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The Journal of Clinical Endocrinology & Metabolism Vol. 86, No. 3 1418-1421
Copyright © 2001 by The Endocrine Society

Rapid Communications

Tissue-Specific Dysregulation of Cortisol Metabolism in Human Obesity

Eva Rask, Tommy Olsson, Stefan Soderberg, Ruth Andrew, Dawn E. W. Livingstone, Owe Johnson and Brian R. Walker

Departments of Public Health and Clinical Medicine (E.R., T.O., SS., O.J.), Ume University Hospital, Ume, Sweden; and Department of Medical Sciences (R.A., D.E.W.L., B.R.W.), University of Edinburgh, Western General Hospital, Edinburgh, United Kingdom

Address correspondence to: Brian R. Walker, M.D., Department of Medical Sciences, Endocrinology Unit, The University of Edinburgh, Western General Hospital, EH4 2XU Edinburgh, United Kingdom.

Abstract

Cortisol has been implicated as a pathophysiological mediator in idiopathic obesity, but circulating cortisol concentrations are not consistently elevated. The tissue-specific responses to cortisol may be influenced as much by local prereceptor metabolism as by circulating concentrations. For example, in liver and adipose tissue cortisol is regenerated from inactive cortisone by 11ß-hydroxysteroid dehydrogenase type 1 (11ß-HSD1). In obese Zucker rats 11ß-HSD1 activity is reduced in liver but enhanced in adipose tissue. This study addressed whether the same tissue-specific disruption of cortisol metabolism occurs in human obesity. 34 men were recruited from the MONICA population study in Northern Sweden to represent a wide range of body composition and insulin insensitivity. Plasma cortisol was measured at 0830h and 1230h, after overnight low-dose dexamethasone suppression, after intravenous corticotropin releasing hormone (CRH), and after oral cortisone administration. Urinary cortisol metabolites were measured in a 24 h sample. A subcutaneous fat biopsy was obtained from 16 participants to measure cortisol metabolism in vitro. Higher body mass index was associated with increased total cortisol metabolite excretion (r = 0.47, p < 0.01), but lower plasma cortisol at 1230 h and after dexamethasone, and no difference in response to CRH. Obese men excreted a greater proportion of glucocorticoid as metabolites of cortisone rather than cortisol (r = 0.43, p < 0.02), and converted less cortisone to cortisol after oral administration (r = 0.49, p < 0.01), suggesting impaired hepatic 11ß-HSD1 activity. By contrast, in vitro 11ß-HSD1 activity in subcutaneous adipose tissue was markedly enhanced in obese men (r = 0.66, p < 0.01). We conclude that in obesity, reactivation of cortisone to cortisol by 11ß-HSD1 in liver is impaired, so that plasma cortisol levels tend to fall, and there may be a compensatory increase in cortisol secretion mediated by a normally functioning hypothalamic-pituitary-adrenal axis. However, changes in 11ß-HSD1 are tissue-specific: strikingly enhanced reactivation of cortisone to cortisol in subcutaneous adipose tissue may exacerbate obesity; and it may be beneficial to inhibit this enzyme in adipose tissue in obese patients.




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G. Valsamakis, A. Anwar, J. W. Tomlinson, C. H. L. Shackleton, P. G. McTernan, R. Chetty, P. J. Wood, A. K. Banerjee, G. Holder, A. H. Barnett, et al.
11{beta}-Hydroxysteroid Dehydrogenase Type 1 Activity in Lean and Obese Males with Type 2 Diabetes Mellitus
J. Clin. Endocrinol. Metab., September 1, 2004; 89(9): 4755 - 4761.
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R. Basu, R. J. Singh, A. Basu, E. G. Chittilapilly, C. M. Johnson, G. Toffolo, C. Cobelli, and R. A. Rizza
Splanchnic Cortisol Production Occurs in Humans: Evidence for Conversion of Cortisone to Cortisol Via the 11-{beta} Hydroxysteroid Dehydrogenase (11{beta}-HSD) Type 1 Pathway
Diabetes, August 1, 2004; 53(8): 2051 - 2059.
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J. W. Tomlinson, J. S. Moore, P. M. S. Clark, G. Holder, L. Shakespeare, and P. M. Stewart
Weight Loss Increases 11{beta}-Hydroxysteroid Dehydrogenase Type 1 Expression in Human Adipose Tissue
J. Clin. Endocrinol. Metab., June 1, 2004; 89(6): 2711 - 2716.
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N. M. Morton, L. Ramage, and J. R. Seckl
Down-Regulation of Adipose 11{beta}-Hydroxysteroid Dehydrogenase Type 1 by High-Fat Feeding in Mice: A Potential Adaptive Mechanism Counteracting Metabolic Disease
Endocrinology, June 1, 2004; 145(6): 2707 - 2712.
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J. M. Paterson, N. M. Morton, C. Fievet, C. J. Kenyon, M. C. Holmes, B. Staels, J. R. Seckl, and J. J. Mullins
Metabolic syndrome without obesity: Hepatic overexpression of 11{beta}-hydroxysteroid dehydrogenase type 1 in transgenic mice
PNAS, May 4, 2004; 101(18): 7088 - 7093.
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D. E. Laaksonen, L. Niskanen, K. Punnonen, K. Nyyssonen, T.-P. Tuomainen, V.-P. Valkonen, R. Salonen, and J. T. Salonen
Testosterone and Sex Hormone-Binding Globulin Predict the Metabolic Syndrome and Diabetes in Middle-Aged Men
Diabetes Care, May 1, 2004; 27(5): 1036 - 1041.
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N. M. Morton, J. M. Paterson, H. Masuzaki, M. C. Holmes, B. Staels, C. Fievet, B. R. Walker, J. S. Flier, J. J. Mullins, and J. R. Seckl
Novel Adipose Tissue-Mediated Resistance to Diet-Induced Visceral Obesity in 11{beta}-Hydroxysteroid Dehydrogenase Type 1-Deficient Mice
Diabetes, April 1, 2004; 53(4): 931 - 938.
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J. Seres, S. R. Bornstein, P. Seres, H. S. Willenberg, K. M. Schulte, W. A. Scherbaum, and M. Ehrhart-Bornstein
Corticotropin-Releasing Hormone System in Human Adipose Tissue
J. Clin. Endocrinol. Metab., February 1, 2004; 89(2): 965 - 970.
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J. R. Seckl, N. M. Morton, K. E. Chapman, and B. R. Walker
Glucocorticoids and 11beta-Hydroxysteroid Dehydrogenase in Adipose Tissue
Recent Prog. Horm. Res., January 1, 2004; 59(1): 359 - 393.
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J. Stokes, B. R. Walker, J. C. Campbell, J. R. Seckl, C. O'Brien, and R. Andrew
Altered Peripheral Sensitivity to Glucocorticoids in Primary Open-Angle Glaucoma
Invest. Ophthalmol. Vis. Sci., December 1, 2003; 44(12): 5163 - 5167.
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T. Tsilchorozidou, J. W. Honour, and G. S. Conway
Altered Cortisol Metabolism in Polycystic Ovary Syndrome: Insulin Enhances 5{alpha}-Reduction But Not the Elevated Adrenal Steroid Production Rates
J. Clin. Endocrinol. Metab., December 1, 2003; 88(12): 5907 - 5913.
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P. Alberts, C. Nilsson, G. Selen, L. O. M. Engblom, N. H. M. Edling, S. Norling, G. Klingstrom, C. Larsson, M. Forsgren, M. Ashkzari, et al.
Selective Inhibition of 11{beta}-Hydroxysteroid Dehydrogenase Type 1 Improves Hepatic Insulin Sensitivity in Hyperglycemic Mice Strains
Endocrinology, November 1, 2003; 144(11): 4755 - 4762.
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Body Fat Distribution and Cortisol Metabolism in Healthy Men: Enhanced 5{beta}-Reductase and Lower Cortisol/Cortisone Metabolite Ratios in Men with Fatty Liver
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Obese Zucker Rats Have Reduced Mineralocorticoid Receptor and 11{beta}-Hydroxysteroid Dehydrogenase Type 1 Expression in Hippocampus--Implications for Dysregulation of the Hypothalamic-Pituitary-Adrenal Axis in Obesity
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Leptin Activation of Corticosterone Production in Hepatocytes May Contribute to the Reversal of Obesity and Hyperglycemia in Leptin-Deficient ob/ob Mice
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J. W. Tomlinson, N. Crabtree, P. M. S. Clark, G. Holder, A. A. Toogood, C. H. L. Shackleton, and P. M. Stewart
Low-Dose Growth Hormone Inhibits 11{beta}-Hydroxysteroid Dehydrogenase Type 1 but Has No Effect upon Fat Mass in Patients with Simple Obesity
J. Clin. Endocrinol. Metab., May 1, 2003; 88(5): 2113 - 2118.
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Is 11beta -Hydroxysteroid Dehydrogenase Type 1 a Therapeutic Target? Effects of Carbenoxolone in Lean and Obese Zucker Rats
J. Pharmacol. Exp. Ther., April 1, 2003; 305(1): 167 - 172.
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T. Dimitriou, C. Maser-Gluth, and T. Remer
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D. Tiosano, I. Eisentein, D. Militianu, G. P. Chrousos, and Z.'e. Hochberg
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J. Clin. Endocrinol. Metab., January 1, 2003; 88(1): 379 - 384.
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R. C. Andrews, O. Herlihy, D. E. W. Livingstone, R. Andrew, and B. R. Walker
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J. Clin. Endocrinol. Metab., December 1, 2002; 87(12): 5587 - 5593.
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Tissue-Specific Changes in Peripheral Cortisol Metabolism in Obese Women: Increased Adipose 11{beta}-Hydroxysteroid Dehydrogenase Type 1 Activity
J. Clin. Endocrinol. Metab., July 1, 2002; 87(7): 3330 - 3336.
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A Transgenic Model of Visceral Obesity and the Metabolic Syndrome
Science, December 7, 2001; 294(5549): 2166 - 2170.
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Glucocorticoid Metabolism and Adrenocortical Reactivity to ACTH in Myotonic Dystrophy
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