A landscape of circular RNA expression in the human heart

Cardiovascular Research

Volumn 113, Issue 3, 2017, Pages 298-309

  Tan, Wilson L W ^a   Lim, Benson T S ^a   Anene Nzelu, Chukwuemeka G O ^a,b   Ackers Johnson, Matthew ^a,b   Dashi, Albert ^a,b   See, Kelvin ^a   Tiang, Zenia ^a,b   Lee, Dominic Paul ^a   Chua, Wee Woon ^b   Luu, Tuan D A ^b   Li, Peter Y Q ^b   Richards, Arthur Mark ^b   Foo, Roger S Y ^a,b  

^a GENOME INSTITUTE OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY HEALTH SYSTEM   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CONNECTIN; RNA; RYANODINE RECEPTOR 2; GENETIC MARKER; MESSENGER RNA; RNA, CIRCULAR;

ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CARDIAC MUSCLE CELL; CONTROLLED STUDY; DMD GENE; EMBRYO; EXON; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; GENE EXPRESSION; HEART; HUMAN; HUMAN CELL; HUMAN EMBRYONIC STEM CELL; HUMAN TISSUE; INTRON; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; RNA SEQUENCE; SANGER SEQUENCING; ANIMAL; BIOLOGY; CASE CONTROL STUDY; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELL; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION STUDY; GENETIC DATABASE; GENETIC MARKER; GENETIC PREDISPOSITION; GENETICS; HEART DISEASES; HIGH THROUGHPUT SEQUENCING; METABOLISM; PHENOTYPE; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SINGLE MOLECULE IMAGING; TIME FACTOR;

ANIMALS; CASE-CONTROL STUDIES; CELL DIFFERENTIATION; CELL LINE; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC ASSOCIATION STUDIES; GENETIC MARKERS; GENETIC PREDISPOSITION TO DISEASE; HEART DISEASES; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; IN SITU HYBRIDIZATION, FLUORESCENCE; MICE; MYOCYTES, CARDIAC; PHENOTYPE; POLYMERASE CHAIN REACTION; RNA; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA; SINGLE MOLECULE IMAGING; TIME FACTORS;

EID: 85015149802     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvw250     Document Type: Article

References (57)

1. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, Xue C, Marinov GK, Khatun J, Williams BA, Zaleski C, Rozowsky J, Roder M, Kokocinski F, Abdelhamid RF, Alioto T, Antoshechkin I, Baer MT, Bar NS, Batut P, Bell K, Bell I, Chakrabortty S, Chen X, Chrast J, Curado J, Derrien T, Drenkow J, Dumais E, Dumais J, Duttagupta R, Falconnet E, Fastuca M, Fejes-Toth K, Ferreira P, Foissac S, Fullwood MJ, Gao H, Gonzalez D, Gordon A, Gunawardena H, Howald C, Jha S, Johnson R, Kapranov P, King B, Kingswood C, Luo OJ, Park E, Persaud K, Preall JB, Ribeca P, Risk B, Robyr D, Sammeth M, Schaffer L, See LH, Shahab A, Skancke J, Suzuki AM, Takahashi H, Tilgner H, Trout D, Walters N, Wang H, Wrobel J, Yu Y, Ruan X, Hayashizaki Y, Harrow J, Gerstein M, Hubbard T, Reymond A, Antonarakis SE, Hannon G, Giddings MC, Ruan Y, Wold B, Carninci P, Guigo R, Gingeras TR. Landscape of transcription in human cells. Nature 2012;489:101–108.
2. Carninci P. The transcriptional landscape of the mammalian genome. Science 2005;309:1559–1563.
3. Quiat D, Olson EN. Review series MicroRNAs in cardiovascular disease: from pathogenesis to prevention and treatment. J Clin Invest 2013;123:11–18.
4. Mayr M, Zampetaki A, Kiechl S. MicroRNA biomarkers for failing hearts? Eur Heart J 2013;34:2782–2783.
5. Thum T, Condorelli G. Long noncoding RNAs and microRNAs in cardiovascular pathophysiology. Circ Res 2015;116:751–762.
6. Thum T. MicroRNA therapeutics in cardiovascular medicine. EMBO Mol Med 2012;4:3–14.
7. Han P, Li W, Lin C-H, Yang J, Shang C, Nurnberg ST, Jin KK, Xu W, Lin C-Y, Lin C-J, Xiong Y, Chien H-C, Zhou B, Ashley E, Bernstein D, Chen P-S, Chen H-SV, Quertermous T, Chang C-P. A long noncoding RNA protects the heart from pathological hypertrophy. Nature 2014;514:102–106.
8. Anderson DM, Anderson KM, Chang CL, Makarewich CA, Nelson BR, McAnally JR, Kasaragod P, Shelton JM, Liou J, Bassel-Duby R, Olson EN. A micropeptide encoded by a putative long noncoding RNA regulates muscle performance. Cell 2015;160:595–606.
9. Rooij E van, Olson EN. MicroRNA therapeutics for cardiovascular disease: opportunities and obstacles. Nat Rev Drug Discov 2012;11:860–872.
10. Li Y, Zheng Q, Bao C, Li S, Guo W, Zhao J, Chen D, Gu J, He X, Huang S. Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res 2015;25:981–984.
11. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, Maier L, Mackowiak SD, Gregersen LH, Munschauer M, Loewer A, Ziebold U, Landthaler M, Kocks C, Noble F le, Rajewsky N. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 2013;495:333–338.
12. Jeck WR, Sorrentino J a, Wang K, Slevin MK, Burd CE, Liu J, Marzluff WF, Sharpless NE. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 2013;19:141–157.
13. Salzman J, Gawad C, Wang PL, Lacayo N, Brown PO. Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS ONE 2012;7.
14. Guo JU, Agarwal V, Guo H, Bartel DP. Expanded identification and characterization of mammalian circular RNAs. Genome Biol 2014;15:409.
15. Valdmanis PN, Kay MA. The expanding repertoire of circular RNAs. Mol Ther 2013;21:1112–1114.
16. € M, Refojo D, Kadener S, Rajewsky N. Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol Cell 2015;58:870–885.
17. Vicens Q, Westhof E. Biogenesis of circular RNAs. Cell 2014;159:13–14.
18. Ashwal-Fluss R, Meyer M, Pamudurti NR, Ivanov A, Bartok O, Hanan M, Evantal N, Memczak S, Rajewsky N, Kadener S. CircRNA biogenesis competes with Pre-mRNA splicing. Mol Cell 2014;56:55–66.
19. Ivanov A, Memczak S, Wyler E, Torti F, Porath HT, Orejuela MR, Piechotta M, Levanon EY, Landthaler M, Dieterich C, Rajewsky N. Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep 2015;10:170–177.
20. Li Z, Huang C, Bao C, Chen L, Lin M, Wang X, Zhong G, Yu B, Hu W, Dai L, Zhu P, Chang Z, Wu Q, Zhao Y, Jia Y, Xu P, Liu H, Shan G. Exon–intron circular RNAs regulate transcription in the nucleus. Nat Struct Mol Biol 2015;22:256–264.
21. Zhang Y, Zhang XO, Chen T, Xiang JF, Yin QF, Xing YH, Zhu S, Yang L, Chen LL. Circular intronic long noncoding RNAs. Mol Cell 2013;51:792–806.
22. Alhasan AA, Izuogu OG, Al-Balool HH, Steyn JS, Evans A, Colzani M, Ghevaert C, Mountford JC, Marenah L, Elliott DJ, Santibanez-Koref M, Jackson MS. Circular RNA enrichment in platelets is a signature of transcriptome degradation. Blood 2016;127:e1–e11.
23. Salzman J, Chen RE, Olsen MN, Wang PL, Brown PO. Cell-type specific features of circular RNA expression. PLoS Genet 2013;9.
24. Venø MT, Hansen TB, Venø ST, Clausen BH, Grebing M, Finsen B, Holm IE, Kjems J. Spatio-temporal regulation of circular RNA expression during porcine embryonic brain development. Genome Biol 2015;16:245.
25. Boeckel J-N, Jaé N, Heumüller AW, Chen W, Boon RA, Stellos K, Zeiher AM, John D, Uchida S, Dimmeler S. Identification and characterization of hypoxia-regulated endothelial circular RNA. Circ Res 2015;117:884–890.
26. Capel B, Swain A, Nicolis S, Hacker A, Walter M, Koopman P, Goodfellow P, Lovell-Badge R. Circular transcripts of the testis-determining gene Sry in adult mouse testis. Cell 1993;73:1019–1030.
27. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, Kjems J. Natural RNA circles function as efficient microRNA sponges. TL-495. Nature 2013;495:384–388.
28. Thomson DW, Dinger ME. Endogenous microRNA sponges: evidence and controversy. Nat Publ Gr 2016;17:272–283.
29. Szabo L, Morey R, Palpant NJ, Wang PL, Afari N, Jiang C, Parast MM, Murry CE, Laurent LC, Salzman J. Statistically based splicing detection reveals neural enrichment and tissue-specific induction of circular RNA during human fetal development. Genome Biol 2015;16:126.
30. Werfel S, Nothjunge S, Schwarzmayr T, Strom T, Meitinger T, Engelhardt S. Characterization of circular RNAs in human, mouse and rat hearts. J Mol Cell Cardiol 2016;98:103–107.
31. Movassagh M, Choy M, Knowles DA, Simeoni I, Penkett C, Goddard M, Foo S. Distinct epigenomic features in end-stage failing human hearts. 2013;124: 2411–2422.
32. Iyer MK, Niknafs YS, Malik R, Singhal U, Sahu A, Hosono Y, Barrette TR, Prensner JR, Evans JR, Zhao S, Poliakov A, Cao X, Dhanasekaran SM, Wu Y-M, Robinson DR, Beer DG, Feng FY, Iyer HK, Chinnaiyan AM. The landscape of long noncoding RNAs in the human transcriptome. Nat Genet 2015;47:199–208.
33. Siggens L, Figg N, Bennett M, Foo R. Nutrient deprivation regulates DNA damage repair in cardiomyocytes via loss of the base-excision repair enzyme OGG1. FASEB J 2012;26:2117–2124.
34. Foo RSY, Chan LKW, Kitsis RN, Bennett MR. Ubiquitination and degradation of the anti-apoptotic protein ARC by MDM2. J Biol Chem 2007;282:5529–5535.
35. Ackers-johnson M, Li PY, Holmes AP, Brien SO, Pavlovic D, Foo RS. A simplified, Langendorff-free method for concomitant isolation of viable cardiac myocytes and non-myocytes from the adult mouse heart right ventricle. Cardiovasc Res 2016;119:909–920.
36. Matkovich SJ, Edwards JR, Grossenheider TC, Strong CDG, Ii GWD. Epigenetic coordination of embryonic heart transcription by dynamically regulated long noncoding RNAs. 2014;111:12264–12269.
37. Lian X, Hsiao C, Wilson G, Zhu K, Hazeltine LB, Azarin SM, Raval KK, Zhang J, Kamp TJ, Palecek SP. Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling. Proc Natl Acad Sci U S A 2012;109:E1848–E1857.
38. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012;7:562–578.
39. Gao Y, Wang J, Zhao F. CIRI: an efficient and unbiased algorithm for de novo circular RNA identification. Genome Biol 2015;16:4.
40. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 2009;25:1754–1760.
41. Jeck WR, Sharpless NE. Detecting and characterizing circular RNAs. Nat Biotechnol 2013;18:1199–1216.
42. Tompkins JD, Jung M, Chen C, Lin Z, Ye J, Godatha S, Lizhar E, Wu X, Hsu D, Couture LA, Riggs AD. EBioMedicine mapping human pluripotent-to-cardiomyocyte differentiation: methylomes, transcriptomes, and exon DNA methylation “memories.” EBIOM 2016;4:74–85.
43. You X, Vlatkovic I, Babic A, Will T, Epstein I, Tushev G, Akbalik G, Wang M, Glock C, Quedenau C, Wang X, Hou J, Liu H, Sun W, Sambandan S, Chen T, Schuman EM, Chen W. Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity. Nat Neurosci 2015;18:603–610.
44. Roberts AM, Ware JS, Herman DS, Schafer S, Baksi J, Bick AG, Buchan RJ, Walsh R, John S, Wilkinson S, Mazzarotto F, Felkin LE, Gong S, MacArthur JAL, Cunningham F, Flannick J, Gabriel SB, Altshuler DM, Macdonald PS, Heinig M, Keogh AM, Hayward CS, Banner NR, Pennell DJ, O’Regan DP, San TR, de Marvao A, Dawes TJW, Gulati A, Birks EJ, Yacoub MH, Radke M, Gotthardt M, Wilson JG, O’Donnell CJ, Prasad SK, Barton PJR, Fatkin D, Hubner N, Seidman JG, Seidman CE, Cook SA. Integrated allelic, transcriptional, and phenomic dissection of the cardiac effects of titin truncations in health and disease. Sci Transl Med 2015;7:270ra6.
45. Herman DS. Truncations of titin causing dilated cardiomyopathy. N Engl J Med 2013;366:619–628.
46. Ponting CP, Grant Belgard T. Transcribed dark matter: meaning or myth? Hum Mol Genet 2010;19:162–168.
47. Nigro JM, Cho KR, Fearon ER, Kern SE, Ruppert JM, Oliner JD, Kinzler KW, Vogelstein B. Scrambled exons. Cell 1991;64:607–613.
48. Werfel S, Nothjunge S, Schwarzmayr T, Strom T-M, Meitinger T, Engelhardt S. Characterization of circular RNAs in human, mouse and rat hearts. J Mol Cell Cardiol 2016;98:103–107.
49. Jakobi T, Czaja-hasse LF, Reinhardt R, Dieterich C. Profiling and validation of the circular RNA repertoire in adult murine hearts. Genom Proteom Bioinf 2016;14:216–223.
50. Li XF, Lytton J. A circularized sodium-calcium exchanger exon 2 transcript. J Biol Chem 1999;274:8153–8160.
51. Gualandi F, Trabanelli C, Rimessi P, Calzolari E, Toffolatti L, Patarnello T, Kunz G, Muntoni F, Ferlini A. Multiple exon skipping and RNA circularisation contribute to the severe phenotypic expression of exon 5 dystrophin deletion. J Med Genet 2003;40:e100.
52. Du WW, Yang W, Chen Y, Wu Z, Foster FS, Yang Z, Li X, Yang BB. Foxo3 circular RNA promotes cardiac senescence by modulating multiple factors associated with stress and senescence responses. Eur Heart J 2016; doi: 10.1093/eurheartj/ehw001.
53. Enuka Y, Lauriola M, Feldman ME, Sas-Chen A, Ulitsky I, Yarden Y. Circular RNAs are long-lived and display only minimal early alterations in response to a growth factor. Nucleic Acids Res 2016;44:1370–1383.
54. Denkinger MD, Leins H, Schirmbeck R, Florian MC, Geiger H. HSC aging and senescent immune remodeling. Trends Immunol 2015;36:815–824.
55. Burd CE, Jeck WR, Liu Y, Sanoff HK, Wang Z, Sharpless NE. Expression of linear and novel circular forms of an INK4/ARF-associated non-coding RNA correlates with atherosclerosis risk. PLoS Genet 2010;6:1–15.
56. Wang K, Long B, Liu F, Wang J-X, Liu C-Y, Zhao B, Zhou L-Y, Sun T, Wang M, Yu T, Gong Y, Liu J, Dong Y-H, Li N, Li P-F. A circular RNA protects the heart from pathological hypertrophy and heart failure by targeting miR-223. Eur Heart J 2016;37:2602–2611.
57. Conn SJ, Pillman KA, Toubia J, Conn VM, Salmanidis M, Phillips CA, Roslan S, Schreiber AW, Gregory PA, Goodall GJ. The RNA binding protein quaking regulates formation of circRNAs. Cell 2015;160:1125–1134.