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The development of muscle fiber type identity in zebrafish cranial muscles

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Abstract

Cranial skeletal muscles underlie breathing, eating, and eye movements. In most animals, at least two types of muscle fibers underlie these critical functions: fast and slow muscle fibers. We describe here the anatomical distribution of slow and fast twitch muscle in the zebrafish (Danio rerio) head in the adult and at an early larval stage just after feeding has commenced. We found that all but one of the cranial muscles examined contain both slow and fast muscle fibers, but the relative proportion of slow muscle in each varies considerably. As in the trunk, slow muscle fibers are found only in an anatomically restricted zone of each muscle, usually on the periphery. The relative proportion of slow and fast muscle in each cranial muscle changes markedly with development, with a pronounced decrease in the proportion of slow muscle with ontogeny. We discuss our results in relation to the functional roles of each muscle in larval and adult life and compare findings among a variety of vertebrates.

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References

  • Akster HA, Osse JWM (1978) Muscle-fiber types in head muscles of Perch Perca-Fluviatilis (L), teleostei—histochemical and electromyographical study. Neth J Zool 28:94–110

    Google Scholar 

  • Anker GC (1978) Morphology of head-muscles of a generalized Haplochromis species—Haplochromis-Elegans Trewavas 1933 (Pisces, Cichlidae). Neth J Zool 28:234–271

    Google Scholar 

  • Bader D, Masaki T, Fischman DA (1982) Immunochemical analysis of myosin heavy-chain during avian myogenesis in vivo and in vitro. J Cell Biol 95:763–770

    Google Scholar 

  • Barends PMG (1979) Relation between fiber type composition and function in the jaw adductor muscle of the Perch (Perca-Fluviatilis, L)—histochemical-study. P K Ned Akad C Biol 82:147–164

    Google Scholar 

  • Cobos AR, Segade LAG, Fuentes I (2001) Muscle fibre types in the suprahyoid muscles of the rat. J Anat 198:283–294

    Google Scholar 

  • Currie PD, Ingham PW (2001) Induction and patterning of embryonic skeletal muscle cells in the Zebrafish. In: Johnston IA (ed) Muscle development and growth. Academic, San Diego, pp 1–14

    Google Scholar 

  • Dent JA, Polson AG, Klymkowsky MW (1989) A whole-mount immunocytochemical analysis of the expression of the intermediate filament protein vimentin in Xenopus. Development 105:61–74

    Google Scholar 

  • Engel WK, Irwin RL (1967) A histochemical-physiological correlation of frog skeletal muscle fibers. Am J Physiol 213:511–518

    Google Scholar 

  • Ferry-Graham LA, Lauder GV (2001) Aquatic prey capture in ray-finned fishes: a century of progress and new directions. J Morphol 248:99–119

    Article  PubMed  Google Scholar 

  • Fetcho JR, Liu KS (1998) Zebrafish as a model system for studying neuronal circuits and behavior. Ann N Y Acad Sci 860:333–345

    Google Scholar 

  • Hernandez LP (2000) Intraspecific scaling of feeding mechanics in an ontogenetic series of zebrafish, Danio rerio. J Exp Biol 203:3033–3043

    Google Scholar 

  • Hernandez LP, Barresi MJF, Devoto SH (2002) Functional morphology and developmental biology of zebrafish: reciprocal illumination from an unlikely couple. Integr Compar Biol 42:222–231

    Google Scholar 

  • Huang RJ, Zhi QX, Izpisua-Belmonte JC, Christ B, Patel K (1999) Origin and development of the avian tongue muscles. Anat Embryol 200:137–152

    Article  PubMed  Google Scholar 

  • Johnston IA, Patterson S, Ward P, Goldspink G (1974) Histochemical demonstration of myofibrillar adenosine-triphosphatase activity in fish muscle. Can J Zool 52:871–877

    Google Scholar 

  • Lannergren J, Smith RS (1966) Types of muscle fibres in toad skeletal muscle. Acta Physiol Scand 68:263–274

    Google Scholar 

  • Lassar AB, Buskin JN, Lockshon D, Davis RL, Apone S, Hauschka SD, Weintraub H (1989) MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell 58:823–831

    Google Scholar 

  • Lauder GV (1985) Aquatic feeding in lower vertebrates. In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional vertebrate morphology. Harvard University Press, Cambridge, pp 230–261

    Google Scholar 

  • Liem KF (1985) Ventilation. In: Hildebrand M, Bramble DM, Liem KF, Wake DB (eds) Functional vertebrate morphology. Harvard University Press, Cambridge, pp 185–209

    Google Scholar 

  • Liem KF (1991) A functional approach to the development of the head in teleosts: implications on constructional morphology and constraints. In: Schmidt-Kittler N, Vogel K (eds) Constructional morphology and evolution. Springer, Berlin Heidelberg New York, pp 231–241

    Google Scholar 

  • Mallatt J (1996) Ventilation and the origin of jawed vertebrates: a new mouth. Zool J Linn Soc Lond 117:329–404

    Google Scholar 

  • Marcucio RS, Noden DM (1999) Myotube heterogeneity in developing chick craniofacial skeletal muscles. Dev Dyn 214:178–194

    Google Scholar 

  • Miller JB, Crow MT, Stockdale FE (1985) Slow and fast myosin heavy chain content defines three types of myotubes in early muscle cell cultures. J Cell Biol 101:1643–1650

    Google Scholar 

  • Mosse PRL, Hudson RCL (1977) Functional roles of different muscle-fiber types identified in myotomes of marine teleosts—behavioral, anatomical and histochemical study. J Fish Biol 11:417–430

    Google Scholar 

  • Noden DM (1983) The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev Biol 96:144–165

    CAS  PubMed  Google Scholar 

  • Ojha J, Datta Munshi JS (1975) Cytochemical differentiation of muscle fibers by succinic dehydrogenase (SDH) activity in the respiratory muscles of an air-breathing fish, Channa punctatus (Bloch). Anat Anz 138:62–68

    Google Scholar 

  • Ono RD, Kaufman L (1983) Muscle-fiber types and functional demands in feeding mechanisms of fishes. J Morphol 177:69–87

    Google Scholar 

  • Osse JWM (1969) Functional morphology of the head of the perch (Perca fluviatilis): an electromyographical study. Neth J Zool 19:289–392

    Google Scholar 

  • Osse JWM (1990) Form changes in fish larvae in relation to changing demands of function. Neth J Zool 40:362–385

    Google Scholar 

  • Osse JWM, van den Boogaart JGM, van Snik GMJ, van der Sluys L (1997) Priorities during early growth of fish larvae. Aquaculture 155:249–258

    Google Scholar 

  • Parichy DM, Johnson SL (2001) Zebrafish hybrids suggest genetic mechanisms for pigment pattern diversification in Danio. Dev Genes Evol 211:319–328

    Google Scholar 

  • van Raamsdonk W, Tekronnie G, Pool CW, van de Laarse W (1980) An immune histochemical and enzymic characterization of the muscle fibres in myotomal muscle of the teleost Brachydanio rerio, Hamilton-Buchanan. Acta Histochem 67:200–216

    Google Scholar 

  • Scapolo PA, Luprano S, Biscotto A, Veggetti A, Mascarello F (1989) The adductor mandibulae muscle in teleost fish with protrusible or non-protrusible jaws—a histochemical and immunohistochemical study. Anat Anzeiger 168:205–221

    Google Scholar 

  • Schilling TF, Kimmel CB (1994) Segment and cell type lineage restrictions during pharyngeal arch development in the zebrafish embryo. Development 120:483–494

    Google Scholar 

  • Schilling TF, Kimmel CB (1997) Musculoskeletal patterning in the pharyngeal segments of the zebrafish embryo. Development 124:2945–2960

    Google Scholar 

  • Sibbing FA (1982) Pharyngeal mastication and food transport in the Carp (Cyprinus-Carpio L)—a cineradiographic and electro-myographic study. J Morphol 172:223–258

    Google Scholar 

  • Stickney HL, Barresi MJ, Devoto SH (2000) Somite development in zebrafish. Dev Dyn 219:287–303

    Google Scholar 

  • Stoiber W, Haslett JR, Sanger AM (1999) Myogenic patterns in teleosts: what does the present evidence really suggest? J Fish Biol 55(suppl A):84–99

    Google Scholar 

  • Suwa M, Nakamura T, Katsuta S (1996) Heredity of muscle fiber composition and correlated response of the synergistic muscle in rats. Am J Physiol Reg I 40:R432–R436

    Google Scholar 

  • Suwa M, Miyazaki T, Nakamura T, Sasaki S, Ohmori H, Katsuta S (1998) Hereditary dominance of fast-twitch fibers in skeletal muscles and relation of thyroid hormone under physiological conditions in rats. Acta Anat 162:40–45

    Google Scholar 

  • Throckmorton GS, Saubert CW (1982) Histochemical properties of some jaw muscles of the lizard Tupinambis-Nigropunctatus (Teiidae). Anat Rec 203:345–352

    Google Scholar 

  • Watanabe K, Sasaki F, Takahama H, Iseki H (1980) Histogenesis and distribution of red and white muscle-fibers of Urodelan larvae. J Anat 130:83–96

    Google Scholar 

  • Westneat MW (1990) Feeding mechanics of teleost fishes (Labridae, Perciformes)—a test of 4-bar linkage models. J Morphol 205:269–295

    Google Scholar 

  • Westneat MW (2003) A biomechanical model for analysis of muscle force, power output and lower jaw motion in fishes. J Theor Biol 223:269–281

    Google Scholar 

  • Wigmore PM, Evans DJ (2002) Molecular and cellular mechanisms involved in the generation of fiber diversity during myogenesis. Int Rev Cytol 216:175–232

    Google Scholar 

  • Winterbottom R (1974) Descriptive synonymy of striated muscles of Teleostei. Proc Acad Nat Sci Phila 125:225–317

    Google Scholar 

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Acknowledgements

We thank Khawla Ziyadeh, Carina Uraiqat, and Juhi Shukla for technical assistance and Ron Gordon and Sera Solovei for animal care. We thank Charles Kimmel and Thomas Schilling for helpful comments on the manuscript. This work was supported by NIH grant HD22486 and a Donaghue Foundation Investigator Award to SHD and by a George Washington University Facilitating Fund Award to LPH. MF20 developed by David Bader and Don Fishman was obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by the University of Iowa, Department of Biological Sciences, Iowa City, IA, USA. We thank Frank Stockdale, Stanford University, for generously providing S58.

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  1. L. Patricia Hernandez

    Present address: Department of Biological Sciences, George Washington University, 2023 G. Street NW, Washington, DC, 20052, USA

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  1. Biology Department, Wesleyan University, Middletown, CT, 06459, USA

    L. Patricia Hernandez, Sara E. Patterson & Stephen H. Devoto

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  1. L. Patricia Hernandez
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  2. Sara E. Patterson
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  3. Stephen H. Devoto
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Correspondence to Stephen H. Devoto.

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Hernandez, L.P., Patterson, S.E. & Devoto, S.H. The development of muscle fiber type identity in zebrafish cranial muscles. Anat Embryol 209, 323–334 (2005). https://doi.org/10.1007/s00429-004-0448-4

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