Calpains, skeletal muscle function and exercise

Clinical and Experimental Pharmacology and Physiology

Volumn 37, Issue 3, 2010, Pages 385-391

  Murphy, Robyn M ^a  

^a LA TROBE UNIVERSITY   (Australia)

Author keywords

calpain; Calpain 1; Calpain 3; Muscle proteolysis; P94

Indexed keywords

CALCIUM; CALPAIN 1; CALPAIN 3;

CONFERENCE PAPER; ENDURANCE; EXERCISE; IN VITRO STUDY; IN VIVO STUDY; LIMB GIRDLE MUSCULAR DYSTROPHY; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE FUNCTION; NONHUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN FUNCTION; SARCOMERE; SKELETAL MUSCLE;

ANIMALS; CALCIUM; CALPAIN; EXERCISE; HUMANS; MUSCLE CONTRACTION; MUSCLE, SKELETAL;

EID: 77649118935     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/j.1440-1681.2009.05310.x     Document Type: Conference Paper

References (64)

1. Sorimachi H, Imajoh-Ohmi S, Emori Y et al. Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m- and mu-types. Specific expression of the mRNA in skeletal muscle. J. Biol. Chem. 1989 264 : 20106 20111.
2. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol. Rev. 2003 83 : 731 801.
3. Dutt P, Croall DE, Arthur JS et al. m-Calpain is required for preimplantation embryonic development in mice. BMC Dev. Biol. 2006 6 : 3 14.
4. Zimmerman UJ, Boring L, Pak JH, Mukerjee N, Wang KK. The calpain small subunit gene is essential: Its inactivation results in embryonic lethality. IUBMB Life 2000 50 : 63 8.
5. Ravulapalli R, Diaz BG, Campbell RL, Davies PL. Homodimerization of calpain-3 penta-EF-hand domain. Biochem. J. 2005 388 : 585 591.
6. Garcia Diaz BE, Moldoveanu T, Kuiper MJ, Campbell RL, Davies PL. Insertion sequence 1 of muscle-specific calpain, p94, acts as an internal propeptide. J. Biol. Chem. 2004 279 : 27656 27666.
7. Sorimachi H, Kinbara K, Kimura S et al. Muscle-specific calpain, p94, responsible for limb girdle muscular dystrophy type 2A, associates with connectin through IS2, a p94-specific sequence. J. Biol. Chem. 1995 270 : 31158 31162.
8. Xu L, Deng X. Protein kinase C promotes nicotine-induced migration and invasion of cancer cells via phosphorylation of micro- and m-calpains. J. Biol. Chem. 2006 281 : 4457 4466.
9. Goll DE, Neti G, Mares SW, Thompson VF. Myofibrillar protein turnover: The proteasome and the calpains. J. Anim. Sci. 2008 86 : E19 35.
10. Saido TC, Sorimachi H, Suzuki K. Calpain: New perspectives in molecular diversity and physiological-pathological involvement. FASEB J. 1994 8 : 814 822.
11. 2+-induced disruption of excitation-contraction coupling in mammalian skeletal muscle fibers. Am. J. Physiol. Cell Physiol. 2009 296 : C1115 22.
12. Mellgren RL, Zhang W, Miyake K, McNeil PL. Calpain is required for the rapid, calcium-dependent repair of wounded plasma membrane. J. Biol. Chem. 2007 282 : 2567 2575.
13. 2+ activation of diffusible and bound pools of μ-calpain in rat skeletal muscle. J. Physiol. 2006 576 : 595 612.
14. Gailly P, De Backer F, Van Schoor M, Gillis JM. In situ measurements of calpain activity in isolated muscle fibres from normal and dystrophin-lacking mdx mice. J. Physiol. 2007 582 : 1261 1275.
15. Lamb GD. Calpains in muscle: Selective and protective? J. Physiol. 2007 582 : 897.
16. 2+ on binding of the calpains to calpastatin. J. Biol. Chem. 1989 264 : 17888 17896.
17. Murphy RM, Snow RJ, Lamb GD. μ-Calpain and calpain-3 are not autolyzed with exhaustive exercise in humans. Am. J. Physiol. Cell Physiol. 2006 290 : C116 22.
18. 2+ requirement of calpain activation. Biochem. Biophys. Res. Commun. 2004 323 : 1131 1133.
19. 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.
20. 2+ in the development of low frequency fatigue in mouse single muscle fibres. J. Physiol. 1996 491 : 813 824.
21. Lamb GD. Mechanisms of excitation-contraction uncoupling relevant to activity-induced muscle fatigue. Appl. Physiol. Nutr. Metab. 2009 34 : 368 372.
22. Murphy RM, Mollica JP, Lamb GD. Plasma membrane removal in rat skeletal muscle fibers reveals caveolin-3 hot-spots at the necks of transverse tubules. Exp. Cell Res. 2009 315 : 1015 1028.
23. Posterino GS, Lamb GD, Stephenson DG. Twitch and tetanic force responses and longitudinal propagation of action potentials in skinned skeletal muscle fibres of the rat. J. Physiol. 2000 527 : 131 137.
24. Mollica JP, Oakhill JS, Lamb GD, Murphy RM. Are genuine changes in protein expression being overlooked? Reassessing western blotting Anal. Biochem. 2009 386 : 270 275.
25. Belcastro AN, Shewchuk LD, Raj DA. Exercise-induced muscle injury: A calpain hypothesis. Mol. Cell. Biochem. 1998 179 : 135 145.
26. Beckmann JS, Spencer M. Calpain 3, the 'gatekeeper' of proper sarcomere assembly, turnover and maintenance. Neuromuscul. Disord. 2008 18 : 913 921.
27. Dargelos E, Moyen C, Dedieu S et al. Development of an inducible system to assess p94 (CAPN3) function in cultured muscle cells. J. Biotechnol. 2002 96 : 271 279.
28. Richard I, Roudaut C, Marchand S et al. Loss of calpain 3 proteolytic activity leads to muscular dystrophy and to apoptosis-associated IκBα/nuclear factor κB pathway perturbation in mice. J. Cell Biol. 2000 151 : 1583 1590.
29. Baghdiguian S, Martin M, Richard I et al. Calpain 3 deficiency is associated with myonuclear apoptosis and profound perturbation of the IκBα/NF-κB pathway in limb-girdle muscular dystrophy type 2A. Nat. Med. 1999 5 : 503 511. (Pubitemid 29220208)
30. Saenz A, Leturcq F, Cobo AM et al. LGMD2A: Genotype-phenotype correlations based on a large mutational survey on the calpain 3 gene. Brain 2005 128 : 732 742.
31. Fougerousse F, Bullen P, Herasse M et al. Human-mouse differences in the embryonic expression patterns of developmental control genes and disease genes. Hum. Mol. Genet. 2000 9 : 165 173.
32. 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.
33. Fougerousse F, Gonin P, Durand M, Richard I, Raymackers JM. Force impairment in calpain 3-deficient mice is not correlated with mechanical disruption. Muscle Nerve 2003 27 : 616 623.
34. Haravuori H, Vihola A, Straub V et al. Secondary calpain3 deficiency in 2q-linked muscular dystrophy: Titin is the candidate gene. Neurology 2001 56 : 869 877.
35. Huebsch KA, Kudryashova E, Wooley CM et al. Mdm muscular dystrophy: Interactions with calpain 3 and a novel functional role for titin's N2A domain. Hum. Mol. Genet. 2005 14 : 2801 2811.
36. Baghdiguian S, Richard I, Martin M et al. Pathophysiology of limb girdle muscular dystrophy type 2A: Hypothesis and new insights into the IκBα/NF-κB survival pathway in skeletal muscle. J. Mol. Med. 2001 79 : 254 261.
37. 2+-dependent intramolecular autolysis. FEBS Lett. 2002 532 : 401 406.
38. 2+ dependency of calpain 3 (p94) activation. Biochemistry 2006 45 : 3714 3722.
39. Sorimachi H, Toyama-Sorimachi N, Saido TC et al. Muscle-specific calpain, p94, is degraded by autolysis immediately after translation, resulting in disappearance from muscle. J. Biol. Chem. 1993 268 : 10593 10605.
40. Branca D, Gugliucci A, Bano D, Brini M, Carafoli E. Expression, partial purification and functional properties of the muscle-specific calpain isoform p94. Eur. J. Biochem. 1999 265 : 839 846.
41. 2+ and is not dependent on stretch. J. Biol. Chem. 2009 284 : 7811 7819.
42. Ono Y, Torii F, Ojima K et al. Suppressed disassembly of autolyzing p94/CAPN3 by N2A connectin/titin in a genetic reporter system. J. Biol. Chem. 2006 281 : 18519 18531.
43. Kramerova I, Kudryashova E, Wu B, Ottenheijm C, Granzier H, Spencer MJ. Novel role of calpain-3 in the triad-associated protein complex regulating calcium release in skeletal muscle. Hum. Mol. Genet. 2008 17 : 3271 3280.
44. Keira Y, Noguchi S, Minami N, Hayashi YK, Nishino I. Localization of calpain 3 in human skeletal muscle and its alteration in limb-girdle muscular dystrophy 2A muscle. J. Biochem. 2003 133 : 659 664.
45. Ojima K, Ono Y, Hata S, Koyama S, Doi N, Sorimachi H. Possible functions of p94 in connectin-mediated signaling pathways in skeletal muscle cells. J. Muscle Res. Cell Motil. 2006 26 : 409 417.
46. Hayashi C, Ono Y, Doi N et al. Multiple molecular interactions implicate the connectin/titin N2A region as a modulating scaffold for p94/calpain 3 activity in skeletal muscle. J. Biol. Chem. 2008 283 : 14801 14814.
47. Taveau M, Bourg N, Sillon G, Roudaut C, Bartoli M, Richard I. Calpain 3 is activated through autolysis within the active site and lyses sarcomeric and sarcolemmal components. Mol. Cell. Biol. 2003 23 : 9127 9135.
48. Duguez S, Bartoli M, Richard I. Calpain 3: A key regulator of the sarcomere? FEBS J. 2006 273 : 3427 3436.
49. Guyon JR, Kudryashova E, Potts A et al. Calpain 3 cleaves filamin C and regulates its ability to interact with γ- and δ-sarcoglycans. Muscle Nerve 2003 28 : 472 483.
50. Cohen N, Kudryashova E, Kramerova I et al. Identification of putative in vivo substrates of calpain 3 by comparative proteomics of overexpressing transgenic and nontransgenic mice. Proteomics 2006 6 : 6075 6084.
51. Ono Y, Kakinuma K, Torii F et al. Possible regulation of the conventional calpain system by skeletal muscle-specific calpain, p94/calpain 3. J. Biol. Chem. 2004 279 : 2761 2771.
52. Kramerova I, Kudryashova E, Wu B et al. Mitochondrial abnormalities, energy deficit and oxidative stress are features of calpain 3 deficiency in skeletal muscle. Hum. Mol. Genet. 2009 18 : 3194 3305.
53. Gentil BJ, Delphin C, Benaud C, Baudier J. Expression of the giant protein AHNAK (desmoyokin) in muscle and lining epithelial cells. J. Histochem. Cytochem. 2003 51 : 339 348.
54. Huang Y, de Morree A, van Remoortere A et al. Calpain 3 is a modulator of the dysferlin protein complex in skeletal muscle. Hum. Mol. Genet. 2008 17 : 1855 1866.
55. Benayoun B, Baghdiguian S, Lajmanovich A et al. NF-κB-dependent expression of the antiapoptotic factor c-FLIP is regulated by calpain 3, the protein involved in limb-girdle muscular dystrophy type 2A. FASEB J. 2008 22 : 1521 1529.
56. Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: Cellular mechanisms. Physiol. Rev. 2008 88 : 287 332.
57. i following acute and long-term downhill running exercise in mice. Cell Calcium 1997 22 : 373 383.
58. 2+- activated proteases in toad muscle fibres. J. Physiol. 2005 564 : 775 789.
59. Murphy RM, Lamb GD. Calpain-3 is activated following eccentric exercise. J. Appl. Physiol. 2009 106 : 2068.
60. Feasson L, Stockholm D, Freyssenet D et al. Molecular adaptations of neuromuscular disease-associated proteins in response to eccentric exercise in human skeletal muscle. J. Physiol. 2002 543 : 297 306.
61. Lehti M, Kivela R, Komi PV, Komulainen J, Kainulainen H, Kyrolainen H. Effects of fatiguing jumping exercise on mRNA expression of titin-complex proteins and calpains. J. Appl. Physiol. 2009 106 : 1419 1424.
62. Murphy RM, Goodman CA, McKenna MJ, Bennie J, Leikis M, Lamb GD. Calpain-3 is autolyzed and hence activated in human skeletal muscle 24 h following a single bout of eccentric exercise. J. Appl. Physiol. 2007 103 : 926 931.
63. Jones SW, Parr T, Sensky PL, Scothern GP, Bardsley RG, Buttery PJ. Fibre type-specific expression of p94, a skeletal muscle-specific calpain. J. Muscle Res. Cell Motil. 1999 20 : 417 424.
64. Ono Y, Hayashi C, Doi N, Tagami M, Sorimachi H. The importance of conserved amino acid residues in p94 protease sub-domain IIb and the IS2 region for constitutive autolysis. FEBS Lett. 2008 582 : 691 698.