Monoclonal antibodies of a diverse isotype induced by an O-antigen glycoconjugate vaccine mediate in vitro and in vivo killing of African invasive nontyphoidal Salmonella

Infection and Immunity

Volumn 83, Issue 9, 2015, Pages 3722-3731

  Goh, Yun Shan ^a,b   Clare, Simon ^a   Micoli, Francesca ^c   Saul, Allan ^c   Mastroeni, Pietro ^a,d   MacLennan, Calman A ^a,e,f  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b AGENCY FOR SCIENCE   (Singapore)

^c GSK   (Italy)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e UNIVERSITY OF OXFORD   (United Kingdom)

^f UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN M ANTIBODY; MONOCLONAL ANTIBODY; O ANTIGEN; O ANTIGEN CRM 197 GLYCOCONJUGATE VACCINE; SALMONELLOSIS VACCINE; UNCLASSIFIED DRUG; BACTERIUM ANTIBODY; IMMUNOGLOBULIN CLASS;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY SPECIFICITY; ARTICLE; BACTERIAL IMMUNITY; BACTERIAL LOAD; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; BACTERIUM ISOLATE; BLOOD CELL; CELL FREE SYSTEM; CELL KILLING; CONTROLLED STUDY; FEMALE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MEDIATOR; MOUSE; NONHUMAN; NONTYPHOIDAL SALMONELLA; OPSONIZATION; PASSIVE IMMUNIZATION; PHAGOCYTOSIS; PRIORITY JOURNAL; SALMONELLA; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SALMONELLOSIS; ANIMAL; C57BL MOUSE; DISEASE MODEL; IMMUNOLOGY; KNOCKOUT MOUSE; SALMONELLA ENTERICA;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIBODIES, MONOCLONAL; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; IMMUNOGLOBULIN ISOTYPES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; O ANTIGENS; SALMONELLA ENTERICA; SALMONELLA INFECTIONS; SALMONELLA VACCINES;

EID: 84939524576     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00547-15     Document Type: Article

References (55)

1. Feasey NA, Dougan G, Kingsley RA, Heyderman RS, Gordon MA. 2012. Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 379:2489-2499. http://dx.doi.org/10.1016/S0140-6736(11)61752-2.
2. Graham SM. 2010. Nontyphoidal salmonellosis in Africa. Curr Opin Infect Dis 23:409-414. http://dx.doi.org/10.1097/QCO.0b013e32833dd25d.
3. MacLennan CA, Levine MM. 2013. Invasive nontyphoidal Salmonella disease in Africa: current status. Expert Rev Anti Infect Ther 11:443-446. http://dx.doi.org/10.1586/eri.13.27.
4. Gordon MA, Banda HT, Gondwe M, Gordon SB, Boeree MJ, Walsh AL, Corkill JE, Hart CA, Gilks CF, Molyneux ME. 2002. Non-typhoidal salmonella bacteraemia among HIV-infected Malawian adults: high mortality and frequent recrudescence. AIDS 16:1633-1641. http://dx.doi.org/10.1097/00002030-200208160-00009.
5. Nielsen MV, Sarpong N, Krumkamp R, Dekker D, Loag W, Amemasor S, Agyekum A, Marks F, Huenger F, Krefis AC, Hagen RM, Adu-Sarkodie Y, May J, Schwarz NG. 2012. Incidence and characteristics of bacteremia among children in rural Ghana. PLoS One 7:e44063. http://dx.doi.org/10.1371/journal.pone.0044063.
6. Tabu C, Breiman RF, Ochieng B, Aura B, Cosmas L, Audi A, Olack B, Bigogo G, Ongus JR, Fields P, Mintz E, Burton D, Oundo J, Feikin DR. 2012. Differing burden and epidemiology of non-Typhi Salmonella bacteremia in rural and urban Kenya, 2006-2009. PLoS One 7:e31237. http://dx.doi.org/10.1371/journal.pone.0031237.
7. Brown A, Hormaeche CE. 1989. The antibody response to salmonellae in mice and humans studied by immunoblots and ELISA. Microb Pathog 6:445-454. http://dx.doi.org/10.1016/0882-4010(89)90086-7.
8. Calderon I, Lobos SR, Rojas HA, Palomino C, Rodriguez LH, Mora GC. 1986. Antibodies to porin antigens of Salmonella typhi induced during typhoid infection in humans. Infect Immun 52:209-212.
9. Guard-Petter J, Keller LH, Rahman MM, Carlson RW, Silvers S. 1996. A novel relationship between O-antigen variation, matrix formation, and invasiveness of Salmonella enteritidis. Epidemiol Infect 117:219-231. http://dx.doi.org/10.1017/S0950268800001394.
10. Murray GL, Attridge SR, Morona R. 2003. Regulation of Salmonella typhimurium lipopolysaccharide O antigen chain length is required for virulence; identification of FepE as a second Wzz. Mol Microbiol 47:1395-1406. http://dx.doi.org/10.1046/j.1365-2958.2003.03383.x.
11. MacLennan CA, Martin LB, Micoli F. 2014. Vaccines against invasive Salmonella disease: current status and future directions. Hum Vaccin Immunother 10:1478-1493. http://dx.doi.org/10.4161/hv.29054.
12. Watson DC, Robbins JB, Szu SC. 1992. Protection of mice against Salmonella typhimurium with an O-specific polysaccharide-protein conjugate vaccine. Infect Immun 60:4679-4686.
13. Rondini S, Micoli F, Lanzilao L, Gavini M, Alfini R, Brandt C, Clare S, Mastroeni P, Saul A, MacLennan CA. 2015. Design of glycoconjugate vaccines against invasive African Salmonella enterica serovar Typhimurium. Infect Immun 83:996-1007. http://dx.doi.org/10.1128/IAI.03079-14.
14. MacLennan CA, Gondwe EN, Msefula CL, Kingsley RA, Thomson NR, White SA, Goodall M, Pickard DJ, Graham SM, Dougan G, Hart CA, Molyneux ME, Drayson MT. 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. http://dx.doi.org/10.1172/JCI33998.
15. Pulickal AS, Gautam S, Clutterbuck EA, Thorson S, Basynat B, Adhikari N, Makepeace K, Rijpkema S, Borrow R, Farrar JJ, Pollard AJ. 2009. Kinetics of the natural, humoral immune response to Salmonella enterica serovar Typhi in Kathmandu, Nepal. Clin Vaccine Immunol 16:1413-1419. http://dx.doi.org/10.1128/CVI.00245-09.
16. Mastroeni P, Villarreal-Ramos B, Hormaeche CE. 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.
17. McSorley SJ, Jenkins MK. 2000. Antibody is required for protection against virulent but not attenuated Salmonella enterica serovar Typhimurium. Infect Immun 68:3344-3348. http://dx.doi.org/10.1128/IAI.68.6.3344-3348.2000.
18. Blanden RV, Mackaness GB, Collins FM. 1966. Mechanisms of acquired resistance in mouse typhoid. J Exp Med 124:585-600. http://dx.doi.org/10.1084/jem.124.4.585.
19. Mastroeni P. 2002. Immunity to systemic Salmonella infections. Curr Mol Med 2:393-406. http://dx.doi.org/10.2174/1566524023362492.
20. Goh YS, Grant AJ, Restif O, McKinley TJ, Armour KL, Clark MR, Mastroeni P. 2011. Human IgG isotypes and activating Fcgamma receptors in the interaction of Salmonella enterica serovar Typhimurium with phagocytic cells. Immunology 133:74-83. http://dx.doi.org/10.1111/j.1365-2567.2011.03411.x.
21. Gondwe EN, Molyneux ME, Goodall M, Graham SM, Mastroeni P, Drayson MT, MacLennan CA. 2010. Importance of antibody and complement for oxidative burst and killing of invasive nontyphoidal Salmonella by blood cells in Africans. Proc Natl Acad Sci U S A 107:3070-3075. http://dx.doi.org/10.1073/pnas.0910497107.
22. Uppington H, Menager N, Boross P, Wood J, Sheppard M, Verbeek S, Mastroeni P. 2006. Effect of immune serum and role of individual Fcgamma receptors on the intracellular distribution and survival of Salmonellae enterica serovar Typhimurium in murine macrophages. Immunology 119:147-158. http://dx.doi.org/10.1111/j.1365-2567.2006.02416.x.
23. Goh YS, Necchi F, Rondini S, O'Shaughnessy CM, Micoli F, Gavini M, Msefula CL, Gondwe EN, Mandala W, Gordon MA, Saul A, MacLennan CA. 2013. Bactericidal potential of S. Typhimurium LPS-specific antibodies from HIV-infected African adults, abstr 74, p 12. 8th Int Conf Typhoid Fever Other Invasive Salmonelloses.
24. MacLennan CA, Gilchrist JJ, Gordon MA, Cunningham AF, Cobbold M, Goodall M, Kingsley RA, van Oosterhout JJ, Msefula CL, Mandala WL, Leyton DL, Marshall JL, Gondwe EN, Bobat S, López-Macías C, Doffinger R, Henderson IR, Zijlstra EE, Dougan G, Drayson MT, MacLennan IC, Molyneux ME. 2010. Dysregulated humoral immunity to nontyphoidal Salmonella in HIV-infected African adults. Science 328:508-512. http://dx.doi.org/10.1126/science.1180346.
25. Kingsley RA, Msefula CL, Thomson NR, Kariuki S, Holt KE, Gordon MA, Harris D, Clarke L, Whitehead S, Sangal V, Marsh K, Achtman M, Molyneux ME, Cormican M, Parkhill J, MacLennan CA, Heyderman RS, Dougan G. 2009. Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res 19:2279-2287. http://dx.doi.org/10.1101/gr.091017.109.
26. Okoro CK, Kingsley RA, Connor TR, Harris SR, Parry CM, Al-Mashhadani MN, Kariuki S, Msefula CL, Gordon MA, de Pinna E, Wain J, Heyderman RS, Obaro S, Alonso PL, Mandomando I, MacLennan CA, Tapia MD, Levine MM, Tennant SM, Parkhill J, Dougan G. 2012. Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet 44:1215-1221. http://dx.doi.org/10.1038/ng.2423.
27. Hoiseth SK, Stocker BA. 1981. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291:238-239. http://dx.doi.org/10.1038/291238a0.
28. Micoli F, Ravenscroft N, Cescutti P, Stefanetti G, Londero S, Rondini S, Maclennan CA. 2014. Structural analysis of O-polysaccharide chains extracted from different Salmonella Typhimurium strains. Carbohydr Res 385:1-8. http://dx.doi.org/10.1016/j.carres.2013.12.003.
29. Hormaeche CE, Mastroeni P, Harrison JA, Demarco de Hormaeche R, Svenson S, Stocker BA. 1996. Protection against oral challenge three months after i.v. immunization of BALB/c mice with live Aro Salmonella typhimurium and Salmonella enteritidis vaccines is serotype (species)-dependent and only partially determined by the main LPS O antigen. Vaccine 14:251-259. http://dx.doi.org/10.1016/0264-410X(95)00249-Z.
30. Berger CN, Brown DJ, Shaw RK, Minuzzi F, Feys B, Frankel G. 2011. Salmonella enterica strains belonging to O serogroup 1,3,19 induce chlorosis and wilting of Arabidopsis thaliana leaves. Environ Microbiol 13:1299-1308. http://dx.doi.org/10.1111/j.1462-2920.2011.02429.x.
31. Goh YS, MacLennan CA. 2013. Invasive African nontyphoidal Salmonella requires high levels of complement for cell-free antibody-dependent killing. J Immunol Methods 387:121-129. http://dx.doi.org/10.1016/j.jim.2012.10.005.
32. Vendrell JP, Delobbe A, Huguet MF, Peraldi F, Serre A, Cannat A. 1987. Biological properties of a panel of murine monoclonal anti-Brucella antibodies. Immunology 61:7-10.
33. Xu Y, Oomen R, Klein MH. 1994. Residue at position 331 in the IgG1 and IgG4 CH2 domains contributes to their differential ability to bind and activate complement. J Biol Chem 269:3469-3474.
34. Rondini S, Lanzilao L, Necchi F, O'Shaughnessy CM, Micoli F, Saul A, MacLennan CA. 2013. Invasive African Salmonella Typhimurium induces bactericidal antibodies against O-antigens. Microb Pathog 63:19-23. http://dx.doi.org/10.1016/j.micpath.2013.05.014.
35. MacLennan CA, Tennant SM. 2013. Comparing the roles of antibodies to nontyphoidal Salmonella enterica in high- and low-income countries and implications for vaccine development. Clin Vaccine Immunol 20:1487-1490. http://dx.doi.org/10.1128/CVI.00465-13.
36. Trebicka E, Jacob S, Pirzai W, Hurley BP, Cherayil BJ. 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. http://dx.doi.org/10.1128/CVI.00289-13.
37. Siggins MK, Cunningham AF, Marshall JL, Chamberlain JL, Henderson IR, MacLennan CA. 2011. Absent bactericidal activity of mouse serum against invasive African nontyphoidal Salmonella results from impaired complement function but not a lack of antibody. J Immunol 186:2365-2371. http://dx.doi.org/10.4049/jimmunol.1000284.
38. Carlin NI, Svenson SB, Lindberg AA. 1987. Role of monoclonal O-antigen antibody epitope specificity and isotype in protection against experimental mouse typhoid. Microb Pathog 2:171-183. http://dx.doi.org/10.1016/0882-4010(87)90019-2.
39. Hiemstra PS, Gorter A, Stuurman ME, Van Es LA, Daha MR. 1987. Activation of the alternative pathway of complement by human serum IgA. Eur J Immunol 17:321-326. http://dx.doi.org/10.1002/eji.1830170304.
40. Bogers WM, Stad RK, Van Es LA, Daha MR. 1992. Both Kupffer cells and liver endothelial cells play an important role in the clearance of IgA and IgG immune complexes. Res Immunol 143:219-224. http://dx.doi.org/10.1016/S0923-2494(92)80170-P.
41. Roos A, Bouwman LH, van Gijlswijk-Janssen DJ, Faber-Krol MC, Stahl GL, Daha MR. 2001. Human IgA activates the complement system via the mannan-binding lectin pathway. J Immunol 167:2861-2868. http://dx.doi.org/10.4049/jimmunol.167.5.2861.
42. Battista P, Circolo A, Borsos T. 1985. Activation of hemolytic complement by mouse monoclonal IgG1 antibody: comparison with rabbit IgG. Mol Immunol 22:215-221. http://dx.doi.org/10.1016/0161-5890(85)90153-1.
43. Coppens I, Alonso S, Antoine R, Jacob-Dubuisson F, Renauld-Mongenie G, Jacobs E, Locht C. 2001. Production of Neisseria meningitidis transferrin-binding protein B by recombinant Bordetella pertussis. Infect Immun 69:5440-5446. http://dx.doi.org/10.1128/IAI.69.9.5440-5446.2001.
44. Seino J, Eveleigh P, Warnaar S, van Haarlem LJ, van Es LA, Daha MR. 1993. Activation of human complement by mouse and mouse/human chimeric monoclonal antibodies. Clin Exp Immunol 94:291-296.
45. Mostov KE, Friedlander M, Blobel G. 1984. The receptor for transepithelial transport of IgA and IgM contains multiple immunoglobulin-like domains. Nature 308:37-43. http://dx.doi.org/10.1038/308037a0.
46. Shibuya A, Sakamoto N, Shimizu Y, Shibuya K, Osawa M, Hiroyama T, Eyre HJ, Sutherland GR, Endo Y, Fujita T, Miyabayashi T, Sakano S, Tsuji T, Nakayama E, Phillips JH, Lanier LL, Nakauchi H. 2000. Fc alpha/mu receptor mediates endocytosis of IgM-coated microbes. Nat Immunol 1:441-446. http://dx.doi.org/10.1038/80886.
47. Shima H, Takatsu H, Fukuda S, Ohmae M, Hase K, Kubagawa H, Wang JY, Ohno H. 2010. Identification of TOSO/FAIM3 as an Fc receptor for IgM. Int Immunol 22:149-156. http://dx.doi.org/10.1093/intimm/dxp121.
48. Kariuki S, Revathi G, Kariuki N, Kiiru J, Mwituria J, Muyodi J, Githinji JW, Kagendo D, Munyalo A, Hart CA. 2006. Invasive multidrugresistant non-typhoidal Salmonella infections in Africa: zoonotic or anthroponotic transmission? J Med Microbiol 55:585-591. http://dx.doi.org/10.1099/jmm.0.46375-0.
49. Ravetch JV, Kinet JP. 1991. Fc receptors. Annu Rev Immunol 9:457-492. http://dx.doi.org/10.1146/annurev.iy.09.040191.002325.
50. Stavnezer J. 1996. Immunoglobulin class switching. Curr Opin Immunol 8:199-205. http://dx.doi.org/10.1016/S0952-7915(96)80058-6.
51. Stavnezer J. 1996. Antibody class switching. Adv Immunol 61:79-146. http://dx.doi.org/10.1016/S0065-2776(08)60866-4.
52. Stevens TL, Bossie A, Sanders VM, Fernandez-Botran R, Coffman RL, Mosmann TR, Vitetta ES. 1988. Regulation of antibody isotype secretion by subsets of antigen-specific helper T cells. Nature 334:255-258. http://dx.doi.org/10.1038/334255a0.
53. Wells TJ, Whitters D, Sevastsyanovich YR, Heath JN, Pravin J, Goodall M, Browning DF, O'Shea MK, Cranston A, De Soyza A, Cunningham AF, MacLennan CA, Henderson IR, Stockley RA. 2014. Increased severity of respiratory infections associated with elevated anti-LPS IgG2 which inhibits serum bactericidal killing. J Exp Med 25:1893-1904. http://dx.doi.org/10.1084/jem.20132444.
54. Taborda CP, Rivera J, Zaragoza O, Casadevall A. 2003. More is not necessarily better: prozone-like effects in passive immunization with IgG. J Immunol 170:3621-3630. http://dx.doi.org/10.4049/jimmunol.170.7.3621.
55. Goodner K, Horsfall FL. 1935. The protective action of Type I antipneumococcus serum in mice. I. Quantitative aspects of the mouse protection test. J Exp Med 62:359.