Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1994 Jun;14(6):4244–4250. doi: 10.1128/mcb.14.6.4244

Myogenic differentiation triggered by antisense acidic fibroblast growth factor RNA.

J C Fox 1, A Y Hsu 1, J L Swain 1
PMCID: PMC358790  PMID: 7515150

Abstract

Acidic fibroblast growth factor (FGF) and related family members regulate differentiation in organisms as diverse as Xenopus laevis and mammals. We utilized a well-characterized model of myogenic development to directly assess the importance of endogenously produced FGF in controlling differentiation. A role for endogenous FGF is suggested by the previous finding that acidic and basic FGF abundance in cultured myocytes decreases during differentiation. In this study we inhibited the endogenous production of FGF in murine Sol 8 myoblasts by using antisense RNA and observed precocious myogenic differentiation. Exogenously supplied acidic FGF rescues this phenotype. Further results suggest that the effect of FGF on myogenic differentiation is mediated in part through inhibition of myogenin expression. These results demonstrate a direct role for endogenously synthesized growth factors in regulating myogenesis and provide support for a general role for related proteins in mammalian development.

Full text

PDF
4244

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alterio J., Courtois Y., Robelin J., Bechet D., Martelly I. Acidic and basic fibroblast growth factor mRNAs are expressed by skeletal muscle satellite cells. Biochem Biophys Res Commun. 1990 Feb 14;166(3):1205–1212. doi: 10.1016/0006-291x(90)90994-x. [DOI] [PubMed] [Google Scholar]
  2. Brunetti A., Goldfine I. D. Role of myogenin in myoblast differentiation and its regulation by fibroblast growth factor. J Biol Chem. 1990 Apr 15;265(11):5960–5963. [PubMed] [Google Scholar]
  3. Burgess W. H., Maciag T. The heparin-binding (fibroblast) growth factor family of proteins. Annu Rev Biochem. 1989;58:575–606. doi: 10.1146/annurev.bi.58.070189.003043. [DOI] [PubMed] [Google Scholar]
  4. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  5. Clegg C. H., Linkhart T. A., Olwin B. B., Hauschka S. D. Growth factor control of skeletal muscle differentiation: commitment to terminal differentiation occurs in G1 phase and is repressed by fibroblast growth factor. J Cell Biol. 1987 Aug;105(2):949–956. doi: 10.1083/jcb.105.2.949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cullen B. R. Trans-activation of human immunodeficiency virus occurs via a bimodal mechanism. Cell. 1986 Sep 26;46(7):973–982. doi: 10.1016/0092-8674(86)90696-3. [DOI] [PubMed] [Google Scholar]
  7. Edmondson D. G., Olson E. N. 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. 1989 May;3(5):628–640. doi: 10.1101/gad.3.5.628. [DOI] [PubMed] [Google Scholar]
  8. Eppenberger H. M., Dawson D. M., Kaplan N. O. The comparative enzymology of creatine kinases. I. Isolation and characterization from chicken and rabbit tissues. J Biol Chem. 1967 Jan 25;242(2):204–209. [PubMed] [Google Scholar]
  9. Fox J. C., Swain J. L. Auto and transactivation of FGF expression: potential mechanism for regulation of myogenic differentiation. In Vitro Cell Dev Biol. 1993 Mar;29A(3 Pt 1):228–230. doi: 10.1007/BF02634188. [DOI] [PubMed] [Google Scholar]
  10. Gospodarowicz D., Weseman J., Moran J. S., Lindstrom J. Effect of fibroblast growth factor on the division and fusion of bovine myoblasts. J Cell Biol. 1976 Aug;70(2 Pt 1):395–405. doi: 10.1083/jcb.70.2.395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Groux-Muscatelli B., Bassaglia Y., Barritault D., Caruelle J. P., Gautron J. Proliferating satellite cells express acidic fibroblast growth factor during in vitro myogenesis. Dev Biol. 1990 Dec;142(2):380–385. doi: 10.1016/0012-1606(90)90358-p. [DOI] [PubMed] [Google Scholar]
  12. Hébert J. M., Basilico C., Goldfarb M., Haub O., Martin G. R. Isolation of cDNAs encoding four mouse FGF family members and characterization of their expression patterns during embryogenesis. Dev Biol. 1990 Apr;138(2):454–463. doi: 10.1016/0012-1606(90)90211-z. [DOI] [PubMed] [Google Scholar]
  13. Kimelman D., Kirschner M. W. An antisense mRNA directs the covalent modification of the transcript encoding fibroblast growth factor in Xenopus oocytes. Cell. 1989 Nov 17;59(4):687–696. doi: 10.1016/0092-8674(89)90015-9. [DOI] [PubMed] [Google Scholar]
  14. Lathrop B., Olson E., Glaser L. Control by fibroblast growth factor of differentiation in the BC3H1 muscle cell line. J Cell Biol. 1985 May;100(5):1540–1547. doi: 10.1083/jcb.100.5.1540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Linkhart T. A., Clegg C. H., Hauschka S. D. Control of mouse myoblast commitment to terminal differentiation by mitogens. J Supramol Struct. 1980;14(4):483–498. doi: 10.1002/jss.400140407. [DOI] [PubMed] [Google Scholar]
  16. Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Montarras D., Pinset C., Chelly J., Kahn A., Gros F. Expression of MyoD1 coincides with terminal differentiation in determined but inducible muscle cells. EMBO J. 1989 Aug;8(8):2203–2207. doi: 10.1002/j.1460-2075.1989.tb08343.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Moore J. W., Dionne C., Jaye M., Swain J. L. The mRNAs encoding acidic FGF, basic FGF and FGF receptor are coordinately downregulated during myogenic differentiation. Development. 1991 Mar;111(3):741–748. doi: 10.1242/dev.111.3.741. [DOI] [PubMed] [Google Scholar]
  19. Sassoon D. A., Garner I., Buckingham M. Transcripts of alpha-cardiac and alpha-skeletal actins are early markers for myogenesis in the mouse embryo. Development. 1988 Sep;104(1):155–164. doi: 10.1242/dev.104.1.155. [DOI] [PubMed] [Google Scholar]
  20. Slack J. M., Darlington B. G., Heath J. K., Godsave S. F. Mesoderm induction in early Xenopus embryos by heparin-binding growth factors. Nature. 1987 Mar 12;326(6109):197–200. doi: 10.1038/326197a0. [DOI] [PubMed] [Google Scholar]
  21. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke N. M., Olson B. J., Klenk D. C. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985 Oct;150(1):76–85. doi: 10.1016/0003-2697(85)90442-7. [DOI] [PubMed] [Google Scholar]
  22. Spizz G., Roman D., Strauss A., Olson E. N. Serum and fibroblast growth factor inhibit myogenic differentiation through a mechanism dependent on protein synthesis and independent of cell proliferation. J Biol Chem. 1986 Jul 15;261(20):9483–9488. [PubMed] [Google Scholar]
  23. Terrell G. E., Swain J. L. Indirect angiogenic agents do not release fibroblast growth factors from extracellular matrix. Matrix. 1991 Apr;11(2):108–114. doi: 10.1016/s0934-8832(11)80214-3. [DOI] [PubMed] [Google Scholar]
  24. Vaidya T. B., Rhodes S. J., Taparowsky E. J., Konieczny S. F. Fibroblast growth factor and transforming growth factor beta repress transcription of the myogenic regulatory gene MyoD1. Mol Cell Biol. 1989 Aug;9(8):3576–3579. doi: 10.1128/mcb.9.8.3576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Yutzey K. E., Rhodes S. J., Konieczny S. F. Differential trans activation associated with the muscle regulatory factors MyoD1, myogenin, and MRF4. Mol Cell Biol. 1990 Aug;10(8):3934–3944. doi: 10.1128/mcb.10.8.3934. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES