The PPE18 of Mycobacterium tuberculosis interacts with TLR2 and activates IL-10 induction in macrophage

Journal of Immunology

Volumn 183, Issue 10, 2009, Pages 6269-6281

  Nair, Shiny ^a   Ramaswamy, Poongothai A ^a   Ghosh, Sudip ^b   Joshi, Dhananjay C ^a   Pathak, Niteen ^a   Siddiqui, Imran ^c   Sharma, Pawan ^c   Hasnain, Seyed E ^a,d,e,f   Mande, Shekhar C ^a   Mukhopadhyay, Sangita ^a  

^a CENTRE FOR DNA FINGERPRINTING AND DIAGNOSTICS   (India)

^b NATIONAL INSTITUTE OF NUTRITION   (India)

^c INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY ICGEB   (India)

^d JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

^e UNIVERSITY OF HYDERABAD   (India)

^f INSTITUTE OF LIFE SCIENCES   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; INTERLEUKIN 10; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN PPE18; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM MUTANT; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MACROPHAGE; MUTATION; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TH2 CELL;

ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CELL LINE; CYTOKINES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES; MAP KINASE KINASE 4; MONOCYTES; MYCOBACTERIUM TUBERCULOSIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TUBERCULOSIS;

EID: 77954230361     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901367     Document Type: Article

References (65)

1. Cole, S. T., R. Brosch, J. Parkhill, T. Garnier, C. Churcher, D. Harris, S. V. Gordon, K. Eiglmeier, S. Gas, C. E. Barry, 3rd, et al. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.
2. Gey van Pittius, N. C., S. L. Sampson, H. Lee, Y. Kim, P. D. van Helden, and R. M. Warren. 2006. Evolution and expansion of the Mycobacterium tuberculosis PE and PPE multigene families and their association with the duplication of the ESAT-6 (esx) gene cluster regions. BMC Evol. Biol. 6: 95.
3. Brennan, M. J., and G. Delogu. 2002. The PE multigene family: a "molecular mantra" for mycobacteria. Trends Microbiol. 10: 246-249.
4. Ramakrishnan, L., N. A. Federspiel, and S. Falkow. 2000. Granuloma-specific expression of Mycobacterium virulence proteins from the glycine-rich PE-PGRS family. Science 288: 1436-1439.
5. Abdallah, A. M., T. Verboom, F. Hannes, M. Safi, M. Strong, D. Eisenberg, R. J. Musters, C. M. Vandenbroucke-Grauls, B. J. Appelmelk, J. Luirink, and W. A. Bitter. 2006. Specific secretion system mediates PPE41 transport in pathogenic mycobacteria. Mol. Microbiol. 62: 667-679.
6. Li, Y., E. Miltner, M. Wu, M. Petrofsky, and L. E. Bermudez. 2005. A Mycobacterium avium PPE gene is associated with the ability of the bacterium to grow in macrophages and virulence in mice. Cell Microbiol. 7: 539-548.
7. Choudhary, R. K., S. Mukhopadhyay, P. Chakhaiyar, N. Sharma, K. J. Murthy, V. M. Katoch, and S. E. Hasnain. 2003. PPE antigen Rv2430c of Mycobacterium tuberculosis induces a strong B-cell response. Infect. Immun. 71: 6338-6343.
8. Rook, G. A., K. Dheda, and A. Zumla. 2005. Immune responses to tuberculosis in developing countries: implications for new vaccines. Nat. Rev. Immunol. 5: 661-667.
9. D'Andrea, A., M. Aste-Amezaga, N. M. Valiante, X. Ma, M. Kubin, and G. Trinchieri. 1993. Interleukin 10 (IL-10) inhibits human lymphocyte interferon γ-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J. Exp. Med. 178: 1041-1048.
10. Redpath, S., P. Ghazal, and N. R. Gascoigne. 2001. Hijacking and exploitation of IL-10 by intracellular pathogens. Trends Microbiol. 9: 86-92. (Pubitemid 32155327)
11. Feng, C. G., M. C. Kullberg, D. Jankovic, A. W. Cheever, P. Caspar, R. L. Coffman, and A. Sher. 2002. Transgenic mice expressing human interleukin-10 in the antigen-presenting cell compartment show increased susceptibility to infection with Mycobacterium avium associated with decreased macrophage effector function and apoptosis. Infect. Immun. 70: 6672-6679.
12. Shaw, T. C., L. H. Thomas, and J. S. Friedland. 2000. Regulation of IL-10 secretion after phagocytosis of Mycobacterium tuberculosis by human monocytic cells. Cytokine 12: 483-486.
13. Balikó, Z., L. Szereday, and J. Szekeres-Bartho. 1998. Th2 biased immune response in cases with active Mycobacterium tuberculosis infection and tuberculin anergy. FEMS Immunol. Med. Microbiol. 22: 199-204.
14. Murray, P. J., and R. A. Young. 1999. Increased antimycobacterial immunity in interleukin-10-deficient mice. Infect. Immun. 67: 3087-3095.
15. Dillon, D. C., M. R. Alderson, C. H. Day, D. M. Lewinsohn, R. Coler, T. Bement, A. Campos-Neto, Y. A. Skeiky, I. M. Orme, A. Roberts, et al. 1999. Molecular characterization and human T-cell responses to a member of a novel Mycobacterium tuberculosis mtb39 gene family. Infect. Immun. 67: 2941-2950.
16. Rehren, G., S. Walters, P. Fontan, I. Smith, and A. M. Zarraga. 2007. Differential gene expression between Mycobacterium bovis and Mycobacterium tuberculosis. Tuberculosis 87: 347-359.
17. Zheng, H., L. Lu, B. Wang, S. Pu, X. Zhang, G. Zhu, W. Shi, L. Zhang, H. Wang, S. Wang, et al. 2008. Genetic basis of virulence attenuation revealed by comparative genomic analysis of Mycobacterium tuberculosis strain H37Ra versus H37Rv. PLoS One 3: e2375.
18. Sampson, S. L., P. Lukey, R. M. Warren, P. D. van Helden, M. Richardson, and M. J. Everett. 2001. Expression, characterization and subcellular localization of the Mycobacterium tuberculosis PPE gene Rv1917c. Tuberculosis 81: 305-317.
19. Pym, A. S., P. Brodin, R. Brosch, M. Huerre, and S. T. Cole. 2008. Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol. Microbiol. 46: 709-717.
20. Khan, N., S. Ghousunnissa, S. M. Jegadeeswaran, D. Thiagarajan, S. E. Hasnain, and S. Mukhopadhyay. 2007. Anti-B7-1/B7-2 antibody elicits innate-effector responses in macrophages through NF-κB-dependent pathway. Int. Immunol. 19: 477-486.
21. Post, F. A., C. Manca, O. Neyrolles, B. Ryffel, D. B. Young, and G. Kaplan. 2001. Mycobacterium tuberculosis 19-kilodalton lipoprotein inhibits Mycobacterium smegmatis-induced cytokine production by human macrophages in vitro. Infect. Immun. 69: 1433-1439.
22. Raiter, A., G. Rodionov, A. Novogrodsky, and B. Hardy. 2000. CD4 T lymphocytes as a primary cellular target for BAT mAb stimulation. Int. Immunol. 12: 1623-1628.
23. Khan, N., S. S. Rahim, C. S. Boddupalli, S. Ghousunnissa, S. Padma, N. Pathak, D. Thiagarajan, S. E. Hasnain, and S. Mukhopadhyay. 2006. Hydrogen peroxide inhibits IL-12 p40 induction in macrophages by inhibiting c-rel translocation to the nucleus through activation of calmodulin protein. Blood 107: 1513-1520.
24. Ma, W., K. Gee, W. Lim, K. Chambers, J. B. Angel, M. Kozlowski, and A. Kumar. 2004. Dexamethasone inhibits IL-12p40 production in lipopolysaccharide- stimulated human monocytic cells by down-regulating the activity of c-Jun N-terminal kinase, the activation protein-1, and NF-κB transcription factors. J. Immunol. 172: 318-330.
25. Eswar, N., M. A. Marti-Renom, B. Webb, M. S. Madhusudhan, D. Eramian, M. Shen, U. Pieper, and A. Sali. 2000. Comparative protein structure modeling with MODELLER. Protocols in Bioinformatics, John Wiley & Sons 15, 5.6.:1-5.6.30.
26. Marti-Renom, M. A., A. C. Stuart, A. Fiser, R. Sanchez, F. Melo, and A. Sali. 2000. Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 29: 291-325.
27. Laskowski, R. A., M. W. MacArthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26: 283-291.
28. Morris, A. L., M. W. MacArthur, E. G. Hutchinson, and J. M. Thornton. 1992. Stereochemical quality of protein structure coordinates. Proteins 12: 345-364.
29. Sorgen, P. L., Y. Hu, L. Guan, H. R. Kaback, and M. E. Girvin. 2002. An approach to membrane protein structure without crystals. Proc. Natl. Acad. Sci. USA 99: 14037-14040.
30. Jin, M. S., S. E. Kim, J. Y. Heo, M. E. Lee, H. M. Kim, S. G. Paik, H. Lee, and J. O. Lee. 2007. Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130: 1071-1082.
31. Gabb, H. A., R. M. Jackson, and M. J. Sternberg. 1997. Modelling protein docking using shape complementarity, electrostatics and biochemical information. J. Mol. Biol. 272: 106-120.
32. Krutzik, P. O., and G. P. Nolan. 2003. Intracellular phospho-protein staining techniques for flow cytometry: monitoring single cell signaling events. Cytometry A 55: 61-70.
33. Boddupalli, C. S., S. Ghosh, S. S. Rahim, S. Nair, N. Z. Ehtesham, S. E. Hasnain, and S. Mukhopadhyay. 2007. Nitric oxide inhibits interleukin-12 p40 through p38 MAPK-mediated regulation of calmodulin and c-rel. Free Radical Biol. Med. 42: 686-697.
34. Stover, C. K., V. F. de la Cruz, T. R. Fuerst, J. E. Burlein, L. A. Benson, L. T. Bennett, G. P. Bansal, J. F. Young, M. H. Lee, G. F. Hatfull, et al. 1991. New use of BCG for recombinant vaccines. Nature 351: 456-460.
35. Bardarov, S., J. Kriakov, C. Carriere, S. Yu, C. Vaamonde, R. A. McAdam, B. R. Bloom, G. F. Hatfull, and W. R. Jacobs, Jr. 1997. Conditionally replicating mycobacteriophages: a system for transposon delivery to Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 94: 10961-10966.
36. Parker, L. C., M. K. Whyte, S. N. Vogel, S. K. Dower, and I. Sabroe. 2004. Toll-like receptor (TLR)2 and TLR4 agonists regulate CCR expression in human monocytic cells. J. Immunol. 172: 4977-4986.
37. Bas, S., L. Neff, M. Vuillet, U. Spenato, T. Seya, M. Matsumoto, and C. Gabay. 2008. The proinflammatory cytokine response to Chlamydia trachomatis elementary bodies in human macrophages is partly mediated by a lipoprotein, the macrophage infectivity potentiator, through TLR2/TLR1/TLR6 and CD14. J. Immunol. 180: 1158-1168.
38. Grabiec, A., G. Meng, S. Fichte, W. Bessler, H. Wagner, and C. J. Kirschning. 2004. Human but not murine toll-like receptor 2 discriminates between tri-palmitoylated and tri-lauroylated peptides. J. Biol. Chem. 279: 48004-48012.
39. Meng, G., A. Grabiec, M. Vallon, B. Ebe, S. Hampel, W. Bessler, H. Wagner, and C. J. Kirschning. 2003. Cellular recognition of tri-/di- palmitoylated peptides is independent from a domain encompassing the N-terminal seven leucine-rich repeat (LRR)/LRR-like motifs of TLR2. J. Biol. Chem. 278: 39822-39829.
40. Pathak, S. K., A. Bhattacharyya, S. Pathak, C. Basak, D. Mandal, M. Kundu, and J. Basu. 2004. 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. 279: 55127-55136.
41. Reiling, N., A. Blumenthal, H. D. Flad, M. Ernst, and S. Ehlers. 2001. Mycobacteria-induced TNF-α and IL-10 formation by human macrophages is differentially regulated at the level of mitogen-activated protein kinase activity. J. Immunol. 167: 3339-3345. (Pubitemid 32852576)
42. Song, C. H., J. S. Lee, S. H. Lee, K. Lim, H. J. Kim, J. K. Park, T. H. Paik, and E. K. Jo. 2003. Role of mitogen-activated protein kinase pathways in the production of tumor necrosis factor-α, interleukin-10, and monocyte chemotactic protein-1 by Mycobacterium tuberculosis H37Rv-infected human monocytes. J. Clin. Immunol. 23: 194-201.
43. Yadav, M., S. K. Roach, and J. S. Schorey. 2004. Increased mitogen-activated protein kinase activity and TNF-α production associated with Mycobacterium smegmatis, but not Mycobacterium avium-infected macrophages, requires prolonged stimulation of the calmodulin/calmodulin kinase and cyclic AMP/protein kinase A pathways. J. Immunol. 172: 5588-5597. (Pubitemid 38542061)
44. Jo, E. K., C. S. Yang, C. H. Choi, and C. V. Harding. 2007. Intracellular signalling cascades regulating innate immune responses to Mycobacteria: branching out from Toll-like receptors. Cell Microbiol. 9: 1087-1098.
45. Souza, C. D., O. A. Evanson, and D. J. Weiss. 2006. Mitogen activated protein kinase p38 pathway is an important component of the anti-inflammatory response in Mycobacterium avium subsp. paratuberculosis-infected bovine monocytes. Microb. Pathog. 41: 59-66.
46. Chanteux, H., A. C. Guisset, C. Pilette, and Y. Sibille. 2007. LPS induces IL-10 production by human alveolar macrophages via MAP kinases- and Sp1-dependent mechanisms. Respir. Res. 8: 71.
47. de Waal Malefyt, R., J. Abrams, B. Bennett, C. G. Figdor, and J. E. de Vries. 1991. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174: 1209-1220.
48. Barr, R. K., T. S. Kendrick, and M. A. Bogoyevitch. 2002. Identification of the critical features of a small peptide inhibitor of JNK activity. J. Biol. Chem. 277: 10987-10997.
49. Huang, Y., T. Li, D. C. Sane, and L. Li. 2004. IRAK1 serves as a novel regulator essential for lipopolysaccharide-induced interleukin-10 gene expression. J. Biol. Chem. 279: 51697-51703.
50. Rahim, S. S., N. Khan, C. S. Boddupalli, S. E. Hasnain, and S. Mukhopadhyay. 2005. Interleukin-10 (IL-10) mediated suppression of IL-12 production in RAW 264.7 cells also involves c-rel transcription factor. Immunology 114: 313-321.
51. Khan, N., K. Alam, S. C. Mande, V. L. Valluri, S. E. Hasnain, and S. Mukhopadhyay. 2008. Mycobacterium tuberculosis heat shock protein 60 modulates immune response to PPD by manipulating the surface expression of TLR2 on macrophages. Cell Microbiol. 10: 1711-1722.
52. Delogu, G., C. Pusceddu, A. Bua, G. Fadda, M. J. Brennan, and S. Zanetti. 2004. Rv1818c-encoded PE-PGRS protein of Mycobacterium tuberculosis is surface exposed and influences bacterial cell structure. Mol. Microbiol. 52: 725-733.
53. Underhill, D. M., A. Ozinsky, K. D. Smith, and A. Aderem. 1999. Toll-like receptor-2 mediates mycobacteria-induced proinflammatory signaling in macrophages. Proc. Natl. Acad. Sci. USA 96: 14459-14463.
54. Basu, S., S. K. Pathak, A. Banerjee, S. Pathak, A. Bhattacharyya, Z. Yang, S. Talarico, M. Kundu, and J. Basu. 2007. Execution of macrophage apoptosis by PE-PGRS33 of Mycobacterium tuberculosis is mediated by Toll-like receptor 2-dependent release of tumor necrosis factor-α. J. Biol. Chem. 282: 1039-1050.
55. Kim, H. M., B. S. Park, J. I. Kim, S. E. Kim, J. Lee, S. C. Oh, P. Enkhbayar, N. Matsushima, H. Lee, O. J. Yoo, and J. O. Lee. 2007. Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran. Cell 130: 906-917.
56. Brodsky, I., and Medzhitov, R. 2007. Two modes of ligand recognition by TLRs. Cell 130: 979-981.
57. Müller, M. R., S. D. Pfannes, M. Ayoub, P. Hoffmann, W. G. Bessler, and K. Mittenbühler. 2001. Immunostimulation by the synthetic lipopeptide P3CSK4: TLR4-independent activation of the ERK1/2 signal transduction pathway in macrophages. Immunology 103: 49-60.
58. Strong, M., M. R. Sawaya, S. Wang, M. Phillips, D. Cascio, and D. Eisenberg. 2006. Toward the structural genomics of complexes: crystal structure of a PE/ PPE protein complex from Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 103: 8060-8065.
59. Riley, R., M. Pellegrini, and D. Eisenberg. 2008. Identifying cognate binding pairs among a large set of paralogs: the case of PE/PPE proteins of Mycobacterium tuberculosis. PLoS Comput. Biol. 4: e1000174.
60. Dheenadhayalan, V., G. Delogu, and M. J. Brennan. 2006. Expression of the PE-PGRS 33 protein in Mycobacterium smegmatis triggers necrosis in macrophages and enhanced mycobacterial survival. Microbes Infect. 8: 262-272.
61. Mukhopadhyay, S., S. Nair, and S. E. Hasnain. 2007. Nitric oxide: friendly rivalry in tuberculosis. Curr. Signal Transduct. Ther. 2: 121-128.
62. Mogensen, T. H. 2009. Pathogen recognition and inflammatory signaling in innate immune defenses. Clin. Microbiol. Rev. 22: 240-273.
63. Pathak, S. K., S. Basu, K. K. Basu, A. Banerjee, S. Pathak, A. Bhattacharyya, T. Kaisho, M. Kundu, and J. Basu. 2007. Direct extracellular interaction between the early secreted antigen ESAT-6 of Mycobacterium tuberculosis and TLR2 inhibits TLR signaling in macrophages. Nat. Immunol. 8: 610-618.
64. Fiorentino, D. F., A. Zlotnik, P. Vieira, T. R. Mosmann, M. Howard, K. W. Moore, and A. O'Garra. 1991. IL-10 acts on the antigen presenting cell to inhibit cytokine production by Th1 cells. J. Immunol. 146: 3444-3452.
65. Netea, M. G., J. W. Van der Meer, R. P. Sutmuller, G. J. Adema, and B. J. Kullberg. 2005. From the Th1/Th2 paradigm towards a Toll-like receptor/ T-helper bias. Antimicrob. Agents Chemother. 49: 3991-3996.