Preadipocyte 11β-hydroxysteroid dehydrogenase type 1 is a keto-reductase and contributes to diet-induced visceral obesity in vivo

Endocrinology

Volumn 149, Issue 4, 2008, Pages 1861-1868

  De Sousa Peixoto, R A ^a   Turban, S ^a   Battle, J H ^a   Chapman, K E ^a   Seckl, J R ^a   Morton, Nicholas M ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE; 11BETA HYDROXYSTEROID DEHYDROGENASE 1; GLUCOCORTICOID; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; MESSENGER RNA; UNCLASSIFIED DRUG; CYCLIN DEPENDENT KINASE INHIBITOR 1B;

ADIPOCYTE; ADIPOSE STROMAL VASCULAR CELL; ADIPOSE TISSUE CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; C57BL 6 MOUSE; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INACTIVATION; HUMAN; HUMAN CELL; LIPID DIET; MESENTERY; MOUSE; NONHUMAN; OBESITY; OMENTUM; PRIORITY JOURNAL; PROADIPOCYTE; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; C57BL MOUSE; ENZYMOLOGY; FAT INTAKE; GENETICS; INTRAABDOMINAL FAT; MALE; METABOLISM; PHYSIOLOGY; STEM CELL;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; ADIPOCYTES; ANIMALS; CYCLIN-DEPENDENT KINASE INHIBITOR P27; DIETARY FATS; INTRA-ABDOMINAL FAT; MALE; MICE; MICE, INBRED C57BL; OBESITY; RNA, MESSENGER; STEM CELLS;

EID: 41549149177     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2007-1028     Document Type: Article

References (44)

1. Peeke PM, Chrousos GP 1995 Hypercortisolism and obesity. Ann NY Acad Sci 771:665-676
2. Rask E, Olsson T, Soderberg S, Andrew R, Livingstone DE, Johnson O, Walker BR 2001 Tissue-specific dysregulation of cortisol metabolism in human obesity. J Clin Endocrinol Metab 86:1418-1421
3. Rask E, Walker BR, Soderberg S, Livingstone DEW, Eliasson M, Johnson O, Andrew R, Olsson T 2002 Tissue-specific changes in peripheral cortisol metabolism in obese women: increased adipose 11β-hydroxysteroid dehydrogenase type 1 activity. J Clin Endocrinol Metab 87:3330-3336
4. Lindsay RS, Wake DJ, Nair S, Bunt J, Livingstone DEW, Permana PA, Tataranni PA, Walker BR 2003 Subcutaneous adipose 11β-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 88:2738-2744
5. Wake DJ, Rask E, Livingstone DEW, Soderberg S, Olsson T, Walker BR 2003 Local and systemic impact of transcriptional up-regulation of 11β-hydroxysteroid dehydrogenase type 1 in adipose tissue in human obesity. J Clin Endocrinol Metab 88:3983-3988
6. Paulmyer-Lacroix O, Boullu S, Oliver C, Alessi MC, Grino M 2002 Expression of the mRNA coding for 11β-hydroxysteroid dehydrogenase type 1 in adipose tissue from obese patients: an in situ hybridization study. J Clin Endocrinol Metab 87:2701-2705
7. Kannisto K, Pietilainen KH, Ehrenborg E, Rissanen A, Kaprio J, Hamsten A, Yki-Jarvinen H 2004 Overexpression of 11β-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 89:4414-4421
8. Livingstone DE, Jones GC, Smith K, Jamieson PM, Andrew R, Kenyon CJ, Walker BR 2000 Understanding the role of glucocorticoids in obesity: tissue-specific alterations of corticosterone metabolism in obese Zucker rats. Endocrinology 141:560-563
9. Masuzaki H, Paterson J, Shinyama H, Morton NM, Mullins JJ, Seckl JR, Flier JS 2001 A transgenic model of visceral obesity and the metabolic syndrome. Science 294:2166-2170
10. Seckl JR, Walker BR 2004 11β-Hydroxysteroid dehydrogenase type 1 as a modulator of glucocorticoid action: from metabolism to memory. Trends Endocrinol Metab 15:418-424
11. Masuzaki H, Yamamoto H, Kenyon CJ, Elmquist JK, Morton NM, Paterson JM, Shinyama H, Sharp MG, Fleming S, Mullins JJ, Seckl JR, Flier JS 2003 Transgenic amplification of glucocorticoid action in adipose tissue causes high blood pressure in mice. J Clin Invest 112:83-90
12. Morton NM, Paterson JM, Masuzaki H, Holmes MC, Staels B, Fievet C, Walker BR, Flier JS, Mullins JJ, Seckl JR 2004 Novel adipose tissue-mediated resistance to diet-induced visceral obesity in 11β-hydroxysteroid dehydrogenase type 1-deficient mice. Diabetes 53:931-938
13. Kershaw EE, Morton NM, Dhillon H, Ramage L, Seckl JR, Flier JS 2005 Adipocyte-specific glucocorticoid inactivation protects against diet-induced obesity. Diabetes 54:1023-1031
14. Michailidou Z, Jensen MD, Dumesic DA, Chapman KE, Seckl JR, Walker BR, Morton NM 2007 Omental 11β-hydroxysteroid dehydrogenase 1 correlates with fat cell size independently of obesity. Obesity (Silver Spring) 15:1155-1163
15. Napolitano A, Voice M, Edwards CR, Seckl JR, Chapman KE 1998 11β-Hydroxysteroid dehydrogenase 1 in adipocytes: expression is differentiation-dependent and hormonally regulated. J Steroid Biochem Mol Biol 64:251-260
16. Berger J, Tanen M, Elbrecht A, Hermanowski-Vosatka A, Moller DE, Wright SD, Thieringer R 2001 Peroxisome proliferator-activated receptor γ ligands inhibit adipocyte 11β-hydroxysteroid dehydrogenase type 1 expression and activity. J Biol Chem 276:12629-12635
17. Atanasov AG, Nashev LG, Schweizer RA, Frick C, Odermatt A 2004 Hexose-6-phosphate dehydrogenase determines the reaction direction of 11β-hydroxysteroid dehydrogenase type 1 as an oxoreductase. FEBS Lett 571:129-133
18. Yang K, Khalil MW, Strutt BJ, Killinger DW 1997 11β-Hydroxysteroid dehydrogenase 1 activity and gene expression in human adipose stromal cells: effect on aromatase activity. J Steroid Biochem Mol Biol 60:247-253
19. Bujalska IJ, Kumar S, Stewart, PM 1997 Does central obesity reflect "Cushing's disease of the omentum"? Lancet 349:1210-1213
20. Bujalska IJ, Walker EA, Hewison M, Stewart PM 2002 A switch in dehydrogenase to reductase activity of 11β-hydroxysteroid dehydrogenase type 1 upon differentiation of human omental adipose stromal cells. J Clin Endocrinol Metab 87:1205-1210
21. Varma MJ, Breuls RG, Schouten TE, Jurgens WJ, Bontkes HJ, Schuurhuis GJ, van Ham SM, van Milligen FJ 2007 Phenotypical and functional characterization of freshly isolated adipose tissue-derived stem cells. Stem Cells Dev 16:91-104
22. Bujalska IJ, Draper N, Michailidou Z, Tomlinson JW, White PC, Chapman KE, Walker EA, Stewart PM 2005 Hexose-6-phosphate dehydrogenase confers oxo-reductase activity upon 11β-hydroxysteroid dehydrogenase type 1. J Mol Endocrinol 34:675-684
23. Ozols J 1995 Lumenal orientation and post-translational modifications of the liver microsomal 11β-hydroxysteroid dehydrogenase. J Biol Chem 270:2305-2312
24. MacDougald OA, Lane MD 1995 Transcriptional regulation of gene expression during adipocyte differentiation. Annu Rev Biochem 64:345-373
25. Bujalska IJ, Kumar S, Hewison M, Stewart PM 1999 Differentiation of adipose stromal cells: the roles of glucocorticoids and 11β- hydroxysteroid dehydrogenase. Endocrinology 140:3188-3196
26. Barzilai N, She L, Liu BQ, Vuguin P, Cohen P, Wang J, Rossetti L 1999 Decreased visceral adiposity accounts for leptin effect on hepatic but not peripheral insulin action. Diabetes 48:94-98
27. Kotelevtsev Y, Holmes MC, Burchell A, Houston PM, Schmoll D, Jamieson P, Best R, Brown R, Edwards CR, Seckl JR, Mullins JJ 1997 11β-Hydroxysteroid dehydrogenase type 1 knockout mice show attenuated glucocorticoid-inducible responses and resist hyperglycemia on obesity or stress. Proc Natl Acad Sci USA 94:14924-14929
28. Jamieson PM, Chapman KE, Edwards CR, Seckl JR 1995 11β-Hydroxysteroid dehydrogenase is an exclusive 11 β- reductase in primary cultures of rat hepatocytes: effect of physicochemical and hormonal manipulations. Endocrinology 136:4754-4761
29. Lee K, Villena JA, Moon YS, Kim KH, Lee S, Kang C, Sul HS 2003 Inhibition of adipogenesis and development of glucose intolerance by soluble preadipocyte factor-1 (Pref-1). J Clin Invest 111:453-461
30. Hunt CR, Ro JH, Dobson DE, Min HY, Spiegelman BM 1986 Adipocyte P2 gene: developmental expression and homology of 5′-flanking sequences among fat cell-specific genes. Proc Natl Acad Sci USA 83:3786-3790
31. Sakai T, Sakaue H, Nakamura T, Okada M, Matsuki Y, Watanabe E, Hiramatsu R, Nakayama K, Nakayama KI, Kasuga M 2006 Skp2 controls adipocyte proliferation during the development of obesity. J Biol Chem 282:2038-2046
32. Zhang JW, Tang QQ, Vinson C, Lane MD 2004 Dominant-negative C/EBP disrupts mitotic clonal expansion and differentiation of 3T3-L1 preadipocytes. Proc Natl Acad Sci USA 101:43-47
33. Thieringer R, Le Grand CB, Carbin L, Cai TQ, Wong B, Wright SD, Hermanowski-Vosatka A 2001 11β-Hydroxysteroid dehydrogenase type 1 is induced in human monocytes upon differentiation to macrophages. J Immunol 167:30-35
34. Gilmour JS, Coutinho AE, Cailhier JF, Man TY, Clay M, Thomas G, Harris HJ, Mullins JJ, Seckl JR, Savill JS, Chapman KE 2006 Local amplification of glucocorticoids by 11β-hydroxysteroid dehydrogenase type 1 promotes macrophage phagocytosis of apoptotic leukocytes. J Immunol 176:7605-7611
35. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante Jr AW 2003 Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112:1796-1808
36. Hadoke PW, Christy C, Kotelevtsev YV, Williams BC, Kenyon CJ, Seckl JR, Mullins JJ, Walker BR 2001 Endothelial cell dysfunction in mice after transgenic knockout of type 2, but not type 1, 11β-hydroxysteroid dehydrogenase. Circulation 104:2832-2837
37. Low SC, Chapman KE, Edwards CR, Seckl JR 1994 'Liver-type' 11β-hydroxysteroid dehydrogenase cDNA encodes reductase but not dehydrogenase activity in intact mammalian COS-7 cells. J Mol Endocrinol 13:167-174
38. Lakshmi V, Monder C 1985 Evidence for independent 11-oxidase and 11-reductase activities of 11β-hydroxysteroid dehydrogenase: enzyme latency, phase transitions, and lipid requirements. Endocrinology 116:552-560
39. I, Hauner H 2003 Effect of BMI and age on adipose tissue cellularity and differentiation capacity in women. Int J Obes Relat Metab Disord 27:889-895
40. Kralli A, Bohen SP, Yamamoto KR 1995 LEM1, an ATP-binding-cassette transporter, selectively modulates the biological potency of steroid hormones. Proc Natl Acad Sci USA 92:4701-4705
41. Kralli A, Yamamoto KR 1996 An FK506-sensitive transporter selectively decreases intracellular levels and potency of steroid hormones. J Biol Chem 271:17152-17156
42. Vo QD, Gruol DJ 1999 Identification of P-glycoprotein mutations causing a loss of steroid recognition and transport. J Biol Chem 274:20318-20327
43. Gruol DJ, Vo QD, Zee MC 1999 Profound differences in the transport of steroids by two mouse P-glycoproteins. Biochem Pharmacol 58:1191-1199
44. Hauner H, Schmid P, Pfeiffer EF 1987 Glucocorticoids and insulin promote the differentiation of human adipocyte precursor cells into fat cells. J Clin Endocrinol Metab 64:832-835