Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Incredible RNA: Dual Functions of Coding and Noncoding

  • Nam, Jin-Wu (Department of Life Science, College of Natural Sciences, Hanyang University) ;
  • Choi, Seo-Won (Department of Life Science, College of Natural Sciences, Hanyang University) ;
  • You, Bo-Hyun (Department of Life Science, College of Natural Sciences, Hanyang University)
  • Received : 2016.02.15
  • Accepted : 2016.03.29
  • Published : 2016.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

Since the RNA world hypothesis was proposed, a large number of regulatory noncoding RNAs (ncRNAs) have been identified in many species, ranging from microorganisms to mammals. During the characterization of these newly discovered RNAs, RNAs having both coding and noncoding functions were discovered, and these were considered bifunctional RNAs. The recent use of computational and high-throughput experimental approaches has revealed increasing evidence of various sources of bifunctional RNAs, such as protein-coding mRNAs with a noncoding isoform and long ncRNAs bearing a small open reading frame. Therefore, the genomic diversity of Janusfaced RNA molecules that have dual characteristics of coding and noncoding indicates that the functional roles of RNAs have to be revisited in cells on a genome-wide scale. Such studies would allow us to further understand the complex gene-regulatory network in cells. In this review, we discuss three major genomic sources of bifunctional RNAs and present a handful of examples of bifunctional RNA along with their functional roles.

Keywords

References

  1. Anderson, D.M., Anderson, K.M., Chang, C.L., Makarewich, C.A., Nelson, B.R., McAnally, J.R., Kasaragod, P., Shelton, J.M., Liou, J., Bassel-Duby, R., et al. (2015). A micropeptide encoded by a putative long noncoding RNA regulates muscle performance. Cell 160, 595-606. https://doi.org/10.1016/j.cell.2015.01.009
  2. Andrews, S.J., and Rothnagel, J.A. (2014). Emerging evidence for functional peptides encoded by short open reading frames. Nat. Rev. Genet. 15, 193-204. https://doi.org/10.1038/nrg3520
  3. Aspden, J.L., Eyre-Walker, Y.C., Phillips, R.J., Amin, U., Mumtaz, M.A., Brocard, M., and Couso, J.P. (2014). Extensive translation of small open reading frames revealed by Poly-Ribo-Seq. Elife 3, e03528.
  4. Bartel, D.P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233. https://doi.org/10.1016/j.cell.2009.01.002
  5. Beadle, G.W., and Tatum, E.L. (1941). Genetic Control of Biochemical Reactions in Neurospora. Proc. Natl. Acad. Sci. USA 27, 499-506. https://doi.org/10.1073/pnas.27.11.499
  6. Bommer, U.A., Borovjagin, A.V., Greagg, M.A., Jeffrey, I.W., Russell, P., Laing, K.G., Lee, M., and Clemens, M.J. (2002). The mRNA of the translationally controlled tumor protein P23/TCTP is a highly structured RNA, which activates the dsRNA-dependent protein kinase PKR. RNA 8, 478-496. https://doi.org/10.1017/S1355838202022586
  7. Bussard, A.E. (2005). A scientific revolution? The prion anomaly may challenge the central dogma of molecular biology. EMBO Rep. 6, 691-694. https://doi.org/10.1038/sj.embor.7400497
  8. Calviello, L., Mukherjee, N., Wyler, E., Zauber, H., Hirsekorn, A., Selbach, M., Landthaler, M., Obermayer, B., and Ohler, U. (2016). Detecting actively translated open reading frames in ribosome profiling data. Nat. Methods 13, 165-170. https://doi.org/10.1038/nmeth.3688
  9. Candeias, M.M., Malbert-Colas, L., Powell, D.J., Daskalogianni, C., Maslon, M.M., Naski, N., Bourougaa, K., Calvo, F., and Fahraeus, R. (2008). P53 mRNA controls p53 activity by managing Mdm2 functions. Nat. Cell Biol. 10, 1098-1105. https://doi.org/10.1038/ncb1770
  10. Cech, T.R., and Steitz, J.A. (2014). The noncoding RNA revolutiontrashing old rules to forge new ones. Cell 157, 77-94. https://doi.org/10.1016/j.cell.2014.03.008
  11. Chooniedass-Kothari, S., Emberley, E., Hamedani, M.K., Troup, S., Wang, X., Czosnek, A., Hube, F., Mutawe, M., Watson, P.H., and Leygue, E. (2004). The steroid receptor RNA activator is the first functional RNA encoding a protein. FEBS Lett. 566, 43-47. https://doi.org/10.1016/j.febslet.2004.03.104
  12. Consortium, E.P. (2012). An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74. https://doi.org/10.1038/nature11247
  13. Crick, F. (1970). Central dogma of molecular biology. Nature 227, 561-563. https://doi.org/10.1038/227561a0
  14. Forster, A.C., and Symons, R.H. (1987). Self-cleavage of plus and minus RNAs of a virusoid and a structural model for the active sites. Cell 49, 211-220. https://doi.org/10.1016/0092-8674(87)90562-9
  15. Gimpel, M., Heidrich, N., Mader, U., Krugel, H., and Brantl, S. (2010). A dual-function sRNA from B. subtilis: SR1 acts as a peptide encoding mRNA on the gapA operon. Mol. Microbiol. 76, 990-1009. https://doi.org/10.1111/j.1365-2958.2010.07158.x
  16. Gong, C., and Maquat, L.E. (2011). lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3' UTRs via Alu elements. Nature 470, 284-288. https://doi.org/10.1038/nature09701
  17. Gonzalez-Porta, M., Frankish, A., Rung, J., Harrow, J., and Brazma, A. (2013). Transcriptome analysis of human tissues and cell lines reveals one dominant transcript per gene. Genome Biol. 14, R70. https://doi.org/10.1186/gb-2013-14-7-r70
  18. Guttman, M., Russell, P., Ingolia, N.T., Weissman, J.S., and Lander, E.S. (2013). Ribosome profiling provides evidence that large noncoding RNAs do not encode proteins. Cell 154, 240-251. https://doi.org/10.1016/j.cell.2013.06.009
  19. Hanada, K., Zhang, X., Borevitz, J.O., Li, W.H., and Shiu, S.H. (2007). A large number of novel coding small open reading frames in the intergenic regions of the Arabidopsis thaliana genome are transcribed and/or under purifying selection. Genome Res. 17, 632-640. https://doi.org/10.1101/gr.5836207
  20. Hangauer, M.J., Vaughn, I.W., and McManus, M.T. (2013). Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs. PLoS Genet. 9, e1003569. https://doi.org/10.1371/journal.pgen.1003569
  21. Hatzoglou, A., Deshayes, F., Madry, C., Lapree, G., Castanas, E., and Tsapis, A. (2002). Natural antisense RNA inhibits the expression of BCMA, a tumour necrosis factor receptor homologue. BMC Mol. Biol. 3, 4. https://doi.org/10.1186/1471-2199-3-4
  22. Hube, F., Velasco, G., Rollin, J., Furling, D., and Francastel, C. (2011). Steroid receptor RNA activator protein binds to and counteracts SRA RNA-mediated activation of MyoD and muscle differentiation. Nucleic Acids Res. 39, 513-525. https://doi.org/10.1093/nar/gkq833
  23. Ingolia, N.T., Brar, G.A., Stern-Ginossar, N., Harris, M.S., Talhouarne, G.J., Jackson, S.E., Wills, M.R., and Weissman, J.S. (2014). Ribosome profiling reveals pervasive translation outside of annotated protein-coding genes. Cell Rep. 8, 1365-1379. https://doi.org/10.1016/j.celrep.2014.07.045
  24. Ingram, V.M. (1957). Gene mutations in human haemoglobin: the chemical difference between normal and sickle cell haemoglobin. Nature 180, 326-328. https://doi.org/10.1038/180326a0
  25. Jansen, G., Groenen, P.J., Bachner, D., Jap, P.H., Coerwinkel, M., Oerlemans, F., van den Broek, W., Gohlsch, B., Pette, D., Plomp, J.J., et al. (1996). Abnormal myotonic dystrophy protein kinase levels produce only mild myopathy in mice. Nat. Genet. 13, 316-324. https://doi.org/10.1038/ng0796-316
  26. Jenny, A., Hachet, O., Zavorszky, P., Cyrklaff, A., Weston, M.D., Johnston, D.S., Erdelyi, M., and Ephrussi, A. (2006). A translation-independent role of oskar RNA in early Drosophila oogenesis. Development 133, 2827-2833. https://doi.org/10.1242/dev.02456
  27. Ji, P., Diederichs, S., Wang, W., Boing, S., Metzger, R., Schneider, P.M., Tidow, N., Brandt, B., Buerger, H., Bulk, E., et al. (2003). MALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene 22, 8031-8041. https://doi.org/10.1038/sj.onc.1206928
  28. Ji, Z., Song, R., Regev, A., and Struhl, K. (2015). Many lncRNAs, 5'UTRs, and pseudogenes are translated and some are likely to express functional proteins. Elife 4, e08890.
  29. Johnston, W.K., Unrau, P.J., Lawrence, M.S., Glasner, M.E., and Bartel, D.P. (2001). RNA-catalyzed RNA polymerization: accurate and general RNA-templated primer extension. Science 292, 1319-1325. https://doi.org/10.1126/science.1060786
  30. Karapetyan, A.R., Buiting, C., Kuiper, R.A., and Coolen, M.W. (2013). Regulatory roles for long ncRNA and mRNA. Cancers (Basel) 5, 462-490. https://doi.org/10.3390/cancers5020462
  31. Kloc, M., Wilk, K., Vargas, D., Shirato, Y., Bilinski, S., and Etkin, L.D. (2005). Potential structural role of non-coding and coding RNAs in the organization of the cytoskeleton at the vegetal cortex of Xenopus oocytes. Development 132, 3445-3457. https://doi.org/10.1242/dev.01919
  32. Kruger, K., Grabowski, P.J., Zaug, A.J., Sands, J., Gottschling, D.E., and Cech, T.R. (1982). Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of tetrahymena. Cell 31, 147-157. https://doi.org/10.1016/0092-8674(82)90414-7
  33. Kumari, P., and Sampath, K. (2015). cncRNAs: Bi-functional RNAs with protein coding and non-coding functions. Semin. Cell Dev. Biol. 47-48, 40-51. https://doi.org/10.1016/j.semcdb.2015.10.024
  34. Lanz, R.B., McKenna, N.J., Onate, S.A., Albrecht, U., Wong, J., Tsai, S.Y., Tsai, M.J., and O'Malley, B.W. (1999). A steroid receptor coactivator, SRA, functions as an RNA and is present in an SRC-1 complex. Cell 97, 17-27. https://doi.org/10.1016/S0092-8674(00)80711-4
  35. Lauressergues, D., Couzigou, J.M., Clemente, H.S., Martinez, Y., Dunand, C., Becard, G., and Combier, J.P. (2015). Primary transcripts of microRNAs encode regulatory peptides. Nature 520, 90-93. https://doi.org/10.1038/nature14346
  36. Lee, R.C., Feinbaum, R.L., and Ambros, V. (1993). The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75, 843-854. https://doi.org/10.1016/0092-8674(93)90529-Y
  37. Lim, S., Kumari, P., Gilligan, P., Quach, H.N., Mathavan, S., and Sampath, K. (2012). Dorsal activity of maternal squint is mediated by a non-coding function of the RNA. Development 139, 2903-2915. https://doi.org/10.1242/dev.077081
  38. Lin, M.F., Jungreis, I., and Kellis, M. (2011). PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions. Bioinformatics 27, i275-282. https://doi.org/10.1093/bioinformatics/btr209
  39. Liu, C., Karam, R., Zhou, Y., Su, F., Ji, Y., Li, G., Xu, G., Lu, L., Wang, C., Song, M., et al. (2014). The UPF1 RNA surveillance gene is commonly mutated in pancreatic adenosquamous carcinoma. Nat. Med. 20, 596-598. https://doi.org/10.1038/nm.3548
  40. Mackowiak, S.D., Zauber, H., Bielow, C., Thiel, D., Kutz, K., Calviello, L., Mastrobuoni, G., Rajewsky, N., Kempa, S., Selbach, M., et al. (2015). Extensive identification and analysis of conserved small ORFs in animals. Genome Biol. 16, 179. https://doi.org/10.1186/s13059-015-0742-x
  41. Mahadevan, M., Tsilfidis, C., Sabourin, L., Shutler, G., Amemiya, C., Jansen, G., Neville, C., Narang, M., Barcelo, J., O'Hoy, K., et al. (1992). Myotonic dystrophy mutation: an unstable CTG repeat in the 3' untranslated region of the gene. Science 255, 1253-1255. https://doi.org/10.1126/science.1546325
  42. Mascarenhas, R., Pietrzak, M., Smith, R.M., Webb, A., Wang, D., Papp, A.C., Pinsonneault, J.K., Seweryn, M., Rempala, G., and Sadee, W. (2015). Allele-selective transcriptome recruitment to polysomes primed for translation: protein-coding and noncoding RNAs, and RNA isoforms. PLoS One 10, e0136798. https://doi.org/10.1371/journal.pone.0136798
  43. Mayba, O., Gilbert, H.N., Liu, J., Haverty, P.M., Jhunjhunwala, S., Jiang, Z., Watanabe, C., and Zhang, Z. (2014). MBASED: allelespecific expression detection in cancer tissues and cell lines. Genome Biol. 15, 405. https://doi.org/10.1186/s13059-014-0405-3
  44. Niazi, F., and Valadkhan, S. (2012). Computational analysis of functional long noncoding RNAs reveals lack of peptide-coding capacity and parallels with 3' UTRs. RNA 18, 825-843. https://doi.org/10.1261/rna.029520.111
  45. Okamoto, M., Higuchi-Takeuchi, M., Shimizu, M., Shinozaki, K., and Hanada, K. (2014). Substantial expression of novel small open reading frames inOryza sativa. Plant Signal. Behav. 9, e27848. https://doi.org/10.4161/psb.27848
  46. Olexiouk, V., Crappe, J., Verbruggen, S., Verhegen, K., Martens, L., and Menschaert, G. (2016). sORFs.org: a repository of small ORFs identified by ribosome profiling. Nucleic Acids Res. 44, D324-329. https://doi.org/10.1093/nar/gkv1175
  47. Reinhart, B.J., Slack, F.J., Basson, M., Pasquinelli, A.E., Bettinger, J.C., Rougvie, A.E., Horvitz, H.R., and Ruvkun, G. (2000). The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403, 901-906. https://doi.org/10.1038/35002607
  48. Rivas, M.A., Pirinen, M., Conrad, D.F., Lek, M., Tsang, E.K., Karczewski, K.J., Maller, J.B., Kukurba, K.R., DeLuca, D.S., Fromer, M., et al. (2015). Human genomics. Effect of predicted protein-truncating genetic variants on the human transcriptome. Science 348, 666-669. https://doi.org/10.1126/science.1261877
  49. Ruiz-Orera, J., Messeguer, X., Subirana, J.A., and Alba, M.M. (2014). Long non-coding RNAs as a source of new peptides. Elife 3, e03523.
  50. Sharif, J., Muto, M., Takebayashi, S., Suetake, I., Iwamatsu, A., Endo, T.A., Shinga, J., Mizutani-Koseki, Y., Toyoda, T., Okamura, K., et al. (2007). The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450, 908-912. https://doi.org/10.1038/nature06397
  51. Shevtsov, S.P., and Dundr, M. (2011). Nucleation of nuclear bodies by RNA. Nat. Cell Biol. 13, 167-173. https://doi.org/10.1038/ncb2157
  52. Sousa, C., Johansson, C., Charon, C., Manyani, H., Sautter, C., Kondorosi, A., and Crespi, M. (2001). Translational and structural requirements of the early nodulin gene enod40, a short-open reading frame-containing RNA, for elicitation of a cell-specific growth response in the alfalfa root cortex. Mol. Cell Biol. 21, 354-366. https://doi.org/10.1128/MCB.21.1.354-366.2001
  53. Verdon, J., Girardin, N., Lacombe, C., Berjeaud, J.-M., and Hechard, Y. (2009). ${\delta}$-hemolysin, an update on a membraneinteracting peptide. Peptides 30, 817-823. https://doi.org/10.1016/j.peptides.2008.12.017
  54. Wadler, C.S., and Vanderpool, C.K. (2007). A dual function for a bacterial small RNA: SgrS performs base pairing-dependent regulation and encodes a functional polypeptide. Proc. Natl. Acad. Sci. USA 104, 20454-20459. https://doi.org/10.1073/pnas.0708102104
  55. Wan, Y., Qu, K., Ouyang, Z., Kertesz, M., Li, J., Tibshirani, R., Makino, D.L., Nutter, R.C., Segal, E., and Chang, H.Y. (2012). Genome-wide measurement of RNA folding energies. Mol. Cell 48, 169-181. https://doi.org/10.1016/j.molcel.2012.08.008
  56. Wang, D., Zavadil, J., Martin, L., Parisi, F., Friedman, E., Levy, D., Harding, H., Ron, D., and Gardner, L.B. (2011). Inhibition of nonsense-mediated RNA decay by the tumor microenvironment promotes tumorigenesis. Mol. Cell Biol. 31, 3670-3680. https://doi.org/10.1128/MCB.05704-11
  57. Wightman, B., Ha, I., and Ruvkun, G. (1993). Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75, 855-862. https://doi.org/10.1016/0092-8674(93)90530-4
  58. Young, T.M., Tsai, M., Tian, B., Mathews, M.B., and Pe'ery, T. (2007). Cellular mRNA activates transcription elongation by displacing 7SK RNA. PLoS One 2, e1010. https://doi.org/10.1371/journal.pone.0001010
  59. Zhang, B., and Cech, T.R. (1997). Peptide bond formation by in vitro selected ribozymes. Nature 390, 96-100. https://doi.org/10.1038/36375
  60. Zhao, J., Ohsumi, T.K., Kung, J.T., Ogawa, Y., Grau, D.J., Sarma, K., Song, J.J., Kingston, R.E., Borowsky, M., and Lee, J.T. (2010). Genome-wide identification of polycomb-associated RNAs by RIP-seq. Mol. Cell 40, 939-953. https://doi.org/10.1016/j.molcel.2010.12.011

Cited by

  1. Global and cell-type specific properties of lincRNAs with ribosome occupancy 2017, https://doi.org/10.1093/nar/gkw909
  2. Activation of theglmSRibozyme Confers Bacterial Growth Inhibition vol.18, pp.5, 2017, https://doi.org/10.1002/cbic.201600491
  3. Biological role of long non-coding RNA in head and neck cancers vol.22, pp.5, 2017, https://doi.org/10.1016/j.rpor.2017.07.001
  4. Genome-Wide Anaplasma phagocytophilum AnkA-DNA Interactions Are Enriched in Intergenic Regions and Gene Promoters and Correlate with Infection-Induced Differential Gene Expression vol.6, 2016, https://doi.org/10.3389/fcimb.2016.00097
  5. Long Noncoding RNA DANCR Is a Positive Regulator of Proliferation and Chondrogenic Differentiation in Human Synovium-Derived Stem Cells vol.36, pp.2, 2017, https://doi.org/10.1089/dna.2016.3544
  6. Non-coding RNAs as a new dawn in tumor diagnosis 2017, https://doi.org/10.1016/j.semcdb.2017.07.035
  7. Are there any HOTTIPs for defining coding potential of lncRNAs, or just a lot of HOTAIR? vol.9, pp.8, 2017, https://doi.org/10.2217/epi-2017-0067
  8. Epigenetic aspects of rheumatoid arthritis: contribution of non-coding RNAs vol.46, pp.6, 2017, https://doi.org/10.1016/j.semarthrit.2017.01.003
  9. Peptide Nucleic Acid-Based Biosensors for Cancer Diagnosis vol.22, pp.11, 2017, https://doi.org/10.3390/molecules22111951
  10. lncRNAs, DNA Methylation, and the Pathobiology of Exfoliation Glaucoma pp.1057-0829, 2017, https://doi.org/10.1097/IJG.0000000000000711
  11. TERIUS: accurate prediction of lncRNA via high-throughput sequencing data representing RNA-binding protein association vol.19, pp.S1, 2018, https://doi.org/10.1186/s12859-018-2013-9
  12. Non-coding transcript variants of protein-coding genes – what are they good for? pp.1555-8584, 2018, https://doi.org/10.1080/15476286.2018.1511675
  13. The Role of Noncoding mRNA Isoforms in the Regulation of Gene Expression vol.54, pp.8, 2018, https://doi.org/10.1134/S1022795418080057
  14. Post-transcriptional Processing of mRNA in Neurons: The Vestiges of the RNA World Drive Transcriptome Diversity vol.11, pp.1662-5099, 2018, https://doi.org/10.3389/fnmol.2018.00304
  15. The Big Entity of New RNA World: Long Non-Coding RNAs in Microvascular Complications of Diabetes vol.9, pp.1664-2392, 2018, https://doi.org/10.3389/fendo.2018.00300
  16. Coding and Non-coding RNAs, the Frontier Has Never Been So Blurred vol.9, pp.1664-8021, 2018, https://doi.org/10.3389/fgene.2018.00140
  17. Coding or Noncoding, the Converging Concepts of RNAs vol.10, pp.None, 2019, https://doi.org/10.3389/fgene.2019.00496
  18. Weighted Gene Co-Expression Analyses Point to Long Non-Coding RNA Hub Genes at Different Schistosoma mansoni Life-Cycle Stages vol.10, pp.None, 2016, https://doi.org/10.3389/fgene.2019.00823
  19. Isolation and genome-wide characterization of cellular DNA:RNA triplex structures vol.47, pp.5, 2019, https://doi.org/10.1093/nar/gky1305
  20. Comprehensive analysis of long noncoding RNAs and mRNAs expression profiles and functional networks during chondrogenic differentiation of murine ATDC5 cells vol.51, pp.8, 2019, https://doi.org/10.1093/abbs/gmz064
  21. The small peptide world in long noncoding RNAs vol.20, pp.5, 2019, https://doi.org/10.1093/bib/bby055
  22. Non-coding RNAs in cancers with chromosomal rearrangements: the signatures, causes, functions and implications vol.11, pp.10, 2016, https://doi.org/10.1093/jmcb/mjz080
  23. Alternative role of noncoding RNAs: coding and noncoding properties vol.20, pp.11, 2016, https://doi.org/10.1631/jzus.b1900336
  24. Long Non-coding RNA in Plants in the Era of Reference Sequences vol.11, pp.None, 2016, https://doi.org/10.3389/fpls.2020.00276
  25. A small protein encoded by a putative lncRNA regulates apoptosis and tumorigenicity in human colorectal cancer cells vol.9, pp.None, 2016, https://doi.org/10.7554/elife.53734
  26. Human Long Noncoding RNA Interactome: Detection, Characterization and Function vol.21, pp.3, 2016, https://doi.org/10.3390/ijms21031027
  27. When Long Noncoding Becomes Protein Coding vol.40, pp.6, 2020, https://doi.org/10.1128/mcb.00528-19
  28. The regulatory role of miR-107 in Coxsackie B3 virus replication vol.12, pp.14, 2016, https://doi.org/10.18632/aging.103488
  29. Long Noncoding RNA AW112010 Promotes the Differentiation of Inflammatory T Cells by Suppressing IL-10 Expression through Histone Demethylation vol.205, pp.4, 2016, https://doi.org/10.4049/jimmunol.2000330
  30. The Interplay between Long Noncoding RNAs and Proteins of the Epigenetic Machinery in Ovarian Cancer vol.12, pp.9, 2016, https://doi.org/10.3390/cancers12092701
  31. A systematic evaluation of bioinformatics tools for identification of long noncoding RNAs vol.27, pp.1, 2016, https://doi.org/10.1261/rna.074724.120
  32. Comprehensive Analysis of ceRNA Regulation Network Involved in the Development of Coronary Artery Disease vol.2021, pp.None, 2021, https://doi.org/10.1155/2021/6658115
  33. A Class of Protein-Coding RNAs Binds to Polycomb Repressive Complex 2 and Alters Histone Methylation vol.11, pp.None, 2016, https://doi.org/10.3389/fonc.2021.739830
  34. Functional Peptides Encoded by Long Non-Coding RNAs in Gastrointestinal Cancer vol.11, pp.None, 2016, https://doi.org/10.3389/fonc.2021.777374
  35. Cytoplasmic cleavage of IMPA1 3′ UTR is necessary for maintaining axon integrity vol.34, pp.8, 2016, https://doi.org/10.1016/j.celrep.2021.108778
  36. Human retroviral antisense mRNAs are retained in the nuclei of infected cells for viral persistence vol.118, pp.17, 2016, https://doi.org/10.1073/pnas.2014783118
  37. Computational Analysis Predicts Hundreds of Coding lncRNAs in Zebrafish vol.10, pp.5, 2016, https://doi.org/10.3390/biology10050371
  38. hns mRNA downregulates the expression of galU and attenuates the motility of Salmonella enterica serovar Typhi vol.311, pp.6, 2016, https://doi.org/10.1016/j.ijmm.2021.151525
  39. Investigation of LINC00493/SMIM26 Gene Suggests Its Dual Functioning at mRNA and Protein Level vol.22, pp.16, 2016, https://doi.org/10.3390/ijms22168477
  40. LncRBase V.2: an updated resource for multispecies lncRNAs and ClinicLSNP hosting genetic variants in lncRNAs for cancer patients vol.18, pp.8, 2021, https://doi.org/10.1080/15476286.2020.1833529
  41. m6A-mediated upregulation of AC008 promotes osteoarthritis progression through the miR-328-3p‒AQP1/ANKH axis vol.53, pp.11, 2021, https://doi.org/10.1038/s12276-021-00696-7