Type i IFNs downregulate myeloid cell IFN-γ receptor by inducing recruitment of an early growth response 3/NGFI-A binding protein 1 complex that silences ifngr1 transcription

Journal of Immunology

Volumn 191, Issue 6, 2013, Pages 3384-3392

  Kearney, Staci J ^a,b   Delgado, Christine ^b   Eshleman, Emily M ^b   Hill, Krista K ^a   O'Connor, Brian P ^a,b   Lenz, Laurel L ^a,b  

^a DEPARTMENT OF MEDICINE   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; DACTINOMYCIN; EARLY GROWTH RESPONSE FACTOR 1; EARLY GROWTH RESPONSE FACTOR 3; GAMMA INTERFERON RECEPTOR; GAMMA INTERFERON RECEPTOR 1; HISTONE H3; HISTONE H4; INTERFERON; RNA POLYMERASE II;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BINDING SITE; BONE MARROW CELL; CELL DENSITY; CELL SURFACE; CONTROLLED STUDY; CYTOKINE RESPONSE; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; IFNGR1 GENE; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; TRANSCRIPTION REGULATION;

ANIMALS; BLOTTING, WESTERN; CHROMATIN IMMUNOPRECIPITATION; DOWN-REGULATION; EARLY GROWTH RESPONSE PROTEIN 3; FLOW CYTOMETRY; GENE SILENCING; HUMANS; INTERFERON TYPE I; MACROPHAGES; MICE; MICE, INBRED C57BL; MYELOID CELLS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, INTERFERON; REPRESSOR PROTEINS; TRANSCRIPTION, GENETIC;

EID: 84884227097     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203510     Document Type: Article

References (70)

1. Borden, E. C., G. C. Sen, G. Uze, R. H. Silverman, R. M. Ransohoff, G. R. Foster, and G. R. Stark. 2007. Interferons at age 50: past, current and future impact on biomedicine. Nat. Rev. Drug Discov. 6: 975-990.
2. Stark, G. R., I. M. Kerr, B. R. Williams, R. H. Silverman, and R. D. Schreiber. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67: 227-264.
3. Hwang, S. Y., P. J. Hertzog, K. A. Holland, S. H. Sumarsono, M. J. Tymms, J. A. Hamilton, G. Whitty, I. Bertoncello, and I. Kola. 1995. A null mutation in the gene encoding a type I interferon receptor component eliminates antiproliferative and antiviral responses to interferons a and b and alters macrophage responses. Proc. Natl. Acad. Sci. USA 92: 11284-11288.
4. Müller, U., U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264: 1918-1921.
5. Decker, T., M. Mü ller, and S. Stockinger. 2005. The yin and yang of type I interferon activity in bacterial infection. Nat. Rev. Immunol. 5: 675-687.
6. Kearney, S., C. Delgado, and L. L. Lenz. 2012. Differential effects of type I and II interferons on myeloid cells and resistance to intracellular bacterial infections. Immunol. Res. 55: 187-200.
7. Rayamajhi, M., J. Humann, S. Kearney, K. K. Hill, and L. L. Lenz. 2010. Antagonistic crosstalk between type I and II interferons and increased host susceptibility to bacterial infections. Virulence 1: 418-422.
8. Decker, T., S. Stockinger, M. Karaghiosoff, M. Müller, and P. Kovarik. 2002. IFNs and STATs in innate immunity to microorganisms. J. Clin. Invest. 109: 1271-1277.
9. Liu, S. Y., D. J. Sanchez, R. Aliyari, S. Lu, and G. Cheng. 2012. Systematic identification of type I and type II interferon-induced antiviral factors. Proc. Natl. Acad. Sci. USA 109: 4239-4244.
10. Ea, C. K., S. Hao, K. S. Yeo, and D. Baltimore. 2012. EHMT1 protein binds to nuclear factor-kB p50 and represses gene expression. J. Biol. Chem. 287: 31207-31217.
11. Icardi, L., S. Lievens, R. Mori, J. Piessevaux, L. De Cauwer, K. De Bosscher, and J. Tavernier 2012. Opposed regulation of type I IFN-induced STAT3 and ISGF3 transcriptional activities by histone deacetylases (HDACS) 1 and 2. FASEB J. 26: 240-249.
12. Mittelstadt, M. L., and R. C. Patel. 2012. AP-1 mediated transcriptional repression of matrix metalloproteinase-9 by recruitment of histone deacetylase 1 in response to interferon b. PLoS One 7: e42152.
13. Antonelli, L. R., A. Gigliotti Rothfuchs, R. Gonçalves, E. Roffê, A. W. Cheever, A. Bafica, A. M. Salazar, C. G. Feng, and A. Sher. 2010. Intranasal poly-IC treatment exacerbates tuberculosis in mice through the pulmonary recruitment of a pathogen-permissive monocyte/macrophage population. J. Clin. Invest. 120: 1674-1682.
14. Rayamajhi, M., J. Humann, K. Penheiter, K. Andreasen, and L. L. Lenz. 2010. Induction of IFN-ab enables Listeria monocytogenes to suppress macrophage activation by IFN-g. J. Exp. Med. 207: 327-337.
15. Cooper, A. M., D. K. Dalton, T. A. Stewart, J. P. Griffin, D. G. Russell, and I. M. Orme. 1993. Disseminated tuberculosis in interferon g gene-disrupted mice. J. Exp. Med. 178: 2243-2247.
16. Dighe, A. S., D. Campbell, C. S. Hsieh, S. Clarke, D. R. Greaves, S. Gordon, K. M. Murphy, and R. D. Schreiber. 1995. Tissue-specific targeting of cytokine unresponsiveness in transgenic mice. Immunity 3: 657-666.
17. Flynn, J. L., J. Chan, K. J. Triebold, D. K. Dalton, T. A. Stewart, and B. R. Bloom. 1993. An essential role for interferon g in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178: 2249-2254.
18. Swirnoff, A. H., and J. Milbrandt. 1995. DNA-binding specificity of NGFI-A and related zinc finger transcription factors. Mol. Cell. Biol. 15: 2275-2287.
19. O'Donovan, K. J., W. G. Tourtellotte, J. Millbrandt, and J. M. Baraban. 1999. The EGR family of transcription-regulatory factors: progress at the interface of molecular and systems neuroscience. Trends Neurosci. 22: 167-173.
20. Abdel-Latif, M. M., H. J. Windle, K. A. Fitzgerald, Y. S. Ang, D. N. Eidhin, M. Li-Weber, K. Sabra, and D. Kelleher. 2004. Helicobacter pylori activates the early growth response 1 protein in gastric epithelial cells. Infect. Immun. 72: 3549-3560.
21. Cullen, E. M., J. C. Brazil, and C. M. O'Connor. 2010. Mature human neutrophils constitutively express the transcription factor EGR-1. Mol. Immunol. 47: 1701-1709.
22. Droin, N. M., M. J. Pinkoski, E. Dejardin, and D. R. Green. 2003. Egr family members regulate nonlymphoid expression of Fas ligand, TRAIL, and tumor necrosis factor during immune responses. Mol. Cell. Biol. 23: 7638-7647.
23. Li, S., T. Miao, M. Sebastian, P. Bhullar, E. Ghaffari, M. Liu, A. L. Symonds, and P. Wang. 2012. The transcription factors Egr2 and Egr3 are essential for the control of inflammation and antigen-induced proliferation of B and T cells. Immunity 37: 685-696.
24. Shi, L., R. Kishore, M. R. McMullen, and L. E. Nagy. 2002. Lipopolysaccharide stimulation of ERK1/2 increases TNF-a production via Egr-1. Am. J. Physiol. Cell Physiol. 282: C1205-C1211.
25. Nebbaki, S. S., F. E. El Mansouri, H. Afif, M. Kapoor, M. Benderdour, N. Duval, J. P. Pelletier, J. Martel-Pelletier, and H. Fahmi. 2012. Egr-1 contributes to IL-1-mediated down-regulation of peroxisome proliferator- activated receptor g expression in human osteoarthritic chondrocytes. Arthritis Res. Ther. 14: R69.
26. Tan, L., H. Peng, M. Osaki, B. K. Choy, P. E. Auron, L. J. Sandell, and M. B. Goldring. 2003. Egr-1 mediates transcriptional repression of COL2A1 promoter activity by interleukin-1b. J. Biol. Chem. 278: 17688-17700.
27. Bahouth, S. W., M. J. Beauchamp, and K. N. Vu. 2002. Reciprocal regulation of b1-adrenergic receptor gene transcription by Sp1 and early growth response gene 1: induction of EGR-1 inhibits the expression of the b1-adrenergic receptor gene. Mol. Pharmacol. 61: 379-390.
28. Huang, R. P., Y. Fan, Z. Ni, D. Mercola, and E. D. Adamson. 1997. Reciprocal modulation between Sp1 and Egr-1. J. Cell. Biochem. 66: 489-499.
29. Khachigian, L. M., A. J. Williams, and T. Collins. 1995. Interplay of Sp1 and Egr-1 in the proximal platelet-derived growth factor A-chain promoter in cultured vascular endothelial cells. J. Biol. Chem. 270: 27679-27686.
30. Chiang, S. Y., J. J. Welch, F. J. Rauscher, III, and T. A. Beerman. 1996. Effect of DNA-binding drugs on early growth response factor-1 and TATA box-binding protein complex formation with the herpes simplex virus latency promoter. J. Biol. Chem. 271: 23999-24004.
31. Tatarowicz, W. A., C. E. Martin, A. S. Pekosz, S. L. Madden, F. J. Rauscher, III, S. Y. Chiang, T. A. Beerman, and N. W. Fraser. 1997. Repression of the HSV-1 latency-associated transcript (LAT) promoter by the early growth response (EGR) proteins: involvement of a binding site immediately downstream of the TATA box. J. Neurovirol. 3: 212-224.
32. Wang, C., S. Dostanic, N. Servant, and L. E. Chalifour. 2005. Egr-1 negatively regulates expression of the sodium-calcium exchanger-1 in cardiomyocytes in vitro and in vivo. Cardiovasc. Res. 65: 187-194.
33. Mager, G. M., R. M. Ward, R. Srinivasan, S. W. Jang, L. Wrabetz, and J. Svaren. 2008. Active gene repression by the Egr2.NAB complex during peripheral nerve myelination. J. Biol. Chem. 283: 18187-18197.
34. Gashler, A. L., S. Swaminathan, and V. P. Sukhatme. 1993. A novel repression module, an extensive activation domain, and a bipartite nuclear localization signal defined in the immediate-early transcription factor Egr-1. Mol. Cell. Biol. 13: 4556-4571.
35. Russo, M. W., C. Matheny, and J. Milbrandt. 1993. Transcriptional activity of the zinc finger protein NGFI-A is influenced by its interaction with a cellular factor. Mol. Cell. Biol. 13: 6858-6865.
36. Svaren, J., B. R. Sevetson, E. D. Apel, D. B. Zimonjic, N. C. Popescu, and J. Milbrandt. 1996. NAB2, a corepressor of NGFI-A (Egr-1) and Krox20, is induced by proliferative and differentiative stimuli. Mol. Cell. Biol. 16: 3545-3553.
37. Russo, M. W., B. R. Sevetson, and J. Milbrandt. 1995. Identification of NAB1, a repressor of NGFI-A- and Krox20-mediated transcription. Proc. Natl. Acad. Sci. USA 92: 6873-6877.
38. Swirnoff, A. H., E. D. Apel, J. Svaren, B. R. Sevetson, D. B. Zimonjic, N. C. Popescu, and J. Milbrandt. 1998. Nab1, a corepressor of NGFI-A (Egr-1), contains an active transcriptional repression domain. Mol. Cell. Biol. 18: 512-524.
39. Srinivasan, R., G. M. Mager, R. M. Ward, J. Mayer, and J. Svaren. 2006. NAB2 represses transcription by interacting with the CHD4 subunit of the nucleosome remodeling and deacetylase (NuRD) complex. J. Biol. Chem. 281: 15129-15137.
40. Heinemeyer, T., E. Wingender, I. Reuter, H. Hermjakob, A. E. Kel, O. V. Kel, E. V. Ignatieva, E. A. Ananko, O. A. Podkolodnaya, F. A. Kolpakov, et al. 1998. Databases on transcriptional regulation: TRANSFAC, TRRD and COMPEL. Nucleic Acids Res. 26: 362-367.
41. Schug, J. 2003. Using TESS to predict transcription factor binding sites in DNA sequences. Curr. Protoc. Bioinformatics Chapter 2, Unit 2.6.
42. Kent, W. J., C. W. Sugnet, T. S. Furey, K. M. Roskin, T. H. Pringle, A. M. Zahler, and D. Haussler. 2002. The human genome browser at UCSC. Genome Res. 12: 996-1006.
43. Ling, P. D., M. K. Warren, and S. N. Vogel. 1985. Antagonistic effect of interferon-b on the interferon-g-induced expression of Ia antigen in murine macrophages. J. Immunol. 135: 1857-1863.
44. Yoshida, R., H. W. Murray, and C. F. Nathan. 1988. Agonist and antagonist effects of interferon a and b on activation of human macrophages: two classes of interferon g receptors and blockade of the high-affinity sites by interferon a or b. J. Exp. Med. 167: 1171-1185.
45. Prinz, M., H. Schmidt, A. Mildner, K. P. Knobeloch, U. K. Hanisch, J. Raasch, D. Merkler, C. Detje, I. Gutcher, J. Mages, et al. 2008. Distinct and nonredun-dant in vivo functions of IFNAR on myeloid cells limit autoimmunity in the central nervous system. Immunity 28: 675-686.
46. Phatnani, H. P., and A. L. Greenleaf. 2006. Phosphorylation and functions of the RNA polymerase II CTD. Genes Dev. 20: 2922-2936.
47. Jenuwein, T., and C. D. Allis. 2001. Translating the histone code. Science 293: 1074-1080.
48. Strahl, B. D., and C. D. Allis. 2000. The language of covalent histone modifications. Nature 403: 41-45.
49. Sakamoto, S., and T. Taniguchi. 2001. Identification of a phorbol ester-responsive element in the interferon-g receptor 1 chain gene. J. Biol. Chem. 276: 37237-37241.
50. Halvorson, L. M., M. Ito, J. L. Jameson, and W. W. Chin. 1998. Steroidogenic factor-1 and early growth response protein 1 act through two composite DNA binding sites to regulate luteinizing hormone b-subunit gene expression. J. Biol. Chem. 273: 14712-14720.
51. Carter, J. H., and W. G. Tourtellotte. 2007. Early growth response transcriptional regulators are dispensable for macrophage differentiation. J. Immunol. 178: 3038-3047.
52. Bach, E. A., M. Aguet, and R. D. Schreiber. 1997. The IFN g receptor: a paradigm for cytokine receptor signaling. Annu. Rev. Immunol. 15: 563-591.
53. Farrar, M. A., and R. D. Schreiber. 1993. The molecular cell biology of interferon-g and its receptor. Annu. Rev. Immunol. 11: 571-611.
54. Bach, E. A., S. J. Szabo, A. S. Dighe, A. Ashkenazi, M. Aguet, K. M. Murphy, and R. D. Schreiber. 1995. Ligand-induced autoregulation of IFN-g receptor b chain expression in T helper cell subsets. Science 270: 1215-1218.
55. Pernis, A., S. Gupta, K. J. Gollob, E. Garfein, R. L. Coffman, C. Schindler, and P. Rothman. 1995. Lack of interferon g receptor b chain and the prevention of interferon g signaling in TH1 cells. Science 269: 245-247.
56. Shah, K. M., S. E. Stewart, W. Wei, C. B. Woodman, J. D. O'Neil, C. W. Dawson, and L. S. Young. 2009. The EBV-encoded latent membrane proteins, LMP2A and LMP2B, limit the actions of interferon by targeting interferon receptors for degradation. Oncogene 28: 3903-3914.
57. Chen, C., L. Guo, M. Shi, M. Hu, M. Hu, M. Yu, T. Wang, L. Song, B. Shen, L. Qian, and N. Guo. 2012. Modulation of IFN-g receptor 1 expression by AP-2a influences IFN-g sensitivity of cancer cells. Am. J. Pathol. 180: 661-671.
58. Li, L., S. He, J. M. Sun, and J. R. Davie. 2004. Gene regulation by Sp1 and Sp3. Biochem. Cell Biol. 82: 460-471.
59. Singhal, A., A. Jaiswal, V. K. Arora, and H. K. Prasad. 2007. Modulation of g interferon receptor 1 by Mycobacterium tuberculosis: a potential immune response evasive mechanism. Infect. Immun. 75: 2500-2510.
60. Kuo, M. H., and C. D. Allis. 1998. Roles of histone acetyltransferases and deacetylases in gene regulation. Bioessays 20: 615-626.
61. Monsalve, E., M. A. Pérez, A. Rubio, M. J. Ruiz-Hidalgo, V. Baladrón, J. J. García-Ramírez, J. C. Gómez, J. Laborda, and M. J. Díaz-Guerra. 2006. Notch-1 up-regulation and signaling following macrophage activation modulates gene expression patterns known to affect antigen-presenting capacity and cytotoxic activity. J. Immunol. 176: 5362-5373.
62. Heng, T. S., M. W. Painter; Immunological Genome Project Consortium. 2008. The Immunological Genome Project: networks of gene expression in immune cells. Nat. Immunol. 9: 1091-1094.
63. Huang, R. P., Y. Fan, I. deBelle, Z. Ni, W. Matheny, and E. D. Adamson. 1998. Egr-1 inhibits apoptosis during the UV response: correlation of cell survival with Egr-1 phosphorylation. Cell Death Differ. 5: 96-106.
64. Jain, N., R. Mahendran, R. Philp, G. R. Guy, Y. H. Tan, and X. Cao. 1996. Casein kinase II associates with Egr-1 and acts as a negative modulator of its DNA binding and transcription activities in NIH 3T3 cells. J. Biol. Chem. 271: 13530-13536.
65. Yu, J., I. de Belle, H. Liang, and E. D. Adamson. 2004. Coactivating factors p300 and CBP are transcriptionally crossregulated by Egr1 in prostate cells, leading to divergent responses. Mol. Cell 15: 83-94.
66. Yu, J., S. S. Zhang, K. Saito, S. Williams, Y. Arimura, Y. Ma, Y. Ke, V. Baron, D. Mercola, G. S. Feng, et al. 2009. PTEN regulation by Akt-EGR1-ARF-PTEN axis. EMBO J. 28: 21-33.
67. Cooke, G. S., S. J. Campbell, J. Sillah, P. Gustafson, B. Bah, G. Sirugo, S. Bennett, K. P. McAdam, O. Sow, C. Lienhardt, and A. V. Hill. 2006. Polymorphism within the interferon-g/receptor complex is associated with pulmonary tuberculosis. Am. J. Respir. Crit. Care Med. 174: 339-343.
68. Velayati, A. A., P. Farnia, S. Khalizadeh, A. M. Farahbod, M. Hasanzadh, and M. F. Sheikolslam. 2011. Interferon-gamma receptor-1 gene promoter polymorphisms and susceptibility to leprosy in children of a single family. Am. J. Trop. Med. Hyg. 84: 627-629.
69. Zhou, J., D. Q. Chen, V. K. Poon, Y. Zeng, F. Ng, L. Lu, J. D. Huang, K. Y. Yuen, and B. J. Zheng. 2009. A regulatory polymorphism in interferon-gamma receptor 1 promoter is associated with the susceptibility to chronic hepatitis B virus infection. Immunogenetics 61: 423-430.
70. Salih, M. A., M. E. Ibrahim, J. M. Blackwell, E. N. Miller, E. A. Khalil, A. M. ElHassan, A. M. Musa, and H. S. Mohamed. 2007. IFNG and IFNGR1 gene polymorphisms and susceptibility to post-kala-azar dermal leishmaniasis in Sudan. Genes Immun. 8: 75-78.