Summary
We report on the existence of a myosin heavy chain (MHC) isoform with unique structural properties in extraocular (EO) muscles. Differences in MHC composition are apparent using a polyclonal antibody prepared against myosin isolated from bovine EO muscle myosin. In enzyme immunoassays and western blotting experiments, this anti-EO myosin antibody reacted specifically with the heavy chains of EO muscle myosin and not with the heavy chains of other myosins. The distribution of this new MHC isoform in the globe rotating muscles from different mammalian species was analysed using a panel of specific anti-myosin antibodies and comparing the histochemical myosin ATPase profile of muscle fibres with their isomyosin content. Most fibres which display a type 2 ATPase reaction pattern were selectively labelled by anti-EO antibodies. A few type 2 fibres were found to react with both anti-EO and anti-2A myosin antibodies and others, located almost exclusively in the orbital layers, reacted with anti-foetals as well as anti-EO antibodies.
The presence of a distinct form of myosin in EO muscle fibres is probably related to the particular functional characteristics of these muscles, which are known to be exceptionally fast-contracting but display a very low tension output.
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References
Alvarado, J. & vanHorn, C. (1975) Muscle cell types of the cat inferior oblique. InBasic Mechanisms of Ocular Motility and their Clinical Implications (edited byLenner Strand, G. andBach-Y-Rita, P.), pp. 15–43. Oxford: Pergamon Press.
Asmussen, G. &Gaunitz, U. (1981) Mechanical properties of the isolated inferior oblique muscle of the rabbit.Pflügers Arch. 392, 183–90.
Asmussen, G., Kiessling, A. &Wohlrab, F. (1971) Histochemical characteristics of muscle fiber types in the mammalian extraocular muscles. Acta Anat.,79, 526–45.
Bach-Y-Rita, P. &Ito, F. (1966)In vivo studies on fast and slow muscle fibers in cat extraocular muscles.J. gen. Physiol.,49, 1177–98.
Barany, M. (1967) ATPase activity of myosin correlated with speed of muscle shortening.J. gen. Physiol.,50, 197–218.
Barany, M. &Close, R. I. (1971) The transformation of myosin in cross-innervated rat muscles.J. Physiol., Lond.,213, 455–74.
Bonner, W. M. &Laskey, R. A. (1974) A film detection method for tritium-labeled proteins and nucleic acids in polyacrylamide gels.Eur. J. Biochem.,46, 83–8.
Buchtal, F. &Schmalbruch, H. (1980) Motor units of mammalian muscle.Physiol. Rev. 60, 91–142.
Bugaisky, L. B., Butler-Browne, G., Sell, S. M. &Whalen, R. G. (1984) Structural differences in the subfragment 1 and rod portions of myosin isozymes from adult and developing rat skeletal muscle.J. biol. Chem. 259, 7212–18.
Burke, L. E., Levine, D. N., Zajac, IIIF. E., Tsairis, P. &Engel, W. K. (1971) Mammalian motor units: Physiological-biochemical correlation in three types of cat gastrocnemius fibers.Science, N. Y. 174, 709–12.
Cantini, M., Sartore, S. &Schiaffino, S. (1980) Myosin types in cultured muscle cells.J. Cell Biol. 85, 903–9.
Caplan, A. I., Fiszman, M. Y. &Eppenberger, H. M. (1983) Molecular and cell isoforms during development.Science, N. Y. 221, 921–7.
Close, R. J. &Luff, A. R. (1973) Dynamic properties of inferior rectus muscle of the rat.J. Physiol., Lond. 236, 259–70.
Cooper, S. &Eccles, J. C. (1930) The isometric responses of mammalian muscles.J. Physiol., Lond. 69, 377–85.
Dalla Libera, L. &Sartore, S. (1981) Immunological and biochemical evidence for atrial-like isomyosin in thyrotoxic rabbit ventricle.Biochim. biophys. Acta 669, 84–92.
Dalla Libera, L., Sartore, S., Pierobon-Bormioli, S. &Schiaffino, S. (1980) Fast-white and fast-red isomyosins in guinea pig muscles.Biochem. biophys. Res. Commun. 96, 1662–70.
Engvall, E. &Perlmann, P. (1972) Enzyme-linked immuno-absorbent assay, Elisa. III. Quantitation of specific antibodies by enzyme-labelled antiimmunoglobulin in antigen coated tubes.J. Immunol. 109 129, 135.
Greaser, M. L. &Gergely, J. (1971) Reconstitution of troponin activity from three protein components.J. biol. Chem. 246, 4226–33.
Gueritaud, J. P., Horcholle-Bossavit, G., Jami, L., Thiesson, D. &Tyc-Dumont, S. (1984) Histochemical analysis of cat extraocular muscle.Neurosci. Lett. Suppl. 18, S229.
Hanson, J., Lennerstrand, G. &Nichols, K. C. (1980) The postnatal development of the inferior oblique muscle of the cat. III. Fiber sizes and histochemical properties.Acta Physiol. Scand. 108, 61–71.
Hess, A. &Pilar, G. (1963) Slow fibres in the extraocular muscles of the cat.J. Physiol., Lond. 169, 780–98.
Jentoft, N. &Dearborn, D. G. (1979) Labeling of protein by reductive methylation using sodium cyanoborohydride.J. biol. Chem. 254, 4359–65.
Laemmli, U. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4.Nature, Lond. 227, 680–5.
Laskey, R. &Mills, A. D. (1975). Quantitative film detection of3H and14C in polyacrylamide gels by fluorography.Eur. J. Biochem. 56, 335–41.
Lennerstrand, G. (1974a) Electrical activity and isometric tension in motor units of the cat's inferior oblique muscle.Acta Physiol. Scand. 91, 458–74.
Lennerstrand, G. (1974b) Mechanical studies on the retractor bulbi muscle and its motor units in the cat.J. Physiol., Lond. 236, 43–55.
Luff, A. R. (1981) Dynamic properties of the inferior rectus, extensor digitorum longus, diaphragm and soleus muscles of the mouse.J. Physiol., Lond. 313, 161–71.
Matyushkin, D. P. (1964) Motor systems in the oculomotor apparatus of high animals.Fedn. Proc. 23, T1103-T1106.
Mayr, R. (1971) Structure and distribution of fiber types in the external eye muscles of the rat.Tissue Cell 3, 433–62.
O'Farrell, P. (1975) High resolution two-dimensional electrophoresis of proteins.J. biol. Chem. 250, 4007–21.
Peachey, L., Takeichi, M. &Nag, A. (1974) Muscle fiber types and innervation in adult cat extraocular muscles. InExploratory Concepts in Muscular Dystrophy II (edited byMilhorat, A.), pp. 246–54. Amsterdam: Excerpta Medica.
Pierobon-Bormioli, S., Sartore, S., Dalla Libera, S., Vitadello, M. &Schiaffino, S. (1981) ‘Fast’ isomyosins and fiber types in mammalian skeletal muscle.J. Histochem. Cytochem. 29, 1179–88.
Pierobon-Bormioli, S., Sartore, S., Vitadello, M. &Schiaffino, S. (1980) ‘Slow’ myosins in vertebrate skeletal muscle. An immunofluorescence study.J. Cell Biol. 85, 672–81.
Pierobon-Bormioli, S., Torresan, P., Sartore, S., Moschini, G. B. &Schiaffino, S. (1979) Immunohistochemical identification of slow-tonic fibers in human extrinsic eye muscles.Invest. Ophthal. Vis. Sci. 18, 303–6.
Richards, E. G., Chung, C. S., Menzel, D. B. &Olcott, H. S. (1967) Chromatography of myosin on diethylaminoethyl Sephadex A-50.Biochemistry 6, 528–40.
Rowlerson, A., Pope, P., Murray, J., Whalen, R. B. &Weeds, A. G. (1981) A novel myosin present in cat jaw-closing muscles.J. Musc. Res Cell Motility 2, 415–38.
Sartore, S. (1981) Immunological cross-reactivity between chicken slow skeletal and ventricular muscle myosin.Biochim. biophys. Acta 667, 143–56.
Sartore, S., Gorza, L. &Schiaffino, S. (1982) Fetal myosin heavy chains in regenerating muscle.Nature, Lond. 298, 294–5.
Schiaffino, S., Gorza, L., Saggin, L., Valfrè, C. &Sartore, S. (1984a) Myosin changes in hypertrophied human atrial and ventricular myocardium. A correlated immunofluorescence and quantitative immunochemical study on serial cryosections.Eur. Heart J. 75 Suppl F, 95–102.
Schiaffino, S., Sartore, S., Mascarello, F. &Rowlerson, A. (1984b) Fast fibres of extraocular muscles contain a characteristic type of myosinJ. Musc. Res. Cell Motility 5, 183.
Towbin, H., Staehelin, T. &Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.Proc. Natn. Acad. Sci. U. S. A. 76, 4350–4.
Vita, G. F., Mastaglia, F. L. &Johnson, M. A. (1980) A histochemical study of fibre types in rat extraocular muscles.J. Neuropath. Appl. Neurobiol. 6, 449–63.
Whalen, R. G., Sell, S. M., Butler-Browne, G. S., Schwartz, K., Bouveret, P. &Pinset-Harstrom, I. (1981) Three myosin heavy-chaiisozymes appear sequentially in rat muscle development.Nature, Lond. 292, 805–9.
Wieczorek, D. S., 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 musculature.J. Cell Biol. 101, 618–29.
Yellin, H. (1969) Unique intrafusal and extraocular muscle fibers exhibiting dual actomyosin ATPase activity.Exp. Neurol. 25, 153–63.
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Sartore, S., Mascarello, F., Rowlerson, A. et al. Fibre types in extraocular muscles: a new myosin isoform in the fast fibres. J Muscle Res Cell Motil 8, 161–172 (1987). https://doi.org/10.1007/BF01753992
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DOI: https://doi.org/10.1007/BF01753992