Calpain 3 Is Activated through Autolysis within the Active Site and Lyses Sarcomeric and Sarcolemmal Components

Molecular and Cellular Biology

Volumn 23, Issue 24, 2003, Pages 9127-9135

  Taveau, Mathieu ^a   Bourg, Nathalie ^a   Sillon, Guillaume ^a   Roudaut, Carinne ^a   Bartoli, Marc ^a   Richard, Isabelle ^a  

^a GÉNÉTHON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN 3; CONNECTIN; CYSTEINE PROTEINASE; FILAMIN;

ANIMAL CELL; ARTICLE; AUTOLYSIS; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME SUBSTRATE; FOCAL ADHESION; GENE MUTATION; LIMB GIRDLE MUSCULAR DYSTROPHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SARCOLEMMA; SARCOMERE; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0344629442     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.24.9127-9135.2003     Document Type: Article

References (38)

1. Andreoli, C., M. Martin, R. Le Borgne, H. Reggio, and P. Mangeat. 1994. Ezrin has properties to self-associate at the plasma membrane. J. Cell Sci. 107:2509-2521.
2. Baghdiguian, S., M. Martin, I. Richard, F. Pons, C. Astier, N. Bourg, R. T. Hay, R. Chemaly, G. Halaby, J. Loiselet, L. V. Anderson, A. Lopez de Munain, M. Fardeau, P. Mangeat, J. S. Beckmann, and G. Lefranc. 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. Nat. Med. 5:503-511.
3. Belkin, A. M., N. I. Zhidkova, F. Balzac, F. Altruda, D. Tomatis, A. Maier, G. Tarone, V. E. Koteliansky, and K. Burridge. 1996. Beta 1D integrin displaces the beta 1A isoform in striated muscles: localization at junctional structures and signaling potential in nonmuscle cells. J. Cell Biol. 132:211-226.
4. Bialkowska, K., S. Kulkarni, X. Du, D. E. Goll, T. C. Saldo, and J. E. Fox. 2000. Evidence that beta3 integrin-induced Rac activation involves the calpain-dependent formation of integrin clusters that are distinct from the focal complexes and focal adhesions that form as Rac and RhoA become active. J. Cell Biol. 151:685-696.
5. Calderwood, D. A., R. Zent, R. Grant, D. J. Rees, R. O. Hynes, and M. H. Ginsberg. 1999. The talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation. J. Biol. Chem. 274:28071-28074.
6. Carragher, N. O., M. A. Westhoff, D. Riley, D. A. Potter, P. Dutt, J. S. Elce, P. A. Greer, and M. C. Frame. 2002. v-Src-induced modulation of the calpain-calpastatin proteolytic system regulates transformation. Mol. Cell. Biol. 22:257-269.
7. Fardeau, M., D. Hillaire, C. Mignard, N. Feingold, D. Mignard, B. de Ubeda, H. Collin, F. M. S. Tom6, I. Richard, and J. S. Beckmann. 1996. Juvenile limb-girdle muscular dystrophy: clinical, histopathological, and genetic data from a small community living in the Reunion Island. Brain 119:295-308.
8. Fougerousse, F., P. Gonin, M. Durand, I. Richard, and J. M. Raymackers. 2003. Force impairment in calpain 3-deficient mice is not correlated with mechanical disruption. Muscle Nerve 27:616-623.
9. Fox, J. E. 2001. Cytoskeletal proteins and platelet signaling. Thromb. Hemost. 86:198-213.
10. Frame, M. C., V. J. Fincham, N. O. Carragher, and J. A. Wyke. 2002. v-Src's hold over actin and cell adhesions. Nat. Rev. Mol. Cell. Biol. 3:233-245.
11. Glading, A., D. A. Lauffenburger, and A. Wells. 2002. Cutting to the chase: calpain proteases in cell motility. Trends Cell Biol. 12:46-54.
12. Herasse, M., Y. Ono, F. Fougerousse, E. Kimura, D. Stockholm, C. Beley, D. Montarras, C. Pinset, H. Sorimachi, K. Suzuki, J. S. Beckmann, and I. Richard. 1999. Expression and functional characteristics of calpain 3 isoforms generated through tissue-specific transcriptional and posttranscriptional events. Mol. Cell. Biol. 19:4047-4055.
13. Horwitz, A., K. Duggan, C. Buck, M. C. Beckerle, and K. Burridge. 1986. Interaction of plasma membrane fibronectin receptor with talin-a transmembrane linkage. Nature 320:531-533.
14. Kinbara, K., S. Ishiura, S. Tomioka, H. Sorimachi, S. Y. Jeong, S. Amano, H. Kawasaki, B. Kolmerer, S. Kimura, S. Labeit, and K. Suzuki. 1998. Purification of native p94, a muscle-specific calpain, and characterization of its autolysis. Biochem. J. 335:589-596.
15. Kinbara, K., H. Sorimachi, S. Ishiura, and K. Suzuki. 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.
16. Kioka, N., S. Sakata, T. Kawauchi, T. Amachi, S. K. Akiyama, K. Okazaki, C. Yaen, K. M. Yamada, and S. Aota. 1999. Vinexin: a novel vinculin-binding protein with multiple SH3 domains enhances actin cytoskeletal organization. J. Cell Biol. 144:59-69.
17. Kumar, A., and A. M. Boriek. 2003. Mechanical stress activates the nuclear factor-kappaB pathway in skeletal muscle fibers: a possible role in Duchenne muscular dystrophy. FASEB J. 17:386-396.
18. Kumar, S., and P. A. Colussi. 1999. Prodomains-adaptors-oligomerization: the pursuit of caspase activation in apoptosis. Trends Biochem. Sci. 24:1-4.
19. Lagord, C., L. Soulet, S. Bonavaud, Y. Bassaglia, C. Rey, G. Barlovatz-Meimon, J. Gautron, and I. Martelly. 1998. Differential myogenicity of satellite cells isolated from extensor digitorum longus (EDL) and soleus rat muscles revealed in vitro. Cell Tissue Res. 291:455-468.
20. Moldoveanu, T., C. M. Hosfield, D. Lim, J. S. Elce, Z. Jia, and P. L. Davies. 2002. A Ca(2+) switch aligns the active site of calpain. Cell 108:649-660.
21. Ono, Y., H. Shimada, H. Sorimachi, I. Richard, T. C. Saido, J. S. Beckmann, S. Ishiura, and K. Suzuki. 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.
22. Parast, M. M., and C. A. Otey. 2000. Characterization of palladin, a novel protein localized to stress fibers and cell adhesions. J. Cell Biol. 150:643-656.
23. Richard, I., O. Broux, V. Allamand, F. Fougerousse, N. Chiannilkulchai, N. Bourg, L. Brenguier, C. Devaud, P. Pasturaud, C. Roudaut, D. Hillaire, M.-R. Passos-Bueno, M. Zatz, J. A. Tischfield, M. Fardeau, C. E. Jackson, D. Cohen, and J. S. Beckmann. 1995. Mutations in the proteolytic enzyme, calpain 3, cause limb-girdle muscular dystrophy type 2A. Cell 81:27-40.
24. Riedl, S. J., P. Fuentes-Prior, M. Renatus, N. Kairies, S. Krapp, R. Huber, G. S. Salvesen, and W. Bode. 2001. Structural basis for the activation of human procaspase-7. Proc. Natl. Acad. Sci. USA 98:14790-14795.
25. Schaffner, W., and C. Weissmann. 1973. A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal. Biochem. 56:502-514.
26. Shi, Y. 2002. Mechanisms of caspase activation and inhibition during apoptosis. Mol. Cell 9:459-470.
27. Shiraha, H., A. Glading, K. Gupta, and A. Wells. 1999. IP-10 inhibits epidermal growth factor-induced motility by decreasing epidermal growth factor receptor-mediated calpain activity. J. Cell Biol. 146:243-254.
28. Sorimachi, H., S. Imajoh-Ohmi, Y. Emori, H. Kawasaki, S. Ohno, Y. Minami, and K. Suzuki. 1989. Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m and mu type. Specific expression of the mRNA in skeletal muscle. J. Biol. Chem. 264:20106-20111.
29. Sorimachi, H., S. Ishiura, and K. Suzuki. 1997. Structure and physiological function of calpains. Biochem. J. 328:721-732.
30. Sorimachi, H., K. Kimbara, S. Kimura, M. Takahashi, S. Ishiura, N. Sasagawa, N. Sorimachi, H. Shimada, K. Tagawa, K. Maruyama, and K. Suzuki. 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.
31. Sorimachi, H., S. Kimura, K. Kinbara, J. Kazama, M. Takahashi, H. Yajima, S. Ishiura, N. Sasagawa, I. Nonaka, H. Sugita, K. Maruyama, and K. Suzuki. 1996. Structure and physiological functions of ubiquitous and tissue-specific calpain species. Muscle-specific calpain, p94, interacts with connectin/titin. Adv. Biophys. 33:101-122.
32. Sorimachi, H., and K. Suzuki. 2001. The structure of calpain. J. Biochem. (Tokyo) 129:653-664.
33. Sorimachi, H., N. Toyama-Sorimachi, T. C. Saido, H. Kawasaki, H. Sugita, M. Miyasaka, K. Arahata, S. Ishiura, and K. Suzuki. 1993. Muscle-specific calpain, p94, is degraded by autolysis immediately after translation, resulting in disappearance from muscle. J. Biol. Chem. 268:10593-10605.
34. Spencer, M. J., J. R. Guyon, H. Sorimachi, A. Potts, I. Richard, M. Herasse, J. Chamberlain, I. Dalkilic, L. M. Kunkel, and J. S. Beckmann. 2002. 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 99:8874-8879.
35. Suwa, A., M. Mitsushima, T. Ito, M. Akamatsu, K. Ueda, T. Amachi, and N. Kioka. 2002. Vinexin beta regulates the anchorage dependence of ERK2 activation stimulated by epidermal growth factor. J. Biol. Chem. 277:13053-13058.
36. Thompson, T. G., Y. M. Chan, A. A. Hack, M. Brosius, M. Rajala, H. G. Lidov, E. M. McNally, S. Watkins, and L. Kunkel. 2000. Filamin 2 (FLN2): a muscle-specific sarcoglycan interacting protein. J. Cell Biol. 148:115-126.
37. Wang, K. K. 2000. Calpain and caspase: can you tell the difference? Trends Neurosci. 23:20-26.
38. Yan, B., D. A. Calderwood, B. Yaspan, and M. H. Ginsberg. 2001. Calpain cleavage promotes talin binding to the beta 3 integrin cytoplasmic domain. J. Biol. Chem. 276:28164-28170.