PDF herunterladen
Int J Sports Med 2020; 41(14): 994-1008
DOI: 10.1055/a-1199-7662
Review

The Role of Calpains in Skeletal Muscle Remodeling with Exercise and Inactivity-induced Atrophy

Hayden W. Hyatt 
1   Applied Physiology and Kinesiology, University of Florida, Gainesville, United States
,
Scott K. Powers
2   Applied Physiology, University of Florida, Gainesville, United States
› Institutsangaben Funding This work was supported by a grant from the National Institutes of Health (NIH R21 AR073956) awarded to SKP.
› Weitere Informationen
Auch verfügbar auf
   Lizenzen und Reprints

Abstract

Calpains are cysteine proteases expressed in skeletal muscle fibers and other cells. Although calpain was first reported to act as a kinase activating factor in skeletal muscle, the consensus is now that calpains play a canonical role in protein turnover. However, recent evidence reveals new and exciting roles for calpains in skeletal muscle. This review will discuss the functions of calpains in skeletal muscle remodeling in response to both exercise and inactivity-induced muscle atrophy. Calpains participate in protein turnover and muscle remodeling by selectively cleaving target proteins and creating fragmented proteins that can be further degraded by other proteolytic systems. Nonetheless, an often overlooked function of calpains is that calpain-mediated cleavage of proteins can result in fragmented proteins that are biologically active and have the potential to actively influence cell signaling. In this manner, calpains function beyond their roles in protein turnover and influence downstream signaling effects. This review will highlight both the canonical and noncanonical roles that calpains play in skeletal muscle remodeling including sarcomere transformation, membrane repair, triad junction formation, regulation of excitation-contraction coupling, protein turnover, cell signaling, and mitochondrial function. We conclude with a discussion of key unanswered questions regarding the roles that calpains play in skeletal muscle.

Key words

calpain - disuse atrophy - proteolysis - muscle remodeling - membrane repair - exercise


Publikationsverlauf

Eingereicht: 13. März 2020

Angenommen: 24. Mai 2020

Artikel online veröffentlicht:
17. Juli 2020

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Meyer WL, Fischer EH, Krebs EG. Activation of skeletal muscle phosphorylase B kinase by Ca. Biochemistry 1964; 3: 1033-1039
    CrossrefPubMedGoogle Scholar
  • 2 Huston RB, Krebs EG. Activation of skeletal muscle phosphorylase kinase by Ca2+. II. Identification of the kinase activating factor as a proteolytic enzyme. Biochemistry 1968; 7: 2116-2122
    PubMedGoogle Scholar
  • 3 Ono Y, Saido TC, Sorimachi H. Calpain research for drug discovery: Challenges and potential. Nat Rev Drug Discov 2016; 15: 854-876 doi:10.1038/nrd.2016.212
    CrossrefPubMedGoogle Scholar
  • 4 Murphy RM. Calpains, skeletal muscle function and exercise. Clin Exp Pharmacol Physiol 2010; 37: 385-391 doi:10.1111/j.1440-1681.2009.05310.x
    CrossrefPubMedGoogle Scholar
  • 5 Campbell RL, Davies PL. Structure-function relationships in calpains. Biochem J 2012; 447: 335-351 doi:10.1042/BJ20120921
    CrossrefPubMedGoogle Scholar
  • 6 Edmunds T, Nagainis PA, Sathe SK. et al. Comparison of the autolyzed and unautolyzed forms of mu- and m-calpain from bovine skeletal muscle. Biochim Biophys Acta 1991; 1077: 197-208
    CrossrefPubMedGoogle Scholar
  • 7 Goll DE, Thompson VF, Li H. et al. The calpain system. Physiol Rev 2003; 83: 731-801 DOI: 10.1152/physrev.00029.2002.
    CrossrefPubMedGoogle Scholar
  • 8 Koohmaraie M. The role of Ca(2+)-dependent proteases (calpains) in post mortem proteolysis and meat tenderness. Biochimie 1992; 74: 239-245
    CrossrefPubMedGoogle Scholar
  • 9 Bartoli M, Richard I. Calpains in muscle wasting. Int J Biochem Cell Biol 2005; 37: 2115-2133 doi:10.1016/j.biocel.2004.12.012
    CrossrefPubMedGoogle Scholar
  • 10 Purintrapiban J, Wang MC, Forsberg NE. Degradation of sarcomeric and cytoskeletal proteins in cultured skeletal muscle cells. Comp Biochem Physiol B Biochem Mol Biol 2003; 136: 393-401
    CrossrefPubMedGoogle Scholar
  • 11 Huang J, Forsberg NE. Role of calpain in skeletal-muscle protein degradation. Proc Natl Acad Sci USA 1998; 95: 12100-12105 doi:10.1073/pnas.95.21.12100
    CrossrefPubMedGoogle Scholar
  • 12 Talbert EE, Smuder AJ, Min K. et al. Calpain and caspase-3 play required roles in immobilization-induced limb muscle atrophy. J Appl Physiol (1985) 2013; 114: 1482-1489 DOI: 10.1152/japplphysiol.00925.2012.
    CrossrefPubMedGoogle Scholar
  • 13 Spencer MJ, Guyon JR, Sorimachi H. et al. Stable expression of calpain 3 from a muscle transgene in vivo: immature muscle in transgenic mice suggests a role for calpain 3 in muscle maturation. Proc Natl Acad Sci USA 2002; 99: 8874-8879 DOI: 10.1073/pnas.132269299.
    CrossrefPubMedGoogle Scholar
  • 14 Cortesio CL, Boateng LR, Piazza TM. et al. Calpain-mediated proteolysis of paxillin negatively regulates focal adhesion dynamics and cell migration. J Biol Chem 2011; 286: 9998-10006 DOI: 10.1074/jbc.M110.187294.
    CrossrefPubMedGoogle Scholar
  • 15 Tan Y, Wu C, De Veyra T. et al. Ubiquitous calpains promote both apoptosis and survival signals in response to different cell death stimuli. J Biol Chem 2006; 281: 17689-17698 DOI: 10.1074/jbc.M601978200.
    CrossrefPubMedGoogle Scholar
  • 16 Yuasa T, Amo-Shiinoki K, Ishikura S. et al. Sequential cleavage of insulin receptor by calpain 2 and gamma-secretase impairs insulin signalling. Diabetologia 2016; 59: 2711-2721 DOI: 10.1007/s00125-016-4102-5.
    CrossrefPubMedGoogle Scholar
  • 17 Beltran L, Chaussade C, Vanhaesebroeck B. et al. Calpain interacts with class IA phosphoinositide 3-kinases regulating their stability and signaling activity. Proc Natl Acad Sci USA 2011; 108: 16217-16222 DOI: 10.1073/pnas.1107692108.
    CrossrefPubMedGoogle Scholar
  • 18 Carragher NO. Calpain inhibition: A therapeutic strategy targeting multiple disease states. Curr Pharm Des 2006; 12: 615-638 doi:10.2174/138161206775474314
    CrossrefPubMedGoogle Scholar
  • 19 Baki A, Tompa P, Alexa A. et al. Autolysis parallels activation of mu-calpain. Biochem J 1996; 318 (Pt 3) 897-901 DOI: doi:10.1042/bj3180897.
    CrossrefPubMedGoogle Scholar
  • 20 Nagainis PA, Wolfe FH, Sathe SK. et al. Autolysis of the millimolar Ca2+-requiring form of the Ca2+-dependent proteinase from chicken skeletal muscle. Biochem Cell Biol 1988; 66: 1023-1031
    CrossrefPubMedGoogle Scholar
  • 21 Murphy RM, Verburg E, Lamb GD. Ca2+ activation of diffusible and bound pools of mu-calpain in rat skeletal muscle. J Physiol 2006; 576: 595-612 doi:10.1113/jphysiol.2006.114090
    CrossrefPubMedGoogle Scholar
  • 22 Chou JS, Impens F, Gevaert K. et al. m-Calpain activation in vitro does not require autolysis or subunit dissociation. Biochim Biophys Acta 2011; 1814: 864-872 DOI: 10.1016/j.bbapap.2011.04.007.
    CrossrefPubMedGoogle Scholar
  • 23 Coolican SA, Hathaway DR. Effect of L-alpha-phosphatidylinositol on a vascular smooth muscle Ca2+-dependent protease. Reduction of the Ca2+ requirement for autolysis. J Biol Chem 1984; 259: 11627-11630
    CrossrefPubMedGoogle Scholar
  • 24 Cong J, Goll DE, Peterson AM. et al. The role of autolysis in activity of the Ca2+-dependent proteinases (mu-calpain and m-calpain). J Biol Chem 1989; 264: 10096-10103
    CrossrefPubMedGoogle Scholar
  • 25 Du M, Li X, Li Z. et al. Phosphorylation regulated by protein kinase A and alkaline phosphatase play positive roles in mu-calpain activity. Food Chem 2018; 252: 33-39 DOI: 10.1016/j.foodchem.2018.01.103.
    CrossrefPubMedGoogle Scholar
  • 26 Smith SD, Jia Z, Huynh KK. et al. Glutamate substitutions at a PKA consensus site are consistent with inactivation of calpain by phosphorylation. FEBS Lett 2003; 542: 115-118 DOI: 10.1016/s0014-5793(03)00361-2.
    CrossrefPubMedGoogle Scholar
  • 27 Hanna RA, Garcia-Diaz BE, Davies PL. Calpastatin simultaneously binds four calpains with different kinetic constants. FEBS Lett 2007; 581: 2894-2898 doi:10.1016/j.febslet.2007.05.035
    CrossrefPubMedGoogle Scholar
  • 28 Hanna RA, Campbell RL, Davies PL. Calcium-bound structure of calpain and its mechanism of inhibition by calpastatin. Nature 2008; 456: 409-412 doi:10.1038/nature07451
    CrossrefPubMedGoogle Scholar
  • 29 Porn-Ares MI, Samali A, Orrenius S. Cleavage of the calpain inhibitor, calpastatin, during apoptosis. Cell Death Differ 1998; 5: 1028-1033 doi:10.1038/sj.cdd.4400424
    CrossrefPubMedGoogle Scholar
  • 30 Di Lisa F, De Tullio R, Salamino F. et al. Specific degradation of troponin T and I by mu-calpain and its modulation by substrate phosphorylation. Biochem J 1995; 308 ( Pt 1) 57-61 DOI: doi:10.1042/bj3080057.
    CrossrefPubMedGoogle Scholar
  • 31 Kishimoto A, Mikawa K, Hashimoto K. et al. Limited proteolysis of protein kinase C subspecies by calcium-dependent neutral protease (calpain). J Biol Chem 1989; 264: 4088-4092
    CrossrefPubMedGoogle Scholar
  • 32 Smuder AJ, Kavazis AN, Hudson MB. et al. Oxidation enhances myofibrillar protein degradation via calpain and caspase-3. Free Radic Biol Med 2010; 49: 1152-1160 DOI: 10.1016/j.freeradbiomed.2010.06.025.
    CrossrefPubMedGoogle Scholar
  • 33 Davies KJ, Delsignore ME. Protein damage and degradation by oxygen radicals. III. Modification of secondary and tertiary structure. J Biol Chem 1987; 262: 9908-9913
    CrossrefPubMedGoogle Scholar
  • 34 Powers SK, Smuder AJ, Judge AR. Oxidative stress and disuse muscle atrophy: cause or consequence?. Curr Opin Clin Nutr Metab Care 2012; 15: 240-245 doi:10.1097/MCO.0b013e328352b4c2
    CrossrefPubMedGoogle Scholar
  • 35 Gailly P, De Backer F, Van Schoor M. et al. In situ measurements of calpain activity in isolated muscle fibres from normal and dystrophin-lacking mdx mice. J Physiol 2007; 582: 1261-1275 DOI: 10.1113/jphysiol.2007.132191.
    CrossrefPubMedGoogle Scholar
  • 36 Wang KK, Posmantur R, Nath R. et al. Simultaneous degradation of alphaII- and betaII-spectrin by caspase 3 (CPP32) in apoptotic cells. J Biol Chem 1998; 273: 22490-22497 DOI: 10.1074/jbc.273.35.22490.
    CrossrefPubMedGoogle Scholar
  • 37 Yan XX, Jeromin A, Jeromin A. Spectrin breakdown products (SBDPs) as potential biomarkers for neurodegenerative diseases. Curr Transl Geriatr Exp Gerontol Rep 2012; 1: 85-93 doi:10.1007/s13670-012-0009-2
    CrossrefPubMedGoogle Scholar
  • 38 Russell AP. Molecular regulation of skeletal muscle mass. Clin Exp Pharmacol Physiol 2010; 37: 378-384 doi:10.1111/j.1440-1681.2009.05265.x
    CrossrefPubMedGoogle Scholar
  • 39 Williams DA, Head SI, Bakker AJ. et al. Resting calcium concentrations in isolated skeletal muscle fibres of dystrophic mice. J Physiol 1990; 428: 243-256 DOI: 10.1113/jphysiol.1990.sp018210.
    CrossrefPubMedGoogle Scholar
  • 40 Ziman AP, Ward CW, Rodney GG. et al. Quantitative measurement of Ca(2)(+) in the sarcoplasmic reticulum lumen of mammalian skeletal muscle. Biophys J 2010; 99: 2705-2714 DOI: 10.1016/j.bpj.2010.08.032.
    CrossrefPubMedGoogle Scholar
  • 41 Baylor SM, Hollingworth S. Sarcoplasmic reticulum calcium release compared in slow-twitch and fast-twitch fibres of mouse muscle. J Physiol 2003; 551: 125-138 doi:10.1113/jphysiol.2003.041608
    CrossrefPubMedGoogle Scholar
  • 42 Armstrong RB, Warren GL, Warren JA. Mechanisms of exercise-induced muscle fibre injury. Sports Med 1991; 12: 184-207 doi:10.2165/00007256-199112030-00004
    CrossrefPubMedGoogle Scholar
  • 43 Raj DA, Booker TS, Belcastro AN. Striated muscle calcium-stimulated cysteine protease (calpain-like) activity promotes myeloperoxidase activity with exercise. Pflugers Arch 1998; 435: 804-809 doi:10.1007/s004240050587
    CrossrefPubMedGoogle Scholar
  • 44 Belcastro AN. Skeletal muscle calcium-activated neutral protease (calpain) with exercise. J Appl Physiol (1985) 1993; 74: 1381-1386 doi:10.1152/jappl.1993.74.3.1381
    CrossrefPubMedGoogle Scholar
  • 45 Arthur GD, Booker TS, Belcastro AN. Exercise promotes a subcellular redistribution of calcium-stimulated protease activity in striated muscle. Can J Physiol Pharmacol 1999; 77: 42-47 doi:10.1139/cjpp-77-1-42
    CrossrefPubMedGoogle Scholar
  • 46 Sultan KR, Dittrich BT, Leisner E. et al. Fiber type-specific expression of major proteolytic systems in fast- to slow-transforming rabbit muscle. Am J Physiol Cell Physiol 2001; 280: C239-C247 DOI: 10.1152/ajpcell.2001.280.2.C239.
    CrossrefPubMedGoogle Scholar
  • 47 Gissel H. Ca2+ accumulation and cell damage in skeletal muscle during low frequency stimulation. Eur J Appl Physiol 2000; 83: 175-180 doi:10.1007/s004210000276
    CrossrefPubMedGoogle Scholar
  • 48 Kanzaki K, Kuratani M, Matsunaga S. et al. Three calpain isoforms are autolyzed in rat fast-twitch muscle after eccentric contractions. J Muscle Res Cell Motil 2014; 35: 179-189 DOI: 10.1007/s10974-014-9378-9.
    CrossrefPubMedGoogle Scholar
  • 49 Kanzaki K, Watanabe D, Kuratani M. et al. Role of calpain in eccentric contraction-induced proteolysis of Ca(2+)-regulatory proteins and force depression in rat fast-twitch skeletal muscle. J Appl Physiol (1985) 2017; 122: 396-405 DOI: 10.1152/japplphysiol.00270.2016.
    CrossrefPubMedGoogle Scholar
  • 50 Zhang BT, Whitehead NP, Gervasio OL. et al. Pathways of Ca(2)(+) entry and cytoskeletal damage following eccentric contractions in mouse skeletal muscle. J Appl Physiol (1985) 2012; 112: 2077-2086 DOI: 10.1152/japplphysiol.00770.2011.
    CrossrefPubMedGoogle Scholar
  • 51 Zhang BT, Yeung SS, Allen DG. et al. Role of the calcium-calpain pathway in cytoskeletal damage after eccentric contractions. J Appl Physiol (1985) 2008; 105: 352-357 DOI: 10.1152/japplphysiol.90320.2008.
    CrossrefPubMedGoogle Scholar
  • 52 Murphy RM, Goodman CA, McKenna MJ. et al. Calpain-3 is autolyzed and hence activated in human skeletal muscle 24 h following a single bout of eccentric exercise. J Appl Physiol (1985) 2007; 103: 926-931 DOI: 10.1152/japplphysiol.01422.2006.
    CrossrefPubMedGoogle Scholar
  • 53 Murphy RM, Snow RJ, Lamb GD. mu-Calpain and calpain-3 are not autolyzed with exhaustive exercise in humans. Am J Physiol Cell Physiol 2006; 290: C116-C122 doi:10.1152/ajpcell.00291.2005
    CrossrefPubMedGoogle Scholar
  • 54 Murphy RM, Vissing K, Latchman H. et al. Activation of skeletal muscle calpain-3 by eccentric exercise in humans does not result in its translocation to the nucleus or cytosol. J Appl Physiol (1985) 2011; 111: 1448-1458 DOI: 10.1152/japplphysiol.00441.2011.
    CrossrefPubMedGoogle Scholar
  • 55 Vermaelen M, Sirvent P, Raynaud F. et al. Differential localization of autolyzed calpains 1 and 2 in slow and fast skeletal muscles in the early phase of atrophy. Am J Physiol Cell Physiol 2007; 292: C1723-C731 DOI: 10.1152/ajpcell.00398.2006.
    CrossrefPubMedGoogle Scholar
  • 56 Raastad T, Owe SG, Paulsen G. et al. Changes in calpain activity, muscle structure, and function after eccentric exercise. Med Sci Sports Exerc 2010; 42: 86-95 DOI: 10.1249/MSS.0b013e3181ac7afa.
    CrossrefPubMedGoogle Scholar
  • 57 Bartoli M, Bourg N, Stockholm D. et al. A mouse model for monitoring calpain activity under physiological and pathological conditions. J Biol Chem 2006; 281: 39672-39680 DOI: 10.1074/jbc.M608803200.
    CrossrefPubMedGoogle Scholar
  • 58 Neti G, Novak SM, Thompson VF. et al. Properties of easily releasable myofilaments: are they the first step in myofibrillar protein turnover?. Am J Physiol Cell Physiol 2009; 296: C1383-C1390 DOI: 10.1152/ajpcell.00022.2009.
    CrossrefPubMedGoogle Scholar
  • 59 Goll DE, Neti G, Mares SW. et al. Myofibrillar protein turnover: the proteasome and the calpains. J Anim Sci 2008; 86: E19-E35 DOI: 10.2527/jas.2007-0395.
    CrossrefPubMedGoogle Scholar
  • 60 Kumar V, Atherton P, Smith K. et al. Human muscle protein synthesis and breakdown during and after exercise. J Appl Physiol (1985) 2009; 106: 2026-2039 DOI: 10.1152/japplphysiol.91481.2008.
    CrossrefPubMedGoogle Scholar
  • 61 Lametsch R, Roepstorff P, Moller HS. et al. Identification of myofibrillar substrates for mu-calpain. Meat Sci 2004; 68: 515-521 DOI: 10.1016/j.meatsci.2004.03.018.
    CrossrefPubMedGoogle Scholar
  • 62 Morgan DL, Allen DG. Early events in stretch-induced muscle damage. J Appl Physiol (1985) 1999; 87: 2007-2015 doi:10.1152/jappl.1999.87.6.2007
    CrossrefPubMedGoogle Scholar
  • 63 Proske U, Morgan DL. Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J Physiol 2001; 537: 333-345 doi:10.1111/j.1469-7793.2001.00333.x
    CrossrefPubMedGoogle Scholar
  • 64 Takekura H, Fujinami N, Nishizawa T. et al. Eccentric exercise-induced morphological changes in the membrane systems involved in excitation-contraction coupling in rat skeletal muscle. J Physiol 2001; 533: 571-583 DOI: 10.1111/j.1469-7793.2001.0571a.x.
    CrossrefPubMedGoogle Scholar
  • 65 McHugh MP. 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 2003; 13: 88-97
    CrossrefPubMedGoogle Scholar
  • 66 Fielding RA, Meredith CN, O’Reilly KP. et al. Enhanced protein breakdown after eccentric exercise in young and older men. J Appl Physiol (1985) 1991; 71: 674-679 DOI: 10.1152/jappl.1991.71.2.674.
    CrossrefPubMedGoogle Scholar
  • 67 Owens DJ, Twist C, Cobley JN. et al. Exercise-induced muscle damage: What is it, what causes it and what are the nutritional solutions?. Eur J Sport Sci 2019; 19: 71-85 DOI: 10.1080/17461391.2018.1505957.
    CrossrefPubMedGoogle Scholar
  • 68 Mellgren RL, Miyake K, Kramerova I. et al. Calcium-dependent plasma membrane repair requires m- or mu-calpain, but not calpain-3, the proteasome, or caspases. Biochim Biophys Acta 2009; 1793: 1886-1893 DOI: 10.1016/j.bbamcr.2009.09.013.
    CrossrefPubMedGoogle Scholar
  • 69 Lek A, Evesson FJ, Lemckert FA. et al. Calpains, cleaved mini-dysferlinC72, and L-type channels underpin calcium-dependent muscle membrane repair. J Neurosci 2013; 33: 5085-5094 DOI: 10.1523/JNEUROSCI.3560-12.2013.
    CrossrefPubMedGoogle Scholar
  • 70 Roche JA, Lovering RM, Bloch RJ. Impaired recovery of dysferlin-null skeletal muscle after contraction-induced injury in vivo. Neuroreport 2008; 19: 1579-1584 doi:10.1097/WNR.0b013e328311ca35
    CrossrefPubMedGoogle Scholar
  • 71 Ingalls CP, Warren GL, Zhang JZ. et al. Dihydropyridine and ryanodine receptor binding after eccentric contractions in mouse skeletal muscle. J Appl Physiol (1985) 2004; 96: 1619-1625 DOI: 10.1152/japplphysiol.00084.2003.
    CrossrefPubMedGoogle Scholar
  • 72 Corona BT, Balog EM, Doyle JA. et al. Junctophilin damage contributes to early strength deficits and EC coupling failure after eccentric contractions. Am J Physiol Cell Physiol 2010; 298: C365-C376 DOI: 10.1152/ajpcell.00365.2009.
    CrossrefPubMedGoogle Scholar
  • 73 Franzini-Armstrong C, Jorgensen AO. Structure and development of E-C coupling units in skeletal muscle. Ann Rev Physiol 1994; 56: 509-534 doi:10.1146/annurev.ph.56.030194.002453
    CrossrefPubMedGoogle Scholar
  • 74 Ito K, Komazaki S, Sasamoto K. et al. Deficiency of triad junction and contraction in mutant skeletal muscle lacking junctophilin type 1. J Cell Biol 2001; 154: 1059-1067 DOI: 10.1083/jcb.200105040.
    CrossrefPubMedGoogle Scholar
  • 75 Kramerova I, Kudryashova E, Wu B. et al. Novel role of calpain-3 in the triad-associated protein complex regulating calcium release in skeletal muscle. Hum Mol Genet 2008; 17: 3271-3280 DOI: 10.1093/hmg/ddn223.
    CrossrefPubMedGoogle Scholar
  • 76 Kramerova I, Kudryashova E, Ermolova N. et al. Impaired calcium calmodulin kinase signaling and muscle adaptation response in the absence of calpain 3. Hum Mol Genet 2012; 21: 3193-3204 DOI: 10.1093/hmg/dds144.
    CrossrefPubMedGoogle Scholar
  • 77 Milic A, Daniele N, Lochmuller H. et al. A third of LGMD2A biopsies have normal calpain 3 proteolytic activity as determined by an in vitro assay. Neuromuscul Disord 2007; 17: 148-156 DOI: 10.1016/j.nmd.2006.11.001.
    CrossrefPubMedGoogle Scholar
  • 78 Ojima K, Ono Y, Ottenheijm C. et al. Non-proteolytic functions of calpain-3 in sarcoplasmic reticulum in skeletal muscles. J Mol Biol 2011; 407: 439-449 DOI: 10.1016/j.jmb.2011.01.057.
    CrossrefPubMedGoogle Scholar
  • 79 Demirel HA, Powers SK, Naito H. et al. Exercise-induced alterations in skeletal muscle myosin heavy chain phenotype: dose-response relationship. J Appl Physiol (1985) 1999; 86: 1002-1008 DOI: 10.1152/jappl.1999.86.3.1002.
    CrossrefPubMedGoogle Scholar
  • 80 Hody S, Croisier JL, Bury T. et al. Eccentric Muscle Contractions: Risks and Benefits. Front Physiol 2019; 10: 536 DOI: 10.3389/fphys.2019.00536.
    CrossrefPubMedGoogle Scholar
  • 81 Rasmussen BB, Phillips SM. Contractile and nutritional regulation of human muscle growth. Exerc Sport Sci Rev 2003; 31: 127-131
    CrossrefPubMedGoogle Scholar
  • 82 Powers SK, Duarte JA, Le Nguyen B. et al. Endurance exercise protects skeletal muscle against both doxorubicin-induced and inactivity-induced muscle wasting. Pflugers Arch 2019; 471: 441-453 DOI: 10.1007/s00424-018-2227-8.
    CrossrefPubMedGoogle Scholar
  • 83 Shanely RA, Zergeroglu MA, Lennon SL. et al. Mechanical ventilation-induced diaphragmatic atrophy is associated with oxidative injury and increased proteolytic activity. Am J Respir Crit Care Med 2002; 166: 1369-1374 DOI: 10.1164/rccm.200202-088OC.
    CrossrefPubMedGoogle Scholar
  • 84 LeBlanc AD, Schneider VS, Evans HJ. et al. Regional changes in muscle mass following 17 weeks of bed rest. J Appl Physiol (1985) 1992; 73: 2172-2178 DOI: 10.1152/jappl.1992.73.5.2172.
    CrossrefPubMedGoogle Scholar
  • 85 Jones SW, Hill RJ, Krasney PA. et al. Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass. FASEB J 2004; 18: 1025-1027 DOI: 10.1096/fj.03-1228fje.
    CrossrefPubMedGoogle Scholar
  • 86 Ferrando AA, Lane HW, Stuart CA. et al. Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am J Physiol 1996; 270: E627-E633 DOI: 10.1152/ajpendo.1996.270.4.E627.
    CrossrefPubMedGoogle Scholar
  • 87 Levine S, Nguyen T, Taylor N. et al. Rapid disuse atrophy of diaphragm fibers in mechanically ventilated humans. N Engl J Med 2008; 358: 1327-1335 DOI: 10.1056/NEJMoa070447.
    CrossrefPubMedGoogle Scholar
  • 88 Rantanen T. Muscle strength, disability and mortality. Scand J Med Sci Sports 2003; 13: 3-8
    CrossrefPubMedGoogle Scholar
  • 89 Salazar JJ, Michele DE, Brooks SV. Inhibition of calpain prevents muscle weakness and disruption of sarcomere structure during hindlimb suspension. J Appl Physiol (1985) 2010; 108: 120-127 doi:10.1152/japplphysiol.01080.2009
    CrossrefPubMedGoogle Scholar
  • 90 Nelson WB, Smuder AJ, Hudson MB. et al. Cross-talk between the calpain and caspase-3 proteolytic systems in the diaphragm during prolonged mechanical ventilation. Crit Care Med 2012; 40: 1857-1863 DOI: 10.1097/CCM.0b013e318246bb5d.
    CrossrefPubMedGoogle Scholar
  • 91 Siklos M, BenAissa M, Thatcher GR. Cysteine proteases as therapeutic targets: does selectivity matter? A systematic review of calpain and cathepsin inhibitors. Acta Pharm Sin B 2015; 5: 506-519 doi:10.1016/j.apsb.2015.08.001
    CrossrefPubMedGoogle Scholar
  • 92 Tidball JG, Spencer MJ. Expression of a calpastatin transgene slows muscle wasting and obviates changes in myosin isoform expression during murine muscle disuse. J Physiol 2002; 545: 819-828 doi:10.1113/jphysiol.2002.024935
    CrossrefPubMedGoogle Scholar
  • 93 Ingalls CP, Wenke JC, Armstrong RB. Time course changes in [Ca2+]i, force, and protein content in hindlimb-suspended mouse soleus muscles. Aviat Space Environ Med 2001; 72: 471-476
    PubMedGoogle Scholar
  • 94 Aweida D, Rudesky I, Volodin A. et al. GSK3-beta promotes calpain-1-mediated desmin filament depolymerization and myofibril loss in atrophy. J Cell Biol 2018; 217: 3698-3714 DOI: 10.1083/jcb.201802018.
    CrossrefPubMedGoogle Scholar
  • 95 Cea LA, Cisterna BA, Puebla C. et al. De novo expression of connexin hemichannels in denervated fast skeletal muscles leads to atrophy. Proc Natl Acad Sci USA 2013; 110: 16229-16234 DOI: 10.1073/pnas.1312331110.
    CrossrefPubMedGoogle Scholar
  • 96 Matecki S, Dridi H, Jung B. et al. Leaky ryanodine receptors contribute to diaphragmatic weakness during mechanical ventilation. Proc Natl Acad Sci USA 2016; 113: 9069-9074 DOI: 10.1073/pnas.1609707113.
    CrossrefPubMedGoogle Scholar
  • 97 Min K, Smuder AJ, Kwon OS. et al. Mitochondrial-targeted antioxidants protect skeletal muscle against immobilization-induced muscle atrophy. J Appl Physiol (1985) 2011; 111: 1459-1466 DOI: 10.1152/japplphysiol.00591.2011.
    CrossrefPubMedGoogle Scholar
  • 98 Powers SK, Hudson MB, Nelson WB. et al. Mitochondria-targeted antioxidants protect against mechanical ventilation-induced diaphragm weakness. Crit Care Med 2011; 39: 1749-1759 DOI: 10.1097/CCM.0b013e3182190b62.
    CrossrefPubMedGoogle Scholar
  • 99 Hyatt H, Deminice R, Yoshihara T. et al. Mitochondrial dysfunction induces muscle atrophy during prolonged inactivity: A review of the causes and effects. Arch Biochem Biophys 2019; 662: 49-60 DOI: 10.1016/j.abb.2018.11.005.
    CrossrefPubMedGoogle Scholar
  • 100 Jaber S, Petrof BJ, Jung B. et al. Rapidly progressive diaphragmatic weakness and injury during mechanical ventilation in humans. Am J Respir Crit Care Med 2011; 183: 364-371 DOI: 10.1164/rccm.201004-0670OC.
    CrossrefPubMedGoogle Scholar
  • 101 Riley DA, Slocum GR, Bain JL. et al. Rat hindlimb unloading: soleus histochemistry, ultrastructure, and electromyography. J Appl Physiol (1985) 1990; 69: 58-66 DOI: 10.1152/jappl.1990.69.1.58.
    CrossrefPubMedGoogle Scholar
  • 102 Busch WA, Stromer MH, Goll DE. et al. Ca 2+ -specific removal of Z lines from rabbit skeletal muscle. J Cell Biol 1972; 52: 367-381 DOI: 10.1083/jcb.52.2.367.
    CrossrefPubMedGoogle Scholar
  • 103 Xiao YY, Wang MC, Purintrapiban J. et al. Roles of mu-calpain in cultured L8 muscle cells: application of a skeletal muscle-specific gene expression system. Comp Biochem Physiol C Toxicol Pharmacol 2003; 134: 439-450
    CrossrefPubMedGoogle Scholar
  • 104 Dayton WR, Goll DE, Zeece MG. et al. A Ca2+-activated protease possibly involved in myofibrillar protein turnover. Purification from porcine muscle. Biochemistry 1976; 15: 2150-2158 DOI: 10.1021/bi00655a019.
    CrossrefPubMedGoogle Scholar
  • 105 Solomon V, Goldberg AL. Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts. J Biol Chem 1996; 271: 26690-26697 doi:10.1074/jbc.271.43.26690
    CrossrefPubMedGoogle Scholar
  • 106 Plant PJ, Bain JR, Correa JE. et al. Absence of caspase-3 protects against denervation-induced skeletal muscle atrophy. J Appl Physiol (1985) 2009; 107: 224-234 DOI: 10.1152/japplphysiol.90932.2008.
    CrossrefPubMedGoogle Scholar
  • 107 Siu PM, Alway SE. Mitochondria-associated apoptotic signalling in denervated rat skeletal muscle. J Physiol 2005; 565: 309-323 doi:10.1113/jphysiol.2004.081083
    CrossrefPubMedGoogle Scholar
  • 108 Du J, Wang X, Miereles C. et al. Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 2004; 113: 115-123 DOI: doi:10.1172/JCI18330.
    CrossrefPubMedGoogle Scholar
  • 109 Chen M, He H, Zhan S. et al. Bid is cleaved by calpain to an active fragment in vitro and during myocardial ischemia/reperfusion. J Biol Chem 2001; 276: 30724-30728 DOI: 10.1074/jbc.M103701200.
    CrossrefPubMedGoogle Scholar
  • 110 Garcia-Perez C, Roy SS, Naghdi S. et al. Bid-induced mitochondrial membrane permeabilization waves propagated by local reactive oxygen species (ROS) signaling. Proc Natl Acad Sci USA 2012; 109: 4497-4502 DOI: 10.1073/pnas.1118244109.
    CrossrefPubMedGoogle Scholar
  • 111 Polster BM, Basanez G, Etxebarria A. et al. Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J Biol Chem 2005; 280: 6447-6454 DOI: 10.1074/jbc.M41326920.
    CrossrefPubMedGoogle Scholar
  • 112 Joza N, Oudit GY, Brown D. et al. Muscle-specific loss of apoptosis-inducing factor leads to mitochondrial dysfunction, skeletal muscle atrophy, and dilated cardiomyopathy. Mol Cell Biol 2005; 25: 10261-10272 DOI: 10.1128/MCB.25.23.10261-10272.2005.
    CrossrefPubMedGoogle Scholar
  • 113 Guo BS, Cheung KK, Yeung SS. et al. Electrical stimulation influences satellite cell proliferation and apoptosis in unloading-induced muscle atrophy in mice. PLoS One 2012; 7: e30348 DOI: 10.1371/journal.pone.0030348.
    CrossrefPubMedGoogle Scholar
  • 114 Badugu R, Garcia M, Bondada V. et al. N terminus of calpain 1 is a mitochondrial targeting sequence. J Biol Chem 2008; 283: 3409-3417 DOI: 10.1074/jbc.M706851200.
    CrossrefPubMedGoogle Scholar
  • 115 Ni R, Zheng D, Xiong S. et al. Mitochondrial Calpain-1 disrupts ATP synthase and induces superoxide generation in type 1 diabetic hearts: A novel mechanism contributing to diabetic cardiomyopathy. Diabetes 2016; 65: 255-268 DOI: 10.2337/db15-0963.
    CrossrefPubMedGoogle Scholar
  • 116 Smith IJ, Dodd SL. Calpain activation causes a proteasome-dependent increase in protein degradation and inhibits the Akt signalling pathway in rat diaphragm muscle. Exp Physiol 2007; 92: 561-573 doi:10.1113/expphysiol.2006.035790
    CrossrefPubMedGoogle Scholar
  • 117 Smith IJ, Lecker SH, Hasselgren PO. Calpain activity and muscle wasting in sepsis. Am J Physiol Endocrinol Metab 2008; 295: E762-E771 doi:10.1152/ajpendo.90226.2008
    CrossrefPubMedGoogle Scholar
  • 118 Chen HH, Liu P, Auger P. et al. Calpain-mediated tau fragmentation is altered in Alzheimer’s disease progression. Sci Rep 2018; 8: 16725 DOI: 10.1038/s41598-018-35130-y.
    CrossrefPubMedGoogle Scholar
  • 119 Harriss DJ, MacSween A, Atkinson G. Ethical Standards in Sport and Exercise Science Research: 2020 Update. Int J Sports Med 2019; 40: 813-817 doi:10.1055/a-1015-3123
    Artikel in Thieme ConnectPubMedGoogle Scholar