Wnt/β-catenin controls follistatin signalling to regulate satellite cell myogenic potential

Skeletal Muscle

Volumn 5, Issue 1, 2015, Pages

  Jones, Andrew E ^a,b   Price, Feodor D ^a,b   Le Grand, Fabien ^c   Soleimani, Vahab D ^a   Dick, Sarah A ^a,b   Megeney, Lynn A ^a,b   Rudnicki, Michael A ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c INSTITUT COCHIN   (France)

Author keywords

Myogenic differentiation; Satellite cell; Skeletal muscle regeneration; Wnt catenin

Indexed keywords

EID: 84928806155     PISSN: None     EISSN: 20445040     Source Type: Journal    
DOI: 10.1186/s13395-015-0038-6     Document Type: Article

References (60)

1. Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol. 1961;9:493-5.
2. Montarras D, Morgan J, Collins C, Relaix F, Zaffran S, Cumano A, et al. Direct isolation of satellite cells for skeletal muscle regeneration. Science. 2005;309:2064-7.
3. Schultz E, Gibson MC, Champion T. Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J Exp Zool. 1978;206:451-6.
4. Charge SB, Rudnicki MA. Cellular and molecular regulation of muscle regeneration. Physiol Rev. 2004;84:209-38.
5. Berkes CA, Tapscott SJ. MyoD and the transcriptional control of myogenesis. Semin Cell Dev Biol. 2005;16:585-95.
6. Bentzinger CF, Wang YX, Rudnicki MA. Building muscle: molecular regulation of myogenesis. Cold Spring Harb Perspect Biol. 2012;4:a008342.
7. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell. 2006;127:469-80.
8. von Maltzahn J, Chang NC, Bentzinger CF, Rudnicki MA. Wnt signaling in myogenesis. Trends Cell Biol. 2012;22:602-9.
9. Le Grand F, Jones AE, Seale V, Scime A, Rudnicki MA. Wnt7a activates the planar cell polarity pathway to drive the symmetric expansion of satellite stem cells. Cell Stem Cell. 2009;4:535-47.
10. Otto A, Schmidt C, Luke G, Allen S, Valasek P, Muntoni F, et al. Canonical Wnt signalling induces satellite-cell proliferation during adult skeletal muscle regeneration. J Cell Sci. 2008;121:2939-50.
11. Brack AS, Conboy IM, Conboy MJ, Shen J, Rando TA. A temporal switch from notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell. 2008;2:50-9.
12. Brack AS, Murphy-Seiler F, Hanifi J, Deka J, Eyckerman S, Keller C, et al. BCL9 is an essential component of canonical Wnt signaling that mediates the differentiation of myogenic progenitors during muscle regeneration. Dev Biol. 2009;335:93-105.
13. 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.
14. Brack AS, Conboy MJ, Roy S, Lee M, Kuo CJ, Keller C, et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science. 2007;317:807-10.
15. Polesskaya A, Seale P, Rudnicki MA. Wnt signaling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration. Cell. 2003;113:841-52.
16. Megeney LA, Kablar B, Garrett K, Anderson JE, Rudnicki MA. MyoD is required for myogenic stem cell function in adult skeletal muscle. Genes Dev. 1996;10:1173-83.
17. Kuang S, Kuroda K, Le Grand F, Rudnicki MA. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell. 2007;129:999-1010.
18. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003;4:249-64.
19. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5:R80.
20. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A. 2001;98:5116-21.
21. Schwender H. siggenes. Multiple testing using SAM and Efron's empirical Bayes approaches. R Package Version 1200. 2009. http://www.bioconductor.org/packages/release/bioc/html/siggenes.html.
22. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, Mesirov JP. GenePattern 2.0. Nat Genet. 2006;38:500-1.
23. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57.
24. da Huang W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37:1-13.
25. Holterman CE, Le Grand F, Kuang S, Seale P, Rudnicki MA. Megf10 regulates the progression of the satellite cell myogenic program. J Cell Biol. 2007;179:911-22.
26. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000;132:365-86.
27. Soleimani VD, Punch VG, Kawabe Y, Jones AE, Palidwor GA, Porter CJ, et al. Transcriptional dominance of Pax7 in adult myogenesis is due to high-affinity recognition of homeodomain motifs. Dev Cell. 2012;22:1208-20.
28. Soleimani VD, Yin H, Jahani-Asl A, Ming H, Kockx CE, van Ijcken WF, et al. Snail regulates MyoD binding-site occupancy to direct enhancer switching and differentiation-specific transcription in myogenesis. Mol Cell. 2012;47:457-68.
29. Lee S-J, McPherron AC. Regulation of myostatin activity and muscle growth. Proc Natl Acad Sci. 2001;98:9306-11.
30. Nakamura T, Takio K, Eto Y, Shibai H, Titani K, Sugino H. Activin-binding protein from rat ovary is follistatin. Science. 1990;247:836-8.
31. Lee SJ, Reed LA, Davies MV, Girgenrath S, Goad ME, Tomkinson KN, et al. Regulation of muscle growth by multiple ligands signaling through activin type II receptors. Proc Natl Acad Sci U S A. 2005;102:18117-22.
32. Liu QC, Zha XH, Faralli H, Yin H, Louis-Jeune C, Perdiguero E, et al. Comparative expression profiling identifies differential roles for Myogenin and p38alpha MAPK signaling in myogenesis. J Mol Cell Biol. 2012;4:386-97.
33. Kim CH, Neiswender H, Baik EJ, Xiong WC, Mei L. Beta-catenin interacts with MyoD and regulates its transcription activity. Mol Cell Biol. 2008;28:2941-51.
34. Pan YC, Wang XW, Teng HF, Wu YJ, Chang HC, Chen SL. Wnt3a signal pathways activate MyoD expression by targeting cis-elements inside and outside its distal enhancer. Biosci Rep. 2015;35(2):e00180.
35. Polychronopoulos P, Magiatis P, Skaltsounis AL, Myrianthopoulos V, Mikros E, Tarricone A, et al. Structural basis for the synthesis of indirubins as potent and selective inhibitors of glycogen synthase kinase-3 and cyclin-dependent kinases. J Med Chem. 2004;47:935-46.
36. Han XH, Jin YR, Seto M, Yoon JK. A WNT/beta-catenin signaling activator, R-spondin, plays positive regulatory roles during skeletal myogenesis. J Biol Chem. 2011;286:10649-59.
37. Rochat A, Fernandez A, Vandromme M, Moles JP, Bouschet T, Carnac G, et al. Insulin and wnt1 pathways cooperate to induce reserve cell activation in differentiation and myotube hypertrophy. Mol Biol Cell. 2004;15:4544-55.
38. van der Velden JL, Langen RC, Kelders MC, Wouters EF, Janssen-Heininger YM, Schols AM. Inhibition of glycogen synthase kinase-3beta activity is sufficient to stimulate myogenic differentiation. Am J Physiol Cell Physiol. 2006;290:C453-62.
39. Zhao P, Hoffman EP. Embryonic myogenesis pathways in muscle regeneration. Dev Dyn. 2004;229:380-92.
40. Murphy MM, Keefe AC, Lawson JA, Flygare SD, Yandell M, Kardon G. Transiently active Wnt/beta-catenin signaling is not required but must be silenced for stem cell function during muscle regeneration. Stem Cell Rep. 2014;3:475-88.
41. Rosenthal N. Muscle cell differentiation. Curr Opin Cell Biol. 1989;1:1094-101.
42. Weintraub H. The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell. 1993;75:1241-4.
43. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT. c-Myc-regulated microRNAs modulate E2F1 expression. Nature. 2005;435:839-43.
44. Sylvestre Y, De Guire V, Querido E, Mukhopadhyay UK, Bourdeau V, Major F, et al. An E2F/miR-20a autoregulatory feedback loop. J Biol Chem. 2007;282:2135-43.
45. Faralli H, Dilworth FJ. Turning on myogenin in muscle: a paradigm for understanding mechanisms of tissue-specific gene expression. Comp Funct Genomics. 2012;2012:836374.
46. Kormish JD, Sinner D, Zorn AM. Interactions between SOX factors and Wnt/beta-catenin signaling in development and disease. Dev Dyn. 2010;239:56-68.
47. Almeida M, Han L, Martin-Millan M, O'Brien CA, Manolagas SC. Oxidative stress antagonizes Wnt signaling in osteoblast precursors by diverting beta-catenin from T cell factor- to forkhead box O-mediated transcription. J Biol Chem. 2007;282:27298-305.
48. Olson LE, Tollkuhn J, Scafoglio C, Krones A, Zhang J, Ohgi KA, et al. Homeodomain-mediated beta-catenin-dependent switching events dictate cell-lineage determination. Cell. 2006;125:593-605.
49. Kioussi C, Briata P, Baek SH, Rose DW, Hamblet NS, Herman T, et al. Identification of a Wnt/Dvl/beta-catenin Pitx2 pathway mediating cell-type-specific proliferation during development. Cell. 2002;111:673-85.
50. Kaidi A, Williams AC, Paraskeva C. Interaction between beta-catenin and HIF-1 promotes cellular adaptation to hypoxia. Nat Cell Biol. 2007;9:210-7.
51. Mulholland DJ, Dedhar S, Coetzee GA, Nelson CC. Interaction of nuclear receptors with the Wnt/beta-catenin/Tcf signaling axis: Wnt you like to know? Endocr Rev. 2005;26:898-915.
52. Hemmati-Brivanlou A, Kelly OG, Melton DA. Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell. 1994;77:283-95.
53. Iemura S, Yamamoto TS, Takagi C, Uchiyama H, Natsume T, Shimasaki S, et al. Direct binding of follistatin to a complex of bone-morphogenetic protein and its receptor inhibits ventral and epidermal cell fates in early Xenopus embryo. Proc Natl Acad Sci U S A. 1998;95:9337-42.
54. Lee SJ. Quadrupling muscle mass in mice by targeting TGF-beta signaling pathways. PLoS One. 2007;2:e789.
55. Lee SJ, Lee YS, Zimmers TA, Soleimani A, Matzuk MM, Tsuchida K, et al. Regulation of muscle mass by follistatin and activins. Mol Endocrinol. 2010;24:1998-2008.
56. Ruvinsky I, Katz M, Dreazen A, Gielchinsky Y, Saada A, Freedman N, et al. Mice deficient in ribosomal protein S6 phosphorylation suffer from muscle weakness that reflects a growth defect and energy deficit. PLoS One. 2009;4:e5618.
57. Winbanks CE, Weeks KL, Thomson RE, Sepulveda PV, Beyer C, Qian H, et al. Follistatin-mediated skeletal muscle hypertrophy is regulated by Smad3 and mTOR independently of myostatin. J Cell Biol. 2012;197:997-1008.
58. Glass DJ. Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol. 2005;37:1974-84.
59. de Groot E, Veltmaat J, Caricasole A, Defize L, van den Eijnden-van RA. Cloning and analysis of the mouse follistatin promoter. Mol Biol Rep. 2000;27:129-39.
60. Han XH, Jin YR, Tan L, Kosciuk T, Lee JS, Yoon JK. Regulation of the follistatin gene by RSPO-LGR4 signaling via activation of the WNT/beta-catenin pathway in skeletal myogenesis. Mol Cell Biol. 2014;34:752-64.