Skip to main content
Erschienen in: Journal of Assisted Reproduction and Genetics 7/2011

01.07.2011 | Gonadal Physiology and Disease

Premature ovarian failure in nobox-deficient mice is caused by defects in somatic cell invasion and germ cell cyst breakdown

verfasst von: Agnieszka Lechowska, Szczepan Bilinski, Youngsok Choi, Yonghyun Shin, Malgorzata Kloc, Aleksandar Rajkovic

Erschienen in: Journal of Assisted Reproduction and Genetics | Ausgabe 7/2011

Einloggen, um Zugang zu erhalten

Abstract

Purpose

To understand the mechanism of premature ovarian failure (POF).

Methods

The ultrastructural (electron microscopy) analysis of primordial ovarian follicles in Nobox deficient mice.

Results

We studied, for the first time, the fate of oogonia in embryonic (prenatal) mouse ovaries and showed that the abolishment of the transition from germ cell cysts to primordial follicles in the ovaries of Nobox deficient mice is caused by defects in germ cell cyst breakdown, leading to the formation of syncytial follicles instead of primordial follicles.

Conclusions

These results indicate that POF syndrome in Nobox deficient mice results from the faulty signaling between somatic and germ line components during embryonic development. In addition, the extremely unusual and abnormal presence of adherens junctions between unseparated oocytes within syncytial follicles indicates that faulty communication between somatic and germ cells is involved in, or leads to, abnormalities in the cell adhesion program.
Literatur
1.
Zurück zum Zitat Choi Y, Rajkovic A. Genetics of early mammalian folliculogenesis. Cell Mol Life Sci. 2006a;63:579–90.PubMedCrossRef Choi Y, Rajkovic A. Genetics of early mammalian folliculogenesis. Cell Mol Life Sci. 2006a;63:579–90.PubMedCrossRef
2.
Zurück zum Zitat Choi Y, Rajkovic A. Characterization of NOBOX DNA binding specificity and its regulation of Gdf9 and Pou5f1 promoters. J Biol Chem. 2006b;281:35747–56.PubMedCrossRef Choi Y, Rajkovic A. Characterization of NOBOX DNA binding specificity and its regulation of Gdf9 and Pou5f1 promoters. J Biol Chem. 2006b;281:35747–56.PubMedCrossRef
3.
Zurück zum Zitat Choi Y, Qin Y, Berger MF, Ballow DJ, Bulyk ML, Rajkovic A. A Microarray analyses of newborn mouse ovaries lacking Nobox. Biol Reprod. 2007;77:312–9.PubMedCrossRef Choi Y, Qin Y, Berger MF, Ballow DJ, Bulyk ML, Rajkovic A. A Microarray analyses of newborn mouse ovaries lacking Nobox. Biol Reprod. 2007;77:312–9.PubMedCrossRef
4.
Zurück zum Zitat Huntriss J, Hinkins M, Picton HM. cDNA cloning and expression of the human NOBOX gene in oocytes and ovarian follicles. Mol Hum Reprod. 2006;12:283–9.PubMedCrossRef Huntriss J, Hinkins M, Picton HM. cDNA cloning and expression of the human NOBOX gene in oocytes and ovarian follicles. Mol Hum Reprod. 2006;12:283–9.PubMedCrossRef
5.
Zurück zum Zitat Qin Y, Choi Y, Zhao H, Simpson JL, Chen ZJ, Rajkovic A. NOBOX homeobox mutation causes premature ovarian failure. Am J Hum Genet. 2007;81:576–81.PubMedCrossRef Qin Y, Choi Y, Zhao H, Simpson JL, Chen ZJ, Rajkovic A. NOBOX homeobox mutation causes premature ovarian failure. Am J Hum Genet. 2007;81:576–81.PubMedCrossRef
6.
Zurück zum Zitat Qin Y, Shi Y, Zhao Y, Carson SA, Simpson JL, Chen ZJ. Mutation analysis of NOBOX homeodomain in Chinese women with premature ovarian failure. Fertil Steril. 2009;91:1507–9.PubMedCrossRef Qin Y, Shi Y, Zhao Y, Carson SA, Simpson JL, Chen ZJ. Mutation analysis of NOBOX homeodomain in Chinese women with premature ovarian failure. Fertil Steril. 2009;91:1507–9.PubMedCrossRef
7.
Zurück zum Zitat Rajkovic A, Pangas SA, Ballow D, Suzumori N, Matzuk MM. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science. 2004;305:1157–9.PubMedCrossRef Rajkovic A, Pangas SA, Ballow D, Suzumori N, Matzuk MM. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science. 2004;305:1157–9.PubMedCrossRef
8.
Zurück zum Zitat Simpson JL. Genetic and phenotypic heterogeneity in ovarian failure: overview of selected candidate genes. Ann NY Acad Sci. 2008;1135:146–54.PubMedCrossRef Simpson JL. Genetic and phenotypic heterogeneity in ovarian failure: overview of selected candidate genes. Ann NY Acad Sci. 2008;1135:146–54.PubMedCrossRef
9.
Zurück zum Zitat Suzumori N, Yan C, Matzuk MM, Rajkovic A. Nobox is a homeobox-encoding gene preferentially expressed in primordial and growing oocytes. Mech Dev. 2002;111:137–41.PubMedCrossRef Suzumori N, Yan C, Matzuk MM, Rajkovic A. Nobox is a homeobox-encoding gene preferentially expressed in primordial and growing oocytes. Mech Dev. 2002;111:137–41.PubMedCrossRef
10.
Zurück zum Zitat Suzumori N, Pangas SA, Rajkovic A. Candidate genes for premature ovarian failure. Curr Med Chem. 2007;14:353–7.PubMedCrossRef Suzumori N, Pangas SA, Rajkovic A. Candidate genes for premature ovarian failure. Curr Med Chem. 2007;14:353–7.PubMedCrossRef
11.
Zurück zum Zitat Kloc M, Bilinski S, Dougherty MT, Brey EM, Etkin LD. Formation, architecture and polarity of female germline cyst in Xenopus. Dev Biol. 2004;266:43–61.PubMedCrossRef Kloc M, Bilinski S, Dougherty MT, Brey EM, Etkin LD. Formation, architecture and polarity of female germline cyst in Xenopus. Dev Biol. 2004;266:43–61.PubMedCrossRef
12.
Zurück zum Zitat Kloc M, Jaglarz M, Dougherty M, Stewart MD, Nel-Themaat L, Bilinski S. Mouse early oocytes are transiently polar: three-dimensional and ultrastructural analysis. Exp Cell Res. 2008;314:3245–54.PubMedCrossRef Kloc M, Jaglarz M, Dougherty M, Stewart MD, Nel-Themaat L, Bilinski S. Mouse early oocytes are transiently polar: three-dimensional and ultrastructural analysis. Exp Cell Res. 2008;314:3245–54.PubMedCrossRef
13.
Zurück zum Zitat Pepling ME, Spradling AC. Female mouse germ cells form synchronously dividing cysts. Development. 1998;125:3323–8.PubMed Pepling ME, Spradling AC. Female mouse germ cells form synchronously dividing cysts. Development. 1998;125:3323–8.PubMed
14.
Zurück zum Zitat Bilinski SM, Jaglarz MK, Dougherty MT, Kloc M. Electron microscopy, immunostaining, cytoskeleton visualization, in situ hybridization, and three-dimensional reconstruction of Xenopus oocytes. Methods. 2010;51:11–9.PubMedCrossRef Bilinski SM, Jaglarz MK, Dougherty MT, Kloc M. Electron microscopy, immunostaining, cytoskeleton visualization, in situ hybridization, and three-dimensional reconstruction of Xenopus oocytes. Methods. 2010;51:11–9.PubMedCrossRef
15.
Zurück zum Zitat Choi Y, Yuan D, Rajkovic A. Germ cell-specific transcriptional regulator Sohlh2 is essential for early mouse folliculogenesis and oocyte-specific gene expression. Biol Reprod. 2008;79:1176–82.PubMedCrossRef Choi Y, Yuan D, Rajkovic A. Germ cell-specific transcriptional regulator Sohlh2 is essential for early mouse folliculogenesis and oocyte-specific gene expression. Biol Reprod. 2008;79:1176–82.PubMedCrossRef
16.
Zurück zum Zitat Greenbaum MP, Yan W, Wu M-H, Lin Y-N, Agno JE, Sharma M, et al. TEX14 is essential for intercellular bridges and fertility in male mice. PNAS. 2006;103:4982–7.PubMedCrossRef Greenbaum MP, Yan W, Wu M-H, Lin Y-N, Agno JE, Sharma M, et al. TEX14 is essential for intercellular bridges and fertility in male mice. PNAS. 2006;103:4982–7.PubMedCrossRef
17.
Zurück zum Zitat Bogard N, Lan L, Xu J, Cohen RS. Rab11 maintains connections between germline stem cells and niche cells in the Drosophila ovary. Development. 2007;134:3413–8.PubMedCrossRef Bogard N, Lan L, Xu J, Cohen RS. Rab11 maintains connections between germline stem cells and niche cells in the Drosophila ovary. Development. 2007;134:3413–8.PubMedCrossRef
18.
Zurück zum Zitat Cerda J, Reidenbach S, Pratzel S, Franke WW. Cadherin-catenin complexes during zebrafish oogenesis: heterotypic junctions between oocytes and follicle cells. Biol Reprod. 1999;61:692–704.PubMedCrossRef Cerda J, Reidenbach S, Pratzel S, Franke WW. Cadherin-catenin complexes during zebrafish oogenesis: heterotypic junctions between oocytes and follicle cells. Biol Reprod. 1999;61:692–704.PubMedCrossRef
19.
Zurück zum Zitat Hierholzer A, Kempler R. Beta-catenin-mediated signaling and cell adhesion in postgastrulation mouse embryos. Dev Dyn. 2010;239:191–9.PubMed Hierholzer A, Kempler R. Beta-catenin-mediated signaling and cell adhesion in postgastrulation mouse embryos. Dev Dyn. 2010;239:191–9.PubMed
20.
Zurück zum Zitat Duta S, Pepling ME (2009) A drop in maternal estradiol levels correlates with cyst breakdown and may affect meiotic cell cycle progression. Biol Rep. 81, abstract 479. Duta S, Pepling ME (2009) A drop in maternal estradiol levels correlates with cyst breakdown and may affect meiotic cell cycle progression. Biol Rep. 81, abstract 479.
21.
Zurück zum Zitat Chen Y, Jefferson WN, Newbold RR, Padilla-Banks E, Pepling ME. Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology. 2007;148:3580–90.PubMedCrossRef Chen Y, Jefferson WN, Newbold RR, Padilla-Banks E, Pepling ME. Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology. 2007;148:3580–90.PubMedCrossRef
22.
Zurück zum Zitat Monti M, Redi C. Oogenesis specific genes (Nobox, Oct4, Bmp15, Gdf9, Oogenesin1 and Oogenesin2) are differentially expressed during natural and gonadotropin-induced mouse follicular development. Mol Reprod Dev. 2009;76:994–1003.PubMedCrossRef Monti M, Redi C. Oogenesis specific genes (Nobox, Oct4, Bmp15, Gdf9, Oogenesin1 and Oogenesin2) are differentially expressed during natural and gonadotropin-induced mouse follicular development. Mol Reprod Dev. 2009;76:994–1003.PubMedCrossRef
Metadaten
Titel
Premature ovarian failure in nobox-deficient mice is caused by defects in somatic cell invasion and germ cell cyst breakdown
verfasst von
Agnieszka Lechowska
Szczepan Bilinski
Youngsok Choi
Yonghyun Shin
Malgorzata Kloc
Aleksandar Rajkovic
Publikationsdatum
01.07.2011
Verlag
Springer US
Erschienen in
Journal of Assisted Reproduction and Genetics / Ausgabe 7/2011
Print ISSN: 1058-0468
Elektronische ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-011-9553-5

Weitere Artikel der Ausgabe 7/2011

Journal of Assisted Reproduction and Genetics 7/2011 Zur Ausgabe

Update Gynäkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert – ganz bequem per eMail.