Skip to main content

Advertisement

SpringerLink
Log in

Myosin isoforms and fibre types in jaw-closing muscles of australian marsupials

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Myosin heavy chains (MyHCs) and fibre types in the masseter muscle of seven species of Australian marsupials (brushtail and ringtail possums, bettong, bandicoot, dunnart, two species of antechinuses) spanning three orders were studied by native myosin electrophoresis, SDS-PAGE, immunoblotting and immunohistochemistry. We found only two fibre types in the masseter muscles of these animals: (1) masticatory fibres expressing masticatory MyHC, and (2) hybrid α/β fibres that co-express α-cardiac and β-cardiac MyHCs. Masticatory fibres predominate in most species, being appropriate for predation or for chewing tough vegetable matter. The relative abundance of α/β fibres decreased from 60% to 0 in the order: ringtail possum > brushtail possum > bettong > bandicoot > dunnart/antechinus. These variations in masseter fibre type are correlated with decreasing amounts of vegetable matter in the diets of these animals. The results are in contrast to earlier work on masseter fibres of macropodids that expressed α-cardiac MyHC almost homogeneously. The fact that the bettong (Family: Potoroidae), which belong to the same marsupial superfamily (Macropodoidea) as kangaroos and wallabies (Family: Macropodidae), has not specialized in the exclusive expression of α-cardiac MyHC as members of the latter family suggests that this specialization was of recent phylogenetic origin (30 million years before present).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

HRP:

horseradish peroxidase

MyHC:

Myosin heavy chain

mAb:

Monoclonal antibody

References

  • Bredman JJ, Wessels A, Weijs WA, Korfage JAM, Soffers CAS, Moorman AFM (1991) Demonstration of cardiac-specific myosin heavy chain in masticatory muscles of human and rabbit. Histochem J 23:160–170

    Article  PubMed  CAS  Google Scholar 

  • Bredman JJ, Weijs WA, Moorman AFM (1992) Presence of cardiac alpha-myosin correlates with histochemical myosin Ca++-ATPase activity in rabbit masseter muscle. Histochem J 24:260–265

    Article  PubMed  CAS  Google Scholar 

  • Cappelli V, Bottinelli R, Poggesi C, Moggio R, Reggiani C (1989) Shortening velocity and myosin and myofibrillar ATPase activity related to myosin isoenzyme composition during postnatal development in rat myocardium. Circ Res 65:446–457

    PubMed  CAS  Google Scholar 

  • Dawson TJ (1995) Kangaroos—biology of the largest marsupials. University of New South Wales Press, Sydney

    Google Scholar 

  • Fitzsimons RB, Hoh JFY (1983) Myosin isoenzymes in fast-twitch and slow-twitch muscles of normal and dystrophic mice. J Physiol 343:539–550

    PubMed  CAS  Google Scholar 

  • Hall S (1980) The diets of two coexisting species of Antechinus (Marsupialia: Dasyuridae). Aust Wildl Res 7:365–378

    Article  Google Scholar 

  • Heinsohn GE (1966) Ecology and reproduction of the Tasmanian bandicoots (Perameles gunnii and Isoodon obesulus). Univ Calif Publ Zool 80:1–107

    Google Scholar 

  • Hoh JFY (1992) Muscle fiber types and function. Curr Opin Rheumatol 4:801–808

    PubMed  CAS  Google Scholar 

  • Hoh JF (2002) ‘Superfast’ or masticatory myosin and the evolution of jaw-closing muscles of vertebrates. J Exp Biol 205:2203–2210

    PubMed  Google Scholar 

  • Hoh JFY, Yeoh GPS (1979) Rabbit skeletal myosin isoenzymes from foetal, fast-twitch and slow-twitch muscles. Nature 280:321–323

    Article  PubMed  CAS  Google Scholar 

  • Hoh JFY, McGrath PA, White RI (1976) Electrophoretic analysis of multiple forms of myosin in fast-twitch and slow-twitch muscles of the chick. Biochem J 157:87–95

    PubMed  CAS  Google Scholar 

  • Hoh JFY, Kwan BTS, Dunlop C, Kim BH (1980) Effects of nerve cross-union and cordotomy on myosin isoenzymes in fast-twitch and slow-twitch muscles of the rat. In: Pette D (ed) Plasticity of muscle Walter de Gruyter, Berlin, pp 339–352

    Google Scholar 

  • Hoh JFY, Hughes S, Chow C, Hale PT, Fitzsimons RB (1988) 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

    Article  PubMed  CAS  Google Scholar 

  • Hoh JF, Kim Y, Sieber LG, Zhong WW, Lucas CA (2000) Jaw-closing muscles of kangaroos express alpha-cardiac myosin heavy chain. J Muscle Res Cell Motil 21:673–680

    Article  PubMed  CAS  Google Scholar 

  • Hoh JFY, Lim JHY, Kang LDH, Lucas CA (2001) Expression of superfast myosin in the jaw-closing muscles of Crocodylus porosus. In: Grigg GC, Seebacher F, Franklin CE (eds) Crocodilian biology and evolution Surrey Beatty, Chipping Norton, pp 156–164

    Google Scholar 

  • Hume ID (1999) Marsupial nutrition, Cambridge University Press, Cambridge

  • Kang LHD, Hughes S, Pettigrew JD, Hoh JFY (1994) Jaw-specific myosin heavy chain gene expression in sheep, dog, monkey, flying fox and microbat jaw-closing muscles. Basic Appl Myol 4:381–392

    Google Scholar 

  • Kato C, Saeki Y, Yanagisawa K (1985) Ca2+ sensitivities and transient tension responses to step-length stretches in feline mechanically-stripped single-fibre jaw-muscle preparations. Arch Oral Biol 30:429–432

    Article  PubMed  CAS  Google Scholar 

  • Lentle RG, Hume ID, Stafford KJ, Kennedy MB, Haslett S, Springett BP (2003) Comparison of tooth morphology and wear patterns in four species of wallabies. Aust J Zool 51:61–79

    Article  Google Scholar 

  • Lindman R, Eriksson PO, Thornell LE (1986) Histochemical enzyme profile of the masseter, temporal and lateral pterygoid muscles of the European hedgehog (Erinaceus europeaus). Arch Oral Biol 31:51–55

    Article  PubMed  CAS  Google Scholar 

  • Loiselle DS, Wendt IR, Hoh JF (1982) Energetic consequences of thyroid-modulated shifts in ventricular isomyosin distribution in the rat. J Muscle Res Cell Motil 3:5–23

    Article  PubMed  CAS  Google Scholar 

  • Lompre A-M, Nadal-Ginard B, Mahdavi V (1984) Expression of the cardiac ventricular α- and β-myosin heavy chain genes is developmentally and hormonally regulated. J Biol Chem 259:6437–6446

    PubMed  CAS  Google Scholar 

  • Lucas CA, Rughani A, Hoh JFY (1995) Expression of extraocular myosin heavy chain in rabbit laryngeal muscle. J Muscle Res Cell Motil 16:368–378

    Article  PubMed  CAS  Google Scholar 

  • Maccatrozzo L, Patruno M, Toniolo L, Reggiani C, Mascarello F (2004) Myosin heavy chain 2B isoform is expressed in specialized eye muscles but not in trunk and limb muscles of cattle. Eur J Histochem 48:357–366

    PubMed  CAS  Google Scholar 

  • Mascarello F, Aureli G, Vegetti A (1979) Muscoli masticatori: determinazione istochimica dei tipi di fibre muscolari. Quad Anat Prat 35:193–213

    Google Scholar 

  • Morton SR, Denny MJS, Read DG (1983) Habitat preferences and diets of sympatric Sminthopsis crassicaudata and S. macroura. (Marsupialia: Dasyuridae). Aust Mammal 6:29–34

    Google Scholar 

  • Pette D, Staron RS (1990) Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev Physiol Biochem Pharmacol 116:2–76

    Google Scholar 

  • Pope B, Hoh JFY, Weeds A (1980) The ATPase activities of rat cardiac myosin isoenzymes. FEBS Lett 118:205–208

    Article  PubMed  CAS  Google Scholar 

  • Qin H, Morris BJ, Hoh JFY (1994) Isolation and structure of cat superfast myosin light chain-2 cDNA and evidence for the identity of its human homologue. Biochem Biophys Res Commun 200:1277–1282

    Article  PubMed  CAS  Google Scholar 

  • Qin H, Hsu MK, Morris BJ, Hoh JF (2002) A distinct subclass of Mammalian striated myosins: structure and molecular evolution of ‘Superfast’ or masticatory Myosin heavy chain. J Mol Evol 55:544–552

    Article  PubMed  CAS  Google Scholar 

  • Rossmanith GH, Hoh JF, Kirman A, Kwan LJ (1986) Influence of V1 and V3 isomyosins on the mechanical behaviour of rat papillary muscle as studied by pseudo-random binary noise modulated length perturbations. J Muscle Res Cell Motil 7:307–319

    Article  PubMed  CAS  Google Scholar 

  • Rowlerson A (1994) An outline of fibre types in vertebrate skeletal muscle: histochemical identification and myosin isoforms. Basic Appl Myol 4:333–352

    Google Scholar 

  • Rowlerson A, Mascarello F, Veggetti A, Carpene E (1983) The fibre-type composition of the first branchial arch muscles in Carnivora and Primates. J Muscle Res Cell Motil 4:443–472

    Article  PubMed  CAS  Google Scholar 

  • Rowlerson A, Pope B, Murray J, Whalen RG, Weeds AG (1981) A novel myosin present in cat jaw-closing muscles. J Muscle Res Cell Motil 2:415–438

    Article  CAS  Google Scholar 

  • Saeki Y, Kato C, Satomi M, Yanagisawa K (1987a) ATPase activity and tension development in mechanically-skinned feline jaw muscle. Arch Oral Biol 32:207–210

    Article  CAS  Google Scholar 

  • Saeki Y, Kato C, Totsuka T, Yanagisawa K (1987b) Mechanical properties and ATPase activity in glycerinated cardiac muscle of hyperthyroid rabbit. Pflugers Arch 408:578–583

    Article  CAS  Google Scholar 

  • Sampson JC (1971) The biology of Bettongia penicillata, Gray 1837. PhD Thesis, University of Western Australia, Perth

  • Sanson GD (1989) Morphological adaptations of teeth to diets and feeding in the Macropodoidea. In: Grigg G, Jarman P, Hume I (eds) Kangaroos, wallabies and rat-kangaroos Surrey Beatty, Chipping Norton, pp 151–168

    Google Scholar 

  • Sata M, Sugiura S, Yamashita H, Momomura S, Serizawa T (1993) Dynamic interaction between cardiac myosin isoforms modifies velocity of actomyosin sliding in vitro. Circ Res 73:696–704

    PubMed  CAS  Google Scholar 

  • Sciote JJ, Kentish JC (1996) Unloaded shortening velocities of rabbit masseter muscle fibres expressing skeletal or alpha-cardiac myosin heavy chains. J Physiol 492:659–667

    PubMed  CAS  Google Scholar 

  • Sciote JJ, Rowlerson A (1998) Skeletal fiber types and spindle distribution in limb and jaw muscles of the adult and neonatal opossum, monodelphis domestica. Anat Rec 251:548–562

    Article  PubMed  CAS  Google Scholar 

  • Sciote JJ, Rowlerson AM, Carlson DS (1995) Myosin expression in the jaw-closing muscles of the domestic cat and american opossum. Arch Oral Biol 40:405–413

    Article  PubMed  CAS  Google Scholar 

  • Sciote JJ, Rowlerson AM, Hopper C, Hunt NP (1994) Fibre type classification and myosin isoforms in the human masseter muscle. J Neurol Sci 126:15–24

    Article  PubMed  CAS  Google Scholar 

  • Sfondrini G, Reggiani C, Gandini P, Bovenzi R, Pellegrino MA (1996) Adaptations of masticatory muscles to a hyperpropulsive appliance in the rat. Am J Orthod Dentofacial Orthop 110:612–617

    Article  PubMed  CAS  Google Scholar 

  • Stedman HH, Kozyak BW, Nelson A, Thesier DM, Su LT, Low DW, Bridges CR, Shrager JB, Minugh-Purvis N, Mitchell MA (2004) Myosin gene mutation correlates with anatomical changes in the human lineage. Nature 428:415–418

    Article  PubMed  CAS  Google Scholar 

  • Strahan R (1992) Encyclopedia of Australian Animals: Mammals. Angus and Robertson, Sydney

    Google Scholar 

  • Talmadge RJ, Roy RR (1993) Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J Appl Physiol 75:2337–2340

    PubMed  CAS  Google Scholar 

  • Thomson JA, Owen WH (1964) A field study of the Australian ringtail possum Pseudocheirus peregrinus (Marsupialia: Phalangeridae). Ecol Monogr 34:27–52

    Article  Google Scholar 

  • Toniolo L, Maccatrozzo L, Patruno M, Caliaro F, Mascarello F, Reggiani C (2005) Expression of eight distinct MHC isoforms in bovine striated muscles: evidence for MHC-2B presence only in extraocular muscles. J Exp Biol 208:4243–4253

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Health and Medical Research Council and the Australian Research Council. WWHZ is a recipient of the Faculty of Medicine Postgraduate Scholarship of the University of Sydney. We thank Prof. Terry Dawson of the University of NSW, Dr Kerry Withers of the University of Southern Queensland, Dr Peter Runham of the University of Western Australia and John Cossey of Sydney University for providing tissue samples. The experiments were done with the approval of the Animal Ethics Review Committee of the University of Sydney and comply with the current laws governing animal experimentation in Australia.

Author information

Authors and Affiliations

  1. Discipline of Physiology and Institute for Biomedical Research, School of Medical Sciences, Faculty of Medicine, Bldg F13, The University of Sydney, 2006, Sydney, NSW, Australia

    Joseph F. Y. Hoh, Lucia H. D. Kang, Louise G. Sieber, Jacqueline H. Y. Lim & Wendy W. H. Zhong

Authors
  1. Joseph F. Y. Hoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lucia H. D. Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Louise G. Sieber
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jacqueline H. Y. Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wendy W. H. Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joseph F. Y. Hoh.

Additional information

Communicated by I.D. Hume

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hoh, J.F.Y., Kang, L.H.D., Sieber, L.G. et al. Myosin isoforms and fibre types in jaw-closing muscles of australian marsupials. J Comp Physiol B 176, 685–695 (2006). https://doi.org/10.1007/s00360-006-0091-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-006-0091-x

Keywords

Search

Navigation