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Cross-bridge kinetics of fast and slow fibres of cat jaw and limb muscles: correlations with myosin subunit composition

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Abstract

Mechanical properties of the jaw-closing muscles of the cat are poorly understood. These muscles are known to differ in myosin and fibre type compositions from limb muscles. This work aims to correlate mechanical properties of single fibres in cat jaw and limb muscles with their myosin subunit compositions. The stiffness minimum frequency, fmin, which reflects isometric cross-bridge kinetics, was measured in Ca2+-activated glycerinated fast and slow fibres from cat jaw and limb muscles for temperatures ranging between 15 and 30°C by mechanical perturbation analysis. At 15°C, fmin was 0.5 Hz for limb-slow fibres, 4–6 Hz for jaw-slow fibres, and 10–13 Hz for limb-fast and jaw-fast fibres. The activation energy for fmin obtained from the slope of the Arrhenius plot for limb-slow fibres was 30–40% higher than values for the other three types of fibres. SDS-PAGE and western blotting using highly specific antibodies verified that limb-fast fibres contained IIA or IIX myosin heavy chain (MyHC). Jaw-fast fibres expressed masticatory MyHC while both jaw-fast and jaw-slow fibres expressed masticatory myosin light chains (MLCs). The nucleotide sequences of the 3′ ends of the slow MyHC cDNAs isolated from cat masseter and soleus cDNA libraries showed identical coding and 3′-untranslated regions, suggesting that jaw-slow and limb-slow fibres express the same slow MyHC gene. We conclude that the isometric cross-bridge cycling kinetics of jaw-fast and limb-fast fibres detected by fmin are indistinguishable in spite of differences in MyHC and light chain compositions. However, jaw-slow fibres, in which the same slow MyHCs are found in combination with MLCs of the jaw type, show enhanced cross-bridge cycling kinetics and reduced activation energy for cross-bridge detachment.

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References

  • Abbott RH (1972) An interpretation of the effects of fiber length and calcium on the mechanical properties of insect flight muscle. Cold Spring Harb Symp Quant Biol 37:647–654

    Google Scholar 

  • Andruchov O, Andruchova O, Wang Y, Galler S (2004) Kinetic properties of myosin heavy chain isoforms in mouse skeletal muscle: comparison with rat, rabbit, and human and correlation with amino acid sequence. Am J Physiol Cell Physiol 287:C1725–C1732

    Article  PubMed  CAS  Google Scholar 

  • Andruchov O, Andruchova O, Galler S (2006a) Fine-tuning of cross-bridge kinetics in cardiac muscle of rat and mouse by myosin light chain isoforms. Pflugers Arch 452:667–673

    Article  PubMed  CAS  Google Scholar 

  • Andruchov O, Andruchova O, Wang Y, Galler S (2006b) Dependence of cross-bridge kinetics on myosin light chain isoforms in rabbit and rat skeletal muscle fibres. J Physiol 571:231–242

    Article  PubMed  CAS  Google Scholar 

  • Bárány M (1967) ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 50:197–218

    Article  PubMed  Google Scholar 

  • Bottinelli R (2001) Functional heterogeneity of mammalian single muscle fibres: do myosin isoforms tell the whole story? Pflugers Arch 443:6–17

    Article  PubMed  CAS  Google Scholar 

  • Bottinelli R, Betto R, Schiaffino S, Reggiani C (1994a) Unloaded shortening velocity and myosin heavy chain and alkali light chain isoform composition in rat skeletal muscle fibres. J Physiol 478:341–349

    PubMed  CAS  Google Scholar 

  • Bottinelli R, Canepari M, Reggiani C, Stienen GJM (1994b) Myofibrillar ATPase activity during isometric contraction and isomyosin composition in rat single skinned muscle fibres. J Physiol 481:663–675

    PubMed  CAS  Google Scholar 

  • Bottinelli R, Canepari M, Cappelli V, Reggiani C (1995) Maximum speed of shortening and ATPase activity in atrial and ventricular myocardia of hyperthyroid rats. Am J Physiol Cell Physiol 38:C785–C790

    Google Scholar 

  • Burke RE, Tsairis P (1974) The correlation of physiological properties with histochemical characteristics in single muscle units. Ann NY Acad Sci 228:145–158

    Article  PubMed  CAS  Google Scholar 

  • Close R, Hoh JFY (1967) Force: velocity properties of kitten muscles. J Physiol 192:815–822

    PubMed  CAS  Google Scholar 

  • Cuminetti R, Rossmanith GH (1980) Small amplitude non-linearities in the mechanical response of an asynchronous flight muscle. J Muscle Res Cell Motil 1:345–356

    Article  PubMed  CAS  Google Scholar 

  • D’Antona G, Megighian A, Bortolotto S, Pellegrino MA, Ragona RM, Staffieri A, Bottinelli R, Reggiani C (2002) Contractile properties and myosin heavy chain isoform composition in single fibre of human laryngeal muscles. J Muscle Res Cell Motil 23:187–195

    Article  PubMed  CAS  Google Scholar 

  • Dechesne C, Leger J, Bouvagnet P, Claviez M, Leger JJ (1985) Fractionation and characterization of two molecular variants of myosin from adult human atrium. J Mol Cell Cardiol 17:753–768

    Article  PubMed  CAS  Google Scholar 

  • Galler S, Schmitt TL, Pette D (1994) Stretch activation, unloaded shortening velocity, and myosin heavy chain isoforms of rat skeletal muscle fibres. J Physiol 478:513–521

    PubMed  CAS  Google Scholar 

  • Galler S, Hilber K, Pette D (1997) Stretch activation and myosin heavy chain isoforms of rat, rabbit and human skeletal muscle fibres. J Mol Cell Cardiol 18:441–448

    CAS  Google Scholar 

  • Hilber K, Galler S, Gohlsch B, Pette D (1999) Kinetic properties of myosin heavy chain isoforms in single fibers from human skeletal muscle. FEBS Lett 455:267–270

    Article  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, 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

    Article  PubMed  CAS  Google Scholar 

  • Hoh JFY, McGrath PA, Hale PT (1978) Electrophoretic analysis of multiple forms of rat cardiac myosin: effects of hypophysectomy and thyroxine replacement. J Mol Cell Cardiol 10:1053–1076

    Article  PubMed  CAS  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 JFY, Walker ML, Lin JJC (1989) A unique isoform of skeletal tropomyosin in cat jaw-closing muscle and its developmental expression. Proc Aust Physiol Pharmacol Soc 20:192P

    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 JF, Kang LH, Sieber LG, Lim JH, Zhong WW (2006) Myosin isoforms and fibre types in jaw-closing muscles of Australian marsupials. J Comp Physiol [B] 176:685–695

    CAS  Google Scholar 

  • Hoh JF, Kim Y, Lim JH, Sieber LG, Lucas CA, Zhong WW (2007) Marsupial cardiac myosins are similar to those of eutherians in subunit composition and in the correlation of their expression with body size. J Comp Physiol [B] 177:153–163

    CAS  Google Scholar 

  • Hoh JFY, Hughes S, Walker ML, Kang LHD, Everett AW (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 Appl Myol 1:285–294

    Google Scholar 

  • 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 

  • Katz B (1939) The relation between force and speed in muscle contraction. J Physiol 96:201–218

    Google Scholar 

  • Kawai M, Brandt PW (1980) Sinusoidal analysis: a high resolution method for correlating biochemical reactions with physiological processes in activated skeletal muscles of rabbit, frog and crayfish. J Muscle Res Cell Motil 1:279–303

    Article  PubMed  CAS  Google Scholar 

  • Kirkeby S (1996) A monoclonal anticarbohydrate antibody detecting superfast myosin in the masseter muscle. Cell Tissue Res 283:85–92

    Article  PubMed  CAS  Google Scholar 

  • Kitsis RN, Scheuer J (1996) Functional significance of alterations in cardiac contractile protein isoforms. Clin Cardiol 19:9–18

    Article  PubMed  CAS  Google Scholar 

  • Larsson L, Moss RL (1993) Maximum velocity of shortening in relation to myosin isoform composition in single fibres from human skeletal muscles. J Physiol 472:595–614

    PubMed  CAS  Google Scholar 

  • Linari M, Bottinelli R, Pellegrino MA, Reconditi M, Reggiani C, Lombardi V (2004) The mechanism of the force response to stretch in human skinned muscle fibres with different myosin isoforms. J Physiol 554:335–352

    Article  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 Motility 16:368–378

    Article  CAS  Google Scholar 

  • Lucas CA, Kang LH, Hoh JF (2000) Monospecific antibodies against the three mammalian fast limb myosin heavy chains. Biochem Biophys Res Commun 272:303–308

    Article  PubMed  CAS  Google Scholar 

  • Oakley BR, Kirsch DR, Morris NR (1980) A simplified ultrasensitive silver stain for detecting proteins in polyacrylamide gels. Anal Biochem 105:361–363

    Article  PubMed  CAS  Google Scholar 

  • Orvis JS, Cardinet GH (1981) Canine muscle fiber types and susceptibility of masticatory muscles to myositis. Muscle Nerve 4:354–359

    Article  PubMed  CAS  Google Scholar 

  • Perrin DD, Sayce IG (1967) Computer calculation of equilibrium concentrations in mixtures of metal ions and complexing species. Talanta 14:833–842

    Article  CAS  PubMed  Google Scholar 

  • Petit J, Chua M, Hunt CC (1993) Maximum shortening speed of motor units of various types in cat lumbrical muscles. J Neurophysiol 69:442–448

    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 

  • Rome LC (1992) Scaling of muscle fibres and locomotion. J Exp Biol 168:243–252

    PubMed  CAS  Google Scholar 

  • Rome LC, Cook C, Syme DA, Connaughton MA, Ashley-Ross M, Klimov A, Tikunov B, Goldman YE (1999) Trading force for speed: why superfast crossbridge kinetics leads to superlow forces. Proc Natl Acad Sci USA 96:5826–5831

    Article  PubMed  CAS  Google Scholar 

  • Rossmanith GH (1986) Tension responses of muscle to n-step pseudo-random length reversals: a frequency domain representation. J Muscle Res Cell Motil 7:299–306

    Article  PubMed  CAS  Google Scholar 

  • Rossmanith GH, Tjokorda OB (1998) Relationship between isometric and isotonic mechanical parameters and cross-bridge kinetics. Clin Exp Pharmacol Physiol 25:522–535

    Article  PubMed  CAS  Google Scholar 

  • Rossmanith GH, Hoh JFY, 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 

  • Rossmanith GH, Hamilton AM, Hoh JFY (1995) Influence of myosin isoforms on tension cost and crossbridge kinetics in skinned rat cardiac muscle. Clin Exp Pharmacol Physiol 22:423–429

    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 Musc Res Cell Motil 2:415–438

    Article  CAS  Google Scholar 

  • Rowlerson A, Heizmann CW, Jenny E (1983) Type-specific proteins of single IIM fibres from cat muscle. Biochem Biophys Res Commun 113:519–525

    Article  PubMed  CAS  Google Scholar 

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

    Article  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 

  • Shelton GD, Cardinet GH III, Bandman E (1987) Canine masticatory muscle disorders: a study of 29 cases. Muscle Nerve 10:753–766

    Article  PubMed  CAS  Google Scholar 

  • Swynghedauw B (1986) Developmental and functional adaptation of contractile proteins in cardiac and skeletal muscles. Physiol Rev 66:710–771

    PubMed  CAS  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 

  • Talmadge RJ, Grossman EJ, Roy RR (1996) Myosin heavy chain composition of adult feline (Felis catus) limb and diaphragm muscles. J Exp Zool 275:413–420

    Article  PubMed  CAS  Google Scholar 

  • Taylor A, Cody FWJ, Bosley MA (1973) Histochemical and mechanical properties of the jaw muscles of the cat. Exp Neurol 38:99–109

    Article  PubMed  CAS  Google Scholar 

  • Thorson J, White DCS (1983) Role of cross-bridge distortion in the small-signal mechanical dynamics of insect and rabbit striated muscle. J Physiol 343:59–84

    PubMed  CAS  Google Scholar 

  • Toniolo L, Patruno M, Maccatrozzo L, Pellegrino MA, Canepari M, Rossi R, D’Antona G, Bottinelli R, Reggiani C, Mascarello F (2004) Fast fibres in a large animal: fibre types, contractile properties and myosin expression in pig skeletal muscles. J Exp Biol 207:1875–1886

    Article  PubMed  CAS  Google Scholar 

  • Wu X, Li ZF, Brooks R, Komives EA, Torpey JW, Engvall E, Gonias SL, Shelton GD (2007) Autoantibodies in canine masticatory muscle myositis recognize a novel myosin binding protein-C family member. J Immunol 179:4939–4944

    PubMed  CAS  Google Scholar 

  • Yamaguchi M (2007) Structure and function of masticatory (superfast) myosin. J Oral Biosci 49:216–218

    Article  Google Scholar 

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Acknowledgements

This work was supported by the Australian Research Council and the National Health and Medical Research Council of Australia. We thank Dr. Jean Leger for the gift of the 2D11 monoclonal antibody and Prof. Bogden Dreher for cat muscle tissues.

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Authors and Affiliations

  1. Discipline of Physiology and the Bosch Institute, University of Sydney, Building F13, Sydney, NSW, 2006, Australia

    Joseph F. Y. Hoh, Zhao-Bo Li, Han Qin & Michael K. H. Hsu

  2. Department of Computing, Division of Information and Communication Sciences, Macquarie University, Sydney, NSW, 2109, Australia

    Gunther H. Rossmanith

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  1. Joseph F. Y. Hoh
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  2. Zhao-Bo Li
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  4. Michael K. H. Hsu
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Correspondence to Joseph F. Y. Hoh.

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Hoh, J.F.Y., Li, ZB., Qin, H. et al. Cross-bridge kinetics of fast and slow fibres of cat jaw and limb muscles: correlations with myosin subunit composition. J Muscle Res Cell Motil 28, 329–341 (2007). https://doi.org/10.1007/s10974-008-9129-x

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  • DOI: https://doi.org/10.1007/s10974-008-9129-x

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