Tumor necrosis factor suppresses NR5A2 activity and intestinal glucocorticoid synthesis to sustain chronic colitis

Science Signaling

Volumn 7, Issue 314, 2014, Pages

  Huang, Sheng Chieh ^a,b   Lee, Cheng Tse ^a,c   Chung, Bon Chu ^a,b,c  

^a INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^b NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CYTOCHROME P450; CYTOCHROME P450 11B1; DEXTRAN SULFATE; GLUCOCORTICOID; I KAPPA B; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIVER RECEPTOR HOMOLOG 1; STRESS ACTIVATED PROTEIN KINASE 1; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CHRONIC INFLAMMATION; COLITIS; CONTROLLED STUDY; CORTICOSTERONE RELEASE; CRYPT CELL; CYTOKINE RELEASE; ENZYME ACTIVATION; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEROID RELEASE; STEROIDOGENESIS; SYNTHESIS; TH1 CELL; TH17 CELL;

ANIMALS; CELL LINE; CHOLESTEROL SIDE-CHAIN CLEAVAGE ENZYME; CHRONIC DISEASE; COLITIS; CORTICOSTERONE; DEXTRAN SULFATE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOCORTICOIDS; HUMANS; INTESTINES; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 8; NF-KAPPA B; RECEPTORS, CYTOPLASMIC AND NUCLEAR; STEROID 11-BETA-HYDROXYLASE; TH1 CELLS; TH17 CELLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84895463233     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2004786     Document Type: Article

References (61)

1. R. B. Sartor, Mechanisms of disease: Pathogenesis of Crohn's disease and ulcerative colitis. Nat. Clin. Pract. Gastroenterol. Hepatol. 3, 390-407 (2006). (Pubitemid 44018812)
2. W. Strober, I. Fuss, P. Mannon, The fundamental basis of inflammatory bowel disease. J. Clin. Invest. 117, 514-521 (2007). (Pubitemid 46348505)
3. R. J. Xavier, D. K. Podolsky, Unravelling the pathogenesis of inflammatory bowel disease. Nature 448, 427-434 (2007). (Pubitemid 47123518)
4. J. M. Reimund, J. Ratajczyk, B. Sola, A. M. Justum, C. D. Muller, Anti-tumor necrosis factor-alpha (TNF-a) treatment strategies in Crohn's disease. Recent Pat. Inflamm. Allergy Drug Discov. 1, 21-34 (2007).
5. J. R. Korzenik, D. K. Podolsky, Evolving knowledge and therapy of inflammatory bowel disease. Nat. Rev. Drug Discov. 5, 197-209 (2006). (Pubitemid 43336033)
6. J. I. Webster, L. Tonelli, E. M. Sternberg, Neuroendocrine regulation of immunity. Annu. Rev. Immunol. 20, 125-163 (2002). (Pubitemid 34295785)
7. M. S. Vacchio, V. Papadopoulos, J. D. Ashwell, Steroid production in the thymus: Implications for thymocyte selection. J. Exp. Med. 179, 1835-1846 (1994). (Pubitemid 24155664)
8. C. E. Gomez-Sanchez, M. Y. Zhou, E. N. Cozza, H. Morita, F. C. Eddleman, E. P. Gomez-Sanchez, Corticosteroid synthesis in the central nervous system. Endocr. Res. 22, 463-470 (1996). (Pubitemid 26424363)
9. I. Cima, N. Corazza, B. Dick, A. Fuhrer, S. Herren, S. Jakob, E. Ayuni, C. Mueller, T. Brunner, Intestinal epithelial cells synthesize glucocorticoids and regulate T cell activation. J. Exp. Med. 200, 1635-1646 (2004). (Pubitemid 40094187)
10. A. Coste, L. Dubuquoy, R. Barnouin, J. S. Annicotte, B. Magnier, M. Notti, N. Corazza, M. C. Antal, D. Metzger, P. Desreumaux, T. Brunner, J. Auwerx, K. Schoonjans, LRH-1-mediated glucocorticoid synthesis in enterocytes protects against inflammatory bowel disease. Proc. Natl. Acad. Sci. U.S.A. 104, 13098-13103 (2007). (Pubitemid 351737599)
11. K. L. Parker, B. P. Schimmer, Steroidogenic factor 1: A key determinant of endocrine development and function. Endocr. Rev. 18, 361-377 (1997). (Pubitemid 27246881)
12. E. R. Simpson, M. R. Waterman, Regulation of the synthesis of steroidogenic enzymes in adrenal cortical cells by ACTH. Annu. Rev. Physiol. 50, 427-440 (1988). (Pubitemid 18088114)
13. M. Mueller, I. Cima, M. Noti, A. Fuhrer, S. Jakob, L. Dubuquoy, K. Schoonjans, T. Brunner, The nuclear receptor LRH-1 critically regulates extra-adrenal glucocorticoid synthesis in the intestine. J. Exp. Med. 203, 2057-2062 (2006). (Pubitemid 44352227)
14. M. Mueller, A. Atanasov, I. Cima, N. Corazza, K. Schoonjans, T. Brunner, Differential regulation of glucocorticoid synthesis in murine intestinal epithelial versus adrenocortical cell lines. Endocrinology 148, 1445-1453 (2007).
15. M. Noti, N. Corazza, C. Mueller, B. Berger, T. Brunner, TNF suppresses acute intestinal inflammation by inducing local glucocorticoid synthesis. J. Exp. Med. 207, 1057-1066 (2010).
16. E. Fayard, J. Auwerx, K. Schoonjans, LRH-1: An orphan nuclear receptor involved in development, metabolism and steroidogenesis. Trends Cell Biol. 14, 250-260 (2004). (Pubitemid 38591329)
17. O. A. Botrugno, E. Fayard, J. S. Annicotte, C. Haby, T. Brennan, O. Wendling, T. Tanaka, T. Kodama, W. Thomas, J. Auwerx, K. Schoonjans, Synergy between LRH-1 and b-catenin induces G1 cyclin-mediated cell proliferation. Mol. Cell 15, 499-509 (2004). (Pubitemid 39141778)
18. H. Takedatsu, K. S. Michelsen, B. Wei, C. J. Landers, L. S. Thomas, D. Dhall, J. Braun, S. R. Targan, TL1A (TNFSF15) regulates the development of chronic colitis by modulating both T-helper 1 and T-helper 17 activation. Gastroenterology 135, 552-567 (2008).
19. Z. G. Liu, Molecular mechanism of TNF signaling and beyond. Cell Res. 15, 24-27 (2005).
20. I. C. Guo, C. Y. Huang, C. K. Wang, B. C. Chung, Activating protein-1 cooperates with steroidogenic factor-1 to regulate 3′,5′-cyclic adenosine 5′-monophosphatedependent human CYP11A1 transcription in vitro and in vivo. Endocrinology 148, 1804-1812 (2007).
21. J. Zalevsky, T. Secher, S. A. Ezhevsky, L. Janot, P. M. Steed, C. O'Brien, A. Eivazi, J. Kung, D. H. Nguyen, S. K. Doberstein, F. Erard, B. Ryffel, D. E. Szymkowski, Dominant-negative inhibitors of soluble TNF attenuate experimental arthritis without suppressing innate immunity to infection. J. Immunol. 179, 1872-1883 (2007).
22. A. K. Akobeng, M. Zachos, Tumor necrosis factor-alpha antibody for induction of remission in Crohn's disease. Cochrane Database Syst. Rev. CD003574 (2004).
23. L. Bertazza, S. Mocellin, The dual role of tumor necrosis factor (TNF) in cancer biology. Curr. Med. Chem. 17, 3337-3352 (2010).
24. S. R. Ruuls, R. M. Hoek, V. N. Ngo, T. McNeil, L. A. Lucian, M. J. Janatpour, H. Körner, H. Scheerens, E. M. Hessel, J. G. Cyster, L. M. McEvoy, J. D. Sedgwick, Membranebound TNF supports secondary lymphoid organ structure but is subservient to secreted TNF in driving autoimmune inflammation. Immunity 15, 533-543 (2001). (Pubitemid 33016439)
25. C. Mueller, N. Corazza, S. Trachsel-Løseth, H. P. Eugster, M. Bühler-Jungo, T. Brunner, M. A. Imboden, Noncleavable transmembrane mouse tumor necrosis factor-a (TNFa) mediates effects distinct from those of wild-type TNFa in vitro and in vivo. J. Biol. Chem. 274, 38112-38118 (1999). (Pubitemid 30026882)
26. A. E. Medvedev, T. Espevik, G. Ranges, A. Sundan, Distinct roles of the two tumor necrosis factor (TNF) receptors in modulating TNF and lymphotoxin a effects. J. Biol. Chem. 271, 9778-9784 (1996). (Pubitemid 26137389)
27. S. M. McFarlane, G. Pashmi, M. C. Connell, A. F. Littlejohn, S. J. Tucker, P. Vandenabeele, D. J. MacEwan, Differential activation of nuclear factor-kB by tumour necrosis factor receptor subtypes. TNFR1 predominates whereas TNFR2 activates transcription poorly. FEBS Lett. 515, 119-126 (2002). (Pubitemid 34273909)
28. E. Mizoguchi, A. Mizoguchi, H. Takedatsu, E. Cario, Y. P. de Jong, C. J. Ooi, R. J. Xavier, C. Terhorst, D. K. Podolsky, A. K. Bhan, Role of tumor necrosis factor receptor 2 (TNFR2) in colonic epithelial hyperplasia and chronic intestinal inflammation in mice. Gastroenterology 122, 134-144 (2002). (Pubitemid 34049202)
29. J. R. Bradley, TNF-mediated inflammatory disease. J. Pathol. 214, 149-160 (2008). (Pubitemid 351160153)
30. R. Stillie, A. W. Stadnyk, Role of TNF receptors, TNFR1 and TNFR2, in dextran sodium sulfate-induced colitis. Inflamm. Bowel Dis. 15, 1515-1525 (2009).
31. A. Lügering, P. Lebiedz, S. Koch, T. Kucharzik, Apoptosis as a therapeutic tool in IBD? Ann. N. Y. Acad. Sci. 1072, 62-77 (2006). (Pubitemid 44448444)
32. S. Danese, Mechanisms of action of infliximab in inflammatory bowel disease: An anti-inflammatory multitasker. Dig. Liver Dis. 40 (Suppl. 2), S225-S228 (2008). (Pubitemid 351878064)
33. R. Atreya, M. Zimmer, B. Bartsch, M. J. Waldner, I. Atreya, H. Neumann, K. Hildner, A. Hoffman, R. Kiesslich, A. D. Rink, T. T. Rau, S. Rose-John, H. Kessler, J. Schmidt, M. F. Neurath, Antibodies against tumor necrosis factor (TNF) induce T-cell apoptosis in patients with inflammatory bowel diseases via TNF receptor 2 and intestinal CD14+ macrophages. Gastroenterology 141, 2026-2038 (2011).
34. P. P. Tak, G. S. Firestein, NF-kB: A key role in inflammatory diseases. J. Clin. Invest. 107, 7-11 (2001). (Pubitemid 32047405)
35. P. K. Roy, F. Rashid, J. Bragg, J. A. Ibdah, Role of the JNK signal transduction pathway in inflammatory bowel disease. World J. Gastroenterol. 14, 200-202 (2008). (Pubitemid 351314299)
36. Z. Han, D. L. Boyle, L. Chang, B. Bennett, M. Karin, L. Yang, A. M. Manning, G. S. Firestein, c-Jun N-terminal kinase is required for metalloproteinase expression and joint destruction in inflammatory arthritis. J. Clin. Invest. 108, 73-81 (2001). (Pubitemid 32634924)
37. P. A. Baeuerle, The inducible transcription activator NF-kB: Regulation by distinct protein subunits. Biochim. Biophys. Acta 1072, 63-80 (1991). (Pubitemid 121007530)
38. W. Lee, P. Mitchell, R. Tjian, Purified transcription factor AP-1 interacts with TPAinducible enhancer elements. Cell 49, 741-752 (1987). (Pubitemid 18094764)
39. H. F. Yang-Yen, J. C. Chambard, Y. L. Sun, T. Smeal, T. J. Schmidt, J. Drouin, M. Karin, Transcriptional interference between c-Jun and the glucocorticoid receptor: Mutual inhibition of DNA binding due to direct protein-protein interaction. Cell 62, 1205-1215 (1990).
40. B. P. Ashburner, S. D. Westerheide, A. S. Baldwin Jr., The p65 (RelA) subunit of NF-kB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol. Cell. Biol. 21, 7065-7077 (2001). (Pubitemid 32916079)
41. M. C. Hu, N. C. Hsu, C. I. Pai, C. K. Wang, B. Chung, Functions of the upstream and proximal steroidogenic factor 1 (SF-1)-binding sites in the CYP11A1 promoter in basal transcription and hormonal response. Mol. Endocrinol. 15, 812-818 (2001). (Pubitemid 32411318)
42. S. R. Bornstein, H. Rutkowski, I. Vrezas, Cytokines and steroidogenesis. Mol. Cell. Endocrinol. 215, 135-141 (2004). (Pubitemid 38333252)
43. I. V. Mikhaylova, T. Kuulasmaa, J. Jääskeläinen, R. Voutilainen, Tumor necrosis factor-a regulates steroidogenesis, apoptosis, and cell viability in the human adrenocortical cell line NCI-H295R. Endocrinology 148, 386-392 (2007). (Pubitemid 46021471)
44. M. Jäättelä, V. Ilvesmäki, R. Voutilainen, U. H. Stenman, E. Saksela, Tumor necrosis factor as a potent inhibitor of adrenocorticotropin-induced cortisol production and steroidogenic P450 enzyme gene expression in cultured human fetal adrenal cells. Endocrinology 128, 623-629 (1991).
45. G. Darling, D. S. Goldstein, R. Stull, C. M. Gorschboth, J. A. Norton, Tumor necrosis factor: Immune endocrine interaction. Surgery 106, 1155-1160 (1989). (Pubitemid 20012396)
46. R. Natarajan, S. Ploszaj, R. Horton, J. Nadler, Tumor necrosis factor and interleukin-1 are potent inhibitors of angiotensin-II-induced aldosterone synthesis. Endocrinology 125, 3084-3089 (1989). (Pubitemid 20010686)
47. M. G. Swain, M. Maric, Tumor necrosis factor-alpha stimulates adrenal glucocorticoid secretion in cholestatic rats. Am. J. Physiol. 270, G987-G991 (1996).
48. H. C. Lan, H. J. Li, G. Lin, P. Y. Lai, B. C. Chung, Cyclic AMP stimulates SF-1-dependent CYP11A1 expression through homeodomain-interacting protein kinase 3-mediated Jun N-terminal kinase and c-Jun phosphorylation. Mol. Cell. Biol. 27, 2027-2036 (2007). (Pubitemid 46418461)
49. N. Sato, M. D. Sadar, N. Bruchovsky, F. Saatcioglu, P. S. Rennie, S. Sato, P. H. Lange, M. E. Gleave, Androgenic induction of prostate-specific antigen gene is repressed by protein-protein interaction between the androgen receptor and AP-1/c-Jun in the human prostate cancer cell line LNCaP. J. Biol. Chem. 272, 17485-17494 (1997). (Pubitemid 27311181)
50. M. Bens, A. Bogdanova, F. Cluzeaud, L. Miquerol, S. Kerneis, J. P. Kraehenbuhl, A. Kahn, E. Pringault, A. Vandewalle, Transimmortalized mouse intestinal cells (m-ICc12) that maintain a crypt phenotype. Am. J. Physiol. 270, C1666-C1674 (1996).
51. W. Y. Chen, L. J. Juan, B. C. Chung, SF-1 (nuclear receptor 5A1) activity is activated by cyclic AMP via p300-mediated recruitment to active foci, acetylation, and increased DNA binding. Mol. Cell. Biol. 25, 10442-10453 (2005).
52. F. Obermeier, N. Dunger, U. G. Strauch, N. Grunwald, H. Herfarth, J. Schölmerich, W. Falk, Contrasting activity of cytosin-guanosin dinucleotide oligonucleotides in mice with experimental colitis. Clin. Exp. Immunol. 134, 217-224 (2003). (Pubitemid 37372272)
53. L. Steidler, W. Hans, L. Schotte, S. Neirynck, F. Obermeier, W. Falk, W. Fiers, E. Remaut, Treatment of murine colitis by Lactococcus lactis secreting interleukin-10. Science 289, 1352-1355 (2000). (Pubitemid 30656052)
54. S. Yui, T. Nakamura, T. Sato, Y. Nemoto, T. Mizutani, X. Zheng, S. Ichinose, T. Nagaishi, R. Okamoto, K. Tsuchiya, H. Clevers, M. Watanabe, Functional engraftment of colon epithelium expanded in vitro from a single adult Lgr5+ stem cell. Nat. Med. 18, 618-623 (2012).
55. T. Sato, R. G. Vries, H. J. Snippert,M. van deWetering, N. Barker, D. E. Stange, J. H. van Es, A. Abo, P. Kujala, P. J. Peters, H. Clevers, Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459, 262-265 (2009).
56. C. Wang, B. L. Lin, The disappearance of an hsc70 species in mung bean seed during germination: Purification and characterization of the protein. Plant Mol. Biol. 21, 317-329 (1993).
57. M. C. Hu, S. J. Chou, Y. Y. Huang, N. C. Hsu, H. Li, B. C. Chung, Tissue-specific, hormonal, and developmental regulation of SCC-LacZ expression in transgenic mice leads to adrenocortical zone characterization. Endocrinology 140, 5609-5618 (1999). (Pubitemid 30645348)
58. C. Tournier, A. J. Whitmarsh, J. Cavanagh, T. Barrett, R. J. Davis, Mitogen-activated protein kinase kinase 7 is an activator of the c-Jun NH2-terminal kinase. Proc. Natl. Acad. Sci. U.S.A. 94, 7337-7342 (1997). (Pubitemid 27345316)
59. M. Treier, L. M. Staszewski, D. Bohmann, Ubiquitin-dependent c-Jun degradation in vivo is mediated by the d domain. Cell 78, 787-798 (1994). (Pubitemid 24294454)
60. M. D. Buzzelli, M. Nagarajan, J. F. Radtka, M. L. Shumate, M. Navaratnarajah, C. H. Lang, R. N. Cooney, Nuclear factor-kB mediates the inhibitory effects of tumor necrosis factor-a on growth hormone-inducible gene expression in liver. Endocrinology 149, 6378-6388 (2008).
61. B. M. Gummow, J. N. Winnay, G. D. Hammer, Convergence of Wnt signaling and steroidogenic factor-1 (SF-1) on transcription of the rat inhibin a gene. J. Biol. Chem. 278, 26572-26579 (2003). (Pubitemid 36876801)