Loss of the pro-apoptotic BH3-only Bcl-2 family member Bim sustains B lymphopoiesis in the absence of IL-7

International Immunology

Volumn 21, Issue 6, 2009, Pages 715-725

  Huntington, Nicholas D ^a,b   Labi, Verena ^c   Cumano, Ana ^a,b   Vieira, Paulo ^a,b   Strasser, Andreas ^d   Villunger, Andreas ^c   Di Santo, James P ^a,b   Alves, Nuno L ^a,b  

^a INSTITUT PASTEUR   (France)

^b INSTITUT PASTEUR   (France)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

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

Author keywords

B lymphopoiesis; Bim; IL 7; Puma

Indexed keywords

BH3 PROTEIN; BIM PROTEIN; IMMUNOGLOBULIN D; IMMUNOGLOBULIN M; INTERLEUKIN 7; PUMA PROTEIN;

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELL MATURATION; CELL SELECTION; CELL SURVIVAL; CONTROLLED STUDY; FLOW CYTOMETRY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; IMMUNOGLOBULIN BLOOD LEVEL; IN VITRO STUDY; LYMPHOCYTE COUNT; LYMPHOPOIESIS; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; SPLEEN;

ADOPTIVE TRANSFER; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; B-LYMPHOCYTES; BONE MARROW; CELL PROLIFERATION; DNA-BINDING PROTEINS; HEMATOPOIETIC STEM CELLS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INTERLEUKIN-7; LYMPHOPOIESIS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS; TUMOR SUPPRESSOR PROTEINS;

EID: 66249096306     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxp043     Document Type: Article

References (41)

1. Strasser, A. 2005. The role of BH3-only proteins in the immune system. Nat. Rev. Immunol. 5:189.
2. von Freeden-Jeffry, U., Vieira, P., Lucian, L. A., McNeil, T., Burdach, S. E. and Murray, R. 1995. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J. Exp. Med. 181:1519.
3. Alves, N. L., Arosa, F. A. and van Lier, R. A. 2007. Common gamma chain cytokines: Dissidence in the details. Immunol. Lett. 108:113.
4. Nutt, S. L. and Kee, B. L. 2007. The transcriptional regulation of B cell lineage commitment. Immunity 26:715.
5. Alves, N. L., van Lier, R. A. and Eldering, E. 2007. Withdrawal symptoms on display: Bcl-2 members under investigation. Trends Immunol. 28:26.
6. Opferman, J. T., Letai, A., Beard, C., Sorcinelli, M. D., Ong, C. C. and Korsmeyer, S. J. 2003. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 426:671.
7. Alves, N. L., Derks, I. A., Berk, E., Spijker, R., van Lier, R. A. and Eldering, E. 2006. The Noxa/Mcl-1 axis regulates susceptibility to apoptosis under glucose limitation in dividing T cells. Immunity 24:703.
8. You, H., Pellegrini, M., Tsuchihara, K. et al. 2006. FOXO3a-dependent regulation of Puma in response to cytokine/growth factor withdrawal. J. Exp. Med. 203:1657.
9. Maurer, U., Charvet, C., Wagman, A. S., Dejardin, E. and Green, D. R. 2006. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol. Cell 21:749.
10. Bauer, A., Villunger, A., Labi, V. et al. 2006. The NF-kappaB regulator Bcl-3 and the BH3-only proteins Bim and Puma control the death of activated T cells. Proc. Natl Acad. Sci. USA 103:10979.
11. Enders, A., Bouillet, P., Puthalakath, H., Xu, Y., Tarlinton, D. M. and Strasser, A. 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.
12. Bouillet, P., Metcalf, D., Huang, D. C. et al. 1999. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286:1735.
13. Erlacher, M., Labi, V., Manzl, C. et al. 2006. Puma cooperates with Bim, the rate-limiting BH3-only protein in cell death during lymphocyte development, in apoptosis induction. J. Exp. Med. 203:2939.
14. Oliver, P. M., Wang, M., Zhu, Y., White, J., Kappler, J. and Marrack, P. 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.
15. Pellegrini, M., Bouillet, P., Robati, M., Belz, G. T., Davey, G. M. and Strasser, A. 2004. Loss of Bim increases T cell production and function in interleukin 7 receptor-deficient mice. J. Exp. Med. 200:1189.
16. Dias, S., Silva, H., Jr, Cumano, A. and Vieira, P. 2005. Interleukin-7 is necessary to maintain the B cell potential in common lymphoid progenitors. J. Exp. Med. 201:971.
17. Espina, B., Liang, M., Russell, R. G. and Hulley, P. A. 2008. Regulation of bim in glucocorticoid-mediated osteoblast apoptosis. J. Cell. Physiol. 215:488.
18. Liang, M., Russell, G. and Hulley, P. A. 2008. Bim, Bak, and Bax regulate osteoblast survival. J. Bone Miner. Res. 23:610.
19. Kawamura, N., Kugimiya, F., Oshima, Y. et al. 2007. Akt1 in osteoblasts and osteoclasts controls bone remodeling. PLoS ONE 2:e1058.
20. Jeffers, J. R., Parganas, E., Lee, Y. et al. 2003. Puma is an essential mediator of p53-dependent and -independent apoptotic pathways. Cancer Cell 4:321.
21. Colucci, F., Soudais, C., Rosmaraki, E., Vanes, L., Tybulewicz, V. L. and Di Santo, J. P. 1999. Dissecting NK cell development using a novel alymphoid mouse model: Investigating the role of the c-abl proto-oncogene in murine NK cell differentiation. J. Immunol. 162:2761.
22. Vosshenrich, C. A., Ranson, T., Samson, S. I. et al. 2005. Roles for common cytokine receptor gamma-chain-dependent cytokines in the generation, differentiation, and maturation of NK cell precursors and peripheral NK cells in vivo. J. Immunol. 174:1213.
23. Villunger, A., Michalak, E. M., Coultas, L. et al. 2003. p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 302:1036.
24. Huntington, N. D., Xu, Y., Puthalakath, H. et al. 2006. CD45 links the B cell receptor with cell survival and is required for the persistence of germinal centers. Nat. Immunol. 7:190.
25. Liu, A., Vosshenrich, C. A., Lagresle-Peyrou, C. et al. 2006. Competition within the early B-cell compartment conditions B-cell reconstitution after hematopoietic stem cell transplantation in nonirradiated recipients. Blood 108:1123.
26. DiSanto, J. P., Muller, W., Guy-Grand, D., Fischer, A. and Rajewsky, K. 1995. Lymphoid development in mice with a targeted deletion of the interleukin 2 receptor gamma chain. Proc. Natl Acad. Sci. USA 92:377.
27. Cao, X., Shores, E. W., Hu-Li, J. et al. 1995. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity 2:223.
28. Ekoff, M., Kaufmann, T., Engstrom, M. et al. 2007. The BH3-only protein Puma plays an essential role in cytokine deprivation induced apoptosis of mast cells. Blood 110:3209.
29. Vosshenrich, C. A., Cumano, A., Muller, W., Di Santo, J. P. and Vieira, P. 2003. Thymic stromal-derived lymphopoietin distinguishes fetal from adult B cell development. Nat. Immunol. 4:773.
30. Sitnicka, E., Bryder, D., Theilgaard-Monch, K., Buza-Vidas, N., Adolfsson, J. and Jacobsen, S. E. 2002. Key role of flt3 ligand in regulation of the common lymphoid progenitor but not in maintenance of the hematopoietic stem cell pool. Immunity 17:463.
31. Fry, T. J. and Mackall, C. L. 2002. Interleukin-7: From bench to clinic. Blood 99:3892.
32. Chappaz, S., Flueck, L., Farr, A. G., Rolink, A. G. and Finke, D. 2007. Increased TSLP availability restores T- and B-cell compartments in adult IL-7 deficient mice. Blood 110:3862.
33. Demehri, S., Liu, Z., Lee, J. et al. 2008. Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity. PLoS Biol. 6:e123.
34. Napolitano, L. A., Grant, R. M., Deeks, S. G. et al. 2001. Increased production of IL-7 accompanies HIV-1-mediated T-cell depletion: Implications for T-cell homeostasis. Nat. Med. 7:73.
35. Maraskovsky, E., Peschon, J. J., McKenna, H., Teepe, M. and Strasser, A. 1998. Overexpression of Bcl-2 does not rescue impaired B lymphopoiesis in IL-7 receptor-deficient mice but can enhance survival of mature B cells. Int. Immunol. 10:1367.
36. Stahl, M., Dijkers, P. F., Kops, G. J. et al. 2002. The forkhead transcription factor FoxO regulates transcription of p27Kip1 and Bim in response to IL-2. J. Immunol. 168:5024.
37. Labi, V., Erlacher, M., Kiessling, S. et al. 2008. Loss of the BH3-only protein Bmf impairs B cell homeostasis and accelerates gamma irradiation-induced thymic lymphoma development. J. Exp. Med. 205:641.
38. Schneider, P. 2005. The role of APRIL and BAFF in lymphocyte activation. Curr. Opin. Immunol. 17:282.
39. Stadanlick, J. E. and Cancro, M. P. 2008. BAFF and the plasticity of peripheral B cell tolerance. Curr. Opin. Immunol. 20:158.
40. Carvalho, T. L., Mota-Santos, T., Cumano, A., Demengeot, J. and Vieira, P. 2001. Arrested B lymphopoiesis and persistence of activated B cells in adult interleukin 7(-/)- mice. J. Exp. Med. 194:1141.
41. Craxton, A., Draves, K. E., Gruppi, A. and Clark, E. A. 2005. BAFF regulates B cell survival by downregulating the BH3-only family member Bim via the ERK pathway. J. Exp. Med. 202:1363.