The Sexual Dimorphism of Human Adipose Depots
Abstract
:1. Introduction
2. Sex Differences in Fat Depots in Lifespan and Aging
3. Sex Differences in Fat Depots and Reproductive Health
4. Sex Differences in Fat Depots and Cardiometabolic Health
5. Determinants of the Fat Depot Repartition According to the Sex
5.1. Genetic Determinants
5.2. Epigenetic Mechanisms
5.3. Cell Determinants
5.3.1. Resident Progenitors
5.3.2. Mature Adipocytes
5.4. Hormonal Determinants
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Becher, T.; Palanisamy, S.; Kramer, D.J.; Eljalby, M.; Marx, S.J.; Wibmer, A.G.; Butler, S.D.; Jiang, C.S.; Vaughan, R.; Schoder, H.; et al. Brown adipose tissue is associated with cardiometabolic health. Nat. Med. 2021, 27, 58–65. [Google Scholar] [CrossRef] [PubMed]
- Arner, P.; Ryden, M. Human white adipose tissue: A highly dynamic metabolic organ. J. Intern. Med. 2022, 291, 611–621. [Google Scholar] [CrossRef] [PubMed]
- Karpe, F.; Pinnick, K.E. Biology of upper-body and lower-body adipose tissue—Link to whole-body phenotypes. Nat. Rev. Endocrinol. 2015, 11, 90–100. [Google Scholar] [CrossRef] [PubMed]
- Kuk, J.L.; Ross, R. Influence of sex on total and regional fat loss in overweight and obese men and women. Int. J. Obes 2009, 33, 629–634. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kochkodan, J.; Telem, D.A.; Ghaferi, A.A. Physiologic and psychological gender differences in bariatric surgery. Surg. Endosc. 2018, 32, 1382–1388. [Google Scholar] [CrossRef] [PubMed]
- Dugan, N.; Thompson, K.J.; Barbat, S.; Prasad, T.; McKillop, I.H.; Maloney, S.R.; Roberts, A.; Gersin, K.S.; Kuwada, T.S.; Nimeri, A. Male gender is an independent risk factor for patients undergoing laparoscopic sleeve gastrectomy or Roux-en-Y gastric bypass: An MBSAQIP(R) database analysis. Surg. Endosc. 2020, 34, 3574–3583. [Google Scholar] [CrossRef] [PubMed]
- Cooper, A.J.; Gupta, S.R.; Moustafa, A.F.; Chao, A.M. Sex/Gender Differences in Obesity Prevalence, Comorbidities, and Treatment. Curr. Obes. Rep. 2021, 10, 458–466. [Google Scholar] [CrossRef]
- NCD Risk Factor Collaboration. Trends in adult body-mass index in 200 countries from 1975 to 2014: A pooled analysis of 1698 population-based measurement studies with 19.2 million participants. Lancet 2016, 387, 1377–1396. [Google Scholar] [CrossRef] [Green Version]
- Wardle, J.; Waller, J.; Jarvis, M.J. Sex differences in the association of socioeconomic status with obesity. Am. J. Public Health 2002, 92, 1299–1304. [Google Scholar] [CrossRef]
- Rose, K.M.; Newman, B.; Mayer-Davis, E.J.; Selby, J.V. Genetic and behavioral determinants of waist-hip ratio and waist circumference in women twins. Obes. Res. 1998, 6, 383–392. [Google Scholar] [CrossRef]
- Salinero, A.E.; Anderson, B.M.; Zuloaga, K.L. Sex differences in the metabolic effects of diet-induced obesity vary by age of onset. Int. J. Obes. 2018, 42, 1088–1091. [Google Scholar] [CrossRef]
- Maric, I.; Krieger, J.P.; van der Velden, P.; Borchers, S.; Asker, M.; Vujicic, M.; Wernstedt Asterholm, I.; Skibicka, K.P. Sex and Species Differences in the Development of Diet-Induced Obesity and Metabolic Disturbances in Rodents. Front. Nutr. 2022, 9, 828522. [Google Scholar] [CrossRef]
- Pond, C.M.; Mattacks, C.A.; Calder, P.C.; Evans, J. Site-specific properties of human adipose depots homologous to those of other mammals. Comp. Biochem. Physiol. Comp. Physiol. 1993, 104, 819–824. [Google Scholar] [CrossRef]
- Kuzawa, C.W. Adipose tissue in human infancy and childhood: An evolutionary perspective. Am. J. Phys. Anthropol. 1998, 107 (Suppl. S27), 177–209. [Google Scholar] [CrossRef]
- Gilsanz, V.; Hu, H.H.; Kajimura, S. Relevance of brown adipose tissue in infancy and adolescence. Pediatr. Res. 2013, 73, 3–9. [Google Scholar] [CrossRef] [Green Version]
- Orsso, C.E.; Colin-Ramirez, E.; Field, C.J.; Madsen, K.L.; Prado, C.M.; Haqq, A.M. Adipose Tissue Development and Expansion from the Womb to Adolescence: An Overview. Nutrients 2020, 12, 2735. [Google Scholar] [CrossRef]
- Taylor, R.W.; Grant, A.M.; Williams, S.M.; Goulding, A. Sex differences in regional body fat distribution from pre-to postpuberty. Obesity 2010, 18, 1410–1416. [Google Scholar] [CrossRef]
- Jackson, A.S.; Stanforth, P.R.; Gagnon, J.; Rankinen, T.; Leon, A.S.; Rao, D.C.; Skinner, J.S.; Bouchard, C.; Wilmore, J.H. The effect of sex, age and race on estimating percentage body fat from body mass index: The Heritage Family Study. Int. J. Obes. Relat. Metab. Disord. 2002, 26, 789–796. [Google Scholar] [CrossRef] [Green Version]
- McCarthy, H.D. Body fat measurements in children as predictors for the metabolic syndrome: Focus on waist circumference. Proc. Nutr. Soc. 2006, 65, 385–392. [Google Scholar]
- Vague, J. Sexual differentiations and distribution of fat. Sem. Hop. 1950, 26, 2387–2390. [Google Scholar]
- Tchernof, A.; Despres, J.P. Pathophysiology of human visceral obesity: An update. Physiol. Rev. 2013, 93, 359–404. [Google Scholar] [CrossRef] [Green Version]
- Griffith, J.F.; Yeung, D.K.; Ma, H.T.; Leung, J.C.; Kwok, T.C.; Leung, P.C. Bone marrow fat content in the elderly: A reversal of sex difference seen in younger subjects. J. Magn. Reson. Imaging 2012, 36, 225–230. [Google Scholar] [CrossRef]
- Beekman, K.M.; Regenboog, M.; Nederveen, A.J.; Bravenboer, N.; den Heijer, M.; Bisschop, P.H.; Hollak, C.E.; Akkerman, E.M.; Maas, M. Gender- and Age-Associated Differences in Bone Marrow Adipose Tissue and Bone Marrow Fat Unsaturation Throughout the Skeleton, Quantified Using Chemical Shift Encoding-Based Water-Fat MRI. Front. Endocrinol. 2022, 13, 815835. [Google Scholar] [CrossRef]
- Drubach, L.A.; Palmer, E.L., 3rd; Connolly, L.P.; Baker, A.; Zurakowski, D.; Cypess, A.M. Pediatric brown adipose tissue: Detection, epidemiology, and differences from adults. J. Pediatr. 2011, 159, 939–944. [Google Scholar] [CrossRef]
- Rockstroh, D.; Landgraf, K.; Wagner, I.V.; Gesing, J.; Tauscher, R.; Lakowa, N.; Kiess, W.; Buhligen, U.; Wojan, M.; Till, H.; et al. Direct evidence of brown adipocytes in different fat depots in children. PLoS ONE 2015, 10, e0117841. [Google Scholar] [CrossRef]
- Malpique, R.; Gallego-Escuredo, J.M.; Sebastiani, G.; Villarroya, J.; Lopez-Bermejo, A.; de Zegher, F.; Villarroya, F.; Ibanez, L. Brown adipose tissue in prepubertal children: Associations with sex, birthweight, and metabolic profile. Int. J. Obes. 2019, 43, 384–391. [Google Scholar] [CrossRef]
- Garcia-Beltran, C.; Cereijo, R.; Plou, C.; Gavalda-Navarro, A.; Malpique, R.; Villarroya, J.; Lopez-Bermejo, A.; de Zegher, F.; Ibanez, L.; Villarroya, F. Posterior Cervical Brown Fat and CXCL14 Levels in the First Year of Life: Sex Differences and Association with Adiposity. J. Clin. Endocrinol. Metab. 2022, 107, e1148–e1158. [Google Scholar] [CrossRef]
- Cypess, A.M.; Lehman, S.; Williams, G.; Tal, I.; Rodman, D.; Goldfine, A.B.; Kuo, F.C.; Palmer, E.L.; Tseng, Y.H.; Doria, A.; et al. Identification and importance of brown adipose tissue in adult humans. N. Engl. J. Med. 2009, 360, 1509–1517. [Google Scholar] [CrossRef] [Green Version]
- Keuper, M.; Jastroch, M. The good and the BAT of metabolic sex differences in thermogenic human adipose tissue. Mol. Cell. Endocrinol. 2021, 533, 111337. [Google Scholar] [CrossRef]
- Fletcher, L.A.; Kim, K.; Leitner, B.P.; Cassimatis, T.M.; O’Mara, A.E.; Johnson, J.W.; Halprin, M.S.; McGehee, S.M.; Brychta, R.J.; Cypess, A.M.; et al. Sexual Dimorphisms in Adult Human Brown Adipose Tissue. Obesity 2020, 28, 241–246. [Google Scholar] [CrossRef]
- Martinez-Tellez, B.; Sanchez-Delgado, G.; Boon, M.R.; Rensen, P.C.N.; Llamas-Elvira, J.M.; Ruiz, J.R. Distribution of Brown Adipose Tissue Radiodensity in Young Adults: Implications for Cold [(18)F]FDG-PET/CT Analyses. Mol. Imaging Biol. 2020, 22, 425–433. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pfannenberg, C.; Werner, M.K.; Ripkens, S.; Stef, I.; Deckert, A.; Schmadl, M.; Reimold, M.; Haring, H.U.; Claussen, C.D.; Stefan, N. Impact of age on the relationships of brown adipose tissue with sex and adiposity in humans. Diabetes 2010, 59, 1789–1793. [Google Scholar] [CrossRef] [PubMed]
- Greendale, G.A.; Sternfeld, B.; Huang, M.; Han, W.; Karvonen-Gutierrez, C.; Ruppert, K.; Cauley, J.A.; Finkelstein, J.S.; Jiang, S.F.; Karlamangla, A.S. Changes in body composition and weight during the menopause transition. JCI Insight 2019, 4, e124865. [Google Scholar] [CrossRef]
- Trivett, C.; Lees, Z.J.; Freeman, D.J. Adipose tissue function in healthy pregnancy, gestational diabetes mellitus and pre-eclampsia. Eur. J. Clin. Nutr. 2021, 75, 1745–1756. [Google Scholar] [CrossRef] [PubMed]
- Straughen, J.K.; Trudeau, S.; Misra, V.K. Changes in adipose tissue distribution during pregnancy in overweight and obese compared with normal weight women. Nutr. Diabetes 2013, 3, e84. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Colleluori, G.; Perugini, J.; Barbatelli, G.; Cinti, S. Mammary gland adipocytes in lactation cycle, obesity and breast cancer. Rev. Endocr. Metab. Disord. 2021, 22, 241–255. [Google Scholar] [CrossRef] [PubMed]
- Ambikairajah, A.; Walsh, E.; Tabatabaei-Jafari, H.; Cherbuin, N. Fat mass changes during menopause: A metaanalysis. Am. J. Obstet. Gynecol. 2019, 221, 393–409.e50. [Google Scholar] [CrossRef]
- Rebuffe-Scrive, M.; Enk, L.; Crona, N.; Lonnroth, P.; Abrahamsson, L.; Smith, U.; Bjorntorp, P. Fat cell metabolism in different regions in women. Effect of menstrual cycle, pregnancy, and lactation. J. Clin. Investig. 1985, 75, 1973–1976. [Google Scholar] [CrossRef] [Green Version]
- Frisch, R.E.; McArthur, J.W. Menstrual cycles: Fatness as a determinant of minimum weight for height necessary for their maintenance or onset. Science 1974, 185, 949–951. [Google Scholar] [CrossRef]
- Chou, S.H.; Mantzoros, C. 20 years of leptin: Role of leptin in human reproductive disorders. J. Endocrinol. 2014, 223, T49–T62. [Google Scholar] [CrossRef]
- Nielsen, N.B.; Hojbjerre, L.; Sonne, M.P.; Alibegovic, A.C.; Vaag, A.; Dela, F.; Stallknecht, B. Interstitial concentrations of adipokines in subcutaneous abdominal and femoral adipose tissue. Regul. Pept. 2009, 155, 39–45. [Google Scholar] [CrossRef]
- Pasquali, R.; Pelusi, C.; Genghini, S.; Cacciari, M.; Gambineri, A. Obesity and reproductive disorders in women. Hum. Reprod. Update 2003, 9, 359–372. [Google Scholar] [CrossRef]
- Supramaniam, P.R.; Mittal, M.; McVeigh, E.; Lim, L.N. The correlation between raised body mass index and assisted reproductive treatment outcomes: A systematic review and meta-analysis of the evidence. Reprod. Health 2018, 15, 34. [Google Scholar] [CrossRef]
- Schneider, J.E.; Klingerman, C.M.; Abdulhay, A. Sense and nonsense in metabolic control of reproduction. Front. Endocrinol. 2012, 3, 26. [Google Scholar] [CrossRef] [Green Version]
- Jarvie, E.; Hauguel-de-Mouzon, S.; Nelson, S.M.; Sattar, N.; Catalano, P.M.; Freeman, D.J. Lipotoxicity in obese pregnancy and its potential role in adverse pregnancy outcome and obesity in the offspring. Clin. Sci. 2010, 119, 123–129. [Google Scholar] [CrossRef] [Green Version]
- Li, M.C.; Minguez-Alarcon, L.; Arvizu, M.; Chiu, Y.H.; Ford, J.B.; Williams, P.L.; Attaman, J.; Hauser, R.; Chavarro, J.E.; Team, E.S. Waist circumference in relation to outcomes of infertility treatment with assisted reproductive technologies. Am. J. Obstet. Gynecol. 2019, 220, 578.e1–578.e13. [Google Scholar] [CrossRef]
- Eisenberg, M.L.; Kim, S.; Chen, Z.; Sundaram, R.; Schisterman, E.F.; Louis, G.M. The relationship between male BMI and waist circumference on semen quality: Data from the LIFE study. Hum. Reprod. 2015, 30, 493–494. [Google Scholar] [CrossRef] [Green Version]
- Bulun, S.E.; Simpson, E.R. Competitive reverse transcription-polymerase chain reaction analysis indicates that levels of aromatase cytochrome P450 transcripts in adipose tissue of buttocks, thighs, and abdomen of women increase with advancing age. J. Clin. Endocrinol. Metab. 1994, 78, 428–432. [Google Scholar]
- McTernan, P.G.; Anderson, L.A.; Anwar, A.J.; Eggo, M.C.; Crocker, J.; Barnett, A.H.; Stewart, P.M.; Kumar, S. Glucocorticoid regulation of p450 aromatase activity in human adipose tissue: Gender and site differences. J. Clin. Endocrinol. Metab. 2002, 87, 1327–1336. [Google Scholar] [CrossRef]
- Bhaskaran, K.; Dos-Santos-Silva, I.; Leon, D.A.; Douglas, I.J.; Smeeth, L. Association of BMI with overall and cause-specific mortality: A population-based cohort study of 3.6 million adults in the UK. Lancet Diabetes Endocrinol. 2018, 6, 944–953. [Google Scholar] [CrossRef] [Green Version]
- O’Keeffe, L.M.; Bell, J.A.; O’Neill, K.N.; Lee, M.A.; Woodward, M.; Peters, S.A.E.; Smith, G.D.; Kearney, P.M. Sex-specific associations of adiposity with cardiometabolic traits in the UK: A multi-life stage cohort study with repeat metabolomics. PLoS Med. 2022, 19, e1003636. [Google Scholar] [CrossRef]
- Lim, K.; Haider, A.; Adams, C.; Sleigh, A.; Savage, D.B. Lipodistrophy: A paradigm for understanding the consequences of “overloading” adipose tissue. Physiol. Rev. 2021, 101, 907–993. [Google Scholar]
- Heo, J.W.; Kim, S.E.; Sung, M.K. Sex Differences in the Incidence of Obesity-Related Gastrointestinal Cancer. Int. J. Mol. Sci. 2021, 22, 1253. [Google Scholar] [CrossRef]
- Stefan, N.; Schick, F.; Haring, H.U. Causes, Characteristics, and Consequences of Metabolically Unhealthy Normal Weight in Humans. Cell Metab. 2017, 26, 292–300. [Google Scholar] [CrossRef] [PubMed]
- Lagou, V.; Magi, R.; Hottenga, J.J.; Grallert, H.; Perry, J.R.B.; Bouatia-Naji, N.; Marullo, L.; Rybin, D.; Jansen, R.; Min, J.L.; et al. Sex-dimorphic genetic effects and novel loci for fasting glucose and insulin variability. Nat. Commun. 2021, 12, 24. [Google Scholar] [CrossRef] [PubMed]
- Peters, S.A.E.; Bots, S.H.; Woodward, M. Sex Differences in the Association Between Measures of General and Central Adiposity and the Risk of Myocardial Infarction: Results from the UK Biobank. J. Am. Heart Assoc. 2018, 7, e008507. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Emdin, C.A.; Khera, A.V.; Natarajan, P.; Klarin, D.; Zekavat, S.M.; Hsiao, A.J.; Kathiresan, S. Genetic Association of Waist-to-Hip Ratio with Cardiometabolic Traits, Type 2 Diabetes, and Coronary Heart Disease. JAMA 2017, 317, 626–634. [Google Scholar] [CrossRef] [PubMed]
- Sun, Y.; Liu, B.; Snetselaar, L.G.; Wallace, R.B.; Caan, B.J.; Rohan, T.E.; Neuhouser, M.L.; Shadyab, A.H.; Chlebowski, R.T.; Manson, J.E.; et al. Association of Normal-Weight Central Obesity with All-Cause and Cause-Specific Mortality Among Postmenopausal Women. JAMA Netw. Open 2019, 2, e197337. [Google Scholar] [CrossRef] [Green Version]
- Manolopoulos, K.N.; Karpe, F.; Frayn, K.N. Gluteofemoral body fat as a determinant of metabolic health. Int. J. Obes. 2010, 34, 949–959. [Google Scholar] [CrossRef] [Green Version]
- Lotta, L.A.; Wittemans, L.B.L.; Zuber, V.; Stewart, I.D.; Sharp, S.J.; Luan, J.; Day, F.R.; Li, C.; Bowker, N.; Cai, L.; et al. Association of Genetic Variants Related to Gluteofemoral vs Abdominal Fat Distribution with Type 2 Diabetes, Coronary Disease, and Cardiovascular Risk Factors. JAMA 2018, 320, 2553–2563. [Google Scholar] [CrossRef] [Green Version]
- Agrawal, S.; Wang, M.; Klarqvist, M.D.R.; Smith, K.; Shin, J.; Dashti, H.; Diamant, N.; Choi, S.H.; Jurgens, S.J.; Ellinor, P.T.; et al. Inherited basis of visceral, abdominal subcutaneous and gluteofemoral fat depots. Nat. Commun. 2022, 13, 3771. [Google Scholar] [CrossRef]
- Hernandez, T.L.; Kittelson, J.M.; Law, C.K.; Ketch, L.L.; Stob, N.R.; Lindstrom, R.C.; Scherzinger, A.; Stamm, E.R.; Eckel, R.H. Fat redistribution following suction lipectomy: Defense of body fat and patterns of restoration. Obesity 2011, 19, 1388–1395. [Google Scholar] [CrossRef]
- Wibmer, A.G.; Becher, T.; Eljalby, M.; Crane, A.; Andrieu, P.C.; Jiang, C.S.; Vaughan, R.; Schoder, H.; Cohen, P. Brown adipose tissue is associated with healthier body fat distribution and metabolic benefits independent of regional adiposity. Cell Rep. Med. 2021, 2, 100332. [Google Scholar] [CrossRef]
- Saito, M.; Okamatsu-Ogura, Y.; Matsushita, M.; Watanabe, K.; Yoneshiro, T.; Nio-Kobayashi, J.; Iwanaga, T.; Miyagawa, M.; Kameya, T.; Nakada, K.; et al. High incidence of metabolically active brown adipose tissue in healthy adult humans: Effects of cold exposure and adiposity. Diabetes 2009, 58, 1526–1531. [Google Scholar] [CrossRef]
- Chen, X.; McClusky, R.; Chen, J.; Beaven, S.W.; Tontonoz, P.; Arnold, A.P.; Reue, K. The number of x chromosomes causes sex differences in adiposity in mice. PLoS Genet. 2012, 8, e1002709. [Google Scholar] [CrossRef] [Green Version]
- Clement, K.; Mosbah, H.; Poitou, C. Rare genetic forms of obesity: From gene to therapy. Physiol. Behav. 2020, 227, 113134. [Google Scholar] [CrossRef]
- Zammouri, J.; Vatier, C.; Capel, E.; Auclair, M.; Storey-London, C.; Bismuth, E.; Mosbah, H.; Donadille, B.; Janmaat, S.; Feve, B.; et al. Molecular and Cellular Bases of Lipodystrophy Syndromes. Front. Endocrinol. 2021, 12, 803189. [Google Scholar] [CrossRef]
- Locke, A.E.; Kahali, B.; Berndt, S.I.; Justice, A.E.; Pers, T.H.; Day, F.R.; Powell, C.; Vedantam, S.; Buchkovich, M.L.; Yang, J.; et al. Genetic studies of body mass index yield new insights for obesity biology. Nature 2015, 518, 197–206. [Google Scholar] [CrossRef] [Green Version]
- Shungin, D.; Winkler, T.W.; Croteau-Chonka, D.C.; Ferreira, T.; Locke, A.E.; Magi, R.; Strawbridge, R.J.; Pers, T.H.; Fischer, K.; Justice, A.E.; et al. New genetic loci link adipose and insulin biology to body fat distribution. Nature 2015, 518, 187–196. [Google Scholar] [CrossRef] [Green Version]
- Koprulu, M.; Zhao, Y.; Wheeler, E.; Dong, L.; Rocha, N.; Li, C.; Griffin, J.D.; Patel, S.; Van de Streek, M.; Glastonbury, C.A.; et al. Identification of Rare Loss-of-Function Genetic Variation Regulating Body Fat Distribution. J. Clin. Endocrinol. Metab. 2022, 107, 1065–1077. [Google Scholar] [CrossRef]
- Deaton, A.M.; Dubey, A.; Ward, L.D.; Dornbos, P.; Flannick, J.; Consortium, A.-T.D.G.; Yee, E.; Ticau, S.; Noetzli, L.; Parker, M.M.; et al. Rare loss of function variants in the hepatokine gene INHBE protect from abdominal obesity. Nat. Commun. 2022, 13, 4319. [Google Scholar] [CrossRef]
- Pulit, S.L.; Stoneman, C.; Morris, A.P.; Wood, A.R.; Glastonbury, C.A.; Tyrrell, J.; Yengo, L.; Ferreira, T.; Marouli, E.; Ji, Y.; et al. Meta-analysis of genome-wide association studies for body fat distribution in 694 649 individuals of European ancestry. Hum. Mol. Genet. 2019, 28, 166–174. [Google Scholar] [CrossRef] [Green Version]
- Sandovici, I.; Fernandez-Twinn, D.S.; Hufnagel, A.; Constancia, M.; Ozanne, S.E. Sex differences in the intergenerational inheritance of metabolic traits. Nat. Metab. 2022, 4, 507–523. [Google Scholar] [CrossRef]
- Stein, A.D.; Kahn, H.S.; Rundle, A.; Zybert, P.A.; van der Pal-de Bruin, K.; Lumey, L.H. Anthropometric measures in middle age after exposure to famine during gestation: Evidence from the Dutch famine. Am. J. Clin. Nutr. 2007, 85, 869–876. [Google Scholar] [CrossRef]
- Andres, A.; Hull, H.R.; Shankar, K.; Casey, P.H.; Cleves, M.A.; Badger, T.M. Longitudinal body composition of children born to mothers with normal weight, overweight, and obesity. Obesity 2015, 23, 1252–1258. [Google Scholar] [CrossRef]
- Lecoutre, S.; Petrus, P.; Ryden, M.; Breton, C. Transgenerational Epigenetic Mechanisms in Adipose Tissue Development. Trends Endocrinol. Metab. 2018, 29, 675–685. [Google Scholar] [CrossRef]
- Soellner, L.; Begemann, M.; Mackay, D.J.; Gronskov, K.; Tumer, Z.; Maher, E.R.; Temple, I.K.; Monk, D.; Riccio, A.; Linglart, A.; et al. Recent Advances in Imprinting Disorders. Clin. Genet. 2017, 91, 3–13. [Google Scholar] [CrossRef] [Green Version]
- Small, K.S.; Todorcevic, M.; Civelek, M.; El-Sayed Moustafa, J.S.; Wang, X.; Simon, M.M.; Fernandez-Tajes, J.; Mahajan, A.; Horikoshi, M.; Hugill, A.; et al. Regulatory variants at KLF14 influence type 2 diabetes risk via a female-specific effect on adipocyte size and body composition. Nat. Genet. 2018, 50, 572–580. [Google Scholar] [CrossRef]
- Chen, Y.T.; Yang, Q.Y.; Hu, Y.; Liu, X.D.; de Avila, J.M.; Zhu, M.J.; Nathanielsz, P.W.; Du, M. Imprinted lncRNA Dio3os preprograms intergenerational brown fat development and obesity resistance. Nat. Commun. 2021, 12, 6845. [Google Scholar] [CrossRef]
- Savva, C.; Helguero, L.A.; Gonzalez-Granillo, M.; Melo, T.; Couto, D.; Buyandelger, B.; Gustafsson, S.; Liu, J.; Domingues, M.R.; Li, X.; et al. Maternal high-fat diet programs white and brown adipose tissue lipidome and transcriptome in offspring in a sex- and tissue-dependent manner in mice. Int. J. Obes. 2022, 46, 831–842. [Google Scholar] [CrossRef]
- Oliva, M.; Munoz-Aguirre, M.; Kim-Hellmuth, S.; Wucher, V.; Gewirtz, A.D.H.; Cotter, D.J.; Parsana, P.; Kasela, S.; Balliu, B.; Vinuela, A.; et al. The impact of sex on gene expression across human tissues. Science 2020, 369, eaba3066. [Google Scholar] [CrossRef] [PubMed]
- Emont, M.P.; Jacobs, C.; Essene, A.L.; Pant, D.; Tenen, D.; Colleluori, G.; Di Vincenzo, A.; Jorgensen, A.M.; Dashti, H.; Stefek, A.; et al. A single-cell atlas of human and mouse white adipose tissue. Nature 2022, 603, 926–933. [Google Scholar] [CrossRef] [PubMed]
- Anderson, W.D.; Soh, J.Y.; Innis, S.E.; Dimanche, A.; Ma, L.; Langefeld, C.D.; Comeau, M.E.; Das, S.K.; Schadt, E.E.; Bjorkegren, J.L.M.; et al. Sex differences in human adipose tissue gene expression and genetic regulation involve adipogenesis. Genome. Res. 2020, 30, 1379–1392. [Google Scholar] [CrossRef] [PubMed]
- Sebo, Z.L.; Rodeheffer, M.S. Assembling the adipose organ: Adipocyte lineage segregation and adipogenesis in vivo. Development 2019, 146, dev172098. [Google Scholar] [CrossRef] [PubMed]
- Gesta, S.; Tseng, Y.H.; Kahn, C.R. Developmental origin of fat: Tracking obesity to its source. Cell 2007, 131, 242–256. [Google Scholar] [CrossRef] [Green Version]
- Gao, H.; Olat, F.; Sandhow, L.; Galitzky, J.; Nguyen, T.; Esteve, D.; Astrom, G.; Mejhert, N.; Ledoux, S.; Thalamas, C.; et al. CD36 Is a Marker of Human Adipocyte Progenitors with Pronounced Adipogenic and Triglyceride Accumulation Potential. Stem Cells 2017, 35, 1799–1814. [Google Scholar] [CrossRef] [Green Version]
- Esteve, D.; Boulet, N.; Belles, C.; Zakaroff-Girard, A.; Decaunes, P.; Briot, A.; Veeranagouda, Y.; Didier, M.; Remaury, A.; Guillemot, J.C.; et al. Lobular architecture of human adipose tissue defines the niche and fate of progenitor cells. Nat. Commun. 2019, 10, 2549. [Google Scholar] [CrossRef] [Green Version]
- White, U.A.; Fitch, M.D.; Beyl, R.A.; Hellerstein, M.K.; Ravussin, E. Differences in In Vivo Cellular Kinetics in Abdominal and Femoral Subcutaneous Adipose Tissue in Women. Diabetes 2016, 65, 1642–1647. [Google Scholar] [CrossRef] [Green Version]
- Tchoukalova, Y.D.; Votruba, S.B.; Tchkonia, T.; Giorgadze, N.; Kirkland, J.L.; Jensen, M.D. Regional differences in cellular mechanisms of adipose tissue gain with overfeeding. Proc. Natl. Acad. Sci. USA 2010, 107, 18226–18231. [Google Scholar] [CrossRef] [Green Version]
- Jeffery, E.; Wing, A.; Holtrup, B.; Sebo, Z.; Kaplan, J.L.; Saavedra-Pena, R.; Church, C.D.; Colman, L.; Berry, R.; Rodeheffer, M.S. The Adipose Tissue Microenvironment Regulates Depot-Specific Adipogenesis in Obesity. Cell Metab. 2016, 24, 142–150. [Google Scholar] [CrossRef] [Green Version]
- Shan, B.; Barker, C.S.; Shao, M.; Zhang, Q.; Gupta, R.K.; Wu, Y. Multilayered omics reveal sex- and depot-dependent adipose progenitor cell heterogeneity. Cell Metab. 2022, 34, 783–799.e7. [Google Scholar] [CrossRef]
- Maurer, S.; Harms, M.; Boucher, J. The colorful versatility of adipocytes: White-to-brown transdifferentiation and its therapeutic potential in humans. FEBS J. 2021, 288, 3628–3646. [Google Scholar] [CrossRef]
- Cinti, S. Pink Adipocytes. Trends Endocrinol. Metab. 2018, 29, 651–666. [Google Scholar] [CrossRef]
- Chau, Y.Y.; Bandiera, R.; Serrels, A.; Martinez-Estrada, O.M.; Qing, W.; Lee, M.; Slight, J.; Thornburn, A.; Berry, R.; McHaffie, S.; et al. Visceral and subcutaneous fat have different origins and evidence supports a mesothelial source. Nat. Cell Biol. 2014, 16, 367–375. [Google Scholar] [CrossRef]
- Westcott, G.P.; Emont, M.P.; Li, J.; Jacobs, C.; Tsai, L.; Rosen, E.D. Mesothelial cells are not a source of adipocytes in mice. Cell Rep. 2021, 36, 109388. [Google Scholar] [CrossRef]
- Norreen-Thorsen, M.; Struck, E.C.; Oling, S.; Zwahlen, M.; Von Feilitzen, K.; Odeberg, J.; Lindskog, C.; Ponten, F.; Uhlen, M.; Dusart, P.J.; et al. A human adipose tissue cell-type transcriptome atlas. Cell Rep. 2022, 40, 111046. [Google Scholar] [CrossRef]
- Arner, P. Differences in lipolysis between human subcutaneous and omental adipose tissues. Ann. Med. 1995, 27, 435–438. [Google Scholar] [CrossRef]
- Jensen, M.D. Role of body fat distribution and the metabolic complications of obesity. J. Clin. Endocrinol. Metab. 2008, 93 (Suppl. S1), S57–S63. [Google Scholar] [CrossRef] [Green Version]
- Andersson, D.P.; Lofgren, P.; Thorell, A.; Arner, P.; Hoffstedt, J. Visceral fat cell lipolysis and cardiovascular risk factors in obesity. Horm. Metab. Res. 2011, 43, 809–815. [Google Scholar] [CrossRef]
- Martin, M.L.; Jensen, M.D. Effects of body fat distribution on regional lipolysis in obesity. J. Clin. Investig. 1991, 88, 609–613. [Google Scholar] [CrossRef] [Green Version]
- Rebuffe-Scrive, M.; Lonnroth, P.; Marin, P.; Wesslau, C.; Bjorntorp, P.; Smith, U. Regional adipose tissue metabolism in men and postmenopausal women. Int. J. Obes. 1987, 11, 347–355. [Google Scholar]
- Rebuffe-Scrive, M.; Eldh, J.; Hafstrom, L.O.; Bjorntorp, P. Metabolism of mammary, abdominal, and femoral adipocytes in women before and after menopause. Metabolism 1986, 35, 792–797. [Google Scholar] [CrossRef]
- Lonnqvist, F.; Thorne, A.; Large, V.; Arner, P. Sex differences in visceral fat lipolysis and metabolic complications of obesity. Arterioscler. Thromb. Vasc. Biol. 1997, 17, 1472–1480. [Google Scholar] [CrossRef]
- Jensen, M.D.; Sarr, M.G.; Dumesic, D.A.; Southorn, P.A.; Levine, J.A. Regional uptake of meal fatty acids in humans. Am. J. Physiol. Endocrinol. Metab. 2003, 285, E1282–E1288. [Google Scholar] [CrossRef] [Green Version]
- Votruba, S.B.; Jensen, M.D. Sex-specific differences in leg fat uptake are revealed with a high-fat meal. Am. J. Physiol. Endocrinol. Metab. 2006, 291, E1115–E1123. [Google Scholar] [CrossRef]
- McQuaid, S.E.; Humphreys, S.M.; Hodson, L.; Fielding, B.A.; Karpe, F.; Frayn, K.N. Femoral adipose tissue may accumulate the fat that has been recycled as VLDL and nonesterified fatty acids. Diabetes 2010, 59, 2465–2473. [Google Scholar] [CrossRef] [Green Version]
- Pan, D.Z.; Miao, Z.; Comenho, C.; Rajkumar, S.; Koka, A.; Lee, S.H.T.; Alvarez, M.; Kaminska, D.; Ko, A.; Sinsheimer, J.S.; et al. Identification of TBX15 as an adipose master trans regulator of abdominal obesity genes. Genome. Med. 2021, 13, 123. [Google Scholar] [CrossRef]
- Racimo, F.; Gokhman, D.; Fumagalli, M.; Ko, A.; Hansen, T.; Moltke, I.; Albrechtsen, A.; Carmel, L.; Huerta-Sanchez, E.; Nielsen, R. Archaic Adaptive Introgression in TBX15/WARS2. Mol. Biol. Evol. 2017, 34, 509–524. [Google Scholar] [CrossRef] [Green Version]
- Tin Tin, S.; Reeves, G.K.; Key, T.J. Body size and composition, physical activity and sedentary time in relation to endogenous hormones in premenopausal and postmenopausal women: Findings from the UK Biobank. Int. J. Cancer 2020, 147, 2101–2115. [Google Scholar] [CrossRef] [Green Version]
- Watts, E.L.; Perez-Cornago, A.; Doherty, A.; Allen, N.E.; Fensom, G.K.; Tin Tin, S.; Key, T.J.; Travis, R.C. Physical activity in relation to circulating hormone concentrations in 117,100 men in UK Biobank. Cancer Causes Control 2021, 32, 1197–1212. [Google Scholar] [CrossRef]
- Bjorntorp, P. The regulation of adipose tissue distribution in humans. Int. J. Obes. Relat. Metab. Disord. 1996, 20, 291–302. [Google Scholar] [PubMed]
- Lee, M.J.; Pramyothin, P.; Karastergiou, K.; Fried, S.K. Deconstructing the roles of glucocorticoids in adipose tissue biology and the development of central obesity. Biochim. Biophys. Acta 2014, 1842, 473–481. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mathew, H.; Castracane, V.D.; Mantzoros, C. Adipose tissue and reproductive health. Metabolism 2018, 86, 18–32. [Google Scholar] [CrossRef] [PubMed]
- De Morentin, P.B.M.; Gonzalez-Garcia, I.; Martins, L.; Lage, R.; Fernandez-Mallo, D.; Martinez-Sanchez, N.; Ruiz-Pino, F.; Liu, J.; Morgan, D.A.; Pinilla, L.; et al. Estradiol regulates brown adipose tissue thermogenesis via hypothalamic AMPK. Cell Metab. 2014, 20, 41–53. [Google Scholar]
- Gavin, K.M.; Cooper, E.E.; Raymer, D.K.; Hickner, R.C. Estradiol effects on subcutaneous adipose tissue lipolysis in premenopausal women are adipose tissue depot specific and treatment dependent. Am. J. Physiol. Endocrinol. Metab. 2013, 304, E1167–E1174. [Google Scholar] [CrossRef] [Green Version]
- Kaikaew, K.; Grefhorst, A.; Visser, J.A. Sex Differences in Brown Adipose Tissue Function: Sex Hormones, Glucocorticoids, and Their Crosstalk. Front. Endocrinol. 2021, 12, 652444. [Google Scholar] [CrossRef]
- Pirastu, N.; Cordioli, M.; Nandakumar, P.; Mignogna, G.; Abdellaoui, A.; Hollis, B.; Kanai, M.; Rajagopal, V.M.; Parolo, P.D.B.; Baya, N.; et al. Genetic analyses identify widespread sex-differential participation bias. Nat. Genet. 2021, 53, 663–671. [Google Scholar] [CrossRef]
- Stevens, V.L.; Carter, B.D.; McCullough, M.L.; Campbell, P.T.; Wang, Y. Metabolomic Profiles Associated with BMI, Waist Circumference, and Diabetes and Inflammation Biomarkers in Women. Obesity 2020, 28, 187–196. [Google Scholar] [CrossRef] [Green Version]
- Bao, X.; Xu, B.; Yin, S.; Pan, J.; Nilsson, P.M.; Nilsson, J.; Melander, O.; Orho-Melander, M.; Engstrom, G. Proteomic Profiles of Body Mass Index and Waist-to-Hip Ratio and Their Role in Incidence of Diabetes. J. Clin. Endocrinol. Metab. 2022, 107, e2982–e2990. [Google Scholar] [CrossRef]
- Abraham, T.; Romani, A.M.P. The Relationship between Obesity and Pre-Eclampsia: Incidental Risks and Identification of Potential Biomarkers for Pre-Eclampsia. Cells 2022, 11, 1548. [Google Scholar] [CrossRef]
- Rahnemaei, F.A.; Abdi, F.; Pakzad, R.; Sharami, S.H.; Mokhtari, F.; Kazemian, E. Association of body composition in early pregnancy with gestational diabetes mellitus: A meta-analysis. PLoS ONE 2022, 17, e0271068. [Google Scholar] [CrossRef]
Indicator | Cut-Off Points |
---|---|
Waist circumference (WC, cm) | >94 Men |
>80 Women | |
Waist-to-hip ratio (WHR) | ≥0.9 Men |
≥0.85 Women | |
BMI (kg/m2) | ≥30 |
Waist circumference (WC, cm) | >94 Men |
>80 Women | |
Waist-to-hip ratio (WHR) | ≥0.9 Men |
≥0.85 Women |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Boulet, N.; Briot, A.; Galitzky, J.; Bouloumié, A. The Sexual Dimorphism of Human Adipose Depots. Biomedicines 2022, 10, 2615. https://doi.org/10.3390/biomedicines10102615
Boulet N, Briot A, Galitzky J, Bouloumié A. The Sexual Dimorphism of Human Adipose Depots. Biomedicines. 2022; 10(10):2615. https://doi.org/10.3390/biomedicines10102615
Chicago/Turabian StyleBoulet, Nathalie, Anais Briot, Jean Galitzky, and Anne Bouloumié. 2022. "The Sexual Dimorphism of Human Adipose Depots" Biomedicines 10, no. 10: 2615. https://doi.org/10.3390/biomedicines10102615