FcγRIIb and BAFF differentially regulate peritoneal B1 cell survival

Journal of Immunology

Volumn 188, Issue 10, 2012, Pages 4792-4800

  Amezcua Vesely, Maria Carolina ^a   Schwartz, Marc ^b   Bermejo, Daniela A ^a   Montes, Carolina L ^a   Cautivo, Kelly M ^c   Kalergis, Alexis M ^c   Rawlings, David J ^b   Acosta Rodríguez, Eva V ^a   Gruppi, Adriana ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^c PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

B CELL ACTIVATING FACTOR; FC RECEPTOR IIB; INTERLEUKIN 4;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; B LYMPHOCYTE; B1 CELL; CELL DIFFERENTIATION; CELL SURVIVAL; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; IN VIVO STUDY; INNATE IMMUNITY; MOUSE; NONHUMAN; PERITONEUM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; UPREGULATION;

EID: 84861146585     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102070     Document Type: Article

References (77)

1. Berland, R., and H. H. Wortis. 2002. Origins and functions of B-1 cells with notes on the role of CD5. Annu. Rev. Immunol. 20: 253-300. (Pubitemid 34293426)
2. Hayakawa, K., and R. R. Hardy. 2000. Development and function of B-1 cells. Curr. Opin. Immunol. 12: 346-353.
3. Martin, F., and J. F. Kearney. 2000. B-cell subsets and the mature preimmune repertoire: marginal zone and B1 B cells as part of a "natural immune memory". Immunol. Rev. 175: 70-79. (Pubitemid 30427157)
4. Baumgarth, N., J. W. Tung, and L. A. Herzenberg. 2005. Inherent specificities in natural antibodies: a key to immune defense against pathogen invasion. Springer Semin. Immunopathol. 26: 347-362. (Pubitemid 40468889)
5. Martin, F., A. M. Oliver, and J. F. Kearney. 2001. Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 14: 617-629. (Pubitemid 32520872)
6. Haas, K. M., J. C. Poe, D. A. Steeber, and T. F. Tedder. 2005. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 23: 7-18. (Pubitemid 41019653)
7. Macpherson, A. J., D. Gatto, E. Sainsbury, G. R. Harriman, H. Hengartner, and R. M. Zinkernagel. 2000. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288: 2222-2226. (Pubitemid 30429609)
8. Tumang, J. R., R. Francés, S. G. Yeo, and T. L. Rothstein. 2005. Spontaneously Ig-secreting B-1 cells violate the accepted paradigm for expression of differentiation-associated transcription factors. J. Immunol. 174: 3173-3177. (Pubitemid 40354018)
9. Hayakawa, K., R. R. Hardy, D. R. Parks, and L. A. Herzenberg. 1983. The "Ly-1 B" cell subpopulation in normal immunodefective, and autoimmune mice. J. Exp. Med. 157: 202-218. (Pubitemid 13176184)
10. Ishida, D., L. Su, A. Tamura, Y. Katayama, Y. Kawai, S. F. Wang, M. Taniwaki, Y. Hamazaki, M. Hattori, and N. Minato. 2006. Rap1 signal controls B cell receptor repertoire and generation of self-reactive B1a cells. Immunity 24: 417-427.
11. Jellusova, J., U. Wellmann, K. Amann, T. H. Winkler, and L. Nitschke. 2010. CD22 3 Siglec-G double-deficient mice have massively increased B1 cell numbers and develop systemic autoimmunity. J. Immunol. 184: 3618-3627.
12. Fukuyama, H., F. Nimmerjahn, and J. V. Ravetch. 2005. The inhibitory Fcγreceptor modulates autoimmunity by limiting the accumulation of immunoglobulin G+ anti-DNA plasma cells. Nat. Immunol. 6: 99-106. (Pubitemid 40136701)
13. Ho, F., J. E. Lortan, I. C. MacLennan, and M. Khan. 1986. Distinct short-lived and long-lived antibody-producing cell populations. Eur. J. Immunol. 16: 1297-1301. (Pubitemid 17171537)
14. Smith, K. G., T. D. Hewitson, G. J. Nossal, and D. M. Tarlinton. 1996. The phenotype and fate of the antibody-forming cells of the splenic foci. Eur. J. Immunol. 26: 444-448. (Pubitemid 26060254)
15. Xiang, Z., A. J. Cutler, R. J. Brownlie, K. Fairfax, K. E. Lawlor, E. Severinson, E. U.Walker, R. A. Manz, D.M. Tarlinton, and K. G. Smith. 2007. FcγRIIb controls bone marrow plasma cell persistence and apoptosis. Nat. Immunol. 8: 419-429. (Pubitemid 46745417)
16. Yuasa, T., S. Kubo, T. Yoshino, A. Ujike, K. Matsumura, M. Ono, J. V. Ravetch, and T. Takai. 1999. Deletion of Fcγ receptor IIB renders H-2b mice susceptible to collagen-induced arthritis. J. Exp. Med. 189: 187-194. (Pubitemid 29047038)
17. Clynes, R., J. S. Maizes, R. Guinamard, M. Ono, T. Takai, and J. V. Ravetch. 1999. Modulation of immune complex-induced inflammation in vivo by the coordinate expression of activation and inhibitory Fc receptors. J. Exp. Med. 189: 179-185. (Pubitemid 29047037)
18. Bolland, S., Y. S. Yim, K. Tus, E. K. Wakeland, and J. V. Ravetch. 2002. Genetic modifiers of systemic lupus erythematosus in FcγRIIB2/2 mice. J. Exp. Med. 195: 1167-1174. (Pubitemid 34517142)
19. Wang, J., I. Taniuchi, Y. Maekawa, M. Howard, M. D. Cooper, and T. Watanabe. 1996. Expression and function of Fas antigen on activated murine B cells. Eur. J. Immunol. 26: 92-96. (Pubitemid 26028417)
20. 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)
21. Schneider, P., F. MacKay, V. Steiner, K. Hofmann, J. L. Bodmer, N. Holler, C. Ambrose, P. Lawton, S. Bixler, H. Acha-Orbea, et al. 1999. BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. J. Exp. Med. 189: 1747-1756. (Pubitemid 29272691)
22. Mackay, F., and J. L. Browning. 2002. BAFF: a fundamental survival factor for B cells. Nat. Rev. Immunol. 2: 465-475. (Pubitemid 37328738)
23. Stohl, W., S. Metyas, S. M. Tan, G. S. Cheema, B. Oamar, D. Xu, V. Roschke, Y. Wu, K. P. Baker, and D. M. Hilbert. 2003. B lymphocyte stimulator overexpression in patients with systemic lupus erythematosus: longitudinal observations. Arthritis Rheum. 48: 3475-3486. (Pubitemid 37531913)
24. Merino, M. C., C. L. Montes, E. V. Acosta-Rodriguez, D. A. Bermejo, M. C. Amezcua-Vesely, and A. Gruppi. 2010. Peritoneum from Trypanosoma cruzi-infected mice is a homing site of Syndecan-1 neg plasma cells which mainly provide non-parasite-specific antibodies. Int. Immunol. 22: 399-410.
25. Reddy, P. V., K. V. Rao, and M. D. Norenberg. 2008. The mitochondrial permeability transition, and oxidative and nitrosative stress in the mechanism of copper toxicity in cultured neurons and astrocytes. Lab. Invest. 88: 816-830.
26. Xu, Z., E. J. Butfiloski, E. S. Sobel, and L. Morel. 2004. Mechanisms of peritoneal B-1a cells accumulation induced by murine lupus susceptibility locus Sle2. J. Immunol. 173: 6050-6058. (Pubitemid 39487760)
27. Su, T. T., and D. J. Rawlings. 2002. Transitional B lymphocyte subsets operate as distinct checkpoints in murine splenic B cell development. J. Immunol. 168: 2101-2110. (Pubitemid 34171808)
28. Hastings, W. D., J. R. Tumang, T. W. Behrens, and T. L. Rothstein. 2006. Peritoneal B-2 cells comprise a distinct B-2 cell population with B-1b-like characteristics. Eur. J. Immunol. 36: 1114-1123.
29. Mizuno, T., X. Zhong, and T. L. Rothstein. 2003. Fas-induced apoptosis in B cells. Apoptosis 8: 451-460. (Pubitemid 37247988)
30. Zhong, X., J. R. Tumang, W. Gao, C. Bai, and T. L. Rothstein. 2007. PD-L2 expression extends beyond dendritic cells/macrophages to B1 cells enriched for VH11/VH12 and phosphatidylcholine binding. Eur. J. Immunol. 37: 2405-2410. (Pubitemid 47423611)
31. Kallies, A., and S. L. Nutt. 2007. Terminal differentiation of lymphocytes depends on Blimp-1. Curr. Opin. Immunol. 19: 156-162. (Pubitemid 46357676)
32. Fairfax, K. A., L. M. Corcoran, C. Pridans, N. D. Huntington, A. Kallies, S. L. Nutt, and D. M. Tarlinton. 2007. Different kinetics of blimp-1 induction in B cell subsets revealed by reporter gene. J. Immunol. 178: 4104-4111. (Pubitemid 46492359)
33. Holodick, N. E., J. R. Tumang, and T. L. Rothstein. 2010. Immunoglobulin secretion by B1 cells: differential intensity and IRF4-dependence of spontaneous IgM secretion by peritoneal and splenic B1 cells. Eur. J. Immunol. 40: 3007-3016.
34. Tzeng, S. J., S. Bolland, K. Inabe, T. Kurosaki, and S. K. Pierce. 2005. The B cell inhibitory Fc receptor triggers apoptosis by a novel c-Abl family kinasedependent pathway. J. Biol. Chem. 280: 35247-35254. (Pubitemid 41532712)
35. Karras, J. G., Z. Wang, L. Huo, R. G. Howard, D. A. Frank, and T. L. Rothstein. 1997. Signal transducer and activator of transcription-3 (STAT3) is constitutively activated in normal, self-renewing B-1 cells but only inducibly expressed in conventional B lymphocytes. J. Exp. Med. 185: 1035-1042. (Pubitemid 27136796)
36. Holodick, N. E., J. R. Tumang, and T. L. Rothstein. 2009. Continual signaling is responsible for constitutive ERK phosphorylation in B-1a cells. Mol. Immunol. 46: 3029-3036.
37. Benedict, C. L., and J. F. Kearney. 1999. Increased junctional diversity in fetal B cells results in a loss of protective anti-phosphorylcholine antibodies in adult mice. Immunity 10: 607-617. (Pubitemid 29262663)
38. Boes, M., A. P. Prodeus, T. Schmidt, M. C. Carroll, and J. Chen. 1998. A critical role of natural immunoglobulin M in immediate defense against systemic bacterial infection. J. Exp. Med. 188: 2381-2386. (Pubitemid 29028511)
39. Baumgarth, N. 2000. Secreted IgM versus BLyS in germinal center formation. Nat. Immunol. 1: 179.
40. Choi, Y. S., and N. Baumgarth. 2008. Dual role for B-1a cells in immunity to influenza virus infection. J. Exp. Med. 205: 3053-3064.
41. Ochsenbein, A. F., T. Fehr, C. Lutz, M. Suter, F. Brombacher, H. Hengartner, and R. M. Zinkernagel. 1999. Control of early viral and bacterial distribution and disease by natural antibodies. Science 286: 2156-2159. (Pubitemid 129516290)
42. Alugupalli, K. R., J. M. Leong, R. T. Woodland, M. Muramatsu, T. Honjo, and R. M. Gerstein. 2004. B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 21: 379-390. (Pubitemid 39208339)
43. Baumgarth, N. 2011. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat. Rev. Immunol. 11: 34-46.
44. Acosta Rodriguez, E. V., E. Zuñiga, C. L. Montes, and A. Gruppi. 2003. Interleukin-4 biases differentiation of B cells from Trypanosoma cruzi-infected mice and restrains their fratricide: role of Fas ligand down-regulation and MHC class II-transactivator up-regulation. J. Leukoc. Biol. 73: 127-136. (Pubitemid 36125683)
45. Rudge, E. U., A. J. Cutler, N. R. Pritchard, and K. G. Smith. 2002. Interleukin 4 reduces expression of inhibitory receptors on B cells and abolishes CD22 and FcγRII-mediated B cell suppression. J. Exp. Med. 195: 1079-1085. (Pubitemid 34412010)
46. Nardelli, B., O. Belvedere, V. Roschke, P. A. Moore, H. S. Olsen, T. S. Migone, S. Sosnovtseva, J. A. Carrell, P. Feng, J. G. Giri, and D. M. Hilbert. 2001. Synthesis and release of B-lymphocyte stimulator from myeloid cells. Blood 97: 198-204. (Pubitemid 32061261)
47. Ng, L. G., C. H. Ng, B. Woehl, A. P. Sutherland, J. Huo, S. Xu, F. Mackay, and K. P. Lam. 2006. BAFF costimulation of Toll-like receptor-activated B-1 cells. Eur. J. Immunol. 36: 1837-1846. (Pubitemid 44089050)
48. Scapini, P., B. Nardelli, G. Nadali, F. Calzetti, G. Pizzolo, C. Montecucco, and M. A. Cassatella. 2003. G-CSF-stimulated neutrophils are a prominent source of functional BLyS. J. Exp. Med. 197: 297-302. (Pubitemid 36184236)
49. Tedder, T. F., J. Tuscano, S. Sato, and J. H. Kehrl. 1997. CD22, a B lymphocytespecific adhesion molecule that regulates antigen receptor signaling. Annu. Rev. Immunol. 15: 481-504. (Pubitemid 27169290)
50. Adachi, T., S. Harumiya, H. Takematsu, Y. Kozutsumi, M. Wabl, M. Fujimoto, and T. F. Tedder. 2012. CD22 serves as a receptor for soluble IgM. Eur. J. Immunol. 42: 241-247.
51. Lajaunias, F., L. Nitschke, T. Moll, E. Martinez-Soria, I. Semac, Y. Chicheportiche, R. M. Parkhouse, and S. Izui. 2002. Differentially regulated expression and function of CD22 in activated B-1 and B-2 lymphocytes. J. Immunol. 168: 6078-6083. (Pubitemid 34620023)
52. Acosta-Rodríguez, E. V., A. Craxton, D. W. Hendricks, M. C. Merino, C. L. Montes, E. A. Clark, and A. Gruppi. 2007. BAFF and LPS cooperate to induce B cells to become susceptible to CD95/Fas-mediated cell death. Eur. J. Immunol. 37: 990-1000. (Pubitemid 46925336)
53. Mackay, F., S. A. Woodcock, P. Lawton, C. Ambrose, M. Baetscher, P. Schneider, J. Tschopp, and J. L. Browning. 1999. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations. J. Exp. Med. 190: 1697-1710. (Pubitemid 30002351)
54. Fletcher, C. A., J. R. Groom, B. Woehl, H. Leung, C. Mackay, and F. Mackay. 2011. Development of autoimmune nephritis in genetically asplenic and splenectomized BAFF transgenic mice. J. Autoimmun. 36: 125-134.
55. Fletcher, C. A., A. P. Sutherland, J. R. Groom, M. L. Batten, L. G. Ng, J. Gommerman, and F. Mackay. 2006. Development of nephritis but not sialadenitis in autoimmune-prone BAFF transgenic mice lacking marginal zone B cells. Eur. J. Immunol. 36: 2504-2514. (Pubitemid 44420606)
56. Smith, K. G., and M. R. Clatworthy. 2010. FcγRIIB in autoimmunity and infection: evolutionary and therapeutic implications. Nat. Rev. Immunol. 10: 328-343.
57. Mohan, C., L. Morel, P. Yang, and E. K. Wakeland. 1998. Accumulation of splenic B1a cells with potent antigen-presenting capability in NZM2410 lupusprone mice. Arthritis Rheum. 41: 1652-1662. (Pubitemid 28459925)
58. Sato, S., N. Ono, D. A. Steeber, D. S. Pisetsky, and T. F. Tedder. 1996. CD19 regulates B lymphocyte signaling thresholds critical for the development of B-1 lineage cells and autoimmunity. J. Immunol. 157: 4371-4378. (Pubitemid 126449355)
59. Whyburn, L. R., K. E. Halcomb, C. M. Contreras, C. A. Lowell, O. N. Witte, and A. B. Satterthwaite. 2003. Reduced dosage of Bruton's tyrosine kinase uncouples B cell hyperresponsiveness from autoimmunity in lyn2/2 mice. J. Immunol. 171: 1850-1858. (Pubitemid 36966468)
60. Pao, L. I., K. P. Lam, J. M. Henderson, J. L. Kutok, M. Alimzhanov, L. Nitschke, M. L. Thomas, B. G. Neel, and K. Rajewsky. 2007. B cell-specific deletion of protein-tyrosine phosphatase Shp1 promotes B-1a cell development and causes systemic autoimmunity. Immunity 27: 35-48. (Pubitemid 47089020)
61. Bygrave, A. E., K. L. Rose, J. Cortes-Hernandez, J. Warren, R. J. Rigby, H. T. Cook, M. J. Walport, T. J. Vyse, and M. Botto. 2004. Spontaneous autoimmunity in 129 and C57BL/6 mice-implications for autoimmunity described in gene-targeted mice. PLoS Biol. 2: E243.
62. Boross, P., V. L. Arandhara, J. Martin-Ramirez, M. L. Santiago-Raber, F. Carlucci, R. Flierman, J. van der Kaa, C. Breukel, J. W. Claassens, M. Camps, et al. 2011. The inhibiting Fc receptor for IgG, FcγRIIB, is a modifier of autoimmune susceptibility. J. Immunol. 187: 1304-1313.
63. 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)
64. Heyman, B. 2003. Feedback regulation by IgG antibodies. Immunol. Lett. 88: 157-161. (Pubitemid 36859980)
65. +(CD5) B cells that recognize phosphatidyl choline: relationship to cells that secrete hemolytic antibody specific for autologous erythrocytes. J. Exp. Med. 168: 687-698.
66. Brundish, D. E., and J. Baddiley. 1968. Pneumococcal C-substance, a ribitol teichoic acid containing choline phosphate. Biochem. J. 110: 573-582.
67. Chen, Y., Y. B. Park, E. Patel, and G. J. Silverman. 2009. IgM antibodies to apoptosis-associated determinants recruit C1q and enhance dendritic cell phagocytosis of apoptotic cells. J. Immunol. 182: 6031-6043.
68. Chou, M. Y., L. Fogelstrand, K. Hartvigsen, L. F. Hansen, D. Woelkers, P. X. Shaw, J. Choi, T. Perkmann, F. Bäckhed, Y. I. Miller, et al. 2009. Oxidationspecific epitopes are dominant targets of innate natural antibodies in mice and humans. J. Clin. Invest. 119: 1335-1349.
69. Notley, C. A., N. Baker, and M. R. Ehrenstein. 2010. Secreted IgM enhances B cell receptor signaling and promotes splenic but impairs peritoneal B cell survival. J. Immunol. 184: 3386-3393.
70. Shaw, P. X., S. Hörkkö, M. K. Chang, L. K. Curtiss, W. Palinski, G. J. Silverman, and J. L. Witztum. 2000. Natural antibodies with the T15 idiotype may act in atherosclerosis, apoptotic clearance, and protective immunity. J. Clin. Invest. 105: 1731-1740.
71. Kim, S. J., D. Gershov, X. Ma, N. Brot, and K. B. Elkon. 2002. I-PLA2 activation during apoptosis promotes the exposure of membrane lysophosphatidylcholine leading to binding by natural immunoglobulin M antibodies and complement activation. J. Exp. Med. 196: 655-665. (Pubitemid 35024443)
72. Clatworthy, M. R., and K. G. Smith. 2004. FcγRIIb balances efficient pathogen clearance and the cytokine-mediated consequences of sepsis. J. Exp. Med. 199: 717-723. (Pubitemid 38316438)
73. Ivanov, I. I., Rde. L. Frutos, N. Manel, K. Yoshinaga, D. B. Rifkin, R. B. Sartor, B. B. Finlay, and D. R. Littman. 2008. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4: 337-349.
74. Lentz, V. M., C. E. Hayes, and M. P. Cancro. 1998. Bcmd decreases the life span of B-2 but not B-1 cells in A/WySnJ mice. J. Immunol. 160: 3743-3747. (Pubitemid 28176076)
75. Shulga-Morskaya, S., M. Dobles, M. E. Walsh, L. G. Ng, F. MacKay, S. P. Rao, S. L. Kalled, and M. L. Scott. 2004. B cell-activating factor belonging to the TNF family acts through separate receptors to support B cell survival and T cellindependent antibody formation. J. Immunol. 173: 2331-2341. (Pubitemid 39063089)
76. Lin,W. Y., Q. Gong, D. Seshasayee, Z. Lin, Q. Ou, S. Ye, E. Suto, J. Shu,W. P. Lee, C. W. Lee, et al. 2007. Anti-BR3 antibodies: a new class of B-cell immunotherapy combining cellular depletion and survival blockade. Blood 110: 3959-3967. (Pubitemid 350248451)
77. +CD702. J. Exp. Med. 208: 67-80.