Impaired innate immunity in mice deficient in interleukin-1 receptor-associated kinase 4 leads to defective type 1 t cell responses, b cell expansion, and enhanced susceptibility to infection with toxoplasma gondii

Infection and Immunity

Volumn 80, Issue 12, 2012, Pages 4298-4308

  Béla, Samantha R ^a,b   Dutra, Míriam S ^a,b   Mui, Ernest ^c   Montpetit, Alexandre ^d   Oliveira, Fernanda S ^b   Oliveira, Sérgio C ^b   Arantes, Rosa M E ^b   Antonelli, Lis R ^a   Mcleod, Rima ^c   Gazzinelli, Ricardo T ^a,b,e  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^c UNIVERSITY OF CHICAGO   (United States)

^d MCGILL UNIVERSITY   (Canada)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 4; INTERLEUKIN 12; RECOMBINANT INTERLEUKIN 12;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; B LYMPHOCYTE ACTIVATION; CELL EXPANSION; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; HOST RESISTANCE; IMMUNE RESPONSE; INFECTION SENSITIVITY; INNATE IMMUNITY; MACROPHAGE; MONOCYTE; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; PARASITISM; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE; TOXOPLASMA GONDII; TOXOPLASMOSIS;

ADULT; ANIMALS; B-LYMPHOCYTES; CHILD; CHILD, PRESCHOOL; DISEASE SUSCEPTIBILITY; FEMALE; GENOTYPE; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; TH1 CELLS; TOXOPLASMA; TOXOPLASMOSIS; TOXOPLASMOSIS, CONGENITAL;

EID: 84870811626     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00328-12     Document Type: Article

References (55)

1. Antonelli LR, et al. 2010. Intranasal poly-IC treatment exacerbates tuberculosis in mice through the pulmonary recruitment of a pathogenpermissive monocyte/macrophage population. J. Clin. Invest. 120:1674-1682.
2. Aosai F, et al. 2006. Toxoplasma gondii-derived heat shock protein 70 stimulates maturation of murine bone marrow-derived dendritic cells via Toll-like receptor 4. Cell Stress Chaperones 11:13-22.
3. Candolfi E, Hunter CA, Remington JS. 1994. Mitogen-and antigenspecific proliferation of T cells in murine toxoplasmosis is inhibited by reactive nitrogen intermediates. Infect. Immun. 62:1995-2001.
4. Cao Z, Henzel WJ, Gao X. 1996. IRAK: a kinase associated with the interleukin-1 receptor. Science 271:1128-1131.
5. Cardenes M, et al. 2006. Autosomal recessive interleukin-1 receptorassociated kinase 4 deficiency in fourth-degree relatives. J. Pediatr. 148: 549-551.
6. Casrouge A, et al. 2006. Herpes simplex virus encephalitis in human UNC-93B deficiency. Science 314:308-312.
7. Chen M, et al. 2002. Involvement of MyD88 in host defense and the down-regulation of anti-heat shock protein 70 autoantibody formation by MyD88 in Toxoplasma gondii-infected mice. J. Parasitol. 88:1017-1019.
8. Davidson DJ, et al. 2006. IRAK-4 mutation (Q293X): rapid detection and characterization of defective post-transcriptional TLR/IL-1R responses in human myeloid and non-myeloid cells. J. Immunol. 177:8202-8211.
9. Debierre-Grockiego F, et al. 2007. Activation of TLR2 and TLR4 by glycosylphosphatidylinositols derived from Toxoplasma gondii. J. Immunol. 179:1129-1137.
10. Denkers EY, Gazzinelli RT. 1998. Regulation and function of T-cellmediated immunity during Toxoplasma gondii infection. Clin. Microbiol. Rev. 11:569-588.
11. Dunay IR, et al. 2008. Gr1(+) inflammatory monocytes are required for mucosal resistance to the pathogen Toxoplasma gondii. Immunity 29:306-317.
12. Dunay IR, Fuchs A, Sibley LD. 2010. Inflammatory monocytes but not neutrophils are necessary to control infection with Toxoplasma gondii in mice. Infect. Immun. 78:1564-1570.
13. Garin A, et al. 2010. Toll-like receptor 4 signaling by follicular dendritic cells is pivotal for germinal center onset and affinity maturation. Immunity 33:84-95.
14. Gazzinelli RT, Denkers EY. 2006. Protozoan encounters with Toll-like receptor signalling pathways: implications for host parasitism. Nat. Rev. Immunol. 6:895-906.
15. Gazzinelli RT, Hakim FT, Hieny S, Shearer GM, Sher A. 1991. Synergistic role of CD4+ and CD8+T lymphocytes in IFN-gamma production and protective immunity induced by an attenuated Toxoplasma gondii vaccine. J. Immunol. 146:286-292.
16. Gazzinelli RT, et al. 1994. Parasite-induced IL-12 stimulates early IFNgamma synthesis and resistance during acute infection with Toxoplasma gondii. J. Immunol. 153:2533-2543.
17. Hayashi S, Chan CC, Gazzinelli R, Roberge FG. 1996. Contribution of nitric oxide to the host parasite equilibrium in toxoplasmosis. J. Immunol. 156:1476-1481.
18. Hill D, Dubey JP. 2002. Toxoplasma gondii: transmission, diagnosis and prevention. Clin. Microbiol. Infect. 8:634-640.
19. Hitziger N, Dellacasa I, Albiger B, Barragan A. 2005. Dissemination of Toxoplasma gondii to immunoprivileged organs and role of Toll/ interleukin-1 receptor signalling for host resistance assessed by in vivo bioluminescence imaging. Cell. Microbiol. 7:837-848.
20. Hwang IY, Park C, Harrison K, Kehrl JH. 2009. TLR4 signaling augments B lymphocyte migration and overcomes the restriction that limits access to germinal center dark zones. J. Exp. Med. 206:2641-2657.
21. Isnardi I, et al. 2008. IRAK-4-and MyD88-dependent pathways are essential for the removal of developing autoreactive B cells in humans. Immunity 29:746-757.
22. Jamieson SE, et al. 2009. Host genetic and epigenetic factors in toxoplasmosis. Mem. Inst. Oswaldo Cruz 104:162-169.
23. Li S, Strelow A, Fontana EJ, Wesche H. 2002. IRAK-4: a novel member of the IRAK family with the properties of an IRAK-kinase. Proc. Natl. Acad. Sci. U. S. A. 99:5567-5572.
24. Liesenfeld O, Kosek JC, Suzuki Y. 1997. Gamma interferon induces Fas-dependent apoptosis of Peyer's patch T cells in mice following peroral infection with Toxoplasma gondii. Infect. Immun. 65:4682-4689.
25. Liu CH, et al. 2006. Cutting edge: dendritic cells are essential for in vivo IL-12 production and development of resistance against Toxoplasma gondii infection in mice. J. Immunol. 177:31-35.
26. Mashayekhi M, et al. 2011. CD8alpha(+) dendritic cells are the critical source of interleukin-12 that controls acute infection by Toxoplasma gondii tachyzoites. Immunity 35:249-259.
27. McLeod R, et al. 2006. Outcome of treatment for congenital toxoplasmosis, 1981-2004: the National Collaborative Chicago-Based, Congenital Toxoplasmosis Study. Clin. Infect. Dis. 42:1383-1394.
28. McLeod R, et al. 1992. Levels of pyrimethamine in sera and cerebrospinal and ventricular fluids from infants treated for congenital toxoplasmosis. Toxoplasmosis Study Group. Antimicrob. Agents Chemother. 36:1040-1048.
29. McLeod R, et al. 1990. Phenotypes and functions of lymphocytes in congenital toxoplasmosis. J. Lab. Clin. Med. 116:623-635.
30. Medvedev AE, et al. 2003. Distinct mutations in IRAK-4 confer hyporesponsiveness to lipopolysaccharide and interleukin-1 in a patient with recurrent bacterial infections. J. Exp. Med. 198:521-531.
31. Melo MB, et al. 2010. UNC93B1 mediates host resistance to infection with Toxoplasma gondii. PLoS Pathog. 6:e1001071.
32. Mets MB, et al. 1996. Eye manifestations of congenital toxoplasmosis. Am. J. Ophthalmol. 122:309-324.
33. Minns LA, et al. 2006. TLR9 is required for the gut-associated lymphoid tissue response following oral infection of Toxoplasma gondii. J. Immunol. 176:7589-7597.
34. Mun HS, et al. 2005. Toll-like receptor 4 mediates tolerance in macrophages stimulated with Toxoplasma gondii-derived heat shock protein 70. Infect. Immun. 73:4634-4642.
35. Oliveira FS, et al. 2011. Interleukin-1 receptor-associated kinase 4 is essential for initial host control of Brucella abortus infection. Infect. Immun. 79:4688-4695.
36. Patel DV, et al. 1996. Resolution of intracranial calcifications in infants with treated congenital toxoplasmosis. Radiology 199:433-440.
37. Peixoto-Rangel AL, et al. 2009. Candidate gene analysis of ocular toxoplasmosis in Brazil: evidence for a role for toll-like receptor 9 (TLR9). Mem. Inst. Oswaldo Cruz 104:1187-1190.
38. Phan L, et al. 2008. Longitudinal study of new eye lesions in children with toxoplasmosis who were not treated during the first year of life. Am. J. Ophthalmol. 146:375-384.
39. Picard C, et al. 2003. Pyogenic bacterial infections in humans with IRAK-4 deficiency. Science 299:2076-2079.
40. Pifer R, Benson A, Sturge CR, Yarovinsky F. 2011. UNC93B1 is essential for TLR11 activation and IL-12-dependent host resistance to Toxoplasma gondii. J. Biol. Chem. 286:3307-3314.
41. Plattner F, et al. 2008. Toxoplasma profilin is essential for host cell invasion and TLR11-dependent induction of an interleukin-12 response. Cell Host Microbe 3:77-87.
42. Roizen N, et al. 2006. Impact of visual impairment on measures of cognitive function for children with congenital toxoplasmosis: implications for compensatory intervention strategies. Pediatrics 118:e379-e390.
43. Scanga CA, et al. 2002. Cutting edge: MyD88 is required for resistance to Toxoplasma gondii infection and regulates parasite-induced IL-12 production by dendritic cells. J. Immunol. 168:5997-6001.
44. Sibley LD, Ajioka JW. 2008. Population structure of Toxoplasma gondii: clonal expansion driven by infrequent recombination and selective sweeps. Annu. Rev. Microbiol. 62:329-351.
45. Sukhumavasi W, et al. 2008. TLR adaptor MyD88 is essential for pathogen control during oral Toxoplasma gondii infection but not adaptive immunity Ninduced by a vaccine strain of the parasite. J. Immunol. 181:3464-3473.
46. Suzuki N, et al. 2002. Severe impairment of interleukin-1 and Toll-like receptor signalling in mice lacking IRAK-4. Nature 416:750-756.
47. Suzuki N, Suzuki S, Yeh WC. 2002. IRAK-4 as the central TIR signaling mediator in innate immunity. Trends Immunol. 23:503-506.
48. Suzuki Y, Orellana MA, Schreiber RD, Remington JS. 1988. Interferongamma: the major mediator of resistance against Toxoplasma gondii. Science 240:516-518.
49. Suzuki Y, et al. 1996. Evidence for genetic regulation of susceptibility to toxoplasmic encephalitis in AIDS patients. J. Infect. Dis. 173:265-268.
50. Tabeta K, et al. 2006. The Unc93b1 mutation 3d disrupts exogenous antigen presentation and signaling via Toll-like receptors 3, 7 and 9. Nat. Immunol. 7:156-164.
51. Takeuchi O, Akira S. 2010. Pattern recognition receptors and inflammation. Cell 140:805-820.
52. Weiss LM, Dubey JP. 2009. Toxoplasmosis: A history of clinical observations. Int. J. Parasitol. 39:895-901.
53. Wesche H, et al. 1999. IRAK-M is a novel member of the Pelle/ interleukin-1 receptor-associated kinase (IRAK) family. J. Biol. Chem. 274:19403-19410.
54. Wilson DC, et al. 2010. Differential regulation of effector-and centralmemory responses to Toxoplasma gondii Infection by IL-12 revealed by racking of Tgd057-specific CD8+T cells. PLoS Pathog. 6:e1000815.
55. Yarovinsky F, et al. 2005. TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308:1626-1629.