Puma cooperates with Bim, the rate-limiting BH3-only protein in cell death during lymphocyte development, in apoptosis induction

Journal of Experimental Medicine

Volumn 203, Issue 13, 2006, Pages 2939-2951

  Erlacher, Miriam ^a,f   Labi, Verena ^a   Manzl, Claudia ^a   Böck, Günther ^a   Tzankov, Alexandar ^b   Häcker, Georg ^c   Michalak, Ewa ^d,e   Strasser, Andreas ^d   Villunger, Andreas ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b UNIVERSITY OF BASEL   (Switzerland)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

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

^e UNIVERSITY OF MELBOURNE   (Australia)

^f UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BH3 PROTEIN; BIM PROTEIN; CALCIUM; PROTEIN BCL 2; PROTEIN P53; PROTEIN PUMA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOIMMUNITY; CALCIUM TRANSPORT; CARCINOGENESIS; CELL DEATH; CELL MATURATION; CELL PROTECTION; CONTROLLED STUDY; HEMATOPOIETIC CELL; HYPERPLASIA; IMMUNE RESPONSE; LYMPHOCYTE; LYMPHOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEOMICS;

ANIMALS; ANTIGENS, CD; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; AUTOANTIBODIES; B-LYMPHOCYTE SUBSETS; CELL DIFFERENTIATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNE SERA; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; LYMPHOCYTES; LYMPHOMA; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; T-LYMPHOCYTE SUBSETS; TUMOR SUPPRESSOR PROTEINS;

EID: 33845913794     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20061552     Document Type: Article

References (33)

1. Strasser, A. 2005. The role of BH3-only proteins in the immune system. Nat. Rev. Immunol. 5:189-200.
2. 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.
3. 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.
4. Certo, M., G. Moore Vdel, M. Nishino, G. Wei, S. Korsmeyer, S.A. Armstrong, and A. Letai. 2006. Mitochondria primed by death signals determine cellular addiction to antiapoptotic BCL-2 family members. Cancer Cell. 9:351-365.
5. Willis, S.N., and J.M. Adams. 2005. Life in the balance: how BH3-only proteins induce apoptosis. Curr. Opin. Cell Biol. 17:617-625.
6. Bouillet, P., D. Metcalf, D.C.S. Huang, D.M. Tarlinton, T.W.H. Kay, F. Köntgen, 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.
7. 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.
8. 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.
9. 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.
10. 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 pro-apoptotic Bcl-2 family member, Bim. Immunity. 16:759-767.
11. 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.
12. 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.
13. 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.
14. Villunger, A., E.M. Michalak, L. Coultas, F. Mullauer, G. Bock, M.J. Ausserlechner, J.M. Adams, and A. Strasser. 2003. p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science. 302:1036-1038.
15. Erlacher, M., E.M. Michalak, P.N. Kelly, V. Labi, H. Niederegger, L. Coultas, J.M. Adams, A. Strasser, and A. Villunger. 2005. BH3-only proteins Puma and Bim are rate-limiting for gamma-radiation and glucocorticoid-induced apoptosis of lymphoid cells in vivo. Blood. 106:4131-4138 .
16. 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.
17. Godfrey, D.I., and A. Zlotnik. 1993. Control points in early T-cell development. Immunol. Today. 14:547-553.
18. 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.
19. Grillot, D.A.M., R. Merino, and G. Nuñez. 1995. Bcl-xL displays restricted distribution during T cell development and inhibits multiple forms of apoptosis but not clonal deletion in transgenic mice. J. Exp. Med. 182:1973-1983.
20. Bouillet, P., S. Cory, L.-C. Zhang, A. Strasser, and J.M. Adams. 2001. Degenerative disorders caused by Bcl-2 deficiency are prevented by loss of its BH3-only antagonist Bim. Dev. Cell. 1:645-653.
21. O'Reilly, L.A., D.C.S. Huang, and A. Strasser. 1996. The cell death inhibitor Bcl-2 and its homologues influence control of cell cycle entry. EMBO J. 15:6979-6990.
22. Hemann, M.T., J.T. Zilfou, Z. Zhao, D.J. Burgess, G.J. Hannon, and S.W. Lowe. 2004. Suppression of tumorigenesis by the p53 target PUMA. Proc. Natl. Acad. Sci. USA. 101:9333-9338.
23. Egle, A., A.W. Harris, P. Bouillet, and S. Cory. 2004. Bim is a suppressor of Myc-induced mouse B cell leukemia. Proc. Natl. Acad. Sci. USA. 101:6164-6169.
24. Egle, A., A.W. Harris, M.L. Bath, L. O'Reilly, and S. Cory. 2004. VavP-Bcl2 transgenic mice develop follicular lymphoma preceded by germinal center hyperplasia. Blood. 103:2276-2283.
25. Wong, H.K., M. Fricker, A. Wyttenbach, A. Villunger, E.M. Michalak, A. Strasser, and A.M. Tolkovsky. 2005. Mutually exclusive subsets of BH3-only proteins are activated by the p53 and c-Jun N-terminal kinase/c-Jun signaling pathways during cortical neuron apoptosis induced by arsenite. Mol. Cell. Biol. 25:8732-8747.
26. 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.
27. Coultas, L., P. Bouillet, K.L. Loveland, S. Meachem, H. Perlman, J.M. Adams, and A. Strasser. 2005. Concomitant loss of proapoptotic BH3-only Bcl-2 antagonists Bik and Bim arrests spermatogenesis. EMBO J. 24:3963-3973.
28. Haks, M.C., P. Krimpenfort, J.H.N. van den Brakel, and A.M. Kruisbeek. 1999. Pre-TCR signaling and inactivation of p53 induces crucial cell survival pathways in pre-T cells. Immunity. 11:91-101.
29. Oliver, P.M., M. Wang, Y. Zhu, J. White, J. Kappler, and P. Marrack. 2004. Loss of Bim allows precursor B cell survival but not precursor B cell differentiation in the absence of interleukin 7. J. Exp. Med. 200:1179-1187.
30. You, H., M. Pellegrini, K. Tsuchihara, K. Yamamoto, G. Hacker, M. Erlacher, A. Villunger, and T.W. Mak. 2006. FOXO3a-dependent regulation of Puma in response to cytokine/growth factor withdrawal. J. Exp. Med. 203:1657-1663.
31. Stahl, M., P.F. Dijkers, G.J. Kops, S.M. Lens, P.J. Coffer, B.M. Burgering, and R.H. Medema. 2002. The forkhead transcription factor FoxO regulates transcription of p27Kip1 and Bim in response to IL-2. J. Immunol. 168:5024-5031.
32. Marquina, R., M.A. Diez, M. Lopez-Hoyos, L. Buelta, A. Kuroki, S. Kikuchi, J. Villegas, M. Pihlgren, C.A. Siegrist, M. Arias, et al. 2004. Inhibition of B cell death causes the development of an IgA nephropathy in (New Zealand white x C57BL/6)F(1)-bcl-2 transgenic mice. J. Immunol. 172:7177-7185.
33. Labi, V., M. Erlacher, S. Kiessling, and A. Villunger. 2006. BH3-only proteins in cell death initiation, malignant disease and anticancer therapy. Cell Death Differ. 13:1325-1338.