Correlation of dystrophin-glycoprotein complex and focal adhesion complex with myosin heavy chain isoforms in rat skeletal muscle

Acta Physiologica

Volumn 195, Issue 4, 2009, Pages 483-494

  Masuda, S ^a   Hayashi, T ^a   Hashimoto, T ^b   Taguchi, S ^c  

^a KYOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF HYOGO   (Japan)

^c Nara Sangyo University   (Japan)

Author keywords

Dystrophin; Force transmission; Integrin; Muscle fibre type; Myosin heavy chain; Sarcolemma

Indexed keywords

BETA1 INTEGRIN; DYSTROPHIN; FOCAL ADHESION KINASE; GLYCOPROTEIN; ISOPROTEIN; MYOSIN HEAVY CHAIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DIAPHRAGM MOVEMENT; EXTENSOR DIGITORUM LONGUS MUSCLE; FAST MUSCLE FIBER; GASTROCNEMIUS MUSCLE; HEART MUSCLE; HISTOCHEMISTRY; MALE; MUSCLE FORCE; NONHUMAN; PLANTARIS MUSCLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SARCOLEMMA; SLOW MUSCLE FIBER; SOLEUS MUSCLE; TIBIALIS ANTERIOR MUSCLE; TISSUE DISTRIBUTION; VASTUS LATERALIS MUSCLE; WESTERN BLOTTING;

ANIMALS; ANTIGENS, CD29; DYSTROPHIN; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GLYCOPROTEINS; ISOENZYMES; MALE; MEMBRANE PROTEINS; MUSCLE FIBERS, FAST-TWITCH; MUSCLE, SKELETAL; MYOCARDIUM; MYOSIN HEAVY CHAINS; RATS; RATS, WISTAR;

EID: 61849088555     PISSN: 17481708     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2008.01944.x     Document Type: Article

References (68)

1. Allen, D.G., Lamb, G.D. Westerblad, H. 2008. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88, 287 332.
2. Babbitt, C.J., Shai, S.Y., Harpf, A.E., Pham, C.G. Ross, R.S. 2002. Modulation of integrins and integrin signaling molecules in the pressure-loaded murine ventricle. Histochem Cell Biol 118, 431 439.
3. Baldwin, K.M. Haddad, F. 2001. Effects of different activity and inactivity paradigms on myosin heavy chain gene expression in striated muscle. J Appl Physiol 90, 345 357.
4. Bär, A. Pette, D. 1988. Three fast myosin heavy chains in adult rat skeletal muscle. FEBS Lett 235, 153 155.
5. Biral, D., Jakubiec-Puka, A., Ciechomska, I., Sandri, M., Rossini, K., Carraro, U. Betto, R. 2000. Loss of dystrophin and some dystrophin-associated proteins with concomitant signs of apoptosis in rat leg muscle overworked in extension. Acta Neuropathol (Berl) 100, 618 626.
6. Bloch, R.J. Gonzalez-Serratos, H. 2003. Lateral force transmission across costameres in skeletal muscle. Exerc Sport Sci Rev 31, 73 78.
7. Bonen, A., Luiken, J.J., Liu, S., Dyck, D.J., Kiens, B., Kristiansen, S., Turcotte, L.P., Van Der Vusse, G.J. Glatz, J.F. 1998. Palmitate transport and fatty acid transporters in red and white muscles. Am J Physiol 275, E471 E478.
8. 1-integrin regulates mechanotransduction and prevents skeletal muscle injury. Am J Physiol Cell Physiol 290, C1660 C1665.
9. Bottinelli, R., Canepari, M., Reggiani, C. Stienen, G.J. 1994. Myofibrillar ATPase activity during isometric contraction and isomyosin composition in rat single skinned muscle fibres. J Physiol 481, 663 675.
10. Brussee, V., Tardif, F. Tremblay, J.P. 1997. Muscle fibers of mdx mice are more vulnerable to exercise than those of normal mice. Neuromuscul Disord 7, 487 492.
11. Burke, R.E., Levine, D.N., Tsairis, P. Zajac, F.E., 3rd. 1973. Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J Physiol 234, 723 748.
12. Caiozzo, V.J., Haddad, F., Baker, M., McCue, S. Baldwin, K.M. 2000. MHC polymorphism in rodent plantaris muscle: effects of mechanical overload and hypothyroidism. Am J Physiol Cell Physiol 278, C709 C717.
13. Caiozzo, V.J., Baker, M.J., Huang, K., Chou, H., Wu, Y.Z. Baldwin, K.M. 2003. Single-fiber myosin heavy chain polymorphism: how many patterns and what proportions? Am J Physiol Regul Integr Comp Physiol 285, R570 R580.
14. Chopard, A., Pons, F., Charpiot, P. Marini, J.F. 2000. Quantitative analysis of relative protein contents by Western blotting: comparison of three members of the dystrophin-glycoprotein complex in slow and fast rat skeletal muscle. Electrophoresis 21, 517 522.
15. Chopard, A., Pons, F. Marini, J.F. 2002. Vinculin and meta-vinculin in fast and slow rat skeletal muscle before and after hindlimb suspension. Pflügers Arch 444, 627 633.
16. Clavel, S., Farout, L., Briand, M., Briand, Y. Jouanel, P. 2002. Effect of endurance training and/or fish oil supplemented diet on cytoplasmic fatty acid binding protein in rat skeletal muscles and heart. Eur J Appl Physiol 87, 193 201.
17. Consolino, C.M. Brooks, S.V. 2004. Susceptibility to sarcomere injury induced by single stretches of maximally activated muscles of mdx mice. J Appl Physiol 96, 633 638.
18. Demirel, H.A., Powers, S.K., Naito, H., Hughes, M. Coombes, J.S. 1999. Exercise-induced alterations in skeletal muscle myosin heavy chain phenotype: dose-response relationship. J Appl Physiol 86, 1002 1008.
19. Dunn, S.E. Michel, R.N. 1997. Coordinated expression of myosin heavy chain isoforms and metabolic enzymes within overloaded rat muscle fibers. Am J Physiol 273, C371 C383.
20. Eddinger, T.J. Moss, R.L. 1987. Mechanical properties of skinned single fibers of identified types from rat diaphragm. Am J Physiol 253, C210 C218.
21. Fitts, R.H. 1994. Cellular mechanisms of muscle fatigue. Physiol Rev 74, 49 94.
22. Fitts, R.H. Widrick, J.J. 1996. Muscle mechanics: adaptations with exercise-training. Exerc Sport Sci Rev 24, 427 473.
23. Flück, M., Carson, J.A., Gordon, S.E., Ziemiecki, A. Booth, F.W. 1999. Focal adhesion proteins FAK and paxillin increase in hypertrophied skeletal muscle. Am J Physiol 277, C152 C162.
24. Gawlik, K.I., Mayer, U., Blomberg, K., Sonnenberg, A., Ekblom, P. Durbeej, M. 2006. Laminin α1 chain mediated reduction of laminin α2 chain deficient muscular dystrophy involves integrin α7β1 and dystroglycan. FEBS Lett 580, 1759 1765.
25. Gayles, E.C., Pagliassotti, M.J., Prach, P.A., Koppenhafer, T.A. Hill, J.O. 1997. Contribution of energy intake and tissue enzymatic profile to body weight gain in high-fat-fed rats. Am J Physiol 272, R188 R194.
26. Gillespie, M.J., Gordon, T. Murphy, P.R. 1987. Motor units and histochemistry in rat lateral gastrocnemius and soleus muscles: evidence for dissociation of physiological and histochemical properties after reinnervation. J Neurophysiol 57, 921 937.
27. Gordon, S.E., Flück, M. Booth, F.W. 2001. Selected Contribution: Skeletal muscle focal adhesion kinase, paxillin, and serum response factor are loading dependent. J Appl Physiol 90, 1174 1183 discussion 1165.
28. Graziotti, G.H., Ríos, C.M. Rivero, J.L. 2001. Evidence for three fast myosin heavy chain isoforms in type II skeletal muscle fibers in the adult llama (Lama glama). J Histochem Cytochem 49, 1033 1044.
29. Grounds, M.D., Sorokin, L. White, J. 2005. Strength at the extracellular matrix-muscle interface. Scand J Med Sci Sports 15, 381 391.
30. Hashimoto, T., Masuda, S., Taguchi, S. Brooks, G.A. 2005. Immunohistochemical analysis of MCT1, MCT2 and MCT4 expression in rat plantaris muscle. J Physiol 567, 121 129.
31. Henneman, E. Olson, C.B. 1965. Relations between structure and function in the design of skeletal muscles. J Neurophysiol 28, 581 598.
32. Henneman, E., Somjen, G. Carpenter, D.O. 1965. Functional significance of cell size in spinal motoneurons. J Neurophysiol 28, 560 580.
33. Hodges, B.L., Hayashi, Y.K., Nonaka, I., Wang, W., Arahata, K. Kaufman, S.J. 1997. Altered expression of the α7β1 integrin in human and murine muscular dystrophies. J Cell Sci 110, 2873 2881.
34. Ho-Kim, M.A. Rogers, P.A. 1992. Quantitative analysis of dystrophin in fast- and slow-twitch mammalian skeletal muscle. FEBS Lett 304, 187 191.
35. Huijing, P.A. 1999. Muscle as a collagen fiber reinforced composite: a review of force transmission in muscle and whole limb. J Biomech 32, 329 345.
36. Kamogawa, Y., Biro, S., Maeda, M., Setoguchi, M., Hirakawa, T., Yoshida, H. Tei, C. 2001. Dystrophin-deficient myocardium is vulnerable to pressure overload in vivo. Cardiovasc Res 50, 509 515.
37. Koulmann, N. Bigard, A.X. 2006. Interaction between signalling pathways involved in skeletal muscle responses to endurance exercise. Pflügers Arch 452, 125 139.
38. Kumar, A., Khandelwal, N., Malya, R., Reid, M.B. Boriek, A.M. 2004. Loss of dystrophin causes aberrant mechanotransduction in skeletal muscle fibers. FASEB J 18, 102 113.
39. Larsson, L., Edström, L., Lindegren, B., Gorza, L. Schiaffino, S. 1991. MHC composition and enzyme-histochemical and physiological properties of a novel fast-twitch motor unit type. Am J Physiol 261, C93 C101.
40. Lindstedt, S.L., McGlothlin, T., Percy, E. Pifer, J. 1998. Task-specific design of skeletal muscle: balancing muscle structural composition. Comp Biochem Physiol B Biochem Mol Biol 120, 35 40.
41. Maeda, M., Biro, S., Kamogawa, Y., Hirakawa, T., Setoguchi, M. Tei, C. 2003. Dystrophin upregulation in pressure-overloaded cardiac hypertrophy in rats. Cell Motil Cytoskeleton 55, 26 35.
42. Mathieu-Costello, O., Ju, Y., Trejo-Morales, M. Cui, L. 2005. Greater capillary-fiber interface per fiber mitochondrial volume in skeletal muscles of old rats. J Appl Physiol 99, 281 289.
43. McClung, J.M., Thompson, R.W., Lowe, L.L. Carson, J.A. 2004. RhoA expression during recovery from skeletal muscle disuse. J Appl Physiol 96, 1341 1348.
44. McCullagh, K.J.A., Poole, R.C., Halestrap, A.P., O'Brien, M. Bonen, A. 1996. Role of the lactate transporter (MCT1) in skeletal muscles. Am J Physiol 271, E143 E150.
45. Meijer, H.J., Baan, G.C. Huijing, P.A. 2006. Myofascial force transmission is increasingly important at lower forces: firing frequency-related length-force characteristics of rat extensor digitorum longus. Acta Physiol (Oxf) 186, 185 195.
46. Monti, R.J., Roy, R.R., Hodgson, J.A. Edgerton, V.R. 1999. Transmission of forces within mammalian skeletal muscles. J Biomech 32, 371 380.
47. Nakatani, T., Nakashima, T., Kita, T., Hirofuji, C., Itoh, K., Itoh, M. Ishihara, A. 1999. Succinate dehydrogenase activities of fibers in the rat extensor digitorum longus, soleus, and cardiac muscles. Arch Histol Cytol 62, 393 399.
48. Okumoto, T., Imoto, T., Katsuta, S. Wada, M. 1996. Severe endurance training fails to change myosin heavy-chain distribution of diaphragm. Respir Physiol 104, 39 43.
49. Pasternak, C., Wong, S. Elson, E.L. 1995. Mechanical function of dystrophin in muscle cells. J Cell Biol 128, 355 361.
50. Paul, A.C., Sheard, P.W., Kaufman, S.J. Duxson, M.J. 2002. Localization of α7 integrins and dystrophin suggests potential for both lateral and longitudinal transmission of tension in large mammalian muscles. Cell Tissue Res 308, 255 265.
51. Petit, J., Filippi, G.M., Emonet-Denand, F., Hunt, C.C. Laporte, Y. 1990. Changes in muscle stiffness produced by motor units of different types in peroneus longus muscle of cat. J Neurophysiol 63, 190 197.
52. Petrof, B.J., Shrager, J.B., Stedman, H.H., Kelly, A.M. Sweeney, H.L. 1993. Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci USA 90, 3710 3714.
53. Pette, D. 2002. The adaptive potential of skeletal muscle fibers. Can J Appl Physiol 27, 423 448.
54. Peuker, H., Conjard, A. Pette, D. 1998. α-Cardiac-like myosin heavy chain as an intermediate between MHCIIa and MHCIβ in transforming rabbit muscle. Am J Physiol 274, C595 C602.
55. Quiroz-Rothe, E. Rivero, J.L. 2004. Coordinated expression of myosin heavy chains, metabolic enzymes, and morphological features of porcine skeletal muscle fiber types. Microsc Res Tech 65, 43 61.
56. Rando, T.A. 2001. The dystrophin-glycoprotein complex, cellular signaling, and the regulation of cell survival in the muscular dystrophies. Muscle Nerve 24, 1575 1594.
57. Rivero, J.L., Talmadge, R.J. Edgerton, V.R. 1999. Interrelationships of myofibrillar ATPase activity and metabolic properties of myosin heavy chain-based fibre types in rat skeletal muscle. Histochem Cell Biol 111, 277 287.
58. Russell, B., Motlagh, D. Ashley, W.W. 2000. Form follows function: how muscle shape is regulated by work. J Appl Physiol 88, 1127 1132.
59. Sieck, G.C., Fournier, M. Enad, J.G. 1989. Fiber type composition of muscle units in the cat diaphragm. Neurosci Lett 97, 29 34.
60. Sieck, G.C., Zhan, W.Z., Prakash, Y.S., Daood, M.J. Watchko, J.F. 1995. SDH and actomyosin ATPase activities of different fiber types in rat diaphragm muscle. J Appl Physiol 79, 1629 1639.
61. Škorjanc, D., Traub, I. Pette, D. 1998. Identical responses of fast muscle to sustained activity by low-frequency stimulation in young and aging rats. J Appl Physiol 85, 437 441.
62. Sréter, F.A., Luff, A.R. Gergely, J. 1975. Effect of cross-reinnervation on physiological parameters and on properties of myosin and sarcoplasmic reticulum of fast and slow muscles of the rabbit. J Gen Physiol 66, 811 821.
63. Talmadge, R.J. Roy, R.R. 1993. Electrophoretic separation of rat skeletal muscle myosin heavy-chain isoforms. J Appl Physiol 75, 2337 2340.
64. Termin, A., Staron, R.S. Pette, D. 1989. Changes in myosin heavy chain isoforms during chronic low-frequency stimulation of rat fast hindlimb muscles. A single-fiber study. Eur J Biochem 186, 749 754.
65. 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.
66. Toyoda, T., Hayashi, T., Miyamoto, L., Yonemitsu, S., Nakano, M., Tanaka, S., Ebihara, K., Masuzaki, H., Hosoda, K., Inoue, G., Otaka, A., Sato, K., Fushiki, T. Nakao, K. 2004. Possible involvement of the α1 isoform of 5′AMP-activated protein kinase in oxidative stress-stimulated glucose transport in skeletal muscle. Am J Physiol Endocrinol Metab 287, E166 E173.
67. Toyoda, T., Tanaka, S., Ebihara, K., Masuzaki, H., Hosoda, K., Sato, K., Fushiki, T., Nakao, K. Hayashi, T. 2006. Low-intensity contraction activates the α1-isoform of 5′-AMP-activated protein kinase in rat skeletal muscle. Am J Physiol Endocrinol Metab 290, E583 E590.
68. 1D-integrin expression and activation of FAK and RhoA. Am J Physiol Cell Physiol 292, C2057 C2069.