TLR2-dependent inhibition of macrophage responses to IFN-γ is mediated by distinct, gene-specific mechanisms

PLoS ONE

Volumn 4, Issue 7, 2009, Pages

  Benson, Sarah A ^a   Ernst, Joel D ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLASS II TRANSACTIVATOR; CXCL11 CHEMOKINE; GAMMA INTERFERON; HISTONE H3; HISTONE H4; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; RNA POLYMERASE II; TATA BINDING PROTEIN; TOLL LIKE RECEPTOR 2; TRANSACTIVATOR PROTEIN; UNCLASSIFIED DRUG; CXCL11 PROTEIN, MOUSE; MHC CLASS II TRANSACTIVATOR PROTEIN; NUCLEAR PROTEIN; PRIMER DNA;

ACETYLATION; ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME BINDING; GENE EXPRESSION; GENETIC TRANSCRIPTION; MACROPHAGE; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROMOTER REGION;

MYCOBACTERIUM TUBERCULOSIS;

ANIMALS; BASE SEQUENCE; CHEMOKINE CXCL11; CHROMATIN IMMUNOPRECIPITATION; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; INTERFERON-GAMMA; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NUCLEAR PROTEINS; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; TOLL-LIKE RECEPTOR 2; TRANS-ACTIVATORS;

EID: 67749110403     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006329     Document Type: Article

References (64)

1. Aderem A, Ulevitch RJ (2000) Toll-like receptors in the induction of the innate immune response. Nature 406: 782-787.
2. Dunne A, O'Neill LA (2003) The interleukin-1 receptor/Toll-like receptor superfamily: signal transduction during inflammation and host defense. Sci STKE 2003: re3.
3. Foster SL, Hargreaves DC, Medzhitov R (2007) Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447: 972-978.
4. Lopez M, Sly LM, Luu Y, Young D, Cooper H, et al. (2003) The 19-kDa Mycobacterium tuberculosis protein induces macrophage apoptosis through Toll-like receptor-2. J Immunol 170: 2409-2416.
5. Mosser DM (2003) The many faces of macrophage activation. J Leukoc Biol 73: 209-212.
6. Mogues T, Goodrich ME, Ryan L, LaCourse R, North RJ (2001) The relative importance of T cell subsets in immunity and immunopathology of airborne Mycobacterium tuberculosis infection in mice. J Exp Med 193: 271-280.
7. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, et al. (1993) Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 178: 2243-2247.
8. Flynn JL, Chan J, Triebold KJ, Dalton DK, Stewart TA, et al. (1993) An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J Exp Med 178: 2249-2254.
9. Flynn JL, Chan J (2001) Immunology of tuberculosis. Annu Rev Immunol 19: 93-129.
10. Murray HW, Granger AM, Teitelbaum RF (1991) Gamma interferon-activated human macrophages and Toxoplasma gondii, Chlamydia psittaci, and Leishmania donovani: antimicrobial role of limiting intracellular iron. Infect Immun 59: 4684-4686.
11. Murray HW, Rubin BY, Rothermel CD (1983) Killing of intracellular Leishmania donovani by lymphokine-stimulated human mononuclear phagocytes. Evidence that interferon-gamma is the activating lymphokine. J Clin Invest 72: 1506-1510.
12. Bhardwaj N, Nash TW, Horwitz MA (1986) Interferon-gamma-activated human monocytes inhibit the intracellular multiplication of Legionella pneumophila. J Immunol 137: 2662-2669.
13. Skerrett SJ, Martin TR (1994) Intratracheal interferon-gamma augments pulmonary defenses in experimental legionellosis. Am J Respir Crit Care Med 149: 50-58.
14. Levy DE, Darnell JE Jr (2002) Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol 3: 651-662.
15. Kovarik P, Stoiber D, Novy M, Decker T (1998) Stat1 combines signals derived from IFN-gamma and LPS receptors during macrophage activation. Embo J 17: 3660-3668.
16. Stoiber D, Kovarik P, Cohney S, Johnston JA, Steinlein P, et al. (1999) Lipopolysaccharide induces in macrophages the synthesis of the suppressor of cytokine signaling 3 and suppresses signal transduction in response to the activating factor IFN-gamma. J Immunol 163: 2640-2647.
17. Yao Y, Xu Q, Kwon MJ, Matta R, Liu Y, et al. (2006) ERK and p38 MAPK signaling pathways negatively regulate CIITA gene expression in dendritic cells and macrophages. J Immunol 177: 70-76.
18. Kincaid EZ, Ernst JD (2003) Mycobacterium tuberculosis exerts gene-selective inhibition of transcriptional responses to IFN-gamma without inhibiting STAT1 function. J Immunol 171: 2042-2049.
19. Lafuse WP, Alvarez GR, Curry HM, Zwelling BS (2006) Mycobacterium tuberculosis and Mycobacterium avium inhibit IFN- gamma -induced gene expression by TLR2-dependent and independent pathways. J Interferon Cytokine Res 26: 548-561.
20. Pai RK, Convery M, Hamilton TA, Boom WH, Harding CV (2003) Inhibition of IFN-gamma-induced class II transactivator expression by a 19-kDa lipoprotein from Mycobacterium tuberculosis: a potential mechanism for immune evasion. J Immunol 171: 175-184.
21. Pai RK, Pennini ME, Tobian AA, Canaday DH, Boom WH, et al. (2004) Prolonged toll-like receptor signaling by Mycobacterium tuberculosis and its 19-kilodalton lipoprotein inhibits gamma interferon-induced regulation of selected genes in macrophages. Infect Immun 72: 6603-6614.
22. Ting LM, Kim AC, Cattamanchi A, Ernst JD (1999) Mycobacterium tuberculosis inhibits IFN-gamma transcriptional responses without inhibiting activation of STAT1. J Immunol 163: 3898-3906.
23. Banaiee N, Kincaid EZ, Buchwald U, Jacobs WR Jr, Ernst JD (2006) Potent inhibition of macrophage responses to IFN-gamma by live virulent Mycobacterium tuberculosis is independent of mature mycobacterial lipoproteins but dependent on TLR2. J Immunol 176: 3019-3027.
24. Fortune SM, Solache A, Jaeger A, Hill PJ, Belisle JT, et al. (2004) Mycobacterium tuberculosis inhibits macrophage responses to IFN-gamma through myeloid differentiation factor 88-dependent and -independent mechanisms. J Immunol 172: 6272-6280.
25. Pennini ME, Pai RK, Schultz DC, Boom WH, Harding CV (2006) Mycobacterium tuberculosis 19-kDa lipoprotein inhibits IFN-gamma-induced chromatin remodeling of MHC2TA by TLR2 and MAPK signaling. J Immunol 176: 4323-4330.
26. Barnes PF, Mistry SD, Cooper CL, Pirmez C, Rea TH, et al. (1989) Compartmentalization of a CD4+ T lymphocyte subpopulation in tuberculous pleuritis. J Immunol 142: 1114-1119.
27. Gomez JE, McKinney JD (2004) M. tuberculosis persistence, latency, and drug tolerance. Tuberculosis (Edinb) 84: 29-44.
28. Kincaid EZ, Wolf AJ, Desvignes L, Mahapatra S, Crick DC, et al. (2007) Codominance of TLR2-Dependent and TLR2-Independent Modulation of MHC Class II in Mycobacterium tuberculosis Infection In Vivo. J Immunol 179: 3187-3195.
29. Jin MS, Kim SE, Heo JY, Lee ME, Kim HM, et al. (2007) Crystal Structure of the TLR1-TLR2 Heterodimer Induced by Binding of a Tri-Acylated Lipopeptide. Cell 130: 1071-1082.
30. Steimle V, Siegrist CA, Mottet A, Lisowska-Grospierre B, Mach B (1994) Regulation of MHC class II expression by interferon-gamma mediated by the transactivator gene CIITA. Science 265: 106-109.
31. Pennini ME, Liu Y, Yang J, Croniger CM, Boom WH, et al. (2007) CCAAT/ enhancer-binding protein beta and delta binding to CIITA promoters is associated with the inhibition of CIITA expression in response to Mycobacterium tuberculosis 19-kDa lipoprotein. J Immunol 179: 6910-6918.
32. Loetscher M, Gerber B, Loetscher P, Jones SA, Piali L, et al. (1996) Chemokine receptor specific for IP10 and mig: structure, function, and expression in activated T-lymphocytes. J Exp Med 184: 963-969.
33. Cole KE, Strick CA, Paradis TJ, Ogborne KT, Loetscher M, et al. (1998) Interferon-inducible T cell alpha chemoattractant (I-TAC): a novel non-ELR CXC chemokine with potent activity on activated T cells through selective high affinity binding to CXCR3. J Exp Med 187: 2009-2021.
34. Fuller C, Flynn JL, Reinhart TA (2003) In situ study of abundant expression of proinflammatory chemokines and cytokines in pulmonary granulomas that develop in cynomolgus macaques experimentally infected with Mycobacterium tuberculosis. Infect Immun 71: 7023-7034.
35. Sierro F, Biben C, Martínez-Munñoz L, Mellado M, Ransohoff RM, et al. (2007) Disrupted cardiac development but normal hematopoiesis in mice deficient in the second CXCL12/SDF-1 receptor, CXCR7. Proc Natl Acad Sci U S A 104: 14759-14764.
36. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41-45.
37. Beg AA, Baltimore D (1996) An essential role for NF-kappaB in preventing TNF-alpha-induced cell death. Science 274: 782-784.
38. Doi TS, Marino MW, Takahashi T, Yoshida T, Sakakura T, et al. (1999) Absence of tumor necrosis factor rescues RelA-deficient mice from embryonic lethality. Proc Natl Acad Sci U S A 96: 2994-2999.
39. Douvas GS, Looker DL, Vatter AE, Crowle AJ (1985) Gamma interferon activates human macrophages to become tumoricidal and leishmanicidal but enhances replication of macrophage-associated mycobacteria. Infect Immun 50: 1-8.
40. Rook GA, Steele J, Ainsworth M, Champion BR (1986) Activation of macrophages to inhibit proliferation of Mycobacterium tuberculosis: comparison of the effects of recombinant gamma-interferon on human monocytes and murine peritoneal macrophages. Immunology 59: 333-338.
41. Lee KK, Workman JL (2007) Histone acetyltransferase complexes: one size doesn't fit all. Nat Rev Mol Cell Biol 8: 284-295.
42. Sengupta N, Seto E (2004) Regulation of histone deacetylase activities. J Cell Biochem 93: 57-67.
43. Wang Y, Curry HM, Zwilling BS, Lafuse WP (2005) Mycobacteria inhibition of IFN-gamma induced HLA-DR gene expression by up-regulating histone deacetylation at the promoter region in human THP-1 monocytic cells. J Immunol 174: 5687-5694.
44. Zhu P, Zhou W, Wang J, Puc J, Ohgi KA, et al. (2007) A histone H2A deubiquitinase complex coordinating histone acetylation and H1 dissociation in transcriptional regulation. Mol Cell 27: 609-621.
45. Pluemsampant S, Safronova OS, Nakahama K, Morita I (2008) Protein kinase CK2 is a key activator of histone deacetylase in hypoxia-associated tumors. Int J Cancer 122: 333-341.
46. Yang SR, Chida AS, Bauter MR, Shafiq N, Seweryniak K, et al. (2006) Cigarette smoke induces proinflammatory cytokine release by activation of NF-kappaB and posttranslational modifications of histone deacetylase in macrophages. Am J Physiol Lung Cell Mol Physiol 291: L46-57.
47. Ito K, Ito M, Elliot WM, Cosio B, Caramori G, et al. (2005) Decreased histone deacetylase activity in chronic obstructive pulmonary disease. N Engl J Med 352: 1967-1976.
48. Hu E, Chen Z, Fredrickson T, Zhu Y, Kirkpatrick R, et al. (2000) Cloning and characterization of a novel human class I histone deacetylase that functions as a transcription repressor. J Biol Chem 275: 15254-15264.
49. Lee H, Rezai-Zadeh N, Seto E (2004) Negative regulation of histone deacetylase 8 activity by cyclic AMP-dependent protein kinase A. Mol Cell Biol 24: 765-773.
50. Pflum MK, Tong JK, Lane WS, Schreiber SL (2001) Histone deacetylase 1 phosphorylation promotes enzymatic activity and complex formation. J Biol Chem 276: 47733-47741.
51. Tsai SC, Seto E (2002) Regulation of histone deacetylase 2 by protein kinase CK2. J Biol Chem 277: 31826-31833.
52. Singh NN, Ramji DP (2008) Protein kinase CK2, an important regulator of the inflammatory response? J Mol Med 86: 887-897.
53. Kalkhove E (2004) CBP and p300: HATs for different occasions. Biochem Pharmacol 68: 1145-1155.
54. Zhang JJ, Vinkemeier U, Gu W, Chakravarti D, Horvath CM, et al. (1996) Two contact regions between Stat1 and CBP/p300 in interferon gamma signaling. Proc Natl Acad Sci U S A 93: 15092-15096.
55. Huang WC, Ju TK, Hung MC, Chen CC (2007) Phosphorylation of CBP by IKKalpha promotes cell growth by switching the binding preference of CBP from p53 to NF-kappaB. Mol Cell 26: 75-87.
56. Yuan LW, Soh JW, Weinstein IB (2002) Inhibition of histone acetyltransferase function of p300 by PKCdelta. Biochim Biophys Acta 1592: 205-211.
57. Gaston K, Jayaraman PS (2003) Transcriptional repression in eukaryotes: repressors and repression mechanisms. Cell Mol Life Sci 60: 721-741.
58. Gupta AK, Kone BC (1999) CCAAT/enhancer binding protein-beta transactivates murine nitric oxide synthase 2 gene in an MTAL cell line. Am J Physiol 276: F599-605.
59. Litvak V, Ramsey SA, Rust AG, Zak DE, Kennedy KA, et al. (2009) Function of C/EBPdelta in a regulatory circuit that discriminates between transient and persistent TLR4-induced signals. Nat Immunol 10: 437-443.
60. Hamon MA, Batsche E, Regnault B, Tham TN, Seveau S, et al. (2007) Histone modifications induced by a family of bacterial toxins. Proc Natl Acad Sci U S A 104: 13467-13472.
61. Weidman MK, Sharma R, Raychaudhuri S, Kundu P, Tsai W, et al. (2003) The interaction of cytoplasmic RNA viruses with the nucleus. Virus Res 95: 75-85.
62. Le May N, Dubaele S, Proietti De Santis L, Billecocq A, Bouloy M, et al. (2004) TFIIH transcription factor, a target for the Rift Valley hemorrhagic fever virus. Cell 116: 541-550.
63. Yuan H, Yoza BK, Lyles DS (1998) Inhibition of host RNA polymerase II-dependent transcription by vesicular stomatitis virus results from inactivation of TFIID. Virology 251: 383-392.
64. Popkin DL, Watson MA, Karaskov E, Dunn GP, Bremner R, et al. (2003) Murine cytomegalovirus paralyzes macrophages by blocking IFN gamma-induced promoter assembly. Proc Natl Acad Sci U S A 100: 14309-14314.