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Review

Advances in improving fertility in women through stem cell-based clinical platforms

, , , , &
Pages 585-593 | Received 01 Dec 2016, Accepted 08 Mar 2017, Published online: 28 Mar 2017

References

  • ESHRE Capri Workshop Group. Failures (with some successes) of assisted reproduction and gamete donation programs. Hum Reprod Update. 2013;19(4):354–365.
  • Dyer S, Chambers GM, de Mouzon J, et al. International committee for monitoring assisted reproductive technologies world report: assisted reproductive technology 2008, 2009 and 2010. Hum Reprod. 2016;31(7):1588–1609.
  • Iliodromiti S, Kelsey TW, Wu O, et al. The predictive accuracy of anti-Müllerian hormone for live birth after assisted conception: a systematic review and meta-analysis of the literature. Hum Reprod Update. 2014;20(4):560–570.
  • Das M, Shehata F, Son W-Y, et al. Ovarian reserve and response to IVF and in vitro maturation treatment following chemotherapy. Hum Reprod. 2012;27(8):2509–2514.
  • May-Panloup P, Boucret L, Chao de la Barca JM, et al. Ovarian ageing: the role of mitochondria in oocytes and follicles. Hum Reprod Update. 2016;22(6):725–743.
  • Benward J. Mandatory counseling for gamete donation recipients: ethical dilemmas. Fertil Steril. 2015;104(3):507–512.
  • Yu D, Wong Y-M, Cheong Y, et al. Asherman syndrome–one century later. Fertil Steril. 2008;89(4):759–779.
  • Sher G, Fisch JD. Effect of vaginal sildenafil on the outcome of in vitro fertilization (IVF) after multiple IVF failures attributed to poor endometrial development. Fertil Steril. 2002;78(5):1073–1076.
  • Aflatoonian B, Ruban L, Jones M, et al. In vitro post-meiotic germ cell development from human embryonic stem cells. Hum Reprod. 2009;24(12):3150–3159.
  • Panula S, Medrano JV, Kee K, et al. Human germ cell differentiation from fetal- and adult-derived induced pluripotent stem cells. Hum Mol Genet. 2011;20(4):752–762.
  • Eguizabal C, Montserrat N, Vassena R, et al. Complete meiosis from human induced pluripotent stem cells. Stem Cells. 2011;29(8):1186–1195.
  • Hu X, Lu H, Cao S, et al. Stem cells derived from human first-trimester umbilical cord have the potential to differentiate into oocyte-like cells in vitro. Int J Mol Med. 2015;35(5):1219–1229.
  • Yu X, Wang N, Qiang R, et al. Human amniotic fluid stem cells possess the potential to differentiate into primordial follicle oocytes in vitro. Biol Reprod. 2014;90(4):73.
  • Bhartiya D, Shaikh A, Anand S, et al. Endogenous, very small embryonic-like stem cells: critical review, therapeutic potential and a look ahead. Hum Reprod Update. 2016;23(1):41–76.
  • Virant-Klun I, Skutella T, Stimpfel M, et al. Ovarian surface epithelium in patients with severe ovarian infertility: a potential source of cells expressing markers of pluripotent/multipotent stem cells. J Biomed Biotechnol. 2011;2011:1–12.
  • Parte S, Bhartiya D, Telang J, 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;20:1451–1464.
  • Vassena R, Eguizabal C, Heindryckx B, et al. Stem cells in reproductive medicine: ready for the patient? Hum Reprod. 2015;30(9):2014–2021.
  • White YA, Woods DC, Takai Y, et al. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med. 2012;18:413–421.
  • Ding X, Liu G, Xu B, et al. Human GV oocytes generated by mitotically active germ cells obtained from follicular aspirates. Sci Rep. 2016;6:28218.
  • Ma Z, Liu R, Wang X, et al. Spontaneous germline potential of human hepatic cell line in vitro. Mol Hum Reprod. 2013;19(4):216–226.
  • Tesarik J, Nagy ZP, Sousa M, et al. Fertilizable oocytes reconstructed from patient’s somatic cell nuclei and donor ooplasts. Reprod Biomed Online. 2001;2(3):160–164.
  • Palermo GD, Takeuchi T, Rosenwaks Z. Technical approaches to correction of oocyte aneuploidy. Hum Reprod. 2002;17(8):2165–2173.
  • Palermo GD, Takeuchi T, Rosenwaks Z. Oocyte-induced haploidization. Reprod Biomed Online. 2002;4(3):237–242.
  • Takeuchi T, Neri QV, Palermo GD. Construction and fertilization of reconstituted human oocytes. Reprod Biomed Online. 2005;11(3):309–318.
  • Couzin-Frankel J. Eggs unlimited. science. 2015;350:620–624.
  • Santamaria X, Cabanillas S, Cervelló I, et al. Autologous cell therapy with CD133+ bone marrow-derived stem cells for refractory Asherman’s syndrome and endometrial atrophy: a pilot cohort study. Hum Reprod. 2016;31(5):1087–1096.
  • Singh N, Mohanty S, Seth T, et al. Autologous stem cell transplantation in refractory Asherman’s syndrome: A novel cell based therapy. J Hum Reprod Sci. 2014;7(2):93–98.
  • Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663–676.
  • Efthymiou AG, Chen G, Rao M, et al. Self-renewal and cell lineage differentiation strategies in human embryonic stem cells and induced pluripotent stem cells. Expert Opin Biol Ther. 2014;14(9):1333–1344.
  • Grskovic M, Ramalho-Santos M. The pluripotent transcriptome. StemBook. Cambridge: Harvard Stem Cell Institute; 2008.
  • Pesce M, Gross MK, Schöler HR. In line with our ancestors: oct-4 and the mammalian germ. Bioessays. 1998;20(9):722–732.
  • Kehler J, Tolkunova E, Koschorz B, et al. Oct4 is required for primordial germ cell survival. EMBO Rep. 2004;5(11):1078–1083.
  • Campolo F, Gori M, Favaro R, et al. Essential role of Sox2 for the establishment and maintenance of the germ cell line. Stem Cells. 2013;31(7):1408–1421.
  • Yamaguchi S, Kurimoto K, Yabuta Y, et al. Conditional knockdown of Nanog induces apoptotic cell death in mouse migrating primordial germ cells. Development. 2009;136(23):4011–4020.
  • Biazar E. Use of umbilical cord and cord blood-derived stem cells for tissue repair and regeneration. Expert Opin Biol Ther. 2014;14(3):301–310.
  • Tsai MS, Lee JL, Chang YJ, et al. Isolation of human multipotent mesenchymal stem cells from second-trimester amniotic fluid using a novel two-stage culture protocol. Hum Reprod. 2004;19(6):1450–1456.
  • De Coppi P, Bartsch G Jr, Siddiqui MM, et al. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol. 2007;25(1):100–106.
  • Ohishi M, Schipani E. Bone marrow mesenchymal stem cells. J Cell Biochem. 2010;109(2):277–282.
  • Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411):143–147.
  • Aghajanova L, Horcajadas JA, Esteban FJ, et al. The bone marrow-derived human mesenchymal stem cell: potential progenitor of the endometrial stromal fibroblast. Biol Reprod. 2010;82(6):1076–1087.
  • Gargett CE, Schwab KE, Deane JA. Endometrial stem/progenitor cells: the first 10 years. Hum Reprod Update. 2016;22(2):137–163.
  • Kucia M, Reca R, Campbell FR, 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(5):857–869.
  • Kucia M, Halasa M, Wysoczynski M, et al. Morphological and molecular characterization of novel population of CXCR4+ SSEA-4+ Oct-4+ very small embryonic-like cells purified from human cord blood: preliminary report. Leukemia. 2007;21(2):297–303.
  • Johnson J, Canning J, Kaneko T, et al. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature. 2004;428(6979):145–150.
  • Stimpfel M, Cerkovnik P, Novakovic S, et al. Putative mesenchymal stem cells isolated from adult human ovaries. J Assist Reprod Genet. 2014;31(8):959–974.
  • Dzafic E, Stimpfel M, Novakovic S, et al. Expression of mesenchymal stem cells-related genes and plasticity of aspirated follicular cells obtained from infertile women. Biomed Res Int. 2014;2014:1–9.
  • Kossowska-Tomaszczuk K, de Geyter C, de Geyter M, et al. The multipotency of luteinizing granulosa cells collected from mature ovarian follicles. Stem Cells. 2009;27(1):210–219.
  • Park TS, Galic Z, Conway AE, et al. Derivation of primordial germ cells from human embryonic and induced pluripotent stem cells is significantly improved by coculture with human fetal gonadal cells. Stem Cells. 2009;27(4):783–795.
  • Kee K, Gonsalves JM, Clark AT, et al. Bone morphogenetic proteins induce germ cell differentiation from human embryonic stem cells. Stem Cells Dev. 2006;15(6):831–837.
  • Chen HF, Kuo HC, Chien CL, et al. Derivation, characterization and differentiation of human embryonic stem cells: comparing serum-containing versus serum-free media and evidence of germ cell differentiation. Hum Reprod. 2007;22(2):567–577.
  • Tilgner K, Atkinson SP, Golebiewska A, et al. Isolation of primordial germ cells from differentiating human embryonic stem cells. Stem Cells. 2008;26(12):3075–3085.
  • Bucay N, Yebra M, Cirulli V, et al. A novel approach for the derivation of putative primordial germ cells and sertoli cells from human embryonic stem cells. Stem Cells. 2009;27(1):68–77.
  • Medrano JV, Ramathal C, Nguyen HN, et al. Divergent RNA-binding proteins, DAZL and VASA, induce meiotic progression in human germ cellsderived in vitro. Stem Cells. 2012;30(3):441–451.
  • Cheng X, Chen S, Yu X, et al. BMP15 gene is activated during human amniotic fluid stem cell differentiation into oocyte-like cells. DNA Cell Biol. 2012;31(7):1198–1204.
  • Qiu P, Bai Y, Pan S, et al. Gender depended potentiality of differentiation of human umbilical cord mesenchymal stem cells into oocyte-Like cells in vitro. Cell Biochem Funct. 2013;31(5):365–373.
  • Easley CA, Simerly CR, Schatten G. Gamete derivation from embryonic stem cells, induced pluripotent stem cells or somatic cell nuclear transfer-derived embryonic stem cells: state of the art. Reprod Fertil Dev. 2014;27(1):89–92.
  • Hussein SM, Batada NN, Vuoristo S, et al. Copy number variation and selection during reprogramming to pluripotency. Nature. 2011;471(7336):58–62.
  • Lister R, Pelizzola M, Kida YS, et al. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature. 2011;471(7336):68–73.
  • Prigione A, Lichtner B, Kuhl H, et al. Human induced pluripotent stem cells harbor homoplasmic and heteroplasmic mitochondrial DNA mutations while maintaining human embryonic stem cell-like metabolic reprogramming. Stem Cells. 2011;29(9):1338–1348.
  • Ishii T. Human iPS cell-derived germ cells: current status and clinical potential. J Clin Med. 2014;3(4):1064–1083.
  • Galat V, Ozen S, Rechitsky S, et al. Cytogenetic analysis of human somatic cell haploidization. Reprod Biomed Online. 2005;10(2):199–204.
  • Tang WW, Dietmann S, Irie N, et al. A unique gene regulatory network resets the human germline epigenome for development. Cell. 2015;161(6):1453–1467.
  • Dunlop CE, Bayne RA, McLaughlin M, et al. Isolation, purification and culture of oogonial stem cells from adult human and bovine ovarian cortex. Lancet. 2014;383:S48.
  • Grieve KM, McLaughlin M, Dunlop CE, et al. The controversial existence and functional potential of oogonial stem cells. Maturitas. 2015;8:278–281.
  • Zou K, Yuan Z, Yang Z, et al. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol. 2009;11:631–636.
  • Zhou L, Wang L, Kang JX, et al. Production of fat-1 transgenic rats using a post-natal female germline stem cell line. Mol Hum Reprod. 2014;20:271–281.
  • Liu Y, Wu C, Lyu Q, et al. Germline stem cells and neo-oogenesis in the adult human ovary. Dev Biol. 2007;306:112–120.
  • Lei L, Spradling AC. Female mice lack adult germ-line stem cells but sustain oogenesis using stable primordial follicles. Proc Nat Acad Sci USA. 2013;110:8585–8590.
  • Oatley J, Hunt PA. Of mice and (wo)men: purified oogonial stem cells from mouse and human ovaries. Biol Reprod. 2012;86:196.
  • Byskov AG, Høyer PE, Yding Andersen C, et al. No evidence for the presence of oogonia in the human ovary after their final clearance during the first two years of life. Hum Reprod. 2011;26(8):2129–2139.
  • Zhang H, Zheng W, Shen Y, et al. Experimental evidence showing that no mitotically active female germline progenitors exist in postnatal mouse ovaries. Proc Natl Acad Sci USA. 2012;109:12580–12585.
  • Zhang H, Panula S, Petropoulos S, et al. Adult human and mouse ovaries lack DDX4-expressing functional oogonial stem cells. Nat Med. 2015;21:1116–1118.
  • Johnson J, Bagley J, Skaznik-Wikiel M, et al. Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell. 2005;122:303–315.
  • Eggan K, Jurga S, Gosden R, et al. Ovulated oocytes in adult mice derive from non-circulating germ cells. Nature. 2006;441:1109–1114.
  • Bhartiya D. Ovarian stem cells are always accompanied by very small embryonic-like stem cells in adult mammalian ovary. J Ovarian Res. 2015;8:70.
  • Sriraman K, Bhartiya D, Anand S, et al. Mouse ovarian very small embryonic-like stem cells resist chemotherapy and retain ability to initiate oocyte-specific differentiation. Reprod Sci. 2015;22:884–903.
  • Virant-Klun I, Stimpfel M, Cvjeticanin B, et al. Small SSEA-4-positive cells from human ovarian cell cultures: related to embryonic stem cells and germinal lineage? J Ovarian Res. 2013;6(1):24.
  • Kurkure P, Prasad M, Dhamankar V, et al. Very small embryonic-like stem cells (VSELs) detected in azoospermic testicular biopsies of adult survivors of childhood cancer. Reprod Biol Endocrinol. 2015;13:122.
  • Virant-Klun I, Zech N, Rožman 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;76:843–856.
  • Zbucka-Kretowska M, Eljaszewicz A, Lipinska D, et al. Effective mobilization of very small embryonic-like stem cells and hematopoietic stem/progenitor cells but not endothelial progenitor cells by follicle-stimulating hormone therapy. Stem Cells Int. 2016;2016:8530207.
  • Edessy M, Hosni HN, Shady Y, et al. Autologous stem cells therapy, the first baby of idiopathic premature ovarian failure. Acta Med Int. 2016;3:19–23.
  • Miyanishi M, Mori Y, Seita J, et al. Do pluripotent stem cells exist in adult mice as very small embryonic stem cells? Stem Cell Rep. 2013;1:198–208.
  • Virant-Klun I, Kenda-Suster N, Smrkolj S. Small putative NANOG, SOX2, and SSEA-4-positive stem cells resembling very small embryonic-like stem cells in sections of ovarian tissue in patients with ovarian cancer. J Ovarian Res. 2016;9:12.
  • Virant-Klun I, Stimpfel M. Novel population of small tumour-initiating stem cells in the ovaries of women with borderline ovarian cancer. Sci Rep. 2016;6:34730.
  • Cohen J, Scott R, Alikani M, et al. Ooplasmic transfer in mature human oocytes. Mol Hum Reprod. 1998;4(3):269–280.
  • Liu J, Zhang H, Zhang Y, et al. Homing and restorative effects of bone marrow-derived mesenchymal stem cells on cisplatin injured ovaries in rats. Mol Cells. 2014;37(12):865–872.
  • Lai D, Wang F, Dong Z, et al. Skin-derived mesenchymal stem cells help restore function to ovaries in a premature ovarian failure mouse model. Plos One. 2014 May 30;9(5):e98749.
  • Takehara Y, Yabuuchi A, Ezoe K, et al. The restorative effects of adipose-derived mesenchymal stem cells on damaged ovarian function. Lab Invest. 2013;93(2):181–193.
  • Lai D, Wang F, Yao X, et al. Human endometrial mesenchymal stem cells restore ovarian function through improving the renewal of germline stem cells in a mouse model of premature ovarian failure. J Transl Med. 2015;13:155.
  • Song D, Zhong Y, Qian C, et al. Human umbilical cord mesenchymal stem cells therapy in cyclophosphamide-induced premature ovarian failure rat model. Biomed Res Int. 2016;2016:1–13.
  • Liu T, Huang Y, Zhang J, et al. Transplantation of human menstrual blood stem cells to treat premature ovarian failure in mouse model. Stem Cells Dev. 2014;23(13):1548–1557.
  • Zhang Q, Xu M, Yao X, et al. Human amniotic epithelial cells inhibit granulosa cell apoptosis induced by chemotherapy and restore the fertility. Stem Cell Res Ther. 2015 Aug 25;6:152.
  • Xia X, Yin T, Yan J, et al. Mesenchymal stem cells enhance angiogenesis and folliclesurvival in human cryopreserved ovariancortex transplantation. Cell Transplant. 2015;24(10):1999–2010.
  • Xia X, Wang T, Yin T, et al. Mesenchymal stem cells facilitate in vitro development of human preantral follicle. Reprod Sci. 2015;22(11):1367–1376.
  • Cervelló I, Gil-Sanchis C, Mas A, et al. Human endometrial side population cells exhibit genotypic, phenotypic and functional features of somatic stem cells. Plos One. 2010 Jun 24;5(6):e10964.
  • Cervelló I, Mas A, Gil-Sanchis C, et al. Reconstruction of endometrium from human endometrial side population cell lines. Plos One. 2011;6(6):e21221.
  • Patel AN, Park E, Kuzman M, et al. Multipotent menstrual blood stromal stem cells: isolation, characterization, and differentiation. Cell Transplant. 2008;17(3):303–311.
  • Gargett CE, Masuda H. Adult stem cells in the endometrium. Mol Hum Reprod. 2010;16(11):818–834.
  • Du H, Taylor HS. Contribution of bone marrow-derived stem cells to endometrium and endometriosis. Stem Cells. 2007;25(8):2082–2086.
  • Ikoma T, Kyo S, Maida Y, et al. Bone marrow-derived cells from male donors can compose endometrial glands in female transplant recipients. Am J Obstet Gynecol. 2009;201(6):608.e1–8.
  • Taylor HS. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. JAMA. 2004;292(1):81–85.
  • Mints M, Jansson M, Sadeghi B, et al. Endometrial endothelial cells are derived from donor stem cells in a bone marrow transplant recipient. Hum Reprod. 2008;23(1):139–143.
  • Cervelló I, Gil-Sanchis C, Mas A, et al. Bone marrow-derived cells from male donors do not contribute to the endometrial side population of the recipient. Plos One. 2012;7(1):e30260.
  • Wolff EF, Uchida N, Donahue RE, et al. Peripheral blood stem cell transplants do not result in endometrial stromal engraftment. Fertil Steril. 2013;99(2):526–532.
  • Murakami K, Bhandari H, Lucas ES, et al. Deficiency in clonogenic endometrial mesenchymal stem cells in obese women with reproductive failure–a pilot study. Plos One. 2013;8(12):e82582.
  • Hikabe O, Hamazaki N, Nagamatsu G, et al. Reconstitution in vitro of the entire cycle of the mouse female germ line. Nature. 2016;539(7628):299–303.
  • Zhang H, Liu K. Cellular and molecular regulation of the activation of mammalian primordial follicles: somatic cells initiate follicle activation in adulthood. Hum Reprod Update. 2015;21(6):779–786.
  • Albertini DF, Gleicher N. A detour in the quest for oogonial stem cells: methods matter. Nat Med. 2015;21(10):1126–1127.
  • Butler MG, Menitove JE. Umbilical cord blood banking: an update. J Assist Reprod Genet. 2011;28(8):669–676.
  • Smitz JE, Gilchrist RB. Are human oocytes from stem cells next? Nat Biotechnol. 2016;34(12):1247–1248.
  • Saitou M, Miyauchi H. Gametogenesis from pluripotent stem cells. Cell Stem Cell. 2016;18(6):721–735.
  • Guo F, Yan L, Guo H, et al. The transcriptome and DNA methylome landscapes of human primordial germ cells. Cell. 2015;161(6):1437–1452.
  • Telfer EE, Zelinski MB. Ovarian follicle culture: advances and challenges for human and nonhuman primates. Fertil Steril. 2013;99(6):1523–1533.
  • Xiao S, Zhang J, Romero MM, et al. In vitro follicle growth supports human oocyte meiotic maturation. Sci Rep. 2015 Nov 27;5:173.
  • Cohen IG, Daley GQ, Adashi EY. Disruptive reproductive technologies. Sci Transl Med. 2017;9(372):eaag2959.

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