NF-κB2/p100 deficiency impairs immune responses to T-cell-independent type 2 antigens

European Journal of Immunology

Volumn 44, Issue 3, 2014, Pages 662-672

  Krljanac, Branislav ^a   Weih, Debra ^a   Jacobsen, Ilse D ^b   Hu, Desheng ^a   Koliesnik, Ievgen ^a   Reppe, Katrin ^c   Witzenrath, Martin ^c   Weih, Falk ^a,d  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b HANS KNÖLL INSTITUTE   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

Alternative NF B pathway; B 1 cells; Marginal zone B cells; Streptococcus pneumoniae; TI 2 immune response

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN M; PROTEIN P100; T CELL INDEPENDENT TYPE 2 ANTIGEN; T LYMPHOCYTE ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; HUMORAL IMMUNITY; IMMUNE RESPONSE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; STREPTOCOCCUS PNEUMONIA;

ALTERNATIVE NF-ΚB PATHWAY; B-1 CELLS; MARGINAL ZONE B CELLS; STREPTOCOCCUS PNEUMONIAE; TI-2 IMMUNE RESPONSE;

ANIMALS; ANTIBODY FORMATION; ANTIGENS, T-INDEPENDENT; B-LYMPHOCYTE SUBSETS; BACTERIA; BACTERIAL INFECTIONS; CELL MOVEMENT; CYTOKINES; GENETIC PREDISPOSITION TO DISEASE; IMMUNITY, HUMORAL; MICE; MICE, KNOCKOUT; NF-KAPPA B P52 SUBUNIT; PROTEIN BINDING; PROTEIN TRANSPORT; RECEPTORS, ANTIGEN, B-CELL; TOLL-LIKE RECEPTORS; TRANSCRIPTION FACTOR RELB;

EID: 84896034143     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343484     Document Type: Article

References (49)

1. Mond, J. J., Lees, A. and Snapper, C. M., T cell-independent antigens type 2. Annu. Rev. Immunol. 1995. 13: 655-692.
2. Vos, Q., Lees, A., Wu, Z. Q., Snapper, C. M. and Mond, J. J., B-cell activation by T-cell-independent type 2 antigens as an integral part of the humoral immune response to pathogenic microorganisms. Immunol. Rev. 2000. 176: 154-170.
3. AlonsoDeVelasco, E., Verheul, A. F., Verhoef, J. and Snippe, H., Streptococcus pneumoniae: virulence factors, pathogenesis, and vaccines. Microbiol. Rev. 1995. 59: 591-603.
4. Guinamard, R., Okigaki, M., Schlessinger, J. and Ravetch, J. V., Absence of marginal zone B cells in Pyk-2-deficient mice defines their role in the humoral response. Nat. Immunol. 2000. 1: 31-36.
5. Martin, F., Oliver, A. M. and Kearney, J. F., Marginal zone and B1 B cells unite in the early response against T-independent blood-borne particulate antigens. Immunity 2001. 14: 617-629.
6. Hsu, M. C., Toellner, K. M., Vinuesa, C. G. and Maclennan, I. C., B cell clones that sustain long-term plasmablast growth in T-independent extrafollicular antibody responses. Proc. Natl. Acad. Sci. USA 2006. 103: 5905-5910.
7. Mebius, R. E. and Kraal, G., Structure and function of the spleen. Nat. Rev. Immunol. 2005. 5: 606-616.
8. Pillai, S., Cariappa, A. and Moran, S. T., Marginal zone B cells. Annu. Rev. Immunol. 2005. 23: 161-196.
9. Cinamon, G., Matloubian, M., Lesneski, M. J., Xu, Y., Low, C., Lu, T., Proia, R. L. et al., Sphingosine 1-phosphate receptor 1 promotes B cell localization in the splenic marginal zone. Nat. Immunol. 2004. 5: 713-720.
10. Van den Eertwegh, A. J., Schellekens, M. M., Boersma, W. J. and Claassen, E., Differential uptake and trapping of TI-2 antigens: an unexpected role for follicular dendritic cells in the induction of TI-2 immune responses. Adv. Exp. Med. Biol. 1993. 329: 345-351.
11. van den Eertwegh, A. J., Laman, J. D., Schellekens, M. M., Boersma, W. J. and Claassen, E., Complement-mediated follicular localization of T-independent type-2 antigens: the role of marginal zone macrophages revisited. Eur. J. Immunol. 1992. 22: 719-726.
12. Baumgarth, N., The double life of a B-1 cell: self-reactivity selects for protective effector functions. Nat. Rev. Immunol. 2011. 11: 34-46.
13. Haas, K. M., Programmed cell death 1 suppresses B-1b cell expansion and long-lived IgG production in response to T cell-independent type 2 antigens. J. Immunol. 2011. 187: 5183-5195.
14. Chelvarajan, R. L., Gilbert, N. L. and Bondada, S., Neonatal murine B lymphocytes respond to polysaccharide antigens in the presence of IL-1 and IL-6. J. Immunol. 1998. 161: 3315-3324.
15. Alugupalli, K. R., Leong, J. M., Woodland, R. T., Muramatsu, M., Honjo, T. and Gerstein, R. M., B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 2004. 21: 379-390.
16. Haas, K. M., Poe, J. C., Steeber, D. A. and Tedder, T. F., B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 2005. 23: 7-18.
17. Alugupalli, K. R., A distinct role for B1b lymphocytes in T cell-independent immunity. Curr. Top. Microbiol. Immunol. 2008. 319: 105-130.
18. Kantor, A. B. and Herzenberg, L. A., Origin of murine B cell lineages. Annu. Rev. Immunol. 1993. 11: 501-538.
19. Nielsen, C. H., Fischer, E. M. and Leslie, R. G., The role of complement in the acquired immune response. Immunology 2000. 100: 4-12.
20. + marginal zone B cell production of pathogenic natural antibodies is C3 independent. J. Immunol. 2011. 186: 1755-1762.
21. Suzuki, K., Maruya, M., Kawamoto, S. and Fagarasan, S., Roles of B-1 and B-2 cells in innate and acquired IgA-mediated immunity. Immunol. Rev. 2010. 237: 180-190.
22. Briles, D. E., Nahm, M., Schroer, K., Davie, J., Baker, P., Kearney, J. and Barletta, R., Antiphosphocholine antibodies found in normal mouse serum are protective against intravenous infection with type 3 Streptococcus pneumoniae. J. Exp. Med. 1981. 153: 694-705.
23. Durand, C. A., Hartvigsen, K., Fogelstrand, L., Kim, S., Iritani, S., Vanhaesebroeck, B., Witztum, J. L. et al., Phosphoinositide 3-kinase p110 delta regulates natural antibody production, marginal zone and B-1 B cell function, and autoantibody responses. J. Immunol. 2009. 183: 5673-5684.
24. Hayden, M. S. and Ghosh, S., NF-kB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 2012. 26: 203-234.
25. Ishikawa, H., Carrasco, D., Claudio, E., Ryseck, R. P. and Bravo, R., Gastric hyperplasia and increased proliferative responses of lymphocytes in mice lacking the COOH-terminal ankyrin domain of NF-kB2. J. Exp. Med. 1997. 186: 999-1014.
26. Guo, F., Weih, D., Meier, E. and Weih, F., Constitutive alternative NF-kB signaling promotes marginal zone B-cell development but disrupts the marginal sinus and induces HEV-like structures in the spleen. Blood 2007. 110: 2381-2389.
27. Weih, D. S., Yilmaz, Z. B. and Weih, F., Essential role of RelB in germinal center and marginal zone formation and proper expression of homing chemokines. J. Immunol. 2001. 167: 1909-1919.
28. Guo, F., Tanzer, S., Busslinger, M. and Weih, F., Lack of nuclear factor-kB2/p100 causes a RelB-dependent block in early B lymphopoiesis. Blood 2008. 112: 551-559.
29. Shriner, A. K., Liu, H., Sun, G., Guimond, M. and Alugupalli, K. R., IL-7-dependent B lymphocytes are essential for the anti-polysaccharide response and protective immunity to Streptococcus pneumoniae. J. Immunol. 2010. 185: 525-531.
30. Garcia de Vinuesa, C., O'Leary, P., Sze, D. M., Toellner, K. M. and MacLennan, I. C., T-independent type 2 antigens induce B cell proliferation in multiple splenic sites, but exponential growth is confined to extrafollicular foci. Eur. J. Immunol. 1999. 29: 1314-1323.
31. Alugupalli, K. R. and Gerstein, R. M., Divide and conquer: division of labor by B-1 B cells. Immunity 2005. 23: 1-2.
32. Briles, D. E., Claflin, J. L., Schroer, K. and Forman, C., Mouse Igg3 antibodies are highly protective against infection with Streptococcus pneumoniae. Nature 1981. 294: 88-90.
33. McLay, J., Leonard, E., Petersen, S., Shapiro, D., Greenspan, N. S. and Schreiber, J. R., Gamma 3 gene-disrupted mice selectively deficient in the dominant IgG subclass made to bacterial polysaccharides. II. Increased susceptibility to fatal pneumococcal sepsis due to absence of anti-polysaccharide IgG3 is corrected by induction of anti-polysaccharide IgG1. J. Immunol. 2002. 168: 3437-3443.
34. Zandvoort, A. and Timens, W., The dual function of the splenic marginal zone: essential for initiation of anti-TI-2 responses but also vital in the general first-line defense against blood-borne antigens. Clin. Exp. Immunol. 2002. 130: 4-11.
35. Cinamon, G., Zachariah, M. A., Lam, O. M., Foss, F. W., Jr. and Cyster, J. G., Follicular shuttling of marginal zone B cells facilitates antigen transport. Nat. Immunol. 2008. 9: 54-62.
36. Wortis, H. H., Teutsch, M., Higer, M., Zheng, J. and Parker, D. C., B-cell activation by crosslinking of surface IgM or ligation of CD40 involves alternative signal pathways and results in different B-cell phenotypes. Proc. Natl. Acad. Sci. USA 1995. 92: 3348-3352.
37. Balazs, M., Martin, F., Zhou, T. and Kearney, J., Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 2002. 17: 341-352.
38. Taccioli, G. E., Rathbun, G., Oltz, E., Stamato, T., Jeggo, P. A. and Alt, F. W., Impairment of V(D)J recombination in double-strand break repair mutants. Science 1993. 260: 207-210.
39. Rosado, M. M., Aranburu, A., Capolunghi, F., Giorda, E., Cascioli, S., Cenci, F., Petrini, S. et al., From the fetal liver to spleen and gut: the highway to natural antibody. Mucosal Immunol. 2009. 2: 351-361.
40. Miyawaki, S., Nakamura, Y., Suzuka, H., Koba, M., Yasumizu, R., Ikehara, S. and Shibata, Y., A new mutation, aly, that induces a generalized lack of lymph nodes accompanied by immunodeficiency in mice. Eur. J. Immunol. 1994. 24: 429-434.
41. Fagarasan, S., Shinkura, R., Kamata, T., Nogaki, F., Ikuta, K., Tashiro, K. and Honjo, T., Alymphoplasia (aly)-type nuclear factor kB-inducing kinase (NIK) causes defects in secondary lymphoid tissue chemokine receptor signaling and homing of peritoneal cells to the gut-associated lymphatic tissue system. J. Exp. Med. 2000. 191: 1477-1486.
42. Carrasco, D., Cheng, J., Lewin, A., Warr, G., Yang, H., Rizzo, C., Rosas, F. et al., Multiple hemopoietic defects and lymphoid hyperplasia in mice lacking the transcriptional activation domain of the c-Rel protein. J. Exp. Med. 1998. 187: 973-984.
43. Foote, J. B. and Kearney, J. F., Generation of B cell memory to the bacterial polysaccharide a-1, 3 dextran. J. Immunol. 2009. 183: 6359-6368.
44. Caamaño, J., Alexander, J., Craig, L., Bravo, R. and Hunter, C. A., The NF-kB family member RelB is required for innate and adaptive immunity to Toxoplasma gondii. J. Immunol. 1999. 163: 4453-4461.
45. Koedel, U., Rupprecht, T., Angele, B., Heesemann, J., Wagner, H., Pfister, H. W. and Kirschning, C. J., MyD88 is required for mounting a robust host immune response to Streptococcus pneumoniae in the CNS. Brain 2004. 127:1437-1445.
46. Shih, V. F.-S., Davis-Turak, J., Macal, M., Huang, J. Q., Ponomarenko, J., Kearns, J., Yu, T. et al., Control of RelB during dendritic cell activation integrates canonical and noncanonical NF-κB pathways. Nat. Immunol. 2012. 13: 1162-1170.
47. Franzoso, G., Carlson, L., Poljak, L., Shores, E. W., Epstein, S., Leonardi, A., Grinberg, A. et al., Mice deficient in nuclear factor (NF)-kB/p52 present with defects in humoral responses, germinal center reactions, and splenic microarchitecture. J. Exp. Med. 1998. 187: 147-159.
48. Wang, X., Belguise, K., O'Neill, C. F., Sanchez-Morgan, N., Romagnoli, M., Eddy, S. F., Mineva, N. D. et al., RelB NF-kB represses estrogen receptor alpha expression via induction of the zinc finger protein Blimp1. Mol. Cell. Biol. 2009. 29: 3832-3844.
49. Kallies, A., Hasbold, J., Tarlinton, D. M., Dietrich, W., Corcoran, L. M., Hodgkin, P. D. and Nutt, S. L., Plasma cell ontogeny defined by quantitative changes in blimp-1 expression. J. Exp. Med. 2004. 200: 967-977.