Human IgG isotypes and activating Fcγ receptors in the interaction of Salmonella enterica serovar Typhimurium with phagocytic cells

Immunology

Volumn 133, Issue 1, 2011, Pages 74-83

  Goh, Yun S ^a   Grant, Andrew J ^a   Restif, Olivier ^a   Mckinley, Trevelyan J ^a   Armour, Kathryn L ^a   Clark, Michael R ^a   Mastroeni, Pietro ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Antibody; Fc receptors; IgG subclasses; Opsonization; Phagocytosis

Indexed keywords

CD52 ANTIGEN; FC RECEPTOR; FC RECEPTOR IIA; IMMUNOGLOBULIN CLASS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN G4; INTERLEUKIN 2 RECEPTOR ALPHA; OUTER MEMBRANE PROTEIN A;

ANTIGEN BINDING; ARTICLE; BACTERIAL COUNT; BACTERIAL LOAD; BACTERIAL STRAIN; CONTROLLED STUDY; HOST CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; NONHUMAN; OPSONIZATION; PHAGOCYTE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SEROTYPE;

FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOGLOBULIN G; IMMUNOGLOBULIN ISOTYPES; MONOCYTES; PHAGOCYTES; RECEPTORS, IGG; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM;

EID: 79953297934     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2011.03411.x     Document Type: Article

References (65)

1. Bhutta ZA, Threlfall J. Addressing the global disease burden of typhoid fever. JAMA 2009; 302:898-9.
2. Gilks CF, Brindle RJ, Otieno LS et al. Life-threatening bacteraemia in HIV-1 seropositive adults admitted to hospital in Nairobi, Kenya. Lancet 1990; 336:545-9.
3. Graham SM, Molyneux EM, Walsh AL, Cheesbrough JS, Molyneux ME, Hart CA. Nontyphoidal Salmonella infections of children in tropical Africa. Pediatr Infect Dis J 2000; 19:1189-96.
4. Graham SM, Hart CA, Molyneux EM, Walsh AL, Molyneux ME. Malaria and Salmonella infections: cause or coincidence? Trans R Soc Trop Med Hyg 2000; 94:227.
5. Bronzan RN, Taylor TE, Mwenechanya J et al. Bacteremia in Malawian children with severe malaria: prevalence, etiology, HIV coinfection, and outcome. J Infect Dis 2007; 195:895-904.
6. Graham SM, Walsh AL, Molyneux EM, Phiri AJ, Molyneux ME. Clinical presentation of non-typhoidal Salmonella bacteraemia in Malawian children. Trans R Soc Trop Med Hyg 2000; 94:310-4.
7. Hohmann EL. Nontyphoidal salmonellosis. Clin Infect Dis 2001; 32:263-9.
8. Mirza SH, Beeching NJ, Hart CA. Multi-drug resistant typhoid: a global problem. J Med Microbiol 1996; 44:317-9.
9. Holmberg SD, Solomon SL, Blake PA. Health and economic impacts of antimicrobial resistance. Rev Infect Dis 1987; 9:1065-78.
10. Coovadia YM, Gathiram V, Bhamjee A, Garratt RM, Mlisana K, Pillay N, Madlalose T, Short M. An outbreak of multiresistant Salmonella typhi in South Africa. Q J Med 1992; 82:91-100.
11. Lee CA, Falkow S. Isolation of hyperinvasive mutants of Salmonella. Methods Enzymol 1994; 236:531-45.
12. Richter-Dahlfors A, Buchan AM, Finlay BB. Murine Salmonellosis studies by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effects on phagocytes in vivo. J Exp Med 1997; 186:569-80.
13. Sheppard M, Webb C, Heath F, Mallows V, Emilianus R, Maskell D, Mastroeni P. Dynamics of bacterial growth and distribution within the liver during Salmonella infection. Cell Microbiol 2003; 5:593-600.
14. Fields PI, Swarson RV, Haidaris CG, Heffron F. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci U S A 1986; 83:5189-93.
15. Dunlap NE, Benjamin WH Jr, Berry AK, Eldridge JH, Briles DE. A 'safe-site' for Salmonella typhimurium is within splenic polymorphonuclear cells. Microb Pathog 1992; 13:181-90.
16. Mastroeni P, Skepper JN, Hormaeche CE. Effect of anti-tumor necrosis factor alpha antibodies on histopathology of primary Salmonella infections. Infect Immun 1995; 63:3674-82.
17. Groisman EA, Parra-Lopez C, Salcedo M, Lipps CJ, Heffron F. Resistance to host antimicrobial peptides is necessary for Salmonella virulence. Proc Natl Acad Sci U S A 1992; 89:11939-43.
18. De Groote MA, Testerman T, Xu Y, Stauffer G, Fang FC. Homocysteine antagonism of nitric oxide-related cytostasis in Salmonella typhimurium. Science 1996; 272:414-7.
19. Shiloh MU, Ruan J, Nathan C. Evaluation of bacterial survival and phagocyte function with a fluorescence-based microplate assay. Infect Immun 1997; 65:3193-8.
20. Shiloh MU, MacMicking JD, Nicholson S et al. Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity 1999; 10:29-38.
21. Vazquez-Torrez A, Jones-Carson J, Mastroeni P, Ischiropoulos H, Fang FC. Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. I. Effect on microbial killing by activated peritoneal macrophages in vitro. J Exp Med 2000; 192:227-36.
22. Mastroeni P, Vazquez-Torrez A, Fang FC, Xu Y, Khan S, Hormaeche CE, Dougan G. Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects of microbial proliferation and host survival in vivo. J Exp Med 2000; 192:237-47.
23. Vazquez-Torres A, Xu Y, Holden D, Lucia S, Dinauer M, Mastroeni P, Fang FC. Salmonella pathogenicity Island 2 (SPI-2)-dependent evasion of the phagocyte NADPH oxidase. Science 2000; 287:1655-8.
24. Mastroeni P, Villarreal-Ramos B, Hormaeche CE. 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; 61:3981-4.
25. Grant AJ, Restif O, McKinley TJ, Sheppard M, Maskell DJ, Mastroeni P. Modelling within-host spatiotemporal dynamics of invasive bacterial disease. PLoS Biol 2008; 6:e74.
26. Mastroeni P, Ugrinovic S, Chandra A, MacLennan C, Doffinger R, Kumararatne D. Resistance and susceptibility to Salmonella infections: lessons from mice and patients with immunodeficiencies. Rev Med Microbiol 2003; 14:53-62.
27. MacLennan CA, Gondwe EN, Msefula CL et al. The neglected role of antibody in protection against bacteremia caused by nontyphoidal strains of Salmonella in African children. J Clin Invest 2008; 118:1553-62.
28. Collins FM. Vaccines and cell-mediated immunity. Bacteriol Rev 1974; 38:371-402.
29. Gondwe EN, Molyneux ME, Goodall M, Graham SM, Mastroeni P, Drayson MT, MacLennan CA. 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 2010; 107:3070-5.
30. Shaheen HI, Girgis NI, Rodier GR, Kamal KA. Evaluation of the response of human humoral antibodies to Salmonella typhi lipopolysaccharide in an area of endemic typhoid fever. Clin Infect Dis 1995; 21:1012-3.
31. Fomsgaard A, Galanos C. Protective properties of a human IgG preparation rich in antibodies to a wide spectrum of lipopolysaccharides. APMIS 1989; 97:1114-20.
32. -Salmonella typhimurium vaccines in the murine typhoid model. Immunology 1997; 90:618-25.
33. Levine MM, Ferreccio C, Black RE, Tacket CO, Germanier R. Progress in vaccines against typhoid fever. Rev Infect Dis 1989; 11(Suppl 3):S552-67.
34. Uppington H, Menager N, Boross P, Wood J, Sheppard M, Verbeek S, Mastroeni P. Effect of immune serum and role of individual Fcgamma receptors on the intracellular distribution and survival of Salmonella enterica serovar Typhimurium in murine macrophages. Immunology 2006; 119:147-58.
35. Menager N, Foster G, Ugrinovic S, Uppington H, Verbeek S, Mastroeni P. Fcgamma receptors are crucial for the expression of acquired resistance to virulent Salmonella enterica serovar Typhimurium in vivo but are not required for the induction of humoral or T-cell-mediated immunity. Immunology 2007; 120:424-32.
36. Crowley MT, Costello PS, Fitzer-Attas CJ, Turner M, Meng F, Lowell C, Tybulewicz VL, DeFranco AL. A critical role for Syk in signal transduction and phagocytosis mediated by Fcgamma receptors on macrophages. J Exp Med 1997; 186:1027-39.
37. Gil-Cruz C, Bobat S, Marshall JL et al. The porin OmpD from nontyphoidal Salmonella is a key target for a protective B1b cell antibody response. Proc Natl Acad Sci U S A 2009; 106:9803-8.
38. Hamid N, Jain SK. Characterization of an outer membrane protein of Salmonella enterica serovar typhimurium that confers protection against typhoid. Clin Vaccine Immunol 2008; 15:1461-71.
39. Udhayakumar V, Muthukkaruppan VR. Protective immunity induced by outer membrane proteins of Salmonella typhimurium in mice. Infect Immun 1987; 55:816-21.
40. Hoiseth SK, Stocker BA. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 1981; 291:238-9.
41. Hautefort I, Proenca MJ, Hinton JC. Single-copy green fluorescent protein gene fusions allow accurate measurement of Salmonella gene expression in vitro and during infection of mammalian cells. Appl Environ Microbiol 2003; 69:7480-91.
42. Riechmann L, Clark MR, Waldmann H, Winter G. Reshaping human antibodies for therapy. Nature 1988; 332:323-7.
43. Redpath S, Michaelsen TE, Sandlie I, Clark MR. The influence of the hinge region length in binding of human IgG to human Fcγ receptors. Hum Immunol 1998; 59:720-7.
44. Armour KL, Clark MR, Hadley AG, Williamson LM. Recombinant human IgG molecules lacking Fcgamma receptor I binding and monocyte triggering activities. Eur J Immunol 1999; 29:13-24.
45. Shen L, Graziano RF, Fanger MW. The functional properties of FcγRI, II and III on myeloid cells: a comparative study of killing of erythrocytes and tumour cells mediated through the different Fc receptors. Mol Immunol 1989; 26:959-69.
46. Dougherty GJ, Selvendran Y, Murdoch S, Palmer DG, Hogg N. The human mononuclear phagocyte high-affinity Fc receptor, FcRI, defined by a monoclonal antibody, 10.1. Eur J Immunol 1987; 17:1453-9.
47. Bredius RG, Fijen CA, De Haas M, Kuijper EJ, Weening RS, Van de Winkel JG, Out TA. Role of neutrophil Fc gamma RIIa (CD32) and Fc gamma RIIIb (CD16) polymorphic forms in phagocytosis of human IgG1- and IgG3-opsonised bacteria and erythrocytes. Immunology 1994; 83:624-30.
48. Edberg JC, Kimberly RP. Cell type-specific glycoforms of Fc gamma RIIIa (CD16): differential ligand binding. J Immunol 1997; 159:3849-57.
49. Rozsnyay Z, Sármay G, Walker M, Maslanka K, Valasek Z, Jefferis R, Gergely J. Distinctive role of IgG1 and IgG3 isotypes in Fc gamma R-mediated functions. Immunology 1989; 66:491-8.
50. Aase A, Michaelsen TE. Opsonophagocytic activity induced by chimeric antibodies of the four human IgG subclasses with or without help from complement. Scand J Immunol 1994; 39:581-9.
51. Roux KH, Strelets L, Michaelsen TE. Flexibility of human IgG subclasses. J Immunol 1997; 159:3372-82.
52. Burton DR, Woof JM. Human antibody effector function. Adv Immunol 1992; 51:1-84.
53. Taylor RR, Allen SJ, Greenwood BM, Riley EM. IgG3 antibodies to Plasmodium falciparum merozoite surface protein 2 (MSP2): increasing prevalence with age and association with clinical immunity to malaria. Am J Trop Med Hyg 1998; 58:406-13.
54. Cavacini LA, Emes CL, Power J, Desharnais FD, Duval M, Montefiori D, Posner MR. Influence of heavy chain constant regions on antigen binding and HIV-1 neutralization by a human monoclonal antibody. J Immunol 1995; 155:3638-44.
55. Carter PB, Collins FM. The route of enteric infection in normal mice. J Exp Med 1974; 139:1189-203.
56. Wain J, Diep TS, Ho VA, Walsh AM, Nguyen TT, Parry CM, White NJ. Quantitation of bacteria in blood of typhoid fever patients and relationship between counts and clinical features, transmissibility, and antibiotic resistance. J Clin Microbiol 1998; 36:1683-7.
57. Robbins JD, Robbins JB. Reexamination of the protective role of the capsular polysaccharide (Vi antigen) of Salmonella typhi. J Infect Dis 1984; 150:436-49.
58. Landy M. Studies on Vi antigen. VI. Immunization of human beings with purified Vi antigen. Am J Hyg 1954; 60:52-62.
59. Keitel WA, Bond NL, Zahradnik JM, Cramton TA, Robbins JB. Clinical and serological responses following primary and booster immunization with Salmonella typhi Vi capsular polysaccharide vaccines. Vaccine 1994; 12:195-9.
60. Brugier JC, Barra A, Schulz D, Preud'homme JL. Subclasses of human vaccinal antibodies to the Vi capsular polysaccharide of Salmonella typhi. Int J Clin Lab Res 1993; 23:38-41.
61. Aase A, Naess LM, Sandin RH et al. Comparison of functional immune responses in humans after intranasal and intramuscular immunisations with outer membrane vesicle vaccines against group B meningococcal disease. Vaccine 2003; 21:2042-51.
62. Van de Winkel JG, Anderson CL. Biology of human immunoglobulin G Fc receptors. J Leukoc Biol 1991; 49:511-24.
63. Anderson CL, Shen L, Eichen DM, Wewers MD, Gill JK. Phagocytosis mediated by three distinct Fc gamma receptor classes on human leukocytes. J Exp Med 1990; 171:1333-45.
64. Schiff DE, Rae J, Martin TR, Davis BH, Curnutte JT. Increased phagocyte FcgammaRI expression and improved Fc gamma-receptor-mediated phagocytosis after in vivo recombinant human interferon-gamma treatment of normal human subjects. Blood 1997; 90:3187-94.
65. Downey GP, Botelho RJ, Butler JR, Moltyaner Y, Chien P, Schreiber AD, Grinstein S. Phagosomal maturation, acidification, and inhibition of bacterial growth in nonphagocytic cells transfected with FcgammaRIIA receptors. J Biol Chem 1999; 274:28436-44.