IFN-γ-producing CD4+ T cells promote generation of protective germinal center-derived IgM+ B cell memory against salmonella typhi

Journal of Immunology

Volumn 192, Issue 11, 2014, Pages 5192-5200

  Perez Shibayama, Christian ^a,b   Gil Cruz, Cristina ^a,b   Pastelin Palacios, Rodolfo ^c   Cervantes Barragan, Luisa ^a,d   Hisaki, Emiliano ^b   Chai, Qian ^a   Onder, Lucas ^a   Scandella, Elke ^a   Regen, Tommy ^e   Waisman, Ari ^e   Isibasi, Armando ^b   Lopez Macias, Constantino ^b   Ludewig, Burkhard ^a  

^a CANTONAL HOSPITAL ST GALLEN   (Switzerland)

^b HOSPITAL DE ESPECIALIDADES   (Mexico)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE RECEPTOR; GAMMA INTERFERON; IMMUNOGLOBULIN M; IMMUNOGLOBULIN M ANTIBODY; INTERLEUKIN 17; OUTER MEMBRANE PROTEIN C; OUTER MEMBRANE PROTEIN F; TYPHOID VACCINE;

ARTICLE; B LYMPHOCYTE; BACTERIAL CLEARANCE; BACTERICIDAL ACTIVITY; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; GERMINAL CENTER; HELPER CELL; HUMAN; HUMAN CELL; IMMUNOGLOBULIN M+ B LYMPHOCYTE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SALMONELLA TYPHI; SIGNAL TRANSDUCTION; TYPHOID FEVER; VACCINATION;

ANIMALS; B-LYMPHOCYTES; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; GERMINAL CENTER; HUMANS; IMMUNOGLOBULIN M; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; MALE; MICE; MICE, KNOCKOUT; SALMONELLA TYPHI; SALMONELLA VACCINES; TYPHOID FEVER;

EID: 84901247777     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1302526     Document Type: Article

References (61)

1. Crump, J. A., S. P. Luby, and E. D. Mintz. 2004. The global burden of typhoid fever. Bull. World Health Organ. 82: 346-353.
2. Buckle, G. C., C. L. Walker, and R. E. Black. 2012. Typhoid fever and paratyphoid fever: systematic review to estimate global morbidity and mortality for 2010. J. Glob. Health 2: 010401.
3. Martin, L. B. 2012. Vaccines for typhoid fever and other salmonelloses. Curr. Opin. Infect. Dis. 25: 489-499.
4. MacLennan, C. A., J. J. Gilchrist, M. A. Gordon, A. F. Cunningham, M. Cobbold, M. Goodall, R. A. Kingsley, J. J. van Oosterhout, C. L. Msefula, W. L. Mandala, et al. 2010. Dysregulated humoral immunity to nontyphoidal Salmonella in HIV-infected African adults. Science 328: 508-512.
5. Monack, D. M. 2012. Salmonella persistence and transmission strategies. Curr. Opin. Microbiol. 15: 100-107.
6. Levine, M. M., C. O. Tacket, and M. B. Sztein. 2001. Host-Salmonella interaction: human trials. Microbes Infect. 3: 1271-1279.
7. Galen, J. E., M. F. Pasetti, S. Tennant, P. Ruiz-Olvera, M. B. Sztein, and M. M. Levine. 2009. Salmonella enterica serovar Typhi live vector vaccines finally come of age. Immunol. Cell Biol. 87: 400-412.
8. Simon, R., and M. M. Levine. 2012. Glycoconjugate vaccine strategies for protection against invasive Salmonella infections. Hum. Vaccin. Immunother. 8: 494-498.
9. Isibasi, A., V. Ortiz-Navarrete, J. Paniagua, R. Pelayo, C. R. González, J. A. García, and J. Kumate. 1992. Active protection of mice against Salmonella typhi by immunization with strain-specific porins. Vaccine 10: 811-813.
10. Singh, M., N. K. Ganguly, L. Kumar, and H. Vohra. 1999. Protective efficacy and immunogenicity of Vi-porin conjugate against Salmonella typhi. Microbiol. Immunol. 43: 535-542.
11. Wetzler, L. M., Y. Ho, and H. Reiser. 1996. Neisserial porins induce B lymphocytes to express costimulatory B7-2 molecules and to proliferate. [Published erratum appears in 1996 J. Exp. Med. 184: 1197.] J. Exp. Med. 183: 1151-1159.
12. Massari, P., P. Henneke, Y. Ho, E. Latz, D. T. Golenbock, and L. M. Wetzler. 2002. Cutting edge: immune stimulation by neisserial porins is toll-like receptor 2 and MyD88 dependent. J. Immunol. 168: 1533-1537.
13. Galdiero, M., M. Galdiero, E. Finamore, F. Rossano, M. Gambuzza, M. R. Catania, G. Teti, A. Midiri, and G. Mancuso. 2004. Haemophilus influenzae porin induces Toll-like receptor 2-mediated cytokine production in human monocytes and mouse macrophages. Infect. Immun. 72: 1204-1209.
14. Cervantes-Barragán, L., C. Gil-Cruz, R. Pastelin-Palacios, K. S. Lang, A. Isibasi, B. Ludewig, and C. López-Macías. 2009. TLR2 and TLR4 signaling shapes specific antibody responses to Salmonella typhi antigens. Eur. J. Immunol. 39: 126-135.
15. Calderón, I., S. R. Lobos, H. A. Rojas, C. Palomino, L. H. Rodríguez, and G. C. Mora. 1986. Antibodies to porin antigens of Salmonella typhi induced during typhoid infection in humans. Infect. Immun. 52: 209-212.
16. Ortiz, V., A. Isibasi, E. García-Ortigoza, and J. Kumate. 1989. Immunoblot detection of class-specific humoral immune response to outer membrane proteins isolated from Salmonella typhi in humans with typhoid fever. J. Clin. Microbiol. 27: 1640-1645.
17. Salazar-González, R. M., C. Maldonado-Bernal, N. E. Ramírez-Cruz, N. Rios- Sarabia, J. Beltrán-Nava, J. Castañón-González, N. Castillo-Torres, J. A. Palma- Aguirre, M. Carrera-Camargo, C. López-Macías, and A. Isibasi. 2004. Induction of cellular immune response and anti-Salmonella enterica serovar typhi bactericidal antibodies in healthy volunteers by immunization with a vaccine candidate against typhoid fever. Immunol. Lett. 93: 115-122.
18. Secundino, I., C. López-Macías, L. Cervantes- Barragán, C. Gil-Cruz, N. Ríos- Sarabia, R. Pastelin-Palacios, M. A. Villasis-Keever, I. Becker, J. L. Puente, E. Calva, and A. Isibasi. 2006. Salmonella porins induce a sustained, lifelong specific bactericidal antibody memory response. Immunology 117: 59-70.
19. Moreno-Eutimio, M. A., A. Tenorio-Calvo, R. Pastelin-Palacios, C. Perez- Shibayama, C. Gil-Cruz, R. López-Santiago, I. Baeza, M. Fernández-Mora, L. Bonifaz, A. Isibasi, et al. 2013. Salmonella Typhi OmpS1 and OmpS2 porins are potent protective immunogens with adjuvant properties. Immunology 139: 459-471.
20. MacLennan, C. A., E. N. Gondwe, C. L. Msefula, R. A. Kingsley, N. R. Thomson, S. A. White, M. Goodall, D. J. Pickard, S. M. Graham, G. Dougan, et al. 2008. The neglected role of antibody in protection against bacteremia caused by nontyphoidal strains of Salmonella in African children. J. Clin. Invest. 118: 1553-1562.
21. Trebicka, E., S. Jacob, W. Pirzai, B. P. Hurley, and B. J. Cherayil. 2013. Role of antilipopolysaccharide antibodies in serum bactericidal activity against Salmonella enterica serovar Typhimurium in healthy adults and children in the United States. Clin. Vaccine Immunol. 20: 1491-1498.
22. 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.
23. Marshall, J. L., A. Flores-Langarica, R. A. Kingsley, J. R. Hitchcock, E. A. Ross, C. López-Macías, J. Lakey, L. B. Martin, K. M. Toellner, C. A. MacLennan, et al. 2012. The capsular polysaccharide Vi from Salmonella typhi is a B1b antigen. J. Immunol. 189: 5527-5532.
24. MacLennan, I. C. 1994. Germinal centers. Annu. Rev. Immunol. 12:117-139.
25. McHeyzer-Williams, M., S. Okitsu, N. Wang, and L. McHeyzer-Williams. 2012. Molecular programming of B cell memory. Nat. Rev. Immunol. 12: 24-34.
26. Weill, J. C., S. Le Gallou, Y. Hao, and C. A. Reynaud. 2013. Multiple players in mouse B cell memory. Curr. Opin. Immunol. 25: 334-338.
27. Dogan, I., B. Bertocci, V. Vilmont, F. Delbos, J. Mégret, S. Storck, C. A. Reynaud, and J. C. Weill. 2009. Multiple layers of B cell memory with different effector functions. Nat. Immunol. 10: 1292-1299.
28. Pape, K. A., J. J. Taylor, R. W. Maul, P. J. Gearhart, and M. K. Jenkins. 2011. Different B cell populations mediate early and late memory during an endogenous immune response. Science 331: 1203-1207.
29. Zinkernagel, R. M. 1996. Immunology taught by viruses. Science 271: 173-178.
30. Hangartner, L., R. M. Zinkernagel, and H. Hengartner. 2006. Antiviral antibody responses: the two extremes of a wide spectrum. Nat. Rev. Immunol. 6: 231-243.
31. Gil-Cruz, C., C. Perez-Shibayama, S. Firner, A. Waisman, I. Bechmann, V. Thiel, L. Cervantes-Barragan, and B. Ludewig. 2012. T helper cell- and CD40-dependent germline IgM prevents chronic virus-induced demyelinating disease. Proc. Natl. Acad. Sci. USA 109: 1233-1238.
32. Cannons, J. L., K. T. Lu, and P. L. Schwartzberg. 2013. T follicular helper cell diversity and plasticity. Trends Immunol. 34: 200-207.
33. Fazilleau, N., L. J. McHeyzer-Williams, H. Rosen, and M. G. McHeyzer-Williams. 2009. The function of follicular helper T cells is regulated by the strength of T cell antigen receptor binding. Nat. Immunol. 10: 375-384.
34. Choi, Y. S., R. Kageyama, D. Eto, T. C. Escobar, R. J. Johnston, L. Monticelli, C. Lao, and S. Crotty. 2011. ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 34: 932-946.
35. Hess, J., C. Ladel, D. Miko, and S. H. Kaufmann. 1996. Salmonella typhimurium aroA- infection in gene-targeted immunodeficient mice: major role of CD4+ TCR-alpha beta cells and IFN-gamma in bacterial clearance independent of intracellular location. J. Immunol. 156: 3321-3326.
36. Mittrucker, H. W., A. Köhler, and S. H. Kaufmann. 2002. Characterization of the murine T-lymphocyte response to Salmonella enterica serovar Typhimurium infection. Infect. Immun. 70: 199-203.
37. MacLennan, C., C. Fieschi, D. A. Lammas, C. Picard, S. E. Dorman, O. Sanal, J. M. MacLennan, S. M. Holland, T. H. Ottenhoff, J. L. Casanova, and D. S. Kumararatne. 2004. Interleukin (IL)-12 and IL-23 are key cytokines for immunity against Salmonella in humans. J. Infect. Dis. 190: 1755-1757.
38. Jouanguy, E., R. Döffinger, S. Dupuis, A. Pallier, F. Altare, and J. L. Casanova. 1999. IL-12 and IFN-gamma in host defense against mycobacteria and salmonella in mice and men. Curr. Opin. Immunol. 11: 346-351.
39. El Malki, K., S. H. Karbach, J. Huppert, M. Zayoud, S. Reissig, R. Schuler, A. Nikolaev, K. Karram, T. Munzel, C. R. Kuhlmann, et al. 2013. An alternative pathway of imiquimod-induced psoriasis-like skin inflammation in the absence of interleukin-17 receptor a signaling. J. Invest. Dermatol. 133: 441-451.
40. Parkhill, J., G. Dougan, K. D. James, N. R. Thomson, D. Pickard, J. Wain, C. Churcher, K. L. Mungall, S. D. Bentley, M. T. Holden, et al. 2001. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413: 848-852.
41. Onder, L., R. Danuser, E. Scandella, S. Firner, Q. Chai, T. Hehlgans, J. V. Stein, and B. Ludewig. 2013. Endothelial cell-specific lymphotoxin-b receptor signaling is critical for lymph node and high endothelial venule formation. J. Exp. Med. 210: 465-473.
42. Wang, Z., M. Raifu, M. Howard, L. Smith, D. Hansen, R. Goldsby, and D. Ratner. 2000. Universal PCR amplification of mouse immunoglobulin gene variable regions: the design of degenerate primers and an assessment of the effect of DNA polymerase 39 to 59 exonuclease activity. J. Immunol. Methods 233: 167-177.
43. Manz, R. A., and A. Radbruch. 2002. Plasma cells for a lifetime? Eur. J. Immunol. 32: 923-927.
44. Grusby, M. J., R. S. Johnson, V. E. Papaioannou, and L. H. Glimcher. 1991. Depletion of CD4+ T cells in major histocompatibility complex class II-deficient mice. Science 253: 1417-1420.
45. Rubtsov, A., P. Strauch, A. Digiacomo, J. Hu, R. Pelanda, and R. M. Torres. 2005. Lsc regulates marginal-zone B cell migration and adhesion and is required for the IgM T-dependent antibody response. Immunity 23: 527-538.
46. 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.
47. Yu, X., T. Tsibane, P. A. McGraw, F. S. House, C. J. Keefer, M. D. Hicar, T. M. Tumpey, C. Pappas, L. A. Perrone, O. Martinez, et al. 2008. Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature 455: 532-536.
48. Throsby, M., E. van den Brink, M. Jongeneelen, L. L. Poon, P. Alard, L. Cornelissen, A. Bakker, F. Cox, E. van Deventer, Y. Guan, et al. 2008. Heterosubtypic neutralizing monoclonal antibodies cross-protective against H5N1 and H1N1 recovered from human IgM+ memory B cells. PLoS ONE 3: e3942.
49. Klein, U., K. Rajewsky, and R. Kuppers. 1998. Human immunoglobulin (Ig)M +IgD+ peripheral blood B cells expressing the CD27 cell surface antigen carry somatically mutated variable region genes: CD27 as a general marker for somatically mutated (memory) B cells. J. Exp. Med. 188: 1679-1689.
50. Seifert, M., and R. Kuppers. 2009. Molecular footprints of a germinal center derivation of human IgM+(IgD+)CD27+ B cells and the dynamics of memory B cell generation. J. Exp. Med. 206: 2659-2669.
51. Manz, R. A., S. Arce, G. Cassese, A. E. Hauser, F. Hiepe, and A. Radbruch. 2002. Humoral immunity and long-lived plasma cells. Curr. Opin. Immunol. 14: 517-521.
52. Bernasconi, N. L., E. Traggiai, and A. Lanzavecchia. 2002. Maintenance of serological memory by polyclonal activation of human memory B cells. Science 298: 2199-2202.
53. Tew, J. G., R. P. Phipps, and T. E. Mandel. 1980. The maintenance and regulation of the humoral immune response: persisting antigen and the role of follicular antigen-binding dendritic cells as accessory cells. Immunol. Rev. 53: 175-201.
54. Weiss, G. E., P. D. Crompton, S. Li, L. A. Walsh, S. Moir, B. Traore, K. Kayentao, A. Ongoiba, O. K. Doumbo, and S. K. Pierce. 2009. Atypical memory B cells are greatly expanded in individuals living in a malaria-endemic area. J. Immunol. 183: 2176-2182.
55. Purtha, W. E., T. F. Tedder, S. Johnson, D. Bhattacharya, and M. S. Diamond. 2011. Memory B cells, but not long-lived plasma cells, possess antigen specificities for viral escape mutants. J. Exp. Med. 208: 2599-2606.
56. Ravindran, R., J. Foley, T. Stoklasek, L. H. Glimcher, and S. J. McSorley. 2005. Expression of T-bet by CD4 T cells is essential for resistance to Salmonella infection. J. Immunol. 175: 4603-4610.
57. Griffin, A. J., and S. J. McSorley. 2011. Generation of Salmonella-specific Th1 cells requires sustained antigen stimulation. Vaccine 29: 2697-2704.
58. Linterman, M. A., L. Beaton, D. Yu, R. R. Ramiscal, M. Srivastava, J. J. Hogan, N. K. Verma, M. J. Smyth, R. J. Rigby, and C. G. Vinuesa. 2010. IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses. J. Exp. Med. 207: 353-363.
59. Yates, J. L., R. Racine, K. M. McBride, and G. M. Winslow. 2013. T celldependent IgM memory B cells generated during bacterial infection are required for IgG responses to antigen challenge. J. Immunol. 191: 1240-1249.
60. Hirota, K., J. E. Turner, M. Villa, J. H. Duarte, J. Demengeot, O. M. Steinmetz, and B. Stockinger. 2013. Plasticity of Th17 cells in Peyer's patches is responsible for the induction of T cell-dependent IgA responses. Nat. Immunol. 14: 372-379.
61. Lee, S. K., D. G. Silva, J. L. Martin, A. Pratama, X. Hu, P. P. Chang, G. Walters, and C. G. Vinuesa. 2012. Interferon-g excess leads to pathogenic accumulation of follicular helper T cells and germinal centers. Immunity 37: 880-892.