Developmental androgen excess disrupts reproduction and energy homeostasis in adult male mice

Journal of Endocrinology

Volumn 219, Issue 3, 2013, Pages 259-268

  Nohara, Kazunari ^a   Liu, Suhuan ^a,e   Meyers, Matthew S ^a   Waget, Aurélie ^c   Ferron, Mathieu ^c,f   Karsenty, Gérard ^c   Burcelin, Rémy ^d   Mauvais Jarvis, Franck ^a,b  

^a NORTHWESTERN UNIVERSITY   (United States)

^b TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c Columbia University ^*  (United States)

^d Université de Toulouse   (France)

^e THE FIRST AFFILIATED HOSPITAL OF XIAMEN UNIVERSITY   (China)

^f CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

Androgens; Energy homeostasis; Reproduction

Indexed keywords

ANDROGEN; GONADOTROPIN; LEPTIN; METASTIN; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY COMPOSITION; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENERGY BALANCE; ENERGY EXPENDITURE; GLUCOSE HOMEOSTASIS; GONADOTROPIN BLOOD LEVEL; HOMEOSTASIS; HYPOGONADISM; HYPOGONADOTROPIC HYPOGONADISM; HYPOTHALAMUS; INSULIN SENSITIVITY; LOCOMOTION; MALE; MOUSE; NERVE CELL; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; REPRODUCTION; SUBCUTANEOUS TISSUE; TESTOSTERONE BLOOD LEVEL; UPREGULATION; WHITE ADIPOSE TISSUE;

ANDROGENS; ENERGY HOMEOSTASIS; REPRODUCTION;

ADIPOSITY; ANDROGENS; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; ENERGY METABOLISM; ENVIRONMENTAL POLLUTANTS; GONADOTROPINS; HYPOGONADISM; HYPOTHALAMUS; INFERTILITY, MALE; KISSPEPTINS; MALE; MICE; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; NEURONS; OBESITY; SUBCUTANEOUS FAT, ABDOMINAL; TESTOSTERONE;

EID: 84890244582     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-13-0230     Document Type: Article

References (46)

1. Abbott DH, Barnett DK, Bruns CM & Dumesic DA 2005 Androgen excess fetal programming of female reproduction: a developmental aetiology for polycystic ovary syndrome? Human Reproduction Update 11 357-374.
2. Ailhaud G, Grimaldi P & Negrel R 1992 Cellular and molecular aspects of adipose tissue development. Annual Review of Nutrition 12 207-233.
3. Alexanderson C, Eriksson E, Stener-Victorin E, Lystig T, Gabrielsson B, Lonn M & Holmang A 2007 Postnatal testosterone exposure results in insulin resistance, enlarged mesenteric adipocytes, and an atherogenic lipid profile in adult female rats: comparisons with estradiol and dihydrotestosterone. Endocrinology 148 5369-5376.
4. d'Anglemont de Tassigny X, Fagg LA, Dixon JP, Day K, Leitch HG, Hendrick AG, Zahn D, Franceschini I, Caraty A, Carlton MB et al. 2007 Hypogonadotropic hypogonadism in mice lacking a functional Kiss1 gene. PNAS 104 10714-10719.
5. Arnold AP & Gorski RA 1984 Gonadal steroid induction of structural sex differences in the central nervous system. Annual Review of Neuroscience 7 413-442.
6. Bouret SG, Draper SJ & Simerly RB 2004 Trophic action of leptin on hypothalamic neurons that regulate feeding. Science 304 108-110.
7. Bruns CM, Baum ST, Colman RJ, Eisner JR, Kemnitz JW, Weindruch R & Abbott DH 2004 Insulin resistance and impaired insulin secretion in prenatally androgenized male rhesus monkeys. Journal of Clinical Endocrinology and Metabolism 89 6218-6223.
8. Chehab FF, Lim ME & Lu R 1996 Correction of the sterility defect in homozygous obese female mice by treatment with the human recombinant leptin. Nature Genetics 12 318-320.
9. Chen J, Ahn KC, Gee NA, Ahmed MI, Duleba AJ, Zhao L, Gee SJ, Hammock BD & Lasley BL 2008 Triclocarban enhances testosterone action: a new type of endocrine disruptor? Endocrinology 149 1173-1179.
10. Corbier P, Edwards DA & Roffi J 1992 The neonatal testosterone surge: a comparative study. Archives Internationales de Physiologie, de Biochimie et de Biophysique 100 127-131.
11. Donato J Jr, Cravo RM, Frazao R, Gautron L, Scott MM, Lachey J, Castro IA, Margatho LO, Lee S, Lee C et al. 2011 Leptin's effect on puberty in mice is relayed by the ventral premammillary nucleus and does not require signaling in Kiss1 neurons. Journal of Clinical Investigation 121 355-368.
12. Eisner JR, Dumesic DA, Kemnitz JW, Colman RJ & Abbott DH 2003 Increased adiposity in female rhesus monkeys exposed to androgen excess during early gestation. Obesity Research 11 279-286.
13. 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.
14. Ferron M, Hinoi E, Karsenty G & Ducy P 2008 Osteocalcin differentially regulates beta cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. PNAS 105 5266-5270.
15. Ferron M, Wei J, Yoshizawa T, Ducy P & Karsenty G 2010 An ELISA-based method to quantify osteocalcin carboxylation in mice. Biochemical and Biophysical Research Communications 397 691-696.
16. Gay VL, Midgley AR Jr & Niswender GD 1970 Patterns of gonadotrophin secretion associated with ovulation. Federation Proceedings 29 1880-1887.
17. Gesta S, Tseng YH & Kahn CR 2007 Developmental origin of fat: tracking obesity to its source. Cell 131 242-256.
18. Haavisto AM, Pettersson K, Bergendahl M, Perheentupa A, Roser JF & Huhtaniemi I 1993 A supersensitive immunofluorometric assay for rat luteinizing hormone. Endocrinology 132 1687-1691.
19. Hotchkiss AK, Furr J, Makynen EA, Ankley GT & Gray LE Jr 2007 In utero exposure to the environmental androgen trenbolone masculinizes female Sprague-Dawley rats. Toxicology Letters 174 31-41.
20. Kauffman AS, Gottsch ML, Roa J, Byquist AC, Crown A, Clifton DK, Hoffman GE, Steiner RA & Tena-SempereM2007 Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 148 1774-1783.
21. Koutcherov Y, Mai JK, Ashwell KW & Paxinos G 2002 Organization of human hypothalamus in fetal development. Journal of Comparative Neurology 446 301-324.
22. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY et al. 2007 Endocrine regulation of energy metabolism by the skeleton. Cell 130 456-469.
23. Louis GW, Greenwald-Yarnell M, Phillips R, Coolen LM, Lehman MN & Myers MG Jr 2011 Molecular mapping of the neural pathways linking leptin to the neuroendocrine reproductive axis. Endocrinology 152 2302-2310.
24. MacLusky NJ & Naftolin F 1981 Sexual differentiation of the central nervous system. Science 211 1294-1302.
25. Morris JA, Jordan CL & Breedlove SM 2004 Sexual differentiation of the vertebrate nervous system. Nature Neuroscience 7 1034-1039.
26. Navarro VM & Tena-Sempere M 2012 Neuroendocrine control by kisspeptins: role in metabolic regulation of fertility. Nature Reviews. Endocrinology 8 40-53.
27. Negri-Cesi P, Colciago A, Pravettoni A, Casati L, Conti L & Celotti F 2008 Sexual differentiation of the rodent hypothalamus: hormonal and environmental influences. Journal of Steroid Biochemistry and Molecular Biology 109 294-299.
28. Nilsson C, Niklasson M, Eriksson E, Bjorntorp P & Holmang A 1998 Imprinting of female offspring with testosterone results in insulin resistance and changes in body fat distribution at adult age in rats. Journal of Clinical Investigation 101 74-78.
29. Nohara K, Zhang Y, Waraich RS, Laque A, Tiano JP, Tong J, Munzberg H & Mauvais-Jarvis F 2011 Early-life exposure to testosterone programs the hypothalamic melanocortin system. Endocrinology 152 1661-1669.
30. Nohara K, Waraich RS, Liu S, Ferron M, Waget A, Meyers MS, Karsenty G, Burcelin R & Mauvais-Jarvis F 2013 Developmental androgen excess programs sympathetic tone and adipose tissue dysfunction and predisposes to a cardiometabolic syndrome in female mice. American Journal of Physiology. Endocrinology and Metabolism 304 E1321-E1330.
31. Pineda R, Garcia-Galiano D, Roseweir A, Romero M, Sanchez-Garrido MA, Ruiz-Pino F, Morgan K, Pinilla L, Millar RP & Tena-Sempere M 2010 Critical roles of kisspeptins in female puberty and preovulatory gonadotropin surges as revealed by a novel antagonist. Endocrinology 151 722-730.
32. 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. American Journal of Physiology. Endocrinology and Metabolism 301 E767-E778.
33. Recabarren SE, Rojas-Garcia PP, Recabarren MP, Alfaro VH, Smith R, Padmanabhan V & Sir-Petermann T 2008 Prenatal testosterone excess reduces sperm count and motility. Endocrinology 149 6444-6448.
34. Sam S, Coviello AD, Sung YA, Legro RS & Dunaif A 2008 Metabolic phenotype in the brothers of women with polycystic ovary syndrome. Diabetes Care 31 1237-1241.
35. 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.
36. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG et al. 2003 The GPR54 gene as a regulator of puberty. New England Journal of Medicine 349 1614-1627.
37. Simerly RB 2002 Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annual Review of Neuroscience 25 507-536.
38. Smith JT, Acohido BV, Clifton DK & Steiner RA 2006 KiSS-1 neurones are direct targets for leptin in the ob/ob mouse. Journal of Neuroendocrinology 18 298-303.
39. Stavreva DA, George AA, Klausmeyer P, Varticovski L, Sack D, Voss TC, Schiltz RL, Blazer VS, Iwanowicz LR & Hager GL 2012 Prevalent glucocorticoid and androgen activity in US water sources. Scientific Reports 2 937.
40. Tena-Sempere M 2006 KiSS-1 and reproduction: focus on its role in the metabolic regulation of fertility. Neuroendocrinology 83 275-281.
41. Weyer C, Funahashi T, Tanaka S, Hotta K, Matsuzawa Y, Pratley RE & Tataranni PA 2001 Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. Journal of Clinical Endocrinology and Metabolism 86 1930-1935.
42. Wolf CJ, Hotchkiss A, Ostby JS, LeBlanc GA & Gray LE Jr 2002 Effects of prenatal testosterone propionate on the sexual development of male and female rats: a dose-response study. Toxicological Sciences 65 71-86.
43. Wu MV, Manoli DS, Fraser EJ, Coats JK, Tollkuhn J, Honda S, Harada N & Shah NM 2009 Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 139 61-72.
44. Xita N & Tsatsoulis A 2006 Review: fetal programming of polycystic ovary syndrome by androgen excess: evidence from experimental, clinical, and genetic association studies. Journal of Clinical Endocrinology and Metabolism 91 1660-1666.
45. Xita N & Tsatsoulis A 2010 Fetal origins of the metabolic syndrome. Annals of the New York Academy of Sciences 1205 148-155.
46. Yildiz BO, Yarali H, Oguz H & Bayraktar M 2003 Glucose intolerance, insulin resistance, and hyperandrogenemia in first degree relatives of women with polycystic ovary syndrome. Journal of Clinical Endocrinology and Metabolism 88 2031-2036.