Identification of responsive cells in the developing somite supports a role for β-catenin-dependent Wnt signaling in maintaining the DML myogenic progenitor pool

Developmental Dynamics

Volumn 239, Issue 1, 2010, Pages 222-236

  Brauner, Ian ^a   Spicer, Douglas B ^b   Krull, Catherine E ^c   Venuti, Judith M ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Maine Medical Center Research Institute   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Dorsomedial lip; Myotome formation; Nuclear beta catenin; Somite; Wnt signaling

Indexed keywords

BETA CATENIN; GREEN FLUORESCENT PROTEIN; TRANSCRIPTION FACTOR PAX5; TRANSCRIPTION FACTOR PAX7; WNT PROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DERMATOME; DOWN REGULATION; EMBRYO; EMBRYO CELL; EMBRYO DEVELOPMENT; GENE ACTIVATION; GENE CONTROL; HUMAN; HUMAN CELL; MUSCLE DEVELOPMENT; MYOTOME; NONHUMAN; PRIORITY JOURNAL; PROGENY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SOMITE; STEM CELL;

ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; CHICK EMBRYO; ELECTROPORATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MESENCHYMAL STEM CELLS; MICROSCOPY, CONFOCAL; MUSCLE DEVELOPMENT; SIGNAL TRANSDUCTION; SOMITES; WNT PROTEINS;

EID: 73949090076     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.22098     Document Type: Article

References (66)

1. Aoki M, Hecht A, Kruse U, Kemler R, Vogt PK. 1999. Nuclear endpoint of Wnt signaling: neoplastic transformation induced by transactivating lymphoid-enhancing factor 1. Proc Natl Acad Sci USA 96:139-144.
2. Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, Huls G, Meeldijk J, Robertson J, van de Wetering M, Pawson T, Clevers H. 2002. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111:251-263.
3. Ben-Yair R, Kalcheim C. 2005. Lineage analysis of the avian dermomyotome sheet reveals the existence of single cells with both dermal and progenitor fates muscle. Development 132:689-701.
4. Borello U, Coletta M, Tajbakhsh S, Leyns L, De Robertis EM, Buckingham M, Cossu G. 1999. Transplacental delivery of the Wnt antagonist Frzb1 inhibits development of caudal paraxial mesoderm and skeletal myogenesis in mouse embryos. Development 126:4247-4255.
5. Borello U, Berarducci B, Murphy P, Bajard L, Buffa V, Piccolo S, Buckingham M, Cossu G. 2006. The Wnt/beta-catenin pathway regulates Gli-mediated Myf5 expression during somitogenesis. Development 133:3723-3732.
6. Brand-Saberi B, Ebensperger C, Wilting J, Balling R, Christ B. 1993. The ventralizing effect of the notochord on somite differentiation in chick embryos. Anat Embryol (Berl) 188:239-45.
7. Brunelli S, Relaix F, Baesso S, Buckingham M, Cossu G. 2007. Beta catenin-independent activation of MyoD in presomitic mesoderm requires PKC and depends on Pax3 transcriptional activity. Dev Biol 304:604-614.
8. Bryson-Richardson RJ, Currie PD. 2008. The genetics of vertebrate myogenesis. Nat Rev Genet 9:632-46.
9. Buffinger N, Stockdale FE. 1994. Myogenic specification in somites: induction by axial structures. Development 120: 1443-1452.
10. Buffinger N, Stockdale FE. 1995. Myogenic specification of somites is mediated by diffusible factors. Dev Biol 169: 96-108.
11. Capdevila J, Tabin C, Johnson RL. 1998. Control of dorsoventral somite patterning by Wnt-1 and β-catenin. Dev Biol 193:182-194.
12. Cauthen CA, Berdougo E, Sandler J, Burrus LW. 2001. Comparative analysis of the expression patterns of Wnts and Frizzleds during early myogenesis in chick embryos. Mech Dev 104:133-138.
13. Chen AE, Ginty DD, Fan CM. 2005. Protein kinase A signalling via CREB controls myogenesis induced by Wnt proteins. Nature 433:317-22.
14. Chi N, Epstein JA. 2002. Getting your Pax straight: Pax proteins in development and disease. Trends Genet 18: 41-47.
15. Cinnamon Y, Ben-Yair R, Kalcheim C. 2006. Differential effects of N-cadherin-mediated adhesion on the development of myotomal waves. Development 133: 1101-1112.
16. Cossu G, Borello U. 1999. Wnt signaling and the activation of myogenesis in mammals. Embo J 18:6867-6872.
17. Denetclaw WF Jr, Christ B, Ordahl CP. 1997. Location and growth of epaxial myotome precursor cells. Development 124:1601-1610.
18. Dietrich S, Schubert FR, Lumsden A. 1997. Control of dorsoventral pattern in the chick paraxial mesoderm. Development 124:3895-3908.
19. Dorsky RI, Sheldahl LC, Moon RT. 2002. A transgenic Lef1/beta-catenin- dependent reporter is expressed in spatially restricted domains throughout zebrafish development. Dev Biol 241:229-237.
20. Fan CM, Lee CS, Tessier-Lavigne M. 1997. A role for WNT proteins in induction of dermomyotome. Dev Biol 191: 160-165.
21. Galli LM, Willert K, Nusse R, Yablonka-Reuveni Z, Nohno T, Denetclaw W, Burrus LW. 2004. A proliferative role for Wnt-3a in chick somites. Dev Biol 269: 489-504.
22. Galli LM, Knight SR, Barnes TL, Doak AK, Kadzik RS, Burrus LW. 2008. Identification and characterization of subpopulations of Pax3 and Pax7 expressing cells in developing chick somites and limb buds. Dev Dyn 237:1862-1874
23. Geetha-Loganathan P, Nimmagadda S, Scaal M, Huang R, Christ B. 2008. Wnt signaling in somite development. Ann Anat 190:208-22.
24. George-Weinstein M, Gerhart J, Blitz J, Simak E, Knudsen KA. 1997. Ncadherin promotes the commitment and differentiation of skeletal muscle precursor cells. Dev Biol 185:14-24.
25. Goichberg P, Geiger B. 1998. Direct involvement of N-cadherin-mediated signaling in muscle differentiation. Mol Biol Cell 9:3119-3131.
26. Goichberg P, Shtutman M, Ben-Ze-ev A, Geiger B. 2001. Recruitment of beta-catenin to cadherin mediated intercellular adhesions is involved in myogenic induction. J Cell Sci 114:1309-1319.
27. Gros J, Scaal M, Marcelle C. 2004. A two-step mechanism for myotome formation in chick. Nature 435:954-958
28. Gros J, Manceau M, Thomé V, Marcelle C. 2005. A common somitic origin for embryonic muscle progenitors and satellite cells. Dev Cell 5:367-377.
29. Hamburger V, Hamilton HL. 1992. A series of normal stages in the development of the chick embryo. Dev Dyn 195:231-272.
30. Ikeya M, Takada S. 1998. Wnt signaling from the dorsal neural tube is required for the formation of the medial dermomyotome. Development 125:4969-4976
31. Kanazawa A, Tsukada S, Kamiyama M, Yanagimoto T, Nakajima M, Maeda S. 2005. Wnt5b partially inhibits canonical Wnt/beta-catenin signaling pathway promotes adipogenesis in 3T3-L1 preadipocytes. Biochem Biophys Res Commun 330:505-510.
32. Kassar-Duchossoy L, Giacone E, Gayraud-Morel B, Jory A, Gomès D, Tajbakhsh S. 2005. Pax3/Pax7 mark a novel population of primitive myogenic cells during development. Genes Dev 19:1426-1431
33. Kenny-Mobbs T, Thorogood P. 1987. Autonomy of differentiation in avian branchial somites and the influence of adjacent tissues. Development 100: 449-462
34. Kim CH, Neiswender H, Baik EJ, Xiong WC, Mei L. 2008. Beta-catenin interacts with MyoD and regulates its transcription activity. Mol Cell Biol 28: 2941-2951.
35. Krull CE. 2004. A primer on using in ovo electroporation to analyze gene function. Dev Dyn 229:433-439.
36. Linask KK, Ludwig C, Han MD, Liu X, Radice GL, Knudsen KA. 1998. N-cadherin/catenin-mediated morphoregulation of somite formation. Dev Biol 202: 85-102.
37. Linker C, Lesbros C, Stark MR, Marcelle C. 2003. Intrinsic signals regulate the initial steps of myogenesis in vertebrates. Development 130:4797-4807.
38. Logan CY, Nusse R. 2004. The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810.
39. Marcelle C, Stark MR, Bronner-Fraser M. 1997. Coordinate actions of BMPs, Wnts, Shh and noggin mediate patterning of the dorsal somite. Development 124:3955-3963.
40. Munsterberg AE, Lassar AB. 1995. Combinatorial signals from the neural tube, floor plate and notochord induce myogenic bHLH gene expression in the somite. Development 121:651-660.
41. Munsterberg AE, Kitajewski J, Bumcrot DA, McMahon AP, Lassar AB. 1995. Combinatorial signaling by Sonic hedgehog and Wnt family members induces myogenic bHLH gene expression in the somite. Genes Dev 9: 2911-2922.
42. Nam JS, Turcotte TJ, Smith PF, Choi S, Yoon JK. 2006. Mouse cristin/R-spondin family proteins are novel ligands for the Frizzled 8 and LRP6 receptors and activate beta-catenin-dependent gene expression. J Biol Chem 281: 13247-13257.
43. Nieto MA, Patel K, Wilkinson DG. 1996. In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol 51:219-235.
44. Olguin HC, Olwin BB. 2004. Pax-7 upregulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev Biol 275:375-388.
45. Ordahl CP, Le Douarin N. 1992. Two myogenic lineages within the developing somite. Development 114:339-353.
46. Ordahl CP, Berdougo E, Venters SJ, Denetclaw WF Jr. 2001. The dermomyotome dorsomedial lip drives growth and morphogenesis of both the primary myotome and dermomyotome epithelium. Development 128:1731-1744.
47. Osumi N, Inoue T. 2001. Gene transfer into cultured mammalian embryos by electroporation. Methods 24:35-42.
48. Perez-Ruiz A, Ono Y, Gnocchi VF, Zammit PS. 2008. beta-Catenin promotes self-renewal of skeletal-muscle satellite cells. J Cell Sci 121:1373-1382
49. Petropoulos H, Iskerjanc IS. 2002. β-Catenin is essential and sufficient for skeletal myogenesis in P19 cells. J Biol Chem 277:15393-15399.
50. Polesskaya A, Seale P, Rudnicki MA. 2003. Wnt signaling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration. Cell 113:841-852.
51. Pownall ME, Strunk KE, Emerson CP Jr. 1996. Notochord signals control the transcriptional cascade of myogenic bHLH genes in somites of quail embryos. Development 122:1475-1488.
52. Relaix F, Rocancourt D, Mansouri A, Buckingham M. 2005. A Pax3/Pax7-dependent population of skeletal muscle progenitor cells. Nature 435:948-953.
53. Reshef R, Maroto M, Lassar AB. 1998. Regulation of dorsal somitic cell fates: BMPs and Noggin control the timing and pattern of myogenic regulator expression. Genes Dev 12:290-303.
54. Ridgeway AG, Petropoulos H, Wilton S, Skerjanc IS. 2000. Wnt signaling regulates the function of MyoD and myogenin. J Biol Chem 275:32398-32405.
55. Scaal M, Gros J, Lesbros C, Marcelle C. 2004. In ovo electroporation of avian somites. Dev Dyn 229:643-650.
56. Schmidt M, Tanaka M, Munsterberg A. 2000. Expression of beta-catenin in the developing chick myotome is regulated by myogenic signals. Development 127: 4105-4113.
57. Spence MS, Yip J, Erickson CA. 1996. The dorsal neural tube organizes the dermamyotome and induces axial myocytes in the avian embryo. Development 122:231-241
58. Stern HM, Hauschka SD. 1995. Neural tube and notochord promote in vitro myogenesis in single somite explants. Dev Biol 167:87-103.
59. Swartz ME, Eberhart J, Pasquale EB, Krull CE. 2001. EphA4/ephrin-A5 interactions in muscle precursor cell migration in the avian forelimb. Development 128:4669-4680.
60. Tajbakhsh S, Borello U, Vivarelli E, Kelly R, Papkoff J, Duprez D, Buckingham M, Cossu G. 1998. Differential activation of Myf5 and MyoD by different Wnts in explants of mouse paraxial mesoderm and the later activation of myogenesis in the absence of Myf5. Development 125:4155-4162.
61. van de Wetering M, Castrop J, Korinek V, Clevers H. 1996. Extensive alternative splicing and dual promoter usage generate Tcf-1 protein isoforms with differential transcription control properties. Mol Cell Biol 16:745-752.
62. Veeman MT, Axelrod JD, Moon RT. 2003. A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev Cell 5:367-377.
63. Venters S, Ordahl CP. 2002. Persistent myogenic capacity of the dermomyotome dorsomedial lip and restriction of myogenic competence. Development 129:3873-3885.
64. Venters SJ, Ordahl CP. 2005. Asymmetric cell divisions are concentrated in the dermomyotome dorsomedial lip during epaxial primary myotome morphogenesis. Anat Embryol Berl 209:449-460.
65. Weidinger G, Moon RT. 2003. When Wnts antagonize Wnts. J Cell Biol 162: 753-755.
66. Zammit PS, Relaix F, Nagata Y, Ruiz AP, Collins CA, Partridge TA, Beauchamp JR. 2006. Pax7 and myogenic progression in skeletal muscle satellite cells. J Cell Sci 119:1824-1832.