An overview of different methods to establish a murine premature ovarian failure model

Negar Pouladvand , Mahnaz Azarnia , Hadis Zeinali , Rouhollah Fathi , Somayeh Tavana

Animal Models and Experimental Medicine ›› 2024, Vol. 7 ›› Issue (6) : 835 -852.

PDF (3127KB)
Animal Models and Experimental Medicine ›› 2024, Vol. 7 ›› Issue (6) : 835 -852. DOI: 10.1002/ame2.12477
REVIEW

An overview of different methods to establish a murine premature ovarian failure model

Author information +
History +
PDF (3127KB)

Abstract

Premature ovarian failure (POF)is defined as the loss of normal ovarian function before the age of 40 and is characterized by increased gonadotropin levels and decreased estradiol levels and ovarian reserve, often leading to infertility. The incomplete understanding of the pathogenesis of POF is a major impediment to the development of effective treatments for this disease, so the use of animal models is a promising option for investigating and identifying the molecular mechanisms involved in POF patients and developing therapeutic agents. As mice and rats are the most commonly used models in animal research, this review article considers studies that used murine POF models. In this review based on the most recent studies, first, we introduce 10 different methods for inducing murine POF models, then we demonstrate the advantages and disadvantages of each one, and finally, we suggest the most practical method for inducing a POF model in these animals. This may help researchers find the method of creating a POF model that is most appropriate for their type of study and suits the purpose of their research.

Keywords

animal model / chemotherapy drugs / mouse / ovarian damage / ovarian reserve / premature

Cite this article

Download citation ▾
Negar Pouladvand, Mahnaz Azarnia, Hadis Zeinali, Rouhollah Fathi, Somayeh Tavana. An overview of different methods to establish a murine premature ovarian failure model. Animal Models and Experimental Medicine, 2024, 7(6): 835-852 DOI:10.1002/ame2.12477

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Pastore LM, Christianson MS, Stelling J, Kearns WG, Segars JH. Reproductive ovarian testing and the alphabet soup of diagnoses: DOR, POI, POF, POR, and FOR. J Assist Reprod Genet. 2018;35(1):17-23.

[2]

Coulam CB. Premature gonadal failure. Fertil Steril. 1982;38(6):645-655.

[3]

Vujovic S, Brincat M, Erel T, et al. EMAS position statement: managing women with premature ovarian failure. Maturitas. 2010;67(1):91-93.

[4]

Abdelzaher WY, Abdel-Hafez SMN, Rofaeil RR, Ali A, Hegazy A, Bahaa HA. The protective effect of fenofibrate, triptorelin, and their combination against premature ovarian failure in rats. Naunyn Schmiedeberg’s Arch Pharmacol. 2021;394(1):137-149.

[5]

Podfigurna-Stopa A, Czyzyk A, Grymowicz M, et al. Premature ovarian insufficiency: the context of long-term effects. J Endocrinol Investig. 2016;39(9):983-990.

[6]

Elkady MA, Shalaby S, Fathi F, El-Mandouh S. Effects of quercetin and rosuvastatin each alone or in combination on cyclophosphamide-induced premature ovarian failure in female albino mice. Hum Exp Toxicol. 2019;38(11):1283-1295.

[7]

Wang XF, Zhang L, Wu QH, Min JX, Ma N, Luo LC. Biological mechanisms of premature ovarian failure caused by psychological stress based on support vector regression. Int J Clin Exp Med. 2015;8(11):21393-21399.

[8]

Pouresmaeili F, Fazeli Z. Premature ovarian failure: a critical condition in the reproductive potential with various genetic causes. Int J Fertil Steril. 2014;8(1):1-12.

[9]

Yang DM, Zhang JQ, Fei YF. Lycium barbarum polysaccharide attenuates chemotherapy-induced ovarian injury by reducing oxidative stress. J Obstet Gynaecol Res. 2017;43(10):1621-1628.

[10]

Abdel-Aziz AM, Mohamed ASM, Abdelazem O, Okasha AMM, Kamel MY. Cilostazol protects against cyclophosphamide-induced ovarian toxicity in female rats: role of cAMP and HO-1. Toxicol Mech Methods. 2020;30(7):526-535.

[11]

Okada K, Fujisawa M. Recovery of spermatogenesis following cancer treatment with cytotoxic chemotherapy and radiotherapy. The world. J Mens Health. 2019;37(2):166-174.

[12]

Bedoschi G, Navarro PA, Oktay K. Chemotherapy-induced damage to ovary: mechanisms and clinical impact. Future Oncol. 2016;12(20):2333-2344.

[13]

Kim S, Kim SW, Han SJ, et al. Molecular mechanism and prevention strategy of chemotherapy-and radiotherapy-induced ovarian damage. Int J Mol Sci. 2021;22(14):7484.

[14]

Di Giacomo M, Barchi M, Baudat F, Edelmann W, Keeney S, Jasin M. Distinct DNA-damage-dependent and -independent responses drive the loss of oocytes in recombination-defective mouse mutants. Proc Natl Acad Sci USA. 2005;102(3):737-742.

[15]

Perez GI, Acton BM, Jurisicova A, et al. Genetic variance modifies apoptosis susceptibility in mature oocytes via alterations in DNA repair capacity and mitochondrial ultrastructure. Cell Death Differ. 2007;14(3):524-533.

[16]

Spears N, Lopes F, Stefansdottir A, et al. Ovarian damage from chemotherapy and current approaches to its protection. Hum Reprod Update. 2019;25(6):673-693.

[17]

Akyol S, Gulec MA, Erdemli HK, Akyol O. Can propolis and caffeic acid phenethyl ester be promising agents against cyclophosphamide toxicity? J Intercult Ethnopharmacol. 2016;5(1):105-107.

[18]

Barberino RS, Silva RLS, Palheta Junior RC, Smitz JE, Matos MHT. Protective effects of antioxidants on cyclophosphamide-induced ovarian toxicity. Biopreserv Biobank. 2023;21(2):121-141.

[19]

Overbeek A, van den Berg MH, van Leeuwen FE, Kaspers GJ, Lambalk CB, van Dulmen-den BE. Chemotherapy-related late adverse effects on ovarian function in female survivors of childhood and young adult cancer: a systematic review. Cancer Treat Rev. 2017;53:10-24.

[20]

Piasecka-Srader J, Blanco FF, Delman DH, et al. Tamoxifen prevents apoptosis and follicle loss from cyclophosphamide in cultured rat Ovaries1. Biol Reprod. 2015;92(5):132.

[21]

Hassanpour A, Yousefian S, Askaripour M, Sharififar F, Ezzatabadipour M. Ovarian protection in cyclophosphamide-treated mice by fennel. Toxicol Rep. 2017;4:160-164.

[22]

Mobasher MA, Hassen MT, Ebiya RA, et al. Ameliorative effect of citrus lemon Peel extract and resveratrol on premature ovarian failure rat model: role of iNOS/Caspase-3 pathway. Molecules. 2022;28(1):122.

[23]

Zheng S, Ma M, Chen Y, Li M. Effects of quercetin on ovarian function and regulation of the ovarian PI3K/Akt/FoxO3a signalling pathway and oxidative stress in a rat model of cyclophosphamide-induced premature ovarian failure. Basic Clin Pharmacol Toxicol. 2022;130(2):240-253.

[24]

Huang CC, Chou CH, Yang YS, et al. Metformin: a novel promising option for fertility preservation during cyclophosphamide-based chemotherapy. Mol Hum Reprod. 2021;27(1):gaaa084.

[25]

Petrillo SK, Desmeules P, Truong TQ, Devine PJ. Detection of DNA damage in oocytes of small ovarian follicles following phosphoramide mustard exposures of cultured rodent ovaries in vitro. Toxicol Appl Pharmacol. 2011;253(2):94-102.

[26]

Nguyen Q-N, Zerafa N, Liew SH, et al. Loss of PUMA protects the ovarian reserve during DNA-damaging chemotherapy and preserves fertility. Cell Death Dis. 2018;9(6):618.

[27]

Bellusci G, Mattiello L, Iannizzotto V, et al. Kinase-independent inhibition of cyclophosphamide-induced pathways protects the ovarian reserve and prolongs fertility. Cell Death Dis. 2019;10(10):726.

[28]

Luan Y, Edmonds ME, Woodruff TK, Kim SY. Inhibitors of apoptosis protect the ovarian reserve from cyclophosphamide. J Endocrinol. 2019;240(2):243-256.

[29]

Mattiello L, Pucci G, Marchetti F, Diederich M, Gonfloni S. Asciminib mitigates DNA damage stress signaling induced by cyclophosphamide in the ovary. Int J Mol Sci. 2021;22(3):1395.

[30]

Kurita T, Cunha GR, Robboy SJ, Mills AA, Medina RT. Differential expression of p63 isoforms in female reproductive organs. Mech Dev. 2005;122(9):1043-1055.

[31]

Suh EK, Yang A, Kettenbach A, et al. p63 protects the female germ line during meiotic arrest. Nature. 2006;444(7119):624-628.

[32]

Wang XQ, Redpath JL, Fan ST, Stanbridge EJ. ATR dependent activation of Chk2. J Cell Physiol. 2006;208(3):613-619.

[33]

Kerr JB, Hutt KJ, Michalak EM, et al. DNA damage-induced primordial follicle oocyte apoptosis and loss of fertility require TAp63-mediated induction of Puma and Noxa. Mol Cell. 2012;48(3):343-352.

[34]

Emori C, Boucher Z, Bolcun-Filas E. CHEK2 signaling is the key regulator of oocyte survival after chemotherapy. Sci Adv. 2023;9(42):eadg0898.

[35]

Bolcun-Filas E, Rinaldi VD, White ME, Schimenti JC. Reversal of female infertility by Chk2 ablation reveals the oocyte DNA damage checkpoint pathway. Science. 2014;343(6170):533-536.

[36]

Pascuali N, Scotti L, Di Pietro M, et al. Ceramide-1-phosphate has protective properties against cyclophosphamide-induced ovarian damage in a mice model of premature ovarian failure. Hum Reprod. 2018;33(5):844-859.

[37]

Zhang B-f, Hu Y, Liu X, et al. The role of AKT and FOXO3 in preventing ovarian toxicity induced by cyclophosphamide. PLoS One. 2018;13(8):e0201136.

[38]

Feng J, Ma WW, Li HX, et al. Melatonin prevents cyclophosphamide-induced primordial follicle loss by inhibiting ovarian granulosa cell apoptosis and maintaining AMH expression. Front Endocrinol (Lausanne). 2022;13:895095.

[39]

Barekati Z, Golkar-Narenji A, Totonchi M, Radpour R, Gourabi H. Effects of amifostine in combination with cyclophosphamide on female reproductive system. Reprod Sci. 2012;19(5):539-546.

[40]

Liu X, Song Y, Zhou F, et al. Network and experimental pharmacology on mechanism of Si-Wu-tang improving ovarian function in a mouse model of premature ovarian failure induced by cyclophosphamide. J Ethnopharmacol. 2023;301:115842.

[41]

Çağlı F, Baktır MA, Dolanbay M, et al. An evaluation of the effects on the ovaries of hyperbaric oxygen therapy in a rat model of premature ovarian failure created with cyclophosphamide. Turk J Obstet Gynecol. 2023;20(1):46-52.

[42]

Kalich-Philosoph L, Roness H, Carmely A, et al. Cyclophosphamide triggers follicle activation and “burnout”; AS101 prevents follicle loss and preserves fertility. Sci Transl Med. 2013;5(185):185ra62.

[43]

Li J, Long H, Cong Y, et al. Quercetin prevents primordial follicle loss via suppression of PI3K/Akt/Foxo3a pathway activation in cyclophosphamide-treated mice. Reprod Biol Endocrinol. 2021;19(1):63.

[44]

Goldman KN, Chenette D, Arju R, et al. mTORC1/2 inhibition preserves ovarian function and fertility during genotoxic chemotherapy. Proc Natl Acad Sci USA. 2017;114(12):3186-3191.

[45]

Zhou L, Xie Y, Li S, et al. Rapamycin prevents cyclophosphamide-induced over-activation of primordial follicle pool through PI3K/Akt/mTOR signaling pathway in vivo. J Ovarian Res. 2017;10(1):56.

[46]

Jeelani R, Khan SN, Shaeib F, et al. Cyclophosphamide and acrolein induced oxidative stress leading to deterioration of metaphase II mouse oocyte quality. Free Radic Biol Med. 2017;110:11-18.

[47]

Melekoglu R, Ciftci O, Eraslan S, Cetin A, Basak N. Beneficial effects of curcumin and capsaicin on cyclophosphamide-induced premature ovarian failure in a rat model. J Ovarian Res. 2018;11(1):33.

[48]

Li S, Liu M, Ma H, et al. Ameliorative effect of recombinant human lactoferrin on the premature ovarian failure in rats after cyclophosphamide treatments. J Ovarian Res. 2021;14(1):17.

[49]

Hamzeh M, Hosseinimehr SJ, Mohammadi HR, Yaghubi Beklar S, Dashti A, Talebpour AF. Atorvastatin attenuates the ovarian damage induced by cyclophosphamide in rat: an experimental study. Int J Reprod Biomed. 2018;16(5):323-334.

[50]

Khedr NF. Protective effect of mirtazapine and hesperidin on cyclophosphamide-induced oxidative damage and infertility in rat ovaries. Exp Biol Med (Maywood). 2015;240(12):1682-1689.

[51]

Yener NA, Sinanoglu O, Ilter E, et al. Effects of spirulina on cyclophosphamide-induced ovarian toxicity in rats: biochemical and histomorphometric evaluation of the ovary. Biochem Res Int. 2013;2013:764262.

[52]

Elsenosi Y, Aziza S, Hussein A, Mohsen AA, Elnahas K. Curcumin and/or hesperidin alleviates oxidative stress and hormonal alterations in a rat model of cyclophosphamide-induced premature ovarian failure. Benha Vet Med J. 2020;39:95-100.

[53]

Wang S, Sun M, Yu L, Wang Y, Yao Y, Wang D. Niacin inhibits apoptosis and rescues premature ovarian failure. Cell Physiol Biochem. 2018;50(6):2060-2070.

[54]

Di Emidio G, Rossi G, Bonomo I, et al. The natural carotenoid crocetin and the synthetic tellurium compound AS101 protect the ovary against cyclophosphamide by modulating SIRT1 and mitochondrial markers. Oxidative Med Cell Longev. 2017;2017:8928604.

[55]

Salminen A, Kaarniranta K, Kauppinen A. Crosstalk between oxidative stress and SIRT1: impact on the aging process. Int J Mol Sci. 2013;14(2):3834-3859.

[56]

Zhang M, Yu X, Li D, et al. Nrf2 signaling pathway mediates the protective effects of daphnetin against D-galactose induced-premature ovarian failure. Front Pharmacol. 2022;13:810524.

[57]

Ma M, Chen XY, Li B, Li XT. Melatonin protects premature ovarian insufficiency induced by tripterygium glycosides: role of SIRT1. Am J Transl Res. 2017;9(4):1580-1602.

[58]

Ma P, Xiao H, Yu C, et al. Enhanced cisplatin chemotherapy by iron oxide nanocarrier-mediated generation of highly toxic reactive oxygen species. Nano Lett. 2017;17(2):928-937.

[59]

Wang Q, Hutt KJ. Evaluation of mitochondria in mouse oocytes following cisplatin exposure. J Ovarian Res. 2021;14(1):65.

[60]

Kelland L. The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer. 2007;7:573-584.

[61]

Gonfloni S, Tella L, Caldarola S, et al. Inhibition of the c-Abl-TAp63 pathway protects mouse oocytes from chemotherapy-induced death. Nat Med. 2009;15:1179-1185.

[62]

Kim SY, Cordeiro MH, Serna VA, et al. Rescue of platinum-damaged oocytes from programmed cell death through inactivation of the p53 family signaling network. Cell Death Dis. 2013;20(8):987-997.

[63]

Gürsoy A, Sade AG. Effects of diosmin administration on cisplatin-induced premature ovarian failure in a rat model. J Contemp Med. 2022;12:912-916.

[64]

Barberino RS, Menezes VG, Ribeiro A, et al. Melatonin protects against cisplatin-induced ovarian damage in mice via the MT1 receptor and antioxidant activity. Biol Reprod. 2017;96(6):1244-1255.

[65]

Damia G, Filiberti L, Vikhanskaya F, et al. Cisplatinum and taxol induce different patterns of p53 phosphorylation. Neoplasia. 2001;3(1):10-16.

[66]

Tuppi M, Kehrloesser S, Coutandin DW, et al. Oocyte DNA damage quality control requires consecutive interplay of CHK2 and CK1 to activate p63. Nat Struct Mol Biol. 2018;25(3):261-269.

[67]

Chang EM, Lim E, Yoon S, et al. Cisplatin induces overactivation of the dormant primordial follicle through PTEN/AKT/FOXO3a pathway which leads to loss of ovarian reserve in mice. PLoS One. 2015;10(12):e0144245.

[68]

Yucebilgin MS, Terek MC, Ozsaran A, et al. Effect of chemotherapy on primordial follicular reserve of rat: an animal model of premature ovarian failure and infertility. Aust NZ J Obstet Gynaecol. 2004;44(1):6-9.

[69]

Jang H, Na Y, Hong K, et al. Synergistic effect of melatonin and ghrelin in preventing cisplatin-induced ovarian damage via regulation of FOXO3a phosphorylation and binding to the p27(Kip1) promoter in primordial follicles. J Pineal Res. 2017;63(3):e12432.

[70]

Eldani M, Luan Y, Xu PC, Bargar T, Kim SY. Continuous treatment with cisplatin induces the oocyte death of primordial follicles without activation. FASEB J. 2020;34(10):13885-13899.

[71]

Altuner D, Gulaboglu M, Yapca OE, Cetin N. The effect of mirtazapine on cisplatin-induced oxidative damage and infertility in rat ovaries. Sci World J. 2013;2013:327240.

[72]

Morgan S, Lopes F, Gourley C, Anderson RA, Spears N. Cisplatin and doxorubicin induce distinct mechanisms of ovarian follicle loss; imatinib provides selective protection only against cisplatin. PLoS One. 2013;8(7):e70117.

[73]

Rawat PS, Jaiswal A, Khurana A, Bhatti JS, Navik U. Doxorubicin-induced cardiotoxicity: an update on the molecular mechanism and novel therapeutic strategies for effective management. Biomed Pharmacother. 2021;139:111708.

[74]

Renu K, Pureti LP, Vellingiri B, Valsala GA. Toxic effects and molecular mechanism of doxorubicin on different organs – an update. Toxin Rev. 2022;41(2):650-674.

[75]

Tokarska-Schlattner M, Zaugg M, Zuppinger C, Wallimann T, Schlattner U. New insights into doxorubicin-induced cardiotoxicity: the critical role of cellular energetics. J Mol Cell Cardiol. 2006;41(3):389-405.

[76]

Clementi ME, Giardina B, Di Stasio E, Mordente A, Misiti F. Doxorubicin-derived metabolites induce release of cytochrome C and inhibition of respiration on cardiac isolated mitochondria. Anticancer Res. 2003;23(3b):2445-2450.

[77]

Thorn CF, Oshiro C, Marsh S, et al. Doxorubicin pathways: pharmacodynamics and adverse effects. Pharmacogenet Genomics. 2011;21(7):440-446.

[78]

Xiao S, Zhang J, Liu M, Iwahata H, Rogers HB, Woodruff TK. Doxorubicin has dose-dependent toxicity on mouse ovarian follicle development, hormone secretion, and oocyte maturation. Toxicol Sci. 2017;157(2):320-329.

[79]

Roti Roti EC, Leisman SK, Abbott DH, Salih SM. Acute doxorubicin insult in the mouse ovary is cell-and follicle-type dependent. PLoS One. 2012;7(8):e42293.

[80]

Perez GI, Knudson CM, Leykin L, Korsmeyer SJ, Tilly JL. Apoptosis-associated signaling pathways are required for chemotherapy-mediated female germ cell destruction. Nat Med. 1997;3(11):1228-1232.

[81]

Ben-Aharon I, Bar-Joseph H, Tzarfaty G, et al. Doxorubicin-induced ovarian toxicity. Reprod Biol Endocrinol. 2010;8(1):20.

[82]

Zhang T, He WH, Feng LL, Huang HG. Effect of doxorubicin-induced ovarian toxicity on mouse ovarian granulosa cells. Regul Toxicol Pharmacol. 2017;86:1-10.

[83]

Ben-Aharon I, Bar-Yosef H, Rizel S, Sulkes A, Stemmer SM, Shalgi R. Doxorubicin induced apoptosis in oocytes—mechanism and possible executers. J Clin Oncol. 2008;26(15_suppl):9611.

[84]

Patel R, Tadi P. Busulfan. StatPearls Publishing; 2023. Accessed https://www.ncbi.nlm.nih.gov/books/NBK555986/

[85]

Chen C, Li S, Hu C, et al. Protective effects of puerarin on premature ovarian failure via regulation of Wnt/β-catenin signaling pathway and oxidative stress. Reprod Sci. 2021;28(4):982-990.

[86]

Jiang Y, Zhao J, Qi HJ, et al. Accelerated ovarian aging in mice by treatment of busulfan and cyclophosphamide. J Zhejiang Univ Sci B. 2013;14(4):318-324.

[87]

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. Stem Cell Res Ther. 2020;11(1):3.

[88]

Luo Q, Yin N, Zhang L, et al. Role of SDF-1/CXCR4 and cytokines in the development of ovary injury in chemotherapy drug induced premature ovarian failure mice. Life Sci. 2017;179:103-109.

[89]

Lee E, Han SE, Park MJ, et al. Establishment of effective mouse model of premature ovarian failure considering treatment duration of anticancer drugs and natural recovery time. J Menopausal Med. 2018;24(3):196-203.

[90]

Bahrehbar K, Rezazadeh Valojerdi M, Esfandiari F, Fathi R, Hassani SN, Baharvand H. Human embryonic stem cell-derived mesenchymal stem cells improved premature ovarian failure. World J Stem Cells. 2020;12(8):857-878.

[91]

Mahran YF, El-Demerdash E, Nada AS, El-Naga RN, Ali AA, Abdel-Naim AB. Growth hormone ameliorates the radiotherapy-induced ovarian follicular loss in rats: impact on oxidative stress, apoptosis and IGF-1/IGF-1R Axis. PLoS One. 2015;10(10):e0140055.

[92]

Constine LS, Woolf PD, Cann D, et al. Hypothalamic–pituitary dysfunction after radiation for brain tumors. N Engl J Med. 1993;328(2):87-94.

[93]

Gosden RG, Wade JC, Fraser HM, Sandow J, Faddy MJ. Impact of congenital or experimental hypogonadotrophism on the radiation sensitivity of the mouse ovary. Hum Reprod. 1997;12(11):2483-2488.

[94]

Simon B, Lee SJ, Partridge AH, Runowicz CD. Preserving fertility after cancer. CA Cancer J Clin. 2005;55(4):211-228; quiz 63–4.

[95]

Martin M, Lefaix J, Delanian S. TGF-beta1 and radiation fibrosis: a master switch and a specific therapeutic target? Int J Radiat Oncol Biol Phys. 2000;47(2):277-290.

[96]

Hosseinimehr SJ. The use of angiotensin II receptor antagonists to increase the efficacy of radiotherapy in cancer treatment. Future Oncol. 2014;10(15):2381-2390.

[97]

Cai L, Zong DK, Tong GQ, Li L. Apoptotic mechanism of premature ovarian failure and rescue effect of traditional Chinese medicine: a review. J Tradit Chin Med. 2021;41(3):492-498.

[98]

Kerr JB, Brogan L, Myers M, et al. The primordial follicle reserve is not renewed after chemical or γ-irradiation mediated depletion. Reproduction. 2012;143(4):469-476.

[99]

Kim W, Lee S, Seo D, et al. Cellular stress responses in radiotherapy. Cells. 2019;8(9):1105.

[100]

Hirao A, Cheung A, Duncan G, et al. Chk2 is a tumor suppressor that regulates apoptosis in both an ataxia telangiectasia mutated (ATM)-dependent and an ATM-independent manner. Mol Cell Biol. 2002;22(18):6521-6532.

[101]

Wallace WHB, Thomson AB, Kelsey TW. The radiosensitivity of the human oocyte. Hum Reprod Open. 2003;18(1):117-121.

[102]

Mahran YF, Badr AM, Aldosari A, Bin-Zaid R, Alotaibi HN. Carvacrol and Thymol modulate the cross-talk between TNF-αand IGF-1 signaling in radiotherapy-induced ovarian failure. Oxidative Med Cell Longev. 2019;2019:3173745.

[103]

Mantawy EM, Said RS, Abdel-Aziz AK. Mechanistic approach of the inhibitory effect of chrysin on inflammatory and apoptotic events implicated in radiation-induced premature ovarian failure: emphasis on TGF-β/MAPKs signaling pathway. Biomed Pharmacother. 2019;109:293-303.

[104]

Chapman C, Cree L, Shelling AN. The genetics of premature ovarian failure: current perspectives. Int J Women’s Health. 2015;7:799-810.

[105]

Dixit H, Rao L, Padmalatha V, et al. Genes governing premature ovarian failure. Reprod Biomed Online. 2010;20(6):724-740.

[106]

Shelling AN, Burton KA, Chand AL, et al. Inhibin: a candidate gene for premature ovarian failure. Hum Reprod. 2000;15(12):2644-2649.

[107]

Goswami D, Conway GS. Premature ovarian failure. Hum Reprod. 2005;11(4):391-410.

[108]

Chen M, Jiang H, Zhang C. Selected genetic factors associated with primary ovarian insufficiency. Int J Mol Sci. 2023;24(5):4423.

[109]

Jagarlamudi K, Reddy P, Adhikari D, Liu K. Genetically modified mouse models for premature ovarian failure (POF). Mol Cell Endocrinol. 2010;315(1–2):1-10.

[110]

Yamada S, Hinch AG, Kamido H, Zhang Y, Edelmann W, Keeney S. Molecular structures and mechanisms of DNA break processing in mouse meiosis. Genes Dev. 2020;34(11–12):806-818.

[111]

Keeney S, Giroux CN, Kleckner N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell. 1997;88(3):375-384.

[112]

Romanienko PJ, Camerini-Otero RD. The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol Cell. 2000;6(5):975-987.

[113]

de Vries SS, Baart EB, Dekker M, et al. Mouse MutS-like protein Msh5 is required for proper chromosome synapsis in male and female meiosis. Genes Dev. 1999;13(5):523-531.

[114]

Harris SE, Chand AL, Winship IM, Gersak K, Aittomäki K, Shelling AN. Identification of novel mutations in FOXL2 associated with premature ovarian failure. Mol Hum Reprod. 2002;8(8):729-733.

[115]

Schmidt D, Ovitt CE, Anlag K, et al. The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development. 2004;131(4):933-942.

[116]

Rajkovic A, Pangas SA, Ballow D, Suzumori N, Matzuk MM. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science. 2004;305(5687):1157-1159.

[117]

Soyal SM, Amleh A, Dean J. FIGalpha, a germ cell-specific transcription factor required for ovarian follicle formation. Development. 2000;127(21):4645-4654.

[118]

Ghadami M, El-Demerdash E, Zhang D, et al. Bone marrow transplantation restores follicular maturation and steroid hormones production in a mouse model for primary ovarian failure. PLoS One. 2012;7(3):e32462.

[119]

Danilovich N, Babu PS, Xing W, Gerdes M, Krishnamurthy H, Sairam MR. Estrogen deficiency, obesity, and skeletal abnormalities in follicle-stimulating hormone receptor knockout (FORKO) female mice. Endocrinology. 2000;141(11):4295-4308.

[120]

Lawson KA, Dunn NR, Roelen BA, et al. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 1999;13(4):424-436.

[121]

Ying Y, Zhao GQ. Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev Biol. 2001;232(2):484-492.

[122]

Tung JY, Rosen MP, Nelson LM, et al. Novel missense mutations of the deleted-in-AZoospermia-like (DAZL) gene in infertile women and men. Reprod Biol Endocrinol. 2006;4:40.

[123]

Ruggiu M, Speed R, Taggart M, et al. The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature. 1997;389(6646):73-77.

[124]

Tsuda M, Sasaoka Y, Kiso M, et al. Conserved role of nanos proteins in germ cell development. Science. 2003;301(5637):1239-1241.

[125]

Cheng S, Altmeppen G, So C, et al. Mammalian oocytes store mRNAs in a mitochondria-associated membraneless compartment. Science. 2022;378(6617):eabq4835.

[126]

Shang L, Ren S, Yang X, et al. EIF4ENIF1 variants in two patients with non-syndromic premature ovarian insufficiency. Eur J Med Genet. 2022;65(10):104597.

[127]

Ding Y, He Z, Sha Y, Kee K, Li L. Eif4enif1 haploinsufficiency disrupts oocyte mitochondrial dynamics and leads to subfertility. Development. 2023;150(23):dev202151.

[128]

Huhtaniemi I, Hovatta O, La Marca A, et al. Advances in the molecular pathophysiology, genetics, and treatment of primary ovarian insufficiency. Trends Endocrinol Metab. 2018;29(6):400-419.

[129]

Xu H, Xia Y, Qin J, Xu J, Li C, Wang Y. Effects of low intensity pulsed ultrasound on expression of B-cell lymphoma-2 and BCL2-associated X in premature ovarian failure mice induced by 4-vinylcyclohexene diepoxide. Reprod Biol Endocrinol. 2021;19(1):113.

[130]

Biswas L, Tyc K, El Yakoubi W, Morgan K, Xing J, Schindler K. Meiosis interrupted: the genetics of female infertility via meiotic failure. Reproduction. 2021;161(2):R13-R35.

[131]

Yuan P, He Z, Sun S, et al. Bi-allelic recessive loss-of-function mutations in FIGLA cause premature ovarian insufficiency with short stature. Clin Genet. 2019;95(3):409-414.

[132]

Zariñán T, Mayorga J, Jardón-Valadez E, et al. A novel mutation in the FSH receptor (I423T) affecting receptor activation and leading to primary ovarian failure. J Clin Endocrinol Metab. 2021;106(2):e5 34-e550.

[133]

Rostami Dovom M, Noroozzadeh M, Mosaffa N, Zadeh-Vakili A, Piryaei A, Ramezani TF. Induced premature ovarian insufficiency by using D galactose and its effects on reproductive profiles in small laboratory animals: a systematic review. J Ovarian Res. 2019;12(1):96.

[134]

Chen YT, Mattison DR, Feigenbaum L, Fukui H, Schulman JD. Reduction in oocyte number following prenatal exposure to a diet high in galactose. Science. 1981;214(4525):1145-1147.

[135]

Li N, Wang J, Wang X, Sun J, Li Z. Icariin exerts a protective effect against d-galactose induced premature ovarian failure via promoting DNA damage repair. Biomed Pharmacother. 2019;118:109218.

[136]

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

[137]

Shang Z, Fan M, Zhang J, Wang Z, Jiang S, Li W. Red ginseng improves D-galactose-induced premature ovarian failure in mice based on network pharmacology. Int J Mol Sci. 2023;24(9):8210.

[138]

Li X, Li X, Deng L. Chrysin reduces inflammation and oxidative stress and improves ovarian function in D-gal-induced premature ovarian failure. Bioengineered. 2022;13(4):8291-8301.

[139]

Lai KW, Cheng LY, Cheung AL, O WS. Inhibitor of apoptosis proteins and ovarian dysfunction in galactosemic rats. Cell Tissue Res. 2003;311(3):417-425.

[140]

Dai F, Wang R, Deng Z, et al. Comparison of the different animal modeling and therapy methods of premature ovarian failure in animal model. Stem Cell Res Ther. 2023;14(1):135.

[141]

Claes A, Ball BA, Scoggin KE, et al. The interrelationship between anti-Müllerian hormone, ovarian follicular populations and age in mares. Equine Vet J. 2015;47(5):537-541.

[142]

Nelson SM, Telfer EE, Anderson RA. The ageing ovary and uterus: new biological insights. Hum Reprod. 2013;19(1):67-83.

[143]

Rah H, Jeon YJ, Lee WS, et al. Association of nitric oxide synthase gene polymorphisms (–786T>C, 4a4b, 894G>T) with primary ovarian insufficiency in Korean women. Maturitas. 2013;74(2):160-165.

[144]

Wu YY, Liang CY, Liu TT, et al. Protective roles and mechanisms of polysaccharides from dendrobium officinal on natural aging-induced premature ovarian failure. Biomed Pharmacother. 2018;101:953-960.

[145]

Ding C, Zou Q, Wang F, et al. Human amniotic mesenchymal stem cells improve ovarian function in natural aging through secreting hepatocyte growth factor and epidermal growth factor. Stem Cell Res Ther. 2018;9(1):55.

[146]

Qin X, Zhao Y, Zhang T, et al. TrkB agonist antibody ameliorates fertility deficits in aged and cyclophosphamide-induced premature ovarian failure model mice. Nat Commun. 2022;13(1):914.

[147]

Nie X, Dai Y, Zheng Y, et al. Establishment of a mouse model of premature ovarian failure using consecutive superovulation. Cell Physiol Biochem. 2018;51(5):2341-2358.

[148]

Tavana S, Valojerdi MR, Azarnia M, Shahverdi A. Restoration of ovarian tissue function and estrous cycle in rat after autotransplantation using hyaluronic acid hydrogel scaffold containing VEGF and bFGF. Growth Factors. 2016;34(3–4):97-106.

[149]

Saber M, Eimani H, Soleimani Mehranjani M, et al. The effect of verapamil on ischaemia/reperfusion injury in mouse ovarian tissue transplantation. Biomed Pharmacother. 2018;108:1313-1319.

[150]

Tavana S, Azarnia M, Valojerdi MR, Shahverdi A. Hyaluronic acid-based hydrogel scaffold without angiogenic growth factors enhances ovarian tissue function after autotransplantation in rats. Biomed Mater. 2016;11(5):055006.

[151]

Lozada Y, Bhagavath B. A review of laparoscopic salpingo-oophorectomy: technique and perioperative considerations. J Minim Invasive Gynecol. 2017;24(3):364-370.

[152]

Seok J, Park H, Choi JH, Lim J-Y, Kim KG, Kim GJ. Placenta-derived mesenchymal stem cells restore the ovary function in an ovariectomized rat model via an antioxidant effect. Antioxidants. 2020;9(7):591.

[153]

Sen Halicioglu B, Kasm S, Mi T. The relationship of 4-vinylcyclohexene diepoxide toxicity with cell death, oxidative stress, and gap junctions in female rat ovaries. Reprod Med Biol. 2021;20(4):543-553.

[154]

Nelson LM. Clinical practice. Primary ovarian insufficiency. N Engl J Med. 2009;360(6):606-614.

[155]

Devine PJ, Sipes IG, Hoyer PB. Effect of 4-vinylcyclohexene diepoxide dosing in rats on GSH levels in liver and ovaries. Toxicol Sci. 2001;62(2):315-320.

[156]

Takai Y, Canning J, Perez GI, et al. Bax, caspase-2, and caspase-3 are required for ovarian follicle loss caused by 4-vinylcyclohexene diepoxide exposure of female mice in vivo. Endocrinology. 2003;144(1):69-74.

[157]

Krysko DV, Mussche S, Leybaert L, D’Herde K. Gap junctional communication and connexin43 expression in relation to apoptotic cell death and survival of granulosa cells. J Histochem Cytochem. 2004;52(9):1199-1207.

[158]

Yin N, Zhao W, Luo Q, Yuan W, Luan X, Zhang H. Restoring ovarian function with human placenta-derived mesenchymal stem cells in autoimmune-induced premature ovarian failure mice mediated by Treg cells and associated cytokines. Reprod Sci. 2018;25(7):1073-1082.

[159]

Nakai M, Tatsumi H, Arai M. Successive pregnancies in a patient with premature ovarian failure. Eur J Obstet Gynecol Reprod Biol. 1984;18(4):217-224.

[160]

Tung KS, Lu CY. Immunologic basis of reproductive failure. Monogr Pathol. 1991;33:308-333.

[161]

Kelkar RL, Meherji PK, Kadam SS, Gupta SK, Nandedkar TD. Circulating auto-antibodies against the zona pellucida and thyroid microsomal antigen in women with premature ovarian failure. J Reprod Immunol. 2005;66(1):53-67.

[162]

Wassarman PM, Litscher ES. The multifunctional zona pellucida and mammalian fertilization. J Reprod Immunol. 2009;83(1–2):45-49.

[163]

Setiady YY, Samy ET, Tung KSK. Maternal autoantibody triggers De novo T cell-mediated neonatal autoimmune disease1. J Immunol. 2003;170(9):4656-4664.

[164]

Wang Z, Wei Q, Wang H, et al. Mesenchymal stem cell therapy using human umbilical cord in a rat model of autoimmune-induced premature ovarian failure. Stem Cells Int. 2020;2020:3249495.

[165]

Tong Z-B, Nelson LM. A mouse gene encoding an oocyte antigen associated with autoimmune premature ovarian failure. Endocrinology. 1999;140(8):3720-3726.

[166]

Kojima A, Prehn RT. Genetic susceptibility to post-thymectomy autoimmune diseases in mice. Immunogenetics. 1981;14(1–2):15-27.

[167]

Taguchi O, Nishizuka Y, Sakakura T, Kojima A. Autoimmune oophoritis in thymectomized mice: detection of circulating antibodies against oocytes. Clin Exp Immunol. 1980;40(3):540-553.

[168]

Zhai QY, Wang JJ, Tian Y, Liu X, Song Z. Review of psychological stress on oocyte and early embryonic development in female mice. Reprod Biol Endocrinol. 2020;18(1):101.

[169]

Gore AC, Attardi B, DeFranco DB. Glucocorticoid repression of the reproductive axis: effects on GnRH and gonadotropin subunit mRNA levels. Mol Cell Endocrinol. 2006;256(1–2):40-48.

[170]

Stephens MA, Wand G. Stress and the HPA axis: role of glucocorticoids in alcohol dependence. Alcohol Res. 2012;34(4):468-483.

[171]

Xu YP, Fu JC, Hong ZL, et al. Psychological stressors involved in the pathogenesis of premature ovarian insufficiency and potential intervention measures. Gynecol Endocrinol. 2024;40(1):2360085.

[172]

Xiang Y, Jiang L, Gou J, et al. Chronic unpredictable mild stress-induced mouse ovarian insufficiency by interrupting lipid homeostasis in the ovary. Front Cell Dev Biol. 2022;10:933674.

[173]

Ghatebi M, Zavareh S, Lashkarbolouki T, Elahdadi SM. Implications from early life stress on the development of mouse ovarian follicles: focus on oxidative stress. J Obstet Gynaecol Res. 2019;45(8):1506-1514.

[174]

Lu H, Ma L, Zhang Y, Feng Y, Zhang J, Wang S. Current animal model systems for ovarian aging research. Aging Dis. 2022;13(4):1183-1195.

[175]

Chon SJ, Umair Z, Yoon M-S. Premature ovarian insufficiency: past, present, and future. Front Cell Dev Biol. 2021;9:672890.

[176]

Moolhuijsen LME, Visser JA. Anti-Müllerian hormone and ovarian reserve: update on assessing ovarian function. J Clin Endocrinol Metab. 2020;105(11):3361-3373.

[177]

Abedy Ghehi F, Fathi R, Abtahi N, et al. Germ cells markers expression in mouse premature ovarian failure model. Pathobiol Rep. 2019;22(3):149-157.

[178]

Cedars MI. Evaluation of female fertility-AMH and ovarian reserve testing. J Clin Endocrinol Metab. 2022;107(6):1510-1519.

[179]

Liu Z, Li F, Xue J, et al. Esculentoside a rescues granulosa cell apoptosis and folliculogenesis in mice with premature ovarian failure. Aging (Albany NY). 2020;12(17):16951-16962.

[180]

Cao LB, Leung CK, Law PW, et al. Systemic changes in a mouse model of VCD-induced premature ovarian failure. Life Sci. 2020;262:118543.

[181]

Puy V, Barroca V, Messiaen S, et al. Mouse model of radiation-induced premature ovarian insufficiency reveals compromised oocyte quality: implications for fertility preservation. Reprod Biomed. 2021;43(5):799-809.

[182]

Long JP, Wan F, Zhang F, Zhou J, Don LF. DTC chemotherapy regimen is associated with higher incidence of premature ovarian failure in women of reproductive age with breast cancer. Eur Rev Med Pharmacol Sci. 2016;20(6):1087-1092.

[183]

Mauri D, Gazouli I, Zarkavelis G, et al. Chemotherapy associated ovarian failure. Front Endocrinol. 2020;11:572388.

[184]

Fleer R, Brendel M. Toxicity, interstrand cross-links and DNA fragmentation induced by ‘activated’ cyclophosphamide in yeast: comparative studies on 4-hydroperoxy-cyclophosphamide, its monofunctional analogon, acrolein, phosphoramide mustard, and nor-nitrogen mustard. Chem Biol Interact. 1982;39(1):1-15.

[185]

Jarrell JF, Bodo L, YoungLai EV, Barr RD, O’Connell GJ. The short-term reproductive toxicity of cyclophosphamide in the female rat. Reprod Toxicol. 1991;5(6):481-485.

[186]

Kitanohara M, Yamamoto T, Masunaga S, Ohishi M, Komatsu Y, Nagase M. Effect of porcine placental extract on the mild menopausal symptoms of climacteric women. Climacteric. 2017;20(2):144-150.

[187]

Zhang T, Yan D, Yang Y, et al. The comparison of animal models for premature ovarian failure established by several different source of inducers. Regul Toxicol Pharmacol. 2016;81:223-232.

[188]

Yao Y, Xu Y, Wang Y. Protective roles and mechanisms of rosmarinic acid in cyclophosphamide-induced premature ovarian failure. J Biochem Mol Toxicol. 2020;34(12):e22591.

[189]

Xing F, Wang M, Ding Z, et al. Protective effect and mechanism of melatonin on cisplatin-induced ovarian damage in mice. J Clin Med. 2022;11(24):7383.

RIGHTS & PERMISSIONS

2024 The Author(s). Animal Models and Experimental Medicine published by John Wiley & Sons Australia, Ltd on behalf of The Chinese Association for Laboratory Animal Sciences.

AI Summary AI Mindmap
PDF (3127KB)

230

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/