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Frontiers in Medical Science Research, 2024, 6(2); doi: 10.25236/FMSR.2024.060214.

Research Progress on the Pathogenesis of Premature Ovarian Failure: A Review

Author(s)

Jiaru Wu1, Zecheng Wang1, Guohong Zhang2, Lin Liu2, Yunfeng Li2

Corresponding Author:
Yunfeng Li
Affiliation(s)

1School of Integrative Medicine, Hebei University of Chinese Medicine, Shijiazhuang, Hebei, China

2Hebei Key Laboratory of Chinese Medicine Research on Cardio-cerebrovascular Disease, Shijiazhuang, Hebei, China

Abstract

Premature ovarian failure (POF) causes tremendous physical and psychological health problems in women worldwide. Many important scientific studies have shown that the pathogenesis of POF may be related to reproductive endocrine hormone levels, granulosa cell apoptosis, mitochondrial dysfunction, immune function, related signalling pathways, genes, and enzyme deficiencies. The modern treatment for POF is hormone replacement therapy, but this method has limitations and cannot meet the needs of patients with POF. Therefore, this paper reviews the research on POF in recent years, and by summarizing its mechanism, we search for a multiway and multimans treatment for POF to explore the optimal treatment plan.

Keywords

premature ovarian failure; pathogenesis; research progress

Cite This Paper

Jiaru Wu, Zecheng Wang, Guohong Zhang, Lin Liu, Yunfeng Li. Research Progress on the Pathogenesis of Premature Ovarian Failure: A Review. Frontiers in Medical Science Research (2024), Vol. 6, Issue 2: 84-97. https://doi.org/10.25236/FMSR.2024.060214.

References

[1] Kawamura K, Kawamura N, Hsueh AJ. Activation of dormant follicles: a new treatment for premature ovarian failure[J]. Curr Opin Obstet Gynecol, 2016, 28(3):217-222.

[2] Li M, Zhu Y, Wei J, et al. The global prevalence of premature ovarian insufficiency: a systematic review and meta-analysis. Climacteric, 2023, 26(2):95-102. 

[3] Genazzani AR, Monteleone P, Giannini A, et al. Hormone therapy in the postmenopausal years: considering benefits and risks in clinical practice[J]. Hum Reprod Update, 2021,27(6):1115-1150.

[4] Li Y, Yan MY, Chen QC,et al. Current Research on Complementary and Alternative Medicine in the Treatment of Premature Ovarian Failure: An Update Review. Evid Based Complement Alternat Med, 2022:2574438. 

[5] Chon SJ, Umair Z, Yoon MS. Premature Ovarian Insufficiency: Past, Present, and Future. Front Cell Dev Biol, 2021;9:672890.

[6] Pastore LM, Christianson MS, Stelling J, et al. Reproductive ovarian testing and the alphabet soup of diagnoses: DOR, POI, POF, POR, and FOR[J]. J Assist Reprod Genet, 2018, 35(1):17-23.

[7] Yang W, CHEN Zhuting C, Jingru Z, et al. Effects of tonifying the kidney and sparing the liver on the hypothalamic-pituitary-ovarian axis in rats with premature ovarian failure[J]. Fujian Traditional Chinese Medicine, 2021,52(06):25-26+35.

[8] Gurbuz AS, Deveer R, Gode F. Evaluation of Dual Trigger with Combination of Gonadotropin-Releasing Hormone Agonist and Human Chorionic Gonadotropin in İmproving Oocyte-Follicle Ratio in Normo-Responder Patients[J]. Niger J Clin Pract, 2021, 24(8):1159-1163.

[9] Jiao X, Meng T, Zhai Y, Zhao L, et al. Ovarian Reserve Markers in Premature Ovarian Insufficiency: Within Different Clinical Stages and Different Etiologies[J]. Front Endocrinol (Lausanne), 2021,12: 601752.

[10] Cagnacci A, Venier M. The Controversial History of Hormone Replacement Therapy[J]. Medicina (Kaunas), 2019, 55(9):602.

[11] Howard JA, Hart KN, Thompson TB. Molecular Mechanisms of AMH Signalling[J]. Front Endocrinol (Lausanne), 2022,13:927824.

[12] Buratini J, Dellaqua TT, Dal Canto M, et al. The putative roles of FSH and AMH in the regulation of oocyte developmental competence: from fertility prognosis to mechanisms underlying age-related subfertility[J]. Hum Reprod Update, 2022, 28(2):232-254. 

[13] Shrikhande L, Shrikhande B, Shrikhande A. AMH and Its Clinical Implications[J]. J Obstet Gynaecol India, 2020,70(5):337-341.

[14] Lv PP, Jin M, Rao JP, et al. Role of anti-Müllerian hormone and testosterone in follicular growth: a cross-sectional study[J]. BMC Endocr Disord, 2020, 20(1):101. 

[15] Moolhuijsen LME, Visser JA. Anti-Müllerian Hormone and Ovarian Reserve: Update on Assessing Ovarian Function[J]. J Clin Endocrinol Metab, 2020, 105(11):3361–3373. 

[16] Cedars MI. Evaluation of Female Fertility-AMH and Ovarian Reserve Testing[J]. J Clin Endocrinol Metab, 2022,107(6):1510-1519.

[17] Danis RB, Sriprasert I, Ho JR, et al. Association of bioavailable inhibin B and oocyte yield in controlled ovarian stimulation[J]. F S Rep, 2021, 2(2):189-194.

[18] Tang Y, Li Y. Evaluation of Serum AMH, INHB Combined with Basic FSH on Ovarian Reserve Function after Laparoscopic Ovarian Endometriosis Cystectomy[J]. Front Surg, 2022, 9:906020. 

[19] Wen J, Huang K, Du X, et al. Can Inhibin B Reflect Ovarian Reserve of Healthy Reproductive Age Women Effectively[J]. Front Endocrinol (Lausanne), 2021, 12:626534.  

[20] A-Ting Z, LIU Yun L. Mechanism of inhibin B involved in follicular dominance[J]. Journal of Reproductive Medicine, 2020, 29(08):1105-1109.

[21] Adams GP, Ratto MH. Ovulation-inducing factor in seminal plasma: a review[J]. Anim Reprod Sci, 2013, 136(3):148-156.

[22] Cai L, Zong DK, Tong GQ, et al. Apoptotic mechanism of premature ovarian failure and rescue effect of Traditional Chinese Medicine: a review[J]. J Tradit Chin Med, 2021,41(3):492-498.

[23] Matsuda F, Inoue N, Manabe N, et al. Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells[J]. J Reprod Dev, 2012;58(1):44-50.

[24] Yoon SY, Yoon JA, Park M, et al. Recovery of ovarian function by human embryonic stem cell-derived mesenchymal stem cells in cisplatin-induced premature ovarian failure in mice[J]. Stem Cell Res Ther, 2020,11(1):255.

[25] Zhang J, Yin H, Jiang H, et al. The protective effects of human umbilical cord mesenchymal stem cell-derived extracellular vesicles on cisplatin-damaged granulosa cells[J]. Taiwan J Obstet Gynecol, 2020, 59(4):527-533.

[26] Liang X, Yan Z, Ma W, et al. Peroxiredoxin 4 protects against ovarian ageing by ameliorating D-galactose-induced oxidative damage in mice[J]. Cell Death Dis, 2020,11(12):1053.

[27] Shi L, Zhang Z, Deng M,et al. Biological mechanisms and applied prospects of mesenchymal stem cells in premature ovarian failure[J]. Medicine (Baltimore), 2022,101(32):e30013.

[28] Yiwen Q, Lu G, Bin L. (2021) Role and mechanism of amino acid metabolism in premature ovarian failure [J]. Geriatrics and Health Care, 2021, 27(04):880-883.

[29] Lin L, Gao W, Chen Y, et al. Reactive oxygen species-induced SIAH1 promotes granulosa cells' senescence in premature ovarian failure[J]. J Cell Mol Med, 2022, 26(8):2417-2427. Epub 2022 Mar 9.

[30] Greene J, Segaran A, Lord S. Targeting OXPHOS and the electron transport chain in cancer; Molecular and therapeutic implications. Semin Cancer Biol, 2022, 86(2):851-859.

[31] Turton N, Cufflin N, Dewsbury M,et al. The Biochemical Assessment of Mitochondrial Respiratory Chain Disorders[J]. Int J Mol Sci, 2022, 23(13):7487.

[32] Scarpulla RC. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network [J]. Biochim Biophys Acta, 2011, 1813(7):1269-1278.

[33] He F, Jin JQ, Qin QQ, et al. Resistin Regulates Fatty Acid Β Oxidation by Suppressing Expression of Peroxisome Proliferator Activator Receptor Gamma-Coactivator 1α (PGC-1α)[J]. Cell Physiol Biochem, 2018;46(5):2165-2172. 

[34] Wang L, Tang J, Wang L, et al. Oxidative stress in oocyte aging and female reproduction[J]. J Cell Physiol, 2021,236(12):7966-7983.

[35] Kirillova A, Smitz JEJ, Sukhikh GT, et al. The Role of Mitochondria in Oocyte Maturation[J]. Cells, 2021,10(9):2484. 

[36] Fukai T, Ushio-Fukai M. Superoxide dismutases: role in redox signaling, vascular function, and diseases [J]. Antioxid Redox Signal, 2011,15(6):1583-1606.

[37] Fernandez-Marcos PJ, Nóbrega-Pereira S. NADPH: new oxygen for the ROS theory of aging[J]. Oncotarget, 2016,7(32):50814-50815.

[38] Jelic MD, Mandic AD, Maricic SM, et al. Oxidative stress and its role in cancer[J]. J Cancer Res Ther, 2021,17(1):22-28.

[39] Su LJ, Zhang JH, Gomez H, et al. Reactive Oxygen Species-Induced Lipid Peroxidation in Apoptosis, Autophagy, and Ferroptosis[J]. Oxid Med Cell Longev,2019:5080843.

[40] Guerra-Castellano A, Díaz-Quintana A, Pérez-Mejías G, et al. Oxidative stress is tightly regulated by cytochrome c phosphorylation and respirasome factors in mitochondria[J]. Proc Natl Acad Sci U S A, 2018,115(31):7955-7960.

[41] Pietraforte D, Paulicelli E, Patrono C, et al. Protein oxidative damage and redox imbalance induced by ionising radiation in CHO cells[J]. Free Radic Res, 2018,52(4):465-479. 

[42] Zhao M, Wang Y, Li L, et al. Mitochondrial ROS promote mitochondrial dysfunction and inflammation in ischemic acute kidney injury by disrupting TFAM-mediated mtDNA maintenance[J]. Theranostics, 2021,11(4):1845-1863.

[43] Kirkinezos IG, Moraes CT. Reactive oxygen species and mitochondrial diseases[J]. Semin Cell Dev Biol, 2001,12(6):449-457. 

[44] Gao X, Yu X, Zhang C, et al. Telomeres and Mitochondrial Metabolism: Implications for Cellular Senescence and Age-related Diseases. Stem Cell Rev Rep, 2022 ,(7):2315-2327.

[45] Toupance S, Fattet AJ, Thornton SN,et al. Ovarian Telomerase and Female Fertility[J]. Biomedicines, 2021,9(7):842.

[46] Wang L, Lu Z, Zhao J, et al. Selective oxidative stress induces dual damage to telomeres and mitochondria in human T cells[J]. Aging Cell, 2021,20(12):e13513. 

[47] Michishita E, McCord RA, Berber E, et al. SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin[J]. Nature, 2008;452(7186):492-496.

[48] Liao CY, Kennedy BK. SIRT6, oxidative stress, and aging[J]. Cell Res, 2016, 26(2):143-144. 

[49] Lin J, Epel E. Stress and telomere shortening: Insights from cellular mechanisms[J]. Ageing Res Rev, 2022,73:101507.

[50] Scarpulla RC. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network [J]. Biochim Biophys Acta, 2011;1813(7):1269-1278.

[51] Schank M, Zhao J, Wang L,et al. Telomeric injury by KML001 in human T cells induces mitochondrial dysfunction through the p53-PGC-1α pathway[J]. Cell Death Dis, 2020,11(12):1030. 

[52] Ranran M, Huihui Z, Ze Y, et al. (2023) Progress on the mechanism of Psyllium and its extracts in the treatment of premature ovarian failure[J]. Global Chinese Medicine, 2023,16(02):348-353.

[53] Grossmann B, Saur S, Rall K, et al. Prevalence of autoimmune disease in women with premature ovarian failure[J]. Eur J Contracept Reprod Health Care, 2020,25(1):72-75. 

[54] Vogt EC, Breivik L, Røyrvik EC, et al. Primary Ovarian Insufficiency in Women With Addison's Disease [J]. J Clin Endocrinol Metab, 2021,106(7):e2656-e2663.

[55] Szeliga A, Calik-Ksepka A, Maciejewska-Jeske M, et al. Autoimmune Diseases in Patients with Premature Ovarian Insufficiency-Our Current State of Knowledge[J]. Int J Mol Sci, 2021,22(5):2594.

[56] Collins G, Patel B, Thakore S, et al. Primary Ovarian Insufficiency: Current Concepts[J]. South Med J, 2017,110(3):147-153.

[57] Bousounis P, Bergo V, Trompouki E. Inflammation, Aging and Hematopoiesis: A Complex Relationship [J]. Cells, 2021,10(6):1386.

[58] Hayden MS, Ghosh S. NF-κB, the first quarter-century: remarkable progress and outstanding questions [J]. Genes Dev, 2012,26(3):203-234.

[59] Birch J, Gil J. Senescence and the SASP: many therapeutic avenues[J]. Genes Dev, 2020,34(23-24):1565-1576.

[60] Lu X, Cui J, Cui L, et al. The effects of human umbilical cord-derived mesenchymal stem cell transplantation on endometrial receptivity are associated with Th1/Th2 balance change and uNK cell expression of uterine in autoimmune premature ovarian failure mice[J]. Stem Cell Res Ther, 2019, 10(1): 214.

[61] Kirshenbaum M, Orvieto R. Premature ovarian insufficiency (POI) and autoimmunity-an update appraisal [J]. J Assist Reprod Genet, 2019,36(11):2207-2215.

[62] Han Y, Yao R, Yang Z, et al. Interleukin-4 activates the PI3K/AKT signaling to promote apoptosis and inhibit the proliferation of granulosa cells[J]. Exp Cell Res, 2022,412(1):113002.

[63] Noël L, Fransolet M, Jacobs N, et al. A paracrine interaction between granulosa cells and leukocytes in the preovulatory follicle causes the increase in follicular G-CSF levels[J]. J Assist Reprod Genet, 2020, 37(2):405-416.

[64] Lei Z. Clinical study on the treatment of patients with early-onset ovarian insufficiency with Zi Kidney Tim Kui Cream Formula based on the changes of immune factors [D]. Xinjiang Medical University, 2021(09).

[65] Ebrahimi M, Akbari Asbagh F. The role of autoimmunity in premature ovarian failure[J]. Iran J Reprod Med, 2015,13(8):461-472.

[66] Hiew LF, Poon CH, You HZ, et al. TGF-β/Smad Signalling in Neurogenesis: Implications for Neuropsychiatric Diseases[J]. Cells, 2021,10(6):1382.

[67] Xueling L, Chunyan H, Gang L, et al. (2021) Recent advances in the pathogenesis of POF and related therapeutic mechanisms[J]. Journal of Jiangsu University (Medical Edition), 31(06):541-548.

[68] Huang B, Lu J, Ding C, et al. Exosomes derived from human adipose mesenchymal stem cells improve ovary function of premature ovarian insufficiency by targeting SMAD[J]. Stem Cell Res Ther, 2018,9(1):216. 

[69] Weiqing Z, Xia L, Li L, et al. Effects of kidney tonifying and menstruation regulating formula on sex hormones, ovarian morphology and TGF-β-1/smad pathway in rats with PCOS model[J]. Modern Journal of Integrative Chinese and Western Medicine, 2020,29(20):2188-2193.

[70] Chiu HC, Li CJ, Yiang GT, et al. Epithelial to Mesenchymal Transition and Cell Biology of Molecular Regulation in Endometrial Carcinogenesis [J]. J Clin Med, 2019,8(4):439.

[71] Glaviano A, Foo ASC, Lam HY, et al. PI3K/AKT/mTOR signaling transduction pathway and targeted therapies in cancer. Mol Cancer. 2023;22(1):138.

[72] Savova MS, Mihaylova LV, Tews D, Wabitsch M, Georgiev MI. Targeting PI3K/AKT signaling pathway in obesity. Biomed Pharmacother. 2023;159:114244.

[73] Yao W, Pan Z, Du X, et al. NORHA, a novel follicular atresia-related lncRNA, promotes porcine granulosa cell apoptosis via the miR-183-96-182 cluster and FoxO1 axis[J]. J Anim Sci Biotechnol, 2021, 12(1):103.

[74] Liu M, Qiu Y, Xue Z, et al. Small extracellular vesicles derived from embryonic stem cells restore ovarian function of premature ovarian failure through PI3K/AKT signaling pathway[J]. Stem Cell Res Ther, 2020, 11(1):3.

[75] Wang S, Lin S, Zhu M, et al. Acupuncture Reduces Apoptosis of Granulosa Cells in Rats with Premature Ovarian Failure Via Restoring the PI3K/Akt Signaling Pathway[J]. Int J Mol Sci, 2019, 20(24): 6311.

[76] Huilan F, Huiping L, Shanshan H, et al. (2019) Research progress on the role of Wnt signaling pathway in the pathogenesis of POF[J]. Hunan Journal of Traditional Chinese Medicine, 2019,35(05):183-185.

[77] Liu J, Xiao Q, Xiao J, et al. Wnt/β-catenin signalling: function, biological mechanisms, and therapeutic opportunities[J]. Signal Transduct Target Ther, 2022,7(1):3.PMID: 34980884

[78] Chen C, Li S, Hu C, Cao W, et al. Protective Effects of Puerarin on Premature Ovarian Failure via Regulation of Wnt/β-catenin Signaling Pathway and Oxidative Stress[J]. Reprod Sci. 2021,8(4):982-990.

[79] YingYing Z, Zhouheng Y, Xin L,et al. Mechanism of SIRT3 in cardiac aging[J]. Chemistry of Life, 2023, 43(02):215-220.

[80] van de Ven RAH, Santos D, Haigis MC. Mitochondrial Sirtuins and Molecular Mechanisms of Aging[J]. Trends Mol Med, 2017,23(4):320-331.

[81] Ji Z, Liu GH, Qu J. Mitochondrial sirtuins, metabolism, and aging. J Genet Genomics, 2022, (4):287-298.

[82] Pollard CL, Gibb Z, Swegen A, et al. NAD+, Sirtuins and PARPs: enhancing oocyte developmental competence [J]. J Reprod Dev, 2022,68(6):345-354. 

[83] Xiu Z, Tang S, Kong P, et al. Zigui-Yichong-Fang protects against cyclophosphamide-induced premature ovarian insufficiency via the SIRT1/Foxo3a pathway. J Ethnopharmacol, 2023, 314:116608.

[84] Cuili W. Mechanism of SIRT6/NF-κB signaling pathway in POF mouse model [D]. Dali University, 2020.

[85] Zhang Y, Yan Z, Qin Q, et al. Transcriptome Landscape of Human Folliculogenesis Reveals Oocyte and Granulosa Cell Interactions[J]. Mol Cell, 2018 ,72(6):1021-1034.

[86] Yunjiao X, Wendi W, Zhibi Z, et al.  Exploration of key protective factors of stress ulcers in rats based on P13K/AKt and NF-kB signaling pathways[J]. Yunnan Journal of Traditional Chinese Medicine, 2021, 42(06):79-83.

[87] Viuff M, Gravholt CH. Turner Syndrome and Fertility[J]. Ann Endocrinol (Paris), 2022,83(4):244-249.

[88] Barros F, Carvalho F, Barros A, et al. Premature ovarian insufficiency: clinical orientations for genetic testing and genetic counseling[J]. Porto Biomed J, 2020,5(3):e62.

[89] Huang AC, Olson SB, Maslen CL. A Review of Recent Developments in Turner Syndrome Research [J]. J Cardiovasc Dev Dis, 2021,8(11):138. PMID: 34821691

[90] Yoon SH, Kim GY, Choi GT,et al. Organ Abnormalities Caused by Turner Syndrome. Cells, 2023, 12(10):1365.

[91] Hagerman PJ, Hagerman R. Fragile X syndrome[J]. Curr Biol, 2021,31(6):R273-R275. 

[92] Lu C, Lin L, Tan H, et al. Fragile X premutation RNA is sufficient to cause primary ovarian insufficiency in mice[J]. Hum Mol Genet, 2012,21(23):5039-5047.

[93] Shelly KE, Candelaria NR, Li Z, et al. Ectopic expression of CGG-repeats alters ovarian response to gonadotropins and leads to infertility in a murine FMR1 premutation model[J]. Hum Mol Genet, 2021, 30(10):923-938. 

[94] Kumar R, Alwani M, Kosta S, et al. (2017) BMP15 and GDF9 Gene Mutations in Premature Ovarian Failure[J]. J Reprod Infertil, 2017,18(1):185-189. 

[95] Ferrarini E, De Marco G, Orsolini F, et al. Characterization of a novel mutation V136L in bone morphogenetic protein 15 identified in a woman affected by POI[J]. J Ovarian Res, 2021,14(1):85. 

[96] Gao M, Yu Z, Yao D, et al. Mesenchymal stem cells therapy: A promising method for the treatment of uterine scars and premature ovarian failure [J]. Tissue Cell, 2022,74:101676.

[97] Nouri N, Shareghi-Oskoue O, Aghebati-Maleki L, et al. Role of miRNAs interference on ovarian functions and premature ovarian failure [J]. Cell Commun Signal, 2022,20(1):198.

[98] Xiaoyan W. Study on the role of epigenetic regulation involved in long noncoding RNAs in early-onset ovarian insufficiency [D]. Shandong University, 2020.

[99] Wang X, Zhang X, Dang Y, et al. Long noncoding RNA HCP5 participates in premature ovarian insufficiency by transcriptionally regulating MSH5 and DNA damage repair via YB1[J]. Nucleic Acids Res, 2020,48(8):4480-4491.

[100] Zhou XY, Li Y, Zhang J, Liu YD, et al. Expression profiles of circular RNA in granulosa cells from women with biochemical premature ovarian insufficiency[J]. Epigenomics, 2020,12(4):319-332.

[101] Yan Z, Dai Y, Fu H, et al. Curcumin exerts a protective effect against premature ovarian failure in mice[J]. J Mol Endocrinol, 2018,60(3):261-271.

[102] Derks B, Rivera-Cruz G, Hagen-Lillevik S, et al. The hypergonadotropic hypogonadism conundrum of classic galactosemia [J]. Hum Reprod Update, 2023, 29(2):246-258.

[103] Pan P, Zheng L, Huang J, et al. Endocrine profiles and cycle characteristics of infertile 17α-hydroxylase/17,20-lyase Deficiency Patients undergoing assisted Reproduction Treatment: a retrospective cohort study [J]. Ovarian Res, 2023, 16(1):111.