Loss of Bim allows precursor B cell survival but not precursor B cell differentiation in the absence of interleukin 7

Journal of Experimental Medicine

Volumn 200, Issue 9, 2004, Pages 1179-1187

  Oliver, Paula M ^a   Wang, Michael ^b   Zhu, Yanan ^b   White, Janice ^a   Kappler, John ^a,b   Marrack, Philippa ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

B cell development; B cell survival; Bcl 2 family; Bim; IL 7

Indexed keywords

BIM PROTEIN; CYTOKINE; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR; PROTEIN BCL 2;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; BONE MARROW CELL; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; HETEROZYGOSITY; LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; STROMA CELL;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; B-LYMPHOCYTES; BONE MARROW CELLS; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL SURVIVAL; DNA, COMPLEMENTARY; FLOW CYTOMETRY; FLUORESCEINS; INTERLEUKIN-7; MEMBRANE PROTEINS; MICE; MICE, MUTANT STRAINS; PROTO-ONCOGENE PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUCCINIMIDES;

EID: 8644247631     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20041129     Document Type: Article

References (47)

1. Li, Y.-S., R. Wasserman, K. Hayakawa, and R.R. Hardy 1996. Identification of the earliest B lineage stage in the mouse bone marrow. Immunity. 5:527-535.
2. Tudor, K.S., K.J. Payne, K. Yamashita, and P.W. Kincade 2000. Functional assessment of precursors from murine bone marrow suggests a sequence of early B lineage differentiation events. Immunity. 12:335-345.
3. Hardy, R.R., C.E. Carmack, S.A. Shinton, J.D. Kemp, and K. Kayakawa. 1991. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J. Exp. Med. 173:1213-1225.
4. Allman, D., and J.P. Miller. 2003. Common lymphoid progenitors, early B-lineage precursors, and IL-7: characterizing the trophic and instructive signals underlying early B cell development. Immunol. Res. 27:131-140.
5. Fleming, H.E., and C.J. Paige. 2002. Cooperation between IL-7 and the pre-B cell receptor: a key to B cell selection. Semin. Immunol. 14:423-430.
6. Cumano, A., B.L. Kee, D.A. Ramsden, A. Marshall, C.J. Paige, and G.E. Wu. 1994. Development of B lymphocytes from lymphoid committed and uncommitted progenitors. Immunol. Rev. 137:5-33.
7. Kee, B.L., and C.J. Paige. 1996. In vitro tracking of IL-7 responsiveness and gene expression during commitment of bipotent B-cell/macrophage progenitors. Curr. Biol. 6:1159-1169.
8. Rolink, A., T. Winkler, F. Melchers, and J. Andersson. 2000. Precursor B cell receptor-dependent B cell proliferation and differentiation does not require the bone marrow or fetal liver environment. J. Exp. Med. 191:23-29.
9. Von Freeden-Jeffry, U., P. Vieira, L.A. Lucian, T. McNeil, S.E. Burdach, and R. Murray. 1995. Lymphopenia in IL-7 gene-deleted mice identifies IL-7 as a nonredundent cytokine. J. Exp. Med. 181:1519-1526.
10. Peschon, J.J., P.J. Morrissey, K.H. Grabstein, F.J. Ramsdell, E. Maraskovsky, B.C. Gliniak, L.S. Park, S.F. Ziegler, D.E. Williams, C.B. Ware, et al. 1994. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J. Exp. Med. 180:1955-1960.
11. Cao, X., E.W. Shores, J. Hu-Li, M.R. Anver, B.L. Kelsall, S.M. Russell, J. Drago, M. Noguchi, A. Grinberg, E.T. Bloom, et al. 1995. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity. 2:223-238.
12. Nosaka, T., J.M. van Deursen, R.A. Tripp, W.E. Thierfelder, B.A. Witthuhn, A.P. McMickle, P.C. Doherty, G.C. Grosveld, and J.N. Ihle. 1995. Defective lymphoid development in mice lacking Jak3. Science. 270:800-802.
13. Miller J.P., D. Izon, W. DeMuth, R. Gerstein, A. Bhandoola, and D. Allman. 2002. The earliest step in B lineage differentiation from common lymphoid progenitors is critically dependent upon interleukin 7. J. Exp. Med. 196:705-711.
14. Corcoran, A.E., P.M. Smart, R.J. Cowling, T. Crompton, M.J. Owen, and A.R. Venkitaraman. 1996. The interleukin-7 receptor alpha chain transmits distinct signals for proliferation and differentiation during B lymphopoiesis. EMBO J. 15:1924-1932.
15. Wei, C., R. Zeff, and I. Goldschneider. 2000. Murine pro-B cells require IL-7 and its receptor complex to up-regulate IL-7R alpha, terminal deoxynucleotidyltransferase, and c mu expression. J. Immunol. 164:1961-1970.
16. Ben-Yehuda, A., E. Wirtheim, A. Abdul-Hai, R. Or, S. Slavin, S. Babaey, and G. Friedman. 1999. Activation of the recombination activating gene 1 (RAG-1) transcript in bone marrow of senescent C57BL/6 mice by recombinant interleukin-7. J. Gerontol. A Biol. Sci. Med. Sci. 54:B143-B148.
17. Corcoran, A.E., A. Riddell, D. Krooshoop, and A.R. Venkitaraman. 1998. Impaired immunoglobulin gene rearrangement in mice lacking the IL-7 receptor. Nature. 391:904-905.
18. Billips, L.G., C.A. Nunez, F.E. Bertrand III, A.K. Stankovic, G.L. Gartland, P.D. Burrows, and MD. Cooper. 1995. Immunoglobulin recombinase gene activity is modulated reciprocally by interleukin 7 and CD19 in B cell progenitors. J. Exp. Med. 182:973-978.
19. Mackay, F., P. Schneider, P. Rennert, and J. Browning. 2003. BAFF and APRIL: a tutorial on B cell survival. Annu. Rev. Immunol. 21:231-264.
20. Vosshenrich, C.A., A. Cumano, W. Muller, J.P. Di Santo, and P. Vieira. 2003. Thymic stromal-derived lymphopoietin distinguishes fetal from adult B cell development. Nat. Immunol. 4:773-779.
21. Park, L.S., U. Martin, K. Garka, B. Gliniak, J.P. Di Santo, W. Muller, D.A. Largaespada, N.G. Copeland, N.A. Jenkins, A.G. Farr, et al. 2002. Cloning of the murine thymic stromal lymphopoietin (TSLP) receptor: formation of a functional heteromeric complex requires interleukin 7 receptor. J. Exp. Med. 192:659-670.
22. Carpino, N., W.E. Thierfelder, M.S. Chang, C. Saris, S.J. Turner, S.F. Ziegler, and J.N. Ihle. 2004. Absence of an essential role for thymic stromal lymphopoietin receptor in murine B-cell development. Mol. Cell. Biol. 24:2584-2592.
23. Sitnicka, E., C. Brakebusch, I.L. Martensson, M. Svensson, W.W. Agace, M. Sigvardsson, N. Buza-Vidas, D. Bryder, C.M. Cilio, H. Ahlenius, et al. 2003. Complementary signaling through flt3 and interleukin-7 receptor α is indispensable for fetal and adult B cell genesis. J. Exp. Med. 198:1495-1506.
24. Ray, R.J., C.J. Paige, C. Furlonger, S.D. Lyman, and R. Rottapel. 1996. Flt3 ligand supports the differentiation of early B cell progenitors in the presence of interleukin-11 and interleukin-7. Eur. J. Immunol. 26:1504-1510.
25. Hirayama, F., S.D. Lyman, S.C. Clark, and M. Ogawa. 1995. The flt3 ligand supports proliferation of lymphohematopoietic progenitors and early B-lymphoid progenitors. Blood. 85:1762-1768.
26. Marshall A.J., H.E. Fleming, G.E. Wu, and C.J. Paige. 1998. Modulation of the IL-7 dose-response threshold during pro-B cell differentiation is dependent on pre-B cell receptor expression. J. Immunol. 161:6038-6045.
27. Fleming, H.E., and C.J. Paige. 2001. Pre-B cell receptor signaling mediates selective response to IL-7 at the pro-B to pre-B cell transition via an ERK/MAP kinase-dependent pathway. Immunity. 15:521-531.
28. Fang, W., D.L. Mueller, C.A. Pennell, J.J. Rivard, Y.S. Li, R.R. Hardy, M.S. Schlissel, and T.W. Behrens. 1996. Frequent aberrant immunoglobulin gene rearrangements in pro-B cells revealed by a bcl-xL transgene. Immunity. 4:291-299.
29. McDonnell, T.J., N. Deane, P.M. Platt, G. Nunez, U. Jaeger, J.P. McKearn, and S.J. Korsmeyer. 1989. Bcl-2-immunoglobulin transgenic mice demonstrate extended B cell survival and follicular lymphoproliferation. Cell. 57:79-88.
30. 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.
31. 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.
32. Von Freeden-Jefrry, U., P. Vieira, L.A. Lucian, T. McNeil, S.E. Burdach, and R. Murray. 1995. Lymphopenia in IL-7 gene deleted mice identifies IL-7 as a nonredundent cytokine. J. Exp. Med. 181:1519-1526.
33. Hasbold, J., A.V. Gett, J.S. Rush, E. Deenick, D. Avery, J. Jun, and P.D. Hodgkin. 1999. Quantitative analysis of lymphocyte differentiation and proliferation in vitro using carboxyfluorescein diacetate succinimidyl ester. Immunol. Cell Biol. 77:516-522.
34. Benschop, R.J., E. Brandl, A.C. Chan, and J.C. Cambier. 2001. Unique signaling properties of B cell antigen receptor in mature and immature B cells: implications for tolerance and activation. J. Immunol. 167:4172-4179.
35. Overbergh, L., D. Valckx, M. Waer, and C. Mathieu. 1999. Quantification of murine cytokine mRNAs using real time quantitative reverse transcriptase PCR. Cytokine. 11:305-312.
36. 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.
37. Tudor, K.S., K.J. Payne, Y. Yamashita, and P.W. Kincade. 2000. Functional assessment of precursors from murine bone marrow suggests a sequence of early B lineage differentiation events. Immunity. 12:335-345.
38. Loffert, D., S. Schaal, A. Ehlich, R.R. Hardy, Y.-R. Zou, W. Muller, and K. Rajewsky. 1994. Early B-cell development in the mouse: insights from mutations introduced by gene targeting. Immunol. Rev. 137:135-152.
39. Young, F., B. Ardman, Y. Shinkai, R. Lansford, T.K. Blackwell, M. Mendelsohn, A. Rolink, F. Melchers, and F.W. Alt. 1994. Influence of immunoglobulin heavy- and light-chain expression on B-cell differentiation. Genes Dev. 8:1043-1057.
40. Ceredig, R., N. Bosco, P.N. Maye, J. Andersson, and A. Rolink. 2003. In interleukin-7-transgenic mice, increasing B lymphopoiesis increases follicular but not marginal zone B cell numbers. Eur. J. Immunol. 33:2567-2576.
41. Alugupalli, K.R., R.M. Gerstein, J. Chen, E. Szomolanyi-Tsuda, R.T. Woodland, and J.M. Leong. 2003. The resolution of relapsing fever borreliosis requires IgM and is concurrent with expansion of B1b lymphocytes. J. Immunol. 170:3819-3827.
42. Fisher, A.G., C. Burdet, M. LeMeur, D. Haasner, P. Gerber, and R. Ceredig. 1993. Lymphoproliferative disorders in an IL-7 transgenic mouse line. Leukemia. 2:S66-S68.
43. Valenzona, H.O., S. Dhanoa, F.D. Finkelman, and D.G. Osmond. 1998. Exogenous interleukin 7 as a proliferative stimulant of early precursor B cells in mouse bone marrow: efficacy of IL-7 injection, IL-7 infusion and IL-7-anti-IL-7 antibody complexes. Cytokine. 10:404-412.
44. Stephan, R.P., C.R. Reilly, and P.L. Witte. 1998. Impaired ability of bone marrow stromal cells to support B-lymphopoiesis with age. Blood. 91:75-88.
45. Andrew, D., and R. Aspinall. 2002. Age-associated thymic atrophy is linked to a decline in IL-7 production. Exp. Gerontol. 37:455-463.
46. Kamada, S., A. Shimono, Y. Shinto, T. Tsujimura, T. Takahashi, T. Noda, Y. Kitamura, H. Kondoh, and Y. Tsujimoto. 1995. bcl-2 deficiency in mice leads to pleiotropic abnormalities: accelerated lymphoid cell death in thymus and spleen, polycystic kidney, hair hypopigmentation, and distorted small intestine. Cancer Res. 55:354-359.
47. Opferman, J.T., A. Letai, C. Beard, M.D. Sorcinelli, C.C. Ong, and S.J. Korsmeyer. 2003. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature. 426:671-676.