A developmental stage-specific switch from DAZL to BOLL occurs during fetal oogenesis in humans, but not mice
Author(s)
He, Jing
Stewart, Kayleigh
Kinnell, Hazel L
Anderson, Richard A
Childs, Andrew J
Type
Journal Article
Abstract
Article
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Corrections (2)
Abstract
Introduction
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Materials and Methods
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13 Aug 2015: He J, Stewart K, Kinnell HL, Anderson RA, Childs AJ (2015) Correction: A Developmental Stage-Specific Switch from DAZL to BOLL Occurs during Fetal Oogenesis in Humans, but Not Mice. PLOS ONE 10(8): e0136009. https://doi.org/10.1371/journal.pone.0136009 View correction
14 Nov 2013: He J, Stewart K, Kinnell HL, Anderson RA, Childs AJ (2013) Correction: A Developmental Stage-Specific Switch from DAZL to BOLL Occurs during Fetal Oogenesis in Humans, but Not Mice. PLOS ONE 8(11): 10.1371/annotation/34304231-e54b-4080-af70-6f957f32d552. https://doi.org/10.1371/annotation/34304231-e54b-4080-af70-6f957f32d552 View correction
Abstract
The Deleted in Azoospermia gene family encodes three germ cell-specific RNA-binding proteins (DAZ, DAZL and BOLL) that are essential for gametogenesis in diverse species. Targeted disruption of Boll in mice causes male-specific spermiogenic defects, but females are apparently fertile. Overexpression of human BOLL promotes the derivation of germ cell-like cells from genetically female (XX), but not male (XY) human ES cells however, suggesting a functional role for BOLL in regulating female gametogenesis in humans. Whether BOLL is expressed during oogenesis in mammals also remains unclear. We have therefore investigated the expression of BOLL during fetal oogenesis in humans and mice. We demonstrate that BOLL protein is expressed in the germ cells of the human fetal ovary, at a later developmental stage than, and almost mutually-exclusive to, the expression of DAZL. Strikingly, BOLL is downregulated, and DAZL re-expressed, as primordial follicles form, revealing BOLL expression to be restricted to a narrow window during fetal oogenesis. By quantifying the extent of co-expression of DAZL and BOLL with markers of meiosis, we show that this window likely corresponds to the later stages of meiotic prophase I. Finally, we demonstrate that Boll is also transiently expressed during oogenesis in the fetal mouse ovary, but is simultaneously co-expressed within the same germ cells as Dazl. These data reveal significant similarities and differences between the expression of BOLL homologues during oogenesis in humans and mice, and raise questions as to the validity of the Boll-/- mouse as a model for understanding BOLL function during human oogenesis.
Authors
Metrics
Comments
Media Coverage
Corrections (2)
Abstract
Introduction
Results
Discussion
Materials and Methods
Supporting Information
Acknowledgments
Author Contributions
References
Reader Comments (0)
Media Coverage
Figures
Corrections
13 Aug 2015: He J, Stewart K, Kinnell HL, Anderson RA, Childs AJ (2015) Correction: A Developmental Stage-Specific Switch from DAZL to BOLL Occurs during Fetal Oogenesis in Humans, but Not Mice. PLOS ONE 10(8): e0136009. https://doi.org/10.1371/journal.pone.0136009 View correction
14 Nov 2013: He J, Stewart K, Kinnell HL, Anderson RA, Childs AJ (2013) Correction: A Developmental Stage-Specific Switch from DAZL to BOLL Occurs during Fetal Oogenesis in Humans, but Not Mice. PLOS ONE 8(11): 10.1371/annotation/34304231-e54b-4080-af70-6f957f32d552. https://doi.org/10.1371/annotation/34304231-e54b-4080-af70-6f957f32d552 View correction
Abstract
The Deleted in Azoospermia gene family encodes three germ cell-specific RNA-binding proteins (DAZ, DAZL and BOLL) that are essential for gametogenesis in diverse species. Targeted disruption of Boll in mice causes male-specific spermiogenic defects, but females are apparently fertile. Overexpression of human BOLL promotes the derivation of germ cell-like cells from genetically female (XX), but not male (XY) human ES cells however, suggesting a functional role for BOLL in regulating female gametogenesis in humans. Whether BOLL is expressed during oogenesis in mammals also remains unclear. We have therefore investigated the expression of BOLL during fetal oogenesis in humans and mice. We demonstrate that BOLL protein is expressed in the germ cells of the human fetal ovary, at a later developmental stage than, and almost mutually-exclusive to, the expression of DAZL. Strikingly, BOLL is downregulated, and DAZL re-expressed, as primordial follicles form, revealing BOLL expression to be restricted to a narrow window during fetal oogenesis. By quantifying the extent of co-expression of DAZL and BOLL with markers of meiosis, we show that this window likely corresponds to the later stages of meiotic prophase I. Finally, we demonstrate that Boll is also transiently expressed during oogenesis in the fetal mouse ovary, but is simultaneously co-expressed within the same germ cells as Dazl. These data reveal significant similarities and differences between the expression of BOLL homologues during oogenesis in humans and mice, and raise questions as to the validity of the Boll-/- mouse as a model for understanding BOLL function during human oogenesis.
Date Issued
2013-09-25
Date Acceptance
2013-07-29
Citation
PLoS ONE, 2013, 8 (9), pp.1-14
ISSN
1932-6203
Publisher
Public Library of Science (PLoS)
Start Page
1
End Page
14
Journal / Book Title
PLoS ONE
Volume
8
Issue
9
Identifier
http://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000325218700016&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=1ba7043ffcc86c417c072aa74d649202
Subjects
Science & Technology
Multidisciplinary Sciences
Science & Technology - Other Topics
GERM-CELL DEVELOPMENT
RNA-BINDING PROTEIN
IN-VIVO
FAMILY PROTEINS
PUMILIO-2 PUM2
REGULATOR DAZL
HUMAN OVARY
DIFFERENTIATION
TRANSLATION
GENE
Publication Status
Published
Article Number
ARTN e73996
Date Publish Online
2013-09-25