Browse > Article
http://dx.doi.org/10.5653/cerm.2019.46.2.43

Primordial follicle activation as new treatment for primary ovarian insufficiency  

Lee, Hye Nam (Department of Obstetrics and Gynecology, Fertility Center, CHA Gangnam Medical Center, CHA University)
Chang, Eun Mi (Department of Obstetrics and Gynecology, Fertility Center, CHA Gangnam Medical Center, CHA University)
Publication Information
Clinical and Experimental Reproductive Medicine / v.46, no.2, 2019 , pp. 43-49 More about this Journal
Abstract
Primordial follicle activation is a process in which individual primordial follicles leave their dormant state and enter a growth phase. While existing hormone stimulation strategies targeted the growing follicles, the remaining dormant primordial follicles were ruled out from clinical use. Recently, in vitro activation (IVA), which is a method for controlling primordial follicle activation, has provided an innovative technology for primary ovarian insufficiency (POI) patients. IVA was developed based on Hippo signaling and phosphatase and tensin homolog (PTEN)/phosphatidylinositol-3-kinase (PI3K)/protein kinase B (AKT)/forkhead box O3 (FOXO3) signaling modulation. With this method, dormant primordial follicles are activated to enter growth phase and developed into competent oocytes. IVA has been successfully applied in POI patients who only have a few remaining remnant primordial follicles in the ovary, and healthy pregnancies and deliveries have been reported. IVA may also provide a promising option for fertility preservation in cancer patients and prepubertal girls whose fertility preservation choices are limited to tissue cryopreservation. Here, we review the basic mechanisms, translational studies, and current clinical results for IVA. Limitations and further study requirements that could potentially optimize IVA for future use will also be discussed.
Keywords
Fertility preservation; Primary ovarian insufficiency; Primordial follicle activation; Ovarian follicle;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Zhai J, Yao G, Dong F, Bu Z, Cheng Y, Sato Y, et al. In vitro activation of follicles and fresh tissue auto-transplantation in primary ovarian insufficiency patients. J Clin Endocrinol Metab 2016;101:4405-12.   DOI
2 Fabregues F, Ferreri J, Calafell JM, Moreno V, Borras A, Manau D, 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 Ovarian Res 2018;11:76.   DOI
3 Check JH, Wilson C, DiAntonio G, DiAntonio A. In vitro fertilization (IVF) outcome in women in overt menopause attempting to induce follicular maturation by follicle stimulating hormone (FSH) receptor down-regulation. Clin Exp Obstet Gynecol 2016;43:181-3.   DOI
4 McLaughlin M, Kinnell HL, Anderson RA, Telfer EE. Inhibition of phosphatase and tensin homologue (PTEN) in human ovary in vitro results in increased activation of primordial follicles but compromises development of growing follicles. Mol Hum Reprod 2014;20:736-44.   DOI
5 McLaughlin M, Albertini DF, Wallace WH, Anderson RA, Telfer EE. Metaphase II oocytes from human unilaminar follicles grown in a multi-step culture system. Mol Hum Reprod 2018;24:135-42.   DOI
6 Resetkova N, Hayashi M, Kolp LA, Christianson MS. Fertility preservation for prepubertal girls: update and current challenges. Curr Obstet Gynecol Rep 2013;2:218-25.   DOI
7 Kallen A, Polotsky AJ, Johnson J. Untapped reserves: controlling primordial follicle growth activation. Trends Mol Med 2018;24:319-31.   DOI
8 Nelson LM. Clinical practice: primary ovarian insufficiency. N Engl J Med 2009;360:606-14.   DOI
9 De Vos M, Devroey P, Fauser BC. Primary ovarian insufficiency. Lancet 2010;376:911-21.   DOI
10 Coulam CB, Adamson SC, Annegers JF. Incidence of premature ovarian failure. Obstet Gynecol 1986;67:604-6.
11 European Society for Human Reproduction and Embryology (ESHRE) Guideline Group on POI, Webber L, Davies M, Anderson R, Bartlett J, Braat D, et al. ESHRE guideline: management of women with premature ovarian insufficiency. Hum Reprod 2016;31:926-37.   DOI
12 McGee EA, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev 2000;21:200-14.   DOI
13 Cordts EB, Christofolini DM, Dos Santos AA, Bianco B, Barbosa CP. Genetic aspects of premature ovarian failure: a literature review. Arch Gynecol Obstet 2011;283:635-43.   DOI
14 Haller-Kikkatalo K, Uibo R, Kurg A, Salumets A. The prevalence and phenotypic characteristics of spontaneous premature ovarian failure: a general population registry-based study. Hum Reprod 2015;30:1229-38.   DOI
15 Woad KJ, Watkins WJ, Prendergast D, Shelling AN. The genetic basis of premature ovarian failure. Aust N Z J Obstet Gynaecol 2006;46:242-4.   DOI
16 Lee WS, Otsuka F, Moore RK, Shimasaki S. Effect of bone morphogenetic protein-7 on folliculogenesis and ovulation in the rat. Biol Reprod 2001;65:994-9.   DOI
17 Skinner MK. Regulation of primordial follicle assembly and development. Hum Reprod Update 2005;11:461-71.   DOI
18 Adhikari D, Flohr G, Gorre N, Shen Y, Yang H, Lundin E, et al. Disruption of Tsc2 in oocytes leads to overactivation of the entire pool of primordial follicles. Mol Hum Reprod 2009;15:765-70.   DOI
19 Ding X, Zhang X, Mu Y, Li Y, Hao J. Effects of BMP4/SMAD signaling pathway on mouse primordial follicle growth and survival via up-regulation of Sohlh2 and c-kit. Mol Reprod Dev 2013;80:70-8.   DOI
20 Tang K, Yang WC, Li X, Wu CJ, Sang L, Yang LG. GDF-9 and bFGF enhance the effect of FSH on the survival, activation, and growth of cattle primordial follicles. Anim Reprod Sci 2012;131:129-34.   DOI
21 Huang EJ, Manova K, Packer AI, Sanchez S, Bachvarova RF, Besmer P. The murine steel panda mutation affects kit ligand expression and growth of early ovarian follicles. Dev Biol 1993;157:100-9.   DOI
22 Bonnet A, Cabau C, Bouchez O, Sarry J, Marsaud N, Foissac S, et al. An overview of gene expression dynamics during early ovarian folliculogenesis: specificity of follicular compartments and bidirectional dialog. BMC Genomics 2013;14:904.   DOI
23 Yoshida H, Takakura N, Kataoka H, Kunisada T, Okamura H, Nishikawa SI. Stepwise requirement of c-kit tyrosine kinase in mouse ovarian follicle development. Dev Biol 1997;184:122-37.   DOI
24 Kezele PR, Nilsson EE, Skinner MK. Insulin but not insulin-like growth factor-1 promotes the primordial to primary follicle transition. Mol Cell Endocrinol 2002;192:37-43.   DOI
25 Nilsson EE, Larsen G, Skinner MK. Roles of Gremlin 1 and Gremlin 2 in regulating ovarian primordial to primary follicle transition. Reproduction 2014;147:865-74.   DOI
26 Nilsson EE, Kezele P, Skinner MK. Leukemia inhibitory factor (LIF) promotes the primordial to primary follicle transition in rat ovaries. Mol Cell Endocrinol 2002;188:65-73.   DOI
27 Durlinger AL, Kramer P, Karels B, de Jong FH, Uilenbroek JT, Grootegoed JA, et al. Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary. Endocrinology 1999;140:5789-96.   DOI
28 Hosaka T, Biggs WH 3rd, Tieu D, Boyer AD, Varki NM, Cavenee WK, et al. Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci U S A 2004;101:2975-80.   DOI
29 Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 2003;301:215-8.   DOI
30 Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, et al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008;319:611-3.   DOI
31 Hu Y, Yuan DZ, Wu Y, Yu LL, Xu LZ, Yue LM, et al. Bisphenol A initiates excessive premature activation of primordial follicles in mouse ovaries via the PTEN signaling pathway. Reprod Sci 2018;25:609-20.   DOI
32 John GB, Gallardo TD, Shirley LJ, Castrillon DH. Foxo3 is a PI3Kdependent molecular switch controlling the initiation of oocyte growth. Dev Biol 2008;321:197-204.   DOI
33 Chang EM, Lim E, Yoon S, Jeong K, Bae S, Lee DR, 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:e0144245.   DOI
34 Xu M, Sun J, Wang Q, Zhang Q, Wei C, Lai D. Chronic restraint stress induces excessive activation of primordial follicles in mice ovaries. PLoS One 2018;13:e0194894.   DOI
35 Matsuda S, Nakanishi A, Wada Y, Kitagishi Y. Roles of PI3K/AKT/PTEN pathway as a target for pharmaceutical therapy. Open Med Chem J 2013;7:23-9.   DOI
36 Imai Y, Yamagishi H, Ono Y, Ueda Y. Versatile inhibitory effects of the flavonoid-derived PI3K/Akt inhibitor, LY294002, on ATPbinding cassette transporters that characterize stem cells. Clin Transl Med 2012;1:24.   DOI
37 Gross ER, Peart JN, Hsu AK, Auchampach JA, Gross GJ. Extending the cardioprotective window using a novel delta-opioid agonist fentanyl isothiocyanate via the PI3-kinase pathway. Am J Physiol Heart Circ Physiol 2005;288:H2744-9.   DOI
38 Gills JJ, Dennis PA. Perifosine: update on a novel Akt inhibitor. Curr Oncol Rep 2009;11:102-10.   DOI
39 Guo Y, Kwiatkowski DJ. Equivalent benefit of rapamycin and a potent mTOR ATP-competitive inhibitor, MLN0128 (INK128), in a mouse model of tuberous sclerosis. Mol Cancer Res 2013;11:467-73.   DOI
40 Albiges L, Chamming's F, Duclos B, Stern M, Motzer RJ, Ravaud A, et al. Incidence and management of mTOR inhibitor-associated pneumonitis in patients with metastatic renal cell carcinoma. Ann Oncol 2012;23:1943-53.   DOI
41 Pan D. The hippo signaling pathway in development and cancer. Dev Cell 2010;19:491-505.   DOI
42 Cheng Y, Feng Y, Jansson L, Sato Y, Deguchi M, Kawamura K, et al. Actin polymerization-enhancing drugs promote ovarian follicle growth mediated by the Hippo signaling effector YAP. FASEB J 2015;29:2423-30.   DOI
43 Adhikari D, Gorre N, Risal S, Zhao Z, Zhang H, Shen Y, 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:e39034.   DOI
44 Li J, Kawamura K, Cheng Y, Liu S, Klein C, Liu S, et al. Activation of dormant ovarian follicles to generate mature eggs. Proc Natl Acad Sci U S A 2010;107:10280-4.   DOI
45 Kawamura K, Cheng Y, Suzuki N, Deguchi M, Sato Y, Takae S, et al. Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc Natl Acad Sci U S A 2013;110:17474-9.   DOI
46 Suzuki N, Yoshioka N, Takae S, Sugishita Y, Tamura M, Hashimoto S, et al. Successful fertility preservation following ovarian tissue vitrification in patients with primary ovarian insufficiency. Hum Reprod 2015;30:608-15.   DOI