Combined loss of proapoptotic genes Bak or Bax with Bim synergizes to cause defects in hematopoiesis and in thymocyte apoptosis

Journal of Experimental Medicine

Volumn 201, Issue 12, 2005, Pages 1949-1960

  Hutcheson, Jack ^a   Scatizzi, John C ^a   Bickel, Emily ^a   Brown, Nathaniel J ^a   Bouillet, Philippe ^b   Strasser, Andreas ^b   Perlman, Harris ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIM PROTEIN; PROTEIN BAK; PROTEIN BAX;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MARROW CELL; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; GENE INTERACTION; GENE LOSS; HEMATOPOIESIS; KNOCKOUT MOUSE; LYMPHOID CELL; MALOCCLUSION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; THYMOCYTE;

ABNORMALITIES, MULTIPLE; ANIMALS; ANTIGENS, CD; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; BLOOD CELL COUNT; CARRIER PROTEINS; CROSSES, GENETIC; HEMATOPOIESIS; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; LEUKOCYTES; LYMPHOCYTES; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; THYMUS GLAND;

EID: 22344434871     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20041484     Document Type: Article

References (58)

1. Strasser, A., L. O'Connor, and V.M. Dixit. 2000. Apoptosis signaling. Annu. Rev. Biochem. 69:217-245.
2. Adams, J.M., and S. Cory. 1998. The Bcl-2 protein family: arbiters of cell survival. Science. 281:1322-1326.
3. Kroemer, G. 1997. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat. Med. 3:614-620.
4. Opferman, J.T., and S.J. Korsmeyer. 2003. Apoptosis in the development and maintenance of the immune system. Nat. Immunol. 4:410-415.
5. Green, D.R., and J.C. Reed. 1998. Mitochondria and apoptosis. Science. 281:1309-1312.
6. Zamzami, N., C. Brenner, I. Marzo, S.A. Susin, and G. Kroemer. 1998. Subcellular and submitochondrial mode of action of Bcl-2-like oncoproteins. Oncogene. 16:2265-2282.
7. Yang, J., X. Liu, K. Bhalla, C.N. Kim, A.M. Ibrado, J. Cai, T.-I. Peng, D.P. Jones, and X. Wang. 1997. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science. 275:1129-1132.
8. Kluck, R.M., E. Bossy-Wetzel, D.R. Green, and D.D. Newmeyer. 1997. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 275:1132-1136.
9. Kuida, K., T.F. Haydar, C. 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.
10. Rao, L., and E. White. 1997. Bcl-2 and the ICE family of apoptotic regulators: making a connection. Curr. Opin. Genet. Dev. 7:52-58.
11. Perlman, H., C. Georganas, L.J. Pagliari, A.E. Koch, K. Haines, and R.M. Pope. 2000. Bcl-2 expression in synovial fibroblasts is essential for maintaining mitochondrial homeostasis and cell viability. J. Immunol. 164:5227-5235.
12. Harris, M.H., and C.B. Thompson. 2000. The role of the Bcl-2 family in the regulation of outer mitochondrial membrane permeability. Cell Death Differ. 7:1182-1191.
13. Ahsen, O.V., N.J. Waterhouse, T. Kuwana, D.D. Newmeyer, and D.R. Green. 2000. The 'harmless' release of cytochrome c. Cell Death Differ. 7:1192-1199.
14. Rathmell, J.C., T. Lindsten, W.X. Zong, R.M. Cinalli, and C.B. Thompson. 2002. Deficiency in Bak and Bax perturbs thymic selection and lymphoid homeostasis. Nat. Immunol. 3:932-939.
15. 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.
16. 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.
17. 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.
18. Rinkenberger, J.L., S. Horning, B. Klocke, K. Roth, and S.J. Korsmeyer. 2000. Mcl-1 deficiency results in peri-implantation embryonic lethality. Genes Dev. 14:23-27.
19. Motoyama, N., F. Wang, K.A. Roth, H. Sawa, K. Nakayama, K. Nakayama, I. Negishi, S. Senju, Q. Zhang, S. Fujii, and D.Y. Loh. 1995. Massive cell death of immature hematopoietic cells and neurons in Bclx-deficient mice. Science. 267:1506-1510.
20. Knudson, C.M., K.S. Tung, W.G. Tourtellotte, G.A. Brown, and S.J. Korsmeyer. 1995. Bax-deficient mice with lymphoid hyperplasia and male germ cell death. Science. 270:96-99.
21. Brunelle, J.K., M.T. Santore, G.R. Budinger, Y. Tang, T.A. Barrett, W.X. Zong, E. Kandel, B. Keith, M.C. Simon, C.B. Thompson, et al. 2004. c-Myc sensitization to oxygen deprivation-induced cell death is dependent on Bax/Bak, but is independent of p53 and hypoxia-inducible factor-1. J. Biol. Chem. 279:4305-4312.
22. Budinger, G.R., M. Tso, D.S. McClintock, D.A. Dean, J.I. Sznajder, and N.S. Chandel. 2002. Hyperoxia-induced apoptosis does not require mitochondrial reactive oxygen species and is regulated by Bcl-2 proteins. J. Biol. Chem. 277:15654-15660.
23. McClintock, D.S., M.T. Santore, V.Y. Lee, J. Brunelle, G.R. Budinger, W.X. Zong, C.B. Thompson, N. Hay, and N.S. Chandel. 2002. Bcl-2 family members and functional electron transport chain regulate oxygen deprivation-induced cell death. Mol. Cell. Biol. 22:94-104.
24. Kandasamy, K., S.M. Srinivasula, E.S. Alnemri, C.B. Thompson, S.J. Korsmeyer, J.L. Bryant, and R.K. Srivastava. 2003. Involvement of proapoptotic molecules Bax and Bak in tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced mitochondrial disruption and apoptosis: differential regulation of cytochrome c and Smac/DIABLO release. Cancer Res. 63:1712-1721.
25. Scorrano, L., S.A. Oakes, J.T. Opferman, E.H. Cheng, M.D. Sorcinelli, T. Pozzan, and S.J. Korsmeyer. 2003. BAX and BAK regulation of endoplasmic reticulum Ca2+: a control point for apoptosis. Science. 300:135-139.
26. Danial, N.N., and S.J. Korsmeyer. 2004. Cell death: critical control points. Cell. 116:205-219.
27. Huang, D.C., and A. Strasser. 2000. BH3-only proteins - essential initiators of apoptotic cell death. Cell. 103:839-842.
28. Krajewski, S., M. Krajewska, and J.C. Reed. 1996. Immunohistochemical analysis of in vivo patterns of Bak expression, a proapoptotic member of the Bcl-2 protein family. Cancer Res. 56:2849-2855.
29. Krajewski, S., M. Krajewska, A. Shabaik, T. Miyashita, H. Wang, and J. Reed. 1994. Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2. Am. J. Pathol. 145:1323-1336.
30. O'Reilly, L.A., L. Cullen, J. Visvader, G.J. Lindeman, C. Print, M.L. Bath, D.C. Huang, and A. Strasser. 2000. The proapoptotic BH3-only protein bim is expressed in hematopoietic, epithelial, neuronal, and germ cells. Am. J. Pathol. 157:449-461.
31. Bouillet, P., J.F. Purton, D.I. Godfrey, L.C. Zhang, L. Coultas, H. Puthalakath, M. Pellegrini, S. Cory, J.M. Adams, and A. Strasser. 2002. BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes. Nature. 415:922-926.
32. Enders, A., P. Bouillet, H. Puthalakath, Y. Xu, D.M. Tarlinton, and A. Strasser. 2003. Loss of the pro-apoptotic BH3-only Bcl-2 family member Bim inhibits BCR stimulation-induced apoptosis and deletion of autoreactive B cells. J. Exp. Med. 198:1119-1126.
33. Villunger, A., V.S. Marsden, Y. Zhan, M. Erlacher, A.M. Lew, P. Bouillet, S. Berzins, D.I. Godfrey, W.R. Heath, and A. Strasser. 2004. Negative selection of semimature CD4+8-HSA+ thymocytes requires the BH3-only protein Bim but is independent of death receptor signaling. Proc. Natl. Acad. Sci. USA. 101:7052-7057.
34. Pellegrini, M., G. Belz, P. Bouillet, and A. Strasser. 2003. Shutdown of an acute T cell immune response to viral infection is mediated by the proapoptotic Bcl-2 homology 3-only protein Bim. Proc. Natl. Acad. Sci. USA. 100:14175-14180.
35. Hildeman, D.A., Y. Zhu, T.C. Mitchell, P. Bouillet, A. Strasser, J. Kappler, and P. Marrack. 2002. Activated T cell death in vivo mediated by proapoptotic bcl-2 family member bim. Immunity. 16:759-767.
36. Bouillet, P., D. Metcalf, D.C. Huang, D.M. Tarlinton, T.W. Kay, F. Kontgen, J.M. Adams, and A. Strasser. 1999. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science. 286:1735-1738.
37. Villunger, A., C. Scott, P. Bouillet, and A. Strasser. 2003. Essential role for the BH3-only protein Bim but redundant roles for Bax, Bcl-2, and Bcl-w in the control of granulocyte survival. Blood. 101:2393-2400.
38. Davey, G.M., C. Kurts, J.F. Miller, P. Bouillet, A. Strasser, A.G. Brooks, F.R. Carbone, and W.R. Heath. 2002. Peripheral deletion of autoreactive CD8 T cells by cross presentation of self-antigen occurs by a Bcl-2-inhibitable pathway mediated by Bim. J. Exp. Med. 196:947-955.
39. Bouillet, P., S. Cory, L.C. Zhang, A. Strasser, and J.M. Adams. 2001. Degenerative disorders caused by Bcl-2 deficiency prevented by loss of its BH3-only antagonist Bim. Dev. Cell. 1:645-653.
40. Coultas, L., P. Bouillet, E.G. Stanley, T.C. Brodnicki, J.M. Adams, and A. Strasser. 2004. Proapoptotic BH3-only Bcl-2 family member Bik/Blk/Nbk is expressed in hemopoietic and endothelial cells but is redundant for their programmed death. Mol. Cell. Biol. 24:1570-1581.
41. Knudson, C.M., and S.J. Korsmeyer. 1997. Bcl-2 and Bax function independently to regulate cell death. Nat. Genet. 16:358-363.
42. Akiyama, T., P. Bouillet, T. Miyazaki, Y. Kadono, H. Chikuda, U.I. Chung, A. Fukuda, A. Hikita, H. Seto, T. Okada, et al. 2003. Regulation of osteoclast apoptosis by ubiquitylation of proapoptotic BH3-only Bcl-2 family member Bim. EMBO J. 22:6653-6664.
43. Green, D.R., and G. Kroemer. 2004. The pathophysiology of mitochondrial cell death. Science. 305:626-629.
44. 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.
45. Li, P., D. Nijhawan, I. Budihardjo, S.M. Srinivasula, M. Ahmad, E.S. Alnemri, and X. Wang. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 91:479-489.
46. Oakes, S.A., J.T. Opferman, T. Pozzan, S.J. Korsmeyer, and L. Scorrano. 2003. Regulation of endoplasmic reticulum Ca2+ dynamics by proapoptotic BCL-2 family members. Biochem. Pharmacol. 66:1335-1340.
47. Villunger, A., E.M. Michalak, L. Coultas, F. Mullauer, G. Bock, M.J. Ausserlechner, J.M. Adams, and A. Strasser. 2003. p53- and druginduced apoptotic responses mediated by BH3-only proteins puma and noxa. Science. 302:1036-1038.
48. Jeffers, J.R., E. Parganas, Y. Lee, C. Yang, J. Wang, J. Brennan, K.H. MacLean, J. Han, T. Chittenden, J.N. Ihle, et al. 2003. Puma is an essential mediator of p53-dependent and -independent apoptotic pathways. Cancer Cell. 4:321-328.
49. Shibue, T., K. Takeda, E. Oda, H. Tanaka, H. Murasawa, A. Takaoka, Y. Morishita, S. Akira, T. Taniguchi, and N. Tanaka. 2003. Integral role of Noxa in p53-mediated apoptotic response. Genes Dev. 17:2233-2238.
50. Takai, Y., J. Canning, G.I. Perez, J.K. Pru, J.J. Schlezinger, D.H. Sherr, R.N. Kolesnick, J. Yuan, R.A. Flavell, S.J. Korsmeyer, and J.L. Tilly. 2003. Bax, caspase-2, and caspase-3 are required for ovarian follicle loss caused by 4-vinylcyclohexene diepoxide exposure of female mice in vivo. Endocrinology. 144:69-74.
51. Kuida, K., T.S. Zheng, S. Na, C.-Y. Kuan, H. Karasuyama, P. Rakic, and R.A. Flavell. 1996. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature. 384:368-372.
52. Seo, S.Y., Y.B. Chen, I. Ivanovska, A.M. Ranger, S.J. Hong, V.L. Dawson, S.J. Korsmeyer, D.S. Bellows, Y. Fannjiang, and J.M. Hardwick. 2004. BAD is a pro-survival factor prior to activation of its proapoptotic function. J. Biol. Chem. 279:42240-42249.
53. Fannjiang, Y., C.H. Kim, R.L. Huganir, S. Zou, T. Lindsten, C.B. Thompson, T. Mito, R.J. Traystman, T. Larsen, D.E. Griffin, et al. 2003. BAK alters neuronal excitability and can switch from anti- to pro-death function during postnatal development. Dev. Cell. 4:575-585.
54. Strasser, A. 2005. The role of BH3-only proteins in the immune system. Nat. Rev. Immunol. 5:189-200.
55. Strasser, A., and M. Pellegrini. 2004. T-lymphocyte death during shutdown of an immune response. Trends Immunol. 25:610-615.
56. Ogilvy, S., D. Metcalf, C.G. Print, M.L. Bath, A.W. Harris, and J.M. Adams. 1999. Constitutive Bcl-2 expression throughout the hematopoietic compartment affects multiple lineages and enhances progenitor cell survival. Proc. Natl. Acad. Sci. USA. 96:14943-14948.
57. Chen, L., S.N. Willis, A. Wei, B.J. Smith, J.I. Fletcher, M.G. Hinds, P.M. Colman, C.L. Day, J.M. Adams, and D.C. Huang. 2005. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol. Cell. 17:393-403.
58. Kuwana, T., L. Bouchier-Hayes, J.E. Chipuk, C. Bonzon, B.A. Sullivan, D.R. Green, and D.D. Newmeyer. 2005. BH3 Domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol. Cell. 17:525-535.