Cutting Edge: B Cells Are Essential for Protective Immunity Against Salmonella Independent of Antibody Secretion

Overview

Journal J Immunol

Specialty Allergy & Immunology

Date 2012 Nov 15

PMID 23150714

Citations 48

Authors

Minelva R Nanton

Sing Sing Way

Mark J Shlomchik

Stephen J McSorley

Affiliations

Soon will be listed here.

Abstract

Typhoid fever and nontyphoidal bacteremia caused by Salmonella remain critical human health problems. B cells are required for protective immunity to Salmonella, but the mechanism of protection remains unclear. In this study, we immunized wild-type, B cell-deficient, Ab-deficient, and class-switched Ab-deficient mice with attenuated Salmonella and examined protection against secondary infection. As expected, wild-type mice were protected and B cell-deficient mice succumbed to secondary infection. Interestingly, mice with B cells but lacking secreted Ab or class-switched Ab had little deficiency in resistance to Salmonella infection. The susceptibility of B cell-deficient mice correlated with marked reductions in CD4 T cell IFN-γ production after secondary infection. Taken together, these data suggest that the primary role of B cells in acquired immunity to Salmonella is via the development of protective T cell immunity.

Citing Articles

Promotion of Colitis in B Cell-Deficient C57BL/6 Mice Infected with Enterotoxigenic .

Jo M, Hwang S, Lee C, Hong J, Kang D, Yoo S Int J Mol Sci. 2024; 25(1).

PMID: 38203534 PMC: 10778593. DOI: 10.3390/ijms25010364.

Vaccine-induced inflammation and inflammatory monocytes promote CD4+ T cell-dependent immunity against murine salmonellosis.

Wang N, Scott T, Kupz A, Shreenivas M, Peres N, Hocking D PLoS Pathog. 2023; 19(9):e1011666.

PMID: 37733817 PMC: 10547166. DOI: 10.1371/journal.ppat.1011666.

B cell activating factor (BAFF) from neutrophils and dendritic cells is required for protective B cell responses against Salmonella typhimurium infection.

Kuley R, Draves K, Fuller D, Giltiay N, Clark E, Giordano D PLoS One. 2021; 16(10):e0259158.

PMID: 34705890 PMC: 8550399. DOI: 10.1371/journal.pone.0259158.

B Cells Control Mucosal-Associated Invariant T Cell Responses to Serovar Typhi Infection Through the CD85j HLA-G Receptor.

Salerno-Goncalves R, Rezwan T, Luo D, Tettelin H, Sztein M Front Immunol. 2021; 12:728685.

PMID: 34659215 PMC: 8517411. DOI: 10.3389/fimmu.2021.728685.

An Outer Membrane Vesicle-Adjuvanted Oral Vaccine Protects Against Lethal, Oral Infection.

Harrell J, Kurtz J, Bauer D, Prior J, Gellings P, Morici L Pathogens. 2021; 10(5).

PMID: 34069796 PMC: 8157261. DOI: 10.3390/pathogens10050616.

References

MacLennan C, Gondwe E, Msefula C, Kingsley R, Thomson N, White S . The neglected role of antibody in protection against bacteremia caused by nontyphoidal strains of Salmonella in African children. J Clin Invest. 2008; 118(4):1553-62. PMC: 2268878. DOI: 10.1172/JCI33998. View

MacLennan C, Gilchrist J, Gordon M, Cunningham A, Cobbold M, Goodall M . Dysregulated humoral immunity to nontyphoidal Salmonella in HIV-infected African adults. Science. 2010; 328(5977):508-12. PMC: 3772309. DOI: 10.1126/science.1180346. View

Black R, Levine M, Ferreccio C, Clements M, Lanata C, Rooney J . Efficacy of one or two doses of Ty21a Salmonella typhi vaccine in enteric-coated capsules in a controlled field trial. Chilean Typhoid Committee. Vaccine. 1990; 8(1):81-4. DOI: 10.1016/0264-410x(90)90183-m. View

Wijburg O, Uren T, Simpfendorfer K, Johansen F, Brandtzaeg P, Strugnell R . Innate secretory antibodies protect against natural Salmonella typhimurium infection. J Exp Med. 2006; 203(1):21-6. PMC: 2118088. DOI: 10.1084/jem.20052093. View

MacLennan C, Fieschi C, Lammas D, Picard C, Dorman S, Sanal O . Interleukin (IL)-12 and IL-23 are key cytokines for immunity against Salmonella in humans. J Infect Dis. 2004; 190(10):1755-7. DOI: 10.1086/425021. View

Mastroeni P, Grant A, Restif O, Maskell D . A dynamic view of the spread and intracellular distribution of Salmonella enterica. Nat Rev Microbiol. 2008; 7(1):73-80. DOI: 10.1038/nrmicro2034. View

Mittrucker H, Raupach B, Kohler A, Kaufmann S . Cutting edge: role of B lymphocytes in protective immunity against Salmonella typhimurium infection. J Immunol. 2000; 164(4):1648-52. DOI: 10.4049/jimmunol.164.4.1648. View

Pasetti M, Simon J, Sztein M, Levine M . Immunology of gut mucosal vaccines. Immunol Rev. 2011; 239(1):125-48. PMC: 3298192. DOI: 10.1111/j.1600-065X.2010.00970.x. View

Mastroeni P, Villarreal-Ramos B, Hormaeche C . Role of T cells, TNF alpha and IFN gamma in recall of immunity to oral challenge with virulent salmonellae in mice vaccinated with live attenuated aro- Salmonella vaccines. Microb Pathog. 1992; 13(6):477-91. DOI: 10.1016/0882-4010(92)90014-f. View

10.

McSorley S, Jenkins M . Antibody is required for protection against virulent but not attenuated Salmonella enterica serovar typhimurium. Infect Immun. 2000; 68(6):3344-8. PMC: 97596. DOI: 10.1128/IAI.68.6.3344-3348.2000. View

11.

Tobar J, Gonzalez P, Kalergis A . Salmonella escape from antigen presentation can be overcome by targeting bacteria to Fc gamma receptors on dendritic cells. J Immunol. 2004; 173(6):4058-65. DOI: 10.4049/jimmunol.173.6.4058. View

12.

Hannum L, Haberman A, Anderson S, Shlomchik M . Germinal center initiation, variable gene region hypermutation, and mutant B cell selection without detectable immune complexes on follicular dendritic cells. J Exp Med. 2000; 192(7):931-42. PMC: 2193308. DOI: 10.1084/jem.192.7.931. View

13.

Ugrinovic S, Menager N, Goh N, Mastroeni P . Characterization and development of T-Cell immune responses in B-cell-deficient (Igh-6(-/-)) mice with Salmonella enterica serovar Typhimurium infection. Infect Immun. 2003; 71(12):6808-19. PMC: 308891. DOI: 10.1128/IAI.71.12.6808-6819.2003. View

14.

Neves P, Lampropoulou V, Calderon-Gomez E, Roch T, Stervbo U, Shen P . Signaling via the MyD88 adaptor protein in B cells suppresses protective immunity during Salmonella typhimurium infection. Immunity. 2010; 33(5):777-90. DOI: 10.1016/j.immuni.2010.10.016. View

15.

Lee S, Liang L, Juarez S, Nanton M, Gondwe E, Msefula C . Identification of a common immune signature in murine and human systemic Salmonellosis. Proc Natl Acad Sci U S A. 2012; 109(13):4998-5003. PMC: 3324033. DOI: 10.1073/pnas.1111413109. View

16.

Gordon M, Kankwatira A, Mwafulirwa G, Walsh A, Hopkins M, Parry C . Invasive non-typhoid salmonellae establish systemic intracellular infection in HIV-infected adults: an emerging disease pathogenesis. Clin Infect Dis. 2010; 50(7):953-62. DOI: 10.1086/651080. View

17.

Dorman S, Holland S . Interferon-gamma and interleukin-12 pathway defects and human disease. Cytokine Growth Factor Rev. 2000; 11(4):321-33. DOI: 10.1016/s1359-6101(00)00010-1. View

18.

Mastroeni P, Simmons C, Fowler R, Hormaeche C, Dougan G . Igh-6(-/-) (B-cell-deficient) mice fail to mount solid acquired resistance to oral challenge with virulent Salmonella enterica serovar typhimurium and show impaired Th1 T-cell responses to Salmonella antigens. Infect Immun. 1999; 68(1):46-53. PMC: 97100. DOI: 10.1128/IAI.68.1.46-53.2000. View

19.

Mastroeni P, Villarreal-Ramos B, Hormaeche C . Adoptive transfer of immunity to oral challenge with virulent salmonellae in innately susceptible BALB/c mice requires both immune serum and T cells. Infect Immun. 1993; 61(9):3981-4. PMC: 281103. DOI: 10.1128/iai.61.9.3981-3984.1993. View

20.

Crump J, Luby S, Mintz E . The global burden of typhoid fever. Bull World Health Organ. 2004; 82(5):346-53. PMC: 2622843. View