ESAT6 differentially inhibits IFN-γ-inducible class II transactivator isoforms in both a TLR2-dependent and -independent manner

Immunology and Cell Biology

Volumn 90, Issue 4, 2012, Pages 411-420

  Kumar, Pavanish ^a   Agarwal, Richa ^a   Siddiqui, Imran ^a   Vora, Hardeep ^a   Das, Gobardhan ^a   Sharma, Pawan ^a  

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

Author keywords

CIITA; ESAT6; M. tuberculosis; MHC II

Indexed keywords

BUTYRIC ACID; CLASS II TRANSACTIVATOR PROTEIN; EARLY SECRETORY ANTIGENIC TARGET 6; GAMMA INTERFERON; HISTONE DEACETYLASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SYNAPTOPHYSIN; TOLL LIKE RECEPTOR 2; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATIN; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; HISTONE ACETYLATION; HISTONE METHYLATION; MACROPHAGE; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CHROMATIN; HISTOCOMPATIBILITY ANTIGENS CLASS II; INTERFERON-GAMMA; MYCOBACTERIUM TUBERCULOSIS; NUCLEAR PROTEINS; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TRANS-ACTIVATORS;

MYCOBACTERIUM TUBERCULOSIS;

EID: 84859974522     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2011.54     Document Type: Article

References (60)

1. World Health Organisation. Estimated TB incidence, prevalence and mortality. (2008) Available at 〈http://www.who.int/mediacentre/factsheets/ fs104/en/index.html〉.
2. Mogues T, Goodrich ME, Ryan L, LaCoarse R, North RJ. The relative importance of T cell subsets in immunity and immunopathology of airborne Mycobacterium tuberculosis infection in mice. J Exp Med 2001; 193: 271-280. (Pubitemid 32524511)
3. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, Bloom BR. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J ExpMed 1993; 178: 2249-2254. (Pubitemid 23344886)
4. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, Orme IM. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 1993; 178: 2243-2247. (Pubitemid 23344885)
5. Fulton SA, Reba SM, Pai RK, Pennini M, Torres M, Harding CV et al. Inhibition of major histocompatibility complex II expression and antigen processing in murine alveolar macrophages by Mycobacterium bovis BCG and the 19-kilodalton mycobacterial lipoprotein. Infect Immun 2004; 72: 2101-2110. (Pubitemid 38419923)
6. Chang ST, Linderman JJ, Kirschner DE. Multiple mechanisms allow Mycobacterium tuberculosis to continuously inhibit MHC class II-mediated antigen presentation by macrophages. Proc Natl Acad Sci USA 2005; 102: 4530-4535. (Pubitemid 40397146)
7. Noss EH, Harding CV, Boom WH. Mycobacterium tuberculosis inhibits MHC class II antigen processing in murine bone marrow macrophages. Cell Immunol 2000; 201: 63-74. (Pubitemid 30337710)
8. Pecora ND, Fulton SA, Reba SM, Drage MG, Simmons DP, Urankar-Nagy NJ et al. Mycobacterium bovis BCG decreases MHC-II expression in vivo on murine lung macrophages and dendritic cells during aerosol infection. Cell Immunol 2009; 254: 94-104.
9. Pennini ME, Pai RK, Schultz DC, Boom WH, Harding CV. Mycobacterium tuberculosis 19-kDa lipoprotein inhibits IFN-gamma-induced chromatin remodeling of MHC2TA by TLR2 and MAPK signaling. J Immunol 2006; 176: 4323-4330. (Pubitemid 44264411)
10. Wojciechowski W, DeSanctis J, Skamene E, RadZioch D. Attenuation of MHC class II expression in macrophages infected with Mycobacterium bovis bacillus Calmette-Guérin involves class II transactivator and depends on the Nramp1 gene. J Immunol 1999; 163: 2688-2696. (Pubitemid 29399194)
11. Noss EH, Pai RK, Sellati TJ, Radolf JD, Belisle J, Golenbock DT et al. Toll-like receptor 2-dependent inhibition of macrophage class II MHC expression and antigen processing by 19-kDa lipoprotein of Mycobacterium tuberculosis. J Immunol 2001; 167: 910-918. (Pubitemid 32660847)
12. Boss JM, Jensen PE. Transcriptional regulation of the MHC class II antigen presentation pathway. Curr Opin Immunol 2003; 15: 105-111. (Pubitemid 35454200)
13. Reith W, Mach B. The bare lymphocyte syndrome and the regulation of MHC expression. Annu Rev Immunol 2001; 19: 331-373. (Pubitemid 32368039)
14. Reith W, LeibundGut-Landmann S, Waldburger J. Regulation of MHC class II gene expression by the class II transactivator. Nat Rev Immunol 2005; 5: 793-806. (Pubitemid 41400853)
15. Ting JP, Trowsdale J. Genetic control of MHC class II expression. Cell 2002; 109(Suppl): S21-S33. (Pubitemid 34457849)
16. Krawczyk M, Seguin-Estevez Q, Leimgruber E, Sperisen P, Schmid C, Bucher P et al. Identification of CIITA regulated genetic module dedicated for antigen presentation. PLoS Genet 2008; 4: e1000058.
17. Muhlethaler-Mottet A, Otten LA, Steimle V, Mach B. Expression of MHC class II molecules in different cellular and functional compartments is controlled by differential usage of multiple promoters of the transactivator CIITA. EMBO J 1997; 16: 2851-2860. (Pubitemid 27226221)
18. Fortune SM, Solache A, Jaeger A, Hill PJ, Belisle J, Bloom BR et al. Mycobacterium tuberculosis inhibits macrophage responses to IFN-gamma through myeloid differentiation factor 88-dependent and -independent mechanisms. J Immunol 2004; 172: 6272-6280. (Pubitemid 38621234)
19. Benson SA, Ernst JD. TLR2-dependent inhibition of macrophage responses to IFN-gamma is mediated by distinct, gene-specific mechanisms. PloS One 2009; 4: e6329.
20. Waldburger JM, Suter T, Fontana A, Acha-Orbea H, Reith W. Selective abrogation of major histocompatibility complex class II expression on extrahematopoietic cells in mice lacking promoter IV of the class II transactivator gene. J Exp Med 2001; 194: 393-406. (Pubitemid 32835036)
21. Pai RK, Askew D, Boom WH, Harding CV. Regulation of class II MHC expression in APCs: roles of types I, III, and IV class II transactivator. J Immunol 2002; 169: 1326-1333. (Pubitemid 34809175)
22. Majlessi L, Brodin P, Brosch R, Rojas MJ, Khun H, Huerre M et al. Influence of ESAT-6 secretion system 1 (RD1) of Mycobacterium tuberculosis on the interaction between mycobacteria and the host immune system. J Immunol 2005; 174: 3570-3579. (Pubitemid 40354066)
23. MacGurn JA, Cox JS. A genetic screen for Mycobacterium tuberculosis mutants defective for phagosome maturation arrest identifies components of the ESX-1 secretion system. Infect Immun 2007; 75: 2668-2678. (Pubitemid 46870147)
24. Lewis KN, Liao R, Guinn KM, Hickey MJ, Smith S, Behr MA et al. Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guérin attenuation. J Infect Dis 2003; 187: 117-123. (Pubitemid 36034479)
25. Carlsson F, Kim J, Dimitru C, Barck KH, Carano RA, Sun M et al. Host-detrimental role of Esx-1-mediated inflammasome activation in mycobacterial infection. PLoS Pathog 2010; 6: e1000895.
26. Pym AS, Brodin P, Brosch R, Huerre M, Cole ST. Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol 2002; 46: 709-717. (Pubitemid 35365606)
27. van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, Pierson J et al. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 2007; 129: 1287-1298.
28. DiGiuseppe Champion PA, Cox JS. Protein secretion systems in Mycobacteria. Cell Microbiol 2007; 9: 1376-1384. (Pubitemid 46774011)
29. Hsu T, Hingley-Wilson SM, Chen B, Dia AZ, Morin PM, Marks CB et al. The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc Natl Acad Sci USA 2003; 100: 12420-12425. (Pubitemid 37271575)
30. Volkman HE, Pozos TC, Zheng J, Davis JM, Rawls JF, Ramakrishnan L. Tuberculous granuloma induction via interaction of a bacterial secreted protein with host epithelium. Science 2010; 327: 466-469.
31. Ganguly N, Giang PH, Gupta C, Basu SK, Siddiqui I, Salunke DM et al. Mycobacterium tuberculosis secretory proteins CFP-10, ESAT-6 and the CFP10: ESAT6 complex inhibit lipopolysaccharide-induced NF-kappaB transactivation by downregulation of reactive oxidative species (ROS) production. Immunol Cell Biol 2008; 86: 98-106.
32. Harboe M, Oettinger T, Wiker HG, Rosenkrands I, Andersen P. Evidence for occurrence of the ESAT-6 protein in Mycobacterium tuberculosis and virulent Mycobacterium bovis and for its absence in Mycobacterium bovis BCG. Infect Immun 1996; 64: 16-22. (Pubitemid 26009335)
33. Kumar K, Tharad M, Ganpathy S, Ram G, Narayan A, Khan JA et al. Phenylalanine-rich peptides potently bind ESAT6, a virulence determinant of Mycobacterium tuberculosis, and concurrently affect the pathogen's growth. PloS One 2009; 4: e7615.
34. Brodin P, Rosenkrands I, Anderson P, Cole ST, Brosch R. ESAT-6 proteins: protective antigens and virulence factors? Trends Microbiol 2004; 12: 500-508. (Pubitemid 39370732)
35. Pathak SK, Basu S, Basu KK, Banerjee A, Pathak S, Bhattacharyya A et al. 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. (Pubitemid 46785125)
36. Candido EPM, Reeves R, Davie JR. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell 1978; 14: 105-113. (Pubitemid 8340438)
37. Sealy L, Chalkley R. The effect of sodium butyrate on histone modification. Cell 1978; 14: 115-121. (Pubitemid 8340439)
38. Boffa LC, Vidali G, Mann RS, Allfrey VG. Suppression of histone deacetylation in vivo and in vitro by sodium butyrate. J Biol Chem 1978; 253: 3364-3366. (Pubitemid 8349780)
39. Vidali G, Boffa LC, Bradbury EM, Allfrey VG. Suppression of histone deacetylation by butyrate leads to accumulation of multiacetylated forms of histones H3 and H4 and increased DNase I-sensitivity of the associated DNA sequences. Proc Natl Acad Sci USA 1978; 75: 2239-2243. (Pubitemid 8350742)
40. Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ et al. Genomicmaps and comparative analysis of histone modifications in human and mouse. Cell 2005; 120: 169-181. (Pubitemid 40174761)
41. Kim TH, Barrera LO, Zheng M, Qu C, Singer MA, Richmond TA et al. A high-resolution map of active promoters in the human genome. Nature 2005; 436: 876-880. (Pubitemid 41160649)
42. Pai RK, Convery M, Hamilton TA, Boom WH, Harding CV. Inhibition of IFN-gammainduced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: a potential mechanism for immune evasion. J Immunol 2003; 171: 175-184. (Pubitemid 36745286)
43. Kincaid EZ, Wolf AJ, Desvignes L, Mahapatra S, Crick DC, Brennan PJ et al. Codominance of TLR2-dependent and TLR2-independent modulation of MHC class II in Mycobacterium tuberculosis infection in vivo. J Immunol 2007; 179: 3187-3195.
44. Yao Y, Xu Q, Kown MJ, Matta R, Liu Y, Hong SC et al. ERK and p38 MAPK signaling pathways negatively regulate CIITA gene expression in dendritic cells and macrophages. J Immunol 2006; 177: 70-76. (Pubitemid 43939117)
45. Kouzarides T. Chromatin modifications and their function. Cell 2007; 128: 693-705. (Pubitemid 46273577)
46. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z et al. High-resolution profiling of histone methylations in the human genome. Cell 2007; 129: 823-837. (Pubitemid 46802390)
47. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006; 441: 349-353. (Pubitemid 44050199)
48. Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell 2007; 128: 707-719. (Pubitemid 46273570)
49. Boeger H, Griesnbeck J, Strattan JS, Kornberg RD. Nucleosomes unfold completely at a transcriptionally active promoter. Mol Cell 2003; 11: 1587-1598. (Pubitemid 36776544)
50. Schones DE, Cui K, Cuddapah S, Roh TY, Barski A, Wang Z, Wei G et al. Dynamic regulation of nucleosome positioning in the human genome. Cell 2008; 132: 887-898. (Pubitemid 351312809)
51. Wang Z, Zang C, Kui K, Schones DE, Barski A, Peng W et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009; 138: 1019-1031.
52. Kadosh D, Struhl K. Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell 1997; 89: 365-371.
53. Rundlett SE, Carmen AA, Suka N, Turner BM, Grunstein M. Transcriptional repression by UME6 involves deacetylation of lysine 5 of histone H4 by RPD3. Nature 1998; 392: 831-835. (Pubitemid 28225326)
54. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007; 447: 407-412. (Pubitemid 46816746)
55. Pray-Grant MG, Daniel JA, Sciltz D, Yates III JR, Grant PA. Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 2005; 433: 434-438. (Pubitemid 40203325)
56. Wysocka J, Swigut T, Xiao H, Milne TA, Kwon SY, Landry J et al. A PHD finger ofNURF couples histone H3 lysine 4 trimethylation with chromatin remodelling. Nature 2006; 442: 86-90. (Pubitemid 44064214)
57. Martin DG, Grimes DE, Baetz K, Howe L. Methylation of histone H3 mediates the association of the NuA3 histone acetyltransferase with chromatin. Mol Cell Biol 2006; 26: 3018-3028.
58. Landmann S, Mühlethaler-Mottet A, Bernasconi L, Suter T, Waldburger JM, Masternak K et al. Maturation of dendritic cells is accompanied by rapid transcriptional silencing of class II transactivator (CIITA) expression. J Exp Med 2001; 194: 379-391. (Pubitemid 32835035)
59. Barbieri G, Deffernnes V, Prod Home T, Vedrenne J, Baton F, Cortes C et al. Isoforms of the class II transactivator protein. Int Immunol 2002; 14: 839-848.
60. Zentilin L, Giacca M. Competitive PCR for precise nucleic acid quantification. Nat Protoc 2007; 2: 2092-2104. (Pubitemid 351565846)