Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis

Journal of Cell Biology

Volumn 162, Issue 1, 2003, Pages 59-69

  Zong, Wei Xing ^a   Li, Chi ^a   Hatzivassiliou, Georgia ^a   Lindsten, Tullia ^a   Yu, Qian Chun ^a   Yuan, Junying ^b   Thompson, Craig B ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Bak; Bax; Ca2+; Caspase 12; ER

Indexed keywords

CASPASE; CASPASE 12; CASPASE 7; PROTEIN BAK; PROTEIN BAX; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONFORMATIONAL TRANSITION; ENDOPLASMIC RETICULUM; ENZYME ACTIVATION; FIBROBLAST; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STRESS;

ANIMALS; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; CALCIUM; CALCIUM SIGNALING; CASPASE 12; CASPASE 7; CASPASES; CELL LINE, TRANSFORMED; ENDOPLASMIC RETICULUM; EUKARYOTIC CELLS; MEMBRANE PROTEINS; MICE; MITOCHONDRIA; MUTATION; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN CONFORMATION; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; STRESS;

ANIMALIA;

EID: 0037810844     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200302084     Document Type: Article

References (51)

1. Abeele, F.V., R. Skryma, Y. Shuba, F. Van Coppenolle, C. Slomianny, M. Roudbaraki, B. Mauroy, F. Wuytack, and N. Prevarskaya. 2002. Bcl-2-dependent modulation of Ca(2+) homeostasis and store-operated channels in prostate cancer cells. Cancer Cell. 1:169-179.
2. Akao, Y., Y. Otsuki, S. Kataoka, Y. Ito, and Y. Tsujimoto. 1994. Multiple subcellular localization of bcl-2: detection in nuclear outer membrane, endoplasmic reticulum membrane, and mitochondrial membranes. Cancer Res. 54:2468-2471.
3. Allen, E., Q.C. Yu, and E. Fuchs. 1996. Mice expressing a mutant desmosomal cadherin exhibit abnormalities in desmosomes, proliferation, and epidermal differentiation. J. Cell Biol. 133:1367-1382.
4. Annis, M.G., N. Zamzami, W. Zhu, L.Z. Penn, G. Kroemer, B. Leber, and D.W. Andrews. 2001. Endoplasmic reticulum localized Bcl-2 prevents apoptosis when redistribution of cytochrome c is a late event. Oncogene. 20:1939-1952.
5. Cecconi, F., G. Alvarez-Bolado, B.I. Meyer, K.A. Rorh, and P. Gruss. 1998. Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell. 94:727-737.
6. Cheng, E.H., M.C. Wei, S. Weiler, R.A. Flavell, T.W. Mak, T. Lindsten, and S.J. Korsmeyer. 2001. BCL-2, BCL-X(L) sequester BH3 domain-only molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol. Cell. 8:705-711.
7. Chittenden, T., E.A. Harrington, R. O'Connor, C. Flemington, R.J. Lutz, G.I. Evan, and B.C. Guild. 1995. Induction of apoptosis by the Bcl-2 homologue Bak. Nature. 374:733-736.
8. Cleary, M.L., and J. Sklar. 1985. Nucleotide sequence of a t(14;18) chromosomal breakpoint in follicular lymphoma and demonstration of a breakpoint-cluster region near a transcriptionally active locus on chromosome 18. Proc. Natl. Acad. Sci. USA. 82:7439-7443.
9. 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.
10. Ferri, K.F., and G. Kroemet. 2001. Organelle-specific initiation of cell death pathways. Nat. Cell Biol. 3:E255-E263.
11. Germain, M., J.P. Mathai, and G.C. Shore. 2002. BH-3-only BIK functions at the endoplasmic reticulum to stimulate cytochrome c release from mitochondria. J. Biol. Chem. 277:18053-18060.
12. Greenhalf, W., C. Stephan, and B. Chaudhuri. 1996. Role of mitochondria and C-terminal membrane anchor of Bcl-2 in Bax induced growth arrest and mortality in Saccharomyces cerevisiae. FEBS Lett. 380:169-175.
13. Griffiths, G.J., L. Dubrez, C.P. Morgan, N.A. Jones, J. Whitehouse, B.M. Corfe, C. Dive, and J.A. Hickman. 1999. Cell damage-induced conformational changes of the pro-apoptotic protein Bak in vivo precede the onset of apoptosis. J. Cell Biol. 144:903-914.
14. Gross, A., J. Jockel, M.C. Wei, and S.J. Korsmeyer. 1998. Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J. 17:3878-3885.
15. Hacki, J., L. Egger, L. Monney, S. Conus, T. Rosse, I. Fellay, and C. Borner. 2000. Apoprotic crosstalk between the endoplasmic reticulum and mitochondria controlled by Bcl-2. Oncogene. 19:2286-2295.
16. Hanada, M., C. Aime-Sempe, T. Sato, and J.C. Reed. 1995. Structure-function analysis of Bcl-2 protein. Identification of conserved domains important for homodimerization with Bcl-2 and heterodimerization with Bax. J. Biol. Chem. 270:11962-11969.
17. Hsu, Y.T., K.G. Wolter, and R.J. Youle. 1997. Cytosol-to-membrane redistribution of Bax and Bcl-X(L) during apoptosis. Proc. Natl. Acad. Sci. USA. 94:3668-3672.
18. Jurgensmeier, J.M., S. Krajewski, R.C. Armstrong, G.M. Wilson, T. Oltersdorf, L.C. Fritz, J.C. Reed, and S. Ottilie. 1997. Bax- and Bak-induced cell death in the fission yeast Schizosaccharomyces pombe. Mol. Biol. Cell. 8:325-339.
19. Kaufman, R.J. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 13:1211-1233.
20. Krajewski, S., S. Tanaka, S. Takayama, M.J. Schibler, W. Fenton, and J.C. Reed. 1993. Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res. 53:4701-4714.
21. Kuida, K., T.F. Haydar, C.Y. Kuan, Y. Gu, C. Taya, H. Karasuyama, M.S. Su, P. Rakic, and R.A. Flavell. 1998. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell. 94:325-337.
22. 2+ homeostasis by altering expression of inositol 1,4,5-trisphosphate receptors. Proc. Natl. Acad. Sci. USA. 99:9830-9835.
23. 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.
24. Li, K., Y. Li, J.M. Shelton, J.A. Richardson, E. Spencer, Z.J. Chen, X. Wang, and R.S. Williams. 2000. Cytochrome c deficiency causes embryonic lethality and attenuates stress-induced apoptosis. Cell. 101:389-399.
25. Lindsten, T., A.J. Ross, A. King, W.X. Zong, J.C. Rathmell, H.A. Shiels, E. Ulrich, K.G. Waymire, P. Mahar, K. Frauwirth, et al. 2000. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol. Cell. 6:1389-1399.
26. Lithgow, T., R. van Driel, J.F. Bertram, and A. Strasser. 1994. The protein product of the oncogene bcl-2 is a component of the nuclear envelope, the endoplasmic reticulum, and the outer mitochondrial membrane. Cell Growth Differ. 5:411-417.
27. 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.
28. Makin, G.W., B.M. Corfe, G.J. Griffiths, A. Thistlethwaite, J.A. Hickman, and C. Dive. 2001. Damage-induced Bax N-terminal change, translocation to mitochondria and formation of Bax dimers/complexes occur regardless of cell fate. EMBO J. 20:6306-6315.
29. Mandic, A., K. Viktorsson, M. Molin, G. Akusjarvi, H. Eguchi, S.I. Hayashi, M. Toi, J. Hansson, S. Linder, and M.C. Shoshan. 2001. Cisplatin induces the proapoptotic conformation of Bak in a δMEKK1-dependent manner. Mol. Cell. Biol. 21:3684-3691.
30. Marsden, V.S., L. O'Connor, L.A. O'Reilly, J. Silke, D. Metcalf, P.G. Ekert, D.C. Huang, F. Cecconi, K. Kuida, K.J. Tomaselli, et al. 2002. Apoptosis initiated by Bcl-2-regulated caspase activation independently of the cytochrome c/Apaf-1/caspase-9 apoptosome. Nature. 419:634-637.
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. Nakagawa, T., and J. Yuan. 2000. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 150:887-894.
33. Nakagawa, T., H. Zhu, N. Morishima, E. Li, J. Xu, B.A. Yankner, and J. Yuan. 2000. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-β. Nature. 403:98-103.
34. Nakano, K., and K.H. Vousden. 2001. PUMA, a novel proapoptotic gene, is induced by p53. Mol. Cell. 7:683-694.
35. Nguyen, M., P.E. Branton, P.A. Walton, Z.N. Oltvai, S.J. Korsmeyer, and G.C. Shore. 1994. Role of membrane anchor domain of Bcl-2 in suppression of apoptosis caused by E1B-defective adenovirus. J. Biol. Chem. 269:16521-16524.
36. 2+ mobilization promotes cytochrome c release during apoptosis. J. Biol. Chem. 277:20301-20308.
37. 2+ stores. J. Biol. Chem. 277:9219-9225.
38. Oda, E., R. Ohki, H. Murasawa, J. Nemoto, T. Shibue, T. Yamashita, T. Tokino, T. Taniguchi, and N. Tanaka. 2000. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science. 288:1053-1058.
39. Oltvai, Z.N., C.L. Milliman, and S.J. Korsmeyer. 1993. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell. 74:609-619.
40. Pan, Z., M.B. Bhat, A.L. Nieminen, and J. Ma. 2001. Synergistic movements of Ca(2+) and Bax in cells undergoing apoptosis. J. Biol. Chem. 276:32257-32263.
41. Pinton, P., D. Ferrari, P. Magalhaes, K. Schulze-Osthoff, F. Di Virgilio, T. Pozzan, and R. Rizzuto. 2000. Reduced loading of intracellular Ca(2+) stores and downregulation of capacitative Ca(2+) influx in Bcl-2-overexpressing cells. J. Cell Biol. 148:857-862.
42. Puthalakath, H., D.C. Huang, L.A. O'Reilly, S.M. King, and A. Strasser. 1999. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell. 3:287-296.
43. 2+ responses. Science. 280:1763-1766.
44. Srivastava, R.K., S.J. Sollott, L. Khan, R. Hansford, E.G. Lakatta, and D.L. Longo. 1999. Bcl-2 and Bcl-X(L) block thapsigargin-induced nitric oxide generation, c-Jun NH(2)-terminal kinase activity, and apoptosis. Mol. Cell. Biol. 19:5659-5674.
45. Wang, N.S., M.T. Unkila, E.Z. Reineks, and C.W. Distelhorst. 2001. Transient expression of wild-type or mitochondrially targeted Bcl-2 induces apoptosis, whereas transient expression of endoplasmic reticulum-targeted Bcl-2 is protective against Bax-induced cell death. J. Biol. Chem. 276:44117-44128.
46. Wang, X. 2001. The expanding role of mitochondria in apoptosis. Genes Dev. 15:2922-2933.
47. Wei, M.C., T. Lindsten, V.K. Mootha, S. Weiler, A. Gross, M. Ashiya, C.B. Thompson, and S.J. Korsmeyer. 2000. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 14:2060-2071.
48. Wei, M.C., W.X. Zong, E.H. Cheng, T. Lindsten, V. Panoutsakopoulou, A.J. Ross, K.A. Roth, G.R. MacGregor, C.B. Thompson, and S.J. Korsmeyer. 2001. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science. 292:727-730.
49. Yu, J., L. Zhang, P.M. Hwang, K.W. Kinzler, and B. Vogelstein. 2001. PUMA induces the rapid apoptosis of colorectal cancer cells. Mol. Cell. 7:673-682.
50. 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.
51. Zong, W.X., T. Lindsten, A.J. Ross, G.R. MacGregor, and C.B. Thompson. 2001. BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev. 15:1481-1486.