Identification, characterization and partial purification of a thiol-protease which cleaves specifically the skeletal muscle ryanodine receptor/Ca2+ release channel

Journal of Membrane Biology

Volumn 161, Issue 1, 1998, Pages 33-43

  Shevchenko, S ^a   Feng, W ^a   Varsanyi, M ^b   Shoshan Barmatz, V ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Calpains; p94; Ryanodine receptor; SR

Indexed keywords

CALPAIN; PROTEINASE; RYANODINE RECEPTOR;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PURIFICATION; LIPID BILAYER; MEMBRANE CONDUCTANCE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; RABBIT; SARCOPLASMIC RETICULUM; SKELETAL MUSCLE;

ANIMALS; BRAIN; CALPAIN; CHROMATOGRAPHY, AFFINITY; EGTAZIC ACID; LIPID BILAYERS; MEMBRANE POTENTIALS; MUSCLE FIBERS, FAST-TWITCH; MUSCLE, SKELETAL; MYOCARDIUM; RABBITS; RYANODINE; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM; SUBSTRATE SPECIFICITY;

ANIMALIA; ORYCTOLAGUS CUNICULUS;

EID: 0031974005     PISSN: 00222631     EISSN: None     Source Type: Journal    
DOI: 10.1007/s002329900312     Document Type: Article

References (55)

1. 2+ levels in myotubes grown from the skeletal muscle of dystrophic (mdx) and normal mice. J. Physiol. 460:1-13
2. Brandt, N.R., Caswell, A.H., Brandt, T., Brew, K., Mellgren, R.L. 1992. Mapping of the calpain proteolysis products of the junctional foot protein of the skeletal muscle triad junction. J. Membrane Biol. 127:35-47
3. 2+ transport properties. J. Biol. Chem. 258:6602-6609
4. Coronado, R., Morrissette, J., Sukhareva, M., Vaughan, D.M. 1994. Structure and function of ryanodine receptors. Am. J. Phys. 266:C1485-C1504
5. Croall, D.E. 1989. Proteolytic modification of calcium-dependent protease in erythrocytes treated with ionomycin and calcium. Biochemistry 28:6882-6888
6. Dayton, W.R., Schollmeyer, J.V., Lepley, R.A., Cortes, L.R. 1981. A calcium-activated protease possibly involved in myofibrillar protein turnover. Biochim. Biophys. Acta 659:48-61
7. De Martino, G.N., Huff, C.A., Croall, D.E. 1986. Autoproteolysis of the small subunit of calcium-dependent protease II activates and regulates protease activity. J. Biol. Chem. 261:12047-12052
8. Fleischer, S., Inui, M. 1989. Biochemistry and biophysics of excitation-contraction coupling. Ann. Rev. Biophys. Biophys. Chem. 18:333-364
9. Franco, A.J. and Lansman, J.B. 1990. Calcium entry through stretch-inactivated ion channels in mdx myotubes. Nature 344: 670-673
10. Gilchrist, J.S.C., Wang, K.K.W., Katz, S., Belcastro, A.N. 1992. Calcium-activated neutral protease effects upon skeletal muscle sarcoplasmic reticulum protein structure and calcium release. J. Biol. Chem. 267:20857-20865
11. Gopalakrishan, R., Barsky, S.H. 1986. Hydrophobic association of calpains with subcellular organs compartmentalization of calpains and the endogenous inhibitor calpastalin in tissues. J. Biol. Chem. 261:13936-13942
12. Guroff, G. 1964. A neutral, calcium-activated protease from soluble fraction of rat brain. J. Biol. Chem. 239:149-155
13. Ilian, M.N., Forsberg, N.E. 1992. Gene expression of calpains and their specific endogenous inhibitor, calpastatin, in skeletal muscle of fed and fasted rabbits. Biochem. J. 287:163-171
14. 2-terminal processing of the large subunit. J. Biochem. 100:633-642
15. Inomata, M., Hayashi, M., Nakamura, M., Imahori, K., Kawashima, S. 1983. Purification and characterization of a calcium-activated neutral protease from rabbit skeletal muscle which requires calcium ions of μM order of concentration. J. Biochem. 93:291-294
16. Kaplan, R.S., Pedersen, F.L. 1985. Determination of microgram quantities of protein in the presence of milligrams level of lipid with amido black 10B. Anal. Biochem. 150:94-104
17. 2+-activated proteases, protein degradation and muscular dystrophy in: Proteases: potential role in health and disease (W.H. Hörl and A. Heidland editors.) pp. 519-532. Plenum, New York
18. 4. Nature 227:680-685
19. 2+ channel activity. Bioenerg. Biomembr. 21:227-245
20. Lai, F.A., Erickson, H.P., Rousseau, F., Liu, Q.Y., Meissner, G. 1988. Purification and reconstitution of the calcium release channel from skeletal muscle. Nature 331:315-319
21. Lowry, O.H., Rosenbrough, N.J., Farr, A.L., Randall, R.J. 1941. Protein measurements with folin phenol reagent. J. Biol. Chem. 193:265-275
22. MacLennan, D.H. 1970. Purification and properties of an adenosine triphosphatase from sarcoplasmic reticulum. J. Biol. Chem. 245:4508-4518
23. Mellgren, R.L. 1980. Canine cardiac calcium-dependent proteases: Resolution of two forms with different requirements for calcium. FEBS Lett. 109:129-133
24. Mellgren, R.L. 1987. Calcium-dependent protease: an enzyme system active at cellular membranes. FASEB J. 1:110-115
25. Mellgren, R.L., Lane, R.D., Kakar, S.S. 1987. Isolated bovine myocardial sarcolemma and sarcoplasmic reticulum vesicles contain tightly bound calcium dependent protease inhibitor. Biochem. Biophys. Res. Commun. 142:1025-1031
26. Merril, C.R., Goldman, D., Van Keuren, M.L. 1983. Silver staining methods for polyacrylamid gel electrophoresis. Meth. Enzymol. 96:230-239
27. 2+ at rest and after cholinergic stimulus is increased in cultured muscle cells from Dunchenne muscular dystrophy patients. Neurology 38:476-480
28. Morrissette, J., Beurg, M., Sukhareva, M., Coronado, R. 1996. Purification and characterization of ryanotoxin. a peptide with actions similar to those of ryanodine. Biophysiol. J. 71:707-721
29. Murachi, T. 1989. Intracellular regulatory system involving calpain and calpastatin. Biochem. Int. 18:263-294
30. 2+-dependent protease [calpain] and its high-molecular weight endogenous inhibitor [calpastatin]. Adv. Enzyme Regul. 19:407-424
31. 2+ release channel of sarcoplasmic reticulum. J. Biol. Chem. 268:1376-1382
32. Penefsky, H.S. 1977. Reversible binding of Pi by beef heart mitochondrial. J. Biol. Chem. 252:2891-2899
33. Puca, G.A., Nola, E., Sica, V., Bresciani, F. 1977. Estragon binding proteins of calf uterus: molecular and functional characterization of the receptor transforming factor: A calcium-activated protease. J. Biol. Chem. 252:1358-1370
34. 2+ release channel. Circ. Res. 67:84-96
35. 2+ activated neural proteinase. Biochem. J. 209:635-641
36. Richard, L. Broux, O., Allamand, V., Fougerousse, F., Chiannikulchai, N., Bourg, N., Brengular, L., Devaud, C. et al. 1994. Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell 81:27-40
37. Rogers, S., Wells, R., Rechsteiner, M. 1986. Amino acid sequences common to rapidly degraded proteins: The PEST hypothesis. Science 234:364-368
38. Saido, C.T., Sorimachi, H., Suzuki, K. 1994. Calpain: New perspectives in molecular diversity and physiological-pathological involvement FASEB J. 8:814-822
39. Saito, A., Seiler, S., Chu, A., Fleischer, S. 1984. Preparation and morphology of sarcoplasmic reticulum terminal cisternae from rabbit skeletal muscle. J. Cell Biol. 99:875-885
40. 2+-activated protease. J. Biol. Chem. 259:8550-8557
41. Shoshan-Barmatz, V., Zarka, A. 1992. A simple, fast, one-step method for purification of the skeletal muscle ryanodine receptor. Biochem. J. 285:61-64
42. 2+ release channel in skeletal muscle. J. Membrane Biol. 142:281-288
43. Sorimachi, H., Imajoh-Ohmi, S., Emori, Y., Kawasaki, H., Ohno, S., Minami, Y., Suzuki, K. 1989. Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m- and μ-types. J. Biol. Chem. 264:20106-20111
44. 2+-binding domain. J. Biol. Chem. 268:19476-19482
45. Sorimachi, H., Kinbara, K., Kimura, S., Takahashi, M., Ishiura, S., Sasagawa, N., Sorimachi, N., Shimada, H., Tagawa, K., Maruyama, K., Suzuki, K. 1995. Muscle-specific calpain. p94, responsible for limb girdle muscular dystrophy type 2A. association with connectin through IS2, a p94-specific sequence. J. Biol. Chem. 270:31158-31162
46. Sorimachi, H., Saido, T.C., Suzuku, K. 1994. New era of calpain research, Discovery of tissue-specific calpains. FEBS Lett. 343:1-5
47. Sorimachi, H., Toyama-Sorimachi, N., Saido, T.C., Kawasaki, H., Sugita, H., Miyasaka, M., Arahata, K., Ishiura, S., 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
48. Sorimachi, H., Tsukahara, T., Okada-Ben, M., Sugita, H., Ishiura, S., Suzuki, K. 1995. Identification of a third ubiquitous calpain species-chicken muscle expresses four distinct calpains. Biochem. Biophys. Acta 1262:381-393
49. Spencer, M.J., Croall, D.E., Tidball, J.G. 1994. Calpains are activated in narcotic fibers from mdx dystrophic mice. J. Biol. Chem. 270:10909-10914
50. Suzuki, K. 1987. Calcium activated neutral protease: domain structure and activity regulation. Trends Biochem. Sci. 12:103-105
51. Tamkun, M.M., Catterall, W.A. 1981. Ion flux studies of voltage-sensitive sodium channel in synaptic nerve-ending particles. Molec. Pharmacol. 19:78-86
52. Tompa, P., Baki, A., Schad, E., Friedrich, P. 1996. The calpain cascade: μ calpain activates m calpain. J. Biol. Chem. 271:33161-33164
53. Wang, K.K.W., Villalobo, A., Roufogalis, B.D. 1989. Calmodulin-binding proteins as calpain substrates. Biochem. J. 262:693-706
54. Xu, L., Jones, R., Meissner, G. 1993. Effects of local anesthetics on single channel behavior of skeletal muscle calcium channel. J. Gen. Physiol. 101:207-233
55. 2+ release channel conformations as reflected in the different effects of propranolol on its ryanodine binding and channel activity. Biochem. J. 315:377-383