Crucial role of gamma interferon-producing CD4+ Th1 cells but dispensable function of cd8+ t cell, B cell, Th2, and Th17 responses in the control of Brucella melitensis infection in mice

Infection and Immunity

Volumn 80, Issue 12, 2012, Pages 4271-4280

  Vitry, Marie Alice ^a   Trez, Carl De ^b   Goriely, Stanislas ^c   Dumoutier, Laure ^d   Akira, Shizuo ^e   Ryffel, Bernhard ^f   Carlier, Yves ^c   Letesson, Jean Jacques ^a   Murailleg, Eric ^c  

^a University of Namur   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^d LUDWIG INSTITUTE FOR CANCER RESEARCH   (Belgium)

^e OSAKA UNIVERSITY   (Japan)

^f UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

BRUCELLA VACCINE; GAMMA INTERFERON; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ARTICLE; B LYMPHOCYTE; BACTERIAL CLEARANCE; BRUCELLA MELITENSIS; BRUCELLOSIS; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG SAFETY; GENETIC DISORDER; HUMORAL IMMUNITY; IMMUNOREGULATION; INTERFERON PRODUCTION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PANEL STUDY; PRIMARY INFECTION; PRIORITY JOURNAL; TH1 CELL; TH17 CELL; TH2 CELL;

ANIMALS; B-LYMPHOCYTES; BRUCELLA MELITENSIS; BRUCELLOSIS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; HUMANS; INTERFERON-GAMMA; MICE; MICE, INBRED C57BL; TH1 CELLS; TH17 CELLS; TH2 CELLS;

EID: 84870784832     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00761-12     Document Type: Article

References (75)

1. Araya LN, Elzer PH, Rowe GE, Enright FM, Winter AJ. 1989. Temporal development of protective cell-mediated and humoral immunity in BALB/c mice infected with Brucella abortus. J. Immunol. 143:3330-3337.
2. -/- mouse model. Clin. Vaccine Immunol. 19:249-260.
3. Baldwin CL, Goenka R. 2006. Host immune responses to the intracellular bacteria Brucella: does the bacteria instruct the host to facilitate chronic infection? Crit. Rev. Immunol. 26:407-442.
4. Baldwin CL, Parent M. 2002. Fundamentals of host immune response against Brucella abortus: what the mouse model has revealed about control of infection. Vet. Microbiol. 90:367-382.
5. Bettelli E, Korn T, Kuchroo VK. 2007. Th17: the third member of the effector T cell trilogy. Curr. Opin. Immunol. 19:652-657.
6. Brandao AP, et al. 2012. Host susceptibility to Brucella abortus infection is more pronounced in IFN-gamma knockout than IL-12/beta2- microglobulin double-deficient mice. Clin. Dev. Immunol. 2012:589494.
7. Colucci F, et al. 1999. Dissecting NK cell development using a novel alymphoid mouse model: investigating the role of the c-abl protooncogene in murine NK cell differentiation. J. Immunol. 162:2761-2765.
8. Cook L, et al. 2008. Evidence that CD8+ dendritic cells enable the development of gammadelta T cells that modulate airway hyperresponsiveness. J. Immunol. 181:309-319.
9. Cooper AM, et al. 2002. Mice lacking bioactive IL-12 can generate protective, antigen-specific cellular responses to mycobacterial infection only if the IL-12 p40 subunit is present. J. Immunol. 168:1322-1327.
10. 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.
11. Copin R, 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. doi:10.1371/journal.ppat.1002575.
12. Corbel MJ. 1997. Brucellosis: an overview. Emerg. Infect. Dis. 3:213-221.
13. Cosgrove D, et al. 1991. Mice lacking MHC class II molecules. Cell 66:1051-1066.
14. Curtis MM, Way SS. 2009. Interleukin-17 in host defence against bacterial, mycobacterial and fungal pathogens. Immunology 126:177-185.
15. Cutler SJ, Whatmore AM, Commander NJ. 2005. Brucellosis-new aspects of an old disease. J. Appl. Microbiol. 98:1270-1281.
16. Das G, Sheridan S, Janeway CA, Jr. 2001. The source of early IFN-gamma that plays a role in Th1 priming. J. Immunol. 167:2004-2010.
17. Elzer PH, et al. 1994. Antibody-mediated protection against Brucella abortus in BALB/c mice at successive periods after infection: variation between virulent strain 2308 and attenuated vaccine strain 19. Immunology 82:651-658.
18. Fernandes DM, Baldwin CL. 1995. Interleukin-10 downregulates protective immunity to Brucella abortus. Infect. Immun. 63:1130-1133.
19. 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 Immunol. Med. Microbiol. 16:193-203.
20. Ficht TA, Kahl-McDonagh MM, Arenas-Gamboa AM, Rice-Ficht AC. 2009. Brucellosis: the case for live, attenuated vaccines. Vaccine 27(Suppl 4):D40-D43.
21. Giambartolomei GH, Scian R, Acosta-Rodriguez E, Fossati CA, Delpino MV. 2012. Brucella abortus-infected macrophages modulate T lymphocytes to promote osteoclastogenesis via IL-17. Am. J. Pathol. 181:887-896.
22. Gill N, Finlay BB. 2011. The gut microbiota: challenging immunology. Nat. Rev. Immunol. 11:636-637.
23. Godfroid J, et al. 2005. From the discovery of the Malta fever's agent to the discovery of a marine mammal reservoir, brucellosis has continuously been a re-emerging zoonosis. Vet. Res. 36:313-326.
24. 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.
25. Grillo MJ, Blasco JM, Gorvel JP, Moriyon I, Moreno E. 2012. What have we learned from brucellosis in the mouse model? Vet. Res. 43:29.
26. Happel KI, et al. 2005. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202:761-769.
27. Happel KI, et al. 2005. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202:761-769.
28. Hemmers S, Mowen KA. 2009. T(H)2 bias: Mina tips the balance. Nat. Immunol. 10:806-808.
29. Huang W, Na L, Fidel PL, Schwarzenberger P. 2004. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J. Infect. Dis. 190:624-631.
30. Izadjoo MJ, et al. 2000. Impaired control of Brucella melitensis infection in Rag1-deficient mice. Infect. Immun. 68:5314-5320.
31. Kawabe T, et al. 1994. The immune responses in CD40-deficient mice: impaired immunoglobulin class switching and germinal center formation. Immunity 1:167-178.
32. Kawai T, Adachi O, Ogawa T, Takeda K, Akira S. 1999. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11:115-122.
33. Kelly-Welch AE, Hanson EM, Boothby MR, Keegan AD. 2003. Interleukin-4 and interleukin-13 signaling connections maps. Science 300: 1527-1528.
34. Khader SA, et al. 2007. IL-23 and IL-17 in the establishment of protective pulmonary CD4+T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 8:369-377.
35. Khader SA, et al. 2005. IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-gamma responses if IL-12p70 is available. J. Immunol. 175:788-795.
36. Kim J, et al. 2008. Beta 2-microglobulin deficient mice catabolize IgG more rapidly than FcRn- alpha-chain deficient mice. Exp. Biol. Med.(Maywood) 233:603-609.
37. Kitamura D, Roes J, Kuhn R, Rajewsky K. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 350:423-426.
38. Ko J, Gendron-Fitzpatrick A, Splitter GA. 2002. Susceptibility of IFN regulatory factor-1 and IFN consensus sequence binding protein-deficient mice to brucellosis. J. Immunol. 168:2433-2440.
39. Kreymborg K, et al. 2007. IL-22 is expressed by Th17 cells in an IL-23-dependent fashion, but not required for the development of autoimmune encephalomyelitis. J. Immunol. 179:8098-8104.
40. Leonard WJ, Spolski R. 2005. Interleukin-21: a modulator of lymphoid proliferation, apoptosis and differentiation. Nat. Rev. Immunol. 5:688-698.
41. Lieberman LA, et al. 2004. IL-23 provides a limited mechanism of resistance to acute toxoplasmosis in the absence of IL-12. J. Immunol. 173: 1887-1893.
42. Locksley RM, et al. 1991. Induction of Th1 and Th2 CD4+subsets during murine Leishmania major infection. Res. Immunol. 142:28-32.
43. Locksley RM, Heinzel FP, Sadick MD, Holaday BJ, Gardner KD, Jr. 1987. Murine cutaneous leishmaniasis: susceptibility correlates with differential expansion of helper T-cell subsets. Ann. Inst. Pasteur Immunol.138:744-749.
44. Locksley RM, Scott P. 1991. Helper T-cell subsets in mouse leishmaniasis:induction, expansion and effector function. Immunol. Today 12:A58-A61.
45. Magram J, et al. 1996. IL-12-deficient mice are defective in IFN gamma production and type 1 cytokine responses. Immunity 4:471-481.
46. Mangan PR, et al. 2006. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441:231-234.
47. Martirosyan A, Moreno E, Gorvel JP. 2011. An evolutionary strategy for a stealthy intracellular Brucella pathogen. Immunol. Rev. 240:211-234.
48. Mattner F, et al. 1996. Genetically resistant mice lacking interleukin-12 are susceptible to infection with Leishmania major and mount a polarized Th2 cell response. Eur. J. Immunol. 26:1553-1559.
49. Mielke ME. 1991. T cell subsets in granulomatous inflammation and immunity to L. Monocytogenes and B. abortus. Behring Inst. Mitt., p 99-111.
50. Mombaerts P, et al. 1992. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68:869-877.
51. Montaraz JA, Winter AJ. 1986. Protection against Brucella abortus in mice with O-polysaccharide-specific monoclonal antibodies. Infect. Im-mun. 51:961-963.
52. Murphy EA, Parent M, Sathiyaseelan J, Jiang X, Baldwin CL. 2001. Immune control of Brucella abortus 2308 infections in BALB/c mice. FEMS Immunol. Med. Microbiol. 32:85-88.
53. Murphy EA, Sathiyaseelan J, Parent MA, Zou B, Baldwin CL. 2001. Interferon-gamma is crucial for surviving a Brucella abortus infection in both resistant C57BL/6 and susceptible BALB/c mice. Immunology 103: 511-518.
54. Nakae S, et al. 2002. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17:375-387.
55. Oliveira SC, Giambartolomei GH, Cassataro J. 2011. Confronting the barriers to develop novel vaccines against brucellosis. Expert Rev. Vaccines 10:1291-1305.
56. Oliveira SC, Splitter GA. 1995. CD8+ type 1 CD44hi CD45 RBlo T lymphocytes control intracellular Brucella abortus infection as demonstrated in major histocompatibility complex class I-and class II-deficient mice. Eur. J. Immunol. 25:2551-2557.
57. Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV. 2006. The new global map of human brucellosis. Lancet Infect. Dis. 6:91-99.
58. Pasquevich KA, et al. 2011. An oral vaccine based on U-Omp19 induces protection against B. abortus mucosal challenge by inducing an adaptive IL-17 immune response in mice. PLoS One 6:e16203. doi:10.1371/ journal.pone.0016203.
59. Pavlov H, Hogarth M, McKenzie IF, Cheers C. 1982. In vivo and in vitro effects of monoclonal antibody to Ly antigens on immunity to infection. Cell. Immunol. 71:127-138.
60. Perkins SD, Smither SJ, Atkins HS. 2010. Towards a Brucella vaccine for humans. FEMS Microbiol. Rev. 34:379-394.
61. Rolan HG, Tsolis RM. 2007. Mice lacking components of adaptive immunity show increased Brucella abortus virB mutant colonization. Infect. Immun. 75:2965-2973.
62. Rolan HG, Xavier MN, Santos RL, Tsolis RM. 2009. Natural antibody contributes to host defense against an attenuated Brucella abortus virB mutant. Infect. Immun. 77:3004-3013.
63. Sathiyaseelan J, et al. 2006. Treatment of Brucella-susceptible mice with IL-12 increases primary and secondary immunity. Cell. Immunol. 243:1-9.
64. Schulz SM, et al. 2008. Protective immunity to systemic infection with attenuated Salmonella enterica serovar Enteritidis in the absence of IL-12 is associated with IL-23-dependent IL-22, but not IL-17. J. Immunol. 181: 7891-7901.
65. Shahinian A, et al. 1993. Differential T cell costimulatory requirements in CD28-deficient mice. Science 261:609-612.
66. Skyberg JA, et al. 2011. Murine and bovine gammadelta T cells enhance innate immunity against Brucella abortus infections. PLoS One 6:e21978. doi:10.1371/journal.pone.0021978.
67. Stevens MG, Pugh GW, Jr, Tabatabai LB. 1992. Effects of gamma inter-feron and indomethacin in preventing Brucella abortus infections in mice. Infect. Immun. 60:4407-4409.
68. Ubeda C, et al. 2012. Familial transmission rather than defective innate immunity shapes the distinct intestinal microbiota of TLR-deficient mice. J. Exp. Med. 209:1445-1456.
69. Umemura M, et al. 2007. IL-17-mediated regulation of innate and ac-quired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J. Immunol. 178:3786-3796.
70. Vance RE, Isberg RR, Portnoy DA. 2009. Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6:10-21.
71. Van Kaer L, Ashton-Ricleardt PG, Ploegh HL, Tonegawa S. 1992. TAP1 mutant mice are deficient in antigen presentation, surface class I molecules, and CD4-8+ T cells. Cell 71:1205-1214.
72. Weiss DS, Takeda K, Akira S, Zychlinsky A, Moreno E. 2005. MyD88, but not Toll-like receptors 4 and 2, is required for efficient clearance of Brucella abortus. Infect. Immun. 73:5137-5143.
73. Winter AJ, Duncan JR, Santisteban CG, Douglas JT, Adams LG. 1989. Capacity of passively administered antibody to prevent establishment of Brucella abortus infection in mice. Infect. Immun. 57:3438-3444.
74. Ye P, et al. 2001. Interleukin-17 and lung host defense against Kleb-siella pneumoniae infection. Am. J. Respir. Cell Mol. Biol. 25:335-340.
75. Zhan Y, Cheers C. 1993. Endogenous gamma interferon mediates resistance to Brucella abortus infection. Infect. Immun. 61:4899-4901.