The putative pore-forming domain of Bax regulates mitochondrial localization and interaction with Bcl-X(L)

Molecular and Cellular Biology

Volumn 20, Issue 5, 2000, Pages 1604-1615

  Nouraini, Shahrzad ^a   Six, Emmanuelle ^a   Matsuyama, Shigemi ^b   Krajewski, Stainslaw ^a   Reed, John C ^a  

^a BURNHAM INSTITUTE   (United States)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BAX; PROTEIN BCL 2;

ANIMAL CELL; APOPTOSIS; ARTICLE; CYTOTOXICITY; MAMMAL CELL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN LOCALIZATION; YEAST CELL;

AMINO ACID SEQUENCE; ANIMALS; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; BINDING SITES; BIOLOGICAL TRANSPORT; COS CELLS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2;

EID: 0033956449     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.5.1604-1615.2000     Document Type: Article

References (51)

1. Antonsson, B., F. Conti, A. Ciavatta, S. Montessuit, S. Lewis, I. Martinou, L. Bernasconi, A. Bernard, J.-J. Mermod, G. Mazzei, K. Maundrell, F. Gambale, R. Sadoul, and J.-C. Martinou. 1997. Inhibition of Bax channel-forming activity by Bcl-2. Science 277:370-372.
2. Chou, J., H. Li, G. Salvesen, J. Yuan, and G. Wagner. 1999. Solution structure of BID. an intracellular amplifier of apoptotic signaling. Cell 96:615-624.
3. Cramer, W. A., J. B. Heymann, S. L. Schendel, B. N. Deriy, F. S. Cohen, P. A. Elkins, and C. V. Stauffacher. 1995. Structure-function of the channel-forming colicins. Annu. Rev. Biophys. Biomol. Struct. 24:611-641.
4. Deckwerth, T. L., J. L. Elliott, C. M. Knudson, E. M. Johnson, Jr., W. D. Snider, and S. J. Korsmeyer. 1996. BAX is required for neuronal death after trophic factor deprivation and during development. Neuron 17:401-411.
5. Desagher, S., A. Osen-Sand, A. Nichols, R. Eskes, S. Montessuit, S. Lauper, K. Maundrell, B. Antonsson, and J.-C. Martinou. 1998. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c depletion during apoptosis. J. Cell Biol. 144:891-901.
6. Goping, I., A. Gross, J. Lavoie, M. Nguyen, R. Jemmerson, K. Roth, S. Korsmeyer, and G. Shore. 1998. Regulated targeting of BAX mitochondria. J. Cell Biol. 143:207-215.
7. Green, D., and J. Reed. 1998. Mitochondria and apoptosis. Science 281: 1309-1312.
8. Gross, A., J. Jockel, M. Wei, and S. Korsmeyer. 1998. Enforced dimerization of Bax results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J. 17:3878-3885.
9. Man, J., P. Sabbatini, D. Perez, L. Rao, D. Modha, and E. White. 1996. The E1B 19K protein blocks apoptosis by interacting with and inhibiting the p53-inducible and death-promoting Bax protein. Genes Dev. 10:461-477.
10. Ho, S., H. Hunt, R. Horton, J. Pullen, and L. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
11. L during apoptosis. Proc. Natl. Acad. Sci. USA 94:3668-3672.
12. Hsu, Y. T., and R. J. Youle. 1997. Nonionic detergents induce dimerization among members of the Bcl-2 family. J. Biol. Chem. 272:13829-13834.
13. Jurgensmeier, J., S. Krajewski, R. Armstrong, G. Wilson, T. Oltersdorf, L. Fritz, J. Reed, and S. Ottilie. 1997. Bax-and Bak-induced cell death in the fission yeast Schizosaccharomyces pombe. Mol. Biol. Cell 8:325-339.
14. Jurgensmeier, J. M., Z. Xie, Q. Deveraux, L. Ellerby. D. Bredesen, and J. C. Reed. 1998. Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad. Sci. USA 5:4997-5002.
15. Knudson, C. M., K. S. K. Tung, W. G. Tourtellotte, G. A. J. Brown, and S. J. Korsmeyer. 1995. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science 270:96-99.
16. Krajewski, S., M. Krajewska, A. Shabaik, T. Miyashita, H.-G. Wang, and J. C. Reed. 1994. Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2. Am. J. Pathol. 145:1323-1333.
17. Krajewski, S., M. Krajewska, A. Shabaik, H.-G. Wang, S. Irie, L. Fong, and J. C. Reed. 1994. Immunohistochemical analysis of in vivo patterns of Bcl-X expression. Cancer Res. 54:5501-5507.
18. Krishtalik, L. I., and W. A. Cramer. 1995. On the physical basis for the cis-positive rule describing protein orientation in biological membranes. FEBS Lett. 369:140-143.
19. Lewis, S., S. Bethell, S. Patel, J.-C. Martinou, and B. Antonsson. 1998. Purification and biochemical properties of soluble recombinant human Bax. Protein Expr. Purif. 13:120-126.
20. Li, H., H. Zhu, C. 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.
21. Manon, S., B. Chaudhuri, and M. Buérin. 1997. Release of cytochrome c and decrease of cytochrome c oxidase in Bax-expressing yeast cells, and prevention of these effects by coexpression of Bel-XL. FEBS Lett. 415:29-32.
22. Marzo, I., C. Brenner, N. Zamzami, J. M. Jurgensmeier, S. A. Susin, H. L. A. Vieira, M.-C. Prevost, Z. Xie, S. Matsuyama, J. C. Reed, and G. Kroemer. 1998. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281:2027-2031.
23. Matsuyama, S., S. Schendel, Z. Xie, and J. Reed. 1998. Cytoprotection by Bcl-2 requires the pore-forming α5 and α6 helices. J. Biol. Chem. 273:30995-31001.
24. Matsuyama, S., Q. Xu, J. Velours, and J. C. Reed. 1998. The mitochondrial F0F1-ATPase proton pump is required for function of proapoptotic protein Bax in yeast and mammalian cells. Mol. Cell 1:327-336.
25. McDonnell, J., D. Fushman, C. Milliman, S. Korsmeyer, and D. Cowburn. 1999. Solution structure of the proapoptotic molecule BID: a structural basis for apoptotic agonists and antagonists. Cell 96:625-634.
26. L forms an ion channel in synthetic lipid membranes. Nature 385:353-357.
27. Miyashita, T., S. Krajewski, M. Krajewska, H. G. Wang, H. K. Lin, B. Hoffman, D. Lieberman, and J. C. Reed. 1994. Tumor suppressor p53 is a regulator of BCL-2 and BAX in gene expression in vitro and in vivo. Oncogene 9:1799-1805.
28. Montal, M. 1996. Protein folds in channel structure. Curr. Opin. Struct. Biol. 6:499-510.
29. Narita, M., S. Shimizu, T. Ito, T. Chittenden, R. J. Lutz, H. Matsuda, and Y. Tsujimoto. 1998. Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc. Natl. Acad. Sci. USA 95:14681-14686.
30. Nechushtan, A., C. Smith, Y.-T. Hsu, and R. Youle. 1999. Conformation of the Bax C-terminus regulates subcellular location and cell death. EMBO J. 18:2330-2341.
31. Oltvai, Z., C. Milliman, and S. Korsmeyer. 1993. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74:609-619.
32. Pastorino, J. G., S. T. Chen, M. Tafani, J. W. Snyder, and J. L. Farber. 1998. The overexpression of Bax produces cell death upon induction of the mitochondrial permeability transition. J. Biol. Chem. 273:7770-7775.
33. Reed, J. 1998. Bcl-2 family proteins. Oncogene 17:3225-3236.
34. Sato, T., M. Hanada, S. Bodrug, S. Irie, N. Iwama, L. H. Boise, C. B. Thompson, E. Golemis, L. Fong, H.-G. Wang, and J. C. Reed. 1994. Interactions among members of the Bcl-2 protein family analyzed with a yeast two-hybrid system. Proc. Natl. Acad. Sci. USA 91:9238-9242.
35. Sattler, M., H. Liang, D. Nettesheim, R. P. Meadows, J. E. Harlan, M. Eberstadt, H. S. Yoon, S. B. Shuker, B. S. Chang, A. J. Minn, C. B. Thompson, and S. W. Fesik. 1997. Structure of Bcl-xL-Bak peptide complex: recognition between regulators of apoptosis. Science 275:983-986.
36. Schendel, S., M. Montal, and J. C. Reed. 1998. Bcl-2 family proteins as ion-channels. Cell Death Differ. 5:372-380.
37. 3 only Bcl-2 family member, BID. J. Biol. Chem. 274:21932-21936.
38. Schendel, S. L., Z. Xie, M. O. Montal, S. Matsuyama, M. Montal, and J. C. Reed. 1997. Channel formation by antiapoptotic protein Bcl-2. Proc. Natl. Acad. Sci. USA 94:5113-5118.
39. Schlesinger, P., A. Gross, X.-M. Yin, K. Yamamoto, M. Saito, G. Waksman, and S. Korsmeyer. 1997. Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2. Proc. Natl. Acad. Sci. USA 94:11357-11362.
40. Shimizu, Y., M. Narita, and Y. Tsujimoto. 1999. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399:483-487.
41. Silverman, J. A., J. A. Mindell, A. Finkelstein, W. H. Shen, and R. J. Collier. 1994. Mutational analysis of the helical hairpin region of diphtheria toxin transmembrane domain. J. Biol. Chem. 269:22524-22532.
42. L prevents cell death following growth factor withdrawal by facilitating mitochondrial ATP/ADP exchange. Mol. Cell 3:159-167.
43. Wang, H. G., U. R. Rapp, and J. C. Reed. 1996. Bcl-2 targets the protein kinase Raf-1 to mitochondria. Cell 87:629-638.
44. Wang, K., A. Gross, G. Waksman, and S. J. Korsmeyer. 1998. Mutagenesis of the BH3 domain of Bax identifies critical residues for dimerization and killing. Mol. Cell. Biol. 18:6083-6089.
45. Wang, K., W.-M. Yin, D. T. Chao, C. L. Milliman, and S. J. Korsmeyer. 1996. BID: a novel BH3 domain-only death agonist. Genes Dev. 10:2859-2869.
46. Wolter, K. G., Y. T. Hsu, C. L. Smith, A. Nechushtan, X. G. Xi, and R. J. Youle. 1997. Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 139:1281-1292.
47. Xiang, J., D. T. Chao, and S. J. Korsmeyer. 1996. BAX-induced cell death may not require interleukin 1β-converting enzyme-like proteases. Proc. Natl. Acad. Sci. USA 93:14559-14563.
48. Yin, X. M., Z. N. Oltvai, and S. J. Korsmeyer. 1994. BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369:321-323.
49. Zha, H., C. Aime-Sempe, T. Sato, and J. C. Reed. 1996. Pro-apoptotic protein Bax heterodimerizes with Bcl-2 and homodimerizes with Bax via a novel domain (BH3) distinct from BH1 and BH2. J. Biol. Chem. 271:7440-7444.
50. Zha, H., H. Fisk, M. Yaffe, N. Mahajan, B. Herman, and J. Reed. 1496. Structure-function comparisons of proapoptotic protein Bax in yeast and mammalian cells. Mol. Cell. Biol. 16:6494-6508.
51. Zha, H., and J. C. Reed. 1997. Heterodimerization-independent functions of cell death regulatory proteins Bax and Bcl-2 in yeast and mammalian cells. J. Biol. Chem. 272:31482-31488.