Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Epigenetic Marks in Polycystic Ovary Syndrome

Author(s): Alicia Beatriz Motta*

Volume 27 , Issue 39 , 2020

Page: [6727 - 6743] Pages: 17

DOI: 10.2174/0929867326666191003154548

Price: $65

Abstract

Polycystic Ovary Syndrome (PCOS) is a common endocrine and metabolic disorder that affects women in their reproductive age. Recent studies have shown that genes have an important role in the etiology of PCOS. However, the precise way in which these genes are transcriptionally and post-transcriptionally regulated is poorly understood.

The aim of the present review is to provide updated information on miRNAs and DNA methylation as epigenetic marks of PCOS.

The data presented here allow concluding that both microRNAs and DNA methylation can be considered as possible useful biomarkers when choosing the treatment for a specific PCOS phenotype and thus represent two important tools for the diagnosis and treatment of PCOS patients.

Keywords: Polycystic ovary syndrome, epigenetic marks, miRNAs, DNA methylation, PCOS phenotypes, PCOS treatment.

[1]
Azziz, R.; Carmina, E.; Dewailly, D.; Diamanti-Kandarakis, E.; Escobar-Morreale, H.F.; Futterweit, W.; Janssen, O.E.; Legro, R.S.; Norman, R.J.; Taylor, A.E.; Witchel, S.F. Task force on the phenotype of the polycystic ovary syndrome of the androgen excess and PCOS society. The androgen excess and PCOS Society criteria for the polycystic ovary syndrome: the complete task force report. Fertil. Steril., 2009, 91(2), 456-488.
[http://dx.doi.org/10.1016/j.fertnstert.2008.06.035] [PMID: 18950759]
[2]
Rotterdam ESHRE/ASRM-sponsored PCOS consensus workshop group. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil. Steril., 2004, 81(1), 19-25.
[http://dx.doi.org/10.1016/j.fertnstert.2003.10.004] [PMID: 14711538]
[3]
Zawadzki, J.K.; Dunaif, A. Diagnostic criteria of polycystic ovary syndrome: towards a rational approach in: Polycystic Ovary Syndrome; Dunaif A.; Givens, J.R.; Haseline, F.P; Merriam, G.R., Ed.; Blackwell Scientific Publications: Boston, MA, USA, 1992.
[4]
Franks, S.; Stark, J.; Hardy, K. Follicle dynamics and anovulation in polycystic ovary syndrome. Hum. Reprod. Update, 2008, 14(4), 367-378.
[http://dx.doi.org/10.1093/humupd/dmn015] [PMID: 18499708]
[5]
Ferreira, S.R.; Motta, A.B. Uterine function: from normal to polycystic ovarian syndrome alterations. Curr. Med. Chem., 2018, 25(15), 1792-1804.
[http://dx.doi.org/10.2174/0929867325666171205144119] [PMID: 29210631]
[6]
Franks, S. Polycystic ovary syndrome. N. Engl. J. Med., 1995, 333(13), 853-861.
[http://dx.doi.org/10.1056/NEJM199509283331307] [PMID: 7651477]
[7]
Dunaif, A. Insulin resistance and the polycystic ovary syndrome: mechanism and implications for pathogenesis. Endocr. Rev., 1997, 18(6), 774-800.
[http://dx.doi.org/10.1210/edrv.18.6.0318 ] [PMID: 9408743]
[8]
Subramaniam, K.; Tripathi, A.; Dabadghao, P. Familial clustering of metabolic phenotype in brothers of women with polycystic ovary syndrome. Gynecol. Endocrinol., 2019, 35(7), 601-603.
[http://dx.doi.org/10.1080/09513590.2019.1566451] [PMID: 30727783]
[9]
Yilmaz, B.; Vellanki, P.; Ata, B.; Yildiz, B.O. Diabetes mellitus and insulin resistance in mothers, fathers, sisters, and brothers of women with polycystic ovary syndrome: a systematic review and meta-analysis. Fertil. Steril., 2018, 110(3), 523-533.e14.
[http://dx.doi.org/10.1016/j.fertnstert.2018.04.024] [PMID: 29960703]
[10]
Torchen, L.C.; Kumar, A.; Kalra, B.; Savjani, G.; Sisk, R.; Legro, R.S.; Dunaif, A. Increased antimüllerian hormone levels and other reproductive endocrine changes in adult male relatives of women with polycystic ovary syndrome. Fertil. Steril., 2016, 106(1), 50-55.
[http://dx.doi.org/10.1016/j.fertnstert.2016.03.029] [PMID: 27042970]
[11]
Chen, Z-J.; Zhao, H.; He, L.; Shi, Y.; Qin, Y.; Shi, Y.; Li, Z.; You, L.; Zhao, J.; Liu, J.; Liang, X.; Zhao, X.; Zhao, J.; Sun, Y.; Zhang, B.; Jiang, H.; Zhao, D.; Bian, Y.; Gao, X.; Geng, L.; Li, Y.; Zhu, D.; Sun, X.; Xu, J.E.; Hao, C.; Ren, C.E.; Zhang, Y.; Chen, S.; Zhang, W.; Yang, A.; Yan, J.; Li, Y.; Ma, J.; Zhao, Y. Genome-wide association study identifies susceptibility loci for polycystic ovary syndrome on chromosome 2p16.3, 2p21 and 9q33.3. Nat. Genet., 2011, 43(1), 55-59.
[http://dx.doi.org/10.1038/ng.732] [PMID: 21151128]
[12]
Shi, Y.; Zhao, H.; Shi, Y.; Cao, Y.; Yang, D.; Li, Z.; Zhang, B.; Liang, X.; Li, T.; Chen, J.; Shen, J.; Zhao, J.; You, L.; Gao, X.; Zhu, D.; Zhao, X.; Yan, Y.; Qin, Y.; Li, W.; Yan, J.; Wang, Q.; Zhao, J.; Geng, L.; Ma, J.; Zhao, Y.; He, G.; Zhang, A.; Zou, S.; Yang, A.; Liu, J.; Li, W.; Li, B.; Wan, C.; Qin, Y.; Shi, J.; Yang, J.; Jiang, H.; Xu, J.E.; Qi, X.; Sun, Y.; Zhang, Y.; Hao, C.; Ju, X.; Zhao, D.; Ren, C.E.; Li, X.; Zhang, W.; Zhang, Y.; Zhang, J.; Wu, D.; Zhang, C.; He, L.; Chen, Z.J. Genome-wide association study identifies eight new risk loci for polycystic ovary syndrome. Nat. Genet., 2012, 44(9), 1020-1025.
[http://dx.doi.org/10.1038/ng.2384] [PMID: 22885925]
[13]
Toledo, S.P.; Brunner, H.G.; Kraaij, R.; Post, M.; Dahia, P.L.; Hayashida, C.Y.; Kremer, H.; Themmen, A.P.; Themmen, A.P. An inactivating mutation of the luteinizing hormone receptor causes amenorrhea in a 46,XX female. J. Clin. Endocrinol. Metab., 1996, 81(11), 3850-3854.
[http://dx.doi.org/10.1210/jcem.81.11.8923827 ] [PMID: 8923827]
[14]
Latronico, A.C.; Lins, T.S.; Brito, V.N.; Arnhold, I.J.; Mendonca, B.B. The effect of distinct activating mutations of the luteinizing hormone receptor gene on the pituitary-gonadal axis in both sexes. Clin. Endocrinol. (Oxf.), 2000, 53(5), 609-613.
[http://dx.doi.org/10.1046/j.1365-2265.2000.01135.x] [PMID: 11106922]
[15]
McAllister, J.M.; Legro, R.S.; Modi, B.P.; Strauss, J.F. III Functional genomics of PCOS: from GWAS to molecular mechanisms. Trends Endocrinol. Metab., 2015, 26(3), 118-124.
[http://dx.doi.org/10.1016/j.tem.2014.12.004] [PMID: 25600292]
[16]
Mutharasan, P.; Galdones, E.; Peñalver Bernabé, B.; Garcia, O.A.; Jafari, N.; Shea, L.D.; Woodruff, T.K.; Legro, R.S.; Dunaif, A.; Urbanek, M. Evidence for chromosome 2p16.3 polycystic ovary syndrome susceptibility locus in affected women of European ancestry. J. Clin. Endocrinol. Metab., 2013, 98(1), E185-E190.
[http://dx.doi.org/10.1210/jc.2012-2471] [PMID: 23118426]
[17]
Moller, D.E.; Yokota, A.; White, M.F.; Pazianos, A.G.; Flier, J.S. A naturally occurring mutation of insulin receptor alanine 1134 impairs tyrosine kinase function and is associated with dominantly inherited insulin resistance. J. Biol. Chem., 1990, 265(25), 14979-14985.
[PMID: 2168397]
[18]
Saxena, R.; Elbers, C.C.; Guo, Y.; Peter, I.; Gaunt, T.R.; Mega, J.L.; Lanktree, M.B.; Tare, A.; Castillo, B.A.; Li, Y.R.; Johnson, T.; Bruinenberg, M.; Gilbert-Diamond, D.; Rajagopalan, R.; Voight, B.F.; Balasubramanyam, A.; Barnard, J.; Bauer, F.; Baumert, J.; Bhangale, T.; Böhm, B.O.; Braund, P.S.; Burton, P.R.; Chandrupatla, H.R.; Clarke, R.; Cooper-DeHoff, R.M.; Crook, E.D.; Davey-Smith, G.; Day, I.N.; de Boer, A.; de Groot, M.C.; Drenos, F.; Ferguson, J.; Fox, C.S.; Furlong, C.E.; Gibson, Q.; Gieger, C.; Gilhuijs-Pederson, L.A.; Glessner, J.T.; Goel, A.; Gong, Y.; Grant, S.F.; Grobbee, D.E.; Hastie, C.; Humphries, S.E.; Kim, C.E.; Kivimaki, M.; Kleber, M.; Meisinger, C.; Kumari, M.; Langaee, T.Y.; Lawlor, D.A.; Li, M.; Lobmeyer, M.T.; Maitland-van der Zee, A.H.; Meijs, M.F.; Molony, C.M.; Morrow, D.A.; Murugesan, G.; Musani, S.K.; Nelson, C.P.; Newhouse, S.J.; O’Connell, J.R.; Padmanabhan, S.; Palmen, J.; Patel, S.R.; Pepine, C.J.; Pettinger, M.; Price, T.S.; Rafelt, S.; Ranchalis, J.; Rasheed, A.; Rosenthal, E.; Ruczinski, I.; Shah, S.; Shen, H.; Silbernagel, G.; Smith, E.N.; Spijkerman, A.W.; Stanton, A.; Steffes, M.W.; Thorand, B.; Trip, M.; van der Harst, P. van der A, D.L.; van Iperen, E.P.; van Setten, J.; van Vliet-Ostaptchouk, J.V.; Verweij, N.; Wolffenbuttel, B.H.; Young, T.; Zafarmand, M.H.; Zmuda, J.M.; Boehnke, M.; Altshuler, D.; McCarthy, M.; Kao, W.H.; Pankow, J.S.; Cappola, T.P.; Sever, P.; Poulter, N.; Caulfield, M.; Dominiczak, A.; Shields, D.C.; Bhatt, D.L.; Zhang, L.; Curtis, S.P.; Danesh, J.; Casas, J.P.; van der Schouw, Y.T.; Onland-Moret, N.C.; Doevendans, P.A.; Dorn, G.W., II; Farrall, M.; FitzGerald, G.A.; Hamsten, A.; Hegele, R.; Hingorani, A.D.; Hofker, M.H.; Huggins, G.S.; Illig, T.; Jarvik, G.P.; Johnson, J.A.; Klungel, O.H.; Knowler, W.C.; Koenig, W.; März, W.; Meigs, J.B.; Melander, O.; Munroe, P.B.; Mitchell, B.D.; Bielinski, S.J.; Rader, D.J.; Reilly, M.P.; Rich, S.S.; Rotter, J.I.; Saleheen, D.; Samani, N.J.; Schadt, E.E.; Shuldiner, A.R.; Silverstein, R.; Kottke-Marchant, K.; Talmud, P.J.; Watkins, H.; Asselbergs, F.W.; de Bakker, P.I.; McCaffery, J.; Wijmenga, C.; Sabatine, M.S.; Wilson, J.G.; Reiner, A.; Bowden, D.W.; Hakonarson, H.; Siscovick, D.S.; Keating, B.J. Large-scale gene-centric meta-analysis across 39 studies identifies type 2 diabetes loci. Am. J. Hum. Genet., 2012, 90(3), 410-425.
[http://dx.doi.org/10.1016/j.ajhg.2011.12.022] [PMID: 22325160]
[19]
Voight, B.F.; Scott, L.J.; Steinthorsdottir, V.; Morris, A.P.; Dina, C.; Welch, R.P.; Zeggini, E.; Huth, C.; Aulchenko, Y.S.; Thorleifsson, G.; McCulloch, L.J.; Ferreira, T.; Grallert, H.; Amin, N.; Wu, G.; Willer, C.J.; Raychaudhuri, S.; McCarroll, S.A.; Langenberg, C.; Hofmann, O.M.; Dupuis, J.; Qi, L.; Segrè, A.V.; van Hoek, M.; Navarro, P.; Ardlie, K.; Balkau, B.; Benediktsson, R.; Bennett, A.J.; Blagieva, R.; Boerwinkle, E.; Bonnycastle, L.L.; Bengtsson Boström, K.; Bravenboer, B.; Bumpstead, S.; Burtt, N.P.; Charpentier, G.; Chines, P.S.; Cornelis, M.; Couper, D.J.; Crawford, G.; Doney, A.S.; Elliott, K.S.; Elliott, A.L.; Erdos, M.R.; Fox, C.S.; Franklin, C.S.; Ganser, M.; Gieger, C.; Grarup, N.; Green, T.; Griffin, S.; Groves, C.J.; Guiducci, C.; Hadjadj, S.; Hassanali, N.; Herder, C.; Isomaa, B.; Jackson, A.U.; Johnson, P.R.; Jørgensen, T.; Kao, W.H.; Klopp, N.; Kong, A.; Kraft, P.; Kuusisto, J.; Lauritzen, T.; Li, M.; Lieverse, A.; Lindgren, C.M.; Lyssenko, V.; Marre, M.; Meitinger, T.; Midthjell, K.; Morken, M.A.; Narisu, N.; Nilsson, P.; Owen, K.R.; Payne, F.; Perry, J.R.; Petersen, A.K.; Platou, C.; Proença, C.; Prokopenko, I.; Rathmann, W.; Rayner, N.W.; Robertson, N.R.; Rocheleau, G.; Roden, M.; Sampson, M.J.; Saxena, R.; Shields, B.M.; Shrader, P.; Sigurdsson, G.; Sparsø, T.; Strassburger, K.; Stringham, H.M.; Sun, Q.; Swift, A.J.; Thorand, B.; Tichet, J.; Tuomi, T.; van Dam, R.M.; van Haeften, T.W.; van Herpt, T.; van Vliet-Ostaptchouk, J.V.; Walters, G.B.; Weedon, M.N.; Wijmenga, C.; Witteman, J.; Bergman, R.N.; Cauchi, S.; Collins, F.S.; Gloyn, A.L.; Gyllensten, U.; Hansen, T.; Hide, W.A.; Hitman, G.A.; Hofman, A.; Hunter, D.J.; Hveem, K.; Laakso, M.; Mohlke, K.L.; Morris, A.D.; Palmer, C.N.; Pramstaller, P.P.; Rudan, I.; Sijbrands, E.; Stein, L.D.; Tuomilehto, J.; Uitterlinden, A.; Walker, M.; Wareham, N.J.; Watanabe, R.M.; Abecasis, G.R.; Boehm, B.O.; Campbell, H.; Daly, M.J.; Hattersley, A.T.; Hu, F.B.; Meigs, J.B.; Pankow, J.S.; Pedersen, O.; Wichmann, H.E.; Barroso, I.; Florez, J.C.; Frayling, T.M.; Groop, L.; Sladek, R.; Thorsteinsdottir, U.; Wilson, J.F.; Illig, T.; Froguel, P.; van Duijn, C.M.; Stefansson, K.; Altshuler, D.; Boehnke, M.; McCarthy, M.I. MAGIC investigators. GIANT Consortium. Twelve type 2 diabetes susceptibility loci identified through large-scale association analysis. Nat. Genet., 2010, 42(7), 579-589.
[http://dx.doi.org/10.1038/ng.609] [PMID: 20581827]
[20]
Rosenfield, R.L.; Ehrmann, D.A. The pathogenesis of polycystic ovary syndrome (PCOS): the hypothesis of PCOS as functional ovarian hyperandrogenism revisited. Endocr. Rev., 2016, 37(5), 467-520.
[http://dx.doi.org/10.1210/er.2015-1104] [PMID: 27459230]
[21]
McAllister, J.M.; Modi, B.; Miller, B.A.; Biegler, J.; Bruggeman, R.; Legro, R.S.; Strauss, J.F. III Overexpression of a DENND1A isoform produces a polycystic ovary syndrome theca phenotype. Proc. Natl. Acad. Sci. USA, 2014, 111(15), E1519-E1527.
[http://dx.doi.org/10.1073/pnas.1400574111] [PMID: 24706793]
[22]
Hayes, M.G.; Urbanek, M.; Ehrmann, D.A.; Armstrong, L.L.; Lee, J.Y.; Sisk, R.; Karaderi, T.; Barber, T.M.; McCarthy, M.I.; Franks, S.; Lindgren, C.M.; Welt, C.K.; Diamanti-Kandarakis, E.; Panidis, D.; Goodarzi, M.O.; Azziz, R.; Zhang, Y.; James, R.G.; Olivier, M.; Kissebah, A.H.; Stener-Victorin, E.; Legro, R.S.; Dunaif, A. Reproductive medicine network. Genome-wide association of polycystic ovary syndrome implicates alterations in gonadotropin secretion in European ancestry populations. Nat. Commun., 2015, 6, 7502.
[http://dx.doi.org/10.1038/ncomms8502] [PMID: 26284813]
[23]
Ren, B.; Guo, W.; Tang, Y.; Zhang, J.; Xiao, N.; Zhang, L.; Li, W. Rhein inhibits the migration of ovarian cancer cells through down-regulation of matrix metalloproteinases. Biol. Pharm. Bull., 2019, 42(4), 568-572.
[http://dx.doi.org/10.1248/bpb.b18-00431] [PMID: 30930417]
[24]
Peng, Y.; Zhang, W.; Yang, P.; Tian, Y.; Su, S.; Zhang, C.; Chen, Z.J.; Zhao, H. ERBB4 confers risk for polycystic ovary syndrome in han chinese. Sci. Rep., 2017, 7, 42000.
[http://dx.doi.org/10.1038/srep42000] [PMID: 28195137]
[25]
Crespo, R.P.; Bachega, T.A.S.S.; Mendonça, B.B.; Gomes, L.G. An update of genetic basis of PCOS pathogenesis. Arch. Endocrinol. Metab., 2018, 62(3), 352-361.
[http://dx.doi.org/10.20945/2359-3997000000049] [PMID: 29972435]
[26]
Jones, M.R.; Goodarzi, M.O. Genetic determinants of polycystic ovary syndrome: progress and future directions. Fertil. Steril., 2016, 106(1), 25-32.
[http://dx.doi.org/10.1016/j.fertnstert.2016.04.040] [PMID: 27179787]
[27]
de Bruin, C.; Dauber, A. Insights from exome sequencing for endocrine disorders. Nat. Rev. Endocrinol., 2015, 11(8), 455-464.
[http://dx.doi.org/10.1038/nrendo.2015.72] [PMID: 25963271]
[28]
Gorsic, L.K.; Kosova, G.; Werstein, B.; Sisk, R.; Legro, R.S.; Hayes, M.G.; Teixeira, J.M.; Dunaif, A.; Urbanek, M. pathogenic anti-müllerian hormone variants in polycystic ovary syndrome. J. Clin. Endocrinol. Metab., 2017, 102(8), 2862-2872.
[http://dx.doi.org/10.1210/jc.2017-00612] [PMID: 28505284]
[29]
Abbott, D.H.; Levine, J.E.; Dumesic, D.A. Translational insight into polycystic ovary syndrome (PCOS) from female monkeys with PCOS-like traits. Curr. Pharm. Des., 2016, 22(36), 5625-5633.
[http://dx.doi.org/10.2174/1381612822666160715133437] [PMID: 27426126]
[30]
Azziz, R. PCOS in 2015: New insights into the genetics of polycystic ovary syndrome. Nat. Rev. Endocrinol., 2016, 12(3), 183.
[http://dx.doi.org/10.1038/nrendo.2016.9] [PMID: 26822926]
[31]
Dunaif, A. Perspectives in polycystic ovary syndrome: from hair to eternity. J. Clin. Endocrinol. Metab., 2016, 101(3), 759-768.
[http://dx.doi.org/10.1210/jc.2015-3780] [PMID: 26908109]
[32]
Ambros, V. microRNAs: tiny regulators with great potential. Cell, 2001, 107(7), 823-826.
[http://dx.doi.org/10.1016/S0092-8674(01)00616-X] [PMID: 11779458]
[33]
Gallo, A.; Tandon, M.; Alevizos, I.; Illei, G.G. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One, 2012, 7(3)e30679
[http://dx.doi.org/10.1371/journal.pone.0030679] [PMID: 22427800]
[34]
Lawrie, C.H.; Gal, S.; Dunlop, H.M.; Pushkaran, B.; Liggins, A.P.; Pulford, K.; Banham, A.H.; Pezzella, F.; Boultwood, J.; Wainscoat, J.S.; Hatton, C.S.; Harris, A.L. Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma. Br. J. Haematol., 2008, 141(5), 672-675.
[http://dx.doi.org/10.1111/j.1365-2141.2008.07077.x] [PMID: 18318758]
[35]
Hanson, E.K.; Lubenow, H.; Ballantyne, J. Identification of forensically relevant body fluids using a panel of differentially expressed microRNAs. Anal. Biochem., 2009, 387(2), 303-314.
[http://dx.doi.org/10.1016/j.ab.2009.01.037] [PMID: 19454234]
[36]
Mitchell, P.S.; Parkin, R.K.; Kroh, E.M.; Fritz, B.R.; Wyman, S.K.; Pogosova-Agadjanyan, E.L.; Peterson, A.; Noteboom, J.; O’Briant, K.C.; Allen, A.; Lin, D.W.; Urban, N.; Drescher, C.W.; Knudsen, B.S.; Stirewalt, D.L.; Gentleman, R.; Vessella, R.L.; Nelson, P.S.; Martin, D.B.; Tewari, M. Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. USA, 2008, 105(30), 10513-10518.
[http://dx.doi.org/10.1073/pnas.0804549105] [PMID: 18663219]
[37]
Osman, A. MicroRNAs in health and disease--basic science and clinical applications. Clin. Lab., 2012, 58(5-6), 393-402.
[PMID: 22783567]
[38]
Fernandez-Valverde, S.L.; Taft, R.J.; Mattick, J.S. MicroRNAs in β-cell biology, insulin resistance, diabetes and its complications. Diabetes, 2011, 60(7), 1825-1831.
[http://dx.doi.org/10.2337/db11-0171] [PMID: 21709277]
[39]
Hulsmans, M.; De Keyzer, D.; Holvoet, P. MicroRNAs regulating oxidative stress and inflammation in relation to obesity and atherosclerosis. FASEB J., 2011, 25(8), 2515-2527.
[http://dx.doi.org/10.1096/fj.11-181149] [PMID: 21507901]
[40]
Carletti, M.Z.; Fiedler, S.D.; Christenson, L.K. MicroRNA 21 blocks apoptosis in mouse periovulatory granulosa cells. Biol. Reprod., 2010, 83(2), 286-295.
[http://dx.doi.org/10.1095/biolreprod.109.081448] [PMID: 20357270]
[41]
Ding, C-F.; Chen, W-Q.; Zhu, Y-T.; Bo, Y-L.; Hu, H-M.; Zheng, R-H. Circulating microRNAs in patients with polycystic ovary syndrome. Hum. Fertil. (Camb.), 2015, 18(1), 22-29.
[http://dx.doi.org/10.3109/14647273.2014.956811] [PMID: 25268995]
[42]
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(5), 1304-1315.
[http://dx.doi.org/10.1159/000358698] [PMID: 24802714]
[43]
Murri, M.; Insenser, M.; Fernández-Durán, E.; San-Millán, J.L.; Escobar-Morreale, H.F. 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(11), E1835-E1844.
[http://dx.doi.org/10.1210/jc.2013-2218] [PMID: 24037889]
[44]
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(1), 14671.
[http://dx.doi.org/10.1038/s41598-017-13250-1] [PMID: 29116087]
[45]
Rau, C-S.; Yang, J.C.; Wu, S.C.; Chen, Y.C.; Lu, T.H.; Lin, M.W.; Wu, Y.C.; Tzeng, S.L.; Wu, C.J.; Hsieh, C.H. Profiling circulating microRNA expression in a mouse model of nerve allotransplantation. J. Biomed. Sci., 2013, 20, 64.
[http://dx.doi.org/10.1186/1423-0127-20-64] [PMID: 24011263]
[46]
Roth, L.W.; McCallie, B.; Alvero, R.; Schoolcraft, W.B.; Minjarez, D.; Katz-Jaffe, M.G. Altered microRNA and gene expression in the follicular fluid of women with polycystic ovary syndrome. J. Assist. Reprod. Genet., 2014, 31(3), 355-362.
[http://dx.doi.org/10.1007/s10815-013-0161-4] [PMID: 24390626]
[47]
Salimi-Asl, M.; Mozdarani, H.; Kadivar, M. Up-regulation of miR-21 and 146a expression and increased DNA damage frequency in a mouse model of polycystic ovary syndrome (PCOS). Bioimpacts, 2016, 6(2), 85-91.
[http://dx.doi.org/10.15171/bi.2016.12] [PMID: 27525225]
[48]
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(7), 3068-3079.
[http://dx.doi.org/10.1210/jc.2013-1715] [PMID: 23666971]
[49]
Scalici, E.; Traver, S.; Mullet, T.; Molinari, N.; Ferrières, 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.
[http://dx.doi.org/10.1038/srep24976] [PMID: 27102646]
[50]
Sirotkin, A.V.; Ovcharenko, D.; Grossmann, R.; Lauková, M.; Mlyncek, M. Identification of microRNAs controlling human ovarian cell steroidogenesis via a genome-scale screen. J. Cell. Physiol., 2009, 219(2), 415-420.
[http://dx.doi.org/10.1002/jcp.21689] [PMID: 19194990]
[51]
Sørensen, A.E.; Wissing, M.L.; Salö, S.; Englund, A.L.M.; Dalgaard, L.T. MicroRNAs related to polycystic ovary syndrome (PCOS). Genes (Basel), 2014, 5(3), 684-708.
[http://dx.doi.org/10.3390/genes5030684] [PMID: 25158044]
[52]
Sørensen, A.E.; Udesen, P.B.; Wissing, M.L.; Englund, A.L.M.; Dalgaard, L.T. MicroRNAs related to androgen metabolism and polycystic ovary syndrome. Chem. Biol. Interact., 2016, 259(Pt A), 8-16.
[http://dx.doi.org/10.1016/j.cbi.2016.06.008] [PMID: 27270454]
[53]
Yin, M.; Wang, X.; Yao, G.; Lü, M.; Liang, M.; Sun, Y.; Sun, F. Transactivation of micrornA-320 by microRNA-383 regulates granulosa cell functions by targeting E2F1 and SF-1 proteins. J. Biol. Chem., 2014, 289(26), 18239-18257.
[http://dx.doi.org/10.1074/jbc.M113.546044] [PMID: 24828505]
[54]
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(4), 4889-4898.
[http://dx.doi.org/10.3892/mmr.2018.8463] [PMID: 29363717]
[55]
Li, C.; Chen, L.; Zhao, Y.; Chen, S.; Fu, L.; Jiang, Y.; Gao, S.; Liu, Z.; Wang, F.; Zhu, X.; Rao, J.; Zhang, J.; Zhou, X. Altered expression of miRNAs in the uterus from a letrozole-induced rat PCOS model. Gene, 2017, 598, 20-26.
[http://dx.doi.org/10.1016/j.gene.2016.10.033] [PMID: 27777110]
[56]
Hossain, M.M.; Cao, M.; Wang, Q.; Kim, J.Y.; Schellander, K.; Tesfaye, D.; Tsang, B.K. Altered expression of miRNAs in a dihydrotestosterone-induced rat PCOS model. J. Ovarian Res., 2013, 6(1), 36.
[http://dx.doi.org/10.1186/1757-2215-6-36] [PMID: 23675970]
[57]
Chang, R.J.; Cook-Andersen, H. Disordered follicle development. Mol. Cell. Endocrinol., 2013, 373(1-2), 51-60.
[http://dx.doi.org/10.1016/j.mce.2012.07.011] [PMID: 22874072]
[58]
Sirotkin, A.V.; Lauková, M.; Ovcharenko, D.; Brenaut, P.; Mlyncek, M. Identification of microRNAs controlling human ovarian cell proliferation and apoptosis. J. Cell. Physiol., 2010, 223(1), 49-56.
[http://dx.doi.org/10.1002/jcp.21999 ] [PMID: 20039279]
[59]
Lu, J.; Zhang, C.; Gu, B.; Zhang, S.; Geng, J.; Chen, Y.; Xie, J. 2017.
[60]
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. J. Assist. Reprod. Genet., 2019, 36(2), 211-221.
[http://dx.doi.org/10.1007/s10815-018-1335-x ] [PMID: 30374732]
[61]
Wang, T.; Liu, Y.; Lv, M.; Xing, Q.; Zhang, Z.; He, X.; Xu, Y.; Wei, Z.; Cao, Y. miR-323-3p regulates the steroidogenesis and cell apoptosis in polycystic ovary syndrome (PCOS) by targeting IGF-1. Gene, 2019, 683, 87-100.
[http://dx.doi.org/10.1016/j.gene.2018.10.006] [PMID: 30300681]
[62]
Zhang, Z.; Chen, C.Z.; Xu, M.Q.; Zhang, L.Q.; Liu, J.B.; Gao, Y.; Jiang, H.; Yuan, B.; Zhang, J.B. MiR-31 and miR-143 affect steroid hormone synthesis and inhibit cell apoptosis in bovine granulosa cells through FSHR. Theriogenology, 2019, 123, 45-53.
[http://dx.doi.org/10.1016/j.theriogenology.2018.09.020] [PMID: 30278258]
[63]
Sun, X-F.; Li, Y-P.; Pan, B.; Wang, Y-F.; Li, J.; Shen, W. Molecular regulation of miR-378 on the development of mouse follicle and the maturation of oocyte in vivo. Cell Cycle, 2018, 17(18), 2230-2242.
[http://dx.doi.org/10.1080/15384101.2018.1520557] [PMID: 30244637]
[64]
Fu, X.; He, Y.; Wang, X.; Peng, D.; Chen, X.; Li, X.; Wan, Q. MicroRNA-16 promotes ovarian granulosa cell proliferation and suppresses apoptosis through targeting PDCD4 in polycystic ovarian syndrome. Cell. Physiol. Biochem., 2018, 48(2), 670-682.
[http://dx.doi.org/10.1159/000491894] [PMID: 30025387]
[65]
Jiang, Y-C.; Ma, J-X. The role of MiR-324-3p in polycystic ovary syndrome (PCOS) via targeting WNT2B. Eur. Rev. Med. Pharmacol. Sci., 2018, 22(11), 3286-3293.
[http://dx.doi.org/10.26355/eurrev_201806_15147 ] [PMID: 29917177]
[66]
Liu, J.; Li, X.; Yao, Y.; Li, Q.; Pan, Z.; Li, Q. miR-1275 controls granulosa cell apoptosis and estradiol synthesis by impairing LRH-1/CYP19A1 axis. Biochim. Biophys. Acta. Gene Regul. Mech., 2018, 1861(3), 246-257.
[http://dx.doi.org/10.1016/j.bbagrm.2018.01.009] [PMID: 29378329]
[67]
Wang, M.; Liu, M.; Sun, J.; Jia, L.; Ma, S.; Gao, J.; Xu, Y.; Zhang, H.; Tsang, S.Y.; Li, X. MicroRNA-27a-3p affects estradiol and androgen imbalance by targeting Creb1 in the granulosa cells in mouse polycytic ovary syndrome model. Reprod. Biol., 2017, 17(4), 295-304.
[http://dx.doi.org/10.1016/j.repbio.2017.09.005] [PMID: 29089199]
[68]
Wang, M.; Sun, J.; Xu, B.; Chrusciel, M.; Gao, J.; Bazert, M.; Stelmaszewska, J.; Xu, Y.; Zhang, H.; Pawelczyk, L.; Sun, F.; Ying, S.; Rahman, N.; Wołczyński, S.; Li, X. Functional characterization of MicroRNA-27a-3p expression in human polycystic ovary syndrome. Endocrinology, 2018, 159(1), 297-309.
[http://dx.doi.org/10.1210/en.2017-00219]]
[69]
Yang, L.; Li, Y.; Wang, X.; Liu, Y.; Yang, L. MicroRNA320a inhibition decreases insulininduced KGN cell proliferation and apoptosis by targeting PCGF1. Mol. Med. Rep., 2017, 16(4), 5706-5712.
[http://dx.doi.org/10.3892/mmr.2017.7270] [PMID: 28849208]
[70]
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(3), 372-383.
[http://dx.doi.org/10.1177/1933719117715129] [PMID: 28673204]
[71]
Li, D.; Xu, D.; Xu, Y.; Chen, L.; Li, C.; Dai, X.; Zhang, L.; Zheng, L. MicroRNA-141-3p targets DAPK1 and inhibits apoptosis in rat ovarian granulosa cells. Cell Biochem. Funct., 2017, 35(4), 197-201.
[http://dx.doi.org/10.1002/cbf.3248] [PMID: 28543175]
[72]
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(6), 902-910.
[http://dx.doi.org/10.1177/1933719116673197] [PMID: 27799458]
[73]
Tiwari, M.; Prasad, S.; Tripathi, A.; Pandey, A.N.; Ali, I.; Singh, A.K.; Shrivastav, T.G.; Chaube, S.K. Apoptosis in mammalian oocytes: a review. Apoptosis, 2015, 20(8), 1019-1025.
[http://dx.doi.org/10.1007/s10495-015-1136-y] [PMID: 25958165]
[74]
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, 250-260.
[http://dx.doi.org/10.1016/j.gene.2018.11.025] [PMID: 30453069]
[75]
Yao, Y.; Niu, J.; Sizhu, S.; Li, B.; Chen, Y.; Li, R.; Yangzong, Q.; Li, Q.; Xu, Y. microRNA-125b regulates apoptosis by targeting bone morphogenetic protein receptor 1B in yak granulosa cells. DNA Cell Biol., 2018, 37(11), 878-887.
[http://dx.doi.org/10.1089/dna.2018.4354] [PMID: 30260685]
[76]
Zhang, H.; Jiang, X.; Zhang, Y.; Xu, B.; Hua, J.; Ma, T.; Zheng, W.; Sun, R.; Shen, W.; Cooke, H.J.; Hao, Q.; Qiao, J.; Shi, Q. microRNA 376a regulates follicle assembly by targeting Pcna in fetal and neonatal mouse ovaries. Reproduction, 2014, 148(1), 43-54.
[http://dx.doi.org/10.1530/REP-13-0508] [PMID: 24686458]
[77]
Zhang, J.; Ji, X.; Zhou, D.; Li, Y.; Lin, J.; Liu, J.; Luo, H.; Cui, S. miR-143 is critical for the formation of primordial follicles in mice. Front. Biosci., 2013, 18, 588-597.
[http://dx.doi.org/10.2741/4122] [PMID: 23276944]
[78]
Bird, A. Perceptions of epigenetics. Nature, 2007, 447(7143), 396-398.
[http://dx.doi.org/10.1038/nature05913] [PMID: 17522671]
[79]
Guo, F.; Li, X.; Liang, D.; Li, T.; Zhu, P.; Guo, H.; Wu, X.; Wen, L.; Gu, T.P.; Hu, B.; Walsh, C.P.; Li, J.; Tang, F.; Xu, G.L. Active and passive demethylation of male and female pronuclear DNA in the mammalian zygote. Cell Stem Cell, 2014, 15(4), 447-459.
[http://dx.doi.org/10.1016/j.stem.2014.08.003] [PMID: 25220291]
[80]
Qu, F.; Wang, F.F.; Yin, R.; Ding, G.L.; El-Prince, M.; Gao, Q.; Shi, B.W.; Pan, H.H.; Huang, Y.T.; Jin, M.; Leung, P.C.; Sheng, J.Z.; Huang, H.F. A molecular mechanism underlying ovarian dysfunction of polycystic ovary syndrome: hyperandrogenism induces epigenetic alterations in the granulosa cells. J. Mol. Med. (Berl.), 2012, 90(8), 911-923.
[http://dx.doi.org/10.1007/s00109-012-0881-4] [PMID: 22349439]
[81]
Yu, Y-Y.; Sun, C-X.; Liu, Y-K.; Li, Y.; Wang, L.; Zhang, W. Promoter methylation of CYP19A1 gene in Chinese polycystic ovary syndrome patients. Gynecol. Obstet. Invest., 2013, 76(4), 209-213.
[http://dx.doi.org/10.1159/000355314] [PMID: 24157654]
[82]
Wang, P.; Zhao, H.; Li, T.; Zhang, W.; Wu, K.; Li, M.; Bian, Y.; Liu, H.; Ning, Y.; Li, G.; Chen, Z.J. Hypomethylation of the LH/choriogonadotropin receptor promoter region is a potential mechanism underlying susceptibility to polycystic ovary syndrome. Endocrinology, 2014, 155(4), 1445-1452.
[http://dx.doi.org/10.1210/en.2013-1764] [PMID: 24527662]
[83]
Sang, Q.; Li, X.; Wang, H.; Wang, H.; Zhang, S.; Feng, R.; Xu, Y.; Li, Q.; Zhao, X.; Xing, Q.; Jin, L.; He, L.; Wang, L. Quantitative methylation level of the EPHX1 promoter in peripheral blood DNA is associated with polycystic ovary syndrome. PLoS One, 2014, 9(2)e88013
[http://dx.doi.org/10.1371/journal.pone.0088013] [PMID: 24505354]
[84]
Wang, X-X.; Wei, J-Z.; Jiao, J.; Jiang, S-Y.; Yu, D-H.; Li, D. Genome-wide DNA methylation and gene expression patterns provide insight into polycystic ovary syndrome development. Oncotarget, 2014, 5(16), 6603-6610.
[http://dx.doi.org/10.18632/oncotarget.2224] [PMID: 25051372]
[85]
Pan, J-X.; Tan, Y.J.; Wang, F.F.; Hou, N.N.; Xiang, Y.Q.; Zhang, J.Y.; Liu, Y.; Qu, F.; Meng, Q.; Xu, J.; Sheng, J.Z.; Huang, H.F. Aberrant expression and DNA methylation of lipid metabolism genes in PCOS: a new insight into its pathogenesis. Clin. Epigenetics, 2018, 10, 6.
[http://dx.doi.org/10.1186/s13148-018-0442-y] [PMID: 29344314]
[86]
Zhao, H.; Zhao, Y.; Ren, Y.; Li, M.; Li, T.; Li, R.; Yu, Y.; Qiao, J. Epigenetic regulation of an adverse metabolic phenotype in polycystic ovary syndrome: the impact of the leukocyte methylation of PPARGC1A promoter. Fertil. Steril., 2017, 107(2), 467-474.e5.
[http://dx.doi.org/10.1016/j.fertnstert.2016.10.039] [PMID: 27889100]
[87]
Li, Q-N.; Guo, L.; Hou, Y.; Ou, X-H.; Liu, Z.; Sun, Q-Y. The DNA methylation profile of oocytes in mice with hyperinsulinaemia and hyperandrogenism as detected by single-cell level whole genome bisulphite sequencing (SC-WGBS) technology. Reprod. Fertil. Dev., 2018, 30(12), 1713-1719.
[http://dx.doi.org/10.1071/RD18002] [PMID: 29929576]
[88]
Pruksananonda, K.; Wasinarom, A.; Sereepapong, W.; Sirayapiwat, P.; Rattanatanyong, P.; Mutirangura, A. Epigenetic modification of long interspersed elements-1 in cumulus cells of mature and immature oocytes from patients with polycystic ovary syndrome. Clin. Exp. Reprod. Med., 2016, 43(2), 82-89.
[http://dx.doi.org/10.5653/cerm.2016.43.2.82] [PMID: 27358825]
[89]
Salehi Jahromi, M.; Hill, J.W.; Ramezani Tehrani, F.; Zadeh-Vakili, A. Hypomethylation of specific CpG sites in the promoter region of steroidogeneic genes (GATA6 and StAR) in prenatally androgenized rats. Life Sci., 2018, 207, 105-109.
[http://dx.doi.org/10.1016/j.lfs.2018.05.052] [PMID: 29859221]
[90]
Desai, V.; Prasad, N.R.; Manohar, S.M.; Sachan, A.; Narasimha, S.R.P.V.L.; Bitla, A.R.R. Oxidative stress in non-obese women with polycystic ovarian syndrome. J. Clin. Diagn. Res., 2014, 8(7), CC01-CC03.
[http://dx.doi.org/10.7860/JCDR/2014/8125.4530 ] [PMID: 25177558]
[91]
Elia, E.M.; Belgorosky, D.; Faut, M.; Vighi, S.; Pustovrh, C.; Luigi, D.; Motta, A.B. The effects of metformin on uterine tissue of hyperandrogenized BALB/c mice. Mol. Hum. Reprod., 2009, 15(7), 421-432.
[http://dx.doi.org/10.1093/molehr/gap033] [PMID: 19482906]
[92]
Luchetti, C.G.; Mikó, E.; Szekeres-Bartho, J.; Paz, D.A.; Motta, A.B. Dehydroepiandrosterone and metformin modulate progesterone-induced blocking factor (PIBF), cyclooxygenase 2 (COX2) and cytokines in early pregnant mice. J. Steroid Biochem. Mol. Biol., 2008, 111(3-5), 200-207.
[http://dx.doi.org/10.1016/j.jsbmb.2008.06.007] [PMID: 18606228]
[93]
Rocha, M.; Diaz-Morales, N.; Rovira-Llopis, S.; Escribano-Lopez, I.; Bañuls, C.; Hernandez-Mijares, A.; Diamanti-Kandarakis, E.; Victor, V.M. Mitochondrial dysfunction and endoplasmic reticulum stress in diabetes. Curr. Pharm. Des., 2016, 22(18), 2640-2649.
[http://dx.doi.org/10.2174/1381612822666160209152033] [PMID: 26861650]
[94]
Zuo, T.; Zhu, M.; Xu, W. Roles of oxidative stress in polycystic ovary syndrome and cancers. Oxid. Med. Cell. Longev., 2016, 20168589318
[http://dx.doi.org/10.1155/2016/8589318] [PMID: 26770659]
[95]
Amalfi, S.; Velez, L.M.; Heber, M.F.; Vighi, S.; Ferreira, S.R.; Orozco, A.V.; Pignataro, O.; Motta, A.B. Prenatal hyperandrogenization induces metabolic and endocrine alterations which depend on the levels of testosterone exposure. PLoS One, 2012, 7(5)e37658
[http://dx.doi.org/10.1371/journal.pone.0037658] [PMID: 22655062]
[96]
Motta, A.B. Editorial (thematic issue: advances in the diagnosis and treatment of polycystic ovarian syndrome). Curr. Pharm. Des., 2016, 22(36), 5505-5507.
[http://dx.doi.org/10.2174/1381612822666160826121954] [PMID: 27568785]
[97]
Eini, F.; Novin, M.G.; Joharchi, K.; Hosseini, A.; Nazarian, H.; Piryaei, A.; Bidadkosh, A. Intracytoplasmic oxidative stress reverses epigenetic modifications in polycystic ovary syndrome. Reprod. Fertil. Dev., 2017, 29(12), 2313-2323.
[http://dx.doi.org/10.1071/RD16428] [PMID: 28442024]
[98]
Salehi Jahromi, M.; Ramezani Tehrani, F.; Hill, J.W.; Noroozzadeh, M.; Zarkesh, M.; Ghasemi, A.; Zadeh-Vakili, A. Alteration in follistatin gene expression detected in prenatally androgenized rats. Gynecol. Endocrinol., 2017, 33(6), 433-437.
[http://dx.doi.org/10.1080/09513590.2017.1290067] [PMID: 28277126]
[99]
Yi, L.; Huang, X.; Guo, F.; Zhou, Z.; Dou, Y.; Huan, J. Yes-associated protein (YAP) signaling regulates lipopolysaccharide-induced tissue factor expression in human endothelial cells. Surgery, 2016, 159(5), 1436-1448.
[http://dx.doi.org/10.1016/j.surg.2015.12.008] [PMID: 26791271]
[100]
Jiang, L-L.; Xie, J.K.; Cui, J.Q.; Wei, D.; Yin, B.L.; Zhang, Y.N.; Chen, Y.H.; Han, X.; Wang, Q.; Zhang, C.L. Promoter methylation of yes-associated protein (YAP1) gene in polycystic ovary syndrome. Medicine (Baltimore), 2017, 96(2)e5768
[http://dx.doi.org/10.1097/MD.0000000000005768] [PMID: 28079802]
[101]
Li, S.; Zhu, D.; Duan, H.; Ren, A.; Glintborg, D.; Andersen, M.; Skov, V.; Thomassen, M.; Kruse, T.; Tan, Q. Differential DNA methylation patterns of polycystic ovarian syndrome in whole blood of Chinese women. Oncotarget, 2017, 8(13), 20656-20666.
[http://dx.doi.org/10.18632/oncotarget.9327] [PMID: 27192117]
[102]
Mannerås-Holm, L.; Benrick, A.; Stener-Victorin, E. Gene expression in subcutaneous adipose tissue differs in women with polycystic ovary syndrome and controls matched pair-wise for age, body weight, and body mass index. Adipocyte, 2014, 3(3), 190-196.
[http://dx.doi.org/10.4161/adip.28731] [PMID: 25068085]
[103]
Kokosar, M.; Benrick, A.; Perfilyev, A.; Fornes, R.; Nilsson, E.; Maliqueo, M.; Behre, C.J.; Sazonova, A.; Ohlsson, C.; Ling, C.; Stener-Victorin, E. Epigenetic and transcriptional alterations in human adipose tissue of polycystic ovary syndrome. Sci. Rep., 2016, 6, 22883.
[http://dx.doi.org/10.1038/srep22883] [PMID: 26975253]
[104]
Saenz-de-Juano, M.D.; Billooye, K.; Smitz, J.; Anckaert, E. The loss of imprinted DNA methylation in mouse blastocysts is inflicted to a similar extent by in vitro follicle culture and ovulation induction. Mol. Hum. Reprod., 2016, 22(6), 427-441.
[http://dx.doi.org/10.1093/molehr/gaw013] [PMID: 26908643]
[105]
Zhu, J-Q.; Zhu, L.; Liang, X-W.; Xing, F-Q.; Schatten, H.; Sun, Q-Y. Demethylation of LHR in dehydroepiandrosterone-induced mouse model of polycystic ovary syndrome. Mol. Hum. Reprod., 2010, 16(4), 260-266.
[http://dx.doi.org/10.1093/molehr/gap089] [PMID: 19828691]
[106]
Arancio, W.; Calogero Amato, M.; Magliozzo, M.; Pizzolanti, G.; Vesco, R.; Giordano, C. Serum miRNAs in women affected by hyperandrogenic polycystic ovary syndrome: the potential role of miR-155 as a biomarker for monitoring the estroprogestinic treatment. Gynecol. Endocrinol., 2018, 34(8), 704-708.
[http://dx.doi.org/10.1080/09513590.2018.1428299] [PMID: 29385860]
[107]
Zhai, J. Metformin regulates key MicroRNAs to improve endome-trial receptivity through increasing implantation marker gene expression in patients with PCOS undergoing IVF/ICSI. Reprod. Sci. Thousand Oaks Calif, 2019, 26(1)193371911882046
[http://dx.doi.org/10.1177/1933719118820466 ]
[108]
Zhao, H.; Zhou, D.; Chen, Y.; Liu, D.; Chu, S.; Zhang, S. Beneficial effects of Heqi san on rat model of polycystic ovary syndrome through the PI3K/AKT pathway. Daru, 2017, 25(1), 21.
[http://dx.doi.org/10.1186/s40199-017-0188-7] [PMID: 29020999]
[109]
Christopher, A.F.; Kaur, R.P.; Kaur, G.; Kaur, A.; Gupta, V.; Bansal, P. MicroRNA therapeutics: discovering novel targets and developing specific therapy. Perspect. Clin. Res., 2016, 7(2), 68-74.
[http://dx.doi.org/10.4103/2229-3485.179431] [PMID: 27141472]
[110]
Chen, B.; Ye, F.; Yu, L.; Jia, G.; Huang, X.; Zhang, X.; Peng, S.; Chen, K.; Wang, M.; Gong, S.; Zhang, R.; Yin, J.; Li, H.; Yang, Y.; Liu, H.; Zhang, J.; Zhang, H.; Zhang, A.; Jiang, H.; Luo, C.; Yang, C.G. Development of cell-active N6-methyladenosine RNA demethylase FTO inhibitor. J. Am. Chem. Soc., 2012, 134(43), 17963-17971.
[http://dx.doi.org/10.1021/ja3064149] [PMID: 23045983]

Rights & Permissions Print Export Cite as
© 2022 Bentham Science Publishers | Privacy Policy