DC-SCRIPT regulates IL-10 production in human dendritic cells by modulating NF-κBp65 activation

Journal of Immunology

Volumn 195, Issue 4, 2015, Pages 1498-1505

  Søndergaard, Jonas Nørskov ^a   Poghosyan, Susanna ^a   Hontelez, Saartje ^a   Louche, Pauline ^a   Looman, Maaike W G ^a   Ansems, Marleen ^a   Adema, Gosse J ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DENDRITIC CELL SPECIFIC TRANSCRIPT PROTEIN; INTERLEUKIN 10; REGULATOR PROTEIN; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; CARRIER PROTEIN; GLUCOCORTICOID RECEPTOR; HISTONE ACETYLTRANSFERASE PCAF; PROTEIN BINDING; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR; TSC22D3 PROTEIN, HUMAN; ZNF366 PROTEIN, HUMAN;

ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; HUMAN; HUMAN CELL; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; INHIBITION KINETICS; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; BIOSYNTHESIS; ENHANCER REGION; ENZYME ACTIVATION; GENE INACTIVATION; GENETICS; IMMUNOLOGY; METABOLISM; PHOSPHORYLATION; RNA INTERFERENCE;

CARRIER PROTEINS; DENDRITIC CELLS; ENHANCER ELEMENTS, GENETIC; ENZYME ACTIVATION; GENE KNOCKOUT TECHNIQUES; HUMANS; INTERLEUKIN-10; P300-CBP TRANSCRIPTION FACTORS; PHOSPHORYLATION; PROTEIN BINDING; RECEPTORS, GLUCOCORTICOID; RNA INTERFERENCE; TOLL-LIKE RECEPTORS; TRANSCRIPTION FACTOR RELA; TRANSCRIPTION FACTORS;

EID: 84938939342     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402924     Document Type: Article

References (55)

1. Steinman, R. M., and J. Banchereau. 2007. Taking dendritic cells into medicine. Nature 449: 419-426.
2. Bakdash, G., S. P. Sittig, T. van Dijk, C. G. Figdor, and I. J. M. de Vries. 2013. The nature of activatory and tolerogenic dendritic cell-derived signal II. Front. Immunol. 4: 53.
3. Gregori, S., D. Tomasoni, V. Pacciani, M. Scirpoli, M. Battaglia, C. F. Magnani, E. Hauben, and M. G. Roncarolo. 2010. Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway. Blood 116: 935-944.
4. Saraiva, M., and A. O'Garra. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10: 170-181.
5. Hilkens, C. M. U., J. D. Isaacs, and A. W. Thomson. 2010. Development of dendritic cell-based immunotherapy for autoimmunity. Int. Rev. Immunol. 29: 156-183.
6. Wimmers, F., G. Schreibelt, A. E. Sköld, C. G. Figdor, and I. J. M. De Vries. 2014. Paradigm shift in dendritic cell-based immunotherapy: from in vitro generated monocyte-derived DCs to naturally circulating DC subsets. Front. Immunol. 5: 165.
7. Banchereau, J., and R. M. Steinman. 1998. Dendritic cells and the control of immunity. Nature 392: 245-252.
8. Trinchieri, G., and A. Sher. 2007. Cooperation of Toll-like receptor signals in innate immune defence. Nat. Rev. Immunol. 7: 179-190.
9. Gronemeyer, H., J. A. Gustafsson, and V. Laudet. 2004. Principles for modulation of the nuclear receptor superfamily. Nat. Rev. Drug Discov. 3: 950-964.
10. Ogawa, S., J. Lozach, C. Benner, G. Pascual, R. K. Tangirala, S. Westin, A. Hoffmann, S. Subramaniam, M. David, M. G. Rosenfeld, and C. K. Glass. 2005. Molecular determinants of crosstalk between nuclear receptors and tolllike receptors. Cell 122: 707-721.
11. Karthaus, N., A. B. van Spriel, M. W. G. Looman, S. Chen, L. M. Spilgies, L. Lieben, G. Carmeliet, M. Ansems, and G. J. Adema. 2014. Vitamin D controls murine and human plasmacytoid dendritic cell function. J. Invest. Dermatol. 134: 1255-1264.
12. Caldenhoven, E., J. Liden, S. Wissink, A. Van de Stolpe, J. Raaijmakers, L. Koenderman, S. Okret, J. A. Gustafsson, and P. T. Van der Saag. 1995. Negative cross-talk between RelA and the glucocorticoid receptor: a possible mechanism for the antiinflammatory action of glucocorticoids. Mol. Endocrinol. 9: 401-412.
13. Kawai, T., and S. Akira. 2007. Signaling to NF-kappaB by Toll-like receptors. Trends Mol. Med. 13: 460-469.
14. Neumann, M., and M. Naumann. 2007. Beyond IkappaBs: alternative regulation of NF-kappaB activity. FASEB J. 21: 2642-2654.
15. Auphan, N., J. A. DiDonato, C. Rosette, A. Helmberg, and M. Karin. 1995. Immunosuppression by glucocorticoids: inhibition of NF-kB activity through IkB synthesis. Science 270: 286-290.
16. Sheppard, K. A., K. M. Phelps, A. J. Williams, D. Thanos, C. K. Glass, M. G. Rosenfeld, M. E. Gerritsen, and T. Collins. 1998. Nuclear integration of glucocorticoid receptor and nuclear factor-kappaB signaling by CREB-binding protein and steroid receptor coactivator-1. J. Biol. Chem. 273: 29291-29294.
17. Perkins, N. D. 2006. Post-translational modifications regulating the activity and function of the nuclear factor kappa B pathway. Oncogene 25: 6717-6730.
18. Sakurai, H., H. Chiba, H. Miyoshi, T. Sugita, and W. Toriumi. 1999. IkappaB kinases phosphorylate NF-kappaB p65 subunit on serine 536 in the transactivation domain. J. Biol. Chem. 274: 30353-30356.
19. Zhong, H., R. E. Voll, and S. Ghosh. 1998. Phosphorylation of NF-kappa B p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol. Cell 1: 661-671.
20. Sabatel, H., E. Di Valentin, G. Gloire, F. Dequiedt, J. Piette, and Y. Habraken. 2012. Phosphorylation of p65(RelA) on Ser(547) by ATM represses NF-kBdependent transcription of specific genes after genotoxic stress. PLoS One 7: e38246.
21. Msaki, A., A. M. Sánchez, L. F. Koh, B. Barré, S. Rocha, N. D. Perkins, and R. F. Johnson. 2011. The role of RelA (p65) threonine 505 phosphorylation in the regulation of cell growth, survival, and migration. Mol. Biol. Cell 22: 3032-3040.
22. Kiernan, R., V. Brès, R. W. M. Ng, M. P. Coudart, S. El Messaoudi, C. Sardet, D. Y. Jin, S. Emiliani, and M. Benkirane. 2003. Post-activation turn-off of NFkappa B-dependent transcription is regulated by acetylation of p65. J. Biol. Chem. 278: 2758-2766.
23. Chen, L. F., Y. Mu, and W. C. Greene. 2002. Acetylation of RelA at discrete sites regulates distinct nuclear functions of NF-kappaB. EMBO J. 21: 6539-6548.
24. Saraiva, M., J. R. Christensen, A. V. Tsytsykova, A. E. Goldfeld, S. C. Ley, D. Kioussis, and A. O'Garra. 2005. Identification of a macrophage-specific chromatin signature in the IL-10 locus. J. Immunol. 175: 1041-1046.
25. Gringhuis, S. I., J. den Dunnen, M. Litjens, B. van Het Hof, Y. van Kooyk, and T. B. H. Geijtenbeek. 2007. C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NFkappaB. Immunity 26: 605-616.
26. Hontelez, S., M. Ansems, N. Karthaus, M. Zuidscherwoude, M. W. Looman, V. Triantis, and G. J. Adema. 2012. Dendritic cell-specific transcript: dendritic cell marker and regulator of TLR-induced cytokine production. J. Immunol. 189: 138-145.
27. Triantis, V., D. E. Trancikova, M. W. Looman, F. C. Hartgers, R. A. J. Janssen, and G. J. Adema. 2006. Identification and characterization of DC-SCRIPT, a novel dendritic cell-expressed member of the zinc finger family of transcriptional regulators. J. Immunol. 176: 1081-1089.
28. Triantis, V., V. Moulin, M. W. G. Looman, F. C. Hartgers, R. A. J. Janssen, and G. J. Adema. 2006. Molecular characterization of the murine homologue of the DC-derived protein DC-SCRIPT. J. Leukoc. Biol. 79: 1083-1091.
29. Lopez-Garcia, J., M. Periyasamy, R. S. Thomas, M. Christian, M. Leao, P. Jat, K. B. Kindle, D. M. Heery, M. G. Parker, L. Buluwela, et al. 2006. ZNF366 is an estrogen receptor corepressor that acts through CtBP and histone deacetylases. Nucleic Acids Res. 34: 6126-6136.
30. Ansems, M., N. Karthaus, S. Hontelez, T. Aalders, M. W. Looman, G. W. Verhaegh, J. A. Schalken, and G. J. Adema. 2012. DC-SCRIPT: AR and VDR regulator lost upon transformation of prostate epithelial cells. Prostate 72: 1708-1717.
31. Sieuwerts, A. M., M. Ansems, M. P. Look, P. N. Span, V. de Weerd, A. van Galen, J. A. Foekens, G. J. Adema, and J. W. Martens. 2010. Clinical significance of the nuclear receptor co-regulator DC-SCRIPT in breast cancer: an independent retrospective validation study. Breast Cancer Res. 12: R103.
32. Ansems, M., S. Hontelez, N. Karthaus, P. N. Span, and G. J. Adema. 2010. Crosstalk and DC-SCRIPT: expanding nuclear receptor modulation. Biochim. Biophys. Acta 1806: 193-199.
33. Hontelez, S., N. Karthaus, M. W. Looman, M. Ansems, and G. J. Adema. 2013. DC-SCRIPT regulates glucocorticoid receptor function and expression of its target GILZ in dendritic cells. J. Immunol. 190: 3172-3179.
34. Ansems, M., S. Hontelez, M. W. G. Looman, N. Karthaus, P. Bult, J. J. Bonenkamp, J. H. Jansen, F. C. G. J. Sweep, P. N. Span, and G. J. Adema. 2010. DC-SCRIPT: nuclear receptor modulation and prognostic significance in primary breast cancer. J. Natl. Cancer Inst. 102: 54-68.
35. Cohen, N., E. Mouly, H. Hamdi, M. C. Maillot, M. Pallardy, V. Godot, F. Capel, A. Balian, S. Naveau, P. Galanaud, et al. 2006. GILZ expression in human dendritic cells redirects their maturation and prevents antigen-specific T lymphocyte response. Blood 107: 2037-2044.
36. de Vries, I. J. M., A. A. O. Eggert, N. M. Scharenborg, J. L. M. Vissers, W. J. Lesterhuis, O. C. Boerman, C. J. A. Punt, G. J. Adema, and C. G. Figdor. 2002. Phenotypical and functional characterization of clinical grade dendritic cells. J. Immunother. 25: 429-438.
37. Schuurhuis, D. H., W. J. Lesterhuis, M. Kramer, M. G. M. Looman, M. van Hout-Kuijer, G. Schreibelt, A. C. I. Boullart, E. H. J. G. Aarntzen, D. Benitez-Ribas, C. G. Figdor, et al. 2009. Polyinosinic polycytidylic acid prevents efficient antigen expression after mRNA electroporation of clinical grade dendritic cells. Cancer Immunol. Immunother. 58: 1109-1115.
38. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
39. Denissov, S., M. van Driel, R. Voit, M. Hekkelman, T. Hulsen, N. Hernandez, I. Grummt, R. Wehrens, and H. Stunnenberg. 2007. Identification of novel functional TBP-binding sites and general factor repertoires. EMBO J. 26: 944-954.
40. Gringhuis, S. I., J. den Dunnen, M. Litjens, M. van der Vlist, B. Wevers, S. C. M. Bruijns, and T. B. H. Geijtenbeek. 2009. Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-kappaB activation through Raf-1 and Syk. Nat. Immunol. 10: 203-213.
41. Hofer, S., M. Rescigno, F. Granucci, S. Citterio, M. Francolini, and P. Ricciardi-Castagnoli. 2001. Differential activation of NF-kappa B subunits in dendritic cells in response to Gram-negative bacteria and to lipopolysaccharide. Microbes Infect. 3: 259-265.
42. Rauert-Wunderlich, H., D. Siegmund, E. Maier, T. Giner, R. C. Bargou, H. Wajant, and T. Stühmer. 2013. The IKK inhibitor Bay 11-7082 induces cell death independent from inhibition of activation of NFkB transcription factors. PLoS One 8: e59292.
43. Buss, H., A. Dörrie, M. L. Schmitz, E. Hoffmann, K. Resch, and M. Kracht. 2004. Constitutive and interleukin-1-inducible phosphorylation of p65 NFkappaB at serine 536 is mediated by multiple protein kinases including IkappaB kinase (IKK)-alpha, IKKbeta, IKKepsilon, TRAF family member-associated (TANK)-binding kinase 1 (TBK1), and an unknown kinase and couples p65 to TATA-binding protein-associated factor II31-mediated interleukin-8 transcription. J. Biol. Chem. 279: 55633-55643.
44. Balasubramanyam, K., V. Swaminathan, A. Ranganathan, and T. K. Kundu. 2003. Small molecule modulators of histone acetyltransferase p300. J. Biol. Chem. 278: 19134-19140.
45. Chimenti, F., B. Bizzarri, E. Maccioni, D. Secci, A. Bolasco, P. Chimenti, R. Fioravanti, A. Granese, S. Carradori, F. Tosi, et al. 2009. A novel histone acetyltransferase inhibitor modulating Gcn5 network: cyclopentylidene-[4-(49-chlorophenyl)thiazol-2-yl)hydrazone. J. Med. Chem. 52: 530-536.
46. Kikuchi, H., F. Kuribayashi, N. Kiwaki, Y. Takami, and T. Nakayama. 2011. GCN5 regulates the superoxide-generating system in leukocytes via controlling gp91-phox gene expression. J. Immunol. 186: 3015-3022.
47. Balasubramanyam, K., R. A. Varier, M. Altaf, V. Swaminathan, N. B. Siddappa, U. Ranga, and T. K. Kundu. 2004. Curcumin, a novel p300/CREB-binding protein-specific inhibitor of acetyltransferase, represses the acetylation of histone/nonhistone proteins and histone acetyltransferase-dependent chromatin transcription. J. Biol. Chem. 279: 51163-51171.
48. Marcu, M. G., Y. J. Jung, S. Lee, E. J. Chung, M. J. Lee, J. Trepel, and L. Neckers. 2006. Curcumin is an inhibitor of p300 histone acetylatransferase. Med. Chem. 2: 169-174.
49. Bowers, E. M., G. Yan, C. Mukherjee, A. Orry, L. Wang, M. A. Holbert, N. T. Crump, C. A. Hazzalin, G. Liszczak, H. Yuan, et al. 2010. Virtual ligand screening of the p300/CBP histone acetyltransferase: identification of a selective small molecule inhibitor. Chem. Biol. 17: 471-482.
50. Ansems, M., J. N. Søndergaard, A. M. Sieuwerts, M. W. G. Looman, M. Smid, A. M. A. de Graaf, V. de Weerd, M. Zuidscherwoude, J. A. Foekens, J. W. M. Martens, and G. J. Adema. 2015. DC-SCRIPT is a novel regulator of the tumor suppressor gene CDKN2B and induces cell cycle arrest in ERa-positive breast cancer cells. Breast Cancer Res. Treat. 149: 693-703.
51. Ho, P. C., Y. C. Tsui, X. Feng, D. R. Greaves, and L. N. Wei. 2012. NF-kBmediated degradation of the coactivator RIP140 regulates inflammatory responses and contributes to endotoxin tolerance. Nat. Immunol. 13: 379-386.
52. Zschiedrich, I., U. Hardeland, A. Krones-Herzig, M. Berriel Diaz, A. Vegiopoulos, J. Müggenburg, D. Sombroek, T. G. Hofmann, R. Zawatzky, X. Yu, et al. 2008. Coactivator function of RIP140 for NFkappaB/RelAdependent cytokine gene expression. Blood 112: 264-276.
53. Chen Lf, W., E. Fischle, Verdin, and W. C. Greene. 2001. Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science 293: 1653-1657.
54. Oh, S. M., S. H. Lee, B. J. Lee, C. W. Pyo, N. K. Yoo, S. Y. Lee, J. Kim, and S. Y. Choi. 2007. A distinct role of neutrophil lactoferrin in RelA/p65 phosphorylation on Ser536 by recruiting TNF receptor-associated factors to IkappaB kinase signaling complex. J. Immunol. 179: 5686-5692.
55. Shukla, S., G. T. MacLennan, P. Fu, J. Patel, S. R. Marengo, M. I. Resnick, and S. Gupta. 2004. Nuclear factor-kappaB/p65 (Rel A) is constitutively activated in human prostate adenocarcinoma and correlates with disease progression. Neoplasia 6: 390-400.