Circular RNAs: Analysis, expression and potential functions

Development (Cambridge)

Volumn 143, Issue 11, 2016, Pages 1838-1847

  Barrett, Steven P ^a   Salzman, Julia ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD CANCER INSTITUTE   (United States)

Author keywords

CircRNA; Development; Non coding RNA; Regulation; Splicing

Indexed keywords

CIRCULAR RNA; RIBOSOME RNA; RNA; UNCLASSIFIED DRUG; RNA, CIRCULAR;

ALU SEQUENCE; ARTICLE; BIOGENESIS; ECTOPIC EXPRESSION; GENE EXPRESSION; GENETIC ANALYSIS; HUMAN; IMMUNOPRECIPITATION; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; REVERSE TRANSCRIPTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SRY GENE; TISSUE SPECIFICITY; TRANS SPLICING; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; RNA SPLICING;

ANIMALS; COMPUTATIONAL BIOLOGY; GENE EXPRESSION REGULATION; HUMANS; MODELS, GENETIC; RNA; RNA SPLICING;

EID: 84973538565     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.128074     Document Type: Article

References (66)

1. Agabian, N. (1990). Trans splicing of nuclear pre-mRNAs. Cell 61, 1157-1160.
2. Artero, R., Prokop, A., Paricio, N., Begemann, G., Pueyo, I., Mlodzik, M., Perez-Alonso, M. and Baylies, M. K. (1998). The muscleblind gene participates in the organization of Z-bands and epidermal attachments of Drosophila muscles and is regulated by Dmef2. Dev. Biol. 195, 131-143.
3. Ashwal-Fluss, R., Meyer, M., Pamudurti, N. R., Ivanov, A., Bartok, O., Hanan, M., Evantal, N., Memczak, S., Rajewsky, N. and Kadener, S. (2014). circRNA biogenesis competes with pre-mRNA splicing. Mol. Cell 56, 55-66.
4. Awan, A. R., Manfredo, A. and Pleiss, J. A. (2013). Lariat sequencing in a unicellular yeast identifies regulated alternative splicing of exons that are evolutionarily conserved with humans. Proc. Natl. Acad. Sci. USA 110, 12762-12767.
5. Barrett, S. P., Wang, P. L. and Salzman, J. (2015). Circular RNA biogenesis can proceed through an exon-containing lariat precursor. Elife 4, e07540.
6. Bazak, L., Levanon, E. Y. and Eisenberg, E. (2014). Genome-wide analysis of Alu editability. Nucleic Acids Res. 42, 6876-6884.
7. Begemann, G., Paricio, N., Artero, R., Kiss, I., Perez-Alonso, M. and Mlodzik, M. (1997). muscleblind, a gene required for photoreceptor differentiation in Drosophila, encodes novel nuclear Cys3His-type zinc-finger-containing proteins. Development 124, 4321-4331.
8. Burd, C. E., Jeck, W. R., Liu, Y., Sanoff, H. K., Wang, Z. and Sharpless, N. E. (2010). Expression of linear and novel circular forms of an INK4/ARF-associated non-coding RNA correlates with atherosclerosis risk. PLoS Genet. 6, e1001233.
9. Cajigas, I. J., Tushev, G., Will, T. J., tom Dieck, S., Fuerst, N. and Schuman, E. M. (2012). The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 74, 453-466.
10. Capel, B., Swain, A., Nicolis, S., Hacker, A., Walter, M., Koopman, P., Goodfellow, P. and Lovell-Badge, R. (1993). Circular transcripts of the testisdetermining gene Sry in adult mouse testis. Cell 73, 1019-1030.
11. Chen, C. Y. and Sarnow, P. (1995). Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science 268, 415-417.
12. Cocquerelle, C., Daubersies, P., Majérus, M. A., Kerckaert, J. P. and Bailleul, B. (1992). Splicing with inverted order of exons occurs proximal to large introns. EMBO J. 11, 1095-1098.
13. Cocquerelle, C., Mascrez, B., Hetuin, D. and Bailleul, B. (1993). Mis-splicing yields circular RNA molecules. FASEB J. 7, 155-160.
14. Cocquet, J., Chong, A., Zhang, G. and Veitia, R. A. (2006). Reverse transcriptase template switching and false alternative transcripts. Genomics 88, 127-131.
15. Conn, S. J., Pillman, K. A., Toubia, J., Conn, V. M., Salmanidis, M., Phillips, C. A., Roslan, S., Schreiber, A. W., Gregory, P. A. and Goodall, G. J. (2015). The RNA binding protein quaking regulates formation of circRNAs. Cell 160, 1125-1134.
16. Denzler, R., Agarwal, V., Stefano, J., Bartel, D. P. and Stoffel, M. (2014). Assessing the ceRNA hypothesis with quantitative measurements of miRNA and target abundance. Mol. Cell 54, 766-776.
17. Dubin, R. A., Kazmi, M. A. and Ostrer, H. (1995). Inverted repeats are necessary for circularization of the mouse testis Sry transcript. Gene 167, 245-248.
18. Engström, P. G., Steijger, T., Sipos, B., Grant, G. R., Kahles, A., Rätsch, G., Goldman, N., Hubbard, T. J., Harrow, J., Guigó, R. et al. (2013). Systematic evaluation of spliced alignment programs for RNA-seq data. Nat. Methods 10, 1185-1191.
19. Glažar, P., Papavasileiou, P. and Rajewsky, N. (2014). circBase: a database for circular RNAs. RNA 20, 1666-1670.
20. Guo, J. U., Agarwal, V., Guo, H. and Bartel, D. P. (2014). Expanded identification and characterization of mammalian circular RNAs. Genome Biol. 15, 409.
21. Hacker, A., Capel, B., Goodfellow, P. and Lovell-Badge, R. (1995). Expression of Sry, the mouse sex determining gene. Development 121, 1603-1614.
22. Hansen, T. B., Wiklund, E. D., Bramsen, J. B., Villadsen, S. B., Statham, A. L., Clark, S. J. and Kjems, J. (2011). miRNA-dependent gene silencing involving Ago2-mediated cleavage of a circular antisense RNA. EMBO J. 30, 4414-4422.
23. Hansen, T. B., Jensen, T. I., Clausen, B. H., Bramsen, J. B., Finsen, B., Damgaard, C. K. and Kjems, J. (2013). Natural RNA circles function as efficient microRNA sponges. Nature 495, 384-388.
24. Hansen, T. B., Venø, M. T., Damgaard, C. K. and Kjems, J. (2015). Comparison of circular RNA prediction tools. Nucleic Acids Res. 44, e58.
25. Higuchi, M., Maas, S., Single, F. N., Hartner, J., Rozov, A., Burnashev, N., Feldmeyer, D., Sprengel, R. and Seeburg, P. H. (2000). Point mutation in an AMPA receptor gene rescues lethality in mice deficient in the RNA-editing enzyme ADAR2. Nature 406, 78-81.
26. Houseley, J. M., Garcia-Casado, Z., Pascual, M., Paricio, N., O’Dell, K. M. C., Monckton, D. G. and Artero, R. D. (2006). Noncanonical RNAs from transcripts of the Drosophila muscleblind gene. J. Hered. 97, 253-260.
27. Ivanov, A., Memczak, S., Wyler, E., Torti, F., Porath, H. T., Orejuela, M. R., Piechotta, M., Levanon, E. Y., Landthaler, M., Dieterich, C. et al. (2015). Analysis of intron sequences reveals hallmarks of circular RNA biogenesis in animals. Cell Rep. 10, 170-177.
28. Jeck, W. R., Sorrentino, J. A., Wang, K., Slevin, M. K., Burd, C. E., Liu, J., Marzluff, W. F. and Sharpless, N. E. (2013). Circular RNAs are abundant, conserved, and associated with ALU repeats. RNA 19, 141-157.
29. Jordan, M. C., Henderson, S. A., Han, T., Fishbein, M. C., Philipson, K. D. and Roos, K. P. (2010). Myocardial function with reduced expression of the sodiumcalcium exchanger. J. Card. Fail. 16, 786-796.
30. Kramer, M. C., Liang, D., Tatomer, D. C., Gold, B., March, Z. M., Cherry, S. and Wilusz, J. E. (2015). Combinatorial control of Drosophila circular RNA expression by intronic repeats, hnRNPs, and SR proteins. Genes Dev. 29, 2168-2182.
31. Kulpa, D., Topping, R. and Telesnitsky, A. (1997). Determination of the site of first strand transfer during Moloney murine leukemia virus reverse transcription and identification of strand transfer-associated reverse transcriptase errors. EMBO J. 16, 856-865.
32. Li, X.-F. and Lytton, J. (1999). A circularized sodium-calcium exchanger exon 2 transcript. J. Biol. Chem. 274, 8153-8160.
33. Li, Z., Huang, C., Bao, C., Chen, L., Lin, M., Wang, X., Zhong, G., Yu, B., Hu, W., Dai, L. et al. (2015). Exon-intron circular RNAs regulate transcription in the nucleus. Nat. Struct. Mol. Biol. 22, 256-264.
34. Liang, D. and Wilusz, J. E. (2014). Short intronic repeat sequences facilitate circular RNA production. Genes Dev. 28, 2233-2247.
35. Luo, G. X. and Taylor, J. (1990). Template switching by reverse transcriptase during DNA synthesis. J. Virol. 64, 4321-4328.
36. Memczak, S., Jens, M., Elefsinioti, A., Torti, F., Krueger, J., Rybak, A., Maier, L., Mackowiak, S. D., Gregersen, L. H., Munschauer, M. et al. (2013). Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495, 333-338.
37. Morris, K. V. and Mattick, J. S. (2014). The rise of regulatory RNA. Nat. Rev. Genet. 15, 423-437.
38. Nigro, J. M., Cho, K. R., Fearon, E. R., Kern, S. E., Ruppert, J. M., Oliner, J. D., Kinzler, K. W. and Vogelstein, B. (1991). Scrambled exons. Cell 64, 607-613.
39. Nishikura, K. (2010). Functions and regulation of RNA editing by ADAR deaminases. Annu. Rev. Biochem. 79, 321-349.
40. Noveroske, J. K., Lai, L., Gaussin, V., Northrop, J. L., Nakamura, H., Hirschi, K. K. and Justice, M. J. (2002). Quaking is essential for blood vessel development. Genesis 32, 218-230.
41. Peng, Z., Yuan, C., Zellmer, L., Liu, S., Xu, N. and Liao, D. J. (2015). Hypothesis: artifacts, including spurious chimeric RNAs with a short homologous sequence, caused by consecutive reverse transcriptions and endogenous random primers. J. Cancer 6, 555-567.
42. Perriman, R. and Ares, M. (1998). Circular mRNA can direct translation of extremely long repeating-sequence proteins in vivo. RNA 4, 1047-1054.
43. Roy, C. K., Olson, S., Graveley, B. R., Zamore, P. D. and Moore, M. J. (2015). Assessing long-distance RNA sequence connectivity via RNA-templated DNA-DNA ligation. Elife 4, e03700.
44. Rybak-Wolf, A., Stottmeister, C., Glažar, P., Jens, M., Pino, N., Giusti, S., Hanan, M., Behm, M., Bartok, O., Ashwal-Fluss, R. et al. (2015). Circular RNAs in the mammalian brain are highly abundant, conserved, and dynamically expressed. Mol. Cell 58, 870-885.
45. Salzman, J., Jiang H. and Wong, W. H. (2011). Statistical modeling of RNA-Seq data. Stat. Sci. 26, 62-83.
46. Salzman, J., Gawad, C.,Wang, P. L., Lacayo, N. and Brown, P. O. (2012). Circular RNAs are the predominant transcript isoform from hundreds of human genes in diverse cell types. PLoS ONE 7, e30733.
47. Salzman, J., Chen, R. E., Olsen, M. N.,Wang, P. L. and Brown, P. O. (2013). Celltype specific features of circular RNA expression. PLoS Genet. 9, e1003777.
48. Schindewolf, C., Braun, S. and Domdey, H. (1996). In vitro generation of a circular exon from a linear pre-mRNA transcript. Nucleic Acids Res. 24, 1260-1266.
49. Sidman, R. L., Dickie, M. M. and Appel, S. H. (1964). Mutant mice (Quaking and Jimpy) with deficient myelination in the central nervous system. Science 144, 309-311.
50. Starke, S., Jost, I., Rossbach, O., Schneider, T., Schreiner, S., Hung, L.-H. and Bindereif, A. (2015). Exon circularization requires canonical splice signals. Cell Rep. 10, 103-111.
51. Surono, A., Takeshima, Y., Wibawa, T., Ikezawa, M., Nonaka, I. and Matsuo, M. (1999). Circular dystrophin RNAs consisting of exons that were skipped by alternative splicing. Hum. Mol. Genet. 8, 493-500.
52. Suzuki, H., Zuo, Y., Wang, J., Zhang, M. Q., Malhotra, A. and Mayeda, A. (2006). Characterization of RNase R-digested cellular RNA source that consists of lariat and circular RNAs from pre-mRNA splicing. Nucleic Acids Res. 34, e63.
53. Szabo, L., Morey, R., Palpant, N. J., Wang, P. L., Afari, N., Jiang, C., Parast, M. M., Murry, C. E., Laurent, L. C. and Salzman, J. (2015). Statistically based splicing detection reveals neural enrichment and tissue-specific induction of circular RNA during human fetal development. Genome Biol. 16, 126.
54. Tabak, H. F., Van der Horst, G., Smit, J., Winter, A. J., Mul, Y. and Groot Koerkamp, M. J. A. (1988). Discrimination betweenRNA circles, interlocked RNA circles and lariats using two-dimensional polyacrylamide gel electrophoresis. Nucleic Acids Res. 16, 6597-6605.
55. Tai, H.-C. and Schuman, E. M. (2006). MicroRNA: microRNAs reach out into dendrites. Curr. Biol. 16, R121-R123.
56. Tsai, M.-C., Manor, O.,Wan, Y., Mosammaparast, N.,Wang, J. K., Lan, F., Shi, Y., Segal, E. and Chang, H. Y. (2010). Long noncoding RNA as modular scaffold of histone modification complexes. Science 329, 689-693.
57. Venø, M. T., Hansen, T. B., Venø, S. T., Clausen, B. H., Grebing, M., Finsen, B., Holm, I. E. and Kjems, J. (2015). Spatio-temporal regulation of circular RNA expression during porcine embryonic brain development. Genome Biol. 16, 245.
58. Vincent, H. A. and Deutscher, M. P. (2006). Substrate recognition and catalysis by the exoribonuclease RNase R. J. Biol. Chem. 281, 29769-29775.
59. Wang, Q., Khillan, J., Gadue, P. and Nishikura, K. (2000). Requirement of the RNA editing deaminase ADAR1 gene for embryonic erythropoiesis. Science 290, 1765-1768.
60. Wang, P. L., Bao, Y., Yee, M.-C., Barrett, S. P., Hogan, G. J., Olsen, M. N., Dinneny, J. R., Brown, P. O. and Salzman, J. (2014). Circular RNA is expressed across the eukaryotic tree of life. PLoS ONE 9, e90859.
61. Westholm, J. O., Miura, P., Olson, S., Shenker, S., Joseph, B., Sanfilippo, P., Celniker, S. E., Graveley, B. R. and Lai, E. C. (2014). Genome-wide analysis of drosophila circular RNAs reveals their structural and sequence properties and age-dependent neural accumulation. Cell Rep. 9, 1966-1980.
62. Yoon, J. H., Abdelmohsen, K., Kim, J., Yang, X., Martindale, J. L., Tominaga-Yamanaka, K., White, E. J., Orjalo, A. V., Rinn, J. L., Kreft, S. G. et al. (2013). Scaffold function of long non-coding RNA HOTAIR in protein ubiquitination. Nat. Commun. 4, 2939.
63. You, X., Vlatkovic, I., Babic, A., Will, T., Epstein, I., Tushev, G., Akbalik, G., Wang, M., Glock, C., Quedenau, C. et al. (2015). Neural circular RNAs are derived from synaptic genes and regulated by development and plasticity. Nat. Neurosci. 18, 603-610.
64. Zaphiropoulos, P. G. (1996). Circular RNAs from transcripts of the rat cytochrome P450 2C24 gene: correlation with exon skipping. Proc. Natl. Acad. Sci. USA 93, 6536-6541.
65. Zaphiropoulos, P. G. (1997). 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. 17, 2985-2993.
66. Zhang, X.-O., Wang, H.-B., Zhang, Y., Lu, X., Chen, L.-L. and Yang, L. (2014). Complementary sequence-mediated exon circularization. Cell 159, 134-147.