In vitro follicle activation as a strategy for assisted reproduction in patients with premature ovarian insufficiency: research advances

doi:10.16352/j.issn.1001-6325.2023.04.0538

Abstract

Abstract: Premature ovarian insufficiency (POI) refers to ovarian dysfunction in women before the age of 40 years, and its pathological basis is the depletion or difficult activation of primordial follicle. POI patients have a low natural conception rate and poor effect of ovulation induction therapy. At present, there is no effective method to restore ovarian function. In vitro activation (IVA) for follicles refers to surgical removal of part of the ovarian tissue, followed by drug or physical intervention in vitro, to activate the patient's remaining follicles. Finally, the tissue is rafted back to the same ovary so that it can develop to the stage of responding to ovulation induction. In conjunction with the above procedure, ovulation induction can obtain mature follicles for in vitro fertilization and embryo transfer. IVA technology is an innovative therapeutic option for POI, and provides a new direction for the treatment of POI patients. This article summarizes the principle of IVA, related signaling pathways and drug targets in each pathway, and reviews the application and optimization of IVA protocols in POI patients, so as to provide a basis for the diagnosis and treatment of patients with POI.

Key words: in vitro follicular activation, premature ovarian insufficiency, PTEN/PI3K/Akt, mTOR, Hippo

CLC Number:

R711.75

LIU Zhan'ao, CHEN Chen. In vitro follicle activation as a strategy for assisted reproduction in patients with premature ovarian insufficiency: research advances[J]. Basic & Clinical Medicine, 2023, 43(4): 538-546.

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URL: http://journal11.magtechjournal.com/Jwk_jcyxylc/EN/10.16352/j.issn.1001-6325.2023.04.0538

http://journal11.magtechjournal.com/Jwk_jcyxylc/EN/Y2023/V43/I4/538

References

[1]陈子江, 秦杰, 乔杰, 等. 早发性卵巢功能不全的临床诊疗中国专家共识[J]. 中华妇产科杂志, 2017, 52: 577-581.
[2]Golezar S, Ramezani Tehrani F, Khazaei S, et al. The global prevalence of primary ovarian insufficiency and early menopause: a meta-analysis[J]. Climacteric, 2019, 22: 403-411.
[3]Panay N, Anderson RA, Nappi RE, et al. Premature ovarian insufficiency: an International Menopause Society White Paper[J]. Climacteric, 2020, 23: 426-446.
[4]Fraison E, Crawford G, Casper G, et al. Pregnancy following diagnosis of premature ovarian insufficiency: a systematic review[J]. Reprod Biomed Online, 2019, 39: 467-476.
[5]Maruyama T. A woman with primary ovarian insufficiency had two live births resulting from intrauterine insemina-tions during 10 years of ovarian follicle monitoring[J]. J Obstet Gynaecol Res, 2020, 46: 2159-2163.
[6]Vo KCT, Kawamura K. In vitro activation early follicles: from the basic science to the clinical perspectives[J]. Int J Mol Sci, 2021, 22: 3785.
[7]Hsueh AJW, Kawamura K. Hippo signaling disruption and ovarian follicle activation in infertile patients[J]. Fertil Steril, 2020, 114: 458-464.
[8]Wang W, Todorov P, Isachenko E, et al. In vitro activation of cryopreserved ovarian tissue: A single-arm meta-analysis and systematic review[J]. Eur J Obstet Gynecol Reprod Biol, 2021, 258: 258-264.
[9]Zhai J, Zhang J, Zhang L, et al. Autotransplantation of the ovarian cortex after in-vitro activation for infertility treatment: a shortened procedure[J]. Hum Reprod, 2021, 36: 2134-2147.
[10]McGee EA, Hsueh AJW. Initial and cyclic recruitment of ovarian follicles[J]. Endocrine Rev, 2000, 21: 200-214.
[11]Lew R. Natural history of ovarian function including assessment of ovarian reserve and premature ovarian failure[J]. Best Pract Res Clin Obstet Gynaecol, 2019, 55: 2-13.
[12]Dewailly D, Andersen CY, Balen A, et al. The physiology and clinical utility of anti-Mullerian hormone in women[J]. Hum Reprod Update, 2014, 20: 370-385.
[13]Anderson RA, Nelson SM. Anti-Mullerian hormone in the diagnosis and prediction of premature ovarian insufficiency[J]. Semin Reprod Med, 2020, 38: 263-269.
[14]Gougeon A. Dynamics of follicular growth in the human: a model from preliminary results[J]. Hum Reprod, 1986, 1: 81-87.
[15]Mauri D, Gazouli I, Zarkavelis G, et al. Chemotherapy associated ovarian failure[J]. Front Endocrinol (Lausanne), 2020, 11: 572388.
[16]Lawrenz B, Coughlan C, Melado L, et al. Step-down of FSH- dosage during ovarian stimulation - basic lessons to be learnt from a randomized controlled trial[J]. Front Endocrinol (Lausanne), 2021, 12: 661707.
[17]Arroyo A, Kim B, Yeh J. Luteinizing hormone action in human oocyte maturation and quality: signaling pathways, regulation, and clinical impact[J]. Reprod Sci, 2020, 27: 1223-1252.
[18]Baerwald A, Pierson R. Ovarian follicular waves during the menstrual cycle: physiologic insights into novel approaches for ovarian stimulation[J]. Fertil Steril, 2020, 114: 443-457.
[19]Baerwald AR, Adams GP, Pierson RA. Ovarian antral folliculogenesis during the human menstrual cycle: a review[J]. Hum Reprod Update, 2012, 18: 73-91.
[20]Maidarti M, Anderson RA, Telfer EE. Crosstalk between PTEN/PI3K/Akt signalling and DNA damage in the oocyte: implications for primordial follicle activation, oocyte quality and ageing[J]. Cells, 2020, 9: 200.
[21]Masciangelo R, Hossay C, Chiti MC, et al. Role of the PI3K and Hippo pathways in follicle activation after grafting of human ovarian tissue[J]. J Assist Reprod Genet, 2020, 37: 101-108.
[22]Terren C, Munaut C. Molecular basis associated with the control of primordial follicle activation during transplanta-tion of cryopreserved ovarian tissue[J]. Reprod Sci, 2021, 28: 1257-1266.
[23]Ford EA, Beckett EL, Roman SD, et al. Advances in human primordial follicle activation and premature ovarian insufficiency[J]. Reproduction, 2020, 159: 15-29.
[24]Kawamura K, Cheng Y, Suzuki N, et al. Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment[J]. Proc Natl Acad Sci U S A, 2013, 110: 17474-17479.
[25]Zhai J, Yao G, Dong F, et al. In vitro activation of follicles and fresh tissue auto-transplantation in primary ovarian insufficiency patients[J]. J Clin Endocrinol Metab, 2016, 101: 4405-4412.
[26]Zhang J, Yan L, Wang Y, et al. In vivo and in vitro activation of dormant primordial follicles by EGF treatment in mouse and human[J]. Clin Transl Med, 2020, 10: 182.
[27]Yan H, Zhang J, Wen J, et al. CDC42 controls the activation of primordial follicles by regulating PI3K signaling in mouse oocytes[J]. BMC Biol, 2018, 16: 73.
[28]Correia B, Sousa MI, Ramalho-Santos J. The mTOR pathway in reproduction: from gonadal function to developmental coordination[J]. Reproduction, 2020, 159: 173-188.
[29]Condon KJ, Sabatini DM. Nutrient regulation of mTORC1 at a glance[J]. J Cell Sci, 2019, 132: 222570.
[30]Zhang T, Du X, Zhao L, et al. SIRT1 facilitates primordial follicle recruitment independent of deacetylase activity through directly modulating Akt1 and mTOR transcription[J]. FASEB J, 2019, 33: 14703-14716.
[31]Sun X, Su Y, He Y, et al. New strategy for in vitro activation of primordial follicles with mTOR and PI3K stimulators[J]. Cell Cycle, 2015, 14: 721-731.
[32]Ma S, Meng Z, Chen R, et al. The Hippo pathway: biology and pathophysiology[J]. Annu Rev Biochem, 2019, 88: 577-604.
[33]Pors SE, Harethardottir L, Olesen HO, et al. Effect of sphingosine-1-phosphate on activation of dormant follicles in murine and human ovarian tissue[J]. Mol Hum Reprod, 2020, 26: 301-311.
[34]Tanaka Y, Hsueh AJ, Kawamura K. Surgical approaches of drug-free in vitro activation and laparoscopic ovarian incision to treat patients with ovarian infertility[J]. Fertil Steril, 2020, 114: 1355-1357.
[35]Zhang X, Han T, Yan L, et al. Resumption of ovarian function after ovarian biopsy/scratch in patients with premature ovarian insufficiency[J]. Reprod Sci, 2019, 26: 207-213.
[36]Ouni E, Bouzin C, Dolmans MM, et al. Spatiotemporal changes in mechanical matrisome components of the human ovary from prepuberty to menopause[J]. Hum Reprod, 2020, 35: 1391-1410.
[37]Suzuki N, Yoshioka N, Takae S, et al. Successful fertility preservation following ovarian tissue vitrification in patients with primary ovarian insufficiency[J]. Hum Reprod, 2015, 30: 608-615.
[38]Fabregues F, Ferreri J, Calafell JM, et al. Pregnancy after drug-free in vitro activation of follicles and fresh tissue autotransplantation in primary ovarian insufficiency patient: a case report and literature review[J]. J Ovarian Res, 2018, 11: 76.
[39]Ferreri J, Fabregues F, Calafell JM, et al. Drug-free in-vitro activation of follicles and fresh tissue autotransplantation as a therapeutic option in patients with primary ovarian insufficiency[J]. Reprod Biomed Online, 2020, 40: 254-260.
[40]Kawamura K, Ishizuka B, Hsueh AJW. Drug-free in-vitro activation of follicles for infertility treatment in poor ovarian response patients with decreased ovarian reserve[J]. Reprod Biomed Online, 2020, 40: 245-253.
[41]Jiao X, Meng T, Zhai Y, et al. Ovarian reserve markers in premature ovarian insufficiency: within different clinical stages and different etiologies[J]. Front Endocrinol(Lausanne), 2021, 12: 601752.
[42]von Wolff M, Roumet M, Stute P, et al. Serum anti-Mullerian hormone (AMH) concentration has limited prognostic value for density of primordial and primary follicles, questioning it as an accurate parameter for the ovarian reserve[J]. Maturitas, 2020, 134: 34-40.
[43]Kasahara Y, Osuka S, Bayasula, et al. Very low levels of serum anti-mullerian hormone as a possible marker for follicle growth in patients with primary ovarian insufficiency under hormone replacement therapy[J]. Reprod Sci, 2021, 28: 31-36.
[44]Piver P, Sallee C, Durand LM, et al. Robot-assisted laparoscopic auto-graft of patchwork ovarian cortex in two steps[J]. J Gynecol Obstet Hum Reprod, 2020, 49: 101730.
[45]Man L, Park L, Bodine R, et al. Co-transplantation of human ovarian tissue with engineered endothelial cells: a cell-based strategy combining accelerated perfusion with direct paracrine delivery[J]. J Vis Exp, 2018,135:57472.
[46]Lim M, Thompson JG, Dunning KR. HYPOXIA AND REPRODUCTIVE HEALTH: Hypoxia and ovarian function: follicle development, ovulation, oocyte maturation[J]. Reproduction, 2021, 161: F33-F40.
[47]Guzel Y, Bildik G, Oktem O. Sphingosine-1-phosphate protects human ovarian follicles from apoptosis in vitro[J]. Eur J Obstet Gynecol Reprod Biol, 2018, 222: 19-24.
[48]Dolmans MM, Donnez J, Cacciottola L. Fertility preservation: the challenge of freezing and transplanting ovarian tissue[J]. Trends Mol Med, 2021, 27: 777-791.
[49]Olesen HO, Pors SE, Jensen LB, et al. N-acetylcysteine protects ovarian follicles from ischemia-reperfusion injury in xenotransplanted human ovarian tissue[J]. Hum Reprod, 2021, 36: 429-443.