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Expression of a novel combination of fast and slow troponin T isoforms in rabbit extraocular muscles

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Summary

The properties of extraocular muscles (EOMs) are quite different from those of the trunk and limb. Here we show that there is a novel pattern of troponin T (TnT) expression in EOMs which most likely contributes to the fine control of ocular movement and may reflect their innervation by cranial motoneurons. Three regions of the muscle were analysed to distinguish the TnT isoforms present in the fast singly-innervated fibres from those in the multiply-innervated fibres. More than 95% of the TnT in the singly-innervated fibres is TnT3f, which exhibits the most graded response to changes in calcium concentration during activation (Schachatet al., J. molec. Biol. 198, 551–4). In multiply-innervated fibres, which exhibit tonic contractures, the slow troponin T TnT2s is expressed. While neither TnT3f nor TnT2s is unique to EOM, this pattern is unusual in two respects: first, both TnT3f and TnT2s are minor components of the trunk and limb musculature, and second, most muscles express several fast and both slow TnT species. Although EOM occupies a highly specialized physiological niche, its unusual physiology is not reflected in the presence of new TnT isoforms but in the expression of a different ratio of the known species of TnT.

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References

  • Abe, H., Komiya, T. &Obinata, T. (1986) Expression of multiple Troponin T variants in neonatal chicken breast muscle.Devel. Biol. 118, 42–51.

    Google Scholar 

  • Bach-Y-Rita, P. &Ito, F. (1966) In vivo studies of fast and slow muscle fibers in cat extraocular muscles.J. gen Physiol. 49, 1177–98.

    PubMed  Google Scholar 

  • Barany, M. (1967) ATPase activity of myosin correlated with speed of shortening.J. gen. Physiol. 50, 197–218.

    PubMed  Google Scholar 

  • Bird, I. M., Dhoot, G. K. &Wilkinson, J. M. (1985) Identification of multiple variants of fast muscle Troponin T in the chicken using monoclonal antibodies.Eur J. Biochem. 150, 517–25.

    PubMed  Google Scholar 

  • Brandt, P. W., Diamond, M. S., Gluck, B., Kawai, M. &Schachat, F. H. (1984) Molecular basis of vertebrate thin filament cooperatively.Carlsberg Res. Commun. 49, 155–67.

    Google Scholar 

  • Brandt, P. W., Diamond, M. S., Rutchik, J. S. &Schachat, F. H. (1987). Cooperative interactions extend the length of the thin filament in skeletal muscle.J. molec. Biol. 195, 885–96.

    PubMed  Google Scholar 

  • Breitbart, R. E., Nguyen, H. T., Medford, R. M., Mahdavi, V. &Nadal-Ginard, B. (1985) Intricate combinatorial patterns of exon splicing generate multiple regulated troponin T isoforms from a single gene.Cell 41, 67–82.

    PubMed  Google Scholar 

  • Briggs, M. M., Klevit, R. E. &Schachat, F. H. (1984) Heterogeneity of contracile proteins. Purification of two species of troponin T from rabbit fast skeletal muscles.J. biol. Chem. 259, 10369–75.

    PubMed  Google Scholar 

  • Briggs, M. M., Lin, J. J. V. &Schachat, F. H. (1987) The extent of amino-terminal heterogeneity in rabbit fast skeletal muscle troponin T.J. Musc. Res. Cell Motility 8, 1–12.

    Google Scholar 

  • Bronson, D. D. &Schachat, F. H. (1982) Heterogeneity of contractile proteins. Differences in tropomyosin in fast, mixed, and slow muscles of the rabbit.J. biol. Chem. 257, 3937–43.

    PubMed  Google Scholar 

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

    Google Scholar 

  • Chiarandini, D. J. &Davidowitz, J. (1979) Structure and function of extraocular muscle fibers. InCurrent Topics in Eye Research (edited byJ. A. Zadunaisky &H. Davson), pp. 91–142. New York: Academic Press.

    Google Scholar 

  • Cooper, S. &Eccles, J. C. (1930) The isometric responses of mammalian muscles.J. Physiol., Lond. 69, 377–85.

    Google Scholar 

  • Davidowitz, J., Phillips, G. &Breinin, G. M. (1977) Organization of the orbital surface layer in rabbit superior recrus.Invest. Ophthalmol. Vis. Sci. 16, 711–29.

    PubMed  Google Scholar 

  • Duke-Elder, S. (1961)System of Ophthalmology, Vol. II, pp. 435–83. St. Louis: C. V. Mosby.

    Google Scholar 

  • Fernand, V. S. V. &Hess, A. (1969) The occurrence, structure, and innervation of slow twitch muscle fibres in the tensor tympanii and stapedius of the cat.J. Physiol., Lond. 200, 547–54.

    Google Scholar 

  • Floyd, K. (1973) Cholinesterase activity in sheep esophageal muscle.J. Anal. 116, 357–73.

    Google Scholar 

  • Hess, A. &Pilar, G. (1963) Slow fibers in the extraocular muscles of the cat.J. Physiol., Lond. 169, 780–98.

    Google Scholar 

  • Imai, H., Hirai, S., Hirono, H. &Hirabayashi, T. (1986) Many isoforms of fast muscle Troponin T from chicken legs.J. Biochem. 99, 923–30.

    PubMed  Google Scholar 

  • Jolesz, F. &Sreter, F. A. (1981) Development, innervation, and activity-induced changes in skeletal muscle.Ann. Rev. Physiol. 43, 531–52.

    Google Scholar 

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

    Google Scholar 

  • Lin, J. J. C., Feramisco, J. R., Blose, S. H. &Matsumura, F. (1984) Monoclonal Antibodies to Cytoskeletal Proteins. InMonoclonal Antibodies and Functional Cell Lines (edited byKennett, R., Bechtol, K., &Mckearn, T.), pp. 119–51. New York: Plenum Publishing.

    Google Scholar 

  • Medford, R. M., Nguyen, H. T., Destree, A. T., Summers, E. &Nadal-Ginard, B. (1984) A novel mechanism of alternative RNA splicing for the developmentally regulated generation of Troponin T isoforms from a single gene.Cell 38, 409–21.

    PubMed  Google Scholar 

  • Moore, G. E., Briggs, M. M. &Schachat, F. H. (1987) Patterns of troponin T expression in mammalian fast, slow and promiscuous muscle fibers.J. Musc. Res. Cell. Motility 8, 13–22.

    Google Scholar 

  • Moore, G. E. &Schachat, F. H. (1985) Molecular heterogeneity of histochemical fibre types: a comparison of fast fibers.J. Musc. Res. Cell. Motility 6, 513–24.

    Google Scholar 

  • Moss, R. L., Gary, G. G. &Greaser, M. L. (1985) The effects of partial extraction of TnC upon the tension-pCa relationship in rabbit skinned skeletal muscle fibersJ. gen. Physiol. 86, 585–600.

    PubMed  Google Scholar 

  • O'Farrell, P. Z., Goodman, H. M. &O'Farrell, P. H. (1977) High resolution two-dimensional electrophoresis of basic as well as acidic proteins.Cell 12, 1133–42.

    PubMed  Google Scholar 

  • Pachter, B. R. (1984) Rat extraocular muscle III. Histochemical variability along the length of multiplyinnervated fibers of the orbital surface layer.Histochemistry 80, 535–8.

    PubMed  Google Scholar 

  • Peachey, L. (1971) The structure of the extraocular muscle fibers of mammals. InThe Control of Eye Movements (edited byBach-Y-Rita, P., Collins, C. &Hyde, J. E. pp. 47–66. New York: Academic Press.

    Google Scholar 

  • Pette, D. &Vrbova, G. (1985) Neural control of phenotypic expression in mammalian muscle fibers.Muscle and Nerve 8, 676–689.

    PubMed  Google Scholar 

  • 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. Ophthalmol. Vis. Sci. 18, 303–6.

    PubMed  Google Scholar 

  • Reichman, H. &Srihari, T. (1983) Enzyme activities. Histochemistry and myosin light chain pattern in extraocular muscles of rabbit.Histochemistry 78, 111–20.

    PubMed  Google Scholar 

  • Reiser, P. J., Moss, R. L., Giulian, G. G. &Greaser, M. J. (1985) Shortening velocity and myosin heavy chains of developing rabbit muscle fibers.J. biol. Chem. 260, 14403–5.

    PubMed  Google Scholar 

  • Salmons, S. &Vrbova, G. (1969) The influence of activity on some contractile characteristics of mammalian fast and slow muscles.J. Physiol., Lond. 201, 535–49.

    Google Scholar 

  • Schachat, F. H., Bronson, D. D. &McDonald, O. B. (1980) Two kinds of slow skeletal muscle fibers which differ in their myosin light chain complements.FEBS Letts. 122, 80–2.

    Google Scholar 

  • Schachat, F. H., Bronson, D. D. &Mcdonald, O. B. (1985) Heterogeneity of contractile proteins. A continuum of troponin-tropomyosin expression in mammalian skeletal muscles.J biol. Chem. 260, 1108–13.

    PubMed  Google Scholar 

  • Schachat, F. H., Diamond, M. S. &Brandt, P. W. (1987) The effect of different troponin T-tropomyosin combinations of thin filament activation.J. molec. Biol. 198, 551–4.

    PubMed  Google Scholar 

  • Torre, M. (1953) Nombre et dimensions des unites motrices dans les muscles extrinsiques de l'oeil et, en general, dans les muscles squelettiques.Schweiz Arch. Neurol. Neuroch. Psychiat. 72, 362–78.

    Google Scholar 

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

    PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Anatomy, Duke University Medical Center, 27710, Durham, NC, USA

    Margaret M. Briggs

  2. Department of Ophthalmology, New York University Medical Center, 10016, New York, NY, USA

    Jean Jacoby & Jacob Davidowitz

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  1. Margaret M. Briggs
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  2. Jean Jacoby
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  3. Jacob Davidowitz
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  4. Frederick H. Schachat
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Briggs, M.M., Jacoby, J., Davidowitz, J. et al. Expression of a novel combination of fast and slow troponin T isoforms in rabbit extraocular muscles. J Muscle Res Cell Motil 9, 241–247 (1988). https://doi.org/10.1007/BF01773894

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  • DOI: https://doi.org/10.1007/BF01773894

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