Community effect triggers terminal differentiation of myogenic cells derived from muscle satellite cells by quenching Smad signaling

Experimental Cell Research

Volumn 317, Issue 2, 2011, Pages 221-233

  Yanagisawa, Michiko ^a,b   Mukai, Atsushi ^a   Shiomi, Kosuke ^a   Song, Si Yong ^c   Hashimoto, Naohiro ^a  

^a NATIONAL CENTER FOR GERIATRICS AND GERONTOLOGY   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c TOKUSHIMA BUNRI UNIVERSITY   (Japan)

Author keywords

ALK; BMP; Community effect; Myogenesis; Osteogenesis; Smad

Indexed keywords

BONE MORPHOGENETIC PROTEIN; MYOGENIN; NOGGIN; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL DENSITY; CELL DIFFERENTIATION; COMPETITIVE INHIBITION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CULTURE MEDIUM; FEMALE; GASTROCNEMIUS MUSCLE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MUSCLE CELL; MUSCLE DEVELOPMENT; MUSCLE REGENERATION; MYOGENIC CELL; NONHUMAN; NONPHOTOCHEMICAL QUENCHING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SKELETAL MUSCLE SATELLITE CELL; STEM CELL;

RATTUS;

EID: 78649482410     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2010.10.011     Document Type: Article

References (57)

1. Cossu G., Borello U. Wnt signaling and the activation of myogenesis in mammals. EMBO J. 1999, 18:6867-6872.
2. Cossu G., Molinaro M. Cell heterogeneity in the myogenic lineage. Curr. Top. Dev. Biol. 1987, 23:185-208.
3. Elia D., Madhala D., Ardon E., Reshef R., Halevy O. Sonic hedgehog promotes proliferation and differentiation of adult muscle cells: involvement of MAPK/ERK and PI3K/Akt pathways. Biochim. Biophys. Acta 2007, 1773:1438-1446.
4. Koleva M., Kappler R., Vogler M., Herwig A., Fulda S., Hahn H. Pleiotropic effects of sonic hedgehog on muscle satellite cells. Cell. Mol. Life Sci. 2005, 62:1863-1870.
5. Straface G., Aprahamian T., Flex A., Gaetani E., Biscetti F., Smith R.C., Pecorini G., Pola E., Angelini F., Stigliano E., Castellot J.J., Losordo D.W., Pola R. Sonic hedgehog regulates angiogenesis and myogenesis during post-natal skeletal muscle regeneration. J. Cell Mol. Med. 2009, 13:2424-2435.
6. Otto A., Schmidt C., Luke G., Allen S., Valasek P., Muntoni F., Lawrence-Watt D., Patel K. Canonical Wnt signalling induces satellite-cell proliferation during adult skeletal muscle regeneration. J. Cell Sci. 2008, 121:2939-2950.
7. Asakura A., Komaki M., Rudnicki M. Muscle satellite cells are multipotential stem cells that exhibit myogenic, osteogenic, and adipogenic differentiation. Differentiation 2001, 68:245-253.
8. Katagiri T., Yamaguchi A., Komaki M., Abe E., Takahashi N., Ikeda T., Rosen V., Wozney J.M., Fujisawa-Sehara A., Suda T. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J. Cell Biol. 1994, 127:1755-1766.
9. Wada M.R., Inagawa-Ogashiwa M., Shimizu S., Yasumoto S., Hashimoto N. Generation of different fates from multipotent muscle stem cells. Development 2002, 129:2987-2995.
10. Yamamoto N., Akiyama S., Katagiri T., Namiki M., Kurokawa T., Suda T. Smad1 and smad5 act downstream of intracellular signalings of BMP-2 that inhibits myogenic differentiation and induces osteoblast differentiation in C2C12 myoblasts. Biochem. Biophys. Res. Commun. 1997, 238:574-580.
11. Nishimura R., Kato Y., Chen D., Harris S.E., Mundy G.R., Yoneda T. Smad5 and DPC4 are key molecules in mediating BMP-2-induced osteoblastic differentiation of the pluripotent mesenchymal precursor cell line C2C12. J. Biol. Chem. 1998, 273:1872-1879.
12. Fujii M., Takeda K., Imamura T., Aoki H., Sampath T.K., Enomoto S., Kawabata M., Kato M., Ichijo H., Miyazono K. Roles of bone morphogenetic protein type I receptors and Smad proteins in osteoblast and chondroblast differentiation. Mol. Biol. Cell 1999, 10:3801-3813.
13. Aoki H., Fujii M., Imamura T., Yagi K., Takehara K., Kato M., Miyazono K. Synergistic effects of different bone morphogenetic protein type I receptors on alkaline phosphatase induction. J. Cell Sci. 2001, 114:1483-1489.
14. Hashimoto N., Murase T., Kondo S., Okuda A., Inagawa-Ogashiwa M. Muscle reconstitution by muscle satellite cell descendants with stem cell-like properties. Development 2004, 131:5481-5490.
15. Nojima J., Kanomata K., Takada Y., Fukuda T., Kokabu S., Ohte S., Takada T., Tsukui T., Yamamoto T.S., Sasanuma H., Yoneyama K., Ueno N., Okazaki Y., Kamijo R., Yoda T., Katagiri T. Dual roles of smad proteins in the conversion from myoblasts to osteoblastic cells by bone morphogenetic proteins. J. Biol. Chem. 2010, 285:15577-15586.
16. Frank N.Y., Kho A.T., Schatton T., Murphy G.F., Molloy M.J., Zhan Q., Ramoni M.F., Frank M.H., Kohane I.S., Gussoni E. Regulation of myogenic progenitor proliferation in human fetal skeletal muscle by BMP4 and its antagonist Gremlin. J. Cell Biol. 2006, 175:99-110.
17. Blau H.M., Pavlath G.K., Hardeman E.C., Chiu C.P., Silberstein L., Webster S.G., Miller S.C., Webster C. Plasticity of the differentiated state. Science 1985, 230:758-766.
18. Mukai A., Hashimoto N. Localized cyclic AMP-dependent protein kinase activity is required for myogenic cell fusion. Exp. Cell Res. 2008, 314:387-397.
19. Yaffe D., Saxel O. A myogenic cell line with altered serum requirements for differentiation. Differentiation 1977, 7:159-166.
20. Mukai A., Kurisaki T., Sato S.B., Kobayashi T., Kondoh G., Hashimoto N. Dynamic clustering and dispersion of lipid rafts contribute to fusion competence of myogenic cells. Exp. Cell Res. 2009, 315:3052-3063.
21. Hashimoto N., Kiyono T., Wada M.R., Umeda R., Goto Y., Nonaka I., Shimizu S., Yasumoto S., Inagawa-Ogashiwa M. Osteogenic properties of human myogenic progenitor cells. Mech. Dev. 2008, 125:257-269.
22. Hashimoto N., Kiyono T., Wada M.R., Shimizu S., Yasumoto S., Inagawa M. Immortalization of human myogenic progenitor cell clone retaining multipotentiality. Biochem. Biophys. Res. Commun. 2006, 348:1383-1388.
23. Hashimoto N., Ogashiwa M. Isolation of a differentiation-defective myoblastic cell line, INC-2, expressing muscle LIM protein under differentiation-inducing conditions. Dev. Growth Differ. 1997, 39:363-372.
24. Hashimoto N., Ogashiwa M., Iwashita S. Role of tyrosine kinase in the regulation of myogenin expression. Eur. J. Biochem. 1995, 227:379-387.
25. Hashimoto N., Ogashiwa M., Okumura E., Endo T., Iwashita S., Kishimoto T. Phosphorylation of a proline-directed kinase motif is responsible for structural changes in myogenin. FEBS Lett. 1994, 352:236-242.
26. Fujisawa-Sehara A., Hanaoka K., Hayasaka M., Hiromasa-Yagami T., Nabeshima Y. Upstream region of the myogenin gene confers transcriptional activation in muscle cell lineages during mouse embryogenesis. Biochem. Biophys. Res. Commun. 1993, 191:351-356.
27. Korchynskyi O., ten Dijke P. Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J. Biol. Chem. 2002, 277:4883-4891.
28. Saito Y., Nonaka I., Qu Z., Balkir L., van Deutekom J.C., Robbins P.D., Pruchnic R., Huard J. Initiation of satellite cell replication in bupivacaine-induced myonecrosis. Acta Neuropathol. (Berl) 1994, 88:252-257.
29. Furukawa Y., Hashimoto N., Yamakuni T., Ishida Y., Kato C., Ogashiwa M., Kobayashi M., Kobayashi T., Nonaka I., Mizusawa H., Song S.Y. Down-regulation of an ankyrin repeat-containing protein, V-1, during skeletal muscle differentiation and its re-expression in the regenerative process of muscular dystrophy. Neuromuscul. Disord. 2003, 13:32-41.
30. Bader D., Masaki T., Fischman D.A. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J. Cell Biol. 1982, 95:763-770.
31. Wright W.E., Sassoon D.A., Lin V.K. Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 1989, 56:607-617.
32. Hirano H., Watanabe T. Microsequencing of proteins electrotransferred onto immobilizing matrices from polyacrylamide gel electrophoresis: application to an insoluble protein. Electrophoresis 1990, 11:573-580.
33. Miyazawa K., Shinozaki M., Hara T., Furuya T., Miyazono K. Two major Smad pathways in TGF-beta superfamily signalling. Genes Cells 2002, 7:1191-1204.
34. Yu P.B., Deng D.Y., Lai C.S., Hong C.C., Cuny G.D., Bouxsein M.L., Hong D.W., McManus P.M., Katagiri T., Sachidanandan C., Kamiya N., Fukuda T., Mishina Y., Peterson R.T., Bloch K.D. BMP type I receptor inhibition reduces heterotopic [corrected] ossification. Nat. Med. 2008, 14:1363-1369.
35. Derynck R., Zhang Y.E. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 2003, 425:577-584.
36. Goto K., Kamiya Y., Imamura T., Miyazono K., Miyazawa K. Selective inhibitory effects of Smad6 on bone morphogenetic protein type I receptors. J. Biol. Chem. 2007, 282:20603-20611.
37. Benezra R., Davis R.L., Lockshon D., Turner D.L., Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 1990, 61:49-59.
38. Jin Y., Murakami N., Saito Y., Goto Y., Koishi K., Nonaka I. Expression of MyoD and myogenin in dystrophic mice, mdx and dy, during regeneration. Acta Neuropathol. 2000, 99:619-627.
39. Kim H.K., Lee Y.S., Sivaprasad U., Malhotra A., Dutta A. Muscle-specific microRNA miR-206 promotes muscle differentiation. J. Cell Biol. 2006, 174:677-687.
40. Liu C.J., Ding B., Wang H., Lengyel P. The MyoD-inducible p204 protein overcomes the inhibition of myoblast differentiation by Id proteins. Mol. Cell. Biol. 2002, 22:2893-2905.
41. Buckingham M. How the community effect orchestrates muscle differentiation. Bioessays 2003, 25:13-16.
42. Gurdon J.B., Lemaire P., Kato K. Community effects and related phenomena in development. Cell 1993, 75:831-834.
43. Gurdon J.B., Tiller E., Roberts J., Kato K. A community effect in muscle development. Curr. Biol. 1993, 3:1-11.
44. Cossu G., Kelly R., Di Donna S., Vivarelli E., Buckingham M. Myoblast differentiation during mammalian somitogenesis is dependent upon a community effect. Proc. Natl Acad. Sci. USA 1995, 92:2254-2258.
45. Cossu G., Tajbakhsh S., Buckingham M. How is myogenesis initiated in the embryo?. Trends Genet. 1996, 12:218-223.
46. Charge S.B.P., Rudnicki M.A. Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 2004, 84:209-238.
47. Sterrenburg E., van der Wees C.G., White S.J., Turk R., de Menezes R.X., van Ommen G.J., den Dunnen J.T., t Hoen P.A. Gene expression profiling highlights defective myogenesis in DMD patients and a possible role for bone morphogenetic protein 4. Neurobiol. Dis. 2006, 23:228-236.
48. Florini J.R., Ewton D.Z., Magri K.A. Hormones, growth factors, and myogenic differentiation. Annu. Rev. Physiol. 1991, 53:201-216.
49. Sun L., Ma K., Wang H., Xiao F., Gao Y., Zhang W., Wang K., Gao X., Ip N., Wu Z. JAK1-STAT1-STAT3, a key pathway promoting proliferation and preventing premature differentiation of myoblasts. J. Cell Biol. 2007, 179:129-138.
50. Moore J.W., Dionne C., Jaye M., Swain J.L. The mRNAs encoding acidic FGF, basic FGF and FGF receptor are coordinately downregulated during myogenic differentiation. Development 1991, 111:741-748.
51. Baron P., Galimberti D., Meda L., Scarpini E., Conti G., Cogiamanian F., Scarlato G. Production of IL-6 by human myoblasts stimulated with Abeta: relevance in the pathogenesis of IBM. Neurology 2001, 57:1561-1565.
52. Thomas M., Langley B., Berry C., Sharma M., Kirk S., Bass J., Kambadur R. Myostatin, a negative regulator of muscle growth, functions by inhibiting myoblast proliferation. J. Biol. Chem. 2000, 275:40235-40243.
53. Buckingham M., Bajard L., Chang T., Daubas P., Hadchouel J., Meilhac S., Montarras D., Rocancourt D., Relaix F. The formation of skeletal muscle: from somite to limb. J. Anat. 2003, 202:59-68.
54. Shi X., Garry D.J. Muscle stem cells in development, regeneration, and disease. Genes Dev. 2006, 20:1692-1708.
55. Balemans W., Van Hul W. Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol. 2002, 250:231-250.
56. Minamizato T., Sakamoto K., Liu T., Kokubo H., Katsube K., Perbal B., Nakamura S., Yamaguchi A. CCN3/NOV inhibits BMP-2-induced osteoblast differentiation by interacting with BMP and Notch signaling pathways. Biochem. Biophys. Res. Commun. 2007, 354:567-573.
57. Gautschi O., Tepper C.G., Purnell P.R., Izumiya Y., Evans C.P., Green T.P., Desprez P.Y., Lara P.N., Gandara D.R., Mack P.C., Kung H.J. Regulation of Id1 expression by SRC: implications for targeting of the bone morphogenetic protein pathway in cancer. Cancer Res. 2008, 68:2250-2258.