Endocrine disruptors and other inhibitors of 11β-hydroxysteroid dehydrogenase 1 and 2: Tissue-specific consequences of enzyme inhibition

Journal of Steroid Biochemistry and Molecular Biology

Volumn 155, Issue , 2016, Pages 207-216

  Vitku, Jana ^a   Starka, Luboslav ^a   Bicikova, Marie ^a   Hill, Martin ^a   Heracek, Jiri ^b,c   Sosvorova, Lucie ^a   Hampl, Richard ^a  

^a INSTITUTE OF ENDOCRINOLOGY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c CHARLES UNIVERSITY   (Czech Republic)

Author keywords

11 hydroxysteroid dehydrogenase; Adipose tissue; Brain; Colon; Endocrine disruptor; Inhibitor; Placenta; Testis

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; 11BETA HYDROXYSTEROID DEHYDROGENASE 1 INHIBITOR; 11BETA HYDROXYSTEROID DEHYDROGENASE 2; 11BETA HYDROXYSTEROID DEHYDROGENASE 2 INHIBITOR; ANTINEOPLASTIC AGENT; ANTIOBESITY AGENT; ENDOCRINE DISRUPTOR; ENZYME INHIBITOR; GLUCOCORTICOID; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOGENESIS; ADIPOSE TISSUE; CANCER RISK; COLON; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME INHIBITION; HUMAN; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PLACENTA; PROADIPOCYTE; REVIEW; RISK FACTOR; STEROID METABOLISM; STROMA CELL; TESTIS; ANTAGONISTS AND INHIBITORS; ANTIBODY SPECIFICITY; BRAIN; CHEMICALLY INDUCED; DIABETES MELLITUS; DRUG EFFECTS; ENZYMOLOGY; FEMALE; MALE; METABOLISM; NEOPLASM; OBESITY; PATHOLOGY; PREGNANCY;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; 11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 2; ADIPOSE TISSUE; BRAIN; COLON; DIABETES MELLITUS; ENDOCRINE DISRUPTORS; ENZYME INHIBITORS; FEMALE; GLUCOCORTICOIDS; HUMANS; MALE; METABOLIC SYNDROME X; NEOPLASMS; OBESITY; ORGAN SPECIFICITY; PLACENTA; PREGNANCY; TESTIS;

EID: 84949321398     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2014.07.007     Document Type: Review

References (141)

1. E. Diamanti-Kandarakis, J.P. Bourguignon, L.C. Giudice, R. Hauser, G.S. Prins, A.M. Soto, R.T. Zoeller, and A.C. Gore Endocrine-disrupting chemicals: an endocrine society scientific statement Endocr. Rev. 30 4 2009 293 342
2. E. Carlsen, A. Giwercman, N. Keiding, and N.E. Skakkebaek Evidence for decreasing quality of semen during past 50 years BMJ 305 6854 1992 609 613
3. A.M. Andersson, N. Jorgensen, K.M. Main, J. Toppari, E. Rajpert-De Meyts, H. Leffers, A. Juul, T.K. Jensen, and N.E. Skakkebaek Adverse trends in male reproductive health: we may have reached a crucial 'tipping point' Int. J. Androl. 31 2 2008 74 80
4. M.D. Anway, A.S. Cupp, M. Uzumcu, and M.K. Skinner Epigenetic transgenerational actions of endocrine disruptors and male fertility Science. 308 5727 2005 1466 1469
5. J.A. Rusiecki, A. Baccarelli, V. Bollati, L. Tarantini, L.E. Moore, and E.C. Bonefeld-Jorgensen Global DNA hypomethylation is associated with high serum-persistent organic pollutants in Greenlandic Inuit Environ. Health Perspect. 116 11 2008 1547 1552
6. D.C. Dolinoy, D. Huang, and R.L. Jirtle Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development Proc. Natl. Acad. Sci. U. S. A. 104 32 2007 13056 13061
7. L. Wang, J. Liu, A. Zhang, P. Cheng, X. Zhang, S. Lv, L. Wu, J. Yu, W. Di, J. Zha, X. Kong, H. Qi, Y. Zhong, and G. Ding BVT. 2733, a selective 11beta-hydroxysteroid dehydrogenase type 1 inhibitor, attenuates obesity and inflammation in diet-induced obese mice PLoS One 7 7 2012 p. e40056
8. J.S. Park, S.D. Rhee, W.H. Jung, N.S. Kang, H.Y. Kim, S.K. Kang, J.H. Ahn, and K.Y. Kim Anti-diabetic and anti-adipogenic effects of a novel selective 11beta-hydroxysteroid dehydrogenase type 1 inhibitor in the diet-induced obese mice Eur. J. Pharmacol. 691 1-3 2012 19 27
9. A. Tiwari INCB-13739, an 11beta-hydroxysteroid dehydrogenase type 1 inhibitor for the treatment of type 2 diabetes IDrugs 13 4 2010 266 275
10. D.A. Katz, W. Liu, C. Locke, P. Jacobson, D.M. Barnes, R. Basu, G. An, M.J. Rieser, D. Daszkowski, F. Groves, G. Heneghan, A. Shah, H. Gevorkyan, S.S. Jhee, L. Ereshefsky, and G.J. Marek Peripheral and central nervous system inhibition of 11beta-hydroxysteroid dehydrogenase type 1 in man by the novel inhibitor ABT-384 Transl. Psychiatry 3 2013 p. e295
11. D. Amelung, H.J. Hubener, L. Roka, and G. Meyerheim Conversion of cortisone to compound F J. Clin. Endocrinol. Metab. 13 9 1953 1125 1126
12. C.R. Edwards, P.M. Stewart, D. Burt, L. Brett, M.A. McIntyre, W.S. Sutanto, E.R. de Kloet, and C. Monder Localisation of 11beta-hydroxysteroid dehydrogenase - tissue specific protector of the mineralocorticoid receptor Lancet 2 8618 1988 986 989
13. J.W. Funder, P.T. Pearce, R. Smith, and A.I. Smith Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated Science. 242 4878 1988 583 585
14. A.G. Atanasov, L.G. Nashev, R.A. Schweizer, C. Frick, and A. Odermatt Hexose-6-phosphate dehydrogenase determines the reaction direction of 11beta-hydroxysteroid dehydrogenase type 1 as an oxoreductase FEBS Lett. 571 1-3 2004 129 133
15. A.G. Atanasov, L.G. Nashev, L. Gelman, B. Legeza, R. Sack, R. Portmann, and A. Odermatt Direct protein-protein interaction of 11beta-hydroxysteroid dehydrogenase type 1 and hexose-6-phosphate dehydrogenase in the endoplasmic reticulum lumen Biochim. Biophys. Acta. 1783 8 2008 1536 1543
16. I.J. Bujalska, N. Draper, Z. Michailidou, J.W. Tomlinson, P.C. White, K.E. Chapman, E.A. Walker, and P.M. Stewart Hexose-6-phosphate dehydrogenase confers oxo-reductase activity upon 11beta-hydroxysteroid dehydrogenase type 1 J. Mol. Endocrinol. 34 3 2005 675 684
17. G. Banhegyi, A. Benedetti, R. Fulceri, and S. Senesi Cooperativity between 11beta-hydroxysteroid dehydrogenase type 1 and hexose-6-phosphate dehydrogenase in the lumen of the endoplasmic reticulum J. Biol. Chem. 279 26 2004 27017 27021
18. A.K. Agarwal, T. Mune, C. Monder, and P.C. White NAD(+)-dependent isoform of 11beta-hydroxysteroid dehydrogenase. Cloning and characterization of cDNA from sheep kidney J Biol Chem. 269 42 1994 25959 25962
19. S. Kenouch, M. Lombes, F. Delahaye, E. Eugene, J.P. Bonvalet, and N. Farman Human skin as target for aldosterone: coexpression of mineralocorticoid receptors and 11 beta-hydroxysteroid dehydrogenase J. Clin. Endocrinol. Metab. 79 5 1994 1334 1341
20. R.S. Ge, Q. Dong, E.M. Niu, C.M. Sottas, D.O. Hardy, J.F. Catterall, S.A. Latif, D.J. Morris, and M.P. Hardy 11{Beta}-hydroxysteroid dehydrogenase 2 in rat Leydig cells: its role in blunting glucocorticoid action at physiological levels of substrate Endocrinology 146 6 2005 2657 2664
21. R.W. Brown, K.E. Chapman, C.R. Edwards, and J.R. Seckl Human placental 11beta-hydroxysteroid dehydrogenase: evidence for and partial purification of a distinct NAD-dependent isoform Endocrinology 132 6 1993 2614 2621
22. V. Lakshmi, R.R. Sakai, B.S. McEwen, and C. Monder Regional distribution of 11beta-hydroxysteroid dehydrogenase in rat brain Endocrinology 128 4 1991 1741 1748
23. M. Bicikova, M. Hill, R. Hampl, and L. Starka Inhibition of rat renal and testicular 11beta-hydroxysteroid dehydrogenase by some antihypertensive drugs, diuretics, and epitestosterone Horm. Metab. Res. 29 9 1997 465 468
24. A.K. Tannin, C. Agarwal, M.I. New, and P.C. White The human gene for 11beta-hydroxysteroid dehydrogenase. Structure, tissue distribution, and chromosomal localization J. Biol. Chem. 266 25 1991 16,653 16658
25. B.R. Walker, J.L. Yau, L.P. Brett, J.R. Seckl, C. Monder, B.C. Williams, and C.R. Edwards 11Beta-hydroxysteroid dehydrogenase in vascular smooth muscle and heart: implications for cardiovascular responses to glucocorticoids Endocrinology 129 6 1991 3305 3312
26. R. Benediktsson, J.L. Yau, S. Low, L.P. Brett, B.E. Cooke, C.R. Edwards, and J.R. Seckl 11Beta-hydroxysteroid dehydrogenase in the rat ovary: high expression in the oocyte J. Endocrinol. 135 1 1992 53 58
27. S. Rauz, C.M. Cheung, P.J. Wood, M. Coca-Prados, E.A. Walker, P.I. Murray, and P.M. Stewart Inhibition of 11beta-hydroxysteroid dehydrogenase type 1 lowers intraocular pressure in patients with ocular hypertension QJM 96 7 2003 481 490
28. Z. Kyossev, P.D. Walker, and W.B. Reeves Immunolocalization of NAD-dependent 11beta-hydroxysteroid dehydrogenase in human kidney and colon Kidney Int. 49 1 1996 271 281
29. G. Hirasawa, H. Sasano, K. Takahashi, K. Fukushima, T. Suzuki, N. Hiwatashi, T. Toyota, Z.S. Krozowski, and H. Nagura Colocalization of 11beta-hydroxysteroid dehydrogenase type II and mineralocorticoid receptor in human epithelia J. Clin. Endocrinol. Metab. 82 11 1997 3859 3863
30. A.L. Albiston, V.R. Obeyesekere, R.E. Smith, and Z.S. Krozowski Cloning and tissue distribution of the human 11beta-hydroxysteroid dehydrogenase type 2 enzyme Mol. Cell. Endocrinol. 105 2 1994 R11 17
31. R.E. Smith, P.J. Little, J.A. Maguire, A.N. Stein-Oakley, and Z.S. Krozowski Vascular localization of the 11beta-hydroxysteroid dehydrogenase type II enzyme Clin. Exp. Pharmacol. Physiol. 23 6-7 1996 549 551
32. E.P. Gomez-Sanchez, V. Ganjam, Y.J. Chen, D.L. Cox, M.Y. Zhou, S. Thanigaraj, and C.E. Gomez-Sanchez The sheep kidney contains a novel unidirectional, high affinity NADP(+)-dependent 11beta-hydroxysteroid dehydrogenase (11beta-HSD-3) Steroids 62 5 1997 444 450
33. M.E. Baker Evolutionary analysis of 11beta-hydroxysteroid dehydrogenase-type 1, -type 2 -type 3 and 17beta-hydroxysteroid dehydrogenase-type 2 in fish FEBS Lett. 574 1-3 2004 167 170
34. M.E. Baker Evolution of 11beta-hydroxysteroid dehydrogenase-type 1 and 11beta-hydroxysteroid dehydrogenase-type 3 FEBS Lett. 584 11 2010 2279 2284
35. C. Huang, B. Wan, B. Gao, S. Hexige, and L. Yu Isolation and characterization of novel human short-chain dehydrogenase/reductase SCDR10B which is highly expressed in the brain and acts as hydroxysteroid dehydrogenase Acta Biochim. Pol. 56 2 2009 279 289
36. M. Ohshima, S. Ohno, and S. Nakajin Inhibitory effects of some possible endocrine-disrupting chemicals on the isozymes of human 11beta-hydroxysteroid dehydrogenase and expression of their mRNA in gonads and adrenal glands Environ. Sci. 12 4 2005 219 230
37. X.L. Moore, I. Hoong, and T.J. Cole Expression of the 11beta-hydroxysteroid dehydrogenase 2 gene in the mouse Kidney Int. 57 4 2000 1307 1312
38. P. Klusonova, M. Kucka, I. Miksik, J. Bryndova, and J. Pacha Chicken 11beta-hydroxysteroid dehydrogenase type 2: partial cloning and tissue distribution Steroids 73 3 2008 348 355
39. P. Klusonova, M. Kucka, P. Ergang, I. Miksik, J. Bryndova, and J. Pacha Cloning of chicken 11beta-hydroxysteroid dehydrogenase type 1 and its tissue distribution J. Steroid Biochem. Mol. Biol. 111 3-5 2008 217 224
40. C.M. Leckie, L.A. Welberg, and J.R. Seckl 11Beta-hydroxysteroid dehydrogenase is a predominant reductase in intact rat Leydig cells J. Endocrinol. 159 2 1998 233 238
41. H.B. Gao, R.S. Ge, V. Lakshmi, A. Marandici, and M.P. Hardy Hormonal regulation of oxidative and reductive activities of 11beta-hydroxysteroid dehydrogenase in rat Leydig cells Endocrinology 138 1 1997 156 161
42. R.S. Ge, and M.P. Hardy Initial predominance of the oxidative activity of type I 11beta-hydroxysteroid dehydrogenase in primary rat Leydig cells and transfected cell lines J. Androl. 21 2 2000 303 310
43. R.S. Ge, D.O. Hardy, J.F. Catterall, and M.P. Hardy Developmental changes in glucocorticoid receptor and 11beta-hydroxysteroid dehydrogenase oxidative and reductive activities in rat Leydig cells Endocrinology 138 12 1997 5089 5095
44. V. Sharp, L.M. Thurston, R.C. Fowkes, and A.E. Michael 11Beta-hydroxysteroid dehydrogenase enzymes in the testis and male reproductive tract of the boar (Sus scrofa domestica) indicate local roles for glucocorticoids in male reproductive physiology Reproduction 134 3 2007 473 482
45. V. Sharp, L.M. Thurston, R.C. Fowkes, and A.E. Michael Expression and activities of 11betaHSD enzymes in the testes and reproductive tracts of sexually immature male pigs J. Steroid Biochem. Mol. Biol. 115 3-5 2009 98 106
46. G.-X. Hu, Q.-Q. Lian, H. Lin, S.A. Latif, D.J. Morris, M.P. Hardy, and R.-S. Ge Rapid mechanisms of glucocorticoid signaling in the Leydig cell Steroids 73 9-10 2008 1018 1024
47. S.A. Latif, M. Shen, R.S. Ge, C.M. Sottas, M.P. Hardy, and D.J. Morris Role of 11beta-OH-C(19) and C(21) steroids in the coupling of 11beta-HSD1 and 17beta-HSD3 in regulation of testosterone biosynthesis in rat Leydig cells Steroids 76 7 2011 682 689
48. B. Legeza, Z. Balazs, L.G. Nashev, and A. Odermatt The microsomal enzyme 17beta-hydroxysteroid dehydrogenase 3 faces the cytoplasm and uses NADPH generated by glucose-6-phosphate dehydrogenase Endocrinology 154 1 2013 205 213
49. R. Hauser, J.S. Barthold, and J.D. Meeker Epidemiologic evidence on the relationship between environmental endocrine disruptors and male reproductive and developmental health A.C. Gore, Endocrine-Disrupting Chemicals: From Basic Research to Clinical Practice 2010 Humana Press Totowa, NJ
50. R. Hampl, J. Kubatova, J. Heracek, V. Sobotka, and L. Starka Hormones and endocrine disruptors in human seminal plasma Endocr. Reg. 47 3 2013 149 158
51. N. Tagawa, S. Kubota, I. Kato, and Y. Kobayashi Resveratrol inhibits 11beta-hydroxysteroid dehydrogenase type 1 activity in rat adipose microsomes J. Endocrinol. 218 3 2013 311 320
52. G.X. Hu, H. Lin, Q.Q. Lian, S.H. Zhou, J. Guo, H.Y. Zhou, Y. Chu, and R.S. Ge Curcumin as a potent and selective inhibitor of 11beta-hydroxysteroid dehydrogenase 1: improving lipid profiles in high-fat-diet-treated rats PLos One 8 3 2013 p. e49976
53. Y.J. Wang, S.L. Huang, Y. Feng, M.M. Ning, and Y. Leng Emodin, an 11beta-hydroxysteroid dehydrogenase type 1 inhibitor, regulates adipocyte function in vitro and exerts anti-diabetic effect in ob/ob mice Acta Pharmacol. Sin. 33 9 2012 1195 1203
54. Y. Feng, S.L. Huang, W. Dou, S. Zhang, J.H. Chen, Y. Shen, J.H. Shen, and Y. Leng Emodin, a natural product, selectively inhibits 11beta-hydroxysteroid dehydrogenase type 1 and ameliorates metabolic disorder in diet-induced obese mice Br. J. Pharmacol. 161 1 2010 113 126
55. R.A. Schweizer, A.G. Atanasov, B.M. Frey, and A. Odermatt A rapid screening assay for inhibitors of 11beta-hydroxysteroid dehydrogenases (11beta-HSD): flavanone selectively inhibits 11beta-HSD1 reductase activity Mol. Cell. Endocrinol. 212 1-2 2003 41 49
56. L.Y. Guo, H.P. He, Y. Leng, Z. Yang, and X.J. Hao Inhibition of 11b-HSD1 by tetracyclic triterpenoids from Euphorbia kansui Molecules 11 2012 826 11838
57. J. Hintzpeter, C. Stapelfeld, C. Loerz, H.J. Martin, and E. Maser Green tea and one of its constituents, epigallocatechine-3-gallate, are potent inhibitors of human 11beta-hydroxysteroid dehydrogenase type 1 PLos One 9 1 2014 p. e84468
58. J. Guo, X. Yuan, L. Qiu, W. Zhu, C. Wang, G. Hu, Y. Chu, L. Ye, Y. Xu, and R.S. Ge Inhibition of human and rat 11beta-hydroxysteroid dehydrogenases activities by bisphenol A Toxicol. Lett. 215 2 2012 126 130
59. J. Guo, H. Deng, H. Li, Q. Zhu, B. Zhao, B. Chen, Y. Chu, and R.S. Ge Effects of methoxychlor and its metabolite 2,2-bis(p-hydroxyphenyl)-1,1,1-trichloroethane on 11beta-hydroxysteroid dehydrogenase activities in vitro Toxicol. Lett. 218 1 2013 18 23
60. R.W. Brown, K.E. Chapman, Y. Kotelevtsev, J.L. Yau, R.S. Lindsay, L. Brett, C. Leckie, P. Murad, V. Lyons, J.J. Mullins, C.R. Edwards, and J.R. Seckl Cloning and production of antisera to human placental 11 beta-hydroxysteroid dehydrogenase type 2 Biochem. J. 313 Pt 3 1996 1007 1017
61. A.G. Atanasov, L.G. Nashev, S. Tam, M.E. Baker, and A. Odermatt Organotins disrupt the 11beta-hydroxysteroid dehydrogenase type 2-dependent local inactivation of glucocorticoids Environ. Health Perspect. 113 11 2005 1600 1606
62. A.G. Atanasov, S. Tam, J.M. Rocken, M.E. Baker, and A. Odermatt Inhibition of 11beta-hydroxysteroid dehydrogenase type 2 by dithiocarbamates Biochem. Biophy. Res. Commun. 308 2 2003 257 262
63. B. Zhao, Y. Chu, Y. Huang, D.O. Hardy, S. Lin, and R.S. Ge Structure-dependent inhibition of human and rat 11beta-hydroxysteroid dehydrogenase 2 activities by phthalates Chem. Biol. Interact. 183 1 2010 79 84
64. B. Zhao, Q. Lian, Y. Chu, D.O. Hardy, X.K. Li, and R.S. Ge The inhibition of human and rat 11beta-hydroxysteroid dehydrogenase 2 by perfluoroalkylated substances J. Steroid Biochem. Mol. Biol. 125 1-2 2011 143 147
65. M.Z. Zhang, J. Xu, B. Yao, H. Yin, Q. Cai, M.J. Shrubsole, X. Chen, V. Kon, W. Zheng, A. Pozzi, and R.C. Harris Inhibition of 11beta-hydroxysteroid dehydrogenase type II selectively blocks the tumor COX-2 pathway and suppresses colon carcinogenesis in mice and humans J. Clin. Invest. 119 4 2009 876 885
66. P.M. Stewart, and S.M. Prescott Can licorice lick colon cancer? J. Clin. Invest. 119 4 2009 760 763
67. R.S. Bresalier, R.S. Sandler, H. Quan, J.A. Bolognese, B. Oxenius, K. Horgan, C. Lines, R. Riddell, D. Morton, A. Lanas, M.A. Konstam, and J.A. Baron Cardiovascular events associated with rofecoxib in a colorectal adenoma chemoprevention trial N. Engl. J. Med. 352 11 2005 1092 1102
68. D. Mukherjee, S.E. Nissen, and E.J. Topol Risk of cardiovascular events associated with selective COX-2 inhibitors JAMA 286 8 2001 954 959
69. M. Fornai, L. Antonioli, R. Colucci, C. Pellegrini, G. Giustarini, L. Testai, A. Martelli, A. Matarangasi, G. Natale, V. Calderone, M. Tuccori, C. Scarpignato, and C. Blandizzi NSAID-induced enteropathy: are the currently available selective COX-2 inhibitors all the same? J. Pharmacol. Exp. Ther. 348 1 2014 86 95
70. C. Scarpignato, and R.H. Hunt Nonsteroidal antiinflammatory drug-related injury to the gastrointestinal tract: clinical picture, pathogenesis, and prevention Gastroenterol. Clin. North Am. 39 3 2010 433 464
71. D.V. Kratschmar, A. Vuorinen, T. Da Cunha, G. Wolber, D. Classen-Houben, O. Doblhoff, D. Schuster, and A. Odermatt Characterization of activity and binding mode of glycyrrhetinic acid derivatives inhibiting 11beta-hydroxysteroid dehydrogenase type 2 J. Steroid Biochem. Mol. Biol. 125 1-2 2011 129 142
72. S. Zbankova, J. Bryndova, M. Kment, and J. Pacha Expression of 11beta-hydroxysteroid dehydrogenase types 1 and 2 in colorectal cancer Cancer Lett. 210 1 2004 95 100
73. M. Moravec, J. Svec, P. Ergang, V. Mandys, L. Rehakova, Z. Zadorova, J. Hajer, M. Kment, and J. Pacha Expression of 11beta-hydroxysteroid dehydrogenase type 2 is deregulated in colon carcinoma Histol. Histopathol. 2013
74. I.J. Bujalska, S. Kumar, and P.M. Stewart Does central obesity reflect Cushing's disease of the omentum? Lancet 349 9060 1997 1210 1213
75. J.H. Goedecke, D.J. Wake, N.S. Levitt, E.V. Lambert, M.R. Collins, N.M. Morton, R. Andrew, J.R. Seckl, and B.R. Walker Glucocorticoid metabolism within superficial subcutaneous rather than visceral adipose tissue is associated with features of the metabolic syndrome in South African women Clin. Endocrinol. 65 1 2006 81 87
76. L. Alberti, A. Girola, L. Gilardini, A. Conti, S. Cattaldo, G. Micheletto, and C. Invitti Type 2 diabetes and metabolic syndrome are associated with increased expression of 11beta-hydroxysteroid dehydrogenase 1 in obese subjects Int. J. Obes. (Lond.) 31 12 2007 1826 1831
77. I.J. Bujalska, E.A. Walker, M. Hewison, and P.M. Stewart A switch in dehydrogenase to reductase activity of 11beta-hydroxysteroid dehydrogenase type 1 upon differentiation of human omental adipose stromal cells J. Clin. Endocrinol. Metab. 87 3 2002 1205 1210
78. S.K. Paulsen, S.B. Pedersen, S. Fisker, and B. Richelsen 11Beta-HSD type 1 expression in human adipose tissue: impact of gender, obesity, and fat localization Obesity (Silver Spring) 15 8 2007 1954 1960
79. G. Torres, M. Ferrario, and V. Mericq Differences in expression, content, and activity of 11beta-HSD1 in adipose tissue between obese men and women ISRN Endocrinol. 2012 2012 787201
80. R.S. Lindsay, D.J. Wake, S. Nair, J. Bunt, D.E. Livingstone, P.A. Permana, P.A. Tataranni, and B.R. Walker Subcutaneous adipose 11beta-hydroxysteroid dehydrogenase type 1 activity and messenger ribonucleic acid levels are associated with adiposity and insulinemia in Pima Indians and Caucasians J. Clin. Endocrinol. Metab. 88 6 2003 2738 2744
81. K. Kannisto, K.H. Pietilainen, E. Ehrenborg, A. Rissanen, J. Kaprio, A. Hamsten, and H. Yki-Jarvinen Overexpression of 11beta-hydroxysteroid dehydrogenase-1 in adipose tissue is associated with acquired obesity and features of insulin resistance: studies in young adult monozygotic twins J. Clin. Endocrinol. Metab. 89 9 2004 4414 4421
82. E. Rask, T. Olsson, S. Soderberg, R. Andrew, D.E. Livingstone, O. Johnson, and B.R. Walker Tissue-specific dysregulation of cortisol metabolism in human obesity J. Clin. Endocrinol. Metab. 86 3 2001 1418 1421
83. Y. Wang, L.H. Liu Du, Y. Nagaoka, W.K. Fan Lutfy, T.C. Friedman, M. Jiang, and Y. Liu Transgenic overexpression of hexose-6-phosphate dehydrogenase in adipose tissue causes local glucocorticoid amplification and lipolysis in male mice Am. J. Physiol. Endocrinol. Metab. 306 5 2014 E543 E551
84. K.N. Hewitt, E.A. Walker, and P.M. Stewart Minireview: hexose-6-phosphate dehydrogenase and redox control of 11{beta}-hydroxysteroid dehydrogenase type 1 activity Endocrinology 146 6 2005 2539 2543
85. I.J. Bujalska, L.L. Gathercole, J.W. Tomlinson, C. Darimont, J. Ermolieff, A.N. Fanjul, P.A. Rejto, and P.M. Stewart A novel selective 11beta-hydroxysteroid dehydrogenase type 1 inhibitor prevents human adipogenesis J. Endocrinol. 197 2 2008 297 307
86. H. Hauner, G. Entenmann, M. Wabitsch, D. Gaillard, G. Ailhaud, R. Negrel, and E.F. Pfeiffer Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium J. Clin. Invest. 84 5 1989 1663 1670
87. F. Gregoire, C. Genart, N. Hauser, and C. Remacle Glucocorticoids induce a drastic inhibition of proliferation and stimulate differentiation of adult rat fat cell precursors Exp. Cell Res. 196 2 1991 270 278
88. N.M. Morton, and J.R. Seckl 11Beta-hydroxysteroid dehydrogenase type 1 and obesity Front. Horm. Res. 36 2008 146 164
89. J.S. Scott, F.W. Goldberg, and A.V. Turnbull Medicinal chemistry of inhibitors of 11beta-hydroxysteroid dehydrogenase type 1 (11beta-HSD1) J. Med. Chem. 57 11 2014 4466 4486
90. P. Anagnostis, N. Katsiki, F. Adamidou, V.G. Athyros, A. Karagiannis, M. Kita, and D.P. Mikhailidis 11Beta-hydroxysteroid dehydrogenase type 1 inhibitors: novel agents for the treatment of metabolic syndrome and obesity-related disorders? Metabolism 62 1 2013 21 33
91. C.D. Pereira, I. Azevedo, R. Monteiro, and M.J. Martins 11Beta-hydroxysteroid dehydrogenase type 1: relevance of its modulation in the pathophysiology of obesity, the metabolic syndrome and type 2 diabetes mellitus Diabetes Obes. Metab. 14 10 2012 869 881
92. A. Odermatt, and L.G. Nashev The glucocorticoid-activating enzyme 11beta-hydroxysteroid dehydrogenase type 1 has broad substrate specificity: physiological and toxicological considerations J. Steroid Biochem. Mol. Biol. 119 1-2 2010 1 13
93. S.H. Baek, H.J. Chung, H.K. Lee, R. D'Souza, Y. Jeon, H.J. Kim, S.J. Kweon, and S.T. Hong Treatment of obesity with the resveratrol-enriched rice DJ-526 Sci. Rep. 4 2014 3879
94. J.A. Baur, K.J. Pearson, N.L. Price, H.A. Jamieson, C. Lerin, A. Kalra, V.V. Prabhu, J.S. Allard, G. Lopez-Lluch, K. Lewis, P.J. Pistell, S. Poosala, K.G. Becker, O. Boss, D. Gwinn, M. Wang, S. Ramaswamy, K.W. Fishbein, R.G. Spencer, E.G. Lakatta, D. Le Couteur, R.J. Shaw, P. Navas, P. Puigserver, D.K. Ingram, R. de Cabo, and D.A. Sinclair Resveratrol improves health and survival of mice on a high-calorie diet Nature 444 7117 2006 337 342
95. S. Costa Cdos, F. Rohden, T.O. Hammes, R. Margis, J.W. Bortolotto, A.V. Padoin, C.C. Mottin, and R.M. Guaragna Resveratrol upregulated SIRT1, FOXO1, and adiponectin and downregulated PPARgamma1-3 mRNA expression in human visceral adipocytes Obes. Surg. 21 3 2011 356 361
96. W.J. Pang, S.D.L. Sun Bai, Y.J. Yang, and G.S. Yang [Effects of resveratrol on pig primary preadipocytes proliferation, differentiation and transcription expression of Sirt1 gene] Sheng Wu Gong Cheng Xue Bao 22 5 2006 850 855
97. H.J. Wang, Q. Wang, Z.M. Lv, C.L. Wang, C.P. Li, and Y.L. Rong Resveratrol appears to protect against oxidative stress and steroidogenesis collapse in mice fed high-calorie and high-cholesterol diet Andrologia 2014
98. B.R. Walker, A.A. Connacher, R.M. Lindsay, D.J. Webb, and C.R. Edwards Carbenoxolone increases hepatic insulin sensitivity in man: a novel role for 11-oxosteroid reductase in enhancing glucocorticoid receptor activation J. Clin. Endocrinol. Metab. 80 11 1995 3155 3159
99. R.C. Andrews, O. Rooyackers, and B.R. Walker Effects of the 11beta-hydroxysteroid dehydrogenase inhibitor carbenoxolone on insulin sensitivity in men with type 2 diabetes J. Clin. Endocrinol. Metab. 88 1 2003 285 291
100. K. Chapman, M. Holmes, and J. Seckl 11Beta-hydroxysteroid dehydrogenases: intracellular gate-keepers of tissue glucocorticoid action Physiol. Rev. 93 3 2013 1139 1206
101. X.Y. Ye, D. Yoon, S.Y. Chen, A. Nayeem, R. Golla, R. Seethala, M. Wang, T. Harper, B.G. Sleczka, A. Apedo, Y.X. Li, B. He, M. Kirby, D.A. Gordon, and J.A. Robl Synthesis and structure-activity relationship of 2-adamantylmethyl tetrazoles as potent and selective inhibitors of human 11beta-hydroxysteroid dehydrogenase type 1 (11beta-HSD1) Bioorg. Med. Chem. Lett. 24 2 2014 654 660
102. J. Wang, B. Sun, M. Hou, X. Pan, and X. Li The environmental obesogen bisphenol A promotes adipogenesis by increasing the amount of 11beta-hydroxysteroid dehydrogenase type 1 in the adipose tissue of children Int. J. Obes. (Lond.) 37 7 2013 999 1005
103. G.G. Kuiper, J.G. Lemmen, B. Carlsson, J.C. Corton, S.H. Safe, P.T. van der Saag, B. van der Burg, and J.A. Gustafsson Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta Endocrinology 139 10 1998 4252 4263
104. V. Delfosse, M. Grimaldi, A. le Maire, W. Bourguet, and P. Bourguet Nuclear receptor profiling of bisphenol-A and its halogenated analogues Vitam. Horm. 94 2014 229 251
105. H. Okada, T. Tokunaga, X. Liu, S. Takayanagi, A. Matsushima, and Y. Shimohigashi Direct evidence revealing structural elements essential for the high binding ability of bisphenol A to human estrogen-related receptor-gamma Environ. Health Perspect. 116 1 2008 32 38
106. H.J. Lee, S. Chattopadhyay, E.Y. Gong, R.S. Ahn, and K. Lee Antiandrogenic effects of bisphenol A and nonylphenol on the function of androgen receptor Toxicol. Sci. 75 1 2003 40 46
107. C. Teng, B. Goodwin, K. Shockley, M. Xia, R. Huang, J. Norris, B.A. Merrick, A.M. Jetten, C.P. Austin, and R.R. Tice Bisphenol A affects androgen receptor function via multiple mechanisms Chem. Biol. Interact. 203 3 2013 556 564
108. K. Moriyama, T. Tagami, T. Akamizu, T. Usui, M. Saijo, N. Kanamoto, Y. Hataya, A. Shimatsu, H. Kuzuya, and K. Nakao Thyroid hormone action is disrupted by bisphenol A as an antagonist J. Clin. Endocrinol. Metab. 87 11 2002 5185 5190
109. R.M. Sargis, D.N. Johnson, R.A. Choudhury, and M.J. Brady Environmental endocrine disruptors promote adipogenesis in the 3T3-L1 cell line through glucocorticoid receptor activation Obesity (Silver Spring) 18 7 2010 1283 1288
110. A. Pereira-Fernandes, H. Demaegdt, K. Vandermeiren, T.L. Hectors, P.G. Jorens, R. Blust, and C. Vanparys Evaluation of a screening system for obesogenic compounds: screening of endocrine disrupting compounds and evaluation of the PPAR dependency of the effect PLoS One 8 10 2013 e77481
111. Y.F. Wang, H.R. Chao, C.H. Wu, C.H. Tseng, Y.T. Kuo, and T.C. Tsou A recombinant peroxisome proliferator response element-driven luciferase assay for evaluation of potential environmental obesogens Biotechnol. Lett. 32 12 2010 1789 1796
112. Y. Sui, N. Ai, S.H. Park, J. Rios-Pilier, J.T. Perkins, W.J. Welsh, and C. Zhou Bisphenol A and its analogues activate human pregnane X receptor Environ. Health Perspect. 120 3 2012 399 405
113. 2+ signals in pancreatic alpha-cells through a nonclassical membrane estrogen receptor within intact islets of Langerhans Environ. Health Perspect. 113 8 2005 969 977
114. J.G. Boucher, A. Boudreau, and E. Atlas Bisphenol A induces differentiation of human preadipocytes in the absence of glucocorticoid and is inhibited by an estrogen-receptor antagonist Nutr. Diabetes 02 2014
115. A. Janesick, and B. Blumberg Minireview: PPARgamma as the target of obesogens J. Steroid Biochem. Mol. Biol. 127 1-2 2011 4 8
116. A. Janesick, and B. Blumberg Obesogens, stem cells and the developmental programming of obesity Int. J. Androl. 35 3 2012 437 448
117. Z. Krozowski, A.L. Albiston, V.R. Obeyesekere, R.K. Andrews, and R.E. Smith The human 11beta-hydroxysteroid dehydrogenase type II enzyme: comparisons with other species and localization to the distal nephron J. Steroid Biochem. Mol. Biol. 55 5-6 1995 457 464
118. B.R. Walker, and C.R. Edwards Licorice-induced hypertension and syndromes of apparent mineralocorticoid excess Endocrinol. Metab. Clin. North Am. 23 2 1994 359 377
119. L. Yu, D.G. Romero, C.E. Gomez-Sanchez, and E.P. Gomez-Sanchez Steroidogenic enzyme gene expression in the human brain Mol. Cell. Endocrinol. 190 1-2 2002 9 17
120. C.S. Wyrwoll, M.C. Holmes, and J.R. Seckl 11Beta-hydroxysteroid dehydrogenases and the brain: from zero to hero, a decade of progress Front. Neuroendocrino. 32 3 2011 265 286
121. T.C. Sandeep, J.L. Yau, A.M. MacLullich, J. Noble, I.J. Deary, B.R. Walker, and J.R. Seckl 11Beta-hydroxysteroid dehydrogenase inhibition improves cognitive function in healthy elderly men and type 2 diabetics Proc. Natl. Acad. Sci. U. S. A. 101 17 2004 6734 6739
122. P.H. Bisschop, M.J. Dekker, W. Osterthun, J. Kwakkel, J.J. Anink, A. Boelen, U.A. Unmehopa, J.W. Koper, S.W. Lamberts, P.M. Stewart, D.F. Swaab, and E. Fliers Expression of 11beta-hydroxysteroid dehydrogenase type 1 in the human hypothalamus J. Neuroendocrinol. 25 5 2013 425 432
123. J.R. Seckl, and B.R. Walker 11Beta-hydroxysteroid dehydrogenase type 1 as a modulator of glucocorticoid action: from metabolism to memory Trends Endocrinol. Metab. 15 9 2004 418 424
124. K. Sooy, S.P. Webster, J. Noble, M. Binnie, B.R. Walker, J.R. Seckl, and J.L. Yau Partial deficiency or short-term inhibition of 11beta-hydroxysteroid dehydrogenase type 1 improves cognitive function in aging mice J. Neurosci. 30 2010 867 13872
125. R.N. Carter, J.M. Paterson, U. Tworowska, D.J. Stenvers, J.J. Mullins, J.R. Seckl, and M.C. Holmes Hypothalamic-pituitary-adrenal axis abnormalities in response to deletion of 11beta-HSD1 is strain-dependent J. Neuroendocrinol. 21 11 2009 879 887
126. K. Sun, K. Yang, and J.R. Challis Differential expression of 11beta-hydroxysteroid dehydrogenase types 1 and 2 in human placenta and fetal membranes J. Clin. Endocrinol. Metab. 82 1 1997 300 305
127. B.R. Walker, and R. Best Clinical investigation of 11beta-hydroxysteroid dehydrogenase Endocr. Res. 21 1-2 1995 379 387
128. Z. Krozowski, J.A. MaGuire, A.N. Stein-Oakley, J. Dowling, R.E. Smith, and R.K. Andrews Immunohistochemical localization of the 11beta-hydroxysteroid dehydrogenase type II enzyme in human kidney and placenta J. Clin. Endocrinol. Metab. 80 7 1995 2203 2209
129. H. Saegusa, Y. Nakagawa, Y.J. Liu, and T. Ohzeki Influence of placental 11beta-hydroxysteroid dehydrogenase (11beta-HSD) inhibition on glucose metabolism and 11beta-HSD regulation in adult offspring of rats Metabolism 48 12 1999 1584 1588
130. B.E. Murphy, S.J. Clark, I.R. Donald, M. Pinsky, and D. Vedady Conversion of maternal cortisol to cortisone during placental transfer to the human fetus Am. J. Obstet. Gynecol. 118 4 1974 538 541
131. A. Hill, R. Paskova, M. Kanceva, J. Velikova, L. Kubatova, K. Kancheva, M. Adamcova, Z. Mikesova, M. Zizka, H. Koucky, V. Sarapatkova, P. Kacer, M. Meloun, and A. Parizek Steroid profiling in pregnancy: a focus on the human fetus J. Steroid Biochem. Mol. Bio. 139 2014 201 222
132. R.S. Lindsay, R.M. Lindsay, C.R. Edwards, and J.R. Seckl Inhibition of 11-beta-hydroxysteroid dehydrogenase in pregnant rats and the programming of blood pressure in the offspring Hypertension 27 6 1996 1200 1204
133. R.S. Lindsay, R.M. Lindsay, B.J. Waddell, and J.R. Seckl Prenatal glucocorticoid exposure leads to offspring hyperglycaemia in the rat: studies with the 11 beta-hydroxysteroid dehydrogenase inhibitor carbenoxolone Diabetologia 39 11 1996 1299 1305
134. D.J. Barker, C. Osmond, J. Golding, D. Kuh, and M.E. Wadsworth Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease BMJ 298 6673 1989 564 567
135. E. Roberts, and P. Wood Birth weight and adult health in historical perspective: evidence from a New Zealand cohort, 1907-1922 Soc. Sci. Med. 107 2014 154 161
136. N. Bergvall, A. Iliadou, T. Tuvemo, and S. Cnattingius Birth characteristics and risk of high systolic blood pressure in early adulthood: socioeconomic factors and familial effects Epidemiology 16 5 2005 635 640
137. J.I. Tang, C.J. Kenyon, J.R. Seckl, and M.J. Nyirenda Prenatal overexposure to glucocorticoids programs renal 11beta-hydroxysteroid dehydrogenase type 2 expression and salt-sensitive hypertension in the rat J. Hypertens. 29 2 2011 282 289
138. L.A. Welberg, J.R. Seckl, and M.C. Holmes Inhibition of 11beta-hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behaviour in the offspring Eur. J. Neurosci. 12 3 2000 1047 1054
139. G.A. Deuchar, D. McLean, P.W. Hadoke, D.G. Brownstein, D.J. Webb, J.J. Mullins, K. Chapman, J.R. Seckl, and Y.V. Kotelevtsev 11beta-hydroxysteroid dehydrogenase type 2 deficiency accelerates atherogenesis and causes proinflammatory changes in the endothelium in apoe-/- mice Endocrinology 152 1 2011 236 246
140. A. Harris, and J. Seckl Glucocorticoids, prenatal stress and the programming of disease Horm. Behav. 59 3 2011 279 289
141. S. Wang, N. Moustaid-Moussa, L. Chen, H. Mo, A. Shastri, R. Su, P. Bapat, I. Kwun, and C.L. Shen Novel insights of dietary polyphenols and obesity J. Nutr. Biochem. 25 1 2014 1 18