D, Brannstrom T, Gredal O, Nilsson P, Marklund SL (2004) Minute quantities of misfolded mutant superoxide dismutase-1 cause amyotrophic lateral sclerosis. Brain 127(Pt 1):73-88. doi:10.1093/brain/awh005 (Pubitemid 38055347)
51. Knebel A, Morrice N, Cohen P (2001) A novel method to identify protein kinase substrates: eEF2 kinase is phosphorylated and inhibited by SAPK4/p38delta. EMBO J 20(16):4360-4369. doi:10.1093/emboj/20.16.4360 (Pubitemid 32772030)
52. Krauss RS (2010) Regulation of promyogenic signal transduction by cell-cell contact and adhesion. Exp Cell Res 316(18):3042-3049. doi:10.1016/j.yexcr.2010.05.008
53. Laeremans H, Rensen SS, Ottenheijm HC, Smits JF, Blankesteijn WM (2010) Wnt/frizzled signalling modulates the migration and differentiation of immortalized cardiac fibroblasts. Cardiovasc Res 87(3):514-523. doi:10.1093/cvr/cvq067
54. Leshem Y, Gitelman I, Ponzetto C, Halevy O (2002) Preferential binding of Grb2 or phosphatidylinositol 3-kinase to the met receptor has opposite effects on HGF-induced myoblast proliferation. Exp Cell Res 274(2):288-298. doi:10.1006/excr 2002.5473
55. Li Q, Ching AK, Chan BC, Chow SK, Lim PL, Ho TC, Ip WK, Wong CK, Lam CW, Lee KK, Chan JY, Chui YL (2004) A death receptor-associated anti-apoptotic protein, BRE, inhibits mitochondrial apoptotic pathway. J Biol Chem 279(50):52106-52116. doi:10.1074/jbc.M408678200 (Pubitemid 39656583)
56. Li X, Iomini C, Hyink D, Wilson PD (2011) PRKX critically regulates endothelial cell proliferation, migration, and vascularlike structure formation. Dev Biol 356(2):475-485. doi:10.1016/ j.ydbio.2011.05.673
57. Li X, Guan Y, Chen Y, Zhang C, Shi C, Zhou F, Yu L, Juan J, Wang X (2013) Expression of Wnt5a and its receptor Fzd2 is changed in the spinal cord of adult amyotrophic lateral sclerosis transgenic mice. Int J Clin Exp Pathol 6(7):1245-1260
58. Lim E, Lee S, Li E, Kim Y, Park S (2011) Ghrelin protects spinal cord motoneurons against chronic glutamate-induced excitotoxicity via ERK1/2 and phosphatidylinositol-3-kinase/Akt/glycogen synthase kinase-3beta pathways. Exp Neurol 230(1):114-122. doi:10.1016/j.expneurol.2011.04.003
59. Liu YF, Deth RC, Devys D (1997) SH3 domain-dependent association of huntingtin with epidermal growth factor receptor signaling complexes. J Biol Chem 272(13):8121-8124 (Pubitemid 27147757)
60. Liu X, Liu M, Zhang J, Bai X, Ramos F, Van Remmen H, Richardson A, Liu FY, Dong LQ, Liu F (2009) Downregulation of Grb2 contributes to the insulin-sensitizing effect of calorie restriction. Am J Physiol Endocrinol Metab 296(5):E1067-E1075. doi:10.1152/ajpendo.9 0714.2008
61. Mangan ME, Olmsted JB (1996) A muscle-specific variant of microtubule-associated protein 4 (MAP4) is required in myogenesis. Development 122(3):771-781 (Pubitemid 26095983)
62. Manzano R, Toivonen JM, Olivan S, Calvo AC, Moreno-Igoa M, Munoz MJ, Zaragoza P, Garcia-Redondo A, Osta R (2011) Altered expression of myogenic regulatory factors in the mouse model of amyotrophic lateral sclerosis. Neurodegener Dis 8(5):386-396. doi:10.1159/000324159
63. Manzano R, Toivonen JM, Calvo AC, Olivan S, Zaragoza P, Rodellar C, Montarras D, Osta R (2013) Altered in vitro proliferation of mouse SOD1-G93A skeletal muscle satellite cells. Neurodegener Dis 11(3):153-164. doi:10.1159/000338061
64. Marcuzzo S, Zucca I, Mastropietro A, de Rosbo NK, Cavalcante P, Tartari S, Bonanno S, Preite L, Mantegazza R, Bernasconi P (2011) Hind limb muscle atrophy precedes cerebral neuronal degeneration in G93A-SOD1 mouse model of amyotrophic lateral sclerosis: a longitudinal MRI study. Exp Neurol 231(1):30-37. doi:10.1016/j.expneurol.2011.05.007
65. Maschietto M, de Camargo B, Brentani H, Grundy P, Sredni ST, Torres C, Mota LD, Cunha IW, Patrao DF, Costa CM, Soares FA, Brentani RR, Carraro DM (2008) Molecular profiling of isolated histological components of Wilms tumor implicates a common role for the Wnt signaling pathway in kidney and tumor development. Oncology 75(1-2):81-91. doi:10.1159/000155210
66. Maschietto M, Trape AP, Piccoli FS, Ricca TI, Dias AA, Coudry RA, Galante PA, Torres C, Fahhan L, Lourenco S, Grundy PE, de Camargo B, de Souza S, Neves EJ, Soares FA, Brentani H, Carraro DM (2011) Temporal blastemal cell gene expression analysis in the kidney reveals new Wnt and related signaling pathway genes to be essential for Wilms' tumor onset. Cell Death Dis 2:e224. doi:10.1038/cddis.2011.105
67. Mello BP, Abrantes EF, Torres CH, Machado-Lima A, Fonseca Rda S, Carraro DM, Brentani RR, Reis LF, Brentani H (2009) Nomatch ORESTES explored as tumor markers. Nucleic Acids Res 37(8):2607-2617. doi:10.1093/nar/gkp074
68. Montarras D, L'Honore A, Buckingham M (2013) Lying low but ready for action: the quiescent muscle satellite cell. FEBS J 280(17):4036-4050. doi:10.1111/febs.12372
69. Mounier R, Chretien F, Chazaud B (2011) Blood vessels and the satellite cell niche. Curr Top Dev Biol 96:121-138. doi:10.1016/B978-0-12-385940-2.00005-X
70. Mylona E, Jones KA, Mills ST, Pavlath GK (2006) CD44 regulates myoblast migration and differentiation. J Cell Physiol 209(2):314-321. doi:10.1002/jcp.20724 (Pubitemid 44484621)
71. Nagata Y, Honda Y, Matsuda R (2010) FGF2 induces ERK phosphorylation through Grb2 and PKC during quiescent myogenic cell activation. Cell Struct Funct 35(1):63-71. doi:10.1247/csf.09024
72. Nizzari M, Venezia V, Repetto E, Caorsi V, Magrassi R, Gagliani MC, Carlo P, Florio T, Schettini G, Tacchetti C, Russo T, Diaspro A, Russo C (2007) Amyloid precursor protein and Presenilin1 interact with the adaptor GRB2 and modulate ERK 1,2 signaling. J Biol Chem 282(18):13833-13844. doi:10.1074/jbc.M610146200 (Pubitemid 47100564)
73. Pasterkamp RJ, Giger RJ (2009) Semaphorin function in neural plasticity and disease. Curr Opin Neurobiol 19(3):263-274. doi:10.1016/j.conb.2009.06.001
74. Peviani M, Tortarolo M, Battaglia E, Piva R, Bendotti C (2013) Specific induction of Akt3 in spinal cord motor neurons is neuroprotective in a mouse model of familial amyotrophic lateral sclerosis. Mol Neurobiol. doi:10.1007/s12035-013-8507-6
75. Puklowski A, Homsi Y, Keller D, May M, Chauhan S, Kossatz U, Grunwald V, Kubicka S, Pich A, Manns MP, Hoffmann I, Gonczy P, Malek NP (2011) The SCF-FBXW5 E3-ubiquitin ligase is regulated by PLK4 and targets HsSAS-6 to control centrosome duplication. Nat Cell Biol 13(8):1004-1009. doi:10.1038/ncb2282
76. Rocha MC, Pousinha PA, Correia AM, Sebastiao AM, Ribeiro JA (2013) Early changes of neuromuscular transmission in the SOD1(G93A) mice model of ALS start long before motor symptoms onset. PLoS ONE 8(9):e73846. doi:10.1371/journal. pone.0073846
77. Rose AJ, Alsted TJ, Jensen TE, Kobbero JB, Maarbjerg SJ, Jensen J, Richter EA (2009) A Ca(2+)-calmodulin-eEF2K-eEF2 signalling cascade, but not AMPK, contributes to the suppression of skeletal muscle protein synthesis during contractions. J Physiol 587(Pt 7):1547-1563. doi:10.1113/jphysiol.2008.167528
78. Sadasivam G, Willmann R, Lin S, Erb-Vogtli S, Kong XC, Ruegg MA, Fuhrer C (2005) Src-family kinases stabilize the neuromuscular synapse in vivo via protein interactions, phosphorylation, and cytoskeletal linkage of acetylcholine receptors. J Neurosci 25(45):10479-10493. doi:10.1523/JNEUROSCI.2103-05.2005 (Pubitemid 41628450)
79. Sadkowski T, Jank M, Zwierzchowski L, Siadkowska E, Oprzadek J, Motyl T (2008) Gene expression profiling in skeletal muscle of Holstein-Friesian bulls with single-nucleotide polymorphism in the myostatin gene 5′-flanking region. J Appl Genet 49(3):237-250. doi:10.1007/BF03195620
80. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34(2):374-378 (Pubitemid 36184095)
81. Sakowski SA, Lunn JS, Busta AS, Oh SS, Zamora-Berridi G, Palmer M, Rosenberg AA, Philip SG, Dowling JJ, Feldman EL (2012) Neuromuscular effects of G93A-SOD1 expression in zebrafish. Mol Neurodegener 7:44. doi:10.1186/1750-1326- 7-44
82. Salinas PC (2007) Modulation of the microtubule cytoskeleton: a role for a divergent canonical Wnt pathway. Trends Cell Biol 17(7):333-342. doi:10.1016/j.tcb.2007.07.003
83. Sanes JR, Lichtman JW (1999) Can molecules explain long-term potentiation? Nat Neurosci 2(7):597-604. doi:10.1038/10154 (Pubitemid 30491209)
84. Saris CG, Groen EJ, van Vught PW, van Es MA, Blauw HM, Veldink JH, van den Berg LH (2013) Gene expression profile of SOD1-G93A mouse spinal cord, blood and muscle. Amyotroph Lateral Scler Frontotemporal Degener 14(3):190-198. doi:10.3109/21678421.2012.749914
85. Scime A, Desrosiers J, Trensz F, Palidwor GA, Caron AZ, Andrade-Navarro MA, Grenier G (2010) Transcriptional profiling of skeletal muscle reveals factors that are necessary to maintain satellite cell integrity during ageing. Mech Ageing Dev 131(1):9-20. doi:10.1016/j.mad.2009.11.001
86. Scorisa JM, Duobles T, Oliveira GP, Maximino JR, Chadi G (2010) The review of the methods to obtain non-neuronal cells to study glial influence on amyotrophic lateral sclerosis pathophysiology at molecular level in vitro. Acta Cir Bras 25(3):281-289. doi:10.1590/S0102-86502010000300011
87. Sethi JK, Vidal-Puig A (2010) Wnt signalling and the control of cellular metabolism. Biochem J 427(1):1-17. doi:10.1042/BJ20091866
88. Shi L, Zhao G, Qiu D, Godfrey WR, Vogel H, Rando TA, Hu H, Kao PN (2005) NF90 regulates cell cycle exit and terminal myogenic differentiation by direct binding to the 3′-untranslated region of MyoD and p21WAF1/CIP1 mRNAs. J Biol Chem 280(19):18981-18989. doi:10.1074/jbc.M411034200 (Pubitemid 41379602)
89. Soos MA, Jensen J, Brown RA, O'Rahilly S, Shepherd PR, Whitehead JP (2001) Class II phosphoinositide 3-kinase is activated by insulin but not by contraction in skeletal muscle. Arch Biochem Biophys 396(2):244-248. doi:10.1006/abbi 2001.2587
90. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ (2004) The IGF-1/PI3 K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14(3):395-403. doi:10.1016/S1097276504002114 (Pubitemid 38591410)
91. Tang MK, Wang CM, Shan SW, Chui YL, Ching AK, Chow PH, Grotewold L, Chan JY, Lee KK (2006) Comparative proteomic analysis reveals a function of the novel death receptor-associated protein BRE in the regulation of prohibitin and p53 expression and proliferation. Proteomics 6(8):2376-2385. doi:10.1002/pmic. 200500603
92. Tatematsu K, Tokunaga C, Nakagawa N, Tanizawa K, Kuroda S, Kikkawa U (1998) Transcriptional activity of RBCK1 protein (RBCC protein interacting with PKC 1): requirement of RING-finger and B-Box motifs and regulation by protein kinases. Biochem Biophys Res Commun 247(2):392-396. doi:10.1006/bbrc 1998.8795
93. Tian Y, Zhang Y, Zhong B, Wang YY, Diao FC, Wang RP, Zhang M, Chen DY, Zhai ZH, Shu HB (2007) RBCK1 negatively regulates tumor necrosis factor- and interleukin-1-triggered NF-kappaB activation by targeting TAB 2/3 for degradation. J Biol Chem 282(23):16776-16782. doi:10.1074/jbc.M701913200 (Pubitemid 47093242)
94. Troyanskaya OG, Garber ME, Brown PO, Botstein D, Altman RB (2002) Nonparametric methods for identifying differentially expressed genes in microarray data. Bioinformatics 18(11):1454-1461 (Pubitemid 35414536)
95. Turner BJ, Lopes EC, Cheema SS (2003) Neuromuscular accumulation of mutant superoxide dismutase 1 aggregates in a transgenic mouse model of familial amyotrophic lateral sclerosis. Neurosci Lett 350(2):132-136. doi:10.1016/S0304-3940(03)00893-0 (Pubitemid 37101429)
96. Tury A, Tolentino K, Zou Y (2013) Altered expression of atypical PKC and Ryk in the spinal cord of a mouse model of amyotrophic lateral sclerosis. Dev Neurobiol. doi:10.1002/dneu.22137
97. Wang S, Guan Y, Chen Y, Li X, Zhang C, Yu L, Zhou F, Wang X (2013) Role of Wnt1 and Fzd1 in the spinal cord pathogenesis of amyotrophic lateral sclerosis-transgenic mice. Biotechnol Lett 35(8):1199-1207. doi:10.1007/s10529- 013-1199-1
98. Wong M, Martin LJ (2010) Skeletal muscle-restricted expression of human SOD1 causesmotor neuron degeneration in transgenic mice. Hum Mol Genet 19(11):2284-2302. doi:10.1093/hmg/ddq106
99. Wu X, Kihara T, Akaike A, Niidome T, Sugimoto H (2010) PI3 K/Akt/mTOR signaling regulates glutamate transporter 1 in astrocytes. Biochem Biophys Res Commun 393(3):514-518. doi:10.1016/j.bbrc.2010.02.038
100. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP (2002) Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res 30(4):e15
101. Yu L, Guan Y, Wu X, Chen Y, Liu Z, Du H, Wang X (2013) Wnt Signaling is altered by spinal cord neuronal dysfunction in amyotrophic lateral sclerosis transgenic mice. Neurochem Res 38(9):1904-1913. doi:10.1007/s11064-013-1096-y
102. Zhao T, Qi Y, Li Y, Xu K (2012) PI3 Kinase regulation of neural regeneration and muscle hypertrophy after spinal cord injury. Mol Biol Rep 39(4):3541-3547. doi:10.1007/s11033-011-1127-1