Skip to main content
Top
Published in: Journal of Ovarian Research 1/2013

Open Access 01-12-2013 | Research

Small SSEA-4-positive cells from human ovarian cell cultures: related to embryonic stem cells and germinal lineage?

Authors: Irma Virant-Klun, Martin Stimpfel, Branko Cvjeticanin, Eda Vrtacnik-Bokal, Thomas Skutella

Published in: Journal of Ovarian Research | Issue 1/2013

Login to get access

Abstract

Background

It has already been found that very small embyronic-like stem cells (VSELs) are present in adult human tissues and organs. The aim of this study was to find if there exists any similar population of cells in cell cultures of reproductive tissues and embryonic stem cells, and if these cells have any relation to pluripotency and germinal lineage.

Methods and results

Here we report that a population of small SSEA-4-positive cells with diameters of up to 4 μm was isolated by fluorescence-activated cell sorting (FACS) from the human ovarian cell cultures after enzymatic degradation of adult cortex tissues. These small cells – putative ovarian stem cells – were also observed during cell culturing of up to 6 months and more. In general, small putative ovarian stem cells, isolated by FACS, showed a relatively low gene expression profile when compared to human embryonic stem cells (hESCs) and human adult fibroblasts; this may reflect the quiescent state of these cells. In spite of that, small putative ovarian stem cells expressed several genes related to primordial germ cells (PGCs), pluripotency and germinal lineage, including VASA. The PGC-related gene PRDM1 was strongly expressed in small putative ovarian stem cells; in both hESCs and fibroblasts it was significantly down-regulated. In addition, putative ovarian stem cells expressed other PGC-related genes, such as PRDM14 and DPPA3. Most of the pluripotency and germinal lineage-related genes were up-regulated in hESCs (except VASA). When compared to fibroblasts, there were several pluripotency-related genes, which were up-regulated in small putative ovarian stem cells. Similar populations of small cells were also isolated by FACS from human testicular and hESC cultures.

Conclusions

Our results confirm the potential embryonic-like character of small putative stem cells isolated from human adult ovaries and their possible relation to germinal lineage.
Appendix
Available only for authorised users
Literature
1.
go back to reference Kucia M, Reca R, Campbell FR, Zuba-Surma E, Majka M, Ratajczak J, Ratajczak MZ: A population of very small embryonic-like (VSEL) CXCR4(+)SSEA-1(+)Oct-4+ stem cells identified in adult bone marrow. Leukemia 2006, 20: 857–869. 10.1038/sj.leu.2404171PubMedCrossRef Kucia M, Reca R, Campbell FR, Zuba-Surma E, Majka M, Ratajczak J, Ratajczak MZ: A population of very small embryonic-like (VSEL) CXCR4(+)SSEA-1(+)Oct-4+ stem cells identified in adult bone marrow. Leukemia 2006, 20: 857–869. 10.1038/sj.leu.2404171PubMedCrossRef
2.
go back to reference Kucia M, Zuba-Surma E, Wysoczynski M, Dobrowolska H, Reca R, Ratajczak J, Ratajczak MZ: Physiological and pathological consequences of identification of very small embryonic like (VSEL) stem cells in adult bone marrow. J Physiol Pharmacol 2006,57(Suppl 5):5–18. Kucia M, Zuba-Surma E, Wysoczynski M, Dobrowolska H, Reca R, Ratajczak J, Ratajczak MZ: Physiological and pathological consequences of identification of very small embryonic like (VSEL) stem cells in adult bone marrow. J Physiol Pharmacol 2006,57(Suppl 5):5–18.
3.
go back to reference Kucia M, Halasa M, Wysoczynski M, Baskiewicz-Masiuk M, Moldenhawer S, Zuba-Surma E, Czajka R, Wojakowski W, Machalinski B, Ratajczak MZ: 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: 297–303. 10.1038/sj.leu.2404470PubMedCrossRef Kucia M, Halasa M, Wysoczynski M, Baskiewicz-Masiuk M, Moldenhawer S, Zuba-Surma E, Czajka R, Wojakowski W, Machalinski B, Ratajczak MZ: 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: 297–303. 10.1038/sj.leu.2404470PubMedCrossRef
4.
go back to reference Zuba-Surma EK, Kucia M, Dawn B, Guo Y, Ratajczak MZ, Bolli R: Bone marrow-derived pluripotent very small embryonic-like stem cells (VSELs) are mobilized after acute myocardial infarction. J Mol Cell Cardiol 2008, 44: 865–873. 10.1016/j.yjmcc.2008.02.279PubMedCentralPubMedCrossRef Zuba-Surma EK, Kucia M, Dawn B, Guo Y, Ratajczak MZ, Bolli R: Bone marrow-derived pluripotent very small embryonic-like stem cells (VSELs) are mobilized after acute myocardial infarction. J Mol Cell Cardiol 2008, 44: 865–873. 10.1016/j.yjmcc.2008.02.279PubMedCentralPubMedCrossRef
5.
go back to reference Wojakowski W, Tendera M, Kucia M, Zuba-Surma E, Paczkowska E, Ciosek J, Hałasa M, Król M, Kazmierski M, Buszman P, Ochała A, Ratajczak J, Machaliński B, Ratajczak MZ: Mobilization of bone marrow-derived Oct-4+ SSEA-4+ very small embryonic-like stem cells in patients with acute myocardial infarction. J Am Coll Cardiol 2009, 53: 1–9. 10.1016/j.jacc.2008.09.029PubMedCrossRef Wojakowski W, Tendera M, Kucia M, Zuba-Surma E, Paczkowska E, Ciosek J, Hałasa M, Król M, Kazmierski M, Buszman P, Ochała A, Ratajczak J, Machaliński B, Ratajczak MZ: Mobilization of bone marrow-derived Oct-4+ SSEA-4+ very small embryonic-like stem cells in patients with acute myocardial infarction. J Am Coll Cardiol 2009, 53: 1–9. 10.1016/j.jacc.2008.09.029PubMedCrossRef
6.
go back to reference Paczkowska E, Kucia M, Koziarska D, Halasa M, Safranow K, Masiuk M, Karbicka A, Nowik M, Nowacki P, Ratajczak MZ, Machalinski B: Clinical evidence that very small embryonic-like stem cells are mobilized into peripheral blood in patients after stroke. Stroke 2009, 40: 1237–1244. 10.1161/STROKEAHA.108.535062PubMedCrossRef Paczkowska E, Kucia M, Koziarska D, Halasa M, Safranow K, Masiuk M, Karbicka A, Nowik M, Nowacki P, Ratajczak MZ, Machalinski B: Clinical evidence that very small embryonic-like stem cells are mobilized into peripheral blood in patients after stroke. Stroke 2009, 40: 1237–1244. 10.1161/STROKEAHA.108.535062PubMedCrossRef
7.
go back to reference Drukała J, Paczkowska E, Kucia M, Młyńska E, Krajewski A, Machaliński B, Madeja Z, Ratajczak MZ: Stem cells, including a population of very small embryonic-like stem cells, are mobilized into peripheral blood in patients after skin burn injury. Stem Cell Rev 2011, 8: 184–194.CrossRef Drukała J, Paczkowska E, Kucia M, Młyńska E, Krajewski A, Machaliński B, Madeja Z, Ratajczak MZ: Stem cells, including a population of very small embryonic-like stem cells, are mobilized into peripheral blood in patients after skin burn injury. Stem Cell Rev 2011, 8: 184–194.CrossRef
8.
go back to reference Marlicz W, Zuba-Surma E, Kucia M, Blogowski W, Starzynska T, Ratajczak MZ: Various types of stem cells, including a population of very small embryonic-like stem cells, are mobilized into peripheral blood in patients with Crohn’s disease. Inflamm Bowel Dis 2012, 18: 1711–1722. 10.1002/ibd.22875PubMedCrossRef Marlicz W, Zuba-Surma E, Kucia M, Blogowski W, Starzynska T, Ratajczak MZ: Various types of stem cells, including a population of very small embryonic-like stem cells, are mobilized into peripheral blood in patients with Crohn’s disease. Inflamm Bowel Dis 2012, 18: 1711–1722. 10.1002/ibd.22875PubMedCrossRef
9.
go back to reference McGuckin C, Jurga M, Ali H, Strbad M, Forraz N: Culture of embryonic-like stem cells from human umbilical cord blood and onward differentiation to neural cells in vitro. Nat Protoc 2008, 3: 1046–1055. 10.1038/nprot.2008.69PubMedCrossRef McGuckin C, Jurga M, Ali H, Strbad M, Forraz N: Culture of embryonic-like stem cells from human umbilical cord blood and onward differentiation to neural cells in vitro. Nat Protoc 2008, 3: 1046–1055. 10.1038/nprot.2008.69PubMedCrossRef
10.
go back to reference Halasa M, Baskiewicz-Masiuk M, Dabkowska E, Machalinski B: An efficient two-step method to purify very small embryonic-like (VSEL) stem cells from umbilical cord blood (UCB). Folia Histochem Cytobiol 2008, 46: 239–243.PubMedCrossRef Halasa M, Baskiewicz-Masiuk M, Dabkowska E, Machalinski B: An efficient two-step method to purify very small embryonic-like (VSEL) stem cells from umbilical cord blood (UCB). Folia Histochem Cytobiol 2008, 46: 239–243.PubMedCrossRef
11.
go back to reference Sauerzweig S, Munsch T, Lessmann V, Reymann KG, Braun H: A population of serum deprivation-induced bone marrow stem cells (SD-BMSC) expresses marker typical for embryonic and neural stem cells. Exp Cell Res 2009, 315: 50–66. 10.1016/j.yexcr.2008.10.007PubMedCrossRef Sauerzweig S, Munsch T, Lessmann V, Reymann KG, Braun H: A population of serum deprivation-induced bone marrow stem cells (SD-BMSC) expresses marker typical for embryonic and neural stem cells. Exp Cell Res 2009, 315: 50–66. 10.1016/j.yexcr.2008.10.007PubMedCrossRef
12.
go back to reference Pang R, Zhang Y, Pan X, Gu R, Hou X, Xiang P, Liu Z, Zhu X, Hu J, Zhao J, Zhang C: Embryonic-like stem cell derived from adult bone marrow: immature morphology, cell surface markers, ultramicrostructure and differentiation into multinucleated fibers in vitro. Cell Mol Biol (Noisy-le-Grand) 2010,56(Suppl):OL1276-OL1285. Pang R, Zhang Y, Pan X, Gu R, Hou X, Xiang P, Liu Z, Zhu X, Hu J, Zhao J, Zhang C: Embryonic-like stem cell derived from adult bone marrow: immature morphology, cell surface markers, ultramicrostructure and differentiation into multinucleated fibers in vitro. Cell Mol Biol (Noisy-le-Grand) 2010,56(Suppl):OL1276-OL1285.
13.
go back to reference Sovalat H, Scrofani M, Eidenschenk A, Pasquet S, Rimelen V, Hénon P: Identification and isolation from either adult human bone marrow or G-CSF-mobilized peripheral blood of CD34(+)/CD133(+)/CXCR4(+)/Lin(-)CD45(-) cells, featuring morphological, molecular, and phenotypic characteristics of very small embryonic-like (VSEL) stem cells. Exp Hematol 2011, 39: 495–505.PubMed Sovalat H, Scrofani M, Eidenschenk A, Pasquet S, Rimelen V, Hénon P: Identification and isolation from either adult human bone marrow or G-CSF-mobilized peripheral blood of CD34(+)/CD133(+)/CXCR4(+)/Lin(-)CD45(-) cells, featuring morphological, molecular, and phenotypic characteristics of very small embryonic-like (VSEL) stem cells. Exp Hematol 2011, 39: 495–505.PubMed
14.
go back to reference Gharib SA, Khalyfa A, Kucia MJ, Dayyat EA, Kim J, Clair HB, Gozal D: Transcriptional landscape of bone marrow-derived very small embryonic-like stem cells during hypoxia. Respir Res 2011, 12: 63. 10.1186/1465-9921-12-63PubMedCentralPubMedCrossRef Gharib SA, Khalyfa A, Kucia MJ, Dayyat EA, Kim J, Clair HB, Gozal D: Transcriptional landscape of bone marrow-derived very small embryonic-like stem cells during hypoxia. Respir Res 2011, 12: 63. 10.1186/1465-9921-12-63PubMedCentralPubMedCrossRef
15.
go back to reference Bhartiya D, Shaikh A, Nagvenkar P, Kasiviswanathan S, Pethe P, Pawani H, Mohanty S, Rao SG, Zaveri K, Hinduja I: Very small embryonic-like stem cells with maximum regenerative potential get discarded during cord blood banking and bone marrow processing for autologous stem cell therapy. Stem Cells Dev 2012, 21: 1–6. 10.1089/scd.2011.0311PubMedCrossRef Bhartiya D, Shaikh A, Nagvenkar P, Kasiviswanathan S, Pethe P, Pawani H, Mohanty S, Rao SG, Zaveri K, Hinduja I: Very small embryonic-like stem cells with maximum regenerative potential get discarded during cord blood banking and bone marrow processing for autologous stem cell therapy. Stem Cells Dev 2012, 21: 1–6. 10.1089/scd.2011.0311PubMedCrossRef
16.
go back to reference Virant-Klun I, Zech N, Rozman P, Vogler A, Cvjeticanin B, Klemenc P, Malicev E, Meden-Vrtovec H: 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. 10.1111/j.1432-0436.2008.00268.xPubMedCrossRef Virant-Klun I, Zech N, Rozman P, Vogler A, Cvjeticanin B, Klemenc P, Malicev E, Meden-Vrtovec H: 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. 10.1111/j.1432-0436.2008.00268.xPubMedCrossRef
17.
go back to reference Virant-Klun I, Rozman P, Cvjeticanin B, Vrtacnik-Bokal E, Novakovic S, Rülicke T, Dovc P, Meden-Vrtovec H: 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: 137–149. 10.1089/scd.2007.0238PubMedCrossRef Virant-Klun I, Rozman P, Cvjeticanin B, Vrtacnik-Bokal E, Novakovic S, Rülicke T, Dovc P, Meden-Vrtovec H: 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: 137–149. 10.1089/scd.2007.0238PubMedCrossRef
18.
go back to reference Virant-Klun I, Skutella T, Stimpfel M, Sinkovec J: 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: ID381928 Virant-Klun I, Skutella T, Stimpfel M, Sinkovec J: 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: ID381928
19.
go back to reference Parte S, Bhartiya D, Telang J, Daithankar V, Salvi V, Zaveri K, Hinduja I: 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. 10.1089/scd.2010.0461PubMedCentralPubMedCrossRef Parte S, Bhartiya D, Telang J, Daithankar V, Salvi V, Zaveri K, Hinduja I: 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. 10.1089/scd.2010.0461PubMedCentralPubMedCrossRef
20.
go back to reference Bhartiya D, Kasiviswanathan S, Unni SK, Pethe P, Dhabalia JV, Patwardhan S, Tongaonkar HB: 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: 1093–1106. 10.1369/jhc.2010.956870PubMedCentralPubMedCrossRef Bhartiya D, Kasiviswanathan S, Unni SK, Pethe P, Dhabalia JV, Patwardhan S, Tongaonkar HB: 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: 1093–1106. 10.1369/jhc.2010.956870PubMedCentralPubMedCrossRef
21.
go back to reference Bhartiya D, Kasiviswanathan S, Shaikh A: Cellular origin of testis derived pluripotent stem cells: a case for very small embryonic-like stem cells (VSELs). Stem Cells Dev 2012, 21: 670–674. 10.1089/scd.2011.0554PubMedCrossRef Bhartiya D, Kasiviswanathan S, Shaikh A: Cellular origin of testis derived pluripotent stem cells: a case for very small embryonic-like stem cells (VSELs). Stem Cells Dev 2012, 21: 670–674. 10.1089/scd.2011.0554PubMedCrossRef
22.
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: ID291038 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: ID291038
23.
go back to reference Kucia M, Machalinski B, Ratajczak MZ: The developmental deposition of epiblast/germ cell-line derived cells in various organs as a hypothetical explanation of stem cell plasticity? Acta Neurobiol Exp (Wars) 2006, 66: 331–341. Kucia M, Machalinski B, Ratajczak MZ: The developmental deposition of epiblast/germ cell-line derived cells in various organs as a hypothetical explanation of stem cell plasticity? Acta Neurobiol Exp (Wars) 2006, 66: 331–341.
24.
go back to reference Shin DM, Liu R, Klich I, Wu W, Ratajczak J, Kucia M, Ratajczak MZ: Molecular signature of adult bone marrow-purified very small embryonic-like stem cells supports their developmental epiblast/germ line origin. Leukemia 2010, 24: 1450–1461. 10.1038/leu.2010.121PubMedCrossRef Shin DM, Liu R, Klich I, Wu W, Ratajczak J, Kucia M, Ratajczak MZ: Molecular signature of adult bone marrow-purified very small embryonic-like stem cells supports their developmental epiblast/germ line origin. Leukemia 2010, 24: 1450–1461. 10.1038/leu.2010.121PubMedCrossRef
25.
go back to reference Shin DM, Zuba-Surma EK, Wu W, Ratajczak J, Wysoczynski M, Ratajczak MZ, Kucia M: Novel epigenetic mechanisms that control pluripotency and quiescence of adult bone marrow-derived Oct4(+) very small embryonic-like stem cells. Leukemia 2009, 23: 2042–2051. 10.1038/leu.2009.153PubMedCentralPubMedCrossRef Shin DM, Zuba-Surma EK, Wu W, Ratajczak J, Wysoczynski M, Ratajczak MZ, Kucia M: Novel epigenetic mechanisms that control pluripotency and quiescence of adult bone marrow-derived Oct4(+) very small embryonic-like stem cells. Leukemia 2009, 23: 2042–2051. 10.1038/leu.2009.153PubMedCentralPubMedCrossRef
26.
go back to reference Shin DM, Liu R, Wu W, Waigel SJ, Zacharias W, Ratajczak MZ, Kucia M: Global gene expression analysis of very small embryonic-like stem cells reveals that the Ezh2-dependent bivalent domain mechanism contributes to their pluripotent state. Stem Cells Dev 2012, 21: 1639–1652. 10.1089/scd.2011.0389PubMedCentralPubMedCrossRef Shin DM, Liu R, Wu W, Waigel SJ, Zacharias W, Ratajczak MZ, Kucia M: Global gene expression analysis of very small embryonic-like stem cells reveals that the Ezh2-dependent bivalent domain mechanism contributes to their pluripotent state. Stem Cells Dev 2012, 21: 1639–1652. 10.1089/scd.2011.0389PubMedCentralPubMedCrossRef
27.
go back to reference International Stem Cell Initiative: Characterization of human embryonic stem cell lines by the international stem cell initiative. Nat Biotechnol 2007, 25: 803–816. 10.1038/nbt1318CrossRef International Stem Cell Initiative: Characterization of human embryonic stem cell lines by the international stem cell initiative. Nat Biotechnol 2007, 25: 803–816. 10.1038/nbt1318CrossRef
28.
go back to reference Horn PA, Tesch H, Staib P, Kube D, Diehl V, Voliotis D: Expression of CD133, a novel hematopoietic precursor antigen, on acute myeloid leukemia cells. Blood 1999, 93: 1435–1437.PubMed Horn PA, Tesch H, Staib P, Kube D, Diehl V, Voliotis D: Expression of CD133, a novel hematopoietic precursor antigen, on acute myeloid leukemia cells. Blood 1999, 93: 1435–1437.PubMed
29.
go back to reference Zhang J, Guo X, Chang DY, Rosen DG, Mercado-Uribe I, Liu J: CD133 expression associated with poor prognosis in ovarian cancer. Mod Pathol 2012, 25: 456–464. 10.1038/modpathol.2011.170PubMedCrossRef Zhang J, Guo X, Chang DY, Rosen DG, Mercado-Uribe I, Liu J: CD133 expression associated with poor prognosis in ovarian cancer. Mod Pathol 2012, 25: 456–464. 10.1038/modpathol.2011.170PubMedCrossRef
30.
go back to reference Bao S, Leitch HG, Gillich A, Nichols J, Tang F, Kim S, Lee C, Zwaka T, Li X, Surani MA: The germ cell determinant Blimp1 is not required for derivation of pluripotent stem cells. Cell Stem Cell 2012, 11: 107–117.CrossRef Bao S, Leitch HG, Gillich A, Nichols J, Tang F, Kim S, Lee C, Zwaka T, Li X, Surani MA: The germ cell determinant Blimp1 is not required for derivation of pluripotent stem cells. Cell Stem Cell 2012, 11: 107–117.CrossRef
31.
go back to reference Ohinata Y, Payer B, O’Carroll D, Ancelin K, Ono Y, Sano M, Barton SC, Obukhanych T, Nussenzweig M, Tarakhovsky A, Saitou M, Surani MA: Blimp1 is a critical determinant of the germ lineage in mice. Nature 2005, 436: 207–213. 10.1038/nature03813PubMedCrossRef Ohinata Y, Payer B, O’Carroll D, Ancelin K, Ono Y, Sano M, Barton SC, Obukhanych T, Nussenzweig M, Tarakhovsky A, Saitou M, Surani MA: Blimp1 is a critical determinant of the germ lineage in mice. Nature 2005, 436: 207–213. 10.1038/nature03813PubMedCrossRef
32.
go back to reference Essers MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, Trumpp A: IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 2009, 458: 904–908. 10.1038/nature07815PubMedCrossRef Essers MA, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, Trumpp A: IFNalpha activates dormant haematopoietic stem cells in vivo. Nature 2009, 458: 904–908. 10.1038/nature07815PubMedCrossRef
33.
go back to reference Aguirre-Ghiso JA: The problem of cancer dormancy: understanding the basic mechanisms and identifying therapeutic opportunities. Cell Cycle 2006, 5: 1740–1743. 10.4161/cc.5.16.3165PubMedCentralPubMedCrossRef Aguirre-Ghiso JA: The problem of cancer dormancy: understanding the basic mechanisms and identifying therapeutic opportunities. Cell Cycle 2006, 5: 1740–1743. 10.4161/cc.5.16.3165PubMedCentralPubMedCrossRef
34.
go back to reference Hobbs RM, Fagoonee S, Papa A, Webster K, Altruda F, Nishinakamura R, Chai L, Pandolfi PP: Functional antagonism between Sall4 and Plzf defines germline progenitors. Cell Stem Cell 2012, 10: 284–298. 10.1016/j.stem.2012.02.004PubMedCentralPubMedCrossRef Hobbs RM, Fagoonee S, Papa A, Webster K, Altruda F, Nishinakamura R, Chai L, Pandolfi PP: Functional antagonism between Sall4 and Plzf defines germline progenitors. Cell Stem Cell 2012, 10: 284–298. 10.1016/j.stem.2012.02.004PubMedCentralPubMedCrossRef
35.
go back to reference Yang J, Liao W, Ma Y: Role of SALL4 in hematopoiesis. Curr Opin Hematol 2012, 19: 287–291. 10.1097/MOH.0b013e328353c684PubMedCrossRef Yang J, Liao W, Ma Y: Role of SALL4 in hematopoiesis. Curr Opin Hematol 2012, 19: 287–291. 10.1097/MOH.0b013e328353c684PubMedCrossRef
36.
go back to reference Makoolati Z, Movahedin M, Forouzandeh-Moghadam M: Bone morphogenetic protein 4 is an efficient inducer for mouse embryonic stem cell differentiation into primordial germ cell. In Vitro Cell Dev Biol Anim 2011, 47: 391–398. 10.1007/s11626-011-9404-9PubMedCrossRef Makoolati Z, Movahedin M, Forouzandeh-Moghadam M: Bone morphogenetic protein 4 is an efficient inducer for mouse embryonic stem cell differentiation into primordial germ cell. In Vitro Cell Dev Biol Anim 2011, 47: 391–398. 10.1007/s11626-011-9404-9PubMedCrossRef
37.
go back to reference Huang H, Gao Q, Peng X, Choi SY, Sarma K, Ren H, Morris AJ, Frohman MA: piRNA-associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial-surface lipid signaling. Dev Cell 2011, 20: 376–387. 10.1016/j.devcel.2011.01.004PubMedCentralPubMedCrossRef Huang H, Gao Q, Peng X, Choi SY, Sarma K, Ren H, Morris AJ, Frohman MA: piRNA-associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial-surface lipid signaling. Dev Cell 2011, 20: 376–387. 10.1016/j.devcel.2011.01.004PubMedCentralPubMedCrossRef
38.
go back to reference Castrillon DH, Quade BJ, Wang TY, Quigley C, Crum CP: The human VASA gene is specifically expressed in the germ cell lineage. PNAS 2000, 97: 9585–9590. 10.1073/pnas.160274797PubMedCentralPubMedCrossRef Castrillon DH, Quade BJ, Wang TY, Quigley C, Crum CP: The human VASA gene is specifically expressed in the germ cell lineage. PNAS 2000, 97: 9585–9590. 10.1073/pnas.160274797PubMedCentralPubMedCrossRef
39.
go back to reference Zwaka TP, Thomson JA: A germ cell origin of embryonic stem cells? Development 2005, 132: 227–233. 10.1242/dev.01586PubMedCrossRef Zwaka TP, Thomson JA: A germ cell origin of embryonic stem cells? Development 2005, 132: 227–233. 10.1242/dev.01586PubMedCrossRef
40.
go back to reference Müller T, Fleischmann G, Eildermann K, Mätz-Rensing K, Horn PA, Sasaki E, Behr R: A novel embryonic stem cell line derived from the common marmoset monkey (Callithrix jacchus) exhibiting germ cell-like characteristics. Hum Reprod 2009, 24: 1359–1372. 10.1093/humrep/dep012PubMedCrossRef Müller T, Fleischmann G, Eildermann K, Mätz-Rensing K, Horn PA, Sasaki E, Behr R: A novel embryonic stem cell line derived from the common marmoset monkey (Callithrix jacchus) exhibiting germ cell-like characteristics. Hum Reprod 2009, 24: 1359–1372. 10.1093/humrep/dep012PubMedCrossRef
Metadata
Title
Small SSEA-4-positive cells from human ovarian cell cultures: related to embryonic stem cells and germinal lineage?
Authors
Irma Virant-Klun
Martin Stimpfel
Branko Cvjeticanin
Eda Vrtacnik-Bokal
Thomas Skutella
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Journal of Ovarian Research / Issue 1/2013
Electronic ISSN: 1757-2215
DOI
https://doi.org/10.1186/1757-2215-6-24

Other articles of this Issue 1/2013

Journal of Ovarian Research 1/2013 Go to the issue