Differential effect of ubiquitous and germline depletion of Integrator complex function on C. elegans physiology.

IF 1.8 4区 生物学 Q3 BIOLOGY
Biology Open Pub Date : 2025-03-12 DOI:10.1242/bio.061930
Brandon M Waddell, Alice Ronita Roy, Carlos Zapien Verdugo, Cheng-Wei Wu
{"title":"Differential effect of ubiquitous and germline depletion of Integrator complex function on C. elegans physiology.","authors":"Brandon M Waddell, Alice Ronita Roy, Carlos Zapien Verdugo, Cheng-Wei Wu","doi":"10.1242/bio.061930","DOIUrl":null,"url":null,"abstract":"<p><p>The Integrator is a metazoan-conserved protein complex with endonuclease activity that functions to cleave various RNA substrates to shape transcriptome homeostasis by coordinating small nuclear RNA biogenesis to premature transcription termination. Depletion of Integrator results in developmental defects across different model systems and has emerged as a causative factor in human neurodevelopmental syndromes. Here, we use the model system Caenorhabditis elegans to enable studying the temporal effects of Integrator depletion on various physiological parameters with the auxin-inducible degron system that permitted depletion of INTS-4 (Integrator subunit) catalytic subunit of the protein complex. We found that Integrator activity is critical and required for C. elegans development within the L1 larval stage, but becomes dispensable for development and lifespan after the animals have reached the L2/L3 stage. Depletion of INTS-4 only shortened lifespan if auxin was introduced at the L1 stage, suggesting that the previously described lifespan reduction by Integrator inhibition is linked to developmental growth defects. We also found that while germline-specific degradation of Integrator results in the accumulation of misprocessed snRNA transcript, it did not impair the development or lifespan but surprisingly increased progeny production. Together, our study illustrates a temporal, and a potential tissue-specific requirement of the Integrator complex function in shaping whole organism development, aging, and reproduction.</p>","PeriodicalId":9216,"journal":{"name":"Biology Open","volume":" ","pages":""},"PeriodicalIF":1.8000,"publicationDate":"2025-03-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Biology Open","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1242/bio.061930","RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"BIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

The Integrator is a metazoan-conserved protein complex with endonuclease activity that functions to cleave various RNA substrates to shape transcriptome homeostasis by coordinating small nuclear RNA biogenesis to premature transcription termination. Depletion of Integrator results in developmental defects across different model systems and has emerged as a causative factor in human neurodevelopmental syndromes. Here, we use the model system Caenorhabditis elegans to enable studying the temporal effects of Integrator depletion on various physiological parameters with the auxin-inducible degron system that permitted depletion of INTS-4 (Integrator subunit) catalytic subunit of the protein complex. We found that Integrator activity is critical and required for C. elegans development within the L1 larval stage, but becomes dispensable for development and lifespan after the animals have reached the L2/L3 stage. Depletion of INTS-4 only shortened lifespan if auxin was introduced at the L1 stage, suggesting that the previously described lifespan reduction by Integrator inhibition is linked to developmental growth defects. We also found that while germline-specific degradation of Integrator results in the accumulation of misprocessed snRNA transcript, it did not impair the development or lifespan but surprisingly increased progeny production. Together, our study illustrates a temporal, and a potential tissue-specific requirement of the Integrator complex function in shaping whole organism development, aging, and reproduction.

整合子复合体功能普遍缺失和种系缺失对秀丽隐杆线虫生理的差异影响。
整合子是一种具有核酸内切酶活性的后生动物保守蛋白复合物,其功能是通过协调小核RNA的生物发生以过早终止转录来切割各种RNA底物以形成转录组稳态。整合子的缺失导致不同模型系统的发育缺陷,并已成为人类神经发育综合征的一个致病因素。在这里,我们使用秀丽隐杆线虫模型系统,通过生长素诱导的降解系统,研究整合子消耗对各种生理参数的时间影响,该系统允许蛋白质复合物的INTS-4(整合子亚基)催化亚基的消耗。我们发现,整合子的活性对于秀丽隐杆线虫在L1幼虫期的发育至关重要,但在动物达到L2/L3幼虫期后,它的发育和寿命就变得必不可少了。如果在L1阶段引入生长素,则INTS-4的耗尽只会缩短寿命,这表明先前描述的Integrator抑制导致的寿命缩短与发育性生长缺陷有关。我们还发现,尽管Integrator的种系特异性降解会导致错误处理的snRNA转录物的积累,但它不会损害发育或寿命,反而会令人惊讶地增加后代的产量。总之,我们的研究说明了整合子复合物在塑造整个生物体发育、衰老和繁殖过程中的时间和潜在的组织特异性需求。
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
Biology Open
Biology Open BIOLOGY-
CiteScore
3.90
自引率
0.00%
发文量
162
审稿时长
8 weeks
期刊介绍: Biology Open (BiO) is an online Open Access journal that publishes peer-reviewed original research across all aspects of the biological sciences. BiO aims to provide rapid publication for scientifically sound observations and valid conclusions, without a requirement for perceived impact.
×
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