Caspases cleave the amino-terminal calpain inhibitory unit of calpastatin during apoptosis in human Jurkat T cells

Journal of Biochemistry

Volumn 127, Issue 2, 2000, Pages 297-305

  Kato, Masahiko ^a   Nonaka, Takashi ^a   Maki, Masatoshi ^b   Kikuchi, Hidehiko ^a,c   Imajoh Ohmi, Shinobu ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c UNIVERSITY OF MIYAZAKI   (Japan)

Author keywords

Apoptosis; Calpain; Calpastatin; Caspase; Jurkat T cell

Indexed keywords

CALPAIN; CALPASTATIN; CASPASE; CASPASE 3; CASPASE 7; ENZYME PRECURSOR;

AMINO TERMINAL SEQUENCE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME DEGRADATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; PROTEIN DEGRADATION; T LYMPHOCYTE;

EID: 0034011860     PISSN: 0021924X     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.jbchem.a022607     Document Type: Article

References (69)

1. Cohen, G.M. (1997) Caspases: the executioners of apoptosis. Biochem. J. 326, 1-16
2. Miller, D.K. (1997) The role of the Caspase family of cysteine protcases in apoptosis. Semin. Immunol. 9, 35-49
3. Porter, A.G. and Janicke, R.U. (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 6, 99-104
4. Orlowski, R.Z. (1999) The role of the ubiquitin-proteasome pathway in apoptosis. Cell Death Differ. 6, 303-313
5. Squier, M.K., Miller, A.C., Malkinson, A.M., and Cohen, J.J. (1994) Calpain activation in apoptosis. J. Cell Physiol. 159, 229-237
6. Kikuchi, H. and Imajoh-Ohmi, S. (1995) Activation and possible involvement of calpain, a calcium-activated cysteine protease, in down-regulation of apoptosis of human monoblast U937 cells. Cell Death Differ. 2, 195-199
7. Knepper-Nicolai, B., Savill, J., and Brown, S.B. (1998) Constitutive apoptosis in human neutrophils requires synergy between calpains and the proteasome downstream of caspases. J. Biol. Chem. 273, 30530-30536
8. Waterhouse, N.J., Finucane, D.M., Green, D.R., Elce, J.S., Kumar, S., Alnemri, E.S., Litwack, G., Khanna, K., Lavin, M.F., and Watters, D.J. (1998) Calpain activation is upstream of caspases in radiation-induced apoptosis. Cell Death Differ. 5, 1051-1061
9. Debiasi, R.L., Squier, M.K., Pike, B., Wynes, M., Dermody, T.S., Cohen, J.J., and Tyler, K.L. (1999) Reovirus-induced apoptosis is preceded by increased cellular calpain activity and is blocked by calpain inhibitors. J. Virol. 73, 695-701
10. Carafoli, E. and Molinari, M. (1998) Calpain: a protease in search of a function?. Biochem. Biophys. Res. Commun. 247, 193-203
11. Moallem, S.A. and Hales, B.F. (1995) Induction of apoptosis and cathepsin D in limbs exposed in vitro to an activated analog of cyclophosphamide. Teratology 52, 3-14
12. Roberts, L.R., Kurosawa, H., Bronk, S.F., Fesmier, P.J., Agellon, L.B., Leung, W.Y., Mao, F., and Gores, G.J. (1997) Cathepsin B contributes to bile salt-induced apoptosis of rat hepatocytes. Gastroenterology 113, 1714-1726
13. Alnemri, E.S., Livingston, D.J., Nicholson, D.W., Salvesen, G., Thornberry, N.A., Wong, W.W., and Yuan, J. (1996) Human ICE/ CED-3 protease nomenclature. Cell 87, 171
14. Van de Craen, M., Van Loo, G., Pype, S., Van Criekinge, W., Van den brande, I., Molemans, F., Fiers, W., Declercq, W., and Vandenabeele, P. (1998) Identification of a new caspase homologue: caspase-14. Cell Death Differ. 5, 838-846
15. Ahmad, M., Srinivasula, S.M., Hegde, R., Mukattash, R., Fernandes-Alnemri, T., and Alnemri, E.S. (1998) Identification and characterization of murine caspase-14, a new member of the caspase family. Cancer Res. 58, 5201-5205
16. Hu, S., Snipas, S.J., Vincenz, C., Salvesen, G., and Dixit, V.M. (1998) Caspase-14 is a novel developmentally regulated protease. J. Biol. Chem. 273, 29648-29653
17. Lazebnik, Y.A., Kaufmann, S.H., Desnoyers, S., Poirier, G.G., and Earnshaw, W.C. (1994) Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371, 346-347
18. Cryns, V.L., Bergeron, L., Zhu, H., Li, H., and Yuan, J. (1996) Specific cleavage of α-fodrin during Fas-and tumor necrosis factor-induced apoptosis is mediated by an interleukin-1β-converting enzyme/Ced-3 protease distinct from the poly (ADP-ribose) polymerase protease. J. Biol. Chem. 271, 31277-31282
19. Janicke, R.U., Ng, P., Sprengart, M.L., and Porter, A.G. (1998) Caspase-3 is required for α-fodrin cleavage but dispensable for cleavage of other death substrates in apoptosis. J. Biol. Chem. 273, 15540-15545
20. Emoto, Y., Manome, Y., Meinhardt, G., Kisaki, H., Kharbanda, S., Robertson, M., Ghayur, T., Wong, W.W., Kamen, R., and Weichselbaum, R. (1995) Proteolytic activation of protein kinase C δ by an ICE-like protease in apoptotic cells. EMBO J. 14, 6148-6156
21. Cheng, E.H., Kirsch, D.G., Clem, R.J., Ravi, R., Kastan, M.B., Bedi, A., Ueno, K., and Hardwick, J.M. (1997) Conversion of Bcl-2 to a Bax-like death effector by caspases. Science 278, 1966-1968
22. Kirsch, D.G., Doseff, A., Chau, B.N., Lim, D.S., de Souza-Pinto, N.C., Hansford, R., Kastan, M.B., Lazebnik, Y.A., and Hardwick, J.M. (1999) Caspase-3-dependent cleavage of bcl-2 promotes release of cytochrome c. J. Biol. Chem. 274, 21155-21161
23. Brancolini, C., Lazarevic, D., Rodriguez, J., and Schneider, C. (1997) Dismantling cell-cell contacts during apoptosis is coupled to a caspase-dependent proteolytic cleavage of β-catenin. J. Cell Biol. 139, 759-771
24. Enari, M., Sakahira, H., Yokoyama, H., Okawa, K., Iwamatsu, A., and Nagata, S. (1998) A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391, 43-50
25. Barkett, M., Xue, D., Horvitz, H.R., and Gilmore, T.D. (1997) Phosphorylation of IxB-α inhibits its cleavage by caspase CPP32 in vitro. J. Biol. Chem. 272, 29419-29422
26. Liu, X., Zou, H., Slaughter, C., and Wang, X. (1997) DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89, 175-184
27. Tang, D. and Kidd, V.J. (1998) Cleavage of DFF-45/ICAD by multiple caspases is essential for its function during apoptosis. J. Biol. Chem. 273, 28549-28552
28. Reuther, J.Y., and Baldwin, A.S., Jr. (1999) Apoptosis promotes a caspase-induced amino-terminal truncation of IκBα that functions as a stable inhibitor of NF-κB. J. Biol. Chem. 274, 20664-20670
29. Chandler, J.M., Cohen, G.M., and MacFarlane, M. (1998) Different subcellular distribution of caspase-3 and caspase-7 following Fas-induced apoptosis in mouse liver. J. Biol. Chem. 273, 10815-10818
30. Kikuchi, H. and Imajoh-Ohmi, S. (1995) Antibodies specific for proteolyzed forms of protein kinase C α. Biochim. Biophys. Acta 1269, 253-259
31. Suzuki, K. and Sorimachi, H. (1998) A novel aspect of calpain activation. FEBS Lett. 433, 1-4
32. Murachi, T. (1989) Intracellular regulatory system involving calpain and calpastatin. Biochem. Int. 18, 263-294
33. Wang, K.K., Posmantur, R., Nadimpalli, R., Nath, R., Mohan, P., Nixon, R.A., Talanian, R.V., Keegan, M., Herzog, L., and Allen, H. (1998) Caspase-mediated fragmentation of calpain inhibitor protein calpastatin during apoptosis. Arch. Biochem. Biophys. 356, 187-196
34. Omura, S., Fujimoto, T., Otoguro, K., Matsuzaki, K., Moriguchi, R., Tanaka, H., and Sasaki, Y. (1991) Lactacystin, a novel microbial metabolite, induces neuritogenesis of neuroblastoma cells. J. Antibiot. 44, 113-116
35. Tsujinaka, T., Kajiwara, Y, Kambayashi, J., Sakon, M., Higuchi, N., Tanaka, T., and Mon, T. (1988) Synthesis of a new cell penetrating calpain inhibitor (calpeptin). Biochem. Biophys. Res. Commun. 153, 1201-1208
36. Imajoh-Ohmi, S., Kawaguchi, T., Sugiyama, S., Tanaka, K., Omura, S., and Kikuchi, H. (1995) Lactacystin, a specific inhibitor of the proteasome, induces apoptosis in human monoblast U937 cells. Biochem. Biophys. Res. Commun. 217, 1070-1077
37. Kikuchi, H., Fujinawa, T., Kuribayashi, F., Nakanishi, A., Imajoh-Ohmi, S., Goto, M., and Kanegasaki, S. (1994) Induction of essential components of the Superoxide generating system in human monoblastic leukemia U937 cells. J. Biochem. 116, 742-746
38. Hitomi, K., Yokoyama, A., and Maki, M. (1998) Expression of biologically active human calpastatin in baculovirus-infected insect cells and in Escherichia coli. Biosci. Biotechnol. Biochem. 62, 136-41
39. Harvey, K.F., Harvey, N.L., Michael, J.M., Parasivam, G., Waterhouse, N., Alnemri, E.S., Watters, D., and Kumar, S. (1998) Caspase-mediated cleavage of the ubiquitin-protein ligase Nedd4 during apoptosis. J. Biol. Chem. 273, 13524-13530
40. 2-terminal processing of the large subunit. J. Biochem. 100, 633-642
41. Wong, G.H. and Goeddel, D.V. (1994) Fas antigen and p55 TNF receptor signal apoptosis through distinct pathways. J. Immunol. 152, 1751-1755
42. Ravi, R., Bedi, A., and Fuchs, E.J. (1998) CD95 (Fast)-induced caspase-mediated proteolysis of NF-κB. Cancer Res. 58, 882-886
43. Sarin, A., Nakajima, H., and Henkart, P.A. (1995) A protease-dependent TCR-induced death pathway in mature lymphocytes. J. Immunol. 154, 5806-5812
44. Wood, D.E., Thomas, A., Devi, L.A., Berman, Y., Beavis, R.C., Reed, J.C., and Newcomb, E.W. (1998) Bax cleavage is mediated by calpain during drug-induced apoptosis. Oncogene 17, 1069-1078
45. Rovere, P., Clementi, E., Ferrarini, M., Heltai, S., Sciorati, C., Sabbadini, M.G., Rugarli, C., and Manfredi, A.A. (1996) CD95 engagement releases calcium from intracellular stores of long term activated, apoptosis-prone γδ T cells. J. Immunol. 156, 4631-4637
46. Nicotera, P. and Orrenius, S. (1998) The role of calcium in apoptosis. Cell Calcium 23, 173-180
47. Talanian, R.V., Quinlan, C., Trautz, S., Hackett, M.C., Mankovich, J.A., Banach, D., Ghayur, T., Brady, K.D., and Wong, W.W. (1997) Substrate specificities of caspase family proteases. J. Biol. Chem. 272, 9677-9682
48. Asada, K., Ishino, Y, Shimada, M., Shimojo, T., Endo, M., Kimizuka, F., Kato, I., Maki, M., Hatanaka, M., and Murachi, T. (1989) cDNA cloning of human calpastatin: sequence homology among human, pig, and rabbit calpastatins. J. Enzyme Inhib. 3, 49-56
49. Takano, E., Maki, M., Mori, H., Hatanaka, M., Marti, T., Titani, K., Kannagi, R., Ooi, T., and Murachi, T. (1988) Pig heart calpastatin: identification of repetitive domain structures and anomalous behavior in polyacrylamide gel electrophoresis. Biochemistry 27, 1964-1972
50. Cong, M., Thompson, V.F., Goll, D.E., and Antin, P.B. (1998) The bovine calpastatin gene promoter and a new N-terminal region of the protein are targets for cAMP-dependent protein kinase activity. J. Biol. Chem. 273, 660-666
51. Emori, Y., Kawasaki, H., Imajoh, S., Imahori, K., and Suzuki, K. (1987) Endogenous inhibitor for calcium-dependent cysteine protease contains four internal repeats that could be responsible for its multiple reactive sites. Proc. Natl. Acad. Sci. USA 84, 3590-3594
52. Lee, W.J., Hatanaka, M., and Maki, M. (1992) Multiple forms of rat calpastatin cDNA in the coding region of functionally unknown amino-terminal domain. Biochim. Biophys. Acta 1129, 251-253
53. Takano, J., Kawamura, T., Murase, M., Hitomi, K., and Maki, M. (1999) Structure of mouse calpastatin isoforms: implications of species-common and species-specific alternative splicing. Biochem. Biophys. Res. Commun. 260, 339-345
54. Imajoh, S., Kawasaki, H., Emori, Y, and Suzuki, K. (1987) Calcium-activated neutral protease inhibitor from rabbit erythrocytes lacks the N-terminal region of the liver inhibitor but retains three inhibitory units. Biochem. Biophys. Res. Commun. 146, 630-637
55. Maki, M., Takano, E., Mori, H., Sato, A., Murachi, T., and Hatanaka, M. (1987) All four internally repetitive domains of pig calpastatin possess inhibitory activities against calpains I and II. FEBS Lett. 223, 174-180
56. Maki, M., Takano, E., Mori, H., Kannagi, R., Murachi, T., and Hatanaka, M. (1987) Repetitive region of calpastatin is a functional unit of the proteinase inhibitor. Biochem. Biophys. Res. Commun. 143, 300-308
57. Emori, Y., Kawasaki, H., Imajoh, S., Minami, Y., and Suzuki, K. (1988) All four repeating domains of the endogenous inhibitor for calcium-dependent protease independently retain inhibitory activity. Expression of the cDNA fragments in Escherichia coli. J. Biol. Chem. 263, 2364-2370
58. Maki, M., Takano, E., Osawa, T., Ooi, T., Murachi, T., and Hatanaka, M. (1988) Analysis of structure-function relationship of pig calpastatin by expression of mutated cDNAs in Escherichia coli. J. Biol. Chem. 263, 10254-10261
59. Maki, M., Bagci, H., Hamaguchi, K, Ueda, M., Murachi, T., and Hatanaka, M. (1989) Inhibition of calpain by a synthetic oligopeptide corresponding to an exon of the human calpastatin gene. J. Biol. Chem. 264, 18866-18869
60. Croall, D.E. and McGrody, K.S. (1994) Domain structure of calpain: mapping the binding site for calpastatin. Biochemistry 33, 13223-13230
61. Kawasaki, H., Emori, Y., Imajoh-Ohmi, S., Minami, Y., and Suzuki, K. (1989) Identification and characterization of inhibitory sequences in four repeating domains of the endogenous inhibitor for calcium-dependent protease. J. Biochem. 106, 274-281
62. Takano, E., Ma, H., Yang, H.Q., Maki, M., and Hatanaka, M. (1995) Preference of calcium-dependent interactions between calmodulin-like domains of calpain and calpastatin subdomains. FEBS Lett. 362, 93-97
63. Yang, H.Q., Ma, H., Takano, E., Hatanaka, M., and Maki, M. (1994) Analysis of calcium-dependent interaction between amino-terminal conserved region of calpastatin functional domain and calmodulin-like domain of μ-calpain large subunit. J. Biol. Chem. 269, 18977-18984
64. Ma, H., Yang, H.Q., Takano, E., Lee, W.J., Hatanaka, M., and Maki, M. (1993) Requirement of different subdomains of calpastatin for calpain inhibition and for binding to calmodulin-like domains. J. Biochem. 113, 591-599
65. Ma, H., Yang, H.Q., Takano, E., Hatanaka, M., and Maki, M. (1994) Amino-terminal conserved region in proteinase inhibitor domain of calpastatin potentiates its calpain inhibitory activity by interacting with calmodulin-like domain of the proteinase. J. Biol. Chem. 269, 24430-24436
66. 2+-activated neutral protease (CANP) and its endogenous inhibitor. FEBS Lett. 187, 47-50
67. 2+-requiring forms of calcium-activated neutral proteases. Biochemistry 28, 449-455
68. Kawasaki, H. and Kawashima, S. (1996) Regulation of the calpain-calpastatin system by membranes. Mol. Membr. Biol. 13, 217-224
69. Kawasaki, H., Emori, Y., and Suzuki, K. (1993) Calpastatin has two distinct sites for interaction with calpain - effect of calpastatin fragments on the binding of calpain to membranes. Arch. Biochem. Biophys. 305, 467-472