Startseite Steroid hormones and the stroma-vascular cells of the adipose tissue
Artikel
Lizenziert
Nicht lizenziert Erfordert eine Authentifizierung

Steroid hormones and the stroma-vascular cells of the adipose tissue

  • Fanny Volat und Anne Bouloumié EMAIL logo
Veröffentlicht/Copyright: 9. August 2013
Veröffentlichen auch Sie bei De Gruyter Brill

Abstract

The stroma-vascular fraction (SVF) of adipose tissue (AT) is a heterogeneous cell fraction composed of progenitor cells, endothelial cells, and immune cells. SVF plays a key role in AT homeostasis and growth as well as in obesity-associated pathologies. The SVF cell composition and phenotype are distinct according to AT location and adiposity. Such discrepancies influence AT function and are involved in obesity-associated disorders such as chronic inflammation. Investigations performed in recent years in rodents and humans provided evidence that the stroma-vascular cells contribute to the conversion of steroid hormones in AT and are also steroid targets. This review describes the link between steroids and SVF depending on gender, adiposity, and AT location and highlights the potential role of sex and corticosteroid hormones in adipogenesis, angiogenesis, and their contributions in AT inflammation.


Corresponding author: Anne Bouloumié, INSERM/UPS UMR1048-I2MC, Equipe 1, 1 avenue Jean Poulhès, BP 84225, 31432 Toulouse Cedex 4, France, Phone: +33 5 61 32 56 42, Fax: +33 5 61 32 56 21; and Université Paul Sabatier (UPS), Unité Mixte de Recherche (UMR) 1048, Institut de Maladies Métaboliques et Cardiovasculaires (I2MC), Toulouse, France

This work was supported by funding from Fondation de la Recherche Médicale, Astra-Zeneca, and INSERM.

References

1. Sengenes C, Miranville A, Lolmede K, Curat CA, Bouloumie A. The role of endothelial cells in inflamed adipose tissue. J Intern Med 2007;262:415–21.10.1111/j.1365-2796.2007.01853.xSuche in Google Scholar PubMed

2. Lolmede K, Duffaut C, Zakaroff-Girard A, Bouloumie A. Immune cells in adipose tissue: key players in metabolic disorders. Diabetes Metab 2011;37:283–90.10.1016/j.diabet.2011.03.002Suche in Google Scholar PubMed

3. Blouin K, Nadeau M, Mailloux J, Daris M, Lebel S, Luu-The V, Tchernof A. Pathways of adipose tissue androgen metabolism in women: depot differences and modulation by adipogenesis. Am J Physiol Endocrinol Metab 2009;296:E244–55.10.1152/ajpendo.00039.2008Suche in Google Scholar PubMed

4. Dieudonne MN, Pecquery R, Boumediene A, Leneveu MC, Giudicelli Y. Androgen receptors in human preadipocytes and adipocytes: regional specificities and regulation by sex steroids. Am J Physiol 1998;274:C1645–52.10.1152/ajpcell.1998.274.6.C1645Suche in Google Scholar PubMed

5. Pedersen SB, Fuglsig S, Sjogren P, Richelsen B. Identification of steroid receptors in human adipose tissue. Eur J Clin Invest 1996;26:1051–6.10.1046/j.1365-2362.1996.380603.xSuche in Google Scholar PubMed

6. Urbanet R, Pilon C, Calcagno A, Peschechera A, Hubert EL, Giacchetti G, Gomez-Sanchez C, Mulatero P, Toffanin M, Sonino N, Zennaro MC, Giorgino F, Vettor R, Fallo F. Analysis of insulin sensitivity in adipose tissue of patients with primary aldosteronism. J Clin Endocrinol Metab 2010;95:4037–42.10.1210/jc.2010-0097Suche in Google Scholar PubMed

7. Caprio M, Feve B, Claes A, Viengchareun S, Lombes M, Zennaro MC. Pivotal role of the mineralocorticoid receptor in corticosteroid-induced adipogenesis. FASEB J 2007;21:2185–94.10.1096/fj.06-7970comSuche in Google Scholar PubMed

8. Ackerman GE, Smith ME, Mendelson CR, MacDonald PC, Simpson ER. Aromatization of androstenedione by human adipose tissue stromal cells in monolayer culture. J Clin Endocrinol Metab 1981;53:412–7.10.1210/jcem-53-2-412Suche in Google Scholar PubMed

9. McTernan PG, Anderson LA, Anwar AJ, Eggo MC, Crocker J, Barnett AH, Stewart PM, Kumar S. Glucocorticoid regulation of p450 aromatase activity in human adipose tissue: gender and site differences. J Clin Endocrinol Metab 2002;87:1327–36.10.1210/jcem.87.3.8288Suche in Google Scholar PubMed

10. Alvarez-Garcia V, Gonzalez A, Martinez-Campa C, Alonso-Gonzalez C, Cos S. Melatonin modulates aromatase activity and expression in endothelial cells. Oncol Rep 2013;29:2058–64.10.3892/or.2013.2314Suche in Google Scholar PubMed

11. Lee MJ, Fried SK, Mundt SS, Wang Y, Sullivan S, Stefanni A, Daugherty BL, Hermanowski-Vosatka A. Depot-specific regulation of the conversion of cortisone to cortisol in human adipose tissue. Obesity (Silver Spring) 2008;16:1178–85.10.1038/oby.2008.207Suche in Google Scholar PubMed PubMed Central

12. Iqbal J, Macdonald LJ, Low L, Seckl JR, Yau CW, Walker BR, Hadoke PW. Contribution of endogenous glucocorticoids and their intravascular metabolism by 11beta-HSDs to postangioplasty neointimal proliferation in mice. Endocrinology 2012;153:5896–905.10.1210/en.2012-1481Suche in Google Scholar PubMed PubMed Central

13. Bujalska IJ, Walker EA, Hewison M, Stewart PM. A switch in dehydrogenase to reductase activity of 11 beta-hydroxysteroid dehydrogenase type 1 upon differentiation of human omental adipose stromal cells. J Clin Endocrinol Metab 2002;87:1205–10.Suche in Google Scholar

14. Svendsen PF, Madsbad S, Nilas L, Paulsen SK, Pedersen SB. Expression of 11beta-hydroxysteroid dehydrogenase 1 and 2 in subcutaneous adipose tissue of lean and obese women with and without polycystic ovary syndrome. Int J Obes (Lond) 2009;33:1249–56.10.1038/ijo.2009.165Suche in Google Scholar PubMed

15. Lavery GG, Walker EA, Draper N, Jeyasuria P, Marcos J, Shackleton CH, Parker KL, White PC, Stewart PM. Hexose-6-phosphate dehydrogenase knock-out mice lack 11 beta-hydroxysteroid dehydrogenase type 1-mediated glucocorticoid generation. J Biol Chem 2006;281:6546–51.10.1074/jbc.M512635200Suche in Google Scholar PubMed

16. Tomlinson JW, Sinha B, Bujalska I, Hewison M, Stewart PM. Expression of 11beta-hydroxysteroid dehydrogenase type 1 in adipose tissue is not increased in human obesity. J Clin Endocrinol Metab 2002;87:5630–5.10.1210/jc.2002-020687Suche in Google Scholar PubMed

17. Briones AM, Nguyen Dinh Cat A, Callera GE, Yogi A, Burger D, He Y, Corrêa JW, Gagnon AM, Gomez-Sanchez CE, Gomez-Sanchez EP, Sorisky A, Ooi TC, Ruzicka M, Burns KD, Touyz RM. Adipocytes produce aldosterone through calcineurin-dependent signaling pathways: implications in diabetes mellitus-associated obesity and vascular dysfunction. Hypertension 2012;59:1069–78.10.1161/HYPERTENSIONAHA.111.190223Suche in Google Scholar PubMed

18. Rodeheffer MS, Birsoy K, Friedman JM. Identification of white adipocyte progenitor cells in vivo. Cell 2008;135:240–9.10.1016/j.cell.2008.09.036Suche in Google Scholar PubMed

19. Sengenes C, Lolmede K, Zakaroff-Girard A, Busse R, Bouloumie A. Preadipocytes in the human subcutaneous adipose tissue display distinct features from the adult mesenchymal and hematopoietic stem cells. J Cell Physiol 2005;205:114–22.10.1002/jcp.20381Suche in Google Scholar PubMed

20. Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, Tallquist MD, Graff JM. White fat progenitor cells reside in the adipose vasculature. Science 2008;322:583–6.10.1126/science.1156232Suche in Google Scholar PubMed PubMed Central

21. Mauvais-Jarvis F, Clegg DJ, Hevener AL. The role of estrogens in control of energy balance and glucose homeostasis. Endocr Rev 2013;34:309–38.10.1210/er.2012-1055Suche in Google Scholar PubMed PubMed Central

22. Dos Santos E, Dieudonné MN, Leneveu MC, Sérazin V, Rincheval V, Mignotte B, Chouillard E, De Mazancourt P, Giudicelli Y, Pecquery R. Effects of 17beta-estradiol on preadipocyte proliferation in human adipose tissue: involvement of IGF1-R signaling. Horm Metab Res 2011;42:514–20.10.1055/s-0030-1249639Suche in Google Scholar

23. Yepuru M, Eswaraka J, Kearbey JD, Barrett CM, Raghow S, Veverka KA, Miller DD, Dalton JT, Narayanan R. Estrogen receptor-{beta}-selective ligands alleviate high-fat diet- and ovariectomy-induced obesity in mice. J Biol Chem 2011;285:31292–303.10.1074/jbc.M110.147850Suche in Google Scholar

24. Hartig SM, Feng Q, Ochsner SA, Xiao R, McKenna NJ, McGuire SE, He B. Androgen receptor agonism promotes an osteogenic gene program in preadipocytes. Biochem Biophys Res Commun 2012;434:357–62.10.1016/j.bbrc.2013.03.078Suche in Google Scholar

25. Caprio M, Antelmi A, Chetrite G, Muscat A, Mammi C, Marzolla V, Fabbri A, Zennaro MC, Fève B. Antiadipogenic effects of the mineralocorticoid receptor antagonist drospirenone: potential implications for the treatment of metabolic syndrome. Endocrinology 2011;152:113–25.10.1210/en.2010-0674Suche in Google Scholar

26. Fujioka K, Kajita K, Wu Z, Hanamoto T, Ikeda T, Mori I, Okada H, Yamauchi M, Uno Y, Morita H, Nagano I, Takahashi Y, Ishizuka T. Dehydroepiandrosterone reduces preadipocyte proliferation via androgen receptor. Am J Physiol Endocrinol Metab 2012;302:E694–704.10.1152/ajpendo.00112.2011Suche in Google Scholar

27. Singh R, Artaza JN, Taylor WE, Braga M, Yuan X, Gonzalez-Cadavid NF, Bhasin S. Testosterone inhibits adipogenic differentiation in 3T3-L1 cells: nuclear translocation of androgen receptor complex with beta-catenin and T-cell factor 4 may bypass canonical Wnt signaling to down-regulate adipogenic transcription factors. Endocrinology 2006;147:141–54.10.1210/en.2004-1649Suche in Google Scholar

28. Heinlein CA, Ting HJ, Yeh S, Chang C. Identification of ARA70 as a ligand-enhanced coactivator for the peroxisome proliferator-activated receptor gamma. J Biol Chem 1999;274:16147–52.10.1074/jbc.274.23.16147Suche in Google Scholar

29. Hauner H, Entenmann G, Wabitsch M, Gaillard D, Ailhaud G, Negrel R, Pfeiffer EF. Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium. J Clin Invest 1989;84:1663–70.10.1172/JCI114345Suche in Google Scholar

30. Gaillard D, Wabitsch M, Pipy B, Negrel R. Control of terminal differentiation of adipose precursor cells by glucocorticoids. J Lipid Res 1991;32:569–79.10.1016/S0022-2275(20)42044-9Suche in Google Scholar

31. Baugh JE, Jr., Floyd ZE, Stephens JM. The modulation of STAT5A/GR complexes during fat cell differentiation and in mature adipocytes. Obesity (Silver Spring) 2007;15:583–90.10.1038/oby.2007.500Suche in Google Scholar PubMed

32. Asada M, Rauch A, Shimizu H, Maruyama H, Miyaki S, Shibamori M, Kawasome H, Ishiyama H, Tuckermann J, Asahara H. DNA binding-dependent glucocorticoid receptor activity promotes adipogenesis via Kruppel-like factor 15 gene expression. Lab Invest 2011;91:203–15.10.1038/labinvest.2010.170Suche in Google Scholar PubMed PubMed Central

33. Hoppmann J, Perwitz N, Meier B, Fasshauer M, Hadaschik D, Lehnert H, Klein J. The balance between gluco- and mineralo-corticoid action critically determines inflammatory adipocyte responses. J Endocrinol 2010;204:153–64.10.1677/JOE-09-0292Suche in Google Scholar PubMed

34. Veilleux A, Côté JA, Blouin K, Nadeau M, Pelletier M, Marceau P, Laberge PY, Luu-The V, Tchernof A. Glucocorticoid-induced androgen inactivation by aldo-keto reductase 1C2 promotes adipogenesis in human preadipocytes. Am J Physiol Endocrinol Metab 2012;302:E941–9.10.1152/ajpendo.00069.2011Suche in Google Scholar PubMed

35. Gormsen LC, Høst C, Hjerrild BE, Pedersen SB, Nielsen S, Christiansen JS, Gravholt CH. Estradiol acutely inhibits whole body lipid oxidation and attenuates lipolysis in subcutaneous adipose tissue: a randomized, placebo-controlled study in postmenopausal women. Eur J Endocrinol 2012;167:543–51.10.1530/EJE-12-0422Suche in Google Scholar PubMed

36. Michailidou Z, Turban S, Miller E, Zou X, Schrader J, Ratcliffe PJ, Hadoke PW, Walker BR, Iredale JP, Morton NM, Seckl JR. Increased angiogenesis protects against adipose hypoxia and fibrosis in metabolic disease-resistant 11beta-hydroxysteroid dehydrogenase type 1 (HSD1)-deficient mice. J Biol Chem 2011;287:4188–97.10.1074/jbc.M111.259325Suche in Google Scholar PubMed PubMed Central

37. Cutolo M, Brizzolara R, Atzeni F, Capellino S, Straub RH, Puttini PC. The immunomodulatory effects of estrogens: clinical relevance in immune-mediated rheumatic diseases. Ann NY Acad Sci 2010;1193:36–42.10.1111/j.1749-6632.2009.05383.xSuche in Google Scholar PubMed

38. Bolego C, Cignarella A, Staels B, Chinetti-Gbaguidi G. Macrophage function and polarization in cardiovascular disease: a role of estrogen signaling? Arterioscler Thromb Vasc Biol 2013;33:1127–34.10.1161/ATVBAHA.113.301328Suche in Google Scholar PubMed

39. Ribas V, Drew BG, Le JA, Soleymani T, Daraei P, Sitz D, Mohammad L, Henstridge DC, Febbraio MA, Hewitt SC, Korach KS, Bensinger SJ, Hevener AL. Myeloid-specific estrogen receptor alpha deficiency impairs metabolic homeostasis and accelerates atherosclerotic lesion development. Proc Natl Acad Sci USA 2012;108:16457–62.10.1073/pnas.1104533108Suche in Google Scholar PubMed PubMed Central

40. Malkin CJ, Pugh PJ, Jones RD, Kapoor D, Channer KS, Jones TH. The effect of testosterone replacement on endogenous inflammatory cytokines and lipid profiles in hypogonadal men. J Clin Endocrinol Metab 2004;89:3313–8.10.1210/jc.2003-031069Suche in Google Scholar PubMed

41. Floryk D, Kurosaka S, Tanimoto R, Yang G, Goltsov A, Park S, Thompson TC. Castration-induced changes in mouse epididymal white adipose tissue. Mol Cell Endocrinol 2011;345:58–67.10.1016/j.mce.2011.07.011Suche in Google Scholar PubMed PubMed Central

42. Patsouris D, Neels JG, Fan W, Li PP, Nguyen MT, Olefsky JM. Glucocorticoids and thiazolidinediones interfere with adipocyte-mediated macrophage chemotaxis and recruitment. J Biol Chem 2009;284:31223–35.10.1074/jbc.M109.041665Suche in Google Scholar PubMed PubMed Central

43. Wamil M, Battle JH, Turban S, Kipari T, Seguret D, de Sousa Peixoto R, Nelson YB, Nowakowska D, Ferenbach D, Ramage L, Chapman KE, Hughes J, Dunbar DR, Seckl JR, Morton NM. Novel fat depot-specific mechanisms underlie resistance to visceral obesity and inflammation in 11 beta-hydroxysteroid dehydrogenase type 1-deficient mice. Diabetes 2011;60:1158–67.10.2337/db10-0830Suche in Google Scholar PubMed PubMed Central

44. Matsumoto S, Takebayashi K, Aso Y. The effect of spironolactone on circulating adipocytokines in patients with type 2 diabetes mellitus complicated by diabetic nephropathy. Metabolism 2006;55:1645–52.10.1016/j.metabol.2006.07.025Suche in Google Scholar PubMed

45. Luo P, Dematteo A, Wang Z, Zhu L, Wang A, Kim H-S, Pozzi A, Stafford JM, Luther JM. Aldosterone deficiency prevents high-fat-feeding-induced hyperglycaemia and adipocyte dysfunction in mice. Diabetologia 2013;56:901–10.10.1007/s00125-012-2814-8Suche in Google Scholar PubMed PubMed Central

Received: 2013-5-17
Accepted: 2013-7-11
Published Online: 2013-08-09
Published in Print: 2013-09-01

©2013 by Walter de Gruyter Berlin Boston

Heruntergeladen am 13.10.2025 von https://www.degruyterbrill.com/document/doi/10.1515/hmbci-2013-0023/html
Button zum nach oben scrollen