Mycobacterial di-O-acyl trehalose inhibits Th-1 cytokine gene expression in murine cells by down-modulation of MAPK signaling

Immunobiology

Volumn 215, Issue 2, 2010, Pages 143-152

  Palma Nicolás, José Prisco ^a   Hernández Pando, Rogelio ^b   Segura, Erika ^a   Ibarra Sánchez, María J ^b   Estrada García, Iris ^c   Zentella Dehesa, Alejandro ^a,b   López Marín, Luz M ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

^c INSTITUTO POLITÉCNICO NACIONAL   (Mexico)

Author keywords

Glycolipids; Immune suppression; MAPK; PKC; Tuberculosis

Indexed keywords

DI O ACYLTREHALOSE; GAMMA INTERFERON; INTERLEUKIN 2; INTERLEUKIN 4; IONOMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHOLIPASE C GAMMA; TREHALOSE; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CELL WALL; BACTERIAL VIRULENCE; CALCIUM SIGNALING; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION REGULATION; LUNG TUBERCULOSIS; LYMPHOCYTE PROLIFERATION; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; TH1 CELL;

ANIMALS; ANTIGENS, BACTERIAL; CELLS, CULTURED; CYTOKINES; DOWN-REGULATION; GLYCOLIPIDS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED BALB C; MYCOBACTERIUM FORTUITUM; MYCOBACTERIUM TUBERCULOSIS; SPLEEN; TH1 CELLS; TRANSCRIPTION, GENETIC; TUBERCULOSIS, PULMONARY;

EID: 71849115738     PISSN: 01712985     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imbio.2009.03.010     Document Type: Article

References (35)

1. Asensio J.A., Arbues A., Perez E., Gicquel B., and Martin C. Live tuberculosis vaccines based on phoP mutants: a step towards clinical trials. Expert Opin. Biol. Ther. 8 (2008) 201-211
2. Besra G.S., Bolton R.C., McNeil M.R., Ridell M., Simpson K.E., Glushka J., van Halbeek H., Brennan P.J., and Minnikin D.E. Structural elucidation of a novel family of acyltrehaloses from Mycobacterium tuberculosis. Biochemistry 31 (1992) 9832-9837
3. Briken V., Porcelli S.A., Besra G.S., and Kremer L. Mycobacterial lipoarabinomannan and related lipoglycans: from biogenesis to modulation of the immune response. Mol. Microbiol. 53 (2004) 391-403
4. Chang S.T., Linderman J.J., and Kirschner D.E. Multiple mechanisms allow Mycobacterium tuberculosis to continuously inhibit MHC class II-mediated antigen presentation by macrophages. Proc. Natl. Acad. Sci. USA 102 (2005) 4530-4535
5. Delgado J.C., Tsai E.Y., Thim S., Baena A., Boussiotis V.A., Reynes J.M., Sath S., Grosjean P., Yunis E.J., and Goldfeld A.E. Antigen-specific and persistent tuberculin anergy in a cohort of pulmonary tuberculosis patients from rural Cambodia. Proc. Natl. Acad. Sci. USA 99 (2002) 7576-7581
6. Dower N.A., Stang S.L., Bottorff D.A., Ebinu J.O., Dickie P., Ostergaard H.L., and Stone J.C. RasGRP is essential for mouse thymocyte differentiation and TCR signaling. Nat. Immunol. 1 (2000) 317-321
7. Ebinu J.O., Stang S.L., Teixeira C., Bottorff D.A., Hooton J., Blumberg P.M., Barry M., Bleakley R.C., Ostergaard H.L., and Stone J.C. RasGRP links T-cell receptor signaling to Ras. Blood 95 (2000) 3199-3203
8. Ellner J.J. Regulation of the human immune response during tuberculosis. J. Lab. Clin. Med. 130 (1997) 469-475
9. Escamilla L., Mancilla R., Glender W., and Lopez-Marin L.M. Mycobacterium fortuitum glycolipids for the serodiagnosis of pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 154 (1996) 1864-1867
10. Flynn J.L., and Chan J. Immunology of tuberculosis. Ann. Rev. Immunol. 19 (2001) 93-129
11. Fournie J.J., Adams E., Mullins R.J., and Basten A. Inhibition of human lymphoproliferative responses by mycobacterial phenolic glycolipids. Infect. Immun. 57 (1989) 3653-3659
12. Franklin R.A., Tordai A., Patel H., Gardner A.M., Johnson G.L., and Gelfand E.W. Ligation of the T cell receptor complex results in activation of the Ras/Raf-1/MEK/MAPK cascade in human T lymphocytes. J. Clin. Invest. 93 (1994) 2134-2140
13. Gercken J., Pryjma J., Ernst M., and Flad H.D. Defective antigen presentation by Mycobacterium tuberculosis-infected monocytes. Infect. Immun. 62 (1994) 3472-3478
14. Giacomini E., Iona E., Ferroni L., Miettinen M., Fattorini L., Orefici G., Julkunen I., and Coccia E.M. Infection of human macrophages and dendritic cells with Mycobacterium tuberculosis induces a differential cytokine gene expression that modulates T cell response. J. Immunol. 166 (2001) 7033-7041
15. Grotzke J.E., and Lewinsohn D.M. Role of CD8+ T lymphocytes in control of Mycobacterium tuberculosis infection. Microb. Infect. 7 (2005) 776-788
16. Hernández-Pando R., Orozco H., Sampieri A., Pavon L., Velasquillo C., Larriva-Sahd J., Alcocer J.M., and Madrid M.V. Correlation between the kinetics of Th1, Th2 cells and pathology in a murine model of experimental pulmonary tuberculosis. Immunology 89 (1996) 26-33
17. Hmama Z., Gabathuler R., Jefferies W.A., de Jong G., and Reiner N.E. Attenuation of HLA-DR expression by mononuclear phagocytes infected with Mycobacterium tuberculosis is related to intracellular sequestration of immature class II heterodimers. J. Immunol. 161 (1998) 4882-4893
18. Kaufmann S.H. How can immunology contribute to the control of tuberculosis?. Nat. Rev. 1 (2001) 20-30
19. Kolch W., Heidecker G., Kochs G., Hummel R., Vahidi H., Mischak H., Finkenzeller G., Marme D., and Rapp U.R. Protein kinase C alpha activates RAF-1 by direct phosphorylation. Nature 364 (1993) 249-252
20. Lee J.S., Song C.H., Kim C.H., Kong S.J., Shon M.H., Suhr J.W., Jung S.S., Lim J.H., Kim H.J., Park J.K., Paik T.H., and Jo E.K. Depressed interleukin-12 production by peripheral blood mononuclear cells after in vitro stimulation with the 30-kDa antigen in recurrent pulmonary tuberculosis patients. Med. Microbiol. Immunol. 192 (2003) 61-69
21. Lee J.S., Song C.H., Lim J.H., Kim H.J., Park J.K., Paik T.H., Kim C.H., Kong S.J., Shon M.H., Jung S.S., and Jo E.K. The production of tumour necrosis factor-alpha is decreased in peripheral blood mononuclear cells from multidrug-resistant tuberculosis patients following stimulation with the 30-kDa antigen of Mycobacterium tuberculosis. Clin. Exp. Immunol. 132 (2003) 443-449
22. Launois P., Blum L., Dieye A., Millan J., Sarthou J.L., and Bach M.A. Phenolic glycolipid-1 from M. leprae inhibits oxygen free radical production by human mononuclear cells. Res. Immunol. 140 (1989) 847-855
23. Manca C., Reed M.B., Freeman S., Mathema B., Kreiswirth B., Barry 3rd C.E., and Kaplan G. Differential monocyte activation underlies strain-specific Mycobacterium tuberculosis pathogenesis. Infect. Immun. 72 (2004) 5511-5514
24. Noss E.H., Harding C.V., and Boom W.H. Mycobacterium tuberculosis inhibits MHC class II antigen processing in murine bone marrow macrophages. Cell Immunol. 201 (2000) 63-74
25. Puente L.G., Stone J.C., and Ostergaard H.L. Evidence for protein kinase C-dependent and -independent activation of mitogen-activated protein kinase in T cells: potential role of additional diacylglycerol binding proteins. J. Immunol. 165 (2000) 6865-6871
26. Reed M.B., Domenech P., Manca C., Su H., Barczak A.K., Kreiswirth B.N., Kaplan G., and Barry 3rd C.E. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431 (2004) 84-87
27. Robinson N., Kolter T., Wolke M., Rybniker J., Hartmann P., and Plum G. Mycobacterial phenolic glycolipid inhibits phagosome maturation and subverts the pro-inflammatory cytokine response. Traffic 9 (2008) 1936-1947
28. Rocha-Ramirez L.M., Estrada-Garcia I., Lopez-Marin L.M., Segura-Salinas E., Mendez-Aragon P., Van Soolingen D., Torres-Gonzalez R., Chacon-Salinas R., Estrada-Parra S., Maldonado-Bernal C., Lopez-Macias C., and Isibasi A. Mycobacterium tuberculosis lipids regulate cytokines, TLR-2/4 and MHC class II expression in human macrophages. Tuberculosis 88 (2008) 212-220
29. Roose J.P., Mollenauer M., Gupta V.A., Stone J., and Weiss A. A diacylglycerol-protein kinase C-RasGRP1 pathway directs Ras activation upon antigen receptor stimulation of T cells. Mol. Cell Biol. 25 (2005) 4426-4441
30. Saavedra R., Segura E., Leyva R., Esparza L.A., and Lopez-Marin L.M. Mycobacterial di-O-acyl-trehalose inhibits mitogen- and antigen-induced proliferation of murine T cells in vitro. Clin. Diagn Lab. Immunol. 8 (2001) 1081-1088
31. + T-cells. Microb. Infect. 8 (2006) 533-540
32. Saha B., Das G., Vohra H., Ganguly N.K., and Mishra G.C. Macrophage-T cell interaction in experimental mycobacterial infection. Selective regulation of co-stimulatory molecules on Mycobacterium-infected macrophages and its implication in the suppression of cell-mediated immune response. Eur. J. Immunol. 24 (1994) 2618-2624
33. Trushin S.A., Pennington K.N., Algeciras-Schimnich A., and Paya C.V. Protein kinase C and calcineurin synergize to activate IkappaB kinase and NF-kappaB in T lymphocytes. J. Biol. Chem. 274 (1999) 22923-22931
34. Trushin S.A., Pennington K.N., Carmona E.M., Asin S., Savoy D.N., Billadeau D.D., and Paya C.V. Protein kinase Calpha (PKCalpha) acts upstream of PKCtheta to activate IkappaB kinase and NF-kappaB in T lymphocytes. Mol. Cell Biol. 23 (2003) 7068-7081
35. van Crevel R., Ottenhoff T.H., and van der Meer J.W. Innate immunity to Mycobacterium tuberculosis. Clin. Microbiol. Rev. 15 (2002) 294-309