The Impact of Intestinal Microbiota Imbalance on the Polycystic Ovary Syndrome

doi:10.12280/gjfckx.20221082

Abstract

Abstract:

Intestinal microbiota is considered as an endocrine organ of the human body. Intestinal microorganisms and their metabolites can participate in human metabolism, immunity, reproduction and other aspects by affecting distant organs and related biological pathways. Intestinal microbiota imbalance plays an important role in the occurrence and development of diseases. Polycystic ovary syndrome (PCOS) has complex pathophysiological processes such as hyperandrogenism, hypothalamic-pituitary-ovarian axis disorders and insulin resistance. Related studies have shown that the intestinal microbiota of PCOS patients and PCOS rodent model is altered, and intestinal microbiota imbalance can lead to disturbances in sex hormone synthesis and insulin secretion and abnormal follicle development by mediating glucocorticoid metabolism, bile acid metabolism and chronic inflammation, suggesting that intestinal microbiota imbalance may play a corresponding role in the development and pathology of PCOS. This review highlights the role of intestinal microbiota imbalance in the pathogenesis of PCOS.

Key words: Gastrointestinal microbiome, Polycystic ovary syndrome, Insulin resistance, Obesity, Hyperandrogenism

WANG Lei, ZHANG Ning. The Impact of Intestinal Microbiota Imbalance on the Polycystic Ovary Syndrome[J]. Journal of International Obstetrics and Gynecology, 2023, 50(3): 256-260.

References 31

[1]	Adak A, Khan MR. An insight into gut microbiota and its functionalities[J]. Cell Mol Life Sci, 2019, 76(3):473-493. doi: 10.1007/s00018-018-2943-4. doi: 10.1007/s00018-018-2943-4 pmid: 30317530
[2]	Durack J, Lynch SV. The gut microbiome: Relationships with disease and opportunities for therapy[J]. J Exp Med, 2019, 216(1):20-40. doi: 10.1084/jem.20180448. doi: 10.1084/jem.20180448
[3]	Tremellen K, Pearce K. Dysbiosis of Gut Microbiota (DOGMA)--a novel theory for the development of Polycystic Ovarian Syndrome[J]. Med Hypotheses, 2012, 79(1):104-112. doi: 10.1016/j.mehy.2012.04.016. doi: 10.1016/j.mehy.2012.04.016 pmid: 22543078
[4]	Jobira B, Frank DN, Pyle L, et al. Obese Adolescents With PCOS Have Altered Biodiversity and Relative Abundance in Gastrointestinal Microbiota[J]. J Clin Endocrinol Metab, 2020, 105(6):e2134-e2144. doi: 10.1210/clinem/dgz263. doi: 10.1210/clinem/dgz263
[5]	Cristofori F, Dargenio VN, Dargenio C, et al. Anti-Inflammatory and Immunomodulatory Effects of Probiotics in Gut Inflammation: A Door to the Body[J]. Front Immunol, 2021, 12:578386. doi: 10.3389/fimmu.2021.578386. doi: 10.3389/fimmu.2021.578386
[6]	Chu W, Han Q, Xu J, et al. Metagenomic analysis identified microbiome alterations and pathological association between intestinal microbiota and polycystic ovary syndrome[J]. Fertil Steril, 2020, 113(6):1286-1298.e4. doi: 10.1016/j.fertnstert.2020.01.027. doi: S0015-0282(20)30028-5 pmid: 32482258
[7]	Zhang J, Sun Z, Jiang S, et al. Probiotic Bifidobacterium lactis V9 Regulates the Secretion of Sex Hormones in Polycystic Ovary Syndrome Patients through the Gut-Brain Axis[J]. mSystems, 2019, 4(2):e00017-19. doi: 10.1128/mSystems.00017-19. doi: 10.1128/mSystems.00017-19
[8]	Qi X, Yun C, Sun L, et al. Gut microbiota-bile acid-interleukin-22 axis orchestrates polycystic ovary syndrome[J]. Nat Med, 2019, 25(8):1225-1233. doi: 10.1038/s41591-019-0509-0. doi: 10.1038/s41591-019-0509-0 pmid: 31332392
[9]	Kusamoto A, Harada M, Azhary J, et al. Temporal relationship between alterations in the gut microbiome and the development of polycystic ovary syndrome-like phenotypes in prenatally androgenized female mice[J]. FASEB J, 2021, 35(11):e21971. doi: 10.1096/fj.202101051R. doi: 10.1096/fj.202101051R
[10]	He F, Li Y. The gut microbial composition in polycystic ovary syndrome with insulin resistance: findings from a normal-weight population[J]. J Ovarian Res, 2021, 14(1):50. doi: 10.1186/s13048-021-00799-9. doi: 10.1186/s13048-021-00799-9 pmid: 33773586
[11]	Lindheim L, Bashir M, Münzker J, et al. Alterations in Gut Microbiome Composition and Barrier Function Are Associated with Reproductive and Metabolic Defects in Women with Polycystic Ovary Syndrome (PCOS): A Pilot Study[J]. PLoS One, 2017, 12(1):e0168390. doi: 10.1371/journal.pone.0168390. doi: 10.1371/journal.pone.0168390
[12]	Zhai L, Wu J, Lam YY, et al. Gut-Microbial Metabolites, Probiotics and Their Roles in Type 2 Diabetes[J]. Int J Mol Sci, 2021, 22(23):12846. doi: 10.3390/ijms222312846. doi: 10.3390/ijms222312846
[13]	Mathur B, Shajahan A, Arif W, et al. Nuclear receptors FXR and SHP regulate protein N-glycan modifications in the liver[J]. Sci Adv, 2021, 7(17):eabf4865. doi: 10.1126/sciadv.abf4865. doi: 10.1126/sciadv.abf4865
[14]	LeValley SL, Tomaro-Duchesneau C, Britton RA. Degradation of the Incretin Hormone Glucagon-Like Peptide-1 (GLP-1) by Enterococcus faecalis Metalloprotease GelE[J]. mSphere, 2020, 5(1):e00585-19. doi: 10.1128/mSphere.00585-19. doi: 10.1128/mSphere.00585-19
[15]	Yang PK, Chou CH, Huang CC, et al. Obesity alters ovarian folliculogenesis through disrupted angiogenesis from increased IL-10 production[J]. Mol Metab, 2021, 49:101189. doi: 10.1016/j.molmet.2021.101189. doi: 10.1016/j.molmet.2021.101189
[16]	Zhou L, Ni Z, Cheng W, et al. Characteristic gut microbiota and predicted metabolic functions in women with PCOS[J]. Endocr Connect, 2020, 9(1):63-73. doi: 10.1530/EC-19-0522. doi: 10.1530/EC-19-0522 pmid: 31972546
[17]	Zhou L, Ni Z, Yu J, et al. Correlation Between Fecal Metabolomics and Gut Microbiota in Obesity and Polycystic Ovary Syndrome[J]. Front Endocrinol(Lausanne), 2020, 11:628. doi: 10.3389/fendo.2020.00628. doi: 10.3389/fendo.2020.00628
[18]	Petersen C, Bell R, Klag KA, et al. T cell-mediated regulation of the microbiota protects against obesity[J]. Science, 2019, 365(6451):eaat9351. doi: 10.1126/science.aat9351. doi: 10.1126/science.aat9351
[19]	Wang D, Liu CD, Tian ML, et al. Propionate promotes intestinal lipolysis and metabolic benefits via AMPK/LSD1 pathway in mice[J]. J Endocrinol, 2019 Sep 1:JOE-19-0188.R1. doi: 10.1530/JOE-19-0188. doi: 10.1530/JOE-19-0188
[20]	Yu C, Liu S, Chen L, et al. Effect of exercise and butyrate supplementation on microbiota composition and lipid metabolism[J]. J Endocrinol, 2019, 243(2):125-135. doi: 10.1530/JOE-19-0122. doi: 10.1530/JOE-19-0122 pmid: 31454784
[21]	Salehi M, Purnell JQ. The Role of Glucagon-Like Peptide-1 in Energy Homeostasis[J]. Metab Syndr Relat Disord, 2019, 17(4):183-191. doi: 10.1089/met.2018.0088. doi: 10.1089/met.2018.0088
[22]	Bai X, Ma J, Wu X, et al. Impact of Visceral Obesity on Structural and Functional Alterations of Gut Microbiota in Polycystic Ovary Syndrome (PCOS): A Pilot Study Using Metagenomic Analysis[J]. Diabetes Metab Syndr Obes, 2023, 16:1-14. doi: 10.2147/DMSO.S388067. doi: 10.2147/DMSO.S388067
[23]	Zeng X, Zhong Q, Li M, et al. Androgen increases klotho expression via the androgen receptor-mediated pathway to induce GCs apoptosis[J]. J Ovarian Res, 2023, 16(1):10. doi: 10.1186/s13048-022-01087-w. doi: 10.1186/s13048-022-01087-w pmid: 36641458
[24]	Ervin SM, Li H, Lim L, et al. Gut microbial β-glucuronidases reactivate estrogens as components of the estrobolome that reactivate estrogens[J]. J Biol Chem, 2019, 294(49):18586-18599. doi: 10.1074/jbc.RA119.010950. doi: 10.1074/jbc.RA119.010950 pmid: 31636122
[25]	Barroso A, Santos-Marcos JA, Perdices-Lopez C, et al. Neonatal exposure to androgens dynamically alters gut microbiota architecture[J]. J Endocrinol, 2020, 247(1):69-85. doi: 10.1530/JOE-20-0277. doi: 10.1530/JOE-20-0277 pmid: 32755996
[26]	Geng S, Yang L, Cheng F, et al. Gut Microbiota Are Associated With Psychological Stress-Induced Defections in Intestinal and Blood-Brain Barriers[J]. Front Microbiol, 2019, 10:3067. doi: 10.3389/fmicb.2019.03067. doi: 10.3389/fmicb.2019.03067 pmid: 32010111
[27]	Doden HL, Pollet RM, Mythen SM, et al. Structural and biochemical characterization of 20β-hydroxysteroid dehydrogenase from Bifidobacterium adolescentis strain L2-32[J]. J Biol Chem, 2019, 294(32):12040-12053. doi: 10.1074/jbc.RA119.009390. doi: 10.1074/jbc.RA119.009390
[28]	Wang X, Xu T, Liu R, et al. High-Fiber Diet or Combined With Acarbose Alleviates Heterogeneous Phenotypes of Polycystic Ovary Syndrome by Regulating Gut Microbiota[J]. Front Endocrinol (Lausanne), 2021, 12:806331. doi: 10.3389/fendo.2021.806331. doi: 10.3389/fendo.2021.806331
[29]	Li T, Zhang T, Gao H, et al. Tempol ameliorates polycystic ovary syndrome through attenuating intestinal oxidative stress and modulating of gut microbiota composition-serum metabolites interaction[J]. Redox Biol, 2021, 41:101886. doi: 10.1016/j.redox.2021.101886. doi: 10.1016/j.redox.2021.101886
[30]	Torres PJ, Ho BS, Arroyo P, et al. Exposure to a Healthy Gut Microbiome Protects Against Reproductive and Metabolic Dysregulation in a PCOS Mouse Model[J]. Endocrinology, 2019, 160(5):1193-1204. doi: 10.1210/en.2019-00050. doi: 10.1210/en.2019-00050 pmid: 30924862
[31]	Huang J, Chen P, Xiang Y, et al. Gut microbiota dysbiosis-derived macrophage pyroptosis causes polycystic ovary syndrome via steroidogenesis disturbance and apoptosis of granulosa cells[J]. Int Immunopharmacol, 2022, 107:108717. doi: 10.1016/j.intimp.2022.108717. doi: 10.1016/j.intimp.2022.108717