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Published in: Reproductive Biology and Endocrinology 1/2017

Open Access 01-12-2017 | Review

Making gametes from alternate sources of stem cells: past, present and future

Authors: Deepa Bhartiya, Sandhya Anand, Hiren Patel, Seema Parte

Published in: Reproductive Biology and Endocrinology | Issue 1/2017

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Abstract

Infertile couples including cancer survivors stand to benefit from gametes differentiated from embryonic or induced pluripotent stem (ES/iPS) cells. It remains challenging to convert human ES/iPS cells into primordial germ-like cells (PGCLCs) en route to obtaining gametes. Considerable success was achieved in 2016 to obtain fertile offspring starting with mouse ES/iPS cells, however the specification of human ES/iPS cells into PGCLCs in vitro is still not achieved. Human ES cells will not yield patient-specific gametes unless and until hES cells are derived by somatic cell nuclear transfer (therapeutic cloning) whereas iPS cells retain the residual epigenetic memory of the somatic cells from which they are derived and also harbor genomic and mitochondrial DNA mutations. Thus, they may not be ideal starting material to produce autologus gametes, especially for aged couples. Pluripotent, very small embryonic-like stem cells (VSELs) have been reported in adult tissues including gonads, are relatively quiescent in nature, survive oncotherapy and can be detected in aged, non-functional gonads. Being developmentally equivalent to PGCs (natural precursors to gametes), VSELs spontaneously differentiate into gametes in vitro. It is also being understood that gonadal stem cells niche is compromised by oncotherapy and with age. Improving the gonadal somatic niche could regenerate non-functional gonads from endogenous VSELs to restore fertility. Niche cells (Sertoli/mesenchymal cells) can be directly transplanted and restore gonadal function by providing paracrine support to endogenous VSELs. This strategy has been successful in several mice studies already and resulted in live birth in a woman with pre-mature ovarian failure.
Literature
1.
go back to reference Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292:154–6.PubMedCrossRef Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature. 1981;292:154–6.PubMedCrossRef
2.
go back to reference Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A. 1981;78:7634–8.PubMedPubMedCentralCrossRef Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A. 1981;78:7634–8.PubMedPubMedCentralCrossRef
3.
go back to reference Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145–7.PubMedCrossRef Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, et al. Embryonic stem cell lines derived from human blastocysts. Science. 1998;282:1145–7.PubMedCrossRef
4.
go back to reference Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–76.PubMedCrossRef Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126:663–76.PubMedCrossRef
5.
go back to reference Ohta H, Kurimoto K, Okamoto I, Nakamura T, Yabuta Y, Miyauchi H, et al. Vitro expansion of mouse primordial germ cell-like cells recapitulates an epigenetic blank slate. EMBO J. 2017;36:1888–907.PubMedCrossRef Ohta H, Kurimoto K, Okamoto I, Nakamura T, Yabuta Y, Miyauchi H, et al. Vitro expansion of mouse primordial germ cell-like cells recapitulates an epigenetic blank slate. EMBO J. 2017;36:1888–907.PubMedCrossRef
7.
go back to reference Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell. 2011;146:519–32.PubMedCrossRef Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell. 2011;146:519–32.PubMedCrossRef
8.
go back to reference Kurimoto K, Saitou M. Mechanism and reconstitution in vitro of germ cell development in mammals. Cold Spring Harb Symp Quant Biol. 2015;80:147–54.PubMedCrossRef Kurimoto K, Saitou M. Mechanism and reconstitution in vitro of germ cell development in mammals. Cold Spring Harb Symp Quant Biol. 2015;80:147–54.PubMedCrossRef
10.
go back to reference Warrier S, Popovic M, van der Jeught M, Heindryckx B. Establishment and characterization of naïve pluripotency in human embryonic stem cells. Methods Mol Biol. 2016;1516:13–46.PubMedCrossRef Warrier S, Popovic M, van der Jeught M, Heindryckx B. Establishment and characterization of naïve pluripotency in human embryonic stem cells. Methods Mol Biol. 2016;1516:13–46.PubMedCrossRef
12.
go back to reference Fattahi A, Latifi Z, Ghasemnejad T, Nejabati HR, Nouri M. Insights into in vitro spermatogenesis in mammals: past, present, future. Mol Reprod Dev. 2017;84:560–75.PubMedCrossRef Fattahi A, Latifi Z, Ghasemnejad T, Nejabati HR, Nouri M. Insights into in vitro spermatogenesis in mammals: past, present, future. Mol Reprod Dev. 2017;84:560–75.PubMedCrossRef
13.
go back to reference Costa JN, Souza GB, Soares MAA, Ribeiro RP, van den Hurk R, Silva JRV. Vitro differentiation of primordial germ cells and oocyte-like cells from stem cells. Histol Histopathol. 2017;10:11917. Costa JN, Souza GB, Soares MAA, Ribeiro RP, van den Hurk R, Silva JRV. Vitro differentiation of primordial germ cells and oocyte-like cells from stem cells. Histol Histopathol. 2017;10:11917.
14.
go back to reference Wang JJ, Ge W, Liu JC, Klinger FG, Dyce PW, De Felici M, Shen W. Complete in vitro oogenesis: Retrospects and prospects. Cell Death Differ. 2017; doi:10.1038/cdd.2017.134. Wang JJ, Ge W, Liu JC, Klinger FG, Dyce PW, De Felici M, Shen W. Complete in vitro oogenesis: Retrospects and prospects. Cell Death Differ. 2017; doi:10.​1038/​cdd.​2017.​134.
15.
16.
go back to reference Bhartiya D, Shaikh A, Anand S, Patel H, Kapoor S, Sriraman K, et al. Endogenous, very small embryonic-like stem cells: critical review, therapeutic potential and a look ahead. Hum Reprod Update. 2016;23:41–76.PubMedCrossRef Bhartiya D, Shaikh A, Anand S, Patel H, Kapoor S, Sriraman K, et al. Endogenous, very small embryonic-like stem cells: critical review, therapeutic potential and a look ahead. Hum Reprod Update. 2016;23:41–76.PubMedCrossRef
18.
go back to reference Kucia M, Reca R, Campbell FR, Zuba-Surma E, Majka M, Ratajczak J, et al. A population of very small embryonic-like (VSEL) CXCR4(+) SSEA-1(+)Oct-4+ stem cells identified in adult bone marrow. Leukemia. 2006;20:857–69.PubMedCrossRef Kucia M, Reca R, Campbell FR, Zuba-Surma E, Majka M, Ratajczak J, et al. A population of very small embryonic-like (VSEL) CXCR4(+) SSEA-1(+)Oct-4+ stem cells identified in adult bone marrow. Leukemia. 2006;20:857–69.PubMedCrossRef
20.
go back to reference Shaikh A, Anand S, Kapoor S, Bhartiya D. Mouse bone marrow VSELs exhibit differentiation into three embryonic germ lineages and hematopoietic & germ cells in culture. Stem Cells Research and Reports. 2017; doi:10.1007/s12015-016-9714-0. Shaikh A, Anand S, Kapoor S, Bhartiya D. Mouse bone marrow VSELs exhibit differentiation into three embryonic germ lineages and hematopoietic & germ cells in culture. Stem Cells Research and Reports. 2017; doi:10.​1007/​s12015-016-9714-0.
21.
go back to reference Havens AM, Sun H, Shiozawa Y, Jung Y, Wang J, Mishra A, et al. Human and murine very small embryonic-like cells represent multipotent tissue progenitors, in vitro and in vivo. Stem Cells Dev. 2014;23:689–701.PubMedCrossRef Havens AM, Sun H, Shiozawa Y, Jung Y, Wang J, Mishra A, et al. Human and murine very small embryonic-like cells represent multipotent tissue progenitors, in vitro and in vivo. Stem Cells Dev. 2014;23:689–701.PubMedCrossRef
22.
go back to reference Monti M, Imberti B, Bianchi N, Pezzotta A, Morigi M, Del Fante C, et al. A novel method for isolation of pluripotent stem cells from human umbilical cord blood. Stem Cells Dev. 2017; doi:10.1089/scd.2017.0012. Monti M, Imberti B, Bianchi N, Pezzotta A, Morigi M, Del Fante C, et al. A novel method for isolation of pluripotent stem cells from human umbilical cord blood. Stem Cells Dev. 2017; doi:10.​1089/​scd.​2017.​0012.
23.
go back to reference Shirazi R, Zarnani AH, Soleimani M, Nayernia K, Ragerdi Kashani I. Differentiation of bone marrow-derived stage-specific embryonic antigen 1 positive pluripotent stem cells into male germ cells. Microsc Res Tech. 2017;80:430–40.PubMedCrossRef Shirazi R, Zarnani AH, Soleimani M, Nayernia K, Ragerdi Kashani I. Differentiation of bone marrow-derived stage-specific embryonic antigen 1 positive pluripotent stem cells into male germ cells. Microsc Res Tech. 2017;80:430–40.PubMedCrossRef
24.
go back to reference Bhartiya D, Kasiviswanathan S, Unni SK, Pethe P, Dhabalia JV, Patwardhan S, et al. Newer insights into premeiotic development of germ cells in adult human testis using Oct-4 as a stem cell marker. J Histochem Cytochem. 2010;58:1093–106.PubMedPubMedCentralCrossRef Bhartiya D, Kasiviswanathan S, Unni SK, Pethe P, Dhabalia JV, Patwardhan S, et al. Newer insights into premeiotic development of germ cells in adult human testis using Oct-4 as a stem cell marker. J Histochem Cytochem. 2010;58:1093–106.PubMedPubMedCentralCrossRef
25.
go back to reference Anand S, Bhartiya D, Sriraman K, Patel H, Manjramkar DD. Very small embryonic-like stem cells survive and restore spermatogenesis after busulphan treatment in mouse testis. J Stem Cell Res Ther. 2014;4:216. doi:10.4172/2157-7633.1000216. Anand S, Bhartiya D, Sriraman K, Patel H, Manjramkar DD. Very small embryonic-like stem cells survive and restore spermatogenesis after busulphan treatment in mouse testis. J Stem Cell Res Ther. 2014;4:216. doi:10.​4172/​2157-7633.​1000216.
26.
go back to reference Anand S, Bhartiya D, Sriraman K, Mallick A. Underlying mechanisms that restore spermatogenesis on transplanting healthy niche cells in busulphan treated mouse testis. Stem Cell Rev. 2016;12:682–97.PubMedCrossRef Anand S, Bhartiya D, Sriraman K, Mallick A. Underlying mechanisms that restore spermatogenesis on transplanting healthy niche cells in busulphan treated mouse testis. Stem Cell Rev. 2016;12:682–97.PubMedCrossRef
27.
go back to reference Patel H, Bhartiya D. Testicular stem cells express follicle stimulating hormone receptors and are directly modulated by FSH. Reprod Sci. 2016;23:1493–508.PubMedCrossRef Patel H, Bhartiya D. Testicular stem cells express follicle stimulating hormone receptors and are directly modulated by FSH. Reprod Sci. 2016;23:1493–508.PubMedCrossRef
28.
go back to reference Virant-Klun I, Zech N, Rozman P, Vogler A, Cvjeticanin B, Klemenc P, et al. Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes. Differentiation. 2008;76:843–56.PubMedCrossRef Virant-Klun I, Zech N, Rozman P, Vogler A, Cvjeticanin B, Klemenc P, et al. Putative stem cells with an embryonic character isolated from the ovarian surface epithelium of women with no naturally present follicles and oocytes. Differentiation. 2008;76:843–56.PubMedCrossRef
29.
go back to reference Virant-Klun I, Rozman P, Cvjeticanin B, Vrtacnik-Bokal E, Novakovic S, Rülicke T, et al. Parthenogenetic embryo-like structures in the human ovarian surface epithelium cell culture in postmenopausal women with no naturally present follicles and oocytes. Stem Cells Dev. 2009;18:137–49.PubMedCrossRef Virant-Klun I, Rozman P, Cvjeticanin B, Vrtacnik-Bokal E, Novakovic S, Rülicke T, et al. Parthenogenetic embryo-like structures in the human ovarian surface epithelium cell culture in postmenopausal women with no naturally present follicles and oocytes. Stem Cells Dev. 2009;18:137–49.PubMedCrossRef
30.
go back to reference Parte S, Bhartiya D, Telang J, Daithankar V, Salvi V, Zaveri K, et al. Detection, characterization, and spontaneous differentiation in vitro of very small embryonic-like putative stem cells in adult mammalian ovary. Stem Cells Dev. 2011;20:1451–64.PubMedPubMedCentralCrossRef Parte S, Bhartiya D, Telang J, Daithankar V, Salvi V, Zaveri K, et al. Detection, characterization, and spontaneous differentiation in vitro of very small embryonic-like putative stem cells in adult mammalian ovary. Stem Cells Dev. 2011;20:1451–64.PubMedPubMedCentralCrossRef
31.
go back to reference Sriraman K, Bhartiya D, Anand S, Bhutda S. Mouse ovarian very small embryonic-like stem cells resist chemotherapy and retain ability to initiate oocyte-specific differentiation. Reprod Sci. 2015;22:884–903.PubMedPubMedCentralCrossRef Sriraman K, Bhartiya D, Anand S, Bhutda S. Mouse ovarian very small embryonic-like stem cells resist chemotherapy and retain ability to initiate oocyte-specific differentiation. Reprod Sci. 2015;22:884–903.PubMedPubMedCentralCrossRef
32.
go back to reference Esmaeilian Y, Atalay A, Erdemli E. Putative germline and pluripotent stem cells in adult mouse ovary and their in vitro differentiation potential into oocyte-like and somatic cells. Zygote. 2017;25(3):358–75.PubMedCrossRef Esmaeilian Y, Atalay A, Erdemli E. Putative germline and pluripotent stem cells in adult mouse ovary and their in vitro differentiation potential into oocyte-like and somatic cells. Zygote. 2017;25(3):358–75.PubMedCrossRef
35.
go back to reference Martinez F. International Society for Fertility Preservation–ESHRE–ASRM Expert Working Group. Update on fertility preservation from the Barcelona International Society for Fertility Preservation-ESHRE-ASRM 2015 expert meeting: Indications, results and future perspectives. Fertil Steril. 2017;108:407–15.PubMedCrossRef Martinez F. International Society for Fertility Preservation–ESHRE–ASRM Expert Working Group. Update on fertility preservation from the Barcelona International Society for Fertility Preservation-ESHRE-ASRM 2015 expert meeting: Indications, results and future perspectives. Fertil Steril. 2017;108:407–15.PubMedCrossRef
38.
go back to reference Bhartiya D. Use of very small embryonic-like stem cells to avoid legal, ethical, and safety issues associated with oncofertility. JAMA Oncol. 2016;2(5):689.PubMedCrossRef Bhartiya D. Use of very small embryonic-like stem cells to avoid legal, ethical, and safety issues associated with oncofertility. JAMA Oncol. 2016;2(5):689.PubMedCrossRef
39.
go back to reference Geijsen N, Horoschak M, Kim K, Gribnau J, Eggan K, Daley GQ. Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature. 2004;427:148–54.PubMedCrossRef Geijsen N, Horoschak M, Kim K, Gribnau J, Eggan K, Daley GQ. Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature. 2004;427:148–54.PubMedCrossRef
40.
go back to reference Nayernia K, Nolte J, Michelmann HW, Lee JH, Rathsack K, Drusenheimer N, et al. In vitro-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice. Dev Cell. 2006;11:125–32.PubMedCrossRef Nayernia K, Nolte J, Michelmann HW, Lee JH, Rathsack K, Drusenheimer N, et al. In vitro-differentiated embryonic stem cells give rise to male gametes that can generate offspring mice. Dev Cell. 2006;11:125–32.PubMedCrossRef
41.
go back to reference Nayernia K, Lee JH, Lako M, Armstrong L, Herbert M, Li M, et al. RETRACTION - in vitro derivation of human sperm from embryonic stem cells. Stem Cells Dev. 2009; Nayernia K, Lee JH, Lako M, Armstrong L, Herbert M, Li M, et al. RETRACTION - in vitro derivation of human sperm from embryonic stem cells. Stem Cells Dev. 2009;
42.
go back to reference Eguizabal C, Montserrat N, Vassena R, Barragan M, Garreta E, Garcia-Quevedo L. Etal. Complete meiosis from human induced pluripotent stem cells. Stem Cells. 2011;29:1186–95.PubMedCrossRef Eguizabal C, Montserrat N, Vassena R, Barragan M, Garreta E, Garcia-Quevedo L. Etal. Complete meiosis from human induced pluripotent stem cells. Stem Cells. 2011;29:1186–95.PubMedCrossRef
43.
go back to reference Panula S, Medrano JV, Kee K, Bergström R, Nguyen HN, Byers B, et al. Human germ cell differentiation from fetal- and adult-derived induced pluripotent stem cells. Hum Mol Genet. 2011;20:752–62.PubMedCrossRef Panula S, Medrano JV, Kee K, Bergström R, Nguyen HN, Byers B, et al. Human germ cell differentiation from fetal- and adult-derived induced pluripotent stem cells. Hum Mol Genet. 2011;20:752–62.PubMedCrossRef
44.
go back to reference Zhou Q, Wang M, Yuan Y, Wang X, Fu R, Wan H, et al. Complete meiosis from embryonic stem cell-derived germ cells in vitro. Cell Stem Cell 2016;18:330–340. Zhou Q, Wang M, Yuan Y, Wang X, Fu R, Wan H, et al. Complete meiosis from embryonic stem cell-derived germ cells in vitro. Cell Stem Cell 2016;18:330–340.
45.
go back to reference Medrano JV, Martínez-Arroyo AM, Míguez JM. MorenoI, Martínez S, Quiñonero a,et al. human somatic cells subjected to genetic induction with six germ line-related factors display meiotic germ cell-like features. Sci Rep. 2016;6:24956. doi:10.1038/srep24956. PubMedPubMedCentralCrossRef Medrano JV, Martínez-Arroyo AM, Míguez JM. MorenoI, Martínez S, Quiñonero a,et al. human somatic cells subjected to genetic induction with six germ line-related factors display meiotic germ cell-like features. Sci Rep. 2016;6:24956. doi:10.​1038/​srep24956.​ PubMedPubMedCentralCrossRef
46.
go back to reference Ishikura Y, Yabuta Y, Ohta H, Hayashi K, Nakamura T, Okamoto I, et al. Vitro derivation and propagation of spermatogonial stem cell activity from mouse pluripotent stem cells. Cell Rep. 2016;17:2789–804.PubMedCrossRef Ishikura Y, Yabuta Y, Ohta H, Hayashi K, Nakamura T, Okamoto I, et al. Vitro derivation and propagation of spermatogonial stem cell activity from mouse pluripotent stem cells. Cell Rep. 2016;17:2789–804.PubMedCrossRef
47.
go back to reference Lim JJ, Sung SY, Kim HJ, Song SH, Hong JY, Yoon TK, et al. Long-term proliferation and characterization of human spermatogonial stem cells obtained from obstructive and non-obstructive azoospermia under exogenous feeder-free culture conditions. Cell Prolif. 2010;43:405–17.PubMedCrossRef Lim JJ, Sung SY, Kim HJ, Song SH, Hong JY, Yoon TK, et al. Long-term proliferation and characterization of human spermatogonial stem cells obtained from obstructive and non-obstructive azoospermia under exogenous feeder-free culture conditions. Cell Prolif. 2010;43:405–17.PubMedCrossRef
48.
go back to reference Izadyar F, Wong J, Maki C, Pacchiarotti J, Ramos T, Howerton K, et al. Identification and characterization of repopulating spermatogonial stem cells from the adult human testis. Hum Reprod. 2011;26:1296–306.PubMedCrossRef Izadyar F, Wong J, Maki C, Pacchiarotti J, Ramos T, Howerton K, et al. Identification and characterization of repopulating spermatogonial stem cells from the adult human testis. Hum Reprod. 2011;26:1296–306.PubMedCrossRef
49.
go back to reference Stimpfel M, Skutella T, Kubista M, Malicev E, Conrad S, Virant-Klun I. Potential stemness of frozen-thawed testicular biopsies without sperm in infertile men included into the in vitro fertilization programme. J Biomed Biotechnol. 2012;2012:291038. doi:10.1155/2012/291038.PubMedPubMedCentralCrossRef Stimpfel M, Skutella T, Kubista M, Malicev E, Conrad S, Virant-Klun I. Potential stemness of frozen-thawed testicular biopsies without sperm in infertile men included into the in vitro fertilization programme. J Biomed Biotechnol. 2012;2012:291038. doi:10.​1155/​2012/​291038.PubMedPubMedCentralCrossRef
51.
go back to reference Bhartiya D, Kasiviswananthan S, Shaikh A. Cellular origin of testis-derived pluripotent stem cells: a case for very small embryonic-like stem cells. Stem Cells Dev. 2012;21(5):670–4.PubMedCrossRef Bhartiya D, Kasiviswananthan S, Shaikh A. Cellular origin of testis-derived pluripotent stem cells: a case for very small embryonic-like stem cells. Stem Cells Dev. 2012;21(5):670–4.PubMedCrossRef
52.
go back to reference KurkureP PM, Dhamankar V, Bakshi G. Very small embryonic-like stem cells (VSELs) detected in azoospermic testicular biopsies of adult survivors of childhood cancer. Reprod Biol Endocrinol. 2015;13:122. doi:10.1186/s12958-015-0121-1.CrossRef KurkureP PM, Dhamankar V, Bakshi G. Very small embryonic-like stem cells (VSELs) detected in azoospermic testicular biopsies of adult survivors of childhood cancer. Reprod Biol Endocrinol. 2015;13:122. doi:10.​1186/​s12958-015-0121-1.CrossRef
53.
go back to reference Ratajczak MZ. Igf2-H19, an imprinted tandem Yin-Yang gene and its emerging role in development, proliferation of pluripotent stem cells, senescence and cancerogenesis. J Stem Cell Res Ther. 2012;2(4). pii: 108. Ratajczak MZ. Igf2-H19, an imprinted tandem Yin-Yang gene and its emerging role in development, proliferation of pluripotent stem cells, senescence and cancerogenesis. J Stem Cell Res Ther. 2012;2(4). pii: 108.
58.
go back to reference Sato T, Katagiri K, Gohbara A, Inoue K, Ogonuki N, Ogura A, et al. Vitro production of functional sperm in cultured neonatal mouse testes. Nature. 2011;471:504–7.PubMedCrossRef Sato T, Katagiri K, Gohbara A, Inoue K, Ogonuki N, Ogura A, et al. Vitro production of functional sperm in cultured neonatal mouse testes. Nature. 2011;471:504–7.PubMedCrossRef
59.
60.
go back to reference Sato T, Katagiri K, Kubota Y, Ogawa T. In Vitro sperm production from mouse spermatogonial stem cell lines using an organ culture method. Nat Protoc. 2013;8:2098–104.PubMedCrossRef Sato T, Katagiri K, Kubota Y, Ogawa T. In Vitro sperm production from mouse spermatogonial stem cell lines using an organ culture method. Nat Protoc. 2013;8:2098–104.PubMedCrossRef
61.
go back to reference Elhija AM, Lunenfeld E, Schlatt S, Huleihel M. Differentiation of murine male germ cells to spermatozoain a soft agar culture system. Asian J Androl. 2012;14:285–93.PubMedCrossRef Elhija AM, Lunenfeld E, Schlatt S, Huleihel M. Differentiation of murine male germ cells to spermatozoain a soft agar culture system. Asian J Androl. 2012;14:285–93.PubMedCrossRef
62.
go back to reference Huleihel M, Nourashrafeddin S, Plant TM. Application of three-dimensional culture systems to study mammalian spermatogenesis, with an emphasis on the rhesus monkey (Macaca Mulatta). Asian J Androl. 2015;17:972–80.PubMedPubMedCentralCrossRef Huleihel M, Nourashrafeddin S, Plant TM. Application of three-dimensional culture systems to study mammalian spermatogenesis, with an emphasis on the rhesus monkey (Macaca Mulatta). Asian J Androl. 2015;17:972–80.PubMedPubMedCentralCrossRef
64.
go back to reference Giudice MG, de Michele F, Poels J, Vermeulen M, Wyns C. Update on fertility restoration from prepubertal spermatogonial stem cells: how far are we from clinical practice? Stem Cell Res. 2017;21:171–7.PubMedCrossRef Giudice MG, de Michele F, Poels J, Vermeulen M, Wyns C. Update on fertility restoration from prepubertal spermatogonial stem cells: how far are we from clinical practice? Stem Cell Res. 2017;21:171–7.PubMedCrossRef
65.
go back to reference Bhartiya D, Anand S. Letter to editor. Effects of oncotherapy on testicular stem cells and niche. Mol Hum Reproduction. 2017;23:654–5.CrossRef Bhartiya D, Anand S. Letter to editor. Effects of oncotherapy on testicular stem cells and niche. Mol Hum Reproduction. 2017;23:654–5.CrossRef
66.
go back to reference Vahdati A, Fathi A, Hajihoseini M, Aliborzi G, Hosseini E. The regenerative effect of bone marrow-derived stem cells in spermatogenesis of infertile hamster. World J Plast Surg. 2017;6:18–25.PubMedPubMedCentral Vahdati A, Fathi A, Hajihoseini M, Aliborzi G, Hosseini E. The regenerative effect of bone marrow-derived stem cells in spermatogenesis of infertile hamster. World J Plast Surg. 2017;6:18–25.PubMedPubMedCentral
67.
go back to reference Maghen L, Shlush E, Gat I, Filice M, Barretto TA, Jarvi K, et al. Human umbilical perivascular cells (HUCPVCs): a novel source of mesenchymal stromal-like (MSC) cells to support the regeneration of the testicular niche. Reproduction. 2017;153:85–95.CrossRef Maghen L, Shlush E, Gat I, Filice M, Barretto TA, Jarvi K, et al. Human umbilical perivascular cells (HUCPVCs): a novel source of mesenchymal stromal-like (MSC) cells to support the regeneration of the testicular niche. Reproduction. 2017;153:85–95.CrossRef
68.
go back to reference Abd Allah SH, Pasha HF, Abdelrahman AA, Mazen NF. Molecular effect of human umbilical cord blood CD34-positive and CD34-negative stem cells and their conjugate in azoospermic mice. Mol Cell Biochem. 2017;428:179–91.PubMedCrossRef Abd Allah SH, Pasha HF, Abdelrahman AA, Mazen NF. Molecular effect of human umbilical cord blood CD34-positive and CD34-negative stem cells and their conjugate in azoospermic mice. Mol Cell Biochem. 2017;428:179–91.PubMedCrossRef
69.
go back to reference Ghasemzadeh-Hasankolaei M, Batavani R, Eslaminejad MB, Sayahpour F. Transplantation of autologous bone marrow mesenchymal stem cells into the testes of infertile male rats and new germ cell formation. Int J Stem Cells. 2016;9:250–63.PubMedPubMedCentralCrossRef Ghasemzadeh-Hasankolaei M, Batavani R, Eslaminejad MB, Sayahpour F. Transplantation of autologous bone marrow mesenchymal stem cells into the testes of infertile male rats and new germ cell formation. Int J Stem Cells. 2016;9:250–63.PubMedPubMedCentralCrossRef
70.
go back to reference Rahmanifar F, Tamadon A, Mehrabani D, Zare S, Abasi S, Keshavarz S, et al. Histomorphometric evaluation of treatment of rat azoospermic seminiferous tubules by allotransplantation of bone marrow-derived mesenchymal stem cells. Iran J Basic Med Sci. 2016;19:653–61.PubMedPubMedCentral Rahmanifar F, Tamadon A, Mehrabani D, Zare S, Abasi S, Keshavarz S, et al. Histomorphometric evaluation of treatment of rat azoospermic seminiferous tubules by allotransplantation of bone marrow-derived mesenchymal stem cells. Iran J Basic Med Sci. 2016;19:653–61.PubMedPubMedCentral
71.
go back to reference Chen H, Tang QL, XY W, Xie LC, Lin LM, Ho GY, Ma L. Differentiation of human umbilical cord mesenchymal stem cells into germ-like cells in mouse seminiferous tubules. Mol Med Rep. 2015;12:819–28.PubMedPubMedCentralCrossRef Chen H, Tang QL, XY W, Xie LC, Lin LM, Ho GY, Ma L. Differentiation of human umbilical cord mesenchymal stem cells into germ-like cells in mouse seminiferous tubules. Mol Med Rep. 2015;12:819–28.PubMedPubMedCentralCrossRef
72.
go back to reference Yang RF, Liu TH, Zhao K, Xiong CL. Enhancement of mouse germ cell-associated genes expression by injection of human umbilical cord mesenchymal stem cells into the testis of chemical-induced azoospermic mice. Asian J Androl. 2014;16:698–704.PubMedPubMedCentralCrossRef Yang RF, Liu TH, Zhao K, Xiong CL. Enhancement of mouse germ cell-associated genes expression by injection of human umbilical cord mesenchymal stem cells into the testis of chemical-induced azoospermic mice. Asian J Androl. 2014;16:698–704.PubMedPubMedCentralCrossRef
73.
go back to reference Sabbaghi MA, Bahrami AR, Feizzade B. Trial evaluation of bone marrow derived mesenchymal stem cells (MSCs) transplantation in revival of spermatogenesis in testicular torsion. Middle East Fertility Society Journal. 2012;17(4):243–9.CrossRef Sabbaghi MA, Bahrami AR, Feizzade B. Trial evaluation of bone marrow derived mesenchymal stem cells (MSCs) transplantation in revival of spermatogenesis in testicular torsion. Middle East Fertility Society Journal. 2012;17(4):243–9.CrossRef
74.
go back to reference Aziz AE, Dalia H, Metwally HG. The effect of stem cell therapy versus melatonin on the changes induced by busulfan in the testes of adult rat: histological and immuno-histochemical studies. The Egyptian J of Histology. 2013; doi:10.1097/01.EHX. 0000425579.77855.ea. Aziz AE, Dalia H, Metwally HG. The effect of stem cell therapy versus melatonin on the changes induced by busulfan in the testes of adult rat: histological and immuno-histochemical studies. The Egyptian J of Histology. 2013; doi:10.​1097/​01.​EHX.​ 0000425579.​77855.​ea.
75.
go back to reference Hübner K, Fuhrmann G, Christenson LK, Kehler J, Reinbold R, De La Fuente R, et al. Derivation of oocytes from mouse embryonic stem cells. Science. 2003;300:1251–6.PubMedCrossRef Hübner K, Fuhrmann G, Christenson LK, Kehler J, Reinbold R, De La Fuente R, et al. Derivation of oocytes from mouse embryonic stem cells. Science. 2003;300:1251–6.PubMedCrossRef
76.
go back to reference Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, Saitou M. Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science. 2012;338:971–5.PubMedCrossRef Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, Saitou M. Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science. 2012;338:971–5.PubMedCrossRef
77.
go back to reference Hayashi K, Saitou M. Generation of eggs from mouse embryonic stem cells and induced pluripotent stem cells. Nat Protoc. 2013;8:1513–24.PubMedCrossRef Hayashi K, Saitou M. Generation of eggs from mouse embryonic stem cells and induced pluripotent stem cells. Nat Protoc. 2013;8:1513–24.PubMedCrossRef
78.
go back to reference Deglincerti A, Brivanlou AH. The generation of sex cells. Cell Res. 2015;25(3):267-8. Deglincerti A, Brivanlou AH. The generation of sex cells. Cell Res. 2015;25(3):267-8.
79.
go back to reference Morohaku K, Hirao Y, Obata Y. Developmental competence of oocytes grown in vitro: has it peaked already. J Reprod Dev. 2016;62:1–5.PubMedCrossRef Morohaku K, Hirao Y, Obata Y. Developmental competence of oocytes grown in vitro: has it peaked already. J Reprod Dev. 2016;62:1–5.PubMedCrossRef
80.
go back to reference Morohaku K, Tanimoto R, Sasaki K, Kawahara-Miki R, Kono T, Hayashi K, Hirao Y, Obata Y. Complete in vitro generation of fertile oocytes from mouse primordial germ cells. Proc Natl Acad Sci U S A. 2016;113:9021–6.PubMedPubMedCentralCrossRef Morohaku K, Tanimoto R, Sasaki K, Kawahara-Miki R, Kono T, Hayashi K, Hirao Y, Obata Y. Complete in vitro generation of fertile oocytes from mouse primordial germ cells. Proc Natl Acad Sci U S A. 2016;113:9021–6.PubMedPubMedCentralCrossRef
81.
go back to reference Hikabe O, Hamazaki N, Nagamatsu G, Obata Y, Hirao Y, Hamada N, et al. Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature. 2016;539:299–303.PubMedCrossRef Hikabe O, Hamazaki N, Nagamatsu G, Obata Y, Hirao Y, Hamada N, et al. Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature. 2016;539:299–303.PubMedCrossRef
83.
go back to reference Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet. 2008;9:129–40.PubMedCrossRef Sasaki H, Matsui Y. Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet. 2008;9:129–40.PubMedCrossRef
84.
go back to reference Hayashi K, Hikabe O, Obata Y, Hirao Y. Reconstitution of mouse oogenesis in a dish from pluripotent stem cells. Nat Protoc. 2017;12:1733–44.PubMedCrossRef Hayashi K, Hikabe O, Obata Y, Hirao Y. Reconstitution of mouse oogenesis in a dish from pluripotent stem cells. Nat Protoc. 2017;12:1733–44.PubMedCrossRef
87.
go back to reference Edessy M, Hosni HN, Shady Y, Waf Y, Bakr S, Kamel M. Autologous stem cells therapy, the first baby of idiopathic premature ovarian failure. Acta Medica International. 2016;3:19–23.CrossRef Edessy M, Hosni HN, Shady Y, Waf Y, Bakr S, Kamel M. Autologous stem cells therapy, the first baby of idiopathic premature ovarian failure. Acta Medica International. 2016;3:19–23.CrossRef
88.
go back to reference Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature. 2004;428:145–50.PubMedCrossRef Johnson J, Canning J, Kaneko T, Pru JK, Tilly JL. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature. 2004;428:145–50.PubMedCrossRef
90.
go back to reference Zou K, Yuan Z, Yang Z, Luo H, Sun K, Zhou L, Xiang J, Shi L, Yu Q, Zhang Y, Hou R, Wu J. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol. 2009;11:631–6.PubMedCrossRef Zou K, Yuan Z, Yang Z, Luo H, Sun K, Zhou L, Xiang J, Shi L, Yu Q, Zhang Y, Hou R, Wu J. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol. 2009;11:631–6.PubMedCrossRef
91.
go back to reference White YA, Woods DC, Takai Y, Ishihara O, Seki H, Tilly JL. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med. 2012;18:413–21.PubMedPubMedCentralCrossRef White YA, Woods DC, Takai Y, Ishihara O, Seki H, Tilly JL. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med. 2012;18:413–21.PubMedPubMedCentralCrossRef
92.
go back to reference Woods DC, Tilly JL. Isolation, characterization and propagation of mitotically active germ cells from adult mouse and human ovaries. Nat Protoc. 2013;8:966–88.PubMedPubMedCentralCrossRef Woods DC, Tilly JL. Isolation, characterization and propagation of mitotically active germ cells from adult mouse and human ovaries. Nat Protoc. 2013;8:966–88.PubMedPubMedCentralCrossRef
93.
go back to reference Eppig JJ, O'Brien MJ. Development in vitro of mouse oocytes from primordial follicles. Biol Reprod. 1996;54:197–207.PubMedCrossRef Eppig JJ, O'Brien MJ. Development in vitro of mouse oocytes from primordial follicles. Biol Reprod. 1996;54:197–207.PubMedCrossRef
94.
go back to reference O'Brien MJ, Pendola JK, Eppig JJA. Revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol Reprod. 2003;68:1682–6.PubMedCrossRef O'Brien MJ, Pendola JK, Eppig JJA. Revised protocol for in vitro development of mouse oocytes from primordial follicles dramatically improves their developmental competence. Biol Reprod. 2003;68:1682–6.PubMedCrossRef
95.
go back to reference Shen W, Li L, Zhang D, Pan Q, Ding M, Deng H. Mouse oocytes derived from fetal germ cells are competent to support the development of embryos by in vitro fertilization. Mol Reprod Dev. 2006;73:1312–7.PubMedCrossRef Shen W, Li L, Zhang D, Pan Q, Ding M, Deng H. Mouse oocytes derived from fetal germ cells are competent to support the development of embryos by in vitro fertilization. Mol Reprod Dev. 2006;73:1312–7.PubMedCrossRef
96.
go back to reference Chiti MC, Dolmans MM, Lucci CM, Paulini F, Donnez J, Amorim CA. Further insights into the impact of mouse follicle stage on graft outcome in an artificial ovary environment. Mol Hum Reprod. 2017;23:381–92.PubMedCrossRef Chiti MC, Dolmans MM, Lucci CM, Paulini F, Donnez J, Amorim CA. Further insights into the impact of mouse follicle stage on graft outcome in an artificial ovary environment. Mol Hum Reprod. 2017;23:381–92.PubMedCrossRef
98.
go back to reference Kniazeva E, Hardy AN, Boukaidi SA, Woodruff TK, Jeruss JS, Shea LD. Primordial follicle transplantation within designer biomaterial grafts produce live births in a mouse infertility model. Sci Rep. 2015;5:17709.PubMedPubMedCentralCrossRef Kniazeva E, Hardy AN, Boukaidi SA, Woodruff TK, Jeruss JS, Shea LD. Primordial follicle transplantation within designer biomaterial grafts produce live births in a mouse infertility model. Sci Rep. 2015;5:17709.PubMedPubMedCentralCrossRef
99.
100.
go back to reference Carvalho BR, Kliemchen J, Woodruff TK. Ethical, moral and other aspects related to fertility preservation in cancer patients. JBRA Assist Reprod. 2017;21:45–8.PubMedPubMedCentral Carvalho BR, Kliemchen J, Woodruff TK. Ethical, moral and other aspects related to fertility preservation in cancer patients. JBRA Assist Reprod. 2017;21:45–8.PubMedPubMedCentral
101.
go back to reference Jensen AK, Macklon KT, Fedder J, Ernst E, Humaidan P, Andersen CY. 86 successful births and 9 ongoing pregnancies worldwide in women transplanted with frozen-thawed ovarian tissue: focus on birth and perinatal outcome in 40 of these children. J Assist Reprod Genet. 2017;34(3):325–36.PubMedCrossRef Jensen AK, Macklon KT, Fedder J, Ernst E, Humaidan P, Andersen CY. 86 successful births and 9 ongoing pregnancies worldwide in women transplanted with frozen-thawed ovarian tissue: focus on birth and perinatal outcome in 40 of these children. J Assist Reprod Genet. 2017;34(3):325–36.PubMedCrossRef
102.
go back to reference Oktay K, Türkçüoğlu I, Rodriguez-Wallberg KA. Four spontaneous pregnancies and three live births following subcutaneous transplantation of frozen banked ovarian tissue: what is the explanation? Fertil Steril. 2011;95(804):e7–10. Oktay K, Türkçüoğlu I, Rodriguez-Wallberg KA. Four spontaneous pregnancies and three live births following subcutaneous transplantation of frozen banked ovarian tissue: what is the explanation? Fertil Steril. 2011;95(804):e7–10.
103.
go back to reference Niikura Y, Niikura T, Tilly JL. Aged mouse ovaries possess rare premeiotic germ cells that can generate oocytes following transplantation into a young host environment. Aging (Albany NY). 2009;1:971–8.CrossRef Niikura Y, Niikura T, Tilly JL. Aged mouse ovaries possess rare premeiotic germ cells that can generate oocytes following transplantation into a young host environment. Aging (Albany NY). 2009;1:971–8.CrossRef
104.
go back to reference Massasa E, Costa XS, Taylor HS. Failure of the stem cell niche rather than loss of oocyte stem cells in the aging ovary. Aging (Albany NY). 2010;2:1–2.CrossRef Massasa E, Costa XS, Taylor HS. Failure of the stem cell niche rather than loss of oocyte stem cells in the aging ovary. Aging (Albany NY). 2010;2:1–2.CrossRef
105.
go back to reference Oktay K, Goswami S, Darzynkiewicz Z. Manipulating ovarian aging: a new frontier in fertility preservation. Aging (Albany NY). 2011;3:19–21.CrossRef Oktay K, Goswami S, Darzynkiewicz Z. Manipulating ovarian aging: a new frontier in fertility preservation. Aging (Albany NY). 2011;3:19–21.CrossRef
107.
go back to reference Wang Z, Wang Y, Yang T, Li J, Yang X. Study of the reparative effects of menstrual derived stem cells on premature ovarian failure in mice. Stem Cell Res Ther. 2017;8:11.PubMedPubMedCentralCrossRef Wang Z, Wang Y, Yang T, Li J, Yang X. Study of the reparative effects of menstrual derived stem cells on premature ovarian failure in mice. Stem Cell Res Ther. 2017;8:11.PubMedPubMedCentralCrossRef
108.
go back to reference Fouad H, Sabry D, Elsetohy K, Fathy N. Therapeutic efficacy of amniotic membrane stem cells and adipose tissue stem cells in rats with chemically induced ovarian failure. J Adv Res. 2016;7:233–41.PubMedCrossRef Fouad H, Sabry D, Elsetohy K, Fathy N. Therapeutic efficacy of amniotic membrane stem cells and adipose tissue stem cells in rats with chemically induced ovarian failure. J Adv Res. 2016;7:233–41.PubMedCrossRef
109.
go back to reference Song D, Zhong Y, Qian C, Zou Q, Ou J, Shi Y. Etal. Human umbilical cord mesenchymal stem cells therapy in cyclophosphamide-induced premature ovarian failure rat model. Bio Med Res Int. 2016:2517514. Song D, Zhong Y, Qian C, Zou Q, Ou J, Shi Y. Etal. Human umbilical cord mesenchymal stem cells therapy in cyclophosphamide-induced premature ovarian failure rat model. Bio Med Res Int. 2016:2517514.
110.
go back to reference Kilic S, Pinarli F, Ozogul C, Tasdemir N, NazSarac G, Delibasi T. Protection from cyclophosphamide-induced ovarian damage with bone marrow-derived mesenchymal stem cells during puberty. Gynecol Endocrinol. 2014;30:135–40.PubMedCrossRef Kilic S, Pinarli F, Ozogul C, Tasdemir N, NazSarac G, Delibasi T. Protection from cyclophosphamide-induced ovarian damage with bone marrow-derived mesenchymal stem cells during puberty. Gynecol Endocrinol. 2014;30:135–40.PubMedCrossRef
111.
go back to reference Liu J, Zhang H, Zhang Y, Li N, Wen Y, Cao F, Ai H, Xue X. Homing and restorative effects of bone marrow-derived mesenchymal stem cells on cisplatin injured ovaries in rats. Mol Cells. 2014;37:865–72.PubMedPubMedCentralCrossRef Liu J, Zhang H, Zhang Y, Li N, Wen Y, Cao F, Ai H, Xue X. Homing and restorative effects of bone marrow-derived mesenchymal stem cells on cisplatin injured ovaries in rats. Mol Cells. 2014;37:865–72.PubMedPubMedCentralCrossRef
112.
go back to reference Liu T, Huang Y, Zhang J, Qin W, Chi H, Chen J, Yu Z, Chen C. Transplantation of human menstrual blood stem cells to treat premature ovarian failure in mouse model. Stem Cells Dev. 2014;23:1548–57.PubMedPubMedCentralCrossRef Liu T, Huang Y, Zhang J, Qin W, Chi H, Chen J, Yu Z, Chen C. Transplantation of human menstrual blood stem cells to treat premature ovarian failure in mouse model. Stem Cells Dev. 2014;23:1548–57.PubMedPubMedCentralCrossRef
113.
go back to reference Lai D, Wang F, Dong Z, Zhang Q. Skin-derived mesenchymal stem cells help restore function to ovaries in a premature ovarian failure mouse model. PLoS One. 2014;9:e98749.PubMedPubMedCentralCrossRef Lai D, Wang F, Dong Z, Zhang Q. Skin-derived mesenchymal stem cells help restore function to ovaries in a premature ovarian failure mouse model. PLoS One. 2014;9:e98749.PubMedPubMedCentralCrossRef
114.
go back to reference Abd-Allah SH, Shalaby SM, Pasha HF, El-Shal AS, Raafat N, Shabrawy SM, et al. Mechanistic action of mesenchymal stem cell injection in the treatment of chemically induced ovarian failure in rabbits. Cytotherapy. 2013;15:64–75.PubMedCrossRef Abd-Allah SH, Shalaby SM, Pasha HF, El-Shal AS, Raafat N, Shabrawy SM, et al. Mechanistic action of mesenchymal stem cell injection in the treatment of chemically induced ovarian failure in rabbits. Cytotherapy. 2013;15:64–75.PubMedCrossRef
115.
go back to reference Wang S, Yu L, Sun M, Mu S, Wang C, Wang D, Yao Y. The therapeutic potential of umbilical cord mesenchymal stem cells in mice premature ovarian failure. Biomed Res Int. 2013;2013:690491.PubMedPubMedCentral Wang S, Yu L, Sun M, Mu S, Wang C, Wang D, Yao Y. The therapeutic potential of umbilical cord mesenchymal stem cells in mice premature ovarian failure. Biomed Res Int. 2013;2013:690491.PubMedPubMedCentral
116.
go back to reference Liu T, Huang Y, Guo L, Cheng W, Zou G. CD44+/CD105+ human amniotic fluid mesenchymal stem cells survive and proliferate in the ovary long-term in a mouse model of chemotherapy-induced premature ovarian failure. Int J Med Sci. 2012;9:592–602.PubMedPubMedCentralCrossRef Liu T, Huang Y, Guo L, Cheng W, Zou G. CD44+/CD105+ human amniotic fluid mesenchymal stem cells survive and proliferate in the ovary long-term in a mouse model of chemotherapy-induced premature ovarian failure. Int J Med Sci. 2012;9:592–602.PubMedPubMedCentralCrossRef
117.
go back to reference Selesniemi K, Lee HJ, Niikura T, Tilly JL. Young adult donor bone marrow infusions into female mice postpone age-related reproductive failure and improve offspring survival. Aging. 2009;1:49–57.CrossRef Selesniemi K, Lee HJ, Niikura T, Tilly JL. Young adult donor bone marrow infusions into female mice postpone age-related reproductive failure and improve offspring survival. Aging. 2009;1:49–57.CrossRef
118.
go back to reference Fu X, He Y, Xie C, Liu W. Bone marrow mesenchymal stem cell transplantation improves ovarian function and structure in rats with chemotherapy-induced ovarian damage. Cytotherapy. 2008;10:353–63.PubMedCrossRef Fu X, He Y, Xie C, Liu W. Bone marrow mesenchymal stem cell transplantation improves ovarian function and structure in rats with chemotherapy-induced ovarian damage. Cytotherapy. 2008;10:353–63.PubMedCrossRef
119.
go back to reference Bhartiya D, Parte S, Patel H, Sriraman K, Zaveri K, Hinduja I. Novel action of FSH on stem cells in adult mammalian ovary induces postnatal oogenesis and primordial follicle assembly. Stem Cells Int. 2016;2016:5096596. doi:10.1155/2016/5096596.PubMedCrossRef Bhartiya D, Parte S, Patel H, Sriraman K, Zaveri K, Hinduja I. Novel action of FSH on stem cells in adult mammalian ovary induces postnatal oogenesis and primordial follicle assembly. Stem Cells Int. 2016;2016:5096596. doi:10.​1155/​2016/​5096596.PubMedCrossRef
120.
121.
go back to reference Bhartiya D. Letter to the editor: rejuvenate eggs or regenerate ovary? Mol Cell Endocrinol. 2017;446:111–3.PubMedCrossRef Bhartiya D. Letter to the editor: rejuvenate eggs or regenerate ovary? Mol Cell Endocrinol. 2017;446:111–3.PubMedCrossRef
124.
go back to reference Yu X, Wang N, Qiang R, Wan Q, Qin M, Chen S, Wang H. Human amniotic fluid stem cells possess the potential to differentiate into primordial follicle oocytes in vitro. Biol Reprod. 2014;90:73.PubMedCrossRef Yu X, Wang N, Qiang R, Wan Q, Qin M, Chen S, Wang H. Human amniotic fluid stem cells possess the potential to differentiate into primordial follicle oocytes in vitro. Biol Reprod. 2014;90:73.PubMedCrossRef
125.
go back to reference Dyce PW, Shen W, Huynh E, Shao H, Villagómez DA, Kidder GM, et al. Analysis of oocyte-like cells differentiated from porcine fetal skin-derived stem cells. Stem Cells Dev. 2011;20:809–19.PubMedCrossRef Dyce PW, Shen W, Huynh E, Shao H, Villagómez DA, Kidder GM, et al. Analysis of oocyte-like cells differentiated from porcine fetal skin-derived stem cells. Stem Cells Dev. 2011;20:809–19.PubMedCrossRef
126.
go back to reference Lee HJ, Selesniemi K, Niikura Y, Niikura T, Klein R, Dombkowski DM, Tilly JL. Bone marrow transplantation generates immature oocytes and rescues long-term fertility in a preclinical mouse model of chemotherapy-induced premature ovarian failure. J Clin Oncol. 2007;25:3198–204.PubMedCrossRef Lee HJ, Selesniemi K, Niikura Y, Niikura T, Klein R, Dombkowski DM, Tilly JL. Bone marrow transplantation generates immature oocytes and rescues long-term fertility in a preclinical mouse model of chemotherapy-induced premature ovarian failure. J Clin Oncol. 2007;25:3198–204.PubMedCrossRef
127.
go back to reference Dyce PW, Wen L, Li J. In vitro germline potential of stem cells derived from fetal porcine skin. Nat Cell Biol. 2006;8:384–90.PubMedCrossRef Dyce PW, Wen L, Li J. In vitro germline potential of stem cells derived from fetal porcine skin. Nat Cell Biol. 2006;8:384–90.PubMedCrossRef
129.
go back to reference Johnson J, Bagley J, Skaznik-Wikiel M, Lee HJ, Adams GB, Niikura Y, et al. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell. 2005;122:303–15.PubMedCrossRef Johnson J, Bagley J, Skaznik-Wikiel M, Lee HJ, Adams GB, Niikura Y, et al. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell. 2005;122:303–15.PubMedCrossRef
130.
go back to reference Hua J, Pan S, Yang C, Dong W, Dou Z, Sidhu KS. Derivation of male germ cell-like lineage from human fetal bone marrow stem cells. Reprod BioMed Online. 2009;19:99–105.PubMedCrossRef Hua J, Pan S, Yang C, Dong W, Dou Z, Sidhu KS. Derivation of male germ cell-like lineage from human fetal bone marrow stem cells. Reprod BioMed Online. 2009;19:99–105.PubMedCrossRef
131.
go back to reference Drusenheimer N, Wulf G, Nolte J, Lee JH, Dev A, Dressel R, et al. Putative human male germ cells from bone marrow stem cells. Soc Reprod Fertil Suppl. 2007;63:69–76.PubMed Drusenheimer N, Wulf G, Nolte J, Lee JH, Dev A, Dressel R, et al. Putative human male germ cells from bone marrow stem cells. Soc Reprod Fertil Suppl. 2007;63:69–76.PubMed
132.
go back to reference Wolf DP, Morey R, Kang E, Ma H, Hayama T, Laurent LC, et al. Concise review: embryonic stem cells derived by somatic cell nuclear transfer: a horse in the race? Stem Cells. 2017;35:26–34.PubMedCrossRef Wolf DP, Morey R, Kang E, Ma H, Hayama T, Laurent LC, et al. Concise review: embryonic stem cells derived by somatic cell nuclear transfer: a horse in the race? Stem Cells. 2017;35:26–34.PubMedCrossRef
133.
go back to reference Yoshihara M, Hayashizaki Y, Murakawa Y. Genomic instability of iPSCs: challenges towards their clinical applications. Stem Cell Rev. 2017;13:7–16.PubMedCrossRef Yoshihara M, Hayashizaki Y, Murakawa Y. Genomic instability of iPSCs: challenges towards their clinical applications. Stem Cell Rev. 2017;13:7–16.PubMedCrossRef
134.
go back to reference Tapia N, Schöler HR. Molecular obstacles to clinical translation of iPSCs. Cell Stem Cell. 2016;19:298–309.PubMedCrossRef Tapia N, Schöler HR. Molecular obstacles to clinical translation of iPSCs. Cell Stem Cell. 2016;19:298–309.PubMedCrossRef
135.
go back to reference Kang E, Wang X, Tippner-Hedges R, Ma H, Folmes CD, Gutierrez NM, et al. Age-related accumulation of somatic mitochondrial DNA mutations in adult-derived human iPSCs. Cell Stem Cell. 2016;18:625–36.PubMedCrossRef Kang E, Wang X, Tippner-Hedges R, Ma H, Folmes CD, Gutierrez NM, et al. Age-related accumulation of somatic mitochondrial DNA mutations in adult-derived human iPSCs. Cell Stem Cell. 2016;18:625–36.PubMedCrossRef
136.
go back to reference Kitada M, Wakao S, Dezawa M. Muse cells and induced pluripotent stem cell: implication of the elite model. Cell Mol Life Sc. 2012;69:3739–50.CrossRef Kitada M, Wakao S, Dezawa M. Muse cells and induced pluripotent stem cell: implication of the elite model. Cell Mol Life Sc. 2012;69:3739–50.CrossRef
138.
go back to reference Ma H, Morey R, O'Neil RC, He Y, Daughtry B, Schultz MD, et al. Abnormalities in human pluripotent cells due to reprogramming mechanisms. Nature. 2014;511:177–83.PubMedPubMedCentralCrossRef Ma H, Morey R, O'Neil RC, He Y, Daughtry B, Schultz MD, et al. Abnormalities in human pluripotent cells due to reprogramming mechanisms. Nature. 2014;511:177–83.PubMedPubMedCentralCrossRef
139.
go back to reference Fazeli Z, Abedindo A, Omrani MD, Ghaderian SMH. Mesenchymal stem cells (MSCs) therapy for recovery of fertility: a systematic review. Stem Cell Rev. 2017; doi:10.1007/s12015-017-9765-x. Fazeli Z, Abedindo A, Omrani MD, Ghaderian SMH. Mesenchymal stem cells (MSCs) therapy for recovery of fertility: a systematic review. Stem Cell Rev. 2017; doi:10.​1007/​s12015-017-9765-x.
140.
go back to reference Ratajczak J, Wysoczynski M, Zuba-Surma E, Wan W, Kucia M, Yoder MC, Ratajczak MZ. Adult murine bone marrow-derived very small embryonic-like stem cells differentiate into the hematopoietic lineage after coculture over OP9 stromal cells. Exp Hematol. 2011;39(2):225–37.PubMedCrossRef Ratajczak J, Wysoczynski M, Zuba-Surma E, Wan W, Kucia M, Yoder MC, Ratajczak MZ. Adult murine bone marrow-derived very small embryonic-like stem cells differentiate into the hematopoietic lineage after coculture over OP9 stromal cells. Exp Hematol. 2011;39(2):225–37.PubMedCrossRef
141.
go back to reference De Felici M. Germ stem cells in the mammalian adult ovary: considerations by a fan of the primordial germ cells. Mol Hum Reprod. 2010;16(9):632–6.PubMedCrossRef De Felici M. Germ stem cells in the mammalian adult ovary: considerations by a fan of the primordial germ cells. Mol Hum Reprod. 2010;16(9):632–6.PubMedCrossRef
142.
go back to reference Virant-Klun I. Very small embryonic-like stem cells: a potential developmental link between germinal lineage and hematopoiesis in humans. Stem Cells Dev. 2016;25(2):101–13.PubMedCrossRef Virant-Klun I. Very small embryonic-like stem cells: a potential developmental link between germinal lineage and hematopoiesis in humans. Stem Cells Dev. 2016;25(2):101–13.PubMedCrossRef
143.
go back to reference Scaldaferri ML, Klinger FG, Farini D, Di Carlo A, Carsetti R, Giorda E, De Felici M. Hematopoietic activity in putative mouse primordial germ cell populations. Mech Dev. 2015;136:53–63.PubMedCrossRef Scaldaferri ML, Klinger FG, Farini D, Di Carlo A, Carsetti R, Giorda E, De Felici M. Hematopoietic activity in putative mouse primordial germ cell populations. Mech Dev. 2015;136:53–63.PubMedCrossRef
Metadata
Title
Making gametes from alternate sources of stem cells: past, present and future
Authors
Deepa Bhartiya
Sandhya Anand
Hiren Patel
Seema Parte
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2017
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-017-0308-8

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