Quantification of the effects of antibodies on the extra- and intracellular dynamics of Salmonella enterica

Journal of the Royal Society Interface

Volumn 10, Issue 79, 2013, Pages

  Restif, Olivier ^a   Goh, Yun S ^a,b   Palayret, Matthieu ^a   Grant, Andrew J ^a   McKinley, Trevelyan J ^a   Clark, Michael R ^a   Mastroeni, Pietro ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

Author keywords

Antibodies; Bacteriology; Infection dynamics; Likelihood; Mathematical model; Salmonella enterica

Indexed keywords

ANTIBODIES; ANTIGEN-ANTIBODY REACTIONS; BACTERIOLOGY; FLUORESCENCE MICROSCOPY; MATHEMATICAL MODELS; SALMONELLA;

BACTERIAL NUMBERS; HUMAN IMMUNOGLOBULIN; IN-VITRO; INFECTION DYNAMICS; INTRACELLULAR DYNAMICS; LIKELIHOOD; MODEL PARAMETERS; RELATIVE EFFICIENCY; SALMONELLA ENTERICA; SALMONELLA INFECTIONS;

DYNAMICS;

BACTERIUM ANTIBODY; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G3; IMMUNOGLOBULIN G4; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN G;

ARTICLE; CELL HETEROGENEITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG EFFICACY; EXTRACELLULAR SPACE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IN VITRO STUDY; INTRACELLULAR SPACE; MACROPHAGE; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; OPSONIZATION; PHAGOCYTE; PHAGOCYTOSIS; QUANTITATIVE ANALYSIS; SALMONELLA ENTERICA; SIMULATION; TYPHOID FEVER; BIOLOGICAL MODEL; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; SALMONELLA TYPHIMURIUM; STATISTICAL MODEL;

BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA;

ANTIBODIES, BACTERIAL; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOGLOBULIN G; LIKELIHOOD FUNCTIONS; MICROSCOPY, FLUORESCENCE; MODELS, IMMUNOLOGICAL; PHAGOCYTES; SALMONELLA TYPHIMURIUM;

EID: 84872255947     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2012.0866     Document Type: Article

References (29)

1. Nowak MA et al. 1997 Viral dynamics of primary viremia and antiretroviral therapy in simian immunodeficiency virus infection. J. Virol. 71, 7518-7525. (Pubitemid 27391692)
2. Grant AJ, Restif O, McKinley TJ, Sheppard M, Maskell DJ, Mastroeni P. 2008 Modelling within-host spatiotemporal dynamics of invasive bacterial disease. PLoS Biol. 6, e74. (doi:10.1371/journal.pbio.0060074)
3. Saenz RA et al. 2010 Dynamics of infection and pathology in influenza. J. Virol. 84, 3974-3983. (doi:10.1128/JVI.02078-09)
4. Metcalf CJE. 2011 Partitioning regulatory mechanisms of within-host malaria dynamics using the effective propagation number. Science 333, 984-988. (doi:10.1126/science.1204588)
5. Edelson BT, Unanue ER. 2001 Intracellular antibody neutralizes listeria growth. Immunity 14, 503-512. (doi:10.1016/S1074-7613(01)00139-X)
6. Joller N, Weber SS, Muller AJ, Sporri R, Selchow P, Sander P, Hilbi H, Oxenius A. 2010 Antibodies protect against intracellular bacteria by Fc receptor-mediated lysosomal targeting. Proc. Natl Acad. Sci. USA 107, 20 441-20 446. (doi:10.1073/pnas.1013827107)
7. Uppington H, Menager N, Boross P, Wood J, Sheppard M, Verbeek S, Mastroeni P. 2006 Effect of immune serum and role of individual Fcγ receptors on the intracellular distribution and survival of Salmonella enterica serovar Typhimurium in murine macrophages. Immunology 119, 147-158. (doi:10.1111/j.1365-2567.2006.02416.x)
8. Bronzan RN et al. 2007 Bacteremia in Malawian children with severe malaria: prevalence, etiology, HIV coinfection, and outcome. J. Infect. Dis. 195, 895-904. (doi:10.1086/511437)
9. Graham SM, Molyneux EM, Walsh AL, Cheesbrough JS, Molyneux ME, Hart CA. 2000 Nontyphoidal Salmonella infections of children in tropical Africa. Pediatr. Infect. Dis. J. 19, 1189-1196. (doi:10.1097/00006454-200012000-00016)
10. Fields PI, Swarson RV, Haidaris CG, Heffron F. 1986 Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc. Natl Acad. Sci. USA 83, 5189-5193. (doi:10.1073/pnas.83.14.5189)
11. Richter-Dahlfors A, Buchan AMJ, Finlay BB. 1997 Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J. Exp. Med. 186, 569-580. (doi:10.1084/jem.186.4.569)
12. Brown SP, Cornell SJ, Sheppard M, Grant AJ, Maskell DJ, Grenfell BT, Mastroeni P. 2006 Intracellular demography and the dynamics of Salmonella enterica infections. PLoS Biol. 4, e349. (doi:10.1371/journal.pbio.0040349)
13. Gog JR et al. 2012 Dynamics of Salmonella infection of macrophages at the single cell level. J. R. Soc. Interface 9, 2696-2707. (doi:10.1098/rsif.2012. 0163)
14. Akeda H, Mitsuyama M, Tatsukawa K, Nomoto K, Takeya K. 1981 The synergistic contribution of macrophages and antibody to protection against Salmonella typhimurium during the early phase of infection. J. Gen. Microbiol. 123, 209-214. (Pubitemid 11126690)
15. 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. (Pubitemid 23260076)
16. Lindow JC, Fimlaid KA, Bunn JY, Kirkpatrick BD. 2011 Antibodies in action: role of human opsonins in killing Salmonella enterica serovar Typhi. Infect. Immun. 79, 3188-3194. (doi:10.1128/IAI.05081-11)
17. 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. USA 107, 3070-3075. (doi:10.1073/pnas.0910497107)
18. Goh YS, Grant AJ, Restif O, McKinley TJ, Armour KL, Clark MR, Mastroeni P. 2011 Human IgG isotypes and activating Fcg receptors in the interaction of Salmonella enterica serovar Typhimurium with phagocytic cells. Immunology 133, 74-83. (doi:10.1111/j.1365-2567.2011.03411.x)
19. Riechmann L, Clark M, Waldmann H, Winter G. 1988 Reshaping human antibodies for therapy. Nature 332, 323-327. (doi:10.1038/332323a0)
20. Redpath SM, Michaelsen TE, Sandlie I, Clark MR. 1998 The influence of the hinge region length in binding of human IgG to human Fcg receptors. Hum. Immunol. 59, 720-727. (doi:10.1016/S0198-8859(98)00075-5)
21. Armour KL, Clark MR, Hadley P, Williamson LM. 1999 Recombinant human IgG molecules lacking Fcg receptor I binding and monocyte triggering activities. Eur. J. Immunol. 29, 2613-2624. (doi:10. 1002/(SICI)1521-4141(199908)29: 08〈2613::AIDIMMU2613〉3.0.CO;2-J)
22. Shen L, Graziano RF, Fanger MW. 1989 The functional properties of FcgRI, II and III on myeloid cells: a comparative study of killing of erythrocytes and tumour cells mediated through the different Fc receptors. Mol. Immunol. 26, 959-969. (doi:10.1016/0161-5890(89)90114-4)
23. Helaine S, Thompson JA, Watson KG, Liu M, Boyle C, Holden DW. 2010 Dynamics of intracellular bacterial replication at the single cell level. Proc. Natl Acad. Sci. USA 107, 3746-3751. (doi:10.1073/pnas.1000041107)
24. R Development Core Team. 2012 R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
25. Burnham KP, Anderson DR. 2001 Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. New York, NY: Springer.
26. Sheppard M, Webb C, Heath F, Mallows V, Emilianus R, Maskell D, Mastroeni P. 2003 Dynamics of bacterial growth and distribution within the liver during Salmonella infection. Cell Microbiol. 5, 593-600. (doi:10.1046/j.1462-5822.2003. 00296.x)
27. Aase A, Michaelsen TE. 1994 Opsonophagocytic activity induced by chimeric antibodies of the four human IgG subclasses with or without help from complement. Scand. J. Immunol. 39, 581-587. (doi:10.1111/j.1365-3083.1994. tb03416.x)
28. Silva MT. 2010 Neutrophils and macrophages work in concert as inducers and effectors of adaptive immunity against extracellular and intracellular microbial pathogens. J. Leukoc. Biol. 87, 805-813. (doi:10.1189/jlb.1109767)
29. Eguchi M, Kikuchi Y. 2010 Binding of Salmonella-specific antibody facilitates specific T cell responses via augmentation of bacterial uptake and induction of apoptosis in macrophages. J. Infect. Dis. 201, 62-70. (doi:10.1086/648615)