Roles of Sex Hormones and Gender in the Gut Microbiota (original) (raw)

  1. Gill SR, Pop M, Deboy RT, et al. Metagenomic analysis of the human distal gut microbiome. Science 2006;312:1355-1359.
    Pubmed pmc CrossRef
  2. Egert M, de Graaf AA, Smidt H, de Vos WM, Venema K. Beyond diversity: functional microbiomics of the human colon. Trends Microbiol 2006;14:86-91.
    Pubmed CrossRef
  3. Possemiers S, Bolca S, Verstraete W, Heyerick A. The intestinal microbiome: a separate organ inside the body with the metabolic potential to influence the bioactivity of botanicals. Fitoterapia 2011;82:53-66.
    Pubmed CrossRef
  4. Johnson BM, Gaudreau MC, Gudi R, Brown R, Gilkeson G, Vasu C. Gut microbiota differently contributes to intestinal immune phenotype and systemic autoimmune progression in female and male lupus-prone mice. J Autoimmun 2020;108:102420.
    Pubmed pmc CrossRef
  5. Cross TL, Kasahara K, Rey FE. Sexual dimorphism of cardiometabolic dysfunction: gut microbiome in the play? Mol Metab 2018;15:70-81.
    Pubmed pmc CrossRef
  6. Yoon K, Kim N. The effect of microbiota on colon carcinogenesis. J Cancer Prev 2018;23:117-125.
    Pubmed pmc CrossRef
  7. Kim YS, Unno T, Kim BY, Park MS. Sex differences in gut microbiota. World J Mens Health 2020;38:48-60.
    Pubmed pmc CrossRef
  8. Sender R, Fuchs S, Milo R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol 2016;14:e1002533.
    Pubmed pmc CrossRef
  9. Mulak A, Taché Y, Larauche M. Sex hormones in the modulation of irritable bowel syndrome. World J Gastroenterol 2014;20:2433-2448.
    Pubmed pmc CrossRef
  10. Kwa M, Plottel CS, Blaser MJ, Adams S. The intestinal microbiome and estrogen receptor-positive female breast cancer. J Natl Cancer Inst 2016;108:djw029.
    Pubmed pmc CrossRef
  11. Chey WD. The role of food in the functional gastrointestinal disorders: introduction to a manuscript series. Am J Gastroenterol 2013;108:694-697.
    Pubmed CrossRef
  12. Molina PE. Endocrine Physiology. 4th ed. New York, NY, USA: Lange medical Books/McGrow HIll 2013.
  13. Chen KL, Madak-Erdogan Z. Estrogen and microbiota crosstalk: should we pay attention? Trends Endocrinol Metab 2016;27:752-755.
    Pubmed CrossRef
  14. Menon R, Watson SE, Thomas LN, et al. Diet complexity and estrogen receptor β status affect the composition of the murine intestinal microbiota. Appl Environ Microbiol 2013;79:5763-5773.
    Pubmed pmc CrossRef
  15. Paterni I, Bertini S, Granchi C, Macchia M, Minutolo F. Estrogen receptor ligands: a patent review update. Expert Opin Ther Pat 2013;23:1247-1271.
    Pubmed CrossRef
  16. Nie X, Xie R, Tuo B. Effects of estrogen on the gastrointestinal tract. Dig Dis Sci 2018;63:583-596.
    Pubmed CrossRef
  17. Meleine M, Matricon J. Gender-related differences in irritable bowel syndrome: potential mechanisms of sex hormones. World J Gastroenterol 2014;20:6725-6743.
    Pubmed pmc CrossRef
  18. Flores R, Shi J, Fuhrman B, et al. Fecal microbial determinants of fecal and systemic estrogens and estrogen metabolites: a cross-sectional study. J Transl Med 2012;10:253.
    Pubmed pmc CrossRef
  19. Walsh J, Olavarria-Ramirez L, Lach G, et al. Impact of host and environmental factors on β-glucuronidase enzymatic activity: implications for gastrointestinal serotonin. Am J Physiol Gastrointest Liver Physiol 2020;318:G816-G826.
    Pubmed CrossRef
  20. Gomez A, Luckey D, Taneja V. The gut microbiome in autoimmunity: sex matters. Clin Immunol 2015;159:154-162.
    Pubmed pmc CrossRef
  21. Colldén H, Landin A, Wallenius V, et al. The gut microbiota is a major regulator of androgen metabolism in intestinal contents. Am J Physiol Endocrinol Metab 2019;317:E1182-E1192.
    Pubmed pmc CrossRef
  22. Shin JH, Park YH, Sim M, Kim SA, Joung H, Shin DM. Serum level of sex steroid hormone is associated with diversity and profiles of human gut microbiome. Res Microbiol 2019;170:192-201.
    Pubmed CrossRef
  23. Hou X, Zhu L, Zhang X, et al. Testosterone disruptor effect and gut microbiome perturbation in mice: early life exposure to doxycycline. Chemosphere 2019;222:722-731.
    Pubmed CrossRef
  24. Yurkovetskiy L, Burrows M, Khan AA, et al. Gender bias in autoimmunity is influenced by microbiota. Immunity 2013;39:400-412.
    Pubmed pmc CrossRef
  25. Zheng Y, Yu J, Liang C, Li S, Wen X, Li Y. Characterization on gut microbiome of PCOS rats and its further design by shifts in high-fat diet and dihydrotestosterone induction in PCOS rats. Bioprocess Biosyst Eng Published Online First: 10 March 2020. doi: 10.1007/s00449-020-02320-w.
    Pubmed CrossRef
  26. Liu R, Zhang C, Shi Y, et al. Dysbiosis of gut microbiota associated with clinical parameters in polycystic ovary syndrome. Front Microbiol 2017;8:324.
    Pubmed pmc CrossRef
  27. Liang Y, Ming Q, Liang J, Zhang Y, Zhang H, Shen T. Gut microbiota dysbiosis in polycystic ovary syndrome: association with obesity - a preliminary report. Can J Physiol Pharmacol 2020;98:803-809.
    Pubmed CrossRef
  28. Jobira B, Frank DN, Pyle L, et al. Obese adolescents with PCOS have altered biodiversity and relative abundance in gastrointestinal microbiota. J Clin Endocrinol Metab 2020;105:e2134-e2144.
    Pubmed pmc CrossRef
  29. Arroyo P, Ho BS, Sau L, Kelley ST, Thackray VG. Letrozole treatment of pubertal female mice results in activational effects on reproduction, metabolism and the gut microbiome. PLoS One 2019;14:e0223274.
    Pubmed pmc CrossRef
  30. Sherman SB, Sarsour N, Salehi M, et al. Prenatal androgen exposure causes hypertension and gut microbiota dysbiosis. Gut Microbes 2018;9:400-421.
    Pubmed pmc CrossRef
  31. Chu W, Zhai J, Xu J, et al. Continuous light-induced PCOS-like changes in reproduction, metabolism, and gut microbiota in sprague-dawley rats. Front Microbiol 2019;10:3145.
    Pubmed pmc CrossRef
  32. Torres PJ, Siakowska M, Banaszewska B, et al. Gut microbial diversity in women with polycystic ovary syndrome correlates with hyperandrogenism. J Clin Endocrinol Metab 2018;103:1502-1511.
    Pubmed pmc CrossRef
  33. Xue J, Li X, Liu P, et al. Inulin and metformin ameliorate polycystic ovary syndrome via anti-inflammation and modulating gut microbiota in mice. Endocr J 2019;66:859-870.
    Pubmed CrossRef
  34. Org E, Mehrabian M, Parks BW, et al. Sex differences and hormonal effects on gut microbiota composition in mice. Gut Microbes 2016;7:313-322.
    Pubmed pmc CrossRef
  35. Markle JG, Frank DN, Mortin-Toth S, et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 2013;339:1084-1088.
    Pubmed CrossRef
  36. Harada N, Hanada K, Minami Y, et al. Role of gut microbiota in sex- and diet-dependent metabolic disorders that lead to early mortality of androgen receptor-deficient male mice. Am J Physiol Endocrinol Metab 2020;318:E525-E537.
    Pubmed CrossRef
  37. Harada N, Hanaoka R, Hanada K, Izawa T, Inui H, Yamaji R. Hypogonadism alters cecal and fecal microbiota in male mice. Gut Microbes 2016;7:533-539.
    Pubmed pmc CrossRef
  38. Poutahidis T, Springer A, Levkovich T, et al. Probiotic microbes sustain youthful serum testosterone levels and testicular size in aging mice. PLoS One 2014;9:e84877.
    Pubmed pmc CrossRef
  39. Song CH, Kim N, Nam RH, Choi SI, Lee HN, Surh YJ. 17β-estradiol supplementation changes gut microbiota diversity in intact and colorectal cancer-induced ICR male mice. Sci Rep 2020;10:12283.
    Pubmed pmc CrossRef
  40. Jašarević E, Morrison KE, Bale TL. Sex differences in the gut microbiome-brain axis across the lifespan. Philos Trans R Soc Lond B Biol Sci 2016;371:20150122.
    Pubmed pmc CrossRef
  41. Sinha T, Vich Vila A, Garmaeva S, et al. Analysis of 1135 gut metagenomes identifies sex-specific resistome profiles. Gut Microbes 2019;10:358-366.
    Pubmed pmc CrossRef
  42. Santos-Marcos JA, Rangel-Zuñiga OA, Jimenez-Lucena R, et al. Influence of gender and menopausal status on gut microbiota. Maturitas 2018;116:43-53.
    Pubmed CrossRef
  43. Koren O, Goodrich JK, Cullender TC, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 2012;150:470-480.
    Pubmed pmc CrossRef
  44. Cox-York KA, Sheflin AM, Foster MT, et al. Ovariectomy results in differential shifts in gut microbiota in low versus high aerobic capacity rats. Physiol Rep 2015;3:e12488.
    Pubmed pmc CrossRef
  45. Lee SM, Kim N, Park JH, Nam RH, Yoon K, Lee DH. Comparative analysis of ileal and cecal microbiota in aged rats. J Cancer Prev 2018;23:70-76.
    Pubmed pmc CrossRef
  46. Sha S, Xu B, Wang X, et al. The biodiversity and composition of the dominant fecal microbiota in patients with inflammatory bowel disease. Diagn Microbiol Infect Dis 2013;75:245-251.
    Pubmed CrossRef
  47. Halfvarson J, Brislawn CJ, Lamendella R, et al. Dynamics of the human gut microbiome in inflammatory bowel disease. Nat Microbiol 2017;2:17004.
    Pubmed pmc CrossRef
  48. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 2007;104:13780-13785.
    Pubmed pmc CrossRef
  49. Kozik AJ, Nakatsu CH, Chun H, Jones-Hall YL. Age, sex, and TNF associated differences in the gut microbiota of mice and their impact on acute TNBS colitis. Exp Mol Pathol 2017;103:311-319.
    Pubmed CrossRef
  50. Shastri P, McCarville J, Kalmokoff M, Brooks SP, Green-Johnson JM. Sex differences in gut fermentation and immune parameters in rats fed an oligofructose-supplemented diet. Biol Sex Differ 2015;6:13.
    Pubmed pmc CrossRef
  51. Takagi T, Naito Y, Inoue R, et al. Differences in gut microbiota associated with age, sex, and stool consistency in healthy Japanese subjects. J Gastroenterol 2019;54:53-63.
    Pubmed CrossRef
  52. Dewulf EM, Cani PD, Claus SP, et al. Insight into the prebiotic concept: lessons from an exploratory, double blind intervention study with inulin-type fructans in obese women. Gut 2013;62:1112-1121.
    Pubmed pmc CrossRef
  53. Feng J, Tang H, Li M, et al. The abundance of fecal
    Faecalibacterium prausnitzii
    in relation to obesity and gender in Chinese adults. Arch Microbiol 2014;196:73-77.
    Pubmed CrossRef
  54. Aguirre de Cárcer D, Cuív PO, Wang T, et al. Numerical ecology validates a biogeographical distribution and gender-based effect on mucosa-associated bacteria along the human colon. ISME J 2011;5:801-809.
    Pubmed pmc CrossRef
  55. Mueller S, Saunier K, Hanisch C, et al. Differences in fecal microbiota in different European study populations in relation to age, gender, and country: a cross-sectional study. Appl Environ Microbiol 2006;72:1027-1033.
    Pubmed pmc CrossRef
  56. Sheng L, Jena PK, Liu HX, et al. Gender differences in bile acids and microbiota in relationship with gender dissimilarity in steatosis induced by diet and FXR inactivation. Sci Rep 2017;7:1748.
    Pubmed pmc CrossRef
  57. Mu Q, Zhang H, Liao X, et al. Control of lupus nephritis by changes of gut microbiota. Microbiome 2017;5:73.
    Pubmed pmc CrossRef
  58. Lee JY, Kim N, Nam RH, et al. Probiotics reduce repeated water avoidance stress-induced colonic microinflammation in wistar rats in a sex-specific manner. PLoS One 2017;12:e0188992.
    Pubmed pmc CrossRef
  59. Zhang H, Wang Z, Li Y, et al. Sex-based differences in gut microbiota composition in response to tuna oil and algae oil supplementation in a d-galactose-induced aging mouse model. Front Aging Neurosci 2018;10:187.
    Pubmed pmc CrossRef
  60. Karunasena E, McMahon KW, Chang D, Brashears MM. Host responses to the pathogen
    Mycobacterium avium
    subsp.
    paratuberculosis
    and beneficial microbes exhibit host sex specificity. Appl Environ Microbiol 2014;80:4481-4490.
    Pubmed pmc CrossRef
  61. Mahnic A, Rupnik M. Different host factors are associated with patterns in bacterial and fungal gut microbiota in Slovenian healthy cohort. PLoS One 2018;13:e0209209.
    Pubmed pmc CrossRef
  62. Strati F, Di Paola M, Stefanini I, et al. Age and gender affect the composition of fungal population of the human gastrointestinal tract. Front Microbiol 2016;7:1227.
    Pubmed pmc CrossRef
  63. Edogawa S, Peters SA, Jenkins GD, et al. Sex differences in NSAID-induced perturbation of human intestinal barrier function and microbiota. FASEB J 2018;32:6615-6625.
    Pubmed pmc CrossRef
  64. Son HJ, Kim N, Song CH, et al. Sex-related alterations of gut microbiota in the C57BL/6 mouse model of inflammatory bowel disease. J Cancer Prev 2019;24:173-182.
    Pubmed pmc CrossRef
  65. Ober C, Loisel DA, Gilad Y. Sex-specific genetic architecture of human disease. 2008;9:911-922.
    Pubmed pmc CrossRef
  66. Claesson MJ, Cusack S, O'Sullivan O, et al. Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci USA 2011;108(suppl 1):4586-4591.
    Pubmed pmc CrossRef
  67. Rincel M, Aubert P, Chevalier J, et al. Multi-hit early life adversity affects gut microbiota, brain and behavior in a sex-dependent manner. Brain Behav Immun 2019;80:179-192.
    Pubmed CrossRef
  68. Clarke G, Grenham S, Scully P, et al. The microbiome-gut-brain axis during early life regulates the hippocampal serotonergic system in a sex-dependent manner. 2013;18:666-673.
    Pubmed CrossRef
  69. Sisk CL, Foster DL. The neural basis of puberty and adolescence. Nat Neurosci 2004;7:1040-1047.
    Pubmed CrossRef
  70. Biagi E, Nylund L, Candela M, et al. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PLoS One 2010;5:e10667.
    Pubmed pmc CrossRef
  71. Lee SM, Kim N, Yoon H, Nam RH, Lee DH. Microbial changes and host response in F344 rat colon depending on sex and age following a high-fat diet. Front Microbiol 2018;9:2236.
    Pubmed pmc CrossRef
  72. Bischoff SC. Microbiota and aging. Curr Opin Clin Nutr Metab Care 2016;19:26-30.
    Pubmed CrossRef
  73. Salles N. Basic mechanisms of the aging gastrointestinal tract. Dig Dis 2007;25:112-117.
    Pubmed CrossRef
  74. Enck P, Zimmermann K, Rusch K, Schwiertz A, Klosterhalfen S, Frick JS. The effects of ageing on the colonic bacterial microflora in adults. Z Gastroenterol 2009;47:653-658.
    Pubmed CrossRef
  75. De Filippo C, Cavalieri D, Di Paola M, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 2010;107:14691-14696.
    Pubmed pmc CrossRef
  76. Lee HS, Cho YH, Park J, Shin HR, Sung MK. Dietary intake of phytonutrients in relation to fruit and vegetable consumption in Korea. J Acad Nutr Diet 2013;113:1194-1199.
    Pubmed CrossRef
  77. Regu GM, Kim H, Kim YJ, et al. Association between dietary carotenoid intake and bone mineral density in Korean adults aged 30-75 years using data from the fourth and fifth korean national health and nutrition examination surveys (2008-2011). Nutrients 2017;9:1025.
    Pubmed pmc CrossRef
  78. Barrasa JI, Olmo N, Lizarbe MA, Turnay J. Bile acids in the colon, from healthy to cytotoxic molecules. Toxicol In Vitro 2013;27:964-977.
    Pubmed CrossRef
  79. Rowland RHIR. Metabolic activities of the gut microflora in relation to cancer. Microb Ecol Health Dis 2000;12:179-185.
    CrossRef
  80. Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 2014;12:661-672.
    Pubmed CrossRef
  81. Bolnick DI, Snowberg LK, Hirsch PE, et al. Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat Commun 2014;5:4500.
    Pubmed pmc CrossRef
  82. Lee JR, Muckerman JE, Wright AM, et al. Sex determines effect of physical activity on diet preference: association of striatal opioids and gut microbiota composition. Behav Brain Res 2017;334:16-25.
    Pubmed pmc CrossRef
  83. Lee SM, Kim N, Yoon H, et al. Compositional and functional changes in the gut microbiota in irritable bowel syndrome patients. Gut Liver Published Online First: 28 March 2020. doi: 10.5009/gnl19379.
    Pubmed pmc CrossRef
  84. Kim YS, Kim N. Sex-gender differences in irritable bowel syndrome. J Neurogastroenterol Motil 2018;24:544-558.
    Pubmed pmc CrossRef
  85. Ait-Belgnaoui A, Payard I, Rolland C, et al.
    Bifidobacterium longum
    and
    Lactobacillus helveticus
    synergistically suppress stress-related visceral hypersensitivity through hypothalamic-pituitary-adrenal axis modulation. J Neurogastroenterol Motil 2018;24:138-146.
    Pubmed pmc CrossRef
  86. Distrutti E, Monaldi L, Ricci P, Fiorucci S. Gut microbiota role in irritable bowel syndrome: new therapeutic strategies. World J Gastroenterol 2016;22:2219-2241.
    Pubmed pmc CrossRef
  87. Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature 2012;489:242-249.
    Pubmed CrossRef
  88. Rivière A, Selak M, Lantin D, Leroy F, De Vuyst L. Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol 2016;7:979.
    Pubmed pmc CrossRef
  89. Encarnação JC, Abrantes AM, Pires A, Botelho MF. Revisit dietary fiber on colorectal cancer: butyrate and its role on prevention and treatment. Cancer Metastasis Rev 2015;34:465-478.
    Pubmed CrossRef
  90. Vemuri R, Sylvia KE, Klein SL, et al. The microgenderome revealed: sex differences in bidirectional interactions between the microbiota, hormones, immunity and disease susceptibility. Semin Immunopathol 2019;41:265-275.
    Pubmed pmc CrossRef
  91. Ou J, Carbonero F, Zoetendal EG, et al. Diet, microbiota, and microbial metabolites in colon cancer risk in rural Africans and African Americans. Am J Clin Nutr 2013;98:111-120.
    Pubmed pmc CrossRef
  92. Lee JY, Kim N, Choi YJ, et al. Expression of tight junction proteins according to functional dyspepsia subtype and sex. J Neurogastroenterol Motil 2020;26:248-258.
    Pubmed pmc CrossRef
  93. Ferrario C, Taverniti V, Milani C, et al. Modulation of fecal clostridiales bacteria and butyrate by probiotic intervention with
    Lactobacillus paracasei
    DG varies among healthy adults. J Nutr 2014;144:1787-1796.
    Pubmed CrossRef