New Hopes in fertility preservation in women with canser (review article)
Subject Areas : Developmental biology of plants and animals , development and differentiation in microorganismsSeyedeh Fatemeh Siadat 1 , Rouhollah Fathi 2
1 - department of biology, faculty of biological sciences, Tehran North Branch,Islamic Azad University,Tehran,Iran
2 - Department of Embryology at Reproductive Biomedicine Research Center, Royan
Institute for Reproductive Biomedicine, ACECR, Tehran, Iran
Keywords: cancer, fertility preservation, ovary freezing and transplantation, artificial ovary, ovarian stem cells,
Abstract :
Recent advances in cancer diagnosis and treatment such as radiotherapy, chemotherapy and bone marrow transplantation have increased life expectancy in these patients. Toxic substances and ionizing radiation threaten endocrine activity and reproductive cycle, causing loss of fertility and early ovarian failure (POF). Common approaches to treating fertility include ovarian Oophoropexy, oocyte and embryo freezing, and freezing of ovarian tissue and transplantation. Cryopreservation of the embryo and oocyte requires hormonal stimuli to increase the number of eggs, but delay the onset of cancer treatment and directly contribute to the development of hormone-dependent tumors. On the other hand, in the freezing of the embryo, there is a need for a sexual partner (the wife or sperm donor) and is not accessible to young girls and children. For this reason, in young patients, in order to preserve fertilization, ovarian tissue cultures and then transplantation are more useful. So far, various methods have been used in ovarian transplantation on different animal and human species. Each of these methods has some advantages and disadvantages. However, many unresolved issues remain with regard to maintaining fertility in cancer patients. On the other hand, hopefuls have been opened to preserve the fertility of cancer patients. The purpose of this study is to update the research on fertility preservation strategies and to summarize the progress made in this regard.
[1] Adhikari D, Gorre N, Risal S, Zhao Z, Zhang H, Shen Y, Liu K.(2012), The safe use of a PTEN inhibitor for the activation of dormant mouse primordial follicles and generation of fertilizable eggs. PloS one, 7(6):e39034.
[2] Ahn RW, Barrett SL, Raja MR, Jozefik JK, Spaho L, Chen H, Bally MB, Mazar AP, Avram MJ, Winter JN.(2013), Nano-encapsulation of arsenic trioxide enhances efficacy against murine lymphoma model while minimizing its impact on ovarian reserve in vitro and in vivo. PloS one, 8(3):e58491.
[3] Ahn RW, Chen F, Chen H, Stern ST, Clogston JD, Patri AK, Raja MR, Swindell EP, Parimi V, Cryns VL et al.(2010), A novel nanoparticulate formulation of arsenic trioxide with enhanced therapeutic efficacy in a murine model of breastcancer. Clinical cancer research: an official journal of the American Association for Cancer Research, 16(14):3607-3617.
[4] Baird D, Webb R, Campbell B, Harkness L, Gosden R.(1999), Long-Term Ovarian Function in Sheep after Ovariectomy and Transplantation of Autografts Stored at− 196 C** This work was supported by Medical Research Council Program Grant 8929853. Endocrinology, 140(1):462-471.
[5] Baker SJ, Spears N.(1999), The role of intra-ovarian interactions in the regulation of follicle dominance. Human reproduction update, 5(2):153-165.
[6] Barrett SL, Shea LD, Woodruff TK. (2010), Noninvasive index of cryorecovery and growth potential for human follicles in vitro. Biology of reproduction, 82(6):1180-1189.
[7] Bedaiwy MA, Hussein MR, Biscotti C, Falcone T.(2006), Cryopreservation of intact human ovary with its vascular pedicle. Human Reproduction, 21 (12): 3258-3269.
[8] Bisharah M, Tulandi T. (2003), Laparoscopic preservation of ovarian function: an underused procedure. American journal of obstetrics and gynecology, 188(2):367-370.
[9] Blumenfeld Z. (2002), Preservation of fertility and ovarian function and minimalization of chemotherapy associated gonadotoxicity and premature ovarian failure: the role of inhibin-A and-B as markers. Molecular and cellular endocrinology, 187 (1): 93-105.
[10] Brito IR, Lima IM, Xu M, Shea LD, Woodruff TK, Figueiredo JR. (2014), Three-dimensional systems for in vitro follicular culture: overview of alginate-based matrices. Reproduction, Fertility and Development, 26(7):915-930.
[11] Chen C. (1986), Pregnancy after human oocyte cryopreservation. The Lancet, 327(8486):884-886.
[12] Chen H, Lv J-Q, Ge H-S, Wu X-M, Xi H-T, Chi H-H, Zhu C-F, Huang J-Y. (2014), Live birth following vitrification of in vitro matured oocytes derived from sibling smaller follicles at follicle selection phase in the context of in vitro fertilization. Gynecological Endocrinology, 30(9):624-626.
[13] Cheng Y, Kim J, Li XX, Hsueh AJ. (2015), Promotion of ovarian follicle growth following mTOR activation: synergistic effects of AKT stimulators. PloS one, 10 (2): e0117769.
[14] Clough KB, Goffinet F, Labib A, Renolleau C, Campana F, Rochefordiere Adl, Durand JC. (1996), Laparoscopic unilateral ovarian transposition prior to irradiation: prospective study of 20 cases. Cancer, 77(12):2638-2645.
[15] Cobo A, Garcia-Velasco JA, Domingo J, Remohí J, Pellicer A. (2013), Is vitrification of oocytes useful for fertility preservation for age-related fertility decline and in cancer patients? Fertility and sterility, 99 (6): 1485-1495.
[16] Colgan TJ, Murphy J, Cole DE, Narod S, Rosen B. (2001), Occult carcinoma in prophylactic oophorectomy specimens: prevalence and association with BRCA germline mutation status. The American journal of surgical pathology, 25 (10): 1283-1289.
[17] Cortvrindt R, Smitz J, Van Steirteghem A. (1996), Ovary and ovulation: In-vitro maturation, fertilization and embryo development of immature oocytes from early preantral follicles from prepuberal mice in a simplified culture system. Human Reproduction, 11(12): 2656-2666.
[18] Dath C, Dethy A, Van Langendonckt A, Van Eyck AS, Amorim CA, Luyckx V, Donnez J, Dolmans MM. (2011), Endothelial cells are essential for ovarian stromal tissue restructuring after xenotransplantation of isolated ovarian stromal cells. Hum Reprod, 26(6):1431-1439.
[19] De Vos M, Smitz J, Woodruff TK. (2014), Fertility preservation in women with cancer. The Lancet, 384(9950):1302-1310.
[20] Deanesly R. (1957), Egg survival in immature rat ovaries grafted after freezing and thawing. Proceedings of the Royal Society of London B: Biological Sciences, 147 (928): 412-421.
[21] Del Mastro L, Ceppi M, Poggio F, Bighin C, Peccatori F, Demeestere I, Levaggi A, Giraudi S, Lambertini M, D’Alonzo A. (2014), Gonadotropin-releasing hormone analogues for the prevention of chemotherapy-induced premature ovarian failure in cancer women: systematic review and meta-analysis of randomized trials. Cancer treatment reviews, 40 (5): 675-683.
[22] Demeestere I, Simon P, Dedeken L, Moffa F, Tsépélidis S, Brachet C, Delbaere A, Devreker F, Ferster A. (2015), Live birth after autograft of ovarian tissue cryopreserved during childhood. Human reproduction, 30(9):2107-2109.
[23] Dolmans M-M, Jadoul P, Gilliaux S, Amorim CA, Luyckx V, Squifflet J, Donnez J, Van Langendonckt A. (2013), A review of 15 years of ovarian tissue bank activities. Journal of assisted reproduction and genetics, 30(3):305-314.
[24] Dolmans M-M, Luyckx V, Donnez J, Andersen CY, Greve T. (2013), Risk of transferring malignant cells with transplanted frozen-thawed ovarian tissue. Fertility and sterility, 99(6):1514-1522.
[25] Donnez J, Dolmans M-M.2015), Ovarian cortex transplantation: 60 reported live births brings the success and worldwide expansion of the technique towards routine clinical practice. Journal of assisted reproduction and genetics, 32(8): 1167-1170.
[26] Donnez J, Dolmans MM, Pellicer A, Diaz-Garcia C, Sanchez Serrano M, Schmidt KT, Ernst E, Luyckx V, Andersen CY. (2013), Restoration of ovarian activity and pregnancy after transplantation of cryopreserved ovarian tissue: a review of 60 cases of reimplantation. Fertility and sterility, 99 (6): 1503-1513.
[27] Donnez J, Dolmans M-M. (2004), Livebirth after cryopreserved ovarian tissue autotransplantation. The Lancet, 364 (9451): 2092-2093.
[28] [28]Donnez J, Dolmans M-M.(2013), Fertility preservation in women. Nature Reviews Endocrinology, 9(12):735-749.
[29] Donnez J, Jadoul P, Squifflet J, Van Langendonckt A, Donnez O, Van Eyck AS, Marinescu C, Dolmans MM. (2010), Ovarian tissue cryopreservation and transplantation in cancer patients. Best practice & research Clinical obstetrics & gynaecology, 24 (1): 87-100.
[30] Dudzinski DM. (2004), Ethical issues in fertility preservation for adolescent cancer survivors: oocyte and ovarian tissue cryopreservation. Journal of pediatric and adolescent gynecology, 17(2): 97-102.
[31] Eimani H, Siadat SF, Eftekhari-Yazdi P, Parivar K, Rezazadeh Valojerdi M, Shahverdi A. (2009), Autologous transplantation of Intact mouse ovaries in gluteus superficialis muscle. Yakhteh Medical Journal, 11 (2): 184-189.
[32] Eimani H, Siadat SF, Eftekhari-Yazdi P, Parivar K, Valojerdi MR, Shahverdi A. (2009), Comparative study between intact and non-intact intramuscular auto-grafted mouse ovaries. Reproductive biomedicine online, 18 (1): 53-60.
[33] Elis A, Tevet A, Yerushalmi R, Blickstein D, Bairy O, Dann EJ, Blumenfeld Z, Abraham A, Manor Y, Shpilberg O. (2006), Fertility status among women treated for aggressive non-Hodgkin's lymphoma. Leukemia & lymphoma, 47 (4): 623-627.
[34] Eppig JJ, O’Brien MJ. (1996), Development in vitro of mouse oocytes from primordial follicles. Biology of reproduction, 54 (1): 197-207.
[35] Ernst EH, Offersen BV, Andersen CY, Ernst E. (2013), Legal termination of a pregnancy resulting from transplanted cryopreserved ovarian tissue due to cancer recurrence. Journal of assisted reproduction and genetics, 30 (7): 975-978.
[36] Farquhar C, Brown J, Marjoribanks J. (2012), Laparoscopic drilling by diathermy or laser for ovulation induction in anovulatory polycystic ovary syndrome. The Cochrane database of systematic reviews: (6) CD001122.
[37] Fathi R, Rezazadeh Valojerdi M, Salehnia M, Ebrahimi B, SalmanYazdi R. (2014), Ovarian Tissue Transplantation: Advantages, Disadvantages and Upcoming Challenges (A Review Article). Journal of Mazandaran University of Medical Sciences, 24 (113): 253-265.
[38] Fathi R, Rezazadeh Valojerdi M, Salehnia M, Najar Asl M, Totonchi M, Salman Yazdi R, Ebrahimi B. (2014), A review on the activity of hormons and growth factors after ovarian tissue transplantation. Modares Journal of Medical Sciences: Pathobiology, 17 (2): 1-12.
[39] Fathi R, Rezazadeh Valojerdi M, Totonchi M, Deheshkar Farahani N, Ebrahimi B, Shabani F, Borjian Boroujeni P. (2014), A Review on the Activity of Angiogenic and Apoptotic Factors in Transplanted Ovarian Tissue. SSU_Journals, 22 (3): 1285-1298.
[40] Fathi R, Valojerdi MR, Ebrahimi B, Eivazkhani F, Akbarpour M, Tahaei LS, Abtahi NS. (2017), Fertility Preservation in Cancer Patients: In Vivo and In Vitro Options. Cell Journal, 19 (2):173.
[41] Fathi R, Valojerdi MR, Salehnia M, Najar-Asl M, Totonchi M, Yazdi RS, Ebrahimi B. (2014), A Review on the Activity of Hormones and Growth Factors after Ovarian Tissue Transplantation. Modares Journal of Medical Sciences: Pathobiology, 17 (2).
[42] Fathi R, Valojerdi MR, Salehnia M. (2013), Effects of different cryoprotectant combinations on primordial follicle survivability and apoptosis incidence after vitrification of whole rat ovary. CryoLetters, 34 (3): 228-238.
[43] Forman EJ, Li X, Ferry KM, Scott K, Treff NR, Scott RT. (2012), Oocyte vitrification does not increase the risk of embryonic aneuploidy or diminish the implantation potential of blastocysts created after intracytoplasmic sperm injection: a novel, paired randomized controlled trial using DNA fingerprinting. Fertility and sterility, 98 (3): 644-649
[44] Goldman KN, Kramer Y, Hodes-Wertz B, Noyes N, McCaffrey C, Grifo JA. (2015), Long-term cryopreservation of human oocytes does not increase embryonic aneuploidy. Fertility and sterility, 103 (3): 662-668.
[45] Gonfloni S, Di Tella L, Caldarola S, Cannata SM, Klinger FG, Di Bartolomeo C, Mattei M, Candi E, De Felici M, Melino G et al. (2009), Inhibition of the c-Abl-TAp63 pathway protects mouse oocytes from chemotherapy-induced death. Nature medicine, 15 (10): 1179-1185.
[46] Gosden R, Boulton M, Grant K, Webb R. (1994), Follicular development from ovarian xenografts in SCID mice. Journal of reproduction and fertility, 101(3): 619-623.
[47] Gosden RG, Mullan J, Picton HM, Yin H, Tan S-L. (2002), Current perspective on primordial follicle cryopreservation and culture for reproductive medicine. Human reproduction update, 8 (2): 105-110.
[48] Green S, SMITH AU, Zuckerman S. (1956), The numbers of oocytes in ovarian autografts after freezing and thawing. Journal of Endocrinology, 13(3): 330-NP.
[49] Hancke K, Strauch O, Kissel C, Gobel H, Schafer W, Denschlag D. (2007), Sphingosine 1-phosphate protects ovaries from chemotherapy-induced damage in vivo. Fertility and sterility, 87(1): 172-177.
[50] Harp R, Leibach J, Black J, Keldahl C, Karow A. (1994), Cryopreservation of murine ovarian tissue. Cryobiology, 31 (4): 336-343.
[51] Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, Saitou M. (2012), Offspring from oocytes derived from in vitro primordial germ cell–like cells in mice. Science, 338 (6109): 971-975.
[52] Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M. (2011), Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell, 146 (4): 519-532.
[53] Hendriks S, Dancet EA, van Pelt AM, Hamer G, Repping S. (2015), Artificial gametes: a systematic review of biological progress towards clinical application. Human reproduction update, 21(3):285-296.
[54] Hermann BP, Sukhwani M, Salati J, Sheng Y, Chu T, Orwig KE. (2011), Separating spermatogonia from cancer cells in contaminated prepubertal primate testis cell suspensions. Human Reproduction, 26 (12): 3222-3231.
[55] Hsueh AJ, Kawamura K, Cheng Y, Fauser BC. (2015), Intraovarian control of early folliculogenesis. Endocrine reviews, 36 (1): 1-24.
[56] Hübner K, Fuhrmann G, Christenson LK, Kehler J, Reinbold R, De La Fuente R, Wood J, Strauss JF, Boiani M, Schöler HR. (2003), Derivation of oocytes from mouse embryonic stem cells. Science, 300 (5623): 1251-1256.
[57] Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. (2004), Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature, 428 (6979): 145-150.
[58] Kalich-Philosoph L, Roness H, Carmely A, Fishel-Bartal M, Ligumsky H, Paglin S, Wolf I, Kanety H, Sredni B, Meirow D. (2013), Cyclophosphamide triggers follicle activation and "burnout"; AS101 prevents follicle loss and preserves fertility. Science translational medicine, 5(185):185ra162.
[59] Kawamura K, Cheng Y, Suzuki N, Deguchi M, Sato Y, Takae S, Ho CH, Kawamura N, Tamura M, Hashimoto S et al. (2013), Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proceedings of the National Academy of Sciences of the United States of America, 110(43):17474-17479.
[60] Kim S-Y, Cordeiro M, Serna V, Ebbert K, Butler LM, Sinha S, Mills AA, Woodruff TK, Kurita T. (2013), Rescue of platinum-damaged oocytes from programmed cell death through inactivation of the p53 family signaling network. Cell death and differentiation, 20 (8): 987.
[61] Laronda MM, Jakus AE, Whelan KA, Wertheim JA, Shah RN, Woodruff TK. (2015) Initiation of puberty in mice following decellularized ovary transplant. Biomaterials, 50: 20-29.
[62] Lee D, Yeoman R, Battaglia D, Stouffer R, Zelinski-Wooten M, Fanton J, Wolf D. (2004), Live birth after ovarian tissue transplant. Nature, 428 (6979): 137-138
[63] Li F, Turan V, Lierman S, Cuvelier C, De Sutter P, Oktay K. (2014), Sphingosine-1-phosphate prevents chemotherapy-induced human primordial follicle death. Hum Reprod, 29 (1): 107-113.
[64] Li J, Kawamura K, Cheng Y, Liu S, Klein C, Liu S, Duan EK, Hsueh AJ. (2010), Activation of dormant ovarian follicles to generate mature eggs. Proceedings of the National Academy of Sciences of the United States of America, 107 (22): 10280-10284.
[65] Lucifero D, Mertineit C, Clarke HJ, Bestor TH, Trasler JM. (2002), Methylation dynamics of imprinted genes in mouse germ cells. Genomics, 79 (4): 530-538.
[66] Luyckx V, Dolmans MM, Vanacker J, Legat C, Fortuno Moya C, Donnez J, Amorim CA. (2014), A new step toward the artificial ovary: survival and proliferation of isolated murine follicles after autologous transplantation in a fibrin scaffold. Fertility and sterility, 101 (4): 1149-1156.
[67] Luyckx V, Dolmans MM, Vanacker J, Scalercio SR, Donnez J, Amorim CA. (2013), First step in developing a 3D biodegradable fibrin scaffold for an artificial ovary. J Ovarian Res, 6 (1): 83.
[68] Mahran YF, El-Demerdash E, Nada AS, Ali AA, Abdel-Naim AB.(2013), Insights into the protective mechanisms of tamoxifen in radiotherapy-induced ovarian follicular loss: impact on insulin-like growth factor 1. Endocrinology, 154 (10): 3888-3899.
[69] Mandelbaum J, Belaisch-Allart J, Junca A-M, Antoine J-M, Plachot M, Alvarez S, Alnot M-O, Salat-Baroux J.(1998), Cryopreservation in human assisted reproduction is now routine for embryos but remains a research procedure for oocytes. Human Reproduction, 13 (suppl_3): 161-174.
[70] Martinez-Madrid B, Camboni A, Dolmans M-M, Nottola S, Van Langendonckt A, Donnez J. (2007), Apoptosis and ultrastructural assessment after cryopreservation of whole human ovaries with their vascular pedicle. Fertility and sterility, 87 (5): 1153-1165.
[71] McLaughlin M, Bromfield J, Albertini D, Telfer E. (2010), Activin promotes follicular integrity and oogenesis in cultured pre-antral bovine follicles. Molecular human reproduction, 16 (9): 644-653.
[72] Meirow D, Hardan I, Dor J, Fridman E, Elizur S, Ra'anani H, Slyusarevsky E, Amariglio N, Schiff E, Rechavi G. (2008), Searching for evidence of disease and malignant cell contamination in ovarian tissue stored from hematologic cancer patients. Human Reproduction, 23 (5): 1007-1013.
[73] Meirow D, Levron J, Eldar-Geva T, Hardan I, Fridman E, Zalel Y, Schiff E, Dor J. (2005), Pregnancy after transplantation of cryopreserved ovarian tissue in a patient with ovarian failure after chemotherapy. New England Journal of Medicine, 353 (3): 318-321.
[74] Moore HC, Unger JM, Phillips K-A, Boyle F, Hitre E, Porter D, Francis PA, Goldstein LJ, Gomez HL, Vallejos CS. (2015), Goserelin for ovarian protection during breast-cancer adjuvant chemotherapy. New England Journal of Medicine, 372 (10): 923-932.
[75] Morice P, Juncker L, Rey A, El-Hassan J, Haie-Meder C, Castaigne D. (2000), Ovarian transposition for patients with cervical carcinoma treated by radiosurgical combination. Fertility and sterility, 74 (4): 743-748.
[76] Morita Y, Perez GI, Paris F, Miranda SR, Ehleiter D, Haimovitz-Friedman A, Fuks Z, Xie Z, Reed JC, Schuchman EH. (2000), Oocyte apoptosis is suppressed by disruption of the acid sphingomyelinase gene or by sphingosine-1-phosphate therapy. Nature medicine, 6 (10): 1109.
[77] Motamed M, Sadr Z, Valojerdi M, Moini A, Oryan S, Totonchi M, Ebrahimi B, Maroufizadeh S, Taghiabadi E, Fathi R. (2017), Tissue engineered human amniotic membrane application in mouse ovarian follicular culture. Annals of Biomedical Engineering: 1-12.
[78] Nelson LM. (2009), Clinical practice. Primary ovarian insufficiency. The New England journal of medicine, 360 (6): 606-614.
[79] Newton H, Aubard Y, Rutherford A, Sharma V, Gosden R. (1996), Ovary and ovulation: Low temperature storage and grafting of human ovarian tissue. Human reproduction, 11(7):1487-1491.
[80] Oktay K, Buyuk E, Rodriguez-Wallberg K, Sahin G. (2010), In vitro maturation improves oocyte or embryo cryopreservation outcome in breast cancer patients undergoing ovarian stimulation for fertility preservation. Reproductive biomedicine online, 20 (5): 634-638.
[81] Oktay K, Buyuk E, Rosenwaks Z, Rucinski J. (2003), A technique for transplantation of ovarian cortical strips to the forearm. Fertility and sterility, 80 (1): 193-198.
[82] Oktay K, Buyuk E, Veeck L, Zaninovic N, Xu K, Takeuchi T, Opsahl M, Rosenwaks Z. (2004), Embryo development after heterotopic transplantation of cryopreserved ovarian tissue. The Lancet, 363 (9412): 837-840.
[83] Oktay K, Economos K, Kan M, Rucinski J, Veeck L, Rosenwaks Z. (2001), Endocrine function and oocyte retrieval after autologous transplantation of ovarian cortical strips to the forearm. Jama, 286 (12): 1490-1493.
[84] Oktay K. (2006), Spontaneous conceptions and live birth after heterotopic ovarian transplantation: is there a germline stem cell connection? Human Reproduction, 21 (6): 1345-1348.
[85] Pacheco BP, Ribas JM, Milone G, Fernandez I, Kvicala R, Mila T, Di Noto A, Ortiz OC, Pavlovsky S. (2001), Use of GnRH analogs for functional protection of the ovary and preservation of fertility during cancer treatment in adolescents: a preliminary report. Gynecologic oncology, 81 (3): 391-397.
[86] Pangas SA, Saudye H, Shea LD, Woodruff TK. (2003), Novel approach for the three-dimensional culture of granulosa cell–oocyte complexes. Tissue engineering, 9 (5): 1013-1021.
[87] Paris F, Perez GI, Fuks Z, Haimovitz-Friedman A, Nguyen H, Bose M, Ilagan A, Hunt PA, Morgan WF, Tilly JL. (2002), Sphingosine 1-phosphate preserves fertility in irradiated female mice without propagating genomic damage in offspring. Nature medicine, 8 (9): 901-902.
[88] Parkes A. (1952), Preservation of living cells at low temperatures. Lectures on the scientific basis of medicine, 2: 250.
[89] Parkes A. (1957), Viability of ovarian tissue after freezing. Proceedings of the Royal Society of London Series B, Biological Sciences, 147 (929): 520-528.
[90] Perez GI, Knudson CM, Leykin L, Korsmeyer SJ, Tilly JL. (1997), Apoptosis-associated signaling pathways are required for chemotherapy-mediated female germ cell destruction. Nature medicine, 3 (11): 1228-1232.
[91] Poirot C, Vacher-Lavenu M-C, Helardot P, Guibert J, Brugières L, Jouannet P. (2002), Human ovarian tissue cryopreservation: indications and feasibility. Human Reproduction, 17 (6): 1447-1452.
[92] Poirot CJ, Martelli H, Genestie C, Golmard JL, Valteau‐Couanet D, Helardot P, Pacquement H, Sauvat F, Tabone MD, Philippe‐Chomette P. (2007), Feasibility of ovarian tissue cryopreservation for prepubertal females with cancer. Pediatric blood & cancer, 49 (1): 74-78.
[93] Rajabzadeh AR, Eimani H, Koochesfahani HM, Shahvardi A-H, Fathi R. (2015), Morphological study of isolated ovarian preantral follicles using fibrin gel plus platelet lysate after subcutaneous transplantation. Cell Journal (Yakhteh) 5, 17 (1): 145.
[94] Reaman GH. (2002), Pediatric oncology: current views and outcomes. Pediatric Clinics of North America, 49 (6): 1305-1318.
[95] Rezazadeh Valojerdi M, Fathi R, Siadat SF. (2016), Fertility Preserving in females Based on cellular and molecular approaches. Book, Royan Institiute publication:Tehran, 64-102.
[96] Rienzi L, Romano S, Albricci L, Maggiulli R, Capalbo A, Baroni E, Colamaria S, Sapienza F, Ubaldi F. (2009), Embryo development of fresh ‘versus’ vitrified metaphase II oocytes after ICSI: a prospective randomized sibling-oocyte study. Human Reproduction, 25 (1): 66-73.
[97] Rosendahl M, Greve T, Andersen CY. (2013), The safety of transplanting cryopreserved ovarian tissue in cancer patients: a review of the literature. Journal of assisted reproduction and genetics, 30 (1): 11-24.
[98] Sadr SZ, Ebrahimi B, Shahhoseini M, Fatehi R, Favaedi R. (2015), Mouse preantral follicle development in two-dimensional and three-dimensional culture systems after ovarian tissue vitrification. European Journal of Obstetrics & Gynecology and Reproductive Biology, 194: 206-211.
[99] Senn A, Vozzi C, Chanson A, De Grandi P, Germond M. (2000), Prospective randomized study of two cryopreservation policies avoiding embryo selection: the pronucleate stage leads to a higher cumulative delivery rate than the early cleavage stage. Fertility and sterility, 74 (5): 946-952.
[100] Sharma GT, Dubey PK, Meur S. (2009), Survival and developmental competence of buffalo preantral follicles using three-dimensional collagen gel culture system. Animal reproduction science, 114(1):115-124.
[101] Shaw J, Bowles J, Koopman P, Wood E, Trounson A. (1996), Ovary and Ovulation: Fresh and cryopreserved ovarian tissue samples from donors with lymphoma transmit the cancer to graft recipients. Human Reproduction, 11 (8): 1668-1673.
[102] Shaw J, Cox S-L, Trounson A, Jenkin G. (2000), Evaluation of the long-term function of cryopreserved ovarian grafts in the mouse, implications for human applications. Molecular and cellular endocrinology, 161 (1): 103-110.
[103] Shaw SL, Quatrano RS. (1996), The role of targeted secretion in the establishment of cell polarity and the orientation of the division plane in Fucus zygotes. Development, 122 (9): 2623-2630.
[104] Siadat SF, Eimani H, Eftekhari-Yazdi P, Parivar K. (2008), Follicular preserving of incised transplanted ovary to mouse gluteus superficialis muscle. Science Reaserch Biology Journal of Islamic Azad University Garmsar Branch, 2 (4): 1-8.
[105] Skory RM, Xu Y, Shea LD, Woodruff TK. (2015), Engineering the ovarian cycle using in vitro follicle culture. Human Reproduction, 30 (6): 1386-1395.
[106] Soares M, Sahrari K, Chiti M, Amorim C, Ambroise J, Donnez J, Dolmans M-M. (2015),The best source of isolated stromal cells for the artificial ovary: medulla or cortex, cryopreserved or fresh? Human Reproduction, 30(7):1589-1598.
[107] Son W-Y, Park S-E, Lee K-A, Lee W-S, Ko J-J, Yoon T-K, Cha K-Y. (1996), Effects of 1, 2-propanediol and freezing-thawing on the in vitro developmental capacity of human immature oocytes. Fertility and sterility, 66 (6): 995-999.
[108] Spears N, Boland NI, Murray AA, Gosden RG. (1994), Mouse oocytes derived from in vitro grown primary ovarian follicles are fertile. Human Reproduction, 9 (3): 527-532.
[109] Stern C, Gook D, Hale L, Agresta F, Oldham J, Rozen G, Jobling T. (2013), First reported clinical pregnancy following heterotopic grafting of cryopreserved ovarian tissue in a woman after a bilateral oophorectomy. Human Reproduction, 28 (11): 2996-2999.
[110] Suh EK, Yang A, Kettenbach A, Bamberger C, Michaelis AH, Zhu Z, Elvin JA, Bronson RT, Crum CP, McKeon F. (2006), p63 protects the female germ line during meiotic arrest. Nature, 444 (7119): 624-628.
[111] Suzuki N, Yoshioka N, Takae S, Sugishita Y, Tamura M, Hashimoto S, Morimoto Y, Kawamura K: .(2015), Successful fertility preservation following ovarian tissue vitrification in patients with primary ovarian insufficiency. Hum Reprod, 30 (3): 608-615.
[112] Sztein J, Sweet H, Farley J, Mobraaten L. (1998), Cryopreservation and orthotopic transplantation of mouse ovaries: new approach in gamete banking. Biology of reproduction, 58 (4): 1071-1074.
[113] Tagler D, Makanji Y, Anderson NR, Woodruff TK, Shea LD. (2013), Supplemented αMEM/F12‐based medium enables the survival and growth of primary ovarian follicles encapsulated in alginate hydrogels. Biotechnology and bioengineering, 110 (12): 3258-3268.
[114] Ting AY, Petroff BK. (2010), Tamoxifen decreases ovarian follicular loss from experimental toxicant DMBA and chemotherapy agents cyclophosphamide and doxorubicin in the rat. J Assist Reprod Genet, 27 (11): 591-597.
[115] Ting AY, Yeoman RR, Lawson MS, Zelinski MB. (2011), In vitro development of secondary follicles from cryopreserved rhesus macaque ovarian tissue after slow-rate freeze or vitrification. Human reproduction, 26 (9): 2461-2472.
[116] Vanacker J, Luyckx V, Dolmans M-M, Des Rieux A, Jaeger J, Van Langendonckt A, Donnez J, Amorim CA. (2012), Transplantation of an alginate–matrigel matrix containing isolated ovarian cells: first step in developing a biodegradable scaffold to transplant isolated preantral follicles and ovarian cells. Biomaterials, 33 (26): 6079-6085.
[117] Verga Falzacappa C, Timperi E, Bucci B, Amendola D, Piergrossi P, D'Amico D, Santaguida MG, Centanni M, Misiti S. (2012), T(3) preserves ovarian granulosa cells from chemotherapy-induced apoptosis. The Journal of endocrinology, 215 (2): 281-289
[118] Waimey KE, Duncan FE, Su HI, Smith K, Wallach H, Jona K, Coutifaris C, Gracia CR, Shea LD, Brannigan RE. (2011), Future directions in oncofertility and fertility preservation: a report from the oncofertility consortium conference. Journal of adolescent and young adult oncology 2013, 2 (1): 25-30.
[119] Waterhouse T, Cox S-L, Snow M, Jenkin G, Shaw J. (2004), Offspring produced from heterotopic ovarian allografts in male and female recipient mice. Reproduction, 127 (6): 689-694.
[120] West ER, Shea LD, Woodruff TK. (2007), Engineering the follicle microenvironment. In: Seminars in reproductive medicine: 2007: Copyright© 2007 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA.: 287-299.
[121] White YA, Woods DC, Takai Y, Ishihara O, Seki H, Tilly JL. (2012), Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nature medicine, 18 (3): 413- 421.
[122] Woodruff TK. (2009), Preserving fertility during cancer treatment. Nature medicine, 15 (10): 1124-1125.
[123] Xu M, Barrett SL, West-Farrell E, Kondapalli LA, Kiesewetter SE, Shea LD, Woodruff TK. (2009), In vitro grown human ovarian follicles from cancer patients support oocyte growth. Human Reproduction, 24 (10): 2531-2540.
[124] Xu M, Fazleabas AT, Shikanov A, Jackson E, Barrett SL, Hirshfeld-Cytron J, Kiesewetter SE, Shea LD, Woodruff TK. (2011), In vitro oocyte maturation and preantral follicle culture from the luteal-phase baboon ovary produce mature oocytes. Biology of reproduction, 84 (4): 689-697.
[125] Xu M, Kreeger PK, Shea LD, Woodruff TK. (2006), Tissue-engineered follicles produce live, fertile offspring. Tissue engineering 12 (10): 2739-2746.
[126] Xu M, Pavone ME, Woodruff T. (2011), Fruitful progress to fertility: preserving oocytes from chemodestruction. Nature medicine, 17 (12): 1562-1563.
[127] Xu M, West-Farrell ER, Stouffer RL, Shea LD, Woodruff TK, Zelinski MB. (2009), Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles. Biology of reproduction, 81 (3): 587-594.
[128] Zelinski MB, Murphy MK, Lawson MS, Jurisicova A, Pau KY, Toscano NP, Jacob DS, Fanton JK, Casper RF, Dertinger SD et al. (2011), In vivo delivery of FTY720 prevents radiation-induced ovarian failure and infertility in adult female nonhuman primates. Fertility and sterility, 95 (4): 1440-1445 e1441-1447.
[129] Zhang H, Panula S, Petropoulos S, Edsgard D, Busayavalasa K, Liu L, Li X, Risal S, Shen Y, Shao J et al. (2015) Adult human and mouse ovaries lack DDX4-expressing functional oogonial stem cells. Nature medicine, 21 (10): 1116-1118.
_||_