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Intra-ovarian stem cell transplantation in management of premature ovarian insufficiency: towards the induced Oogonial Stem Cell (iOSC)
Corresponding Author(s) : Suleyman Aydin
Cellular and Molecular Biology,
Vol. 66 No. 1: Issue 1
Abstract
The specialized resident-stem cells in gonads are tasked with restorating damaged ovarian cells following injury to maintain sequential reproductive events. When we talk about premature ovarian insufficiency (POI) we accept the existence of decreased stem cell and their regenerative abilities. The present study was to explain how restorating damaged ovarian cells following injury to maintain sequential reproductive events in evidence-based medicine indexed in PubMed and Web of Science. The exact mechanism is unclear stem cells transfer may improve compromised ovarian function and fertility outcome in women with POI. Soluble factors secreted by stem cell may rescue impaired mitochondrial function in oogonial stem cells, enhance metabolic capacity of resident stem cells, induce local neovascularization in the ovary, and activate gene shifting between transferred stem cells and germ cell precursors. This review may provide insight into how stem cells show some of their beneficial effects on compromised ovarian microenvironment and germ cell niche and paves the way for clinical trials for improving ovarian function of women with POI. We also had the opportunity to share our hypothesis about the design and development of induced oogonial stem cell (iOSC) and its use in POI.
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- Coulam CB, Adamson SC, Annegers JF. Incidence of premature ovarian failure. Obstet Gynecol 1986; 67:604-6.
- Herraiz S, Romeu M, Buigues A, Martínez S, Díaz-García C, Gómez-Seguí I, et al. Autologous stem cell ovarian transplantation to increase reproductive potential in patients who are poor responders. Fertil Steril 2018; 110:496-505.
- Herraiz S, Buigues A, Díaz-García C, Romeu M, Martínez S, Gómez-Seguí I, et al. Fertility rescue and ovarian follicle growth promotion by bone marrow stem cell infusion. Fertil Steril 2018; 109:908-18.
- Fazeli Z, Abedindo A, Omrani MD, Ghaderian SMH. Mesenchymal stem cells (MSCs) therapy for recovery of fertility: a systematic review. Stem Cell Rev 2018; 14:1-12.
- Bhartiya D, Anand S, PatelH, Parte S. Making gametes from alternate sources of stem cells: past, present and future. Reprod Biol Endocrinol 2017; 15:1-14.
- Liu K, Guo L, Zhou Z, Pan M, Yan C. Mesenchymal stem cells transfer mitochondria into cerebral microvasculature and promote recovery from ischemic stroke. Microvasc Res 2019; 123:74-80.
- Newell C, Sabouny R, Hittel DS, Shutt TE, Khan A, Klein MS, et al. Mesenchymal Stem Cells Shift Mitochondrial Dynamics and Enhance Oxidative Phosphorylation in Recipient Cells. Front Physiol 2018; 9:1572.
- Mauro A, Martelli A, Berardinelli P, Russo V, Bernabò N, Di Giacinto O, et al. Effect of antiprogesterone RU486 on VEGF expression and blood vessel remodeling on ovarian follicles before ovulation. PLoS One 2014; 9:e95910.
- Pan HA, Wu MH, Cheng YC, Wu LH, Chang FM. Quantification of ovarian stromal Doppler signals in poor responders undergoing in vitro fertilization with three-dimensional power Doppler ultrasonography. Am J Obstet Gynecol 2004; 190:338-44.
- Jankowska K. Premature ovarian failure. Prz Menopauzalny 2017; 16:51-6.
- Kinch RAH, Plunkett ER, Smout MS, Carr DH. Primary ovarian failure: a clinicopathological and cytogenetic study. Am J Obstet Gynecol 1965; 91:630-41.
- Lonsdale RN, Roberts PF, Trowell JE. Autoimmune oophoritis associated with polycystic ovaries. Histopathology 1991; 19:77-81.
- Biscotti CV, Hart WR, Lucas JG. Cystic ovarian enlargement resulting from autoimmune oophoritis. Obstet Gynecol 1989; 74:492-5.
- Eisenbarth GS (ed.) Immunoendocrinology: Scientific and Clinical Aspects, Contemporary Endocrinology.: Springer Science and Business Media, New York. 2011.
- Cervello I, Gil-Sanchis C, Santamaria X, Cabanillas S, Díaz A, Faus A, et al. Human CD133(+) bone marrow–derived stem cells promote endometrial proliferation in a murine model of Asherman syndrome. Fertil Steril 2015; 104:1552-60.
- Liu J, Deutsch U, Jeong J, Lobe CG. Constitutive notch signaling in adult transgenic mice inhibits bFGF-induced angiogenesis and blocks ovarian follicle development. Genesis 2014; 52:809-16.
- Bhartiya D. Letter to the editor: rejuvenate eggs or regenerate ovary? Mol Cell Endocrinol 2017; 446:111-3.
- Zhu Y, Yuan M, Meng HY, Wang AY, Guo QY, Wang Y, et al. Basic scienceandclinical applicationofplatelet-rich plasmafor cartilagedefects and osteoarthritis: a review. Osteoarthritis Cartilag 2013; 2:1627-37.
- Pietrzak WS, Eppley BL. Platelet rich plasma: biology and new technology. J Craniofac Surg 2005; 16:1043e54.
- Slater NJ, van der Kolk M, Hendriks T, van Goor H, Bleichrodt RP. Biologic grafts for ventral hernia repair: a systematic review. Am J Surg 2013; 205:220-30.
- Celik O, Esrefoglu M, Hascalik S, Gul M, Tagluk ME, Elter K, et al, Use ofvporcine small intestinal submucosa to reconstruct an ovarian defect. Int JvGynaecol Obstet 2009; 106:218-22.
- Shi XL, Gu JY, Ha B, Xu HY, Fang L, Ding YT. Magnetically labeled mesenchymal stem cells after autologous transplantation into acutely injured liver. World J Gastroenterol 2010; 16:3674-9.
- Bernardo ME, Fibbe WE. Safety and efficacy of mesenchymal stromal cell therapy in autoimmune disorders. Ann N Y Acad Sci 2012; 1266:107-17.
- Maijenburg MW, van der Schoot CE, Voermans C. Mesenchymal stromal cell migration: possibilities to improve cellular therapy. Stem Cells Dev 2012; 21:19-29.
- Hsu Y-C, Wu Y-T, Yu T-H, Wei Y-H. Mitochondria in mesenchymal stem cell biology and cell therapy: from cellular differentiation to mitochondrial transfer. Semin Cell Dev Biol 2016; 52:119-31.
- Gnecchi M, Zhang Z, Ni A, Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008; 103:1204-19.
- Liu Y, Yi XC, Guo G, Long QF, Wang XA, Zhong J, et al. Basic fibroblast growth factor increases the transplantationmediated therapeutic effect of bone mesenchymal stem cells following traumatic brain injury. Mol Med Rept 2014; 9:333-9.
- Garside SA, Harlow CR, Hillier SG, Fraser HM, Thomas FH. Thrombospondin- 1 inhibits angiogenesis and promotes follicular atresia in a novel in vitro angiogenesis assay. Endocrinology 2010; 151:1280-9.
- Zou K, Yuan Z, Yang Z, Luo H, Sun K, Zhou L, et al. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol 2009; 11:631-6.
- White YAR, 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.
- 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.
- 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.
- 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.
- Virant-Klun I1, 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.
- Parte S, Bhartiya D, Patel H, Daithankar V, Chauhan A, Zaveri K, et al. Dynamics associated with spontaneous differentiation of ovarian stem cells in vitro. J Ovarian Res 2014; 7:25.
- Martin JJ, Woods DC, Tilly JL. Implications and Current Limitations of Oogenesis from Female Germline or Oogonial Stem Cells in Adult Mammalian Ovaries. Cells 2019; 8:93.
- Virant-Klun I. Postnatal oogenesis in humans: a review of recent findings. Stem Cells Cloning 2015; 8:49-60.
- Lipskind S, Lindsey JS, Gerami-Naini B. An embryonic and induced pluripotent stem cell model for ovarian granulosa cell development and steroidogenesis. Reprod Sci 2018; 25:712-26.
- Fujiwara Y, Komiya T, Kawabata H, Sato M, Fujimoto H, Furusawa M, et al. Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc Natl Acad Sci USA 1994; 91:12258-62.
- Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M, Noce T. Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 2000; 93:139-49.
- Clarkson YL, McLaughlin M, Waterfall M, Dunlop CE, Skehel PA, Anderson RA, et al. Initial characterisation of adult human ovarian cell populations isolated by DDX4 expression and aldehyde dehydrogenase activity. Sci Rep 2018; 8:6953.
- De Felici M. Germ stem cells in the mammalian adult ovary: considerations by a fan of the primordial germ cells. Mol Hum Reprod 2010; 16:632-6.
- Eguizabal C, Montserrat N, Vassena R, Barragan M, Garreta E, Garcia-Quevedo L, et al. Complete meiosis from human induced pluripotent stem cells. Stem Cells 2011; 29:1186-95.
- 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.
- 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; 17:2789-2804.
References
Coulam CB, Adamson SC, Annegers JF. Incidence of premature ovarian failure. Obstet Gynecol 1986; 67:604-6.
Herraiz S, Romeu M, Buigues A, Martínez S, Díaz-García C, Gómez-Seguí I, et al. Autologous stem cell ovarian transplantation to increase reproductive potential in patients who are poor responders. Fertil Steril 2018; 110:496-505.
Herraiz S, Buigues A, Díaz-García C, Romeu M, Martínez S, Gómez-Seguí I, et al. Fertility rescue and ovarian follicle growth promotion by bone marrow stem cell infusion. Fertil Steril 2018; 109:908-18.
Fazeli Z, Abedindo A, Omrani MD, Ghaderian SMH. Mesenchymal stem cells (MSCs) therapy for recovery of fertility: a systematic review. Stem Cell Rev 2018; 14:1-12.
Bhartiya D, Anand S, PatelH, Parte S. Making gametes from alternate sources of stem cells: past, present and future. Reprod Biol Endocrinol 2017; 15:1-14.
Liu K, Guo L, Zhou Z, Pan M, Yan C. Mesenchymal stem cells transfer mitochondria into cerebral microvasculature and promote recovery from ischemic stroke. Microvasc Res 2019; 123:74-80.
Newell C, Sabouny R, Hittel DS, Shutt TE, Khan A, Klein MS, et al. Mesenchymal Stem Cells Shift Mitochondrial Dynamics and Enhance Oxidative Phosphorylation in Recipient Cells. Front Physiol 2018; 9:1572.
Mauro A, Martelli A, Berardinelli P, Russo V, Bernabò N, Di Giacinto O, et al. Effect of antiprogesterone RU486 on VEGF expression and blood vessel remodeling on ovarian follicles before ovulation. PLoS One 2014; 9:e95910.
Pan HA, Wu MH, Cheng YC, Wu LH, Chang FM. Quantification of ovarian stromal Doppler signals in poor responders undergoing in vitro fertilization with three-dimensional power Doppler ultrasonography. Am J Obstet Gynecol 2004; 190:338-44.
Jankowska K. Premature ovarian failure. Prz Menopauzalny 2017; 16:51-6.
Kinch RAH, Plunkett ER, Smout MS, Carr DH. Primary ovarian failure: a clinicopathological and cytogenetic study. Am J Obstet Gynecol 1965; 91:630-41.
Lonsdale RN, Roberts PF, Trowell JE. Autoimmune oophoritis associated with polycystic ovaries. Histopathology 1991; 19:77-81.
Biscotti CV, Hart WR, Lucas JG. Cystic ovarian enlargement resulting from autoimmune oophoritis. Obstet Gynecol 1989; 74:492-5.
Eisenbarth GS (ed.) Immunoendocrinology: Scientific and Clinical Aspects, Contemporary Endocrinology.: Springer Science and Business Media, New York. 2011.
Cervello I, Gil-Sanchis C, Santamaria X, Cabanillas S, Díaz A, Faus A, et al. Human CD133(+) bone marrow–derived stem cells promote endometrial proliferation in a murine model of Asherman syndrome. Fertil Steril 2015; 104:1552-60.
Liu J, Deutsch U, Jeong J, Lobe CG. Constitutive notch signaling in adult transgenic mice inhibits bFGF-induced angiogenesis and blocks ovarian follicle development. Genesis 2014; 52:809-16.
Bhartiya D. Letter to the editor: rejuvenate eggs or regenerate ovary? Mol Cell Endocrinol 2017; 446:111-3.
Zhu Y, Yuan M, Meng HY, Wang AY, Guo QY, Wang Y, et al. Basic scienceandclinical applicationofplatelet-rich plasmafor cartilagedefects and osteoarthritis: a review. Osteoarthritis Cartilag 2013; 2:1627-37.
Pietrzak WS, Eppley BL. Platelet rich plasma: biology and new technology. J Craniofac Surg 2005; 16:1043e54.
Slater NJ, van der Kolk M, Hendriks T, van Goor H, Bleichrodt RP. Biologic grafts for ventral hernia repair: a systematic review. Am J Surg 2013; 205:220-30.
Celik O, Esrefoglu M, Hascalik S, Gul M, Tagluk ME, Elter K, et al, Use ofvporcine small intestinal submucosa to reconstruct an ovarian defect. Int JvGynaecol Obstet 2009; 106:218-22.
Shi XL, Gu JY, Ha B, Xu HY, Fang L, Ding YT. Magnetically labeled mesenchymal stem cells after autologous transplantation into acutely injured liver. World J Gastroenterol 2010; 16:3674-9.
Bernardo ME, Fibbe WE. Safety and efficacy of mesenchymal stromal cell therapy in autoimmune disorders. Ann N Y Acad Sci 2012; 1266:107-17.
Maijenburg MW, van der Schoot CE, Voermans C. Mesenchymal stromal cell migration: possibilities to improve cellular therapy. Stem Cells Dev 2012; 21:19-29.
Hsu Y-C, Wu Y-T, Yu T-H, Wei Y-H. Mitochondria in mesenchymal stem cell biology and cell therapy: from cellular differentiation to mitochondrial transfer. Semin Cell Dev Biol 2016; 52:119-31.
Gnecchi M, Zhang Z, Ni A, Dzau VJ. Paracrine mechanisms in adult stem cell signaling and therapy. Circ Res 2008; 103:1204-19.
Liu Y, Yi XC, Guo G, Long QF, Wang XA, Zhong J, et al. Basic fibroblast growth factor increases the transplantationmediated therapeutic effect of bone mesenchymal stem cells following traumatic brain injury. Mol Med Rept 2014; 9:333-9.
Garside SA, Harlow CR, Hillier SG, Fraser HM, Thomas FH. Thrombospondin- 1 inhibits angiogenesis and promotes follicular atresia in a novel in vitro angiogenesis assay. Endocrinology 2010; 151:1280-9.
Zou K, Yuan Z, Yang Z, Luo H, Sun K, Zhou L, et al. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol 2009; 11:631-6.
White YAR, 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.
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.
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.
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.
Virant-Klun I1, 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.
Parte S, Bhartiya D, Patel H, Daithankar V, Chauhan A, Zaveri K, et al. Dynamics associated with spontaneous differentiation of ovarian stem cells in vitro. J Ovarian Res 2014; 7:25.
Martin JJ, Woods DC, Tilly JL. Implications and Current Limitations of Oogenesis from Female Germline or Oogonial Stem Cells in Adult Mammalian Ovaries. Cells 2019; 8:93.
Virant-Klun I. Postnatal oogenesis in humans: a review of recent findings. Stem Cells Cloning 2015; 8:49-60.
Lipskind S, Lindsey JS, Gerami-Naini B. An embryonic and induced pluripotent stem cell model for ovarian granulosa cell development and steroidogenesis. Reprod Sci 2018; 25:712-26.
Fujiwara Y, Komiya T, Kawabata H, Sato M, Fujimoto H, Furusawa M, et al. Isolation of a DEAD-family protein gene that encodes a murine homolog of Drosophila vasa and its specific expression in germ cell lineage. Proc Natl Acad Sci USA 1994; 91:12258-62.
Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M, Noce T. Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 2000; 93:139-49.
Clarkson YL, McLaughlin M, Waterfall M, Dunlop CE, Skehel PA, Anderson RA, et al. Initial characterisation of adult human ovarian cell populations isolated by DDX4 expression and aldehyde dehydrogenase activity. Sci Rep 2018; 8:6953.
De Felici M. Germ stem cells in the mammalian adult ovary: considerations by a fan of the primordial germ cells. Mol Hum Reprod 2010; 16:632-6.
Eguizabal C, Montserrat N, Vassena R, Barragan M, Garreta E, Garcia-Quevedo L, et al. Complete meiosis from human induced pluripotent stem cells. Stem Cells 2011; 29:1186-95.
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.
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; 17:2789-2804.