Containment of aerogenic Mycobacterium tuberculosis infection in mice does not require MyD88 adaptor function for TLR2, -4 and -9

European Journal of Immunology

Volumn 38, Issue 3, 2008, Pages 680-694

  Hölscher, Christoph ^a   Reiling, Norbert ^a   Schaible, Ulrich E ^b,c   Hölscher, Alexandria ^a   Bathmann, Clara ^a   Korbel, Daniel ^c   Lenz, Insa ^a   Sonntag, Tanja ^a   Kröger, Svenja ^a   Akira, Shizuo ^d   Mossmann, Horst ^e   Kirschning, Carsten J ^f   Wagner, Hermann ^f   Freudenberg, Marina ^e   Ehlers, Stefan ^a,g  

^a RESEARCH CENTER BORSTEL   (Germany)

^b MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^c LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^d OSAKA UNIVERSITY   (Japan)

^e MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^f TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^g UNIVERSITY OF KIEL   (Germany)

Author keywords

Bacterial infection; Monocyte macrophage; Mycobacterium; Rodent; TLR

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; CPG OLIGONUCLEOTIDE; CPG-OLIGONUCLEOTIDE; GUANINE NUCLEOTIDE BINDING PROTEIN; IFI1 PROTEIN, MOUSE; LIPOPOLYSACCHARIDE; MYD88 PROTEIN, MOUSE; NOS2 PROTEIN, MOUSE; OLIGODEOXYRIBONUCLEOTIDE; TLR2 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE; TLR9 PROTEIN, MOUSE; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; EFFECTOR CELL; HOST RESISTANCE; IMMUNE RESPONSE; INFECTION SENSITIVITY; LUNG TUBERCULOSIS; MACROPHAGE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; WILD TYPE; ANIMAL; ANIMAL ANATOMY; C57BL MOUSE; CELLULAR IMMUNITY; DRUG EFFECT; DRUG POTENTIATION; GENE EXPRESSION; GENETICS; IMMUNOLOGY; INNATE IMMUNITY; LUNG; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; PHYSIOLOGY; TUBERCULOSIS;

ANIMAL STRUCTURES; ANIMALS; CYTOKINES; GENE EXPRESSION; GTP-BINDING PROTEINS; IMMUNITY, CELLULAR; IMMUNITY, NATURAL; INTERFERON TYPE II; LIPOPOLYSACCHARIDES; LUNG; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYCOBACTERIUM TUBERCULOSIS; MYELOID DIFFERENTIATION FACTOR 88; NITRIC OXIDE SYNTHASE TYPE II; OLIGODEOXYRIBONUCLEOTIDES; T-LYMPHOCYTES; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 9; TUBERCULOSIS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 43649084921     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200736458     Document Type: Article

References (54)

1. Kau̧fmann, S. H., Tuberculosis: Back on the immunologists' agenda. Immunity 2006. 24: 351-357.
2. Maher, D. and Raviglione, M., Global epidemiology of tuberculosis. Clin. Chest Med. 2005. 26: 167-182, v.
3. Kaufmann, S. H., How can immunology contribute to the control of tuberculosis? Nat. Rev. Immunol. 2001. 1: 20-30.
4. North, R. J. and Jung, Y. J., Immunity to tuberculosis. Annu. Rev. Immunol. 2004. 22: 599-623.
5. Flynn, J. L. and Chan, J., Immunology of tuberculosis. Annu. Rev. Immunol. 2001. 19: 93-129.
6. + T cells through IL-12 produced by Listeria-induced macrophages. Science 1993. 260: 547-549.
7. Trinchieri, G., Interleukin-12 and its role in the generation of TH1 cells. Immunol. Today 1993. 14: 335-338.
8. Schaible, U. E., Sturgill-Koszycki, S., Schlesinger, P. H. and Russell, D. G., Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J. Immunol. 1998. 160: 1290-1296.
9. MacMicking, J. D., Taylor, G. A. and McKinney, J. D., Immune control of tuberculosis by IFN-gamma-inducible LRG-47. Science 2003. 302: 654-659.
10. Gutierrez, M. G., Master, S. S., Singh, S. B., Taylor, G. A., Colombo, M. I. and Deretic, V., Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 2004. 119: 753-766.
11. MacMicking, J. D., North, R. J., LaCourse, R., Mudgett, J. S., Shah, S. K. and Nathan, C. F., Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. USA 1997. 94: 5243-5248.
12. Gilleron, M., Quesniaux, V. F. and Puzo, G., Acylation state of the phosphatidylinositol hexamannosides from Mycobacterium bovis bacillus Calmette Guerin and Mycobacterium tuberculosis H37Rv and its implication in Toll-like receptor response. J. Biol. Chem. 2003. 278: 29880-29889.
13. Jones, B.W., Means, T. K., Heldwein, K. A., Keen, M. A., Hill, P. J., Belisle, J. T. and Fenton, M. J., Different Toll-like receptor agonists induce distinct macrophage responses. J. Leukoc. Biol. 2001. 69: 1036-1044.
14. Means, T. K., Lien, E., Yoshimura, A., Wang, S., Golenbock, D. T. and Fenton, M. J., The CD14 ligands lipoarabinomannan and lipopolysaccharide differ in their requirement for Toll-like receptors. J. Immunol. 1999. 163: 6748-6755.
15. Thoma-Uszynski, S., Stenger, S., Takeuchi, O., Ochoa, M. T., Engele, M., Sieling, P. A., Barnes, P. F. et al., Induction of direct antimicrobial activity through mammalian toll-like receptors. Science 2001. 291: 1544-1547.
16. Means, T. K., Wang, S., Lien, E., Yoshimura, A., Golenbock, D. T. and Fenton, M. J., Human toll-like receptors mediate cellular activation by Mycobacterium tuberculosis. J. Immunol. 1999. 163: 3920-3927.
17. Means, T. K., Jones, B. W., Schromm, A. B., Shurtleff, B. A., Smith, J. A., Keane, J., Golenbock, D. T. et al., Differential effects of a Toll-like receptor antagonist on Mycobacterium tuberculosis-induced macrophage responses. J. Immunol. 2001. 166: 4074-4082.
18. Krieg, A. M., CpG motifs in bacterial DNA and their immune effects. Annu. Rev. Immunol. 2002. 20: 709-760.
19. Bafica, A., Scanga, C. A., Feng, C. G., Leifer, C., Cheever, A. and Sher, A., TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J. Exp. Med. 2005. 202: 1715-1724.
20. Reiling, N., Holscher, C., Fehrenbach, A., Kroger, S., Kirschning, C. J., Goyert, S. and Ehlers, S., Cutting edge: Toll-like receptor (TLR)2- and TLR4-mediated pathogen recognition in resistance to airborne infectionwith Mycobacterium tuberculosis. J. Immunol. 2002. 169: 3480-3484.
21. Shi, S., Blumenthal, A., Hickey, C.M., Gandotra, S., Levy, D. and Ehrt, S., Expression of many immunologically important genes in Mycobacterium tuberculosis-infected macrophages is independent of both TLR2 and TLR4 but dependent on IFN-alphabeta receptor and STAT1. J. Immunol. 2005. 175: 3318-3328.
22. Abel, B., Thieblemont, N., Quesniaux, V. J., Brown, N., Mpagi, J., Miyake, K., Bihl, F. and Ryffel, B., Toll-like receptor 4 expression is required to control chronic Mycobacterium tuberculosis infection in mice. J. Immunol. 2002. 169: 3155-3162.
23. Drennan, M. B., Nicolle, D., Quesniaux, V. J., Jacobs, M., Allie, N., Mpagi, J., Fremond, C. et al., Toll-like receptor 2-deficient mice succumb to Mycobacterium tuberculosis infection. Am. J. Pathol. 2004. 164: 49-57.
24. Shim, T. S., Turner, O. C. and Orme, I.M., Toll-like receptor 4 plays no role in susceptibility of mice to Mycobacterium tuberculosis infection. Tuberculosis (Edinb.) 2003. 83: 367-371.
25. Sugawara, I., Yamada, H., Li, C., Mizuno, S., Takeuchi, O. and Akira, S., Mycobacterial infection in TLR2 and TLR6 knockout mice. Microbiol. Immunol. 2003. 47: 327-336.
26. Ryffel, B., Fremond, C., Jacobs, M., Parida, S., Botha, T., Schnyder, B. and Quesniaux, V., Innate immunity to mycobacterial infection in mice: Critical role for toll-like receptors. Tuberculosis (Edinb.) 2005. 85: 395-405.
27. Scanga, C. A., Bafica, A., Feng, C. G., Cheever, A. W., Hieny, S. and Sher, A., 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. 2004. 72: 2400-2404.
28. Medzhitov, R., Preston-Hurlburt, P., Kopp, E., Stadlen, A., Chen, C., Ghosh, S. and Janeway, C. A. Jr., MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 1998. 2: 253-258.
29. Kawai, T., Adachi, O., Ogawa, T., Takeda, K. and Akira, S., Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 1999. 11: 115-122.
30. Scanga, C. A., Aliberti, J., Jankovic, D., Tilloy, F., Bennouna, S., Denkers, E. Y., Medzhitov, R. and Sher, A., Cutting edge: MyD88 is required for resistance to Toxoplasma gondii infection and regulates parasite-induced IL-12 production by dendritic cells. J. Immunol. 2002. 168: 5997-6001.
31. Seki, E., Tsutsui, H., Tsuji, N. M., Hayashi, N., Adachi, K., Nakano, H., Futatsugi-Yumikura, S. et al., Critical roles of myeloid differentiation factor 88-dependent proinflammatory cytokine release in early phase clearance of Listeria monocytogenes in mice. J. Immunol. 2002. 169: 3863-3868.
32. Takeuchi, O., Hoshino, K. and Akira, S., Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J. Immunol. 2000. 165: 5392-5396.
33. Feng, C. G., Scanga, C. A., Collazo-Custodio, C. M., Cheever, A.W., Hieny, S., Caspar, P. and Sher, A., Mice lacking myeloid differentiation factor 88 display profound defects in host resistance and immune responses to Mycobacterium avium infection not exhibited by Toll-like receptor 2 (TLR2)- and TLR4-deficient animals. J. Immunol. 2003. 171: 4758-4764.
34. Fremond, C. M., Yeremeev, V., Nicolle, D.M., Jacobs, M., Quesniaux, V. F. and Ryffel, B., Fatal Mycobacterium tuberculosis infection despite adaptive immune response in the absence of MyD88. J. Clin. Invest. 2004. 114: 1790-1799.
35. Quesniaux, V., Fremond, C., Jacobs, M., Parida, S., Nicolle, D., Yeremeev, V., Bihl, F. et al., Toll-like receptor pathways in the immune responses to mycobacteria. Microbes Infect. 2004. 6: 946-959.
36. + T cells. Eur J. Immunol. 2006. 36: 1156-1167.
37. Shi, S., Nathan, C., Schnappinger, D., Drenkow, J., Fuortes, M., Block, E., Ding, A. et al., MyD88 primes macrophages for full-scale activation by interferon-gamma yet mediates few responses to Mycobacterium tuberculosis. J. Exp. Med. 2003. 198: 987-997.
38. Carroll, P., Muttucumaru, D. G. and Parish, T., Use of a tetracycline-inducible system for conditional expression in Mycobacterium tuberculosis and Mycobarterium smegmatis. Appl. Environ. Microbiol. 2005. 71: 3077-3084.
39. Brightbill, H. D., Libraty, D. H., Krutzik, S. R., Yang, R. B., Belisle, J. T., Bleharski, J. R., Maitland, M. et al., Host defense mechanisms triggered by microbial lipoproteins through toll-like receptors. Science 1999. 285: 732-736.
40. Underhill, D. M., Ozinsky, A., Smith, X D. and Aderem, A., Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc. Natl. Acad. Sci. USA 1999. 96: 14459-14463.
41. Kamath, A. B., Alt, J., Debbabi, H. and Behar, S. M., Toll-like receptor 4-defective C3H/HeJ mice are not more susceptible than other C3H substrains to infection with Mycobacterium tuberculosis. Infect. Immun. 2003. 71: 4112-4118.
42. Branger, J., Leemans, J. C., Florquin, S., Weijer, S., Speelman, P. and van der Poll, T., Toll-like receptor 4 plays a protective role in pulmonary tuberculosis in mice. Int. Immunol. 2004. 16: 509-516.
43. Flynn, J. L., Chan, J., Triebold, K. J., Dalton, D. K., Stewart, T. A. and Bloom, B. R., An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 1993. 178: 2249-2254.
44. Cooper, A. M., Dalton, D. K., StewaRT, T. A., Griffin, J. P., Russell, D. G. and Orme, I. M., Disseminated tuberculosis in interferon gamma gene-disrupted mice. J. Exp. Med. 1993. 178: 2243-2247.
45. Han, J., MyD88 beyond Toll. Nat. Immunol. 2006. 7: 370-371.
46. Sun, D. and Ding, A., MyD88-mediated stabilization of interferon-gamma-induced cytokine and chemokine mRNA. Nat. Immunol. 2006. 7, 375-381.
47. Blander, J. M. and Medzhitov, R., Regulation of phagosome maturation by signals from toll-like receptors. Science 2004. 304: 1014-1018.
48. Yates, R. M. and Russell, D. G., Phagosome maturation proceeds independently of stimulation of toll-like receptors 2 and 4. Immunity 2005. 23: 409-417
49. Sugawara, I., Yamada, H., Kaneko, H., Mizuno, S., Takeda, K. and Akira, S., Role of interleukin-18 (IL-18) in mycobacterial infection in IL-18-gene-disrupted mice. Infect. Immun. 1999. 67: 2585-2589.
50. Fremond, C. M., Togbe, D., Doz, E., Rose, S., Vasseur, V., Maillet, I., Jacobs, M. et al., IL-1 receptor-mediated signal is an essential component of MyD88-dependent innate response to Mycobacterium tuberculosis infection. J Immunol. 2007. 179: 1178-1189.
51. Martinon, F. and Tschopp, J., NLRs join TLR as innate sensors of pathogens. Trends Immunol. 2005. 28: 447-454.
52. van der Wel, N., Hava, D., Houben, D., Fluitsma, D., van Zon, M., Pierson, J., Brenner, M. and Peters, P. J., M. tuberculosis and M. leprue translocate from the phagolysosome to the cytosol in myeloid cells. Cell 2007. 129: 1287-1298.
53. Holscher, C., Holscher, A., Ruckerl, D., Yoshimoto, T., Yoshida, H., Mak, T., Saris, C. and Ehlers, S., The IL-27 receptor chain WSX-1 differentially regulates antibacterial immunity and survival during experimental tuberculosis. J. Immunol. 2005. 174: 3534-3544.
54. Holscher, C., Kohler, G., Muller, U., Mossmann, H., Schaub, G. A. and Brombacher, F., Defective nitric oxide effector functions lead to extreme susceptibility of Trypanosoma cruzi-infected mice deficient in gamma interferon receptor or inducible nitric oxide synthase. Infect. Immun. 1998. 66: 1208-1215.