Login Register Cart 0
Generic placeholder image

Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Pathways Involved in Premature Ovarian Failure: A Systematic Review of Experimental Studies

Author(s): Michail Pargianas, Styliani Salta, Katerina Apostolopoulou, Leandros Lazaros , Maria Kyrgiou, Andrea Tinelli, Antonio Malvasi, Ioannis Kalogiannidis, Ioannis Georgiou and Ioannis P. Kosmas*

Volume 26, Issue 18, 2020

Page: [2087 - 2095] Pages: 9

DOI: 10.2174/1381612826666200316160145

Price: $65

Abstract

Premature ovarian failure (POF), which may be undetectable for a long time, is associated with impaired fertility. The mechanisms involved in the pathogenesis of POF as well as the concomitant treatments are still unclear. Although many data exist, mainly produced by the study of transgenic animals under various experimental conditions, they remain fragmented. A systematic review of the pathways involved in premature ovarian failure was conducted. Data extraction was performed from experimental studies until 2019. The molecular processes and their correlation with the follicular developmental stage have been described. Furthermore, the effects in other cells, such as oocytes, granulosa and theca cells have been reported. An overall estimation was conducted.

Keywords: Fertility, folliculogenesis, ovary, POF, transgenic, follicular.

« Previous Next »
[1]
Meduri G, Bachelot A, Cocca MP, et al. Molecular pathology of the FSH receptor: new insights into FSH physiology. Mol Cell Endocrinol 2008; 282(1-2): 130-42.
[http://dx.doi.org/10.1016/j.mce.2007.11.027] [PMID: 18248882]
[2]
Hasegawa A, Kumamoto K, Mochida N, Komori S, Koyama K. Gene expression profile during ovarian folliculogenesis. J Reprod Immunol 2009; 83(1-2): 40-4.
[http://dx.doi.org/10.1016/j.jri.2009.09.002] [PMID: 19857904]
[3]
Calounova G, Livera G, Zhang XQ, Liu K, Gosden RG, Welsh M. The Src homology 2 domain-containing adapter protein B (SHB) regulates mouse oocyte maturation. PLoS One 2010; 5(6): e11155
[http://dx.doi.org/10.1371/journal.pone.0011155] [PMID: 20585392]
[4]
Devi YS, Seibold AM, Shehu A, et al. Inhibition of MAPK by prolactin signaling through the short form of its receptor in the ovary and decidua: involvement of a novel phosphatase. J Biol Chem 2011; 286(9): 7609-18.
[http://dx.doi.org/10.1074/jbc.M110.166603] [PMID: 21199871]
[5]
Reggiani PC, Barbeito CG, Zuccolilli GO, et al. Neonatal thymulin gene therapy prevents ovarian dysgenesis and attenuates reproductive derangements in nude female mice. Endocrinology 2012; 153(8): 3922-8.
[http://dx.doi.org/10.1210/en.2012-1183] [PMID: 22700775]
[6]
Shibanuma K, Tong ZB, Vanderhoof VH, Vanevski K, Nelson LM. Investigation of KIT gene mutations in women with 46,XX spontaneous premature ovarian failure. BMC Womens Health 2002; 2(1): 8.
[http://dx.doi.org/10.1186/1472-6874-2-8] [PMID: 12153702]
[7]
Hui ES, Udofa EA, Soto J, et al. Investigation of the human stem cell factor KIT ligand gene, KITLG, in women with 46,XX spontaneous premature ovarian failure. Fertil Steril 2006; 85(5): 1502-7.
[http://dx.doi.org/10.1016/j.fertnstert.2005.10.071] [PMID: 16647379]
[8]
Reddy P, Liu L, Adhikari D, et al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Hum Mol Genet 2008; 18: 2813-4.
[http://dx.doi.org/10.1126/science.1152257]
[9]
Reddy P, Adhikari D, Zheng W, et al. PDK1 signaling in oocytes controls reproductive aging and lifespan by manipulating the survival of primordial follicles. Hum Mol Genet 2009; 18(15): 2813-24.
[http://dx.doi.org/10.1093/hmg/ddp217] [PMID: 19423553]
[10]
Jagarlamudi K, Liu L, Adhikari D, et al. Oocyte-specific deletion of Pten in mice reveals a stage-specific function of PTEN/PI3K signaling in oocytes in controlling follicular activation. PLoS One 2009; 4(7): e6186
[http://dx.doi.org/10.1371/journal.pone.0006186] [PMID: 19587782]
[11]
Brown C, LaRocca J, Pietruska J, et al. Subfertility caused by altered follicular development and oocyte growth in female mice lacking PKB alpha/Akt1. Biol Reprod 2010; 82(2): 246-56.
[http://dx.doi.org/10.1095/biolreprod.109.077925] [PMID: 19794155]
[12]
Adhikari D, Zheng W, Shen Y, et al. Tsc/mTORC1 signaling in oocytes governs the quiescence and activation of primordial follicles. Hum Mol Genet 2010; 19(3): 397-410.
[http://dx.doi.org/10.1093/hmg/ddp483] [PMID: 19843540]
[13]
Adhikari D, Flohr G, Gorre N, et al. Disruption of Tsc2 in oocytes leads to overactivation of the entire pool of primordial follicles. Mol Hum Reprod 2009; 15(12): 765-70.
[http://dx.doi.org/10.1093/molehr/gap092] [PMID: 19843635]
[14]
Adhikari D, Gorre N, Risal S, et al. The safe use of a PTEN inhibitor for the activation of dormant mouse primordial follicles and generation of fertilizable eggs. PLoS One 2012; 7(6): e39034
[http://dx.doi.org/10.1371/journal.pone.0039034] [PMID: 22761722]
[15]
Lu C, Lin L, Tan H, et al. Fragile X premutation RNA is sufficient to cause primary ovarian insufficiency in mice. Hum Mol Genet 2012; 21(23): 5039-47.
[http://dx.doi.org/10.1093/hmg/dds348] [PMID: 22914733]
[16]
Fan HY, Shimada M, Liu Z, et al. Selective expression of KrasG12D in granulosa cells of the mouse ovary causes defects in follicle development and ovulation. Development 2008; 135(12): 2127-37.
[http://dx.doi.org/10.1242/dev.020560] [PMID: 18506027]
[17]
Yang X, Zhou Y, Peng S, et al. Differentially expressed plasma microRNAs in premature ovarian failure patients and the potential regulatory function of mir-23a in granulosa cell apoptosis. Reproduction 2012; 144(2): 235-44.
[http://dx.doi.org/10.1530/REP-11-0371] [PMID: 22653319]
[18]
Sobinoff AP, Mahony M, Nixon B, Roman SD, McLaughlin EA. Understanding the Villain: DMBA-induced preantral ovotoxicity involves selective follicular destruction and primordial follicle activation through PI3K/Akt and mTOR signaling. Toxicol Sci 2011; 123(2): 563-75.
[http://dx.doi.org/10.1093/toxsci/kfr195] [PMID: 21785161]
[19]
Sobinoff AP, Nixon B, Roman SD, McLaughlin EA. Staying alive: PI3K pathway promotes primordial follicle activation and survival in response to 3MC-induced ovotoxicity. Toxicol Sci 2012; 128(1): 258-71.
[http://dx.doi.org/10.1093/toxsci/kfs137] [PMID: 22505044]
[20]
Tu X, Kuang Z, Gong X, et al. The Influence of LepR tyrosine site mutations on mouse ovary development and related gene expression changes. PLoS One 2015; 10(11): e0141800
[http://dx.doi.org/10.1371/journal.pone.0141800] [PMID: 26529315]
[21]
Tu X, Liu M, Tang J, et al. The ovarian estrogen synthesis function was impaired in Y123F mouse and partly restored by exogenous FSH supplement. Reprod Biol Endocrinol 2018; 16(1): 44.
[http://dx.doi.org/10.1186/s12958-018-0365-7] [PMID: 29728128]
[22]
Xia H, Zhang R, Guan H, Zhang W. Follicle loss and PTEN/PI3K/mTOR signaling pathway activated in LepR-mutated mice. Gynecol Endocrinol 2019; 35(1): 44-8.
[http://dx.doi.org/10.1080/09513590.2018.1490714] [PMID: 30145913]
[23]
Kezele PR, Ague JM, Nilsson E, Skinner MK. Alterations in the ovarian transcriptome during primordial follicle assembly and development. Biol Reprod 2005; 72(1): 241-55.
[http://dx.doi.org/10.1095/biolreprod.104.032060] [PMID: 15371273]
[24]
Zimmermann RC, Hartman T, Kavic S, et al. Vascular endothelial growth factor receptor 2-mediated angiogenesis is essential for gonadotropin-dependent follicle development. J Clin Invest 2003; 112(5): 659-69.
[http://dx.doi.org/10.1172/JCI200318740] [PMID: 12952915]
[25]
Nakhuda GS, Zimmermann RC, Bohlen P, Liao F, Sauer MV, Kitajewski J. Inhibition of the vascular endothelial cell (VE)-specific adhesion molecule VE-cadherin blocks gonadotropin-dependent folliculogenesis and corpus luteum formation and angiogenesis. Endocrinology 2005; 146(3): 1053-9.
[http://dx.doi.org/10.1210/en.2004-0977] [PMID: 15591148]
[26]
Jeon YJ, Choi Y, Shim SH, et al. Vascular endothelial growth factor gene polymorphisms in Korean patients with premature ovarian failure. Eur J Obstet Gynecol Reprod Biol 2011; 159(1): 138-42.
[http://dx.doi.org/10.1016/j.ejogrb.2011.07.007] [PMID: 21831507]
[27]
Rah H, Jeon YJ, Lee BE, et al. Association of kinase insert domaincontaining receptor (KDR) gene polymorphisms with idiopathic recurrent spontaneous abortion in Korean women Fertil Steril 2013; 99(): 753-60. e8
[28]
Fu Y, Zhao Z, Wu Y, et al. Therapeutic mechanisms of Tongmai Dasheng Tablet on tripterygium glycosides induced rat model for premature ovarian failure. J Ethnopharmacol 2012; 139(1): 26-33.
[http://dx.doi.org/10.1016/j.jep.2011.08.077] [PMID: 22101081]
[29]
Abdel-Ghani MA, Shimizu T, Suzuki H. Expression pattern of vascular endothelial growth factor in canine folliculogenesis and its effect on the growth and development of follicles after ovarian organ culture. Reprod Domest Anim 2014; 49(5): 734-9.
[http://dx.doi.org/10.1111/rda.12357] [PMID: 25041787]
[30]
Fang Y, Lu X, Liu L, et al. Vascular endothelial growth factor induces anti‑Müllerian hormone receptor 2 overexpression in ovarian granulosa cells of in vitro fertilization/intracytoplasmic sperm injection patients. Mol Med Rep 2016; 13(6): 5157-62.
[http://dx.doi.org/10.3892/mmr.2016.5173] [PMID: 27109000]
[31]
Yang Z, Du X, Wang C, et al. Therapeutic effects of human umbilical cord mesenchymal stem cell-derived microvesicles on premature ovarian insufficiency in mice. Stem Cell Res Ther 2019; 10(1): 250.
[http://dx.doi.org/10.1186/s13287-019-1327-5] [PMID: 31412919]
[32]
Elvin JA, Yan C, Wang P, Nishimori K, Matzuk MM. Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol Endocrinol 1999; 13(6): 1018-34.
[http://dx.doi.org/10.1210/mend.13.6.0309] [PMID: 10379899]
[33]
Pangas SA, Li X, Robertson EJ, Matzuk MM. Premature luteinization and cumulus cell defects in ovarian-specific Smad4 knockout mice. Mol Endocrinol 2006; 20(6): 1406-22.
[http://dx.doi.org/10.1210/me.2005-0462] [PMID: 16513794]
[34]
Nilsson E, Rogers N, Skinner MK. Actions of anti-Mullerian hormone on the ovarian transcriptome to inhibit primordial to primary follicle transition. Reproduction 2007; 134(2): 209-21.
[http://dx.doi.org/10.1530/REP-07-0119] [PMID: 17660231]
[35]
Hardy K, Mora JM, Dunlop C, Carzaniga R, Franks S, Fenwick MA. Nuclear exclusion of SMAD2/3 in granulosa cells is associated with primordial follicle activation in the mouse ovary. J Cell Sci 2018; 131(17): 131.
[http://dx.doi.org/10.1242/jcs.218123] [PMID: 30111581]
[36]
Zhou S, Zhao D, Liu S, Zeng W, Zhang C. TGF-β1 sustains germ cell cyst reservoir via restraining follicle formation in the chicken. Cell Biol Int 2019; 44(3): 861-72.
[PMID: 31825139]
[37]
Sonigo C, Beau I, Grynberg M, Binart N. AMH prevents primordial ovarian follicle loss and fertility alteration in cyclophosphamide-treated mice. FASEB J 2019; 33(1): 1278-87.
[http://dx.doi.org/10.1096/fj.201801089R] [PMID: 30113879]
[38]
Sonigo C, Beau I, Binart N, Grynberg M. Anti-müllerian hormone in fertility preservation: clinical and therapeutic applications. Clin Med Insights Reprod Health 2019; 13: 1179558119854755
[http://dx.doi.org/10.1177/1179558119854755] [PMID: 31258345]
[39]
Racki WJ, Richter JD. CPEB controls oocyte growth and follicle development in the mouse. Development 2006; 133(22): 4527-37.
[http://dx.doi.org/10.1242/dev.02651] [PMID: 17050619]
[40]
Liu L, Rajareddy S, Reddy P, et al. Infertility caused by retardation of follicular development in mice with oocyte-specific expression of Foxo3a. Development 2007; 134(1): 199-209.
[http://dx.doi.org/10.1242/dev.02667] [PMID: 17164425]
[41]
Rajareddy S, Reddy P, Du C, et al. p27kip1 (cyclin-dependent kinase inhibitor 1B) controls ovarian development by suppressing follicle endowment and activation and promoting follicle atresia in mice. Mol Endocrinol 2007; 21(9): 2189-202.
[http://dx.doi.org/10.1210/me.2007-0172] [PMID: 17565040]
[42]
Hanrahan JP, Gregan SM, Mulsant P, et al. Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol Reprod 2004; 70(4): 900-9.
[http://dx.doi.org/10.1095/biolreprod.103.023093] [PMID: 14627550]
[43]
Kim JH, Yoon S, Park M, et al. Differential apoptotic activities of wild-type FOXL2 and the adult-type granulosa cell tumor-associated mutant FOXL2 (C134W). Oncogene 2011; 30(14): 1653-63.
[http://dx.doi.org/10.1038/onc.2010.541] [PMID: 21119601]
[44]
Caburet S, Georges A, L’Hôte D, Todeschini AL, Benayoun BA, Veitia RA. The transcription factor FOXL2: at the crossroads of ovarian physiology and pathology. Mol Cell Endocrinol 2012; 356(1-2): 55-64.
[http://dx.doi.org/10.1016/j.mce.2011.06.019] [PMID: 21763750]
[45]
Kuo FT, Bentsi-Barnes IK, Barlow GM, Pisarska MD. Mutant Forkhead L2 (FOXL2) proteins associated with premature ovarian failure (POF) dimerize with wild-type FOXL2, leading to altered regulation of genes associated with granulosa cell differentiation. Endocrinology 2011; 152(10): 3917-29.
[http://dx.doi.org/10.1210/en.2010-0989] [PMID: 21862621]
[46]
Thanatsis N, Kaponis A, Koika V, Georgopoulos NA, Decavalas GO. Reduced Foxo3a, FoxL2, and p27 mRNA expression in human ovarian tissue in premature ovarian insufficiency Horm 2019; 18(4): 537-38.
[47]
Jang H, Lee OH, Lee Y, et al. Melatonin prevents cisplatin-induced primordial follicle loss via suppression of PTEN/AKT/FOXO3a pathway activation in the mouse ovary. J Pineal Res 2016; 60(3): 336-47.
[http://dx.doi.org/10.1111/jpi.12316] [PMID: 26882203]
[48]
Fotovati A, Abu-Ali S, Nakayama K, Nakayama KI. Impaired ovarian development and reduced fertility in female mice deficient in Skp2. J Anat 2011; 218(6): 668-77.
[http://dx.doi.org/10.1111/j.1469-7580.2011.01370.x] [PMID: 21450015]
[49]
Lechowska A, Bilinski S, Choi Y, Shin Y, Kloc M, Rajkovic A. Premature ovarian failure in nobox-deficient mice is caused by defects in somatic cell invasion and germ cell cyst breakdown. J Assist Reprod Genet 2011; 28(7): 583-9.
[http://dx.doi.org/10.1007/s10815-011-9553-5] [PMID: 21369782]
[50]
Maity R, Nair SR, Caspi RR, Nelson LM. Post-thymectomy murine experimental autoimmune oophoritis is associated with reduced natural killer cell activity. Am J Reprod Immunol 1997; 38(5): 360-5.
[http://dx.doi.org/10.1111/j.1600-0897.1997.tb00312.x] [PMID: 9352028]
[51]
Qin CR, Yao JL, Zhu WJ, Wu WQ, Xie JS. FOXE1 polyalanine tract length screening by MLPA in idiopathic premature ovarian failure. Reprod Biol Endocrinol 2011; 9: 158.
[http://dx.doi.org/10.1186/1477-7827-9-158] [PMID: 22177572]
[52]
Dal Pra C, Chen S, Furmaniak J, et al. Autoantibodies to steroidogenic enzymes in patients with premature ovarian failure with and without Addison’s disease. Eur J Endocrinol 2003; 148(5): 565-70.
[http://dx.doi.org/10.1530/eje.0.1480565] [PMID: 12720541]
[53]
Chen S, Sawicka J, Betterle C, et al. Autoantibodies to steroidogenic enzymes in autoimmune polyglandular syndrome, Addison’s disease, and premature ovarian failure. J Clin Endocrinol Metab 1996; 81(5): 1871-6.
[PMID: 8626850]
[54]
Pires ES, Khole VV. A block in the road to fertility: autoantibodies to heat-shock protein 90-beta in human ovarian autoimmunity. Fertil Steril 2009; 92(4): 1395-409.
[http://dx.doi.org/10.1016/j.fertnstert.2008.08.068] [PMID: 19022436]
[55]
Mande PV, Thomas S, Khan S, Jadhav S, Khole VV. Immunization with ovarian autoantigens leads to reduced fertility in mice following follicular dysfunction. Reproduction 2012; 143(3): 309-23.
[http://dx.doi.org/10.1530/REP-11-0221] [PMID: 22143970]
[56]
Bagavant H, Adams S, Terranova P, et al. Autoimmune ovarian inflammation triggered by proinflammatory (Th1) T cells is compatible with normal ovarian function in mice. Biol Reprod 1999; 61(3): 635-42.
[http://dx.doi.org/10.1095/biolreprod61.3.635] [PMID: 10456839]
[57]
Bagavant H, Sharp C, Kurth B, Tung KS. Induction and immunohistology of autoimmune ovarian disease in cynomolgus macaques (Macaca fascicularis). Am J Pathol 2002; 160(1): 141-9.
[http://dx.doi.org/10.1016/S0002-9440(10)64358-1] [PMID: 11786408]
[58]
Fu L, Feng W, Li SR, Huang BY. ZP3 peptides administered orally suppress murine experimental autoimmune ovarian disease. J Reprod Immunol 2007; 75(1): 40-7.
[http://dx.doi.org/10.1016/j.jri.2007.02.009] [PMID: 17418903]
[59]
Shi X, Li N, Liao C, Shu Q, Zhu F. Glucocorticoid or androgen for autoimmune premature ovary failure in mice. Zhong Nan Da Xue Xue Bao Yi Xue Ban 2009; 34(7): 576-81.
[PMID: 19648666]
[60]
Otani Y, Ichii O, Otsuka-Kanazawa S, Chihara M, Nakamura T, Kon Y. MRL/MpJ-Fas(lpr) mice show abnormalities in ovarian function and morphology with the progression of autoimmune disease. Autoimmunity 2015; 48(6): 402-11.
[http://dx.doi.org/10.3109/08916934.2015.1031889] [PMID: 25857350]
[61]
Cachot J, Bultelle F, Drouot L, et al. Molecular cloning of flounder Xp18, a newly identified highly conserved protein mainly expressed in the ovary. Gene 2003; 307: 13-21.
[http://dx.doi.org/10.1016/S0378-1119(03)00460-8] [PMID: 12706884]
[62]
Handa V, Goldwater D, Stiles D, et al. Long CGG-repeat tracts are toxic to human cells: implications for carriers of Fragile X premutation alleles. FEBS Lett 2005; 579(12): 2702-8.
[http://dx.doi.org/10.1016/j.febslet.2005.04.004] [PMID: 15862312]
[63]
Oldenburg RA, van Dooren MF, de Graaf B, et al. A genome-wide linkage scan in a Dutch family identifies a premature ovarian failure susceptibility locus. Hum Reprod 2008; 23(12): 2835-41.
[http://dx.doi.org/10.1093/humrep/den278] [PMID: 18689850]
[64]
Wang B, Suo P, Chen B, et al. Haplotype analysis of chemokine CXCL12 polymorphisms and susceptibility to premature ovarian failure in Chinese women. Hum Reprod 2011; 26(4): 950-4.
[http://dx.doi.org/10.1093/humrep/der001] [PMID: 21296802]
[65]
Padovano V, Lucibello I, Alari V, et al. The POF1B candidate gene for premature ovarian failure regulates epithelial polarity. J Cell Sci 2011; 124(Pt 19): 3356-68.
[http://dx.doi.org/10.1242/jcs.088237] [PMID: 21940798]
[66]
Wang B, Ni F, Li L, et al. Analysis of cyclin-dependent kinase inhibitor 1B mutation in Han Chinese women with premature ovarian failure. Reprod Biomed Online 2010; 21(2): 212-4.
[http://dx.doi.org/10.1016/j.rbmo.2010.04.025] [PMID: 20615757]
[67]
Tanaka T, Utsunomiya T, Utsunomiya H, Umesaki N. Irinotecan HCl, an anticancer topoisomerase I inhibitor, frequently induces ovarian failure in premenopausal and perimenopausal women. Oncol Rep 2008; 19(5): 1123-33.
[http://dx.doi.org/10.3892/or.19.5.1123] [PMID: 18425367]
[68]
Mazaud S, Guigon CJ, Lozach A, et al. Establishment of the reproductive function and transient fertility of female rats lacking primordial follicle stock after fetal gamma-irradiation. Endocrinology 2002; 143(12): 4775-87.
[http://dx.doi.org/10.1210/en.2002-220464] [PMID: 12446605]
[69]
Lieman HJ, Adel TE, Forst C, von Hagen S, Santoro N. Effects of aging and estradiol supplementation on GH axis dynamics in women. J Clin Endocrinol Metab 2001; 86(8): 3918-23.
[http://dx.doi.org/10.1210/jcem.86.8.7751] [PMID: 11502833]
[70]
Boerboom D, Paquet M, Hsieh M, et al. Misregulated Wnt/beta-catenin signaling leads to ovarian granulosa cell tumor development. Cancer Res 2005; 65(20): 9206-15.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-1024] [PMID: 16230381]

Rights & Permissions Print Cite
Article Metrics
56
1
© 2024 Bentham Science Publishers | Privacy Policy