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Sexual differences in the control of energy homeostasis
Open accessAbstract
The prevalence of obesity has reached epidemic proportion with enormous costs in both human lives and healthcare dollars spent. Obesity-related metabolic disorders are much lower in premenopausal women than men; however, there is a dramatic increase following menopause in women. The health risks associated with obesity vary depending on the location of adipose tissue. Adipose tissue distributed in the abdominal visceral carry a much greater risk for metabolic disorders than does adipose tissue distributed subcutaneously. There are distinct sex-dependent differences in the regional fat distribution, women carry more fat subcutaneously whereas men carry more fat viscerally. Males and females differ with respect to their regulation of energy homeostasis. Peripheral adiposity hormones such as leptin and insulin as well as sex hormones directly influence energy balance. Sexual dimorphisms in energy balance, body fat distribution, and the role sex hormones have in mediating these differences are the focus of this review.
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“Estrogen actions in hypothalamic nuclei differentially control food intake, energy expenditure, and white adipose tissue distribution [22,66,67].”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [22]
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“Significant sex differences and sex hormone influences on carbohydrate and lipid metabolism are apparent”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [22]
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“important sex differences exist in mitochondrial function [14–16], substrate utilization, and insulin sensitivity [17–24], immune responses [25–28], muscle morphology and body composition [29–32], iron metabolism [33–40], thermoregulation [41–44], hydration [45,46]{Sims, 2008 #55, [47–53], appetite control [54–59], and energy availability and endocrine function [60–65].”
From International society of sports nutrition position stand: nutritional concerns of the female athlete (2023) · cites this paper as [22]
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“Like leptin, the class of gonadal steroid estrogens also exerts a potent influence on energy balance, adiposity and glucose homeostasis [9].”
InfluentialSelf-citationCell and molecular mechanisms behind diet‐induced hypothalamic inflammation and obesity
Ávalos, Y., Kerr, B., Maliqueo, M. A., & Dorfman, M. D. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12598 · Cited by 55
Childhood and adolescent obesity and long‐term cognitive consequences during aging
Wang, J., Freire, D., Knable, L. A., Zhao, W., Gong, B., Mazzola, P., Ho, L., Levine, S., & Pasinetti, G. M. (2014) · The Journal of Comparative Neurology · doi:10.1002/cne.23708 · Cited by 55
“All those acknowledged have agreed to be listed.”
BackgroundRousso-Noori, L., Knobler, H., Levy-Apter, E., Kuperman, Y., Neufeld-Cohen, A., Keshet, Y., Akepati, V. R., Klinghoffer, R. A., Chen, A., & Elson, A. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.02.017 · Cited by 55
“Gender-specific differences exist also in the relative importance of signaling by leptin or insulin to body weight regulation, with leptin playing a more prominent role in females (Clegg et al., 2003; Shi et al., 2009).”
BackgroundChronic High Fat Diet Consumption Impairs Metabolic Health of Male Mice
Morselli, E., Criollo, A., Rodríguez‐Navas, C., & Clegg, D. J. (2015) · Inflammation and Cell Signaling · doi:10.14800/ics.561 · Cited by 54
Self-citationObesity and High-Fat Diet Induce Distinct Changes in Placental Gene Expression and Pregnancy Outcome
Mahany, E. B., Han, X., Borges, B. C., Cruz‐Machado, S. D. S., Allen, S. J., García-Galiano, D., Hoenerhoff, M. J., Bellefontaine, N., & Elias, C. F. (2018) · Endocrinology · doi:10.1210/en.2017-03053 · Cited by 52
Turan, Ş., Poyraz, C. A., Sağlam, N. G. U., Demirel, Ö. F., Haliloğlu, Ö., Kadıoğlu, P., & Duran, A. (2018) · Archives of Sexual Behavior · doi:10.1007/s10508-018-1189-4 · Cited by 52
Xu, M., Zhou, E. Y., & Shi, H. (2025) · Cells · doi:10.3390/cells14050384 · Cited by 58
“Gene expression contributes to diet-induced sex-specific weight gain and fat distribution in both humans and laboratory animal models [137,138].”
Self-citationEstradiol regulates insulin signaling and inflammation in adipose tissue
Shen, M., Kumar, S. P. D. S., & Shi, H. (2014) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci-2014-0007 · Cited by 52
“Female’s metabolism and energy balance were influenced by estrogen [27–30], especially during proestus-estrus when endogenous estrogen is high and has greatest physiological effects [31].”
Self-citationAldehyde Dehydrogenase 1A1: Friend or Foe to Female Metabolism?
Petrosino, J. M., DiSilvestro, D. J., & Ziouzenkova, O. (2014) · Nutrients · doi:10.3390/nu6030950 · Cited by 52
“The differences in metabolic rate [52–54] and energy homeostasis between males and females is dependent on actions of sex hormones [55–57] and expression of ER receptors in different tissues, including muscle [56,58] and adipose [59–65].”
BackgroundSecretome of Adipose Tissue as the Key to Understanding the Endocrine Function of Adipose Tissue
Pogodziński, D., Ostrowska, L., Smarkusz-Zarzecka, J., & Zyśk, B. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23042309 · Cited by 57
“such as estrogens, androgens, glucocorticoids and growth hormones [5,6].”
BackgroundOverview of the Physiological Control of Eating
Langhans, W., & Geary, N. (2009) · Forum of nutrition/Bibliotheca Nutritio et dieta · doi:10.1159/000264392 · Cited by 49
Perimenopausal risk factors and future health
The ESHRE Capri Workshop Group (2011) · Human Reproduction Update · doi:10.1093/humupd/dmr020 · Cited by 47
“Estrogens are suggested to stimulate lipolysis and inhibit lipogenesis in visceral adipocytes via stimulation of the estrogen receptor alpha, thus limiting fat storage in visceral adipocytes in premenopausal women (Shi et al., 2009).”
BackgroundInfluentialNeurobiology of estrogen status in deep craniofacial pain
Bereiter, D. A., & Okamoto, K. (2011) · International review of neurobiology · doi:10.1016/b978-0-12-385198-7.00010-2 · Cited by 46
Factors Associated with Beta-Cell Dysfunction in Type 2 Diabetes: The BETADECLINE Study
Russo, G. T., Giorda, C. B., Cercone, S., Nicolucci, A., Cucinotta, D., & on behalf of BetaDecline Study Group (2014) · PLoS ONE · doi:10.1371/journal.pone.0109702 · Cited by 47
“Thus, metabolic diseases are less prevalent among premenopausal women [32] and hormone-related differences in regional fat distribution and function obviously play a crucial role in this context [33] Furthermore, two hormonal intervention studies, the Women’s Health Initiative Study [34] and the Heart and Oestrogen/Pr…”
ResultSchneider, J. E., Brozek, J. M., & Keen‐Rhinehart, E. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.03.011 · Cited by 48
Choi, D. K., Oh, T. S., Choi, J., Mukherjee, R., Wang, X., Liu, H., & Yun, J. W. (2011) · Cellular Physiology and Biochemistry · doi:10.1159/000335807 · Cited by 44
Diet-Induced Obesity in the Selenocysteine Lyase Knockout Mouse
Seale, L. A., Gilman, C. L., Hashimoto, A. C., Ogawa-Wong, A. N., & Berry, M. J. (2015) · Antioxidants and Redox Signaling · doi:10.1089/ars.2015.6277 · Cited by 45
“Both male and female Scly KO mice presented similar aggravated obesity; however, we selected male mice to be further analyzed in our study, as gender-specific mechanisms were found to regulate energy metabolism (58) and selenium metabolism (33, 54).”
Tørris, C., Molin, M., & Småstuen, M. C. (2017) · Nutrients · doi:10.3390/nu9030247 · Cited by 46
“Both testosterone and estrogen levels have been associated with components of MetS [76], and ovarian hormones, such as estrogen, have been suggested to have a protective role regarding MetS, at least before menopause [77].”
BackgroundYasrebi, A., Rivera, J. A., Krumm, E. A., Yang, J. A., & Roepke, T. A. (2017) · Endocrinology · doi:10.1210/en.2016-1535 · Cited by 40
Female Nur77-Deficient Mice Show Increased Susceptibility to Diet-Induced Obesity
Perez‐Sieira, S., Martínez, G., Porteiro, B., López, M., Vidal, A., Nogueiras, R., & Diéguez, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053836 · Cited by 41
“Additionally, as it is well established that there are sexual differences in the control of energy homeostasis [17], we also uncovered critical gender differences in the Nur77 signaling by using male and female mice lacking Nur77 fed with a HFD of 45% calories from fat.”
BackgroundWhitaker, K. W., Totoki, K., & Reyes, T. M. (2011) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2011.02.007 · Cited by 41
“The mechanistic explanation for the observed sex difference is beyond the scope of the current study, but known sex differences in metabolic regulation (22) and the interaction of sex hormones with food intake, activity and metabolic rate are likely to play an important role.”
BackgroundYasrebi, A., Hsieh, A., Mamounis, K. J., Krumm, E. A., Yang, J., Magby, J. P., Hu, P., & Roepke, T. A. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.11.007 · Cited by 40
“In 57 ovariectomized rodent models, E2 regulates many aspects of energy homeostasis through both 58 peripheral actions and central mechanisms (reviewed in Mauvais-Jarvis et al., 2013; Roepke, 59 2009; Shi et al., 2009).”
MethodCaron, B., Patin, É., Rotival, M., Charbit, B., Albert, M. L., Quintana‐Murci, L., Duffy, D., Rausell, A., Abel, L., Alcover, A., et al. (2022) · Genome Medicine · doi:10.1186/s13073-022-01032-y · Cited by 43
“8% for Leptin [55], 39% for Stromelysin-1 (MMP3) [51, 56], 36.”
InfluentialEstrogen sulfotransferase regulates body fat and glucose homeostasis in female mice
Khor, V. K., Dhir, R. N., Yin, X., Ahima, R. S., & Song, W. (2010) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00707.2009 · Cited by 38
The ZEB1 Transcription Factor Is a Novel Repressor of Adiposity in Female Mice
Saykally, J. N., Doğan, S., Cleary, M. P., & Sanders, M. M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008460 · Cited by 39
“As considerable data indicate that estrogen protects against weight gain [32,33], it seems plausible that ZEB1 might mediate estrogen’s effects on adiposity.”
BackgroundMethodSex Differences in the Metabolic Effects of Testosterone in Sheep
Clarke, S. D., Clarke, I. J., Rao, A., Cowley, M. A., & Henry, B. A. (2011) · Endocrinology · doi:10.1210/en.2011-1634 · Cited by 42
“This may represent divergence in adipose content because females have been shown to have higher adiposity than males (41), and NEFA levels exhibit a positive correlation with fat levels (42).”
BackgroundDDM-Spain, Pollán, M., Lope, V., Miranda-García, J., García, M., Casanova, F., Sánchez‐Contador, C., Santamariña, C., Moreo, P., Vidal, C., et al. (2012) · Breast Cancer Research and Treatment · doi:10.1007/s10549-012-2108-3 · Cited by 36
“Visceral fat varies inversely with estrogen levels [36], and the cessation of gonadal estrogen production at menopause is associated with the emergence of a more android pattern [31].”
BackgroundRole of human pregnane X receptor in high fat diet-induced obesity in pre-menopausal female mice
Spruiell, K., Jones, D., Cullen, J. M., Awumey, E. M., Gonzalez, F. J., & Gyamfi, M. A. (2014) · Biochemical Pharmacology · doi:10.1016/j.bcp.2014.03.019 · Cited by 36
“Previous reports have shown that the deficiency of estrogens or estrogen receptors results in visceral fat accumulation, impairment of insulin sensitivity and lipid metabolism, hypercholesterolemia, and cardiovascular disease risk [77,78].”
BackgroundGender‐specific transcriptomic response to environmental exposure in flemish adults
Coster, S. D., van Leeuwen, D. M., Jennen, D. G. J., Koppen, G., Hond, E. D., Nelen, V., Schoeters, G. E. R., Baeyens, W., van Delft, J. H. M., Kleinjans, J. C. S., et al. (2013) · Environmental and Molecular Mutagenesis · doi:10.1002/em.21774 · Cited by 36
“However, after menopause, when estrogen levels in women decrease, these disorders become more prevalent in females [Shi et al., 2009].”
BackgroundSexual dimorphism in adipose tissue mitochondrial function and metabolic flexibility in obesity
MacCannell, A. D. V., Futers, T. S., Whitehead, A., Moran, A., Witte, K. K., & Roberts, L. D. (2021) · International Journal of Obesity · doi:10.1038/s41366-021-00843-0 · Cited by 38
“tissue distribution and adiposity, which may translate to differences in the prevalence of metabolic syndrome and type 2 diabetes [13, 14].”
BackgroundKlemettilä, J.-P., Kampman, O., Seppälä, N., Viikki, M., Hämäläinen, M., Moilanen, E., Mononen, N., Lehtimäki, T. J., & Leinonen, E. V. J. (2014) · European Psychiatry · doi:10.1016/j.eurpsy.2014.08.006 · Cited by 34
“Estrogen and testosterone modulate leptin synthesis and secretion [61].”
Emerging roles for hypothalamic microglia as regulators of physiological homeostasis
Rosin, J. M., & Kurrasch, D. M. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100748 · Cited by 37
Fekry, B., Ribas‐Latre, A., Baumgartner, C., Mohamed, A. M. T., Kolonin, M. G., Sladek, F. M., Younes, M., & Eckel‐Mahan, K. L. (2019) · Cancer Research · doi:10.1158/0008-5472.can-19-1277 · Cited by 35
“Consistent with previous reports, WT females were protected from HF diet-induced obesity (34,35).”
ResultLi, C., Xu, J.-J., Hu, H., Shi, C.-Y., Yu, C., Sheng, J., Wu, Y., & Huang, H. (2020) · Molecular Metabolism · doi:10.1016/j.molmet.2020.101135 · Cited by 33
“believed that the protective effect of the obesity-related metabolic disorder might be attributed to sex hormones, especially estrogen [38].”
BackgroundEffects of metabolic state on the regulation of melanocortin circuits
Lieu, L., Chau, D., Afrin, S., Dong, Y., Alhadeff, A. L., Betley, J. N., & Williams, K. W. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113039 · Cited by 35
“These patterns are not limited to rodents as sex differences in energy expenditure regulation are conserved across species, including humans [49, 153, 164].”
Lin, L., Jung, K., Lee, H.-L., Le, J., Colleluori, G., Wood, C. P., Palese, F., Squire, E., Ramirez, J., Su, S., et al. (2023) · Cell Metabolism · doi:10.1016/j.cmet.2023.05.002 · Cited by 32
Id1 Promotes Obesity by Suppressing Brown Adipose Thermogenesis and White Adipose Browning
Patil, M., Sharma, B. K., Elattar, S., Chang, J., Kapil, S., Yuan, J., & Ande, S. (2017) · Diabetes · doi:10.2337/db16-1079 · Cited by 31
“Sex-dependent differences in energy intake, storage, and expenditure are well known, and these physiological mechanisms are under the control of sex hormones (43).”
BackgroundKISS1 expression in human female adipose tissue
Cockwell, H., Wilkinson, D. A., Bouzayen, R., Imran, S. A., Brown, R., & Wilkinson, M. (2012) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-012-2514-0 · Cited by 33
“Differences in gene expression between subcutaneous and visceral fat are known [17] and our observation that KISS1 expression is 2.”
Background
Metadata
- Authors
- Shi, H., Seeley, R. J., & Clegg, D. J.
- Affiliations
- University of Cincinnati (US)
- The University of Texas Southwestern Medical Center (US)
- Corresponding author
- Clegg, Deborah J.
- Venue
- Frontiers in Neuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2009-08
- Volume
- 30
- Issue
- 3
- Pages
- 396-404
- ISSN
- 0091-3022 (ISSN-L)
- PMC
- PMC4517605
- OpenAlex
- W2073795741
- Cited by
- 242
- References
- 187
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 12 · 2023: 9 · 2022: 15 · 2021: 10 · 2020: 10 · 2019: 15 · 2018: 17 · 2017: 17 · 2016: 12 · 2015: 12 · 2014: 20 · 2013: 17 · 2012: 16
- FWCI
- 2.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Frontiers in Neuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute of Diabetes and Digestive and Kidney Diseases (DK73689, R01DK073689, F32DK075255)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Keywords
- sexual dimorphism, energy homeostasis, obesity, menopause, sex hormones, leptin, insulin, visceral adipose tissue, subcutaneous adipose tissue, regional fat distribution, energy balance, metabolic disorders
- MeSH terms
- Animals, Energy Metabolism, Estrogens, Female, Homeostasis, Humans, Male, Metabolic Diseases, Models, Biological, Obesity, Sex Characteristics, Body Fat Distribution
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