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Published in: European Journal of Applied Physiology 5/2010

01-11-2010 | Original Article

The effects of eccentric contraction on myofibrillar proteins in rat skeletal muscle

Authors: Keita Kanzaki, Mai Kuratani, Takaaki Mishima, Satoshi Matsunaga, Noriyuki Yanaka, Sachio Usui, Masanobu Wada

Published in: European Journal of Applied Physiology | Issue 5/2010

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Abstract

The present study investigated the effects of eccentric muscle contractions (ECC) on the content of myofibrillar proteins (my-proteins) and the catalytic activity of myofibrillar ATPase (my-ATPase) in skeletal muscles. Rat extensor digitorum longus and tibialis anterior muscles were exposed to 200-repeated ECC or isometric contractions (ISC) and used for measures of force output and for biochemical analyses, respectively. Whereas in ISC-treated muscles, full restoration of tetanic force was attained after 2 days of recovery, force developed by ECC-treated muscles remained depressed (P < 0.05) after 6 days. The total my-protein content and the relative content of myosin heavy chain (MHC) in total my-proteins were unaltered during 4 days of recovery after ECC, but fell (P < 0.05) to 55.9 and 63.4% after 6 days of recovery, respectively. my-ATPase activity expressed on a my-protein weight basis was unaltered immediately after ECC. However, it decreased (P < 0.05) to 75.3, 45.3, and 49.3% after 2, 4 and 6 days of recovery, respectively. Total maximal calpain activity measured at 5 mM Ca2+ was significantly augmented (P < 0.05) after 2 days of recovery, reaching a level of threefold higher after 6 days. These alterations were specific for ECC and not observed for ISC. These results suggest that depressions in my-ATPase activity contribute to ECC-induced decreases in force and power which can take a number of days to recover.
Literature
go back to reference Allen DG (2001) Eccentric muscle damage: mechanisms of early reduction of force. Acta Physiol Scand 171:311–319CrossRefPubMed Allen DG (2001) Eccentric muscle damage: mechanisms of early reduction of force. Acta Physiol Scand 171:311–319CrossRefPubMed
go back to reference Baker AJ, Brandes R, Schendel TM, Trocha SD, Miller RG, Weiner MW (1994) Energy use by contractile and noncontractile processes in skeletal muscle estimated by 31P-NMR. Am J Physiol 266:C825–C831PubMed Baker AJ, Brandes R, Schendel TM, Trocha SD, Miller RG, Weiner MW (1994) Energy use by contractile and noncontractile processes in skeletal muscle estimated by 31P-NMR. Am J Physiol 266:C825–C831PubMed
go back to reference Bárány M (1967) ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 50:197–218CrossRefPubMed Bárány M (1967) ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 50:197–218CrossRefPubMed
go back to reference Bottinelli R, Canepari M, Reggiani C, Stienen GJM (1994) Myofibrillar ATPase activity during isometric contraction and isomyosin composition in rat single skinned muscle fibres. J Physiol (Lond) 481:663–675 Bottinelli R, Canepari M, Reggiani C, Stienen GJM (1994) Myofibrillar ATPase activity during isometric contraction and isomyosin composition in rat single skinned muscle fibres. J Physiol (Lond) 481:663–675
go back to reference Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMed Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMed
go back to reference Clarkson PM, Nosaka K, Braun B (1992) Muscle function after exercise-induced muscle damage and rapid adaptation. Med Sci Sports Exerc 24:512–520PubMed Clarkson PM, Nosaka K, Braun B (1992) Muscle function after exercise-induced muscle damage and rapid adaptation. Med Sci Sports Exerc 24:512–520PubMed
go back to reference Corona BT, Balog EM, Doyle JA, Rupp JC, Luke RC, Ingalls CP (2010) Junctophilin damage contributes to early strength deficits and EC coupling failure after eccentric contractions. Am J Physiol 298:C365–C376CrossRef Corona BT, Balog EM, Doyle JA, Rupp JC, Luke RC, Ingalls CP (2010) Junctophilin damage contributes to early strength deficits and EC coupling failure after eccentric contractions. Am J Physiol 298:C365–C376CrossRef
go back to reference Dargelos E, Poussard S, Brulé C, Daury L, Cottin P (2008) Calcium-dependent proteolytic system and muscle dysfunctions: a possible role of calpains in sarcopenia. Biochimie 90:359–368CrossRefPubMed Dargelos E, Poussard S, Brulé C, Daury L, Cottin P (2008) Calcium-dependent proteolytic system and muscle dysfunctions: a possible role of calpains in sarcopenia. Biochimie 90:359–368CrossRefPubMed
go back to reference Faulkner JA, Jones DA, Round JM (1989) Injury to skeletal muscles of mice by forced lengthening during contractions. Q J Exp Physiol 74:661–670PubMed Faulkner JA, Jones DA, Round JM (1989) Injury to skeletal muscles of mice by forced lengthening during contractions. Q J Exp Physiol 74:661–670PubMed
go back to reference Ferreira LF, Reid MB (2008) Muscle-derived ROS and thiol regulation in muscle fatigue. J Appl Physiol 104:853–860CrossRefPubMed Ferreira LF, Reid MB (2008) Muscle-derived ROS and thiol regulation in muscle fatigue. J Appl Physiol 104:853–860CrossRefPubMed
go back to reference Fielding RA, Manfredi TJ, Ding W, Fiatarone MA, Evans WJ, Cannon JG (1993) Acute phase response in exercise. III. Neutrophil and IL-1 beta accumulation in skeletal muscle. Am J Physiol 265:R166–R172PubMed Fielding RA, Manfredi TJ, Ding W, Fiatarone MA, Evans WJ, Cannon JG (1993) Acute phase response in exercise. III. Neutrophil and IL-1 beta accumulation in skeletal muscle. Am J Physiol 265:R166–R172PubMed
go back to reference Gagnon J, Gregory P, Kurowski T, Zak R (1990) Changes in protein synthesis during induced muscle fiber transformation. In: Pette D (ed) The dynamic state of muscle fibers. Walter de Gruyter, Berlin, pp 481–495 Gagnon J, Gregory P, Kurowski T, Zak R (1990) Changes in protein synthesis during induced muscle fiber transformation. In: Pette D (ed) The dynamic state of muscle fibers. Walter de Gruyter, Berlin, pp 481–495
go back to reference Gibala MJ, MacDougall JD, Tarnopolsky MA, Stauber WT, Elorriaga A (1995) Changes in human skeletal muscle ultrastructure and force production after acute resistance exercise. J Appl Physiol 78:702–708PubMed Gibala MJ, MacDougall JD, Tarnopolsky MA, Stauber WT, Elorriaga A (1995) Changes in human skeletal muscle ultrastructure and force production after acute resistance exercise. J Appl Physiol 78:702–708PubMed
go back to reference Goll DE, Thompson VF, Li H, Wei W, Cong J (2003) The calpain system. Physiol Rev 83:731–801PubMed Goll DE, Thompson VF, Li H, Wei W, Cong J (2003) The calpain system. Physiol Rev 83:731–801PubMed
go back to reference Ingalls CP, Warren GL, Armstrong RB (1998a) Dissociation of force production from MHC and actin contents in muscles injured by eccentric contractions. J Muscle Res Cell Motil 19:215–224CrossRefPubMed Ingalls CP, Warren GL, Armstrong RB (1998a) Dissociation of force production from MHC and actin contents in muscles injured by eccentric contractions. J Muscle Res Cell Motil 19:215–224CrossRefPubMed
go back to reference Ingalls CP, Warren GL, Williams JH, Ward CW, Armstrong RB (1998b) E-C coupling failure in mouse EDL muscle after in vivo eccentric contractions. J Appl Physiol 85:56–67 Ingalls CP, Warren GL, Williams JH, Ward CW, Armstrong RB (1998b) E-C coupling failure in mouse EDL muscle after in vivo eccentric contractions. J Appl Physiol 85:56–67
go back to reference Ingalls CP, Warren GL, Zhang J-Z, Hamilton SL, Armstrong RB (2004) Dihydropyridine and ryanodine receptor binding after eccentric contraction. J Appl Physiol 96:1619–1625CrossRefPubMed Ingalls CP, Warren GL, Zhang J-Z, Hamilton SL, Armstrong RB (2004) Dihydropyridine and ryanodine receptor binding after eccentric contraction. J Appl Physiol 96:1619–1625CrossRefPubMed
go back to reference Keira Y, Noguchi S, Minami N, Hayashi YK, Nishino I (2003) Localization of calpain 3 in human skeletal muscle and its alteration in limb-girdle muscular dystrophy 2A muscle. J Biochem (Tokyo) 133:659–664 Keira Y, Noguchi S, Minami N, Hayashi YK, Nishino I (2003) Localization of calpain 3 in human skeletal muscle and its alteration in limb-girdle muscular dystrophy 2A muscle. J Biochem (Tokyo) 133:659–664
go back to reference Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz A-G, Ahn B-W, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478CrossRefPubMed Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz A-G, Ahn B-W, Shaltiel S, Stadtman ER (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478CrossRefPubMed
go back to reference Levine RL, Wehr N, Williams JA, Stadtman ER, Shacter E (2000) Determination of carbonyl groups in oxidized proteins. Methods Mol Biol 99:15–24PubMed Levine RL, Wehr N, Williams JA, Stadtman ER, Shacter E (2000) Determination of carbonyl groups in oxidized proteins. Methods Mol Biol 99:15–24PubMed
go back to reference Lynch GS, Fary CJ, Williams DA (1997) Quantitative measurement of resting skeletal muscle [Ca2+]i following acute and long-term downhill running exercise in mice. Cell Calcium 22:373–383CrossRefPubMed Lynch GS, Fary CJ, Williams DA (1997) Quantitative measurement of resting skeletal muscle [Ca2+]i following acute and long-term downhill running exercise in mice. Cell Calcium 22:373–383CrossRefPubMed
go back to reference Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, Goldberg AL, Schiaffino S, Sandri M (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6:458–471CrossRefPubMed Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, Goldberg AL, Schiaffino S, Sandri M (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6:458–471CrossRefPubMed
go back to reference Matsunaga S, Harmon S, Gohlsch B, Ohlendieck K, Pette D (2001) Inactivation of sarcoplasmic reticulum Ca2+-ATPase in low-frequency stimulated rat muscle. J Muscle Res Cell Motil 22:685–691CrossRefPubMed Matsunaga S, Harmon S, Gohlsch B, Ohlendieck K, Pette D (2001) Inactivation of sarcoplasmic reticulum Ca2+-ATPase in low-frequency stimulated rat muscle. J Muscle Res Cell Motil 22:685–691CrossRefPubMed
go back to reference Matsunaga S, Inashima S, Yamada T, Watanabe H, Hazama T, Wada M (2003) Oxidation of sarcoplasmic reticulum Ca2+-ATPase induced by high-intensity exercise. Pflügers Arch 446:394–399PubMed Matsunaga S, Inashima S, Yamada T, Watanabe H, Hazama T, Wada M (2003) Oxidation of sarcoplasmic reticulum Ca2+-ATPase induced by high-intensity exercise. Pflügers Arch 446:394–399PubMed
go back to reference Mishima T, Kuratani M, Kanzaki K, Yamada T, Matsunaga S, Wada M (2009) No relationship between enzyme activity and structure of nucleotide binding site in sarcoplasmic reticulum Ca2+-ATPase from short-term stimulated rat muscle. Acta Physiol 196:401–409CrossRef Mishima T, Kuratani M, Kanzaki K, Yamada T, Matsunaga S, Wada M (2009) No relationship between enzyme activity and structure of nucleotide binding site in sarcoplasmic reticulum Ca2+-ATPase from short-term stimulated rat muscle. Acta Physiol 196:401–409CrossRef
go back to reference Murphy RM, Verburg E, Lamb GD (2006) Ca2+ activation of diffusible and bound pools of μ-calpain in rat skeletal muscle. J Physiol (Lond) 576:595–612CrossRef Murphy RM, Verburg E, Lamb GD (2006) Ca2+ activation of diffusible and bound pools of μ-calpain in rat skeletal muscle. J Physiol (Lond) 576:595–612CrossRef
go back to reference Murphy RM, Goodman CA, McKenna MJ, Bennie J, Leikis M, Lamb GD (2007) Calpain-3 is autolyzed and hence activated in human skeletal muscle 24 h following a single bout of eccentric exercise. J Appl Physiol 103:926–931CrossRefPubMed Murphy RM, Goodman CA, McKenna MJ, Bennie J, Leikis M, Lamb GD (2007) Calpain-3 is autolyzed and hence activated in human skeletal muscle 24 h following a single bout of eccentric exercise. J Appl Physiol 103:926–931CrossRefPubMed
go back to reference Pette D, Staron RS (1990) Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev Physiol Biochem Pharmacol 116:1–76PubMed Pette D, Staron RS (1990) Cellular and molecular diversities of mammalian skeletal muscle fibers. Rev Physiol Biochem Pharmacol 116:1–76PubMed
go back to reference Raser KJ, Posner A, Wang KKW (1995) Casein zymography: a method to study micro-calpain, m-calpain, and their inhibitory agents. Arch Biochem Biophys 319:211–216CrossRefPubMed Raser KJ, Posner A, Wang KKW (1995) Casein zymography: a method to study micro-calpain, m-calpain, and their inhibitory agents. Arch Biochem Biophys 319:211–216CrossRefPubMed
go back to reference Rathbone CR, Wenke JC, Warren GL, Armstrong RB (2003) Importance of satellite cells in the strength recovery after eccentric contraction-induced muscle injury. Am J Physiol 285:R1490–R1495 Rathbone CR, Wenke JC, Warren GL, Armstrong RB (2003) Importance of satellite cells in the strength recovery after eccentric contraction-induced muscle injury. Am J Physiol 285:R1490–R1495
go back to reference Schollmeyer JE (1986) Role of Ca2+ and Ca2+-activated protease in myoblast fusion. Exp Cell 162:411–422CrossRef Schollmeyer JE (1986) Role of Ca2+ and Ca2+-activated protease in myoblast fusion. Exp Cell 162:411–422CrossRef
go back to reference Sultan KR, Dittrich BT, Pette D (2000) Calpain activity in fast, slow, transforming and regenerating skeletal muscle. Am J Physiol 279:C639–C647 Sultan KR, Dittrich BT, Pette D (2000) Calpain activity in fast, slow, transforming and regenerating skeletal muscle. Am J Physiol 279:C639–C647
go back to reference Takekura H, Fujinami N, Nishizawa T, Ogasawara H, Kasuga N (2001) Eccentric exercise-induced morphological changes in the membrane systems involved in excitation-contraction coupling in rat skeletal muscle. J Physiol (Lond) 553:571–583CrossRef Takekura H, Fujinami N, Nishizawa T, Ogasawara H, Kasuga N (2001) Eccentric exercise-induced morphological changes in the membrane systems involved in excitation-contraction coupling in rat skeletal muscle. J Physiol (Lond) 553:571–583CrossRef
go back to reference Talbot JA, Morgan DL (1996) Quantitative analysis of sarcomere non-uniformities in active muscle following a stretch. J Muscle Res Cell Mortil 17:261–268CrossRef Talbot JA, Morgan DL (1996) Quantitative analysis of sarcomere non-uniformities in active muscle following a stretch. J Muscle Res Cell Mortil 17:261–268CrossRef
go back to reference Termin A, Pette D (1992) Changes in myosin heavy-chain isoform synthesis of chronically stimulated rat fast-twitch muscle. Eur J Biochem 204:569–573CrossRefPubMed Termin A, Pette D (1992) Changes in myosin heavy-chain isoform synthesis of chronically stimulated rat fast-twitch muscle. Eur J Biochem 204:569–573CrossRefPubMed
go back to reference Tsika RW, Herrick RE, Baldwin KM (1987) Interaction of compensatory overload and hindlimb suspension on myosin isoform expression. J Appl Physiol 62:2180–2186PubMed Tsika RW, Herrick RE, Baldwin KM (1987) Interaction of compensatory overload and hindlimb suspension on myosin isoform expression. J Appl Physiol 62:2180–2186PubMed
go back to reference Wada M, Kikuchi K, Katsuta S (1992) Changes in myosin heavy-chain and light-chain isoforms following sustained exercise. In: Sato Y, Poortmans J, Hashimoto I, Oshida Y (eds) Integration of medicine and sports sciences. Karger, Basel, pp 309–317 Wada M, Kikuchi K, Katsuta S (1992) Changes in myosin heavy-chain and light-chain isoforms following sustained exercise. In: Sato Y, Poortmans J, Hashimoto I, Oshida Y (eds) Integration of medicine and sports sciences. Karger, Basel, pp 309–317
go back to reference Yamada T, Mishima T, Sakamoto M, Sugiyama M, Matsunaga S, Wada M (2006) Oxidation of myosin heavy chain and reduction in force production in hyperthyroid rat soleus. J Appl Physiol 100:1520–1526CrossRefPubMed Yamada T, Mishima T, Sakamoto M, Sugiyama M, Matsunaga S, Wada M (2006) Oxidation of myosin heavy chain and reduction in force production in hyperthyroid rat soleus. J Appl Physiol 100:1520–1526CrossRefPubMed
go back to reference Yoshida M, Suzuki A, Shimizu T, Ozawa E (1992) Proteinase-sensitive sites on isolated rabbit dystrophin. J Biochem 112:433–439PubMed Yoshida M, Suzuki A, Shimizu T, Ozawa E (1992) Proteinase-sensitive sites on isolated rabbit dystrophin. J Biochem 112:433–439PubMed
go back to reference You T, Goldfarb AH, Bloomer RJ, Nguyen L, Sha X, McKenzie MJ (2005) Oxidative stress response in normal and antioxidant supplemented rats to a downhill run: changes in blood and skeletal muscles. Can J Appl Physiol 30:677–689PubMed You T, Goldfarb AH, Bloomer RJ, Nguyen L, Sha X, McKenzie MJ (2005) Oxidative stress response in normal and antioxidant supplemented rats to a downhill run: changes in blood and skeletal muscles. Can J Appl Physiol 30:677–689PubMed
go back to reference Zhang B-T, Yeung SS, Allen DG, Qin L, Yeung EW (2008) Role of the calcium-calpain pathway in cytoskeletal damage after eccentric contractions. J Appl Physiol 105:352–357CrossRefPubMed Zhang B-T, Yeung SS, Allen DG, Qin L, Yeung EW (2008) Role of the calcium-calpain pathway in cytoskeletal damage after eccentric contractions. J Appl Physiol 105:352–357CrossRefPubMed
Metadata
Title
The effects of eccentric contraction on myofibrillar proteins in rat skeletal muscle
Authors
Keita Kanzaki
Mai Kuratani
Takaaki Mishima
Satoshi Matsunaga
Noriyuki Yanaka
Sachio Usui
Masanobu Wada
Publication date
01-11-2010
Publisher
Springer-Verlag
Published in
European Journal of Applied Physiology / Issue 5/2010
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-010-1579-3

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