The ataxia telangiectasia mutated kinase pathway regulates IL-23 expression by human dendritic cells

Journal of Immunology

Volumn 190, Issue 7, 2013, Pages 3246-3255

  Wang, Qunwei ^a   Franks, Hester A ^a   Lax, Stephanie J ^a   El Refaee, Mohamed ^a   Malecka, Anna ^a   Shah, Sabaria ^a   Spendlove, Ian ^a   Gough, Michael J ^b   Seedhouse, Claire ^a   Madhusudan, Srinivasan ^a   Patel, Poulam M ^a   Jackson, Andrew M ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b EARLE A CHILES RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; INTERLEUKIN 12P70; INTERLEUKIN 23; MESSENGER RNA; PROTEIN P19; PROTEIN P35; PROTEIN P40; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; X BOX PROTEIN 1;

ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; DNA DAMAGE; ENDOPLASMIC RETICULUM STRESS; ENZYME INHIBITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RADIATION EXPOSURE; TH17 CELL; X RAY;

CELL CYCLE PROTEINS; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-23; LYMPHOCYTE ACTIVATION; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TH17 CELLS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 84875437631     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201484     Document Type: Article

References (75)

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. Roses, R. E., S. Xu, M. Xu, U. Koldovsky, G. Koski, and B. J. Czerniecki. 2008. Differential production of IL-23 and IL-12 by myeloid-derived dendritic cells in response to TLR agonists. J. Immunol. 181: 5120-5127.
3. Taylor, P. R., G. D. Brown, D. M. Reid, J. A. Willment, L. Martinez-Pomares, S. Gordon, and S. Y. Wong. 2002. The beta-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages. J. Immunol. 169: 3876-3882.
4. Li, Y., N. Chu, A. Hu, B. Gran, A. Rostami, and G. X. Zhang. 2008. Inducible IL-23p19 expression in human microglia via p38 MAPK and NF-kappaB signal pathways. Exp. Mol. Pathol. 84: 1-8.
5. Liao, J. J., M. C. Huang, and E. J. Goetzl. 2007. Cutting edge: Alternative signaling of Th17 cell development by sphingosine 1-phosphate. J. Immunol. 178: 5425-5428.
6. Stritesky, G. L., N. Yeh, and M. H. Kaplan. 2008. IL-23 promotes maintenance but not commitment to the Th17 lineage. J. Immunol. 181: 5948-5955.
7. Melton, A. C., S. L. Bailey-Bucktrout, M. A. Travis, B. T. Fife, J. A. Bluestone, and D. Sheppard. 2010. Expression of avb8 integrin on dendritic cells regulates Th17 cell development and experimental autoimmune encephalomyelitis in mice. J. Clin. Invest. 120: 4436-4444.
8. Ouyang, W., J. K. Kolls, and Y. Zheng. 2008. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28: 454-467.
9. Mills, K. H. 2008. Induction, function and regulation of IL-17-producing T cells. Eur. J. Immunol. 38: 2636-2649.
10. Zhu, X., L. A. Mulcahy, R. A. Mohammed, A. H. Lee, H. A. Franks, L. Kilpatrick, A. Yilmazer, E. C. Paish, I. O. Ellis, P. M. Patel, and A. M. Jackson. 2008. IL-17 expression by breast-cancer-associated macrophages: IL-17 promotes invasiveness of breast cancer cell lines. Breast Cancer Res. 10: R95.
11. Kim, H. R., H. S. Kim, M. K. Park, M. L. Cho, S. H. Lee, and H. Y. Kim. 2007. The clinical role of IL-23p19 in patients with rheumatoid arthritis. Scand. J. Rheumatol. 36: 259-264.
12. Numasaki, M., J. Fukushi, M. Ono, S. K. Narula, P. J. Zavodny, T. Kudo, P. D. Robbins, H. Tahara, and M. T. Lotze. 2003. Interleukin-17 promotes angiogenesis and tumor growth. Blood 101: 2620-2627.
13. Alexandrakis, M. G., C. A. Pappa, S. Miyakis, A. Sfiridaki, M. Kafousi, A. Alegakis, and E. N. Stathopoulos. 2006. Serum interleukin-17 and its relationship to angiogenic factors in multiple myeloma. Eur. J. Intern. Med. 17: 412-416.
14. Zou, W., and N. P. Restifo. 2010. T(H)17 cells in tumour immunity and immunotherapy. Nat. Rev. Immunol. 10: 248-256.
15. Cannon, M. J., H. Goyne, P. J. Stone, and M. Chiriva-Internati. 2011. Dendritic cell vaccination against ovarian cancer - tipping the Treg/TH17 balance to therapeutic advantage? Expert Opin. Biol. Ther. 11: 441-445.
16. Kryczek, I., M. Banerjee, P. Cheng, L. Vatan, W. Szeliga, S. Wei, E. Huang, E. Finlayson, D. Simeone, T. H. Welling, et al. 2009. Phenotype, distribution, generation, and functional and clinical relevance of Th17 cells in the human tumor environments. Blood 114: 1141-1149.
17. Sfanos, K. S., T. C. Bruno, C. H. Maris, L. Xu, C. J. Thoburn, A. M. DeMarzo, A. K. Meeker, W. B. Isaacs, and C. G. Drake. 2008. Phenotypic analysis of prostate-infiltrating lymphocytes reveals TH17 and Treg skewing. Clin. Cancer Res. 14: 3254-3261.
18. Iwakura, Y., and H. Ishigame. 2006. The IL-23/IL-17 axis in inflammation. J. Clin. Invest. 116: 1218-1222.
19. Volpe, E., N. Servant, R. Zollinger, S. I. Bogiatzi, P. Hupé, E. Barillot, and V. Soumelis. 2008. A critical function for transforming growth factor-beta, interleukin 23 and proinflammatory cytokines in driving and modulating human T (H)-17 responses. Nat. Immunol. 9: 650-657.
20. Manel, N., D. Unutmaz, and D. R. Littman. 2008. The differentiation of human T (H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat. Immunol. 9: 641-649.
21. Acosta-Rodriguez, E. V., G. Napolitani, A. Lanzavecchia, and F. Sallusto. 2007. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8: 942-949.
22. MacLennan, C., C. Fieschi, D. A. Lammas, C. Picard, S. E. Dorman, O. Sanal, J. M. MacLennan, S. M. Holland, T. H. Ottenhoff, J. L. Casanova, and D. S. Kumararatne. 2004. Interleukin (IL)-12 and IL-23 are key cytokines for immunity against Salmonella in humans. J. Infect. Dis. 190: 1755-1757.
23. Wiekowski, M. T., M. W. Leach, E. W. Evans, L. Sullivan, S. C. Chen, G. Vassileva, J. F. Bazan, D. M. Gorman, R. A. Kastelein, S. Narula, and S. A. Lira. 2001. Ubiquitous transgenic expression of the IL-23 subunit p19 induces multiorgan inflammation, runting, infertility, and premature death. J. Immunol. 166: 7563-7570.
24. Hao, J. S., and B. E. Shan. 2006. Immune enhancement and anti-tumour activity of IL-23. Cancer Immunol. Immunother. 55: 1426-1431.
25. Goodridge, H. S., W. Harnett, F. Y. Liew, and M. M. Harnett. 2003. Differential regulation of interleukin-12 p40 and p35 induction via Erk mitogen-activated protein kinase-dependent and -independent mechanisms and the implications for bioactive IL-12 and IL-23 responses. Immunology 109: 415-425.
26. Jackson, A. M., L. A. Mulcahy, X. W. Zhu, D. O'Donnell, and P. M. Patel. 2008. Tumour-mediated disruption of dendritic cell function: inhibiting the MEK1/2-p44/ 42 axis restores IL-12 production and Th1-generation. Int. J. Cancer 123: 623-632.
27. Jang, M. S., Y. M. Son, G. R. Kim, Y. J. Lee, W. K. Lee, S. H. Cha, S. H. Han, and C. H. Yun. 2009. Synergistic production of interleukin-23 by dendritic cells derived from cord blood in response to costimulation with LPS and IL-12. J. Leukoc. Biol. 86: 691-699.
28. Jackson, A. M., L. A. Mulcahy, J. Porte, H. A. Franks, M. El Refaee, Q. Wang, S. Shah, X. Zhu, and P. M. Patel. 2010. Role of mitogen-activated protein kinase and PI3K pathways in the regulation of IL-12-family cytokines in dendritic cells and the generation of T H-responses. Eur. Cytokine Netw. 21: 319-328.
29. Wang, Q., H. A. Franks, J. Porte, M. El Refaee, S. Shah, J. Crooks, P. M. Patel, and A. M. Jackson. 2011. Novel approach for interleukin-23 up-regulation in human dendritic cells and the impact on T helper type 17 generation. Immunology 134: 60-72.
30. Utsugi, M., K. Dobashi, T. Ishizuka, T. Kawata, T. Hisada, Y. Shimizu, A. Ono, and M. Mori. 2006. Rac1 negatively regulates lipopolysaccharide-induced IL-23 p19 expression in human macrophages and dendritic cells and NF-kappaB p65 trans activation plays a novel role. J. Immunol. 177: 4550-4557.
31. Goodridge, H. S., R. M. Simmons, and D. M. Underhill. 2007. Dectin-1 stimulation by Candida albicans yeast or zymosan triggers NFAT activation in macrophages and dendritic cells. J. Immunol. 178: 3107-3115.
32. Leibundgut-Landmann, S., F. Osorio, G. D. Brown, and C. Reis e Sousa. 2008. Stimulation of dendritic cells via the dectin-1/Syk pathway allows priming of cytotoxic T-cell responses. Blood 112: 4971-4980.
33. Robinson, M. J., F. Osorio, M. Rosas, R. P. Freitas, E. Schweighoffer, O. Gross, J. S. Verbeek, J. Ruland, V. Tybulewicz, G. D. Brown, et al. 2009. Dectin-2 is a Syk-coupled pattern recognition receptor crucial for Th17 responses to fungal infection. J. Exp. Med. 206: 2037-2051.
34. Slack, E. C., M. J. Robinson, P. Hernanz-Falcón, G. D. Brown, D. L. Williams, E. Schweighoffer, V. L. Tybulewicz, and C. Reis e Sousa. 2007. Syk-dependent ERK activation regulates IL-2 and IL-10 production by DC stimulated with zymosan. Eur. J. Immunol. 37: 1600-1612.
35. LeibundGut-Landmann, S., O. Gross, M. J. Robinson, F. Osorio, E. C. Slack, S. V. Tsoni, E. Schweighoffer, V. Tybulewicz, G. D. Brown, J. Ruland, and C. Reis e Sousa. 2007. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 8: 630-638.
36. Dillon, S., S. Agrawal, K. Banerjee, J. Letterio, T. L. Denning, K. Oswald-Richter, D. J. Kasprowicz, K. Kellar, J. Pare, T. van Dyke, et al. 2006. Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigenpresenting cells and immunological tolerance. J. Clin. Invest. 116: 916-928.
37. Shumilina, E., N. Zahir, N. T. Xuan, and F. Lang. 2007. Phosphoinositide 3-kinase dependent regulation of Kv channels in dendritic cells. Cell. Physiol. Biochem. 20: 801-808.
38. Bonifazi, P., C. D'Angelo, S. Zagarella, T. Zelante, S. Bozza, A. De Luca, G. Giovannini, S. Moretti, R. G. Iannitti, F. Fallarino, et al. 2010. Intranasally delivered siRNA targeting PI3K/Akt/mTOR inflammatory pathways protects from aspergillosis. Mucosal Immunol. 3: 193-205.
39. Davies, S. P., H. Reddy, M. Caivano, and P. Cohen. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351: 95-105.
40. Bain, J., L. Plater, M. Elliott, N. Shpiro, C. J. Hastie, H. McLauchlan, I. Klevernic, J. S. Arthur, D. R. Alessi, and P. Cohen. 2007. The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408: 297-315.
41. Carnero, A., and J. C. Lacal. 1998. Wortmannin, an inhibitor of phosphatidylinositol 3-kinase, induces oocyte maturation through a MPF-MAPK-dependent pathway. FEBS Lett. 422: 155-159.
42. Boulton, S., S. Kyle, L. Yalçintepe, and B. W. Durkacz. 1996. Wortmannin is a potent inhibitor of DNA double strand break but not single strand break repair in Chinese hamster ovary cells. Carcinogenesis 17: 2285-2290.
43. Ecay, T. W., J. L. Dickson, and T. D. Conner. 2000. Wortmannin inhibition of forskolin-stimulated chloride secretion by T84 cells. Biochim. Biophys. Acta 1467: 54-64.
44. Ethier, M. F., and J. M. Madison. 2002. LY294002, but not wortmannin, increases intracellular calcium and inhibits calcium transients in bovine and human airway smooth muscle cells. Cell Calcium 32: 31-38.
45. Westbrook, A. M., and R. H. Schiestl. 2010. Atm-deficient mice exhibit increased sensitivity to dextran sulfate sodium-induced colitis characterized by elevated DNA damage and persistent immune activation. Cancer Res. 70: 1875-1884.
46. Weintz, G., J. V. Olsen, K. Frühauf, M. Niedzielska, I. Amit, J. Jantsch, J. Mages, C. Frech, L. Dölken, M. Mann, and R. Lang. 2010. The phosphoproteome of tolllike receptor-activated macrophages. Mol. Syst. Biol. 6: 371.
47. Brzostek-Racine, S., C. Gordon, S. Van Scoy, and N. C. Reich. 2011. The DNA damage response induces IFN. J. Immunol. 187: 5336-5345.
48. Capasso, M., L. G. Durrant, M. Stacey, S. Gordon, J. Ramage, and I. Spendlove. 2006. Costimulation via CD55 on human CD4+ T cells mediated by CD97. J. Immunol. 177: 1070-1077.
49. Pandita, T. K., H. B. Lieberman, D. S. Lim, S. Dhar, W. Zheng, Y. Taya, and M. B. Kastan. 2000. Ionizing radiation activates the ATM kinase throughout the cell cycle. Oncogene 19: 1386-1391.
50. Canman, C. E., D. S. Lim, K. A. Cimprich, Y. Taya, K. Tamai, K. Sakaguchi, E. Appella, M. B. Kastan, and J. D. Siliciano. 1998. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281: 1677-1679.
51. He, L., S. O. Kim, O. Kwon, S. J. Jeong, M. S. Kim, H. G. Lee, H. Osada, M. Jung, J. S. Ahn, and B. Y. Kim. 2009. ATM blocks tunicamycin-induced endoplasmic reticulum stress. FEBS Lett. 583: 903-908.
52. Goodall, J. C., C. Wu, Y. Zhang, L. McNeill, L. Ellis, V. Saudek, and J. S. Gaston. 2010. Endoplasmic reticulum stress-induced transcription factor, CHOP, is crucial for dendritic cell IL-23 expression. Proc. Natl. Acad. Sci. USA 107: 17698-17703.
53. Derheimer, F. A., and M. B. Kastan. 2010. Multiple roles of ATM in monitoring and maintaining DNA integrity. FEBS Lett. 584: 3675-3681.
54. Guo, Z., S. Kozlov, M. F. Lavin, M. D. Person, and T. T. Paull. 2010. ATM activation by oxidative stress. Science 330: 517-521.
55. Guo, Z., R. Deshpande, and T. T. Paull. 2010. ATM activation in the presence of oxidative stress. Cell Cycle 9: 4805-4811.
56. Shao, L., H. Fujii, I. Colmegna, H. Oishi, J. J. Goronzy, and C. M. Weyand. 2009. Deficiency of the DNA repair enzyme ATM in rheumatoid arthritis. J. Exp. Med. 206: 1435-1449.
57. Hickson, I., Y. Zhao, C. J. Richardson, S. J. Green, N. M. Martin, A. I. Orr, P. M. Reaper, S. P. Jackson, N. J. Curtin, and G. C. Smith. 2004. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64: 9152-9159.
58. Eaton, J. S., Z. P. Lin, A. C. Sartorelli, N. D. Bonawitz, and G. S. Shadel. 2007. Ataxia-telangiectasia mutated kinase regulates ribonucleotide reductase and mitochondrial homeostasis. J. Clin. Invest. 117: 2723-2734.
59. Crescenzi, E., G. Palumbo, J. de Boer, and H. J. Brady. 2008. Ataxia telangiectasia mutated and p21CIP1 modulate cell survival of drug-induced senescent tumor cells: implications for chemotherapy. Clin. Cancer Res. 14: 1877-1887.
60. Liu, Y., K. R. Shreder, W. Gai, S. Corral, D. K. Ferris, and J. S. Rosenblum. 2005. Wortmannin, a widely used phosphoinositide 3-kinase inhibitor, also potently inhibits mammalian polo-like kinase. Chem. Biol. 12: 99-107.
61. Espinosa, A., V. Dardalhon, S. Brauner, A. Ambrosi, R. Higgs, F. J. Quintana, M. Sjöstrand, M. L. Eloranta, J. Ní Gabhann, O. Winqvist, et al. 2009. Loss of the lupus autoantigen Ro52/Trim21 induces tissue inflammation and systemic autoimmunity by disregulating the IL-23-Th17 pathway. J. Exp. Med. 206: 1661-1671.
62. Smith, S., J. N. Gabhann, R. Higgs, K. Stacey, M. Wahren-Herlenius, A. Espinosa, M. G. Totaro, A. Sica, E. Ball, A. Bell, et al. 2012. Enhanced interferon regulatory factor 3 binding to the interleukin-23p19 promoter correlates with enhanced interleukin-23 expression in systemic lupus erythematosus. Arthritis Rheum. 64: 1601-1609.
63. Higgs, R., J. Ní Gabhann, N. Ben Larbi, E. P. Breen, K. A. Fitzgerald, and C. A. Jefferies. 2008. The E3 ubiquitin ligase Ro52 negatively regulates IFNbeta production post-pathogen recognition by polyubiquitin-mediated degradation of IRF3. J. Immunol. 181: 1780-1786.
64. Yoneyama, M., M. Kikuchi, K. Matsumoto, T. Imaizumi, M. Miyagishi, K. Taira, E. Foy, Y. M. Loo, M. Gale, Jr., S. Akira, et al. 2005. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175: 2851-2858.
65. Alexopoulou, L., A. C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732-738.
66. Merrick, A., F. Errington, K. Milward, D. O'Donnell, K. Harrington, A. Bateman, H. Pandha, R. Vile, E. Morrison, P. Selby, and A. Melcher. 2005. Immunosuppressive effects of radiation on human dendritic cells: reduced IL-12 production on activation and impairment of naive T-cell priming. Br. J. Cancer 92: 1450-1458.
67. Cao, H., J. A. Robinson, Z. Jiang, J. S. Melville, S. P. Golovan, M. W. Jones, and A. M. Verrinder Gibbins. 2004. A high-resolution radiation hybrid map of porcine chromosome 6. Anim. Genet. 35: 367-378.
68. Li, Y., and D. Q. Yang. 2010. The ATM inhibitor KU-55933 suppresses cell proliferation and induces apoptosis by blocking Akt in cancer cells with overactivated Akt. Mol. Cancer Ther. 9: 113-125.
69. Yang, Y., F. Xia, N. Hermance, A. Mabb, S. Simonson, S. Morrissey, P. Gandhi, M. Munson, S. Miyamoto, and M. A. Kelliher. 2011. A cytosolic ATM/NEMO/RIP1 complex recruits TAK1 to mediate the NF-kappaB and p38 mitogenactivated protein kinase (MAPK)/MAPK-activated protein 2 responses to DNA damage. Mol. Cell. Biol. 31: 2774-2786.
70. Zeng, L., Y. P. Liu, H. Sha, H. Chen, L. Qi, and J. A. Smith. 2010. XBP-1 couples endoplasmic reticulum stress to augmented IFN-beta induction via a cis-acting enhancer in macrophages. J. Immunol. 185: 2324-2330.
71. Iwakoshi, N. N., M. Pypaert, and L. H. Glimcher. 2007. The transcription factor XBP-1 is essential for the development and survival of dendritic cells. J. Exp. Med. 204: 2267-2275.
72. Hirai, M., N. Kadowaki, T. Kitawaki, H. Fujita, A. Takaori-Kondo, R. Fukui, K. Miyake, T. Maeda, S. Kamihira, Y. Miyachi, and T. Uchiyama. 2011. Bortezomib suppresses function and survival of plasmacytoid dendritic cells by targeting intracellular trafficking of Toll-like receptors and endoplasmic reticulum homeostasis. Blood 117: 500-509.
73. DeLay, M. L., M. J. Turner, E. I. Klenk, J. A. Smith, D. P. Sowders, and R. A. Colbert. 2009. HLA-B27 misfolding and the unfolded protein response augment interleukin-23 production and are associated with Th17 activation in transgenic rats. Arthritis Rheum. 60: 2633-2643.
74. Back, S. H., M. Schröder, K. Lee, K. Zhang, and R. J. Kaufman. 2005. ER stress signaling by regulated splicing: IRE1/HAC1/XBP1. Methods 35: 395-416.
75. Bakkenist, C. J., and M. B. Kastan. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421: 499-506.