Comparison of splice sites reveals that long noncoding RNAs are evolutionarily well conserved

RNA

Volumn 21, Issue 5, 2015, Pages 801-812

  Nitsche, Anne ^a   Rose, Dominic ^b,c   Fasold, Mario ^a,d   Reiche, Kristin ^e,f   Stadler, Peter F ^a,f,g,h,i,j  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c MLL MUNICH LEUKEMIA LABORATORY   (Germany)

^d ecSeq Bioinformatics   (Germany)

^e HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^f FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

^g MAX PLANCK INSTITUTE FOR MATHEMATICS IN THE SCIENCES   (Germany)

^h UNIVERSITY OF VIENNA   (Austria)

ⁱ UNIVERSITY OF COPENHAGEN   (Denmark)

^j SANTA FE INSTITUTE   (United States)

more..

Author keywords

Conservation; Evolution; Evolutionary plasticity; IncRNA; long noncoding RNAs; Multiple sequence alignments; Splice sites

Indexed keywords

LONG UNTRANSLATED RNA; MESSENGER RNA; RNA SPLICING;

ARTICLE; EXON; HUMAN; INTRON; NONHUMAN; PLACENTAL MAMMALS; PLASTICITY; PRIORITY JOURNAL; RNA SEQUENCE; RNA SPLICING; SEQUENCE ALIGNMENT; TRANSCRIPTOMICS; ANIMAL; CHROMOSOMAL MAPPING; COMPARATIVE STUDY; CONSERVED SEQUENCE; GENETICS; MAMMAL; METABOLISM; MOLECULAR EVOLUTION; PHYLOGENY; PRIMATE; SEQUENCE ANALYSIS;

EUTHERIA; VERTEBRATA;

ANIMALS; CHROMOSOME MAPPING; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; HUMANS; MAMMALS; PHYLOGENY; PRIMATES; RNA SPLICE SITES; RNA SPLICING; RNA, LONG NONCODING; RNA, MESSENGER; SEQUENCE ANALYSIS, RNA;

EID: 84928029167     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.046342.114     Document Type: Article

References (71)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Baldo L, Santos ME, Salzburger W. 2011. Comparative transcriptomics of Eastern African cichlid fishes shows signs of positive selection and a large contribution of untranslated regions to genetic diversity. Genome Biol Evol 3: 443-455.
3. Benton MJ, Donoghue PC. 2007. Paleontological evidence to date the tree of life. Mol Biol Evol 24: 26-53.
4. Blanchette M, Kent WJ, Riemer C, Elnitski L, Smit A, Roskin KM, Baertsch R, Rosenbloom K, Clawson H, Green ED, et al. 2004. Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res 14: 708-715.
5. Bouchard M, Grote D, Craven SE, Sun Q, Steinlein P, Busslinger M. 2005. Identification of PAX2-regulated genes by expression profiling of the mid-hindbrain organizer region. Development 132: 2633-2643.
6. Bräutigam A, Kajala K, Wullenweber J, Sommer M, Gagneul D, Weber KL, Carr KM, Gowik U, Mass J, Lercher MJ, et al. 2011. An mRNA blueprint for C4 photosynthesis derived from comparative transcriptomics of closely related C3 and C4 species. Plant Physiol 155: 142-156.
7. Burd CE, Jeck WR, Liu Y, Sanoff HK, Wang Z, Sharpless NE. 2010. Expression of linear and novel circular forms of an INK4/ARF-associated non-coding RNA correlates with atherosclerosis risk. PLoS Genet 6: e1001233.
8. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL. 2011. Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25: 1915-1927.
9. Chan AS, Thorner PS, Squire JA, Zielenska M. 2002. Identification of a novel gene NCRMS on chromosome 12q21 with differential expression between rhabdomyosarcoma subtypes. Oncogene 21: 3029-3037.
10. Chodroff RA, Goodstadt L, Sirey TM, Oliver PL, Davies KE, Green ED, Molnár Z, Ponting CP. 2010. Long noncoding RNA genes: conservation of sequence and brain expression among diverse amniotes. Genome Biol 11: R72.
11. The ENCODE Project Consortium. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
12. Eng L, Coutinho G, Nahas S, Yeo G, Tanouye R, Babaei M, Dörk T, Burge C, Gatti RA. 2004. Nonclassical splicing mutations in the coding and noncoding regions of the ATM gene: maximum entropy estimates of splice junction strengths. Hum Mutat 23: 67-76.
13. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, et al. 2009. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458: 223-227.
14. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, et al. 2011. lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477: 295-300.
15. Hackermüller J, Reiche K, Otto C, Hösler N, Blumert C, Brocke-Heidrich K, Böhlig L, Nitsche A, Kasack K, Ahnert P, et al. 2014. Cell cycle, oncogenic and tumor suppressor pathways regulate numerous long and macro non-protein-coding RNAs. Genome Biol 15: R48.
16. Harrow J, Denoeud F, Frankish A, Reymond A, Chen C, Chrast J, Lagarde J, Gilbert J, Storey R, Swarbreck D, et al. 2006. GENCODE: producing a reference annotation for ENCODE. Genome Biol 7 Suppl 1: S4.1-S4.9.
17. Hasegawa M, Thorne JL, Kishino H. 2003. Time scale of eutherian evolution estimated without assuming a constant rate of molecular evolution. Genes Genet Syst 78: 267-283.
18. Hashimshony T, Yanai I. 2010. Revealing developmental networks by comparative transcriptomics. Transcription 1: 154-158.
19. He S, Gu W, Li Y, Zhu H. 2013. ANRIL/CDKN2B-AS shows two-stage clade-specific evolution and becomes conserved after transposon insertions in simians. BMC Evol Biol 13: 247.
20. Hertel J, Lindemeyer M, Missal K, Fried C, Tanzer A, Flamm C, Hofacker IL, Stadler PF, The Students of Bioinformatics Computer Labs 2004 and 2005. 2006. The expansion of the metazoan microRNA repertoire. BMC Genomics 7: 25.
21. Hiller M, Findeiss S, Lein S, Marz M, Nickel C, Rose D, Schulz C, Backofen R, Prohaska SJ, Reuter G, et al. 2009. Conserved introns reveal novel transcripts in Drosophila melanogaster. Genome Res 19: 1289-1300.
22. Holdt LM, Beutner F, Scholz M, Gielen S, Gäbel G, Bergert H, Schuler G, Thiery J, Teupser D. 2010. ANRIL expression is associated with atherosclerosis risk at chromosome 9p21. Arterioscler Thromb Vasc Biol 30: 620-627.
23. Holdt LM, Hoffmann S, Sass K, Langenberger D, Scholz M, Krohn K, Finstermeier K, Stahringer A, Wilfert W, Beutner F, et al. 2013. Alu elements in ANRIL non-coding RNA at chromosome 9p21 modulate atherogenic cell functions through trans-regulation of gene networks. PLoS Genet 9: e1003588.
24. Hong X, Scofield DG, Lynch M. 2006. Intron size, abundance, and distribution within untranslated regions of genes. Mol Biol Evol 23: 2392-2404.
25. Kapranov P, Willingham AT, Gingeras TR. 2007. Genome-wide transcription and the implications for genomic organization. Nat Rev Genetics 8: 413-423.
26. Kapranov P, St Laurent G, Raz T, Ozsolak F, Reynolds P, Sorensen PHB, Reaman G, Milos P, Arceci RJ, Thompson JF, et al. 2010. The majority of total nuclear-encoded non-ribosomal RNA in a human cell is 'dark matter' un-annotated RNA. BMC Biol 8: 149.
27. Kim VN. 2005. MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6: 376-385.
28. Kino T, Hurt DE, Ichijo T, Nader N, Chrousos GP. 2010. Noncoding RNA GAS5 is a growth arrest- and starvation-associated repressor of the glucocorticoidreceptor. Sci Signal 3: ra8.
29. Lee AP, Koh EG, Tay A, Brenner S, Venkatesh B. 2006. Highly conserved syntenic blocks at the vertebrate HOX loci and conserved regulatory elements within and outside HOX gene clusters. Proc Natl Acad Sci 103: 6994-6999.
30. Lestrade L, Weber MJ. 2006. snoRNA-LBME-db, a comprehensive database of human H/ACA and C/D box snoRNAs. Nucleic Acids Res 34: D158-D162.
31. Lin MF, Jungreis I, Kellis M. 2011. PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions. Bioinformatics 27: i275-i282.
32. Louro R, Smirnova AS, Verjovski-Almeida S. 2009. Long intronic noncoding RNA transcription: expression noise or expression choice? Genomics 93: 291-298.
33. Maeda N, Kasukawa T, Oyama R, Gough J, Frith M, Engström PG, Lenhard B, Aturaliya RN, Batalov S, Beisel KW, et al. 2006. Transcript annotation in FANTOM3: mouse gene catalog based on physical cDNAs. PLoS Genet 2: e62.
34. Mainguy G, Koster J, Woltering J, Jansen H, Durston A. 2007. Extensive polycistronism and antisense transcription in the mammalian Hox clusters. PLoS One 2: e356.
35. Makarova JA, Kramerov DA. 2009. Analysis of C/D box snoRNA genes in vertebrates: the number of copies decreases in placental mammals. Genomics 94: 11-19.
36. Managadze D, Lobkovsky AE, Wolf YI, Shabalina SA, Rogozin IB, Koonin EV. 2013. The vast, conserved mammalian lincRNome. PLoS Comput Biol 9: e1002917.
37. Marques AC, Ponting CP. 2009. Catalogues of mammalian long noncoding RNAs: modest conservation and incompleteness. Genome Biol 10: R124.
38. Marz M, Gruber AR, Höner zu Siederdissen C, Amman F, Badelt S, Bartschat S, Bernhart SH, Beyer W, Kehr S, Lorenz R, et al. 2011. Animal snoRNAs and scaRNAs with exceptional structures. RNA Biol 8: 938-946.
39. Maxwell ES, Fournier MJ. 1995. The small nucleolar RNAs. Annu Rev Biochem 64: 897-934.
40. Mercer TR, Dinger ME, Mattick JS. 2009. Long noncoding RNAs: insights into function. Nat Rev Genet 10: 155-159.
41. Mercer TR, Wilhelm D, Dinger ME, Soldà G, Korbie DJ, Glazov EA, Truong V, Schwenke M, Simons C, Matthaei KI, et al. 2011. Expression of distinct RNAs from 3′ untranslated regions. Nucleic Acids Res 39: 2393-2403.
42. Natale A, Sims C, Chiusano ML, Amoroso A, D'Aniello E, Fucci L, Krumlauf R, Branno M, Locascio A. 2011. Evolution of anterior HOX regulatory elements among chordates. BMC Evol Biol 11: 330.
43. Necsulea A, Soumillon M, Warnefors M, Liechti A, Daish T, Zeller U, Baker JC, Grützner F, Kaessmann H. 2014. The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 505: 635-640.
44. Pang KC, Frith MC, Mattick JS. 2006. Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function. Trends Genet 22: 1-5.
45. Pasmant E, Sabbagh A, Vidaud M, Bièche I. 2010. ANRIL, a long, noncoding RNA, is an unexpected major hotspot in GWAS. FASEB J 25: 444-448.
46. Paten B, Herrero J, Beal K, Fitzgerald S, Birney E. 2008. Enredo and Pecan: genome-wide mammalian consistency-based multiple alignment with paralogs. Genome Res 18: 1814-1828.
47. Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, Fan L, Sandelin A, Rinn JL, Regev A, et al. 2012. Systematic identification of long non-coding RNAs expressed during zebrafish embryogenesis. Genome Res 22: 577-591.
48. Ponjavic J, Ponting CP, Lunter G. 2007. Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res 17: 556-565.
49. Punnamoottil B, Herrmann C, Pascual-Anaya J, D'Aniello S, Garcia-Fernàndez J, Akalin A, Becker TS, Rinkwitz S. 2010. Cis-regulatory characterization of sequence conservation surrounding the HOX4 genes. Dev Biol 340: 269-282.
50. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, et al. 2007. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311-1323.
51. Rose D, Hiller M, Schutt K, Hackermüller J, Backofen R, Stadler PF. 2011. Computational discovery of human coding and noncoding transcripts with conserved splice sites. Bioinformatics 27: 1894-1900.
52. Schorderet P, Duboule D. 2011. Structural and functional differences in the long non-coding RNA hotair in mouse and human. PLoS Genet 7: e1002071.
53. Scofield DG, Hong X, Lynch M. 2007. Position of the final intron in full-length transcripts: determined by NMD? Mol Biol Evol 24: 896-899.
54. Sempere LF, Cole CN, McPeek MA, Peterson KJ. 2006. The phylogenetic distribution of metazoan microRNAs: insights into evolutionary complexity and constraint. J Exp Zool B Mol Dev Evol 306: 575-588.
55. Shao P, Yang JH, Zhou H, Guan DG, Qu LH. 2009. Genome-wide analysis of chicken snoRNAs provides unique implications for the evolution of vertebrate snoRNAs. BMC Genomics 10: 86.
56. Smith CM, Steitz JA. 1998. Classification of GAS5 as a multi-small-nucleolar-RNA (snoRNA) host gene and a member of the 5′ terminaloligopyrimidine gene family reveals common features of snoRNA host genes. Mol Cell Biol 18: 6897-6909.
57. Suzuki M, Hayashizaki Y. 2004. Mouse-centric comparative transcriptomics of protein coding and non-coding RNAs. Bioessays 26: 833-843.
58. Tanzer A, Amemiya CT, Kim CB, Stadler PF. 2005. Evolution of micro-RNAs located within Hox gene clusters. J Exp Zool B Mol Dev Evol 304: 75-85.
59. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY. 2010. Long noncoding RNA as modular scaffold of histone modification complexes. Science 329: 689-693.
60. Ulitsky I, Shkumatava A, Jan CH, Sive H, Bartel DP. 2011. Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 147: 1537-1550.
61. Wang J, Liu X, Wu H, Ni P, Gu Z, Qiao Y, Chen N, Sun F, Fan Q. 2010. CREB up-regulates long non-coding RNA, HULC expression through interaction with microRNA-372 in liver cancer. Nucleic Acids Res 38: 5366-5383.
62. Wang KC, Yang YW, Liu B, Sanyal A, Corces-Zimmerman R, Chen Y, Lajoie BR, Protacio A, Flynn RA, Gupta RA, et al. 2011. A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472: 120-124.
63. Washietl S, Hofacker IL, Stadler PF. 2005. Fast and reliable prediction of noncoding RNAs. Proc Natl Acad Sci 102: 2454-2459.
64. Washietl S, Findeiß S, Müller S, Kalkhof S, von Bergen M, Hofacker IL, Stadler PF, Goldman N. 2011. RNAcode: robust prediction of protein coding regions in comparative genomics data. RNA 17: 578-594.
65. Washietl S, Kellis M, Garber M. 2014. Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals. Genome Res 24: 616-628.
66. Weidman JR, Maloney KA, Jirtle RL. 2006. Comparative phylogenetic analysis reveals multiple non-imprinted isoforms of opossum Dlk1. Mamm Genome 17: 157-167.
67. Williams GT, Mourtada-Maarabouni M, Farzaneh F. 2011. A critical role for non-coding RNA GAS5 in growth arrest and rapamycin inhibition in human T-lymphocytes. Biochem Soc Trans 39: 482-486.
68. Yamanoue Y, Miya M, Inoue JG, Matsuura K, Nishida M. 2006. The mitochondrial genome of spotted green pufferfish Tetraodon nigroviridis (Teleostei: Tetraodontiformes) and divergence time estimation among model organisms in fishes. Genes Genet Syst 81: 29-39.
69. Yeo G, Burge CB. 2004. Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J Comput Biol 11: 377-394.
70. Zhang X, Rice K, Wang Y, Chen W, Zhong Y, Nakayama Y, Zhou Y, Klibanski A. 2010. Maternally expressed gene 3 (MEG3) noncoding ribonucleic acid: isoform structure, expression, and functions. Endocrinology 151: 939-947.
71. Zhu J, Sanborn JZ, Diekhans M, Lowe CB, Pringle TH, Haussler D. 2007. Comparative genomics search for losses of long-established genes on the human lineage. PLoS Comput Biol 3: e247.