Skip to main content
Top
Published in: European Journal of Applied Physiology 3/2008

01-06-2008 | Original Article

Effects of concentric and repeated eccentric exercise on muscle damage and calpain–calpastatin gene expression in human skeletal muscle

Authors: Kristian Vissing, Kristian Overgaard, Anders Nedergaard, Anne Fredsted, Peter Schjerling

Published in: European Journal of Applied Physiology | Issue 3/2008

Login to get access

Abstract

The purpose of this study was to compare the responsiveness of changes in Ca2+-content and calpain–calpastatin gene expression to concentric and eccentric single-bout and repeated exercise. An exercise group (n = 14) performed two bouts of bench-stepping exercise with 8 weeks between exercise bouts, and was compared to a control-group (n = 6). Muscle strength and soreness and plasma creatine kinase and myoglobin were measured before and during 7 days following exercise bouts. Muscle biopsies were collected from m. vastus lateralis of both legs prior to and at 3, 24 h and 7 days after exercise and quantified for muscle Ca2+-content and mRNA levels for calpain isoforms and calpastatin. Exercise reduced muscle strength and increased muscle soreness predominantly in the eccentric leg (P < 0.05). These responses as well as plasma levels of creatine kinase and myoglobin were all attenuated after the repeated eccentric exercise bout (P < 0.05). Total muscle Ca2+-content did not differ between interventions. mRNA levels for calpain 2 and calpastatin were upregulated exclusively by eccentric exercise 24 h post-exercise (P < 0.05), with no alteration in expression between bouts. Calpain 1 and calpain 3 mRNA did not change at any specific time point post-exercise for either intervention. Our mRNA results suggest a regulation on the calpain–calpastatin expression response to muscle damaging eccentric exercise, but not concentric exercise. Although a repeated bout effect was demonstrated in terms of muscle function, no immediate support was provided to suggest that regulation of expression of specific system components is involved in the repeated bout adaptation.
Appendix
Available only for authorised users
Literature
go back to reference Arendt-Nielsen L (2002) Clinical use of pain measurement techniques. Ugeskr Laeger 164:1790–1795PubMed Arendt-Nielsen L (2002) Clinical use of pain measurement techniques. Ugeskr Laeger 164:1790–1795PubMed
go back to reference Belcastro AN (1993) Skeletal muscle calcium-activated neutral protease (calpain) with exercise. J Appl Physiol 74:1381–1386PubMed Belcastro AN (1993) Skeletal muscle calcium-activated neutral protease (calpain) with exercise. J Appl Physiol 74:1381–1386PubMed
go back to reference Belcastro AN, Shewchuk LD, Raj DA (1998) Exercise-induced muscle injury: a calpain hypothesis. Mol Cell Biochem 179:135–145PubMedCrossRef Belcastro AN, Shewchuk LD, Raj DA (1998) Exercise-induced muscle injury: a calpain hypothesis. Mol Cell Biochem 179:135–145PubMedCrossRef
go back to reference Busquets S, Garcia-Martinez C, Alvarez B, Carbo N, Lopez-Soriano FJ, Argiles JM (2000) Calpain-3 gene expression is decreased during experimental cancer cachexia. Biochim Biophys Acta 1475:5–9PubMed Busquets S, Garcia-Martinez C, Alvarez B, Carbo N, Lopez-Soriano FJ, Argiles JM (2000) Calpain-3 gene expression is decreased during experimental cancer cachexia. Biochim Biophys Acta 1475:5–9PubMed
go back to reference Dheda K, Huggett JF, Chang JS, Kim LU, Bustin SA, Johnson MA, Rook GA, Zumla A (2005) The implications of using an inappropriate reference gene for real-time reverse transcription PCR data normalization. Anal Biochem 344:141–143. doi:10.1016/j.ab.2005.05.022 PubMedCrossRef Dheda K, Huggett JF, Chang JS, Kim LU, Bustin SA, Johnson MA, Rook GA, Zumla A (2005) The implications of using an inappropriate reference gene for real-time reverse transcription PCR data normalization. Anal Biochem 344:141–143. doi:10.​1016/​j.​ab.​2005.​05.​022 PubMedCrossRef
go back to reference Dietrichson P, Coakley J, Smith PE, Griffiths RD, Helliwell TR, Edwards RH (1987) Conchotome and needle percutaneous biopsy of skeletal muscle. J Neurol Neurosurg Psychiatry 50:1461–1467PubMed Dietrichson P, Coakley J, Smith PE, Griffiths RD, Helliwell TR, Edwards RH (1987) Conchotome and needle percutaneous biopsy of skeletal muscle. J Neurol Neurosurg Psychiatry 50:1461–1467PubMed
go back to reference Edwards RH, Young A, Hosking GP, Jones DA (1977) Human skeletal muscle function: description of tests and normal values. Clin Sci Mol Med 52:283–290PubMed Edwards RH, Young A, Hosking GP, Jones DA (1977) Human skeletal muscle function: description of tests and normal values. Clin Sci Mol Med 52:283–290PubMed
go back to reference Feasson L, Stockholm D, Freyssenet D, Richard I, Duguez S, Beckmann JS, Denis C (2002) Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle. J Physiol 543:297–306PubMedCrossRef Feasson L, Stockholm D, Freyssenet D, Richard I, Duguez S, Beckmann JS, Denis C (2002) Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle. J Physiol 543:297–306PubMedCrossRef
go back to reference Friden J, Sjostrom M, Ekblom B (1983) Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med 4:170–176PubMedCrossRef Friden J, Sjostrom M, Ekblom B (1983) Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med 4:170–176PubMedCrossRef
go back to reference Gissel H, Clausen T (1999) Excitation-induced Ca2+ uptake in rat skeletal muscle. Am J Physiol 276:R331–R339PubMed Gissel H, Clausen T (1999) Excitation-induced Ca2+ uptake in rat skeletal muscle. Am J Physiol 276:R331–R339PubMed
go back to reference Gissel H, Clausen T (2001) Excitation-induced Ca2+ influx and skeletal muscle cell damage. Acta Physiol Scand 171:327–334PubMedCrossRef Gissel H, Clausen T (2001) Excitation-induced Ca2+ influx and skeletal muscle cell damage. Acta Physiol Scand 171:327–334PubMedCrossRef
go back to reference Huang J, Forsberg NE (1998) Role of calpain in skeletal-muscle protein degradation. Proc Natl Acad Sci USA 95:12100–12105PubMedCrossRef Huang J, Forsberg NE (1998) Role of calpain in skeletal-muscle protein degradation. Proc Natl Acad Sci USA 95:12100–12105PubMedCrossRef
go back to reference Jonsdottir IH, Schjerling P, Ostrowski K, Asp S, Richter EA, Pedersen BK (2000) Muscle contractions induce interleukin-6 mRNA production in rat skeletal muscles. J Physiol 528(Pt 1):157–163PubMedCrossRef Jonsdottir IH, Schjerling P, Ostrowski K, Asp S, Richter EA, Pedersen BK (2000) Muscle contractions induce interleukin-6 mRNA production in rat skeletal muscles. J Physiol 528(Pt 1):157–163PubMedCrossRef
go back to reference Kinbara K, Ishiura S, Tomioka S, Sorimachi H, Jeong SY, Amano S, Kawasaki H, Kolmerer B, Kimura S, Labeit S, Suzuki K (1998) Purification of native p94, a muscle-specific calpain, and characterization of its autolysis. Biochem J 335(Pt 3):589–596PubMed Kinbara K, Ishiura S, Tomioka S, Sorimachi H, Jeong SY, Amano S, Kawasaki H, Kolmerer B, Kimura S, Labeit S, Suzuki K (1998) Purification of native p94, a muscle-specific calpain, and characterization of its autolysis. Biochem J 335(Pt 3):589–596PubMed
go back to reference Konig N, Raynaud F, Feane H, Durand M, Mestre-Frances N, Rossel M, Ouali A, Benyamin Y (2003) Calpain 3 is expressed in astrocytes of rat and Microcebus brain. J Chem Neuroanat 25:129–136PubMedCrossRef Konig N, Raynaud F, Feane H, Durand M, Mestre-Frances N, Rossel M, Ouali A, Benyamin Y (2003) Calpain 3 is expressed in astrocytes of rat and Microcebus brain. J Chem Neuroanat 25:129–136PubMedCrossRef
go back to reference Malm C (2001) Exercise-induced muscle damage and inflammation: fact or fiction? Acta Physiol Scand 171:233–239PubMedCrossRef Malm C (2001) Exercise-induced muscle damage and inflammation: fact or fiction? Acta Physiol Scand 171:233–239PubMedCrossRef
go back to reference McHugh MP (2003) Recent advances in the understanding of the repeated bout effect: the protective effect against muscle damage from a single bout of eccentric exercise. Scand J Med Sci Sports 13:88–97PubMedCrossRef McHugh MP (2003) Recent advances in the understanding of the repeated bout effect: the protective effect against muscle damage from a single bout of eccentric exercise. Scand J Med Sci Sports 13:88–97PubMedCrossRef
go back to reference Nedergaard A, Vissing K, Overgaard K, Kjaer M, Schjerling P (2007) Expression patterns of atrogenic and ubiquitin proteasome component genes with exercise: effect of different loading patterns and repeated exercise bouts. J Appl Physiol 103:1513–1522. doi:10.1152/japplphysiol.01445.2006 PubMedCrossRef Nedergaard A, Vissing K, Overgaard K, Kjaer M, Schjerling P (2007) Expression patterns of atrogenic and ubiquitin proteasome component genes with exercise: effect of different loading patterns and repeated exercise bouts. J Appl Physiol 103:1513–1522. doi:10.​1152/​japplphysiol.​01445.​2006 PubMedCrossRef
go back to reference Nosaka K, Sakamoto K, Newton M, Sacco P (2001) How long does the protective effect on eccentric exercise-induced muscle damage last? Med Sci Sports Exerc 33:1490–1495PubMedCrossRef Nosaka K, Sakamoto K, Newton M, Sacco P (2001) How long does the protective effect on eccentric exercise-induced muscle damage last? Med Sci Sports Exerc 33:1490–1495PubMedCrossRef
go back to reference Nosaka K, Newton MJ, Sacco P (2005) Attenuation of protective effect against eccentric exercise-induced muscle damage. Can J Appl Physiol 30:529–542PubMed Nosaka K, Newton MJ, Sacco P (2005) Attenuation of protective effect against eccentric exercise-induced muscle damage. Can J Appl Physiol 30:529–542PubMed
go back to reference Overgaard K, Fredsted A, Hyldal A, Ingemann-Hansen T, Gissel H, Clausen T (2004) Effects of running distance and training on Ca2+ content and damage in human muscle. Med Sci Sports Exerc 36:821–829PubMedCrossRef Overgaard K, Fredsted A, Hyldal A, Ingemann-Hansen T, Gissel H, Clausen T (2004) Effects of running distance and training on Ca2+ content and damage in human muscle. Med Sci Sports Exerc 36:821–829PubMedCrossRef
go back to reference Schjerling P (2001) The importance of internal controls in mRNA quantification. J Appl Physiol 90:401–402PubMed Schjerling P (2001) The importance of internal controls in mRNA quantification. J Appl Physiol 90:401–402PubMed
go back to reference Sorichter S, Mair J, Koller A, Gebert W, Rama D, Calzolari C, Artner-Dworzak E, Puschendorf B (1997) Skeletal troponin I as a marker of exercise-induced muscle damage. J Appl Physiol 83:1076–1082PubMed Sorichter S, Mair J, Koller A, Gebert W, Rama D, Calzolari C, Artner-Dworzak E, Puschendorf B (1997) Skeletal troponin I as a marker of exercise-induced muscle damage. J Appl Physiol 83:1076–1082PubMed
go back to reference Sorimachi H, Toyama-Sorimachi N, Saido TC, Kawasaki H, Sugita H, Miyasaka M, Arahata K, Ishiura S, Suzuki K (1993) Muscle-specific calpain, p94, is degraded by autolysis immediately after translation, resulting in disappearance from muscle. J Biol Chem 268:10593–10605PubMed Sorimachi H, Toyama-Sorimachi N, Saido TC, Kawasaki H, Sugita H, Miyasaka M, Arahata K, Ishiura S, Suzuki K (1993) Muscle-specific calpain, p94, is degraded by autolysis immediately after translation, resulting in disappearance from muscle. J Biol Chem 268:10593–10605PubMed
go back to reference Stupka N, Tarnopolsky MA, Yardley NJ, Phillips SM (2001) Cellular adaptation to repeated eccentric exercise-induced muscle damage. J Appl Physiol 91:1669–1678PubMed Stupka N, Tarnopolsky MA, Yardley NJ, Phillips SM (2001) Cellular adaptation to repeated eccentric exercise-induced muscle damage. J Appl Physiol 91:1669–1678PubMed
go back to reference Tidball JG, Spencer MJ (2002) Expression of a calpastatin transgene slows muscle wasting and obviates changes in myosin isoform expression during murine muscle disuse. J Physiol 545:819–828PubMedCrossRef Tidball JG, Spencer MJ (2002) Expression of a calpastatin transgene slows muscle wasting and obviates changes in myosin isoform expression during murine muscle disuse. J Physiol 545:819–828PubMedCrossRef
go back to reference Warren GL, Lowe DA, Armstrong RB (1999) Measurement tools used in the study of eccentric contraction-induced injury. Sports Med 27:43–59PubMedCrossRef Warren GL, Lowe DA, Armstrong RB (1999) Measurement tools used in the study of eccentric contraction-induced injury. Sports Med 27:43–59PubMedCrossRef
go back to reference Wei W, Fareed MU, Evenson A, Menconi MJ, Yang H, Petkova V, Hasselgren PO (2005) Sepsis stimulates calpain activity in skeletal muscle by decreasing calpastatin activity but does not activate caspase-3. Am J Physiol Regul Integr Comp Physiol 288:R580–R590. doi:10.1152/ajpregu.00341.2004 PubMed Wei W, Fareed MU, Evenson A, Menconi MJ, Yang H, Petkova V, Hasselgren PO (2005) Sepsis stimulates calpain activity in skeletal muscle by decreasing calpastatin activity but does not activate caspase-3. Am J Physiol Regul Integr Comp Physiol 288:R580–R590. doi:10.​1152/​ajpregu.​00341.​2004 PubMed
go back to reference Williams AB, Decourten-Myers GM, Fischer JE, Luo G, Sun X, Hasselgren PO (1999) Sepsis stimulates release of myofilaments in skeletal muscle by a calcium-dependent mechanism. FASEB J 13:1435–1443PubMed Williams AB, Decourten-Myers GM, Fischer JE, Luo G, Sun X, Hasselgren PO (1999) Sepsis stimulates release of myofilaments in skeletal muscle by a calcium-dependent mechanism. FASEB J 13:1435–1443PubMed
Metadata
Title
Effects of concentric and repeated eccentric exercise on muscle damage and calpain–calpastatin gene expression in human skeletal muscle
Authors
Kristian Vissing
Kristian Overgaard
Anders Nedergaard
Anne Fredsted
Peter Schjerling
Publication date
01-06-2008
Publisher
Springer-Verlag
Published in
European Journal of Applied Physiology / Issue 3/2008
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-008-0709-7

Other articles of this Issue 3/2008

European Journal of Applied Physiology 3/2008 Go to the issue