Hedgehog and Wnt coordinate signaling in myogenic progenitors and regulate limb regeneration

Developmental Biology

Volumn 371, Issue 1, 2012, Pages 23-34

  Singh, Bhairab N ^a   Doyle, Michelle J ^a   Weaver, Cyprian V ^a   Koyano Nakagawa, Naoko ^a   Garry, Daniel J ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Blastema; Dedifferentiation; Regeneration; Signaling pathways

Indexed keywords

CYCLOPAMINE; MYOSIN HEAVY CHAIN; PROTEIN P21; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR PAX7; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR POSTERIOR PATTERNING; ARTICLE; BLASTEMA; CELL CYCLE S PHASE; CELL DEDIFFERENTIATION; CELL DENSITY; CELL EXPANSION; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; G1 PHASE CELL CYCLE CHECKPOINT; G2 PHASE CELL CYCLE CHECKPOINT; LIMB REGENERATION; MOLECULAR DYNAMICS; MORPHOGENESIS; MOUSE; MUSCLE CELL; MYOGENIC STEM CELL; NONHUMAN; NOTOPHTHALMUS VIRIDESCENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEM CELL; WNT SIGNALING PATHWAY;

AMPHIBIA; ERINACEIDAE; SALAMANDRIDAE;

EID: 84866517710     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.07.033     Document Type: Article

References (56)

1. Akimenko M.A., Mari-Beffa M., Becerra J., Geraudie J. Old questions, new tools, and some answers to the mystery of fin regeneration. Dev. Dyn. 2003, 226:190-201.
2. Alvarez-Medina R., Le Dreau G., Ros M., Martí E. Hedgehog activation is required upstream of Wnt signaling to control neural progenitor proliferation. Development 2009, 136:3301-3309.
3. Bren-Mattison Y., Olwin B.B. Sonic hedgehog inhibits the terminal differentiation of limb myoblasts committed to the slow muscle lineage. Dev. Biol. 2002, 242:130-148.
4. Bren-Mattison Y., Hausburg M., Olwin B.B. Growth of limb muscle is dependent on skeletal-derived Indian hedgehog. Dev. Biol. 2011, 356:486-495.
5. Brockes J.P., Kumar A. Plasticity and reprogramming of differentiated cells in amphibian regeneration. Nat. Rev. Mol. Cell Biol. 2002, 3:566-574.
6. Campbell L.J., Crews C.M. Wound epidermis formation and function in urodele amphibian limb regeneration. Cell Mol. Life. Sci. 2008, 65:73-79.
7. Casimir C.M., Gates P.B., Patient R.K., Brockes J.P. Evidence for dedifferentiation and metaplasia in amphibian limb regeneration from inheritance of DNA methylation. Development 1988, 104:657-668.
8. Caubit X., Nicolas S., Le Parco Y. Possible roles for Wnt genes in growth and axial patterning during regeneration of the tail in urodele amphibians. Dev. Dyn. 1997, 210:1-10.
9. Chablais F., Jazwinska A. IGF signaling between blastema and wound epidermis is required for fin regeneration. Development 2010, 137:871-879.
10. Charge S.B., Rudnicki M.A. Cellular and molecular regulation of muscle regeneration. Physiol. Rev. 2004, 84:209-238.
11. Chen J.K., Taipale J., Cooper M.K., Beachy P.A. Inhibition of Hedgehog signaling by direct binding of cyclopamine to Smoothened. Genes Dev. 2002, 16:2743-2748.
12. Chiang C., Litingtung Y., Harris M.P., Simandl B.K., Li Y., Beachy P.A., Fallon J.F. Manifestation of the limb prepattern: limb development in the absence of sonic hedgehog function. Dev. Biol. 2001, 236:421-435.
13. Collins C.A., Olsen I., Zammit P.S., Heslop L., Petrie A., Partridge T.A., Morgan J.E. Stem cell function, self-renewal, and behavioral heterogeneity of cells from the adult muscle satellite cell niche. Cell 2005, 122:289-301.
14. Duprez D., Fournier-Thibault C., Le Douarin N. Sonic Hedgehog induces proliferation of committed skeletal muscle cells in the chick limb. Development 1998, 125:495-505.
15. Echeverri K., Clarke J.D., Tanaka E.M. In vivo imaging indicates muscle fiber dedifferentiation is a major contributor to the regenerating tail blastema. Dev. Biol. 2001, 236:151-164.
16. Endo T., Yokoyama H., Tamura K., Ide H. Shh expression in developing and regenerating limb buds of Xenopus laevis. Dev. Dyn. 1997, 209:227-232.
17. Gardiner D.M., Endo T., Bryant S.V. The molecular basis of amphibian limb regeneration: integrating the old with the new. Semin. Cell Dev. Biol. 2002, 13:345-352.
18. Globus M., Vethamany-Globus S., Lee Y.C. Effect of apical epidermal cap on mitotic cycle and cartilage differentiation in regeneration blastemata in the newt Notophthalmus viridescens. Dev. Biol 1980, 75:358-372.
19. Goodrich L.V., Johnson R.L., Milenkovic L., McMahon J.A., Scott M.P. Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev. 1996, 10:301-312.
20. Hanken J., Wassersug R. The visible skeleton. Funct. Photogr. 1981, 16:22-26.
21. Harfe B.D., Scherz P.J., Nissim S., Tian H., McMahon A.P., Tabin C.J. Evidence for an expansion-based temporal Shh gradient in specifying vertebrate digit identities. Cell 2004, 118:517-528.
22. Imokawa Y., Yoshizato K. Expression of Sonic hedgehog gene in regenerating newt limb blastemas recapitulates that in developing limb buds. Proc. Natl. Acad. Sci. 1997, 94:9159-9164.
23. Iovine M.K. Conserved mechanisms regulate outgrowth in zebrafish fins. Nat. Chem. Biol. 2007, 3:613-618.
24. Kawakami Y., Rodriguez Esteban C., Raya M., Kawakami H., Marti M., Dubova I., Izpisua Belmonte J.C. Wnt/beta-catenin signaling regulates vertebrate limb regeneration. Genes Dev. 2006, 20:3232-3237.
25. Knopf F., Hammond C., Chekuru A., Kurth T., Hans S., Weber C.W., Mahatma G., Fisher S., Brand M., Schulte-Merker S., Weidinger G. Bone regenerates via dedifferentiation of osteoblasts in the zebrafish fin. Dev. Cell 2011, 20:713-724.
26. 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.
27. Kragl M., Knapp D., Nacu E., Khattak S., Maden M., Epperlein H.H., Tanaka E.M. Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature 2009, 460:60-65.
28. Lentz T.L. Cytological studies of muscle dedifferentiation and differentiation during limb regeneration of the newt Triturus. Am. J. Anat. 1969, 124:447-479.
29. Lewandoski M., Sun X., Martin G.R. Fgf8 signaling from the AER is essential for normal limb development. Nature Genet. 2000, 26:460-463.
30. Lin G., Slack J.M. Requirement for Wnt and FGF signaling in Xenopus tadpole tail regeneration. Dev. Biol. 2008, 316:323-335.
31. Lo D.C., Allen F., Brockes J.P. Reversal of muscle differentiation during urodele limb regeneration. Proc. Natl. Acad. Sci. 1993, 90:7230-7234.
32. McGann C.J., Odelberg S.J., Keating M.T. Mammalian myotube dedifferentiation induced by newt regeneration extract. Proc. Natl. Acad. Sci. 2001, 98:13699-13704.
33. Minina E., Kreschel C., Naski M.C., Ornitz D.M., Vortkamp A. Interaction of FGF, Ihh/Pthlh, and BMP signaling integrates chondrocyte proliferation and hypertrophic differentiation. Dev. Cell 2002, 3:1-20.
34. Morrison J.I., Loof S., He P., Simon A. Salamander limb regeneration involves the activation of a multipotent skeletal muscle satellite cell population. J. Cell Biol. 2006, 172:433-440.
35. Panman L., Galli A., Lagarde N., Michos O., Soete G., Zuniga A., Zeller R. Differential regulation of gene expression in the digit forming area of the mouse limb bud by SHH and gremlin 1/FGF-mediated epithelial-mesenchymal signaling. Development 2006, 133:3419-3428.
36. Poss K.D., Shen J., Keating M.T. Induction of lef1 during zebrafish fin regeneration. Dev. Dyn. 2000, 219:282-286.
37. Poss K.D., Keating M.T., Nechiporuk A. Tales of regeneration in zebrafish. Dev. Dyn. 2003, 226:202-210.
38. Schnapp E., Kragl M., Rubin L., Tanaka E.M. Hedgehog signaling controls dorsoventral patterning, blastema cell proliferation and cartilage induction during axolotl tail regeneration. Development 2005, 132:3243-3253.
39. Scherz P.J., McGlinn E., Nissim S., Tabin C.J. Extended exposure to Sonic hedgehog is required for patterning the posterior digits of the vertebrate limb. Dev. Biol. 2007, 308:343-354.
40. Singh B.N., Koyano-Nakagawa N., Garry J.P., Weaver C.V. Heart of newt: a recipe for regeneration. J. Cardiovasc. Transl. Res. 2010, 3:397-409.
41. Slack J.M. Amphibian muscle regeneration-dedifferentiation or satellite cells?. Trends Cell Biol. 2006, 16:273-275.
42. Stoick-Cooper C.L., Weidinger G., Riehle K.J., Hubbert C., Major M.B., Fausto N., Moon R.T. Distinct Wnt signaling pathways have opposing roles in appendage regeneration. Development 2007, 134:479-489.
43. Stopper G.F., Wagner G.P. Inhibition of Sonic hedgehog signaling leads to posterior digit loss in Ambystoma mexicanum: parallels to natural digit reduction in urodeles. Dev. Dyn 2007, 236:321-331.
44. Tanaka E.M. Cell differentiation and cell fate during urodele tail and limb regeneration. Curr. Opin. Genet. Dev 2003, 13:497-501.
45. te Welscher P., Zuniga A., Kuijper S., Drenth T., Goedemans H.J., Meijlink F., Zeller R. Progression of vertebrate limb development through SHH-mediated counteraction of GLI3. Science 2002, 298:827-830.
46. Tickle C. Making digit patterns in the vertebrate limb. Nat. Rev. Mol. Cell Biol. 2006, 7:45-53.
47. Tsonis P.A., Vergara M.N., Spence J.R., Madhavan M., Kramer E.L., Call M.K., Santiago W.G., Vallance J.E., Robbins D.J., Del Rio-Tsonis K. A novel role of the hedgehog pathway in lens regeneration. Dev. Biol. 2004, 267:450-461.
48. Verheyden J.M., Sun X. An Fgf/Gremlin inhibitory feedback loop triggers termination of limb bud outgrowth. Nature 2008, 454:638-641.
49. Wallace H. Vertebrate Limb Regeneration 1981, Wiley and Sons, New York.
50. Whitehead G.G., Makino S., Lien C.L., Keating M.T. fgf20 is essential for initiating zebrafish fin regeneration. Science 2005, 310:1957-1960.
51. Yaffe D., Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 1977, 270:725-727.
52. Yokoyama H., Ogino H., Stoick-Cooper C.L., Grainger R.M., Moon R.T. Wnt/beta-catenin signaling has an essential role in the initiation of limb regeneration. Dev. Biol. 2007, 306:170-178.
53. Yokoyama H., Maruoka T., Ochi H., Aruga A., Ohgo S., Ogino H., Tamura K. Different requirement for Wnt/Β-Catenin signaling in limb regeneration of larval and adult Xenopus. PLoS One 2011, 6:e21721.
54. Zeller R. It takes time to make a pinky: unexpected insights into how SHH patterns vertebrate digits. Sci. STKE 2004, 259. pe 53.
55. Zeller R., Lopez-Rios J., Zuniga A. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat. Rev. Genet. 2009, 10:845-858.
56. Zuniga A., Haramis A.P., McMahon A.P., Zeller R. Signal relay by BMP antagonism controls the SHH/FGF4 feedback loop in vertebrate limb buds. Nature 1999, 401:598-602.