Control of peripheral B-cell development

Current Opinion in Immunology

Volumn 19, Issue 2, 2007, Pages 143-149

  Casola, Stefano ^a  

^a FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; B CELL ACTIVATING FACTOR; B LYMPHOCYTE RECEPTOR; CD19 ANTIGEN; CD28 ANTIGEN; CD79A ANTIGEN; CELL SURFACE RECEPTOR; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; CYTOKINE; FLT3 LIGAND; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN HEAVY CHAIN; IMMUNOGLOBULIN J CHAIN; LYMPHOCYTE ANTIGEN RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; PROTEIN BCL 10; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BLNK; PROTEIN MCL 1; PROTEIN P100; PROTEIN P52; SYNDECAN 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CIITA; TRANSCRIPTION FACTOR PRDM1; UNCLASSIFIED DRUG;

ANTIGEN RECOGNITION; APOPTOSIS; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL COMPARTMENTALIZATION; CELL FATE; CELL LINEAGE; IMMUNE RESPONSE; IMMUNOSTIMULATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE SUBPOPULATION; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; SYSTEMATIC REVIEW; TRANSCRIPTION REGULATION;

ANIMALS; B-CELL ACTIVATION FACTOR RECEPTOR; B-LYMPHOCYTE SUBSETS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LYMPHOPOIESIS; MICE; RECEPTORS, ANTIGEN, B-CELL; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 33847669211     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coi.2007.02.010     Document Type: Review

References (51)

1. hi splenic B cells are an immature developmental intermediate in the production of long-lived marrow-derived B cells. J Immunol 151 (1993) 4431-4444
2. Rajewsky K. Clonal selection and learning in the antibody system. Nature 381 (1996) 751-758
3. Lopes-Carvalho T., and Kearney J.F. Development and selection of marginal zone B cells. Immunol Rev 197 (2004) 192-205
4. Hardy R.R. B-1 B cell development. J Immunol 177 (2006) 2749-2754
5. Gu H., Tarlinton D., Muller W., Rajewsky K., and Forster I. Most peripheral B cells in mice are ligand selected. J Exp Med 173 (1991) 1357-1371
6. Levine M.H., Haberman A.M., Sant'Angelo D.B., Hannum L.G., Cancro M.P., Janeway Jr. C.A., and Shlomchik M.J. A B-cell receptor-specific selection step governs immature to mature B cell differentiation. Proc Natl Acad Sci USA 97 (2000) 2743-2748
7. Hayakawa K., Asano M., Shinton S.A., Gui M., Allman D., Stewart C.L., Silver J., and Hardy R.R. Positive selection of natural autoreactive B cells. Science 285 (1999) 113-116
8. Wen L., Brill-Dashoff J., Shinton S.A., Asano M., Hardy R.R., and Hayakawa K. Evidence of marginal-zone B cell-positive selection in spleen. Immunity 23 (2005) 297-308. Using an anti-Thy-1 BCR transgenic system, this study shows that MZ B cells are generated from transitional cells in response to BCR-mediated antigen recognition. The amount of antigen required for MZ B-cell differentiation was significantly lower than that promoting the generation of B-1 cells from the same precursors. In the absence of soluble antigen, immature B cells gave rise to FO B cells. These data support a model in which strong BCR signals give rise to B-1 cells, intermediate signals drive MZ B-cell development, whereas weak signals are compatible with FO B-cell differentiation. This study also shows that surface markers associated with MZ B-cell development can be induced in vitro in transgenic immature B cells as long as a combination of self-antigen, BAFF and Notch-2 signals are provided to the cells, thus identifying the minimal requirements to initiate MZ B-cell differentiation.
9. Pillai S., Cariappa A., and Moran S.T. Positive selection and lineage commitment during peripheral B-lymphocyte development. Immunol Rev 197 (2004) 206-218
10. Casola S., Otipoby K.L., Alimzhanov M., Humme S., Uyttersprot N., Kutok J.L., Carroll M.C., and Rajewsky K. B cell receptor signal strength determines B cell fate. Nat Immunol 5 (2004) 317-327
11. Heltemes L.M., and Manser T. Level of B cell antigen receptor surface expression influences both positive and negative selection of B cells during primary development. J Immunol 169 (2002) 1283-1292
12. ••], this study demonstrates, through a series of transplantation assays, that B-1 and B-2 B-cell progenitors can be distinguished from each other on the basis of the expression of a restricted number of surface markers (including CD19 and CD45R). Studies in vitro have also shown that the two progenitor B cells have a different response to thymic stromal lymphopoietin and IL-7. Finally, evidence is provided for the emergence of the two B-1 subsets (B1-a and B1-b) at different times during ontogeny, with B1-a appearing earlier.
13. + progeny. By contrast, B-2 progenitors express CD138 and I-A from the stage at which progenitors undergo Ig rearrangements.
14. Norvell A., Mandik L., and Monroe J.G. Engagement of the antigen-receptor on immature murine B lymphocytes results in death by apoptosis. J Immunol 154 (1995) 4404-4413
15. Karnell F.G., Brezski R.J., King L.B., Silverman M.A., and Monroe J.G. Membrane cholesterol content accounts for developmental differences in surface B cell receptor compartmentalization and signaling. J Biol Chem 280 (2005) 25621-25628
16. Pierce S.K. Lipid rafts and B-cell activation. Nat Rev Immunol 2 (2002) 96-105
17. Sproul T.W., Malapati S., Kim J., and Pierce S.K. Cutting edge: B cell antigen receptor signaling occurs outside lipid rafts in immature B cells. J Immunol 165 (2000) 6020-6023
18. Kraus M., Alimzhanov M.B., Rajewsky N., and Rajewsky K. Survival of resting mature B lymphocytes depends on BCR signaling via the Igα/β heterodimer. Cell 117 (2004) 787-800
19. Lam K.P., Kuhn R., and Rajewsky K. In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell 90 (1997) 1073-1083
20. Vigorito E., Gambardella L., Colucci F., McAdam S., and Turner M. Vav proteins regulate peripheral B-cell survival. Blood 106 (2005) 2391-2398
21. Ng L.G., Mackay C.R., and Mackay F. The BAFF/APRIL system: life beyond B lymphocytes. Mol Immunol 42 (2005) 763-772
22. Schiemann B., Gommerman J.L., Vora K., Cachero T.G., Shulga-Morskaya S., Dobles M., Frew E., and Scott M.L. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293 (2001) 2111-2114
23. Sasaki Y., Casola S., Kutok J.L., Rajewsky K., and Schmidt-Supprian M. TNF family member B cell-activating factor (BAFF) receptor-dependent and -independent roles for BAFF in B cell physiology. J Immunol 173 (2004) 2245-2252
24. Woodland R.T., Schmidt M.R., and Thompson C.B. BLyS and B cell homeostasis. Semin Immunol 18 (2006) 318-326
25. Siebenlist U., Brown K., and Claudio E. Control of lymphocyte development by nuclear factor-κB. Nat Rev Immunol 5 (2005) 435-445
26. Hatada E.N., Do R.K., Orlofsky A., Liou H.C., Prystowsky M., MacLennan I.C., Caamano J., and Chen-Kiang S. NF-κB1 p50 is required for BLyS attenuation of apoptosis but dispensable for processing of NF-κB2 p100 to p52 in quiescent mature B cells. J Immunol 171 (2003) 761-768
27. Jun J.E., Wilson L.E., Vinuesa C.G., Lesage S., Blery M., Miosge L.A., Cook M.C., Kucharska E.M., Hara H., Penninger J.M., et al. Identifying the MAGUK protein Carma-1 as a central regulator of humoral immune responses and atopy by genome-wide mouse mutagenesis. Immunity 18 (2003) 751-762
28. Ruland J., Duncan G.S., Elia A., del Barco Barrantes I., Nguyen L., Plyte S., Millar D.G., Bouchard D., Wakeham A., Ohashi P.S., et al. Bcl10 is a positive regulator of antigen receptor-induced activation of NF-κB and neural tube closure. Cell 104 (2001) 33-42
29. Ruland J., Duncan G.S., Wakeham A., and Mak T.W. Differential requirement for Malt1 in T and B cell antigen receptor signaling. Immunity 19 (2003) 749-758
30. Ruefli-Brasse A.A., French D.M., and Dixit V.M. Regulation of NF-κB-dependent lymphocyte activation and development by paracaspase. Science 302 (2003) 1581-1584
31. Pasparakis M., Schmidt-Supprian M., and Rajewsky K. IκB kinase signaling is essential for maintenance of mature B cells. J Exp Med 196 (2002) 743-752
32. Yamada T., Mitani T., Yorita K., Uchida D., Matsushima A., Iwamasa K., Fujita S., and Matsumoto M. Abnormal immune function of hemopoietic cells from alymphoplasia (aly) mice, a natural strain with mutant NF-κB-inducing kinase. J Immunol 165 (2000) 804-812
33. Kaisho T., Takeda K., Tsujimura T., Kawai T., Nomura F., Terada N., and Akira S. IκB kinase α is essential for mature B cell development and function. J Exp Med 193 (2001) 417-426
34. Sasaki Y., Derudder E., Hobeika E., Pelanda R., Reth M., Rajewsky K., and Schmidt-Supprian M. Canonical NF-κB activity, dispensable for B cell development, replaces BAFF-receptor signals and promotes B cell proliferation upon activation. Immunity 24 (2006) 729-739. In this study, the analysis of mice either lacking Nemo or expressing a constitutive active form of Ikk2, specifically in B cells, reveals a critical contribution of the canonical NF-κB pathway to peripheral B-cell differentiation. Loss of Nemo in developing B cells led to a significant reduction in FO B cell numbers and to a loss of both MZ and B-1a B cells. Conversely, constitutive activation of Ikk2 in developing B cells promoted an accumulation of FO and, especially, MZ B cells. Strikingly, constitutive activation of the canonical NF-κB pathway in developing B cells, rescued the major developmental defects observed in BAFF-R- (but not CD19-) deficient animals and replaced BAFF-R function to promote enhanced in vitro and in vivo B-cell survival. These data thus identify canonical NF-κB activity as a possible critical modulator of BAFF-R function in vivo.
35. Wang J.H., Avitahl N., Cariappa A., Friedrich C., Ikeda T., Renold A., Andrikopoulos K., Liang L., Pillai S., Morgan B.A., et al. Aiolos regulates B cell activation and maturation to effector state. Immunity 9 (1998) 543-553
36. Cariappa A., Tang M., Parng C., Nebelitskiy E., Carroll M., Georgopoulos K., and Pillai S. The follicular versus marginal zone B lymphocyte cell fate decision is regulated by Aiolos, Btk, and CD21. Immunity 14 (2001) 603-615
37. Tanigaki K., Han H., Yamamoto N., Tashiro K., Ikegawa M., Kuroda K., Suzuki A., Nakano T., and Honjo T. Notch-RBP-J signaling is involved in cell fate determination of marginal zone B cells. Nat Immunol 3 (2002) 443-450
38. Kuroda K., Han H., Tani S., Tanigaki K., Tun T., Furukawa T., Taniguchi Y., Kurooka H., Hamada Y., Toyokuni S., et al. Regulation of marginal zone B cell development by MINT, a suppressor of Notch/RBP-J signaling pathway. Immunity 18 (2003) 301-312
39. Saito T., Chiba S., Ichikawa M., Kunisato A., Asai T., Shimizu K., Yamaguchi T., Yamamoto G., Seo S., Kumano K., et al. Notch2 is preferentially expressed in mature B cells and indispensable for marginal zone B lineage development. Immunity 18 (2003) 675-685
40. Hozumi K., Negishi N., Suzuki D., Abe N., Sotomaru Y., Tamaoki N., Mailhos C., Ish-Horowicz D., Habu S., and Owen M.J. Delta-like 1 is necessary for the generation of marginal zone B cells but not T cells in vivo. Nat Immunol 5 (2004) 638-644
41. Thomas M.D., Kremer C.S., Ravichandran K.S., Rajewsky K., and Bender T.P. c-Myb is critical for B cell development and maintenance of follicular B cells. Immunity 23 (2005) 275-286
42. Mikkola I., Heavey B., Horcher M., and Busslinger M. Reversion of B cell commitment upon loss of Pax5 expression. Science 297 (2002) 110-113
43. Horcher M., Souabni A., and Busslinger M. Pax5/BSAP maintains the identity of B cells in late B lymphopoiesis. Immunity 14 (2001) 779-790
44. Delogu A., Schebesta A., Sun Q., Aschenbrenner K., Perlot T., and Busslinger M. Gene repression by Pax5 in B cells is essential for blood cell homeostasis and is reversed in plasma cells. Immunity 24 (2006) 269-281. In this report, compelling evidence is provided for Pax-5-mediated gene repression. This analysis of gene expression profiles performed on B cells at different stages of development, before and after induced Pax5 inactivation, has revealed the existence of more than 100 genes under the negative control of Pax-5. A large number of these genes, repressed both in B cell progenitors and in mature B cells, are normally expressed in other lineages of the hematopoietic system. This suggests that Pax-5 acts throughout B cell development to actively prevent expression of non-B cell specific genes that could interfere with B-cell identity and function. Pax-5 also represses plasma cell specific genes, including the master regulator Blimp-1, thus preventing premature terminal differentiation.
45. Xie H., Ye M., Feng R., and Graf T. Stepwise reprogramming of B cells into macrophages. Cell 117 (2004) 663-676
46. Su I.H., Basavaraj A., Krutchinsky A.N., Hobert O., Ullrich A., Chait B.T., and Tarakhovsky A. Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat Immunol 4 (2003) 124-131
47. Kloosterman W.P., and Plasterk R.H. The diverse functions of microRNAs in animal development and disease. Dev Cell 11 (2006) 441-450
48. Chen C.Z., Li L., Lodish H.F., and Bartel D.P. MicroRNAs modulate hematopoietic lineage differentiation. Science 303 (2004) 83-86
49. Cobb B.S., Nesterova T.B., Thompson E., Hertweck A., O'Connor E., Godwin J., Wilson C.B., Brockdorff N., Fisher A.G., Smale S.T., et al. T cell lineage choice and differentiation in the absence of the RNase III enzyme Dicer. J Exp Med 201 (2005) 1367-1373
50. Muljo S.A., Ansel K.M., Kanellopoulou C., Livingston D.M., Rao A., and Rajewsky K. Aberrant T cell differentiation in the absence of Dicer. J Exp Med 202 (2005) 261-269
51. Cattoretti G., Shaknovich R., Smith P.M., Jack H.M., Murty V.V., and Alobeid B. Stages of germinal center transit are defined by B cell transcription factor coexpression and relative abundance. J Immunol 177 (2006) 6930-6939