Inactivation of the myogenic bHLH gene MRF4 results in up-regulation of myogenin and rib anomalies

Genes and Development

Volumn 9, Issue 11, 1995, Pages 1388-1399

  Zhang, Wei ^a   Behringer, Richard R ^a   Olson, Eric N ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

basic helix loop helix; muscle gene expression; Myogenesis

Indexed keywords

HELIX LOOP HELIX PROTEIN; MYOGENIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RIB MALFORMATION; SOMITE;

ANIMALIA;

EID: 0029047267     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.9.11.1388     Document Type: Article

References (68)

1. Black, B., J. Martin, and E.N. Olson. 1995. The mouse MRF4 promoter is transactivated directly and indirectly by muscle-specific transcription factors. J. Biol. Chem. 270: 2889-2892.
2. Bober, E., G.E. Lyons, T. Braun, G. Cossu, M. Buckingham, and H.H. Arnold. 1991. The muscle regulatory gene, Myf-6, has a biphasic pattern of expression during early mouse development. J. Cell Biol. 113: 1255-1265.
3. Braun, T. and H.H. Arnold. 1995. Inactivation of Myf-6 and Myf-5 genes in mice leads to alterations in skeletal muscle development. EMBO J. 14: 1176-1186.
4. Braun, T., G. Buschhausen-Denker, E. Bober, E. Tannich, and H.H. Arnold. 1989. A novel human muscle factor related to but distinct from MyoD1 induces myogenic conversion in 10T1/2 fibroblasts. EMBO J. 8: 701-709.
5. Braun, T., E. Bober, B. Winter, N. Rosenthal, and H.H. Arnold. 1990. Myf-6, a new member of the human gene family of myogenic determination factors: Evidence for a gene cluster on chromosome 12. EMBO J. 9: 821-831.
6. Braun, T., M.A. Rudnicki, H.H. Arnold, and R. Jaenisch. 1992. Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 71: 369-382.
7. Braun, T., E. Bober, M.A. Rudnicki, R. Jaenisch, and H.H. Arnold. 1994. MyoD expression marks the onset of skeletal myogenesis in Myf-5 mutant mice. Development 120: 3083-3092.
8. Breitbart, R.E. and B. Nadal-Ginard. 1987. Developmentally induced, muscle-specific trans factors control the differential splicing of alternative and constitutive troponin T exons. Cell 49: 793-803.
9. Buckingham, M. 1992. Making muscle in mammals. Trends Genet. 8: 144-148.
10. Buskin, J.N., J.B. Jaynes, J.S. Chamberlain, and S.D. Hauschka. 1985. The mouse muscle creatine kinase cDNA and deduced amino acid sequences: Comparison to evolutionarily related enzymes. J. Mol. Evol. 22: 334-341.
11. Chakraborty, T. and E.N. Olson. 1991. Domains outside of the DNA-binding domain impart target gene specificity to myogenin and MRF4. Mol. Cell. Biol. 11: 6103-6108.
12. Chakraborty, T., T.J. Brennan, and E.N. Olson. 1991. Differential trans-activation of a muscle-specific enhancer by myogenic helix-loop-helix proteins is separable from DNA binding. J. Biol. Chem. 266: 2878-2882.
13. Cheng, T.-C., M. Wallace, J.P. Merlie, and E.N. Olson. 1993. Separable regulatory elements govern myogenin transcription in embryonic somites and limb buds. Science 261: 215-218.
14. Chevallier, A., M. Kieny, and A. Mauger. 1977. Limb-somite relationship. Origin of the limb musculature. J. Embryol. Exp. Morphol. 41: 245-258.
15. Christ, B., H. Jacob, and M. Jacob. 1977. Experimental analysis of the origin of the wing musculature in avian embryos. Anat. Embryol. 150: 171-186.
16. Cserjesi, P., D. Brown, K.L. Ligon, G. Lyons, N.G. Copeland, D.J. Gilbert, N.A. fenkins, and E.N. Olson. 1995. Scleraxis: A basic-helix-loop-helix protein that prefigures skeletal formation during mouse embryogenesis. Development 121: 1099-1110.
17. Davis, R.L., H. Weintraub, and A.B. Lassar. 1987. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51: 987-1000.
18. DeNardi, C., S. Ausoni, P. Moretti, L. Gorza, M. Velleca, M. Buckingham, and S. Schiaffino. 1993. Type 2X-myosin heavy chain is coded by a muscle fiber type-specific and developmentally regulated gene. J. Cell Biol. 123: 823-835.
19. Edmondson, D.G. and E.N. Olson. 1989. A gene with homology to the myc similarity region of MyoD1 is expressed during myogenesis and is sufficient to activate the muscle differentiation program. Genes & Dev. 3: 628-640.
20. Edmondson, D.G., T.-C. Cheng, P. Cserjesi, T. Chakraborty, and E.N. Olson. 1992. Analysis of the myogenin promoter reveals an indirect pathway for positive autoregulation mediated by the muscle-specific enhancer factor MEF-2. Mol. Cell. Biol. 12: 3665-3677.
21. Eftemie, R., H.R. Brenner, and A. Buonanno. 1991. Myogenin and MyoD join a family of skeletal muscle genes regulated by electrical activity. Proc. Natl. Acad. Sci. 88: 1349-1353.
22. Emerson, C.P., Jr. 1990. Myogenesis and developmental control genes. Curr. Opin. Genet. Dev. 2: 21065-21075.
23. Fort, P., L. Marty, M. Piechaczyk, S. el Sabrouty, C. Dani, P. Jeantuer, and J.M. Blanchard. 1985. Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res. 13: 1431-1442.
24. Fujisawa-Sehara, A., Y. Nabeshima, T. Komiya, T. Uetsuki, A. Asakura, and Y.-I. Nabeshima. 1992. Differential trans-activation of muscle-specific regulatory elements including the myosin light chain box by chicken MyoD, myogenin, and MRF4. J. Biol Chem. 267: 10031-10038.
25. Garner, I., D. Sassoon, J. Vandekerckhove, S. Alonso, and M. Buckingham. 1989. A developmental study of the abnormal expression of α-cardiac and α-skeletal actins in the striated muscle of a mutant mouse. Dev. Biol. 134: 236-245.
26. Hannon, K., C.K. Smith, K.R. Bales, and R.F. Santerre. 1992. Temporal and quantitative analysis of myogenic regulatory and growth factor gene expression in the developing mouse embryo. Dev. Biol. 151: 137-144.
27. Hasty, P., A. Bradley, J.H. Morris, J.M. Venuti, and E.N. Olson. 1993. Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene. Nature 364: 501-506.
28. Hinterberger, T.J., D.A. Sassoon, S.J. Rhodes, and S.F. Konieczny. 1991. Expression of the muscle regulatory factor MRF4 during somite and skeletal myofiber development. Dev. Biol. 147: 144-156.
29. Hollenberg, S.M., P.F. Cheng, and H. Weintraub. 1993. Use of a conditional MyoD transcription factor in studies of MyoD trans-activation and muscle determination. Proc. Natl. Acad. Sci. 90: 8028-8032.
30. Hu, M.C.T., S.B. Sharp, and N. Davidson. 1986. The complete sequence of the mouse skeletal α-actin gene reveals several conserved and inverted repeat sequences outside of the protein coding region. Mol Cell. Biol. 6: 15-25.
31. Hughes, S.M., J.M. Taylor, S.J. Tapscott, C.M. Gurley, W.J. Carter, and C.A. Peterson. 1993. Selective accumulation of MyoD and myogenin mRNAs in fast and slow adult skeletal muscle is controlled by innervation and hormones. Development 118: 1137-1147.
32. Jan, Y.N. and L.Y. Jan. 1993. HLH proteins, fly neurogenesis, and vertebrate myogenesis. Cell 75: 827-830.
33. Jennings, C.G.B. 1992. Expression of the myogenic gene MRF4 during Xenopus development. Dev. Biol. 150: 121-132.
34. Koppe, R.I., P.L. Hallauer, G. Karpati, and K.E.M. Hastings. 1989. cDNA clone and expression analysis of rodent fast and slow troponin I mRNAs. J. Biol. Chem. 264: 14327-14333.
35. LaPolla, R.D., K.M. Mayne, and N. Davidson. 1984. Isolation and characterization of a cDNA clone for the complete protein coding region of the delta subunit of the mouse acetylcholine receptor. Proc. Natl. Acad. Sci. 81: 7970-7974.
36. Lyons, G.E., S. Schiaffino, D.A. Sassoon, P. Barton, and M. Buckingham. 1990. Developmental regulation of myosin gene expression in mouse cardiac muscle. J. Cell Biol. 111: 2427-2436.
37. Maier, A., L. Gorza, S. Schiaffino, and D. Pette. 1988. A combined histochemical and immunohistochemical study on the dynamics of fast-to-slow fiber transformation in chronically stimulated rabbit muscle. Cell Tissue Res. 254: 59-68.
38. Mak, K.-L., R.Q. To, Y. Kong, and S.F. Konieczny. 1992. The MRF4 activation domain is required to induce muscle-specific gene expression. Mol. Cell. Biol. 12: 4334-4346.
39. Mansour, S.L., K.R. Thomas, and M.R. Capecchi. 1988. Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: A general strategy for targeting mutations to non-selectable genes. Nature 336: 348-352.
40. Martin, J.F., J.M. Miano, C.M. Hustad, N.G. Copeland, N.A. Jenkins, and E.N. Olson. 1994. A Mef2 gene that generates a muscle-specific isoform via alternative mRNA splicing. Mol. Cell. Biol. 14: 1647-1656.
41. McMahon, A.P. and A. Bradley. 1990. The Wnt-1 (int-1) protooncogene is required for development of a large region of the mouse brain. Cell 62: 1073-1085.
42. Medford, R.M., R.M. Wydro, H.T. Nguyen, and B. Nadal-Ginard. 1980. Cystoplasmic processing of myosin heavy chain messenger RNA: Evidence provided by using a recombinant DNA plasmid. Proc. Natl. Acad. Sci. 77: 5749-5753.
43. Miller-Hance, W.C., M. LaCorbiere, SJ. Fuller, S.M. Evans, G. Lyons, C. Schmidt, J. Robbins, and K.R. Chien, K.R. 1993. In vitro chamber specification during embryonic stem cell cardiogenesis. J. Biol. Chem. 268: 25244-25252.
44. Miner, J.H. and B.J. Wold. 1990. Herculin, a fourth member of the MyoD family of myogenic regulatory genes. Proc. Natl. Acad. Sci. 87: 1089-1093.
45. Minty, A.J., S. Alonso, M. Caravatti, and M.E. Buckingham. 1982. A fetal skeletal muscle actin mRNA in the mouse and its identity with cardiac actin mRNA. Cell 30: 185-192.
46. Nabeshima, Y.K., K. Hanaoka, M. Hayasaka, S. Esumi, S. Li, and I. Nonaka. 1993. Myogenin gene disruption results in perinatal lethality because of severe muscle defect. Nature 364: 532-535.
47. Olson, E.N. 1990. The MyoD family, a paradigm for development? Genes & Dev. 4: 1454-1461.
48. Olson, E.N. and W.H. Klein. 1994. bHLH factors in muscle development: Dead lines and commitments, what to leave in and what to leave out. Genes & Dev. 8: 1-8.
49. Ott, M.-O., E. Bober, G.E. Lyons, H.H. Arnold, and M. Buckingham. 1991. Early expression of the myogenic regulatory gene, myf5, in precursor cells of skeletal muscle in the mouse embryo. Development 111: 1097-1107.
50. Ramirez-Solis, R., J. Rivera-Pérez, J.D. Wallace, M. Wims, H. Zheng, and A. Bradley. 1992. Genomic DNA microextraction: A method to screen numerous samples. Anal. Biochem. 201:331-335.
51. Rhodes, S.J. and S.F. Konieczny. 1989. Identification of MRF4: A new member of the muscle regulatory factor gene family. Genes & Dev. 3: 2050-2061.
52. Rudnicki, M.A., T. Braun, S. Hinuma, and R. Jaenisch. 1992. Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71: 383-390.
53. Rudnicki, M.A., P.N.J. Schnegelsberg, R.H. Stead, T. Braun, H.H. Arnold, and R. Jaenisch. 1993. MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75: 1351-1359.
54. Rugh, R. 1990. Organogeny. In The mouse, its reproduction and development, pp. 220-222. Oxford University Press, New York.
55. Sassoon, D.A., I. Garner, and M. Buckingham. 1988. Transcripts of alpha-cardiac and alpha-skeletal actins are early markers for myogenesis in the mouse embryo. Development 104: 155-164.
56. Sassoon, D.A., G.E. Lyons, W.E. Wright, V.K. Lin, A.B. Lassar, H. Weintraub, and M. Buckingham. 1989. Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis. Nature 341: 303-307.
57. Schiaffino, S., L. Gorza, S. Sartore, L. Saggin, and M. Carli. 1986. Embryonic myosin heavy chain as a differentiation marker of developing human skeletal muscle and rhabdomyosarcoma. A monoclonal antibody study. Exp. Cell Res. 163:211-220.
58. Schiaffino, S., L. Gorza, S. Sartore, L. Saggin, S. Ausoni, M. Vianello, K. Gundersen, and T. Lomo. 1989. Three myosin heavy chain isoforms in type 2 skeletal muscle fibers. J. Muscle Res. Cell Motil. 10: 197-205.
59. Smith, T.H., A.M. Kachinsky, and J.B. Miller. 1994. Somite subdomains, muscle cell origins, and the four muscle regulatory factor proteins. J. Cell Biol. 127: 95-105.
60. Sunyer, T. and J.P. Merlie. 1993. Cell type- and differentiation-dependent expression from the mouse acetylcholine receptor ε-subunit promoter. J. Neurosci. Res. 36: 224-234.
61. Tajbakhsh, S. and M. Buckingham. 1994. Mouse limb muscle is determined in the absence of the earliest myogenic factor myf-5. Proc. Natl. Acad. Sci. 91: 747-751.
62. Venuti, J.M., J.S. Morris, J.L. Vivian, E.N. Olson, and W.H. Klein. 1995. Myogenin is required for late but not early aspects of myogenesis during mouse development. J. Cell Biol. 128: 563-576.
63. Wachtler, F. and B. Christ. 1992. The basic embryology of skeletal muscle formation in vertebrates: The avian model. Semin. Dev. Biol. 3: 217-227.
64. Weintraub, H. 1993. The MyoD family and myogenesis: Redundancy, networks, and thresholds. Cell 75: 1241-1244.
65. Weintraub, H., R.L. Davis, S.J. Tapscott, M. Thayer, M. Krause, R. Benezra, K.T. Blackwell, D. Turner, R. Rupp, S.M. Hollenberg, Y. Zhuang, and A.B. Lassar. 1991. The myoD gene family: Nodal point during specification of the muscle cell lineage. Science 251: 761-766.
66. Weydert, A., P. Barton, A.J. Harris, C. Pinset, and M. Buckingham. 1987. Developmental pattern of mouse skeletal myosin heavy chain gene transcripts in vivo and in vitro. Cell 49: 121-129.
67. Wright, W.E., D.A. Sassoon, and V.K. Lin. 1989. Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell 56: 607-617.
68. Yutzey, K.E., S.J. Rhodes, and S.F. Konieczny. 1990. Differential trans-activation associated with the muscle regulatory factors MyoD1, myogenin and MRF4. Mol. Cell. Biol. 10: 3934-3944.