Preview

Meditsinskiy sovet = Medical Council

Advanced search

Fat tissue and adrenal function: mechanisms of mutual influence

https://doi.org/10.21518/2079-701X-2019-4-70-77

Abstract

The mechanisms of mutual influence of fat tissue and the hypothalamo-pituitary-adrenal (HPA) axis include the regulation of the metabolism of adipocytes by adrenal cortex hormones, on the one part, and the effect of adipocytes and adipocytokines on secretion, metabolism and action of steroid hormones in target cells - on the other part.

Glucocorticoids contribute to the differentiation of preadipocytes into mature adipocytes; brown fat tissue transforms into white under the effect of GC. Mineralocorticoids are also involved in the process of adipocyte differentiation, regulate adipokine expression, and induce oxidative stress in fat tissue. There is evidence that suggest that circulating dehydroepiandrosterone sulfate (DHEAS), obesity, insulin sensitivity are associated with the presence of cardiovascular diseases.

Orexigenic neuropeptides and inflammatory mediators, which trigger the synthesis of corticotropin-releasing hormone (CRH) in the hypothalamic paraventricular nuclei, are considered as possible mechanisms of (HPA) axis activation in obesity. Expression of 1ip-hydroxysteroid dehydrogenase type 1 (11P-HSD1) in fat tissue and the formation of cortisol from cortisone at the tissue level can be considered as one of the factors involved in development of insulin resistance. The autocrine and paracrine regulatory effect of these hormones on adipocyte function is the consequence of aldosterone production and aromatization of androgens by fat tissue.

About the Authors

N. V. Mazurina
Federal State Budgetary Institution National Medical Research Center of Endocrinology of the Ministry of Health of the Russian Federation
Russian Federation

Mazurina Natalya Valentinovna - Cand. of Sci. (Med.), Leading Researcher, Department of Therapeutic Endocrinology.

117036, Moscow, Dm. Ulyanova St., 11; eLibrary SPIN: 9067-3062



E. V. Ershova
Federal State Budgetary Institution National Medical Research Center of Endocrinology of the Ministry of Health of the Russian Federation
Russian Federation

Ershova Ekaterina Vladimirovna -Cand. of Sci. (Med.), Leading Researcher, Department of Therapeutic Endocrinology.

117036, Moscow, Dm. Ulyanova St., 11; eLibrary SPIN: 6728-3764



E. A. Troshina
Federal State Budgetary Institution National Medical Research Center of Endocrinology of the Ministry of Health of the Russian Federation
Russian Federation

Troshina Ekaterina Anatolyevna - Corr.Member of RAS, Professor, Deputy Director, Institute of Clinical Endocrinology, Head of Department of Therapeutic Endocrinology.

117036, Moscow, Dm. Ulyanova St., 11; eLibrary SPIN: 8821-8990



E. S. Senyushkina
Federal State Budgetary Institution National Medical Research Center of Endocrinology of the Ministry of Health of the Russian Federation
Russian Federation

Senyushkina Evgeniya Semenovna -Researcher, Department of Therapeutic Endocrinology.

117036, Moscow, Dm. Ulyanova St., 11; Tel.: +7 (906) 898-49-61; Library SPIN: 4250-5123



A. N. Tyulpakov
Federal State Budgetary Institution National Medical Research Center of Endocrinology of the Ministry of Health of the Russian Federation
Russian Federation

Tyulpakov Anatoliy Nikolaevich -Dr. of Sci. (Med.), Deputy Director of Center, Director of Institute of Personalized Medicine, Head of Department of Hereditary Endocrino-pathies.

117036, Moscow, Dm. Ulyanova St., 11; eLibrarySPIN: 8396-1798



V. A. Ioutsi
Federal State Budgetary Institution National Medical Research Center of Endocrinology of the Ministry of Health of the Russian Federation
Russian Federation

Ioutsi Vitaly Alekseevich - Cand. of Sci. (Chem.), Head of Metabolism Research Laboratory of Institute of Personalized Medicine.

117036, Moscow, Dm. Ulyanova St., 11; eLibrary SPIN: 9734-0997



References

1. Abraham S., Rubino D., Sinaii N., et aL. Cortisol, obesity, and the metabolic syndrome: a cross-sectional study of obese subjects and review of the literature. Obesity (Silver Spring). 2013;21(1):E105-117. doi: 10.1002/oby.20083.

2. Stalder T., Kirschbaum C., Alexander N., et al. Cortisol in hair and the metabolic syndrome. Journal Clinical Endocrinology Metabolism. 2013;98(6):2573-2580. doi:10.1210/jc.2013-1056.

3. Kuehl L., Hinkelmann K., Muhtz C., et al. Hair cortisol and cortisol awakening response are associated with criteria of the metabolic syndrome in opposite directions. Psychoneuroendocrinology. 2015;51:365-370. doi:10.1016/j.psyneuen.2014.09.012.

4. Vogelzangs N., Suthers K., Ferrucci L., et al. Hypercortisolemic depression is associated with the metabolic syndrome in late-life. Psychoneuroendocrinology. 2007;32(2):151-159. doi: 10.1016/j.psyneuen.2006.11.009.

5. Almadi T., Cathers I., Chow C. Associations among work-related stress, cortisol, inflammation, and metabolic syndrome. Psychophysiology. 2013;50(9):821-830. doi:10.1111/psyp.12069.

6. Jackson S., Kirschbaum C., Steptoe A. Hair cortisol and adiposity in a population-based sample of 2,527 men and women aged 54 to 87 years. Obesity. 2017;25(3):539-544. doi: 10.1002/oby.21733.

7. Pasquali R., Vicennati V., Gambineri A. Adrenal and gonadal function in obesity. Journal of Endocrinological Investigation. 2002 Nov;25(10):893-8. doi: 10.1007/BF03344053.

8. Adrenocortical Dysfunction in Obesity and the Metabolic Syndrom. Hormone and Metabolic Research. 2008 Aug;40(8):515-7. doi: 10.1055/s-2008-1073154.

9. Adipose Tissue and Adrenal Glands: Novel Pathophysiological Mechanisms and Clinical Applications. Hindawi Publishing Corporation International Journal of Endocrinology. 2014 June 11. Article ID 614074, 8 pages http//dx.doi.org/10.1155/2014/61407.

10. Impact of Adrenal Steroids on Regulation of Adipose Tissue. Comprehensive Physiology. 2017 Sep 12;7(4):1425-1447. doi: 10.1002/cphy.c160037.

11. Gardner D., Shobek D. Basic and clinical endocrinology. Book 2. Trans. from English under the editorship of Corr. Member of RAMS, Prof. G.A. Melnichenko M.: BINOM Publishing House, 2018:451-476. (In Russ).

12. Bjorntorp P Hormonal control of regional fat distribution. Hum Reprod. 1997;12(suppl 1):21-25.

13. Rebuffe-Scrive M., Walsh U., McEwen B., Rodin J. Effect of chronic stress and exogenous glucocorticoids on regional fat distribution and metabolism. Physiol Behav. 1992;52(3):583-590.

14. Peckett AJ., Wright D.C. and Riddell M.C. Theeffects of glucocorticoids on adipose tissue lipid metabolism. Metabolism: Clinical and Experimental. 2011;60(11):1500-1510.

15. Lee M., Pramyothin P., K. Karastergiou, and Fried S.K. Deconstructing the roles of glucocorticoids in adipose tissue biology and the development of central obesity. Biochimica et Biophysica Acta: Molecular Basis of Disease. 2014;1842(3):473-481.

16. Tomlinson JJ., Boudreau A., Wu D., Atlas E. and Hachre RJ.G. Modulation of early human preadipocyte differentiation by glucocorticoids, Endocrinology. 2006;147(11):5284-5293.

17. Strack A.M., Bradbury MJ. and Dallman M.F. Corticosterone decreases nonshivering thermogenesis and increases lipid storage in brown adipose tissue.American Journal of Physiology: Regulatory Integrative and Comparative Physiology. 1995;268(1, part 2):R183-R191.

18. Kronenberg G.M., Melmed S., Polonsky K.S., Larsen PR. Diseases of adrenal cortex and endocrine arterial hypertension. Endocrinology according to Williams. Translated from English under the editorship of I.I. Dedov, G.A. Melnichenko. M.: Reed Elsiver, 2010. 208 p. (In Russ).

19. Funder J.W., Pearce P.T., Smith R. and Smith A.I. Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated. Science. 1988;242(4878):583-585.

20. Feher T. and Bodrogi L. A comparative study of steroid concentrations in human adipose tissue and the peripheral circulation, Clinica Chimica Acta. 1982;126(2):135-141.

21. Andrology: Men's health and dysfunction of the reproductive system. Under the editorship of N. Nishlag and G.M. Bere. Translated from English under the editorship of Dedov I.I. M.: International Information Agency, 2005. 554 p. (In Russ).

22. Kalinchenko S.Yu., Tyuzikov I.A. Practical andrology. M.: Practical medicine, 2009. 400 p. (In Russ).

23. Jockenhovel F. Male Hyрogonadism. AuflageBremen: Uni-Med, 2004. 185 р.

24. Rozhivanov R.V. Syndrome of hypogonadism in men. Ozhirenie i Metabolizm. 2014;11(2):30-34. doi: 10.14341/OMET2014230-34. (In Russ).

25. Dedov I.I., Fadeev V.V., Melnichenko G.A. Adrenal insufficiency. M.: Znanie, 2002. 302 p. (In Russ).

26. Maistrenko N.A. Adrenal Surgery. Under the editorship of A.P. Kalinin, N.A. Maistenko. M.: Meditsina, 2000. 216 p. (In Russ).

27. Kattayl V.M., Arki R.A. Pathophysiology of the endocrine system: Translated from English SPb.: Nevsky dialect; BINOM, 2001. 336 p. (In Russ).

28. Fadeev V.V. Adrenal insufficiency (clinical picture, diagnosis, treatment): recommendations for doctors. M.: Medpraktika, 2008. 44 p. (In Russ).

29. Orentreich N., Brind J.L., Rizer R.L., and Vogelman J.H. Age changes and sex differences in serum dehydroepiandrosterone sulfate concentrations throughout adulthood, Journal of Clinical Endocrinology and Metabolism. 1984;59(3):551-555.

30. Trivedi D.P. and Khaw K.T. Dehydroepiandrosterone sulfate and mortality in elderly men and women, Journal of Clinical Endocrinology and Metabolism. 2001;86(9):4171-4177.

31. Rice S.PL., Zhang L., Grennan-Jones F. et al. Dehydroepiandrosterone (DHEA) treatment in vitro inhibits adipogenesis in human omental but not subcutaneous adipose tissue, Molecular and Cellular Endocrinology. 2010;320(1-2):51-57.

32. Hernandez-Morante JJ., Milagro F., Gabaldon J.A., Martinez J.A., Zamora S. and Garaulet M. Effect of DHEA-sulfate on adiponectin gene expression in adipose tissue fromdifferent fat depots in morbidly obese humans. European Journal of Endocrinology. 2006;155(4):593-600.

33. Kochan Z., Karbowska J. Dehydroepiandrosterone upregulates resistin gene expression in white adipose tissue. Molecular and Cellular Endocrinology. 2004;218(1-2):57-64.

34. Tchernof A. and Labrie F. Dehydroepiandrosterone, obesity and cardiovascular disease risk: a review of human studies. European Journal of Endocrinology. 2004;151(1):1-14.

35. Villareal D.T. and Holloszy J.O. Effect of DHEA on abdominal fat and insulin action in elderly women and men: a randomized controlled trial. Journal of the American Medical Association. 2004;292(18):2243-2248.

36. Mayes J.S. and Watson G.H. Direct effects of sex steroid hormones on adipose tissues and obesity. Obesity Reviews. 2004;5(4):197-216.

37. Ramirez M.E., McMurry M.P., Wiebke G.A. et al. Evidence for sex steroid inhibition of lipoprotein lipase in men: comparison of abdominal and femoral adipose tissue. Metabolism: Clinical and Experimental. 1997;46(2):179-185.

38. Brann D.W., de Sevilla L., Zamorano P.L., and Mahesh V.B. Regulation of leptin gene expression and secretion by steroid hormones. Steroids. 1999;64(9):659-663.

39. Seckl J.R. and Walker B.R. Minireview: 11b-Hydroxysteroid Dehydrogenase Type 1 - A Tissue-Specific Amplifier of Glucocorticoid Action. Endocrinology. 2001;142(4)1371-1376. doi:10.1210/endo.142.4.8114.

40. Kilgour R.D., Cardiff K., Rosenthall L. et al. Use of prediction equations to determine the accuracy of whole-body fat and fat-free mass and appendicular skeletal muscle mass measurements from a single abdominal image using computed tomography in advanced cancer patients. Applied Physiology, Nutrition, and Metabolism. 2016;41(1):70-75. doi: 10.1139/apnm-2015-0068.

41. Koska J., De Courten B., Wake DJ. et al. 11-Hydroxysteroid Dehydrogenase Type 1 in Adipose Tissue and Prospective Changes in Body Weight and Insulin Resistance. Obesity. 2006 September;14(9):1515-1522.

42. Gyllenhammer L.E., Alderete T.L., Mahurka S. et. al. Adipose tissue 11(3HSD1 gene expression, pcell function and ectopic fat in obese African Americans versus Hispanics. Obesity (Silver Spring). 2014 Jan; 22(1):14-8. doi: 10.1002/oby.20571.

43. Wake DJ., Walker B.R. Inhibition of 11(3-hydroxysteroid dehydrogenase type 1 in obesity. Endocrine. 2006 February;29(1):101-108. doi: 10.1385/ENDO:29:1:101.

44. Stimson R.H., Walker.B.R. The role and regulation of 11(3-hydroxysteroid dehydrogenase type 1 in obesity and the metabolic syndrome, Hormone Molecular Biology and Clinical Investigation.2013 Sep;15(2):37-48. doi: 10.1515/hmbci-2013-0015.

45. Anagnostis P., Athyros V.G., Tziomalos K. et al. The Pathogenetic Role of Cortisol in the Metabolic Syndrome: A Hypothesis. The Journal of Clinical Endocrinology & Metabolism. 2009 August 1;94(Issue 8):2692-2701. doi: 10.1210/jc.2009-0370.

46. Hirata A., Maeda N., Hiuge A. et al. Blockade of mineralocorticoid receptor reverses adipocyte dysfunction and insulinresistance in obese mice. Cardiovascular Research. 2009;84(1):164-172.

47. Zennaro M., Caprio M., and F'eve B. Mineralocorticoid receptors in the metabolic syndrome. Trends in Endocrinology and Metabolism. 2009;20(9):444-451.

48. Feraco A., Armani A., Mammi C., Fabbri A., Rosano G.M.C., and Caprio M. Role of mineralocorticoid receptor and reninangiotensin-aldosterone system in adipocyte dysfunction and obesity. Journal of Steroid Biochemistry and Molecular Biology. 2013;137:99-106.

49. Ehrhart-Bornstein M., Lamounier-Zepter V., Schraven A. et al. Human adipocytes secrete mineralocorticoid-releasing factors. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(2):14211-14216.

50. Goodfriend T.L., Ball D.L., Egan B.M., Campbell W.B. and Nithipatikom K. Epoxy-keto derivative of linoleic acid stimulates aldosterone secretion, Hypertension. 2004;43(2):358-363.

51. Human adipocytes induce an ERK1/2 MAP kinasesmediated upregulation of steroidogenic acute regulatory protein (StAR) and an angiotensin II - sensitization in human adrenocortical cells. International Journal of Obesity. 2007;31:1605-1616.

52. Briones A.M., Cat A.N.D., Callera G.E. et al. Adipocytes produce aldosterone through calcineurin-dependent signaling pathways: implications in diabetes mellitus-associated obesity and vascular dysfunction. Hypertension. 2012;59(5):1069-1078.

53. Guo C., Ricchiuti V., Lian B.O. et al. Mineralocorticoid receptor blockade reverses obesity-related changes in expression of adiponectin, peroxisome proliferator-activated receptor-, and proinflammatory adipokines. Circulation. 2008;117(17):2253-2261.

54. Gerstein H.C., Yusuf S., Mann J.F.E. et al. Effects of Ramipril on cardiovascular and microvascular outcomes in people with diabetes mellitus: results of the HOPE study and MICROHOPE substudy. The Lancet. 2000;355(9200):253-259.

55. Pitt B., Zannad F., Remme WJ. et al., The effect of spironolactone on morbidity and mortality in patients with severe heart failure. The New England Journal of Medicine. 1999;341(10):709-717.

56. Pitt B., Remme W., Zannad F. et al. Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. The New England Journal of Medicine. 2003;348(14):1309-1321.

57. Pasquali R., Casimirri F., Cantobelli S., Labate A.M. Insulin and androgen relationships with abdominal body fat distribution in women with and without hyperandrogenism. Hormone research in Paediatrics. 1993;39(5-6):179-87. doi. org/10.1159/000182732.

58. Ohlson L.O., Larsson B., Svardsudd K. et al. The influence of body fat distribution on the incidence of diabetes mellitus. 13.5 years of follow-up of the participants in the study of men born in 1913. Diabetes. 1985 Oct;34(10):1055-8.

59. Incollingo Rodriguez A.C., Epel E.S., White M.L. et al., Hypothalamic-pituitary-adrenal axis dysregulation and cortisol activity in obesity: A systematic review. Psychoneuroendocrinology. 2015 Dec;62:301-18. doi: 10.1016/j.psyneuen.2015.08.014.

60. Rosmond R., Bjorntorp P. The interactions between hypothalamic-pituitary-adrenal axis activity, testosterone, insulin-like growth factor I and abdominal obesity with metabolism and blood pressure in men. International Journal of Obesity and Related Metabolic Disorders. 1998 Dec;22(12):1184-96.

61. Moyer A.E., Rodin J., Grilo C.M. et al. Stress-induced cortisol response and fat distribution in women, Obesity Research homepage. 1994 May;2(3):255-62.

62. Duclos M., Gatta B., CorcuffJ.B. et al. Fat distribution in obese women is associated with subtle alterations of the hypothalamic-pituitary-adrenal axis activity and sensitivity to glucocorticoids. Clincal Endocrinology 2001 Oct;55(4):447-54.

63. Jessop D.S., Dallman M.F., Fleming D. et al. Resistance to glucocorticoid feedback in obesity. The Journal of Clinical Endocrinology & Metabolism. 2001 September 1;86(Issue 9):4109-4114. doi: 10.1210/jcem.86.9.7826.

64. Xiao F.Y., Lu F.E. Research advancement of adipocytokine adiponectin. Sheng Li Ke Xue Jin Zhan.. 2003 Oct;34(4):309-13.

65. Seres J., Bornstein S.R., Seres P. et al. Corticotropin-releasing hormone system in human adipose tissue. The Journal of Clinical Endocrinology & Metabolism. 2004 February 1;89(Issue 2):965-970. doi: 10.1210/jc.2003-031299.

66. Fahlbusch F.B., Ruebner M., Volkert G. et al., Corticotropin-releasing hormone stimulates expression of leptin, 11beta-HSD2 and syncytin-1 in primary human trophoblasts. Reproductive Biology and Endocrinology 2012 Sep 12;10:80. doi: 10.1186/1477-7827-10-80.

67. Subbannayya T., Balakrishnan L., Sudarshan G. et al., An integrated map of corticotropin-releasing hormone signaling pathway. Journal of Cell Communication and Signaling. 2013 Dec;7(4):295-300. doi: 10.1007/s12079-013-0197-3.

68. Dermitzaki E., Liapakis G., Androulidaki A. et al. Corticotrophin-Releasing Factor (CRF) and the urocortins are potent regulators of the inflammatory phenotype of human and mouse white adipocytes and the differentiation of mouse 3T3L1 pre-adipocytes. PLoS One._ 2014 May 16;9(5):e97060. doi: 10.1371/journal.pone.0097060.

69. Kanczkowski W., Sue M., Bornstein S.R. The adrenal gland microenvironment in health, disease and during regeneration. HORMONES. 2017;16(3):251-265. doi: 10.14310/horm.2002.1744.

70. Swierczynska M.M., Lamounier-Zepter V., Bornstein S.R., Eaton S., Lipoproteins and hedgehog signaling - possible implications for the adrenal glandfunction. EurJ Clin Invest. 2013;43:1178-1183.

71. Kraemer F.B. Adrenal cholesterol utilization. Mol Cell Endocrinol. 2007;265-266:42-45.

72. Sarel I., Widmaier E.P. Stimulation of steroidogenesis in cultured rat adrenocortical cells by unsaturated fatty acids. Am J Physiol. 1995;268:R1484-R1490.

73. Tsai Y.Y., Rainey W.E., Bollag W.B. Very lowdensity lipoprotein (VLDL)-induced signals mediating aldosterone production. J Endocrinol. 2017;232:R115-R129.

74. Tsai Y.Y., Rainey W.E., Johnson M.H., Bollag W.B. VLDL-activated cell signaling pathways that stimulateadrenal cell aldosterone production. Mol Cell Endocrinol. 2016;433:138-146.

75. Trifan A., Chiriac S., Stanciu C. Update on adrenal insufficiency in patients with liver cirrhosis. World J Gastroenterol. 2013;19:445-456.

76. Vergeer M., Korporaal SJ., Franssen R., et al. Genetic variant of the scavenger receptor BI in humans. N Engl J Med. 2011;364:136-145.

77. Illingworth D.R., Lees A.M., Lees R.S. Adrenal cortical function in homozygous familial hypercholesterolemia. Metabolism. 1983;32:1045-1052.

78. Mina T.H., Lahti M., Drake AJ., et al. Maternal lipids in pregnancy are associated with increased offspring cortisol reactivity in childhood. Psychoneuroendocrinology. 2017;83:79-83.

79. Swierczynska M.M., Mateska I., Peitzsch M., et al. Changes in morphology and function of adrenal cortex in mice fed a high-fat diet. Int J Obes (Lond). 2015;39:321-330.


Review

For citations:


Mazurina NV, Ershova EV, Troshina EA, Senyushkina ES, Tyulpakov AN, Ioutsi VA. Fat tissue and adrenal function: mechanisms of mutual influence. Meditsinskiy sovet = Medical Council. 2019;(4):70-77. (In Russ.) https://doi.org/10.21518/2079-701X-2019-4-70-77

Views: 1088


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2079-701X (Print)
ISSN 2658-5790 (Online)