The role of the transcription factor CREB in immune function

Journal of Immunology

Volumn 185, Issue 11, 2010, Pages 6413-6419

  Wen, Andy Y ^a   Sakamoto, Kathleen M ^b   Miller, Lloyd S ^c  

^a Division of Pediatric Critical Care   (United States)

^b Division of Pediatric Hematology and Oncology   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLOOXYGENASE 2; GAMMA INTERFERON; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; JANUS KINASE; MACROPHAGE MIGRATION INHIBITION FACTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; TATA BINDING PROTEIN; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CIRCADIAN RHYTHM; CYTOKINE PRODUCTION; GLUCOSE HOMEOSTASIS; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE RESPONSE; MACROPHAGE; MONOCYTE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SPERMATOGENESIS; TH1 CELL; TH17 CELL; TH2 CELL;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; HUMANS; IMMUNITY, CELLULAR;

EID: 78650666211     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001829     Document Type: Article

References (69)

1. Shaywitz, A. J., and M. E. Greenberg. 1999. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 68:821-861.
2. Mayr, B., and M. Montminy. 2001. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2:599-609.
3. Sakamoto, K. M., and D. A. Frank. 2009. CREB in the pathophysiology of cancer: implications for targeting transcription factors for cancer therapy.. Clin. Cancer Res. 15:2583-2587.
4. Brindle, P., S. Linke, and M. Montminy. 1993. Protein-kinase-A-dependent activator in transcription factor CREB reveals new role for CREM repressors. Nature 364:821-824.
5. Enslen, H., H. Tokumitsu, and T. R. Soderling. 1995. Phosphorylation of CREB by CaM-kinase IV activated by CaM-kinase IV kinase. Biochem. Biophys. Res. Commun. 207:1038-1043.
6. Gubina, E., X. Luo, E. Kwon, K. Sakamoto, Y. F. Shi, and R. A. Mufson. 2001. betac cytokine receptor-induced stimulation of cAMP response element binding protein phosphorylation requires protein kinase C in myeloid cells: a novel cytokine signal transduction cascade. J. Immunol. 167:4303-4310.
7. Conkright, M. D., G. Canettieri, R. Screaton, E. Guzman, L. Miraglia, J. B. Hogenesch, and M. Montminy. 2003. TORCs: transducers of regulated CREB activity. Mol. Cell 12:413-423.
8. Impey, S., S. R. McCorkle, H. Cha-Molstad, J. M. Dwyer, G. S. Yochum, J. M. Boss, S. McWeeney, J. J. Dunn, G. Mandel, and R. H. Goodman. 2004. Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell 119:1041-1054.
9. Brenner, S., S. Prösch, K. Schenke-Layland, U. Riese, U. Gausmann, and C. Platzer. 2003. cAMP-induced Interleukin-10 promoter activation depends on CCAAT/enhancer-binding protein expression and monocytic differentiation. J. Biol. Chem. 278:5597-5604.
10. Hughes-Fulford, M., E. Sugano, T. Schopper, C. F. Li, J. B. Boonyaratanakornkit, and A. Cogoli. 2005. Early immune response and regulation of IL-2 receptor subunits. Cell. Signal. 17:1111-1124.
11. Takeuchi, O., and S. Akira. 2010. Pattern recognition receptors and inflammation. Cell 140:805-820.
12. Medzhitov, R. 2010. Inflammation 2010: new adventures of an old flame. Cell 140:771-776.
13. Ghosh, S., and M. S. Hayden. 2008. New regulators of NF-kappaB in inflammation. Nat. Rev. Immunol. 8:837-848.
14. Medzhitov, R., and T. Horng. 2009. Transcriptional control of the inflammatory response. Nat. Rev. Immunol. 9:692-703.
15. Ollivier, V., G. C. Parry, R. R. Cobb, D. de Prost, and N. Mackman. 1996. Elevated cyclic AMP inhibits NF-kappaB-mediated transcription in human monocytic cells and endothelial cells. J. Biol. Chem. 271:20828-20835.
16. Parry, G. C., and N. Mackman. 1997. Role of cyclic AMP response elementbinding protein in cyclic AMP inhibition of NF-kappaB-mediated transcription. J. Immunol. 159:5450-5456.
17. Pigazzi, M., E. Manara, E. Baron, and G. Basso. 2009. miR-34b targets cyclic AMP-responsive element binding protein in acute myeloid leukemia. Cancer Res. 69:2471-2478.
18. Park, J. M., F. R. Greten, A. Wong, R. J. Westrick, J. S. Arthur, K. Otsu, A. Hoffmann, M. Montminy, and M. Karin. 2005. Signaling pathways and genes that inhibit pathogen-induced macrophage apoptosis-CREB and NF-kappaB as key regulators. Immunity 23:319-329.
19. Hsu, L. C., J. M. Park, K. Zhang, J. L. Luo, S. Maeda, R. J. Kaufman, L. Eckmann, D. G. Guiney, and M. Karin. 2004. The protein kinase PKR is required for macrophage apoptosis after activation of Toll-like receptor 4. Nature 428:341-345.
20. Agarwal, N., G. Lamichhane, R. Gupta, S. Nolan, and W. R. Bishai. 2009. Cyclic AMP intoxication of macrophages by a Mycobacterium tuberculosis adenylate cyclase. Nature 460:98-102.
21. Cheng, J. C., K. Kinjo, D. R. Judelson, J. Chang, W. S. Wu, I. Schmid, D. B. Shankar, N. Kasahara, R. Stripecke, R. Bhatia, et al. 2008. CREB is a critical regulator of normal hematopoiesis and leukemogenesis. Blood 111:1182-1192.
22. Kwon, E. M., M. A. Raines, J. Blenis, and K. M. Sakamoto. 2000. Granulocytemacrophage colony-stimulating factor stimulation results in phosphorylation of cAMP response element-binding protein through activation of pp90RSK. Blood 95:2552-2558.
23. Tschopp, J., and K. Schroder. 2010. NLRP3 inflammasome activation: The convergence of multiple signalling pathways on ROS production? Nat. Rev. Immunol. 10:210-215.
24. Gavala, M. L., Z. A. Pfeiffer, and P. J. Bertics. 2008. The nucleotide receptor P2RX7 mediates ATP-induced CREB activation in human and murine monocytic cells. J. Leukoc. Biol. 84:1159-1171.
25. Potucek, Y. D., J. M. Crain, and J. J. Watters. 2006. Purinergic receptors modulate MAP kinases and transcription factors that control microglial inflammatory gene expression. Neurochem. Int. 49:204-214.
26. Brautigam, V. M., C. Frasier, M. Nikodemova, and J. J. Watters. 2005. Purinergic receptor modulation of BV-2 microglial cell activity: potential involvement of p38 MAP kinase and CREB. J. Neuroimmunol. 166:113-125.
27. Bowdish, D. M., D. J. Davidson, D. P. Speert, and R. E. Hancock. 2004. The human cationic peptide LL-37 induces activation of the extracellular signalregulated kinase and p38 kinase pathways in primary human monocytes. J. Immunol. 172:3758-3765.
28. Yu, J., N. Mookherjee, K. Wee, D. M. Bowdish, J. Pistolic, Y. Li, L. Rehaume, and R. E. Hancock. 2007. Host defense peptide LL-37, in synergy with inflammatory mediator IL-1beta, augments immune responses by multiple pathways. J. Immunol. 179:7684-7691.
29. Saraiva, M., and A. O'Garra. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10:170-181.
30. Boonstra, A., R. Rajsbaum, M. Holman, R. Marques, C. Asselin-Paturel, J. P. Pereira, E. E. Bates, S. Akira, P. Vieira, Y. J. Liu, et al. 2006. Macrophages and myeloid dendritic cells, but not plasmacytoid dendritic cells, produce IL-10 in response to MyD88-and TRIF-dependent TLR signals, and TLR-independent signals. J. Immunol. 177:7551-7558.
31. Netea, M. G., R. Sutmuller, C. Hermann, C. A. Van der Graaf, J. W. Van der Meer, J. H. van Krieken, T. Hartung, G. Adema, and B. J. Kullberg. 2004. Toll-like receptor 2 suppresses immunity against Candida albicans through induction of IL-10 and regulatory T cells. J. Immunol. 172:3712-3718.
32. Ananieva, O., J. Darragh, C. Johansen, J. M. Carr, J. McIlrath, J. M. Park, A. Wingate, C. E. Monk, R. Toth, S. G. Santos, et al. 2008. The kinases MSK1 and MSK2 act as negative regulators of Toll-like receptor signaling. Nat. Immunol. 9:1028-1036.
33. Martin, M., K. Rehani, R. S. Jope, and S. M. Michalek. 2005. Toll-like receptormediated cytokine production is differentially regulated by glycogen synthase kinase 3. Nat. Immunol. 6:777-784.
34. Brightbill, H. D., S. E. Plevy, R. L. Modlin, and S. T. Smale. 2000. A prominent role for Sp1 during lipopolysaccharide-mediated induction of the IL-10 promoter in macrophages. J. Immunol. 164:1940-1951.
35. Chan, M. M., B. K. Cheung, J. C. Li, L. L. Chan, and A. S. Lau. 2009. A role for glycogen synthase kinase-3 in antagonizing mycobacterial immune evasion by negatively regulating IL-10 induction. J. Leukoc. Biol. 86:283-291.
36. Tone, M., M. J. Powell, Y. Tone, S. A. Thompson, and H. Waldmann. 2000. IL-10 gene expression is controlled by the transcription factors Sp1 and Sp3. J. Immunol. 165:286-291.
37. Kelly, E. K., L. Wang, and L. B. Ivashkiv. 2010. Calcium-activated pathways and oxidative burst mediate zymosan-induced signaling and IL-10 production in human macrophages. J. Immunol. 184:5545-5552.
38. Gee, K., J. B. Angel, S. Mishra, M. A. Blahoianu, and A. Kumar. 2007. IL-10 regulation by HIV-Tat in primary human monocytic cells: involvement of calmodulin/calmodulin-dependent protein kinase-activated p38 MAPK and Sp-1 and CREB-1 transcription factors. J. Immunol. 178:798-807.
39. Gee, K., J. B. Angel, W. Ma, S. Mishra, N. Gajanayaka, K. Parato, and A. Kumar. 2006. Intracellular HIV-Tat expression induces IL-10 synthesis by the CREB-1 transcription factor through Ser133 phosphorylation and its regulation by the ERK1/2 MAPK in human monocytic cells. J. Biol. Chem. 281:31647-31658.
40. Li, J. C., and A. S. Lau. 2007. A role for mitogen-activated protein kinase and Ets-1 in the induction of interleukin-10 transcription by human immunodeficiency virus-1 Tat. Immunology 121:337-348.
41. Akridge, R. E., L. K. Oyafuso, and S. G. Reed. 1994. IL-10 is induced during HIV-1 infection and is capable of decreasing viral replication in human macrophages. J. Immunol. 153:5782-5789.
42. Zhou, J. H., S. R. Broussard, K. Strle, G. G. Freund, R. W. Johnson, R. Dantzer, and K. W. Kelley. 2001. IL-10 inhibits apoptosis of promyeloid cells by activating insulin receptor substrate-2 and phosphatidylinositol 3′-kinase. J. Immunol. 167:4436-4442.
43. Schroder, K., P. J. Hertzog, T. Ravasi, and D. A. Hume. 2004. Interferon-gamma: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 75:163-189.
44. Hu, X., P. K. Paik, J. Chen, A. Yarilina, L. Kockeritz, T. T. Lu, J. R. Woodgett, and L. B. Ivashkiv. 2006. IFN-gamma suppresses IL-10 production and synergizes with TLR2 by regulating GSK3 and CREB/AP-1 proteins. Immunity 24:563-574.
45. Grimes, C. A., and R. S. Jope. 2001. CREB DNA binding activity is inhibited by glycogen synthase kinase-3 beta and facilitated by lithium. J. Neurochem. 78:1219-1232.
46. Solomou, E. E., Y. T. Juang, and G. C. Tsokos. 2001. Protein kinase C-theta participates in the activation of cyclic AMP-responsive element-binding protein and its subsequent binding to the-180 site of the IL-2 promoter in normal human T lymphocytes. J. Immunol. 166:5665-5674.
47. Yeh, J. H., P. Lecine, J. A. Nunes, S. Spicuglia, P. Ferrier, D. Olive, and J. Imbert. 2001. Novel CD28-responsive enhancer activated by CREB/ATF and AP-1 families in the human interleukin-2 receptor alpha-chain locus. Mol. Cell. Biol. 21:4515-4527.
48. Mayall, T. P., P. L. Sheridan, M. R. Montminy, and K. A. Jones. 1997. Distinct roles for P-CREB and LEF-1 in TCR alpha enhancer assembly and activation on chromatin templates in vitro. Genes Dev. 11:887-899.
49. Anderson, S. J., S. Miyake, and D. Y. Loh. 1989. Transcription from a murine T-cell receptor V beta promoter depends on a conserved decamer motif similar to the cyclic AMP response element. Mol. Cell. Biol. 9:4835-4845.
50. Gao, M. H., and P. B. Kavathas. 1993. Functional importance of the cyclic AMP response element-like decamer motif in the CD8 alpha promoter. J. Immunol. 150:4376-4385.
51. Gupta, A., and C. Terhorst. 1994. CD3 delta enhancer. CREB interferes with the function of a murine CD3-delta A binding factor (M delta AF). J. Immunol. 152:3895-3903.
52. Barton, K., N. Muthusamy, M. Chanyangam, C. Fischer, C. Clendenin, and J. M. Leiden. 1996. Defective thymocyte proliferation and IL-2 production in transgenic mice expressing a dominant-negative form of CREB. Nature 379:81-85.
53. Zhang, F., M. Rincon, R. A. Flavell, and T. M. Aune. 2000. Defective Th function induced by a dominant-negative cAMP response element binding protein mutation is reversed by Bcl-2. J. Immunol. 165:1762-1770.
54. Yano, S., P. Ghosh, H. Kusaba, M. Buchholz, and D. L. Longo. 2003. Effect of promoter methylation on the regulation of IFN-gamma gene during in vitro differentiation of human peripheral blood T cells into a Th2 population. J. Immunol. 171:2510-2516.
55. Pasquinelli, V., J. C. Townsend, J. O. Jurado, I. B. Alvarez, M. F. Quiroga, P. F. Barnes, B. Samten, and V. E. García. 2009. IFN-gamma production during active tuberculosis is regulated by mechanisms that involve IL-17, SLAM, and CREB. J. Infect. Dis. 199:661-665.
56. Grady, G. C., S. M. Mason, J. Stephen, J. C. Zúñiga- Pflücker, and A. M. Michie. 2004. Cyclic adenosine 5′-monophosphate response element binding protein plays a central role in mediating proliferation and differentiation downstream of the pre-TCR complex in developing thymocytes. J. Immunol. 173:1802-1810.
57. Muthusamy, N., and J. M. Leiden. 1998. A protein kinase C-, Ras-, and RSK2-dependent signal transduction pathway activates the cAMP-responsive elementbinding protein transcription factor following T cell receptor engagement. J. Biol. Chem. 273:22841-22847.
58. Yu, C. T., H. M. Shih, and M. Z. Lai. 2001. Multiple signals required for cyclic AMP-responsive element binding protein (CREB) binding protein interaction induced by CD3/CD28 costimulation. J. Immunol. 166:284-292.
59. Hsueh, Y. P., H. E. Liang, S. Y. Ng, and M. Z. Lai. 1997. CD28-costimulation activates cyclic AMP-responsive element-binding protein in T lymphocytes. J. Immunol. 158:85-93.
60. Kaiser, M., G. R. Wiggin, K. Lightfoot, J. S. Arthur, and A. Macdonald. 2007. MSK regulate TCR-induced CREB phosphorylation but not immediate early gene transcription. Eur. J. Immunol. 37:2583-2595.
61. Sakaguchi, S., M. Miyara, C. M. Costantino, and D. A. Hafler. 2010. FOXP3+ regulatory T cells in the human immune system. Nat. Rev. Immunol. 10:490-500.
62. Polansky, J. K., K. Kretschmer, J. Freyer, S. Floess, A. Garbe, U. Baron, S. Olek, A. Hamann, H. von Boehmer, and J. Huehn. 2008. DNA methylation controls Foxp3 gene expression. Eur. J. Immunol. 38:1654-1663.
63. Polansky, J. K., L. Schreiber, C. Thelemann, L. Ludwig, M. Krüger, R. Baumgrass, S. Cording, S. Floess, A. Hamann, and J. Huehn. 2010. Methylation matters: binding of Ets-1 to the demethylated Foxp3 gene contributes to the stabilization of Foxp3 expression in regulatory T cells. J. Mol. Med. 88:1029-1040 (epub ahead of print).
64. Kim, H. P., and W. J. Leonard. 2007. CREB/ATF-dependent T cell receptorinduced FoxP3 gene expression: a role for DNA methylation. J. Exp. Med. 204:1543-1551.
65. Ruan, Q., V. Kameswaran, Y. Tone, L. Li, H. C. Liou, M. I. Greene, M. Tone, and Y. H. Chen. 2009. Development of Foxp3 (+) regulatory t cells is driven by the c-Rel enhanceosome. Immunity 31:932-940.
66. Yasuda, T., H. Sanjo, G. Pagès, Y. Kawano, H. Karasuyama, J. Pouysségur, M. Ogata, and T. Kurosaki. 2008. Erk kinases link pre-B cell receptor signaling to transcriptional events required for early B cell expansion. Immunity 28:499-508.
67. Blois, J. T., J. M. Mataraza, I. Mecklenbraüker, A. Tarakhovsky, and T. C. Chiles. 2004. B cell receptor-induced cAMP-response element-binding protein activation in B lymphocytes requires novel protein kinase Cdelta. J. Biol. Chem. 279:30123-30132.
68. 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.
69. Smale, S. T. 2010. Seq-ing LPS-induced enhancers. Immunity 32:296-298.