Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochrome c release to the cytosol

Journal of Cell Biology

Volumn 160, Issue 7, 2003, Pages 1115-1127

  Breckenridge, David G ^a   Stojanovic, Marina ^a   Marcellus, Richard C ^b   Shore, Gordon C ^a  

^a MCGILL UNIVERSITY   (Canada)

^b INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

Author keywords

Apoptosis; BAX; BID; Caspase 8; Drp1

Indexed keywords

ADENOVIRUS VECTOR; APOPTOSOME; CASPASE 8; CYTOCHROME C; DYNAMIN; DYNAMIN RELATED PROTEIN 1; FAS ANTIGEN; MEMBRANE PROTEIN; MUTANT PROTEIN; PROTEIN BAP31; PROTEIN P20; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; ENZYME RELEASE; HUMAN; HUMAN CELL; MITOCHONDRIAL MEMBRANE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; STRESS;

ADENOVIRIDAE; ANIMALS; ANTIGENS, CD95; APOPTOSIS; CALCIUM; CASPASES; CELL LINE; CHO CELLS; CRICETINAE; CYTOCHROME C GROUP; CYTOSKELETAL PROTEINS; CYTOSOL; ENDOPLASMIC RETICULUM; FIBROBLASTS; HEAT-SHOCK PROTEINS; HELA CELLS; HSP20 HEAT-SHOCK PROTEINS; HUMANS; MEMBRANE PROTEINS; MITOCHONDRIA; MODELS, BIOLOGICAL; MUSCLE PROTEINS; RATS; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; UTROPHIN;

ADENOVIRIDAE;

EID: 0037417334     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200212059     Document Type: Article

References (59)

1. Adachi, T., W.W. Schamel, K.M. Kim, T. Watanabe, B. Becker, P.J. Nielsen, and M. Reth. 1996. The specificity of association of the IgD molecule with the accessory proteins BAP31/BAP29 lies in the IgD transmembrane sequence. EMBO J. 15:1534-1541.
2. Bereiter-Hahn, J., and M. Voth. 1994. Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria. Microsc. Res. Tech. 27:198-219.
3. Berridge, M.J., P. Lipp, and M.D. Boorman. 2000. The versatility and universality of calcium signalling. Nat. Rev. Mol. Cell Biol. 1:11-21.
4. Bett, A.J., W. Haddara, L. Prevec, and F.L. Graham. 1994. An efficient and flexible system for construction of adenovirus vectors with insertions or deletions in early regions 1 and 3. Proc. Natl. Acad. Sci. USA. 91:8802-8806.
5. Bleazard, W., J.M. McCaffery, E.J. King, S. Bale, A. Mozdy, Q. Tieu, J. Nunnari, and J.M. Shaw. 1999. The dynamin-related GTPase Dnm 1 regulates mitochondrial fission in yeast. Nat. Cell Biol. 1:298-304.
6. Breckenridge, D.G., and G.C. Shore. 2000. Regulation of apoptosis by E1A and Myc oncoproteins. Crit. Rev. Eukaryot. Gene Exp. 10:273-280.
7. Breckenridge, D.G., and G.C. Shore. 2002. The endoplasmic reticulum and apoptosis. In Genetics of Apoptosis. S. Grimm, editor. BIOS Scientific Publishers Inc., Oxford. 95-113.
8. Breckenridge, D.G., M. Nguyen, S. Kuppig, M. Reth, and G.C. Shore. 2002. The procaspase-8 isoform, procaspase-8L, recruited to the BAP31 complex at the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA. 99:4331-4336.
9. Budihardjo, I., H. Oliver, M. Lutter, X. Luo, and X. Wang. 1999. Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell Dev. Biol. 15:269-290.
10. 2+ to the mitochondrial permeability transition induced by tert-butylhydroperoxide in rat hepatocytes. Hepatology. 29:1523-1531.
11. Cheng, E.H., D.G. Kirsch, R.J, Clem, R. Ravi, M.B. Kastan, A. Bedi, K. Ueno, and J.M. Hardwick. 1997. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science. 278:1966-1968.
12. Clem, R.J., E.H. Cheng, C.L. Karp, D.G. Kirsch, K. Ueno, A. Takahashi, M.B. Kastan, D.E. Griffin, W.C. Earnshaw, M.A. Veliuona, and J.M. Hardwick. 1998. Modulation of cell death by Bcl-XL through caspase interaction. Proc. Natl. Acad. Sci. USA. 95:554-559.
13. Collins, T.J., M.J. Berridge, P. Lipp, and M.D. Bootman. 2002. Mitochondria are morphologically and functionally heterogeneous within cells. EMBO J. 21:1616-1627.
14. Cory, S., and J.M. Adams. 2002. The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer. 2:647-656.
15. Deng, Y., Y. Lin, and X. Wu. 2002. TRAIL-induced apoptosis requires Bax-dependent mitochondrial release of Smac/DIABLO. Genes Dev. 16:33-45.
16. Desagher, S., and J.C. Martinou. 2000. Mitochondria as the central control point ofapoptosis. Trends Cell Biol. 10:369-377.
17. Desagher, S., A. Osen-Sand, A. Nichols, R. Eskes, S. Montessuit, S. Lauper, K. Maundrell, B. Antonsson, and J.C. Martinou. 1999. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144:891-901.
18. 2+ concentration within the endoplasmic reticulum. Proc. Natl. Acad Sci. USA. 97:5723-5728.
19. Frank, S., B. Gaume, E.S. Bergmann-Leitner, W.W. Leitner, E.G. Robert, F. Catez, C.L. Smith, and R.J. Youle. 2001. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev. Cell. 1:515-525.
20. Fulda, S., W. Wick, M. Weller, and K.M. Debatin. 2002. Smac agonists sensitize for Apo2L/TRAIL-or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat. Med. 8:808-815.
21. Goping, I.S., D.G. Millar, and G.C. Shore. 1995. Identification of the human mitochondrial protein import receptor, huMas20p. Complementation of delta mas20 in yeast. FEBS Lett. 373:45-50.
22. Green, D.R., and J.C. Reed. 1998. Mitochondria and apoptosis. Science. 281:1309-1312.
23. Hajnoczky, G., G. Csordas, M. Madesh, and P. Pacher. 2000. Control of apoptosis by IP(3) and ryanodine receptor driven calcium signals. Cell Calcium. 28:349-363.
24. Korsmeyer, S.J., M.C. Wei, M. Saito, S. Weiler, K.J. Oh, and P.H. Schlesinger. 2000. Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ. 7:1166-1173.
25. Krammer, P.H. 2000. CD95's deadly mission in the immune system. Nature. 407:789-795.
26. Labrousse, A.M., M.D. Zappaterra, D.A. Rube, and A.M. van der Bliek. 1999. C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol. Cell. 4:815-826.
27. Li, H., H. Zhu, C.J. Xu, and J. Yuan. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94:491-501.
28. Li, S., Y. Zhao, X. He, T.H. Kim, D.K. Kuharsky, H. Rabinowich, J. Chen, C. Du, and X.M. Yin. 2002. Relief of extrinsic pathway inhibition by the Biddependent mitochondrial release of Smac in Fas-mediated hepatocyte apoptosis. J. Biol. Chem. 277:26912-26920.
29. Lin, Y., A. Devin, Y. Rodriguez, and Z.G. Liu. 1999. Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev. 13:2514-2526.
30. Luo, X., I. Budihardjo, H. Zou, C. Slaughter, and X. Wang. 1998. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 94:481-490.
31. Mathai, J.P., M. Germain, R.C. Marcellus, and G.C. Shore. 2002. Induction and endoplasmic reticulum location of BIK/NBK in response to apoptotic signaling by E1A and p53. Oncogene. 21:2534-2544.
32. 2+ uptake into mitochondria in vitro and in situ in single cardiac myocytes. J. Biol. Chem. 273:10223-10231.
33. Mootha, V.K., M.C. Wei, K.F. Buttle, L. Scorrano, V. Panoutsakopoulou, C.A. Mannella, and S.J. Korsmeyer. 2001. A reversible component of mitochondrial respiratory dysfunction in apoptosis can be rescued by exogenous cytochrome c. EMBO J. 20:661-671.
34. Muzio, M., B.R. Stockwell, H.R. Stennicke, G.S. Salvesen, and V.M. Dixit. 1998. An induced proximity model for caspase-8 activation. J. Biol. Chem. 273:2926-2930.
35. Nakamura, K., E. Bossy-Wetzel, K. Burns, M.P. Fadel, M. Lozyk, I.S. Goping, M. Opas, R.C. Bleackley, D.R. Green, and M. Michalak. 2000. Changes in endoplasmic reticulum luminal environment affect cell sensitivity to apoptosis. J. Cell Biol. 150:731-740.
36. Ng, F.W., M. Nguyen, T. Kwan, P.E. Branton, D.W. Nicholson, J.A. Cromlish, and G.C. Shore. 1997. p28 Bap31, a Bcl-2/Bcl-XL- and procaspase-8-associated protein in the endoplasmic reticulum. J. Cell Biol. 139:327-338.
37. Nguyen, M., P.E. Branton, S. Roy, D.W. Nicholson, E.S. Alnemri, W.C. Yeh, T.W. Mak, and G.C. Shore. 1998. E1A-induced processing of procaspase-8 can occur independently of FADD and is inhibited by Bcl-2. J. Biol. Chem. 273:33099-33102.
38. Nguyen, M., D.G. Breckenridge, A. Ducret, and G.C. Shore. 2000. Caspase-resistant BAP31 inhibits fas-mediated apoptotic membrane fragmentation and release of cytochrome c from mitochondria. Mol. Cell. Biol. 20:6731-6740.
39. Osteryoung, K.W. 2001. Organelle fission in eukaryotes. Curr. Opin. Microbiol. 4:639-646.
40. Pacher, P., and G. Hajnoczky. 2001. Propagation of the apoptotic signal by mirochondrial waves. EMBO J. 20:4107-4021.
41. Petit, P.X., M. Goubern, P. Diolez, S.A. Susin, N. Zamzami, and G. Kroemer. 1998. Disruption of the outer mitochondrial membrane as a result of large amplitude swelling: the impact of irreversible permeability transition. FEBS Lett. 426:111-116.
42. 2+ influx in Bcl-2-overexpressing cells. J. Cell Biol. 148:857-862.
43. 2+ concentration of the endoplasmic reticulum is a key determinant of ceramide-induced apoptosis: significance for the molecular mechanism of Bcl-2. EMBO J. 20:2690-2701.
44. 2+ responses. Science. 280:1763-1766.
45. Ruffolo, S.C., D.G. Breckenridge, M. Nguyen, I.S. Goping, A. Gross, S.J. Korsmeyer, H. Li, J. Yuan, and G.C. Shore. 2000. BID-dependent and BID-independent pathways for BAX insertion into mitochondria. Cell Death Differ. 7:1101-1108.
46. Scaffidi, C., S. Fulda, A. Srinivasan, C. Friesen, F. Li, K.J. Tomaselli, K.M. Debatin, P.H. Krammer, and M.E. Peter. 1998. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17:1675-1687.
47. Schulze-Osthoff, K., D. Ferrari, M. Los, S. Wesselborg, and M.E. Peter. 1998. Apoptosis signaling by death receptors. Eur. J. Biochem. 254:439-459.
48. Scorrano, L., M. Ashiya, K. Buttle, S. Weiler, S.A. Oakes, C.A. Mannella, and S.J. Korsmeyer. 2002. A distinct pathway remodels mitochondrial cistae and mobilizes cytochrome during apoptosis. Dev. Cell. 2:55-67.
49. 2+ from sarcoplasmic reticulum to mitochondtia in rat ventricular myocytes. J. Bioenerg. Biomembr. 32:97-104.
50. Shaw, J.M., and J. Nunnari. 2002. Mitochondrial dynamics and division in budding yeast. Trends Cell Biol. 12:178-184.
51. Smirnova, E., L. Gripatic, D.L. Shurland, and A.M. van der Bliek. 2001. Dynamin-related protein Drp1 is required for mitochondtial division in mammalian cells. Mol. Biol. Cell. 12:2245-2256.
52. Smirnova, E., D.L, Shurland, S.N. Ryazantsev, and A.M. van det Bliek. 1998. A human dynamin-related protein controls the distribution of mitochondria. J. Cell Biol. 143:351-358.
53. Stegh, A.H., H. Herrmann, S. Lampel, D. Weisenberger, K. Andra, M. Seper, G. Wiche, P.H. Krammer, and M.E. Peter. 2000. Identification of the cytolinker plectin as a major early in vivo substrate for caspase 8 during CD95-and tumor necrosis factor receptor-mediated apoptosis. Mol. Cell. Biol. 20:5665-5679.
54. Szalai, G., R. Krishnamurthy, and G. Hajnoczky. 1999. Apoptosis driven by IP(3)-linked mitochondrial calcium signals. EMBO J. 18:6349-6361.
55. Wang, B., M. Nguyen, D.G. Breckenridge, M. Stojanovic, P.A. Clemons, S. Kuppig, and G.C. Shore. 2003. Uncleaved BAP31 in association with A4 protein at the endoplasmic reticulum is an inhibitor of Fas-initiated release of cytochrome c from mitochondria. J. Biol. Chem. In press.
56. Wang, J., H.J. Chun, W. Wong, D.M. Spencer, and M.J. Lenardo. 2001. Caspase-10 is an initiator caspase in death receptor signaling. Proc. Natl. Acad. Sci. USA. 98:13884-13888.
57. Yin, X.M., K. Wang, A. Gtoss, Y. Zhao, S. Zinkel, B. Klocke, K.A. Roth, and S.J. Korsmeyer. 1999. Bid-deficient mice are resistant to Fas-induced hepatocellular apoptosis. Nature. 400:886-891.
58. Yoshida, H., Y.Y. Kong, R. Yoshida, A.J. Elia, A. Hakem, R. Hakem, J.M. Penninger, and T.W. Mak. 1998. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell. 94:739-750.
59. Zhu, W., A. Cowie, G.W. Wasfy, L.Z. Penn, B. Leber, and D.W. Andrews. 1996. Bcl-2 mutants with restricted subcellular location reveal spatially distinct pathways for apoptosis in different cell types. EMBO J. 15:4130-4141.