Programmed cell death 1 suppresses B-1b cell expansion and long-lived IgG production in response to T cell-independent type 2 antigens

Journal of Immunology

Volumn 187, Issue 10, 2011, Pages 5183-5195

  Haas, Karen M ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE RECEPTOR; CD86 ANTIGEN; FICOLL; HERMES ANTIGEN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G2C; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN M; LEUKOSIALIN; LYMPHOCYTE ANTIGEN; MONOCLONAL ANTIBODY; PICRIC ACID; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; T CELL INDEPENDENT TYPE 2 ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B 1B CELL; B LYMPHOCYTE; CELL DIFFERENTIATION; CELL EXPANSION; CONTROLLED STUDY; IMMUNOGLOBULIN PRODUCTION; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PERITONEAL CAVITY; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION;

ANIMALS; ANTIGENS, T-INDEPENDENT; B-LYMPHOCYTE SUBSETS; CELL DIFFERENTIATION; CELLS, CULTURED; DOWN-REGULATION; FICOLL; GROWTH INHIBITORS; HAPTENS; IMMUNOGLOBULIN G; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROGRAMMED CELL DEATH 1 RECEPTOR; TIME FACTORS; TRINITROBENZENES;

EID: 81455141948     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101990     Document Type: Article

References (69)

1. Wuorimaa, T., and H. Käyhty. 2002. Current state of pneumococcal vaccines. Scand. J. Immunol. 56: 111-129. (Pubitemid 34779853)
2. Vos, Q., A. Lees, Z. Q. Wu, C. M. Snapper, and J. J. Mond. 2000. B-cell activation by T-cell-independent type 2 antigens as an integral part of the humoral immune response to pathogenic microorganisms. Immunol. Rev. 176: 154-170.
3. Wang, T. T., and A. H. Lucas. 2004. The capsule of Bacillus anthracis behaves as a thymus-independent type 2 antigen. Infect. Immun. 72: 5460-5463. (Pubitemid 39223435)
4. Weintraub, A. 2003. Immunology of bacterial polysaccharide antigens. Carbohydr. Res. 338: 2539-2547. (Pubitemid 37521236)
5. Lee, K. C., C. Shiozawa, A. Shaw, and E. Diener. 1976. Requirement for accessory cells in the antibody response to T cell-independent antigens in vitro. Eur. J. Immunol. 6: 63-68.
6. Pinschewer, D. D., A. F. Ochsenbein, A. B. Satterthwaite, O. N. Witte, H. Hengartner, and R. M. Zinkernagel. 1999. A Btk transgene restores the antiviral TI-2 antibody responses of xid mice in a dose-dependent fashion. Eur. J. Immunol. 29: 2981-2987. (Pubitemid 30099022)
7. Freer, G., C. Burkhart, I. Ciernik, M. F. Bachmann, H. Hengartner, and R. M. Zinkernagel. 1994. Vesicular stomatitis virus Indiana glycoprotein as a T-cell-dependent and -independent antigen. J. Virol. 68: 3650-3655. (Pubitemid 24177389)
8. Mazza, G., D. W. Dunne, and A. E. Butterworth. 1990. Antibody isotype responses to the Schistosoma mansoni schistosomulum in the CBA/N mouse induced by different stages of the parasite life cycle. Parasite Immunol. 12: 529-543. (Pubitemid 20317282)
9. Parra, C., J. M. González, E. Castañeda, and S. Fiorentino. 2005. Anti-glucuronoxylomannan IgG1 specific antibodies production in Cryptococcus neoformans resistant mice. Biomedica 25: 110-119.
10. Ortqvist, A. 2001. Pneumococcal vaccination: current and future issues. Eur. Respir. J. 18: 184-195. (Pubitemid 32717448)
11. González-Fernández, A., J. Faro, and C. Fernández. 2008. Immune responses to polysaccharides: lessons from humans and mice. Vaccine 26: 292-300.
12. Weller, S., C. A. Reynaud, and J. C. Weill. 2005. Vaccination against encapsulated bacteria in humans: paradoxes. Trends Immunol. 26: 85-89.
13. Klein Klouwenberg, P., and L. Bont. 2008. Neonatal and infantile immune responses to encapsulated bacteria and conjugate vaccines. Clin. Dev. Immunol. 2008: 628963.
14. 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)
15. Hsu, M. C., K. M. Toellner, C. G. Vinuesa, and I. C. Maclennan. 2006. B cell clones that sustain long-term plasmablast growth in T-independent extrafollicular antibody responses. Proc. Natl. Acad. Sci. USA 103: 5905-5910.
16. Foote, J. B., and J. F. Kearney. 2009. Generation of B cell memory to the bacterial polysaccharide alpha-1,3 dextran. J. Immunol. 183: 6359-6368.
17. 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)
18. Gil-Cruz, C., S. Bobat, J. L. Marshall, R. A. Kingsley, E. A. Ross, I. R. Henderson, D. L. Leyton, R. E. Coughlan, M. Khan, K. T. Jensen, et al. 2009. The porin OmpD from nontyphoidal Salmonella is a key target for a protective B1b cell antibody response. Proc. Natl. Acad. Sci. USA 106: 9803-9808.
19. Colombo, M. J., and K. R. Alugupalli. 2008. Complement factor H-binding protein, a putative virulence determinant of Borrelia hermsii, is an antigenic target for protective B1b lymphocytes. J. Immunol. 180: 4858-4864.
20. Alugupalli, K. R. 2008. A distinct role for B1b lymphocytes in T cell-independent immunity. Curr. Top. Microbiol. Immunol. 319: 105-130.
21. 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)
22. Cole, L. E., Y. Yang, K. L. Elkins, E. T. Fernandez, N. Qureshi, M. J. Shlomchik, L. A. Herzenberg, L. A. Herzenberg, and S. N. Vogel. 2009. Antigen-specific B-1a antibodies induced by Francisella tularensis LPS provide long-term protection against F. tularensis LVS challenge. Proc. Natl. Acad. Sci. USA 106: 4343-4348.
23. Baumgarth, N. 2011. The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat. Rev. Immunol. 11: 34-46.
24. Obukhanych, T. V., and M. C. Nussenzweig. 2006. T-independent type II immune responses generate memory B cells. J. Exp. Med. 203: 305-310. (Pubitemid 43290839)
25. Patterson, H. C., M. Kraus, Y. M. Kim, H. Ploegh, and K. Rajewsky. 2006. The B cell receptor promotes B cell activation and proliferation through a non-ITAM tyrosine in the Igalpha cytoplasmic domain. Immunity 25: 55-65. (Pubitemid 44066828)
26. Fruman, D. A., A. B. Satterthwaite, and O. N. Witte. 2000. Xid-like phenotypes: a B cell signalosome takes shape. Immunity 13: 1-3.
27. Haas, K. M., J. C. Poe, and T. F. Tedder. 2009. CD21/35 promotes protective immunity to Streptococcus pneumoniae through a complement-independent but CD19-dependent pathway that regulates PD-1 expression. J. Immunol. 183: 3661-3671.
28. Okazaki, T., and T. Honjo. 2007. PD-1 and PD-1 ligands: from discovery to clinical application. Int. Immunol. 19: 813-824. (Pubitemid 47241890)
29. Nishimura, H., N. Minato, T. Nakano, and T. Honjo. 1998. Immunological studies on PD-1 deficient mice: implication of PD-1 as a negative regulator for B cell responses. Int. Immunol. 10: 1563-1572. (Pubitemid 28451451)
30. Samardzic, T., D. Marinkovic, C.-P. Danzer, J. Gerlach, L. Nitschke, and T. Wirth. 2002. Reduction of marginal zone B cells in CD22-deficient mice. Eur. J. Immunol. 32: 561-567. (Pubitemid 34173347)
31. Guinamard, R., M. Okigaki, J. Schlessinger, and J. V. Ravetch. 2000. Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response. Nat. Immunol. 1: 31-36.
32. Haas, K. M., M. Hasegawa, D. A. Steeber, J. C. Poe, M. D. Zabel, C. B. Bock, D. R. Karp, D. E. Briles, J. H. Weis, and T. F. Tedder. 2002. Complement receptors CD21/35 link innate and protective immunity during Streptococcus pneumoniae infection by regulating IgG3 antibody responses. Immunity 17: 713-723. (Pubitemid 35477791)
33. Cobern, L., and P. Selvaraj. 1995. An enzymatic method to determine receptor-mediated endocytosis. J. Biochem. Biophys. Methods 30: 249-255.
34. Ohdan, H., K. G. Swenson, H. S. Kruger Gray, Y. G. Yang, Y. Xu, A. D. Thall, and M. Sykes. 2000. Mac-1-negative B-1b phenotype of natural antibody-producing cells, including those responding to Gal alpha 1,3Gal epitopes in alpha 1,3-galactosyltransferase-deficient mice. J. Immunol. 165: 5518-5529.
35. Yang, Y., J. W. Tung, E. E. Ghosn, L. A. Herzenberg, and L. A. Herzenberg. 2007. Division and differentiation of natural antibody-producing cells in mouse spleen. Proc. Natl. Acad. Sci. USA 104: 4542-4546. (Pubitemid 47186261)
36. Kawahara, T., H. Ohdan, G. Zhao, Y. G. Yang, and M. Sykes. 2003. Peritoneal cavity B cells are precursors of splenic IgM natural antibody-producing cells. J. Immunol. 171: 5406-5414. (Pubitemid 37432827)
37. -B cells with anti-Ig, but not LPS, induces surface CD5: two B-cell activation pathways. Int. Immunol. 3: 467-476.
38. Zhong, X., C. Bai, W. Gao, T. B. Strom, and T. L. Rothstein. 2004. Suppression of expression and function of negative immune regulator PD-1 by certain pattern recognition and cytokine receptor signals associated with immune system danger. Int. Immunol. 16: 1181-1188. (Pubitemid 39136735)
39. Racine, R., M. Chatterjee, and G. M. Winslow. 2008. CD11c expression identifies a population of extrafollicular antigen-specific splenic plasmablasts responsible for CD4 T-independent antibody responses during intracellular bacterial infection. J. Immunol. 181: 1375-1385.
40. Taillardet, M., G. Haffar, P. Mondière, M. J. Asensio, H. Gheit, N. Burdin, T. Defrance, and L. Genestier. 2009. The thymus-independent immunity conferred by a pneumococcal polysaccharide is mediated by long-lived plasma cells. Blood 114: 4432-4440.
41. Slifka, M. K., M. Matloubian, and R. Ahmed. 1995. Bone marrow is a major site of long-term antibody production after acute viral infection. J. Virol. 69: 1895-1902.
42. Keir, M. E., M. J. Butte, G. J. Freeman, and A. H. Sharpe. 2008. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 26: 677-704. (Pubitemid 351600389)
43. Swanson, C. L., T. J. Wilson, P. Strauch, M. Colonna, R. Pelanda, and R. M. Torres. 2010. Type I IFN enhances follicular B cell contribution to the T cell-independent antibody response. J. Exp. Med. 207: 1485-1500.
44. Martin, F., and J. F. Kearney. 2002. Marginal-zone B cells. Nat. Rev. Immunol. 2: 323-335. (Pubitemid 37328755)
45. Hayakawa, K., R. R. Hardy, M. Honda, L. A. Herzenberg, A. D. Steinberg, and L. A. Herzenberg. 1984. Ly-1 B cells: functionally distinct lymphocytes that secrete IgM autoantibodies. Proc. Natl. Acad. Sci. USA 81: 2494-2498.
46. Shriner, A. K., H. Liu, G. Sun, M. Guimond, and K. R. Alugupalli. 2010. IL-7-dependent B lymphocytes are essential for the anti-polysaccharide response and protective immunity to Streptococcus pneumoniae. J. Immunol. 185: 525-531.
47. 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)
48. Racine, R., M. McLaughlin, D. D. Jones, S. T. Wittmer, K. C. MacNamara, D. L. Woodland, and G. M. Winslow. 2011. IgM production by bone marrow plasmablasts contributes to long-term protection against intracellular bacterial infection. J. Immunol. 186: 1011-1021.
49. Whitmore, A. C., H. R. Neely, R. Diz, and P. M. Flood. 2004. Rapid induction of splenic and peritoneal B-1a cells in adult mice by thymus-independent type-2 antigen. J. Immunol. 173: 5406-5414. (Pubitemid 39392124)
50. Shih, T. A., M. Roederer, and M. C. Nussenzweig. 2002. Role of antigen receptor affinity in T cell-independent antibody responses in vivo. Nat. Immunol. 3: 399-406. (Pubitemid 34308629)
51. de Vinuesa, C. G., M. C. Cook, J. Ball, M. Drew, Y. Sunners, M. Cascalho, M. Wabl, G. G. Klaus, and I. C. MacLennan. 2000. Germinal centers without T cells. J. Exp. Med. 191: 485-494.
52. Deenick, E. K., J. Hasbold, and P. D. Hodgkin. 1999. Switching to IgG3, IgG2b, and IgA is division linked and independent, revealing a stochastic framework for describing differentiation. J. Immunol. 163: 4707-4714. (Pubitemid 29501231)
53. Rush, J. S., M. Liu, V. H. Odegard, S. Unniraman, and D. G. Schatz. 2005. Expression of activation-induced cytidine deaminase is regulated by cell division, providing a mechanistic basis for division-linked class switch recombination. Proc. Natl. Acad. Sci. USA 102: 13242-13247. (Pubitemid 41325008)
54. Velu, V., K. Titanji, B. Zhu, S. Husain, A. Pladevega, L. Lai, T. H. Vanderford, L. Chennareddi, G. Silvestri, G. J. Freeman, et al. 2009. Enhancing SIV-specific immunity in vivo by PD-1 blockade. Nature 458: 206-210.
55. Titanji, K., V. Velu, L. Chennareddi, M. Vijay-Kumar, A. T. Gewirtz, G. J. Freeman, and R. R. Amara. 2010. Acute depletion of activated memory B cells involves the PD-1 pathway in rapidly progressing SIV-infected macaques. J. Clin. Invest. 120: 3878-3890.
56. Good-Jacobson, K. L., C. G. Szumilas, L. Chen, A. H. Sharpe, M. M. Tomayko, and M. J. Shlomchik. 2010. PD-1 regulates germinal center B cell survival and the formation and affinity of long-lived plasma cells. Nat. Immunol. 11: 535-542.
57. Hippen, K. L., L. E. Tze, and T. W. Behrens. 2000. CD5 maintains tolerance in anergic B cells. J. Exp. Med. 191: 883-890.
58. Bikah, G., J. Carey, J. R. Ciallella, A. Tarakhovsky, and S. Bondada. 1996. CD5-mediated negative regulation of antigen receptor-induced growth signals in B-1 B cells. Science 274: 1906-1909. (Pubitemid 26424770)
59. O'Keefe, T. L., G. T. Williams, F. D. Batista, and M. S. Neuberger. 1999. Deficiency in CD22, a B cell-specific inhibitory receptor, is sufficient to predispose to development of high affinity autoantibodies. J. Exp. Med. 189: 1307-1313. (Pubitemid 29198268)
60. Poe, J. C., S. H. Smith, K. M. Haas, K. Yanaba, T. Tsubata, T. Matsushita, and T. F. Tedder. 2011. Amplified B Lymphocyte CD40 Signaling Drives Regulatory B10 Cell Expansion in Mice. PLoS ONE 6: e22464.
61. Nishimura, H., M. Nose, H. Hiai, N. Minato, and T. Honjo. 1999. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 11: 141-151. (Pubitemid 29428807)
62. Nishimura, H., T. Okazaki, Y. Tanaka, K. Nakatani, M. Hara, A. Matsumori, S. Sasayama, A. Mizoguchi, H. Hiai, N. Minato, and T. Honjo. 2001. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 291: 319-322. (Pubitemid 32096320)
63. Otipoby, K. L., K. B. Andersson, K. E. Draves, S. J. Klaus, A. G. Farr, J. D. Kerner, R. M. Perlmutter, C.-L. Law, and E. A. Clark. 1996. CD22 regulates thymus-independent responses and the lifespan of B cells. Nature 384: 634-637.
64. Nitschke, L., R. Carsetti, B. Ocker, G. Köhler, and M. C. Lamers. 1997. CD22 is a negative regulator of B-cell receptor signalling. Curr. Biol. 7: 133-143. (Pubitemid 27155622)
65. Sato, S., A. S. Miller, M. Inaoki, C. B. Bock, P. J. Jansen, M. L. K. Tang, and T. F. Tedder. 1996. CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice. Immunity 5: 551-562. (Pubitemid 27062065)
66. Haas, K. M., S. Sen, I. G. Sanford, A. S. Miller, J. C. Poe, and T. F. Tedder. 2006. CD22 ligand binding regulates normal and malignant B lymphocyte survival in vivo. J. Immunol. 177: 3063-3073. (Pubitemid 44277823)
67. Tarakhovsky, A., W. Müller, and K. Rajewsky. 1994. Lymphocyte populations and immune responses in CD5-deficient mice. Eur. J. Immunol. 24: 1678-1684. (Pubitemid 24203778)
68. Duong, B. H., H. Tian, T. Ota, G. Completo, S. Han, J. L. Vela, M. Ota, M. Kubitz, N. Bovin, J. C. Paulson, and D. Nemazee. 2010. Decoration of T-independent antigen with ligands for CD22 and Siglec-G can suppress immunity and induce B cell tolerance in vivo. [Published erratum appears in 2010 J. Exp. Med. 207: 445.] J. Exp. Med. 207: 173-187.
69. Griffin, D. O., N. E. Holodick, and T. L. Rothstein. 2011. Human B1 cells in umbilical cord and adult peripheral blood express the novel phenotype CD20+ CD27+ CD43+ CD702. J. Exp. Med. 208: 67-80.