1932

Abstract

Biological sex is a fundamental source of phenotypic variability across species. Males and females have different nutritional needs and exhibit differences in nutrient digestion and utilization, leading to different health outcomes throughout life. With personalized nutrition gaining popularity in scientific research and clinical practice, it is important to understand the fundamentals of sex differences in nutrition research. Here, we review key studies that investigate sex dimorphism in nutrition research: sex differences in nutrient intake and metabolism, sex-dimorphic response in nutrient-restricted conditions, and sex differences in diet and gut microbiome interactions. Within each area above, factors from sex chromosomes, sex hormones, and sex-specific loci are highlighted.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-nutr-062220-105852
2022-08-22
2024-06-22
Loading full text...

Full text loading...

/deliver/fulltext/nutr/42/1/annurev-nutr-062220-105852.html?itemId=/content/journals/10.1146/annurev-nutr-062220-105852&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Acharya KD, Gao X, Bless EP, Chen J, Tetel MJ 2019. Estradiol and high fat diet associate with changes in gut microbiota in female ob/ob mice. Sci. Rep. 9:20192
    [Google Scholar]
  2. 2.
    Arnold AP. 2009. The organizational-activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues. Horm. Behav. 55:570–78
    [Google Scholar]
  3. 3.
    Arnold AP. 2019. Rethinking sex determination of non-gonadal tissues. Curr. Top. Dev. Biol. 134:289–315
    [Google Scholar]
  4. 4.
    Arnold AP. 2020. Four Core Genotypes and XY* mouse models: update on impact on SABV research. Neurosci. Biobehav. Rev. 119:1–8
    [Google Scholar]
  5. 5.
    Arnold AP, Breedlove SM. 1985. Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm. Behav. 19:469–98
    [Google Scholar]
  6. 6.
    Asarian L, Geary N. 2006. Modulation of appetite by gonadal steroid hormones. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361:1251–63
    [Google Scholar]
  7. 7.
    Asarian L, Geary N. 2013. Sex differences in the physiology of eating. Am. J. Physiol. Regul. Integr. Comp. Physiol. 305:R1215–67
    [Google Scholar]
  8. 8.
    Astafev AA, Patel SA, Kondratov RV. 2017. Calorie restriction effects on circadian rhythms in gene expression are sex dependent. Sci. Rep. 7:9716
    [Google Scholar]
  9. 9.
    Backhed F, Manchester JK, Semenkovich CF, Gordon JI. 2007. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. PNAS 104:979–84
    [Google Scholar]
  10. 10.
    Bazhan N, Jakovleva T, Feofanova N, Denisova E, Dubinina A et al. 2019. Sex differences in liver, adipose tissue, and muscle transcriptional response to fasting and refeeding in mice. Cells 8:1529
    [Google Scholar]
  11. 11.
    Becker JB, Arnold AP, Berkley KJ, Blaustein JD, Eckel LA et al. 2005. Strategies and methods for research on sex differences in brain and behavior. Endocrinology 146:1650–73
    [Google Scholar]
  12. 12.
    Blaak E. 2001. Gender differences in fat metabolism. Curr. Opin. Clin. Nutr. Metab. Care 4:499–502
    [Google Scholar]
  13. 13.
    Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Org E et al. 2014. Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat. Commun. 5:4500
    [Google Scholar]
  14. 14.
    Brandhorst S, Choi IY, Wei M, Cheng CW, Sedrakyan S et al. 2015. A periodic diet that mimics fasting promotes multi-system regeneration, enhanced cognitive performance, and healthspan. Cell Metab 22:86–99
    [Google Scholar]
  15. 15.
    Brestoff JR, Artis D. 2013. Commensal bacteria at the interface of host metabolism and the immune system. Nat. Immunol. 14:676–84
    [Google Scholar]
  16. 16.
    Bridgewater LC, Zhang C, Wu Y, Hu W, Zhang Q et al. 2017. Gender-based differences in host behavior and gut microbiota composition in response to high fat diet and stress in a mouse model. Sci. Rep. 7:10776
    [Google Scholar]
  17. 17.
    Burgoyne PS, Arnold AP. 2016. A primer on the use of mouse models for identifying direct sex chromosome effects that cause sex differences in non-gonadal tissues. Biol. Sex Differ. 7:68
    [Google Scholar]
  18. 18.
    Butera PC. 2010. Estradiol and the control of food intake. Physiol. Behav. 99:175–80
    [Google Scholar]
  19. 19.
    Byrne CS, Chambers ES, Morrison DJ, Frost G. 2015. The role of short chain fatty acids in appetite regulation and energy homeostasis. Int. J. Obes. 39:1331–38
    [Google Scholar]
  20. 20.
    Cani PD. 2018. Human gut microbiome: hopes, threats and promises. Gut 67:1716–25
    [Google Scholar]
  21. 21.
    Carabotti M, Scirocco A, Maselli MA, Severi C. 2015. The gut-brain axis: interactions between enteric microbiota, central and enteric nervous systems. Ann. Gastroenterol. 28:203–9
    [Google Scholar]
  22. 22.
    Chai JK, Blaha V, Meguid MM, Laviano A, Yang ZJ, Varma M. 1999. Use of orchiectomy and testosterone replacement to explore meal number-to-meal size relationship in male rats. Am. J. Physiol. 276:R1366–73
    [Google Scholar]
  23. 23.
    Chen X, McClusky R, Chen J, Beaven SW, Tontonoz P et al. 2012. The number of x chromosomes causes sex differences in adiposity in mice. PLOS Genet 8:e1002709
    [Google Scholar]
  24. 24.
    Chen X, Wang L, Loh DH, Colwell CS, Tache Y et al. 2015. Sex differences in diurnal rhythms of food intake in mice caused by gonadal hormones and complement of sex chromosomes. Horm. Behav. 75:55–63
    [Google Scholar]
  25. 25.
    Childs CE. 2020. Sex hormones and n-3 fatty acid metabolism. Proc. Nutr. Soc. 79:219–24
    [Google Scholar]
  26. 26.
    Childs CE, Romeu-Nadal M, Burdge GC, Calder PC. 2008. Gender differences in the n-3 fatty acid content of tissues. Proc. Nutr. Soc. 67:19–27
    [Google Scholar]
  27. 27.
    Cho I, Yamanishi S, Cox L, Methe BA, Zavadil J et al. 2012. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 488:621–26
    [Google Scholar]
  28. 28.
    Christensen P, Meinert Larsen T, Westerterp-Plantenga M, Macdonald I, Martinez JA et al. 2018. Men and women respond differently to rapid weight loss: metabolic outcomes of a multi-centre intervention study after a low-energy diet in 2500 overweight, individuals with pre-diabetes (PREVIEW). Diabetes Obes. Metab. 20:2840–51
    [Google Scholar]
  29. 29.
    Clegg DJ, Brown LM, Woods SC, Benoit SC. 2006. Gonadal hormones determine sensitivity to central leptin and insulin. Diabetes 55:978–87
    [Google Scholar]
  30. 30.
    Cox LM, Schafer MJ, Sohn J, Vincentini J, Weiner HL et al. 2019. Calorie restriction slows age-related microbiota changes in an Alzheimer's disease model in female mice. Sci. Rep. 9:17904
    [Google Scholar]
  31. 31.
    Culbert KM, Sisk CL, Klump KL. 2021. A narrative review of sex differences in eating disorders: Is there a biological basis?. Clin. Ther. 43:95–111
    [Google Scholar]
  32. 32.
    Dalla C, Shors TJ. 2009. Sex differences in learning processes of classical and operant conditioning. Physiol. Behav. 97:229–38
    [Google Scholar]
  33. 33.
    Daly CM, Saxena J, Singh J, Bullard MR, Bondy EO et al. 2020. Sex differences in response to a high fat, high sucrose diet in both the gut microbiome and hypothalamic astrocytes and microglia. Nutr. Neurosci. 25:32135
    [Google Scholar]
  34. 34.
    Dominianni C, Sinha R, Goedert JJ, Pei Z, Yang L et al. 2015. Sex, body mass index, and dietary fiber intake influence the human gut microbiome. PLOS ONE 10:e0124599
    [Google Scholar]
  35. 35.
    Ervin SM, Li H, Lim L, Roberts LR, Liang X et al. 2019. Gut microbial β-glucuronidases reactivate estrogens as components of the estrobolome that reactivate estrogens. J. Biol. Chem. 294:18586–99
    [Google Scholar]
  36. 36.
    Falony G, Joossens M, Vieira-Silva S, Wang J, Darzi Y et al. 2016. Population-level analysis of gut microbiome variation. Science 352:560–64
    [Google Scholar]
  37. 37.
    Fox HS. 1992. Androgen treatment prevents diabetes in nonobese diabetic mice. J. Exp. Med. 175:1409–12
    [Google Scholar]
  38. 38.
    Freire T, Senior AM, Perks R, Pulpitel T, Clark X et al. 2020. Sex-specific metabolic responses to 6 hours of fasting during the active phase in young mice. J. Physiol. 598:2081–92
    [Google Scholar]
  39. 39.
    Gabel K, Hoddy KK, Haggerty N, Song J, Kroeger CM et al. 2018. Effects of 8-hour time restricted feeding on body weight and metabolic disease risk factors in obese adults: a pilot study. Nutr. Healthy Aging 4:345–53
    [Google Scholar]
  40. 40.
    Gao X, Zhang M, Xue J, Huang J, Zhuang R et al. 2018. Body mass index differences in the gut microbiota are gender specific. Front. Microbiol. 9:1250
    [Google Scholar]
  41. 41.
    Geary N, Asarian L, Korach KS, Pfaff DW, Ogawa S. 2001. Deficits in E2-dependent control of feeding, weight gain, and cholecystokinin satiation in ER-α null mice. Endocrinology 142:4751–57
    [Google Scholar]
  42. 42.
    Grgurevic N, Budefeld T, Rissman EF, Tobet SA, Majdic G. 2008. Aggressive behaviors in adult SF-1 knockout mice that are not exposed to gonadal steroids during development. Behav. Neurosci. 122:876–84
    [Google Scholar]
  43. 43.
    Grgurevic N, Budefeld T, Spanic T, Tobet SA, Majdic G. 2012. Evidence that sex chromosome genes affect sexual differentiation of female sexual behavior. Horm. Behav. 61:719–24
    [Google Scholar]
  44. 44.
    Gruenewald DA, Matsumoto AM. 1993. Reduced gonadotropin-releasing hormone gene expression with fasting in the male rat brain. Endocrinology 132:480–82
    [Google Scholar]
  45. 45.
    Haro C, Rangel-Zuñiga OA, Alcalá-Díaz JF, Gómez-Delgado F, Pérez-Martínez P et al. 2016. Intestinal microbiota is influenced by gender and body mass index. PLOS ONE 11:e0154090
    [Google Scholar]
  46. 46.
    Horikoshi M, Mgi R, van de Bunt M, Surakka I, Sarin AP et al. 2015. Discovery and fine-mapping of glycaemic and obesity-related trait loci using high-density imputation. PLOS Genet 11:e1005230
    [Google Scholar]
  47. 47.
    Husain R, Duncan MT, Cheah SH, Ch'ng SL. 1987. Effects of fasting in Ramadan on tropical Asiatic Moslems. Br. J. Nutr. 58:41–48
    [Google Scholar]
  48. 48.
    Jasarevic E, Morrison KE, Bale TL. 2016. Sex differences in the gut microbiome-brain axis across the lifespan. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371:20150122
    [Google Scholar]
  49. 49.
    Just S, Mondot S, Ecker J, Wegner K, Rath E et al. 2018. The gut microbiota drives the impact of bile acids and fat source in diet on mouse metabolism. Microbiome 6:134
    [Google Scholar]
  50. 50.
    Kaliannan K, Robertson RC, Murphy K, Stanton C, Kang C et al. 2018. Estrogen-mediated gut microbiome alterations influence sexual dimorphism in metabolic syndrome in mice. Microbiome 6:205
    [Google Scholar]
  51. 51.
    Kane AE, Sinclair DA, Mitchell JR, Mitchell SJ. 2018. Sex differences in the response to dietary restriction in rodents. Curr. Opin. Physiol. 6:28–34
    [Google Scholar]
  52. 52.
    Karunasena E, McMahon KW, Chang D, Brashears MM 2014. Host responses to the pathogen Mycobacterium avium subsp. paratuberculosis and beneficial microbes exhibit host sex specificity. Appl. Environ. Microbiol. 80:4481–90
    [Google Scholar]
  53. 53.
    Kasai C, Sugimoto K, Moritani I, Tanaka J, Oya Y et al. 2015. Comparison of the gut microbiota composition between obese and non-obese individuals in a Japanese population, as analyzed by terminal restriction fragment length polymorphism and next-generation sequencing. BMC Gastroenterol 15:100
    [Google Scholar]
  54. 54.
    Kilpelainen TO, Zillikens MC, Stancakova A, Finucane FM, Ried JS et al. 2011. Genetic variation near IRS1 associates with reduced adiposity and an impaired metabolic profile. Nat. Genet. 43:753–60
    [Google Scholar]
  55. 55.
    Knip M, Siljander H. 2016. The role of the intestinal microbiota in type 1 diabetes mellitus. Nat. Rev. Endocrinol. 12:154–67
    [Google Scholar]
  56. 56.
    Lagou V, Magi R, Hottenga JJ, Grallert H, Perry JRB et al. 2021. Sex-dimorphic genetic effects and novel loci for fasting glucose and insulin variability. Nat. Commun. 12:24
    [Google Scholar]
  57. 57.
    Lessan N, Ali T. 2019. Energy metabolism and intermittent fasting: the Ramadan perspective. Nutrients 11:1192
    [Google Scholar]
  58. 58.
    Li W, Dowd SE, Scurlock B, Acosta-Martinez V, Lyte M. 2009. Memory and learning behavior in mice is temporally associated with diet-induced alterations in gut bacteria. Physiol. Behav. 96:557–67
    [Google Scholar]
  59. 59.
    Link JC, Chen X, Prien C, Borja MS, Hammerson B et al. 2015. Increased high-density lipoprotein cholesterol levels in mice with XX versus XY sex chromosomes. Arterioscler. Thromb. Vasc. Biol. 35:1778–86
    [Google Scholar]
  60. 60.
    Link JC, Reue K. 2017. Genetic basis for sex differences in obesity and lipid metabolism. Annu. Rev. Nutr. 37:225–45
    [Google Scholar]
  61. 61.
    Link JC, Wiese CB, Chen X, Avetisyan R, Ronquillo E et al. 2020. X chromosome dosage of histone demethylase KDM5C determines sex differences in adiposity. J. Clin. Investig. 130:5688–702
    [Google Scholar]
  62. 62.
    Lombardi P, Goldin B, Boutin E, Gorbach SL. 1978. Metabolism of androgens and estrogens by human fecal microorganisms. J. Steroid. Biochem. 9:795–801
    [Google Scholar]
  63. 63.
    Loos RJ, Yeo GS. 2014. The bigger picture of FTO: the first GWAS-identified obesity gene. Nat. Rev. Endocrinol. 10:51–61
    [Google Scholar]
  64. 64.
    Lwin R, Darnell B, Oster R, Lawrence J, Foster J et al. 2008. Effect of oral estrogen on substrate utilization in postmenopausal women. Fertil. Steril. 90:1275–78
    [Google Scholar]
  65. 65.
    Macdiarmid JI, Vail A, Cade JE, Blundell JE. 1998. The sugar-fat relationship revisited: differences in consumption between men and women of varying BMI. Int. J. Obes. Relat. Metab. Disord. 22:1053–61
    [Google Scholar]
  66. 66.
    Marino M, Masella R, Bulzomi P, Campesi I, Malorni W, Franconi F. 2011. Nutrition and human health from a sex-gender perspective. Mol. Aspects Med. 32:1–70
    [Google Scholar]
  67. 67.
    Markle JG, Frank DN, Mortin-Toth S, Robertson CE, Feazel LM et al. 2013. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339:1084–88
    [Google Scholar]
  68. 68.
    Martens JH, Barg H, Warren MJ, Jahn D. 2002. Microbial production of vitamin B12. Appl. Microbiol. Biotechnol. 58:275–85
    [Google Scholar]
  69. 69.
    Martin B, Golden E, Carlson OD, Egan JM, Mattson MP, Maudsley S. 2008. Caloric restriction: impact upon pituitary function and reproduction. Ageing Res. Rev. 7:209–24
    [Google Scholar]
  70. 70.
    Martin B, Pearson M, Kebejian L, Golden E, Keselman A et al. 2007. Sex-dependent metabolic, neuroendocrine, and cognitive responses to dietary energy restriction and excess. Endocrinology 148:4318–33
    [Google Scholar]
  71. 71.
    Mattson MP, Longo VD, Harvie M. 2017. Impact of intermittent fasting on health and disease processes. Ageing Res. Rev. 39:46–58
    [Google Scholar]
  72. 72.
    Mauvais-Jarvis F. 2015. Sex differences in metabolic homeostasis, diabetes, and obesity. Biol. Sex Differ. 6:14
    [Google Scholar]
  73. 73.
    Mauvais-Jarvis F, Clegg DJ, Hevener AL. 2013. The role of estrogens in control of energy balance and glucose homeostasis. Endocr. Rev. 34:309–38
    [Google Scholar]
  74. 74.
    McKenzie S, Phillips SM, Carter SL, Lowther S, Gibala MJ, Tarnopolsky MA. 2000. Endurance exercise training attenuates leucine oxidation and BCOAD activation during exercise in humans. Am. J. Physiol. Endocrinol. Metab. 278:E580–87
    [Google Scholar]
  75. 75.
    McShane TM, Wise PM. 1996. Life-long moderate caloric restriction prolongs reproductive life span in rats without interrupting estrous cyclicity: effects on the gonadotropin-releasing hormone/luteinizing hormone axis. Biol. Reprod. 54:70–75
    [Google Scholar]
  76. 76.
    Min Y, Ma X, Sankaran K, Ru Y, Chen L et al. 2019. Sex-specific association between gut microbiome and fat distribution. Nat. Commun. 10:2408
    [Google Scholar]
  77. 77.
    Mitchell SJ, Madrigal-Matute J, Scheibye-Knudsen M, Fang E, Aon M et al. 2016. Effects of sex, strain, and energy intake on hallmarks of aging in mice. Cell Metab 23:1093–112
    [Google Scholar]
  78. 78.
    Moreno-Indias I, Sanchez-Alcoholado L, Sanchez-Garrido MA, Martin-Nunez GM, Perez-Jimenez F et al. 2016. Neonatal androgen exposure causes persistent gut microbiota dysbiosis related to metabolic disease in adult female rats. Endocrinology 157:4888–98
    [Google Scholar]
  79. 79.
    Mueller S, Saunier K, Hanisch C, Norin E, Alm L et al. 2006. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl. Environ. Microbiol. 72:1027–33
    [Google Scholar]
  80. 80.
    Muka T, Asllanaj E, Avazverdi N, Jaspers L, Stringa N et al. 2017. Age at natural menopause and risk of type 2 diabetes: a prospective cohort study. Diabetologia 60:1951–60
    [Google Scholar]
  81. 81.
    Nakagawa S, Lagisz M, Hector KL, Spencer HG. 2012. Comparative and meta-analytic insights into life extension via dietary restriction. Aging Cell 11:401–9
    [Google Scholar]
  82. 82.
    Navarro-Barron E, Hernandez C, Llera-Herrera R, Garcia-Gasca A, Gomez-Gil B. 2019. Overfeeding a high-fat diet promotes sex-specific alterations on the gut microbiota of the zebrafish (Danio rerio). Zebrafish 16:268–79
    [Google Scholar]
  83. 83.
    Nohara K, Zhang Y, Waraich RS, Laque A, Tiano JP et al. 2011. Early-life exposure to testosterone programs the hypothalamic melanocortin system. Endocrinology 152:1661–69
    [Google Scholar]
  84. 84.
    O'Toole PW, Jeffery IB 2015. Gut microbiota and aging. Science 350:1214–15
    [Google Scholar]
  85. 85.
    Org E, Mehrabian M, Parks BW, Shipkova P, Liu X et al. 2016. Sex differences and hormonal effects on gut microbiota composition in mice. Gut Microbes 7:313–22
    [Google Scholar]
  86. 86.
    Parks BW, Sallam T, Mehrabian M, Psychogios N, Hui ST et al. 2015. Genetic architecture of insulin resistance in the mouse. Cell Metab 21:334–47
    [Google Scholar]
  87. 87.
    Peng C, Xu X, Li Y, Li X, Yang X et al. 2020. Sex-specific association between the gut microbiome and high-fat diet-induced metabolic disorders in mice. Biol. Sex Differ. 11:5
    [Google Scholar]
  88. 88.
    Pentti K, Tuppurainen MT, Honkanen R, Sandini L, Kroger H et al. 2009. Hormone therapy protects from diabetes: the Kuopio osteoporosis risk factor and prevention study. Eur. J. Endocrinol. 160:979–83
    [Google Scholar]
  89. 89.
    Pitkanen HT, Oja SS, Kemppainen K, Seppa JM, Mero AA. 2003. Serum amino acid concentrations in aging men and women. Amino Acids 24:413–21
    [Google Scholar]
  90. 90.
    Qin Y, Roberts JD, Grimm SA, Lih FB, Deterding LJ et al. 2018. An obesity-associated gut microbiome reprograms the intestinal epigenome and leads to altered colonic gene expression. Genome Biol 19:7
    [Google Scholar]
  91. 91.
    Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE et al. 2013. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341:1241214
    [Google Scholar]
  92. 92.
    Romanski SA, Nelson RM, Jensen MD. 2000. Meal fatty acid uptake in adipose tissue: gender effects in nonobese humans. Am. J. Physiol. Endocrinol. Metab. 279:E455–62
    [Google Scholar]
  93. 93.
    Salpeter SR, Walsh JM, Ormiston TM, Greyber E, Buckley NS, Salpeter EE. 2006. Meta-analysis: effect of hormone-replacement therapy on components of the metabolic syndrome in postmenopausal women. Diabetes Obes. Metab. 8:538–54
    [Google Scholar]
  94. 94.
    Sampathkumar NK, Bravo JI, Chen Y, Danthi PS, Donahue EK et al. 2020. Widespread sex dimorphism in aging and age-related diseases. Hum. Genet. 139:333–56
    [Google Scholar]
  95. 95.
    Santos-Marcos JA, Haro C, Vega-Rojas A, Alcala-Diaz JF, Molina-Abril H et al. 2019. Sex differences in the gut microbiota as potential determinants of gender predisposition to disease. Mol. Nutr. Food Res. 63:e1800870
    [Google Scholar]
  96. 96.
    Sato J, Kanazawa A, Ikeda F, Yoshihara T, Goto H et al. 2014. Gut dysbiosis and detection of “live gut bacteria” in blood of Japanese patients with type 2 diabetes. Diabetes Care 37:2343–50
    [Google Scholar]
  97. 97.
    Schele E, Grahnemo L, Anesten F, Hallen A, Backhed F, Jansson JO. 2013. The gut microbiota reduces leptin sensitivity and the expression of the obesity-suppressing neuropeptides proglucagon (Gcg) and brain-derived neurotrophic factor (Bdnf) in the central nervous system. Endocrinology 154:3643–51
    [Google Scholar]
  98. 98.
    Schurz H, Salie M, Tromp G, Hoal EG, Kinnear CJ, Moller M. 2019. The X chromosome and sex-specific effects in infectious disease susceptibility. Hum. Genom. 13:2
    [Google Scholar]
  99. 99.
    Sender R, Fuchs S, Milo R 2016. Are we really vastly outnumbered? Revisiting the ratio of bacterial to host cells in humans. Cell 164:337–40
    [Google Scholar]
  100. 100.
    Seu E, Groman SM, Arnold AP, Jentsch JD. 2014. Sex chromosome complement influences operant responding for a palatable food in mice. Genes Brain Behav 13:527–34
    [Google Scholar]
  101. 101.
    Shi H, Strader AD, Woods SC, Seeley RJ. 2007. Sexually dimorphic responses to fat loss after caloric restriction or surgical lipectomy. Am. J. Physiol. Endocrinol. Metab. 293:E316–26
    [Google Scholar]
  102. 102.
    Smith GI, Atherton P, Villareal DT, Frimel TN, Rankin D et al. 2008. Differences in muscle protein synthesis and anabolic signaling in the postabsorptive state and in response to food in 65–80 year old men and women. PLOS ONE 3:e1875
    [Google Scholar]
  103. 103.
    Steemburgo T, Azevedo MJ, Gross JL, Milagro FI, Campion J, Martinez JA. 2013. The rs9939609 polymorphism in the FTO gene is associated with fat and fiber intakes in patients with type 2 diabetes. J. Nutrigenet. Nutrigenom. 6:97–106
    [Google Scholar]
  104. 104.
    Sullivan EL, Daniels AJ, Koegler FH, Cameron JL. 2005. Evidence in female rhesus monkeys (Macaca mulatta) that nighttime caloric intake is not associated with weight gain. Obes. Res. 13:2072–80
    [Google Scholar]
  105. 105.
    Tipton KD. 2001. Gender differences in protein metabolism. Curr. Opin. Clin. Nutr. Metab. Care 4:493–98
    [Google Scholar]
  106. 106.
    Toth MJ, Poehlman ET, Matthews DE, Tchernof A, MacCoss MJ. 2001. Effects of estradiol and progesterone on body composition, protein synthesis, and lipoprotein lipase in rats. Am. J. Physiol. Endocrinol. Metab. 280:E496–501
    [Google Scholar]
  107. 107.
    Trace SE, Baker JH, Penas-Lledo E, Bulik CM. 2013. The genetics of eating disorders. Annu. Rev. Clin. Psychol. 9:589–620
    [Google Scholar]
  108. 108.
    Uhlenhaut NH, Jakob S, Anlag K, Eisenberger T, Sekido R et al. 2009. Somatic sex reprogramming of adult ovaries to testes by FOXL2 ablation. Cell 139:1130–42
    [Google Scholar]
  109. 109.
    Upadhyay A, Anjum B, Godbole NM, Rajak S, Shukla P et al. 2019. Time-restricted feeding reduces high-fat diet associated placental inflammation and limits adverse effects on fetal organ development. Biochem. Biophys. Res. Commun. 514:415–21
    [Google Scholar]
  110. 110.
    Valle A, Catala-Niell A, Colom B, Garcia-Palmer FJ, Oliver J, Roca P. 2005. Sex-related differences in energy balance in response to caloric restriction. Am. J. Physiol. Endocrinol. Metab. 289:E15–22
    [Google Scholar]
  111. 111.
    van Genugten RE, Utzschneider KM, Tong J, Gerchman F, Zraika S et al. 2006. 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 55:3529–35
    [Google Scholar]
  112. 112.
    Ventura-Clapier R, Dworatzek E, Seeland U, Kararigas G, Arnal JF et al. 2017. Sex in basic research: concepts in the cardiovascular field. Cardiovasc. Res. 113:711–24
    [Google Scholar]
  113. 113.
    Volpi E, Lucidi P, Bolli GB, Santeusanio F, De Feo P. 1998. Gender differences in basal protein kinetics in young adults. J. Clin. Endocrinol. Metab. 83:4363–67
    [Google Scholar]
  114. 114.
    von Schwartzenberg RJ, Bisanz JE, Lyalina S, Spanogiannopoulos P, Ang QY et al. 2021. Caloric restriction disrupts the microbiota and colonization resistance. Nature 595:272–77
    [Google Scholar]
  115. 115.
    Wallis KF, Melnyk SB, Miousse IR. 2020. Sex-specific effects of dietary methionine restriction on the intestinal microbiome. Nutrients 12:781
    [Google Scholar]
  116. 116.
    Waltz M, Saylor KW, Fisher JA, Walker RL. 2021. Biomedical researchers' perceptions of the NIH's sex as a biological variable policy for animal research: results from a U.S. national survey. J. Womens Health 30:1395–1405
    [Google Scholar]
  117. 117.
    Wang JJ, Wang J, Pang XY, Zhao LP, Tian L, Wang XP. 2016. Sex differences in colonization of gut microbiota from a man with short-term vegetarian and inulin-supplemented diet in germ-free mice. Sci. Rep. 6:36137
    [Google Scholar]
  118. 118.
    Wang T, Cai G, Qiu Y, Fei N, Zhang M et al. 2012. Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J 6:320–29
    [Google Scholar]
  119. 119.
    Weger BD, Gobet C, Yeung J, Martin E, Jimenez S et al. 2019. The mouse microbiome is required for sex-specific diurnal rhythms of gene expression and metabolism. Cell Metab 29:362–82.e8
    [Google Scholar]
  120. 120.
    Wilson RA, Stathis CG, Hayes A, Cooke MB. 2020. Intermittent fasting and high-intensity exercise elicit sexual-dimorphic and tissue-specific adaptations in diet-induced obese mice. Nutrients 12:1764
    [Google Scholar]
  121. 121.
    Wirth A, Steinmetz B. 1998. Gender differences in changes in subcutaneous and intra-abdominal fat during weight reduction: an ultrasound study. Obes. Res. 6:393–99
    [Google Scholar]
  122. 122.
    Wu BN, O'Sullivan AJ. 2011. Sex differences in energy metabolism need to be considered with lifestyle modifications in humans. J. Nutr. Metab. 2011:391809
    [Google Scholar]
  123. 123.
    Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG et al. 2012. Human gut microbiome viewed across age and geography. Nature 486:222–27
    [Google Scholar]
  124. 124.
    Yoon K, Kim N. 2021. Roles of sex hormones and gender in the gut microbiota. J. Neurogastroenterol. Motil. 27:314–25
    [Google Scholar]
  125. 125.
    Zhang Z, Hyun JE, Thiesen A, Park H, Hotte N et al. 2020. Sex-specific differences in the gut microbiome in response to dietary fiber supplementation in IL-10-deficient mice. Nutrients 12:2088
    [Google Scholar]
/content/journals/10.1146/annurev-nutr-062220-105852
Loading
/content/journals/10.1146/annurev-nutr-062220-105852
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error