Skip to main content
Log in

Early Gene Expression Changes in Skeletal Muscle from SOD1G93A Amyotrophic Lateral Sclerosis Animal Model

  • Original Research
  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Amyotrophic lateral sclerosis (ALS) is a neurodegenerative disease characterized by loss of motor neurons. Familial ALS is strongly associated to dominant mutations in the gene for Cu/Zn superoxide dismutase (SOD1). Recent evidences point to skeletal muscle as a primary target in the ALS mouse model. Wnt/PI3 K signaling pathways and epithelial–mesenchymal transition (EMT) have important roles in maintenance and repair of skeletal muscle. Wnt/PI3 K pathways and EMT gene expression profile were investigated in gastrocnemius muscle from SOD1G93A mouse model and age-paired wild-type control in the presymptomatic ages of 40 and 80 days aiming the early neuromuscular abnormalities that precede motor neuron death in ALS. A customized cDNA microarray platform containing 326 genes of Wnt/PI3 K and EMT was used and results revealed eight up-regulated (Loxl2, Pik4ca, Fzd9, Cul1, Ctnnd1, Snf1lk, Prkx, Dner) and nine down-regulated (Pik3c2a, Ripk4, Id2, C1qdc1, Eif2ak2, Rac3, Cds1, Inppl1, Tbl1x) genes at 40 days, and also one up-regulated (Pik3ca) and five down-regulated (Cd44, Eef2 k, Fzd2, Crebbp, Piki3r1) genes at 80 days. Also, protein–protein interaction networks grown from the differentially expressed genes of 40 and 80 days old mice have identified Grb2 and Src genes in both presymptomatic ages, thus playing a potential central role in the disease mechanisms. mRNA and protein levels for Grb2 and Src were found to be increased in 80 days old ALS mice. Gene expression changes in the skeletal muscle of transgenic ALS mice at presymptomatic periods of disease gave further evidence of early neuromuscular abnormalities that precede motor neuron death. The results were discussed in terms of initial triggering for neuronal degeneration and muscle adaptation to keep function before the onset of symptoms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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

    CAS  PubMed  Google Scholar 

  • 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

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Cai JJ, Borenstein E, Petrov DA (2010) Broker genes in human disease. Genome Biol Evol 2:815–825. doi:10.1093/gbe/evq064

    PubMed Central  PubMed  Google Scholar 

  • 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/ars 2012.4524

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Casey LM, Lyon HD, Olmsted JB (2003) Muscle-specific microtubule-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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Claycomb WC, Lanson NA Jr (1987) Proto-oncogene expression in proliferating and differentiating cardiac and skeletal muscle. Biochem J 247(3):701–706

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Collins CA, Partridge TA (2005) Self-renewal of the adult skeletal muscle satellite cell. Cell Cycle 4(10):1338–1341. doi:2114

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Dias P, Dilling M, Houghton P (1994) The molecular basis of skeletal muscle differentiation. Semin Diagn Pathol 11(1):3–14

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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 SOD1G93A-mediated toxicity. Cell Metab 8(5):425–436. doi:10.1016/j.cmet.2008.09.002

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Gurney ME (1994) Transgenic-mouse model of amyotrophic lateral sclerosis. N Engl J Med 331(25):1721–1722. doi:10.1056/NEJM199412223312516

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Li X, Iomini C, Hyink D, Wilson PD (2011) PRKX critically regulates endothelial cell proliferation, migration, and vascular-like structure formation. Dev Biol 356(2):475–485. doi:10.1016/j.ydbio.2011.05.673

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mangan ME, Olmsted JB (1996) A muscle-specific variant of microtubule-associated protein 4 (MAP4) is required in myogenesis. Development 122(3):771–781

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mello BP, Abrantes EF, Torres CH, Machado-Lima A, Fonseca Rda S, Carraro DM, Brentani RR, Reis LF, Brentani H (2009) No-match ORESTES explored as tumor markers. Nucleic Acids Res 37(8):2607–2617. doi:10.1093/nar/gkp074

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Sanes JR, Lichtman JW (1999) Can molecules explain long-term potentiation? Nat Neurosci 2(7):597–604. doi:10.1038/10154

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Sethi JK, Vidal-Puig A (2010) Wnt signalling and the control of cellular metabolism. Biochem J 427(1):1–17. doi:10.1042/BJ20091866

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Wong M, Martin LJ (2010) Skeletal muscle-restricted expression of human SOD1 causes motor neuron degeneration in transgenic mice. Hum Mol Genet 19(11):2284–2302. doi:10.1093/hmg/ddq106

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Grant #2010/20457-7, São Paulo Research Foundation (FAPESP).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gerson Chadi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 965 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Oliveira, G.P., Maximino, J.R., Maschietto, M. et al. Early Gene Expression Changes in Skeletal Muscle from SOD1G93A Amyotrophic Lateral Sclerosis Animal Model. Cell Mol Neurobiol 34, 451–462 (2014). https://doi.org/10.1007/s10571-014-0029-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10571-014-0029-x

Keywords

Navigation