Jaelyn Z. Current, Heather L. Chaney, Mingxiang Zhang, Emily M. Dugan, Gianna L. Chimino, Jianbo Yao
{"title":"牛长非编码 RNA(OOSNCR1、OOSNCR2 和 OOSNCR3)的特征及其在卵母细胞成熟和早期胚胎发育中的作用。","authors":"Jaelyn Z. Current, Heather L. Chaney, Mingxiang Zhang, Emily M. Dugan, Gianna L. Chimino, Jianbo Yao","doi":"10.1016/j.repbio.2024.100915","DOIUrl":null,"url":null,"abstract":"<div><p>In mammals, early embryogenesis relies heavily on the regulation of maternal transcripts including protein-coding and non-coding RNAs stored in oocytes. In this study, the expression of three bovine oocyte expressed long non-coding RNAs (lncRNAs), <em>OOSNCR1, OOSNCR2,</em> and <em>OOSNCR3,</em> was characterized in somatic tissues, the ovarian follicle, and throughout early embryonic development. Moreover, the functional requirement of each transcript during oocyte maturation and early embryonic development was investigated using a siRNA-mediated knockdown approach. Tissue distribution analysis revealed that <em>OOSNCR1, OOSNCR2</em> and <em>OOSNCR3</em> are predominantly expressed in fetal ovaries. Follicular cell expression analysis revealed that these lncRNAs are highly expressed in the oocytes, with minor expression detected in the cumulus cells (CCs) and mural granulosa cells (mGCs). The expression for all three genes was highest during oocyte maturation, decreased at fertilization, and ceased altogether by the 16-cell stage. Knockdown of <em>OOSNCR1</em>, <em>OOSNCR2</em> and <em>OOSNCR3</em> in immature oocytes was achieved by microinjection of the cumulus-enclosed germinal vesicle (GV) oocytes with siRNAs targeting these lncRNAs. Knockdown of <em>OOSNCR1</em>, <em>OOSNCR2</em> and <em>OOSNCR3</em> did not affect cumulus expansion, but oocyte survival at 12 h post-insemination was significantly reduced. In addition, knockdown of <em>OOSNCR1</em>, <em>OOSNCR2</em> and <em>OOSNCR3</em> in immature oocytes resulted in a decreased rate of blastocyst development, and reduced expression of genes associated with oocyte competency such as nucleoplasmin 2 (<em>NPM2</em>), growth differentiation factor 9 (<em>GDF9</em>), bone morphogenetic protein 15 (<em>BMP15</em>), and <em>JY-1</em> in MII oocytes. The data herein suggest a functional requirement of <em>OOSNCR1, OOSNCR2,</em> and <em>OOSNCR3</em> during bovine oocyte maturation and early embryogenesis.</p></div>","PeriodicalId":21018,"journal":{"name":"Reproductive biology","volume":"24 3","pages":"Article 100915"},"PeriodicalIF":2.5000,"publicationDate":"2024-06-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Characterization of bovine long non-coding RNAs, OOSNCR1, OOSNCR2 and OOSNCR3, and their roles in oocyte maturation and early embryonic development\",\"authors\":\"Jaelyn Z. Current, Heather L. Chaney, Mingxiang Zhang, Emily M. Dugan, Gianna L. Chimino, Jianbo Yao\",\"doi\":\"10.1016/j.repbio.2024.100915\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div><p>In mammals, early embryogenesis relies heavily on the regulation of maternal transcripts including protein-coding and non-coding RNAs stored in oocytes. In this study, the expression of three bovine oocyte expressed long non-coding RNAs (lncRNAs), <em>OOSNCR1, OOSNCR2,</em> and <em>OOSNCR3,</em> was characterized in somatic tissues, the ovarian follicle, and throughout early embryonic development. Moreover, the functional requirement of each transcript during oocyte maturation and early embryonic development was investigated using a siRNA-mediated knockdown approach. Tissue distribution analysis revealed that <em>OOSNCR1, OOSNCR2</em> and <em>OOSNCR3</em> are predominantly expressed in fetal ovaries. Follicular cell expression analysis revealed that these lncRNAs are highly expressed in the oocytes, with minor expression detected in the cumulus cells (CCs) and mural granulosa cells (mGCs). The expression for all three genes was highest during oocyte maturation, decreased at fertilization, and ceased altogether by the 16-cell stage. Knockdown of <em>OOSNCR1</em>, <em>OOSNCR2</em> and <em>OOSNCR3</em> in immature oocytes was achieved by microinjection of the cumulus-enclosed germinal vesicle (GV) oocytes with siRNAs targeting these lncRNAs. Knockdown of <em>OOSNCR1</em>, <em>OOSNCR2</em> and <em>OOSNCR3</em> did not affect cumulus expansion, but oocyte survival at 12 h post-insemination was significantly reduced. In addition, knockdown of <em>OOSNCR1</em>, <em>OOSNCR2</em> and <em>OOSNCR3</em> in immature oocytes resulted in a decreased rate of blastocyst development, and reduced expression of genes associated with oocyte competency such as nucleoplasmin 2 (<em>NPM2</em>), growth differentiation factor 9 (<em>GDF9</em>), bone morphogenetic protein 15 (<em>BMP15</em>), and <em>JY-1</em> in MII oocytes. The data herein suggest a functional requirement of <em>OOSNCR1, OOSNCR2,</em> and <em>OOSNCR3</em> during bovine oocyte maturation and early embryogenesis.</p></div>\",\"PeriodicalId\":21018,\"journal\":{\"name\":\"Reproductive biology\",\"volume\":\"24 3\",\"pages\":\"Article 100915\"},\"PeriodicalIF\":2.5000,\"publicationDate\":\"2024-06-26\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Reproductive biology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://www.sciencedirect.com/science/article/pii/S1642431X24000615\",\"RegionNum\":3,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q3\",\"JCRName\":\"REPRODUCTIVE BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Reproductive biology","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S1642431X24000615","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"REPRODUCTIVE BIOLOGY","Score":null,"Total":0}
Characterization of bovine long non-coding RNAs, OOSNCR1, OOSNCR2 and OOSNCR3, and their roles in oocyte maturation and early embryonic development
In mammals, early embryogenesis relies heavily on the regulation of maternal transcripts including protein-coding and non-coding RNAs stored in oocytes. In this study, the expression of three bovine oocyte expressed long non-coding RNAs (lncRNAs), OOSNCR1, OOSNCR2, and OOSNCR3, was characterized in somatic tissues, the ovarian follicle, and throughout early embryonic development. Moreover, the functional requirement of each transcript during oocyte maturation and early embryonic development was investigated using a siRNA-mediated knockdown approach. Tissue distribution analysis revealed that OOSNCR1, OOSNCR2 and OOSNCR3 are predominantly expressed in fetal ovaries. Follicular cell expression analysis revealed that these lncRNAs are highly expressed in the oocytes, with minor expression detected in the cumulus cells (CCs) and mural granulosa cells (mGCs). The expression for all three genes was highest during oocyte maturation, decreased at fertilization, and ceased altogether by the 16-cell stage. Knockdown of OOSNCR1, OOSNCR2 and OOSNCR3 in immature oocytes was achieved by microinjection of the cumulus-enclosed germinal vesicle (GV) oocytes with siRNAs targeting these lncRNAs. Knockdown of OOSNCR1, OOSNCR2 and OOSNCR3 did not affect cumulus expansion, but oocyte survival at 12 h post-insemination was significantly reduced. In addition, knockdown of OOSNCR1, OOSNCR2 and OOSNCR3 in immature oocytes resulted in a decreased rate of blastocyst development, and reduced expression of genes associated with oocyte competency such as nucleoplasmin 2 (NPM2), growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15), and JY-1 in MII oocytes. The data herein suggest a functional requirement of OOSNCR1, OOSNCR2, and OOSNCR3 during bovine oocyte maturation and early embryogenesis.
期刊介绍:
An official journal of the Society for Biology of Reproduction and the Institute of Animal Reproduction and Food Research of Polish Academy of Sciences in Olsztyn, Poland.
Reproductive Biology is an international, peer-reviewed journal covering all aspects of reproduction in vertebrates. The journal invites original research papers, short communications, review articles and commentaries dealing with reproductive physiology, endocrinology, immunology, molecular and cellular biology, receptor studies, animal breeding as well as andrology, embryology, infertility, assisted reproduction and contraception. Papers from both basic and clinical research will be considered.