Abstract
We have shown previously that in addition to the adult myosin heavy chain (MyHC) isoform present throughout the length of each fast-twitch glycolytic muscle fibre within the pectoralis of the mature chicken, the neonatal isoform is retained in the tapered ends of these fibres. This work, however, has been the only published report of this phenomenon. Here, we tested the hypothesis that similar to the chicken, the ends of mature pigeon pectoralis muscle fibres contain developmental MyHC isoform(s). A histological stain was used to visualize endomysium to assist in the analysis of transverse sections of pectoralis muscle from four mature pigeons. Immunocytochemical techniques were used to localize MyHC isoform(s) characteristic of pigeon pectoralis development. We show that within mature pigeon pectoralis, the ends of both fast-twitch glycolytic and fast-twitch oxidative-glycolytic fibre types express MyHC isoform(s) characteristic of their earlier development. Thus, we extend our findings on chicken to another species and an additional muscle fibre type. Retention of developmental MyHC isoform(s) within the tapered ends of mature muscle fibres may be more widespread than is currently appreciated.
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Alder C (1978) Gelatin-chrome alum: a better section adhesive. Histologic J 8: 115.
Bandman E, Bourke DL, Wick M (1990) Regulation of myosin heavy chain expression during development, maturation, and regeneration in avian muscles: The role of myogenic and non-myogenic factors. In: Pette D, ed. The Dynamic State of Muscle Fibers. Berlin: Walter de Gruyter, pp. 127-138.
Bandman E, Moore LA, Arrizubieta MJ, Tidyman WE, Herman L, Wick M (1994) The evolution of the chicken sarcomeric myosin heavy chain multigene family. Soc Gen Physiol Ser 49: 129-139.
Caldwell JH, Milton RL (1988) Sodium channel distribution in normal and denervated rodent and snake skeletal muscle. J Physiol (London) 401: 145-161.
Condon K, Astrow HS, Thompson WJ (1992) The role of innervation in the differentiation of early muscle fiber types in the rat. In: Kelly AM, Blau HM, eds. Neuromuscular Development and Disease. New York: Raven Press Ltd., pp. 239-250.
Crow MT, Stockdale FE (1986) Myosin expression and specialization among the earliest muscle fibers of the developing avian limb. Dev Biol 113: 238-254.
Daniels MP (1997) Intercellular communication that mediates formation of the neuromuscular junction. Mol Neurobiol 14: 143-170.
Dial KP (1992) Activity patterns of the wing muscles of the pigeon (Columba livia) during different modes of flight. J Exp Zool 262: 357-373.
Dix DJ, Eisenberg BR (1990) Myosin mRNA accumulation and myofibrillogenesis at the myotendinous junction of skeletal muscle fibers. J Cell Biol 111: 1885-1894.
Dubowitz V (1985) Muscle Biopsy a Practical Approach. Philadelphia: Bailliere-Tindall.
Fredette BJ, Landmesser LT (1991) A reevaluation of the role of innervation in primary and secondary myogenesis in developing chick muscle. Dev Biol 143: 19-35.
Gaunt AS, Gans C (1992) Serially arranged myofibers: an unappreciated variant in muscle architecture. Experientia 48: 864-868.
George JC, Berger AJ (1966) Avian Myology. NewYork: Academic Press.
Gille U, Salomon F-V, Kattein S (1998) Posthatching myofiber development in the m. pectoralis of white Pekin ducks. Anat Rec 250: 154-158.
Hartley RS, Bandman E, Yablonka-Reuveni Z (1991) Myoblasts from fetal and adult skeletal muscle regulate myosin expression differently. Dev Biol 148: 249-260.
Hijikata T, Ishikawa H (1997) Functional morphology of serially linked skeletal muscle fibers. Acta Anat 159: 99-107.
Navarette R, Vrbova G (1993) Activity-dependent interactions between motoneurones and muscles: their role in the development of the motor unit. Prog Neurobiol 41: 93-124.
Raikow RJ (1985) Locomotor systems: In: King AS, McLelland J, eds. Form and Function of Birds. Vol 3, New York: Academic Press, pp. 57-146.
Rathgeber EE, Rosser BWC (1998) Increase in oxidative capacity of pigeon pectoralis muscle before and after fledging. Can J Zool 76: 1778-1782.
Reiser PJ, Greaser ML, Moss RL (1996) Contractile properties and protein isoforms of single fibres from the chicken pectoralis red strip muscle. J Physiol (London) 493: 553-562.
Rosser BWC, George JC (1986) The avian pectoralis: histochemical characterization and distribution of muscle fiber types. Can J Zool 64: 1174-1185.
Rosser BWC, Waldbillig DM, Lovo SD, Armstrong JD, Bandman E (1995) Myosin heavy chain expression within the tapered ends of skeletal muscle fibers. Anat Rec 242: 462-470.
Rosser BWC, Wick M, Waldbillig DM, Bandman E (1996) Heterogeneity of myosin heavy chain expression in fast-twitch fiber types of mature avian pectoralis muscle. Biochem Cell Biol 74: 715-728.
Rosser BWC, Wick M, Waldbillig DM, Wright D-J, Farrar CM, Bandman E (1998) Expression of myosin heavy chain isoforms during development of domestic pigeon pectoralis muscle. Int JDev Biol 42: 653-661.
Rushbrook JI, Huang JM, Weiss C, Yao TT, Baez-Siconolfi L, Becker E (1998) Protein and mRNA analysis of myosin heavy chain in developing avian pectoralis major muscle. J Musc Res Cell Motil 19: 157-168.
Sanes RJ (1997) Genetic analysis of postsynaptic differentiation at the vertebrate neuromuscular junction. Curr Opin Neurobiol 7: 93-100.
Sellers JR, Goodson HV (1995) Motor Proteins 2: myosin. Protein Profile 2(12): 1323-1423.
Sibley CG, Ahlquist JE (1990) Phylogeny and Classification of Birds a Study in Molecular Evolution. New Haven: Yale University Press.
Swatland HJ (1981) Allometric growth of histochemical types of muscle fibers in ducks. Growth 45: 58-65.
Swatland HJ (1982) Elimination of sarcoplasmic argyrophilia in the delineation of muscle fibre boundaries with silver. Mikroskopie 39: 317-322.
Tidyman WE, Moore LA, Bandman E (1997) Expression of fast myosin heavy chain transcripts in developing and dystrophic chicken skeletal muscle. Dev Dyn 208: 491-504.
Tobalske BW, Olson NE, Dial KP (1997) Flight style of the blackbilled magpie: variation in wing kinematics, neuromuscular control, and muscle composition. J Exp Zool 279: 313-329.
Torrella JR, Fouces V, Palomeque J, Viscor G (1993) Innervation distribution pattern, nerve ending structure, and fiber types in pigeon skeletal muscle. Anat Rec 237: 178-186.
Torrella JR, Fouces V, Palomeque J, Viscor G (1998) Capillarity and fiber types in locomotory muscles of wild common coots, Fulica atra. J Morphol 237: 147-164.
Trotter JA (1991) Dynamic shape of tapered skeletal muscle fibers. J Morphol 207: 211-223.
Trotter JA (1993) Functional morphology of force transmission in skeletal muscle. A brief review. Acta Anat 146: 205-222.
Trotter JA, Salgado JD, Ozbaysal R, Gaunt AS (1992) The composite structure of quail pectoralis muscle. J Morphol 212: 27-35.
Walton J, Karpati G, Hilton-Jones D (1994) Disorders of Voluntary Muscle. Avon: The Bath Press.
Washabaugh CH, Ontell MP, Shan Z, Hoffman EP, Ontell M (1998) Role of the nerve in determining fetal skeletal muscle phenotype. Dev Dyn 211: 177-190.
Weiss A, Leinwand LA (1996) The mammalian myosin heavy chain gene family. Annu Rev Cell Dev Biol 12: 417-439.
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Bartnik, B.L., Waldbillig, D.M., Bandman, E. et al. Persistent Expression of Developmental Myosin Heavy Chain Isoforms in the Tapered Ends of Adult Pigeon Pectoralis Muscle Fibres. Histochem J 31, 321–329 (1999). https://doi.org/10.1023/A:1003770018926
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DOI: https://doi.org/10.1023/A:1003770018926