Testosterone treatment improves metabolic syndrome-induced adipose tissue derangements

Journal of Endocrinology

Volumn 215, Issue 3, 2012, Pages 347-362

  Maneschi, Elena ^a   Morelli, Annamaria ^a   Filippi, Sandra ^a   Cellai, Ilaria ^a   Comeglio, Paolo ^a   Mazzanti, Benedetta ^b   Mello, Tommaso ^a   Calcagno, Alessandra ^c   Sarchielli, Erica ^a   Vignozzi, Linda ^a   Saad, Farid ^d   Vettor, Roberto ^c   Vannelli, Gabriella B ^a   Maggi, Mario ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b CAREGGI UNIVERSITY HOSPITAL   (Italy)

^c UNIVERSITY OF PADOVA   (Italy)

^d BAYER PHARMA AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; GLUCOSE; GLUCOSE TRANSPORTER 4; PERILIPIN; PROTEIN; STAMP2 PROTEIN; TESTOSTERONE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTRAABDOMINAL FAT; LIPID DIET; MALE; METABOLIC SYNDROME X; NONHUMAN; OXYGENATION; PRIORITY JOURNAL; PROADIPOCYTE; RABBIT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; INTRA-ABDOMINAL FAT; MALE; METABOLIC SYNDROME X; RABBITS; RECEPTORS, ANDROGEN; TESTOSTERONE;

EID: 84872198265     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-12-0333     Document Type: Article

References (60)

1. Aguiari P, Leo S, Zavan B, Vindigni V, Rimessi A, Bianchi K, Franzin C, Cortivo R, Rossato M, Vettor R et al. 2008 High glucose induces adipogenic differentiation of muscle-derived stem cells. PNAS 105 1226-1231. (doi:10.1073/pnas.0711402105)
2. Boström P, Andersson L, Rutberg M, Perman J, Lidberg U, Johansson BR, Fernandez-Rodriguez J, Ericson J, Nilsson T, Borén J et al. 2007 SNARE proteins mediate fusion between cytosolic lipid droplets and are implicated in insulin sensitivity. Nature Cell Biology 9 1286-1293. (doi:10.1038/ ncb1648)
3. Brasaemle DL 2007 Thematic review series: adipocyte biology. The perilipin family of structural lipid droplet proteins: stabilization of lipid droplets and control of lipolysis. Journal of Lipid Research 48 2547-2559. (doi:10.1194/ jlr.R700014-JLR200)
4. ChristodoulidesC, LaudesM,CawthornWP, Schinner S, SoosM,O'Rahilly S, Sethi JK & Vidal-Puig A 2006 The Wnt antagonist Dickkopf-1 and its receptors are coordinately regulated during early human adipogenesis. Journal of Cell Science 119 2613-2620. (doi:10.1242/jcs.02975)
5. Christodoulides C, Lagathu C, Sethi JK & Vidal-Puig A 2009 Adipogenesis and WNT signalling. Trends in Endocrinology and Metabolism 20 16-24. (doi:10.1016/j.tem.2008.09.002)
6. Chun KH, Araki K, Jee Y, Lee DH, Oh BC, Huang H, Park KS, Lee SW, Zabolotny JM & Kim YB 2012 Regulation of glucose transport by ROCK1 differs from that of ROCK2 and is controlled by actin polymerization. Endocrinology 153 1649-1662. (doi:10.1210/ en.2011-1036)
7. Corona G, Mannucci E, Schulman C, Petrone L, Mansani R, Cilotti A, Balercia G, Chiarini V, Forti G & Maggi M 2006 Psychobiologic correlates of the metabolic syndrome and associated sexual dysfunction. European Urology 50 595-604. (doi:10.1016/j.eururo.2006.02.053)
8. Corona G, Mannucci E, Forti G & Maggi M 2009 Hypogonadism, ED, metabolic syndrome and obesity: a pathological link supporting cardiovascular diseases. International Journal of Andrology 32 587-598. (doi:10.1111/j.1365-2605.2008.00951.x)
9. Corona G, Monami M, Rastrelli G, Aversa A, Tishova Y, Saad F, Lenzi A, Forti G, Mannucci E & Maggi M 2011a Testosterone and metabolic syndrome: a meta-analysis study. Journal of Sexual Medicine 8 272-283. (doi:10.1111/j.1743-6109.2010.01991.x)
10. Corona G, Monami M, Rastrelli G, Melani C, Balzi D, Sforza A, Forti G, Mannucci E & Maggi M 2011b Is metabolic syndrome a useless category in subjects with high cardiovascular risk? Results from a cohort study in men with erectile dysfunction Journal of Sexual Medicine 8 504-511. (doi:10.1111/j.1743-6109.2010.02126.x)
11. De Lean A, Munson PJ & Rodbard D 1978 Simultaneous analysis of families of sigmoidal curves: applications to bioassay, radioligand assay, and physiological dose-response curves. American Journal of Physiology 235 97-102.
12. Després JP & Lemieux I 2006 Abdominal obesity and metabolic syndrome. Nature 444 881-887. (doi:10.1038/nature05488)
13. Esposito K, Giugliano F, Ciotola M, De Sio M, D'Armiento M & Giugliano D 2008 Obesity and sexual dysfunction, male and female. International Journal of Impotence Research 20 358-365. (doi:10.1038/ ijir.2008.9)
14. FanW, Yanase T, Nomura M, Okabe T, Goto K, Sato T, Kawano H, Kato S & Nawata H 2005 Androgen receptor null male mice develop late-onset obesity caused by decreased energy expenditure and lipolytic activity but show normal insulin sensitivity with high adiponectin secretion. Diabetes 54 1000-1008. (doi:10.2337/diabetes.54.4.1000)
15. Filippi S, Vignozzi L, Morelli A, Chavalmane AK, Sarchielli E, Fibbi B, Saad F, Sandner P, Ruggiano P, Vannelli GB et al. 2009 Testosterone partially ameliorates metabolic profile and erectile responsiveness to PDE5 inhibitors in an animal model of male metabolic syndrome. Journal of Sexual Medicine 6 3274-3288. (doi:10.1111/j.1743-6109.2009.01467.x)
16. Fu M,Wang C, Li Z, Sakamaki T & Pestell RG 2004 Minireview: cyclin D1: normal and abnormal functions. Endocrinology 145 5439-5447. (doi:10.1210/en.2004-0959)
17. Gupta V, Bhasin S, Guo W, Singh R, Miki R, Chauhan P, Choong K, Tchkonia T, Lebrasseur NK, Flanagan JN et al. 2008 Effects of dihydrotestosterone on differentiation and proliferation of human mesenchymal stem cells and preadipocytes. Molecular and Cellular Endocrinology 296 32-40. (doi:10.1016/j.mce.2008.08.019)
18. Halvorsen YD, Bond A, Sen A, Franklin DM, Lea-Currie YR, Sujkowski D, Ellis PN, Wilkison WO & Gimble JM 2001 Thiazolidinediones and glucocorticoids synergistically induce differentiation of human adipose tissue stromal cells: biochemical, cellular, and molecular analysis. Metabolism 50 407-413. (doi:10.1053/meta.2001.21690)
19. Hirata Y, Hosaka T, Iwata T, Le CT, Jambaldorj B, Teshigawara K, Harada N, Sakaue H, Sakai T, Yoshimoto K et al. 2011 Vimentin binds IRAP and is involved in GLUT4 vesicle trafficking. Biochemical and Biophysical Research Communications 405 96-101. (doi:10.1016/j.bbrc.2010.12.134)
20. Hishida T, Naito K, Osada S, Nishizuka M & Imagawa M 2008 Crucial roles of D-type cyclins in the early stage of adipocyte differentiation. Biochemical and Biophysical Research Communications 370 289-294. (doi:10.1016/j.bbrc. 2008.03.091)
21. Hosogai N, Fukuhara A, Oshima K, Miyata Y, Tanaka S, Segawa K, Furukawa S, Tochino Y, Komuro R, Matsuda M et al. 2007 Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes 56 901-911. (doi:10.2337/db06-0911)
22. Huang S & Czech MP 2007 The GLUT4 glucose transporter. Cell Metabolism 5 237-252. (doi:10.1016/j.cmet.2007.03.006)
23. Jacobsson B & Smith U 1972 Effect of cell size on lipolysis and antilipolytic action of insulin in human fat cells. Journal of Lipid Research 13 651-656.
24. Kapoor D, Malkin CJ, Channer KS & Jones TH 2005 Androgens, insulin resistance and vascular disease in men. Clinical Endocrinology 63 239-250. (doi:10.1111/j.1365-2265.2005.02299.x)
25. Korkmaz CG, Korkmaz KS, Kurys P, Elbi C, Wang L, Klokk TI, Hammarstrom C, Troen G, Svindland A, Hager GL et al. 2005 Molecular cloning and characterization of STAMP2, an androgen-regulated six transmembrane protein that is overexpressed in prostate cancer. Oncogene 24 4934-4945. (doi:10.1038/sj.onc.1208677)
26. Kupelian V, Page ST, Araujo AB, Travison TG, Bremner WJ & McKinlay JB 2006 Low sex hormone-binding globulin, total testosterone, and symptomatic androgen deficiency are associated with development of the metabolic syndrome in nonobese men. Journal of Clinical Endocrinology and Metabolism 91 843-850. (doi:10.1210/jc.2005-1326)
27. Laaksonen DE, Niskanen L, Punnonen K, Nyyssönen K, Tuomainen TP, Salonen R, Rauramaa R & Salonen JT 2003 Sex hormones, inflammation and the metabolic syndrome: a population-based study. European Journal of Endocrinology 149 601-608. (doi:10.1530/eje.0.1490601)
28. Lin HY, Xu Q, Yeh S, Wang RS, Sparks JD & Chang C 2005 Insulin and leptin resistance with hyperleptinemia in mice lacking androgen receptor. Diabetes 54 1717-1725. (doi:10.2337/diabetes.54.6.1717)
29. Lin Y, Kokontis J, Tang F, Godfrey B, Liao S, Lin A, Chen Y & Xiang J 2006 Androgen and its receptor promote Bax-mediated apoptosis. Molecular and Cellular Biology 26 1908-1916. (doi:10.1128/MCB.26.5.1908-1916.2006)
30. Mazzanti B, Aldinucci A, Biagioli T, Barilaro A, Urbani S, Dal Pozzo S, Amato MP, Siracusa G, Crescioli C, Manuelli C et al. 2008 Differences in mesenchymal stem cell cytokine profiles between MS patients and healthy donors: implication for assessment of disease activity and treatment. Journal of Neuroimmunology 199 142-150. (doi:10.1016/j.jneuroim.2008. 05.006)
31. Morelli A, Comeglio P, Filippi S, Sarchielli E, Vignozzi L, Maneschi E, Cellai I, Gacci M, Lenzi A, Vannelli GB et al. 2012a Mechanism of action of phosphodiesterase type 5 inhibition in metabolic syndrome-associated prostate alterations: an experimental study in the rabbit. Prostate. In press. (doi:10.1002/pros.22584)
32. Morelli A, Comeglio P, Filippi S, Sarchielli E, Cellai I, Vignozzi L, Yehiely-Cohen R, Maneschi E, Gacci M, Carini M et al. 2012b Testosterone and farnesoid X receptor agonist INT-747 counteract high fat diet-induced bladder alterations in a rabbit model of metabolic syndrome. Journal of Steroid Biochemistry and Molecular Biology 132 80-92. (doi:10.1016/ j.jsbmb.2012.02.007)
33. Moreno-Navarrete JM, Ortega F, Serrano M, Pérez-Pérez R, Sabater M, Ricart W, Tinahones F, Peral B & Fernández-Real JM 2011 Decreased STAMP2 expression in association with visceral adipose tissue dysfunction. Journal of Clinical Endocrinology and Metabolism 96 1816-1825. (doi:10.1210/ jc.2011-0310)
34. Niskanen L, Laaksonen DE, Punnonen K, Mustajoki P, Kaukua J & Rissanen A 2004 Changes in sex hormone-binding globulin and testosterone during weight loss and weight maintenance in abdominally obese men with the metabolic syndrome. Diabetes, Obesity & Metabolism 6 208-215. (doi:10.1111/j.1462-8902.2004.00335.x)
35. Oh JY, Barrett-Connor E, Wedick NM, Wingard DL & Rancho Bernardo Study 2002 Endogenous sex hormones and the development of type 2 diabetes in older men and women: the Rancho Bernardo study. Diabetes Care 25 55-60. (doi:10.2337/diacare.25.1.55)
36. Olefsky JM 1976 The effects of spontaneous obesity on insulin binding, glucose transport, and glucose oxidation of isolated rat adipocytes. Journal of Clinical Investigation 57 842-851. (doi:10.1172/JCI108360)
37. O'Rourke RW, White AE, Metcalf MD, Olivas AS, Mitra P, Larison WG, Cheang EC, Varlamov O, Corless CL, Roberts CT Jr et al. 2011 Hypoxia-induced inflammatory cytokine secretion in human adipose tissue stromovascular cells. Diabetologia 54 1480-1490. (doi:10.1007/s00125- 011-2103-y)
38. Quarta C, Bellocchio L, Mancini G, Mazza R, Cervino C, Braulke LJ, Fekete C, Latorre R, Nanni C, Bucci M et al. 2010 CB(1) signaling in forebrain and sympathetic neurons is a key determinant of endocannabinoid actions on energy balance. Cell Metabolism 11 273-285. (doi:10.1016/ j.cmet.2010.02.015)
39. Raimondi L, De Paoli P, Mannucci E, Lonardo G, Sartiani L, Banchelli G, Pirisino R, Mugelli A & Cerbai E 2004 Restoration of cardiomyocyte functional properties by angiotensin II receptor blockade in diabetic rats. Diabetes 53 1927-1933. (doi:10.2337/diabetes.53.7.1927)
40. Rosano GM, Sheiban I, Massaro R, Pagnotta P, Marazzi G, Vitale C, Mercuro G, Volterrani M, Aversa A & Fini M 2007 Low testosterone levels are associated with coronary artery disease in male patients with angina. International Journal of Impotence Research 19 176-182. (doi:10.1038/sj.ijir. 3901504)
41. Rosen ED & MacDougald OA 2006 Adipocyte differentiation from the inside out. Nature Reviews. Molecular Cell Biology 7 885-896. (doi:10.1038/ nrm2066)
42. Salans LB & Dougherty JW 1971 The effect of insulin upon glucose metabolism by adipose cells of different size. Influence of cell lipid and protein content, age, and nutritional state. Journal of Clinical Investigation 50 1399-1410. (doi:10.1172/JCI106623)
43. Sato T, Matsumoto T, Yamada T, Watanabe T, Kawano H & Kato S 2003 Late onset of obesity in male androgen receptor-deficient (AR KO) mice. Biochemical and Biophysical Research Communications 300 167-171. (doi:10.1016/S0006-291X(02)02774-2)
44. Singh R, Artaza JN, Taylor WE, Gonzalez-Cadavid NF & Bhasin S 2003 Androgens stimulate myogenic differentiation and inhibit adipogenesis in C3H 10T1/2 pluripotent cells through an androgen receptor-mediated pathway. Endocrinology 144 5081-5088. (doi:10.1210/en.2003-0741)
45. Singh R, Artaza JN, Taylor WE, Braga M, Yuan X, Gonzalez-Cadavid NF & Bhasin S 2006 Testosterone inhibits adipogenic differentiation in 3T3-L1 cells: nuclear translocation of androgen receptor complex with b-catenin and T-cell factor 4 may bypass canonical Wnt signaling to down-regulate adipogenic transcription factors. Endocrinology 147 141-154. (doi:10.1210/ en.2004-1649)
46. Smith U 1971 Effect of cell size on lipid synthesis by human adipose tissue in vitro. Journal of Lipid Research 12 65-70.
47. Stellato RK, Feldman HA, Hamdy O, Horton ES & McKinlay JB 2000 Testosterone, sex hormone-binding globulin, and the development of type 2 diabetes in middle-aged men: prospective results from the Massachusetts male aging study. Diabetes Care 23 490-494. (doi:10.2337/ diacare.23.4.490)
48. Student AK, Hsu RY & Lane MD 1980 Induction of fatty acid synthetase synthesis in differentiating 3T3-L1 preadipocytes. Journal of Biological Chemistry 255 4745-4750.
49. Trayhurn P,Wang B &Wood IS 2008 Hypoxia in adipose tissue: a basis for the dysregulation of tissue function in obesity? British Journal of Nutrition 100 227-235. (doi:10.1017/S0007114508971282)
50. Varlamov O, White AE, Carroll JM, Bethea CL, Reddy A, Slayden O, O'Rourke RW & Roberts CT Jr 2012 Androgen effects on adipose tissue architecture and function in nonhuman primates. Endocrinology 153 3100-3110. (doi:10.1210/en.2011-2111)
51. Vettor R, Milan G, Rossato M & Federspil G 2005 Review article: adipocytokines and insulin resistance. Alimentary Pharmacology & Therapeutics 2 3-10. (doi:10.1111/j.1365-2036.2005.02587.x)
52. Vettor R, Milan G, Franzin C, Sanna M, De Coppi P, Rizzuto R & Federspil G 2009 The origin of intermuscular adipose tissue and its pathophysiological implications. American Journal of Physiology. Endocrinology and Metabolism 297 E987-E998. (doi:10.1152/ajpendo.00229.2009)
53. Vignozzi L, Morelli A, Filippi S, Comeglio P, Chavalmane AK, Marchetta M, Toce M, Yehiely-Cohen R, Vannelli GB, Adorini L et al. 2011 Farnesoid X receptor activation improves erectile function in animal models of metabolic syndrome and diabetes. Journal of Sexual Medicine 8 57-77. (doi:10.1111/j.1743-6109.2010.02073.x)
54. Vignozzi L, Morelli A, Sarchielli E, Comeglio P, Filippi S, Cellai I, Maneschi E, Serni S, Gacci M, Carini M et al. 2012 Testosterone protects from metabolic syndrome-associated prostate inflammation: an experimental study in rabbit. Journal of Endocrinology 212 71-84. (doi:10.1530/ JOE-11-0289)
55. Virtue S & Vidal-Puig A 2010 Adipose tissue expandability, lipotoxicity and the metabolic syndrome - an allostatic perspective. Biochimica et Biophysica Acta 1801 338-349. (doi:10.1016/j.bbalip.2009.12.006)
56. Waki H & Tontonoz P 2007 STAMPing out Inflammation. Cell 129 451-452. (doi:10.1016/j.cell.2007.04.022)
57. Wellen KE, Fucho R, Gregor MF, Furuhashi M, Morgan C, Lindstad T, Vaillancourt E, Gorgun CZ, Saatcioglu F & Hotamisligil GS 2007 Coordinated regulation of nutrient and inflammatory responses by STAMP2 is essential for metabolic homeostasis. Cell 129 537-548. (doi:10.1016/j.cell.2007.02.049)
58. Yanase T, Fan W, Kyoya K, Min L, Takayanagi R, Kato S & Nawata H 2008 Androgens and metabolic syndrome: lessons from androgen receptor knock out (ARKO) mice. Journal of Steroid Biochemistry and Molecular Biology 109 254-257. (doi:10.1016/j.jsbmb.2008.03.017)
59. Ye J, Gao Z, Yin J & He Q 2007 Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. American Journal of Physiology. Endocrinology and Metabolism 293 1118-1128. (doi:10.1152/ajpendo.00435.2007)
60. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, Benhaim P, Lorenz HP & Hedrick MH 2001 Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Engineering 7 211-228. (doi:10.1089/107632701300062859)