Sex differences in metabolic homeostasis, diabetes, and obesity

Franck Mauvais-Jarvis1
1Section of Endocrinology & Metabolism, Department of Medicine, Tulane University Health Sciences Center, 1430 Tulane Avenue, New Orleans, LA, 70112, USA

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Klein SL, Schiebinger L, Stefanick ML, Cahill L, Danska J, et al. Opinion: sex inclusion in basic research drives discovery. Proc Natl Acad Sci U S A. 2015;112:5257–8.

Clayton JA, Collins FS. Policy: NIH to balance sex in cell and animal studies. Nature. 2014;509:282–3.

NOT-OD-15-102 Consideration of sex as a biological variable in NIH-funded research http://grants.nih.gov/grants/guide/notice-files/NOT-OD-15-102.html .

Whitfield J. Everything you always wanted to know about sexes. PLoS Biol. 2004;2, e183.

Birky Jr CW. Uniparental inheritance of mitochondrial and chloroplast genes: mechanisms and evolution. Proc Natl Acad Sci U S A. 1995;92:11331–8.

Turner RM. Tales from the tail: what do we really know about sperm motility? J Androl. 2003;24:790–803.

Vague J. La differenciation sexuelle. Facteur determinant des formes de l'obesite. Presse Med. 1947;55:339.

Enzi G, Gasparo M, Biondetti PR, Fiore D, Semisa M, et al. Subcutaneous and visceral fat distribution according to sex, age, and overweight, evaluated by computed tomography. Am J Clin Nutr. 1986;44:739–46.

Karastergiou K, Smith SR, Greenberg AS, Fried SK. Sex differences in human adipose tissues—the biology of pear shape. Biol Sex Differ. 2012;3:13.

Palmer BF, Clegg DJ. The sexual dimorphism of obesity. Mol Cell Endocrinol. 2015;402:113–9.

Rodriguez-Cuenca S, Pujol E, Justo R, Frontera M, Oliver J, et al. Sex-dependent thermogenesis, differences in mitochondrial morphology and function, and adrenergic response in brown adipose tissue. J Biol Chem. 2002;277:42958–63.

Cypess AM, Lehman S, Williams G, Tal I, Rodman D, et al. Identification and importance of brown adipose tissue in adult humans. N Engl J Med. 2009;360:1509–17.

Nookaew I, Svensson PA, Jacobson P, Jernas M, Taube M, et al. Adipose tissue resting energy expenditure and expression of genes involved in mitochondrial function are higher in women than in men. J Clin Endocrinol Metab. 2013;98:E370–378.

Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med. 1996;334:292–5.

Nishizawa H, Shimomura I, Kishida K, Maeda N, Kuriyama H, et al. Androgens decrease plasma adiponectin, an insulin-sensitizing adipocyte-derived protein. Diabetes. 2002;51:2734–41.

Nagy TR, Gower BA, Trowbridge CA, Dezenberg C, Shewchuk RM, et al. Effects of gender, ethnicity, body composition, and fat distribution on serum leptin concentrations in children. J Clin Endocrinol Metab. 1997;82:2148–52.

Rosenbaum M, Nicolson M, Hirsch J, Heymsfield SB, Gallagher D, et al. Effects of gender, body composition, and menopause on plasma concentrations of leptin. J Clin Endocrinol Metab. 1996;81:3424–7.

Uranga AP, Levine J, Jensen M. Isotope tracer measures of meal fatty acid metabolism: reproducibility and effects of the menstrual cycle. Am J Physiol Endocrinol Metab. 2005;288:E547–555.

Carter SL, Rennie C, Tarnopolsky MA. Substrate utilization during endurance exercise in men and women after endurance training. Am J Physiol Endocrinol Metab. 2001;280:E898–907.

Henderson GC. Sexual dimorphism in the effects of exercise on metabolism of lipids to support resting metabolism. Front Endocrinol. 2014;5:162.

Horton TJ, Pagliassotti MJ, Hobbs K, Hill JO. Fuel metabolism in men and women during and after long-duration exercise. J Appl Physiol. 1998;85:1823–32.

Braun B, Mawson JT, Muza SR, Dominick SB, Brooks GA, et al. Women at altitude: carbohydrate utilization during exercise at 4,300 m. J Appl Physiol. 2000;88:246–56.

Lovejoy JC, Champagne CM, de Jonge L, Xie H, Smith SR. Increased visceral fat and decreased energy expenditure during the menopausal transition. Int J Obes. 2008;32:949–58.

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.

Djouadi F, Weinheimer CJ, Saffitz JE, Pitchford C, Bastin J, et al. A gender-related defect in lipid metabolism and glucose homeostasis in peroxisome proliferator-activated receptor alpha-deficient mice. J Clin Invest. 1998;102:1083–91.

Widdowson EM. The response of the sexes to nutritional stress. Proc Nutr Soc. 1976;35:175–80.

Wade GN. Gonadal hormones and behavioral regulation of body weight. Physiol Behav. 1972;8:523–34.

Shi H, Strader AD, Woods SC, Seeley RJ. Sexually dimorphic responses to fat loss after caloric restriction or surgical lipectomy. Am J Physiol Endocrinol Metab. 2007;293:E316–326.

Cortright RN, Koves TR. Sex differences in substrate metabolism and energy homeostasis. Can J Appl Physiol. 2000;25:288–311.

Banning C. The Netherlands during German occupation. Food shortage and public health, first half of 1945. Ann Am Acad Pol Soc Sci. 1946;245:93–110.

Nohara K, Zhang Y, Waraich RS, Laque A, Tiano JP, et al. Early-life exposure to testosterone programs the hypothalamic melanocortin system. Endocrinology. 2011;152:1661–9.

Clegg DJ, Riedy CA, Smith KA, Benoit SC, Woods SC. Differential sensitivity to central leptin and insulin in male and female rats. Diabetes. 2003;52:682–7.

Hallschmid M, Benedict C, Schultes B, Fehm HL, Born J, et al. Intranasal insulin reduces body fat in men but not in women. Diabetes. 2004;53:3024–9.

Frias JP, Macaraeg GB, Ofrecio J, Yu JG, Olefsky JM, et al. Decreased susceptibility to fatty acid-induced peripheral tissue insulin resistance in women. Diabetes. 2001;50:1344–50.

Nuutila P, Knuuti MJ, Maki M, Laine H, Ruotsalainen U, et al. Gender and insulin sensitivity in the heart and in skeletal muscles. Studies using positron emission tomography. Diabetes. 1995;44:31–6.

Basu R, Dalla Man C, Campioni M, Basu A, Klee G, et al. Effects of age and sex on postprandial glucose metabolism: differences in glucose turnover, insulin secretion, insulin action, and hepatic insulin extraction. Diabetes. 2006;55:2001–14.

Perseghin G, Scifo P, Pagliato E, Battezzati A, Benedini S, et al. Gender factors affect fatty acids-induced insulin resistance in nonobese humans: effects of oral steroidal contraception. J Clin Endocrinol Metab. 2001;86:3188–96.

Glumer C, Jorgensen T, Borch-Johnsen K. Prevalences of diabetes and impaired glucose regulation in a Danish population: the Inter99 study. Diabetes Care. 2003;26:2335–40.

Sicree RA, Zimmet PZ, Dunstan DW, Cameron AJ, Welborn TA, et al. Differences in height explain gender differences in the response to the oral glucose tolerance test—the AusDiab study. Diabet Med. 2008;25:296–302.

van Genugten RE, Utzschneider KM, Tong J, Gerchman F, Zraika S, et al. Effects of sex and hormone replacement therapy use on the prevalence of isolated impaired fasting glucose and isolated impaired glucose tolerance in subjects with a family history of type 2 diabetes. Diabetes. 2006;55:3529–35.

Williams JW, Zimmet PZ, Shaw JE, de Courten MP, Cameron AJ, et al. Gender differences in the prevalence of impaired fasting glycaemia and impaired glucose tolerance in Mauritius. Does sex matter? Diabet Med. 2003;20:915–20.

Gale EA, Gillespie KM. Diabetes and gender. Diabetologia. 2001;44:3–15.

Mauvais-Jarvis F, Sobngwi E, Porcher R, Riveline JP, Kevorkian JP, et al. Ketosis-prone type 2 diabetes in patients of sub-Saharan African origin: clinical pathophysiology and natural history of beta-cell dysfunction and insulin resistance. Diabetes. 2004;53:645–53.

Umpierrez GE, Smiley D, Kitabchi AE. Narrative review: ketosis-prone type 2 diabetes mellitus. Ann Intern Med. 2006;144:350–7.

Louet JF, Smith SB, Gautier JF, Molokhia M, Virally ML, et al. Gender and neurogenin3 influence the pathogenesis of ketosis-prone diabetes. Diab Obes Metab. 2008;10:912–20.

Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004;27:1047–53.

Kelly T, Yang W, Chen CS, Reynolds K, He J. Global burden of obesity in 2005 and projections to 2030. Int J Obes. 2008;32:1431–7.

Ford ES, Giles WH, Mokdad AH. Increasing prevalence of the metabolic syndrome among U.S. adults. Diabetes Care. 2004;27:2444–9.

Al-Lawati JA, Mohammed AJ, Al-Hinai HQ, Jousilahti P. Prevalence of the metabolic syndrome among Omani adults. Diabetes Care. 2003;26:1781–5.

Gu D, Reynolds K, Wu X, Chen J, Duan X, et al. Prevalence of the metabolic syndrome and overweight among adults in China. Lancet. 2005;365:1398–405.

Gupta R, Deedwania PC, Gupta A, Rastogi S, Panwar RB, et al. Prevalence of metabolic syndrome in an Indian urban population. Int J Cardiol. 2004;97:257–61.

Navarro G, Allard C, Xu W, Mauvais-Jarvis F. The role of androgens in metabolism, obesity, and diabetes in males and females. Obesity (Silver Spring). 2015;23:713–9.

Waraich RS, Mauvais-Jarvis F. Paracrine and intracrine contributions of androgens and estrogens to adipose tissue biology: physiopathological aspects. Horm Mol Biol Clin Investig. 2013;14:49–55.

Deslypere JP, Verdonck L, Vermeulen A. Fat tissue: a steroid reservoir and site of steroid metabolism. J Clin Endocrinol Metab. 1985;61:564–70.

Borg W, Shackleton CH, Pahuja SL, Hochberg RB. Long-lived testosterone esters in the rat. Proc Natl Acad Sci U S A. 1995;92:1545–9.

Mauvais-Jarvis F. Estrogen sulfotransferase: intracrinology meets metabolic diseases. Diabetes. 2012;61:1353–4.

Gao J, He J, Shi X, Stefanovic-Racic M, Xu M, et al. Sex-specific effect of estrogen sulfotransferase on mouse models of type 2 diabetes. Diabetes. 2012;61:1543–51.

Corbier P, Edwards DA, Roffi J. The neonatal testosterone surge: a comparative study. Arch Int Physiol Biochim Biophys. 1992;100:127–31.

Arnold AP, Gorski RA. Gonadal steroid induction of structural sex differences in the central nervous system. Annu Rev Neurosci. 1984;7:413–42.

MacLusky NJ, Naftolin F. Sexual differentiation of the central nervous system. Science. 1981;211:1294–302.

Simerly RB. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci. 2002;25:507–36.

Morris JA, Jordan CL, Breedlove SM. Sexual differentiation of the vertebrate nervous system. Nat Neurosci. 2004;7:1034–9.

Negri-Cesi P, Colciago A, Pravettoni A, Casati L, Conti L, et al. Sexual differentiation of the rodent hypothalamus: hormonal and environmental influences. J Steroid Biochem Mol Biol. 2008;109:294–9.

Wu MV, Manoli DS, Fraser EJ, Coats JK, Tollkuhn J, et al. Estrogen masculinizes neural pathways and sex-specific behaviors. Cell. 2009;139:61–72.

Mauvais-Jarvis F. Developmental androgenization programs metabolic dysfunction in adult mice: clinical implications. Adipocyte. 2014;3:151–4.

Nohara K, Waraich RS, Liu S, Ferron M, Waget A, et al. Developmental androgen excess programs sympathetic tone and adipose tissue dysfunction and predisposes to a cardiometabolic syndrome in female mice. Am J Physiol Endocrinol Metab. 2013;304:E1321–1330.

Alexanderson C, Eriksson E, Stener-Victorin E, Lystig T, Gabrielsson B, et al. 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. 2007;148:5369–76.

Barnes RB, Rosenfield RL, Ehrmann DA, Cara JF, Cuttler L, et al. Ovarian hyperandrogynism as a result of congenital adrenal virilizing disorders: evidence for perinatal masculinization of neuroendocrine function in women. J Clin Endocrinol Metab. 1994;79:1328–33.

Eisner JR, Dumesic DA, Kemnitz JW, Colman RJ, Abbott DH. Increased adiposity in female rhesus monkeys exposed to androgen excess during early gestation. Obes Res. 2003;11:279–86.

Hague WM, Adams J, Rodda C, Brook CG, de Bruyn R, et al. The prevalence of polycystic ovaries in patients with congenital adrenal hyperplasia and their close relatives. Clin Endocrinol. 1990;33:501–10.

Nilsson C, Niklasson M, Eriksson E, Bjorntorp P, Holmang A. Imprinting of female offspring with testosterone results in insulin resistance and changes in body fat distribution at adult age in rats. J Clin Invest. 1998;101:74–8.

Burgoyne PS. A Y-chromosomal effect on blastocyst cell number in mice. Development. 1993;117:341–5.

Ray PF, Conaghan J, Winston RM, Handyside AH. Increased number of cells and metabolic activity in male human preimplantation embryos following in vitro fertilization. J Reprod Fertil. 1995;104:165–71.

Chen X, McClusky R, Chen J, Beaven SW, Tontonoz P, et al. The number of x chromosomes causes sex differences in adiposity in mice. PLoS Genet. 2012;8, e1002709.

Chen X, McClusky R, Itoh Y, Reue K, Arnold AP. X and Y chromosome complement influence adiposity and metabolism in mice. Endocrinology. 2013;154:1092–104.

Nohara K, Liu S, Meyers MS, Waget A, Ferron M, et al. Developmental androgen excess disrupts reproduction and energy homeostasis in adult male mice. J Endocrinol. 2013;219:259–68.

Arnold AP, Lusis AJ. Understanding the sexome: measuring and reporting sex differences in gene systems. Endocrinology. 2012;153:2551–5.

Yang X, Schadt EE, Wang S, Wang H, Arnold AP, et al. Tissue-specific expression and regulation of sexually dimorphic genes in mice. Genome Res. 2006;16:995–1004.

Mittelstrass K, Ried JS, Yu Z, Krumsiek J, Gieger C, et al. Discovery of sexual dimorphisms in metabolic and genetic biomarkers. PLoS Genet. 2011;7, e1002215.

Donnelly LA, Doney AS, Hattersley AT, Morris AD, Pearson ER. The effect of obesity on glycaemic response to metformin or sulphonylureas in Type 2 diabetes. Diabet Med. 2006;23:128–33.

Kim YM, Cha BS, Kim DJ, Choi SH, Kim SK, et al. Predictive clinical parameters for therapeutic efficacy of rosiglitazone in Korean type 2 diabetes mellitus. Diabetes Res Clin Pract. 2005;67:43–52.