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Spatial and temporal patterns of myosin heavy chain expression in developing rat extraocular muscle

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Summary

The present study describes transitions in myosin heavy chain expression in the extraocular muscles of rats between the ages of E17 and adult. The unique phenotype of the extraocular muscle is reflected in its fibre type composition, which is comprised by six distinct profiles, each defined by location (orbital versus global layer) and innervation pattern (single versus multiple terminals). During extraocular muscle myogenesis, developmental myosin heavy chains were expressed in both primary and secondary fibres from embryonic day E17 through the first postnatal week. At this time, the downregulation of developmental myosin heavy chain isoforms began in the global layer in a fibre type-specific manner, reaching completion only after the first postnatal month. By contrast, developmental isoforms were retained in the overwhelming majority of orbital layer fibres into adulthood and expressed differentially along the length of these fibres. Fast myosin heavy chain was detected pre- and postnatally in developing secondary fibres and in all of the singly innervated fibre types and one of the multiply innervated fibre types in the adult. As many as four fast isoforms were detected in maturing extraocular muscle, including the extraocular muscle-specific myosin heavy chain. Slow myosin heavy chain was expressed in primary fibres throughout development and in one of the multiply innervated fibre types in the adult. In contrast, the pure fast-twitch retractor bulbi initially expressed slow myosin heavy chain in fibres destined to switch to the fast myosin heavy chain developmental programme. Based upon spatial and temporal patterns of myosin heavy chain isoform transitions, we suggest that epigenetic influences, rather than purely myogenic stage-specific factors, are critical in determining the unique extraocular muscle phenotype.

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References

  • Asiedu S. & Shafiq S. A. (1972) Actomyosin ATPase activity of the anterior latissimus dorsi muscle of the chicken. Exp. Neurol. 35, 211–13.

    Google Scholar 

  • Asmussen G. & Marechal G. (1989) Maximal shortening velocities of isomyosins and fibre types in soleus muscle of mice, rats, and guinea-pigs. J. Physiol. 416, 245–54.

    Google Scholar 

  • Asmussen G., Traub I. & Pette D. (1993) Electrophoretic analysis of myosin heavy chain isoform patterns in extraocular muscles of the rat. FEBS Lett. 335, 243–5.

    Google Scholar 

  • Bottinelli K., Schiaffino S. & Reggiani C. (1991) Force-velocity relations and myosin heavy chain isoform compositions of skinned fibres from rat skeletal muscle. J. Physiol. 437, 655–72.

    Google Scholar 

  • Brooke M. H. & Kaiser K. K. (1970) Muscle fiber types: how many and what kind? Arch. Neurol. 23, 369–79.

    Google Scholar 

  • Butler-Browne G. S. & Whalen R. G. (1984) Myosin isozyme transitions occurring during the postnatal development of the rat soleus muscle. Dev. Biol. 102, 324–34.

    Google Scholar 

  • Carraro U. & Catani C. (1983) A sensitive SDS-PAGE method reveals the heterogeneous nature of the embryonic myosin. Biochem. Biophys. Res. Comm. 116, 793–802.

    Google Scholar 

  • Chiarandini D. J. & Davidowitz J. (1979) Structure and function of extraocular muscle fibers. Curr. Top. Eye Res. 1, 91–142.

    Google Scholar 

  • Cho M., Hughes S. M., Karsch-Mizrachi I., Travis M., Leinwand L. A. & Blau H. M. (1994) Fast myosin heavy chains expressed in secondary mammalian muscle fibers at their time of inception. J. Cell Sci. 107, 2361–71.

    Google Scholar 

  • Condon K., Silberstein L., Blau H. M. & Thompson W. J. (1990) Development of muscle fiber types in the prenatal rat hindlimb. Dev. Biol. 138, 256–74.

    Google Scholar 

  • Couly G. F., Coltey P. M. & Ledouarin N. M. (1992) The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114, 1–15.

    CAS  PubMed  Google Scholar 

  • D'Albis A., Couteaux R., Janmot C. & Roulet A. (1989) Specific programs of myosin expression in the postnatal development of rat muscles. Eur. J. Biochem. 183, 583–90.

    Google Scholar 

  • Dix D. J. & Eisenberg B. R. (1990) Redistribution of myosin heavy chain mRNA at the myotendinous junction of stretched muscle fibers. J. Cell Biol. 111, 1885–94.

    Google Scholar 

  • Ecob-Prince M., Hill M. & Brown W. (1989) Immunocytochemical demonstration of myosin heavy chain expression in human muscle. J. Neurol. Sci. 91, 71–8.

    Google Scholar 

  • Edman K. A. P., Reggiani C., Schiaffino S. & Te Kronne G. (1988) Maximum velocity of shortening related to myosin isoform composition in frog skeletal muscle fibers. J. Physiol. 395, 679–94.

    Google Scholar 

  • Engel W. K. & Irwin R. L. (1967) A histochemical-physiological correlation of frog skeletal muscle fibers. Am. J. Physiol. 213, 511–18.

    Google Scholar 

  • Fedde M. R. (1969) Electrical properties and acetylcholine sensitivity of singly and multiply innervated avian muscle fibers. J. Gen. Physiol. 164, 219–29.

    Google Scholar 

  • Fredette B. J. & Landmesser L. T. (1991) Relationship of primary and secondary myogenesis to fiber type development in embryonic chick muscle. Dev. Biol. 143, 1–18.

    Google Scholar 

  • Goldspink G. (1983) Alterations in myofibril size and structure during growth, exercise, and changes in environmental temperature. In Handbook of Physiology, (edited by Peachey L. D., Adrian R. H. & Geiger S. R.) pp. 539–54. Bethesda: American Physiological Society.

    Google Scholar 

  • Guyton D. L. & Weingarten P. E. (1994) Sensory torsion as the cause of primary oblique muscle overaction/underaction and A- and V-pattern strabismus. Binoc. Vis. Eye Muscle Qtrly 9, 209–36.

    Google Scholar 

  • Hoh J. F. Y. & Hughes S. (1988) Myogenic and neurogenic regulation of myosin gene expression in cat jaw-closing muscles regenerating in fast and slow limb muscle beds. J. Muscle Res. Cell Motil. 9, 59–72.

    Google Scholar 

  • Hughes S. M. & Blau H. M. (1992) Muscle fiber pattern is independent of cell lineage in postnatal rodent development. Cell 68, 659–71.

    Google Scholar 

  • Hughes S. M., Cho M., Karsch-Mizrachi I., Travis M., Silberstein L., Leinwand L. A. & Blau H. M. (1993) Three slow myosin heavy chains sequentially expressed in developing mammalian skeletal muscle. Dev. Biol. 158, 183–99.

    Google Scholar 

  • Jacobs-El J., Ashley W. & Russell B. (1993) IIX and slow myosin expression follow mitochondrial increases in transforming muscle fibers. Am. J. Physiol. 265, C79–84.

    Google Scholar 

  • Jacoby J., Ko K., Weiss C. & Rushbrook J. I. (1989b) Systematic variation in myosin expression along extraocular muscle fibres of the adult rat. J. Muscle Res. Cell Motil. 11, 25–40.

    Google Scholar 

  • Kelly A. M. & Rubinstein N. A. (1980) Why are fetal muscles slow? Nature 288, 206–9.

    Google Scholar 

  • Kelly A. M. & Rubinstein N. A. (1994) The diversity of muscle fiber types and its origin during development. In Myology (edited by Engel A. G. & Franzini-Armstrong C.) pp. 119–133. New York: McGraw-Hill.

    Google Scholar 

  • Kelly A. M., Rosser B. W. C., Hoffman R., Panettieri R. A., Schiaffino S., Rubinstein N. A. & Nemeth P. M. (1991) Metabolic and contractile protein expression in developing rat diaphragm muscle. J. Neurosci. 11, 1231–42.

    Google Scholar 

  • Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.

    PubMed  Google Scholar 

  • Lewis P. R. (1977) Metal precipitation methods for hydrolytic enzymes. In Staining Methods for Sectioned Material (edited by Lewis P. R. & Knight D. P.) pp. 137–224. Amsterdam: North Holland.

    Google Scholar 

  • Lucas C. A., Rughani A. & Hoh J. F. Y. (1995) Expression of extraocular myosin heavy chain in rabbit laryngeal muscle. J. Muscle Res. Cell Motil. 16, 368–78.

    Google Scholar 

  • Mascarello F. & Rowlerson A. M. (1992) Myosin isoform transitions during development of extra-ocular and masticatory muscles in the fetal rat. Anat. Embryol. 185, 143–53.

    Google Scholar 

  • Marini J.-F., Pons F., Anoal M. & Leger J. J. (1989) Anti-myosin heavy chain monoclonal antibodies reveal two 2B (fast) fiber subtypes. J. Histochem. Cytochem. 37, 1721–9.

    Google Scholar 

  • Narusawa M., Fitzsimons R. B., Izumo S., Nadalginard B., Rubinstein N. A. & Kelly A. M. (1987) Slow myosin in developing rat skeletal muscle. J. Cell Biol. 104, 447–59.

    Google Scholar 

  • Pavlath G. K., Rich K., Webster S. G. & Blau H. M. (1989) Localization of muscle gene products in nuclear domains. Nature 337, 570–3.

    Google Scholar 

  • Pin C. L. & Merrifield P. A. (1993) Embryonic and fetal rat myoblasts express different phenotypes following differentiation in vitro. Dev. Genetics 14, 356–68.

    Google Scholar 

  • Porter J. D. & Baker R. S. (1992) Prenatal morphogenesis of primate extraocular muscle: neuromuscular junction formation and fiber type differentiation. Invest. Ophthalmol. Vis. Sci. 33, 657–72.

    Google Scholar 

  • Porter J. D. & Hauser K. F. (1993) Survival of extraocular muscle in long-term organotypic culture: differential influence of appropriate and inappropriate motoneurons. Dev. Biol. 160, 39–50.

    Google Scholar 

  • Porter J. D., Burns L. A. & May P. J. (1989) Morphological substrate for eyelid movements: innervation and structure of primate levator palpabrae superioris and orbicularis oculi muscles. J. Comp. Neurol. 287, 64–81.

    Google Scholar 

  • Porter J. D., Baker R. S., Ragusa R. J. & Brueckner J. K. (1995) Extraocular muscles: basic and clinical aspects of structure and function. Surv. Ophthalmol. 39, 451–84.

    Google Scholar 

  • Robinson D. A. (1981) Control of eye movements. In Handbook of Physiology, (edited by Brooks V.B.) pp. 1275–320. Bethesda: American Physiological Society.

    Google Scholar 

  • Rubinstein N. A. & Kelly A. M. (1981) Development of muscle fiber specialization in the rat hindlimb. J. Cell Biol. 90, 128–44.

    Google Scholar 

  • Rushbrook J. I., Weiss C., Ko K., Feuerman M. H., Carleton S., Ing A. & Jacoby J. (1994) Identification of alpha-cardiac myosin heavy chain mRNA and protein in extraocular muscle of the adult rabbit. J. Muscle Res. Cell Motil. 15, 505–15.

    Google Scholar 

  • Russell S. D., Cambon N. A. & Whalen R. G. (1993) Two types of neonatal-to-adult fast myosin heavy chain transitions in rat hindlimb muscle fibers. Dev. Biol. 157, 359–70.

    Google Scholar 

  • Salviati G., Biasia E. & Aloisi M. (1986) Synthesis of fast myosin induced by fast ectopic innervation of rat soleus muscle is restricted to the eptopic endplate region. Nature 322, 637–9.

    Google Scholar 

  • Sartore S., Mascarello F., Rowlerson A., Gorza L., Ausoni S., Vianello M. & Schiaffino S. (1987) Fibre types in extraocular muscles: a new myosin isoform in the fast fibers. J. Muscle Res. Cell Motil. 8, 161–72.

    Google Scholar 

  • Schiaffino S., Gorza L., Sartore S., Saggin L. & Carli M. (1986) Embryonic myosin heavy chain as a differentiation marker of developing human skeletal muscle and rhabdomyosarcoma. Exp. Cell Res. 163, 211–20.

    Google Scholar 

  • Schiaffino S., Gorza L., Pitton G., Saggin L., Ausoni S., Sartore S. & Lomo T. (1988) Embryonic and neonatal myosin heavy chain in denervated and paralyzed rat skeletal muscle. Dev. Biol. 127, 1–11.

    Google Scholar 

  • Schiaffino S., Gorza L., Sartore S., Saggin L., Ausoni S., Vianello M., Gunderson K. & Lomo T. (1989) Three myosin heavy chain isoforms in type 2 skeletal muscle fibers. J. Muscle Res. Cell Motil. 10, 197–205.

    Google Scholar 

  • Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H. & Provenzano M. D. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem. 150, 76–85.

    Google Scholar 

  • Spencer R. F. & Porter J. D. (1988) Structural organization of the extraocular muscles. In Reviews in Oculomotor Research (edited by Buttner-Ennever J. A.) pp. 33–79. New York: Elsevier Science Publishers.

    Google Scholar 

  • Staron R. S. & Pette D. (1987) Nonuniform myosin expression along single fibers of chronically stimulated and contralateral rabbit tibialis anterior muscles. Pflügers Arch. 409, 67–73.

    Google Scholar 

  • Stockdale F. E. & Miller J. B. (1987) The cellular basis of myosin heavy chain isoform expression during development of avian skeletal muscles. Dev. Biol. 123, 1–9.

    Google Scholar 

  • Sutherland C. J., Elsom V. L., Gordon M. L., Dunwoodie S. L. & Hardeman E. C. (1993) Coordination of skeletal muscle gene expression occurs late in mammalian development. Dev. Biol. 146, 167–78.

    Google Scholar 

  • Talmadge R. J. & Roy R. R. (1993) Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J. Appl. Physiol. 75, 2337–40.

    Google Scholar 

  • Wahl C. M., Noden D. M. & Baker R. (1994) Developmental relations between sixth nerve motor neurons and their targets in the chick embryo. Dev. Dyn. 201, 191–202.

    Google Scholar 

  • Whalen R. G., Sell S. M., Butler-Browne G. S., Schwartz D., Bouveret P. & Pinset-Harstrom I. (1981) Three myosin heavy-chain isoforms appear sequentially in rat muscle development. Nature 292, 805–9.

    Google Scholar 

  • Wieczorek D. F., Periasamy M., Butler-Browne G. S., Whalen R. G. & Nadal-Ginard B. (1985) Coexpression of multiple myosin heavy chain genes, in addition to a tissue-specific one, in extraocular muscle. J. Cell Biol. 101, 618–29.

    Google Scholar 

  • Williams P., Watt P., Bicik V. & Goldspink G. (1986) Effect of strech combined with electrical stimulation on the type of sarcomeres produced at the ends of muscle fibers. Exp. Neurol. 93, 500–9.

    Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy and Neurobiology, University of Kentucky Medical Center, 40536-0084, Lexington, KY, USA

    Jennifer K. Brueckner, Olga Itkis & John D. Porter

  2. Department of Ophthalmology, University of Kentucky Medical Center, 40536-0084, Lexington, KY, USA

    Jennifer K. Brueckner, Olga Itkis & John D. Porter

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  1. Jennifer K. Brueckner
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Brueckner, J.K., Itkis, O. & Porter, J.D. Spatial and temporal patterns of myosin heavy chain expression in developing rat extraocular muscle. J Muscle Res Cell Motil 17, 297–312 (1996). https://doi.org/10.1007/BF00240928

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