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. 1990 Oct 1;111(4):1623–1629. doi: 10.1083/jcb.111.4.1623

Regulation of proliferation and differentiation of myoblasts derived from adult mouse skeletal muscle by specific isoforms of PDGF

PMCID: PMC2116257  PMID: 2211828

Abstract

The expression of receptors and the mitogenic response to PDGF by C2 myoblasts, derived from adult mouse skeletal muscle, was investigated. Employing 125I-PDGF binding assays, we showed that the cells exhibit high level binding of PDGF-BB (approximately 165 x 10(3) molecules/cell at saturation) and much lower binding of the PDGF-AA and PDGF-AB (6-12 x 10(3) molecules/cell at saturation). This indicates that the C2 myoblasts express high levels of PDGF receptor beta-subunits and low levels of alpha-subunits. PDGF-BB enhances the proliferation of C2 cells maintained in 2% FCS by about fivefold. PDGF-AB had a moderate effect on cell proliferation (less than twofold) and PDGF-AA had no effect. Inverse effects of PDGF isoforms on the frequency of differentiated myoblasts were observed; the frequency of myosin- positive cells was reduced in the presence of PDGF-BB while PDGF-AA and PDGF-AB had no effect. PDGF may thus act to increase the number of myoblasts that participate in muscle regeneration following muscle trauma by stimulating the proliferation and by inhibiting the differentiation of myogenic cells.

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Selected References

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  1. Allen R. E., Boxhorn L. K. Regulation of skeletal muscle satellite cell proliferation and differentiation by transforming growth factor-beta, insulin-like growth factor I, and fibroblast growth factor. J Cell Physiol. 1989 Feb;138(2):311–315. doi: 10.1002/jcp.1041380213. [DOI] [PubMed] [Google Scholar]
  2. Allen R. E., Dodson M. V., Luiten L. S. Regulation of skeletal muscle satellite cell proliferation by bovine pituitary fibroblast growth factor. Exp Cell Res. 1984 May;152(1):154–160. doi: 10.1016/0014-4827(84)90239-8. [DOI] [PubMed] [Google Scholar]
  3. Bader D., Masaki T., Fischman D. A. Immunochemical analysis of myosin heavy chain during avian myogenesis in vivo and in vitro. J Cell Biol. 1982 Dec;95(3):763–770. doi: 10.1083/jcb.95.3.763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bischoff R. Analysis of muscle regeneration using single myofibers in culture. Med Sci Sports Exerc. 1989 Oct;21(5 Suppl):S164–S172. [PubMed] [Google Scholar]
  5. Bischoff R. Enzymatic liberation of myogenic cells from adult rat muscle. Anat Rec. 1974 Dec;180(4):645–661. doi: 10.1002/ar.1091800410. [DOI] [PubMed] [Google Scholar]
  6. Bischoff R. Proliferation of muscle satellite cells on intact myofibers in culture. Dev Biol. 1986 May;115(1):129–139. doi: 10.1016/0012-1606(86)90234-4. [DOI] [PubMed] [Google Scholar]
  7. Bowen-Pope D. F., Hart C. E., Seifert R. A. Sera and conditioned media contain different isoforms of platelet-derived growth factor (PDGF) which bind to different classes of PDGF receptor. J Biol Chem. 1989 Feb 15;264(5):2502–2508. [PubMed] [Google Scholar]
  8. Campion D. R. The muscle satellite cell: a review. Int Rev Cytol. 1984;87:225–251. doi: 10.1016/s0074-7696(08)62444-4. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. DiMario J., Strohman R. C. Satellite cells from dystrophic (mdx) mouse muscle are stimulated by fibroblast growth factor in vitro. Differentiation. 1988 Nov;39(1):42–49. doi: 10.1111/j.1432-0436.1988.tb00079.x. [DOI] [PubMed] [Google Scholar]
  11. Florini J. R., Magri K. A. Effects of growth factors on myogenic differentiation. Am J Physiol. 1989 Apr;256(4 Pt 1):C701–C711. doi: 10.1152/ajpcell.1989.256.4.C701. [DOI] [PubMed] [Google Scholar]
  12. Grotendorst G. R., Chang T., Seppä H. E., Kleinman H. K., Martin G. R. Platelet-derived growth factor is a chemoattractant for vascular smooth muscle cells. J Cell Physiol. 1982 Nov;113(2):261–266. doi: 10.1002/jcp.1041130213. [DOI] [PubMed] [Google Scholar]
  13. Hammacher A., Mellström K., Heldin C. H., Westermark B. Isoform-specific induction of actin reorganization by platelet-derived growth factor suggests that the functionally active receptor is a dimer. EMBO J. 1989 Sep;8(9):2489–2495. doi: 10.1002/j.1460-2075.1989.tb08385.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hart C. E., Forstrom J. W., Kelly J. D., Seifert R. A., Smith R. A., Ross R., Murray M. J., Bowen-Pope D. F. Two classes of PDGF receptor recognize different isoforms of PDGF. Science. 1988 Jun 10;240(4858):1529–1531. doi: 10.1126/science.2836952. [DOI] [PubMed] [Google Scholar]
  15. Hart I. K., Richardson W. D., Bolsover S. R., Raff M. C. PDGF and intracellular signaling in the timing of oligodendrocyte differentiation. J Cell Biol. 1989 Dec;109(6 Pt 2):3411–3417. doi: 10.1083/jcb.109.6.3411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Heldin C. H., Bäckström G., Ostman A., Hammacher A., Rönnstrand L., Rubin K., Nistér M., Westermark B. Binding of different dimeric forms of PDGF to human fibroblasts: evidence for two separate receptor types. EMBO J. 1988 May;7(5):1387–1393. doi: 10.1002/j.1460-2075.1988.tb02955.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Heldin C. H., Ernlund A., Rorsman C., Rönnstrand L. Dimerization of B-type platelet-derived growth factor receptors occurs after ligand binding and is closely associated with receptor kinase activation. J Biol Chem. 1989 May 25;264(15):8905–8912. [PubMed] [Google Scholar]
  18. Heldin C. H., Westermark B. Platelet-derived growth factors: a family of isoforms that bind to two distinct receptors. Br Med Bull. 1989 Apr;45(2):453–464. doi: 10.1093/oxfordjournals.bmb.a072334. [DOI] [PubMed] [Google Scholar]
  19. Jennische E., Skottner A., Hansson H. A. Satellite cells express the trophic factor IGF-I in regenerating skeletal muscle. Acta Physiol Scand. 1987 Jan;129(1):9–15. doi: 10.1111/j.1748-1716.1987.tb08034.x. [DOI] [PubMed] [Google Scholar]
  20. Jin P., Rahm M., Claesson-Welsh L., Heldin C. H., Sejersen T. Expression of PDGF A-chain and beta-receptor genes during rat myoblast differentiation. J Cell Biol. 1990 May;110(5):1665–1672. doi: 10.1083/jcb.110.5.1665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Moss F. P., Leblond C. P. Satellite cells as the source of nuclei in muscles of growing rats. Anat Rec. 1971 Aug;170(4):421–435. doi: 10.1002/ar.1091700405. [DOI] [PubMed] [Google Scholar]
  22. Raines E. W., Ross R. Platelet-derived growth factor. I. High yield purification and evidence for multiple forms. J Biol Chem. 1982 May 10;257(9):5154–5160. [PubMed] [Google Scholar]
  23. Ross R., Raines E. W., Bowen-Pope D. F. The biology of platelet-derived growth factor. Cell. 1986 Jul 18;46(2):155–169. doi: 10.1016/0092-8674(86)90733-6. [DOI] [PubMed] [Google Scholar]
  24. Saad A. D., Obinata T., Fischman D. A. Immunochemical analysis of protein isoforms in thick myofilaments of regenerating skeletal muscle. Dev Biol. 1987 Feb;119(2):336–349. doi: 10.1016/0012-1606(87)90039-x. [DOI] [PubMed] [Google Scholar]
  25. Schultz E., Albright D. J., Jaryszak D. L., David T. L. Survival of satellite cells in whole muscle transplants. Anat Rec. 1988 Sep;222(1):12–17. doi: 10.1002/ar.1092220104. [DOI] [PubMed] [Google Scholar]
  26. Schultz E., Gibson M. C., Champion T. Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J Exp Zool. 1978 Dec;206(3):451–456. doi: 10.1002/jez.1402060314. [DOI] [PubMed] [Google Scholar]
  27. Seifert R. A., Hart C. E., Phillips P. E., Forstrom J. W., Ross R., Murray M. J., Bowen-Pope D. F. Two different subunits associate to create isoform-specific platelet-derived growth factor receptors. J Biol Chem. 1989 May 25;264(15):8771–8778. [PubMed] [Google Scholar]
  28. Seppä H., Grotendorst G., Seppä S., Schiffmann E., Martin G. R. Platelet-derived growth factor in chemotactic for fibroblasts. J Cell Biol. 1982 Feb;92(2):584–588. doi: 10.1083/jcb.92.2.584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Snow M. H. Myogenic cell formation in regenerating rat skeletal muscle injured by mincing. II. An autoradiographic study. Anat Rec. 1977 Jun;188(2):201–217. doi: 10.1002/ar.1091880206. [DOI] [PubMed] [Google Scholar]
  30. Venkatasubramanian K., Solursh M. Chemotactic behavior of myoblasts. Dev Biol. 1984 Aug;104(2):428–433. doi: 10.1016/0012-1606(84)90098-8. [DOI] [PubMed] [Google Scholar]
  31. Watt D. J., Morgan J. E., Clifford M. A., Partridge T. A. The movement of muscle precursor cells between adjacent regenerating muscles in the mouse. Anat Embryol (Berl) 1987;175(4):527–536. doi: 10.1007/BF00309688. [DOI] [PubMed] [Google Scholar]
  32. Yablonka-Reuveni Z., Anderson S. K., Bowen-Pope D. F., Nameroff M. Biochemical and morphological differences between fibroblasts and myoblasts from embryonic chicken skeletal muscle. Cell Tissue Res. 1988 May;252(2):339–348. doi: 10.1007/BF00214376. [DOI] [PubMed] [Google Scholar]
  33. Yablonka-Reuveni Z., Nameroff M. Skeletal muscle cell populations. Separation and partial characterization of fibroblast-like cells from embryonic tissue using density centrifugation. Histochemistry. 1987;87(1):27–38. doi: 10.1007/BF00518721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Yablonka-Reuveni Z., Quinn L. S., Nameroff M. Isolation and clonal analysis of satellite cells from chicken pectoralis muscle. Dev Biol. 1987 Jan;119(1):252–259. doi: 10.1016/0012-1606(87)90226-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Yaffe D., Saxel O. Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature. 1977 Dec 22;270(5639):725–727. doi: 10.1038/270725a0. [DOI] [PubMed] [Google Scholar]
  36. Zadeh B. J., González-Sánchez A., Fischman D. A., Bader D. M. Myosin heavy chain expression in embryonic cardiac cell cultures. Dev Biol. 1986 May;115(1):204–214. doi: 10.1016/0012-1606(86)90241-1. [DOI] [PubMed] [Google Scholar]

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