Differential timing of antibody-mediated phagocytosis and cell-free killing of invasive African Salmonella allows immune evasion

European Journal of Immunology

Volumn 44, Issue 4, 2014, Pages 1093-1098

  Siggins, Matthew K ^a,b   O'Shaughnessy, Colette M ^a   Pravin, John ^a   Cunningham, Adam F ^a   Henderson, Ian R ^a   Drayson, Mark T ^a   Maclennan, Calman A ^a,b  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

Author keywords

Antibodies; Complement; Opsonization; Phagocytosis; Salmonella

Indexed keywords

BACTERIUM ANTIBODY; COMPLEMENT COMPONENT C3; COMPLEMENT MEMBRANE ATTACK COMPLEX; IMMUNOGLOBULIN G;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; BACTERIUM DETECTION; BACTERIUM ISOLATE; CELL KILLING; CELLULAR IMMUNITY; COMPLEMENT DEPOSITION; CONTROLLED STUDY; HUMAN; IMMUNE EVASION; INVASIVE SPECIES; MONOCYTE; NEUTROPHIL; NONHUMAN; OPSONIZATION; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; SALMONELLA ENTERITIDIS; SALMONELLA TYPHIMURIUM; SUSCEPTIBLE POPULATION;

ANTIBODIES; COMPLEMENT; OPSONIZATION; PHAGOCYTOSIS; SALMONELLA;

ADULT; ANTIBODIES, BACTERIAL; BLOOD BACTERICIDAL ACTIVITY; COMPLEMENT C3; COMPLEMENT C5B; COMPLEMENT MEMBRANE ATTACK COMPLEX; FLOW CYTOMETRY; HOST-PATHOGEN INTERACTIONS; HUMANS; KINETICS; MICROBIAL VIABILITY; MONOCYTES; NEUTROPHILS; OPSONIN PROTEINS; PHAGOCYTOSIS; SALMONELLA ENTERITIDIS; SALMONELLA TYPHIMURIUM; SERUM; TIME FACTORS;

EID: 84898009481     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343529     Document Type: Article

References (22)

1. MacLennan, C., Fieschi, C., Lammas, D. A., Picard, C., Dorman, S. E., Sanal, O., MacLennan, J. M. et al., Interleukin (IL)-12 and IL-23 are key cytokines for immunity against Salmonella in humans. J. Infect. Dis. 2004. 190: 1755-1757.
2. Bustamante, J., Boisson-Dupuis, S., Jouanguy, E., Picard, C., Puel, A., Abel, L. and Casanova, J. L., Novel primary immunodeficiencies revealed by the investigation of paediatric infectious diseases. Curr. Opin. Immunol. 2008. 20: 39-48.
3. McSorley, S. J. and Jenkins, M. K., Antibody is required for protection against virulent but not attenuated Salmonella enterica serovar typhimurium. Infect. Immun. 2000. 68: 3344-3348.
4. Reddy, E. A., Shaw, A. V. and Crump, J. A., Community-acquired bloodstream infections in Africa: a systematic review and meta-analysis. Lancet Infect. Dis. 2010. 10: 417-432.
5. Feasey, N. A., Dougan, G., Kingsley, R. A., Heyderman, R. S. and Gordon, M. A., Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 2012. 379: 2489-2499.
6. MacLennan, C. A., Gondwe, E. N., Msefula, C. L., Kingsley, R. A., Thomson, N. R., White, S. A., Goodall, M. et al., The neglected role of antibody in protection against bacteremia caused by nontyphoidal strains of Salmonella in African children. J. Clin. Invest. 2008. 118: 1553-1562.
7. Gondwe, E. N., Molyneux, M. E., Goodall, M., Graham, S. M., Mastroeni, P., Drayson, M. T. and Maclennan, C. A., Importance of antibody and complement for oxidative burst and killing of invasive nontyphoidal Salmonella by blood cells in Africans. Proc. Natl. Acad. Sci. USA 2010. 107: 3070-3075.
8. Hohmann, E. L., Nontyphoidal salmonellosis. Clin. Infect. Dis. 2001. 32: 263-269.
9. Lammas, D. A., De Heer, E., Edgar, J. D., Novelli, V., Ben-Smith, A., Baretto, R., Drysdale, P. et al., Heterogeneity in the granulomatous response to mycobacterial infection in patients with defined genetic mutations in the interleukin 12-dependent interferon-gamma production pathway. Int. J. Exp. Pathol. 2002. 83: 1-20.
10. Warren, J., Mastroeni, P., Dougan, G., Noursadeghi, M., Cohen, J., Walport, M. J. and Botto, M., Increased susceptibility of C1q-deficient mice to Salmonella enterica serovar Typhimurium infection. Infect. Immun. 2002. 70: 551-557.
11. Mastroeni, P., Grant, A., Restif, O. and Maskell, D., A dynamic view of the spread and intracellular distribution of Salmonella enterica. Nat. Rev. Microbiol. 2009. 7: 73-80.
12. Siggins, M. K., Cunningham, A. F., Marshall, J. L., Chamberlain, J. L., Henderson, I. R. and MacLennan, C. A., Absent bactericidal activity of mouse serum against invasive African nontyphoidal Salmonella results from impaired complement function but not a lack of antibody. J. Immunol. 2011. 186: 2365-2371.
13. Taylor, P. W., Bactericidal and bacteriolytic activity of serum against gram-negative bacteria. Microbiol. Rev. 1983. 47: 46-83.
14. MacLennan, C. A., Gilchrist, J. J., Gordon, M. A., Cunningham, A. F., Cobbold, M., Goodall, M., Kingsley, R. A. et al., Dysregulated humoral immunity to nontyphoidal Salmonella in HIV-infected African adults. Science 2010. 328: 508-512.
15. Herrada, A. A., Contreras, F. J., Tobar, J. A., Pacheco, R. and Kalergis, A. M., Immune complex-induced enhancement of bacterial antigen presentation requires Fcgamma receptor III expression on dendritic cells. Proc. Natl. Acad. Sci. USA 2007. 104: 13402-13407.
16. Riquelme, S. A., Bueno, S. M. and Kalergis, A. M., IgG keeps virulent Salmonella from evading dendritic cell uptake. Immunology 2012. 136: 291-305.
17. Joller, N., Weber, S. S., Müller, A. J., Spörri, R., Selchow, P., Sander, P., Hilbi, H. et al., Antibodies protect against intracellular bacteria by Fc receptor-mediated lysosomal targeting. Proc. Natl. Acad. Sci. USA 2010. 107: 20441-20446.
18. Drecktrah, D., Knodler, L. A., Ireland, R. and Steele-Mortimer, O., The mechanism of Salmonella entry determines the vacuolar environment and intracellular gene expression. Traffic 2006. 7: 39-51.
19. Vazquez-Torres, A., Xu, Y., Jones-Carson, J., Holden, D. W., Lucia, S. M., Dinauer, M. C., Mastroeni, P. et al., Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 2000. 287: 1655-1658.
20. Gordon, M. A., Kankwatira, A. M., Mwafulirwa, G., Walsh, A. L., Hopkins, M. J., Parry, C. M., Faragher et al., Invasive non-typhoid salmonellae establish systemic intracellular infection in HIV-infected adults: an emerging disease pathogenesis. Clin. Infect. Dis. 2010. 50: 953-962.
21. Mastroeni, P., Villarreal-Ramos, B. and Hormaeche, C. E., 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: 477-491.
22. Kingsley, R. A., Msefula, C. L., Thomson, N. R., Kariuki, S., Holt, K. E., Gordon, M. A., Harris et al., Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res. 2009. 19: 2279-2287.