Novel role of calpain-3 in the triad-associated protein complex regulating calcium release in skeletal muscle

Human Molecular Genetics

Volumn 17, Issue 21, 2008, Pages 3271-3280

  Kramerova, Irina ^a   Kudryashova, Elena ^a   Wu, Benjamin ^a   Ottenheijm, Coen ^b   Granzier, Henk ^b   Spencer, Melissa J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALPAIN 3; FRUCTOSE BISPHOSPHATE ALDOLASE; RYANODINE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; EXCITATION CONTRACTION COUPLING; IN VIVO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SKELETAL MUSCLE; TWO HYBRID SYSTEM; WILD TYPE;

ANIMALS; CALCIUM; CALPAIN; CELL LINE; FRUCTOSE-BISPHOSPHATE ALDOLASE; HUMANS; MICE; MUSCLE PROTEINS; MUSCLE, SKELETAL; PROTEIN TRANSPORT; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL;

EID: 54449100812     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn223     Document Type: Article

References (42)

1. Kramerova, I., Beckmann, J.S. and Spencer, M.J. (2007) Molecular and cellular basis of calpainopathy (limb girdle muscular dystrophy type 2A). Biochim. Biophys. Acta, 1772, 128-144.
2. Milic, A., Daniele, N., Lochmuller, H., Mora, M., Comi, G.P., Moggio, M., Noulet, F., Walter, M.C., Morandi, L., Poupiot, J. et al. (2007) A third of LGMD2A biopsies have normal calpain 3 proteolytic activity as determined by an in vitro assay. Neuromuscul. Disord., 17, 148-156.
3. Kramerova, I., Kudryashova, E., Tidball, J.G. and Spencer, M.J. (2004) Null mutation of calpain 3 (p94) in mice causes abnormal sarcomere formation in vivo and in vitro. Hum. Mol. Genet., 13, 1373-1388.
4. Sorimachi, H., Kinbara, K., Kimura, S., Takahashi, M., Ishiura, S., Sasagawa, N., Sorimachi, N., Shimada, H., Tagawa, K., Maruyama, K. et al. (1995) Muscle-specific calpain, p94, responsible for limb girdle muscular dystrophy type 2A, associates with connectin through IS2, a p94-specific sequence. J. Biol. Chem., 270, 31158-31162.
5. Kinbara, K., Sorimachi, H., Ishiura, S. and Suzuki, K. (1997) Muscle-specific calpain, p94, interacts with the extreme C-terminal region of connectin, a unique region flanked by two immunoglobulin C2 motifs. Arch. Biochem. Biophys., 342, 99-107.
6. Garvey, S.M., Rajan, C., Lerner, A.P., Frankel, W.N. and Cox, G.A. (2002) The muscular dystrophy with myositis (mdm) mouse mutation disrupts a skeletal muscle-specific domain of titin. Genomics, 79, 146-149.
7. Haravuori, H., Mäkelä-Bengs, P., Udd, B., Partanen, J., Pulkkinen, L., Somer, H. and Peltonen, L. (1998) Assignment of the tibial muscular dystrophy locus to chromosome 2q31. Am. J. Hum. Genet., 62, 620-626.
8. Udd, B., Vihola, A., Sarparanta, J., Richard, I. and Hackman, P. (2005) Titinopathies and extension of the M-line mutation phenotype beyond distal myopathy and LGMD2J. Neurology, 64, 636-642.
9. Gamblin, S.J., Davies, G.J., Grimes, J.M., Jackson, R.M., Littlechild, J.A. and Watson, H.C. (1991) Activity and specificity of human aldolases. J. Mol. Biol., 219, 573-576.
10. 2+ transport. Circ. Res., 77, 88-97.
11. Franzini-Armstrong, C. (1994) The sarcoplasmic reticulum and the transverse tubules. In Engel, A.G. and Franzini-Armstrong, C. (eds), Myology. McGaw-Hill, Inc., New York, pp. 176-199.
12. Han, J.W., Thieleczek, R., Varsanyi, M. and Heilmeyer, L.M., Jr (1992) Compartmentalized ATP synthesis in skeletal muscle triads. Biochemistry, 31, 377-384.
13. 2+ release by glycolysis in cat atrial myocytes. J. Physiol., 564, 697-714.
14. Seo, I.R., Moh, S.H., Lee, E.H., Meissner, G. and Kim do, H. (2006) Aldolase potentiates DIDS activation of the ryanodine receptor in rabbit skeletal sarcoplasmic reticulum. Biochem. J., 399, 325-333.
15. Yao, D.C., Tolan, D.R., Murray, M.F., Harris, D.J., Darras, B.T., Geva, A. and Neufeld, E.J. (2004) Hemolytic anemia and severe rhabdomyolysis caused by compound heterozygous mutations of the gene for erythrocyte/ muscle isozyme of aldolase, ALDOA(Arg303X/Cys338Tyr). Blood, 103, 2401-2403.
16. Kreuder, J., Borkhardt, A., Repp, R., Pekrun, A., Gottsche, B., Gottschalk, U., Reichmann, H., Schachenmayr, W., Schlegel, K. and Lampert, F. (1996) Brief report: Inherited metabolic myopathy and hemolysis due to a mutation in aldolase A. N. Engl. J. Med., 334, 1100-1104.
17. Kramerova, I., Kudryashova, E., Wu, B. and Spencer, M.J. (2006) Regulation of the M-cadherin-beta-catenin complex by calpain 3 during terminal stages of myogenic differentiation. Mol. Cell Biol., 26, 8437-8447.
18. Sorimachi, H., Toyama-Sorimachi, N., Saido, T.C., Kawasaki, H., Sugita, H., Miyasaka, M., Arahata, K., Ishiura, S. and Suzuki, K. (1993) Muscle-specific calpain, p94, is degraded by autolysis immediately after translation, resulting in disappearance from muscle. J. Biol. Chem. 268, 10593-10605.
19. Taveau, M., Bourg, N., Sillon, G., Roudaut, C., Bartoli, M. and Richard, I. (2003) Calpain 3 is activated through autolysis within the active site and lyses sarcomeric and sarcolemmal components. Mol. Cell Biol. 23, 9127-9135.
20. Knudson, C.M. and Campbell, K.P. (1989) Albumin is a major protein component of transverse tubule vesicles isolated from skeletal muscle. J. Biol. Chem., 264, 10795-10798.
21. Bayer, K.U., Harbers, K. and Schulman, H. (1998) AlphaKAP is an anchoring protein for a novel CaM kinase II isoform in skeletal muscle. EMBO J., 17, 5598-5605.
22. 2+/calmodulin-dependent manner. J. Biol. Chem., 279, 35176-35182.
23. Edmunds, T., Nagainis, P.A., Sathe, S.K., Thompson, V.F. and Goll, D.E. (1991) Comparison of the autolyzed and unautolyzed forms of mu- and m-calpain from bovine skeletal muscle. Biochim. Biophys. Acta, 1077, 197-208.
24. Anderson, L.V.B., Harrison R.M., Pogue, R., Vafiadaki, E., Pollift, C., Davison, K., Moss, J.A., Keers, S., Pyle, A., Shaw, P.J. et al. (2000) Secondary reduction in calpain 3 expression in patients with limb girdle muscular dystrophy type 2B and Miyoshi myopathy (primary dysferlinopathies). Neuromus. Dis., 10, 553-559.
25. Chrobakova, T., Hermanova, M., Kroupova, I., Vondracek, P., Marikova, T., Mazanec, R., Zamecnik, J., Stanek, J., Havlova, M. and Fajkusova, L. (2004) Mutations in Czech LGMD2A patients revealed by analysis of calpain3 mRNA and their phenotypic outcome. Neuromus. Dis., 14 659-665.
26. Huang, Y., Verheesen, P., Roussis, A., Frankhuizen, W., Ginjaar, I., Haldane, F., Laval, S., Anderson, L.V., Verrips, T., Frants, R.R. et al. (2005) Protein studies in dysferlinopathy patients using Ilama-derived antibody fragments selected by phage display. Eur. J. Hum. Genet., 13, 721-730.
27. Bansal, D. and Campbell, K.P. (2004) Dysferlin and the plasma membrane repair in muscular dystrophy. Trends Cell Biol., 14, 206-213.
28. Klinge, L., Laval, S., Keers, S., Haldane, F., Straub, V., Barresi, R. and Bushby, K. (2007) From T-tubule to sarcolemma: Damage-induced dysferlin translocation in early myogenesis. FASEB J., 21, 1768-1776.
29. Ampong, B.N., Imamura, M., Matsumiya, T., Yoshida, M. and Takeda, S. (2005) Intracellular localization of dysferlin and its association with the dihydropyridine receptor. Acta Myol., 24, 134-144.
30. Jia, Z., Petrounevitch, V., Wong, A., Moldoveanu, T., Davies, P.L., Elce, J.S. and Beckmann, J.S. (2001) Mutations in calpain 3 associated with limb girdle muscular dystrophy: Analysis by molecular modeling and by mutation in m-calpain. Biophys. J., 80, 2590-2596.
31. Ono, Y., Shimada, H., Sorimachi, H., Richard, I., Saido, T.C., Beckmann, J.S., Ishiura, S. and Suzuki, K. (1998) Functional defects of a muscle-specific calpain, p94, caused by mutations associated with limb-girdle muscular dystrophy type 2A. J. Biol. Chem., 273, 17073-17078.
32. Baghdiguian, S., Martin, M., Richard, I., Pons, F., Astier, C., Bourg, N., Hay, R.T., Chemaly, R., Halaby, G., Loiselet, J. et al. (1999) Calpain 3 deficiency is associated with myonuclear apoptosis and profound perturbation of the IkappaB alpha/NF-kappaB pathway in limb-girdle muscular dystrophy type 2A [published erratum appears in Nat. Med. (1999) 5(7), 849]. Nat. Med., 5, 503-511.
33. Kramerova, I., Kudryashova, E., Venkatraman, G. and Spencer, M.J. (2005) Calpain 3 participates in sarcomere remodeling by acting upstream of the ubiquitin-proteasome pathway. Hum. Mol. Genet., 14, 2125-2134.
34. Benayoun, B., Baghdiguian, S., Lajmanovich, A., Bartoli, M., Daniele, N., Gicquel, E., Bourg, N., Raynaud, F., Pasquier, M.A., Suel, L. et al. (2008) NF-kappaB-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., 22, 1521-1529.
35. Goll, D.E., Thompson, V.F., Li, H., Wei, W. and Cong, J. (2003) The calpain system. Physiol. Rev., 83, 731-801.
36. Guyon, J.R., Kudryashova, E., Potts, A., Dalkilic, I., Brosius, M.A., Thompson, T.G., Beckmann, J.S., Kunkel, L.M. and Spencer, M.J. (2003) Calpain 3 cleaves filamin C and regulates its ability to interact with gamma- and delta-sarcoglycans. Muscle Nerve, 28, 472-483.
37. Duguez, S., Bartoli, M. and Richard, I. (2006) Calpain 3: A key regulator of the sarcomere? FEBS J., 273, 3427-3436.
38. Knight, P.J. and Trinick, J.A. (1982) Preparation of myofibrils. Methods Enzymol., 85, 9-12.
39. Miller, G., Peter, A.K., Espinoza, E., Heighway, J. and Crosbie, R.H. (2006) Over-expression of microspan, a novel component of the sarcoplasmic reticulum, causes severe muscle pathology with triad abnormalities. J. Muscle Res. Cell Motil., 27, 545-558.
40. Capote, J., Bolanos, P., Schuhmeier, R.P., Melzer, W. and Caputo, C. (2005) Calcium transients in developing mouse skeletal muscle fibres. J. Physiol., 564, 451-464.
41. Westerblad, H. and Allen, D.G. (1991) Changes of myoplasmic calcium concentration during fatigue in single mouse muscle fibers. J. Gen. Physiol., 98, 615-635.
42. Pinniger, G.J., Bruton, J.D., Westerblad, H. and Ranatunga, K.W. (2005) Effects of a myosin-II inhibitor (N-benzyl-p-toluene sulphonamide, BTS) on contractile characteristics of intact fast-twitch mammalian muscle fibres. J. Muscle Res. Cell Motil., 26, 135-141.