Procaspase-9 is attached to the mitochondrial outer membrane in the early stages of apoptosis

• Autorzy: Milisav I , Suput D.
• Języki publikacji: EN

Abstrakty

EN

Procaspase-9 is the zymogen form of one of the apoptosis initiators, caspase-9. Its cellular location may differ depending on the cell type; it is found throughout the cytosol, although some of it may be associated with the mitochondria. Procaspase-9 relocates from the cytosol to the mitochondria shortly after the triggering of apoptosis in rat hepatocytes. We investigated whether the mitochondrial protein import machineries import procaspase-9. The combined results of protein import analyses, mitochondrial fractionation and protease treatments of intact and swollen mitochondria imply that procaspase-9 attaches to the outer surface of the mitochondrial outer membrane.

Słowa kluczowe

EN

caspase-9; apoptosis initiator; procaspase-9; mitochondrion; apoptosis; protein import; rotenone; localization

• Wydawca: -
• Czasopismo: Cellular and Molecular Biology Letters
• Rocznik: 2007
• Tom: 12
• Numer: 4
• Opis fizyczny: p.509-522,fig.,ref.

Twórcy

autor

Milisav I

• University of Ljubljana, Zaloska 4, SI-1000 Ljubljana, Slovenia

autor

Suput D.

Bibliografia

• 1. Kerr, J.F.R, Wyllie, H. and Currie, A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26 (1972) 239-257.
• 2. Cohen, G.M. Caspases: the executioners of apoptosis. Biochem. J. 326 (1997) 1-16.
• 3. Salvesen, G.S. and Dixit, V.M. Caspases: intracellular signaling by proteolysis. Cell 91 (1997) 443-446.
• 4. Slee, E.A., Harte, M.T., Kluck, R.M., Wolf, B.B., Casiano, C.A., Newmeyer, D.D., Wang, H.G., Reed, J.C., Nicholson, D.W., Alnemri, E.S., Green, D.R. and Martin, S.J. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J. Cell Biol. 144 (1999) 281-292.
• 5. Robertson, J.D., Enoksson, M., Suomela, M., Zhivotovsky, B. and Orrenius, S. Caspase-2 acts upstream of mitochondria to promote cytochrome c release during etoposide-induced apoptosis. J. Biol. Chem. 277 (2002) 29803-29809.
• 6. Morishima, N., Nakanishi, K., Takenouchi, H., Shibata, T. and Yasuhiko, Y. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J. Biol. Chem. 277 (2002) 34287-34294.
• 7. Luo, X., Budihardjo, I., Zou, H., Slaughter, C. and Wang, X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94 (1998) 481-490.
• 8. Li, H., Zhu, H., Xu, C. and Yuan, J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94 (1998) 491-501.
• 9. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S.M., Ahmad, M., Alnemri, E.S. and Wang, X. Cytochrome c and dATP-dependent formation of Apaf1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91 (1997) 479-489.
• 10. Cardone, M.H., Roy, N., Stennicke, H.R., Salvesen, G.S., Franke, T.F., Stanbridge, E., Frisch, S. and Reed, J.C. Regulation of cell death protease caspase-9 by phosphorylation. Science 13 (1998) 1318-1321.
• 11. Shikama, Y.U.M., Miyashita, T. and Yamada, M. Comprehensive studies on subcellular localizations and cell death-inducing activities of eight GFPtagged apoptosis-related caspases. Exp. Cell Res. 264 (2001) 315-325.
• 12. Shimohama, S., Tanino, H. and Fujimoto, S. Differential subcellular localization of caspase family proteins in the adult rat brain, Neuroscience Lett. 315 (2001) 125-128.
• 13. van Loo, G., Saelens, X., Matthijssens, F., Schotte, P., Beyaert, R., Declercq, W. and Vandenabeele, P. Caspases are not localized in mitochondria during life or death. Cell Death Diff. 9 (2002) 1207-1211.
• 14. Potokar, M., Milisav, I., Kreft, M., Stenovec, M. and Zorec, R. Apoptosis triggered redistribution of caspase-9 from cytoplasm to mitochondria. FEBS Lett. 544 (2003) 153-159.
• 15. Zhivotovsky, B., Samali, A., Gahm, A. and Orrenius, S. Caspases: their intracellular localization and translocation during apoptosis. Cell Death Differ. 6 (1999) 644-651.
• 16. Yuan, H., Mutomba, M., Prinz, I. and Gottlieb, R.A. Differential processing of cytosolic and mitochondrial caspases. Mitochondrion 1 (2001) 61-69.
• 17. Susin, S.A., Lorenzo, H.K., Zamzami, N., Marzo, I., Brenner, C., Larochette, N., Prévost, M.-C., Alzari, P.M. and Kroemer, G. Mitochondrial release of caspase-2 and -9 during the apoptotic process. J. Exp. Med. 189 (1999) 381-393.
• 18. Krajewski, S., Krajewska, M., Ellerby, L.M., Welsh, K., Xie, Z., Deveraux, Q.L., Salvesen, G.S., Bredesen, D.E., Rosenthal, R.E., Fiskum, G. and Reed, J. Release of caspase-9 from mitochondria during neuronal apoptosis and cerebral ischemia. Proc. Natl. Acad. Sci. USA 96 (1999) 5752-5757.
• 19. Chandra, D. and Tang, D.G. Mitochondrially localized active caspase-9 and caspase-3 result mostly from translocation from the cytosol and partly from caspase-mediated activation in the organelle. J. Biol. Chem. 278 (2003) 17408-17420.
• 20. Saleh, A., Srinivasula, S.M., Acharya, S., Fishel, R. and Alnemri, E.S. Cytochrome c and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation. J. Biol. Chem. 274 (1999) 17941-17945.
• 21. Cain, K., Brown, D.G., Langlais, C. and Cohen, G.M. Caspase activation involves the formation of the aposome, a large (approximately 700 kDa) caspase-activating complex, J. Biol. Chem. 274 (1999) 22686-22692.
• 22. Ritter, P.M., Marti, A., Blanc, C., Baltzer, A., Krajewski, S., Reed, J.C. and Jaggi, R. Nuclear localization of procaspase-9 and processing by a caspase3-like activity in mammary epithelial cells. Eur. J. Cell Biol. 79 (2001) 358- 364.
• 23. Bitzer, M., Armeanu, S., Prinz, F., Ungerechts, G., Wybranietz, W., Spiegel, M., Bernlöhr, C., Cecconi, F., Gregor, M., Neubert, W.J., Schulze-Osthoff, K. and Lauer, U.M. Caspase-8 and Apaf-1-independent caspase-9 activation in Sendai virus-infected cells. J. Biol. Chem. 277 (2002) 29817-29824.
• 24. Mokranjac, D. and Neupert, W. Protein import into mitochondria. Biochem. Soc. Trans. 33 (2005) 1019-1023.
• 25. Hoogenraad, N.J., Ward, L.A. and Ryan, M.T. Import and assembly of proteins into mitochondria of mammalian cells, Biochim. Biophys. Acta 1592 (2002) 97-105.
• 26. Stojanovski, D., Rissler, M., Pfanner, N. and Meisinger, C. Mitochondrial morphology and protein import – a tight connection? Biochim. Biophys. Acta 1763 (2006) 414-421.
• 27. Hartl, F.-U., Pfanner, N., Nicholson, D.W. and Neupert, W. Mitochondrial protein import. Biochim. Biophys. Acta 988 (1989) 1-45.
• 28. Matocha, M.F. and Waterman, M.R. Discriminatory processing of the precursor forms of cytochrome P-450SCC and adrenodoxin by adrenocortical and heart mitochondria. J. Biol. Chem. 259 (1984) 8672-8678.
• 29. Matocha, M.F. and Waterman, M.R. Synthesis and processing of mitochondrial steroid hydroxylases. J. Biol. Chem. 260 (1985) 12259- 12265.
• 30. DeSousa, G., Dou, M., Barbe, D., Lacarelle, B., Placidi, M. and Rahmani, R. Freshli isolated or cryopreserved human hepatocytes in primary culture: influence of drug metabolism on hepatotoxicity. Toxicol. in vitro 5 (1991) 483-486.
• 31. Daum, G., Böhni, P. C. and Schatz, G. Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J. Biol. Chem. 257 (1982) 13028-13033.
• 32. Werner, S. and Neupert, W. Functional and biogenetical heterogeneity of the inner membrane of rat-liver mitochondria. Eur. J. Biochem. 25 (1972) 379- 396.
• 33. Bauer, M.F., Gempel, K., Reichert, A.S., Rappold, G.A., Lichtner, P., Gerbitz, K.-D., Neupert, W., Brunner, M. and Hofmann, S. Genetic and structural characterization of the human mitochondrial inner membrane translocase, J. Mol. Biol. 289 (1999) 69-82.
• 34. Duan, H., Orth, K., Chinnaiyan, A.M., Poirier, G.G., Froelich, C.J., He, W.W. and Dixit, V.M. ICE-LAP-6, a novel member of the ICE/Ced-3 gene family, is activated by the cytotoxic T cell protease granzyme B. J. Biol. Chem. 271 (1996) 16720-16724.
• 35. Rothbauer, U., Hofmann, S., Mühlenbein, N., Paschen, S.A., Gerbitz, K.-D., Neupert, W., Brunner, M. and Bauer, M.F. Role of the Deafness Dystonia Peptide 1 (DDP1) in Import of Human Tim23 into the Inner Membrane of Mitochondria. J. Biol. Chem. 276 (2001) 37327-37334.
• 36. Ungermann, C., Neupert, W. and Cyr, D.M. The role of Hsp70 in conferring unidirectionality on protein translocation into mitochondria. Science 266 (1994) 1250-1253.
• 37. Pelham, H.R. and Jackson, R.J. An efficient mRNA-dependent translation system from reticulocyte lysates. Eur. J. Biochem. 67 (1976) 247-256.
• 38. Luciano, P., Geoffroy, S., Brandt, A., Hernandez, J.-F. and Géli, V. Functional cooperation of the mitochondrial processing peptidase subunits. J. Mol. Biol. 272 (1997) 213-225.
• 39. Kaldi, K., Bauer, M.F., Sirrenberg, C., Neupert, W. and Brunner, M. Biogenesis of Tim23 and Tim17, integral components of the TIM machinery for matrix-targeted preproteins. EMBO J. 17 (1998) 1569-1576.
• 40. Gordon, D.M., Shi, Q., Dancis, A., Pain, D. Maturation of frataxin within mammalian and yeast mitochondria: one-step processing by matrix processing peptidase. Hum. Mol. Genet. 8 (1999) 2255-2262.