Adipose circular RNAs exhibit dynamic regulation in obesity and functional role in adipogenesis

Ng, M. et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 384, 766–781 (2014).

Arner, P. & Kulyte, A. MicroRNA regulatory networks in human adipose tissue and obesity. Nat. Rev. Endocrinol. 11, 276–288 (2015).

Kim, H. J. et al. MicroRNAs are required for the feature maintenance and differentiation of brown adipocytes. Diabetes 63, 4045–4056 (2014).

Sun, L. et al. Long noncoding RNAs regulate adipogenesis. Proc. Natl Acad. Sci. USA 110, 3387–3392 (2013).

Knoll, M., Lodish, H. F. & Sun, L. Long non-coding RNAs as regulators of the endocrine system. Nat. Rev. Endocrinol. 11, 151–160 (2015).

Zhao, X. Y., Li, S., Wang, G. X., Yu, Q. & Lin, J. D. A long noncoding RNA transcriptional regulatory circuit drives thermogenic adipocyte differentiation. Mol. Cell 55, 372–382 (2014).

Alvarez-Dominguez, J. R. et al. De novo reconstruction of adipose tissue transcriptomes reveals long non-coding RNA regulators of brown adipocyte development. Cell Metab. 21, 764–776 (2015).

Yang, L. et al. Integrative transcriptome analyses of metabolic responses in mice define pivotal lncRNA metabolic regulators. Cell Metab. 24, 627–639 (2016).

Ding, C. et al. De novo reconstruction of human adipose transcriptome reveals conserved lncRNAs as regulators of brown adipogenesis. Nat. Commun. 9, 1329 (2018).

Bai, Z. et al. Dynamic transcriptome changes during adipose tissue energy expenditure reveal critical roles for long noncoding RNA regulators. PLoS Biol. 15, e2002176 (2017).

Lo, K. A. et al. Adipocyte long-noncoding RNA transcriptome analysis of obese mice identified lnc-leptin, which regulates leptin. Diabetes 67, 1045–1056 (2018).

Starke, S. et al. Exon circularization requires canonical splice signals. Cell Rep. 10, 103–111 (2015).

Salzman, J., Gawad, C., Wang, P. L., Lacayo, N. & Brown, P. O. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS ONE 7, e30733 (2012).

Capel, B. et al. Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 73, 1019–1030 (1993).

Cocquerelle, C., Daubersies, P., Majerus, M. A., Kerckaert, J. P. & Bailleul, B. Splicing with inverted order of exons occurs proximal to large introns. EMBO J. 11, 1095–1098 (1992).

Nigro, J. M. et al. Scrambled exons. Cell 64, 607–613 (1991).

Wang, P. L. et al. Circular RNA is expressed across the eukaryotic tree of life. PLoS ONE 9, e90859 (2014).

Salzman, J., Chen, R. E., Olsen, M. N., Wang, P. L. & Brown, P. O. Cell-type specific features of circular RNA expression. PLoS Genet. 9, e1003777 (2013).

Memczak, S. et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495, 333–338 (2013).

Jeck, W. R. et al. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19, 141–157 (2013).

Chen, L. L. The biogenesis and emerging roles of circular RNAs. Nat. Rev. Mol. Cell Biol. 17, 205–211 (2016).

Li, Z. et al. Exon-intron circular RNAs regulate transcription in the nucleus. Nat. Struct. Mol. Biol. 22, 256–264 (2015).

Zhang, Y. et al. Circular intronic long noncoding RNAs. Mol. Cell 51, 792–806 (2013).

Zhang, Y. et al. The biogenesis of nascent circular RNAs. Cell Rep. 15, 611–624 (2016).

Ashwal-Fluss, R. et al. circRNA biogenesis competes with pre-mRNA splicing. Mol. Cell 56, 55–66 (2014).

Ivanov, A. et al. Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep. 10, 170–177 (2015).

Zhang, X. O. et al. Complementary sequence-mediated exon circularization. Cell 159, 134–147 (2014).

Kramer, M. C. et al. Combinatorial control of Drosophila circular RNA expression by intronic repeats, hnRNPs, and SR proteins. Genes Dev. 29, 2168–2182 (2015).

Rybak-Wolf, A. et al. Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol. Cell 58, 870–885 (2015).

Zheng, Q. et al. Circular RNA profiling reveals an abundant circHIPK3 that regulates cell growth by sponging multiple miRNAs. Nat. Commun. 7, 11215 (2016).

Hansen, T. B. et al. Natural RNA circles function as efficient microRNA sponges. Nature 495, 384–388 (2013).

Piwecka, M. et al. Loss of a mammalian circular RNA locus causes miRNA deregulation and affects brain function. Science 357, eaam8526 (2017).

Du, W. W. et al. Foxo3 circular RNA retards cell cycle progression via forming ternary complexes with p21 and CDK2. Nucleic Acids Res. 44, 2846–2858 (2016).

Legnini, I. et al. Circ-ZNF609 is a circular RNA that can be translated and functions in myogenesis. Mol. Cell 66, 22–37.e29 (2017).

Pamudurti, N. R. et al. Translation of circRNAs. Mol. Cell 66, 9–21.e27 (2017).

Yang, Y. et al. Extensive translation of circular RNAs driven by N6-methyladenosine. Cell Res. 27, 626–641 (2017).

Chen, Y., Li, C., Tan, C. & Liu, X. Circular RNAs: a new frontier in the study of human diseases. J. Med. Genet. 53, 359–365 (2016).

Guarnerio, J. et al. Oncogenic role of fusion-circRNAs derived from cancer-associated chromosomal translocations. Cell 166, 1055–1056 (2016).

Li, Y. et al. Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res. 25, 981–984 (2015).

Memczak, S., Papavasileiou, P., Peters, O. & Rajewsky, N. Identification and characterization of circular RNAs as a new class of putative biomarkers in human blood. PLoS ONE 10, e0141214 (2015).

Viereck, J. & Thum, T. Circulating noncoding RNAs as biomarkers of cardiovascular disease and injury. Circ. Res. 120, 381–399 (2017).

Xu, H., Guo, S., Li, W. & Yu, P. The circular RNA Cdr1as, via miR-7 and its targets, regulates insulin transcription and secretion in islet cells. Sci. Rep. 5, 12453 (2015).

Shan, K. et al. Circular non-coding RNA HIPK3 mediates retinal vascular dysfunction in diabetes mellitus. Circulation 136, 1629–1642 (2017).

Li, A., Huang, W., Zhang, X., Xie, L. & Miao, X. Identification and characterization of circRNAs of two pig breeds as a new biomarker in metabolism-related diseases. Cell. Physiol. Biochem. 47, 2458–2470 (2018).

Gao, Y., Wang, J. & Zhao, F. CIRI: an efficient and unbiased algorithm for de novo circular RNA identification. Genome Biol. 16, 4 (2015).

Zheng, Y. & Zhao, F. Detection and reconstruction of circular RNAs from transcriptomic data. Methods Mol. Biol. 1724, 1–8 (2018).

Reilly, S. M. & Saltiel, A. R. Adapting to obesity with adipose tissue inflammation. Nat. Rev. Endocrinol. 13, 633–643 (2017).

Yamamoto, M., Cid, E., Bru, S. & Yamamoto, F. Rare and frequent promoter methylation, respectively, of TSHZ2 and 3 genes that are both downregulated in expression in breast and prostate cancers. PLoS ONE 6, e17149 (2011).

Santos, J. S., Fonseca, N. A., Vieira, C. P., Vieira, J. & Casares, F. Phylogeny of the teashirt-related zinc finger (tshz) gene family and analysis of the developmental expression of tshz2 and tshz3b in the zebrafish. Dev. Dyn. 239, 1010–1018 (2010).

Ebert, M. S., Neilson, J. R. & Sharp, P. A. MicroRNA sponges: competitive inhibitors of small RNAs in mammalian cells. Nat. Methods 4, 721–726 (2007).

Guo, H., Ingolia, N. T., Weissman, J. S. & Bartel, D. P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466, 835–840 (2010).

Holdt, L. M. et al. Circular non-coding RNA ANRIL modulates ribosomal RNA maturation and atherosclerosis in humans. Nat. Commun. 7, 12429 (2016).

Abdelmohsen, K. et al. Identification of HuR target circular RNAs uncovers suppression of PABPN1 translation by CircPABPN1. RNA Biol. 14, 361–369 (2017).

Xue, R. et al. Clonal analyses and gene profiling identify genetic biomarkers of the thermogenic potential of human brown and white preadipocytes. Nat. Med. 21, 760–768 (2015).