IFN regulatory factor 8 restricts the size of the marginal zone and follicular B cell pools

Journal of Immunology

Volumn 186, Issue 3, 2011, Pages 1458-1466

  Feng, Jianxun ^a   Wang, Hongsheng ^a   Shin, Dong Mi ^a   Masiuk, Marek ^a,b   Qi, Chen Feng ^a   Morse III, Herbert C ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b POMERANIAN MEDICAL UNIVERSITY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

CD19 ANTIGEN; CD23 ANTIGEN; COMPLEMENT COMPONENT C3D RECEPTOR; CRE RECOMBINASE; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; CELL EXPANSION; CELL MATURATION; CONTROLLED STUDY; FOLLICULAR B LYMPHOCYTE; GENE DELETION; GENE EXPRESSION PROFILING; GENE INACTIVATION; INFLAMMATION; LYMPHOCYTE COUNT; MARGINAL ZONE B LYMPHOCYTE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; B-LYMPHOCYTE SUBSETS; CELL DIFFERENTIATION; FEMALE; GENE DELETION; INTERFERON REGULATORY FACTORS; LYMPHOCYTE COUNT; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTAGENESIS, INSERTIONAL; POINT MUTATION; PROTEIN STRUCTURE, TERTIARY; SPLEEN;

EID: 79251561555     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001950     Document Type: Article

References (48)

1. Casellas, R., T. A. Shih, M. Kleinewietfeld, J. Rakonjac, D. Nemazee, K. Rajewsky, and M. C. Nussenzweig. 2001. Contribution of receptor editing to the antibody repertoire. Science 291: 1541-1544.
2. Halverson, R., R. M. Torres, and R. Pelanda. 2004. Receptor editing is the main mechanism of B cell tolerance toward membrane antigens. Nat. Immunol. 5: 645-650.
3. Retter, M. W., and D. Nemazee. 1998. Receptor editing occurs frequently during normal B cell development. J. Exp. Med. 188: 1231-1238.
4. Wardemann, H., J. Hammersen, and M. C. Nussenzweig. 2004. Human auto-antibody silencing by immunoglobulin light chains. J. Exp. Med. 200: 191-199.
5. Allman, D., R. C. Lindsley, W. DeMuth, K. Rudd, S. A. Shinton, and R. R. Hardy. 2001. Resolution of three nonproliferative immature splenic B cell subsets reveals multiple selection points during peripheral B cell maturation. J. Immunol. 167: 6834-6840.
6. Loder, F., B. Mutschler, R. J. Ray, C. J. Paige, P. Sideras, R. Torres, M. C. Lamers, and R. Carsetti. 1999. B cell development in the spleen takes place in discrete steps and is determined by the quality of B cell receptor-derived signals. J. Exp. Med. 190: 75-89.
7. Gururajan, M., A. Simmons, T. Dasu, B. T. Spear, C. Calulot, D. A. Robertson, D. L. Wiest, J. G. Monroe, and S. Bondada. 2008. Early growth response genes regulate B cell development, proliferation, and immune response. J. Immunol. 181: 4590-4602.
8. Wang, D., S. A. John, J. L. Clements, D. H. Percy, K. P. Barton, and L. A. Garrett-Sinha. 2005. Ets-1 deficiency leads to altered B cell differentiation, hyper-responsiveness to TLR9 and autoimmune disease. Int. Immunol. 17: 1179-1191.
9. Becker-Herman, S., F. Lantner, and I. Shachar. 2002. Id2 negatively regulates B cell differentiation in the spleen. J. Immunol. 168: 5507-5513. (Pubitemid 34556129)
10. Cariappa, A., M. Tang, C. Parng, E. Nebelitskiy, M. Carroll, K. Georgopoulos, and S. Pillai. 2001. The follicular versus marginal zone B lymphocyte cell fate decision is regulated by Aiolos, Btk, and CD21. Immunity 14: 603-615.
11. Wang, J. H., N. Avitahl, A. Cariappa, C. Friedrich, T. Ikeda, A. Renold, K. Andrikopoulos, L. Liang, S. Pillai, B. A. Morgan, and K. Georgopoulos. 1998. Aiolos regulates B cell activation and maturation to effector state. Immunity 9: 543-553.
12. Weih, D. S., Z. B. Yilmaz, and F. Weih. 2001. Essential role of RelB in germinal center and marginal zone formation and proper expression of homing chemokines. J. Immunol. 167: 1909-1919.
13. Quong, M. W., A. Martensson, A. W. Langerak, R. R. Rivera, D. Nemazee, and C. Murre. 2004. Receptor editing and marginal zone B cell development are regulated by the helix-loop-helix protein, E2A. J. Exp. Med. 199: 1101-1112.
14. Guo, F., D. Weih, E. Meier, and F. Weih. 2007. Constitutive alternative NF-kappaB signaling promotes marginal zone B-cell development but disrupts the marginal sinus and induces HEV-like structures in the spleen. Blood 110: 2381-2389.
15. Zhang, X. K., O. Moussa, A. LaRue, S. Bradshaw, I. Molano, D. D. Spyropoulos, G. S. Gilkeson, and D. K. Watson. 2008. The transcription factor Fli-1 modulates marginal zone and follicular B cell development in mice. J. Immunol. 181: 1644-1654.
16. Tamura, T., H. Yanai, D. Savitsky, and T. Taniguchi. 2008. The IRF family transcription factors in immunity and oncogenesis. Annu. Rev. Immunol. 26: 535-584.
17. Holtschke, T., J. Löhler, Y. Kanno, T. Fehr, N. Giese, F. Rosenbauer, J. Lou, K. P. Knobeloch, L. Gabriele, J. F. Waring, et al. 1996. Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell 87: 307-317.
18. Tailor, P., T. Tamura, H. J. Kong, T. Kubota, M. Kubota, P. Borghi, L. Gabriele, and K. Ozato. 2007. The feedback phase of type I interferon induction in dendritic cells requires interferon regulatory factor 8. Immunity 27: 228-239.
19. Tamura, T., T. Nagamura-Inoue, Z. Shmeltzer, T. Kuwata, and K. Ozato. 2000. ICSBP directs bipotential myeloid progenitor cells to differentiate into mature macrophages. Immunity 13: 155-165.
20. Tailor, P., T. Tamura, H. C. Morse, III, and K. Ozato. 2008. The BXH2 mutation in IRF8 differentially impairs dendritic cell subset development in the mouse. Blood 111: 1942-1945.
21. Turcotte, K., S. Gauthier, A. Tuite, A. Mullick, D. Malo, and P. Gros. 2005. A mutation in the Icsbp1 gene causes susceptibility to infection and a chronic myeloid leukemia-like syndrome in BXH-2 mice. J. Exp. Med. 201: 881-890.
22. Wang, H., C. H. Lee, C. Qi, P. Tailor, J. Feng, S. Abbasi, T. Atsumi, and H. C. Morse, III. 2008. IRF8 regulates B-cell lineage specification, commitment, and differentiation. Blood 112: 4028-4038.
23. Lu, R., K. L. Medina, D. W. Lancki, and H. Singh. 2003. IRF-4,8 orchestrate the pre-B-to-B transition in lymphocyte development. Genes Dev. 17: 1703-1708. (Pubitemid 36870333)
24. Ma, S., S. Pathak, L. Trinh, and R. Lu. 2008. Interferon regulatory factors 4 and 8 induce the expression of Ikaros and Aiolos to down-regulate pre-B-cell receptor and promote cell-cycle withdrawal in pre-B-cell development. Blood 111: 1396-1403.
25. Ma, S., A. Turetsky, L. Trinh, and R. Lu. 2006. IFN regulatory factor 4 and 8 promote Ig light chain kappa locus activation in pre-B cell development. J. Immunol. 177: 7898-7904. (Pubitemid 44846305)
26. Lee, C. H., M. Melchers, H. Wang, T. A. Torrey, R. Slota, C. F. Qi, J. Y. Kim, P. Lugar, H. J. Kong, L. Farrington, et al. 2006. Regulation of the germinal center gene program by interferon (IFN) regulatory factor 8/IFN consensus sequence-binding protein. J. Exp. Med. 203: 63-72.
27. Zhou, J. X., C. H. Lee, C. F. Qi, H. Wang, Z. Naghashfar, S. Abbasi, and H. C. Morse, III. 2009. IFN regulatory factor 8 regulates MDM2 in germinal center B cells. J. Immunol. 183: 3188-3194.
28. Qi, C. F., Z. Li, M. Raffeld, H. Wang, A. L. Kovalchuk, and H. C. Morse, III. 2009. Differential expression of IRF8 in subsets of macrophages and dendritic cells and effects of IRF8 deficiency on splenic B cell and macrophage compartments. Immunol. Res. 45: 62-74.
29. Wang, H., J. Ye, L. W. Arnold, S. K. McCray, and S. H. Clarke. 2001. A VH12 transgenic mouse exhibits defects in pre-B cell development and is unable to make IgM+ B cells. J. Immunol. 167: 1254-1262.
30. Shin, D. M., D. J. Shaffer, H. Wang, D. C. Roopenian, and H. C. Morse, III. 2008. NOTCH is part of the transcriptional network regulating cell growth and survival in mouse plasmacytomas. Cancer Res. 68: 9202-9211.
31. Wang, H., and H. C. Morse, III. 2009. IRF8 regulates myeloid and B lymphoid lineage diversification. Immunol. Res. 43: 109-117.
32. Hobeika, E., S. Thiemann, B. Storch, H. Jumaa, P. J. Nielsen, R. Pelanda, and M. Reth. 2006. Testing gene function early in the B cell lineage in mb1-cre mice. Proc. Natl. Acad. Sci. USA 103: 13789-13794.
33. Lam, K. P., R. Kühn, and K. Rajewsky. 1997. In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell 90: 1073-1083.
34. Bannish, G., E. M. Fuentes-Pananá, J. C. Cambier, W. S. Pear, and J. G. Monroe. 2001. Ligand-independent signaling functions for the B lymphocyte antigen receptor and their role in positive selection during B lymphopoiesis. J. Exp. Med. 194: 1583-1596.
35. Fuentes-Pananá, E. M., G. Bannish, F. G. Karnell, J. F. Treml, and J. G. Monroe. 2006. Analysis of the individual contributions of Igalpha (CD79a)- and Igbeta (CD79b)-mediated tonic signaling for bone marrow B cell development and peripheral B cell maturation. J. Immunol. 177: 7913-7922.
36. Hayakawa, K., M. Asano, S. A. Shinton, M. Gui, L. J. Wen, J. Dashoff, and R. R. Hardy. 2003. Positive selection of anti-thy-1 autoreactive B-1 cells and natural serum autoantibody production independent from bone marrow B cell development. J. Exp. Med. 197: 87-99.
37. Hayakawa, K., M. Asano, S. A. Shinton, M. Gui, D. Allman, C. L. Stewart, J. Silver, and R. R. Hardy. 1999. Positive selection of natural autoreactive B cells. Science 285: 113-116.
38. Heltemes, L. M., and T. Manser. 2002. Level of B cell antigen receptor surface expression influences both positive and negative selection of B cells during primary development. J. Immunol. 169: 1283-1292.
39. Martin, F., and J. F. Kearney. 2002. Marginal-zone B cells. Nat. Rev. Immunol. 2: 323-335.
40. Pillai, S., and A. Cariappa. 2009. The follicular versus marginal zone B lymphocyte cell fate decision. Nat. Rev. Immunol. 9: 767-777.
41. Saito, T., S. Chiba, M. Ichikawa, A. Kunisato, T. Asai, K. Shimizu, T. Yamaguchi, G. Yamamoto, S. Seo, K. Kumano, et al. 2003. Notch2 is preferentially expressed in mature B cells and indispensable for marginal zone B lineage development. Immunity 18: 675-685.
42. Tanigaki, K., H. Han, N. Yamamoto, K. Tashiro, M. Ikegawa, K. Kuroda, A. Suzuki, T. Nakano, and T. Honjo. 2002. Notch-RBP-J signaling is involved in cell fate determination of marginal zone B cells. Nat. Immunol. 3: 443-450.
43. Hozumi, K., N. Negishi, D. Suzuki, N. Abe, Y. Sotomaru, N. Tamaoki, C. Mailhos, D. Ish-Horowicz, S. Habu, and M. J. Owen. 2004. Delta-like 1 is necessary for the generation of marginal zone B cells but not T cells in vivo. Nat. Immunol. 5: 638-644.
44. Oyama, T., K. Harigaya, A. Muradil, K. Hozumi, S. Habu, H. Oguro, A. Iwama, K. Matsuno, R. Sakamoto, M. Sato, et al. 2007. Mastermind-1 is required for Notch signal-dependent steps in lymphocyte development in vivo. Proc. Natl. Acad. Sci. USA 104: 9764-9769.
45. Kuroda, K., H. Han, S. Tani, K. Tanigaki, T. Tun, T. Furukawa, Y. Taniguchi, H. Kurooka, Y. Hamada, S. Toyokuni, and T. Honjo. 2003. Regulation of marginal zone B cell development by MINT, a suppressor of Notch/RBP-J signaling pathway. Immunity 18: 301-312.
46. Witt, C. M., V. Hurez, C. S. Swindle, Y. Hamada, and C. A. Klug. 2003. Activated Notch2 potentiates CD8 lineage maturation and promotes the selective development of B1 B cells. Mol. Cell. Biol. 23: 8637-8650.
47. Moran, S. T., A. Cariappa, H. Liu, B. Muir, D. Sgroi, C. Boboila, and S. Pillai. 2007. Synergism between NF-kappa B1/p50 and Notch2 during the development of marginal zone B lymphocytes. J. Immunol. 179: 195-200.
48. Polli, M., A. Dakic, A. Light, L. Wu, D. M. Tarlinton, and S. L. Nutt. 2005. The development of functional B lymphocytes in conditional PU.1 knock-out mice. Blood 106: 2083-2090.