ERp57-associated mitochondrial μ-calpain truncates apoptosis-inducing factor

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1783, Issue 10, 2008, Pages 1955-1963

  Ozaki, Taku ^a   Yamashita, Tetsuro ^b   Ishiguro, Sei ichi ^a  

^a Hirosaki University   (Japan)

^b IWATE UNIVERSITY   (Japan)

Author keywords

Apoptosis inducing factor (AIF); ERp57; MALDI TOFMS; Mitochondrial calpain; Mitochondrial intermembrane space

Indexed keywords

5,5' DITHIOBIS(2 NITROBENZOIC ACID); APOPTOSIS INDUCING FACTOR; ARSENOSOBENZENE; CALPAIN 1; CALPASTATIN; CASEIN; CHAPERONE; ERP57 PROTEIN; ISOMERASE INHIBITOR; PROTEIN DISULFIDE ISOMERASE; PROTEIN SUBUNIT; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; IMMUNOPRECIPITATION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; ZYMOGRAPHY;

ANIMALS; APOPTOSIS INDUCING FACTOR; CALCIUM; CALPAIN; MITOCHONDRIA; PROTEIN BINDING; PROTEIN DISULFIDE-ISOMERASE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 50849127125     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2008.05.011     Document Type: Article

References (65)

1. Ishiura S. Calcium-dependent proteolysis in living cells. Life Sci. 29 (1981) 1079-1087
2. Goll D.E., Thompson V.F., Li H., Wei W., and Cong J. The calpain system. Physiol. Rev. 83 (2003) 731-801
3. Suzuki K., Hata S., Kawabata Y., and Sorimachi H. Structure, activation, and biology of calpain. Diabetes 53 Suppl 1 (2004) S12-S18
4. Sorimachi H., Imajoh-Ohmi S., Emori Y., Kawasaki H., Ohno S., Minami Y., and Suzuki K. Molecular cloning of a novel mammalian calcium-dependent protease distinct from both m- and mu-types. Specific expression of the mRNA in skeletal muscle. J. Biol. Chem. 264 (1989) 20106-20111
5. Sorimachi H., Ishiura S., and Suzuki K. A novel tissue-specific calpain species expressed predominantly in the stomach comprises two alternative splicing products with and without Ca(2+)-binding domain. J. Biol. Chem. 268 (1993) 19476-19482
6. Lee H.J., Sorimachi H., Jeong S.Y., Ishiura S., and Suzuki K. Molecular cloning and characterization of a novel tissue-specific calpain predominantly expressed in the digestive tract. Biol. Chem. 379 (1998) 175-183
7. Yoshimura N., Kikuchi T., Sasaki T., Kitahara A., Hatanaka M., and Murachi T. Two distinct Ca2+ proteases (calpain I and calpain II) purified concurrently by the same method from rat kidney. J. Biol. Chem. 258 (1983) 8883-8889
8. Murachi T. Calcium-dependent proteinases and specific inhibitors: Calpain and calpastatin. Biochem. Soc. Symp. 49 (1984) 149-167
9. Murachi T. Intracellular regulatory system involving calpain and calpastatin. Biochem. Int. 18 (1989) 263-294
10. Wendt A., Thompson V.F., and Goll D.E. Interaction of calpastatin with calpain: a review. Biol. Chem. 385 (2004) 465-472
11. Melloni E., Averna M., Stifanese R., De Tullio R., Defranchi E., Salamino F., and Pontremoli S. Association of calpastatin with inactive calpain: A novel mechanism to control the activation of the protease?. J. Biol. Chem. 281 (2006) 24945-24954
12. Beer D.G., Hjelle J.J., Petersen D.R., and Malkinson A.M. Calcium-activated proteolytic activity in rat liver mitochondria. Biochem. Biophys. Res. Commun. 109 (1982) 1276-1283
13. Tavares A., and Duque-Magalhaes M.C. Demonstration of three calpains in the matrix of rat liver mitochondria. Biomed. Biochim. Acta 50 (1991) 523-529
14. Gores G.J., Miyoshi H., Botla R., Aguilar H.I., and Bronk S.F. Induction of the mitochondrial permeability transition as a mechanism of liver injury during cholestasis: a potential role for mitochondrial proteases. Biochim. Biophys. Acta 1366 (1998) 167-175
15. Arnoult D., Akarid K., Grodet A., Petit P.X., Estaquier J., and Ameisen J.C. On the evolution of programmed cell death: apoptosis of the unicellular eukaryote leishmania major involves cysteine proteinase activation and mitochondrion permeabilization. Cell Death Differ. 9 (2002) 65-81
16. Endo S., Ishiguro S., and Tamai M. Possible mechanism for the decrease of mitochondrial aspartate aminotransferase activity in ischemic and hypoxic rat retinas. Biochim. Biophys. Acta 1450 (1999) 385-396
17. Polster B.M., Basanez G., Etxebarria A., Hardwick J.M., and Nicholls D.G. Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J. Biol. Chem. 280 (2005) 6447-6454
18. Shulga N., and Pastorino J.G. Acyl coenzyme A-binding protein augments bid-induced mitochondrial damage and cell death by activating mu-calpain. J. Biol. Chem. 281 (2006) 30824-30833
19. Badugu R., Garcia M., Bondada V., Joshi A., and Geddes J.W. N-terminal of calpain 1 is a mitochondrial targeting sequence. J. Biol. Chem. 283 (2008) 3409-3417
20. Garcia M., Bondada V., and Geddes J.W. Mitochondrial localization of mu-calpain. Biochem. Biophys. Res. Commun. 338 (2005) 1241-1247
21. Arrington D.D., Van Vleet T.R., and Schnellmann R.G. Calpain 10: a mitochondrial calpain and its role in calcium-induced mitochondrial dysfunction. Am. J. Physiol., Cell Physiol. 291 (2006) C1159-C1171
22. Giguere C.J., Covington M.D., and Schnellmann R.G. Mitochondrial calpain 10 activity and expression in the kidney of multiple species. Biochem. Biophys. Res. Commun. 366 (2008) 258-262
23. Ozaki T., Tomita H., Tamai M., and Ishiguro S. Characteristics of mitochondrial calpains. J. Biochem. (Tokyo) 142 (2007) 365-376
24. Barnoy S., Zipser Y., Glaser T., Grimberg Y., and Kosower N.S. Association of calpain (Ca(2+)-dependent thiol protease) with its endogenous inhibitor calpastatin in myoblasts. J. Cell Biochem. 74 (1999) 522-531
25. Urade R., Nasu M., Moriyama T., Wada K., and Kito M. Protein degradation by the phosphoinositide-specific phospholipase C-alpha family from rat liver endoplasmic reticulum. J. Biol. Chem. 267 (1992) 15152-15159
26. Jessop C.E., Chakravarthi S., Garbi N., Hammerling G.J., Lovell S., and Bulleid N.J. ERp57 is essential for efficient folding of glycoproteins sharing common structural domains. EMBO J. 26 (2007) 28-40
27. Grillo C., D'Ambrosio C., Consalvi V., Chiaraluce R., Scaloni A., Maceroni M., Eufemi M., and Altieri F. DNA-binding activity of the ERp57 C-terminal domain is related to a redox-dependent conformational change. J. Biol. Chem. 282 (2007) 10299-10310
28. Elliott J.G., Oliver J.D., and High S. The thiol-dependent reductase ERp57 interacts specifically with N-glycosylated integral membrane proteins. J. Biol. Chem. 272 (1997) 13849-13855
29. Molinari M., and Helenius A. Glycoproteins form mixed disulphides with oxidoreductases during folding in living cells. Nature 402 (1999) 90-93
30. Silvennoinen L., Myllyharju J., Ruoppolo M., Orru S., Caterino M., Kivirikko K.I., and Koivunen P. Identification and characterization of structural domains of human ERp57: association with calreticulin requires several domains. J. Biol. Chem. 279 (2004) 13607-13615
31. Frickel E.M., Frei P., Bouvier M., Stafford W.F., Helenius A., Glockshuber R., and Ellgaard L. ERp57 is a multifunctional thiol-disulfide oxidoreductase. J. Biol. Chem. 279 (2004) 18277-18287
32. Pollock S., Kozlov G., Pelletier M.F., Trempe J.F., Jansen G., Sitnikov D., Bergeron J.J., Gehring K., Ekiel I., and Thomas D.Y. Specific interaction of ERp57 and calnexin determined by NMR spectroscopy and an ER two-hybrid system. EMBO J. 23 (2004) 1020-1029
33. Newmeyer D.D., and Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell 112 (2003) 481-490
34. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M., Larochette N., Goodlett D.R., Aebersold R., Siderovski D.P., Penninger J.M., and Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397 (1999) 441-446
35. Klein J.A., Longo-Guess C.M., Rossmann M.P., Seburn K.L., Hurd R.E., Frankel W.N., Bronson R.T., and Ackerman S.L. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 419 (2002) 367-374
36. Parsons D.F., Williams G.R., and Chance B. Characteristics of isolated and purified preparations of the outer and inner membranes of mitochondria. Ann. N.Y. Acad. Sci. 137 (1966) 643-666
37. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
38. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
39. Tamura T., Yamashita T., Segawa H., and Taira H. N-linked oligosaccharide chains of sendai virus fusion protein determine the interaction with endoplasmic reticulum molecular chaperones. FEBS Lett. 513 (2002) 153-158
40. Tomita Y., Yamashita T., Sato H., and Taira H. Kinetics of interactions of sendai virus envelope glycoproteins, F and HN, with endoplasmic reticulum-resident molecular chaperones, BiP, calnexin, and calreticulin. J. Biochem. (Tokyo) 126 (1999) 1090-1100
41. Feener E.P., Shen W.C., and Ryser H.J. Cleavage of disulfide bonds in endocytosed macromolecules. A processing not associated with lysosomes or endosomes. J. Biol. Chem. 265 (1990) 18780-18785
42. Kalef E., and Gitler C. Purification of vicinal dithiol-containing proteins by arsenical-based affinity chromatography. Methods Enzymol. 233 (1994) 395-403
43. Guthapfel R., Gueguen P., and Quemeneur E. Reexamination of hormone-binding properties of protein disulfide-isomerase. Eur. J. Biochem. 242 (1996) 315-319
44. Towbin H., Staehelin T., and Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U. S. A. 76 (1979) 4350-4354
45. Hellman U., Wernstedt C., Gonez J., and Heldin C.H. Improvement of an "in-gel" digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal. Biochem. 224 (1995) 451-455
46. Raser K.J., Posner A., and Wang K.K. Casein zymography: a method to study mu-calpain, m-calpain, and their inhibitory agents. Arch. Biochem. Biophys. 319 (1995) 211-216
47. Arthur J.S., and Mykles D.L. Calpain zymography with casein or fluorescein isothiocyanate casein. Methods Mol. Biol. 144 (2000) 109-116
48. Ishiguro S., Yamamoto H., Yanai N., and Takeuchi T. Quantitative analysis of mouse tyrosinase by enzyme-linked immunosorbent assay. J. Biochem. (Tokyo) 99 (1986) 1081-1085
49. Ishiguro S., Fukuda K., Kanno C., and Mizuno K. Accumulation of immunoreactive opsin on plasma membranes in degenerating rod cells of rd/rd mutant mice. Cell Struct. Funct. 12 (1987) 141-155
50. Taylor S.W., Fahy E., Zhang B., Glenn G.M., Warnock D.E., Wiley S., Murphy A.N., Gaucher S.P., Capaldi R.A., Gibson B.W., and Ghosh S.S. Characterization of the human heart mitochondrial proteome. Nat. Biotechnol. 21 (2003) 281-286
51. Kar P., Chakraborti T., Roy S., Choudhury R., and Chakraborti S. Identification of calpastatin and mu-calpain and studies of their association in pulmonary smooth muscle mitochondria. Arch. Biochem. Biophys. 466 (2007) 290-299
52. Kar P., Chakraborti T., Samanta K., and Chakraborti S. Submitochondrial localization of associated mu-calpain and calpastatin. Arch. Biochem. Biophys. 470 (2008) 176-186
53. Herrmann J.M., and Neupert W. Protein transport into mitochondria. Curr. Opin. Microbiol. 3 (2000) 210-214
54. Endo T., Yamamoto H., and Esaki M. Functional cooperation and separation of translocators in protein import into mitochondria, the double-membrane bounded organelles. J. Cell Sci. 116 (2003) 3259-3267
55. Wiedemann N., Frazier A.E., and Pfanner N. The protein import machinery of mitochondria. J. Biol. Chem. 279 (2004) 14473-14476
56. Koehler C.M. New developments in mitochondrial assembly. Annu. Rev. Cell Dev. Biol. 20 (2004) 309-335
57. Naoe M., Ohwa Y., Ishikawa D., Ohshima C., Nishikawa S., Yamamoto H., and Endo T. Identification of Tim40 that mediates protein sorting to the mitochondrial intermembrane space. J. Biol. Chem. 279 (2004) 47815-47821
58. Peaper D.R., Wearsch P.A., and Cresswell P. Tapasin and ERp57 form a stable disulfide-linked dimer within the MHC class I peptide-loading complex. EMBO J. 24 (2005) 3613-3623
59. Santos S.G., Campbell E.C., Lynch S., Wong V., Antoniou A.N., and Powis S.J. Major histocompatibility complex class I-ERp57-tapasin interactions within the peptide-loading complex. J. Biol. Chem. 282 (2007) 17587-17593
60. Herrmann J.M., and Kohl R. Catch me if you can! Oxidative protein trapping in the intermembrane space of mitochondria. J. Cell Biol. 176 (2007) 559-563
61. Sanges D., Comitato A., Tammaro R., and Marigo V. Apoptosis in retinal degeneration involves cross-talk between apoptosis-inducing factor (AIF) and caspase-12 and is blocked by calpain inhibitors. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 17366-17371
62. Otera H., Ohsakaya S., Nagaura Z., Ishihara N., and Mihara K. Export of mitochondrial AIF in response to proapoptotic stimuli depends on processing at the intermembrane space. EMBO J. 24 (2005) 1375-1386
63. Cao G., Xing J., Xiao X., Liou A.K., Gao Y., Yin X.M., Clark R.S., Graham S.H., and Chen J. Critical role of calpain I in mitochondrial release of apoptosis-inducing factor in ischemic neuronal injury. J. Neurosci. 27 (2007) 9278-9293
64. Gallina A., Hanley T.M., Mandel R., Trahey M., Broder C.C., Viglianti G.A., and Ryser H.J. Inhibitors of protein-disulfide isomerase prevent cleavage of disulfide bonds in receptor-bound glycoprotein 120 and prevent HIV-1 entry. J. Biol. Chem. 277 (2002) 50579-50588
65. Kozlov G., Maattanen P., Schrag J.D., Pollock S., Cygler M., Nagar B., Thomas D.Y., and Gehring K. Crystal structure of the bb' domains of the protein disulfide isomerase ERp57. Structure 14 (2006) 1331-1339