BMP signalling permits population expansion by preventing premature myogenic differentiation in muscle satellite cells

Cell Death and Differentiation

Volumn 18, Issue 2, 2011, Pages 222-234

  Ono, Y ^a   Calhabeu, F ^a   Morgan, J E ^b   Katagiri, T ^c   Amthor, H ^d   Zammit, P S ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c SAITAMA MEDICAL UNIVERSITY   (Japan)

^d Sorbonne Université   (France)

Author keywords

BMP; Id1; Noggin; satellite cell; skeletal muscle; Smad

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR 1A; INHIBITOR OF DIFFERENTIATION 1; NOGGIN; SMAD1 PROTEIN; SMAD4 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL DIVISION; CELL FUNCTION; CELL FUSION; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; GENE INACTIVATION; MOUSE; MUSCLE DEVELOPMENT; MUSCLE INJURY; MUSCLE REGENERATION; MYOBLAST; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SKELETAL MUSCLE SATELLITE CELL; UPREGULATION;

ANIMALS; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL PROLIFERATION; MICE; PHOSPHORYLATION; PYRAZOLES; PYRIMIDINES; RECOMBINANT PROTEINS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION; SMAD PROTEINS;

EID: 78651330854     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2010.95     Document Type: Article

References (39)

1. Zammit PS. All muscle satellite cells are equal, but are some more equal than others? J Cell Sci 2008;121: 2975-2982.
2. Zammit PS, Golding JP, Nagata Y, Hudon V, Partridge TA, Beauchamp JR. Muscle satellite cells adopt divergent fates: a mechanism for self-renewal? J Cell Biol 2004;166: 347-357.
3. Halevy O, Piestun Y, Allouh MZ, Rosser BW, Rinkevich Y, Reshef R et al. Pattern of Pax7 expression during myogenesis in the posthatch chicken establishes a model for satellite cell differentiation and renewal. Dev Dyn 2004;231: 489-502.
4. Collins CA, Olsen I, Zammit PS, Heslop L, Petrie A, Partridge TA et al. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 2005;122: 289-301.
5. Feng XH, Derynck R. Specificity and versatility in TGF-beta signaling through Smads. Annu Rev Cell Dev Biol 2005;21: 659-693.
6. Hollnagel A, Oehlmann V, Heymer J, Ruther U, Nordheim A. Id genes are direct targets of bone morphogenetic protein induction in embryonic stem cells. J Biol Chem 1999;274: 19838-19845.
7. Katagiri T, Imada M, Yanai T, Suda T, Takahashi N, Kamijo R. Identification of a BMPresponsive element in Id1, the gene for inhibition of myogenesis. Genes Cells 2002;7: 949-960.
8. 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.
9. Jen Y, Weintraub H, Benezra R. Overexpression of Id protein inhibits the muscle differentiation program: in vivo association of Id with E2A proteins. Genes Dev 1992;6: 1466-1479.
10. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW et al. Novel regulators of bone formation: molecular clones and activities. Science 1988;242: 1528-1534.
11. Reshef R, Maroto M, Lassar AB. Regulation of dorsal somitic cell fates: BMPs and Noggin control the timing and pattern of myogenic regulator expression. Genes Dev 1998;12: 290-303.
12. Réem-Kalma Y, Lamb T, Frank D. Competition between noggin and bone morphogenetic protein 4 activities may regulate dorsalization during Xenopus development. Proc Natl Acad Sci USA 1995;92: 12141-12145.
13. Hirsinger E, Duprez D, Jouve C, Malapert P, Cooke J, Pourquie O. Noggin acts downstream of Wnt and Sonic Hedgehog to antagonize BMP4 in avian somite patterning. Development 1997;124: 4605-4614.
14. Amthor H, Christ B, Weil M, Patel K. The importance of timing differentiation during limb muscle development. Curr Biol 1998;8: 642-652.
15. Wada MR, Inagawa-Ogashiwa M, Shimizu S, Yasumoto S, Hashimoto N. Generation of different fates from multipotent muscle stem cells. Development 2002;129: 2987-2995.
16. Katagiri T, Yamaguchi A, Komaki M, Abe E, Takahashi N, Ikeda T et al. Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J Cell Biol 1994;127: 1755-1766.
17. 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.
18. Dahlqvist C, Blokzijl A, Chapman G, Falk A, Dannaeus K, Ibanez CF et al. Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 2003;130: 6089-6099.
19. Kaplan FS, Shen Q, Lounev V, Seemann P, Groppe J, Katagiri T et al. Skeletal metamorphosis in fibrodysplasia ossificans progressiva (FOP). J Bone Miner Metab 2008;26: 521-530.
20. Lounev VY, Ramachandran R, Wosczyna MN, Yamamoto M, Maidment AD, Shore EM et al. Identification of progenitor cells that contribute to heterotopic skeletogenesis. J Bone Joint Surg Am 2009;91: 652-663.
21. Yu PB, Deng DY, Lai CS, Hong CC, Cuny GD, Bouxsein ML et al. BMP type I receptor inhibition reduces heterotopic ossification. Nat Med 2008;14: 1363-1369.
22. Namiki M, Akiyama S, Katagiri T, Suzuki A, Ueno N, Yamaji N et al. A kinase domaintruncated type I receptor blocks bone morphogenetic protein-2-induced signal transduction in C2C12 myoblasts. J Biol Chem 1997;272: 22046-22052.
23. Kodaira K, Imada M, Goto M, Tomoyasu A, Fukuda T, Kamijo R et al. Purification and identification of a BMP-like factor from bovine serum. Biochem Biophys Res Commun 2006;345: 1224-1231.
24. Ono Y, Boldrin L, Knopp P, Morgan JE, Zammit PS. Muscle satellite cells are a functionally heterogeneous population in both somite-derived and branchiomeric muscles. Dev Biol 2010;337: 29-41.
25. Ono Y, Gnocchi VF, Zammit PS, Nagatomi R. Presenilin-1 acts via Id1 to regulate the function of muscle satellite cells in a gamma-secretase-independent manner. J Cell Sci 2009;122: 4427-4438.
26. Yu PB, Hong CC, Sachidanandan C, Babitt JL, Deng DY, Hoyng SA et al. Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat Chem Biol 2008;4: 33-41.
27. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 1990;61: 49-59.
28. Akiyama S, Katagiri T, Namiki M, Yamaji N, Yamamoto N, Miyama K et al. Constitutively active BMP type I receptors transduce BMP-2 signals without the ligand in C2C12 myoblasts. Exp Cell Res 1997;235: 362-369.
29. Kumar D, Shadrach JL, Wagers AJ, Lassar AB. Id3 is a direct transcriptional target of Pax7 in quiescent satellite cells. Mol Biol Cell 2009;20: 3170-3177.
30. Clever JL, Sakai Y, Wang RA, Schneider D. Inefficient skeletal muscle repair in inhibitor of differentiation (Id) knockout mice suggests a crucial role for bmp signaling during adult muscle regeneration. Am J Physiol Cell Physiol 2010;298: C1087-C1099.
31. Sterrenburg E, van der Wees CG, White SJ, Turk R, de Menezes RX, van Ommen GJ et al. Gene expression profiling highlights defective myogenesis in DMD patients and a possible role for bone morphogenetic protein 4. Neurobiol Dis 2006;23: 228-236.
32. Xiao Q, Du Y, Wu W, Yip HK. Bone morphogenetic proteins mediate cellular response and, together with Noggin, regulate astrocyte differentiation after spinal cord injury. Exp Neurol 2010;221: 353-366.
33. Liu R, Ginn SL, Lek M, North KN, Alexander IE, Little DG et al. Myoblast sensitivity and fibroblast insensitivity to osteogenic conversion by BMP-2 correlates with the expression of Bmpr-1a. BMC Musculoskelet Disord 2009;10: 51.
34. Conboy IM, Rando TA. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 2002;3: 397-409.
35. Nakashima A, Katagiri T, Tamura M. Cross-talk between Wnt and bone morphogenetic protein 2 (BMP-2) signaling in differentiation pathway of C2C12 myoblasts. J Biol Chem 2005;280: 37660-37668.
36. Takayama K, Suzuki A, Manaka T, Taguchi S, Hashimoto Y, Imai Y et al. RNA interference for noggin enhances the biological activity of bone morphogenetic proteins in vivo and in vitro. J Bone Miner Metab 2009;27: 402-411.
37. Goldstein M, Meller I, Orr-Urtreger A. FGFR1 over-expression in primary rhabdomyosarcoma tumors is associated with hypomethylation of a 50 CpG island and abnormal expression of the AKT1, NOG, and BMP4 genes. Genes Chromosomes Cancer 2007;46: 1028-1038.
38. Tylzanowski P, Mebis L, Luyten FP. The Noggin null mouse phenotype is strain dependent and haploinsufficiency leads to skeletal defects. Dev Dyn 2006;235: 1599-1607.
39. Kariyawasam HH, Xanthou G, Barkans J, Aizen M, Kay AB, Robinson DS. Basal expression of bone morphogenetic protein receptor is reduced in mild asthma. Am J Respir Crit Care Med 2008;177: 1074-1081.