Skip to main content
SpringerLink
Log in

Effects of Sex Hormones and Exercise on Adipose Tissue

  • Chapter
  • First Online:
Sex Hormones, Exercise and Women

  • 2216 Accesses

Abstract

Adipose tissue is an essential body organ that is profoundly affected by both exercise and female sex hormones. As the body’s major energy reservoir, adipose tissue is extremely sensitive to exercise. That is, exercise-mediated increases in circulating catecholamines are a major stimulus for adipocyte lipolysis, the process that allows for mobilization of the lipid stored in adipose tissue for use by other cells of the body. A major physiological and anatomical difference between sexes is that females have significantly more relative adipose tissue. This important difference is clearly mediated by female sex hormones (e.g., estrogen), which dictate body fat distribution patterns, and appear to also affect the physiological function of adipose tissue. For example, ovary-intact female adipose tissue appears to be more metabolically active and less susceptible to insulin resistance and inflammation compared to that from age-matched males. There are also important differences between males and females in brown adipose tissue (BAT) metabolism, such that females have more relative BAT than males and BAT from females appears more active. It is likely that the female hormone, estrogen plays a large role in those sex differences and estrogen receptor alpha appears to mediate those effects. Finally, there are many interesting similarities between how exercise and estrogen affect the function of adipose tissue. The purpose of this chapter is to provide the reader with a basic understanding of the how exercise and estrogen affect adipose tissue physiology and function; this is done via a comprehensive overview of the most recent scientific literature on this topic.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Bloor ID, Symonds ME. Sexual dimorphism in white and brown adipose tissue with obesity and inflammation. Horm Behav. 2014;66(1):95–103.

    Article  PubMed  Google Scholar 

  • Bluher M. Importance of estrogen receptors in adipose tissue function. Mol Metabol. 2013;2(3):130–2.

    Article  CAS  Google Scholar 

  • Bostrom P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, et al. A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature. 2012;481(7382):463–8.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bradley RL, Jeon JY, Liu FF, Maratos-Flier E. Voluntary exercise improves insulin sensitivity and adipose tissue inflammation in diet-induced obese mice. Am J Physiol Endocrinol Metab. 2008;295(3):E586–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Braun B, Horton T. Endocrine regulation of exercise substrate utilization in women compared to men. Exerc Sport Sci Rev. 2001;29(4):149–54.

    Article  CAS  PubMed  Google Scholar 

  • Braun B, Mawson JT, Muza SR, Dominick SB, Brooks GA, Horning MA, et al. Women at altitude: carbohydrate utilization during exercise at 4,300 m. J Appl Physiol (1985). 2000;88(1):246–56.

    CAS  Google Scholar 

  • Bruun JM, Helge JW, Richelsen B, Stallknecht B. Diet and exercise reduce low-grade inflammation and macrophage infiltration in adipose tissue but not in skeletal muscle in severely obese subjects. Am J Physiol Endocrinol Metab. 2006;290(5):E961–7.

    Article  CAS  PubMed  Google Scholar 

  • Bulow J, Gjeraa K, Enevoldsen LH, Simonsen L. Lipid mobilization from human abdominal, subcutaneous adipose tissue is independent of sex during steady-state exercise. Clin Physiol Funct Imaging. 2006;26(4):205–11.

    Article  CAS  PubMed  Google Scholar 

  • Calles-Escandon J, Poehlman ET. Aging, fat oxidation and exercise. Aging. 1997;9(1-2):57–63.

    CAS  PubMed  Google Scholar 

  • Campbell SE, Febbraio MA. Effects of ovarian hormones on exercise metabolism. Curr Opin Clin Nutr Metab Care. 2001;4(6):515–20.

    Article  CAS  PubMed  Google Scholar 

  • Campfield LA, Smith FJ, Guisez Y, Devos R, Burn P. OB protein: a peripheral signal linking adiposity and central neural networks. Appetite. 1996;26(3):302.

    Article  CAS  PubMed  Google Scholar 

  • Chehab FF, Mounzih K, Lu R, Lim ME. Early onset of reproductive function in normal female mice treated with leptin. Science. 1997;275(5296):88–90.

    Article  CAS  PubMed  Google Scholar 

  • Cherneva RV, Georgiev OB, Petrova DS, Mondeshki TL, Ruseva SR, Cakova AD, et al. Resistin – the link between adipose tissue dysfunction and insulin resistance in patients with obstructive sleep apnea. J Diabetes Metab Disord. 2013;12(1):5.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Crocker MK, Stern EA, Sedaka NM, Shomaker LB, Brady SM, Ali AH, et al. Sexual dimorphisms in the associations of BMI and body fat with indices of pubertal development in girls and boys. J Clin Endocrinol Metab. 2014;99(8):E1519–29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davis KE, Neinast MD, Sun K, Bills JD, Zehr JA, Zeve D, Hahne LD, et al. The sexually dimorphic role of adipose and adipocyte estrogen receptors in modulating adipose tissue expansion, inflammation, and fibrosis. Mol Metab. 2013;2(3):227–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D'Eon TM, Souza SC, Aronovitz M, Obin MS, Fried SK, Greenberg AS. Estrogen regulation of adiposity and fuel partitioning. Evidence of genomic and non-genomic regulation of lipogenic and oxidative pathways. J Biol Chem. 2005;280(43):35983–91.

    Article  PubMed  CAS  Google Scholar 

  • Devries MC. Sex-based differences in endurance exercise muscle metabolism: impact on exercise and nutritional strategies to optimize health and performance in women. Exp Physiol. 2016;101(2):243–9.

    Article  PubMed  Google Scholar 

  • Duckles SP, Krause DN. Mechanisms of cerebrovascular protection: oestrogen, inflammation and mitochondria. Acta Physiol (Oxf). 2011;203(1):149–54.

    Article  CAS  Google Scholar 

  • Endlich PW, Claudio ER, da Silva Goncalves WL, Gouvea SA, Moyses MR, de Abreu GR. Swimming training prevents fat deposition and decreases angiotensin II-induced coronary vasoconstriction in ovariectomized rats. Peptides. 2013;47:29–35.

    Article  CAS  PubMed  Google Scholar 

  • Enevoldsen LH, Stallknecht B, Fluckey JD, Galbo H. Effect of exercise training on in vivo lipolysis in intra-abdominal adipose tissue in rats. Am J Physiol Endocrinol Metab. 2000;279(3):E585–92.

    CAS  PubMed  Google Scholar 

  • Fabrizi M, Marchetti V, Mavilio M, Marino A, Casagrande V, Cavalera M, et al. IL-21 is a major negative regulator of IRF4-dependent lipolysis affecting Tregs in adipose tissue and systemic insulin sensitivity. Diabetes. 2014.

    Google Scholar 

  • Fain JN. Release of interleukins and other inflammatory cytokines by human adipose tissue is enhanced in obesity and primarily due to the nonfat cells. Vitam Horm. 2006;74:443–77.

    Article  CAS  PubMed  Google Scholar 

  • Ferrante Jr AW. Macrophages, fat, and the emergence of immunometabolism. J Clin Invest. 2013;123(12):4992–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer A, et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med. 2009;15(8):930–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Filippov S, Pinkosky SL, Lister RJ, Pawloski C, Hanselman JC, Cramer CT, et al. ETC-1002 regulates immune response, leukocyte homing, and adipose tissue inflammation via LKB1-dependent activation of macrophage AMPK. J Lipid Res. 2013;54(8):2095–108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foryst-Ludwig A, Kreissl MC, Benz V, Brix S, Smeir E, Ban Z, et al. Adipose tissue lipolysis promotes exercise-induced cardiac hypertrophy involving the lipokine C16:1n7-palmitoleate. J Biol Chem. 2015;290(39):23603–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frayn KN, Shadid S, Hamlani R, Humphreys SM, Clark ML, Fielding BA, et al. Regulation of fatty acid movement in human adipose tissue in the postabsorptive-to-postprandial transition. Am J Physiol. 1994;266(3 Pt 1):E308–17.

    CAS  PubMed  Google Scholar 

  • Frayn KN, Karpe F, Fielding BA, Macdonald IA, Coppack SW. Integrative physiology of human adipose tissue. Int J Obes Relat Metab Disord. 2003;27(8):875–88.

    Article  CAS  PubMed  Google Scholar 

  • Fried SK, Bunkin DA, Greenberg AS. Omental and subcutaneous adipose tissues of obese subjects release interleukin-6: depot difference and regulation by glucocorticoid. J Clin Endocrinol Metab. 1998;83(3):847–50.

    CAS  PubMed  Google Scholar 

  • Frisch RE. Body weight, body fat, and ovulation. Trends Endocrinol Metab. 1991;2(5):191–7.

    Article  CAS  PubMed  Google Scholar 

  • Gao H, Bryzgalova G, Hedman E, Khan A, Efendic S, Gustafsson JA, et al. Long-term administration of estradiol decreases expression of hepatic lipogenic genes and improves insulin sensitivity in ob/ob mice: a possible mechanism is through direct regulation of signal transducer and activator of transcription 3. Mol Endocrinol. 2006;20(6):1287–99.

    Article  CAS  PubMed  Google Scholar 

  • Gao D, Madi M, Ding C, Fok M, Steele T, Ford C, et al. Interleukin-1beta mediates macrophage-induced impairment of insulin signaling in human primary adipocytes. Am J Physiol Endocrinol Metab. 2014.

    Google Scholar 

  • Gesta S, Tseng YH, Kahn CR. Developmental origin of fat: tracking obesity to its source. Cell. 2007;131(2):242–56.

    Article  CAS  PubMed  Google Scholar 

  • Giordano A, Smorlesi A, Frontini A, Barbatelli G, Cinti S. White, brown and pink adipocytes: the extraordinary plasticity of the adipose organ. Eur J Endocrinol. 2014;170(5):R159–71.

    Article  CAS  PubMed  Google Scholar 

  • Gohil K, Henderson S, Terblanche SE, Brooks GA, Packer L. Effects of training and exhaustive exercise on the mitochondrial oxidative capacity of brown adipose tissue. Biosci Rep. 1984;4(11):987–93.

    Article  CAS  PubMed  Google Scholar 

  • Hackney AC, McCracken-Compton MA, Ainsworth B. Substrate responses to submaximal exercise in the midfollicular and midluteal phases of the menstrual cycle. Int J Sport Nutr. 1994;4(3):299–308.

    Article  CAS  PubMed  Google Scholar 

  • Hahn WS, Kuzmicic J, Burrill JS, Donoghue MA, Foncea R, Jensen MD, et al. Proinflammatory cytokines differentially regulate adipocyte mitochondrial metabolism, oxidative stress, and dynamics. Am J Physiol Endocrinol Metab. 2014;306(9):E1033–45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haizlip KM, Harrison BC, Leinwand LA. Sex-based differences in skeletal muscle kinetics and fiber-type composition. Physiology. 2015;30(1):30–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halaas JL, Gajiwala KS, Maffei M, Cohen SL, Chait BT, Rabinowitz D, et al. Weight-reducing effects of the plasma protein encoded by the obese gene. Science. 1995;269(5223):543–6.

    Article  CAS  PubMed  Google Scholar 

  • Handschin C, Choi CS, Chin S, Kim S, Kawamori D, Kurpad AJ, et al. Abnormal glucose homeostasis in skeletal muscle-specific PGC-1alpha knockout mice reveals skeletal muscle-pancreatic beta cell crosstalk. J Clin Invest. 2007;117(11):3463–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hellstrom L, Blaak E, Hagstrom-Toft E. Gender differences in adrenergic regulation of lipid mobilization during exercise. Int J Sports Med. 1996;17(6):439–47.

    Article  CAS  PubMed  Google Scholar 

  • Higa TS, Spinola AV, Fonseca-Alaniz MH, Evangelista FS. Remodeling of white adipose tissue metabolism by physical training prevents insulin resistance. Life Sci. 2014;103(1):41–8.

    Article  CAS  PubMed  Google Scholar 

  • Hirata K. Blood flow to brown adipose tissue and norepinephrine- induced calorigenesis in physically trained rats. Jpn J Physiol. 1982a;32(2):279–91.

    Article  CAS  PubMed  Google Scholar 

  • Hirata K. Enhanced calorigenesis in brown adipose tissue in physically trained rats. Jpn J Physiol. 1982b;32(4):647–53.

    Article  CAS  PubMed  Google Scholar 

  • Hjemdahl P, Linde B. Influence of circulating NE and Epi on adipose tissue vascular resistance and lipolysis in humans. Am J Physiol. 1983;245(3):H447–52.

    CAS  PubMed  Google Scholar 

  • Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-linked insulin resistance. Science. 1993;259(5091):87–91.

    Article  CAS  PubMed  Google Scholar 

  • Howe LR, Subbaramaiah K, Hudis CA, Dannenberg AJ. Molecular pathways: adipose inflammation as a mediator of obesity-associated cancer. Clin Cancer Res. 2013;19(22):6074–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jenkins NT, Padilla J, Arce-Esquivel AA, Bayless DS, Martin JS, Leidy HJ, et al. Effects of endurance exercise training, metformin, and their combination on adipose tissue leptin and IL-10 secretion in OLETF rats. J Appl Physiol. 2012;113(12):1873–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joseph AM, Pilegaard H, Litvintsev A, Leick L, Hood DA. Control of gene expression and mitochondrial biogenesis in the muscular adaptation to endurance exercise. Essays Biochem. 2006;42:13–29.

    Article  CAS  PubMed  Google Scholar 

  • Jurrissen TJ, Sheldon RD, Gastecki ML, Woodford ML, Zidon TM, Rector RS, et al. Ablation of eNOS does not promote adipose tissue inflammation. Am J Physiol Regul Integr Comp Physiol. 2016;310(8):744–51.

    Article  Google Scholar 

  • Kawanishi N, Yano H, Yokogawa Y, Suzuki K. Exercise training inhibits inflammation in adipose tissue via both suppression of macrophage infiltration and acceleration of phenotypic switching from M1 to M2 macrophages in high-fat-diet-induced obese mice. Exerc Immunol Rev. 2010;16:105–18.

    PubMed  Google Scholar 

  • Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G. Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab. 2001;280(5):E745–51.

    CAS  PubMed  Google Scholar 

  • Kim JH, Cho HT, Kim YJ. The role of estrogen in adipose tissue metabolism: insights into glucose homeostasis regulation. Endocr J. 2014;61(11):1055–67.

    Article  CAS  PubMed  Google Scholar 

  • Ko SH, Lee JK, Lee HJ, Ye SK, Kim HS, Chung MH. 8-Oxo-2'-deoxyguanosine ameliorates features of metabolic syndrome in obese mice. Biochem Biophys Res Commun. 2014;443(2):610–6.

    Article  CAS  PubMed  Google Scholar 

  • Lambadiari V, Triantafyllou K, Dimitriadis GD. Insulin action in muscle and adipose tissue in type 2 diabetes: the significance of blood flow. World J Diabetes. 2015;6(4):626–33.

    PubMed  PubMed Central  Google Scholar 

  • Lapid K, Lim A, Clegg DJ, Zeve D, Graff JM. Oestrogen signalling in white adipose progenitor cells inhibits differentiation into brown adipose and smooth muscle cells. Nat Commun. 2014;5:5196.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laqueur GL, Harrison MB. Glandular adipose tissue associated with cytotoxic suprarenal contraction and diabetes mellitus. Am J Pathol. 1951;27(2):231–45.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Larue-Achagiotis C, Rieth N, Goubern M, Laury MC, Louis-Sylvestre J. Exercise-training reduces BAT thermogenesis in rats. Physiol Behav. 1995;57(5):1013–7.

    Article  CAS  PubMed  Google Scholar 

  • Leblanc J, Dussault J, Lupien D, Richard D. Effect of diet and exercise on norepinephrine-induced thermogenesis in male and female rats. J Appl Physiol. 1982;52(3):556–61.

    CAS  PubMed  Google Scholar 

  • Lemoine S, Granier P, Tiffoche C, Berthon PM, Rannou-Bekono F, Thieulant ML, et al. Effect of endurance training on oestrogen receptor alpha transcripts in rat skeletal muscle. Acta Physiol Scand. 2002;174(3):283–9.

    Article  CAS  PubMed  Google Scholar 

  • Luglio HF. Estrogen and body weight regulation in women: the role of estrogen receptor alpha (ER-alpha) on adipocyte lipolysis. Acta Med Indones. 2014;46(4):333–8.

    PubMed  Google Scholar 

  • Martinez de Morentin PB, Gonzalez-Garcia I, Martins L, Lage R, Fernandez-Mallo D, Martinez-Sanchez N, et al. Estradiol regulates brown adipose tissue thermogenesis via hypothalamic AMPK. Cell Metab. 2014;20(1):41–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mattiasson I, Rendell M, Tornquist C, Jeppsson S, Hulthen UL. Effects of estrogen replacement therapy on abdominal fat compartments as related to glucose and lipid metabolism in early postmenopausal women. Horm Metab Res. 2002;34(10):583–8.

    Article  CAS  PubMed  Google Scholar 

  • McNelis JC, Olefsky JM. Macrophages, immunity, and metabolic disease. Immunity. 2014;41(1):36–48.

    Article  CAS  PubMed  Google Scholar 

  • Merry TL, Ristow M. Mitohormesis in exercise training. Free Radic Biol Med. 2015;pii:S0891-5849(15)01141-7.

    Google Scholar 

  • Metz L, Gerbaix M, Masgrau A, Guillet C, Walrand S, Boisseau N, et al. Nutritional and exercise interventions variably affect estrogen receptor expression in the adipose tissue of male rats. Nutr Res. 2016;36(3):280–9.

    Article  CAS  PubMed  Google Scholar 

  • Miao H, Ou J, Ma Y, Guo F, Yang Z, Wiggins M, et al. Macrophage CGI-58 deficiency activates ROS-inflammasome pathway to promote insulin resistance in mice. Cell Rep. 2014;7(1):223–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nadal-Casellas A, Proenza AM, Llado I, Gianotti M. Effects of ovariectomy and 17-beta estradiol replacement on rat brown adipose tissue mitochondrial function. Steroids. 2011;76(10-11):1051–6.

    Article  CAS  PubMed  Google Scholar 

  • Nadal-Casellas A, Bauza-Thorbrugge M, Proenza AM, Gianotti M, Llado I. Sex-dependent differences in rat brown adipose tissue mitochondrial biogenesis and insulin signaling parameters in response to an obesogenic diet. Mol Cell Biochem. 2012;373(1-2):125–35.

    Article  PubMed  CAS  Google Scholar 

  • Natoli G, Monticelli S. Macrophage activation: glancing into diversity. Immunity. 2014;40(2):175–7.

    Article  CAS  PubMed  Google Scholar 

  • Nigro M, Santos AT, Barthem CS, Louzada RA, Fortunato RS, Ketzer LA, et al. A change in liver metabolism but not in brown adipose tissue thermogenesis is an early event in ovariectomy-induced obesity in rats. Endocrinology. 2014;155(8):2881–91.

    Article  PubMed  CAS  Google Scholar 

  • Nozu T, Kikuchi K, Ogawa K, Kuroshima A. Effects of running training on in vitro brown adipose tissue thermogenesis in rats. Int J Biometeorol. 1992;36(2):88–92.

    Article  CAS  PubMed  Google Scholar 

  • Ogasawara J, Izawa T, Sakurai T, Sakurai T, Shirato K, Ishibashi Y, et al. The molecular mechanism underlying continuous exercise training-induced adaptive changes of lipolysis in white adipose cells. J Obes. 2015;2015:473430.

    Article  PubMed  PubMed Central  Google Scholar 

  • Oh-ishi S, Kizaki T, Toshinai K, Haga S, Fukuda K, Nagata N, et al. Swimming training improves brown-adipose-tissue activity in young and old mice. Mech Ageing Dev. 1996;89(2):67–78.

    Article  CAS  PubMed  Google Scholar 

  • Oliveira AG, Araujo TG, Carvalho BM, Guadagnini D, Rocha GZ, Bagarolli RA, et al. Acute exercise induces a phenotypic switch in adipose tissue macrophage polarization in diet-induced obese rats. Obesity. 2013.

    Google Scholar 

  • O'Rourke RW, White AE, Metcalf MD, Winters BR, Diggs BS, Zhu X, et al. Systemic inflammation and insulin sensitivity in obese IFN-gamma knockout mice. Metabolism. 2012;61(8):1152–61.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Osborn O, Olefsky JM. The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med. 2012;18(3):363–74.

    Article  CAS  PubMed  Google Scholar 

  • O'Sullivan AJ. Does oestrogen allow women to store fat more efficiently? A biological advantage for fertility and gestation. Obes Rev. 2009;10(2):168–77.

    Article  PubMed  CAS  Google Scholar 

  • O'Sullivan AJ, Martin A, Brown MA. Efficient fat storage in premenopausal women and in early pregnancy: a role for estrogen. J Clin Endocrinol Metab. 2001;86(10):4951–6.

    Article  PubMed  Google Scholar 

  • Park YM, Rector RS, Thyfault JP, Zidon TM, Padilla J, Welly RJ, et al. Effects of ovariectomy and intrinsic aerobic capacity on tissue-specific insulin sensitivity. Am J Physiol Endocrinol Metab. 2016;310(3):190–9.

    Article  Google Scholar 

  • Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, et al. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: potential role of PGC1 and NRF1. Proc Natl Acad Sci U S A. 2003;100(14):8466–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedersen L, Hojman P. Muscle-to-organ cross talk mediated by myokines. Adipocyte. 2012;1(3):164–7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Peirce V, Carobbio S, Vidal-Puig A. The different shades of fat. Nature. 2014;510(7503):76–83.

    Article  CAS  PubMed  Google Scholar 

  • Petersen AM, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol. 2005;98(4):1154–62.

    Article  CAS  PubMed  Google Scholar 

  • Ramos RH, Warren MP. The interrelationships of body fat, exercise, and hormonal status and their impact on reproduction and bone health. Semin Perinatol. 1995;19(3):163–70.

    Article  CAS  PubMed  Google Scholar 

  • Rettberg JR, Yao J, Brinton RD. Estrogen: a master regulator of bioenergetic systems in the brain and body. Front Neuroendocrinol. 2014;35(1):8–30.

    Article  CAS  PubMed  Google Scholar 

  • Richard D, Labrie A, Rivest S. Tissue specificity of SNS response to exercise in mice exposed to low temperatures. Am J Physiol. 1992;262(5 Pt 2):R921–5.

    CAS  PubMed  Google Scholar 

  • Ro SH, Semple I, Ho A, Park HW, Lee JH. Sestrin2, a regulator of thermogenesis and mitohormesis in brown adipose tissue. Front Endocrinol (Lausanne). 2015;6:114.

    Google Scholar 

  • Sanchez-Delgado G, Martinez-Tellez B, Olza J, Aguilera CM, Gil A, Ruiz JR. Role of exercise in the activation of brown adipose tissue. Ann Nutr Metab. 2015;67(1):21–32.

    Article  CAS  PubMed  Google Scholar 

  • Santosa S, Jensen MD. The sexual dimorphism of lipid kinetics in humans. Front Endocrinol (Lausanne). 2015;6:103.

    Google Scholar 

  • Saunders TJ, Palombella A, McGuire KA, Janiszewski PM, Despres JP, Ross R. Acute exercise increases adiponectin levels in abdominally obese men. J Nutr Metabol. 2012;2012:148729.

    Google Scholar 

  • Schmidt S, Monk JM, Robinson LE, Mourtzakis M. The integrative role of leptin, oestrogen and the insulin family in obesity-associated breast cancer: potential effects of exercise. Obes Rev. 2015;16(6):473–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimizu I, Aprahamian T, Kikuchi R, Shimizu A, Papanicolaou KN, MacLauchlan S, et al. Vascular rarefaction mediates whitening of brown fat in obesity. J Clin Invest. 2014;124(5):2099–112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shinoda M, Latour MG, Lavoie JM. Effects of physical training on body composition and organ weights in ovariectomized and hyperestrogenic rats. Int J Obes Relat Metab Disord. 2002;26(3):335–43.

    Article  CAS  PubMed  Google Scholar 

  • Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, et al. Autophagy regulates lipid metabolism. Nature. 2009;458(7242):1131–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sites CK, Brochu M, Tchernof A, Poehlman ET. Relationship between hormone replacement therapy use with body fat distribution and insulin sensitivity in obese postmenopausal women. Metabolism. 2001;50(7):835–40.

    Article  CAS  PubMed  Google Scholar 

  • Sorisky A, Molgat AS, Gagnon A. Macrophage-induced adipose tissue dysfunction and the preadipocyte: should I stay (and differentiate) or should I go? Adv Nutr. 2013;4(1):67–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Speaker KJ, Cox SS, Paton MM, Serebrakian A, Maslanik T, Greenwood BN, et al. Six weeks of voluntary wheel running modulates inflammatory protein (MCP-1, IL-6, and IL-10) and DAMP (Hsp72) responses to acute stress in white adipose tissue of lean rats. Brain Behav Immun. 2014;39:87–98.

    Article  CAS  PubMed  Google Scholar 

  • Stallknecht B, Vinten J, Ploug T, Galbo H. Increased activities of mitochondrial enzymes in white adipose tissue in trained rats. Am J Physiol. 1991;261(3 Pt 1):E410–4.

    CAS  PubMed  Google Scholar 

  • Stanford KI, Middelbeek RJ, Townsend KL, An D, Nygaard EB, Hitchcox KM, et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest. 2013;123(1):215–23.

    Article  CAS  PubMed  Google Scholar 

  • Stanford KI, Middelbeek RJ, Goodyear LJ. Exercise effects on white adipose tissue: beiging and metabolic adaptations. Diabetes. 2015;64(7):2361–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Starkie R, Ostrowski SR, Jauffred S, Febbraio M, Pedersen BK. Exercise and IL-6 infusion inhibit endotoxin-induced TNF-alpha production in humans. FASEB J. 2003;17(8):884–6.

    CAS  PubMed  Google Scholar 

  • St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell. 2006;127(2):397–408.

    Article  CAS  PubMed  Google Scholar 

  • Strawford A, Antelo F, Christiansen M, Hellerstein MK. Adipose tissue triglyceride turnover, de novo lipogenesis, and cell proliferation in humans measured with 2H2O. Am J Physiol Endocrinol Metab. 2004;286(4):E577–88.

    Article  CAS  PubMed  Google Scholar 

  • Summermatter S, Handschin C. PGC-1alpha and exercise in the control of body weight. Int J Obes (Lond). 2012;36(11):1428–35.

    Article  CAS  Google Scholar 

  • Sun T, Cao L, Ping NN, Wu Y, Liu DZ, Cao YX. Formononetin upregulates nitric oxide synthase in arterial endothelium through estrogen receptors and MAPK pathways. J Pharm Pharmacol. 2016;68(3):342–51.

    Article  CAS  PubMed  Google Scholar 

  • Sutherland LN, Bomhof MR, Capozzi LC, Basaraba SA, Wright DC. Exercise and adrenaline increase PGC-1{alpha} mRNA expression in rat adipose tissue. J Physiol. 2009;587(Pt 7):1607–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tchernof A, Despres JP. Pathophysiology of human visceral obesity: an update. Physiol Rev. 2013;93(1):359–404.

    Article  CAS  PubMed  Google Scholar 

  • Tchernof A, Calles-Escandon J, Sites CK, Poehlman ET. Menopause, central body fatness, and insulin resistance: effects of hormone-replacement therapy. Coron Artery Dis. 1998;9(8):503–11.

    Article  CAS  PubMed  Google Scholar 

  • Thomas DM, Bouchard C, Church T, Slentz C, Kraus WE, Redman LM, et al. Why do individuals not lose more weight from an exercise intervention at a defined dose? An energy balance analysis. Obes Rev. 2012;13(10):835–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson D, Karpe F, Lafontan M, Frayn K. Physical activity and exercise in the regulation of human adipose tissue physiology. Physiol Rev. 2012;92(1):157–91.

    Article  CAS  PubMed  Google Scholar 

  • Thong FS, McLean C, Graham TE. Plasma leptin in female athletes: relationship with body fat, reproductive, nutritional, and endocrine factors. J Appl Physiol. 2000;88(6):2037–44.

    CAS  PubMed  Google Scholar 

  • Tiraby C, Tavernier G, Lefort C, Larrouy D, Bouillaud F, Ricquier D, et al. Acquirement of brown fat cell features by human white adipocytes. J Biol Chem. 2003;278(35):33370–6.

    Article  CAS  PubMed  Google Scholar 

  • Toniolo A, Fadini GP, Tedesco S, Cappellari R, Vegeto E, Maggi A, et al. Alternative activation of human macrophages is rescued by estrogen treatment in vitro and impaired by menopausal status. J Clin Endocrinol Metab. 2015;100(1):E50–8.

    Article  CAS  PubMed  Google Scholar 

  • Tsatsanis C, Zacharioudaki V, Androulidaki A, Dermitzaki E, Charalampopoulos I, Minas V, et al. Adiponectin induces TNF-alpha and IL-6 in macrophages and promotes tolerance to itself and other pro-inflammatory stimuli. Biochem Biophys Res Commun. 2005;335(4):1254–63.

    Article  CAS  PubMed  Google Scholar 

  • van Harmelen V, Skurk T, Hauner H. Primary culture and differentiation of human adipocyte precursor cells. Methods Mol Med. 2005;107:125–35.

    PubMed  Google Scholar 

  • Varlamov O, Bethea CL, Roberts Jr CT. Sex-specific differences in lipid and glucose metabolism. Front Endocrinol (Lausanne). 2014;5:241.

    Google Scholar 

  • Velickovic K, Cvoro A, Srdic B, Stokic E, Markelic M, Golic I, et al. Expression and subcellular localization of estrogen receptors alpha and beta in human fetal brown adipose tissue. J Clin Endocrinol Metab. 2014.

    Google Scholar 

  • Vicente-Salar N, Urdampilleta Otegui A, Roche CE. Endurance training in fasting conditions: biological adaptations and body weight management. Nutr Hosp. 2015;32(n06):2409–20.

    PubMed  Google Scholar 

  • Vieira Potter VJ, Strissel KJ, Xie C, Chang E, Bennett G, Defuria J, et al. Adipose tissue inflammation and reduced insulin sensitivity in ovariectomized mice occurs in the absence of increased adiposity. Endocrinology. 2012;153(9):4266–77.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vieira VJ, Valentine RJ, Wilund KR, Antao N, Baynard T, Woods JA. Effects of exercise and low-fat diet on adipose tissue inflammation and metabolic complications in obese mice. Am J Physiol Endocrinol Metab. 2009;296(5):E1164–71.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vieira-Potter VJ, Zidon TM, Padilla J. Exercise and estrogen make fat cells "Fit". Exerc Sport Sci Rev. 2015;43(3):172–8.

    Article  PubMed  PubMed Central  Google Scholar 

  • Villarreal-Molina MT, Antuna-Puente B. Adiponectin: anti-inflammatory and cardioprotective effects. Biochimie. 2012;94(10):2143–9.

    Article  CAS  PubMed  Google Scholar 

  • Vosselman MJ, Hoeks J, Brans B, Pallubinsky H, Nascimento EB, van der Lans AA, et al. Low brown adipose tissue activity in endurance-trained compared with lean sedentary men. Int J Obes (Lond). 2015;39(12):1696–702.

    Article  CAS  Google Scholar 

  • Wade GN, Gray JM. Cytoplasmic 17 beta-[3H]estradiol binding in rat adipose tissues. Endocrinology. 1978;103(5):1695–701.

    Article  CAS  PubMed  Google Scholar 

  • Wade GN, Gray JM, Bartness TJ. Gonadal influences on adiposity. Int J Obes. 1985;9 Suppl 1:83–92.

    CAS  PubMed  Google Scholar 

  • Wallenius V, Wallenius K, Ahren B, Rudling M, Carlsten H, Dickson SL, et al. Interleukin-6-deficient mice develop mature-onset obesity. Nat Med. 2002;8(1):75–9.

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Eckel RH. Lipoprotein lipase: from gene to obesity. Am J Physiol Endocrinol Metab. 2009;297(2):E271–88.

    Article  CAS  PubMed  Google Scholar 

  • Wehling M, Schultz A, Losel R. Nongenomic actions of estrogens: exciting opportunities for pharmacology. Maturitas. 2006;54(4):321–6.

    Article  CAS  PubMed  Google Scholar 

  • Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante Jr AW. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest. 2003;112(12):1796–808.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wiik A, Gustafsson T, Esbjornsson M, Johansson O, Ekman M, Sundberg CJ, et al. Expression of oestrogen receptor alpha and beta is higher in skeletal muscle of highly endurance-trained than of moderately active men. Acta Physiol Scand. 2005;184(2):105–12.

    Article  CAS  PubMed  Google Scholar 

  • Wohlers LM, Spangenburg EE. 17beta-estradiol supplementation attenuates ovariectomy-induced increases in ATGL signaling and reduced perilipin expression in visceral adipose tissue. J Cell Biochem. 2010;110(2):420–7.

    CAS  PubMed  Google Scholar 

  • Xu X, Ying Z, Cai M, Xu Z, Li Y, Jiang SY, et al. Exercise ameliorates high-fat diet-induced metabolic and vascular dysfunction, and increases adipocyte progenitor cell population in brown adipose tissue. Am J Physiol Regul Integr Comp Physiol. 2011;300(5):R1115–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu X, Grijalva A, Skowronski A, van Eijk M, Serlie MJ, Ferrante Jr AW. Obesity activates a program of lysosomal-dependent lipid metabolism in adipose tissue macrophages independently of classic activation. Cell Metab. 2013;18(6):816–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamashita H, Yamamoto M, Sato Y, Izawa T, Komabayashi T, Saito D, et al. Effect of running training on uncoupling protein mRNA expression in rat brown adipose tissue. Int J Biometeorol. 1993;37(1):61–4.

    Article  CAS  PubMed  Google Scholar 

  • Yamauchi T, Kamon J, Waki H, Terauchi Y, Kubota N, Hara K, et al. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity. Nat Med. 2001;7(8):941–6.

    Article  CAS  PubMed  Google Scholar 

  • Yang X, Wang X, Liu D, Yu L, Xue B, Shi H. Epigenetic regulation of macrophage polarization by DNA methyltransferase 3b. Mol Endocrinol. 2014;28(4):565–74.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Nutrition and Exercise Physiology, University of Missouri, 204 Gwynn Hall, Columbia, MO, 65211, USA

    Victoria J. Vieira-Potter Ph.D.

Authors
  1. Victoria J. Vieira-Potter Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Victoria J. Vieira-Potter Ph.D. .

Editor information

Editors and Affiliations

  1. Department of Nutrition, University of North Carolina, Chapel Hill, North Carolina, USA

    Anthony C. Hackney

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Vieira-Potter, V.J. (2017). Effects of Sex Hormones and Exercise on Adipose Tissue. In: Hackney, A. (eds) Sex Hormones, Exercise and Women. Springer, Cham. https://doi.org/10.1007/978-3-319-44558-8_15

Download citation

  • DOI: https://doi.org/10.1007/978-3-319-44558-8_15

  • Published:

  • Publisher Name: Springer, Cham

  • Print ISBN: 978-3-319-44557-1

  • Online ISBN: 978-3-319-44558-8

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics

Search

Navigation