ESAT-6 induced COX-2 expression involves coordinated interplay between PI3K and MAPK signaling

Molecular Immunology

Volumn 49, Issue 4, 2012, Pages 655-663

  A, Senthil Kumar ^a   Bansal, Kushagra ^a   Holla, Sahana ^a   Verma Kumar, Shalu ^a   Sharma, Pawan ^b   Balaji, Kithiganahalli Narayanaswamy ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

COX 2; ESAT 6; MAPK; Mycobacteria; PI3K; TLR2

Indexed keywords

CYCLOOXYGENASE 2; EARLY SECRETORY ANTIGENIC TARGET 6; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; STRESS ACTIVATED PROTEIN KINASE 1; TOLL LIKE RECEPTOR 2; TRANSCRIPTION FACTOR AP 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; MACROPHAGE FUNCTION; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUBERCULOSIS;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CELL LINE; CYCLOOXYGENASE 2; DINOPROSTONE; IMMUNITY, INNATE; MACROPHAGES; MAP KINASE SIGNALING SYSTEM; MICE; MICE, INBRED C57BL; MITOGEN-ACTIVATED PROTEIN KINASE 8; MITOGEN-ACTIVATED PROTEIN KINASE 9; MYCOBACTERIUM INFECTIONS; MYCOBACTERIUM TUBERCULOSIS; NF-KAPPA B; ONCOGENE PROTEIN V-AKT; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHATIDYLINOSITOL 3-KINASES; TOLL-LIKE RECEPTOR 2; TRANSCRIPTION FACTOR AP-1;

CORYNEBACTERINEAE; MYCOBACTERIUM TUBERCULOSIS;

EID: 84555217911     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2011.11.011     Document Type: Article

References (47)

1. Bansal K., Elluru S.R., Narayana Y., Chaturvedi R., Patil S.A., Kaveri S.V., Bayry J., Balaji K.N. PE_PGRS antigens of Mycobacterium tuberculosis induce maturation and activation of human dendritic cells. J. Immunol. 2011, 184:3495-3504.
2. Bansal K., Kapoor N., Narayana Y., Puzo G., Gilleron M., Balaji K.N. PIM2 induced COX-2 and MMP-9 expression in macrophages requires PI3K and Notch1 signaling. PLoS One 2009, 4:e4911.
3. Bansal K., Narayana Y., Patil S.A., Balaji K.N. M. bovis BCG induced expression of COX-2 involves nitric oxide-dependent and -independent signaling pathways. J. Leukoc. Biol. 2009, 85:804-816.
4. Bansal K., Sinha A.Y., Ghorpade D.S., Togarsimalemath S.K., Patil S.A., Kaveri S.V., Balaji K.N., Bayry J. Src homology 3-interacting domain of Rv1917c of Mycobacterium tuberculosis induces selective maturation of human dendritic cells by regulating PI3K-MAPK-NF-kappaB signaling and drives Th2 immune responses. J. Biol. Chem. 2010, 285:36511-36522.
5. Basu S., Pathak S., Pathak S.K., Bhattacharyya A., Banerjee A., Kundu M., Basu J. Mycobacterium avium-induced matrix metalloproteinase-9 expression occurs in a cyclooxygenase-2-dependent manner and involves phosphorylation- and acetylation-dependent chromatin modification. Cell. Microbiol. 2007, 9:2804-2816.
6. Blumenthal A., Ehlers S., Ernst M., Flad H.D., Reiling N. Control of mycobacterial replication in human macrophages: roles of extracellular signal-regulated kinases 1 and 2 and p38 mitogen-activated protein kinase pathways. Infect. Immun. 2002, 70:4961-4967.
7. Brodin P., Majlessi L., Marsollier L., de Jonge M.I., Bottai D., Demangel C., Hinds J., Neyrolles O., Butcher P.D., Leclerc C., Cole S.T., Brosch R. Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect. Immun. 2006, 74:88-98.
8. Brodin P., Rosenkrands I., Andersen P., Cole S.T., Brosch R. ESAT-6 proteins: protective antigens and virulence factors?. Trends Microbiol. 2004, 12:500-508.
9. Brown J.R., DuBois R.N. COX-2: a molecular target for colorectal cancer prevention. J. Clin. Oncol. 2005, 23:2840-2855.
10. Caparros E., Munoz P., Sierra-Filardi E., Serrano-Gomez D., Puig-Kroger A., Rodriguez-Fernandez J.L., Mellado M., Sancho J., Zubiaur M., Corbi A.L. DC-SIGN ligation on dendritic cells results in ERK and PI3K activation and modulates cytokine production. Blood 2006, 107:3950-3958.
11. Cartharius K., Frech K., Grote K., Klocke B., Haltmeier M., Klingenhoff A., Frisch M., Bayerlein M., Werner T. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 2005, 21:2933-2942.
12. Chen X., Zhou B., Li M., Deng Q., Wu X., Le X., Wu C., Larmonier N., Zhang W., Zhang H., Wang H., Katsanis E. CD4(+)CD25(+)FoxP3(+) regulatory T cells suppress Mycobacterium tuberculosis immunity in patients with active disease. Clin. Immunol. 2007, 123:50-59.
13. Davis J.M., Ramakrishnan L. The role of the granuloma in expansion and dissemination of early tuberculous infection. Cell 2009, 136:37-49.
14. Fitzpatrick F.A., Soberman R. Regulated formation of eicosanoids. J. Clin. Invest. 2001, 107:1347-1351.
15. Flynn J.L., Chan J. Immunology of tuberculosis. Annu. Rev. Immunol. 2001, 19:93-129.
16. Green J.A., Elkington P.T., Pennington C.J., Roncaroli F., Dholakia S., Moores R.C., Bullen A., Porter J.C., Agranoff D., Edwards D.R., Friedland J.S. Mycobacterium tuberculosis upregulates microglial matrix metalloproteinase-1 and -3 expression and secretion via NF-kappaB- and activator protein-1-dependent monocyte networks. J. Immunol. 2010, 184:6492-6503.
17. Guinn K.M., Hickey M.J., Mathur S.K., Zakel K.L., Grotzke J.E., Lewinsohn D.M., Smith S., Sherman D.R. Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis. Mol. Microbiol. 2004, 51:359-370.
18. Harper K.A., Tyson-Capper A.J. Complexity of COX-2 gene regulation. Biochem. Soc. Trans. 2008, 36:543-545.
19. Hilkens C.M., Snijders A., Vermeulen H., van der Meide P.H., Wierenga E.A., Kapsenberg M.L. Accessory cell-derived IL-12 and prostaglandin E2 determine the IFN-gamma level of activated human CD4+ T cells. J. Immunol. 1996, 156:1722-1727.
20. Jo E.K., Yang C.S., Choi C.H., Harding C.V. Intracellular signalling cascades regulating innate immune responses to Mycobacteria: branching out from Toll-like receptors. Cell. Microbiol. 2007, 9:1087-1098.
21. Jones B.W., Means T.K., Heldwein K.A., Keen M.A., Hill P.J., Belisle J.T., Fenton M.J. Different Toll-like receptor agonists induce distinct macrophage responses. J. Leukoc. Biol. 2001, 69:1036-1044.
22. Kalinski P., Vieira P.L., Schuitemaker J.H., de Jong E.C., Kapsenberg M.L. Prostaglandin E(2) is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer. Blood 2001, 97:3466-3469.
23. Khan K.N., Stanfield K., Trajkovic D., Harris R.K. Cyclooxygenase-2 expression in inflammatory lung lesions of nonhuman primates. Vet. Pathol. 2000, 37:512-516.
24. Koul A., Herget T., Klebl B., Ullrich A. Interplay between mycobacteria and host signalling pathways. Nat. Rev. Microbiol. 2004, 2:189-202.
25. Maiti D., Bhattacharyya A., Basu J. Lipoarabinomannan from Mycobacterium tuberculosis promotes macrophage survival by phosphorylating Bad through a phosphatidylinositol 3-kinase/Akt pathway. J. Biol. Chem. 2001, 276:329-333.
26. Nakahara T., Moroi Y., Uchi H., Furue M. Differential role of MAPK signaling in human dendritic cell maturation and Th1/Th2 engagement. J. Dermatol. Sci. 2006, 42:1-11.
27. Narayana Y., Balaji K.N. NOTCH1 up-regulation and signaling involved in Mycobacterium bovis BCG-induced SOCS3 expression in macrophages. J. Biol. Chem. 2008, 283:12501-12511.
28. Pathak S.K., Basu S., Basu K.K., Banerjee A., Pathak S., Bhattacharyya A., Kaisho T., Kundu M., Basu J. Direct extracellular interaction between the early secreted antigen ESAT-6 of Mycobacterium tuberculosis and TLR2 inhibits TLR signaling in macrophages. Nat. Immunol. 2007, 8:610-618.
29. Pathak S.K., Bhattacharyya A., Pathak S., Basak C., Mandal D., Kundu M., Basu J. Toll-like receptor 2 and mitogen- and stress-activated kinase 1 are effectors of Mycobacterium avium-induced cyclooxygenase-2 expression in macrophages. J. Biol. Chem. 2004, 279:55127-55136.
30. Pieters J. Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microb. 2008, 3:399-407.
31. Qiao D., Yang B.Y., Li L., Ma J.J., Zhang X.L., Lao S.H., Wu C.Y. ESAT-6- and CFP-10-specific Th1, Th22 and Th17 cells in tuberculous pleurisy may contribute to the local immune response against Mycobacterium tuberculosis infection. Scand. J. Immunol. 2011, 73:330-337.
32. Rangel Moreno J., Estrada Garcia I., De La Luz Garcia Hernandez M., Aguilar Leon D., Marquez R., Hernandez Pando R. The role of prostaglandin E2 in the immunopathogenesis of experimental pulmonary tuberculosis. Immunology 2002, 106:257-266.
33. *CFP-10 complex. Implications for pathogenesis and virulence. J. Biol. Chem. 2002, 277:21598-21603.
34. Schorey J.S., Cooper A.M. Macrophage signalling upon mycobacterial infection: the MAP kinases lead the way. Cell. Microbiol. 2003, 5:133-142.
35. Shibata Y., Gabbard J., Yamashita M., Tsuji S., Smith M., Nishiyama A., Henriksen R.A., Myrvik Q.N. Heat-killed BCG induces biphasic cyclooxygenase 2+ splenic macrophage formation-role of IL-10 and bone marrow precursors. J. Leukoc. Biol. 2006, 80:590-598.
36. Shibata Y., Henriksen R.A., Honda I., Nakamura R.M., Myrvik Q.N. Splenic PGE2-releasing macrophages regulate Th1 and Th2 immune responses in mice treated with heat-killed BCG. J. Leukoc. Biol. 2005, 78:1281-1290.
37. Stanley S.A., Johndrow J.E., Manzanillo P., Cox J.S. The Type I IFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J. Immunol. 2007, 178:3143-3152.
38. Stanley S.A., Raghavan S., Hwang W.W., Cox J.S. Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:13001-13006.
39. Stewart G.R., Robertson B.D., Young D.B. Tuberculosis: a problem with persistence. Nat. Rev. Microbiol. 2003, 1:97-105.
40. Surh Y.J., Kundu J.K. Signal transduction network leading to COX-2 induction: a road map in search of cancer chemopreventives. Arch. Pharm. Res. 2005, 28:1-15.
41. Toossi Z., Gogate P., Shiratsuchi H., Young T., Ellner J.J. Enhanced production of TGF-beta by blood monocytes from patients with active tuberculosis and presence of TGF-beta in tuberculous granulomatous lung lesions. J. Immunol. 1995, 154:465-473.
42. Ulrichs T., Kaufmann S.H. New insights into the function of granulomas in human tuberculosis. J. Pathol. 2006, 208:261-269.
43. van der Pouw Kraan T.C., van Lier R.A., Aarden L.A. PGE2 and the immune response. A central role for prostaglandin E2 in downregulating the inflammatory immune response. Mol. Med. Today 1995, 1:61.
44. Vilcek J., Klion A., Henriksen-DeStefano D., Zemtsov A., Davidson D.M., Davidson M., Friedman-Kien A.E., Le J. Defective gamma-interferon production in peripheral blood leukocytes of patients with acute tuberculosis. J. Clin. Immunol. 1986, 6:146-151.
45. Wang X., Barnes P.F., Dobos-Elder K.M., Townsend J.C., Chung Y.T., Shams H., Weis S.E., Samten B. ESAT-6 inhibits production of IFN-gamma by Mycobacterium tuberculosis-responsive human T cells. J. Immunol. 2009, 182:3668-3677.
46. Waters W.R., Palmer M.V., Whipple D.L., Carlson M.P., Nonnecke B.J. Diagnostic implications of antigen-induced gamma interferon, nitric oxide, and tumor necrosis factor alpha production by peripheral blood mononuclear cells from Mycobacterium bovis-infected cattle. Clin. Diagn. Lab. Immunol. 2003, 10:960-966.
47. Wu C.Y., Wang K., McDyer J.F., Seder R.A. Prostaglandin E2 and dexamethasone inhibit IL-12 receptor expression and IL-12 responsiveness. J. Immunol. 1998, 161:2723-2730.