Extra-adrenal glucocorticoid synthesis in the intestinal epithelium: More than a drop in the ocean?

Seminars in Immunopathology

Volumn 31, Issue 2, 2009, Pages 237-248

  Noti, Mario ^a   Sidler, Daniel ^a   Brunner, Thomas ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

Inflammatory bowel disease (IBD); Intestinal glucocorticoid synthesis; Intestinal immune homeostasis; Liver receptor homologue 1 (LRH 1); Tumor necrosis factor (TNF )

Indexed keywords

GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; HYDROCORTISONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIVER RECEPTOR HOMOLOG 1; STEROID RECEPTOR COACTIVATOR 1; TRANSCRIPTION FACTOR AP 1; TUMOR NECROSIS FACTOR ALPHA;

ADRENAL CORTEX; ADRENAL GLAND; ANTIINFLAMMATORY ACTIVITY; BRAIN; CARCINOGENESIS; CELL CYCLE; COLON CARCINOMA; DISEASE MODEL; ENTERITIS; HORMONE RELEASE; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INTESTINE EPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; REVIEW; SKIN; STEROIDOGENESIS; THYMUS; VASCULAR ENDOTHELIUM;

ADRENAL GLANDS; ANIMALS; GLUCOCORTICOIDS; HUMANS; INFLAMMATORY BOWEL DISEASES; INTESTINAL MUCOSA; ORGAN SPECIFICITY;

EID: 70349301389     PISSN: 18632297     EISSN: 18632300     Source Type: Journal    
DOI: 10.1007/s00281-009-0159-2     Document Type: Review

References (84)

1. I Takahashi H Kiyono 1999 Gut as the largest immunologic tissue JPEN J Parenter Enteral Nutr 23 S7 S12 doi: 10.1177/014860719902300107 10483885 doi: 10.1177/014860719902300107 1:CAS:528:DC%2BD3cXlvFGgtbc%3D
2. M Boirivant A Amendola A Butera 2008 Intestinal microflora and immunoregulation Mucosal Immunol 1 Suppl 1 S47 S49 doi: 10.1038/mi.2008.52 19079229 doi: 10.1038/mi.2008.52 1:CAS:528:DC%2BD1cXht1CmsLbP
3. MA McGuckin R Eri LA Simms TH Florin G Radford-Smith 2009 Intestinal barrier dysfunction in inflammatory bowel diseases Inflamm Bowel Dis 15 100 113 doi: 10.1002/ibd.20539 18623167 doi: 10.1002/ibd.20539
4. J Lee JM Gonzales-Navajas E Raz 2008 The "polarizing- tolerizing" mechanism of intestinal epithelium: its relevance to colonic homeostasis Semin Immunopathol 30 3 9 doi: 10.1007/s00281-007-0099-7 18026955 doi: 10.1007/s00281-007-0099-7 (Pubitemid 351178626)
5. JL Coombes F Powrie 2008 Dendritic cells in intestinal immune regulation Nat Rev Immunol 8 435 446 doi: 10.1038/nri2335 18500229 doi: 10.1038/nri2335 1:CAS:528:DC%2BD1cXmt1Ojt7w%3D (Pubitemid 351733420)
6. JG Magalhaes I Tattoli SE Girardin 2007 The intestinal epithelial barrier: how to distinguish between the microbial flora and pathogens Semin Immunol 19 106 115 doi: 10.1016/j.smim.2006.12.006 17324587 doi: 10.1016/j.smim.2006.12.006 1:CAS:528:DC%2BD2sXmtVOksr4%3D (Pubitemid 46810286)
7. AJ Macpherson 2006 IgA adaptation to the presence of commensal bacteria in the intestine Curr Top Microbiol Immunol 308 117 136 doi: 10.1007/3-540-30657-9-5 16922088 doi: 10.1007/3-540-30657-9-5 1:CAS:528:DC%2BD28XpvFelt74%3D
8. D Artis 2008 Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut Nat Rev Immunol 8 411 420 doi: 10.1038/nri2316 18469830 doi: 10.1038/nri2316 1:CAS:528:DC%2BD1cXmt1OjtrY%3D (Pubitemid 351733416)
9. D Kelly S Conway R Aminov 2005 Commensal gut bacteria: mechanisms of immune modulation Trends Immunol 26 326 333 doi: 10.1016/j.it.2005.04.008 15922949 doi: 10.1016/j.it.2005.04.008 1:CAS:528:DC%2BD2MXks1Wqu70%3D (Pubitemid 40732666)
10. JL Round SK Mazmanian 2009 The gut microbiota shapes intestinal immune responses during health and disease Nat Rev Immunol 9 5 313 23 19343057 doi: 10.1038/nri2515 1:CAS:528:DC%2BD1MXjvF2gtbk%3D
11. NH Salzman MA Underwood CL Bevins 2007 Paneth cells, defensins, and the commensal microbiota: a hypothesis on intimate interplay at the intestinal mucosa Semin Immunol 19 70 83 doi: 10.1016/j.smim.2007.04.002 17485224 doi: 10.1016/j.smim.2007.04.002 1:CAS:528:DC%2BD2sXmtVOksrs%3D (Pubitemid 46824070)
12. A Izcue JL Coombes F Powrie 2006 Regulatory T cells suppress systemic and mucosal immune activation to control intestinal inflammation Immunol Rev 212 256 271 doi: 10.1111/j.0105-2896.2006.00423.x 16903919 doi: 10.1111/j.0105-2896. 2006.00423.x 1:CAS:528:DC%2BD28XpvFegtLk%3D (Pubitemid 44116713)
13. C Becker MC Fantini MF Neurath 2006 TGF-beta as a T cell regulator in colitis and colon cancer Cytokine Growth Factor Rev 17 97 106 doi: 10.1016/j.cytogfr.2005.09.004 16298544 doi: 10.1016/j.cytogfr.2005.09.004 1:CAS:528:DC%2BD28Xos1Cruw%3D%3D (Pubitemid 43117519)
14. F Powrie R Correa-Oliveira S Mauze RL Coffman 1994 Regulatory interactions between CD45RBhigh and CD45RBlow CD4+ T cells are important for the balance between protective and pathogenic cell-mediated immunity J Exp Med 179 589 600 doi: 10.1084/jem.179.2.589 7905019 doi: 10.1084/jem.179.2.589 1:CAS:528:DyaK2cXhtVCltLw%3D
15. F Powrie MW Leach 1995 Genetic and spontaneous models of inflammatory bowel disease in rodents: evidence for abnormalities in mucosal immune regulation Ther Immunol 2 115 123 8729882 1:CAS:528:DyaK28XisVCnsLg%3D
16. I Cima N Corazza B Dick A Fuhrer S Herren S Jakob E Ayuni C Mueller T Brunner 2004 Intestinal epithelial cells synthesize glucocorticoids and regulate T cell activation J Exp Med 200 1635 1646 doi: 10.1084/jem.20031958 15596520 doi: 10.1084/jem.20031958 1:CAS:528:DC%2BD2cXhtFGmurbJ (Pubitemid 40094187)
17. C Cancedda G Filaci F Puppo M Ghio P Contini F Indiveri 2002 Immune homeostasis requires several biologic factors including glucocorticoid hormones Ann N Y Acad Sci 966 49 63 12114258 doi: 10.1111/j.1749-6632.2002.tb04201.x 1:CAS:528:DC%2BD38XlvVWmsbw%3D
18. BL Wajchenberg F Prestes Cesar H Okada I Torres de Toledo e Souza AC Lerario VC Borghi DA Malerbi A Giurna Filho B Liberman D Gianella 1984 Glucocorticoids, glucose metabolism and hypothalamic-pituitary-adrenal axis Adv Exp Med Biol 171 25 44 6372395 1:CAS:528:DyaL2cXktVWjs74%3D
19. M Berglund JA Thomas EH Hornquist OH Hultgren 2008 Toll-like receptor cross-hyporesponsiveness is functional in interleukin-1-receptor-associated kinase-1 (IRAK-1)-deficient macrophages: differential role played by IRAK-1 in regulation of tumour necrosis factor and interleukin-10 production Scand J Immunol 67 473 479 doi: 10.1111/j.1365-3083.2008.02096.x 18405325 doi: 10.1111/j.1365-3083.2008.02096.x 1:CAS:528:DC%2BD1cXmtFOgtL4%3D
20. M Beato P Herrlich G Schutz 1995 Steroid hormone receptors: many actors in search of a plot Cell 83 851 857 doi: 10.1016/0092-8674(95)90201-5 8521509 doi: 10.1016/0092-8674(95)90201-5 1:CAS:528:DyaK2MXhtVSnu7nL (Pubitemid 26006527)
21. JE Kunicka MA Talle GH Denhardt M Brown LA Prince G Goldstein 1993 Immunosuppression by glucocorticoids: inhibition of production of multiple lymphokines by in vivo administration of dexamethasone Cell Immunol 149 39 49 doi: 10.1006/cimm.1993.1134 8513511 doi: 10.1006/cimm.1993.1134 1:CAS:528:DyaK3sXks1entr4%3D
22. WY Almawi HN Beyhum AA Rahme MJ Rieder 1996 Regulation of cytokine and cytokine receptor expression by glucocorticoids J Leukoc Biol 60 563 572 8929546 1:CAS:528:DyaK28XntVCmt7k%3D
23. T Unlap RS Jope 1995 Inhibition of NFkB DNA binding activity by glucocorticoids in rat brain Neurosci Lett 198 41 44 doi: 10.1016/0304-3940(95) 11963-W 8570092 doi: 10.1016/0304-3940(95)11963-W 1:CAS:528:DyaK2MXosVOmtb4%3D
24. MJ Schaaf JA Cidlowski 2002 Molecular mechanisms of glucocorticoid action and resistance J Steroid Biochem Mol Biol 83 37 48 doi: 10.1016/S0960-0760(02) 00263-7 12650700 doi: 10.1016/S0960-0760(02)00263-7 1:CAS:528: DC%2BD3sXitFahsrw%3D (Pubitemid 37040640)
25. K De Bosscher W Vanden Berghe G Haegeman 2000 Mechanisms of anti-inflammatory action and of immunosuppression by glucocorticoids: negative interference of activated glucocorticoid receptor with transcription factors J Neuroimmunol 109 16 22 doi: 10.1016/S0165-5728(00)00297-6 10969176 doi: 10.1016/S0165-5728(00)00297-6 (Pubitemid 30676418)
26. RI Scheinman A Gualberto CM Jewell JA Cidlowski AS Baldwin Jr 1995 Characterization of mechanisms involved in transrepression of NF-kappa B by activated glucocorticoid receptors Mol Cell Biol 15 943 953 7823959 1:CAS:528:DyaK2MXjtlant70%3D
27. M Karin 1998 New twists in gene regulation by glucocorticoid receptor: is DNA binding dispensable? Cell 93 487 490 doi: 10.1016/S0092-8674(00)81177-0 9604923 doi: 10.1016/S0092-8674(00)81177-0 1:CAS:528:DyaK1cXjsFWhsr8%3D (Pubitemid 28240709)
28. A Amsterdam K Tajima R Sasson 2002 Cell-specific regulation of apoptosis by glucocorticoids: implication to their anti-inflammatory action Biochem Pharmacol 64 843 850 doi: 10.1016/S0006-2952(02)01147-4 12213578 doi: 10.1016/S0006-2952(02)01147-4 1:CAS:528:DC%2BD38Xms1ymsrk%3D (Pubitemid 35232258)
29. A Amsterdam R Sasson 2002 The anti-inflammatory action of glucocorticoids is mediated by cell type specific regulation of apoptosis Mol Cell Endocrinol 189 1 9 doi: 10.1016/S0303-7207(01)00722-5 12039060 doi: 10.1016/S0303-7207(01) 00722-5 1:CAS:528:DC%2BD38XitlaqsLY%3D (Pubitemid 34229159)
30. D Iglesias-Serret M de Frias AF Santidrian L Coll-Mulet AM Cosialls M Barragan A Domingo J Gil G Pons 2007 Regulation of the proapoptotic BH3-only protein BIM by glucocorticoids, survival signals and proteasome in chronic lymphocytic leukemia cells Leukemia 21 281 287 doi: 10.1038/sj.leu.2404483 17151701 doi: 10.1038/sj.leu.2404483 1:CAS:528:DC%2BD2sXotFGqsg%3D%3D (Pubitemid 46158121)
31. M Erlacher EM Michalak PN Kelly V Labi H Niederegger L Coultas JM Adams A Strasser A Villunger 2005 BH3-only proteins Puma and Bim are rate-limiting for gamma-radiation- and glucocorticoid-induced apoptosis of lymphoid cells in vivo Blood 106 4131 4138 doi: 10.1182/blood-2005-04-1595 16118324 doi: 10.1182/blood-2005-04-1595 1:CAS:528:DC%2BD2MXhtlaltr3O (Pubitemid 41775918)
32. Z Wang MH Malone H He KS McColl CW Distelhorst 2003 Microarray analysis uncovers the induction of the proapoptotic BH3-only protein Bim in multiple models of glucocorticoid-induced apoptosis J Biol Chem 278 23861 23867 doi: 10.1074/jbc.M301843200 12676946 doi: 10.1074/jbc.M301843200 1:CAS:528: DC%2BD3sXkslygur8%3D (Pubitemid 36830212)
33. TR Cupps AS Fauci 1982 Corticosteroid-mediated immunoregulation in man Immunol Rev 65 133 155 doi: 10.1111/j.1600-065X.1982.tb00431.x 6214495 doi: 10.1111/j.1600-065X.1982.tb00431.x 1:STN:280:DyaL3s%2FgsFGjsg%3D%3D
34. M Perretti F D'Acquisto 2009 Annexin A1 and glucocorticoids as effectors of the resolution of inflammation Nat Rev Immunol 9 62 70 doi: 10.1038/nri2470 19104500 doi: 10.1038/nri2470 1:CAS:528:DC%2BD1cXhsFartbzP
35. DB Kaufman R Shapiro MR Lucey WS Cherikh RT Bustami DB Dyke 2004 Immunosuppression: practice and trends Am J Transplant 4 Suppl 9 38 53 doi: 10.1111/j.1600-6135.2004.00397.x 15113354 doi: 10.1111/j.1600-6135.2004.00397.x (Pubitemid 38858994)
36. O Di Munno A Delle Sedie 2008 Effects of glucocorticoid treatment on focal and systemic bone loss in rheumatoid arthritis J Endocrinol Invest 31 43 47 18791351
37. ER Simpson 1979 Cholesterol side-chain cleavage, cytochrome P450, and the control of steroidogenesis Mol Cell Endocrinol 13 213 227 doi: 10.1016/0303-7207(79)90082-0 221289 doi: 10.1016/0303-7207(79)90082-0 1:CAS:528:DyaE1MXksV2ksr4%3D
38. SR Bornstein M Ehrhart-Bornstein 2000 Basic and clinical aspects of intraadrenal regulation of steroidogenesis Z Rheumatol 59 Suppl 2: II 12 17
39. W Wang C Zhang A Marimuthu HI Krupka M Tabrizizad R Shelloe U Mehra K Eng H Nguyen C Settachatgul B Powell MV Milburn BL West 2005 The crystal structures of human steroidogenic factor-1 and liver receptor homologue-1 Proc Natl Acad Sci U S A 102 7505 7510 doi: 10.1073/pnas.0409482102 15897460 doi: 10.1073/pnas.0409482102 1:CAS:528:DC%2BD2MXkslOntL0%3D (Pubitemid 40741001)
40. W Arlt PM Stewart 2005 Adrenal corticosteroid biosynthesis, metabolism, and action Endocrinol Metab Clin North Am 34 293 313 doi: 10.1016/j.ecl.2005.01. 002 15850843 doi: 10.1016/j.ecl.2005.01.002 1:CAS:528:DC%2BD2MXltlOmsL0%3D viii (Pubitemid 40602722)
41. JC Buckingham 2006 Glucocorticoids: exemplars of multi-tasking Br J Pharmacol 147 Suppl 1 S258 S268 doi: 10.1038/sj.bjp. 0706456 16402112 doi: 10.1038/sj.bjp.0706456 1:CAS:528:DC%2BD28XisVClsw%3D%3D
42. S Meeking 2007 Treatment of acute adrenal insufficiency Clin Tech Small Anim Pract 22 36 39 doi: 10.1053/j.ctsap. 2007.02.006 17542196 doi: 10.1053/j.ctsap.2007.02.006
43. JA Gonzalo A Gonzalez-Garcia C Martinez G Kroemer 1993 Glucocorticoid-mediated control of the activation and clonal deletion of peripheral T cells in vivo J Exp Med 177 1239 1246 doi: 10.1084/jem.177.5.1239 8478606 doi: 10.1084/jem.177.5.1239 1:CAS:528:DyaK3sXitVGms7s%3D
44. AH Payne DB Hales 2004 Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones Endocr Rev 25 947 970 doi: 10.1210/er.2003-0030 15583024 doi: 10.1210/er.2003-0030 1:CAS:528: DC%2BD2MXjslWntg%3D%3D (Pubitemid 39657774)
45. D Annane 2005 Glucocorticoids in the treatment of severe sepsis and septic shock Curr Opin Crit Care 11 449 453 doi: 10.1097/01.ccx.0000176691. 95562.43 16175031 doi: 10.1097/01.ccx.0000176691.95562.43 (Pubitemid 41482700)
46. MS Vacchio JD Ashwell 1997 Thymus-derived glucocorticoids regulate antigen-specific positive selection J Exp Med 185 2033 2038 doi: 10.1084/jem.185.11.2033 9166432 doi: 10.1084/jem.185.11.2033 1:CAS:528:DyaK2sXjsF2gt7g%3D (Pubitemid 27247089)
47. MS Vacchio JY Lee JD Ashwell 1999 Thymus-derived glucocorticoids set the thresholds for thymocyte selection by inhibiting TCR-mediated thymocyte activation J Immunol 163 1327 1333 10415031 1:CAS:528:DyaK1MXkslOhu7c%3D
48. Lechner O, Wiegers GJ, Oliveira-Dos-Santos AJ, Dietrich H, Recheis H, Waterman M, Boyd R, Wick G 2000 Glucocorticoid production in the murine thymus Eur J Immunol 30 337 346 doi: 10.1002/1521-4141(200002)30:2<337::AID- IMMU337>3.0.CO;2-L (Pubitemid 30098825)
49. A Pazirandeh Y Xue I Rafter J Sjovall M Jondal S Okret 1999 Paracrine glucocorticoid activity produced by mouse thymic epithelial cells FASEB J 13 893 901 10224232 1:CAS:528:DyaK1MXjtFGks7s%3D
50. E Davies SM MacKenzie 2003 Extra-adrenal production of corticosteroids Clin Exp Pharmacol Physiol 30 437 445 doi: 10.1046/j.1440-1681.2003.03867.x 12823256 doi: 10.1046/j.1440-1681.2003.03867.x 1:CAS:528:DC%2BD3sXls1KrtLs%3D (Pubitemid 36836558)
51. Keeney DS, Jenkins CM, Waterman MR 1995 Developmentally regulated expression of adrenal 17 alpha-hydroxylase cytochrome P450 in the mouse embryo Endocrinology 136 4872 4879 doi: 10.1210/en.136.11.4872 doi: 10.1210/en.136.11.4872
52. T Brunner D Arnold C Wasem S Herren C Frutschi 2001 Regulation of cell death and survival in intestinal intraepithelial lymphocytes Cell Death Differ 8 706 714 doi: 10.1038/sj.cdd.4400854 11464215 doi: 10.1038/sj.cdd.4400854 1:CAS:528:DC%2BD3MXlvVKgsLo%3D (Pubitemid 32685168)
53. AG Atanasov D Leiser C Roesselet M Noti N Corazza K Schoonjans T Brunner 2008 Cell cycle-dependent regulation of extra-adrenal glucocorticoid synthesis in murine intestinal epithelial cells FASEB J 22 4117 4125 doi: 10.1096/fj.08-114157 18711026 doi: 10.1096/fj.08-114157 1:CAS:528: DC%2BD1cXhsVKgu77O
54. M Mueller I Cima M Noti A Fuhrer S Jakob L Dubuquoy K Schoonjans T Brunner 2006 The nuclear receptor LRH-1 critically regulates extra-adrenal glucocorticoid synthesis in the intestine J Exp Med 203 2057 2062 doi: 10.1084/jem.20060357 16923850 doi: 10.1084/jem.20060357 1:CAS:528: DC%2BD28XptlSgs74%3D (Pubitemid 44352227)
55. M Mueller A Atanasov I Cima N Corazza K Schoonjans T Brunner 2007 Differential regulation of glucocorticoid synthesis in murine intestinal epithelial versus adrenocortical cell lines Endocrinology 148 1445 1453 doi: 10.1210/en.2006-0591 17170096 doi: 10.1210/en.2006-0591 1:CAS:528: DC%2BD2sXitlWnt7w%3D (Pubitemid 46272831)
56. P Val AM Lefrancois-Martinez G Veyssiere A Martinez 2003 SF-1 a key player in the development and differentiation of steroidogenic tissues Nucl Recept 1 8 doi: 10.1186/1478-1336-1-8 14594453 doi: 10.1186/1478-1336-1-8 (Pubitemid 39130372)
57. ML Bland CA Jamieson SF Akana SR Bornstein G Eisenhofer MF Dallman HA Ingraham 2000 Haploinsufficiency of steroidogenic factor-1 in mice disrupts adrenal development leading to an impaired stress response Proc Natl Acad Sci U S A 97 14488 14493 doi: 10.1073/pnas.97.26.14488 11121051 doi: 10.1073/pnas.97.26.14488 1:CAS:528:DC%2BD3MXitVCqtw%3D%3D (Pubitemid 32016603)
58. E Fayard J Auwerx K Schoonjans 2004 LRH-1: an orphan nuclear receptor involved in development, metabolism and steroidogenesis Trends Cell Biol 14 250 260 doi: 10.1016/j.tcb.2004.03.008 15130581 doi: 10.1016/j.tcb.2004.03.008 1:CAS:528:DC%2BD2cXjvVemu74%3D (Pubitemid 38591329)
59. D Saxena R Escamilla-Hernandez L Little-Ihrig AJ Zeleznik 2007 Liver receptor homolog-1 and steroidogenic factor-1 have similar actions on rat granulosa cell steroidogenesis Endocrinology 148 726 734 doi: 10.1210/en.2006-0108 17095585 doi: 10.1210/en.2006-0108 1:CAS:528: DC%2BD2sXhtlOjtLw%3D (Pubitemid 46150778)
60. C Labelle-Dumais M Jacob-Wagner JF Pare L Belanger D Dufort 2006 Nuclear receptor NR5A2 is required for proper primitive streak morphogenesis Dev Dyn 235 3359 3369 doi: 10.1002/dvdy.20996 17075876 doi: 10.1002/dvdy.20996 1:CAS:528:DC%2BD2sXmsVWitA%3D%3D (Pubitemid 44888201)
61. A Coste L Dubuquoy R Barnouin JS Annicotte B Magnier M Notti N Corazza MC Antal D Metzger P Desreumaux T Brunner J Auwerx K Schoonjans 2007 LRH-1-mediated glucocorticoid synthesis in enterocytes protects against inflammatory bowel disease Proc Natl Acad Sci U S A 104 13098 13103 doi: 10.1073/pnas.0702440104 17670946 doi: 10.1073/pnas.0702440104 1:CAS:528:DC%2BD2sXpt1GgsL4%3D (Pubitemid 351737599)
62. MA Boivin D Ye JC Kennedy R Al-Sadi C Shepela TY Ma 2007 Mechanism of glucocorticoid regulation of the intestinal tight junction barrier Am J Physiol Gastrointest Liver Physiol 292 G590 G598 doi: 10.1152/ajpgi.00252.2006 17068119 doi: 10.1152/ajpgi.00252.2006 1:CAS:528:DC%2BD2sXjt1Glt70%3D (Pubitemid 46263506)
63. N Harke J Leers S Kietz D Drenckhahn C Forster 2008 Glucocorticoids regulate the human occludin gene through a single imperfect palindromic glucocorticoid response element Mol Cell Endocrinol 295 39 47 doi: 10.1016/j.mce.2008.08.011 18782596 doi: 10.1016/j.mce.2008.08.011 1:CAS:528:DC%2BD1cXhtlaltbnL
64. T Kimura 1986 Transduction of ACTH signal from plasma membrane to mitochondria in adrenocortical steroidogenesis. Effects of peptide, phospholipid, and calcium J Steroid Biochem 25 711 716 doi: 10.1016/0022- 4731(86)90299-2 3027455 doi: 10.1016/0022-4731(86)90299-2 1:CAS:528: DyaL2sXnvVOqtw%3D%3D (Pubitemid 17227948)
65. N Watanabe H Inoue Y Fujii-Kuriyama 1994 Regulatory mechanisms of cAMP-dependent and cell-specific expression of human steroidogenic cytochrome P450scc (CYP11A1) gene Eur J Biochem 222 825 834 doi: 10.1111/j.1432-1033.1994. tb18929.x 8026494 doi: 10.1111/j.1432-1033.1994.tb18929.x 1:CAS:528: DyaK2cXlt1Kku7k%3D (Pubitemid 24212295)
66. D Rosenberg L Groussin X Bertagna J Bertherat 2002 cAMP pathway alterations from the cell surface to the nucleus in adrenocortical tumors Endocr Res 28 765 775 doi: 10.1081/ERC-120017071 12530696 doi: 10.1081/ERC-120017071 1:CAS:528:DC%2BD3sXhtVSgtb0%3D (Pubitemid 36050044)
67. S Burendahl E Treuter L Nilsson 2008 Molecular dynamics simulations of human LRH-1: the impact of ligand binding in a constitutively active nuclear receptor Biochemistry 47 5205 5215 doi: 10.1021/bi7025084 18410128 doi: 10.1021/bi7025084 1:CAS:528:DC%2BD1cXks1Wntrc%3D (Pubitemid 351620757)
68. YS Kim JH Ryu SJ Han KH Choi KB Nam IH Jang B Lemaitre PT Brey WJ Lee 2000 Gram-negative bacteria-binding protein, a pattern recognition receptor for lipopolysaccharide and beta-1, 3-glucan that mediates the signaling for the induction of innate immune genes in Drosophila melanogaster cells J Biol Chem 275 32721 32727 doi: 10.1074/jbc.M003934200 10827089 doi: 10.1074/jbc.M003934200 1:CAS:528:DC%2BD3cXnslOitbg%3D
69. YK Lee YH Choi S Chua YJ Park DD Moore 2006 Phosphorylation of the hinge domain of the nuclear hormone receptor LRH-1 stimulates transactivation J Biol Chem 281 7850 7855 doi: 10.1074/jbc.M509115200 16439367 doi: 10.1074/jbc.M509115200 1:CAS:528:DC%2BD28Xitl2kt7w%3D (Pubitemid 43847400)
70. OA Botrugno E Fayard JS Annicotte C Haby T Brennan O Wendling T Tanaka T Kodama W Thomas J Auwerx K Schoonjans 2004 Synergy between LRH-1 and beta-catenin induces G1 cyclin-mediated cell proliferation Mol Cell 15 499 509 doi: 10.1016/j.molcel.2004.07.009 15327767 doi: 10.1016/j.molcel.2004.07.009 1:CAS:528:DC%2BD2cXns1ynurs%3D (Pubitemid 39141778)
71. K Schoonjans L Dubuquoy J Mebis E Fayard O Wendling C Haby K Geboes J Auwerx 2005 Liver receptor homolog 1 contributes to intestinal tumor formation through effects on cell cycle and inflammation Proc Natl Acad Sci U S A 102 2058 2062 doi: 10.1073/pnas.0409756102 15684064 doi: 10.1073/pnas.0409756102 1:CAS:528:DC%2BD2MXhvFGru7Y%3D (Pubitemid 40262011)
72. P Rutgeerts 1998 Medical therapy of inflammatory bowel disease Digestion 59 453 469 doi: 10.1159/000007523 9705531 doi: 10.1159/000007523 1:CAS:528:DyaK1cXlsVyks74%3D (Pubitemid 28375571)
73. A Cerny FV Chisari 1999 Pathogenesis of chronic hepatitis C: immunological features of hepatic injury and viral persistence Hepatology 30 595 601 doi: 10.1002/hep. 510300312 10462362 doi: 10.1002/hep.510300312 1:STN:280:DyaK1MzptFOktg%3D%3D
74. G Van Assche S Vermeire P Rutgeerts 2008 Optimizing treatment of inflammatory bowel diseases with biologic agents Curr Gastroenterol Rep 10 591 596 doi: 10.1007/s11894-008-0107-7 19006616 doi: 10.1007/s11894-008-0107-7
75. MF Neurath I Fuss M Pasparakis L Alexopoulou S Haralambous KH Meyer zum Buschenfelde W Strober G Kollias 1997 Predominant pathogenic role of tumor necrosis factor in experimental colitis in mice Eur J Immunol 27 1743 1750 doi: 10.1002/eji.1830270722 9247586 doi: 10.1002/eji.1830270722 1:CAS:528: DyaK2sXks1CltL4%3D (Pubitemid 27302858)
76. Y Naito T Takagi O Handa T Ishikawa S Nakagawa T Yamaguchi N Yoshida M Minami M Kita J Imanishi T Yoshikawa 2003 Enhanced intestinal inflammation induced by dextran sulfate sodium in tumor necrosis factor-alpha deficient mice J Gastroenterol Hepatol 18 560 569 doi: 10.1046/j.1440-1746.2003.03034.x 12702049 doi: 10.1046/j.1440-1746.2003.03034.x 1:CAS:528:DC%2BD3sXkslyjtLo%3D (Pubitemid 36645291)
77. DR Ebach R Newberry WF Stenson 2005 Differential role of tumor necrosis factor receptors in TNBS colitis Inflamm Bowel Dis 11 533 540 doi: 10.1097/01.MIB.0000163698.34592.30 15905700 doi: 10.1097/01.MIB.0000163698. 34592.30 (Pubitemid 40826340)
78. P Rutgeerts S Vermeire G Van Assche 2009 Biological therapies for inflammatory bowel diseases Gastroenterology 136 1182 1197 doi: 10.1053/j.gastro.2009.02.001 19249397 doi: 10.1053/j.gastro.2009.02.001 1:CAS:528:DC%2BD1MXkslWgsbw%3D
79. G Kassiotis G Kollias 2001 Uncoupling the proinflammatory from the immunosuppressive properties of tumor necrosis factor (TNF) at the p55 TNF receptor level: implications for pathogenesis and therapy of autoimmune demyelination J Exp Med 193 427 434 doi: 10.1084/jem.193.4.427 11181695 doi: 10.1084/jem.193.4.427 1:CAS:528:DC%2BD3MXhtlGmtLc%3D (Pubitemid 32524474)
80. L Zheng G Fisher RE Miller J Peschon DH Lynch MJ Lenardo 1995 Induction of apoptosis in mature T cells by tumour necrosis factor Nature 377 348 351 doi: 10.1038/377348a0 7566090
81. T Zhou CK Edwards III P Yang Z Wang H Bluethmann JD Mountz 1996 Greatly accelerated lymphadenopathy and autoimmune disease in lpr mice lacking tumor necrosis factor receptor I J Immunol 156 2661 2665 8609380 1:CAS:528: DyaK28Xit1eitrk%3D (Pubitemid 126660608)
82. P Matthys A Billiau 1997 Cytokines and cachexia Nutrition 13 763 770 doi: 10.1016/S0899-9007(97)00185-8 9290087 doi: 10.1016/S0899-9007(97)00185-8 1:CAS:528:DyaK2sXmt1SrsL0%3D (Pubitemid 27382443)
83. DR Clayburgh TA Barrett Y Tang JB Meddings LJ Van Eldik DM Watterson LL Clarke RJ Mrsny JR Turner 2005 Epithelial myosin light chain kinase-dependent barrier dysfunction mediates T cell activation-induced diarrhea in vivo J Clin Invest 115 2702 2715 doi: 10.1172/JCI24970 16184195 doi: 10.1172/JCI24970 1:CAS:528:DC%2BD2MXhtVygt7nN (Pubitemid 41434398)
84. EM Rubin VD Raptopoulos 2005 Images in clinical medicine. The virtual apple core of a colonic carcinoma N Engl J Med 352 2733 doi: 10.1056/NEJMicm040235 15987922 doi: 10.1056/NEJMicm040235 1:CAS:528: DC%2BD2MXls1Sktb8%3D (Pubitemid 41007828)