Hostname: page-component-7479d7b7d-k7p5g Total loading time: 0 Render date: 2024-07-11T22:21:05.437Z Has data issue: false hasContentIssue false
  • English
  • Français

Role of Mael in early oogenesis and during germ-cell differentiation from embryonic stem cells in mice in vitro

Published online by Cambridge University Press:  15 February 2013

I. Bahena ,
E. Xu ,
M. Betancourt ,
E. Casas ,
Y. Ducolomb ,
C. González  and
E. Bonilla
I. Bahena
Affiliation:
Department of Health Sciences, Universidad Autónoma Metropolitana-Iztapalapa, México DF 09340, México.
E. Xu
Affiliation:
Feinberg School of Medicine, Northwestern University, Chicago IL 60611, USA.
M. Betancourt
Affiliation:
Department of Health Sciences, Universidad Autónoma Metropolitana-Iztapalapa, México DF 09340, México.
E. Casas
Affiliation:
Department of Health Sciences, Universidad Autónoma Metropolitana-Iztapalapa, México DF 09340, México.
Y. Ducolomb
Affiliation:
Department of Health Sciences, Universidad Autónoma Metropolitana-Iztapalapa, México DF 09340, México.
C. González
Affiliation:
Department of Health Sciences, Universidad Autónoma Metropolitana-Iztapalapa, México DF 09340, México.
E. Bonilla*
Affiliation:
Departamento de Ciencias de la Salud, Universidad Autónoma Metropolitana-Iztapalapa, Av. San Rafael Atlixco # 186, Col Vicentina, México DF 09340, México. Feinberg School of Medicine, Northwestern University, Chicago IL 60611, USA.
*
All correspondence to: Edmundo Bonilla. Departamento de Ciencias de la Salud, Universidad Autónoma Metropolitana-Iztapalapa, Av. San Rafael Atlixco # 186, Col Vicentina, México DF 09340, México. Tel: +52 55 58046557. Fax: +52 55 58044727. e-mail: mundo@xanum.uam.mx
Get access Rights & Permissions [Opens in a new window]

Summary

In a previous study, we have identified a set of conserved spermatogenic genes whose expression is restricted to testis and ovary and that are developmentally regulated. One of these genes, the transcription factor Mael, has been reported to play an essential role in mouse spermatogenesis. Nevertheless, the role of Mael in mouse oogenesis has not been defined. In order to analyse the role of Mael in mouse oogenesis, the expression of this gene was blocked during early oogenesis in mouse in vitro using RNAi technology. In addition, the role of Mael during differentiation of embryonic stem cells (ESC) into germ cells in vitro was analysed. Results show that downregulation of Mael by a specific short interfering RNA disrupted fetal oocyte growth and differentiation in fetal ovary explants in culture and the expression of several germ-cell markers in ESC during their differentiation. These results suggest that there is an important role for Mael in early oogenesis and during germ-cell differentiation from embryonic stem cells in mouse in vitro.

Keywords

ESCGerm cellsMaelOogenesisRNAisiRNA
Type
Research Article
Information
Zygote , Volume 22 , Issue 4 , November 2014 , pp. 513 - 520
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aravin, A.A., van der Heijden, G.W., Castaneda, J., Vagin, V.V., Hannon, G.J. & Bortvin, A. (2009). Cytoplasmic compartmentalization of the fetal piRNA pathway in mice. PLoS Genet. 5, e1000764.Google Scholar
Bonilla, E. & del Mazo, J. (2010). Deregulation of the Sod1 and Nd1 genes in mouse fetal oocytes exposed to mono-(2-ethylhexyl) phthalate (MEHP). Reprod. Toxicol. 30, 387–92.CrossRefGoogle ScholarPubMed
Bonilla, E. & Xu, E.Y. (2008). Identification and characterization of novel mammalian spermatogenic genes conserved from fly to human. Mol. Hum. Reprod. 14, 137–42.Google Scholar
Chen, W., Jia, W., Wang, K., Zhou, Q., Leng, Y., Duan, T. & Kang, J. (2012). Retinoic acid regulates germ cell differentiation in mouse embryonic stem cells through a Smad-dependent pathway. Biochem. Biophys. Res. Commun. 418, 571–7.Google Scholar
Childs, A.J., Saunders, P.T. & Anderson, R.A. (2008). Modelling germ cell development in vitro. Mol. Hum. Reprod. 14, 501–11.CrossRefGoogle ScholarPubMed
Choi, Y., Yuan, D. & Rajkovic, A. (2008). Germ cell-specific transcriptional regular sohlh2 is essential for early mouse folliculogenesis and oocyte specific gene expression. Biol. Reprod. 79, 1176–82.CrossRefGoogle Scholar
Clark, A.T., Bodnar, M.S., Fox, M., Rodriquez, R.T., Abeyta, M.J., Firpo, M.T. & Pera, R.A. (2004). Spontaneous differentiation of germ cells from human embryonic stem cells in vitro. Hum. Mol. Genet. 13, 727–39.Google Scholar
Clegg, N.J., Findley, S.D., Mahowald, A.P. & Ruohola-Baker, H. (2001). Maelstrom is required to position the MTOC in stage 2–6 Drosophila oocytes. Dev. Genes Evol. 211, 44–8.CrossRefGoogle ScholarPubMed
Costa, Y., Speed, R.M., Gautier, P., Semple, C.A., Maratou, K., Turner, J.M. & Cooke, H.J. (2006). Mouse MAELSTROM: the link between meiotic silencing of unsynapsed chromatin and microRNA pathway? Hum. Mol. Genet. 15, 2324–34.Google Scholar
De Felici, M. (1991). In vitro culture systems form germ cells from mouse embryo: primordial germ cells and oocytes. In: Mazo, J.D. (ed.) Reproductive Toxicology: In Vitro Germ Cell Developmental Toxicology from Science to Social and Industrial Demand. New York: Plenum Press, pp. 41–50.Google Scholar
Geijsen, N., Horoschak, M., Kim, K., Gribnau, J., Eggan, K. & Daley, G.Q. (2004). Derivation of embryonic germ cells and male gametes from embryonic stem cells. Nature 427, 148–54.Google Scholar
Ginsburg, M., Snow, M.H. & McLaren, A. (1990). Primordial germ cells in the mouse embryo during gastrulation. Development 110, 521–8.Google Scholar
Girard, A. & Hannon, G.J. (2008). Conserved themes in small-RNA-mediated transposon control. Trends Cell Biol. 18, 136–48.CrossRefGoogle ScholarPubMed
Han, J.S. & Boeke, J.D. (2005). LINE-1 retrotransposons: modulators of quantity and quality of mammalian gene expression? Bioessays 27, 775–84.Google Scholar
Haston, K.M., Tung, J.Y. & Reijo Pera, R.A. (2009). Dazl functions in maintenance of pluripotency and genetic and epigenetic programs of differentiation in mouse primordial germ cells in vivo and in vitro. PLoS One 4, e5654.Google Scholar
Hough, S.R., Clements, I., Welch, P.J. & Wiederholt, K.A. (2006). Differentiation of mouse embryonic stem cells after RNA interference-mediated silencing of OCT4 and Nanog. Stem Cells 24, 1467–75.CrossRefGoogle ScholarPubMed
Hübner, K., Fuhrmann, G., Christenson, L.K., Kehler, J., Reinbold, R., De La Fuente, R., Wood, J., Strauss, J.F. 3rd, Boiani, M. & Schöler, H.R. (2003). Derivation of oocytes from mouse embryonic stem cells. Science 300, 1251–56.CrossRefGoogle ScholarPubMed
Hyslop, L., Stojkovic, M., Armstrong, L., Walter, T., Stojkovic, P., Przyborski, S., Herbert, M., Murdoch, A., Strachan, T. & Lako, M. (2005). Downregulation of NANOG induces differentiation of human embryonic stem cells to extraembryonic lineages. Stem Cells 23, 1035–43.CrossRefGoogle ScholarPubMed
Kee, K., Angeles, V.T., Flores, M., Nguyen, H.N. & Reijo Pera, R.A. (2009). Human DAZL, DAZ and BOULE genes modulate primordial germ-cell and haploid gamete formation. Nature 462, 222–5.Google Scholar
Keller, G.M. (1995). In vitro differentiation of embryonic stem cells. Curr. Opin. Cell Biol. 7, 862–9.Google Scholar
Kerr, C.L. & Cheng, L. (2010). The dazzle in germ cell differentiation. J. Mol. Cell Biol. 2, 26–9.CrossRefGoogle ScholarPubMed
Kim, K.H., Kim, E.Y. & Lee, K.A. (2008). SEBOX is essential for early embryogenesis at the two-cell stage in the mouse. Biol. Reprod. 79, 1192–201.Google Scholar
Lawson, K.A., Dunn, N.R., Roelen, B.A., Zeinstra, L.M., Davis, A.M., Wright, C.V., Korving, J.P. & Hogan, B.L. (1999). Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 13, 424–36.Google Scholar
Ling, V. & Neben, S. (1997). In vitro differentiation of embryonic stem cells: immunophenotypic analysis of cultured embryoid bodies. J. Cell Physiol. 171, 104–15.Google Scholar
Makoolati, Z., Movahedin, M. & Forouzandeh-Moghadam, M. (2011). Bone morphogenetic protein 4 is an efficient inducer for mouse embryonic stem cell differentiation into primordial germ cell. In Vitro Cell Dev. Biol. Anim. 47, 391–8.Google Scholar
Martinez, J., Patkaniowska, A., Urlaub, H., Lührmann, R. & Tuschl, T. (2002). Single-stranded antisense siRNAs guide target RNA cleavage in RNAi. Cell 110, 563–74.CrossRefGoogle ScholarPubMed
McLaren, A. (2003). Primordial germ cells in the mouse. Dev. Biol. 262, 1–15.Google Scholar
Moreno, D.L., Salazar, Z., Betancourt, M., Casas, E., Ducolomb, Y., González, C. & Bonilla, E. (2012). Sebox plays an important role during the early mouse oogenesis in vitro. Zygote 18, 1–5.Google Scholar
O'Donnell, K.A., Burns, K.H. & Boeke, J.D. (2008). A descent into the nuage: the maelstrom of transposon control. Dev. Cell 15, 179–81.Google Scholar
Pangas, S.A. & Rajkovic, A. (2006). Transcriptional regulation of early oogenesis: in search of masters. Hum. Reprod. Update 12, 65–76.Google Scholar
Pedersen, T. & Peters, H. (1968). Proposal for a classification of oocytes and follicles in the mouse ovary. J. Reprod. Fertil. 17, 555–7.CrossRefGoogle ScholarPubMed
Pek, J.W., Lim, A.K. & Kai, T. (2009). Drosophila maelstrom ensures proper germline stem cell lineage differentiation by repressing microRNA-7. Dev. Cell 17, 417–24.Google Scholar
Soper, S.F., van der Heijden, G.W., Hardiman, T.C., Goodheart, M., Martin, S.L., de Boer, P. & Bortvin, A. (2008). Mouse maelstrom, a component of nuage, is essential for spermatogenesis and transposon repression in meiosis. Dev. Cell 15, 285–97.Google Scholar
Thomson, M., Liu, S.J., Zou, L.N., Smith, Z., Meissner, A. & Ramanathan, S. (2011). Pluripotency factors in embryonic stem cells regulate differentiation into germ layers. Cell 145, 875–89.Google Scholar
Toyooka, Y., Tsunekawa, N., Akasu, R. & Noce, T. (2003). Embryonic stem cells can form germ cells in vitro. Proc. Natl. Acad. Sci. USA 100, 11457–62.Google Scholar
Wang, C. & Roy, S.K. (2006). Expression of growth differentiation factor 9 in the oocytes is essential for the development of primordial follicles in the hamster ovary. Endocrinology 147, 1725–34.Google Scholar
Xu, B., Hua, J., Zhang, Y., Jiang, X., Zhang, H., Ma, T., Zheng, W., Sun, R., Shen, W., Sha, J., Cooke, H.J. & Shi, Q. (2011). Proliferating cell nuclear antigen (PCNA) regulates primordial follicle assembly by promoting apoptosis of oocytes in fetal and neonatal mouse ovaries. PLoS One 6, e16046.CrossRefGoogle ScholarPubMed
Zhao, G.Q., Deng, K., Labosky, P.A., Liaw, L. & Hogan, B.L. (1996). The gene encoding bone morphogenetic protein 8B is required for the initiation and maintenance of spermatogenesis in the mouse. Genes Dev. 10, 1657–69.Google Scholar
Zhou, G.B., Meng, Q.G. & Li, N. (2010). In vitro derivation of germ cells from embryonic stem cells in mammals. Mol. Reprod. Dev. 77, 586–94.Google Scholar