Analysis of pig transcriptomes suggests a global regulation mechanism enabling temporary bursts of circular RNAs

References

• Hsu MT, Coca-Prados M. Electron microscopic evidence for the circular form of RNA in the cytoplasm of eukaryotic cells. Nature. 1979;280(5720):339–340.
   PubMed Web of Science ®Google Scholar
• Holdt LM. Kohlmaier A and Teupser D. Molecular roles and function of circular RNAs in eukaryotic cells. Cell Mol Life Sci. 2018;75(6):1071–1098.
   PubMed Web of Science ®Google Scholar
• Jeck WR, Sorrentino JA, Wang K, et al. Circular RNAs are abundant, conserved, and associated with ALU repeats. Rna. 2013;19(2):141–157.
   PubMed Web of Science ®Google Scholar
• Memczak S, Jens M, Elefsinioti A, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. 2013;495(7441):333–338.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zhang XO, Chen T, et al. Circular intronic long noncoding RNAs. Mol Cell. 2013;51(6):792–806.
   PubMed Web of Science ®Google Scholar
• Osman I. Tay ML and Pek JW. Stable intronic sequence RNAs (sisRNAs): a new layer of gene regulation. Cell Mol Life Sci. 2016;73(18):3507–3519.
   PubMed Web of Science ®Google Scholar
• Gardner EJ, Nizami ZF, Talbot CC Jr., et al. Stable intronic sequence RNA (sisRNA), a new class of noncoding RNA from the oocyte nucleus of Xenopus tropicalis. Genes Dev. 2012;26(22):2550–2559.
   PubMed Web of Science ®Google Scholar
• Talhouarne GJS, Gall JG. Lariat intronic RNAs in the cytoplasm of vertebrate cells. Proc Natl Acad Sci U S A. 2018;115(34):E7970–E77.
   PubMed Web of Science ®Google Scholar
• Taggart AJ, Lin CL, Shrestha B, et al. Large-scale analysis of branchpoint usage across species and cell lines. Genome Res. 2017;27(4):639–649.
   PubMed Web of Science ®Google Scholar
• Talhouarne GJ, Gall JG. Lariat intronic RNAs in the cytoplasm of Xenopus tropicalis oocytes. Rna. 2014;20(9):1476–1487.
   PubMed Web of Science ®Google Scholar
• Huang S, Yang B, Chen BJ, et al. The emerging role of circular RNAs in transcriptome regulation. Genomics. 2017;109(5–6):401–407.
   PubMed Web of Science ®Google Scholar
• Li HM, Ma XL, Li HG. Intriguing circles: conflicts and controversies in circular RNA research. Wiley Interdiscip Rev RNA. 2019;e1538.
   PubMed Web of Science ®Google Scholar
• Hansen TB, Jensen TI, Clausen BH, et al. Natural RNA circles function as efficient microRNA sponges. Nature. 2013;495(7441):384–388.
   PubMed Web of Science ®Google Scholar
• Dhamija S, Menon MB. Non-coding transcript variants of protein-coding genes – what are they good for? RNA Biol. 2018;1025–1031.
   Google Scholar
• Wilusz JE. Circular RNAs: unexpected outputs of many protein-coding genes. RNA Biol. 2017;14(8):1007–1017.
   PubMed Web of Science ®Google Scholar
• Chen W, Schuman E. Circular RNAs in brain and other tissues: a functional enigma. Trends Neurosci. 2016;39(9):597–604.
   PubMed Web of Science ®Google Scholar
• Li Z, Huang C, Bao C, et al. Exon-intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol. 2015;22(3):256–264.
   PubMed Web of Science ®Google Scholar
• Mahmoudi E, Cairns MJ. Circular RNAs are temporospatially regulated throughout development and ageing in the rat. Sci Rep. 2019;9(1):2564.
   PubMedGoogle Scholar
• Zhou T, Xie X, Li M, et al. Rat BodyMap transcriptomes reveal unique circular RNA features across tissue types and developmental stages. Rna. 2018;24:1443–1456.
   Web of Science ®Google Scholar
• Westholm JO, Miura P, Olson S, et al. Genome-wide analysis of drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Rep. 2014;9(5):1966–1980.
   PubMed Web of Science ®Google Scholar
• Veno MT, Hansen TB, Veno ST, et al. Spatio-temporal regulation of circular RNA expression during porcine embryonic brain development. Genome Biol. 2015;16:245.
   PubMed Web of Science ®Google Scholar
• Szabo L, Morey R, Palpant NJ, et al. Statistically based splicing detection reveals neural enrichment and tissue-specific induction of circular RNA during human fetal development. Genome Biol. 2015;16:126.
   PubMed Web of Science ®Google Scholar
• Dang Y, Yan L, Hu B, et al. Tracing the expression of circular RNAs in human pre-implantation embryos. Genome Biol. 2016;17(1):130.
   PubMedGoogle Scholar
• Knupp D, Miura P. CircRNA accumulation: A new hallmark of aging? Mech Ageing Dev. 2018;173:71–79.
   PubMed Web of Science ®Google Scholar
• Hanan M. Soreq H and Kadener S. CircRNAs in the brain. RNA Biol. 2017;14(8):1028–1034.
   PubMed Web of Science ®Google Scholar
• Gruner H, Cortes-Lopez M, Cooper DA, et al. CircRNA accumulation in the aging mouse brain. Sci Rep. 2016;6:38907.
   PubMed Web of Science ®Google Scholar
• Rybak-Wolf A, Stottmeister C, Glazar P, et al. Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol Cell. 2015;58(5):870–885.
   PubMed Web of Science ®Google Scholar
• Abdelmohsen K, Panda AC, De S, et al. Circular RNAs in monkey muscle: age-dependent changes. Aging (Albany NY). 2015;7(11):903–910.
   PubMedGoogle Scholar
• Gorlach A, Holdenrieder S. Circular RNA maps paving the road to biomarker development? J Mol Med. 2017;95(11):1137–1141.
   PubMed Web of Science ®Google Scholar
• Robic A, Feve K, Riquet J, et al. Transcript levels of genes implicated in steroidogenesis in the testes and fat tissue in relation to androstenone accumulation in fat of pubertal pigs. Domest Anim Endocrinol. 2016;57:1–9.
   PubMed Web of Science ®Google Scholar
• Liang G, Yang Y, Niu G, et al. Genome-wide profiling of Sus scrofa circular RNAs across nine organs and three developmental stages. DNA Res. 2017;24(5):523–535.
   PubMed Web of Science ®Google Scholar
• Dong WW, Li HM, Qing XR, et al. Identification and characterization of human testis derived circular RNAs and their existence in seminal plasma. Sci Rep. 2016;6:39080.
   PubMed Web of Science ®Google Scholar
• Hansen TB. Improved circRNA identification by combining prediction algorithms. Front Cell Dev Biol. 2018;6:20.
   PubMed Web of Science ®Google Scholar
• Afgan E, Baker D, Batut B, et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res. 2018;46(W1):W537–W44.
   PubMed Web of Science ®Google Scholar
• Cheng J, Metge F, Dieterich C. Specific identification and quantification of circular RNAs from sequencing data. Bioinformatics. 2016;32(7):1094–1096.
   PubMed Web of Science ®Google Scholar
• Dobin A, Davis CA, Schlesinger F, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29(1):15–21.
   PubMed Web of Science ®Google Scholar
• Suzuki H, Zuo Y, Wang J, et al. Characterization of RNase R-digested cellular RNA source that consists of lariat and circular RNAs from pre-mRNA splicing. Nucleic Acids Res. 2006;34(8):e63.
   PubMed Web of Science ®Google Scholar
• Ragan C, Goodall GJ, Shirokikh NE, et al. Insights into the biogenesis and potential functions of exonic circular RNA. Sci Rep. 2019;9(1):2048.
   PubMedGoogle Scholar
• Project e. Enhancing GTEx by bridging the gaps between genotype, gene expression, and disease. Nat Genet. 2017;49(12):1664–1670.
   PubMed Web of Science ®Google Scholar
• Klein BJ, Piao L, Xi Y, et al. The histone-H3K4-specific demethylase KDM5B binds to its substrate and product through distinct PHD fingers. Cell Rep. 2014;6(2):325–335.
   PubMed Web of Science ®Google Scholar
• Jakobi T, Dieterich C. Computational approaches for circular RNA analysis. Wiley Interdiscip Rev RNA. 2019;10(3):e1528.
   PubMed Web of Science ®Google Scholar
• Konarska MM, Grabowski PJ, Padgett RA, et al. Characterization of the branch site in lariat RNAs produced by splicing of mRNA precursors. Nature. 1985;313(6003):552–557.
   PubMed Web of Science ®Google Scholar
• Kristensen LS, Okholm TLH, Veno MT, et al. Circular RNAs are abundantly expressed and upregulated during human epidermal stem cell differentiation. RNA Biol. 2018;15(2):280–291.
   PubMed Web of Science ®Google Scholar
• Salzman J, Gawad C, Wang PL, et al. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS One. 2012;7(2):e30733.
   PubMed Web of Science ®Google Scholar
• Ashwal-Fluss R, Meyer M, Pamudurti NR, et al. circRNA biogenesis competes with pre-mRNA splicing. Mol Cell. 2014;56(1):55–66.
   PubMed Web of Science ®Google Scholar
• Li M, Xie X, Zhou J, et al. Quantifying circular RNA expression from RNA-seq data using model-based framework. Bioinformatics. 2017;33(14):2131–2139.
   PubMed Web of Science ®Google Scholar
• Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011;12:323.
   PubMed Web of Science ®Google Scholar
• Kong Z, Wan X, Zhang Y, et al. Androgen-responsive circular RNA circSMARCA5 is up-regulated and promotes cell proliferation in prostate cancer. Biochem Biophys Res Commun. 2017;493(3):1217–1223.
   PubMed Web of Science ®Google Scholar
• Maass PG, Glazar P, Memczak S, et al. A map of human circular RNAs in clinically relevant tissues. J Mol Med. 2017;95(11):1179–1189.
   PubMed Web of Science ®Google Scholar
• Liang D, Tatomer DC, Luo Z, et al. The output of protein-coding genes shifts to circular RNAs when the pre-mRNA processing machinery is limiting. Mol Cell. 2017;68(5):940–54 e3.
   PubMed Web of Science ®Google Scholar
• Zamaratskaia G, Babol J, Madej A. et al. Age-related variation of plasma concentrations of skatole, androstenone, testosterone, oestradiol-17 beta, oestrone sulphate, dehydroepiandrosterone sulphate, triiodothyronine and IGF-1 in six entire male pigs. Reprod Domest Anim. 2004;39(3):168–172. doi:10.1111/j.1439-0531.2004.00496.x
   PubMed Web of Science ®Google Scholar
• Kanematsu N, Jin W, Watanabe G, et al. Age-related changes of reproductive hormones in young Meishan boars. J Reprod Dev. 2006;52(5):651–656.
   PubMed Web of Science ®Google Scholar