Pax3 synergizes with Gli2 and Zic1 in transactivating the Myf5 epaxial somite enhancer

Developmental Biology

Volumn 383, Issue 1, 2013, Pages 7-14

  Himeda, Charis L ^a   Barro, Marietta V ^b   Emerson, Charles P ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Gli; Myf5; Myogenesis; Pax; Skeletal muscle; Zic

Indexed keywords

CELL PROTEIN; MYOGENIC FACTOR 5; TRANSCRIPTION FACTOR GLI2; TRANSCRIPTION FACTOR PAX3; UNCLASSIFIED DRUG; ZIC1 PROTEIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; MESODERM; MOLECULAR DYNAMICS; MOLECULAR MODEL; MOUSE; MUSCLE DEVELOPMENT; NEURAL CREST; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SOMITE;

ERINACEIDAE; MYOXUS;

EID: 84885483275     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.09.006     Document Type: Article

References (61)

1. Anderson C., Williams V.C., Moyon B., Daubas P., Tajbakhsh S., Buckingham M.E., Shiroishi T., Hughes S.M., Borycki A.G. Sonic hedgehog acts cell-autonomously on muscle precursor cells to generate limb muscle diversity. Genes Dev. 2012, 26:2103-2117.
2. Aruga J., Mizugishi K., Koseki H., Imai K., Balling R., Noda T., Mikoshiba K. Zic1 regulates the patterning of vertebral arches in cooperation with Gli3. Mech. Dev. 1999, 89:141-150.
3. Bajard L., Relaix F., Lagha M., Rocancourt D., Daubas P., Buckingham M.E. A novel genetic hierarchy functions during hypaxial myogenesis: Pax3 directly activates Myf5 in muscle progenitor cells in the limb. Genes Dev. 2006, 20:2450-2464.
4. Bober E., Franz T., Arnold H.H., Gruss P., Tremblay P. Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 1994, 120:603-612.
5. Borello U., Berarducci B., Murphy P., Bajard L., Buffa V., Piccolo S., Buckingham M., Cossu G. The Wnt/beta-catenin pathway regulates Gli-mediated Myf5 expression during somitogenesis. Development 2006, 133:3723-3732.
6. Borycki A., Brown A.M., Emerson C.P. Shh and Wnt signaling pathways converge to control Gli gene activation in avian somites. Development 2000, 127:2075-2087.
7. Borycki A.G., Brunk B., Tajbakhsh S., Buckingham M., Chiang C., Emerson C.P. Sonic hedgehog controls epaxial muscle determination through Myf5 activation. Development 1999, 126:4053-4063.
8. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
9. Braun T., Rudnicki M.A., Arnold H.H., Jaenisch R. Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 1992, 71:369-382.
10. Brewster R., Lee J., Altaba A.Ruiz i Gli/Zic factors pattern the neural plate by defining domains of cell differentiation. Nature 1998, 393:579-583.
11. Buchberger A., Freitag D., Arnold H.H. A homeo-paired domain-binding motif directs Myf5 expression in progenitor cells of limb muscle. Development 2007, 134:1171-1180.
12. Carvajal J.J., Keith A., Rigby P.W. Global transcriptional regulation of the locus encoding the skeletal muscle determination genes Mrf4 and Myf5. Genes Dev. 2008, 22:265-276.
13. Corry G.N., Raghuram N., Missiaen K.K., Hu N., Hendzel M.J., Underhill D.A. The PAX3 paired domain and homeodomain function as a single binding module in vivo to regulate subnuclear localization and mobility by a mechanism that requires base-specific recognition. J. Mol. Biol. 2010, 402:178-193.
14. Daubas P., Buckingham M.E. Direct molecular regulation of the myogenic determination gene Myf5 by Pax3, with modulation by Six1/4 factors, is exemplified by the -111kb-Myf5 enhancer. Dev. Biol. 2013, 376:236-244.
15. Dignam J.D., Lebovitz R.M., Roeder R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983, 11:1475-1489.
16. Ding Q., Motoyama J., Gasca S., Mo R., Sasaki H., Rossant J., Hui C.C. Diminished sonic hedgehog signaling and lack of floor plate differentiation in Gli2 mutant mice. Development 1998, 125:2533-2543.
17. Ebert P.J., Timmer J.R., Nakada Y., Helms A.W., Parab P.B., Liu Y., Hunsaker T.L., Johnson J.E. Zic1 represses Math1 expression via interactions with the Math1 enhancer and modulation of Math1 autoregulation. Development 2003, 130:1949-1959.
18. Francetic T., Li Q. Skeletal myogenesis and Myf5 activation. Transcription 2011, 2:109-114.
19. Goulding M., Lumsden A., Paquette A.J. Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 1994, 120:957-971.
20. Goulding M.D., Chalepakis G., Deutsch U., Erselius J.R., Gruss P. Pax-3, a novel murine DNA binding protein expressed during early neurogenesis. Embo J. 1991, 10:1135-1147.
21. Gustafsson M.K., Pan H., Pinney D.F., Liu Y., Lewandowski A., Epstein D.J., Emerson C.P. Myf5 is a direct target of long-range Shh signaling and Gli regulation for muscle specification. Genes Dev. 2002, 16:114-126.
22. Himeda C.L., Ranish J.A., Hauschka S.D. Quantitative proteomic identification of MAZ as a transcriptional regulator of muscle-specific genes in skeletal and cardiac myocytes. Mol. Cell. Biol. 2008, 28:6521-6535.
23. Horst D., Ustanina S., Sergi C., Mikuz G., Juergens H., Braun T., Vorobyov E. Comparative expression analysis of Pax3 and Pax7 during mouse myogenesis. Int. J. Dev. Biol. 2006, 50:47-54.
24. Hoth C.F., Milunsky A., Lipsky N., Sheffer R., Clarren S.K., Baldwin C.T. Mutations in the paired domain of the human PAX3 gene cause Klein-Waardenburg syndrome (WS-III) as well as Waardenburg syndrome type I (WS-I). Am. J. Hum. Genet. 1993, 52:455-462.
25. Houtmeyers R., Souopgui J., Tejpar S., Arkell R. The ZIC gene family encodes multi-functional proteins essential for patterning and morphogenesis. Cell. Mol. Life Sci. 2013.
26. Hu J.K., McGlinn E., Harfe B.D., Kardon G., Tabin C.J. Autonomous and nonautonomous roles of Hedgehog signaling in regulating limb muscle formation. Genes Dev. 2012, 26:2088-2102.
27. Huang R., Stolte D., Kurz H., Ehehalt F., Cann G.M., Stockdale F.E., Patel K., Christ B. Ventral axial organs regulate expression of myotomal Fgf-8 that influences rib development. Dev. Biol. 2003, 255:30-47.
28. Hui C.C., Angers S. Gli proteins in development and disease. Annu. Rev. Cell Dev. Biol. 2011, 27:513-537.
29. Kassar-Duchossoy L., Gayraud-Morel B., Gomes D., Rocancourt D., Buckingham M., Shinin V., Tajbakhsh S. Mrf4 determines skeletal muscle identity in Myf5:Myod double-mutant mice. Nature 2004, 431:466-471.
30. Koyabu Y., Nakata K., Mizugishi K., Aruga J., Mikoshiba K. Physical and functional interactions between Zic and Gli proteins. J. Biol. Chem. 2001, 276:6889-6892.
31. Kruger M., Mennerich D., Fees S., Schafer R., Mundlos S., Braun T. Sonic hedgehog is a survival factor for hypaxial muscles during mouse development. Development 2001, 128:743-752.
32. Lee H.C., Huang H.Y., Lin C.Y., Chen Y.H., Tsai H.J. Foxd3 mediates zebrafish myf5 expression during early somitogenesis. Dev. Biol. 2006, 290:359-372.
33. von Maltzahn J., Chang N.C., Bentzinger C.F., Rudnicki M.A. Wnt signaling in myogenesis. Trends Cell Biol. 2012, 22:602-609.
34. Mansouri A., Hallonet M., Gruss P. Pax genes and their roles in cell differentiation and development. Curr. Opin. Cell Biol. 1996, 8:851-857.
35. Matise M.P., Epstein D.J., Park H.L., Platt K.A., Joyner A.L. Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development 1998, 125:2759-2770.
36. McDermott A., Gustafsson M., Elsam T., Hui C.C., Emerson C.P., Borycki A.G. Gli2 and Gli3 have redundant and context-dependent function in skeletal muscle formation. Development 2005, 132:345-357.
37. Merzdorf C.S. Emerging roles for zic genes in early development. Dev. Dyn. 2007, 236:922-940.
38. Mizugishi K., Aruga J., Nakata K., Mikoshiba K. Molecular properties of Zic proteins as transcriptional regulators and their relationship to GLI proteins. J. Biol. Chem. 2001, 276:2180-2188.
39. Mizugishi K., Hatayama M., Tohmonda T., Ogawa M., Inoue T., Mikoshiba K., Aruga J. Myogenic repressor I-mfa interferes with the function of Zic family proteins. Biochem. Biophys. Res. Commun. 2004, 320:233-240.
40. Nagai T., Aruga J., Takada S., Gunther T., Sporle R., Schughart K., Mikoshiba K. The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation. Dev. Biol. 1997, 182:299-313.
41. Nelson J.D., Denisenko O., Bomsztyk K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat. Protoc. 2006, 1:179-185.
42. Noll M. Evolution and role of Pax genes. Curr. Opin. Genet. Dev. 1993, 3:595-605.
43. Ott M.O., Bober E., Lyons G., Arnold H., Buckingham M. Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 1991, 111:1097-1107.
44. Pan H., Gustafsson M.K., Aruga J., Tiedken J.J., JC J.C., Emerson C.P. A role for Zic1 and Zic2 in Myf5 regulation and somite myogenesis. Dev. Biol. 2011, 351:120-127.
45. Park H.L., Bai C., Platt K.A., Matise M.P., Beeghly A., Hui C.C., Nakashima M., Joyner A.L. Mouse Gli1 mutants are viable but have defects in SHH signaling in combination with a Gli2 mutation. Development 2000, 127:1593-1605.
46. Pownall M.E., Gustafsson M.K., Emerson C.P. Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu. Rev. Cell Dev. Biol. 2002, 18:747-783.
47. Riobo N.A., Haines G.M., Emerson C.P. Protein kinase C-delta and mitogen-activated protein/extracellular signal-regulated kinase-1 control GLI activation in hedgehog signaling. Cancer Res. 2006, 66:839-845.
48. Rudnicki M.A., Braun T., Hinuma S., Jaenisch R. Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 1992, 71:383-390.
49. Salero E., Perez-Sen R., Aruga J., Gimenez C., Zafra F. Transcription factors Zic1 and Zic2 bind and transactivate the apolipoprotein E gene promoter. J. Biol. Chem. 2001, 276:1881-1888.
50. Sanyal A., Lajoie B.R., Jain G., Dekker J. The long-range interaction landscape of gene promoters. Nature 2012, 489:109-113.
51. Sasaki H., Nishizaki Y., Hui C., Nakafuku M., Kondoh H. Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of Shh signaling. Development 1999, 126:3915-3924.
52. Sato T., Sasai N., Sasai Y. Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. Development 2005, 132:2355-2363.
53. Sato T., Rocancourt D., Marques L., Thorsteinsdottir S., Buckingham M. A Pax3/Dmrt2/Myf5 regulatory cascade functions at the onset of myogenesis. PLoS Genet. 2010, 6:e1000897.
54. Summerbell D., Ashby P.R., Coutelle O., Cox D., Yee S., Rigby P.W. The expression of Myf5 in the developing mouse embryo is controlled by discrete and dispersed enhancers specific for particular populations of skeletal muscle precursors. Development 2000, 127:3745-3757.
55. Tajbakhsh S., Buckingham M.E. Mouse limb muscle is determined in the absence of the earliest myogenic factor myf-5. Proc. Natl. Acad. Sci. USA 1994, 91:747-751.
56. Teboul L., Hadchouel J., Daubas P., Summerbell D., Buckingham M., Rigby P.W. The early epaxial enhancer is essential for the initial expression of the skeletal muscle determination gene Myf5 but not for subsequent, multiple phases of somitic myogenesis. Development 2002, 129:4571-4580.
57. Teboul L., Summerbell D., Rigby P.W. The initial somitic phase of Myf5 expression requires neither Shh signaling nor Gli regulation. Genes Dev. 2003, 17:2870-2874.
58. Weintraub H., Davis R., Tapscott S., Thayer M., Krause M., Benezra R., Blackwell T.K., Turner D., Rupp R., Hollenberg S., et al. The myoD gene family: nodal point during specification of the muscle cell lineage. Science 1991, 251:761-766.
59. Williams B.A., Ordahl C.P. Pax-3 expression in segmental mesoderm marks early stages in myogenic cell specification. Development 1994, 120:785-796.
60. Yang Y., Hwang C.K., Junn E., Lee G., Mouradian M.M. ZIC2 and Sp3 repress Sp1-induced activation of the human D1A dopamine receptor gene. J. Biol. Chem. 2000, 275:38863-38869.
61. Zammit P.S., Carvajal J.J., Golding J.P., Morgan J.E., Summerbell D., Zolnerciks J., Partridge T.A., Rigby P.W., Beauchamp J.R. Myf5 expression in satellite cells and spindles in adult muscle is controlled by separate genetic elements. Dev. Biol. 2004, 273:454-465.