Critical role of B cell lymphoma 10 in BAFF-regulated NF-κB activation and survival of anergic B cells

Journal of Immunology

Volumn 189, Issue 11, 2012, Pages 5185-5193

  Yu, Mei ^a,b   Chen, Yuhong ^b   He, Yinghong ^a,b   Podd, Andrew ^a,c   Fu, Guoping ^b   Wright, Jacqueline A ^d   Kleiman, Eden ^d   Khan, Wasif N ^d   Wen, Renren ^b   Wang, Demin ^a,b,c  

^a NANJING UNIVERSITY   (China)

^b BLOOD RESEARCH INSTITUTE   (United States)

^c MEDICAL COLLEGE OF WISCONSIN   (United States)

^d UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ACTIVATING FACTOR; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYSOZYME; NF KAPPA B2; PROTEIN BCL 10; PROTEIN P100; PROTEIN P50; PROTEIN P52; TRANSCRIPTION FACTOR REL; TRANSCRIPTION FACTOR RELB; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; B LYMPHOCYTE; BIOACCUMULATION; CELL NUCLEUS; CELL SURVIVAL; CLONAL ANERGY; CONTROLLED STUDY; EGG; ENZYME PHOSPHORYLATION; GENE TARGETING; IMMUNOLOGICAL TOLERANCE; IMMUNOREACTIVITY; IMMUNOREGULATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; B-CELL ACTIVATING FACTOR; B-LYMPHOCYTES; BCL-X PROTEIN; CELL SURVIVAL; CLONAL ANERGY; GENE EXPRESSION REGULATION; I-KAPPA B KINASE; MICE; MICE, TRANSGENIC; MURAMIDASE; NF-KAPPA B; NF-KAPPA B P52 SUBUNIT; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-REL; SIGNAL TRANSDUCTION; SPLEEN; TRANSCRIPTION FACTOR RELB;

EID: 84869825522     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102952     Document Type: Article

References (70)

1. Nemazee, D. 1996. Antigen receptor "capacity" and the sensitivity of self-tolerance. Immunol. Today 17: 25-29. (Pubitemid 26019254)
2. Wardemann, H., S. Yurasov, A. Schaefer, J. W. Young, E. Meffre, and M. C. Nussenzweig. 2003. Predominant autoantibody production by early human B cell precursors. Science 301: 1374-1377. (Pubitemid 37075812)
3. Rajewsky, K. 1996. Clonal selection and learning in the antibody system. Nature 381: 751-758. (Pubitemid 26243107)
4. Nemazee, D. 2000. Receptor selection in B and T lymphocytes. Annu. Rev. Immunol. 18: 19-51. (Pubitemid 30365373)
5. Healy, J. I., and C. C. Goodnow. 1998. Positive versus negative signaling by lymphocyte antigen receptors. Annu. Rev. Immunol. 16: 645-670. (Pubitemid 28183380)
6. Radic, M. Z., and M. Zouali. 1996. Receptor editing, immune diversification, and self-tolerance. Immunity 5: 505-511. (Pubitemid 27062061)
7. Sandel, P. C., and J. G. Monroe. 1999. Negative selection of immature B cells by receptor editing or deletion is determined by site of antigen encounter. Immunity 10: 289-299. (Pubitemid 29165284)
8. Nossal, G. J. 1994. Negative selection of lymphocytes. Cell 76: 229-239. (Pubitemid 24046686)
9. Radic, M. Z., J. Erikson, S. Litwin, and M. Weigert. 1993. B lymphocytes may escape tolerance by revising their antigen receptors. J. Exp. Med. 177: 1165-1173.
10. Gay, D., T. Saunders, S. Camper, and M. Weigert. 1993. Receptor editing: an approach by autoreactive B cells to escape tolerance. J. Exp. Med. 177: 999-1008. (Pubitemid 23097389)
11. Tiegs, S. L., D. M. Russell, and D. Nemazee. 1993. Receptor editing in self-reactive bone marrow B cells. J. Exp. Med. 177: 1009-1020. (Pubitemid 23097390)
12. 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. (Pubitemid 32179219)
13. Edry, E., and D. Melamed. 2004. Receptor editing in positive and negative selection of B lymphopoiesis. J. Immunol. 173: 4265-4271. (Pubitemid 39280653)
14. Nemazee, D. A., and K. Bürki. 1989. Clonal deletion of B lymphocytes in a transgenic mouse bearing anti-MHC class I antibody genes. Nature 337: 562-566. (Pubitemid 19045542)
15. Hartley, S. B., J. Crosbie, R. Brink, A. B. Kantor, A. Basten, and C. C. Goodnow. 1991. Elimination from peripheral lymphoid tissues of self-reactive B lymphocytes recognizing membrane-bound antigens. Nature 353: 765-769. (Pubitemid 21912617)
16. Goodnow, C. C., J. Crosbie, S. Adelstein, T. B. Lavoie, S. J. Smith-Gill, R. A. Brink, H. Pritchard-Briscoe, J. S. Wotherspoon, R. H. Loblay, K. Raphael, et al. 1988. Altered immunoglobulin expression and functional silencing of self-reactive B lymphocytes in transgenic mice. Nature 334: 676-682.
17. Nossal, G. J., and B. L. Pike. 1980. Clonal anergy: persistence in tolerant mice of antigen-binding B lymphocytes incapable of responding to antigen or mitogen. Proc. Natl. Acad. Sci. USA 77: 1602-1606. (Pubitemid 10073810)
18. Cyster, J. G., and C. C. Goodnow. 1995. Antigen-induced exclusion from follicles and anergy are separate and complementary processes that influence peripheral B cell fate. Immunity 3: 691-701. (Pubitemid 26091145)
19. Merrell, K. T., R. J. Benschop, S. B. Gauld, K. Aviszus, D. Decote-Ricardo, L. J. Wysocki, and J. C. Cambier. 2006. Identification of anergic B cells within a wild-type repertoire. Immunity 25: 953-962. (Pubitemid 44894955)
20. 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. (Pubitemid 27408521)
21. Gauld, S. B., R. J. Benschop, K. T. Merrell, and J. C. Cambier. 2005. Maintenance of B cell anergy requires constant antigen receptor occupancy and signaling. Nat. Immunol. 6: 1160-1167. (Pubitemid 41541794)
22. Batten, M., J. Groom, T. G. Cachero, F. Qian, P. Schneider, J. Tschopp, J. L. Browning, and F. Mackay. 2000. BAFF mediates survival of peripheral immature B lymphocytes. J. Exp. Med. 192: 1453-1466.
23. Moore, P. A., O. Belvedere, A. Orr, K. Pieri, D. W. LaFleur, P. Feng, D. Soppet, M. Charters, R. Gentz, D. Parmelee, et al. 1999. BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator. Science 285: 260-263. (Pubitemid 29330000)
24. Thien, M., T. G. Phan, S. Gardam, M. Amesbury, A. Basten, F. Mackay, and R. Brink. 2004. Excess BAFF rescues self-reactive B cells from peripheral deletion and allows them to enter forbidden follicular and marginal zone niches. Immunity 20: 785-798. (Pubitemid 38757447)
25. Lesley, R., Y. Xu, S. L. Kalled, D. M. Hess, S. R. Schwab, H. B. Shu, and J. G. Cyster. 2004. Reduced competitiveness of autoantigen-engaged B cells due to increased dependence on BAFF. Immunity 20: 441-453. (Pubitemid 38482122)
26. Schiemann, B., J. L. Gommerman, K. Vora, T. G. Cachero, S. Shulga-Morskaya, M. Dobles, E. Frew, and M. L. Scott. 2001. An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway. Science 293: 2111-2114. (Pubitemid 32848063)
27. Thompson, J. S., S. A. Bixler, F. Qian, K. Vora, M. L. Scott, T. G. Cachero, C. Hession, P. Schneider, I. D. Sizing, C. Mullen, et al. 2001. BAFF-R, a newly identified TNF receptor that specifically interacts with BAFF. Science 293: 2108-2111. (Pubitemid 32848062)
28. O'Connor, B. P., V. S. Raman, L. D. Erickson, W. J. Cook, L. K. Weaver, C. Ahonen, L. L. Lin, G. T. Mantchev, R. J. Bram, and R. J. Noelle. 2004. BCMA is essential for the survival of long-lived bone marrow plasma cells. J. Exp. Med. 199: 91-98.
29. Seshasayee, D., P. Valdez, M. Yan, V. M. Dixit, D. Tumas, and I. S. Grewal. 2003. Loss of TACI causes fatal lymphoproliferation and autoimmunity, establishing TACI as an inhibitory BLyS receptor. Immunity 18: 279-288. (Pubitemid 36263002)
30. Hsu, B. L., S. M. Harless, R. C. Lindsley, D. M. Hilbert, and M. P. Cancro. 2002. Cutting edge: BLyS enables survival of transitional and mature B cells through distinct mediators. J. Immunol. 168: 5993-5996. (Pubitemid 34620011)
31. Ghosh, S., M. J. May, and E. B. Kopp. 1998. NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16: 225-260. (Pubitemid 28183365)
32. Li, Q., and I. M. Verma. 2002. NF-κB regulation in the immune system. Nat. Rev. Immunol. 2: 725-734.
33. Baeuerle, P. A., and D. Baltimore. 1988. IκB: a specific inhibitor of the NF-κB transcription factor. Science 242: 540-546. (Pubitemid 18263193)
34. Pomerantz, J. L., and D. Baltimore. 2002. Two pathways to NF-κB. Mol. Cell 10: 693-695.
35. Claudio, E., K. Brown, S. Park, H. Wang, and U. Siebenlist. 2002. BAFF-induced NEMO-independent processing of NF-κB2 in maturing B cells. Nat. Immunol. 3: 958-965. (Pubitemid 35154010)
36. Kayagaki, N., M. Yan, D. Seshasayee, H. Wang, W. Lee, D. M. French, I. S. Grewal, A. G. Cochran, N. C. Gordon, J. Yin, et al. 2002. BAFF/BLyS receptor 3 binds the B cell survival factor BAFF ligand through a discrete surface loop and promotes processing of NF-κB2. Immunity 17: 515-524. (Pubitemid 35223539)
37. Vallabhapurapu, S., A. Matsuzawa, W. Zhang, P. H. Tseng, J. J. Keats, H. Wang, D. A. Vignali, P. L. Bergsagel, and M. Karin. 2008. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-κB signaling. Nat. Immunol. 9: 1364-1370.
38. Gardam, S., F. Sierro, A. Basten, F. Mackay, and R. Brink. 2008. TRAF2 and TRAF3 signal adapters act cooperatively to control the maturation and survival signals delivered to B cells by the BAFF receptor. Immunity 28: 391-401.
39. Hatada, E. N., R. K. Do, A. Orlofsky, H. C. Liou, M. Prystowsky, I. C. MacLennan, J. Caamano, and S. Chen-Kiang. 2003. 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: 761-768. (Pubitemid 36871386)
40. Ramakrishnan, P., W. Wang, and D. Wallach. 2004. Receptor-specific signaling for both the alternative and the canonical NF-κB activation pathways by NF-κB-inducing kinase. Immunity 21: 477-489. (Pubitemid 39370504)
41. Thome, M., F. Martinon, K. Hofmann, V. Rubio, V. Steiner, P. Schneider, C. Mattmann, and J. Tschopp. 1999. Equine herpesvirus-2 E10 gene product, but not its cellular homologue, activates NF-κB transcription factor and c-Jun N-terminal kinase. J. Biol. Chem. 274: 9962-9968.
42. Srinivasula, S. M., M. Ahmad, J. H. Lin, J. L. Poyet, T. Fernandes-Alnemri, P. N. Tsichlis, and E. S. Alnemri. 1999. CLAP, a novel caspase recruitment domain-containing protein in the tumor necrosis factor receptor pathway, regulates NF-κB activation and apoptosis. J. Biol. Chem. 274: 17946-17954.
43. Costanzo, A., C. Guiet, and P. Vito. 1999. c-E10 is a caspase-recruiting domain-containing protein that interacts with components of death receptors signaling pathway and activates nuclear factor-κB. J. Biol. Chem. 274: 20127-20132.
44. Yan, M., J. Lee, S. Schilbach, A. Goddard, and V. Dixit. 1999. mE10, a novel caspase recruitment domain-containing proapoptotic molecule. J. Biol. Chem. 274: 10287-10292.
45. Koseki, T., N. Inohara, S. Chen, R. Carrio, J. Merino, M. O. Hottiger, G. J. Nabel, and G. Núñez. 1999. CIPER, a novel NF κB-activating protein containing a caspase recruitment domain with homology to herpesvirus-2 protein E10. J. Biol. Chem. 274: 9955-9961.
46. Ruland, J., G. S. Duncan, A. Elia, I. del Barco Barrantes, L. Nguyen, S. Plyte, D. G. Millar, D. Bouchard, A. Wakeham, P. S. Ohashi, and T. W. Mak. 2001. Bcl10 is a positive regulator of antigen receptor-induced activation of NF-κB and neural tube closure. Cell 104: 33-42. (Pubitemid 32144970)
47. Xue, L., S. W. Morris, C. Orihuela, E. Tuomanen, X. Cui, R. Wen, and D. Wang. 2003. Defective development and function of Bcl10-deficient follicular, marginal zone and B1 B cells. Nat. Immunol. 4: 857-865. (Pubitemid 37098656)
48. Lin, X., and D. Wang. 2004. The roles of CARMA1, Bcl10, and MALT1 in antigen receptor signaling. Semin. Immunol. 16: 429-435. (Pubitemid 39488023)
49. Thome, M. 2004. CARMA1, BCL-10 and MALT1 in lymphocyte development and activation. Nat. Rev. Immunol. 4: 348-359. (Pubitemid 38649277)
50. Matsumoto, R., D. Wang, M. Blonska, H. Li, M. Kobayashi, B. Pappu, Y. Chen, D. Wang, and X. Lin. 2005. Phosphorylation of CARMA1 plays a critical role in T cell receptor-mediated NF-κB activation. Immunity 23: 575-585. (Pubitemid 41779480)
51. Sommer, K., B. Guo, J. L. Pomerantz, A. D. Bandaranayake, M. E. Moreno-García, Y. L. Ovechkina, and D. J. Rawlings. 2005. Phosphorylation of the CARMA1 linker controls NF-κB activation. Immunity 23: 561-574. (Pubitemid 41779479)
52. Schuman, J., Y. Chen, A. Podd, M. Yu, H. H. Liu, R. Wen, Z. J. Chen, and D. Wang. 2009. A critical role of TAK1 in B-cell receptor-mediated nuclear factor κB activation. Blood 113: 4566-4574.
53. 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. (Pubitemid 29330125)
54. Uren, A. G., K. O'Rourke, L. A. Aravind, M. T. Pisabarro, S. Seshagiri, E. V. Koonin, and V. M. Dixit. 2000. Identification of paracaspases and meta-caspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell 6: 961-967.
55. Stadanlick, J. E., M. Kaileh, F. G. Karnell, J. L. Scholz, J. P. Miller, W. J. Quinn, III, R. J. Brezski, L. S. Treml, K. A. Jordan, J. G. Monroe, et al. 2008. Tonic B cell antigen receptor signals supply an NF-κB substrate for prosurvival BLyS signaling. Nat. Immunol. 9: 1379-1387.
56. Castro, I., J. A. Wright, B. Damdinsuren, K. L. Hoek, G. Carlesso, N. P. Shinners, R. M. Gerstein, R. T. Woodland, R. Sen, and W. N. Khan. 2009. B cell receptor-mediated sustained c-Rel activation facilitates late transitional B cell survival through control of B cell activating factor receptor and NF-κB2. J. Immunol. 182: 7729-7737.
57. Craxton, A., K. E. Draves, A. Gruppi, and E. A. Clark. 2005. BAFF regulates B cell survival by downregulating the BH3-only family member Bim via the ERK pathway. J. Exp. Med. 202: 1363-1374. (Pubitemid 41668739)
58. Patke, A., I. Mecklenbräuker, H. Erdjument-Bromage, P. Tempst, and A. Tarakhovsky. 2006. BAFF controls B cell metabolic fitness through a PKCβ- and Akt-dependent mechanism. J. Exp. Med. 203: 2551-2562. (Pubitemid 44664624)
59. Yamada, T., T. Mitani, K. Yorita, D. Uchida, A. Matsushima, K. Iwamasa, S. Fujita, and M. Matsumoto. 2000. Abnormal immune function of hemopoietic cells from alymphoplasia (aly) mice, a natural strain with mutant NF-κB-inducing kinase. J. Immunol. 165: 804-812. (Pubitemid 30484747)
60. Tusche, M. W., L. A. Ward, F. Vu, D. McCarthy, M. Quintela-Fandino, J. Ruland, J. L. Gommerman, and T. W. Mak. 2009. Differential requirement of MALT1 for BAFF-induced outcomes in B cell subsets. J. Exp. Med. 206: 2671-2683.
61. Kurosaki, T. 1999. Genetic analysis of B cell antigen receptor signaling. Annu. Rev. Immunol. 17: 555-592. (Pubitemid 29241134)
62. Kurosaki, T., and M. Hikida. 2009. Tyrosine kinases and their substrates in B lymphocytes. Immunol. Rev. 228: 132-148.
63. Fu, C., C. W. Turck, T. Kurosaki, and A. C. Chan. 1998. BLNK: a central linker protein in B cell activation. Immunity 9: 93-103. (Pubitemid 28361298)
64. Carter, R. H., and D. T. Fearon. 1992. CD19: lowering the threshold for antigen receptor stimulation of B lymphocytes. Science 256: 105-107.
65. Fruman, D. A., S. B. Snapper, C. M. Yballe, L. Davidson, J. Y. Yu, F. W. Alt, and L. C. Cantley. 1999. Impaired B cell development and proliferation in absence of phosphoinositide 3-kinase p85α. Science 283: 393-397.
66. Wang, D., J. Feng, R. Wen, J. C. Marine, M. Y. Sangster, E. Parganas, A. Hoffmeyer, C. W. Jackson, J. L. Cleveland, P. J. Murray, and J. N. Ihle. 2000. Phospholipase Cγ2 is essential in the functions of B cell and several Fc receptors. Immunity 13: 25-35.
67. Rhee, S. G., and Y. S. Bae. 1997. Regulation of phosphoinositide-specific phospholipase C isozymes. J. Biol. Chem. 272: 15045-15048.
68. Rhee, S. G., and K. D. Choi. 1992. Regulation of inositol phospholipid-specific phospholipase C isozymes. J. Biol. Chem. 267: 12393-12396.
69. Shinners, N. P., G. Carlesso, I. Castro, K. L. Hoek, R. A. Corn, R. T. Woodland, M. L. Scott, D. Wang, and W. N. Khan. 2007. Bruton's tyrosine kinase mediates NF-κB activation and B cell survival by B cell-activating factor receptor of the TNF-R family. J. Immunol. 179: 3872-3880.
70. Hikida, M., S. Johmura, A. Hashimoto, M. Takezaki, and T. Kurosaki. 2003. Coupling between B cell receptor and phospholipase C-γ2 is essential for mature B cell development. J. Exp. Med. 198: 581-589. (Pubitemid 37040392)