Summary
The intrinsic laryngeal muscles of mammals are functionally heterogeneous, some of these muscles (e.g. the thyroarytenoid) contract extremely rapidly, like extraocular muscle, whilst others (e.g. the cricothyroid) contract as fast as limb fast muscle. The extraordinarily rapid contraction speed of extraocular muscles is associated with a fast myosin not found in limb muscles. In this work we explored the possibility that the thyroarytenoid muscle may also express this extraocular-specific fast myosin by raising a monoclonal antibody (mab 4A6) against its heavy chain. Electrophoretic separation of native isomyosins revealed that both the extraocular and the thyroarytenoid have two similar bands migrating ahead of bands found in limb fast or cricothyroid myosins. These two bands bound mab 4A6. The thyroarytenoid muscle can be divided into two divisions, a vocalis division which is important in phonation and an external division which functions in closing the glottis. Fibres in the vocalis are heterogeneous, some stain with mab 4A6, whilst others stain with mabs against limb myosin heavy chains. Fibres in the external division stain almost homogeneous with mab 4A6. The immunohistochemical staining pattern in the cricothyroid muscle resembled that of fast limb muscle: no fibres stained with mab 4A6. Thus, the high speed of contraction of the thyroarytenoid is associated with the same myosin heavy chain found in extraocular muscles, this characteristic is presumably an evolutionary adaptation for rapid closure of the glottis to enhance airway defense mechanisms.
Similar content being viewed by others
References
ABO EL-ENENE, M. A. (1975) Significance of the pattern of motor innervation of the intrinsic laryngeal muscles of cat. Acta Anat. 93, 543–53.
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.
ASMUSSEN, G., BECKERS-BLEUKX, G. & MARéCHAL, G. (1994) Force-velocity relation of the rabbit inferior oblique muscle; influence of temperature. Pflügers Arch. 426, 542–7.
BARANY, M. (1967) ATPase activity of myosin correlated with speed of muscle shortening. J. Gen. Physiol. 50, 197–218.
BOTTINELLI, R., 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.
CAMPBELL, A. M. (1984) Monoclonal Antibody Technology. Amsterdam: Elsevier.
CATZ, D. S., FISCHER, L. M., MOSCHELLA, M. C., TOBIAS, M. L. & KELLEY, D. B. (1992) Sexually dimorphic expression of a laryngeal-specific, androgen-regulated myosin heavy chain gene during xenopus-laevis development. Devl Biol. 154, 366–76.
CLOSE, R. I. & LUFF, A. R. (1974) Dynamic properties of inferior rectus muscle of the rat. J. Physiol. 236, 259–70.
COOPER, S. & ECCLES, J. C. (1930) The isometric responses of mammalian muscles. J. Physiol. 69, 377–85.
COULY, G. F., COLTY, P. M. & LEDOUARIN, N. M. (1992) The developmental fate of the cephalic mesoderm in quail-chick chimeras. Development 114, 1–15.
FINK, B. R. & DEMAREST, R. J. (1978) Laryngeal Biomechanics. Cambridge: Harvard University Press.
HALL-CRAGGS, E. C. B. (1968) The contraction times and enzyme activity of two rabbit laryngeal muscles. J. Anat. 102, 241–55.
HAST, M. H. (1969) The primate larynx. A comparative physiological study of intrinsic muscles. Acta Otolaryng. 67, 84–92.
HAVENITH, M. G., VISSER, R., SCHRIJVERS-VAN SCHENDEL, J. M. & BOSMAN, F. T. (1990) Muscle fiber typing in routinely processed skeletal muscle with monoclonal antibodies. Histochemistry 93, 497–9.
HOH, J. F. Y. (1991) Myogenic regulation of mammalian skeletal muscle fibres. News Physiol. Sci. 6, 1–6.
HOH, J. F. Y. (1992) Muscle fibre types and function. Curr. Opin. Rheumatol. 4, 801–8.
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.
HOH, J. F. Y. & HUGHES, S. (1989) Immunocytochemical analysis of the perinatal development of cat masseter muscle using anti-myosin antibodies. J Muscle Res. Cell Motil. 10, 312–25.
HOH, J. F. Y. & YEOH, G. (1979) Rabbit skeletal myosin isoenzymes from fetal fast-twitch and slow-twitch muscles. Nature 280, 321–3.
HOH, J. F. Y., MCGRATH, P. A. & WHITE, R. I. (1976) Electrophoretic analysis of multiple forms of myosin in fast-twitch and slow-twitch muscles of the chick. Biochem. J. 157, 87–95.
HOH, J. F. Y., HUGHES, S., CHOW, C., HALE, P. T. & FITZSIMONS, R. B. (1988a) Immunocytochemical and electrophoretic analyses of changes in myosin gene expression in cat posterior temporalis muscle during postnatal development. J. Muscle Res. Cell Motil. 9, 48–58.
HOH, J. F. Y., HUGHES, S., HALE, P. T. & FITZSIMONS, R. B. (1988b) Immunocytochemical and electrophoretic analyses of changes in myosin gene expression in cat limb fast and slow muscles during postnatal development. J. Muscle Res. Cell Motil. 9, 30–47.
HOH, J. F. Y., HUGHES, S., HUGH, G. & POZGAJ, I. (1989) Three hierarchies in skeletal muscle fibre classification; allotype, isotype and phenotype. In Cellular and Molecular Biology of Muscle Development. UCLA Symposium on Molecular and Cellular Biology, New Series, vol. 93 (edited by STOCKDALE, F. & KEDES, L.) pp. 15–26. New York: Alan R. Liss Inc.
HOH, J. F. Y., HUGHES, S., WALKER, M. L., KANG, L. D. H. & EVERETT, A. W. (1991) Slow myosin heavy chains in cat jaw and limb muscles are phenotypically distinct: expression of jaw-specific slow myosin phenotype in regenerated and chronically stimulated jaw muscles. Basic Applied Myol. 4, 285–94.
HUNT, P., WILKINSON, D. & KRUMLAUF, R. (1991) Patterning the vertebrate head: murine Hox 2 genes mark distinct subpopulations of premigratory and migrating cranial neural crest. Development 112, 43–50.
JACOBY, J. (1990) Systematic variation in myosin expression along extraocular muscle fibres of the adult rat. J. Muscle Res. Cell Motil. 11, 25–40.
LANNERGREN, J. (1987) Contractile properties and myosin isoenzymes of various kinds of Xenopus twitch muscle fibres. J. Muscle Res. Cell Motil. 8, 260–73.
MARTENSSON, A. & SKOGLUND, C. R. (1964) Contraction properties of intrinsic laryngeal muscles. Acta Physiol. Scand. 60, 318–36.
MCGINNIS, W. & KRUMLAUF, R. (1992) Homeobox genes and axial patterning. Cell 68, 283–302.
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.
NODEN, D. M. (1983) The embryonic origins of avian cephalic and cervical muscles and associated connective tissues. Amer. J. Anat. 168, 257–76.
NODEN, D. M. (1993) Spatial integration among cells forming the cranial peripheral nervous system. J. Neurobiol. 24, 248–61.
OLSON, E. N. (1990) MyoD family: a paradigm for development? Genes Dev. 4, 1454–61.
OTT, M., BOBER, E., LYONS, G., ARNOLD, H. & BUCKINGHAM, M. (1991) Early expression of the myogenic regulatory gene, myf-5, in precursor cells of skeletal muscle in the mouse embryo. Development 111, 1097–107.
PACHTER, B. R. (1984) Rat extraocular muscle 3. Histochemical variability along the length of multiply-innervated fibres of the orbital layer. Histochemistry 80, 535–8.
ROSSI, G. & CORTESINA, G. (1965) Morphological study of laryngeal muscles in man. Acta Oto-laryng. 59, 575–92.
ROSSMANITH, G. H., HOH, J. F. Y., KIRMAN, A. & KWAN, L. J. (1986) Influence of V1 and V3 isomyosins on the mechanical behaviour of rat papillary muscle as studied by pseudo-random binary noise modulated perturbations. J. Muscle Res. Cell. Motil. 7, 307–19.
ROWLERSON, A., POPE, B., MURRAY, J., WHALEN, R. G. & WEEDS, A. G. (1981) A novel myosin present in cat jaw-closing muscles. J. Muscle Res. Cell Motil. 2, 415–38.
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 fibres. J. Muscle Res. Cell Motil. 8, 161–72.
SASSOON, D., WRIGHT, W. E., LIN, V., LASSAR, A., WEINTRAUB, H. & BUCKINGHAM, M. (1989) Expression of two myogenic regulatory factors, myogenin and MyoD1, during mouse embryogenesis. Nature 341, 303–7.
SPERBER, G. H. (1989) Craniofacial Embryology. 4th edition. London: Wright.
SYROVY, I. & GUTMANN, E. (1971) ATPase activity of two rabbit laryngeal muscles. Experientia 27, 248.
WACHTLER, F., JACOB, H. J., JACOB, M. & CHRIST, B. (1984) The extraocular muscles in birds are derived from the prechordal plate. Naturwissenschaften 71, 379–80.
WEINTRAUB, H., DAVIS, R., TAPSCOTT, S., THAYER, M., KRAUSE, M., BENEZRA, R., BLACKWELL, T. K., TURNER, D., RUPP, R., HOLLENBERG, S., ZHUANG, Y. & LASSAR, A. (1991) The myoD gene family-nodal point during specification of the muscle cell lineage. Science 251, 761–6.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Lucas, C.A., Rughani, A. & Hoh, J.F.Y. Expression of extraocular myosin heavy chain in rabbit laryngeal muscle. J Muscle Res Cell Motil 16, 368–378 (1995). https://doi.org/10.1007/BF00114502
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00114502