Abstract
Precise regulation of numerous cellular events is essential for cell function and survival. Proteolysis in the cytosol is one of the important systems that modulate cellular functions internally. In muscle tissues, the involvement of several classes of proteases in various cellular events has been studied extensively, including their roles in myofibrillar protein turnover, myoblast fusion, cell cycle progression, and so on. Calpain, an intracellular Ca2+-dependent cysteine protease, is considered one of the most significant proteases in muscle tissues in both normal and pathological conditions. Muscular dystrophy is a group of neuromuscular disorders that present with necrosis and irregularly sized muscle fibers. Excessive degradation of myofibrillar proteins is responsible for this pathological change. Since degenerative muscle is often accompanied by an elevated cytosolic Ca2+ concentration, it is almost certain that proteolysis by calpain initiates the fiber necrosis. Therefore, the study of calpain in muscular dystrophy has aimed principally at developing means of suppressing calpain activity. Recent studies have revealed another aspect of the relationship between calpain and muscular dystrophy. A mutation in p94, also called calpain 3, is responsible for limb-girdle muscular dystrophy type 2A (LGMD2A). This provides definitive evidence that the calpain system is vital for normal muscle function. Moreover, it suggests for the first time that the activity of one calpain species might oppose the effect of another. In this chapter, we briefly review the molecular structure of calpain and focus on the uncertain, but likely, pathophysiological roles of calpain in muscle diseases based on current knowledge.
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References
Anderson, L.V.B. and Davison, K., 1999, Multiplex Western blotting system for the analysis of muscular dystrophy proteins, Am. J. Pathol. 154, 1017–1022.
Anderson, L.V., Davison, K., Mossa, J.A., Richard, I., Fardeau, M., Tome, F.M., Hubner, C., Lasa, A., Colomer, J. and Beckmann, J.S., 1998, Characterization of monoclonal antibodies to calpain 3 and protein expression in muscle from patients with limb-girdle muscular dystrophy type 2A, Am. J. Pathol. 153, 1169–1179.
Araishi, K., Sasaoka, T., Imamura, M., Noguchi, S., Hama, H., Wakabayashi, E., Yoshida, M., Hori, T. and Ozawa, E., 1999, Loss of the sarcoglycan complex and sarcospan leads to muscular dystrophy in β-sarcoglycan-deficient mice, Hum. Mol. Genet. 8, 1589–1598.
Baghdiguian, S., Martin, M., Richard, I., Pons, F., Astier, C., Bourg, N., Hay, R.T., Chemaly, R., Halaby, G., Loiselet, J., Anderson, L.V.B., de Munain, A.L., Fardeau, M., Mangeat, P., Beckmann, J.S. and Lefranc, G., 1999, Calpain 3 deficiency is associated with myonuclear apoptosis and profound perturbation of the Ikfialpha/NF-kB pathway in limb-girdle muscular dystrophy type 2A, Nat. Med. 5, 503–511.
Barnes, T.M. and Hodgkin, J., 1996, The tra-3 sex determination gene of Caenorhabditis elegans encodes a member of the calpain regulatory protease family, EMBO J. 15, 4477–4484.
Beckmann, J.S. and Bushby, K.M., 1996, Advances in the molecular genetics of the limb-girdle type of autosomal recessive progressive muscular dystrophy, Curr. Opin. Neurol. 9, 389–393.
Blanchard, H., Grochulski, P., Li, Y., Arthur, J.S., Davies, P.L., Elce, J.S. and Cygler, M., 1997, Structure of a calpain Ca2+-binding domain reveals a novel EF-hand and Ca2+-induced conformational changes, Nat. Struct. Bio. 4, 532–538.
Bonnemann, C.G., McNally, E.M. and Kunkel, L.M., 1996, Beyond dystrophin: Current progress in the muscular dystrophies, Curr. Opin. Pediatr. 8, 569–582.
Branca, D., Gugliucci, A., Bano, D., Brini, M. and Carafoli, E., 1999, Expression, partial purification and functional properties of the muscle-specific calpain isoform p94, Eur. J. Biochem. 265, 839–846.
Brenman, J.E., Chao, D.S., Xia, H., Aldape, K. and Bredt, D.S., 1995, Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy, Cell 82, 743–752.
Brook, J.D., McCurrach, M.E., Harley, H.G., Buckler, A.J., Church, D., Aburatani, H., Hunter, K., Stanton, V.P., Thirion, J.P, Hudson, T, Sohn, R., Zemelman, B., Snell, R.G., Rundle, S.A., Crow, S., Davies, J., Shelbourne, P., Buxton, J., Jones, C., Juvonen, V., Johnson, K., Harper, P.S., Shaw, D.J. and Housman, D.E., 1992, Molecular basis of myotonic dystrophy: Expansion of a trinucleotide (CTG) repeat at the 3′ end of a transcript encoding a protein kinase family member, Cell 68, 799–808.
Bushby, K.M.D., 1999, Making sense of the limb-girdle muscular dystrophies, Brain 122, 1403–1420.
Carafoli, E. and Molinari, M., 1998, Calpain: A protease in search of a function?, Biochem. Biophys. Res. Commun. 247, 193–203.
Chou, F.L., Angelini, C., Daentl, D., Garcia, C., Greco, C., Hausmanowa-Petrusewicz, I., Fidzianska, A., Wessel, H. and Hoffman, E.P., 1999, Calpain III mutation analysis of a heterogeneous limb-girdle muscular dystrophy population, Neurol. 52, 1015–1020.
Coral-Vazquez, R., Cohn, R.D., Moore, S.A., Hill, J.A., Weiss, R.M., Davisson, R.L., Straub, V., Barresi, R., Bansal, D., Hrstka, R.F., Williamson, R. and Campbell, K.P., 1999, Disruption of the sarcoglycan-sarcospan complex in vascular smooth muscle: A novel mechanism for cardiomyopathy and muscular dystrophy, Cell 98, 465–474.
David, L.L. and Shearer, T.R., 1993, Beta-crystallins insolubilized by calpain II in vitro contain cleavage sites similar to beta-crystallins insolubilized during cataract, FEBS Lett. 324, 265–270.
Dear, N., Matena, K., Vingron, M. and Boehm, T., 1997, A new subfamily of vertebrate calpains lacking a calmodulin-like domain: Implications for calpain regulation and evolution, Genomics 45, 175–184.
Delaney, S.J., Hayward, D.C., Barleben, F., Fischbach, K.F. and Gabor-Miklos, G.L., 1991, Molecular cloning and analysis of small optic lobes, a structural brain gene of Drosophila melanogaster, Proc. Natl. Acad. Sci. USA 88, 7213–7218.
Denison, S.H., Orejas, M. and Arst. Jr., H.N., 1995, Signaling of ambient pH in Aspergillus involves a cysteine protease, J. Biol. Chem. 270, 28519–28522.
Duclos, F., Straub, V., Moore, S.A., Venzke, D.P., Hrstka, R.F., Crosbie, R.H., Durbeej, M., Lebakken, C.S., Ettinger, A.J., van der Meulen, J., Holt, K.H., Lim, L.E., Sanes, J.R., Davidson, B.L., Faulkner, J.A., Williamson, R. and Campbell, K.P., 1998, Progressive muscular dystrophy in alpha-sarcoglycan-deficient mice, J. Cell. Biol. 142, 1461–1471.
Emery, A.E.H., 1998, The muscular dystrophies, BMJ 317, 991–995.
Fardeau, M., Hillaire, D., Mignard, C., Feingold, N., Feingold, J., Mignard, D., deUbeda, B., Collin, H., Tome, F.M.S., Richard, I. and Beckmann, J.S., 1996, Juvenile limb-girdle muscular dystrophy: Clinical, histopathological, and genetic data from a small community living in the Reunion Island, Brain 119, 295–308.
Fong, P.Y., Turner, P.R., Denetclaw, W.F. and Steinhardt, R.A., 1990, Increased activity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin, Science 250, 673–676.
Fougerousse, F., Bullen, P., Herasse, M., Lindsay, S., Richard, I., Lee, S., Suel, L., McMahon, A., Durand, D., Robson, S., Wilson, D., Abitbol, M., Beckmann, J.S. and Strachan, T, 2000, Human-mouse differences in the embryonic expression patterns of developmental control genes and disease genes, Hum. Mol. Genet. 9, 165–173.
Franz, T., Vingron, M., Boehm, T. and Dear, T.N., 1999, Capn7: A highly divergent vertebrate calpain with a novel C-terminal domain, Mamm. Genome 10, 318–321.
Futai, E., Maeda, T., Sorimachi, H., Kitamoto, K., Ishiura, S. and Suzuki, K., 1999, The protease activity of a calpain-like cysteine protease in Saccharomyces cerevisiae is required for alkaline adaptation and sporulation, Mol. Gen. Genet. 260, 559–568.
Goll, D.E., Thompson, V.F., Taylo, R.G., Ouali, A. and Chou, R.G.R., 1999, Calpain: Pharmacology and Toxicology of Calcium-Dependent Protease, Taylor & Francis, Philadelphia, pp. 127–160.
Greenberg, D.A., 1999, Neuromuscular disease and calcium channels, Muscle Nerve 22, 1341–1349.
Gregorio, C.C., Trombitas, K., Centner, T, Kolmerer, B., Stier, G, Kunke, K., Suzuki, K., Obermayr, F, Herrmann, B., Granzier, H., Sorimachi, H. and Labeit, S., 1998, The NH2 terminus of titin spans the Z-disc: Its interaction with a novel 19-kD ligand (T-cap) is required for sarcomeric integrity, J. Cell. Biol. 143, 1013–1027.
Hack, A.A., Ly, C.T., Jiang, F., Clendenin, C.J., Sigrist, K.S., Wollmann, R.L. and McNally, E.M., 1998, Gamma-sarcoglycan deficiency leads to muscle membrane defects and apoptosis independent of dystrophin, J. Cell. Biol. 142, 1279–1287.
Haravuori, H., Makela-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.
Herasse, M., Ono, Y., Fougerousse, F., Kimura, E., Stockholm, D., Beley, C., Montarras, D., Pinset, C., Sorimachi, H., Suzuki, K., Beckmann, J.S. and Richard, I., 1999, Expression and functional characteristics of calpain 3 isoforms generated through tissue-specific transcriptional and posttranscriptional events, Mol. Cell. Biol. 19, 4047–4055.
Hoffman, E.P., Brown, R.H., Jr. and Kunkel, L.M., 1987, Dystrophin: The protein product of the Duchenne muscular dystrophy locus, Cell 51, 919–928.
Hopf, F.W., Turner, P.R., Denetclaw, W.F., Jr., Reddy, P. and Steinhardt, R.A., 1996, A critical evaluation of resting intracellular free calcium regulation in dystrophic mdx muscle, Am. J. Physiol. 271, 1325–1339.
Hosfield, C.H., Elce, J.S., Davies, P.L. and Jia, Z., 1999, Crystal structure of calpain reveals the structural basis for Ca+-dependent protease activity and a novel mode of enzyme activation, EMBO J. 18, 6880–6889.
Imbert, N., Vandebrouck, C., Constantin, B., Duport, G., Guillou, C., Cognard, C. and Raymond, G., 1996, Hypo-osmotic shocks induce elevation of resting calcium level in Duchenne muscular dystrophy myotubes contracting in vitro, Neuromuscul. Disord. 6, 351–360.
Ishiura, S., Murofushi, H., Suzuki, K. and Imahori, K., 1978, Studies of a calcium-activated neutral protease from chicken skeletal muscle. I. Purification and characterization, J. Biochem. 84, 225–230.
Jones, S.W., Parr, T., Sensky, P.L., Scothern, G.P., Bardsley, R.G. and Buttery, P.J., 1999, Fiber type-specific expression of p94, a skeletal muscle-specific calpain, J. Muscle Res. Cell Motil. 20, 417–424.
Kamei, M, Webb, G.C., Young, I.G. and Campbell, H.D., 1998, SOLH, a human homologue of the Drosophila melanogaster small optic lobes gene is a member of the calpain and zinc-finger gene families and maps to human chromosome 16pl3.3 near CATM (cataract with microphtalmia), Genomics 51, 197–206.
Kawai, H., Akaike, M., Kunishige, M., Inui, T, Adachi, K., Kimura, C., Kawajiri, M., Nishida, Y, Endo, I., Kashiwagi, S., Nishino, H., Fujiwara, T, Okuno, S., Roudaut, C., Richard, I., Beckmann, J.S., Miyoshi, K. and Matsumoto, T, 1998, Clinical, pathological, and genetic features of limb-girdle muscular dystrophy type 2A with new calpain 3 gene mutations in seven patients from three Japanese families, Muscle Nerve 21, 1493–1501.
Kawasaki, H., Nakayama, S. and Kretsinger, R.H., 1998, Classification and evolution of EF-hand proteins, Biometals 11, 277–295.
Kimura, Y, Koga, H., Araki, N., Mugita, N., Fujita, N., Takeshima, H., Nishi, T., Yamashima, T., Saido, T.C., Yamasaki, T., Moritake, K., Saya, H. and Nakao, M., 1998, The involvement of calpain-dependent proteolysis of the tumor suppressor NF2 (merlin) in schwannomas and meningiomas, Nat. Med. 4, 915–922.
Kinbara, K., Ishiura, S., Tomioka, S., Sorimachi, H, Jeong, S.Y., Amano, S., Kawasaki, H., Kolmerer, B., Kimura, S., Labeit, S. and Suzuki, K., 1998, Purification of native p94, a muscle-specific calpain, and characterization of its autolysis, Biochem. J 335, 589–596.
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.
Lin, G.D., Chattopadhyay, D., Maki, M., Wang, K.K.W., Carson, M., Jin, L., Yuen, P.W., Takano, E., Hatanaka, M., DeLucas, L.J. and Narayana, S.V., 1997, Crystal structure of calcium bound domain VI of calpain at 1.9A resolution and its role in enzyme assembly, regulation, and inhibitor binding, Nat. Struct. Biol. 4, 539–547.
Liu, L.A. and Enfvall, E., 1999, Sarcoglycan isoforms in skeletal muscle, J. Biol. Chem. 274, 38171–38176.
Ma, H., Fukiage, C., Azuma, M. and Shearer, T.R., 1997, Cloning and expression of mRNA for calpain Lp82 from rat lens: Spice variant of p94, Invest. Ophthalmol. Vis. Sci. 39, 454–461.
Menke, A. and Joskusch, H., 1991, Decreased osmotic stability of dystrophin-less muscle cells from the mdx mouse, Nature 349, 69–71.
McArdle, A., Maglara, A., Appleton, P., Watson, A.J., Grierson, I. and Jackson, M.J., 1999, Apoptosis in multinucleated skeletal muscle myotubes, Lab. Invest. 79, 1069–1076.
Minami, N., Nishino, I., Kobayashi, O., Ikezoe, K., Goto, Y. and Nonaka, I., 1999, Mutations of calpain 3 gene in patients with sporadic limb-girdle muscular dystrophy in Japan, J. Neurol. Sci. 171,31–37.
Moreira, E.S., Wiltshire, T.J., Faulkner, G., Nilforoushan, A., Vainzof, M., Suzuki, O.T., Valle, G., Reeves, R., Zatz, M., Passos-Bueno, M.R. and Jenne, D.E., 2000, Limb-girdle muscular dystrophy type 2G is caused by mutations in the gene encoding the sarcomeric protein telethonin, Nat. Genet. 24, 163–166.
Mugita, N., Kimura, Y., Ogawa, M., Saa, H. and Nakao, M., 1997, Identification of a novel, tissue-specific calpain htra-3: A human homologue of the Caenorhabditis elegans sex determination gene, Biochem. Biophys. Res. Commun. 239, 845–850.
Mukasa, T., Momoi, T. and Momoi, M.Y., 1999, Activation of caspase-3 apoptotic pathways in skeletal muscle fibers in laminin alpha2-deficient mice, Biochem. Biophys. Res. Commun. 260, 139–142.
Murachi, T., Tanaka, K., Hatanaka, M. and Murakami, T., 1981, Intracellular Ca2+-dependent protease (calpain) and its high-molecular-weight endogenous inhibitor (calpastatin), Adv. Enz.Reg. 19, 407–424.
Ohno, S., Emori, Y., Imajoh, S., Kawasaki, H., Kisaragi, M. and Suzuki, K., 1984, Evolutionary origin of a calcium-dependent protease by fusion of genes for a thiol protease and a calcium-binding protein?, Nature 312, 566–570.
Ono, Y., Sorimachi, H. and Suzuki, K., 1998a, Structure and physiology of calpain, an enigmatic protease, Biochem. Biophys. Res. Commun. 245, 289–294.
Ono, Y., Shimada, H., Sorimachi, H., Richard, I., Saido, T.C., Beckmann, J.S., Ishiura, S. and Suzuki, K., 1998b, 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.
Ozawa, E., Noguchi, S., Mizuno, Y, Hagiwara, Y and Yoshida, M., 1998, From dystrophino-pathy to sarcoglycanopathy: Evolution of a concept of muscular dystrophy, Muscle Nerve 21, 431–438.
Poussard, S., Duvert, M., Balcerzak, D., Ramassamy, S., Brustis, J.J., Cottin, P. and Ducastaing, A., 1996, Evidence for implication of muscle-specific calpain (p94) in myofibrillar integrity, Cell Growth Differ. 7, 1461–1469.
Rabbani, N., Moses, L., Anandavalli, T.E. and Anandaraj, M.P., 1984, Calcium-activated neutral protease from muscle and platelets of Duchenne muscular dystrophy cases, Clin. Chim. Acta 143, 163–168.
Richard, I., Broux, O., Allamand, V., Fougerousse, F., Chiannilkulchai, N., Bourg, N., Brenguier, L., Davaud, C., Pasturaud, P., Roudaut, C., Hillaire, D., Passos-Bueno, M.R., Zatz, M., Tischrield, J.A., Fardeu, M., Jackson, C.E., Cohen, D. and Beckmann, J.S., 1995, Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A, Cell 81, 27–10.
Richard, I., Roudaut, C., Saenz, A., Pogue, R., Grimbergen, J.E.M.A., Anderson, L.V.B., Beley, C., Cobo, A., de Diego, C., Eymard, B., Gallano, P., Ginjaar, H.B., Lasa, A., Pollitt, C., Topaloglu, H., Urtizverea, J.A., de Visser, M., van der Kooi, A., Bushby, K., Bakker, E., Lopez de Munain, A., Fardeau, M. and Beckmann, J.S., 1999, Calpainopathy — A survey of mutations and polymorphisms, Am. J. Hum. Genet. 64, 1524–1540.
Saido, T.C., Shibata, M., Takenawa, T., Murofushi, H. and Suzuki, K., 1992, Positive regulation of μ-calpain action by polyphosphoinositides, J. Biol. Chem. 267, 24585–24590.
Saido, T.C., Sorimachi, H. and Suzuki, K., 1994, Calpain: New perspective in molecular diversity and physiological-pathological involvement, FASEB J. 8, 814–822.
Sakihama, T., Kakidani, H., Zenita, K., Yumoto, N., Kikuchi, T., Sasaki, T., Kannagi, R., Nakanishi, S., Ohmori, M., Takio, K. and Murachi, T., 1985, A putative Ca2+-binding protein: Structure of the light subunit of porcine calpain elucidated by molecular cloning and protein sequence analysis, Proc. Natl. Acad. Sci. USA 82, 6075–6079.
Satoh, M., Takahashi, M., Sakamoto, T., Hiroe, M., Marumo, F. and Kimura, A., 1999, Structural analysis of the titin gene in hypertrophic cardiomyopathy: Identification of a novel disease gene, Biochem. Biophys. Res. Commun 262, 411–417.
Shevchenko, S., Feng, W., Varsanyi, M. and Shoshan-Barmatz, B., 1998, Identification, characterization and partial purification of a thiol-protease which cleaves specifically the skeletal muscle ryanodine receptor/Ca2+ release channel, J. Membrane Biol. 161, 33–43.
Sorimachi, H., Imajoh-Ohmi, S., Emori, Y., Kawasaki, H., Ohno, S., Minami, Y. and Suzuki, K., 1989, Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m-and M-types, J. Biol. Chem. 264, 20106–20111.
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.
Sorimachi, H., Kinbara, K., Kimura, S., Takahashi, M., Ishiura, S., Sasagawa, S., Sorimachi, N., Shimada, H., Tagawa, K., Maruyama, K. and Suzuki, K., 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.
Sorimachi, H., Ishiura, S. and Suzuki, K, 1997, Structure and physiological function of calpains, Biochem. J. 328, 721–732.
Sorimachi, H., Minami, N., Ono, Y, Suzuki, K. and Nonaka, I., 2000, Limb-girdle muscular dystrophy with calpain 3 (p94) gene mutations (calpainopathy), Neurosci. News 3, 20–27.
Spencer, M.J., Tidball, J.G., Anderson, L.V., Bushby, K.M., Harris, J.B., Passos-Bueno, M.R., Somer, H., Vainzof, M. and Zatz, M., 1997, Absence of calpain 3 in a form of limb-girdle muscular dystrophy (LGMD2A), J. Neurol. Sci. 146, 173–178.
Strobl, S., Fernandez-Catalan, C., Braun, M., Huber, R., Masumoto, H., Nakagawa, K., Irie, A., Sorimachi, H., Bourenkow, G., Bartunik, H., Suzuki, K. and Bode, W., 2000, The crystal structure of calcium-free human m-calpain suggests an electrostatic switch mechanism for activation by calcium, Proc. Natl. Acad. Sci. USA 97, 588–592.
Sugita, H., Ishiura, S., Suzuki, K. and Imahori, K., 1980, Ca2+-activated neutral protease and its inhibitors: In vitro effect on intact myofibrils, Muscle Nerve 3, 335–339.
Sugiyama, Y, Suzuki, A., Kishikawa, M., Akutsu, R., Hirose, T, Waye, M.M.Y, Tsui, S.K.W., Yoshida, S. and Ohno, S., 2000, Muscle develops a specific form of small heat shock protein complex composed of MKBP/HSPB2 and HSPB3 during myogenic differentiation, J. Biol. Chem. 275, 1095–1104.
Suzuki, K. and Sorimachi, H., 1998, A novel aspect of calpain activation, FEBS Lett. 433, 1–4.
Suzuki, K., Tsuji, S., Kubota, S., Kimura, Y. and Imahori, K, 1981, Limited autolysis of Ca2+-activated neutral protease (CANP) changes its sensitivity to Ca2+ ions, J. Biochem. 90, 275–278.
Takahashi-Nakamura, M., Tsuji, S., Suzuki, K. and Imahori, K, 1981, Purification and characterization of an inhibitor of calcium-activated neutral protease from rabbit skeletal muscle, J. Biochem. 90, 1538–1589.
Taverna, D., Disatnik, M.H., Rayburn, H., Branson, R.T., Yang, J., Rando, T.A. and Hynes, R.O., 1998, Dystrophic muscle in mice chimeric for expression of alpha5 integrin, J. Cell. Biol. 143, 849–859.
Thompson, T.G., Chan, Y.M., Hack, A.A., Brosius, M., Rajala, M., Lidov, H.G., McNally, E.M., Watkins, S. and Kunkel, L.M., 2000, Filamin 2 (FLN2). A muscle-specific sarcoglycan interacting protein, J. Cell. Biol. 148, 115–126.
Toniolo, D. and Minetti, C., 1999, Muscular dystrophies: Alterations in a limited number of cellular pathways?, Curr. Opin. Genet. Dev. 9, 275–282.
Tsujinaka, T., Fujita, J., Ebisui, C., Yano, M., Kominaimi, E., Suzuki, K., Tanaka, K., Katsume, A., Ohsugi, Y., Shiozaki, H. and Monden, M., 1996, Interleukin 6 receptor antibody inhibits muscle atrophy and modulates proteolytic systems in interleukin 6 transgenic mice, J. Clin. Invest. 97, 244–249.
Turner, P.R., Westwood, T., Regen, C.M. and Steinhardt, R.A., 1988, Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice, Nature 335, 735–738.
Turner, P.R., Schults, R., Ganguly, B. and Steinhardt, R.A., 1993, Proteolysis results in altered leak channel kinetics and elevated free calcium in mdx muscle, J. Membr. Biol. 133, 243–251.
Yoshida, K. and Harada, K., 1997, Proteolysis of erythrocyte-type and brain-type ankyrins in rat heart after postischemic reperfusion, J. Biochem. 133, 279–285.
Yoshizawa, T., Sorimachi, H., Tomioka, S., Ishiura, S. and Suzuki, K., 1995, A catalytic subunit of calpain possesses full proteolytic activity, FEBS Lett. 358, 101–103.
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Ono, Y., Hata, S., Sorimachi, H., Suzuki, K. (2000). Calcium and Muscle Disease: Pathophysiology of Calpains and Limb-Girdle Muscular Dystrophy Type 2A (LGMD2A). In: Pochet, R., Donato, R., Haiech, J., Heizmann, C., Gerke, V. (eds) Calcium: The Molecular Basis of Calcium Action in Biology and Medicine. Springer, Dordrecht. https://doi.org/10.1007/978-94-010-0688-0_26
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