The neglected role of antibody in protection against bacteremia caused by nontyphoidal strains of Salmonella in African children

Journal of Clinical Investigation

Volumn 118, Issue 4, 2008, Pages 1553-1562

  MacLennan, Calman A ^a,b,c   Gondwe, Esther N ^a,d   Msefula, Chisomo L ^a,d   Kingsley, Robert A ^e   Thomson, Nicholas R ^e   White, Sarah A ^a,c   Goodall, Margaret ^b   Pickard, Derek J ^e   Graham, Stephen M ^a,d   Dougan, Gordon ^e   Hart, C Anthony ^c   Molyneux, Malcolm E ^a,d   Drayson, Mark T ^b  

^a UNIVERSITY OF MALAWI   (Malawi)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

^d LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM ANTIBODY; COMPLEMENT MEMBRANE ATTACK COMPLEX; LIPOPOLYSACCHARIDE; MANNOSE BINDING LECTIN; SALMONELLA ANTIBODY; UNCLASSIFIED DRUG;

ANTIBODY PRODUCTION; ARTICLE; BACTEREMIA; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; CASE REPORT; CHILD; COMPLEMENT SYSTEM; FEMALE; HUMAN; INFANT; INFECTION PREVENTION; LEUKOCYTE; MALAWI; MALE; NORMAL HUMAN; PRIORITY JOURNAL; PROTECTION; SALMONELLA; SERUM;

ADOLESCENT; AGE DISTRIBUTION; ANTIBODIES; BACTEREMIA; BACTERIAL PROTEINS; BASE SEQUENCE; CHILD; CHILD, PRESCHOOL; HUMANS; INFANT; INFANT, NEWBORN; LIPOPOLYSACCHARIDES; MALAWI; MOLECULAR SEQUENCE DATA; SALMONELLA; TYPHOID FEVER;

EID: 41849113486     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI33998     Document Type: Article

References (44)

1. Graham, S.M., et al. 2000. Nontyphoidal Salmonella infections of children in tropical Africa. Pediatr. Infect. Dis. J. 19:1189-1196.
2. Graham, S.M. 2002. Salmonellosis in children in developing and developed countries and populations. Curr. Opin. Infect. Dis. 15:507-512.
3. Brent, A.J., et al. 2006. Salmonella bacteremia in Kenyan children. Pediatr. Infect. Dis. J. 25:230-236.
4. Hohmann, E.L. 2001. Nontyphoidal salmonellosis. Clin. Infect. Dis. 32:263-269.
5. Gordon, M.A., et al. 2002. Non-typhoidal salmonella bacteraemia among HIV-infected Malawian adults: high mortality and frequent recrudescence. AIDS. 16:1633-1641.
6. Kariuki, S., et al. 2002. Lack of clonal relationship between non-typhi Salmonella strain types from humans and those isolated from animals living in close contacts. FEMS Immunol. Med. Microbiol. 33:165-171.
7. Becker, D., et al. 2006. Robust Salmonella metabolism limits possibilities for new antimicrobials. Nature. 440:303-307.
8. Mastroeni, P. 2002. Immunity to systemic Salmonella infections. Curr. Mol. Med. 2:393-406.
9. Mastroeni, P., et al. 2003. Resistance and susceptibility to Salmonella infections: lessons from mice and patients with immunodeficiencies. Rev. Med. Microbiol. 14:53-62.
10. Fields, P.I., Swanson, R.V., Haidaris, C.G., and Heffron, F. 1986. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc. Natl. Acad. Sci. U. S. A. 83:5189-5193.
11. Blanden, R.V., Mackaness, G.B., and Collins, F.M. 1966. Mechanisms of acquired resistance in mouse typhoid. J. Exp. Med. 124:585-600.
12. Jouanguy, E., et al. 1999. IL-12 and IFN-γ in host defense against mycobacteria and salmonella in mice and men. Curr. Opin. Immunol. 11:346-351.
13. MacLennan, C., et al. 2004. Interleukin (IL)-12 and IL-23 are key cytokines for immunity against salmonella in humans. J. Infect. Dis. 190:1755-1757.
14. Taylor, P.W. 1983. Bactericidal and bacteriolytic activity of serum against gram-negative bacteria. Microbiol. Rev. 47:46-83.
15. Heffernan, E.J., Harwood, J., Fierer, J., and Guiney, D. 1992. The Salmonella typhimurium virulence plasmid complement resistance gene rck is homologous to a family of virulence-related outer membrane protein genes, including pagC and ail. J. Bacteriol. 174:84-91.
16. Muschel, L.H., and Larsen, L.J. 1970. The sensitivity of smooth and rough gram-negative bacteria to the immune bactericidal reaction. Proc. Soc. Exp. Biol. Med. 133:345-348.
17. Liang-Takasaki, C.J., Grossman, N., and Leive, L. 1983. Salmonellae activate complement differentially via the alternative pathway depending on the structure of their lipopolysaccharide O-antigen. J. Immunol. 130:1867-1870.
18. Casadevall, A. 1998. Antibody-mediated protection against intracellular pathogens. Trends Microbiol. 6:102-107.
19. Acharya, I.L., et al. 1987. Prevention of typhoid fever in Nepal with the Vi capsular polysaccharide of Salmonella typhi. A preliminary report. N. Engl. J. Med. 317:1101-1104.
20. Xu, H.R., Hsu, H.S., Moncure, C.W., and King, R.A. 1993. Correlation of antibody titres induced by vaccination with protection in mouse typhoid. Vaccine. 11:725-729.
21. Mastroeni, P., Villarreal-Ramos, B., and Hormaeche, C.E. 1993. 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. 61:3981-3984.
22. McSorley, S.J., and Jenkins, M.K. 2000. Antibody is required for protection against virulent but not attenuated Salmonella enterica serovar Typhimurium. Infect. Immun. 68:3344-3348.
23. Collins, F.M. 1969. Effect of specific immune mouse serum on the growth of Salmonella enteritidis in nonvaccinated mice challenged by various routes. J. Bacteriol. 97:667-675.
24. Cunningham, A.F., et al. 2007. Salmonella induces a switched antibody response without germinal centers that impedes the extracellular spread of infection. J. Immunol. 178:6200-6207.
25. Jolliff, C.R., et al. 1982. Reference intervals for serum IgG, IgA, IgM, C3, and C4 as determined by rate nephelometry. Clin. Chem. 28:126-128.
26. Goldschneider, I., Gotschlich, E.C., and Artenstein, M.S. 1969. Human immunity to the meningococcus. I. The role of humoral antibodies. J. Exp. Med. 129:1307-1326.
27. Ross, S.C., and Densen, P. 1984. Complement deficiency states and infection: epidemiology, pathogenesis and consequences of neisserial and other infections in an immune deficiency. Medicine. 63:243-273.
28. Robbins, J.B., Kenny, K., and Suter, E. 1965. The isolation and biological activities of rabbit γM-and γG-anti-Salmonella typhimurium antibodies. J. Exp. Med. 122:385-402.
29. Michael, J.G., Whitby, J.L., and Landy, M. 1962. Studies on natural antibodies to gram-negative bacteria. J. Exp. Med. 115:131-146.
30. Glynn, A.A., and Milne, C.M. 1967. A kinetic study of bacteriolytic and bactericidal action of human serum. Immunology. 12:639-653.
31. Gökalp, A.S., Toksoy, H.B., Türkay, S., Bakici, M.Z., and Kaya, R. 1994. Intravenous immunoglobulin in the treatment of Salmonella typhimurium infections in preterm neonates. Clin. Pediatr. (Phila.) 33:349-352.
32. Dumestre-Pérard, C., Doerr, E., Colomb, M.G., and Loos, M. 2007. Involvement of complement pathways in patients with bacterial septicemia. Mol. Immunol. 44:1631-1638.
33. Devyatyarova-Johnson, M., et al. 2000. The lipopolysaccharide structures of Salmonella enterica serovar Typhimurium and Neisseria gonorrhoeae determine the attachment of human mannose-binding lectin to intact organisms. Infect. Immun. 68:3894-3899.
34. Roantree, R.J., and Rantz, L.A. 1960. A study of the relationship of the normal bactericidal activity of human serum to bacterial infection. J. Clin. Invest. 39:72-81.
35. Elgefors, B., and Olling, S. 1978. The significance of serum-sensitive bacilli in gram-negative bacteremia. Scand. J. Infect. Dis. 10:203-207.
36. Brown, S.P., et al. 2006. Intracellular demography and the dynamics of Salmonella enterica infections. PLoS Biol. 4:e349.
37. Joiner, K.A., Hammer, C.H., Brown, E.J., Cole, R.J., and Frank, M.M. 1982. Studies on the mechanism of bacterial resistance to complement-mediated killing I. Terminal complement components are deposited and released from Salmonella minnesota S218 without causing bacterial death. J. Exp. Med. 155:797-808.
38. Joiner, K.A., Hammer, C.H., Brown, E.J., and Frank, M.M. 1982. Studies on the mechanism of bacterial resistance to complement-mediated killing II. C8 and C9 release C5b67 from the surface of Salmonella minnesota S218 because the terminal complex does not insert into the bacterial outer membrane. J. Exp. Med. 155:809-819.
39. Heffernan, E.J., et al. 1992. Mechanism of resistance to complement-mediated killing of bacteria encoded by the Salmonella typhimurium virulence plasmid gene rck. J. Clin. Invest. 90:953-964.
40. Frank, M.M., Joiner, K., and Hammer, C. 1987. The function of antibody and complement in the lysis of bacteria. Rev. Infect. Dis. 9:S537-S545.
41. Joiner, K.A., Tartanian, A.B., Hammer, C.H., and Schweinle, J.E. 1989. Multimeric C9 within C5b-9 deposits in unique locations in the cell wall of Salmonella typhimurium. J. Immunol. 142:4450-4457.
42. Tsai, C.M., and Frasch, C.E. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119:115-119.
43. Datsenko, K.A., and Wanner, B.L. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
44. Osborn, M.J., Rosen, S.M., Rothfield, L., and Horecker, B.L. 1962. Biosynthesis of bacterial lipopolysaccharide. I. Enzymatic incorporation of galactose in a mutant strain of Salmonella. Proc. Natl. Acad. Sci. U. S. A. 48:1831-1838.