Intestinal steroidogenesis

Steroids

Volumn 103, Issue , 2015, Pages 64-71

  Bouguen, Guillaume ^a,b,c   Dubuquoy, Laurent ^d,e   Desreumaux, Pierre ^d,e,f   Brunner, Thomas ^g   Bertin, Benjamin ^d,e  

^a PONTCHAILLOU UNIVERSITY HOSPITAL   (France)

^b Univ Rennes   (France)

^c UNIVERSITÉ DE RENNES 1   (France)

^d UNIV LILLE   (France)

^e UNIVERSITÉ DE LILLE   (France)

^f LILLE UNIVERSITY HOSPITAL   (France)

^g UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Colorectal cancer; Glucocorticoids; Inflammatory bowel diseases; Intestinal epithelial cells; Intestinal steroidogenesis; Liver receptor homolog 1

Indexed keywords

LIVER RECEPTOR HOMOLOG 1; STEROIDOGENIC FACTOR 1; STEROID;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; COLORECTAL CANCER; DENDRITIC CELL; DOWN REGULATION; ESTROGEN METABOLISM; EX VIVO STUDY; HUMAN; IMMUNOSTIMULATION; INFLAMMATORY BOWEL DISEASE; INTESTINE EPITHELIUM CELL; INTESTINE FUNCTION; NONHUMAN; PROTEIN EXPRESSION; REGULATORY MECHANISM; SMALL INTESTINAL TISSUE; STEROID METABOLISM; STEROIDOGENESIS; THIN LAYER CHROMATOGRAPHY; ANIMAL; BIOSYNTHESIS; CYTOLOGY; INTESTINE; METABOLISM;

ANIMALS; HUMANS; INTESTINES; STEROIDS;

EID: 84938873923     PISSN: 0039128X     EISSN: 18785867     Source Type: Journal    
DOI: 10.1016/j.steroids.2014.12.022     Document Type: Review

References (98)

1. P.J. Sansonetti War and peace at mucosal surfaces Nat Rev Immunol 4 2004 953 964
2. J. Walter, and R. Ley The human gut microbiome: ecology and recent evolutionary changes Annu Rev Microbiol 65 2011 411 429
3. N. Kamada, S.U. Seo, G.Y. Chen, and G. Nunez Role of the gut microbiota in immunity and inflammatory disease Nat Rev Immunol 13 2013 321 335
4. K.J. Maloy, and F. Powrie Intestinal homeostasis and its breakdown in inflammatory bowel disease Nature 474 2011 298 306
5. L.W. Peterson, and D. Artis Intestinal epithelial cells: regulators of barrier function and immune homeostasis Nat Rev Immunol 14 2014 141 153
6. Y. Goto, and I.I. Ivanov Intestinal epithelial cells as mediators of the commensal-host immune crosstalk Immunol Cell Biol 91 2013 204 214
7. M. Rimoldi, M. Chieppa, V. Salucci, F. Avogadri, A. Sonzogni, G.M. Sampietro, and et al. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells Nat Immunol 6 2005 507 514
8. I.D. Iliev, E. Mileti, G. Matteoli, M. Chieppa, and M. Rescigno Intestinal epithelial cells promote colitis-protective regulatory T-cell differentiation through dendritic cell conditioning Mucosal Immunol 2 2009 340 350
9. I.D. Iliev, I. Spadoni, E. Mileti, G. Matteoli, A. Sonzogni, G.M. Sampietro, and et al. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells Gut 58 2009 1481 1489
10. M.S. Vacchio, V. Papadopoulos, and J.D. Ashwell Steroid production in the thymus: implications for thymocyte selection J Exp Med 179 1994 1835 1846
11. A. Pazirandeh, Y. Xue, I. Rafter, J. Sjovall, M. Jondal, and S. Okret Paracrine glucocorticoid activity produced by mouse thymic epithelial cells Faseb J 13 1999 893 901
12. O. Lechner, G.J. Wiegers, A.J. Oliveira-Dos-Santos, H. Dietrich, H. Recheis, M. Waterman, and et al. Glucocorticoid production in the murine thymus Eur J Immunol 30 2000 337 346
13. D. Thiboutot, S. Jabara, J.M. McAllister, A. Sivarajah, K. Gilliland, Z. Cong, and et al. Human skin is a steroidogenic tissue: steroidogenic enzymes and cofactors are expressed in epidermis, normal sebocytes, and an immortalized sebocyte cell line (SEB-1) J Invest Dermatol 120 2003 905 914
14. C.E. Gomez-Sanchez, M.Y. Zhou, E.N. Cozza, H. Morita, F.C. Eddleman, and E.P. Gomez-Sanchez Corticosteroid synthesis in the central nervous system Endocr Res 22 1996 463 470
15. A.P. Croft, M.J. O'Callaghan, S.G. Shaw, G. Connolly, C. Jacquot, and H.J. Little Effects of minor laboratory procedures, adrenalectomy, social defeat or acute alcohol on regional brain concentrations of corticosterone Brain Res 1238 2008 12 22
16. H.J. Little, A.P. Croft, M.J. O'Callaghan, S.P. Brooks, G. Wang, and S.G. Shaw Selective increases in regional brain glucocorticoid: a novel effect of chronic alcohol Neuroscience 156 2008 1017 1027
17. I. Cima, N. Corazza, B. Dick, A. Fuhrer, S. Herren, S. Jakob, and et al. Intestinal epithelial cells synthesize glucocorticoids and regulate T cell activation J Exp Med 200 2004 1635 1646
18. D. Sidler, P. Renzulli, C. Schnoz, B. Berger, S. Schneider-Jakob, C. Fluck, and et al. Colon cancer cells produce immunoregulatory glucocorticoids Oncogene 30 2011 2411 2419
19. Bouguen G, Langlois A, Djouina M, Branche J, Koriche D, Dewaeles E, et al. Intestinal steroidogenesis controls PPARgamma expression in the colon and is impaired during UC. Gut. Published on line first 2014 july 22.
20. N. Hostettler, P. Bianchi, C. Gennari-Moser, D. Kassahn, K. Schoonjans, N. Corazza, and et al. Local glucocorticoid production in the mouse lung is induced by immune cell stimulation Allergy 67 2012 227 234
21. L. Dalla Valle, P. Belvedere, C. Simontacchi, and L. Colombo Extraglandular hormonal steroidogenesis rats J Steroid Biochem Mol Biol 43 1992 1095 1098
22. L. Dalla Valle, J. Couet, Y. Labrie, J. Simard, P. Belvedere, C. Simontacchi, and et al. Occurrence of cytochrome P450c17 mRNA and dehydroepiandrosterone biosynthesis in the rat gastrointestinal tract Mol Cell Endocrinol 111 1995 83 92
23. S. Vianello, M.R. Waterman, L. Dalla Valle, and L. Colombo Developmentally regulated expression and activity of 17alpha-hydroxylase/C-17,20-lyase cytochrome P450 in rat liver Endocrinology 138 1997 3166 3174
24. D.S. Keeney, Y. Ikeda, M.R. Waterman, and K.L. Parker Cholesterol side-chain cleavage cytochrome P450 gene expression in the primitive gut of the mouse embryo does not require steroidogenic factor 1 Mol Endocrinol 9 1995 1091 1098
25. J. Pacha, and I. Miksik Distribution of 11 beta-hydroxysteroid dehydrogenase along the rat intestine Life Sci 54 1994 745 749
26. C.B. Whorwood, M.L. Ricketts, and P.M. Stewart Epithelial cell localization of type 2 11 beta-hydroxysteroid dehydrogenase in rat and human colon Endocrinology 135 1994 2533 2541
27. P. Belvedere, L. Dalla Valle, S. Vianello, O. Carnevali, and L. Colombo Hormonal steroidogenesis in liver and small intestine of the green frog, Rana esculenta L. Life Sci 69 2001 2921 2930
28. Y. Wang, and W. Ge Cloning of zebrafish ovarian P450c17 (CYP17, 17alpha-hydroxylase/17,20-lyase) and characterization of its expression in gonadal and extra-gonadal tissues Gen Comp Endocrinol 135 2004 241 249
29. A. Coste, L. Dubuquoy, R. Barnouin, J.S. Annicotte, B. Magnier, M. Notti, and et al. LRH-1-mediated glucocorticoid synthesis in enterocytes protects against inflammatory bowel disease Proc Natl Acad Sci USA 104 2007 13098 13103
30. O.V. Dominguez, and L.T. Samuels Mechanism of inhibition of adrenal steroid 11beta-hydroxylase by methopyrapone (metopirone) Endocrinology 73 1963 304 309
31. R. Sampath-Kumar, M. Yu, M.W. Khalil, and K. Yang Metyrapone is a competitive inhibitor of 11beta-hydroxysteroid dehydrogenase type 1 reductase J Steroid Biochem Mol Biol 62 1997 195 199
32. A.G. Atanasov, D. Leiser, C. Roesselet, M. Noti, N. Corazza, K. Schoonjans, and et al. Cell cycle-dependent regulation of extra-adrenal glucocorticoid synthesis in murine intestinal epithelial cells Faseb J 22 2008 4117 4125
33. T. Sano, G. Hirasawa, J. Takeyama, A.D. Darnel, T. Suzuki, T. Moriya, and et al. 17 beta-Hydroxysteroid dehydrogenase type 2 expression and enzyme activity in the human gastrointestinal tract Clin Sci (Lond) 101 2001 485 491
34. A. Papadimitriou, and K.N. Priftis Regulation of the hypothalamic-pituitary-adrenal axis Neuroimmunomodulation 16 2009 265 271
35. M.B. Sewer, and M.R. Waterman Insights into the transcriptional regulation of steroidogenic enzymes and StAR Rev Endocr Metab Disord 2 2001 269 274
36. B.P. Schimmer, and P.C. White Minireview: steroidogenic factor 1: its roles in differentiation, development, and disease Mol Endocrinol 24 2010 1322 1337
37. X. Luo, Y. Ikeda, and K.L. Parker A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation Cell 77 1994 481 490
38. K.L. Parker, and B.P. Schimmer Steroidogenic factor 1: a key determinant of endocrine development and function Endocr Rev 18 1997 361 377
39. M.S. Ramayya, J. Zhou, T. Kino, J.H. Segars, C.A. Bondy, and G.P. Chrousos Steroidogenic factor 1 messenger ribonucleic acid expression in steroidogenic and nonsteroidogenic human tissues: Northern blot and in situ hybridization studies J Clin Endocrinol Metab 82 1997 1799 1806
40. M. Mueller, A. Atanasov, I. Cima, N. Corazza, K. Schoonjans, and T. Brunner Differential regulation of glucocorticoid synthesis in murine intestinal epithelial versus adrenocortical cell lines Endocrinology 148 2007 1445 1453
41. O.A. Botrugno, E. Fayard, J.S. Annicotte, C. Haby, T. Brennan, O. Wendling, and et al. Synergy between LRH-1 and beta-catenin induces G1 cyclin-mediated cell proliferation Mol Cell 15 2004 499 509
42. M. Mueller, I. Cima, M. Noti, A. Fuhrer, S. Jakob, L. Dubuquoy, and et al. The nuclear receptor LRH-1 critically regulates extra-adrenal glucocorticoid synthesis in the intestine J Exp Med 203 2006 2057 2062
43. M. Noti, N. Corazza, G. Tuffin, K. Schoonjans, and T. Brunner Lipopolysaccharide induces intestinal glucocorticoid synthesis in a TNFalpha-dependent manner Faseb J 24 2010 1340 1346
44. Y.K. Lee, Y.H. Choi, S. Chua, Y.J. Park, and D.D. Moore Phosphorylation of the hinge domain of the nuclear hormone receptor LRH-1 stimulates transactivation J Biol Chem 281 2006 7850 7855
45. M. Noti, N. Corazza, C. Mueller, B. Berger, and T. Brunner TNF suppresses acute intestinal inflammation by inducing local glucocorticoid synthesis J Exp Med 207 2010 1057 1066
46. S.C. Huang, C.T. Lee, and B.C. Chung Tumor necrosis factor suppresses NR5A2 activity and intestinal glucocorticoid synthesis to sustain chronic colitis Sci Signal 7 2014 ra20
47. L. Drozdowski, and A.B. Thomson Intestinal hormones and growth factors: effects on the small intestine World J Gastroenterol 15 2009 385 406
48. T. Miyata, Y. Minai, and M. Haga Impaired growth of small intestinal epithelium by adrenalectomy in weaning rats Acta Histochem Cytochem 41 2008 83 88
49. K.Y. Yeh, M. Yeh, and P.R. Holt Thyroxine and cortisone cooperate to modulate postnatal intestinal enzyme differentiation in the rat Am J Physiol 260 1991 G371 G378
50. C. Schaeffer, M. Diab-Assef, M. Plateroti, F. Laurent-Huck, J.M. Reimund, M. Kedinger, and et al. Cytokine gene expression during postnatal small intestinal development: regulation by glucocorticoids Gut 47 2000 192 198
51. M.C. Biol-N'garagba, E. Niepceron, B. Mathian, and P. Louisot Glucocorticoid-induced maturation of glycoprotein galactosylation and fucosylation processes in the rat small intestine J Steroid Biochem Mol Biol 84 2003 411 422
52. N.N. Nanthakumar, C.E. Klopcic, I. Fernandez, and W.A. Walker Normal and glucocorticoid-induced development of the human small intestinal xenograft Am J Physiol Regul Integr Comp Physiol 285 2003 R162 R170
53. N.N. Nanthakumar, C. Young, J.S. Ko, D. Meng, J. Chen, T. Buie, and et al. Glucocorticoid responsiveness in developing human intestine: possible role in prevention of necrotizing enterocolitis Am J Physiol Gastrointest Liver Physiol 288 2005 G85 G92
54. M.A. Boivin, D. Ye, J.C. Kennedy, R. Al-Sadi, C. Shepela, and T.Y. Ma Mechanism of glucocorticoid regulation of the intestinal tight junction barrier Am J Physiol Gastrointest Liver Physiol 292 2007 G590 G598
55. A. Fischer, M. Gluth, F. Weege, U.F. Pape, B. Wiedenmann, D.C. Baumgart, and et al. Glucocorticoids regulate barrier function and claudin expression in intestinal epithelial cells via MKP-1 Am J Physiol Gastrointest Liver Physiol 306 2014 G218 G228
56. L. Lu, T. Li, G. Williams, E. Petit, M. Borowsky, and W.A. Walker Hydrocortisone induces changes in gene expression and differentiation in immature human enterocytes Am J Physiol Gastrointest Liver Physiol 300 2011 G425 G432
57. T. Rhen, and J.A. Cidlowski Antiinflammatory action of glucocorticoids - new mechanisms for old drugs N Engl J Med 353 2005 1711 1723
58. K. De Bosscher, and G. Haegeman Minireview: latest perspectives on antiinflammatory actions of glucocorticoids Mol Endocrinol 23 2009 281 291
59. Y. Jia, J. Domenico, K. Takeda, J. Han, M. Wang, M. Armstrong, and et al. Steroidogenic enzyme Cyp11a1 regulates Type 2 CD8+ T cell skewing in allergic lung disease Proc Natl Acad Sci USA 110 2013 8152 8157
60. L.H. Zeuthen, L.N. Fink, and H. Frokiaer Epithelial cells prime the immune response to an array of gut-derived commensals towards a tolerogenic phenotype through distinct actions of thymic stromal lymphopoietin and transforming growth factor-beta Immunology 123 2008 197 208
61. C. Stahn, M. Lowenberg, D.W. Hommes, and F. Buttgereit Molecular mechanisms of glucocorticoid action and selective glucocorticoid receptor agonists Mol Cell Endocrinol 275 2007 71 78
62. L. Fajas, D. Auboeuf, E. Raspe, K. Schoonjans, A.M. Lefebvre, R. Saladin, and et al. The organization, promoter analysis, and expression of the human PPARgamma gene J Biol Chem 272 1997 18779 18789
63. L. Dubuquoy, C. Rousseaux, X. Thuru, L. Peyrin-Biroulet, O. Romano, P. Chavatte, and et al. PPARgamma as a new therapeutic target in inflammatory bowel diseases Gut 55 2006 1341 1349
64. M. Ricote, A.C. Li, T.M. Willson, C.J. Kelly, and C.K. Glass The peroxisome proliferator-activated receptor-gamma is a negative regulator of macrophage activation Nature 391 1998 79 82
65. C. Jiang, A.T. Ting, and B. Seed PPAR-gamma agonists inhibit production of monocyte inflammatory cytokines Nature 391 1998 82 86
66. P. Tontonoz, and B.M. Spiegelman Fat and beyond: the diverse biology of PPARgamma Annu Rev Biochem 77 2008 289 312
67. C.K. Glass, and K. Saijo Nuclear receptor transrepression pathways that regulate inflammation in macrophages and T cells Nat Rev Immunol 10 2010 365 376
68. D. Ron, and P. Walter Signal integration in the endoplasmic reticulum unfolded protein response Nat Rev Mol Cell Biol 8 2007 519 529
69. D.J. Todd, A.H. Lee, and L.H. Glimcher The endoplasmic reticulum stress response in immunity and autoimmunity Nat Rev Immunol 8 2008 663 674
70. A. Kaser, A.H. Lee, A. Franke, J.N. Glickman, S. Zeissig, H. Tilg, and et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease Cell 134 2008 743 756
71. A. Kaser, and R.S. Blumberg Endoplasmic reticulum stress in the intestinal epithelium and inflammatory bowel disease Semin Immunol 21 2009 156 163
72. I. Das, C.W. Png, I. Oancea, S.Z. Hasnain, R. Lourie, M. Proctor, and et al. Glucocorticoids alleviate intestinal ER stress by enhancing protein folding and degradation of misfolded proteins J Exp Med 210 2013 1201 1216
73. G. Fiorelli, L. Picariello, V. Martineti, F. Tonelli, and M.L. Brandi Estrogen synthesis in human colon cancer epithelial cells J Steroid Biochem Mol Biol 71 1999 223 230
74. G. Fiorelli, L. Picariello, V. Martineti, I. Tognarini, F. Tonelli, and M.L. Brandi Estrogen metabolism in human colorectal cancer cells J Steroid Biochem Mol Biol 81 2002 281 289
75. M.A. English, P.M. Stewart, and M. Hewison Estrogen metabolism and malignancy: analysis of the expression and function of 17beta-hydroxysteroid dehydrogenases in colonic cancer Mol Cell Endocrinol 171 2001 53 60
76. R. Sato, T. Suzuki, Y. Katayose, K. Miura, K. Shiiba, Y. Miki, and et al. Aromatase in colon carcinoma Anticancer Res 32 2012 3069 3075
77. R. Sato, T. Suzuki, Y. Katayose, K. Miura, K. Shiiba, H. Tateno, and et al. Steroid sulfatase and estrogen sulfotransferase in colon carcinoma: regulators of intratumoral estrogen concentrations and potent prognostic factors Cancer Res 69 2009 914 922
78. O.O. Oduwole, M.J. Makinen, V.V. Isomaa, A. Pulkka, P. Jernvall, T.J. Karttunen, and et al. 17Beta-hydroxysteroid dehydrogenase type 2: independent prognostic significance and evidence of estrogen protection in female patients with colon cancer J Steroid Biochem Mol Biol 87 2003 133 140
79. O.O. Oduwole, V.V. Isomaa, P.A. Nokelainen, F. Stenback, and P.T. Vihko Downregulation of estrogen-metabolizing 17 beta-hydroxysteroid dehydrogenase type 2 expression correlates inversely with Ki67 proliferation marker in colon-cancer development Int J Cancer 97 2002 1 6
80. S. Narayan, G. Rajakumar, H. Prouix, and P. Singh Estradiol is trophic for colon cancer in mice: effect on ornithine decarboxylase and c-myc messenger RNA Gastroenterology 103 1992 1823 1832
81. M.B. Hoff, W.W. Chang, and K.M. Mak Effect of estrogen on cell proliferation in colonic mucosa of the mouse Virchows Arch B Cell Pathol Incl Mol Pathol 35 1981 263 273
82. M. Campbell-Thompson, I.J. Lynch, and B. Bhardwaj Expression of estrogen receptor (ER) subtypes and ERbeta isoforms in colon cancer Cancer Res 61 2001 632 640
83. P.A. Konstantinopoulos, A. Kominea, G. Vandoros, G.P. Sykiotis, P. Andricopoulos, I. Varakis, and et al. Oestrogen receptor beta (ERbeta) is abundantly expressed in normal colonic mucosa, but declines in colon adenocarcinoma paralleling the tumour's dedifferentiation Eur J Cancer 39 2003 1251 1258
84. O. Wada-Hiraike, O. Imamov, H. Hiraike, K. Hultenby, T. Schwend, Y. Omoto, and et al. Role of estrogen receptor beta in colonic epithelium Proc Natl Acad Sci USA 103 2006 2959 2964
85. M. Looijer-van Langen, N. Hotte, L.A. Dieleman, E. Albert, C. Mulder, and K.L. Madsen Estrogen receptor-beta signaling modulates epithelial barrier function Am J Physiol Gastrointest Liver Physiol 300 2011 G621 G626
86. D.C. Baumgart, and S.R. Carding Inflammatory bowel disease: cause and immunobiology Lancet 369 2007 1627 1640
87. D.C. Baumgart, and W.J. Sandborn Inflammatory bowel disease: clinical aspects and established and evolving therapies Lancet 369 2007 1641 1657
88. D.C. Baumgart, and W.J. Sandborn Crohn's disease Lancet 380 2012 1590 1605
89. I. Ordas, L. Eckmann, M. Talamini, D.C. Baumgart, and W.J. Sandborn Ulcerative colitis Lancet 380 2012 1606 1619
90. S. Danese, and C. Fiocchi Ulcerative colitis N Engl J Med 365 2011 1713 1725
91. C.A. Anderson, G. Boucher, C.W. Lees, A. Franke, M. D'Amato, K.D. Taylor, and et al. Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47 Nat Genet 43 2011 246 252
92. H. Khalili, L.M. Higuchi, A.N. Ananthakrishnan, J.M. Richter, D. Feskanich, C.S. Fuchs, and et al. Oral contraceptives, reproductive factors and risk of inflammatory bowel disease Gut 62 2013 1153 1159
93. P.A. Foster Oestrogen and colorectal cancer: mechanisms and controversies Int J Colorectal Dis 28 2013 737 749
94. H.R. Wilkins, K. Doucet, V. Duke, A. Morra, and N. Johnson Estrogen prevents sustained COLO-205 human colon cancer cell growth by inducing apoptosis, decreasing c-myb protein, and decreasing transcription of the anti-apoptotic protein bcl-2 Tumour Biol 31 2010 16 22
95. S. Han, and J. Roman Peroxisome proliferator-activated receptor gamma: a novel target for cancer therapeutics? Anticancer Drugs 18 2007 237 244
96. M. Schwab, V. Reynders, S. Loitsch, Y.M. Shastri, D. Steinhilber, O. Schroder, and et al. PPARgamma is involved in mesalazine-mediated induction of apoptosis and inhibition of cell growth in colon cancer cells Carcinogenesis 29 2008 1407 1414
97. J. Feilchenfeldt, M.A. Brundler, C. Soravia, M. Totsch, and C.A. Meier Peroxisome proliferator-activated receptors (PPARs) and associated transcription factors in colon cancer: reduced expression of PPARgamma-coactivator 1 (PGC-1) Cancer Lett 203 2004 25 33
98. A. Mukherji, A. Kobiita, T. Ye, and P. Chambon Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs Cell 153 2013 812 827