Zhangqiang Ma, Ruichen Luo, Yue Xue, Liping Zheng, Chong Zhou, Sitian Fang, Na Hu, Houpeng Wang, Xiu Cheng, Tao Luo, Liaoliao Hu
{"title":"年龄相关长链非编码RNA lnc81通过TEAD2-CCN1/2通路调控小鼠卵巢颗粒细胞增殖和凋亡","authors":"Zhangqiang Ma, Ruichen Luo, Yue Xue, Liping Zheng, Chong Zhou, Sitian Fang, Na Hu, Houpeng Wang, Xiu Cheng, Tao Luo, Liaoliao Hu","doi":"10.1002/jcp.70090","DOIUrl":null,"url":null,"abstract":"<div>\n \n <p>Ovarian granulosa cells (GCs) are pivotal for follicular homeostasis, and their dysregulated apoptosis drives age-related ovarian aging. The Hippo signaling pathway, modulated by long noncoding RNAs (lncRNAs), is implicated in regulating GCs proliferation and ovarian aging. TEAD2 (Transcriptional Enhanced Associate Domain 2), a key downstream transcription factor of the Hippo signaling pathway, plays a critical role in regulating cell proliferation, apoptosis, and embryonic stem cell self-renewal. However, the precise molecular mechanisms by which lncRNAs influence the Hippo pathway in GCs are not fully understood. Through comprehensive RNA-seq analysis of ovarian tissues across three distinct age groups (3-, 11-, and 17-month-old mice), we identified lnc81 as a senescence-associated lncRNA that physically interacts with TEAD2. RNA immunoprecipitation (RIP) assays demonstrated direct binding between lnc81 and TEAD2, while subcellular fractionation coupled with qRT-PCR revealed predominant nuclear localization of lnc81 in granulosa cells (GCs). Importantly, lnc81 expression exhibited a progressive, age-dependent elevation during ovarian aging. Functional characterization showed that lnc81 knockdown in GCs significantly: (i) Inhibited cellular proliferation (as evidenced by decreased <i>Pcna</i> expression). (ii) Promoted apoptosis (indicated by increased BAX/BCL-2 ratio and elevated TUNEL-positive cells). Mechanistically, while lnc81 depletion upregulated CCN1/CCN2 protein levels, it did not affect TEAD2 expression, suggesting that lnc81 regulates TEAD2 transcriptional activity rather than modulating its protein stability. Our findings highlight lnc81 as a nuclear lncRNA that interacts with TEAD2 to amplify CCN1/CCN2 signaling, thereby promoting GC apoptosis and ovarian aging. This mechanistic insight positions lnc81 as a potential biomarker for age-related ovarian decline and a candidate target for therapeutic intervention.</p></div>","PeriodicalId":15220,"journal":{"name":"Journal of Cellular Physiology","volume":"240 9","pages":""},"PeriodicalIF":4.0000,"publicationDate":"2025-09-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"The Age-Associated Long Noncoding RNA lnc81 Regulates Ovarian Granulosa Cell Proliferation and Apoptosis Through TEAD2-CCN1/2 Pathway in Mice\",\"authors\":\"Zhangqiang Ma, Ruichen Luo, Yue Xue, Liping Zheng, Chong Zhou, Sitian Fang, Na Hu, Houpeng Wang, Xiu Cheng, Tao Luo, Liaoliao Hu\",\"doi\":\"10.1002/jcp.70090\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div>\\n \\n <p>Ovarian granulosa cells (GCs) are pivotal for follicular homeostasis, and their dysregulated apoptosis drives age-related ovarian aging. The Hippo signaling pathway, modulated by long noncoding RNAs (lncRNAs), is implicated in regulating GCs proliferation and ovarian aging. TEAD2 (Transcriptional Enhanced Associate Domain 2), a key downstream transcription factor of the Hippo signaling pathway, plays a critical role in regulating cell proliferation, apoptosis, and embryonic stem cell self-renewal. However, the precise molecular mechanisms by which lncRNAs influence the Hippo pathway in GCs are not fully understood. Through comprehensive RNA-seq analysis of ovarian tissues across three distinct age groups (3-, 11-, and 17-month-old mice), we identified lnc81 as a senescence-associated lncRNA that physically interacts with TEAD2. RNA immunoprecipitation (RIP) assays demonstrated direct binding between lnc81 and TEAD2, while subcellular fractionation coupled with qRT-PCR revealed predominant nuclear localization of lnc81 in granulosa cells (GCs). Importantly, lnc81 expression exhibited a progressive, age-dependent elevation during ovarian aging. Functional characterization showed that lnc81 knockdown in GCs significantly: (i) Inhibited cellular proliferation (as evidenced by decreased <i>Pcna</i> expression). (ii) Promoted apoptosis (indicated by increased BAX/BCL-2 ratio and elevated TUNEL-positive cells). Mechanistically, while lnc81 depletion upregulated CCN1/CCN2 protein levels, it did not affect TEAD2 expression, suggesting that lnc81 regulates TEAD2 transcriptional activity rather than modulating its protein stability. Our findings highlight lnc81 as a nuclear lncRNA that interacts with TEAD2 to amplify CCN1/CCN2 signaling, thereby promoting GC apoptosis and ovarian aging. This mechanistic insight positions lnc81 as a potential biomarker for age-related ovarian decline and a candidate target for therapeutic intervention.</p></div>\",\"PeriodicalId\":15220,\"journal\":{\"name\":\"Journal of Cellular Physiology\",\"volume\":\"240 9\",\"pages\":\"\"},\"PeriodicalIF\":4.0000,\"publicationDate\":\"2025-09-10\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Journal of Cellular Physiology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://onlinelibrary.wiley.com/doi/10.1002/jcp.70090\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"CELL BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Cellular Physiology","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1002/jcp.70090","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"CELL BIOLOGY","Score":null,"Total":0}
The Age-Associated Long Noncoding RNA lnc81 Regulates Ovarian Granulosa Cell Proliferation and Apoptosis Through TEAD2-CCN1/2 Pathway in Mice
Ovarian granulosa cells (GCs) are pivotal for follicular homeostasis, and their dysregulated apoptosis drives age-related ovarian aging. The Hippo signaling pathway, modulated by long noncoding RNAs (lncRNAs), is implicated in regulating GCs proliferation and ovarian aging. TEAD2 (Transcriptional Enhanced Associate Domain 2), a key downstream transcription factor of the Hippo signaling pathway, plays a critical role in regulating cell proliferation, apoptosis, and embryonic stem cell self-renewal. However, the precise molecular mechanisms by which lncRNAs influence the Hippo pathway in GCs are not fully understood. Through comprehensive RNA-seq analysis of ovarian tissues across three distinct age groups (3-, 11-, and 17-month-old mice), we identified lnc81 as a senescence-associated lncRNA that physically interacts with TEAD2. RNA immunoprecipitation (RIP) assays demonstrated direct binding between lnc81 and TEAD2, while subcellular fractionation coupled with qRT-PCR revealed predominant nuclear localization of lnc81 in granulosa cells (GCs). Importantly, lnc81 expression exhibited a progressive, age-dependent elevation during ovarian aging. Functional characterization showed that lnc81 knockdown in GCs significantly: (i) Inhibited cellular proliferation (as evidenced by decreased Pcna expression). (ii) Promoted apoptosis (indicated by increased BAX/BCL-2 ratio and elevated TUNEL-positive cells). Mechanistically, while lnc81 depletion upregulated CCN1/CCN2 protein levels, it did not affect TEAD2 expression, suggesting that lnc81 regulates TEAD2 transcriptional activity rather than modulating its protein stability. Our findings highlight lnc81 as a nuclear lncRNA that interacts with TEAD2 to amplify CCN1/CCN2 signaling, thereby promoting GC apoptosis and ovarian aging. This mechanistic insight positions lnc81 as a potential biomarker for age-related ovarian decline and a candidate target for therapeutic intervention.
期刊介绍:
The Journal of Cellular Physiology publishes reports of high biological significance in areas of eukaryotic cell biology and physiology, focusing on those articles that adopt a molecular mechanistic approach to investigate cell structure and function. There is appreciation for the application of cellular, biochemical, molecular and in vivo genetic approaches, as well as the power of genomics, proteomics, bioinformatics and systems biology. In particular, the Journal encourages submission of high-interest papers investigating the genetic and epigenetic regulation of proliferation and phenotype as well as cell fate and lineage commitment by growth factors, cytokines and their cognate receptors and signal transduction pathways that influence the expression, integration and activities of these physiological mediators. Similarly, the Journal encourages submission of manuscripts exploring the regulation of growth and differentiation by cell adhesion molecules in addition to the interplay between these processes and those induced by growth factors and cytokines. Studies on the genes and processes that regulate cell cycle progression and phase transition in eukaryotic cells, and the mechanisms that determine whether cells enter quiescence, proliferate or undergo apoptosis are also welcomed. Submission of papers that address contributions of the extracellular matrix to cellular phenotypes and physiological control as well as regulatory mechanisms governing fertilization, embryogenesis, gametogenesis, cell fate, lineage commitment, differentiation, development and dynamic parameters of cell motility are encouraged. Finally, the investigation of stem cells and changes that differentiate cancer cells from normal cells including studies on the properties and functions of oncogenes and tumor suppressor genes will remain as one of the major interests of the Journal.