Generic placeholder image

Current Diabetes Reviews


ISSN (Print): 1573-3998
ISSN (Online): 1875-6417

Review Article

Unravelling the Crosstalk between Estrogen Deficiency and Gut-biota Dysbiosis in the Development of Diabetes Mellitus

Author(s): Rishabh, Seema Bansal*, Akriti Goel, Sumeet Gupta, Deepti Malik and Nitin Bansal*

Volume 20, Issue 10, 2024

Published on: 24 January, 2024

Article ID: e240124226067 Pages: 11

DOI: 10.2174/0115733998275953231129094057

Price: $65


Estrogens are classically considered essential hormonal signals, but they exert profound effects in a number of physiological and pathological states, including glucose homeostasis and insulin resistance. Estrogen deficiency after menopause in most women leads to increased androgenicity and changes in body composition, and it is recommended to manipulate the β-cell function of the pancreas, insulin-induced glucose transport, and hepatic glucose output, hence, the increasing incidence of type 2 diabetes mellitus. Recently, studies have reported that gut biota alteration due to estrogen deficiency contributes to altered energy metabolism and, hence, accentuates the pathology of diabetes mellitus. Emerging research suggests estrogen deficiency via genetic disposition or failure of ovaries to function in old age modulates the insulin resistance and glucose secretion workload on pancreatic beta cells by decreasing the levels of good bacteria such as Akkermansia muciniphila, Bifidobacterium spp., Lactobacillus spp., Faecalibacterium prausnitzii, Roseburia spp., and Prevotella spp., and increasing the levels of bad bacteria’s such as Bacteroides spp., Clostridium difficile, Escherichia coli, and Enterococcus spp. Alteration in these bacteria's concentrations in the gut further leads to the development of impaired glucose uptake by the muscles, increased gluconeogenesis in the liver, and increased lipolysis and inflammation in the adipose tissues. Thus, the present review paper aims to clarify the intricate interactions between estrogen deficiency, gut microbiota regulation, and the development of diabetes mellitus.

Keywords: Estrogen, menopause, gut-biota dysbiosis, diabetes mellitus, human physiology, pancreas.

Muthiah M, Ng CH, Chan KE, et al. Type 2 diabetes mellitus in metabolic-associated fatty liver disease vs. type 2 diabetes mellitus non-alcoholic fatty liver disease: A longitudinal cohort analysis. Ann Hepatol 2023; 28(1): 100762.
[] [PMID: 36182031]
García-Llorca A, Kararigas G. Sex-related effects of gut microbiota in metabolic syndrome-related diabetic retinopathy. Microorganisms 2023; 11(2): 447.
[] [PMID: 36838411]
Chen KL, Madak-Erdogan Z. Estrogen and microbiota crosstalk: Should we pay attention? Trends Endocrinol Metab 2016; 27(11): 752-5.
[] [PMID: 27553057]
Kan B, Hou J, Leslie WD, Jiang D, Zhang J, Yang S. Associations of estrogen therapy and non-estrogen anti-resorptive therapy with diabetes mellitus risk: A classical and Bayesian meta-analysis. Bone 2023; 171: 116738.
[] [PMID: 36933854]
Acharya KD, Graham M, Raman H, et al. Estradiol-mediated protection against high-fat diet induced anxiety and obesity is associated with changes in the gut microbiota in female mice. Sci Rep 2023; 13(1): 4776.
[] [PMID: 36959275]
Baker JM, Al-Nakkash L, Herbst-Kralovetz MM. Estrogen–gut microbiome axis: Physiological and clinical implications. Maturitas 2017; 103: 45-53.
[] [PMID: 28778332]
Santos-Marcos JA, Mora-Ortiz M, Tena-Sempere M, Lopez-Miranda J, Camargo A. Interaction between gut microbiota and sex hormones and their relation to sexual dimorphism in metabolic diseases. Biol Sex Differ 2023; 14(1): 4.
[] [PMID: 36750874]
Kang DH, Kim MJ, Mohamed EA, et al. Regulation of uterus and placenta remodeling under high estradiol levels in gestational diabetes mellitus models. Biol Reprod 2023; 109(2): 215-26.
[] [PMID: 37255320]
Inada A, Yasunami Y, Yoshiki A, Nabeshima Y, Inada O. Greb1 transiently accelerates pancreatic β-cell proliferation in diabetic mice exposed to estradiol. Am J Pathol 2023; 193(8): 1081-100.
[] [PMID: 37516458]
Zhang X, Yan Y, Zhang F, et al. Analysis of the effect of hyaluronic acid on intestinal flora and its metabolites in diabetic mice via high-throughput sequencing and nontargeted metabolomics. J Funct Foods 2023; 103: 105496.
Park S, Sim KS, Heo W, Kim JH. Protective effects of coumestrol on metabolic dysfunction and its estrogen receptor-mediated action in ovariectomized mice. Nutrients 2023; 15(4): 954.
[] [PMID: 36839308]
Wu X, Kim MJ, Yang HJ, Park S. Chitosan alleviated menopausal symptoms and modulated the gut microbiota in estrogen-deficient rats. Eur J Nutr 2021; 60(4): 1907-19.
[] [PMID: 32910260]
Hases L, Stepanauskaite L, Birgersson M, et al. High-fat diet and estrogen modulate the gut microbiota in a sex-dependent manner in mice. Commun Biol 2023; 6(1): 20.
[] [PMID: 36624306]
Acharya KD, Gao X, Bless EP, Chen J, Tetel MJ. Estradiol and high fat diet associate with changes in gut microbiota in female ob/ob mice. Sci Rep 2019; 9(1): 20192.
[] [PMID: 31882890]
Tao Z, Cheng Z. Hormonal regulation of metabolism—recent lessons learned from insulin and estrogen. Clin Sci 2023; 137(6): 415-34.
[] [PMID: 36942499]
Guo M, Cao X, Ji D, et al. Gut microbiota and acylcarnitine metabolites connect the beneficial association between estrogen and lipid metabolism disorders in ovariectomized mice. Microbiol Spectr 2023; 11(3): e00149-23.
[] [PMID: 37140372]
Fabre A, Tramunt B, Montagner A, et al. Membrane estrogen receptor-α contributes to female protection against high-fat diet-induced metabolic disorders. Front Endocrinol 2023; 14: 1215947.
[] [PMID: 37529599]
Kaliannan K, Robertson RC, Murphy K, et al. Estrogen-mediated gut microbiome alterations influence sexual dimorphism in metabolic syndrome in mice. Microbiome 2018; 6(1): 205.
[] [PMID: 30424806]
Chen KL, Madak-Erdogan Z. Estrogens and female liver health. Steroids 2018; 133: 38-43.
[] [PMID: 29100781]
Leonard LM, Choi MS, Cross TWL. Maximizing the estrogenic potential of soy isoflavones through the gut microbiome: Implication for cardiometabolic health in postmenopausal women. Nutrients 2022; 14(3): 553.
[] [PMID: 35276910]
Ahmed F, Kamble PG, Hetty S, et al. Role of estrogen and its receptors in adipose tissue glucose metabolism in pre-and postmenopausal women. J Clin Endocrinol Metab 2022; 107(5): e1879-89.
[] [PMID: 35084504]
Bansal S, Chopra K. Distinct role of estrogen receptor-alpha and beta on postmenopausal diabetes-induced vascular dysfunction. Gen Comp Endocrinol 2014; 206: 51-9.
[] [PMID: 24967951]
Park S, Kim DS, Kang ES, Kim DB, Kang S. Low-dose brain estrogen prevents menopausal syndrome while maintaining the diversity of the gut microbiomes in estrogen-deficient rats. Am J Physiol Endocrinol Metab 2018; 315(1): E99-E109.
[] [PMID: 29558207]
Unger CA, Aladhami AK, Hope MC III, et al. Skeletal muscle endogenous estrogen production ameliorates the metabolic consequences of a high-fat diet in male mice. Endocrinology 2023; 164(8): bqad105.
[] [PMID: 37421340]
Bansal S, Chopra K. Differential role of estrogen receptor modulators in depression-like behavior and memory impairment in rats with postmenopausal diabetes. Menopause 2015; 22(10): 1117-24.
[] [PMID: 25756691]
Kaur SP, Bansal S, Chopra K. 17α-Estradiol: A candidate neuroserm and non-feminizing estrogen for postmenopausal neuronal complications. Steroids 2015; 96: 7-15.
[] [PMID: 25595449]
Mkhize BC, Mosili P, Ngubane PS, Sibiya NH, Khathi A. The relationship between Renin–Angiotensin–Aldosterone System (RAAS) activity, osteoporosis and estrogen deficiency in type 2 diabetes. Int J Mol Sci 2023; 24(15): 11963.
[] [PMID: 37569338]
Riant E, Waget A, Cogo H, Arnal JF, Burcelin R, Gourdy P. Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice. Endocrinology 2009; 150(5): 2109-17.
[] [PMID: 19164473]
Bansal S, Chopra K. Selective ER-α agonist alleviates vascular endothelial dysfunction in ovariectomized type 2 diabetic rats. Mol Cell Endocrinol 2018; 460: 152-61.
[] [PMID: 28736253]
Qi X, Yun C, Pang Y, Qiao J. The impact of the gut microbiota on the reproductive and metabolic endocrine system. Gut Microbes 2021; 13(1): 1894070.
[] [PMID: 33722164]
Isola JVV, Ko S, Ocañas SR, Stout MB. Role of estrogen receptor α in aging and chronic disease. Adv Geriatr 2023; 5(2): e230005.
[PMID: 37425648]
Lye HS, Kuan CY, Ewe JA, Fung WY, Liong MT. The improvement of hypertension by probiotics: Effects on cholesterol, diabetes, renin, and phytoestrogens. Int J Mol Sci 2009; 10(9): 3755-75.
[] [PMID: 19865517]
Peng C, Xu X, Li Y, et al. Sex-specific association between the gut microbiome and high-fat diet-induced metabolic disorders in mice. Biol Sex Differ 2020; 11(1): 5.
[] [PMID: 31959230]
Bansal S, Mahendiratta S, Agrawal M, et al. Role of protein tyrosine phosphatase 1B inhibitor in central insulin resistance and associated cognitive deficits. Brain Res Bull 2021; 171: 113-25.
[] [PMID: 33684458]
Bansal S, Chopra K. P2-120: Selective ER-B activation mitigates cognitive impairment in type 2 diabetic ovariectomized rats. Alzheimers Dement 2016; 12(7S_Part_13): 658-P658.
Singh V, Park YJ, Lee G, Unno T, Shin JH. Dietary regulations for microbiota dysbiosis among post-menopausal women with type 2 diabetes. Crit Rev Food Sci Nutr 2022; 1-16.
[] [PMID: 35635755]
Ma B, Zhang K, Guo M, et al. Gut microbiota and acylcarnitine connect the beneficial association between estrogen and lipid metabolism disorders in ovariectomized mice. Res Square 2022; 2022: 2286266.
Chaudhary R, Gupta S, Chauhan S. Protein uncoupling as an innovative practice in diabetes mellitus treatment: A metabolic disorder. Endocr Metab Immune Disord Drug Targets 2023; 23(4): 494-502.
Zengul AG, Demark-Wahnefried W, Barnes S, et al. Associations between dietary fiber, the fecal microbiota and estrogen metabolism in postmenopausal women with breast cancer. Nutr Cancer 2021; 73(7): 1108-17.
[] [PMID: 32590914]
Cross TWL, Kasahara K, Rey FE. Sexual dimorphism of cardiometabolic dysfunction: Gut microbiome in the play? Mol Metab 2018; 15: 70-81.
[] [PMID: 29887245]
Chaudhary R. The role of medicinal plants in the diabetic wound healing process. Curr Diabetes Rev 2023; 19(4): e240222201410.
[] [PMID: 35209827]
Torres Irizarry VC, Jiang Y, He Y, Xu P. Hypothalamic estrogen signaling and adipose tissue metabolism in energy homeostasis. Front Endocrinol 2022; 13: 898139.
[] [PMID: 35757435]
Chen J, Xu J, Sun Y, et al. Gut microbiota dysbiosis ameliorates in LNK-deficient mouse models with obesity-induced insulin resistance improvement. J Clin Med 2023; 12(5): 1767.
[] [PMID: 36902554]
Carter S, McKenzie S, Mourtzakis M, Mahoney DJ, Tarnopolsky MA. Short-term 17β-estradiol decreases glucose R a but not whole body metabolism during endurance exercise. J Appl Physiol 2001; 90(1): 139-46.
[] [PMID: 11133904]
Clegg DJ, Mauvais-Jarvis F. An integrated view of sex differences in metabolic physiology and disease. Mol Metab 2018; 15: 1-2.
[] [PMID: 30032908]
Yang R, Jia Q, Mehmood S, Ma S, Liu X. Genistein ameliorates inflammation and insulin resistance through mediation of gut microbiota composition in type 2 diabetic mice. Eur J Nutr 2021; 60(4): 2155-68.
[] [PMID: 33068158]
Pal SC, Eslam M, Mendez-Sanchez N. Detangling the interrelations between MAFLD, insulin resistance, and key hormones. Hormones 2022; 21(4): 573-89.
[] [PMID: 35921046]
Park S, Zhang T, Yue Y, et al. Alleviation of metabolic disturbance by substituting kanjang high in bacillus for salt through modulation of gut microbiota in estrogen-deficient rats. Foods 2022; 11(13): 1951.
[] [PMID: 35804768]
Vieira AT, Castelo PM, Ribeiro DA, Ferreira CM. Influence of oral and gut microbiota in the health of menopausal women. Front Microbiol 2017; 8: 1884.
[] [PMID: 29033921]
Mahboobifard F, Pourgholami MH, Jorjani M, et al. Estrogen as a key regulator of energy homeostasis and metabolic health. Biomed Pharmacother 2022; 156: 113808.
[] [PMID: 36252357]
Sun Q, Wedick NM, Pan A, et al. Gut microbiota metabolites of dietary lignans and risk of type 2 diabetes: A prospective investigation in two cohorts of U.S. women. Diabetes Care 2014; 37(5): 1287-95.
[] [PMID: 24550220]
Nadal A, Alonso-Magdalena P, Soriano S, Quesada I, Ropero AB. The pancreatic β-cell as a target of estrogens and xenoestrogens: Implications for blood glucose homeostasis and diabetes. Mol Cell Endocrinol 2009; 304(1-2): 63-8.
[] [PMID: 19433249]
Acharya KD, Friedline RH, Ward DV, et al. Differential effects of Akkermansia-enriched fecal microbiota transplant on energy balance in female mice on high-fat diet. Front Endocrinol 2022; 13: 1010806.
[] [PMID: 36387852]
Liebmann M, Asuaje Pfeifer M, Grupe K, Scherneck S. Estradiol (E2) improves glucose-stimulated insulin secretion and stabilizes GDM progression in a prediabetic mouse model. Int J Mol Sci 2022; 23(12): 6693.
[] [PMID: 35743136]
Muñoz-Garach A, Diaz-Perdigones C, Tinahones FJ. Microbiota y diabetes mellitus tipo 2. Endocrinol Nutr 2016; 63(10): 560-8.
[] [PMID: 27633134]
Barros RPA, Machado UF, Warner M, Gustafsson JÅ. Muscle GLUT4 regulation by estrogen receptors ERβ and ERα. Proc Natl Acad Sci 2006; 103(5): 1605-8.
[] [PMID: 16423895]
Yang HJ, Zhang T, Wu XG, et al. Aqueous blackcurrant extract improves insulin sensitivity and secretion and modulates the gut microbiome in non-obese type 2 diabetic rats. Antioxidants 2021; 10(5): 756.
[] [PMID: 34068659]
Mazidi M, Rezaie P, Kengne AP, Mobarhan MG, Ferns GA. Gut microbiome and metabolic syndrome. Diabetes Metab Syndr 2016; 10(2): S150-7.
[] [PMID: 26916014]
Eaton SA, Sethi JK. Immunometabolic links between estrogen, adipose tissue and female reproductive metabolism. Biology 2019; 8(1): 8.
[] [PMID: 30736459]
Dockman RL, Carpenter JM, Diaz AN, Benbow RA, Filipov NM. Sex differences in behavior, response to LPS, and glucose homeostasis in middle-aged mice. Behav Brain Res 2022; 418: 113628.
[] [PMID: 34687827]
Kumar P. Protective potential of 17-β-estradiol on oxidative stress and renal metabolism in aged female rats. Nephrol Dialy Transplant 2023; 38(S1): 6773.
Bjune JI, Strømland PP, Jersin RÅ, Mellgren G, Dankel SN. Metabolic and epigenetic regulation by estrogen in adipocytes. Front Endocrinol 2022; 13: 828780.
[] [PMID: 35273571]
Chen Q, Mei C, Guo M, et al. Lactobacillus plantarum CCFM1180 attenuates obesity induced by oestrogen deficiency by activating oestrogen receptor alpha in abdominal adipose tissue and regulating gut microbiota-derived metabolites. Food Sci Hum Wellness 2023.
Zhao L, Fang J, Tang S, et al. PM 2.5 and serum metabolome and insulin resistance, potential mediation by the gut microbiome: A population-based panel study of older adults in China. Environ Health Perspect 2022; 130(2): 027007.
[] [PMID: 35157499]
Dos Santos RS, Medina-Gali RM, Babiloni-Chust I, Marroqui L, Nadal A. In vitro assays to identify metabolism-disrupting chemicals with diabetogenic activity in a human pancreatic β-cell model. Int J Mol Sci 2022; 23(9): 5040.
[] [PMID: 35563431]
Ryuk JA, Kang S, Daily JW, Ko BS, Park S. Moderate intake of aspartame and sucralose with meals, but not fructose, does not exacerbate energy and glucose metabolism in estrogen-deficient rats. J Clin Biochem Nutr 2019; 65(3): 223-31.
[] [PMID: 31777424]
Guevara-Cruz M, Godinez-Salas ET, Sanchez-Tapia M, et al. Genistein stimulates insulin sensitivity through gut microbiota reshaping and skeletal muscle AMPK activation in obese subjects. BMJ Open Diabetes Res Care 2020; 8(1): e000948.
[] [PMID: 32152146]
Sau L, Olmstead CM, Cui LJ, et al. Alterations in gut microbiota do not play a causal role in diet-independent weight gain caused by ovariectomy. J Endocr Soc 2021; 51: 173.
Miranda CL, Johnson LA, de Montgolfier O, et al. Non-estrogenic xanthohumol derivatives mitigate insulin resistance and cognitive impairment in high-fat diet-induced obese mice. Sci Rep 2018; 8(1): 613.
[] [PMID: 29330372]
De Paoli M, Wood DW, Bohn MK, et al. Investigating the protective effects of estrogen on β-cell health and the progression of hyperglycemia-induced atherosclerosis. Am J Physiol Endocrinol Metab 2022; 323(3): E254-66.
[] [PMID: 35830687]
Wang HL, Wang L, Zhao CY, Lan HY. Role of TGF-beta signaling in beta cell proliferation and function in diabetes. Biomolecules 2022; 12(3): 373.
[] [PMID: 35327565]
Saavedra-Peña RM, Taylor N, Flannery C, Rodeheffer MS. Estradiol cycling drives female obesogenic adipocyte hyperplasia. Cell Rep 2023; 42(4): 112390.
[] [PMID: 37053070]
Qin W, Ren X, Zhao L, Guo L. Exposure to perfluorooctane sulfonate reduced cell viability and insulin release capacity of β cells. J Environ Sci 2022; 115: 162-72.
[] [PMID: 34969446]
Park S, Yuan H, Zhang T, Wu X, Huang SK, Cho SM. Long-term silk peptide intake promotes skeletal muscle mass, reduces inflammation, and modulates gut microbiota in middle-aged female rats. Biomed Pharmacother 2021; 137: 111415.
[] [PMID: 33761619]
Zhu L, Martinez MN, Emfinger CH, Palmisano BT, Stafford JM. Estrogen signaling prevents diet-induced hepatic insulin resistance in male mice with obesity. Am J Physiol Endocrinol Metab 2014; 306(10): E1188-97.
[] [PMID: 24691030]
Chen J, Chen Z, Khan BA, Hou K. Editorial: Role of gut microbiota in diabetes mellitus and tumor immunity. Front Immunol 2023; 14: 1185080.
[] [PMID: 37090694]
Song Z, Yan A, Guo Z, et al. Targeting metabolic pathways: A novel therapeutic direction for type 2 diabetes. Front Cell Infect Microbiol 2023; 13: 1218326.
[] [PMID: 37600949]
Brettle H, Tran V, Drummond GR, et al. Sex hormones, intestinal inflammation, and the gut microbiome: Major influencers of the sexual dimorphisms in obesity. Front Immunol 2022; 13: 971048.
[] [PMID: 36248832]
Bajinka O, Tan Y, Darboe A, Ighaede-Edwards IG, Abdelhalim KA. The gut microbiota pathway mechanisms of diabetes. AMB Express 2023; 13(1): 16.
[] [PMID: 36754883]
Addanki S. Roles of nutrition, obesity, and estrogens in diabetes mellitus: Human leads to an experimental approach to prevention. Prev Med 1981; 10(5): 577-89.
[] [PMID: 7029515]
Ionescu RF, Enache RM, Cretoiu SM, Gaspar BS. Gut microbiome changes in gestational diabetes. Int J Mol Sci 2022; 23(21): 12839.
[] [PMID: 36361626]
Longo S, Rizza S, Federici M. Microbiota-gut-brain axis: Relationships among the vagus nerve, gut microbiota, obesity, and diabetes. Acta Diabetol 2023; 60(8): 1007-17.
[] [PMID: 37058160]
Huang W, Lin Z, Sun A, et al. The role of gut microbiota in diabetic peripheral neuropathy rats with cognitive dysfunction. Front Microbiol 2023; 14: 1156591.
[] [PMID: 37266023]
Chen L, Liu B, Ren L, et al. High-fiber diet ameliorates gut microbiota, serum metabolism and emotional mood in type 2 diabetes patients. Front Cell Infect Microbiol 2023; 13: 1069954.
[] [PMID: 36794003]
Bai Z, Huang X, Wu G, et al. Polysaccharides from red kidney bean alleviating hyperglycemia and hyperlipidemia in type 2 diabetic rats via gut microbiota and lipid metabolic modulation. Food Chem 2023; 404(Pt A): 134598.
[] [PMID: 36444040]
Gu Y, Chen H, Li X, et al. Lactobacillus paracasei IMC 502 ameliorates type 2 diabetes by mediating gut microbiota– SCFA –hormone/inflammation pathway in mice. J Sci Food Agric 2023; 103(6): 2949-59.
[] [PMID: 36221226]
Fang H, e-Lacerda RR, Schertzer JD. Obesity promotes a leaky gut, inflammation and pre-diabetes by lowering gut microbiota that metabolise ethanolamine. Gut 2023; 72(10): 1809-11.
[] [PMID: 37105722]
Sowmiya T, Silambanan S. Association of gut microbiota and diabetes mellitus. Curr Diabetes Rev 2023; 19(7): 15-8.
Balint L, Socaciu C, Socaciu AI, et al. Quantitative, targeted analysis of gut microbiota derived metabolites provides novel biomarkers of early diabetic kidney disease in type 2 diabetes mellitus patients. Biomolecules 2023; 13(7): 1086.
[] [PMID: 37509122]
Mauvais-Jarvis F. Menopause, estrogens, and glucose homeostasis in women. Adv Exp Med Biol 2017; 217-25.
Mishra SP, Wang B, Jain S, et al. A mechanism by which gut microbiota elevates permeability and inflammation in obese/diabetic mice and human gut. Gut 2023; 72(10): 1848-65.
[] [PMID: 36948576]
Gannon OJ, Naik JS, Riccio D, et al. Menopause causes metabolic and cognitive impairments in a chronic cerebral hypoperfusion model of vascular contributions to cognitive impairment and dementia. Biol Sex Differ 2023; 14(1): 34.
[] [PMID: 37221553]
Greenhill C. Gut microbiota influences effectiveness of anti-diabetic drug. Nat Rev Endocrinol 2023; 19(7): 379.
[] [PMID: 37221401]
Leppänen J, Nuotio P, Randell K, et al. High estradiol levels during a long agonist IVF protocol are associated with decreased food intake, higher leptin concentrations, and lower levels of high-sensitivity C-reactive protein. Arch Gynecol Obstet 2023; 308(3): 883-91.
[] [PMID: 36797524]
Chleilat F, Schick A, Deleemans JM, et al. Paternal high protein diet modulates body composition, insulin sensitivity, epigenetics, and gut microbiota intergenerationally in rats. FASEB J 2021; 35(9): e21847.
[] [PMID: 34405464]
Huang F, Zhao R, Xia M, Shen GX. Impact of cyanidin-3-glucoside on gut microbiota and relationship with metabolism and inflammation in high fat-high sucrose diet-induced insulin resistant mice. Microorganisms 2020; 8(8): 1238.
[] [PMID: 32824001]
Li ZH, Jiang YY, Long CY, Peng Q, Yue RS. The gut microbiota‐astrocyte axis: Implications for type 2 diabetic cognitive dysfunction. CNS Neurosci Ther 2023; 29(S1): 59-73.
[] [PMID: 36601656]
Blasco-Baque V, Serino M, Vergnes JN, et al. High-fat diet induces periodontitis in mice through lipopolysaccharides (LPS) receptor signaling: Protective action of estrogens. PLoS One 2012; 7(11): e48220.
[] [PMID: 23133617]
Adegoke EO, Rahman MS, Amjad S, et al. Environmentally relevant doses of endocrine disrupting chemicals affect male fertility by interfering with sertoli cell glucose metabolism in mice. Chemosphere 2023; 337: 139277.
[] [PMID: 37364641]
Mao ZH, Gao ZX, Liu DW, Liu ZS, Wu P. Gut microbiota and its metabolites – molecular mechanisms and management strategies in diabetic kidney disease. Front Immunol 2023; 14: 1124704.
[] [PMID: 36742307]
Bryzgalova G, Lundholm L, Portwood N, et al. Mechanisms of antidiabetogenic and body weight-lowering effects of estrogen in high-fat diet-fed mice. Am J Physiol Endocrinol Metab 2008; 295(4): E904-12.
[] [PMID: 18697913]
Romani AMP. The controversy on the beneficial effect of phytoestrogens in diabetic treatment in postmenopausal women. Biochem Pharmacol 2021; 190: 114619.
[] [PMID: 34051210]
Ruan Q, Chen Y, Wen J, et al. Regulatory mechanisms of the edible alga Ulva lactuca polysaccharide via modulation of gut microbiota in diabetic mice. Food Chem 2023; 409: 135287.
[] [PMID: 36603475]
Safari-Alighiarloo N, Emami Z, Rezaei-Tavirani M, Alaei-Shahmiri F, Razavi S. Gut microbiota and their associated metabolites in diabetes: A cross talk between host and microbes-a review. Metab Syndr Relat Disord 2023; 21(1): 3-15.
[] [PMID: 36301254]
Chen C, Lei H, Zhao Y, et al. A novel small molecule effectively ameliorates estrogen deficiency-induced osteoporosis by targeting the gut-bone signaling axis. Eur J Pharmacol 2023; 954: 175868.
[] [PMID: 37369296]
Liu Y, Zhou Y, Mao T, et al. The relationship between menopausal syndrome and gut microbes. BMC Womens Health 2022; 22(1): 437.
[] [PMID: 36348390]
Zhao H, Chen J, Li X, Sun Q, Qin P, Wang Q. Compositional and functional features of the female premenopausal and postmenopausal gut microbiota. FEBS Lett 2019; 593(18): 2655-64.
[] [PMID: 31273779]
Xiao HH, Yu X, Yang C, et al. Prenylated isoflavonoids-rich extract of erythrinae cortex exerted bone protective effects by modulating gut microbial compositions and metabolites in ovariectomized rats. Nutrients 2021; 13(9): 2943.
[] [PMID: 34578822]
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(4-5): 192-201.
[] [PMID: 30940469]
Zeibich L, Koebele SV, Bernaud VE, et al. Surgical menopause and estrogen therapy modulate the gut microbiota, obesity markers, and spatial memory in rats. Front Cell Infect Microbiol 2021; 11: 702628.
[] [PMID: 34660336]
Chadchan SB, Singh V, Kommagani R. Female reproductive dysfunctions and the gut microbiota. J Mol Endocrinol 2022; 69(3): R81-94.
[] [PMID: 35900833]
Zhang T, Yue Y, Jeong SJ, et al. Improvement of estrogen deficiency symptoms by the intake of long-term fermented soybeans (Doenjang) rich in bacillus species through modulating gut microbiota in estrogen-deficient rats. Foods 2023; 12(6): 1143.
[] [PMID: 36981070]
Elkafas H, Walls M, Al-Hendy A, Ismail N. Gut and genital tract microbiomes: Dysbiosis and link to gynecological disorders. Front Cell Infect Microbiol 2022; 12: 1059825.
[] [PMID: 36590579]
Qu Y, Wu Y, Cheng W, et al. Amelioration of cognitive impairment using epigallocatechin-3-gallate in ovariectomized mice fed a high-fat diet involves remodeling with Prevotella and Bifidobacteriales. Front Pharmacol 2023; 13: 1079313.
[] [PMID: 36686657]
Kim CH. Complex regulatory effects of gut microbial short-chain fatty acids on immune tolerance and autoimmunity. Cell Mol Immunol 2023; 20(4): 341-50.
[] [PMID: 36854801]
Wu J, Yang K, Fan H, Wei M, Xiong Q. Targeting the gut microbiota and its metabolites for type 2 diabetes mellitus. Front Endocrinol 2023; 14: 1114424.
[] [PMID: 37229456]
Piccioni A, Rosa F, Mannucci S, et al. Gut microbiota, LADA, and type 1 diabetes mellitus: An evolving relationship. Biomedicines 2023; 11(3): 707.
[] [PMID: 36979685]
Lyu Z, Hu Y, Guo Y, Liu D. Modulation of bone remodeling by the gut microbiota: A new therapy for osteoporosis. Bone Res 2023; 11(1): 31.
[] [PMID: 37296111]
Alsharairi NA. Exploring the diet-gut microbiota-epigenetics crosstalk relevant to neonatal diabetes. Genes 2023; 14(5): 1017.
[] [PMID: 37239377]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy