Hoxa-11 and Hoxa-13 are involved in repression of MyoD during limb muscle development

Development Growth and Differentiation

Volumn 45, Issue 5-6, 2003, Pages 485-498

  Yamamoto, Masakazu ^a,b   Kuroiwa, Atsushi ^a  

^a NAGOYA UNIVERSITY   (Japan)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Hoxa 11; Hoxa 13; Limb; Muscle; MyoD

Indexed keywords

HOX PROTEIN; MYOD PROTEIN; PROTEIN HOXA 11; PROTEIN HOXA 13; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARM MUSCLE; ARTICLE; CONTROLLED STUDY; ELECTROPORATION; EMBRYO; EMBRYO DEVELOPMENT; FLEXOR CARPI RADIALIS MUSCLE; FLEXOR MUSCLE; GENE DISRUPTION; GENE EXPRESSION REGULATION; LIMB DEVELOPMENT; MOUSE; MUSCLE DEVELOPMENT; MUSCLE MASS; MYOBLAST; NONHUMAN; PRECURSOR; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INDUCTION;

ANIMALS; BODY PATTERNING; CELL LINE; CHICK EMBRYO; CHICKENS; CODON; DNA, COMPLEMENTARY; ELECTROPORATION; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MUSCLES; MYOD PROTEIN; PROTEIN STRUCTURE, TERTIARY; TIME FACTORS; TRANSFECTION;

ANIMALIA;

EID: 0347319062     PISSN: 00121592     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1440-169X.2003.00715.x     Document Type: Article

References (62)

1. Amthor, H., Christ, B., Rashid-Doubell, F., Kemp, C. F., Lang, E. & Patel, K. 2002. Follistatin regulates bone morphogenetic protein-7 (BMP-7) activity to stimulate embryonic muscle growth. Dev. Biol. 243, 115-127.
2. Amthor, H., Christ, B., Weil, M. & Patel, K. 1998. The importance of timing differentiation during limb muscle development. Curr. Biol. 8, 642-652.
3. Bendall, A. J., Ding, J., Hu, G., Shen, M. M. & Abate-Shen, C. 1999. Msx1 antagonizes the myogenic activity of Pax3 in migrating limb muscle precursors. Development 126, 4965-4976.
4. Blau, H. M., Chiu, C. P. & Webster, C. 1983. Cytoplasmic activation of human nuclear genes in stable heterocaryons. Cell 32, 1171-1180.
5. Bober, E., Franz, T., Arnold, H. H., Gruss, P. & Tremblay, P. 1994. Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 120, 603-612.
6. Braissant, O. & Wahli, W. 1998. A simplified in situ hybridization protocol using non-radioactively labeled probes to detect abundant and rare mRNA on tissue sections. Biochemica 72, 10-16.
7. Branford, W. W., Benson, G. V., Ma, L., Maas, R. L. & Potter, S. S. 2000. Characterization of Hoxa-10/Hoxa-11 transheterozygotes reveals functional redundancy and regulatory interactions. Dev. Biol. 224, 373-387.
8. Buckingham, M., Bajard, L., Chang, T. et al. 2003. The formation of skeletal muscle: from somite to limb. J. Anat. 202, 59-68.
9. Chevallier, A., Kieny, M. & Mauger, A. 1977. Limb-somite relationship: origin of the limb musculature. J. Embryol. Exp. Morph. 41, 245-258.
10. Christ, B., Jacob, H. J. & Jacob, M. 1977. Experimental analysis of the origin of the wing musculature in avian embryos. Anat. Embryol. (Berl) 150, 171-186.
11. Christ, B. & Ordahl, C. P. 1995. Early stages of chick somite development. Anat. Embryol. (Berl) 191, 381-396.
12. Daston, G., Lamar, E., Olivier, M. & Goulding, M. 1996. Pax-3 is necessary for migration but not differentiation of limb muscle precursors in the mouse. Development 122, 1017-1027.
13. de la Brousse, F. C. & Emerson, C. P. Jr 1990. Localized expression of a myogenic regulatory gene, qmf1, in the somite dermatome of avian embryos. Genes Dev. 4, 567-581.
14. Delfini, M., Hirsinger, E., Pourquié, O. & Duprez, D. 2000. Delta 1-activated notch inhibits muscle differentiation without affecting Myf5 and Pax3 expression in chick limb myogenesis. Development 127, 5213-5224.
15. Dietrich, S., Schubert, F. R. & Lumsden, A. 1997. Control of dorsoventral pattern in the chick paraxial mesoderm. Development 124, 3895-3908.
16. Duboule, D. 1991. Patterning in the vertebrate limb. Curr. Opin. Genet. Dev. 1, 211-216.
17. Duboule, D. & Morata, G. 1994. Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet. 10, 358-364.
18. Duprez, D. 2002. Signals regulating muscle formation in the limb during embryonic development. Int. J. Dev. Biol. 46, 915-925.
19. Duprez, D., Fournier-Thibault, C. & Le Douarin, N. 1998. Sonic Hedgehog induces proliferation of committed skeletal muscle cells in the chick limb. Development 125, 495-505.
20. Fekete, D. M. & Cepko, C. L. 1993. Replication-competent retroviral vectors encoding alkaline phosphatase reveal spatial restriction of viral gene expression/transduction in the chick embryo. Mol. Cell Biol. 13, 2604-2613.
21. Fromental-Ramain, C., Warot, X., Messadecq, N., LeMeur, M., Dollé, P. & Chambon, P. 1996. Hoxa-13 and Hoxd-13 play a crucial role in the patterning of the limb autopod. Development 122, 2997-3011.
22. Fujisawa-Sehara, A., Nabeshima, Y., Hosoda, Y. & Obinata, T. 1990. Myogenin contains two domains conserved among myogenic factors. J. Biol. Chem. 265, 15 219-15 223.
23. Fujisawa-Sehara, A., Nabeshima, Y., Komiya, T., Uetsuki, T. & Asakura, A. 1992. Differential trans-activation of muscle-specific regulatory elements including the mysosin light chain box by chicken MyoD, myogenin, and MRF4. J. Biol. Chem. 267, 10 031-10 038.
24. Greig, S. & Akam, M. 1993. Homeotic genes autonomously specify one aspect of pattern in the Drosophila mesoderm. Nature 362, 630-632.
25. Haack, H. & Gruss, P. 1993. The establishment of murine Hox-1 expression domains during patterning of the limb. Dev. Biol. 157, 410-422.
26. Hashimoto, K., Yokouchi, Y., Yamamoto, M. & Kuroiwa, A. 1999. Distinct signaling molecules control Hoxa-11 and Hoxa-13 expression in the muscle precursor and mesenchyme of the chick limb bud. Development 126, 2771-2783.
27. Hayashi, K. & Ozawa, E. 1995. Myogenic cell migration from somites is induced by tissue contact with medial region of the presumptive limb mesoderm in chick embryos. Development 121, 661-669.
28. Houghton, L. & Rosenthal, N. 1999. Regulation of a muscle-specific transgene by persistent expression of Hox genes in postnatal murine limb muscle. Dev. Dyn. 216, 385-397.
29. Houzelstein, D., Auda-Boucher, G., Chéraud, Y. et al. 1999. The homeobox gene Msx1 is expressed in a subset of somites, and in muscle progenitor cells migrating into the forelimb. Development 126, 2689-2701.
30. Houzelstein, D., Cohen, A., Buckingham, M. E. & Robert, B. 1997. Insertional mutation of the mouse Msx1 homeobox gene by an nlacZ reporter gene. Mech. Dev. 65, 123-133.
31. Hughes, S. H., Greenhouse, J. J., Petropoulos, C. J. & Sutrave, P. 1987. Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. J. Virol. 61, 3004-3012.
32. Itoh, N., Mima, T. & Mikawa, T. 1996. Loss of fibroblast growth factor receptors is necessary for terminal differentiation of embryonic limb muscle. Development 122, 291-300.
33. Kablar, B., Krastel, K., Ying, C., Asakura, A., Tapscott, S. J. & Rudnicki, M. A. 1997. MyoD and Myf-5 differentially regulate the development of limb versus trunk skeletal muscle. Development 124, 4729-4738.
34. Kawakami, A., Kimura-Kawakami, M., Nomura, T. & Fujisawa, H. 1997. Distributions of PAX6 and PAX7 proteins suggest their involvement in both early and late phases of chick brain development. Mech. Dev. 66, 119-130.
35. Lin-Jones, J. & Hauschka, S. D. 1996. Myogenic determination factor expression in the developing avian limb bud: an RT-PCR analysis. Dev. Biol. 174, 407-422.
36. Maroto, M., Reshef, R., Münsterberg, A. E., Koester, S., Goulding, M. & Lassar, A. B. 1997. Ectopic Pax-3 activates MyoD and Myf-5 expression in embryonic mesoderm and neural tissue. Cell 89, 139-148.
37. McGinnis, W. & Krumlauf, R. 1992. Homeobox genes and axial patterning. Cell 68, 283-302.
38. Michelson, A. M. 1994. Muscle pattern diversification in Drosophila is determined by the autonomous function of homeotic genes in the embryonic mesoderm. Development 120, 755-768.
39. Momose, T., Tonegawa, A., Takeuchi, J., Ogawa, H., Umesono, K. & Yasuda, K. 1999. Efficient targeting of gene expression in chick embryos by microelectroporation. Dev. Growth Differ. 41, 335-344.
40. Niwa, H., Yamamura, K. & Miyazaki, J. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199.
41. Ogawa, H., Inouye, S., Tsuji, F. I., Yasuda, K. & Umesono, K. 1995. Localization, trafficking, and temperature-dependence of the Aequorea green fluorescent protein in cultured vertebrate cells. Proc. Natl Acad. Sci. USA 92, 11 899-11 903.
42. Ordahl, C. P. & Le Douarin, N. M. 1992. Two myogenic lineages within the developing somite. Development 114, 339-353.
43. Plaza, S., Prince, F., Jaeger, J. et al. 2001. Molecular basis for the inhibition of Drosophila eye development by Antennapedia. EMBO J. 20, 802-811.
44. Rijli, F. M. & Chambon, P. 1997. Genetic interactions of Hox genes in limb development: learning from compound mutants. Curr. Opin. Genet. Dev. 7, 481-487.
45. Robson, L. G., Kara, T., Crawley, A. & Tickle, C. 1994. Tissue and cellular patterning of the musculature in chick wings. Development 120, 1265-1276.
46. Roy, S. & VijayRaghavan, K. 1997. Homeotic genes and the regulation of myoblast migration, fusion, and fibre-specific gene expression during adult myogenesis in Drosophila. Development 124, 3333-3341.
47. Satokata, I. & Maas, R. 1994. Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat. Genet. 6, 348-356.
48. Scaal, M., Bonafede, A., Dathe, V. et al. 1999. SF/HGF is a mediator between limb patterning and muscle development. Development 126, 4885-4893.
49. Schramm, C. & Solursh, M. 1990. The formation of premuscle masses during chick wing bud development. Anat. Embryol. (Berl) 182, 235-247.
50. Shellswell, G. B. & Wolpert, L. 1977. The pattern of muscle and tendon development in the chick wing. In: Vertebrate Limb and Somite Morphgenesis (eds D. A. Ede, J. R. Hinchliffe & M. Balls). Cambridge: Cambridge University Press.
51. Shen, W. F., Krishnan, K., Lawrence, H. J. & Largman, C. 2001. The HOX homeodomain proteins block CBP histone acetyl-transferase activity. Mol. Cell Biol. 21, 7509-7522.
52. Song, K., Wang, Y. & Sassoon, D. 1992. Expression of Hox-7.1 in myoblasts inhibits terminal differentiation and induces cell transformation. Nature 360, 477-481.
53. Stadler, H. S., Higgins, K. M. & Capecchi, M. R. 2001. Loss of Eph-receptor expression correlates with loss of cell adhesion and chondrogenic capacity in Hoxa13 mutant limbs. Development 128, 4177-4188.
54. Swartz, M., Eberhart, J., Mastick, G. S. & Krull, C. E. 2001a. Sparking new frontiers: using in vivo electroporation for genetic manipulations. Dev. Biol. 233, 13-21.
55. Swartz, M. E., Eberhart, J., Pasquale, E. B. & Krull, C. E. 2001b. EphA4/ephrin-A5 interactions in muscle precursor cell migration in the avian forelimb. Development 128, 4669-4680.
56. Tajbakhsh, S. & Buckingham, M. E. 1994. Mouse limb muscle is determined in the absence of the earliest myogenic factor Myf-5. Proc. Natl Acad. Sci. USA 91, 747-751.
57. Tajbakhsh, S., Rocancourt, D., Cossu, G. & Buckingham, M. 1997. Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of. Myod. Cell 89, 127-138.
58. Woloshin, P., Song, K., Degnin, C. et al. 1995. MSX1 inhibits myoD expression in fibroblast x 10T1/2 cell hybrids. Cell 82, 611-620.
59. Yaffe, D. & Saxel, O. 1977. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270, 725-727.
60. Yamamoto, M., Gotoh, Y., Tamura, K. et al. 1998. Coordinated expression of Hoxa-11 and Hoxa-13 during limb muscle patterning. Development 125, 1325-1335.
61. Yokouchi, Y., Nakazato, S., Yamamoto, M. et al. 1995. Mis-expression of Hoxa-13 induces cartilage homeotic transformation and changes cell adhesiveness in chick limb buds. Genes Dev. 9, 2509-2522.
62. Yokouchi, Y., Sasaki, H. & Kuroiwa, A. 1991. Homeobox gene expression correlated with the bifurcation process of limb cartilage development. Nature 353, 443-445.