Polarization of primary human monocytes by IFN-γ induces chromatin changes and recruits RNA pol II to the TNF-α promoter

Journal of Immunology

Volumn 180, Issue 8, 2008, Pages 5257-5266

  Garrett, Stacey ^a   Dietzmann Maurer, Kelly ^a   Song, Li ^a   Sullivan, Kathleen E ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; GAMMA INTERFERON; HISTONE H4; INTERLEUKIN 4; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; RNA POLYMERASE II; TUMOR NECROSIS FACTOR ALPHA; ACTIVATING TRANSCRIPTION FACTOR; FAM48A PROTEIN, HUMAN; HDAC3 PROTEIN, HUMAN; HISTONE; HISTONE DEACETYLASE; LIPOPOLYSACCHARIDE; TRANSCRIPTION FACTOR;

ACETYLATION; ARTICLE; CHROMATIN; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MONOCYTE; POLARIZATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REPOLARIZATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; CELL CULTURE; CELL POLARITY; GENETICS; IMMUNOLOGY; METABOLISM;

ACETYLATION; ACTIVATING TRANSCRIPTION FACTORS; CELL POLARITY; CELLS, CULTURED; CHROMATIN; HISTONE DEACETYLASES; HISTONES; HUMANS; INTERFERON TYPE II; INTERLEUKIN-4; LIPOPOLYSACCHARIDES; MAP KINASE SIGNALING SYSTEM; MONOCYTES; PROMOTER REGIONS (GENETICS); RNA POLYMERASE II; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 45949109295     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.8.5257     Document Type: Article

References (72)

1. Raes, G., R. Van den Bergh, P. De Baetselier, G. H. Ghassabeh, C. Scotton, M. Locati, A. Mantovani, and S. Sozzani. 2005. Arginase-1 and Ym1 are markers for murine, but not human, alternatively activated myeloid cells. J. Immunol. 174: 6561-6562.
2. Martinez, F. O., S. Gordon, M. Locati, and A. Mantovani. 2006. Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 177: 7303-7311.
3. Mantovani, A., A. Sica, S. Sozzani, P. Allavena, A. Vecchi, and M. Locati. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol. 25: 677-686.
4. Mantovani, A., A. Sica, and M. Locati. 2005. Macrophage polarization comes of age. Immunity 23: 344-346.
5. Beutler, B., V. Tkacenko, I. Milsark, N. Krochin, and A. Cerami. 1986. Effect of γ interferon on cachectin expression by mononuclear phagocytes: reversal of the lpsd (endotoxin resistance) phenotype. J. Exp. Med. 164: 1791-1796.
6. Beutler, B., and T. Brown. 1991. A CAT reporter construct allows ultrasensitive estimation of TNF synthesis and suggests that the TNF gene has been silenced in non-macrophage cell lines. J. Clin. Invest. 87: 1336-1344.
7. Nagorsen, D., S. Deola, K. Smith, E. Wang, V. Monsurro, P. Zanovello, F. M. Marincola, and M. C. Panelli. 2005. Polarized monocyte response to cytokine stimulation. Genome Biol. 6: R15.
8. Lee, J. Y., and K. E. Sullivan. 2001. γ Interferon and lipopolysaccharide interact at the level of transcription to induce tumor necrosis factor α expression. Infect. Immun. 69: 2847-2852.
9. Tsai, E. Y., J. Yie, D. Thanos, and A. E. Goldfeld. 1996. Cell-type-specific regulation of the human tumor necrosis factor α gene in B cells and T cells by NFATp and ATF-2/JUN. Mol. Cell. Biol. 16: 5232-5244.
10. Brinkman, B. M., J. B. Telliez, A. R. Schievella, L. L. Lin, and A. E. Goldfeld. 1999. Engagement of tumor necrosis factor (TNF) receptor 1 leads to ATF-2- and p38 mitogen-activated protein kinase-dependent TNF-α gene expression. J. Biol. Chem. 274: 30882-30886.
11. Falvo, J. V., B. M. Brinkman, A. V. Tsytsykova, E. Y. Tsai, T. P. Yao, A. L. Kung, and A. E. Goldfeld. 2000. A stimulus-specific role for CREB-binding protein (CBP) in T cell receptor-activated tumor necrosis factor α gene expression. Proc. Natl. Acad. Sci. USA 97: 3925-3929.
12. Tsai, E. Y., J. V. Falvo, A. V. Tsytsykova, A. K. Barczak, A. M. Reimold, L. H. Glimcher, M. J. Fenton, D. C. Gordon, I. F. Dunn, and A. E. Goldfeld.
13. A lipopolysaccharide-specific enhancer complex involving Ets, Elk-1, Sp1, and CREB binding protein and p300 is recruited to the tumor necrosis factor α promoter in vivo. Mol. Cell. Biol. 20: 6084-6094.
14. Tsytsykova, A. V., and A. E. Goldfeld. 2002. Inducer-specific enhanceosome formation controls tumor necrosis factor α gene expression in T lymphocytes. Mol. Cell. Biol. 22: 2620-2631.
15. Barthel, R., A. V. Tsytsykova, A. K. Barczak, E. Y. Tsai, C. C. Dascher, M. B. Brenner, and A. E. Goldfeld. 2003. Regulation of tumor necrosis factor α gene expression by mycobacteria involves the assembly of a unique enhanceosome dependent on the coactivator proteins CBP/p300. Mol. Cell. Biol. 23: 526-533.
16. Barthel, R., and A. E. Goldfeld. 2003. T cell-specific expression of the human TNF-α gene involves a functional and highly conserved chromatin signature in intron 3. J. Immunol. 171: 3612-3619.
17. Esensten, J. H., A. V. Tsytsykova, C. Lopez-Rodriguez, F. A. Ligeiro, A. Rao, and A. E. Goldfeld. 2005. NFAT5 binds to the TNF promoter distinctly from NFATp, c, 3 and 4, and activates TNF transcription during hypertonic stress alone. Nucleic Acids Res. 33: 3845-3854.
18. Ranjbar, S., R. Rajsbaum, and A. E. Goldfeld. 2006. Transactivator of transcription from HIV type 1 subtype E selectively inhibits TNF gene expression via interference with chromatin remodeling of the TNF locus. J. Immunol. 176: 4182-4190.
19. Yao, J., N. Mackman, T. S. Edgington, and S.-T. Fan. 1997. Lipopolysaccharide induction of the tumor necrosis factor-α promoter in human monocytic cells. J. Biol. Chem. 272: 17795-17801.
20. Sullivan, K. E., A. Suriano, K. Dietzmann, J. Lin, D. Goldman, and M. A. Petri. 2007. The TNFα locus is altered in monocytes from patients with systemic lupus erythematosus. Clin. Immunol. 123: 74-81.
21. Sullivan, K. E., A. B. Reddy, K. Dietzmann, A. R. Suriano, V. P. Kocieda, M. Stewart, and M. Bhatia. 2007. Epigenetic regulation of tumor necrosis factor α. Mol. Cell. Biol. 27: 5147-5160.
22. Lee, J. Y., N. A. Kim, A. Sanford, and K. E. Sullivan. 2003. Histone acetylation and chromatin conformation are regulated separately at the TNF α promoter in monocytes and macrophages. J. Leukocyte Biol. 73: 862-871.
23. Guenther, M. G., S. S. Levine, L. A. Boyer, R. Jaenisch, and R. A. Young. 2007. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130: 77-88.
24. Barski, A., S. Cuddapah, K. Cui, T. Y. Roh, D. E. Schones, Z. Wang, G. Wei, I. Chepelev, and K. Zhao. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
25. Sandelin, A., P. Carninci, B. Lenhard, J. Ponjavic, Y. Hayashizaki, and D. A. Hume. 2007. Mammalian RNA polymerase II core promoters: insights from genome-wide studies. Nat. Rev. Genet. 8: 424-436.
26. Saccani, S., and G. Natoli. 2002. Dynamic changes in histone H3 Lys 9 methylation occurring at tightly regulated inducible inflammatory genes. Genes Dev. 16: 2219-2224.
27. El Gazzar, M., B. K. Yoza, J. Y. Hu, S. L. Cousart, and C. E. McCall. 2007. Epigenetic silencing of tumor necrosis factor α during endotoxin tolerance. J. Biol. Chem. 282: 26857-26864.
28. Foster, S. L., D. C. Hargreaves, and R. Medzhitov. 2007. Gene-specific control of inflammation by TLR-induced chromatin modifications. Nature 447: 972-978.
29. Wahl, S. M., I. M. Katona, B. M. Stadler, R. L. Wilder, W. E. Helsel, and L. M. Wahl. 1984. Isolation of human mononuclear cell subsets by counterflow centrifugal elutriation (CCE). II. Functional properties of B-lymphocyte-, T-lymphocyte-, and monocyte-enriched fractions. Cell. Immunol. 85: 384-395.
30. Suriano, A. R., A. N. Sanford, N. Kim, M. Oh, S. Kennedy, M. J. Henderson, K. Dietzmann, and K. E. Sullivan. 2005. GCF2/LRRFIP1 represses tumor necrosis factor α expression. Mol. Cell. Biol. 25: 9073-9081.
31. Sullivan, K. E. 1997. Four conserved motifs regulate transcription of the gene encoding human complement component C2. J. Immunol. 158: 5868-5873.
32. Patrone, G., F. Puppo, R. Cusano, M. Scaranari, I. Ceccherini, A. Puliti, and R. Ravazzolo. 2000. Nuclear run-on assay using biotin labeling, magnetic bead capture and analysis by fluorescence-based RT-PCR. BioTechniques 29: 1012-1014: 1016-1017.
33. Tsai, E. Y., J. Jain, P. A. Pesavento, A. Rao, and A. E. Goldfield. 1996. Tumor necrosis factor α gene regulation in activated T cells involves ATF-2/Jun. and NFATp. Mol. Cell. Biol. 16: 459-467.
34. Kawasaki, H., L. Schiltz, R. Chiu, K. Itakura, K. Taira, Y. Nakatani, and K. K. Yokoyama. 2000. ATF-2 has intrinsic histone acetyltransferase activity which is modulated by phosphorylation. Nature 405: 195-200.
35. Mahlknecht, U., J. Will, A. Varin, D. Hoelzer, and G. Herbein. 2004. Histone deacetylase 3, a class I histone deacetylase, suppresses MAPK11-mediated activating transcription factor-2 activation and represses TNF gene expression. J. Immunol. 173: 3979-3990.
36. Tang, X., D. Metzger, S. Leeman, and S. Amar. 2006. LPS-induced TNF-α factor (LITAF) -deficient mice express reduced LPS-induced cytokine: evidence for LITAF-dependent LPS signaling pathways. Proc. Natl. Acad. Sci. USA 103: 13777-13782.
37. Olson, C. M., M. N. Hedrick, H. Izadi, T. C. Bates, E. R. Olivera, and J. Anguita. 2007. p38 mitogen-activated protein kinase controls NF-κB transcriptional activation and tumor necrosis factor α production through RelA phosphorylation mediated by mitogen- and stress-activated protein kinase 1 in response to Borrelia burgdorferi antigens. Infect. Immun. 75: 270-277.
38. Schmeck, B., W. Beermann, V. van Laak, J. Zahlten, B. Opitz, M. Witzenrath, A. C. Hocke, T. Chakraborty, M. Kracht, S. Rosseau, et al. 2005. Intracellular bacteria differentially regulated endothelial cytokine release by MAPK-dependent histone modification. J. Immunol. 175: 2843-2850.
39. Thakur, V., M. T. Pritchard, M. R. McMullen, Q. Wang, and L. E. Nagy. 2006. Chronic ethanol feeding increases activation of NADPH oxidase by lipopolysaccharide in rat Kupffer cells: role of increased reactive oxygen in LPS-stimulated ERK1/2 activation and TNF-α production. J. Leukocyte Biol. 79: 1348-1356.
40. Lai, W. C., M. Zhou, U. Shankavaram, G. Peng, and L. M. Wahl. 2003. Differential regulation of lipopolysaccharide-induced monocyte matrix met al.loproteinase (MMP) -1 and MMP-9 by p38 and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinases. J. Immunol. 170: 6244-6249.
41. Hai, T. W., M. Horikoshi, R. G. Roeder, and M. R. Green. 1988. Analysis of the role of the transcription factor ATF in the assembly of a functional preinitiation complex. Cell 54: 1043-1051.
42. Zhu, W., J. S. Downey, J. Gu, F. Di Padova, H. Gram, and J. Han. 2000. Regulation of TNF expression by multiple mitogen-activated protein kinase pathways. J. Immunol. 164: 6349-6358.
43. Soutoglou, E., and I. Talianidis. 2002. Coordination of PIC assembly and chromatin remodeling during differentiation-induced gene activation. Science 295: 1901-1904.
44. Hatzis, P., and I. Talianidis. 2002. Dynamics of enhancer-promoter communication during differentiation-induced gene activation. Mol. Cell 10: 1467-1477.
45. Avni, O., D. Lee, F. Macian, S. J. Szabo, L. H. Glimcher, and A. Rao. 2002. TH cell differentiation is accompanied by dynamic changes in histone acetylation of cytokine genes. Nat. Immunol. 3: 643-651.
46. Fields, P. E., G. R. Lee, S. T. Kim, V. V. Bartsevich, and R. A. Flavell. 2004. Th2-specific chromatin remodeling and enhancer activity in the Th2 cytokine locus control region. Immunity 21: 865-876.
47. Guo, L., J. Hu-Li, J. Zhu, C. J. Watson, M. J. Difilippantonio, C. Pannetier, and W. E. Paul. 2002. In TH2 cells the IL4 gene has a series of accessibility states associated with distinctive probabilities of IL-4 production. Proc. Natl. Acad. Sci. USA 99: 10623-10628.
48. O'Neill, L. P., and B. M. Turner. 1995. Histone H4 acetylation distinguishes coding regions of the human genome from heterochromatin in a differentiationdependent but transcription-independent manner. EMBO J. 14: 3946-3957.
49. Vettese-Dadey, M., P. A. Grant, T. R. Hebbes, C. Crane-Robinson, C. D. Allis, and J. L. Workman. 1996. Acetylation of histone H4 plays a primary role in enhancing transcription factor binding to nucleosomal DNA in vitro. EMBO J. 15: 2508-2518.
50. Kouskouti, A., and I. Talianidis. 2005. Histone modifications defining active genes persist after transcriptional and mitotic inactivation. EMBO J. 24: 347-357.
51. Heintzman, N. D., R. K. Stuart, G. Hon, Y. Fu, C. W. Ching, R. D. Hawkins, L. O. Barrera, S. Van Calcar, C. Qu, K. A. Ching, et al. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39: 311-318.
52. Bernstein, B. E., M. Kamal, K. Lindblad-Toh, S. Bekiranov, D. K. Bailey D. J. Huebert, S. McMahon, E. K. Karlsson, E. J. Kulbokas, III, T. R. Gingeras, et al. 2005. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120: 169-181.
53. Bernstein, B. E., E. L. Humphrey, R. L. Erlich, R. Schneider, P. Bouman, J. S. Liu, T. Kouzarides, and S. L. Schreiber. 2002. Methylation of histone H3 Lys 4 in coding regions of active genes. Proc. Natl. Acad. Sci. USA 99: 8695-8700.
54. Reik, W. 2007. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447: 425-432.
55. Stout, R. D., C. Jiang, B. Matta, I. Tietzel, S. K. Watkins, and J. Suttles. 2005. Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J. Immunol. 175: 342-349.
56. Garn, H., and H. Renz. 2007. Epidemiological and immunological evidence for the hygiene hypothesis. Immunobiology 212: 441-452.
57. Mishra, N., D. R. Brown, I. M. Olorenshaw, and G. M. Kammer. 2001. Trichostatin A reverses skewed expression of CD154, interleukin-10, and interferon-7 gene and protein expression in lupus T cells. Proc. Natl. Acad. Sci. USA 98: 2628-2633.
58. Vashisht Gopal, Y. N., T. S. Arora, and M. W. Van Dyke. 2006. Tumor necrosis factor-α depletes histone deacetylase 1 protein through IKK2. EMBO Rep. 7: 291-296.
59. Nusinzon, I., and C. M. Horvath. 2003. Interferon-stimulated transcription and innate antiviral immunity require deacetylase activity and histone deacetylase 1. Proc. Natl. Acad. Sci. USA 100: 14742-14747.
60. Guenther, M. G., R. G. Jenner, B. Chevalier, T. Nakamura, C. M. Croce, E. Canaani, and R. A. Young. 2005. Global and Hox-specific roles for the MLL1 methyltransferase. Proc. Natl. Acad. Sci. USA 102: 8603-8608.
61. Kotlyarov, A., A. Neininger, C. Schubert, R. Eckert, C. Birchmeier, H. D. Volk, and M. Gaestel. 1999. MAPKAP kinase 2 is essential for LPS-induced TNF-α biosynthesis. Nat. Cell Biol. 1: 94-97.
62. Winzen, R., M. Kracht, B. Ritter, A. Wilhelm, C. Y. Chen, A. B. Shyu, M. Muller, M. Gaestel, K. Resch, and H. Holtmann. 1999. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 18: 4969-4980.
63. Rutault, K., C. A. Hazzalin, and L. C. Mahadevan. 2001. Combinations of ERK and p38 MAPK inhibitors ablate tumor necrosis factor-α (TNF-α) mRNA induction: evidence for selective destabilization of TNF-α transcripts. J. Biol. Chem. 276: 6666-6674.
64. Carter, A. B., M. M. Monick, and G. W. Hunninghake. 1999. Both Erk and p38 kinases are necessary for cytokine gene transcription. Am. J. Respir. Cell Mol. Biol. 20: 751-758.
65. Swantek, J. L., M. H. Cobb, and T. D. Geppert. 1997. Jun. N-terminal kinase /stress-activated protein kinase (JNK/SAPK) is required for lipopolysaccharide stimulation of tumor necrosis factor α (TNF-α) translation: glucocorticoids inhibit TNF-α translation by blocking JNK/SAPK. Mol. Cell. Biol. 17: 6274-6282.
66. Saccani, S., S. Pantano, and G. Natoli. 2002. p38-Dependent marking of inflammatory genes for increased NF-κB recruitment. Nat. Immunol. 3: 69-75.
67. Agalioti, T., G. Chen, and D. Thanos. 2002. Deciphering the transcriptional histone acetylation code for a human gene. Cell 111: 381-392.
68. Vicent, G. P., C. Ballare, A. S. Nacht, J. Clausell, A. Subtil-Rodriguez, I. Quiles, A. Jordan, and M. Beato. 2006. Induction of progesterone target genes requires activation of Erk and Msk kinases and phosphorylation of histone H3. Mol. Cell 24: 367-381.
69. Zhang, X., J. P. Edwards, and D. M. Mosser. 2006. Dynamic and transient remodeling of the macrophage IL-10 promoter during transcription. J. Immunol. 177: 1282-1288.
70. Hogan, L. H., W. Markofski, A. Bock, B. Barger, J. D. Morrissey, andM. Sandor. 2001. Mycobacterium bovis BCG-induced granuloma formation depends on γ interferon and CD40 ligand but does not require CD28. Infect. Immun. 69: 2596-2603.
71. Takimoto, H., H. Maruyama, K. I. Shimada, R. Yakabe, I. Yano, and Y. Kumazawa. 2006. Interferon-γ independent formation of pulmonary granuloma in mice by injections with trehalose dimycolate (cord factor), lipoarabinomannan and phosphatidylinositol mannosides isolated from Mycobacterium tuberculosis. Clin. Exp. Immunol. 144: 134-141.
72. Aly, S., T. Laskay, J. Mages, A. Malzan, R. Lang, and S. Ehlers. 2007. Interferon-γ-dependent mechanisms of mycobacteria-induced pulmonary immunopathology: the role of angiostasis and CXCR3-targeted chemokines for granuloma necrosis. J. Pathol. 212: 295-305.