Promoter analysis reveals critical roles for SMAD-3 and ATF-2 in expression of IL-23 p19 in macrophages

Journal of Immunology

Volumn 181, Issue 7, 2008, Pages 4523-4533

  Al Salleeh, Fahd ^a   Petro, Thomas M ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; DNA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 23P19; MITOGEN ACTIVATED PROTEIN KINASE; NEUTRALIZING ANTIBODY; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN P19; SHORT HAIRPIN RNA; SMAD3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TOLL LIKE RECEPTOR AGONIST; TRANSFORMING GROWTH FACTOR BETA1; ATF2 PROTEIN, MOUSE; IRF3 PROTEIN, MOUSE; IRF7 PROTEIN, MOUSE; MEMBRANE PROTEIN; SMAD3 PROTEIN, MOUSE; TLR3 PROTEIN, MOUSE; TLR7 PROTEIN, MOUSE; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL ACTIVATION; CHROMOSOME; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME INHIBITION; EXPRESSION VECTOR; FEMALE; GENE DELETION; GENE MUTATION; IMMUNOPRECIPITATION; MACROPHAGE; MOUSE; MURINE ENCEPHALOMYELITIS VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SPLEEN; VIRUS INFECTION; ANIMAL; BIOSYNTHESIS; CELL LINE; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; VIROLOGY;

ACTIVATING TRANSCRIPTION FACTOR 2; ANIMALS; BASE SEQUENCE; CELL LINE; FEMALE; GENE EXPRESSION REGULATION, VIRAL; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERON REGULATORY FACTOR-7; INTERLEUKIN-23 SUBUNIT P19; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MOLECULAR SEQUENCE DATA; NF-KAPPA B; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; THEILOVIRUS; TOLL-LIKE RECEPTOR 3; TOLL-LIKE RECEPTOR 7;

EID: 58149311502     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.7.4523     Document Type: Article

References (67)

1. Oppmann, B., R. Lesley, B. Blom, J. C. Timans, Y. Xu, B. Hunte, F. Vega, N. Yu, J. Wang, K. Singh, et al. 2000. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13: 715-725.
2. Cua, D. J., J. Sherlock, Y. Chen, C. A. Murphy, B. Joyce, B. Seymour, L. Lucian, W. To, S. Kwan, T. Churakova, et al. 2003. Interleukin-23 rather than interleukin- 12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421: 744-748.
3. Wolf, S. F., P. A. Temple, M. Kobayashi, D. Young, M. Dicig, L. Lowe, R. Dzialo, L. Fitz, C. Ferenz, R. M. Hewick, et al. 1991. Cloning of cDNA for natural killer cell stimulatory factor, a heterodimeric cytokine with multiple biologic effects on T and natural killer cells. J. Immunol. 146: 3074-3081.
4. Lankford, C. S., and D. M. Frucht. 2003. A unique role for IL-23 in promoting cellular immunity. J. Leukocyte Biol. 73: 49-56.
5. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132.
6. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201: 233-240.
7. Belladonna, M. L., J. C. Renauld, R. Bianchi, C. Vacca, F. Fallarino, C. Orabona, M. C. Fioretti, U. Grohmann, and P. Puccetti. 2002. IL-23 and IL-12 have overlapping, but distinct, effects on murine dendritic cells. J. Immunol. 168: 5448-5454. (Pubitemid 34556122)
8. + T cells through IL-12 produced by Listeria-induced macrophages. Science 260: 547-549.
9. Nguyen, K. B., T. P. Salazar-Mather, M. Y. Dalod, J. B. Van Deusen, X. Q. Wei, F. Y. Liew, M. A. Caligiuri, J. E. Durbin, and C. A. Biron. 2002. Coordinated and distinct roles for IFN-αβ, IL-12, and IL-15 regulation of NK cell responses to viral infection. J. Immunol. 169: 4279-4287.
10. Gately, M. K., U. Gubler, M. J. Brunda, R. R. Nadeau, T. D. Anderson, J. M. Lipman, and U. Sarmiento. 1994. Interleukin-12: a cytokine with therapeutic potential in oncology and infectious diseases. Ther. Immunol. 1: 187-196. (Pubitemid 24278712)
11. Huang, W., L. Na, P. L. Fidel, and P. Schwarzenberger. 2004. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J. Infect. Dis. 190: 624-631. (Pubitemid 38982105)
12. McIntyre, K. W., D. J. Shuster, K. M. Gillooly, R. R. Warrier, S. E. Connaughton, L. B. Hall, L. H. Arp, M. K. Gately, and J. Magram. 1996. Reduced incidence and severity of collagen-induced arthritis in interleukin-12-deficient mice. Eur. J. Immunol. 26: 2933-2938. (Pubitemid 26411497)
13. Malfait, A. M., D. M. Butler, D. H. Presky, R. N. Maini, F. M. Brennan, and M. Feldmann. 1998. Blockade of IL-12 during the induction of collagen-induced arthritis (CIA) markedly attenuates the severity of the arthritis. Clin. Exp. Immunol. 111: 377-383.
14. Murphy, C. A., C. L. Langrish, Y. Chen, W. Blumenschein, T. McClanahan, R. A. Kastelein, J. D. Sedgwick, and D. J. Cua. 2003. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198: 1951-1957.
15. Thakker, P., M. W. Leach, W. Kuang, S. E. Benoit, J. P. Leonard, and S. Marusic. 2007. IL-23 is critical in the induction but not in the effector phase of experimental autoimmune encephalomyelitis. J. Immunol. 178: 2589-2598. (Pubitemid 46233462)
16. Nakae, S., A. Nambu, K. Sudo, and Y. Iwakura. 2003. Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J. Immunol. 171: 6173-6177. (Pubitemid 37467240)
17. Olson, J. K., A. M. Ercolini, and S. D. Miller. 2005. A virus-induced molecular mimicry model of multiple sclerosis. Curr. Top. Microbiol. Immunol. 296: 39-53. (Pubitemid 41667260)
18. Lipton, H. L., J. Kratochvil, P. Sethi, and M. C. Dal Canto. 1984. Theiler's virus antigen detected in mouse spinal cord 2 1/2 years after infection. Neurology 34: 1117-1119.
19. Petro, T. M. 2005. ERK-MAP-kinases differentially regulate expression of IL-23 p19 compared with p40 and IFN-β in Theiler's virus-infected RAW264.7 cells. Immunol. Lett. 97: 47-53.
20. Al-Salleeh, F., and T. M. Petro. 2007. TLR3 and TLR7 are involved in expression of IL-23 subunits while TLR3 but not TLR7 is involved in expression of IFN-β by Theiler's virus-infected RAW264.7 cells. Microbes Infect. 9: 1384-1392. (Pubitemid 47539212)
21. Ozinsky, A., D. M. Underhill, J. D. Fontenot, A. M. Hajjar, K. D. Smith, C. B. Wilson, L. Schroeder, and A. Aderem. 2000. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between Toll-like receptors. Proc. Natl. Acad. Sci. USA 97: 13766-13771.
22. Rock, F. L., G. Hardiman, J. C. Timans, R. A. Kastelein, and J. F. Bazan. 1998. A family of human receptors structurally related to Drosophila Toll. Proc. Natl. Acad. Sci. USA 95: 588-593.
23. Takeda, K., and S. Akira. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17: 1-14.
24. Carmody, R. J., Q. Ruan, H. C. Liou, and Y. H. Chen. 2007. Essential roles of c-Rel in TLR-induced IL-23 p19 gene expression in dendritic cells. J. Immunol. 178: 186-191.
25. Mise-Omata, S., E. Kuroda, J. Niikura, U. Yamashita, Y. Obata, and T. S. Doi. 2007. A proximal κB site in the IL-23 p19 promoter is responsible for RelA- and c-Rel-dependent transcription. J. Immunol. 179: 6596-6603.
26. Kollet, J., C. Witek, J. D. Gentry, X. Liu, S. D. Schwartzbach, and T. M. Petro. 2001. Deletional analysis of the murine IL-12 p35 promoter comparing IFN-γ and lipopolysaccharide stimulation. J. Immunol. 167: 5653-5663. (Pubitemid 33062755)
27. + cytotoxic T cell activation and memory in virus infection. J. Immunol. 149: 1326-1333.
28. Steinman, R. M. 1991. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9: 271-296.
29. -ΔΔ C(T) method. Methods 25: 402-408.
30. Tasheva, E. S., B. Klocke, and G. W. Conrad. 2004. Analysis of transcriptional regulation of the small leucine rich proteoglycans. Mol. Vis. 10: 758-772.
31. Cartharius, K., K. Frech, K. Grote, B. Klocke, M. Haltmeier, A. Klingenhoff, M. Frisch, M. Bayerlein, and T. Werner. 2005. MatInspector and beyond: promoter analysis based on transcription factor binding sites. Bioinformatics 21: 2933-2942. (Pubitemid 40916416)
32. Massague, J., and D. Wotton. 2000. Transcriptional control by the TGF-β/Smad signaling system. EMBO J. 19: 1745-1754. (Pubitemid 30204386)
33. Roberts, A. B., and R. Derynck. 2001. Meeting report: signaling schemes for TGF-η. Sci. STKE 2001: PE43.
34. Honda, K., and T. Taniguchi. 2006. IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat. Rev. Immunol. 6: 644-658. (Pubitemid 44298214)
35. Lipton, H. L., G. Twaddle, and M. L. Jelachich. 1995. The predominant virus antigen burden is present in macrophages in Theiler's murine encephalomyelitis virus-induced demyelinating disease. J. Virol. 69: 2525-2533.
36. Dahlberg, A., M. R. Auble, and T. M. Petro. 2006. Reduced expression of IL-12 p35 by SJL/J macrophages responding to Theiler's virus infection is associated with constitutive activation of IRF-3. Virology 353: 422-432. (Pubitemid 44397134)
37. Dennler, S., M.-J. Goumans, and P. ten Dijke. 2002. Transforming growth factor β signal transduction. J. Leukocyte Biol. 71: 731-740.
38. Morton, S., R. J. Davis, and P. Cohen. 2004. Signalling pathways involved in multisite phosphorylation of the transcription factor ATF-2. FEBS Lett. 572: 177-183. (Pubitemid 39092532)
39. Hause, L., F. M. Al-Salleeh, and T. M. Petro. 2007. Expression of IL-27 p28 by Theiler's virus-infected macrophages depends on TLR3 and TLR7 activation of JNK-MAP-kinases. Antiviral Res. 76: 159-167. (Pubitemid 47410320)
40. Petro, T. M. 2005. Disparate expression of IL-12 by SJL/J and B10.S macrophages during Theiler's virus infection is associated with activity of TLR7 and mitogen-activated protein kinases. Microbes Infect. 7: 224-232.
41. Sato, M., H. Suemori, N. Hata, M. Asagiri, K. Ogasawara, K. Nakao, T. Nakaya, M. Katsuki, S. Noguchi, N. Tanaka, and T. Taniguchi. 2000. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-α/β gene induction. Immunity 13: 539-548. (Pubitemid 30951877)
42. Panne, D., T. Maniatis, and S. C. Harrison. 2007. An atomic model of the interferon- β enhanceosome. Cell 129: 1111-1123.
43. Kollet, J. I., and T. M. Petro. 2006. IRF-1 and NF-κB p50/cRel bind to distinct regions of the proximal murine IL-12 p35 promoter during costimulation with IFN-γ and LPS. Mol. Immunol. 43: 623-633.
44. Baker, J. C., and R. M. Harland. 1996. A novel mesoderm inducer, Madr2, functions in the activin signal transduction pathway. Genes Dev. 10: 1880-1889.
45. Zhang, Y., X. Feng, R. We, and R. Derynck. 1996. Receptor-associated Mad homologues synergize as effectors of the TGF-β response. Nature 383: 168-172. (Pubitemid 26303979)
46. Liu, F., A. Hata, J. C. Baker, J. Doody, J. Carcamo, R. M. Harland, and J. Massague. 1996. A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381: 620-623. (Pubitemid 26177480)
47. Chen, X., E. Weisberg, V. Fridmacher, M. Watanabe, G. Naco, and M. Whitman. 1997. Smad4 and FAST-1 in the assembly of activin-responsive factor. Nature 389: 85-89. (Pubitemid 27387696)
48. Massague, J., and Y.-G. Chen. 2000. Controlling TGF-β signaling. Genes Dev. 14: 627-644.
49. Derynck, R., and Y. E. Zhang. 2003. Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 425: 577-584. (Pubitemid 37280136)
50. Muzio, M., N. Polentarutti, D. Bosisio, M. K. Prahladan, and A. Mantovani. 2000. Toll-like receptors: a growing family of immune receptors that are differentially expressed and regulated by different leukocytes. J. Leukocyte Biol. 67: 450-456. (Pubitemid 30679773)
51. Livingstone, C., G. Patel, and N. Jones. 1995. ATF-2 contains a phosphorylation-dependent transcriptional activation domain. EMBO J. 14: 1785-1797.
52. Van Dam, H., D. Wilhelm, I. Herr, A. Steffen, P. Herrlich, and P. Angel. 1995. ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents. EMBO J. 14: 1798-1811.
53. Hanafusa, H., J. Ninomiya-Tsuji, N. Masuyama, M. Nishita, J. Fujisawa, H. Shibuya, K. Matsumoto, and E. Nishida. 1999. Involvement of the p38 mitogen- activated protein kinase pathway in transforming growth factor-β-induced gene expression. J. Biol. Chem. 274: 27161-27167. (Pubitemid 129520243)
54. Falvo, J. V., B. S. Parekh, C. H. Lin, E. Fraenkel, and T. Maniatis. 2000. Assembly of a functional β interferon enhanceosome is dependent on ATF-2-c-jun heterodimer orientation. Mol. Cell. Biol. 20: 4814-4825.
55. Sarkar, S. N., K. L. Peters, C. P. Elco, S. Sakamoto, S. Pal, and G. C. Sen. 2004. Novel roles of TLR3 tyrosine phosphorylation and PI3 kinase in double-stranded RNA signaling. Nat. Struct. Mol. Biol. 11: 1060-1067.
56. Taniguchi, T., K. Ogasawara, A. Takaoka, and N. Tanaka. 2001. IRF family of transcription factors as regulators of host defense. Annu. Rev. Immunol. 19: 623-655. (Pubitemid 32368048)
57. Mamane, Y., C. Heylbroeck, P. Genin, M. Algarte, M. J. Servant, C. LePage, C. DeLuca, H. Kwon, R. Lin, and J. Hiscott. 1999. Interferon regulatory factors: the next generation. Gene 237: 1-14. (Pubitemid 29406192)
58. Fan, C. M., and T. Maniatis. 1989. Two different virus-inducible elements are required for human β-interferon gene regulation. EMBO J. 8: 101-110.
59. Tailor, P., T. Tamura, and K. Ozato. 2006. IRF family proteins and type I interferon induction in dendritic cells. Cell Res. 16: 134-140. (Pubitemid 43247968)
60. Ghosh, S., and M. Karin. 2002. Missing pieces in the NF-κB puzzle. Cell 109 (Suppl.): S81-S96.
61. Baldwin, A. S., Jr. 1996. The NF-κB and IκB proteins: new discoveries and insights. Annu. Rev. Immunol. 14: 649-683.
62. DiDonato, J. A., F. Mercurio, and M. Karin. 1995. Phosphorylation of IκBα precedes but is not sufficient for its dissociation from NF-κB. Mol. Cell. Biol. 15: 1302-1311.
63. Woronicz, J. D., X. Gao, Z. Cao, M. Rothe, and D. V. Goeddel. 1997. IκB kinase-β: NF-κB activation and complex formation with IκB kinase-α and NIK. Science 278: 866-869. (Pubitemid 27467924)
64. Steurbaut, S., B. Rombaut, and R. Vrijsen. 2006. Persistent infection of RAW264.7 macrophages with the DA strain of Theiler's murine encephalomyelitis virus: an in vitro model to study viral persistence. J. Neurovirol. 12: 108-115. (Pubitemid 44574602)
65. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5: 730-737. (Pubitemid 39023305)
66. Andrejeva, J., K. S. Childs, D. F. Young, T. S. Carlos, N. Stock, S. Goodbourn, and R. E. Randall. 2004. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-β promoter. Proc. Natl. Acad. Sci. USA 101: 17264-17269. (Pubitemid 39627808)
67. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K. J. Ishii, et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105. (Pubitemid 43827959)