Y box-binding protein 1 regulates zebrafish folliculogenesis partly through p21-mediated control of follicle cell proliferation.

IF 3.7 2区 生物学 Q1 DEVELOPMENTAL BIOLOGY
Development Pub Date : 2024-11-01 Epub Date: 2024-11-08 DOI:10.1242/dev.202898
Bo Zhu, Zhiwei Zhang, Lakhansing Pardeshi, Yingying Chen, Wei Ge
{"title":"Y box-binding protein 1 regulates zebrafish folliculogenesis partly through p21-mediated control of follicle cell proliferation.","authors":"Bo Zhu, Zhiwei Zhang, Lakhansing Pardeshi, Yingying Chen, Wei Ge","doi":"10.1242/dev.202898","DOIUrl":null,"url":null,"abstract":"<p><p>Y box-binding protein 1 (Ybx1/ybx1) regulates gene expression through DNA/RNA binding. In zebrafish, Ybx1 is highly abundant in primary growth (PG) follicles in the ovary, but decreases precipitously as the follicles enter the secondary growth (SG). To understand Ybx1 function in folliculogenesis, we created a ybx1 mutant using TALEN and observed disrupted folliculogenesis during the previtellogenic (PV) to early vitellogenic (EV) transition of SG, resulting in underdeveloped ovaries and infertility. Expression and western blot analyses revealed differential gene expression between ybx1-/- and control ovaries, with significantly increased expression of cdkn1a (p21), a cell cycle inhibitor, in ybx1-/- follicles. While cdkn1a knockout via CRISPR/Cas9 was embryonically lethal, the heterozygote (cdkn1a+/-) displayed advanced follicle activation and maturation, contrasting with the ybx1-/- phenotype. Partial loss of p21 alleviated the ybx1-/- phenotype, restoring folliculogenesis with normal PG-PV and PV-EV transitions in ybx1-/-;cdkn1a+/- mutants. While ybx1-/- mutant follicle cells displayed poor proliferation in vivo and in vitro, the cells from the ybx1-/-;cdkn1a+/- follicles resumed normal proliferation. In conclusion, Ybx1 is crucial for early folliculogenesis in zebrafish, potentially by repressing cdkn1a expression, either directly or indirectly.</p>","PeriodicalId":11375,"journal":{"name":"Development","volume":null,"pages":null},"PeriodicalIF":3.7000,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Development","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1242/dev.202898","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/11/8 0:00:00","PubModel":"Epub","JCR":"Q1","JCRName":"DEVELOPMENTAL BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Y box-binding protein 1 (Ybx1/ybx1) regulates gene expression through DNA/RNA binding. In zebrafish, Ybx1 is highly abundant in primary growth (PG) follicles in the ovary, but decreases precipitously as the follicles enter the secondary growth (SG). To understand Ybx1 function in folliculogenesis, we created a ybx1 mutant using TALEN and observed disrupted folliculogenesis during the previtellogenic (PV) to early vitellogenic (EV) transition of SG, resulting in underdeveloped ovaries and infertility. Expression and western blot analyses revealed differential gene expression between ybx1-/- and control ovaries, with significantly increased expression of cdkn1a (p21), a cell cycle inhibitor, in ybx1-/- follicles. While cdkn1a knockout via CRISPR/Cas9 was embryonically lethal, the heterozygote (cdkn1a+/-) displayed advanced follicle activation and maturation, contrasting with the ybx1-/- phenotype. Partial loss of p21 alleviated the ybx1-/- phenotype, restoring folliculogenesis with normal PG-PV and PV-EV transitions in ybx1-/-;cdkn1a+/- mutants. While ybx1-/- mutant follicle cells displayed poor proliferation in vivo and in vitro, the cells from the ybx1-/-;cdkn1a+/- follicles resumed normal proliferation. In conclusion, Ybx1 is crucial for early folliculogenesis in zebrafish, potentially by repressing cdkn1a expression, either directly or indirectly.

Y盒结合蛋白1(Ybx1)在斑马鱼卵泡发生中的作用:通过抑制 p21 (cdkn1a) 促进卵泡细胞增殖。
Y 盒结合蛋白 1(YB-1;Ybx1/ybx1)通过 DNA/RNA 结合调节基因表达。在斑马鱼中,Ybx1在卵巢初级生长(PG)卵泡中含量很高,但当卵泡进入次级生长(SG)阶段时,Ybx1的含量会急剧下降。为了了解 Ybx1 在卵泡发生过程中的功能,我们利用 TALEN 创建了一个 ybx1 突变体,并观察到卵泡发生在卵黄发生前期(PV)向卵黄发生早期(EV)转变的过程中受到破坏,导致卵巢发育不全和不孕。表达和 Western 印迹分析显示,ybx1-/-卵泡和对照卵泡的基因表达存在差异,ybx1-/-卵泡中细胞周期抑制剂 cdkn1a(p21)的表达显著增加。虽然通过CRISPR/Cas9敲除cdkn1a会导致胚胎死亡,但杂合子(cdkn1a+/-)显示出卵泡的提前活化和成熟,与ybx1-/-的表型形成鲜明对比。p21 的部分缺失缓解了 ybx1-/- 的表型,恢复了 ybx1-/-;cdkn1a+/- 突变体的卵泡发生,PG-PV 和 PV-EV 转变正常。ybx1-/-突变体卵泡细胞在体内和体外的增殖能力都很差,而来自ybx1-/-;p21+/-卵泡的细胞则恢复了正常增殖。总之,Ybx1对斑马鱼早期卵泡的形成至关重要,它可能直接或间接地抑制了cdkn1a的表达。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Development
Development 生物-发育生物学
CiteScore
6.70
自引率
4.30%
发文量
433
审稿时长
3 months
期刊介绍: Development’s scope covers all aspects of plant and animal development, including stem cell biology and regeneration. The single most important criterion for acceptance in Development is scientific excellence. Research papers (articles and reports) should therefore pose and test a significant hypothesis or address a significant question, and should provide novel perspectives that advance our understanding of development. We also encourage submission of papers that use computational methods or mathematical models to obtain significant new insights into developmental biology topics. Manuscripts that are descriptive in nature will be considered only when they lay important groundwork for a field and/or provide novel resources for understanding developmental processes of broad interest to the community. Development includes a Techniques and Resources section for the publication of new methods, datasets, and other types of resources. Papers describing new techniques should include a proof-of-principle demonstration that the technique is valuable to the developmental biology community; they need not include in-depth follow-up analysis. The technique must be described in sufficient detail to be easily replicated by other investigators. Development will also consider protocol-type papers of exceptional interest to the community. We welcome submission of Resource papers, for example those reporting new databases, systems-level datasets, or genetic resources of major value to the developmental biology community. For all papers, the data or resource described must be made available to the community with minimal restrictions upon publication. To aid navigability, Development has dedicated sections of the journal to stem cells & regeneration and to human development. The criteria for acceptance into these sections is identical to those outlined above. Authors and editors are encouraged to nominate appropriate manuscripts for inclusion in one of these sections.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信