Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2020

Open Access 01-12-2020 | Research

Systematic identification of long intergenic non-coding RNAs expressed in bovine oocytes

Authors: Jian Wang, Prasanthi P. Koganti, Jianbo Yao

Published in: Reproductive Biology and Endocrinology | Issue 1/2020

Login to get access

Abstract

Background

Long non-coding RNAs (lncRNAs) are key regulators of diverse cellular processes. Although a number of studies have reported the identification of bovine lncRNAs across many tissues, very little is known about the identity and characteristics of lncRNAs in bovine oocytes.

Methods

A bovine oocyte cDNA library was constructed and sequenced using the Illumina HiSeq 2000 sequencing system. The oocyte transcriptome was constructed using the ab initio assembly software Scripture and Cufflinks. The assembled transcripts were categorized to identify the novel intergenic transcripts, and the coding potential of these novel transcripts was assessed using CPAT and PhyloCSF. The resulting candidate long intergenic non-coding RNAs (lincRNAs) transcripts were further evaluated to determine if any of them contain any known protein coding domains in the Pfam database. RT-PCR was used to analyze the expression of oocyte-expressed lincRNAs in various bovine tissues.

Results

A total of 85 million raw reads were generated from sequencing of the bovine oocyte library. Transcriptome reconstruction resulted in the assembly of a total of 42,396 transcripts from 37,678 genomic loci. Analysis of the assembled transcripts using the step-wide pipeline resulted in the identification of 1535 oocyte lincRNAs corresponding to 1183 putative non-coding genes. A comparison of the oocyte lincRNAs with the lncRNAs reported in other bovine tissues indicated that 970 of the 1535 oocyte lincRNAs appear to be unique to bovine oocytes. RT-PCR analysis of 5 selected lincRNAs showed either specific or predominant expression of 4 lincRNAs in the fetal ovary. Functional prediction of the oocyte-expressed lincRNAs suggested their involvement in oogenesis through regulating their neighboring protein-coding genes.

Conclusions

This study provides a starting point for future research aimed at understanding the roles of lncRNAs in controlling oocyte development and early embryogenesis in cattle.
Appendix
Available only for authorised users
Literature
1.
go back to reference Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, et al. Landscape of transcription in human cells. Nature. 2012;489:101–8.PubMedPubMedCentralCrossRef Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, et al. Landscape of transcription in human cells. Nature. 2012;489:101–8.PubMedPubMedCentralCrossRef
2.
go back to reference Consortium TEP. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57–74.CrossRef Consortium TEP. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57–74.CrossRef
4.
go back to reference Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS. Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci U S A. 2008;105:716–21.PubMedPubMedCentralCrossRef Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS. Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci U S A. 2008;105:716–21.PubMedPubMedCentralCrossRef
5.
go back to reference Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A. 2009;106:11667–72.PubMedPubMedCentralCrossRef Khalil AM, Guttman M, Huarte M, Garber M, Raj A, Rivea Morales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, et al. Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A. 2009;106:11667–72.PubMedPubMedCentralCrossRef
6.
go back to reference Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, et al. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol. 2010;28:503–10.PubMedPubMedCentralCrossRef Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, et al. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol. 2010;28:503–10.PubMedPubMedCentralCrossRef
7.
go back to reference Brawand D, Soumillon M, Necsulea A, Julien P, Csardi G, Harrigan P, Weier M, Liechti A, Aximu-Petri A, Kircher M, et al. The evolution of gene expression levels in mammalian organs. Nature. 2011;478:343–8.PubMedCrossRef Brawand D, Soumillon M, Necsulea A, Julien P, Csardi G, Harrigan P, Weier M, Liechti A, Aximu-Petri A, Kircher M, et al. The evolution of gene expression levels in mammalian organs. Nature. 2011;478:343–8.PubMedCrossRef
8.
go back to reference Ulitsky I, Shkumatava A, Jan CH, Sive H, Bartel DP. Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell. 2011;147:1537–50.PubMedPubMedCentralCrossRef Ulitsky I, Shkumatava A, Jan CH, Sive H, Bartel DP. Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell. 2011;147:1537–50.PubMedPubMedCentralCrossRef
9.
go back to reference Li T, Wang S, Wu R, Zhou X, Zhu D, Zhang Y. Identification of long non-protein coding RNAs in chicken skeletal muscle using next generation sequencing. Genomics. 2012;99:292–8.PubMedCrossRef Li T, Wang S, Wu R, Zhou X, Zhu D, Zhang Y. Identification of long non-protein coding RNAs in chicken skeletal muscle using next generation sequencing. Genomics. 2012;99:292–8.PubMedCrossRef
10.
go back to reference Wang J, Fu L, Koganti PP, Wang L, Hand JM, Ma H, Yao J. Identification and functional prediction of large Intergenic noncoding RNAs (lincRNAs) in rainbow trout (Oncorhynchus mykiss). Mar Biotechnol (NY). 2016;18:271–82.CrossRef Wang J, Fu L, Koganti PP, Wang L, Hand JM, Ma H, Yao J. Identification and functional prediction of large Intergenic noncoding RNAs (lincRNAs) in rainbow trout (Oncorhynchus mykiss). Mar Biotechnol (NY). 2016;18:271–82.CrossRef
11.
go back to reference Volders PJ, Helsens K, Wang X, Menten B, Martens L, Gevaert K, Vandesompele J, Mestdagh P. LNCipedia: a database for annotated human lncRNA transcript sequences and structures. Nucleic Acids Res. 2013;41:D246–51.PubMedCrossRef Volders PJ, Helsens K, Wang X, Menten B, Martens L, Gevaert K, Vandesompele J, Mestdagh P. LNCipedia: a database for annotated human lncRNA transcript sequences and structures. Nucleic Acids Res. 2013;41:D246–51.PubMedCrossRef
12.
go back to reference Zhao Y, Li H, Fang S, Kang Y, Wu W, Hao Y, Li Z, Bu D, Sun N, Zhang MQ, Chen R. NONCODE 2016: An informative and valuable data source of long non-coding RNAs. Nucleic Acids Res. 2016;44:D203–8.PubMedCrossRef Zhao Y, Li H, Fang S, Kang Y, Wu W, Hao Y, Li Z, Bu D, Sun N, Zhang MQ, Chen R. NONCODE 2016: An informative and valuable data source of long non-coding RNAs. Nucleic Acids Res. 2016;44:D203–8.PubMedCrossRef
13.
go back to reference Huang W, Long N, Khatib H. Genome-wide identification and initial characterization of bovine long non-coding RNAs from EST data. Anim Genet. 2012;43:674–82.PubMedCrossRef Huang W, Long N, Khatib H. Genome-wide identification and initial characterization of bovine long non-coding RNAs from EST data. Anim Genet. 2012;43:674–82.PubMedCrossRef
14.
15.
go back to reference Weikard R, Hadlich F, Kuehn C. Identification of novel transcripts and noncoding RNAs in bovine skin by deep next generation sequencing. BMC Genomics. 2013;14:789.PubMedPubMedCentralCrossRef Weikard R, Hadlich F, Kuehn C. Identification of novel transcripts and noncoding RNAs in bovine skin by deep next generation sequencing. BMC Genomics. 2013;14:789.PubMedPubMedCentralCrossRef
16.
go back to reference Billerey C, Boussaha M, Esquerre D, Rebours E, Djari A, Meersseman C, Klopp C, Gautheret D, Rocha D. Identification of large intergenic non-coding RNAs in bovine muscle using next-generation transcriptomic sequencing. BMC Genomics. 2014;15:499.PubMedPubMedCentralCrossRef Billerey C, Boussaha M, Esquerre D, Rebours E, Djari A, Meersseman C, Klopp C, Gautheret D, Rocha D. Identification of large intergenic non-coding RNAs in bovine muscle using next-generation transcriptomic sequencing. BMC Genomics. 2014;15:499.PubMedPubMedCentralCrossRef
17.
go back to reference Koufariotis LT, Chen YP, Chamberlain A, Vander Jagt C, Hayes BJ. A catalogue of novel bovine long noncoding RNA across 18 tissues. PLoS One. 2015;10:e0141225.PubMedPubMedCentralCrossRef Koufariotis LT, Chen YP, Chamberlain A, Vander Jagt C, Hayes BJ. A catalogue of novel bovine long noncoding RNA across 18 tissues. PLoS One. 2015;10:e0141225.PubMedPubMedCentralCrossRef
18.
go back to reference Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature. 2009;458:223–7.PubMedPubMedCentralCrossRef Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature. 2009;458:223–7.PubMedPubMedCentralCrossRef
19.
go back to reference Sheik Mohamed J, Gaughwin PM, Lim B, Robson P, Lipovich L. Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells. Rna. 2010;16:324–37.PubMedPubMedCentralCrossRef Sheik Mohamed J, Gaughwin PM, Lim B, Robson P, Lipovich L. Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells. Rna. 2010;16:324–37.PubMedPubMedCentralCrossRef
20.
go back to reference Dinger ME, Amaral PP, Mercer TR, Pang KC, Bruce SJ, Gardiner BB, Askarian-Amiri ME, Ru K, Solda G, Simons C, et al. Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res. 2008;18:1433–45.PubMedPubMedCentralCrossRef Dinger ME, Amaral PP, Mercer TR, Pang KC, Bruce SJ, Gardiner BB, Askarian-Amiri ME, Ru K, Solda G, Simons C, et al. Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res. 2008;18:1433–45.PubMedPubMedCentralCrossRef
21.
go back to reference Bettegowda A, Patel OV, Ireland JJ, Smith GW. Quantitative analysis of messenger RNA abundance for ribosomal protein L-15, cyclophilin-a, phosphoglycerokinase, beta-glucuronidase, glyceraldehyde 3-phosphate dehydrogenase, beta-actin, and histone H2A during bovine oocyte maturation and early embryogenesis in vitro. Mol Reprod Dev. 2006;73:267–78.PubMedCrossRef Bettegowda A, Patel OV, Ireland JJ, Smith GW. Quantitative analysis of messenger RNA abundance for ribosomal protein L-15, cyclophilin-a, phosphoglycerokinase, beta-glucuronidase, glyceraldehyde 3-phosphate dehydrogenase, beta-actin, and histone H2A during bovine oocyte maturation and early embryogenesis in vitro. Mol Reprod Dev. 2006;73:267–78.PubMedCrossRef
22.
go back to reference Rosenbloom KR, Armstrong J, Barber GP, Casper J, Clawson H, Diekhans M, Dreszer TR, Fujita PA, Guruvadoo L, Haeussler M, et al. The UCSC genome browser database: 2015 update. Nucleic Acids Res. 2015;43:D670–81.PubMedCrossRef Rosenbloom KR, Armstrong J, Barber GP, Casper J, Clawson H, Diekhans M, Dreszer TR, Fujita PA, Guruvadoo L, Haeussler M, et al. The UCSC genome browser database: 2015 update. Nucleic Acids Res. 2015;43:D670–81.PubMedCrossRef
23.
go back to reference Flicek P, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, Fitzgerald S, et al. Ensembl 2012. Nucleic Acids Res. 2012;40:D84–90.PubMedCrossRef Flicek P, Amode MR, Barrell D, Beal K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fairley S, Fitzgerald S, et al. Ensembl 2012. Nucleic Acids Res. 2012;40:D84–90.PubMedCrossRef
24.
go back to reference Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28:511–5.PubMedPubMedCentralCrossRef Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28:511–5.PubMedPubMedCentralCrossRef
25.
go back to reference Lin MF, Jungreis I, Kellis M. PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions. Bioinformatics. 2011;27:i275–82.PubMedPubMedCentralCrossRef Lin MF, Jungreis I, Kellis M. PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions. Bioinformatics. 2011;27:i275–82.PubMedPubMedCentralCrossRef
26.
go back to reference Wang L, Park HJ, Dasari S, Wang S, Kocher JP, Li W. CPAT: coding-potential assessment tool using an alignment-free logistic regression model. Nucleic Acids Res. 2013;41:e74.PubMedPubMedCentralCrossRef Wang L, Park HJ, Dasari S, Wang S, Kocher JP, Li W. CPAT: coding-potential assessment tool using an alignment-free logistic regression model. Nucleic Acids Res. 2013;41:e74.PubMedPubMedCentralCrossRef
28.
go back to reference Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 2011;25:1915–27.PubMedPubMedCentralCrossRef Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 2011;25:1915–27.PubMedPubMedCentralCrossRef
29.
go back to reference Murdoch WJ, Dailey RA, Inskeep EK. Preovulatory changes prostaglandins E2 and F2 alpha in ovine follicles. J Anim Sci. 1981;53:192–205.PubMedCrossRef Murdoch WJ, Dailey RA, Inskeep EK. Preovulatory changes prostaglandins E2 and F2 alpha in ovine follicles. J Anim Sci. 1981;53:192–205.PubMedCrossRef
30.
go back to reference Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;14:R36.PubMedPubMedCentralCrossRef Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013;14:R36.PubMedPubMedCentralCrossRef
31.
go back to reference Canovas A, Rincon G, Islas-Trejo A, Wickramasinghe S, Medrano JF. SNP discovery in the bovine milk transcriptome using RNA-Seq technology. Mamm Genome. 2010;21:592–8.PubMedPubMedCentralCrossRef Canovas A, Rincon G, Islas-Trejo A, Wickramasinghe S, Medrano JF. SNP discovery in the bovine milk transcriptome using RNA-Seq technology. Mamm Genome. 2010;21:592–8.PubMedPubMedCentralCrossRef
32.
go back to reference Huang W, Nadeem A, Zhang B, Babar M, Soller M, Khatib H. Characterization and comparison of the leukocyte transcriptomes of three cattle breeds. PLoS One. 2012;7:e30244.PubMedPubMedCentralCrossRef Huang W, Nadeem A, Zhang B, Babar M, Soller M, Khatib H. Characterization and comparison of the leukocyte transcriptomes of three cattle breeds. PLoS One. 2012;7:e30244.PubMedPubMedCentralCrossRef
33.
34.
go back to reference Baldwin RLt WS, Li W, Li C, Bequette BJ, Li RW. Quantification of Transcriptome responses of the rumen epithelium to butyrate infusion using RNA-seq technology. Gene Regul Syst Bio. 2012;6:67–80. Baldwin RLt WS, Li W, Li C, Bequette BJ, Li RW. Quantification of Transcriptome responses of the rumen epithelium to butyrate infusion using RNA-seq technology. Gene Regul Syst Bio. 2012;6:67–80.
35.
go back to reference Li RW, Rinaldi M, Capuco AV. Characterization of the abomasal transcriptome for mechanisms of resistance to gastrointestinal nematodes in cattle. Vet Res. 2011;42:114.PubMedPubMedCentralCrossRef Li RW, Rinaldi M, Capuco AV. Characterization of the abomasal transcriptome for mechanisms of resistance to gastrointestinal nematodes in cattle. Vet Res. 2011;42:114.PubMedPubMedCentralCrossRef
36.
go back to reference Driver AM, Penagaricano F, Huang W, Ahmad KR, Hackbart KS, Wiltbank MC, Khatib H. RNA-Seq analysis uncovers transcriptomic variations between morphologically similar in vivo- and in vitro-derived bovine blastocysts. BMC Genomics. 2012;13:118.PubMedPubMedCentralCrossRef Driver AM, Penagaricano F, Huang W, Ahmad KR, Hackbart KS, Wiltbank MC, Khatib H. RNA-Seq analysis uncovers transcriptomic variations between morphologically similar in vivo- and in vitro-derived bovine blastocysts. BMC Genomics. 2012;13:118.PubMedPubMedCentralCrossRef
37.
go back to reference Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, Fan L, Sandelin A, Rinn JL, Regev A, Schier AF. Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res. 2012;22:577–91.PubMedPubMedCentralCrossRef Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, Fan L, Sandelin A, Rinn JL, Regev A, Schier AF. Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res. 2012;22:577–91.PubMedPubMedCentralCrossRef
38.
go back to reference Luo H, Sun S, Li P, Bu D, Cao H, Zhao Y. Comprehensive characterization of 10,571 mouse large intergenic noncoding RNAs from whole transcriptome sequencing. PLoS One. 2013;8:e70835.PubMedPubMedCentralCrossRef Luo H, Sun S, Li P, Bu D, Cao H, Zhao Y. Comprehensive characterization of 10,571 mouse large intergenic noncoding RNAs from whole transcriptome sequencing. PLoS One. 2013;8:e70835.PubMedPubMedCentralCrossRef
39.
go back to reference Ponjavic J, Ponting CP, Lunter G. Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res. 2007;17:556–65.PubMedPubMedCentralCrossRef Ponjavic J, Ponting CP, Lunter G. Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res. 2007;17:556–65.PubMedPubMedCentralCrossRef
40.
go back to reference Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, et al. Long noncoding RNAs with enhancer-like function in human cells. Cell. 2010;143:46–58.PubMedPubMedCentralCrossRef Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, et al. Long noncoding RNAs with enhancer-like function in human cells. Cell. 2010;143:46–58.PubMedPubMedCentralCrossRef
41.
go back to reference Kadakkuzha BM, Liu XA, McCrate J, Shankar G, Rizzo V, Afinogenova A, Young B, Fallahi M, Carvalloza AC, Raveendra B, Puthanveettil SV. Transcriptome analyses of adult mouse brain reveal enrichment of lncRNAs in specific brain regions and neuronal populations. Front Cell Neurosci. 2015;9:63.PubMedPubMedCentralCrossRef Kadakkuzha BM, Liu XA, McCrate J, Shankar G, Rizzo V, Afinogenova A, Young B, Fallahi M, Carvalloza AC, Raveendra B, Puthanveettil SV. Transcriptome analyses of adult mouse brain reveal enrichment of lncRNAs in specific brain regions and neuronal populations. Front Cell Neurosci. 2015;9:63.PubMedPubMedCentralCrossRef
43.
go back to reference Zhao H, Li T, Zhao Y, Tan T, Liu C, Liu Y, Chang L, Huang N, Li C, Fan Y, et al. Single-cell Transcriptomics of human oocytes: environment-driven metabolic competition and compensatory mechanisms during oocyte maturation. Antioxid Redox Signal. 2019;30:542–59.PubMedCrossRef Zhao H, Li T, Zhao Y, Tan T, Liu C, Liu Y, Chang L, Huang N, Li C, Fan Y, et al. Single-cell Transcriptomics of human oocytes: environment-driven metabolic competition and compensatory mechanisms during oocyte maturation. Antioxid Redox Signal. 2019;30:542–59.PubMedCrossRef
44.
go back to reference Stephenson JL, Brackett BG. Influences of zinc on fertilisation and development of bovine oocytes in vitro. Zygote. 1999;7:195–201.PubMedCrossRef Stephenson JL, Brackett BG. Influences of zinc on fertilisation and development of bovine oocytes in vitro. Zygote. 1999;7:195–201.PubMedCrossRef
45.
go back to reference Kong BY, Duncan FE, Que EL, Kim AM, O'Halloran TV, Woodruff TK. Maternally-derived zinc transporters ZIP6 and ZIP10 drive the mammalian oocyte-to-egg transition. Mol Hum Reprod. 2014;20:1077–89.PubMedPubMedCentralCrossRef Kong BY, Duncan FE, Que EL, Kim AM, O'Halloran TV, Woodruff TK. Maternally-derived zinc transporters ZIP6 and ZIP10 drive the mammalian oocyte-to-egg transition. Mol Hum Reprod. 2014;20:1077–89.PubMedPubMedCentralCrossRef
47.
go back to reference Swain JE, Wang X, Saunders TL, Dunn R, Smith GD. Specific inhibition of mouse oocyte nuclear protein phosphatase-1 stimulates germinal vesicle breakdown. Mol Reprod Dev. 2003;65:96–103.PubMedCrossRef Swain JE, Wang X, Saunders TL, Dunn R, Smith GD. Specific inhibition of mouse oocyte nuclear protein phosphatase-1 stimulates germinal vesicle breakdown. Mol Reprod Dev. 2003;65:96–103.PubMedCrossRef
48.
go back to reference Wang X, Swain JE, Bollen M, Liu XT, Ohl DA, Smith GD. Endogenous regulators of protein phosphatase-1 during mouse oocyte development and meiosis. Reproduction. 2004;128:493–502.PubMedCrossRef Wang X, Swain JE, Bollen M, Liu XT, Ohl DA, Smith GD. Endogenous regulators of protein phosphatase-1 during mouse oocyte development and meiosis. Reproduction. 2004;128:493–502.PubMedCrossRef
50.
go back to reference Zheng P, Dean J. Oocyte-specific genes affect folliculogenesis, fertilization, and early development. Semin Reprod Med. 2007;25:243–51.PubMedCrossRef Zheng P, Dean J. Oocyte-specific genes affect folliculogenesis, fertilization, and early development. Semin Reprod Med. 2007;25:243–51.PubMedCrossRef
51.
go back to reference Sirard MA. The Ovarian Follicle of Cows as a Model for Human. In: Schatten H, Constantinescu GM, editors. Animal Models and Human Reproduction. Hoboken: Wiley; 2017. p. 127–39. Sirard MA. The Ovarian Follicle of Cows as a Model for Human. In: Schatten H, Constantinescu GM, editors. Animal Models and Human Reproduction. Hoboken: Wiley; 2017. p. 127–39.
52.
go back to reference Simmet K, Zakhartchenko V, Philippou-Massier J, Blum H, Klymiuk N, Wolf E. OCT4/POU5F1 is required for NANOG expression in bovine blastocysts. Proc Natl Acad Sci U S A. 2018;115:2770–5.PubMedPubMedCentralCrossRef Simmet K, Zakhartchenko V, Philippou-Massier J, Blum H, Klymiuk N, Wolf E. OCT4/POU5F1 is required for NANOG expression in bovine blastocysts. Proc Natl Acad Sci U S A. 2018;115:2770–5.PubMedPubMedCentralCrossRef
Metadata
Title
Systematic identification of long intergenic non-coding RNAs expressed in bovine oocytes
Authors
Jian Wang
Prasanthi P. Koganti
Jianbo Yao
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2020
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-020-00573-4

Other articles of this Issue 1/2020

Reproductive Biology and Endocrinology 1/2020 Go to the issue