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Published in: Reproductive Biology and Endocrinology 1/2021

Open Access 01-12-2021 | Polycystic Ovary Syndrome | Review

Non-coding RNAs in polycystic ovary syndrome: a systematic review and meta-analysis

Authors: Liangshan Mu, Xiaoting Sun, Mixue Tu, Dan Zhang

Published in: Reproductive Biology and Endocrinology | Issue 1/2021

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Abstract

Background

Genetic, environmental and epigenetical factors may play important roles in the pathogenesis of polycystic ovary syndrome (PCOS), however the etiology of PCOS remains unclear. Studies indicated that non-coding RNAs (ncRNAs) were involved in the occurrence and development of PCOS. Thus, we aim to perform a systematic review and meta-analysis to investigate the presence and dysregulated expression of ncRNAs in human PCOS.

Methods

We searched in PubMed, Medline, Web of Science and Embase until July 2019 and summarized all eligible publications focusing on microRNAs (miRNAs), long non-coding RNAs (lncRNAs), circular RNAs (circRNAs) and small interfering RNAs (siRNAs) in PCOS.

Results

Sixty-seven articles were included in our systematic review and 9 articles were included in meta-analysis. There is little overlap between studies when comparing miRNA profiles. Sensitivity analysis showed that the expression of miR-93 was upregulated in PCOS patients (WMD 0.75, P < 0.00001), without heterogeneity among remaining studies (I2 = 0%).

Conclusion

A large number of ncRNAs with altered levels were observed in plasma, serum, follicular fluid, granulosa cells or other issues from PCOS patients. Aberrant ncRNAs expression in PCOS may lead to aberrant steroidogenesis, adipocyte dysfunction, altered ovarian cell proliferation and/or apoptosis and have the potential to be used as diagnostic biomarkers.
Appendix
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Literature
1.
go back to reference Escobar-Morreale HF. Polycystic ovary syndrome: definition, aetiology, diagnosis and treatment. Nat Rev Endocrinol. 2018;14:270–84.PubMedCrossRef Escobar-Morreale HF. Polycystic ovary syndrome: definition, aetiology, diagnosis and treatment. Nat Rev Endocrinol. 2018;14:270–84.PubMedCrossRef
2.
go back to reference Azziz R, Carmina E, Chen Z, Dunaif A, Laven JS, Legro RS, Lizneva D, Natterson-Horowtiz B, Teede HJ, Yildiz BO. Polycystic ovary syndrome. Nat Rev Dis Primers. 2016;2:16057.CrossRefPubMed Azziz R, Carmina E, Chen Z, Dunaif A, Laven JS, Legro RS, Lizneva D, Natterson-Horowtiz B, Teede HJ, Yildiz BO. Polycystic ovary syndrome. Nat Rev Dis Primers. 2016;2:16057.CrossRefPubMed
3.
go back to reference Azziz R, Carmina E, Dewailly D, Diamanti-Kandarakis E, Escobar-Morreale HF, Futterweit W, Janssen OE, Legro RS, Norman RJ, Taylor AE, et al. Positions statement: criteria for defining polycystic ovary syndrome as a predominantly hyperandrogenic syndrome: an androgen excess society guideline. J Clin Endocrinol Metab. 2006;91:4237–45.CrossRefPubMed Azziz R, Carmina E, Dewailly D, Diamanti-Kandarakis E, Escobar-Morreale HF, Futterweit W, Janssen OE, Legro RS, Norman RJ, Taylor AE, et al. Positions statement: criteria for defining polycystic ovary syndrome as a predominantly hyperandrogenic syndrome: an androgen excess society guideline. J Clin Endocrinol Metab. 2006;91:4237–45.CrossRefPubMed
4.
go back to reference Lindholm A, Andersson L, Eliasson M, Bixo M, Sundstrom-Poromaa I. Prevalence of symptoms associated with polycystic ovary syndrome. Int J Gynaecol Obstet. 2008;102:39–43.PubMedCrossRef Lindholm A, Andersson L, Eliasson M, Bixo M, Sundstrom-Poromaa I. Prevalence of symptoms associated with polycystic ovary syndrome. Int J Gynaecol Obstet. 2008;102:39–43.PubMedCrossRef
5.
go back to reference Orio F, Muscogiuri G, Nese C, Palomba S, Savastano S, Tafuri D, Colarieti G, La Sala G, Colao A, Yildiz BO. Obesity, type 2 diabetes mellitus and cardiovascular disease risk: an uptodate in the management of polycystic ovary syndrome. Eur J Obstet Gynecol Reprod Biol. 2016;207:214–9.PubMedCrossRef Orio F, Muscogiuri G, Nese C, Palomba S, Savastano S, Tafuri D, Colarieti G, La Sala G, Colao A, Yildiz BO. Obesity, type 2 diabetes mellitus and cardiovascular disease risk: an uptodate in the management of polycystic ovary syndrome. Eur J Obstet Gynecol Reprod Biol. 2016;207:214–9.PubMedCrossRef
6.
go back to reference Jin P, Xie Y. Treatment strategies for women with polycystic ovary syndrome. Gynecol Endocrinol. 2018;34:272–7.PubMedCrossRef Jin P, Xie Y. Treatment strategies for women with polycystic ovary syndrome. Gynecol Endocrinol. 2018;34:272–7.PubMedCrossRef
7.
go back to reference Piva R, Spandidos DA, Gambari R. From microRNA functions to microRNA therapeutics: novel targets and novel drugs in breast cancer research and treatment (review). Int J Oncol. 2013;43:985–94.PubMedPubMedCentralCrossRef Piva R, Spandidos DA, Gambari R. From microRNA functions to microRNA therapeutics: novel targets and novel drugs in breast cancer research and treatment (review). Int J Oncol. 2013;43:985–94.PubMedPubMedCentralCrossRef
8.
go back to reference Cech TR, Steitz JA. The noncoding RNA revolution-trashing old rules to forge new ones. Cell. 2014;157:77–94.PubMedCrossRef Cech TR, Steitz JA. The noncoding RNA revolution-trashing old rules to forge new ones. Cell. 2014;157:77–94.PubMedCrossRef
9.
10.
13.
go back to reference Qu S, Yang X, Li X, Wang J, Gao Y, Shang R, Sun W, Dou K, Li H. Circular RNA: A new star of noncoding RNAs. Cancer Lett. 2015;365:141–8.CrossRefPubMed Qu S, Yang X, Li X, Wang J, Gao Y, Shang R, Sun W, Dou K, Li H. Circular RNA: A new star of noncoding RNAs. Cancer Lett. 2015;365:141–8.CrossRefPubMed
14.
go back to reference Munker R, Calin George A. MicroRNA profiling in cancer: table 1. Clin Sci. 2011;121:141–58.CrossRef Munker R, Calin George A. MicroRNA profiling in cancer: table 1. Clin Sci. 2011;121:141–58.CrossRef
15.
go back to reference Murri M, Insenser M, Fernandez-Duran E, San-Millan JL, Escobar-Morreale HF. Effects of polycystic ovary syndrome (PCOS), sex hormones, and obesity on circulating miRNA-21, miRNA-27b, miRNA-103, and miRNA-155 expression. J Clin Endocrinol Metab. 2013;98:E1835–44.PubMedCrossRef Murri M, Insenser M, Fernandez-Duran E, San-Millan JL, Escobar-Morreale HF. Effects of polycystic ovary syndrome (PCOS), sex hormones, and obesity on circulating miRNA-21, miRNA-27b, miRNA-103, and miRNA-155 expression. J Clin Endocrinol Metab. 2013;98:E1835–44.PubMedCrossRef
16.
go back to reference Naji M, Aleyasin A, Nekoonam S, Arefian E, Mahdian R. Differential expression of miR-93 and miR-21 in granulosa cells and follicular fluid of polycystic ovary syndrome associating with different phenotypes. Sci Rep. 2017;7:14671.PubMedPubMedCentralCrossRef Naji M, Aleyasin A, Nekoonam S, Arefian E, Mahdian R. Differential expression of miR-93 and miR-21 in granulosa cells and follicular fluid of polycystic ovary syndrome associating with different phenotypes. Sci Rep. 2017;7:14671.PubMedPubMedCentralCrossRef
17.
go back to reference Lin L, Du T, Huang J, Huang LL, Yang DZ. Identification of differentially expressed microRNAs in the ovary of polycystic ovary syndrome with hyperandrogenism and insulin resistance. Chin Med J. 2015;128:169–74.PubMedPubMedCentralCrossRef Lin L, Du T, Huang J, Huang LL, Yang DZ. Identification of differentially expressed microRNAs in the ovary of polycystic ovary syndrome with hyperandrogenism and insulin resistance. Chin Med J. 2015;128:169–74.PubMedPubMedCentralCrossRef
18.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol. 2009;62:1006–12.PubMedCrossRef Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol. 2009;62:1006–12.PubMedCrossRef
19.
go back to reference Stroup DF. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Jama. 2000;283:2008.CrossRefPubMed Stroup DF. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Jama. 2000;283:2008.CrossRefPubMed
21.
go back to reference Aziz O, Constantinides V, Tekkis PP, Athanasiou T, Purkayastha S, Paraskeva P, Darzi AW, Heriot AG. Laparoscopic versus open surgery for rectal cancer: a meta-analysis. Ann Surg Oncol. 2006;13:413–24.PubMedCrossRef Aziz O, Constantinides V, Tekkis PP, Athanasiou T, Purkayastha S, Paraskeva P, Darzi AW, Heriot AG. Laparoscopic versus open surgery for rectal cancer: a meta-analysis. Ann Surg Oncol. 2006;13:413–24.PubMedCrossRef
22.
go back to reference Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75:843–54.CrossRefPubMed Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75:843–54.CrossRefPubMed
23.
go back to reference Hannon GJ, Rivas FV, Murchison EP, Steitz JA. The expanding universe of noncoding RNAs. Cold Spring Harb Symp Quant Biol. 2006;71:551–64.PubMedCrossRef Hannon GJ, Rivas FV, Murchison EP, Steitz JA. The expanding universe of noncoding RNAs. Cold Spring Harb Symp Quant Biol. 2006;71:551–64.PubMedCrossRef
24.
go back to reference Long W, Zhao C, Ji C, Ding H, Cui Y, Guo X, Shen R, Liu J. Characterization of serum microRNAs profile of PCOS and identification of novel non-invasive biomarkers. Cell Physiol Biochem. 2014;33:1304–15.PubMedCrossRef Long W, Zhao C, Ji C, Ding H, Cui Y, Guo X, Shen R, Liu J. Characterization of serum microRNAs profile of PCOS and identification of novel non-invasive biomarkers. Cell Physiol Biochem. 2014;33:1304–15.PubMedCrossRef
25.
go back to reference Sang Q, Yao Z, Wang H, Feng R, Wang H, Zhao X, Xing Q, Jin L, He L, Wu L, Wang L. Identification of microRNAs in human follicular fluid: characterization of microRNAs that govern steroidogenesis in vitro and are associated with polycystic ovary syndrome in vivo. J Clin Endocrinol Metab. 2013;98:3068–79.PubMedCrossRef Sang Q, Yao Z, Wang H, Feng R, Wang H, Zhao X, Xing Q, Jin L, He L, Wu L, Wang L. Identification of microRNAs in human follicular fluid: characterization of microRNAs that govern steroidogenesis in vitro and are associated with polycystic ovary syndrome in vivo. J Clin Endocrinol Metab. 2013;98:3068–79.PubMedCrossRef
26.
go back to reference Chen YH, Heneidi S, Lee JM, Layman LC, Stepp DW, Gamboa GM, Chen BS, Chazenbalk G, Azziz R. miRNA-93 inhibits GLUT4 and is overexpressed in adipose tissue of polycystic ovary syndrome patients and women with insulin resistance. Diabetes. 2013;62:2278–86.PubMedPubMedCentralCrossRef Chen YH, Heneidi S, Lee JM, Layman LC, Stepp DW, Gamboa GM, Chen BS, Chazenbalk G, Azziz R. miRNA-93 inhibits GLUT4 and is overexpressed in adipose tissue of polycystic ovary syndrome patients and women with insulin resistance. Diabetes. 2013;62:2278–86.PubMedPubMedCentralCrossRef
27.
go back to reference Jiang L, Huang J, Li L, Chen Y, Chen X, Zhao X, Yang D. MicroRNA-93 promotes ovarian granulosa cells proliferation through targeting CDKN1A in polycystic ovarian syndrome. J Clin Endocrinol Metab. 2015;100:E729–38.PubMedPubMedCentralCrossRef Jiang L, Huang J, Li L, Chen Y, Chen X, Zhao X, Yang D. MicroRNA-93 promotes ovarian granulosa cells proliferation through targeting CDKN1A in polycystic ovarian syndrome. J Clin Endocrinol Metab. 2015;100:E729–38.PubMedPubMedCentralCrossRef
28.
go back to reference Imbar T, Eisenberg I. Regulatory role of microRNAs in ovarian function. Fertil Steril. 2014;101:1524–30.PubMedCrossRef Imbar T, Eisenberg I. Regulatory role of microRNAs in ovarian function. Fertil Steril. 2014;101:1524–30.PubMedCrossRef
29.
go back to reference Munker R, Calin GA. MicroRNA profiling in cancer. Clin Sci (Lond). 2011;121:141–58.CrossRef Munker R, Calin GA. MicroRNA profiling in cancer. Clin Sci (Lond). 2011;121:141–58.CrossRef
30.
go back to reference Ding CF, Chen WQ, Zhu YT, Bo YL, Hu HM, Zheng RH. Circulating microRNAs in patients with polycystic ovary syndrome. Hum Fertil (Camb). 2015;18:22–9.CrossRef Ding CF, Chen WQ, Zhu YT, Bo YL, Hu HM, Zheng RH. Circulating microRNAs in patients with polycystic ovary syndrome. Hum Fertil (Camb). 2015;18:22–9.CrossRef
31.
go back to reference Jiang L, Li W, Wu M, Cao S. Ciculating miRNA-21 as a biomarker predicts polycystic ovary syndrome (PCOS) in patients. Clin Lab. 2015;61:1009–15.PubMed Jiang L, Li W, Wu M, Cao S. Ciculating miRNA-21 as a biomarker predicts polycystic ovary syndrome (PCOS) in patients. Clin Lab. 2015;61:1009–15.PubMed
32.
go back to reference Sathyapalan T, David R, Gooderham NJ, Atkin SL. Increased expression of circulating miRNA-93 in women with polycystic ovary syndrome may represent a novel, non-invasive biomarker for diagnosis. Sci Rep. 2015;5:16890.PubMedPubMedCentralCrossRef Sathyapalan T, David R, Gooderham NJ, Atkin SL. Increased expression of circulating miRNA-93 in women with polycystic ovary syndrome may represent a novel, non-invasive biomarker for diagnosis. Sci Rep. 2015;5:16890.PubMedPubMedCentralCrossRef
33.
go back to reference Song J, Luo S, Li S-W. miRNA-592 is downregulated and may target LHCGR in polycystic ovary syndrome patients. Reprod Biol. 2015;15:229–37.PubMedCrossRef Song J, Luo S, Li S-W. miRNA-592 is downregulated and may target LHCGR in polycystic ovary syndrome patients. Reprod Biol. 2015;15:229–37.PubMedCrossRef
34.
go back to reference Zhao C, Liu X, Shi Z, Zhang J, Zhang J, Jia X, Ling X. Role of serum miRNAs in the prediction of ovarian hyperstimulation syndrome in polycystic ovarian syndrome patients. Cell Physiol Biochem. 2015;35:1086–94.PubMedCrossRef Zhao C, Liu X, Shi Z, Zhang J, Zhang J, Jia X, Ling X. Role of serum miRNAs in the prediction of ovarian hyperstimulation syndrome in polycystic ovarian syndrome patients. Cell Physiol Biochem. 2015;35:1086–94.PubMedCrossRef
35.
go back to reference Jiang L, Huang J, Chen Y, Yang Y, Li R, Li Y, Chen X, Yang D. Identification of several circulating microRNAs from a genome-wide circulating microRNA expression profile as potential biomarkers for impaired glucose metabolism in polycystic ovarian syndrome. Endocrine. 2016;53:280–90.PubMedCrossRef Jiang L, Huang J, Chen Y, Yang Y, Li R, Li Y, Chen X, Yang D. Identification of several circulating microRNAs from a genome-wide circulating microRNA expression profile as potential biomarkers for impaired glucose metabolism in polycystic ovarian syndrome. Endocrine. 2016;53:280–90.PubMedCrossRef
36.
go back to reference Song DK, Sung Y-A, Lee H. The role of serum microRNA-6767-5p as a biomarker for the diagnosis of polycystic ovary syndrome. PLoS One. 2016;11:e0163756–6. Song DK, Sung Y-A, Lee H. The role of serum microRNA-6767-5p as a biomarker for the diagnosis of polycystic ovary syndrome. PLoS One. 2016;11:e0163756–6.
37.
go back to reference Eisenberg I, Nahmias N, Novoselsky Persky M, Greenfield C, Goldman-Wohl D, Hurwitz A, Haimov-Kochman R, Yagel S, Imbar T. Elevated circulating micro-ribonucleic acid (miRNA)-200b and miRNA-429 levels in anovulatory women. Fertil Steril. 2017;107:269–75.PubMedCrossRef Eisenberg I, Nahmias N, Novoselsky Persky M, Greenfield C, Goldman-Wohl D, Hurwitz A, Haimov-Kochman R, Yagel S, Imbar T. Elevated circulating micro-ribonucleic acid (miRNA)-200b and miRNA-429 levels in anovulatory women. Fertil Steril. 2017;107:269–75.PubMedCrossRef
38.
go back to reference Hosseini AH, Kohan L, Aledavood A, Rostami S. Association of miR-146a rs2910164 and miR-222 rs2858060 polymorphisms with the risk of polycystic ovary syndrome in Iranian women: A case-control study. Taiwan J Obstet Gynecol. 2017;56:652–6.PubMedCrossRef Hosseini AH, Kohan L, Aledavood A, Rostami S. Association of miR-146a rs2910164 and miR-222 rs2858060 polymorphisms with the risk of polycystic ovary syndrome in Iranian women: A case-control study. Taiwan J Obstet Gynecol. 2017;56:652–6.PubMedCrossRef
39.
go back to reference Xiong W, Lin Y, Xu L, Tamadon A, Zou S, Tian F, Shao R, Li X, Feng Y. Circulatory microRNA 23a and microRNA 23b and polycystic ovary syndrome (PCOS): the effects of body mass index and sex hormones in an Eastern Han Chinese population. J Ovarian Res. 2017;10:10. Xiong W, Lin Y, Xu L, Tamadon A, Zou S, Tian F, Shao R, Li X, Feng Y. Circulatory microRNA 23a and microRNA 23b and polycystic ovary syndrome (PCOS): the effects of body mass index and sex hormones in an Eastern Han Chinese population. J Ovarian Res. 2017;10:10.
40.
go back to reference Ebrahimi SO, Reiisi S, Barjui SP. Increased risk of polycystic ovary syndrome (PCOS) associated with CC genotype of miR-146a gene variation. Gynecol Endocrinol. 2018;34:793–7.PubMedCrossRef Ebrahimi SO, Reiisi S, Barjui SP. Increased risk of polycystic ovary syndrome (PCOS) associated with CC genotype of miR-146a gene variation. Gynecol Endocrinol. 2018;34:793–7.PubMedCrossRef
41.
go back to reference Murri M, Insenser M, Fernandez-Duran E, San-Millan JL, Luque-Ramirez M, Escobar-Morreale HF. Non-targeted profiling of circulating microRNAs in women with polycystic ovary syndrome (PCOS): effects of obesity and sex hormones. Metabolism. 2018;86:49–60.PubMedCrossRef Murri M, Insenser M, Fernandez-Duran E, San-Millan JL, Luque-Ramirez M, Escobar-Morreale HF. Non-targeted profiling of circulating microRNAs in women with polycystic ovary syndrome (PCOS): effects of obesity and sex hormones. Metabolism. 2018;86:49–60.PubMedCrossRef
42.
go back to reference Naji M, Nekoonam S, Aleyasin A, Arefian E, Mahdian R, Azizi E, Shabani Nashtaei M, Amidi F. Expression of miR-15a, miR-145, and miR-182 in granulosa-lutein cells, follicular fluid, and serum of women with polycystic ovary syndrome (PCOS). J Ovarian Res. 2018;297:221–31. Naji M, Nekoonam S, Aleyasin A, Arefian E, Mahdian R, Azizi E, Shabani Nashtaei M, Amidi F. Expression of miR-15a, miR-145, and miR-182 in granulosa-lutein cells, follicular fluid, and serum of women with polycystic ovary syndrome (PCOS). J Ovarian Res. 2018;297:221–31.
43.
go back to reference Nanda D, Chandrasekaran SP, Ramachandran V, Kalaivanan K, Carani Venkatraman A. Evaluation of serum miRNA-24, miRNA-29a and miRNA-502-3p expression in PCOS subjects: correlation with biochemical parameters related to PCOS and insulin resistance. Indian J Clin Biochem. 2019;35:169–1781.PubMedCrossRefPubMedCentral Nanda D, Chandrasekaran SP, Ramachandran V, Kalaivanan K, Carani Venkatraman A. Evaluation of serum miRNA-24, miRNA-29a and miRNA-502-3p expression in PCOS subjects: correlation with biochemical parameters related to PCOS and insulin resistance. Indian J Clin Biochem. 2019;35:169–1781.PubMedCrossRefPubMedCentral
44.
go back to reference Rashad NM, Ateya MA, Saraya YS, Elnagar WM, Helal KF, Lashin ME, Abdelrhman AA, Alil AE, Yousef MS. Association of miRNA - 320 expression level and its target gene endothelin-1 with the susceptibility and clinical features of polycystic ovary syndrome. J Ovarian Res. 2019;12:39.PubMedPubMedCentralCrossRef Rashad NM, Ateya MA, Saraya YS, Elnagar WM, Helal KF, Lashin ME, Abdelrhman AA, Alil AE, Yousef MS. Association of miRNA - 320 expression level and its target gene endothelin-1 with the susceptibility and clinical features of polycystic ovary syndrome. J Ovarian Res. 2019;12:39.PubMedPubMedCentralCrossRef
45.
go back to reference Roth LW, McCallie B, Alvero R, Schoolcraft WB, Minjarez D, Katz-Jaffe MG. Altered microRNA and gene expression in the follicular fluid of women with polycystic ovary syndrome. J Assist Reprod Genet. 2014;31:355–62.PubMedPubMedCentralCrossRef Roth LW, McCallie B, Alvero R, Schoolcraft WB, Minjarez D, Katz-Jaffe MG. Altered microRNA and gene expression in the follicular fluid of women with polycystic ovary syndrome. J Assist Reprod Genet. 2014;31:355–62.PubMedPubMedCentralCrossRef
46.
go back to reference Yin M, Wang X, Yao G, Lu M, Liang M, Sun Y, Sun F. Transactivation of miR-320 by miR-383 regulates granulosa cell functions by targeting E2F1 and SF-1*. J Biol Chem. 2014;289:18239–57.PubMedPubMedCentralCrossRef Yin M, Wang X, Yao G, Lu M, Liang M, Sun Y, Sun F. Transactivation of miR-320 by miR-383 regulates granulosa cell functions by targeting E2F1 and SF-1*. J Biol Chem. 2014;289:18239–57.PubMedPubMedCentralCrossRef
47.
go back to reference Scalici E, Traver S, Mullet T, Molinari N, Ferrieres A, Brunet C, Belloc S, Hamamah S. Circulating microRNAs in follicular fluid, powerful tools to explore in vitro fertilization process. Sci Rep. 2016;6:24976.PubMedPubMedCentralCrossRef Scalici E, Traver S, Mullet T, Molinari N, Ferrieres A, Brunet C, Belloc S, Hamamah S. Circulating microRNAs in follicular fluid, powerful tools to explore in vitro fertilization process. Sci Rep. 2016;6:24976.PubMedPubMedCentralCrossRef
48.
go back to reference Sorensen AE, Wissing ML, Englund AL, Dalgaard LT. MicroRNA species in follicular fluid associating with polycystic ovary syndrome and related intermediary phenotypes. J Clin Endocrinol Metab. 2016;101:1579–89.PubMedPubMedCentralCrossRef Sorensen AE, Wissing ML, Englund AL, Dalgaard LT. MicroRNA species in follicular fluid associating with polycystic ovary syndrome and related intermediary phenotypes. J Clin Endocrinol Metab. 2016;101:1579–89.PubMedPubMedCentralCrossRef
49.
go back to reference Naji M, Aleyasin A, Nekoonam S, Arefian E, Mahdian R, Amidi F. Differential expression of miR-93 and miR-21 in granulosa cells and follicular fluid of polycystic ovary syndrome associating with different phenotypes. Sci Rep. 2017;7:14671.PubMedPubMedCentralCrossRef Naji M, Aleyasin A, Nekoonam S, Arefian E, Mahdian R, Amidi F. Differential expression of miR-93 and miR-21 in granulosa cells and follicular fluid of polycystic ovary syndrome associating with different phenotypes. Sci Rep. 2017;7:14671.PubMedPubMedCentralCrossRef
50.
go back to reference Xue Y, Lv J, Xu P, Gu L, Cao J, Xu L, Xue K, Li Q. Identification of microRNAs and genes associated with hyperandrogenism in the follicular fluid of women with polycystic ovary syndrome. J Cell Biochem. 2018;119:3913–21.PubMedCrossRef Xue Y, Lv J, Xu P, Gu L, Cao J, Xu L, Xue K, Li Q. Identification of microRNAs and genes associated with hyperandrogenism in the follicular fluid of women with polycystic ovary syndrome. J Cell Biochem. 2018;119:3913–21.PubMedCrossRef
51.
go back to reference Yao L, Li M, Hu J, Wang W, Gao M. MiRNA-335-5p negatively regulates granulosa cell proliferation via SGK3 in PCOS. Reproduction. 2018;156:439–49.PubMed Yao L, Li M, Hu J, Wang W, Gao M. MiRNA-335-5p negatively regulates granulosa cell proliferation via SGK3 in PCOS. Reproduction. 2018;156:439–49.PubMed
52.
go back to reference Zhang H, Gao ZN, Zhang YJ, Wang HH, Li YF. MiR-873-5p regulated LPS-induced oxidative stress via targeting heme oxygenase-1 (HO-1) in KGN cells. RSC Adv. 2018;8:39098–105.CrossRefPubMedPubMedCentral Zhang H, Gao ZN, Zhang YJ, Wang HH, Li YF. MiR-873-5p regulated LPS-induced oxidative stress via targeting heme oxygenase-1 (HO-1) in KGN cells. RSC Adv. 2018;8:39098–105.CrossRefPubMedPubMedCentral
53.
go back to reference Shi L, Liu S, Zhao W, Shi J. miR-483-5p and miR-486-5p are down-regulated in cumulus cells of metaphase II oocytes from women with polycystic ovary syndrome. Reprod BioMed Online. 2015;31:565–72.PubMedCrossRef Shi L, Liu S, Zhao W, Shi J. miR-483-5p and miR-486-5p are down-regulated in cumulus cells of metaphase II oocytes from women with polycystic ovary syndrome. Reprod BioMed Online. 2015;31:565–72.PubMedCrossRef
54.
go back to reference Liu S, Zhang X, Shi C, Lin J, Chen G, Wu B, Wu L, Shi H, Yuan Y, Zhou W, et al. Altered microRNAs expression profiling in cumulus cells from patients with polycystic ovary syndrome. J Transl Med. 2015;13:238.PubMedPubMedCentralCrossRef Liu S, Zhang X, Shi C, Lin J, Chen G, Wu B, Wu L, Shi H, Yuan Y, Zhou W, et al. Altered microRNAs expression profiling in cumulus cells from patients with polycystic ovary syndrome. J Transl Med. 2015;13:238.PubMedPubMedCentralCrossRef
55.
go back to reference Xu B, Zhang YW, Tong XH, Liu YS. Characterization of microRNA profile in human cumulus granulosa cells: identification of microRNAs that regulate notch signaling and are associated with PCOS. Mol Cell Endocrinol. 2015;404:26–36.PubMedCrossRef Xu B, Zhang YW, Tong XH, Liu YS. Characterization of microRNA profile in human cumulus granulosa cells: identification of microRNAs that regulate notch signaling and are associated with PCOS. Mol Cell Endocrinol. 2015;404:26–36.PubMedCrossRef
56.
go back to reference Huang X, Liu C, Hao CF, Tang QQ, Liu RM, Lin SX, Zhang LP, Yan W. Identification of altered microRNAs and mRNAs in the cumulus cells of PCOS patients: miRNA-509-3p promotes oestradiol secretion by targeting MAP 3K8. Reproduction. 2016;151:643–55.PubMedCrossRef Huang X, Liu C, Hao CF, Tang QQ, Liu RM, Lin SX, Zhang LP, Yan W. Identification of altered microRNAs and mRNAs in the cumulus cells of PCOS patients: miRNA-509-3p promotes oestradiol secretion by targeting MAP 3K8. Reproduction. 2016;151:643–55.PubMedCrossRef
57.
go back to reference Cai G, Ma X, Chen B, Huang Y, Liu S, Yang H, Zou W. MicroRNA-145 negatively regulates cell proliferation through targeting IRS1 in isolated ovarian granulosa cells from patients with polycystic ovary syndrome. Reprod Sci. 2017;24:902–10.PubMedCrossRef Cai G, Ma X, Chen B, Huang Y, Liu S, Yang H, Zou W. MicroRNA-145 negatively regulates cell proliferation through targeting IRS1 in isolated ovarian granulosa cells from patients with polycystic ovary syndrome. Reprod Sci. 2017;24:902–10.PubMedCrossRef
58.
go back to reference Zhang CL, Wang H, Yan CY, Gao XF, Ling XJ. Deregulation of RUNX2 by miR-320a deficiency impairs steroidogenesis in cumulus granulosa cells from polycystic ovary syndrome (PCOS) patients. Biochem Biophys Res Commun. 2017;482:1469–76.PubMedCrossRef Zhang CL, Wang H, Yan CY, Gao XF, Ling XJ. Deregulation of RUNX2 by miR-320a deficiency impairs steroidogenesis in cumulus granulosa cells from polycystic ovary syndrome (PCOS) patients. Biochem Biophys Res Commun. 2017;482:1469–76.PubMedCrossRef
59.
go back to reference He T, Liu Y, Jia Y, Wang H, Yang X, Lu G, Liu H, Shi Y. MicroRNA-141 and MicroRNA-200c are overexpressed in granulosa cells of polycystic ovary syndrome patients. Front Med (Lausanne). 2018;5:299.CrossRef He T, Liu Y, Jia Y, Wang H, Yang X, Lu G, Liu H, Shi Y. MicroRNA-141 and MicroRNA-200c are overexpressed in granulosa cells of polycystic ovary syndrome patients. Front Med (Lausanne). 2018;5:299.CrossRef
60.
go back to reference Mao Z, Fan L, Yu Q, Luo S, Wu X, Tang J, Kang G, Tang L. Abnormality of Klotho signaling is involved in polycystic ovary syndrome. Reprod Sci. 2018;25:372–83.PubMedCrossRef Mao Z, Fan L, Yu Q, Luo S, Wu X, Tang J, Kang G, Tang L. Abnormality of Klotho signaling is involved in polycystic ovary syndrome. Reprod Sci. 2018;25:372–83.PubMedCrossRef
61.
go back to reference Wang M, Sun J, Xu B, Chrusciel M, Gao J, Bazert M, Stelmaszewska J, Xu Y, Zhang H, Pawelczyk L, et al. Functional characterization of microRNA-27a-3p expression in human polycystic ovary syndrome. Endocrinology. 2018;159:297–309.PubMedCrossRef Wang M, Sun J, Xu B, Chrusciel M, Gao J, Bazert M, Stelmaszewska J, Xu Y, Zhang H, Pawelczyk L, et al. Functional characterization of microRNA-27a-3p expression in human polycystic ovary syndrome. Endocrinology. 2018;159:297–309.PubMedCrossRef
62.
go back to reference Zhong Z, Li F, Li Y, Qin S, Wen C, Fu Y, Xiao Q. Inhibition of microRNA-19b promotes ovarian granulosa cell proliferation by targeting IGF-1 in polycystic ovary syndrome. Mol Med Rep. 2018;17:4889–98.PubMedPubMedCentral Zhong Z, Li F, Li Y, Qin S, Wen C, Fu Y, Xiao Q. Inhibition of microRNA-19b promotes ovarian granulosa cell proliferation by targeting IGF-1 in polycystic ovary syndrome. Mol Med Rep. 2018;17:4889–98.PubMedPubMedCentral
63.
go back to reference Geng Y, Sui C, Xun Y, Lai Q, Jin L. MiRNA-99a can regulate proliferation and apoptosis of human granulosa cells via targeting IGF-1R in polycystic ovary syndrome. Mol Hum Reprod. 2019;25:638–6.CrossRef Geng Y, Sui C, Xun Y, Lai Q, Jin L. MiRNA-99a can regulate proliferation and apoptosis of human granulosa cells via targeting IGF-1R in polycystic ovary syndrome. Mol Hum Reprod. 2019;25:638–6.CrossRef
64.
go back to reference Li Y, Xiang Y, Song Y, Wan L, Yu G, Tan L. Dysregulated miR-142, −33b, and −423 in granulosa cells target TGFBR1 and SMAD7: a possible role in polycystic ovary syndrome. Mol Hum Reprod. 2019;25:638–46. Li Y, Xiang Y, Song Y, Wan L, Yu G, Tan L. Dysregulated miR-142, −33b, and −423 in granulosa cells target TGFBR1 and SMAD7: a possible role in polycystic ovary syndrome. Mol Hum Reprod. 2019;25:638–46.
65.
go back to reference Luo H, Han Y, Liu J, Zhang Y. Identification of microRNAs in granulosa cells from patients with different levels of ovarian reserve function and the potential regulatory function of miR-23a in granulosa cell apoptosis. Gene. 2019;686:250–60.PubMedCrossRef Luo H, Han Y, Liu J, Zhang Y. Identification of microRNAs in granulosa cells from patients with different levels of ovarian reserve function and the potential regulatory function of miR-23a in granulosa cell apoptosis. Gene. 2019;686:250–60.PubMedCrossRef
66.
go back to reference Wang Y, Xu S, Wang Y, Qi G, Hou Y, Sun C, Wu X. Identification and potential value of candidate microRNAs in granulosa cells of polycystic ovary syndrome. Technol Health Care. 2019;27:579–87.PubMedCrossRef Wang Y, Xu S, Wang Y, Qi G, Hou Y, Sun C, Wu X. Identification and potential value of candidate microRNAs in granulosa cells of polycystic ovary syndrome. Technol Health Care. 2019;27:579–87.PubMedCrossRef
67.
go back to reference Song Y, Yu G, Xiang Y, Li Y, Wan L, Tan L. Altered miR-186 and miR-135a contribute to granulosa cell dysfunction by targeting ESR2: A possible role in polycystic ovary syndrome. Mol Cell Endocrinol. 2019;494:110478.PubMedCrossRef Song Y, Yu G, Xiang Y, Li Y, Wan L, Tan L. Altered miR-186 and miR-135a contribute to granulosa cell dysfunction by targeting ESR2: A possible role in polycystic ovary syndrome. Mol Cell Endocrinol. 2019;494:110478.PubMedCrossRef
68.
go back to reference Hou Y, Wang Y, Xu S, Qi G, Wu X. Bioinformatics identification of microRNAs involved in polycystic ovary syndrome based on microarray data. Mol Med Rep. 2019;20:281–91.PubMedPubMedCentral Hou Y, Wang Y, Xu S, Qi G, Wu X. Bioinformatics identification of microRNAs involved in polycystic ovary syndrome based on microarray data. Mol Med Rep. 2019;20:281–91.PubMedPubMedCentral
69.
go back to reference McCallie B, Schoolcraft WB, Katz-Jaffe MG. Aberration of blastocyst microRNA expression is associated with human infertility. Fertil Steril. 2010;93:2374–82.PubMedCrossRef McCallie B, Schoolcraft WB, Katz-Jaffe MG. Aberration of blastocyst microRNA expression is associated with human infertility. Fertil Steril. 2010;93:2374–82.PubMedCrossRef
70.
go back to reference Wu HL, Heneidi S, Chuang TY, Diamond MP, Layman LC, Azziz R, Chen YH. The expression of the miR-25/93/106b family of micro-RNAs in the adipose tissue of women with polycystic ovary syndrome. J Clin Endocrinol Metab. 2014;99:E2754–61.PubMedPubMedCentralCrossRef Wu HL, Heneidi S, Chuang TY, Diamond MP, Layman LC, Azziz R, Chen YH. The expression of the miR-25/93/106b family of micro-RNAs in the adipose tissue of women with polycystic ovary syndrome. J Clin Endocrinol Metab. 2014;99:E2754–61.PubMedPubMedCentralCrossRef
71.
go back to reference Xiang Y, Song Y, Li Y, Zhao D, Ma L, Tan L. miR-483 is Down-regulated in polycystic ovarian syndrome and inhibits KGN cell proliferation via targeting insulin-like growth factor 1 (IGF1). Med Sci Monit. 2016;22:3383–93.PubMedPubMedCentralCrossRef Xiang Y, Song Y, Li Y, Zhao D, Ma L, Tan L. miR-483 is Down-regulated in polycystic ovarian syndrome and inhibits KGN cell proliferation via targeting insulin-like growth factor 1 (IGF1). Med Sci Monit. 2016;22:3383–93.PubMedPubMedCentralCrossRef
72.
go back to reference Yuan WTL. MicroRNA-320 inhibits insulin resistance in patients with PCOS through regulating ERK1/2 signaling pathway. Biomed Res Int. 2017;28:4946–9. Yuan WTL. MicroRNA-320 inhibits insulin resistance in patients with PCOS through regulating ERK1/2 signaling pathway. Biomed Res Int. 2017;28:4946–9.
73.
go back to reference McAllister JM, Han AX, Modi BP, Teves ME, Mavodza GR, Anderson ZL, Shen T, Christenson LK, Archer KJ, Strauss JF. MicroRNA profiling reveals miRNA-130b-3p mediates DENND1A variant 2 expression and androgen biosynthesis. Endocrinology. 2019;160:1964–81.PubMedPubMedCentralCrossRef McAllister JM, Han AX, Modi BP, Teves ME, Mavodza GR, Anderson ZL, Shen T, Christenson LK, Archer KJ, Strauss JF. MicroRNA profiling reveals miRNA-130b-3p mediates DENND1A variant 2 expression and androgen biosynthesis. Endocrinology. 2019;160:1964–81.PubMedPubMedCentralCrossRef
74.
go back to reference Kim SJ, Veenstra-VanderWeele J, Hanna GL, Gonen D, Leventhal BL, Cook EH Jr. Mutation screening of human 5-HT (2B) receptor gene in early-onset obsessive-compulsive disorder. Mol Cell Probes. 2000;14:47–52.PubMedCrossRef Kim SJ, Veenstra-VanderWeele J, Hanna GL, Gonen D, Leventhal BL, Cook EH Jr. Mutation screening of human 5-HT (2B) receptor gene in early-onset obsessive-compulsive disorder. Mol Cell Probes. 2000;14:47–52.PubMedCrossRef
75.
go back to reference Vanderhyden BCAD. Role of cumulus cells and serum on the in vitro maturation, fertilization, and subsequent development of rat oocytes. Biol Reprod. 1989;40:720–8.PubMedCrossRef Vanderhyden BCAD. Role of cumulus cells and serum on the in vitro maturation, fertilization, and subsequent development of rat oocytes. Biol Reprod. 1989;40:720–8.PubMedCrossRef
77.
go back to reference Quinn JJ, Chang HY. Unique features of long non-coding RNA biogenesis and function. Nat Rev Genet. 2016;17:47–62.PubMedCrossRef Quinn JJ, Chang HY. Unique features of long non-coding RNA biogenesis and function. Nat Rev Genet. 2016;17:47–62.PubMedCrossRef
78.
go back to reference Nakagawa S, Shimada M, Yanaka K, Mito M, Arai T, Takahashi E, Fujita Y, Fujimori T, Standaert L, Marine JC, Hirose T. The lncRNA Neat1 is required for corpus luteum formation and the establishment of pregnancy in a subpopulation of mice. Development. 2014;141:4618–27.PubMedPubMedCentralCrossRef Nakagawa S, Shimada M, Yanaka K, Mito M, Arai T, Takahashi E, Fujita Y, Fujimori T, Standaert L, Marine JC, Hirose T. The lncRNA Neat1 is required for corpus luteum formation and the establishment of pregnancy in a subpopulation of mice. Development. 2014;141:4618–27.PubMedPubMedCentralCrossRef
79.
go back to reference Liu Z, Hao C, Song D, Zhang N, Bao H, Qu Q. Androgen receptor coregulator CTBP1-AS is associated with polycystic ovary syndrome in Chinese women: A preliminary study. Reprod Sci. 2015;22:829–37.PubMedPubMedCentralCrossRef Liu Z, Hao C, Song D, Zhang N, Bao H, Qu Q. Androgen receptor coregulator CTBP1-AS is associated with polycystic ovary syndrome in Chinese women: A preliminary study. Reprod Sci. 2015;22:829–37.PubMedPubMedCentralCrossRef
80.
go back to reference Liu ZT, Hao CF, Huang X, Zhang N, Bao HC, Qu QL. Peripheral blood leukocyte expression level of IncRNA steroid receptor RNA activator (SRA) and its association with polycystic ovary syndrome: a case control study. Gynecol Endocrinol. 2015;31:363–8.PubMedCrossRef Liu ZT, Hao CF, Huang X, Zhang N, Bao HC, Qu QL. Peripheral blood leukocyte expression level of IncRNA steroid receptor RNA activator (SRA) and its association with polycystic ovary syndrome: a case control study. Gynecol Endocrinol. 2015;31:363–8.PubMedCrossRef
81.
go back to reference Huang X, Hao CF, Bao HC, Wang MM, Dai HG. Aberrant expression of long noncoding RNAs in cumulus cells isolated from PCOS patients. J Assist Reprod Genet. 2016;33:111–21.PubMedCrossRef Huang X, Hao CF, Bao HC, Wang MM, Dai HG. Aberrant expression of long noncoding RNAs in cumulus cells isolated from PCOS patients. J Assist Reprod Genet. 2016;33:111–21.PubMedCrossRef
82.
go back to reference Liu YD, Li Y, Feng SX, Ye DS, Chen X, Zhou XY, Chen SL. Long noncoding RNAs: potential regulators involved in the pathogenesis of polycystic ovary syndrome. Endocrinology. 2017;158:3890–9.PubMedCrossRef Liu YD, Li Y, Feng SX, Ye DS, Chen X, Zhou XY, Chen SL. Long noncoding RNAs: potential regulators involved in the pathogenesis of polycystic ovary syndrome. Endocrinology. 2017;158:3890–9.PubMedCrossRef
83.
go back to reference Huang X, Pan J, Wu B, Teng X. Construction and analysis of a lncRNA (PWRN2)-mediated ceRNA network reveal its potential roles in oocyte nuclear maturation of patients with PCOS. Reprod Biol Endocrinol. 2018;16:73.PubMedPubMedCentralCrossRef Huang X, Pan J, Wu B, Teng X. Construction and analysis of a lncRNA (PWRN2)-mediated ceRNA network reveal its potential roles in oocyte nuclear maturation of patients with PCOS. Reprod Biol Endocrinol. 2018;16:73.PubMedPubMedCentralCrossRef
84.
go back to reference Jiao J, Shi B, Wang T, Fang Y, Cao T, Zhou Y, Wang X, Li D. Characterization of long non-coding RNA and messenger RNA profiles in follicular fluid from mature and immature ovarian follicles of healthy women and women with polycystic ovary syndrome. Hum Reprod. 2018;33:1735–48.PubMedCrossRef Jiao J, Shi B, Wang T, Fang Y, Cao T, Zhou Y, Wang X, Li D. Characterization of long non-coding RNA and messenger RNA profiles in follicular fluid from mature and immature ovarian follicles of healthy women and women with polycystic ovary syndrome. Hum Reprod. 2018;33:1735–48.PubMedCrossRef
85.
go back to reference Lin H, Xing W, Li Y, Xie Y, Tang X, Zhang Q. Downregulation of serum long noncoding RNA GAS5 may contribute to insulin resistance in PCOS patients. Gynecol Endocrinol. 2018;34:784–8.PubMedCrossRef Lin H, Xing W, Li Y, Xie Y, Tang X, Zhang Q. Downregulation of serum long noncoding RNA GAS5 may contribute to insulin resistance in PCOS patients. Gynecol Endocrinol. 2018;34:784–8.PubMedCrossRef
86.
go back to reference Zhao J, Xu J, Wang W, Zhao H, Liu H, Liu X, Liu J, Sun Y, Dunaif A, Du Y, Chen ZJ. Long non-coding RNA LINC-01572:28 inhibits granulosa cell growth via a decrease in p27 (Kip1) degradation in patients with polycystic ovary syndrome. EBioMedicine. 2018;36:526–38.PubMedPubMedCentralCrossRef Zhao J, Xu J, Wang W, Zhao H, Liu H, Liu X, Liu J, Sun Y, Dunaif A, Du Y, Chen ZJ. Long non-coding RNA LINC-01572:28 inhibits granulosa cell growth via a decrease in p27 (Kip1) degradation in patients with polycystic ovary syndrome. EBioMedicine. 2018;36:526–38.PubMedPubMedCentralCrossRef
87.
go back to reference Yang R, Chen J, Wang L, Deng A. LncRNA BANCR participates in polycystic ovary syndrome by promoting cell apoptosis. Mol Med Rep. 2019;19:1581–6.PubMed Yang R, Chen J, Wang L, Deng A. LncRNA BANCR participates in polycystic ovary syndrome by promoting cell apoptosis. Mol Med Rep. 2019;19:1581–6.PubMed
88.
go back to reference Li Qin C-cH, Yan X-m, Wang Y, Zhong-yi, Wei X-c. Long non-coding RNA H19 is associated with polycystic ovary syndrome in Chinese women: a preliminary study. Endocr J. 2019;66:587–95.PubMedCrossRef Li Qin C-cH, Yan X-m, Wang Y, Zhong-yi, Wei X-c. Long non-coding RNA H19 is associated with polycystic ovary syndrome in Chinese women: a preliminary study. Endocr J. 2019;66:587–95.PubMedCrossRef
89.
go back to reference Shan K, Liu C, Liu BH, Chen X, Dong R, Liu X, Zhang YY, Liu B, Zhang SJ, Wang JJ, et al. Circular noncoding RNA HIPK3 mediates retinal vascular dysfunction in diabetes mellitus. Circulation. 2017;136:1629–42.PubMedCrossRef Shan K, Liu C, Liu BH, Chen X, Dong R, Liu X, Zhang YY, Liu B, Zhang SJ, Wang JJ, et al. Circular noncoding RNA HIPK3 mediates retinal vascular dysfunction in diabetes mellitus. Circulation. 2017;136:1629–42.PubMedCrossRef
90.
go back to reference Legnini I, Di Timoteo G, Rossi F, Morlando M, Briganti F, Sthandier O, Fatica A, Santini T, Andronache A, Wade M, et al. Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell. 2017;66:22–37 e29.PubMedPubMedCentralCrossRef Legnini I, Di Timoteo G, Rossi F, Morlando M, Briganti F, Sthandier O, Fatica A, Santini T, Andronache A, Wade M, et al. Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol Cell. 2017;66:22–37 e29.PubMedPubMedCentralCrossRef
91.
go back to reference Rybak-Wolf A, Stottmeister C, Glažar P, Jens M, Pino N, Giusti S, Hanan M, Behm M, Bartok O, Ashwal-Fluss R, et al. Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol Cell. 2015;58:870–85.PubMedCrossRef Rybak-Wolf A, Stottmeister C, Glažar P, Jens M, Pino N, Giusti S, Hanan M, Behm M, Bartok O, Ashwal-Fluss R, et al. Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol Cell. 2015;58:870–85.PubMedCrossRef
93.
go back to reference Dang Y, Yan L, Hu B, Fan X, Ren Y, Li R, Lian Y, Yan J, Li Q, Zhang Y, et al. Tracing the expression of circular RNAs in human pre-implantation embryos. Genome Biol. 2016;17:130.PubMedPubMedCentralCrossRef Dang Y, Yan L, Hu B, Fan X, Ren Y, Li R, Lian Y, Yan J, Li Q, Zhang Y, et al. Tracing the expression of circular RNAs in human pre-implantation embryos. Genome Biol. 2016;17:130.PubMedPubMedCentralCrossRef
94.
go back to reference Cheng J, Huang J, Yuan S, Zhou S, Yan W, Shen W, Chen Y, Xia X, Luo A, Zhu D, Wang S. Circular RNA expression profiling of human granulosa cells during maternal aging reveals novel transcripts associated with assisted reproductive technology outcomes. PLoS One. 2017;12:e0177888.PubMedPubMedCentralCrossRef Cheng J, Huang J, Yuan S, Zhou S, Yan W, Shen W, Chen Y, Xia X, Luo A, Zhu D, Wang S. Circular RNA expression profiling of human granulosa cells during maternal aging reveals novel transcripts associated with assisted reproductive technology outcomes. PLoS One. 2017;12:e0177888.PubMedPubMedCentralCrossRef
95.
go back to reference Che Q, Liu M, Xu J, Liu Y, Cao X, Dong X, Liu S. Characterization of circular RNA expression profiles in cumulus cells from patients with polycystic ovary syndrome. Fertil Steril. 2019;111:1243–51.PubMedCrossRef Che Q, Liu M, Xu J, Liu Y, Cao X, Dong X, Liu S. Characterization of circular RNA expression profiles in cumulus cells from patients with polycystic ovary syndrome. Fertil Steril. 2019;111:1243–51.PubMedCrossRef
96.
go back to reference Ma Z, Zhao H, Zhang Y, Liu X, Hao C. Novel circular RNA expression in the cumulus cells of patients with polycystic ovary syndrome; 2019.CrossRef Ma Z, Zhao H, Zhang Y, Liu X, Hao C. Novel circular RNA expression in the cumulus cells of patients with polycystic ovary syndrome; 2019.CrossRef
97.
go back to reference Wang LP, Peng XY, Lv XQ, Liu L, Li XL, He X, Lv F, Pan Y, Wang L, Liu KF, Zhang XM. High throughput circRNAs sequencing profile of follicle fluid exosomes of polycystic ovary syndrome patients. J Cell Physiol. 2019;234:15537–47.CrossRef Wang LP, Peng XY, Lv XQ, Liu L, Li XL, He X, Lv F, Pan Y, Wang L, Liu KF, Zhang XM. High throughput circRNAs sequencing profile of follicle fluid exosomes of polycystic ovary syndrome patients. J Cell Physiol. 2019;234:15537–47.CrossRef
98.
go back to reference Zhang C, Liu J, Lai M, Li J, Zhan J, Wen Q, Ma H. Circular RNA expression profiling of granulosa cells in women of reproductive age with polycystic ovary syndrome. Arch Gynecol Obstet. 2019;300:431–40.PubMedPubMedCentralCrossRef Zhang C, Liu J, Lai M, Li J, Zhan J, Wen Q, Ma H. Circular RNA expression profiling of granulosa cells in women of reproductive age with polycystic ovary syndrome. Arch Gynecol Obstet. 2019;300:431–40.PubMedPubMedCentralCrossRef
99.
go back to reference Grunweller A, Hartmann RK. RNA interference as a gene-specific approach for molecular medicine. Curr Med Chem. 2005;12:3143–61.PubMedCrossRef Grunweller A, Hartmann RK. RNA interference as a gene-specific approach for molecular medicine. Curr Med Chem. 2005;12:3143–61.PubMedCrossRef
100.
101.
go back to reference Anjali G, Kaur S, Lakra R, Taneja J, Kalsey GS, Nagendra A, Shrivastav TG, Devi MG, Malhotra N, Kriplani A, Singh R. FSH stimulates IRS-2 expression in human granulosa cells through cAMP/SP1, an inoperative FSH action in PCOS patients. Cell Signal. 2015;27:2452–66.PubMedCrossRef Anjali G, Kaur S, Lakra R, Taneja J, Kalsey GS, Nagendra A, Shrivastav TG, Devi MG, Malhotra N, Kriplani A, Singh R. FSH stimulates IRS-2 expression in human granulosa cells through cAMP/SP1, an inoperative FSH action in PCOS patients. Cell Signal. 2015;27:2452–66.PubMedCrossRef
102.
go back to reference Li L, Mo H, Zhang J, Zhou Y, Peng X, Luo X. The role of heat shock protein 90B1 in patients with polycystic ovary syndrome. PLoS One. 2016;11:e0152837.PubMedPubMedCentralCrossRef Li L, Mo H, Zhang J, Zhou Y, Peng X, Luo X. The role of heat shock protein 90B1 in patients with polycystic ovary syndrome. PLoS One. 2016;11:e0152837.PubMedPubMedCentralCrossRef
103.
go back to reference Song WJ, Shi X, Zhang J, Chen L, Fu SX, Ding YL. Akt-mTOR signaling mediates abnormalities in the proliferation and apoptosis of ovarian granulosa cells in patients with polycystic ovary syndrome. Gynecol Obstet Investig. 2018;83:124–32.CrossRef Song WJ, Shi X, Zhang J, Chen L, Fu SX, Ding YL. Akt-mTOR signaling mediates abnormalities in the proliferation and apoptosis of ovarian granulosa cells in patients with polycystic ovary syndrome. Gynecol Obstet Investig. 2018;83:124–32.CrossRef
104.
go back to reference Guan GZD, Zheng Y, Wen L, Yu D, Lu Y, Zhao Y. microRNA-423-3p promotes tumor progression via modulation of AdipoR2 in laryngeal carcinoma. Int J Clin Exp Pathol 75683-5691. 2014;7:1936–2625. Guan GZD, Zheng Y, Wen L, Yu D, Lu Y, Zhao Y. microRNA-423-3p promotes tumor progression via modulation of AdipoR2 in laryngeal carcinoma. Int J Clin Exp Pathol 75683-5691. 2014;7:1936–2625.
105.
go back to reference Wickham EP 3rd, Tao T, Nestler JE, McGee EA. Activation of the LH receptor up regulates the type 2 adiponectin receptor in human granulosa cells. J Assist Reprod Genet. 2013;30:963–8.PubMedPubMedCentralCrossRef Wickham EP 3rd, Tao T, Nestler JE, McGee EA. Activation of the LH receptor up regulates the type 2 adiponectin receptor in human granulosa cells. J Assist Reprod Genet. 2013;30:963–8.PubMedPubMedCentralCrossRef
106.
go back to reference Comim FV, Hardy K, Franks S. Adiponectin and its receptors in the ovary: further evidence for a link between obesity and hyperandrogenism in polycystic ovary syndrome. PLoS One. 2013;8:e80416.PubMedPubMedCentralCrossRef Comim FV, Hardy K, Franks S. Adiponectin and its receptors in the ovary: further evidence for a link between obesity and hyperandrogenism in polycystic ovary syndrome. PLoS One. 2013;8:e80416.PubMedPubMedCentralCrossRef
107.
go back to reference Carmina ER, F., Jannì A. Increased DHEAs levels in PCO syndrome: evidence for the existence of two subgroups of patients. J Endocrinol Investig. 1986;9:5–9.CrossRef Carmina ER, F., Jannì A. Increased DHEAs levels in PCO syndrome: evidence for the existence of two subgroups of patients. J Endocrinol Investig. 1986;9:5–9.CrossRef
108.
go back to reference Steinberger ES, Smith KD, Rodriguez-Rigau LJ. Testosterone, dehydroepiandrosterone, and dehydroepiandrosterone sulfate in hyperandrogenic women. J Clin Endocrinol Metab. 1984;59:471–7.PubMedCrossRef Steinberger ES, Smith KD, Rodriguez-Rigau LJ. Testosterone, dehydroepiandrosterone, and dehydroepiandrosterone sulfate in hyperandrogenic women. J Clin Endocrinol Metab. 1984;59:471–7.PubMedCrossRef
109.
go back to reference Hoffman DI, Klove K, Lobo RA. The prevalence and significance of elevated dehydroepiandrosterone sulfate levels in anovulatory women. Fertil Steril. 1984;42:76–81.PubMedCrossRef Hoffman DI, Klove K, Lobo RA. The prevalence and significance of elevated dehydroepiandrosterone sulfate levels in anovulatory women. Fertil Steril. 1984;42:76–81.PubMedCrossRef
110.
go back to reference Apparao KBCL, Lovely LP, Gui Y, Lininger RA, Lessey BA. Elevated endometrial androgen receptor expression in women with polycystic ovarian syndrome. Biol Reprod. 2002;66:297–304.PubMedCrossRef Apparao KBCL, Lovely LP, Gui Y, Lininger RA, Lessey BA. Elevated endometrial androgen receptor expression in women with polycystic ovarian syndrome. Biol Reprod. 2002;66:297–304.PubMedCrossRef
111.
go back to reference Hillier SG, Tetsuka M, Fraser HM. Location and developmental regulation of androgen receptor in primate ovary. Hum Reprod. 1997;12:107–11.PubMedCrossRef Hillier SG, Tetsuka M, Fraser HM. Location and developmental regulation of androgen receptor in primate ovary. Hum Reprod. 1997;12:107–11.PubMedCrossRef
112.
go back to reference Sen A, Prizant H, Light A, Biswas A, Hayes E, Lee H-J, Barad D, Gleicher N, Hammes SR. Androgens regulate ovarian follicular development by increasing follicle stimulating hormone receptor and microRNA-125b expression. Proc Natl Acad Sci U S A. 2014;111:3008–13.PubMedPubMedCentralCrossRef Sen A, Prizant H, Light A, Biswas A, Hayes E, Lee H-J, Barad D, Gleicher N, Hammes SR. Androgens regulate ovarian follicular development by increasing follicle stimulating hormone receptor and microRNA-125b expression. Proc Natl Acad Sci U S A. 2014;111:3008–13.PubMedPubMedCentralCrossRef
113.
go back to reference Leivonen SK, Makela R, Ostling P, Kohonen P, Haapa-Paananen S, Kleivi K, Enerly E, Aakula A, Hellstrom K, Sahlberg N, et al. Protein lysate microarray analysis to identify microRNAs regulating estrogen receptor signaling in breast cancer cell lines. Oncogene. 2009;28:3926–36.PubMedCrossRef Leivonen SK, Makela R, Ostling P, Kohonen P, Haapa-Paananen S, Kleivi K, Enerly E, Aakula A, Hellstrom K, Sahlberg N, et al. Protein lysate microarray analysis to identify microRNAs regulating estrogen receptor signaling in breast cancer cell lines. Oncogene. 2009;28:3926–36.PubMedCrossRef
114.
go back to reference Schomberg DW, Couse JF, Mukherjee A, Lubahn DB, Sar M, Mayo KE, Korach KS. Targeted disruption of the estrogen receptor-alpha gene in female mice: characterization of ovarian responses and phenotype in the adult. Endocrinology. 1999;140:2733–44.PubMedCrossRef Schomberg DW, Couse JF, Mukherjee A, Lubahn DB, Sar M, Mayo KE, Korach KS. Targeted disruption of the estrogen receptor-alpha gene in female mice: characterization of ovarian responses and phenotype in the adult. Endocrinology. 1999;140:2733–44.PubMedCrossRef
115.
go back to reference Zhao JJ, Lin J, Yang H, Kong W, He L, Ma X, Coppola D, Cheng JQ. MicroRNA-221/222 negatively regulates estrogen receptor alpha and is associated with tamoxifen resistance in breast cancer. J Biol Chem. 2008;283:31079–86.PubMedPubMedCentralCrossRef Zhao JJ, Lin J, Yang H, Kong W, He L, Ma X, Coppola D, Cheng JQ. MicroRNA-221/222 negatively regulates estrogen receptor alpha and is associated with tamoxifen resistance in breast cancer. J Biol Chem. 2008;283:31079–86.PubMedPubMedCentralCrossRef
116.
go back to reference Leygue EDH, Watson PH, Murphy LC. Expression of the steroid receptor RNA activator in human breast tumors. Cancer Res. 1999;59:4190–3.PubMed Leygue EDH, Watson PH, Murphy LC. Expression of the steroid receptor RNA activator in human breast tumors. Cancer Res. 1999;59:4190–3.PubMed
117.
go back to reference Lanz RB, Chua SS, Barron N, Soder BM, DeMayo F, O'Malley BW. Steroid receptor RNA activator stimulates proliferation as well as apoptosis in vivo. Mol Cell Biol. 2003;23:7163–76.PubMedPubMedCentralCrossRef Lanz RB, Chua SS, Barron N, Soder BM, DeMayo F, O'Malley BW. Steroid receptor RNA activator stimulates proliferation as well as apoptosis in vivo. Mol Cell Biol. 2003;23:7163–76.PubMedPubMedCentralCrossRef
118.
go back to reference Zhao X, Patton JR, Davis SL, Florence B, Ames SJ, Spanjaard RA. Regulation of nuclear receptor activity by a pseudouridine synthase through posttranscriptional modification of steroid receptor RNA activator. Mol Cell. 2004;15:549–58.PubMedCrossRef Zhao X, Patton JR, Davis SL, Florence B, Ames SJ, Spanjaard RA. Regulation of nuclear receptor activity by a pseudouridine synthase through posttranscriptional modification of steroid receptor RNA activator. Mol Cell. 2004;15:549–58.PubMedCrossRef
119.
go back to reference Takayama K, Tsutsumi S, Katayama S, Okayama T, Horie-Inoue K, Ikeda K, Urano T, Kawazu C, Hasegawa A, Ikeo K, et al. Integration of cap analysis of gene expression and chromatin immunoprecipitation analysis on array reveals genome-wide androgen receptor signaling in prostate cancer cells. Oncogene. 2010;30:619–30.PubMedCrossRef Takayama K, Tsutsumi S, Katayama S, Okayama T, Horie-Inoue K, Ikeda K, Urano T, Kawazu C, Hasegawa A, Ikeo K, et al. Integration of cap analysis of gene expression and chromatin immunoprecipitation analysis on array reveals genome-wide androgen receptor signaling in prostate cancer cells. Oncogene. 2010;30:619–30.PubMedCrossRef
121.
go back to reference Ling HY, Ou HS, Feng SD, Zhang XY, Tuo QH, Chen LX, Zhu BY, Gao ZP, Tang CK, Yin WD, et al. CHANGES IN microRNA (miR) profile and effects of miR-320 in insulin-resistant 3T3-L1 adipocytes. Clin Exp Pharmacol Physiol. 2009;36:e32–9.PubMedCrossRef Ling HY, Ou HS, Feng SD, Zhang XY, Tuo QH, Chen LX, Zhu BY, Gao ZP, Tang CK, Yin WD, et al. CHANGES IN microRNA (miR) profile and effects of miR-320 in insulin-resistant 3T3-L1 adipocytes. Clin Exp Pharmacol Physiol. 2009;36:e32–9.PubMedCrossRef
122.
go back to reference Vendola KAZJ, Adesanya OO, Weil SJ, Bondy CA. Androgens stimulate early stages of follicular growth in the primate ovary. J Clin Invest. 1998;101:2622–9.PubMedPubMedCentralCrossRef Vendola KAZJ, Adesanya OO, Weil SJ, Bondy CA. Androgens stimulate early stages of follicular growth in the primate ovary. J Clin Invest. 1998;101:2622–9.PubMedPubMedCentralCrossRef
123.
go back to reference Chen X, Zhao G, Wang F, Gao F, Luo H, Wang Y, Du Y, Chen X, Xue C, Dong Z, Song G. Upregulation of miR-513b inhibits cell proliferation, migration, and promotes apoptosis by targeting high mobility group-box 3 protein in gastric cancer. Tumour Biol. 2014;35:11081–9.PubMedCrossRef Chen X, Zhao G, Wang F, Gao F, Luo H, Wang Y, Du Y, Chen X, Xue C, Dong Z, Song G. Upregulation of miR-513b inhibits cell proliferation, migration, and promotes apoptosis by targeting high mobility group-box 3 protein in gastric cancer. Tumour Biol. 2014;35:11081–9.PubMedCrossRef
124.
go back to reference Stubbs SA, Stark J, Dilworth SM, Franks S, Hardy K. Abnormal preantral folliculogenesis in polycystic ovaries is associated with increased granulosa cell division. J Clin Endocrinol Metab. 2007;92:4418–26.PubMedCrossRef Stubbs SA, Stark J, Dilworth SM, Franks S, Hardy K. Abnormal preantral folliculogenesis in polycystic ovaries is associated with increased granulosa cell division. J Clin Endocrinol Metab. 2007;92:4418–26.PubMedCrossRef
Metadata
Title
Non-coding RNAs in polycystic ovary syndrome: a systematic review and meta-analysis
Authors
Liangshan Mu
Xiaoting Sun
Mixue Tu
Dan Zhang
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2021
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-020-00687-9

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