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Expression of myosin heavy chain and of myogenic regulatory factor genes in fast or slow rabbit muscle satellite cell cultures

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Summary

We investigated the myogenic properties of rabbit fast or slow muscle satellite cells during their differentiation in culture, with a particular attention to the expression of myosin heavy chain and myogenic regulatory factor genes. Satellite cells were isolated from Semimembranosus proprius (slow-twitch muscle; 100% type I fibres) and Semimembranosus accessorius (fast-twitch muscle; almost 100% type II fibres) muscles of 3-month-old rabbits. Satellite cells in culture possess different behaviours according to their origin. Cells isolated from slow muscle proliferate faster, fuse earlier into more numerous myotubes and mature more rapidly into striated contractile fibres than do cells isolated from fast muscle. This pattern of proliferation and differentiation is also seen in the expression of myogenic regulatory factor genes. Myf5 is detected in both fast or slow 6-day-old cell cultures, when satellite cells are in the exponential stage of proliferation. MyoD and myogenin are subsequently detected in slow satellite cell cultures, but their expression in fast cell cultures is delayed by 2 and 4 days respectively. MRF4 is detected in both types of cultures when they contain striated and contractile myofibres. Muscle-specific myosin heavy chains are expressed earlier in slow satellite cell cultures. No adult myosin heavy chain isoforms are detected in fast cell cultures for 13 days, whereas cultures from slow cells express neonatal, adult slow and adult fast myosin heavy chain isoforms at that time. In both fast and slow satellite cell cultures containing striated contractile fibres, neonatal and adult myosin heavy chain isoforms are coexpressed. However, cultures made from satellite cells derived from slow muscles express the slow myosin heavy chain isoform, in addition to the neonatal and the fast isoforms. These results are further supported by the expression of the mRNA encoding the adult myosin heavy chain isoforms. These data provide further evidence for the existence of satellite cell diversity between two rabbit muscles of different fibre-type composition, and also suggest the existence of differently preprogrammed satellite cells.

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References

  • AIGNER, S., GOHLSCH, B., HäMäLäINEN, N., STARON, R. S., UBER, A., WEHRLE, U. & PETTE, D. (1993) Fast myosin heavy chain diversity in skeletal muscles of the rabbit: heavy chain IId, not IIb predominates. Eur. J. Biochem. 211, 367–72.

    Google Scholar 

  • ALBAGLI-CURIEL, O., CARNAC, G., VANDROMME, M., VINCENT, S., CRéPIEUX, P. & BONNIEU, A. (1993) Serum-induced inhibition of myogenesis is differentially relieved by retinoic acid and triiodithyronine in C2 murine muscle cells. Differentiation 52, 201–10.

    Google Scholar 

  • ALLBROOK, D. B. (1981) Skeletal muscle regeneration. Muscle Nerve 4, 234–45.

    Google Scholar 

  • BACOU, F. & NOUGUèS, J. (1980) Alterations of enzymatic activities during red and white muscle differentiation in vitro. Exp. Cell. Res. 129, 455–60.

    Google Scholar 

  • BACOU, F. & VIGNERON, P. (1988) Propriétés des fibres musculaires squelettiques. 1. Influence de l'innervation motrice. Reprod. Nutr. Develop. 28, 1387–453.

    Google Scholar 

  • BACOU, F., VIGNERON, P. & MASSOULIé, J. (1982) Acetylcholinesterase forms in fast and slow rabbit muscle. Nature 296, 661–4.

    Google Scholar 

  • BARJOT, C., JBILO, O., CHATONNET, A. & BACOU, F. (1993) Expression of acetylcholinesterage gene during in vitro differentiation of rabbit muscle satellite cells. Neuromusc. Disord. 3, 443–6.

    Google Scholar 

  • BISCHOFF, R. (1974) Enzymatic liberation of myogenic cells from adult rat muscle. Anat. Rec. 180, 645–62.

    Google Scholar 

  • BISCHOFF, R. (1986) A satellite cell mitogen from crushed adult muscle. Dev. Biol. 115, 140–7.

    Google Scholar 

  • BISCHOFF, R. (1990) Interaction between satellite cells and skeletal muscle fibres. Development 109, 943–52.

    Google Scholar 

  • BLAU, H. M. & WEBSTER, C. (1981) Isolation and characterization of human muscle cells. Proc. Natl. Acad. Sci. USA 78, 5623–7.

    Google Scholar 

  • BULLER, A. J., ECCLES, J. C. & ECCLES, R. M. (1960) Interactions between motoneurones and muscles in respect of the characteristic speeds of their responses. J. Physiol. 150, 417–39.

    Google Scholar 

  • CAMPION, D. R. (1984) The muscle satellite cells: a review. Int. Rev. Cytol. 87, 225–51.

    Google Scholar 

  • CARNAC, G., ALBAGLI-CURIEL, O., LEVIN, A. & BONNIEU, A. (1993) 9-cis-retinoic acid regulates the expression of the muscle determination gene myf5. Endocrinology 133, 2171–6.

    Google Scholar 

  • CATHALA, G., SAVOURET, J. F., MENDEZ, B., WEST, B. L., KARIN, M., MARTIAL, J. A. & BAXTER, J. D. (1983) A method for isolation of intact, translationally active ribonucleic acid. DNA 2, 329–35.

    Google Scholar 

  • CHOMCZYNSKI, P. & SCCCHI, N. (1987) Single-step method of RNA isolation by acid guanidium thiocyanatephenol-chlorophorm extraction. Anal. Biochem. 162, 156–9.

    Google Scholar 

  • CLOSE, R. (1972) Dynamic properties of mammalian skeletal muscles. Physiol. Rev. 52, 129–97.

    Google Scholar 

  • COSSU, G., ZANI, B., COLETTA, M., BOUCHè, M., PACIFICI, M. & MOLINARO, M. (1980) In vitro differentiation of satellite cells isolated from normal and dystrophic mammalian muscles. A comparison with embryonic myogenic cells. Cell. Diff 9, 357–68.

    Google Scholar 

  • CROW, M. T. & STOCKDALE, F. E. (1986a) Myosin expression and specialization among the earliest muscle fibers of the developing avian limb. Dev. Biol. 113, 238–54.

    Google Scholar 

  • CROW, M. T. & STOCKDALE, F. E. (1986b) The developmental program of fast myosin heavy chain expression in avian skeletal muscles. Dev. Biol. 118, 333–42.

    Google Scholar 

  • DAVIS, R. L., WEINTRAUB, H. & LASSAR, A. B. (1987) Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51, 987–1000.

    Google Scholar 

  • Di, MARIO, J. X., FERNYAK, S. E. & STOCKDALE, F. E. (1993) Myoblasts transferred to the limbs of embryos are committed to specific fibre fates. Nature 362, 165–7.

    Google Scholar 

  • DODSON, M. V., MARTIN, E. L., BRANNON, M. A., MATHISON, B. A. & McFARLAND, D. C. (1987) Optimization of bovine satellite cell-derived myotube formation in vitro. Tissue & Cell 19, 159–66.

    Google Scholar 

  • DüSTERHöFT, S. & PETTE, D. (1993) Satellite cells from slow rat muscle express slow myosin under appropriate culture conditions. Differentiation 53, 25–33.

    Google Scholar 

  • DüSTERHöFT, S., YABLONKA-REUVENI, Z. & PETTE, D. (1990) Characterization of myosin isoforms in satellite cell cultures from adult rat diaphragm, soleus and tibialis anterior muscles. Differentiation 45, 185–91.

    Google Scholar 

  • EDMONSON, D. G. & OLSON, E. N. (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, 628–40.

    Google Scholar 

  • EDOM, F., MOULY, V., BARBET, J. P., FISZMAN, M. & BUTLER-BROWNE, G. S. (1994) Clones of human satellite cells can express in vitro both fast and slow myosin heavy chains. Dev. Biol. 164, 219–29.

    Google Scholar 

  • EMERSON, C. P. (1993) Skeletal myogenesis: genetics and embryology to the fore. Curr. Opin. Gen. Dev. 3, 265–74.

    Google Scholar 

  • FELDMAN, J. L. & STOCKDALE, F. E. (1991) Skeletal muscle satellite cell diversity: satellite cells form fibers of different types in cell culture. Dev. Biol. 143, 320–34.

    Google Scholar 

  • FELDMAN, J. L. & STOCKDALE, F. E. (1992) Temporal appearance of satellite cells during myogenesis. Dev. Biol. 153, 217–26.

    Google Scholar 

  • GIBSON, M. C. & SCHULTZ, E. (1982) The distribution of satellite cells and their relationship to specific fiber types in soleus and extensor digitorum longus muscles. Anat. Rec. 202, 329–37.

    Google Scholar 

  • GIBSON, M. C. & SCHULTZ, E. (1983) Age-related differences in absolute numbers of skeletal muscle satellite cells. Muscle Nerve 6, 574–80.

    Google Scholar 

  • GROUX-MUSCATELLI, B., BASSAGLIA, Y., BARRITAULT, D., CARUELLE, J. P. & GAUTRON, J. (1990) Proliferating satellite cells express acidic fibroblast growth factor during in vitro myogenesis. Dev. Biol. 142, 380–5.

    Google Scholar 

  • HARTLEY, R. S., BANDMAN, E. & YABLONKA-REUVENI, Z. (1992) Skeletal muscle satellite cells appear during late chicken embryogenesis. Dev. Biol. 153, 206–16.

    Google Scholar 

  • KELLY, A. M. (1978) Satellite cells and myofiber growth in the rat soleus and digitorum longus muscles Dev. Biol. 65, 1–10.

    Google Scholar 

  • Le, MOIGNE, A., MARTELLY, I., BARLOVATZ-MEIMON, G., FRANQUINET, R., AAMIRI, A., FRISDAL, E., BASSAGLIA, Y., MORACZEWSKI, G. & GAUTRON, J. (1990) Characterization of myogenesis from adult satellite cells cultured in vitro. Int. J. Dev. Biol. 34, 171–80.

    Google Scholar 

  • LOWRY, O. H., ROSEBROUGH, N. J., FARR, A. L. & RANDALL, R. J. (1951) Protein measurement with folin phenol reagent. J. Biol. Chem. 193, 265–75.

    Google Scholar 

  • MARINI, J.-F., PONS, F., ANOAL, M., J., Léger & J. J., Léger (1989) Anti-myosin heavy chain monoclonal antibodies reveal two IIB (fast) fiber subtypes. J. Histochem. Cytochem. 37, 1721–9.

    Google Scholar 

  • MAURO, A. (1961) Satellite cell of skeletal muscle fibers. J. Biophys. Biochem. Cytol. 9, 493–5.

    Google Scholar 

  • McCORMICK, K. M. & THOMAS, D. P. (1992) Exercice-induced satellite cell activation in senescent soleus muscle. J. Appl. Physiol. 72, 888–93.

    Google Scholar 

  • MONTARRAS, D., CHELLY, J., BOBER, E., ARNOLD, H., OTT, M. O., GROS, F. & PINSET, C. (1991) Developmental pattern in the expression of myf5, myoD, myogenin and MRF4 during myogenesis. New. Biol. 3, 592–601.

    Google Scholar 

  • MOSS, F. P. & LEBLOND, C. P. (1970) Nature of dividing nuclei in skeletal muscle of growing rats. J. Cell. Biol. 4, 459–62.

    Google Scholar 

  • NOUGUèS, J. & BACOU, F. (1977) Enzymatic activities of muscle fibres differentiated, in vitro, from pectoralis major (white) and adductor magnus (red) muscles of chick embryos. Experientia 33, 714–15.

    Google Scholar 

  • OLSON, E. N. & KLEIN, W. H. (1993) bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev. 8, 1–8.

    Google Scholar 

  • PETTE, D. & VRBOVá, G. (1992) Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev. Physiol. Biochem. Pharmacol. 120, 116–202.

    Google Scholar 

  • REZNIK, M. (1976) Origin of the myogenic cell in the adult striated muscle of mammals. A review and a hypothesis. Differentiation 7, 65–73.

    Google Scholar 

  • ROBERTS, P. & McGEACHIE, J. K. (1992) The effects of preand posttransplantation exercice on satellite cell activation and the regeneration of skeletal muscle transplants: a morphometric and autoradiographic study in mice. J. Anat. 180, 67–74.

    Google Scholar 

  • SALMONS, S. & VRBOVA, G. (1969) The influence of activity on some contractile characteristics of mammalian fast and slow muscle. J. Physiol. 201, 535–49.

    Google Scholar 

  • SASSOON, D. A. (1993) Myogenic regulatory factors: dissecting their role and regulation during vertebrate embryogenesis. Dev. Biol. 156, 11–23.

    Google Scholar 

  • SCHULTZ, E. (1989) Satellite cell behavior during skeletal muscle growth and regeneration. Med. Sci. Sport. Exerc. 5, 181–6.

    Google Scholar 

  • SCHULTZ, E. & JARYSZAK, D. L. (1985) Effects of skeletal muscle regeneration on the proliferation potential of satellite cells. Mech. Ageing. Dev. 30, 63–72.

    Google Scholar 

  • SCHULTZ, E. & McCORMICK, K. M. (1994) Skeletal muscle satellite cells. Rev. Physiol. Biochem. Pharmacol. 123, 213–57.

    Google Scholar 

  • SMITH, T. H., BLOCK, N. E., RHODES, S. J., KONIECZNY, S. F. & MILLER, J. B. (1993) A unique pattern of the four muscle regulatory factor proteins distinguishes somitic from embryonic, fetal and newborn mouse myogenic cells. Development, 117, 1125–33.

    Google Scholar 

  • SMITHII, C. K., JANNEY, M. J. & ALLEN, R.E. (1994) Temporal expression of myogenic regulatory genes during activation, proliferation, and differentiation of rat skeletal muscle satellite cells. J. Cell. Physiol. 159, 379–85.

    Google Scholar 

  • STOCKDALE, F. E., MILLER, J. B., FELDMAN, J. L., LAMSON, G. & HAGER, J. (1989) Myogenic cell lineages: commitment and modulation during differentiation of avian muscle. In Cellular and molecular biology of muscle development, UCLA symposia on molecular and cellular biology new series, Vol 93, (edited by KEDES, L. H. & STOCKDALE, F. E.) pp. 3–13, New York: AR Liss.

    Google Scholar 

  • TOWBIN, H., STAEHELIN, T. & GORDON, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to notrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350–4.

    Google Scholar 

  • VINCENT, S., MARTY, L. & FORT, P. (1993) S26 ribosomal protein RNA: an invariant control for gene regulation experiments in eucaryotic cells and tissues. Nucleic. Acids. Res. 21, 1498.

    Google Scholar 

  • WEINTRAUB, H., DAVIS, R., TAPSCOTT, S., THAYER, M., GRAUSE, M., BENEZRA, R., BLACKWELL, T., TURNER, D., RUPP, R., HOLLENBERG, S., ZHUANG, Y. & LASSAR, A. (1991) The myoD gene family: nodal point during specification of myogenic cell lineage. Science 251, 761–6.

    Google Scholar 

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Authors and Affiliations

  1. Laboratoire de Différenciation Cellulaire et Croissance, Institut National de la Recherche Agronomique, 2 Place Pierre Viala, 34060, Montpellier Cedex 1

    Catherine Barjot, Marie-Laurence Cotten & Francis Bacou

  2. Département de Biologie Moléculaire, Institut Pasteur, 25 rue du Dr. Roux, 75015, Paris, France

    Christiane Goblet & Robert G. Whalen

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  1. Catherine Barjot
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  2. Marie-Laurence Cotten
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  3. Christiane Goblet
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  5. Francis Bacou
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Barjot, C., Cotten, ML., Goblet, C. et al. Expression of myosin heavy chain and of myogenic regulatory factor genes in fast or slow rabbit muscle satellite cell cultures. J Muscle Res Cell Motil 16, 619–628 (1995). https://doi.org/10.1007/BF00130243

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