Identification and characterization of circular RNAs as a new class of putative biomarkers in human blood

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Memczak, Sebastian ^a   Papavasileiou, Panagiotis ^a   Peters, Oliver ^b   Rajewsky, Nikolaus ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; CIRCULAR RNA; MESSENGER RNA; RNA ISOFORM; UNCLASSIFIED DRUG; RNA; RNA, CIRCULAR;

ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; QUANTITATIVE ANALYSIS; REPRODUCIBILITY; RNA ANALYSIS; RNA EXTRACTION; RNA SEQUENCE; RNA SPLICING; SEQUENCE ANALYSIS; BLOOD; BRAIN; GENETICS; ISOLATION AND PURIFICATION; LIVER; METABOLISM;

BIOMARKERS; BRAIN; HUMANS; LIVER; RNA;

EID: 84949238604     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0141214     Document Type: Article

References (40)

1. Batista PJ, Chang HY. Long Noncoding RNAs: Cellular Address Codes in Development and Disease. Cell. Elsevier Inc; 2013 Mar 14; 152(6): 1298-307
2. Cech TR, Steitz JA. The Noncoding RNA Revolution-Trashing Old Rules to Forge New Ones. Cell. Elsevier Inc; 2014 Mar 27; 157(1): 77-94
3. Jeck WR, Sharpless NE. Detecting and characterizing circular RNAs. Nature Biotechnology. Nature Publishing Group; 2014 May 1; 32(5): 453-61
4. Ashwal-Fluss R, Meyer M, Pamudurti NR, Ivanov A, Bartok O, Hanan M, et al. circRNA Biogenesis Competes with Pre-mRNA Splicing. Molecular Cell. Elsevier Inc. Elsevier Inc; 2014 Sep 17; 56: 1-12
5. Starke S, Jost I, Rossbach O, Schneider T, Schreiner S, Hung L-H, et al. Exon Circularization Requires Canonical Splice Signals. Cell Reports. 2015 Jan; 10(1): 103-11. doi: 10.1016/j.celrep.2014.12.002PMID: 25543144
6. Sanger HL, Klotz G, Riesner D, Gross HJ, Kleinschmidt AK. Viroids are single-stranded covalently closed circular RNA molecules existing as highly base-paired rod-like structures. Proceedings of the National Academy of Sciences of the United States of America. 1976 Nov; 73(11): 3852-6. PMID: 1069269
7. Grabowski PJ, Zaug AJ, Cech TR. The intervening sequence of the ribosomal RNA precursor is converted to a circular RNA in isolated nuclei of tetrahymena. Cell. 1981 Feb; 23(2): 467-76. PMID: 6162571
8. Kos A, Dijkema R, Arnberg AC, Van der Meide PH, Schellekens H. The hepatitis delta (d) virus possesses a circular RNA. Nature. Nature Publishing Group; 1986; 323
9. Nigro JM, Cho KR, Fearon ER, Kern SE, Ruppert JM, Oliner JD, et al. Scrambled exons. Cell. 1991Feb; 64(3): 607-13. PMID: 1991322
10. Cocquerelle C, Daubersies P, Majérus MA, Kerckaert JP, Bailleul B. Splicing with inverted order of exons occurs proximal to large introns. EMBO J. 1992 Mar; 11(3): 1095-8. PMID: 1339341
11. Cocquerelle C, Mascrez B, Hetuin D, Bailleul B. Mis-splicing yields circular RNA molecules. FASEB J. 1993 Jan; 7(1): 155-60. PMID: 7678559
12. Capel B, Swain A, Nicolis S, Hacker A, Walter M, Koopman P, et al. Circular transcripts of the testisdetermining gene Sry in adult mouse testis. Cell. 1993 Jun; 73(5): 1019-30. PMID: 7684656
13. Chao CW, Chan DC, Kuo A, Leder P. The mouse formin (Fmn) gene: abundant circular RNA transcripts and gene-Targeted deletion analysis. Molecular Medicine. The Feinstein Institute for Medical Research; 1998 Sep 1; 4(9): 614
14. Zaphiropoulos PG. Circular RNAs from transcripts of the rat cytochrome P450 2C24 gene: correlation with exon skipping. Proceedings of the National Academy of Sciences of the United States of America. 1996 Jun 25; 93(13): 6536-41. PMID: 8692851
15. Zaphiropoulos PG. Exon skipping and circular RNA formation in transcripts of the human cytochrome P-450 2C18 gene in epidermis and of the rat androgen binding protein gene in testis. Mol Cell Biol. 1997 Jun; 17(6): 2985-93. PMID: 9154796
16. 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. Public Library of Science; 2010 Dec 2; 6(12): e1001233. Available: http://dx.plos.org/10.1371/journal.pgen. 1001233.s008
17. Danan M, Schwartz S, Edelheit S, Sorek R. Transcriptome-wide discovery of circular RNAs in Archaea. Nucleic Acids Res. 2012 Apr 14; 40(7): 3131-42. doi: 10.1093/nar/gkr1009 PMID: 22140119
18. 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(2): e30733. doi: 10.1371/journal.pone.0030733 PMID: 22319583
19. Jeck WR, Sorrentino JA, Wang K, Slevin MK, Burd CE, Liu J, et al. Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA. 2013 Jan 16; 19(2): 141-57. doi: 10.1261/rna.035667.112 PMID: 23249747
20. Memczak S, Jens M, Elefsinioti A, Torti F, Krueger J, Rybak A, et al. Circular RNAs are a large class of animal RNAs with regulatory potency. Nature. Nature Publishing Group.; 2013 Mar 21; 495(7441): 333-8
21. Salzman J, Chen RE, Olsen MN, Wang PL, Brown PO. Cell-Type Specific Features of Circular RNA Expression. Moran JV, editor. PLoS Genetics. 2013 Sep 5; 9(9): e1003777. doi: 10.1371/journal.pgen. 1003777 PMID: 24039610
22. Wang PL, Bao Y, Yee M-C, Barrett SP, Hogan GJ, Olsen MN, et al. Circular RNA is expressed across the eukaryotic tree of life. PLoS ONE. 2014; 9(3): e90859
23. Guo JU, Agarwal V, Guo H, Bartel DP. Expanded identification and characterization of mammalian circular RNAs. 2014 Jul 29; 15: 1-14
24. You X, Vlatkovic I, Babic A, Will T, Epstein I, Tushev G, et al. Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity. Nat Neurosci. 2015 Feb 25
25. Rybak-Wolf A, Stottmeister C, Glažar P, Jens M, Pino N, Giusti S, et al. Circular RNAs in the Mammalian Brain Are Highly Abundant, Conserved, and Dynamically Expressed. Molecular Cell. Elsevier Inc; 2015 Apr 21; 58: 1-17
26. Zhang Y, Zhang X-O, Chen T, Xiang J-F, Yin Q-F, Xing Y-H, et al. Circular Intronic Long Noncoding RNAs. Molecular Cell. Elsevier Inc; 2013 Sep 10; 51: 1-15
27. Zhang X-O, Wang H-B, Zhang Y, Lu X, Chen L-L, Yang L. Complementary Sequence-Mediated Exon Circularization. Cell. 2014 Sep; 159
28. Liang D, Wilusz JE. Short intronic repeat sequences facilitate circular RNA production. Genes and Development. 2014 Oct 3; 28
29. Conn SJ, Pillman KA, Toubia J, Conn VM, Salmanidis M, Phillips CA, et al. The RNA Binding Protein Quaking Regulates Formation of circRNAs. Cell. 2015 Mar; 160(6): 1125-34. doi: 10.1016/j.cell.2015.02.014 PMID: 25768908
30. Ivanov A, Memczak S, Wyler E, Torti F, Porath HT, Orejuela MR, et al. Analysis of Intron Sequences Reveals Hallmarks of Circular RNA Biogenesis in Animals. CellReports. The Authors; 2015 Jan 13; 10 (2): 170-7
31. Hansen TB, Jensen TI, Clausen BH, Bramsen JB, Finsen B, Damgaard CK, et al. Natural RNA circles function as efficient microRNA sponges. Nature. 2013 Mar 21; 495(7441): 384-8. doi: 10.1038/nature11993 PMID: 23446346
32. Koh W, Pan W, Gawad C, Fan HC, Kerchner GA, Wyss-Coray T, et al. Noninvasive in vivo monitoring of tissue-specific global gene expression in humans. Proceedings of the National Academy of Sciences. 2014 May 20; 111(20): 7361-6
33. Bahn JH, Zhang Q, Li F, Chan TM, Lin X, Kim Y, et al. The Landscape of MicroRNA, Piwi-Interacting RNA, and Circular RNA in Human Saliva. Clinical Chemistry. 2014 Nov 6; 61
34. Li Y, Zheng Q, Bao C, Li S, Guo W, Zhao J, et al. Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res. 2015 Jul 3
35. Lukiw W. Circular RNA (circRNA) in Alzheimers disease (AD). Frontiers; 2013; 4: 307
36. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, et al. The human genome browser at UCSC. Genome Research. 2002 Jun; 12(6): 996-1006. PMID: 12045153
37. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nature Methods. 2012 Mar 4; 9 (4): 357-9. doi: 10.1038/nmeth.1923 PMID: 22388286
38. Glažar P, Papavasileiou P, Rajewsky N. circBase: a database for circular RNAs. RNA. 2014 Nov; 20 (11): 1666-70. doi: 10.1261/rna.043687.113 PMID: 25234927
39. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNAseq aligner. Bioinformatics. 2013 Dec 26; 29(1): 15-21. doi: 10.1093/bioinformatics/bts635 PMID: 23104886
40. Anders S, Pyl PT, Huber W. HTSeq-A Python framework to work with high-Throughput sequencing data. 2014 Feb