TLR adaptor MyD88 is essential for pathogen control during oral Toxoplasma gondii infection but not adaptive immunity induced by a vaccine strain of the parasite

Journal of Immunology

Volumn 181, Issue 5, 2008, Pages 3464-3473

  Sukhumavasi, Woraporn ^a   Egan, Charlotte E ^a   Warren, Amy L ^a   Taylor, Gregory A ^b   Fox, Barbara A ^c   Bzik, David J ^c   Denkers, Eric Y ^a  

^a Department of Obstetrics Gynecology   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GUANOSINE TRIPHOSPHATASE; INTERLEUKIN 12; MYELOID DIFFERENTIATION FACTOR 88; URACIL; VACCINE; PROTOZOAL VACCINE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUXOTROPHY; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HOST PARASITE INTERACTION; IMMUNE RESPONSE; IMMUNITY; INFECTION; INTESTINE MUCOSA; MOUSE; MOUTH INFECTION; NEUTROPHIL; NONHUMAN; PARASITE; PRIORITY JOURNAL; PROTOZOAL INFECTION; TOXOPLASMA GONDII; VIRULENCE; ANIMAL; BIOSYNTHESIS; GENETICS; IMMUNOLOGY; MOUSE MUTANT; PARASITOLOGY; PHYSIOLOGY; T LYMPHOCYTE; TOXOPLASMA; TOXOPLASMOSIS;

ANIMALS; FEMALE; IMMUNITY; INTERFERON TYPE II; INTESTINAL MUCOSA; MICE; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; PROTOZOAN VACCINES; T-LYMPHOCYTES; TOXOPLASMA; TOXOPLASMOSIS;

EID: 51549098030     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.5.3464     Document Type: Article

References (63)

1. Medzhitov, R. 2007. Recognition of microorganisms and activation of the immune response. Nature 449: 819-826. (Pubitemid 47598622)
2. Uematsu, S., and S. Akira. 2008. Toll-like receptors (TLRs) and their ligands. Handb. Exp. Pharmacol. 183: 1-20.
3. Kawai, T., O. Adachi, T. Ogawa, K. Takeda, and S. Akira. 1999. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11: 115-122.
4. Kawai, T., and S. Akira. 2007. TLR signaling. Semin. Immunol. 19: 24-32.
5. O'Neill, L., A., and A. G. Bowie. 2007. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7: 353-364.
6. Edelson, B. T., and E. R. Unanue. 2002. MyD88-dependent but Toll-like receptor 2-independent innate immunity to Listeria: no role for either in macrophage listericidal activity. J. Immunol. 169: 3869-3875.
7. Macedo, G. C., D. M. Magnani, N. B. Carvalho, O. Bruna-Romero, R. T. Gazzinelli, and S. C. Oliveira. 2008. Central role of MyD88-dependent dendritic cell maturation and proinflammatory cytokine production to control Brucella abortus infection. J. Immunol. 180: 1080-1087.
8. Takeuchi, O., K. Hoshino, and S. Akira. 2000. Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J. Immunol. 165: 5392-5396. (Pubitemid 30836143)
9. Scanga, C. A., A. Bafica, C. G. Feng, A. W. Cheever, S. Hieny, and A. Sher. 2004. MyD88-deficient mice display a profound loss in resistance to Mycobacterium tuberculosis associated with partially impaired Th1 cytokine and nitric oxide synthase 2 expression. Infect. Immun. 72: 2400-2404.
10. Gazzinelli, R. T., and E. Y. Denkers. 2006. Protozoan encounters with Toll-like receptor signalling pathways: implications for host parasitism. Nat. Rev. Immunol. 6: 895-906.
11. Adachi, K., H. Tsutsui, S. Kashiwamura, E. Seki, H. Nakano, O. Takeuchi, K. Takeda, K. Okumura, L. Van Kaer, H. Okamura, et al. 2001. Plasmodium berghei infection in mice induces liver injury by an IL-12- and Toll-like receptor/ myeloid differentiation factor 88-dependent mechanism. J. Immunol. 167: 5928-5934. (Pubitemid 33062788)
12. Campos, M. A., M. Closel, E. P. Valente, J. E. Cardoso, S. Akira, J. I. Alvarez-Leite, C. Ropert, and R. T. Gazzinelli. 2004. Impaired production of proinflammatory cytokines and host resistance to acute infection with Trypanosoma cruzi in mice lacking functional myeloid differentiation factor 88. J. Immunol. 172: 1711-1718.
13. Muraille, E., C. De Trez, M. Brait, P. De Baetselier, O. Leo, and Y. Carlier. 2003. Genetically resistant mice lacking MyD88-adapter protein display a high susceptibility to Leishmania major infection associated with a polarized Th2 response. J. Immunol. 170: 4237-4241. (Pubitemid 36428190)
14. Scanga, C. A., J. Aliberti, D. Jankovic, F. Tilloy, S. Bennouna, E. Y. Denkers, R. Medzhitov, and A. Sher. 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.
15. Hitziger, N., I. Dellacasa, B. Albiger, and A. Barragan. 2005. Dissemination of Toxoplasma gondii to immunoprivileged organs and role of Toll/interleukin-1 receptor signalling for host resistance assessed by in vivo bioluminsecence imaging. Cell Microbiol. 6: 837-848.
16. Campos, M. A. S., I. C. Almeida, O. Takeuchi, S. Akira, E. P. Valente, D. O. Procópio, L. R. Travassos, J. A. Smith, D. T. Golenbock, and R. T. Gazzinelli. 2001. Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite. J. Immunol. 167: 416-423.
17. Parroche, P., F. N. Lauw, N. Goutagny, E. Latz, B. G. Monks, A. Visintin, K. A. Halmen, M. Lamphier, M. Olivier, D. C. Bartholomeu, et al. 2007. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proc. Natl. Acad. Sci. USA 104: 1919-1924. (Pubitemid 46239879)
18. Yarovinsky, F., D. Zhang, J. F. Anderson, G. L. Bannenberg, C. N. Serhan, M. S. Hayden, S. Hieny, F. S. Sutterwala, R. A. Flavell, S. Ghosh, and A. Sher. 2005. TLR11 activation of dendritic cells by a protozoan profilin-like protein. Science 308: 1626-1629. (Pubitemid 40807512)
19. Bafica, A., H. C. Santiago, R. Goldszmid, C. Ropert, R. T. Gazzinelli, and A. Sher. 2006. Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection. J. Immunol. 177: 3515-3519. (Pubitemid 44359881)
20. Napolitani, G., A. Rinaldi, F. Bertoni, F. Sallusto, and A. Lanzavecchia. 2005. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat. Immunol. 6: 769-776. (Pubitemid 43090462)
21. Trinchieri, G., and A. Sher. 2007. Cooperation of Toll-like receptor signals in innate immune defence. Nat. Rev. Immunol. 7: 179-190. (Pubitemid 46310482)
22. Kabelitz, D., and R. Medzhitov. 2007. Innate immunity-cross-talk with adaptive immunity through pattern recognition receptors and cytokines. Curr. Opin. Immunol. 19: 1-3. (Pubitemid 46091738)
23. Pasare, C., and R. Medzhitov. 2004. Toll-dependent control mechanisms of CD4 T cell activation. Immunity 21: 733-741. (Pubitemid 39487894)
24. Schnare, M., G. M. Barton, A. C. Holt, K. Takeda, S. Akira, and R. Medzhitov. 2001. Toll-like receptors control activation of adaptive immune responses. Nat. Immunol. 2: 947-950. (Pubitemid 32976167)
25. Way, S. S., T. R. Kollmann, A. M. Hajjar, and C. B. Wilson. 2003. Cutting edge: protective cell-mediated immunity to Listeria monocytogenes in the absence of myeloid differentiation factor 88. J. Immunol. 171: 533-537.
26. Kursar, M., H. W. Mittrucker, M. Koch, A. Kohler, M. Herma, and S. H. Kaufmann. 2004. Protective T cell response against intracellular pathogens in the absence of Toll-like receptor signaling via myeloid differentiation factor 88. Int. Immunol. 16: 415-421. (Pubitemid 38313150)
27. Bolz, D. D., R. S. Sundsbak, Y. Ma, S. Akira, C. J. Kirschning, J. F. Zachary, J. H. Weis, and J. J. Weis. 2004. MyD88 plays a unique role in host defense but not arthritis development in Lyme disease. J. Immunol. 173: 2003-2010.
28. Guay, H. M., T. A. Andreyeva, R. L. Garcea, R. M. Welsh, and E. Szomolanyi-Tsuda. 2007. MyD88 is required for the formation of long-term humoral immunity to virus infection. J. Immunol. 178: 5124-5131.
29. Zhou, S., E. A. Kurt-Jones, L. Mandell, A. Cerny, M. Chan, D. T. Golenbock, and R. W. Finberg. 2005. MyD88 is critical for the development of innate and adaptive immunity during acute lymphocytic choriomeningitis virus infection. Eur. J. Immunol. 35: 822-830. (Pubitemid 40425538)
30. Denkers, E. Y., and R. T. Gazzinelli. 1998. Regulation and function of T cellmediated immunity during Toxoplasma gondii infection. Clin. Microbiol. Rev. 11: 569-588.
31. Peterson, E., and O. Liesenfeld. 2007. Clinical disease and diagnostics. In Toxoplasma gondii. The Model Apicomplexan: Perspectives and Methods. L. M. Weiss, and K. Kim, eds. Academic Press, Amsterdam, p. 81.
32. Debierre-Grockiego, F., M. A. Campos, N. Azzouz, J. Schmidt, U. Bieker, M. G. Resende, D. S. Mansur, R. Weingart, R. R. Schmidt, D. T. Golenbock, et al. 2007. Activation of TLR2 and TLR4 by glycosylphosphatidylinositols derived from Toxoplasma gondii. J. Immunol. 179: 1129-1137.
33. Plattner, F., F. Yarovinsky, S. Romero, D. Didry, M. F. Carlier, A. Sher, and D. Soldati-Favre. 2008. Toxoplasma profilin is essential for host cell invasion and TLR dependent induction of interleukin-12. Cell Host Microbe 14: 77-87.
34. Yarovinsky, F., and A. Sher. 2006. Toll-like receptor recognition of Toxoplasma gondii. Int. J. Parasitol. 36: 255-259. (Pubitemid 43376107)
35. + T cell response. Immunity 25: 655-664.
36. Taylor, G. A., M. Jeffers, D. A. Largaespada, N. A. Jenkins, N. G. Copeland, and G. F. Woude. 1996. Identification of a novel GTPase, the inducibly expressed GTPase, that accumulates in response to interferon γ. J. Biol. Chem. 271: 20399-20405.
37. Sukhumavasi, W., C. E. Egan, and E. Y. Denkers. 2007. Mouse neutrophils require JNK2 MAPK for Toxoplasma gondii-induced IL-12p40 and CCL2/MCP-1 release. J. Immunol. 179: 3570-3577.
38. Kim, L., B. A. Butcher, and E. Y. Denkers. 2004. Toxoplasma gondii interferes with lipopolysaccharide-induced mitogen-activated protein kinase activation by mechanisms distinct from endotoxin tolerance. J. Immunol. 172: 3003-3010. (Pubitemid 38263688)
39. Gavrilescu, L. C., B. A. Butcher, L. Del Rio, G. A. Taylor, and E. Y. Denkers. 2004. STAT1 is essential for antimicrobial function but dispensable for γ interferon production during Toxoplasma gondii infection. Infect. Immun. 72: 1257-1264.
40. Bliss, S. K., B. A. Butcher, and E. Y. Denkers. 2000. Rapid recruitment of neutrophils with prestored IL-12 during microbial infection. J. Immunol. 165: 4515-4521.
41. +-activated macrophages induced during acute toxoplasmosis. J. Leukocyte Biol. 74: 1-11.
42. Suzuki, Y., M. A. Orellana, R. D. Schreiber, and J. S. Remington. 1988. Interferon- γ: the major mediator of resistance against Toxoplasma gondii. Science 240: 516-518. (Pubitemid 18121089)
43. -/- setting. Immunity 16: 429-439.
44. Taylor, G. A., C. M. Collazo, G. S. Yap, K. Nguyen, T. A. Gregorio, L. S. Taylor, B. Eagleson, L. Secret, E. A. Southon, S. W. Reid, et al. 2000. Pathogen-specific loss of host resistance in mice lacking the IFN-γ-inducible gene IGTP. Proc. Natl. Acad. Sci. USA 97: 751-755.
45. Bliss, S. K., Y. Zhang, and E. Y. Denkers. 1999. Murine neutrophil stimulation by Toxoplasma gondii antigen drives high level production of IFN-γ-independent IL-12. J. Immunol. 163: 2081-2088.
46. Fox, B. A., and D. J. Bzik. 2002. De novo pyrimidine biosynthesis is required for virulence of Toxoplasma gondii. Nature 415: 926-929. (Pubitemid 34174756)
47. Shaw, M. H., G. J. Freeman, M. F. Scott, B. A. Fox, D. J. Bzik, Y. Belkaid, and G. S. Yap. 2006. Tyk2 negatively regulates adaptive Th1 immunity by mediating IL-10 signaling and promoting IFN-γ-dependent IL-10 reactivation. J. Immunol. 176: 7263-7271.
48. Larosa, D. F., J. S. Stumhofer, A. E. Gelman, A. H. Rahman, D. K. Taylor, C. A. Hunter, and L. A. Turka. 2008. T cell expression of MyD88 is required for resistance to Toxoplasma gondii. Proc. Natl. Acad. Sci. USA 105: 3855-3860.
49. Heimesaat, M. M., S. Bereswill, A. Fischer, D. Fuchs, D. Struck, J. Niebergall, H. K. Jahn, I. R. Dunay, A. Moter, D. M. Gescher, et al. 2006. Gram-negative bacteria aggravate murine small intestinal Th1-type immunopathology following oral infection with Toxoplasma gondii. J. Immunol. 177: 8785-8795.
50. Kelsall, B. L., and F. Leon. 2005. Involvement of intestinal dendritic cells in oral tolerance, immunity to pathogens, and inflammatory bowel disease. Immunol. Rev. 206: 132-148.
51. Gavin, A. L., K. Hoebe, B. Duong, T. Ota, C. Martin, B. Beutler, and D. Nemazee. 2006. Adjuvant-enhanced antibody responses in the absence of toll-like receptor signaling. Science 314: 1936-1938.
52. + T cell priming during respiratory fungal infection. Immunity 25: 665-675.
53. Bafica, A., C. A. Scanga, C. G. Feng, C. Leifer, A. Cheever, and A. Sher. 2005. TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J. Exp. Med. 202: 1715-1724. (Pubitemid 41815877)
54. Fremond, C. M., V. Yeremeev, D. M. Nicolle, M. Jacobs, V. F. Quesniaux, and B. Ryffel. 2004. Fatal Mycobacterium tuberculosis infection despite adaptive immune response in the absence of MyD88. J. Clin. Invest. 114: 1790-1799.
55. Holscher, C., N. Reiling, U. E. Schaible, A. Holscher, C. Bathmann, D. Korbel, I. Lenz, T. Sonntag, S. Kroger, S. Akira, et al. 2008. Containment of aerogenic Mycobacterium tuberculosis infection in mice does not require MyD88 adaptor function for TLR2, -4 and -9. Eur. J. Immunol. 38: 680-694.
56. Reiling, N., S. Ehlers, and C. Holscher. 2008. MyDths and un-TOLLed truths: sensor, instructive and effector immunity to tuberculosis. Immunol. Lett. 116: 15-23.
57. Minns, L. A., L. C. Menard, D. M. Foureau, S. Darche, C. Ronet, D. W. Mielcarz, D. Buzoni-Gatel, and L. H. M. Kasper. 2006. TLR9 is required for the gut-associated lymphoid tissue response following oral infection of Toxoplasma gondii. J. Immunol. 176: 7589-7597.
58. Lebeis, S. L., B. Bommarius, C. A. Parkos, M. A. Sherman, and D. Kalman. 2007. TLR signaling mediated by MyD88 is required for a protective innate immune response by neutrophils to Citrobacter rodentium. J. Immunol. 179: 566-577.
59. Rodriguez, N., F. Fend, L. Jennen, M. Schiemann, N. Wantia, C. U. Prazeres da Costa, S. Durr, U. Heinzmann, H. Wagner, and T. Miethke. 2005. Polymorphonuclear neutrophils improve replication of Chlamydia pneumoniae in vivo upon MyD88-dependent attraction. J. Immunol. 174: 4836-4844. (Pubitemid 40504567)
60. + cell subpopulations during microbial infection. Immunol. Res. 40: 35-48.
61. Halonen, S. K., G. A. Taylor, and L. M. Weiss. 2001. Gamma interferon-induced inhibition of Toxoplasma gondii in astrocytes is mediated by IGTP. Infect. Immun. 69: 5573-5576.
62. Ling, Y. M., M. H. Shaw, C. Ayala, I. Coppens, G. A. Taylor, D. J. Ferguson, and G. S. Yap. 2006. Vacuolar and plasma membrane stripping and autophagic elimination of Toxoplasma gondii in primed effector macrophages. J. Exp. Med. 203: 2063-2071. (Pubitemid 44352228)
63. Kim, L., B. A. Butcher, C. W. Lee, S. Uematsu, S. Akira, and E. Y. Denkers. 2006. Toxoplasma gondii genotype determines MyD88-dependent signaling in infected macrophages. J. Immunol. 177: 2584-2591. (Pubitemid 44201017)