Pulmonary TCR γδ T cells induce the early inflammation of granuloma formation by a glycolipid trehalose 6,6′-dimycolate (TDM) isolated from Mycobacterium tuberculosis

References

• WHO. Global tuberculosis control: WHO report. Geneva: World Health Organization; 2011.
   Google Scholar
• Cosma, C.L., Sherman, D.R., Ramakrishnan, L. The secret lives of the pathogenic mycobacteria. Annu Rev Microbiol 2003, 57, 641–676.
   PubMed Web of Science ®Google Scholar
• Ulrichs, T., Kaufmann, S.H. New insights into the function of granulomas in human tuberculosis. J Pathol 2006, 208, 261–269.
   PubMed Web of Science ®Google Scholar
• Russell, D.G., Mwandumba, H.C., Rhoades, E.E. Mycobacterium and the coat of many lipids. J Cell Biol 2002, 158, 421–426.
   Google Scholar
• Rhoades, E., Hsu, F., Torrelles, J.B., Turk, J., Chatterjee, D., Russell, D.G. Identification and macrophage-activating activity of glycolipids released from intracellular Mycobacteriumbovis BCG. Mol Microbiol 2003, 48, 875–888.
   Google Scholar
• Geisel, R.E., Sakamoto, K., Russell, D.G., Rhoades, E.R. In vivo activity of released cell wall lipids of Mycobacteriumbovis bacillus Calmette-Guérin is due principally to trehalose mycolates. J Immunol 2005, 174, 5007–5015.
   PubMed Web of Science ®Google Scholar
• Indrigo, J., Hunter, R.L. Jr, Actor, J.K. Cord factor trehalose 6,6′-dimycolate (TDM) mediates trafficking events during mycobacterial infection of murine macrophages. Microbiology (Reading, Engl) 2003, 149, 2049–2059.
   PubMed Web of Science ®Google Scholar
• Takimoto, H., Maruyama, H., Shimada, K.I., Yakabe, R., Yano, I., Kumazawa, Y. Interferon-γ independent formation of pulmonary granuloma in mice by injections with trehalose dimycolate (cord factor), lipoarabinomannan and phosphatidylinositol mannosides isolated from Mycobacterium tuberculosis. Clin Exp Immunol 2006, 144, 134–141.
   Google Scholar
• Petrofsky, M., Bermudez, L.E. Neutrophils from Mycobacterium avium-infected mice produce TNF-α, IL-12, and IL-1 β and have a putative role in early host response. Clin Immunol 1999, 91, 354–358.
   PubMedGoogle Scholar
• Pedrosa, J., Saunders, B.M., Appelberg, R., Orme, I.M., Silva, M.T., Cooper, A.M. Neutrophils play a protective nonphagocytic role in systemic Mycobacterium tuberculosis infection of mice. Infect Immun 2000, 68, 577–583.
   PubMed Web of Science ®Google Scholar
• Seiler, P., Aichele, P., Bandermann, S., Hauser, A.E., Lu, B., Gerard, N.P., Gerard, C., Ehlers, S., Mollenkopf, H.J., Kaufmann, S.H. Early granuloma formation after aerosol Mycobacterium tuberculosis infection is regulated by neutrophils via CXCR3-signaling chemokines. Eur J Immunol 2003, 33, 2676–2686.
   PubMed Web of Science ®Google Scholar
• Yao, Z., Painter, S.L., Fanslow, W.C., Ulrich, D., Macduff, B.M., Spriggs, M.K., Armitage, R.J. Human IL-17: a novel cytokine derived from T cells. J Immunol 1995, 155, 5483–5486.
   PubMed Web of Science ®Google Scholar
• Fossiez, F., Djossou, O., Chomarat, P., Flores-Romo, L., Ait-Yahia, S., Maat, C., Pin, J.J., Garrone, P., Garcia, E., Saeland, S., Blanchard, D., Gaillard, C., Das Mahapatra, B., Rouvier, E., Golstein, P., Banchereau, J., Lebecque, S. T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. J Exp Med 1996, 183, 2593–2603.
   PubMed Web of Science ®Google Scholar
• Spriggs, M.K. Interleukin-17 and its receptor. J Clin Immunol 1997, 17, 366–369.
   PubMed Web of Science ®Google Scholar
• Infante-Duarte, C., Horton, H.F., Byrne, M.C., Kamradt, T. Microbial lipopeptides induce the production of IL-17 in Th cells. J Immunol 2000, 165, 6107–6115.
   PubMed Web of Science ®Google Scholar
• Happel, K.I., Zheng, M., Young, E., Quinton, L.J., Lockhart, E., Ramsay, A.J., Shellito, J.E., Schurr, J.R., Bagby, G.J., Nelson, S., Kolls, J.K. Cutting edge: roles of Toll-like receptor 4 and IL-23 in IL-17 expression in response to Klebsiella pneumoniae infection. J Immunol 2003, 170, 4432–4436.
   PubMed Web of Science ®Google Scholar
• Jovanovic, D.V., Di Battista, J.A., Martel-Pelletier, J., Jolicoeur, F.C., He, Y., Zhang, M., Mineau, F., Pelletier, J.P. IL-17 stimulates the production and expression of proinflammatory cytokines, IL-β and TNF-α, by human macrophages. J Immunol 1998, 160, 3513–3521.
   PubMed Web of Science ®Google Scholar
• Laan, M., Cui, Z.H., Hoshino, H., Lötvall, J., Sjöstrand, M., Gruenert, D.C., Skoogh, B.E., Lindén, A. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J Immunol 1999, 162, 2347–2352.
   PubMed Web of Science ®Google Scholar
• Schwarzenberger, P., Huang, W., Ye, P., Oliver, P., Manuel, M., Zhang, Z., Bagby, G., Nelson, S., Kolls, J.K. Requirement of endogenous stem cell factor and granulocyte-colony-stimulating factor for IL-17-mediated granulopoiesis. J Immunol 2000, 164, 4783–4789.
   PubMed Web of Science ®Google Scholar
• Umemura, M., Yahagi, A., Hamada, S., Begum, M.D., Watanabe, H., Kawakami, K., Suda, T., Sudo, K., Nakae, S., Iwakura, Y., Matsuzaki, G. IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J Immunol 2007, 178, 3786–3796.
   PubMed Web of Science ®Google Scholar
• Brennan, P., Ballou, C.E. Biosynthesis of mannophosphoinositides by Mycobacterium phlei. The family of dimannophosphoinositides. J Biol Chem 1967, 242, 3046–3056.
   Google Scholar
• Yano, I., Tomiyasu, I., Kaneda, K., Kato, Y., Sumi, Y., Kurano, S., Sugimoto, N., Sawai, H. Isolation of mycolic acid-containing glycolipids in Nocardia rubra and their granuloma forming activity in mice. J Pharmacobio-dyn 1987, 10, 113–123.
   Google Scholar
• Watanabe, K., Hasunuma, R., Horikoshi, T., Yamana, H., Maruyama, H., Fujiwara, N., Kumazawa, Y., Yano, I.. Induction of hypersensitivity to endotoxin lethality in mice by treatement with trehalose 6,6′-dimycolate but not with 2,3,6,6′-tetaacyl trehalose 2′-sulfate. J Endotoxin Res 1999, 5, 23–30.
   Google Scholar
• Yamagami, H., Matsumoto, T., Fujiwara, N., Arakawa, T., Kaneda, K., Yano, I., Kobayashi, K. Trehalose 6,6′-dimycolate (cord factor) of Mycobacterium tuberculosis induces foreign-body- and hypersensitivity-type granulomas in mice. Infect Immun 2001, 69, 810–815.
   Google Scholar
• Beckman, E.M., Porcelli, S.A., Morita, C.T., Behar, S.M., Furlong, S.T., Brenner, M.B. Recognition of a lipid antigen by CD1-restricted α β+ T cells. Nature 1994, 372, 691–694.
   PubMed Web of Science ®Google Scholar
• Porcelli, S.A., Modlin, R.L. The CD1 system: antigen-presenting molecules for T cell recognition of lipids and glycolipids. Annu Rev Immunol 1999, 17, 297–329.
   PubMed Web of Science ®Google Scholar
• De Libero, G., Mori, L. Recognition of lipid antigens by T cells. Nat Rev Immunol 2005, 5, 485–496.
   PubMed Web of Science ®Google Scholar
• Sieling, P.A., Chatterjee, D., Porcelli, S.A., Prigozy, T.I., Mazzaccaro, R.J., Soriano, T., Bloom, B.R., Brenner, M.B., Kronenberg, M., Brennan, P.J. CD1-restricted T cell recognition of microbial lipoglycan antigens. Science 1995, 269, 227–230.
   PubMed Web of Science ®Google Scholar
• Moody, D.B., Reinhold, B.B., Guy, M.R., Beckman, E.M., Frederique, D.E., Furlong, S.T., Ye, S., Reinhold, V.N., Sieling, P.A., Modlin, R.L., Besra, G.S., Porcelli, S.A. Structural requirements for glycolipid antigen recognition by CD1b-restricted T cells. Science 1997, 278, 283–286.
   PubMed Web of Science ®Google Scholar
• Martin, L.H., Calabi, F., Lefebvre, F.A., Bilsland, C.A., Milstein, C. Structure and expression of the human thymocyte antigens CD1a, CD1b, and CD1c. Proc Natl Acad Sci USA 1987, 84, 9189–9193.
   Google Scholar
• Wang, C.R., Chen, G.H., Mandy, W.J. Identification of a rabbit class I-like thymocyte-specific antigen. J Immunol 1987, 138, 3352–3359.
   Google Scholar
• Calabi, F., Belt, K.T., Yu, C.Y., Bradbury, A., Mandy, W.J., Milstein, C. The rabbit CD1 and the evolutionary conservation of the CD1 gene family. Immunogenetics 1989, 30, 370–377.
   Google Scholar
• Bradbury, A., Belt, K.T., Neri, T.M., Milstein, C., Calabi, F. Mouse CD1 is distinct from and co-exists with TL in the same thymus. EMBO J 1988, 7, 3081–3086.
   PubMed Web of Science ®Google Scholar
• Balk, S.P., Bleicher, P.A., Terhorst, C. Isolation and expression of cDNA encoding the murine homologues of CD1. J Immunol 1991, 146, 768–774.
   Google Scholar
• Sugawara, I., Udagawa, T., Hua, S.C., Reza-Gholizadeh, M., Otomo, K., Saito, Y., Yamada, H. Pulmonary granulomas of guinea pigs induced by inhalation exposure of heat-treated BCG Pasteur, purified trehalose dimycolate and methyl ketomycolate. J Med Microbiol 2002, 51, 131–137.
   Google Scholar
• Hiromatsu, K., Dascher, C.C., LeClair, K.P., Sugita, M., Furlong, S.T., Brenner, M.B., Porcelli, S.A. Induction of CD1-restricted immune responses in guinea pigs by immunization with mycobacterial lipid antigens. J Immunol 2002, 169, 330–339.
   PubMed Web of Science ®Google Scholar
• Kawashima, T., Norose, Y., Watanabe, Y., Enomoto, Y., Narazaki, H., Watari, E., Tanaka, S., Takahashi, H., Yano, I., Brenner, M.B., Sugita, M. Cutting edge: major CD8 T cell response to live bacillus Calmette-Guérin is mediated by CD1 molecules. J Immunol 2003, 170, 5345–5348.
   Google Scholar
• Khader, S.A., Bell, G.K., Pearl, J.E., Fountain, J.J., Rangel-Moreno, J., Cilley, G.E., Shen, F., Eaton, S.M., Gaffen, S.L., Swain, S.L., Locksley, R.M., Haynes, L., Randall, T.D., Cooper, A.M. IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 2007, 8, 369–377.
   PubMed Web of Science ®Google Scholar
• Wozniak, T.M., Ryan, A.A., Triccas, J.A., Britton, W.J. Plasmid interleukin-23 (IL-23), but not plasmid IL-27, enhances the protective efficacy of a DNA vaccine against Mycobacterium tuberculosis infection. Infect Immun 2006, 74, 557–565.
   PubMed Web of Science ®Google Scholar
• Happel, K.I., Lockhart, E.A., Mason, C.M., Porretta, E., Keoshkerian, E., Odden, A.R., Nelson, S., Ramsay, A.J. Pulmonary interleukin-23 gene delivery increases local T-cell immunity and controls growth of Mycobacterium tuberculosis in the lungs. Infect Immun 2005, 73, 5782–5788.
   PubMed Web of Science ®Google Scholar
• Lockhart, E., Green, A.M., Flynn, J.L. IL-17 production is dominated by γδ T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J Immunol 2006, 177, 4662–4669.
   PubMed Web of Science ®Google Scholar
• Peng, M.Y., Wang, Z.H., Yao, C.Y., Jiang, L.N., Jin, Q.L., Wang, J., Li, B.Q. Interleukin 17-producing γ δ T cells increased in patients with active pulmonary tuberculosis. Cell Mol Immunol 2008, 5, 203–208.
   PubMed Web of Science ®Google Scholar
• Happel, K.I., Dubin, P.J., Zheng, M., Ghilardi, N., Lockhart, C., Quinton, L.J., Odden, A.R., Shellito, J.E., Bagby, G.J., Nelson, S., Kolls, J.K. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J Exp Med 2005, 202, 761–769.
   PubMed Web of Science ®Google Scholar
• Ye, P., Rodriguez, F.H., Kanaly, S., Stocking, K.L., Schurr, J., Schwarzenberger, P., Oliver, P., Huang, W., Zhang, P., Zhang, J., Shellito, J.E., Bagby, G.J., Nelson, S., Charrier, K., Peschon, J.J., Kolls, J.K. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 2001, 194, 519–527.
   PubMed Web of Science ®Google Scholar
• Hayday, A.C. [γ][δ] cells: a right time and a right place for a conserved third way of protection. Annu Rev Immunol 2000, 18, 975–1026.
   PubMed Web of Science ®Google Scholar
• Ferrick, D.A., Schrenzel, M.D., Mulvania, T., Hsieh, B., Ferlin, W.G., Lepper, H. Differential production of interferon-γ and interleukin-4 in response to Th1- and Th2-stimulating pathogens by γ δ T cells in vivo. Nature 1995, 373, 255–257.
   PubMed Web of Science ®Google Scholar
• Rhodes, K.A., Andrew, E.M., Newton, D.J., Tramonti, D., Carding, S.R. A subset of IL-10-producing γδ T cells protect the liver from Listeria-elicited, CD8(+) T cell-mediated injury. Eur J Immunol 2008, 38, 2274–2283.
   Google Scholar
• Hamada, S., Umemura, M., Shiono, T., Hara, H., Kishihara, K., Tanaka, K., Mayuzumi, H., Ohta, T., Matsuzaki, G. Importance of murine Vδ1γδ T cells expressing interferon-γ and interleukin-17A in innate protection against Listeria monocytogenes infection. Immunology 2008, 125, 170–177.
   Google Scholar
• Okamoto Yoshida, Y., Umemura, M., Yahagi, A., O’Brien, R.L., Ikuta, K., Kishihara, K., Hara, H., Nakae, S., Iwakura, Y., Matsuzaki, G. Essential role of IL-17A in the formation of a mycobacterial infection-induced granuloma in the lung. J Immunol 2010, 184, 4414–4422.
   PubMed Web of Science ®Google Scholar
• D’Souza, C.D., Cooper, A.M., Frank, A.A., Mazzaccaro, R.J., Bloom, B.R., Orme, I.M. An anti-inflammatory role for γ δ T lymphocytes in acquired immunity to Mycobacterium tuberculosis. J Immunol 1997, 158, 1217–1221.
   PubMedGoogle Scholar