Hematopoietic androgen receptor deficiency promotes visceral fat deposition in male mice without impairing glucose homeostasis

Andrology

Volumn 3, Issue 4, 2015, Pages 787-796

  Rubinow, K B ^a   Wang, S ^a   Den Hartigh, L J ^a   Subramanian, S ^a   Morton, G J ^a   Buaas, F W ^b   Lamont, D ^b   Gray, N ^b   Braun, R E ^b   Page, S T ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b JACKSON LABORATORY   (United States)

Author keywords

Androgen receptor; Androgens; Immunology; Metabolic syndrome; Obesity; Testosterone

Indexed keywords

ADIPONECTIN; ANDROGEN RECEPTOR; CHOLESTEROL; GLUCOSE; INSULIN; INTERLEUKIN 6; LEPTIN; TESTOSTERONE; TRIACYLGLYCEROL;

ADIPOSE TISSUE; ANDROGEN DEFICIENCY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; BODY FAT DISTRIBUTION; BONE MARROW CELL; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; FAT MASS; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE TOLERANCE; HEMATOPOIETIC CELL; INSULIN BLOOD LEVEL; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; INTRAABDOMINAL FAT; LIPID DIET; LIPID STORAGE; MACROPHAGE; MALE; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PARACRINE SIGNALING; PHENOTYPE; PRIORITY JOURNAL; SUBCUTANEOUS FAT; ADIPOCYTE; ANIMAL; BLOOD; C57BL MOUSE; DEFICIENCY; IMMUNOLOGY; INSULIN RESISTANCE; KNOCKOUT MOUSE; LIPOGENESIS; LIVER; METABOLISM; OBESITY; PHYSIOLOGY; RANDOMIZATION;

ADIPOCYTES; ADIPONECTIN; ADIPOSITY; ANIMALS; BONE MARROW CELLS; DIET, HIGH-FAT; GLUCOSE; INSULIN RESISTANCE; INTRA-ABDOMINAL FAT; LIPOGENESIS; LIVER; MACROPHAGES; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; PARACRINE COMMUNICATION; RANDOM ALLOCATION; RECEPTORS, ANDROGEN;

EID: 84937518739     PISSN: 20472919     EISSN: 20472927     Source Type: Journal    
DOI: 10.1111/andr.12055     Document Type: Article

References (48)

1. Allan CA, Strauss BJ & McLachlan RI. (2007) Body composition, metabolic syndrome and testosterone in ageing men. Int J Impot Res 19, 448-457.
2. Bastard JP, Maachi M, Lagathu C, Kim MJ, Caron M, Vidal H, Capeau J & Feve B. (2006) Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 17, 4-12.
3. Blouin K, Nadeau M, Perreault M, Veilleux A, Drolet R, Marceau P, Mailloux J, Luu-The V & Tchernof A. (2010) Effects of androgens on adipocyte differentiation and adipose tissue explant metabolism in men and women. Clin Endocrinol (Oxf) 72, 176-188.
4. Braga-Basaria M, Dobs AS, Muller DC, Carducci MA, John M, Egan J & Basaria S. (2006) Metabolic syndrome in men with prostate cancer undergoing long-term androgen-deprivation therapy. J Clin Oncol 24, 3979-3983.
5. Cao H. (2014) Adipocytokines in obesity and metabolic disease. J Endocrinol 220, T47-T59.
6. Chakraborty P, William Buaas F, Sharma M, Smith BE, Greenlee AR, Eacker SM & Braun RE. (2014) Androgen-dependent sertoli cell tight junction remodeling is mediated by multiple tight junction components. Mol Endocrinol 28, 1055-1072.
7. Chazenbalk G, Bertolotto C, Heneidi S, Jumabay M, Trivax B, Aronowitz J, Yoshimura K, Simmons CF, Dumesic DA & Azziz R. (2011) Novel pathway of adipogenesis through cross-talk between adipose tissue macrophages, adipose stem cells and adipocytes: evidence of cell plasticity. PLoS ONE 6, e17834.
8. Chazenbalk G, Singh P, Irge D, Shah A, Abbott DH & Dumesic DA. (2013) Androgens inhibit adipogenesis during human adipose stem cell commitment to preadipocyte formation. Steroids 78, 920-926.
9. Corona G, Rastrelli G, Morelli A, Vignozzi L, Mannucci E & Maggi M. (2011) Hypogonadism and metabolic syndrome. J Endocrinol Invest 34, 557-567.
10. Dieudonne MN, Pecquery R, Leneveu MC & Giudicelli Y. (2000) Opposite effects of androgens and estrogens on adipogenesis in rat preadipocytes: evidence for sex and site-related specificities and possible involvement of insulin-like growth factor 1 receptor and peroxisome proliferator-activated receptor gamma2. Endocrinology 141, 649-656.
11. Ding EL, Song Y, Malik VS & Liu S. (2006) Sex differences of endogenous sex hormones and risk of type 2 diabetes: a systematic review and meta-analysis. JAMA 295, 1288-1299.
12. Dubois V, Laurent M, Boonen S, Vanderschueren D & Claessens F. (2012) Androgens and skeletal muscle: cellular and molecular action mechanisms underlying the anabolic actions. Cell Mol Life Sci 69, 1651-1667.
13. Eggers H, Brendel B, Duijndam A & Herigault G. (2011) Dual-echo Dixon imaging with flexible choice of echo times. Magn Reson Med 65, 96-107.
14. Fan W, 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.
15. Figueroa F, Davicino R, Micalizzi B, Oliveros L & Forneris M. (2012) Macrophage secretions modulate the steroidogenesis of polycystic ovary in rats: effect of testosterone on macrophage pro-inflammatory cytokines. Life Sci 90, 733-739.
16. Folch J, Lees M & Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226, 497-509.
17. Gerriets VA & MacIver NJ. (2014) Role of T cells in malnutrition and obesity. Front Immunol 5, 379.
18. Gilliver SC, Ashworth JJ, Mills SJ, Hardman MJ & Ashcroft GS. (2006) Androgens modulate the inflammatory response during acute wound healing. J Cell Sci 119, 722-732.
19. Gupta V, Bhasin S, Guo W, Singh R, Miki R, Chauhan P, Choong K, Tchkonia T, Lebrasseur NK, Flanagan JN, Hamilton JA, Viereck JC, Narula NS, Kirkland JL & Jasuja R. (2008) Effects of dihydrotestosterone on differentiation and proliferation of human mesenchymal stem cells and preadipocytes. Mol Cell Endocrinol 296, 32-40.
20. Kanda H, Tateya S, Tamori Y, Kotani K, Hiasa K, Kitazawa R, Kitazawa S, Miyachi H, Maeda S, Egashira K & Kasuga M. (2006) MCP-1 contributes to macrophage infiltration into adipose tissue, insulin resistance, and hepatic steatosis in obesity. J Clin Invest 116, 1494-1505.
21. Kawano H, Sato T, Yamada T, Matsumoto T, Sekine K, Watanabe T, Nakamura T, Fukuda T, Yoshimura K, Yoshizawa T, Aihara K, Yamamoto Y, Nakamichi Y, Metzger D, Chambon P, Nakamura K, Kawaguchi H & Kato S. (2003) Suppressive function of androgen receptor in bone resorption. Proc Natl Acad Sci U S A 100, 9416-9421.
22. Keating NL, O'Malley A, Freedland SJ & Smith MR. (2012) Diabetes and cardiovascular disease during androgen deprivation therapy: observational study of veterans with prostate cancer. J Natl Cancer Inst 104, 1518-1523.
23. Kerwin W, Xu D, Liu F, Saam T, Underhill H, Takaya N, Chu B, Hatsukami T & Yuan C. (2007) Magnetic resonance imaging of carotid atherosclerosis: plaque analysis. Top Magn Reson Imaging 18, 371-378.
24. Keuper M, Blüher M, Schön MR, Möller P, Dzyakanchuk A, Amrein K, Debatin KM, Wabitsch M & Fischer-Posovszky P. (2011) An inflammatory micro-environment promotes human adipocyte apoptosis. Mol Cell Endocrinol 339, 105-113.
25. Kotnik P, Keuper M, Wabitsch M & Fischer-Posovszky P. (2013) Interleukin-1β downregulates RBP4 secretion in human adipocytes. PLoS ONE 8, e57796.
26. Lacasa D, Taleb S, Keophiphath M, Miranville A & Clement K. (2007) Macrophage-secreted factors impair human adipogenesis: involvement of proinflammatory state in preadipocytes. Endocrinology 148, 868-877.
27. Lai JJ, Lai KP, Chuang KH, Chang P, Yu IC, Lin WJ & Chang C. (2009) Monocyte/macrophage androgen receptor suppresses cutaneous wound healing in mice by enhancing local TNF-alpha expression. J Clin Invest 119, 3739-3751.
28. Lai JJ, Lai KP, Zeng W, Chuang KH, Altuwaijri S & Chang C. (2012) Androgen receptor influences on body defense system via modulation of innate and adaptive immune systems: lessons from conditional AR knockout mice. Am J Pathol 181, 1504-1512.
29. Lin HY, Yu IC, Wang RS, Chen YT, Liu NC, Altuwaijri S, Hsu CL, Ma WL, Jokinen J, Sparks JD, Yeh S & Chang C. (2008) Increased hepatic steatosis and insulin resistance in mice lacking hepatic androgen receptor. Hepatology 47, 1924-1935.
30. Mauras N, Hayes V, Welch S, Rini A, Helgeson K, Dokler M, Veldhuis JD & Urban RJ. (1998) Testosterone deficiency in young men: marked alterations in whole body protein kinetics, strength, and adiposity. J Clin Endocrinol Metab 83, 1886-1892.
31. Nishizawa H, Shimomura I, Kishida K, Maeda N, Kuriyama H, Nagaretani H, Matsuda M, Kondo H, Furuyama N, Kihara S, Nakamura T, Tochino Y, Funahashi T & Matsuzawa Y. (2002) Androgens decrease plasma adiponectin, an insulin-sensitizing adipocyte-derived protein. Diabetes 51, 2734-2741.
32. Page ST, Herbst KL, Amory JK, Coviello AD, Anawalt BD, Matsumoto AM & Bremner WJ. (2005) Testosterone administration suppresses adiponectin levels in men. J Androl 26, 85-92.
33. Pasquali R. (2006) Obesity and androgens: facts and perspectives. Fertil Steril 85, 1319-1340.
34. Rana K, Fam BC, Clarke MV, Pang TP, Zajac JD & MacLean HE. (2011) Increased adiposity in DNA binding-dependent androgen receptor knockout male mice associated with decreased voluntary activity and not insulin resistance. Am J Physiol Endocrinol Metab 301, E767-E778.
35. Rana K, Lee NK, Zajac JD & Maclean HE (2014) Expression of androgen receptor target genes in skeletal muscle. Asian J Androl 16, 675-683.
36. Ray R, Novotny NM, Crisostomo PR, Lahm T, Abarbanell A & Meldrum DR. (2008) Sex steroids and stem cell function. Mol Med 14, 493-501.
37. 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. (2011) Myeloid-specific estrogen receptor alpha deficiency impairs metabolic homeostasis and accelerates atherosclerotic lesion development. Proc Natl Acad Sci U S A 108, 16457-16462.
38. Rubinow KB, Snyder CN, Amory JK, Hoofnagle AN & Page ST. (2012) Acute testosterone deprivation reduces insulin sensitivity in men. Clin Endocrinol (Oxf) 76, 281-288.
39. Rubinow KB, Wall VZ, Nelson J, Mar D, Bomsztyk K, Askari B, Lai M, Smith KD, Han MS, Vivekanandan-Giri A, Pennathur S, Albert CJ, Ford DA, Davis RJ & Bornfeldt KE (2013) Acyl-CoA Synthetase 1 is Induced by Gram-Negative Bacteria and Lipopolysaccharide and is Required for Phospholipid Turnover in Stimulated Macrophages. J Biol Chem 288, 9957-9970.
40. Serreze DV & Leiter EH. (1991) Development of diabetogenic T cells from NOD/Lt marrow is blocked when an allo-H-2 haplotype is expressed on cells of hemopoietic origin, but not on thymic epithelium. J Immunol 147, 1222-1229.
41. Shaikh SR, Haas KM, Beck MA & Teague H (2014) The effects of diet-induced obesity on B cell function. Clin Exp Immunol 179, 90-99.
42. Subramanian S, Goodspeed L, Wang S, Kim J, Zeng L, Ioannou GN, Haigh WG, Yeh MM, Kowdley KV, O'Brien KD, Pennathur S & Chait A. (2011) Dietary cholesterol exacerbates hepatic steatosis and inflammation in obese LDL receptor-deficient mice. J Lipid Res 52, 1626-1635.
43. Suganami T & Ogawa Y. (2010) Adipose tissue macrophages: their role in adipose tissue remodeling. J Leukoc Biol 88, 33-39.
44. Tagzirt M, Corseaux D, Pasquesoone L, Mouquet F, Roma-Lavisse C, Ung A, Lorenzi R, Jude B, Elkalioubie A, Van Belle E, Susen S & Dupont A. (2014) Alterations in neutrophil production and function at an early stage in the high-fructose rat model of metabolic syndrome. Am J Hypertens 27, 1096-1104.
45. Tang W, Zeve D, Suh JM, Bosnakovski D, Kyba M, Hammer RE, Tallquist MD & Graff JM. (2008) White fat progenitor cells reside in the adipose vasculature. Science 322, 583-586.
46. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA & Chen H. (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112, 1821-1830.
47. 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. J Steroid Biochem Mol Biol 109, 254-257.
48. Zarotsky V, Huang MY, Carman W, Morgentaler A, Singhal PK, Coffin D & Jones TH. (2014) Systematic literature review of the risk factors, comorbidities, and consequences of hypogonadism in men. Andrology 2, 819-834.