Dazl Determines Primordial Follicle Formation Through the Translational Regulation of Tex14

Overview

Journal FASEB J

Specialties Biology
Physiology

Date 2019 Oct 30

PMID 31659914

Citations 7

Authors

Roseanne Rosario

James H Crichton

Hazel L Stewart

Andrew J Childs

Ian R Adams

Richard A Anderson

Affiliations

Soon will be listed here.

Abstract

Deleted in azoospermia-like (DAZL) is a germ cell RNA-binding protein that is essential for entry and progression through meiosis. The phenotype of the Dazl knockout mouse has extensive germ cell loss because of incomplete meiosis. We have created a Dazl hypomorph model using short interfering RNA knockdown in mouse fetal ovary cultures, allowing investigation of Dazl function in germ cell maturation. Dazl hypomorph ovaries had a phenotype of impaired germ cell nest breakdown with a 66% reduction in total follicle number and an increase in the proportion of primordial follicles (PMFs), with smaller oocytes within these follicles. There was no significant early germ cell loss or meiotic delay. Immunostaining of intercellular bridge component testis-expressed protein (Tex)14 showed ∼59% reduction in foci number and size, without any change in Tex14 mRNA levels. TEX14 expression was also confirmed in the human fetal ovary across gestation. Using 3'UTR-luciferase reporter assays, translational regulation of TEX14 was demonstrated to be DAZL-dependant. Dazl is therefore essential for normal intercellular bridges within germ cell nests and their timely breakdown, with a major impact on subsequent assembly of PMFs.-Rosario, R., Crichton, J. H., Stewart, H. L., Childs, A. J., Adams, I. R., Anderson, R. A. Dazl determines primordial follicle formation through the translational regulation of Tex14.

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References

Bartoloni L, Cazzadore C, Ferlin A, Garolla A, Foresta C . Lack of the T54A polymorphism of the DAZL gene in infertile Italian patients. Mol Hum Reprod. 2004; 10(8):613-5. DOI: 10.1093/molehr/gah073. View

Tung J, Rosen M, Nelson L, Turek P, Witte J, Cramer D . Novel missense mutations of the Deleted-in-AZoospermia-Like (DAZL) gene in infertile women and men. Reprod Biol Endocrinol. 2006; 4:40. PMC: 1557510. DOI: 10.1186/1477-7827-4-40. View

Reynolds N, Collier B, Bingham V, Gray N, Cooke H . Translation of the synaptonemal complex component Sycp3 is enhanced in vivo by the germ cell specific regulator Dazl. RNA. 2007; 13(7):974-81. PMC: 1894923. DOI: 10.1261/rna.465507. View

Ruggiu M, Speed R, Taggart M, McKay S, Kilanowski F, Saunders P . The mouse Dazla gene encodes a cytoplasmic protein essential for gametogenesis. Nature. 1997; 389(6646):73-7. DOI: 10.1038/37987. View

Tung J, Rosen M, Nelson L, Turek P, Witte J, Cramer D . Variants in Deleted in AZoospermia-Like (DAZL) are correlated with reproductive parameters in men and women. Hum Genet. 2005; 118(6):730-40. DOI: 10.1007/s00439-005-0098-5. View

Rosario R, Smith R, Adams I, Anderson R . RNA immunoprecipitation identifies novel targets of DAZL in human foetal ovary. Mol Hum Reprod. 2017; 23(3):177-186. PMC: 5943682. DOI: 10.1093/molehr/gax004. View

Livak K, Schmittgen T . Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2002; 25(4):402-8. DOI: 10.1006/meth.2001.1262. View

Rosario R, Adams I, Anderson R . Is there a role for DAZL in human female fertility?. Mol Hum Reprod. 2016; 22(6):377-83. PMC: 4884919. DOI: 10.1093/molehr/gaw024. View

Eberhart C, Maines J, Wasserman S . Meiotic cell cycle requirement for a fly homologue of human Deleted in Azoospermia. Nature. 1996; 381(6585):783-5. DOI: 10.1038/381783a0. View

10.

Chen H, Welling M, Bloch D, Munoz J, Mientjes E, Chen X . DAZL limits pluripotency, differentiation, and apoptosis in developing primordial germ cells. Stem Cell Reports. 2014; 3(5):892-904. PMC: 4235140. DOI: 10.1016/j.stemcr.2014.09.003. View

11.

Venables J, Ruggiu M, Cooke H . The RNA-binding specificity of the mouse Dazl protein. Nucleic Acids Res. 2001; 29(12):2479-83. PMC: 55744. DOI: 10.1093/nar/29.12.2479. View

12.

Saunders P, Cooke H, de Rooij D . Nature of the spermatogenic arrest in Dazl -/- mice. Biol Reprod. 2001; 65(3):771-6. DOI: 10.1095/biolreprod65.3.771. View

13.

Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A . Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002; 3(7):RESEARCH0034. PMC: 126239. DOI: 10.1186/gb-2002-3-7-research0034. View

14.

de Cuevas M, Lilly M, Spradling A . Germline cyst formation in Drosophila. Annu Rev Genet. 1997; 31:405-28. DOI: 10.1146/annurev.genet.31.1.405. View

15.

Stefansdottir A, Johnston Z, Powles-Glover N, Anderson R, Adams I, Spears N . Etoposide damages female germ cells in the developing ovary. BMC Cancer. 2016; 16(1):482. PMC: 4980800. DOI: 10.1186/s12885-016-2505-9. View

16.

Jenkins H, Malkova B, Edwards T . Kinked β-strands mediate high-affinity recognition of mRNA targets by the germ-cell regulator DAZL. Proc Natl Acad Sci U S A. 2011; 108(45):18266-71. PMC: 3215079. DOI: 10.1073/pnas.1105211108. View

17.

Zerbetto I, Gromoll J, Luisi S, Reis F, Nieschlag E, Simoni M . Follicle-stimulating hormone receptor and DAZL gene polymorphisms do not affect the age of menopause. Fertil Steril. 2008; 90(6):2264-8. DOI: 10.1016/j.fertnstert.2007.10.036. View

18.

Fukuda K, Masuda A, Naka T, Suzuki A, Kato Y, Saga Y . Requirement of the 3'-UTR-dependent suppression of DAZL in oocytes for pre-implantation mouse development. PLoS Genet. 2018; 14(6):e1007436. PMC: 6010300. DOI: 10.1371/journal.pgen.1007436. View

19.

ABERCROMBIE M . Estimation of nuclear population from microtome sections. Anat Rec. 2010; 94:239-47. DOI: 10.1002/ar.1090940210. View

20.

Lin Y, Page D . Dazl deficiency leads to embryonic arrest of germ cell development in XY C57BL/6 mice. Dev Biol. 2005; 288(2):309-16. DOI: 10.1016/j.ydbio.2005.06.032. View