CD4+ T Cell-derived IL-10 Promotes Brucella abortus Persistence via Modulation of Macrophage Function

PLoS Pathogens

Volumn 9, Issue 6, 2013, Pages

  Xavier, Mariana N ^a,b   Winter, Maria G ^a   Spees, Alanna M ^a   Nguyen, Kim ^a   Atluri, Vidya L ^a   Silva, Teane M A ^a,b   Bäumler, Andreas J ^a   Müller, Werner ^c   Santos, Renato L ^b   Tsolis, Renée M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 6; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL SURVIVAL; BRUCELLA ABORTUS; BRUCELLOSIS; CD4+ CD25+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOFLUORESCENCE MICROSCOPY; INFECTION CONTROL; INFLAMMATION; MACROPHAGE FUNCTION; MOUSE; NECROSIS; NEUTROPHIL; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR BLOCKING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THROMBOSIS; VASCULITIS;

ANIMALS; BRUCELLA ABORTUS; BRUCELLOSIS; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; INTERLEUKIN-10; MACROPHAGE ACTIVATION; MACROPHAGES; MICE; MICE, KNOCKOUT; MICROBIAL VIABILITY; NF-KAPPA B;

BACTERIA (MICROORGANISMS); BRUCELLA MELITENSIS BIOVAR ABORTUS; MUS;

EID: 84879548508     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003454     Document Type: Article

References (41)

1. Svetic A, Jian YC, Lu P, Finkeiman FD, Gause WC, (1993) Brucella abortus induces a novel cytokine gene expression pattern characterized by elevated IL-10 and IFN-g in CD4+ T cells. International Immunology 5: 877-883.
2. Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV, (2006) The new global map of human brucellosis. Lancet Infect Dis 6: 91-99.
3. Corbel MJ, (1997) Brucellosis: an overview. Emerg Infect Dis 3: 213-221.
4. Atluri VL, Xavier MN, de Jong MF, den Hartigh AB, Tsolis RM, (2011) Interactions of the Human Pathogenic Brucella Species with Their Hosts. Ann Rev Microbiol 65: 523-541.
5. Fernandes DM, Baldwin CL, (1995) Interleukin-10 downregulates protective immunity to Brucella abortus. Infection and Immunity 63: 1130-1133.
6. Fernandes DM, Jiang X, Jung JH, Baldwin CL, (1996) Comparison of T cell cytokines in resistant and susceptible mice infected with virulent Brucella abortus strain 2308. FEMS Immunology & Medical Microbiology 16: 193-203.
7. Murphy EA, Sathiyaseelan J, Parent MA, Zou B, Baldwin CL, (2001) Interferon-γ is crucial for surviving a Brucella abortus infection in both resistant C57BL/6 and susceptible BALB/c mice. Immunology 103: 511-518.
8. Barquero-Calvo E, Chaves-Olarte E, Weiss DS, Guzman-Verri C, Chacon-Diaz C, et al. (2007) Brucella abortus uses a stealthy strategy to avoid activation of the innate immune system during the onset of infection. PLoS ONE 2: e631.
9. Martirosyan A, Moreno E, Gorvel J-P, (2011) An evolutionary strategy for a stealthy intracellular Brucella pathogen. Immunological Reviews 240: 211-234.
10. Andersen-Nissen E, Smith KD, Strobe KL, Barrett SL, Cookson BT, et al. (2005) Evasion of Toll-like receptor 5 by flagellated bacteria. Proc Natl Acad Sci U S A 102: 9247-9252.
11. Saraiva M, O'Garra A, (2010) The regulation of IL-10 production by immune cells. Nat Rev Immunol 10: 170-181.
12. Sabat R, Grütz G, Warszawska K, Kirsch S, Witte E, et al. (2010) Biology of interleukin-10. Cytokine & Growth Factor Reviews 21: 331-344.
13. Belkaid Y, Hoffmann KF, Mendez S, Kamhawi S, Udey MC, et al. (2001) The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure. J Exp Med 194: 1497-1506.
14. Chang WLW, Barry PA, (2010) Attenuation of innate immunity by cytomegalovirus IL-10 establishes a long-term deficit of adaptive antiviral immunity. Proceedings of the National Academy of Sciences 107: 22647-22652.
15. Redford PS, Murray PJ, O'Garra A, (2011) The role of IL-10 in immune regulation during M. tuberculosis infection. Mucosal Immunol 4: 261-270.
16. Fernández-Lago L, Monte M, Chordi A, (1996) Endogenous gamma interferon and interleukin-10 in Brucella abortus 2308 infection in mice. FEMS Immunology & Medical Microbiology 15: 109-114.
17. Budak F, Göral G, Heper Y, Yilmaz E, Aymak F, et al. (2007) IL-10 and IL-6 gene polymorphisms as potential host susceptibility factors in Brucellosis. Cytokine 38: 32-36.
18. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A, (2001) Interleukin-10 and the interleukin-10 receptor. Annual Review of Immunology 19: 683-765.
19. Kamanaka M, Kim ST, Wan YY, Sutterwala FS, Lara-Tejero M, et al. (2006) Expression of Interleukin-10 in Intestinal Lymphocytes Detected by an Interleukin-10 Reporter Knockin tiger Mouse. Immunity 25: 941-952.
20. Shevach EM, (2002) CD4+CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2: 389-400.
21. Roers A, Siewe L, Strittmatter E, Deckert M, Schlüter D, et al. (2004) T Cell-specific Inactivation of the Interleukin 10 Gene in Mice Results in Enhanced T Cell Responses but Normal Innate Responses to Lipopolysaccharide or Skin Irritation. The Journal of Experimental Medicine 200: 1289-1297.
22. Hunt AC, Bothwell PW, (1967) Histological findings in human brucellosis. J Clin Pathol 20: 267-272.
23. Celli J, (2006) Surviving inside a macrophage: the many ways of Brucella. Res Microbiol 157: 93-98.
24. Starr T, Ng TW, Wehrly TD, Knodler LA, Celli J, (2008) Brucella intracellular replication requires trafficking through the late endosomal/lysosomal compartment. Traffic 9: 678-694.
25. Wang P, Wu P, Siegel MI, Egan RW, Billah MM, (1995) Interleukin (IL)-10 Inhibits Nuclear Factor B (NFB) Activation in Human Monocytes. Journal of Biological Chemistry 270: 9558-9563.
26. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O'Garra A, (1991) IL-10 inhibits cytokine production by activated macrophages. The Journal of Immunology 147: 3815-3822.
27. Pils MC, Pisano F, Fasnacht N, Heinrich J-M, Groebe L, et al. (2010) Monocytes/macrophages and/or neutrophils are the target of IL-10 in the LPS endotoxemia model. European Journal of Immunology 40: 443-448.
28. Suraud V, Olivier M, Bodier CC, Guilloteau LA, (2007) Differential expression of homing receptors and vascular addressins in tonsils and draining lymph nodes: Effect of Brucella infection in sheep. Veterinary Immunology and Immunopathology 115: 239-250.
29. Goenka R, Parent MA, Elzer PH, Baldwin CL, (2011) B Cell-deficient Mice Display Markedly Enhanced Resistance to the Intracellular Bacterium Brucella abortus. J Infect Dis 203: 1136-1146.
30. Skendros P, Boura P, Chrisagis D, Raptopoulou-Gigi M, (2007) Diminished percentage of CD4+ T-lymphocytes expressing interleukine-2 receptor alpha in chronic brucellosis. Journal of Infection 54: 192-197.
31. Pasquali P, Thornton AM, Vendetti S, Pistoia C, Petrucci P, et al. (2010) CD4+CD25+ T regulatory cells limit effector T cells and favor the progression of brucellosis in BALB/c mice. Microbes and Infection 12: 3-10.
32. O'Leary S, O'Sullivan MP, Keane J, (2011) IL-10 Blocks Phagosome Maturation in Mycobacterium tuberculosis-infected Human Macrophages. American Journal of Respiratory Cell and Molecular Biology 45: 172-180.
33. Barquero-Calvo E, Martirosyan A, Ordoñez-Rueda D, Arce-Gorvel V, Alfaro-Alarcón A, et al. (2013) Neutrophils Exert a Suppressive Effect on Th1 Responses to Intracellular Pathogen Brucella abortus. PLoS Pathog 9: e1003167.
34. Kreutzer DL, Dreyfus LA, Robertson DC, (1979) Interaction of polymorphonuclear leukocytes with smooth and rough strains of Brucella abortus. Infect Immun 23: 737-742.
35. Copin R, De Baetselier P, Carlier Y, Letesson JJ, Muraille E, (2007) MyD88-Dependent Activation of B220-CD11b+LY-6C+ Dendritic Cells during Brucella melitensis Infection. J Immunol 178: 5182-5191.
36. Peyron P, Vaubourgeix J, Poquet Y, Levillain F, Botanch C, et al. (2008) Foamy macrophages from tuberculous patients' granulomas constitute a nutrient-rich reservoir for M. tuberculosis persistence. PLoS Pathog 4: e1000204.
37. Copin R, Vitry M-A, Hanot Mambres D, Machelart A, De Trez C, et al. (2012) In Situ Microscopy Analysis Reveals Local Innate Immune Response Developed around Brucella Infected Cells in Resistant and Susceptible Mice. PLoS Pathog 8: e1002575.
38. Belkaid Y, Hoffmann KF, Mendez S, Kamhawi S, Udey MC, et al. (2001) The Role of Interleukin (IL)-10 in the Persistence of Leishmania major in the Skin after Healing and the Therapeutic Potential of Anti'ÄìIL-10 Receptor Antibody for Sterile Cure. The Journal of Experimental Medicine 194: 1497-1506.
39. Alton GG, Jones LM, Pietz DE (1975) Laboratory Techniques in Brucellosis. 2nd edition. Geneva: World Health Organization.
40. Rolan HG, Tsolis RM, (2007) Mice lacking components of adaptive immunity show increased Brucella abortus virB mutant colonization. Infect Immun 75: 2965-2973.
41. Rolán HG, Tsolis RM, (2008) Inactivation of the Type IV Secretion System Reduces the Th1 Polarization of the Immune Response to Brucella abortus Infection. Infection and Immunity 76: 3207-3213.