Evolutionary conservation of long non-coding RNAs; Sequence, structure, function

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 3, 2014, Pages 1063-1071

  Johnsson, Per ^a   Lipovich, Leonard ^b   Grandér, Dan ^a   Morris, Kevin V ^c,d  

^a KAROLINSKA INSTITUTE   (Sweden)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Antisense RNA; Epigenetic; Evolution; Long non coding RNA; Polypurines; Secondary structure

Indexed keywords

COMPLEMENTARY RNA; HOX PROTEIN; LONG UNTRANSLATED RNA; MESSENGER RNA; PROTEIN NEAT2; STEROID RECEPTOR; TRANSCRIPTOME; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; COMPLEX FORMATION; GENE FUNCTION; GENE STRUCTURE; GENETIC ASSOCIATION; GENETIC CONSERVATION; HIGH THROUGHPUT SEQUENCING; HUMAN; INTERSPERSED REPEAT; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIMATE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; REGULATORY SEQUENCE; RNA ANALYSIS; RNA GENE; RNA SEQUENCE; RNA STRUCTURE; RNA TRANSCRIPTION; SEQUENCE ANALYSIS; SPECIES CONSERVATION;

MAMMALIA; PRIMATES;

ANTISENSE RNA; EPIGENETIC; EVOLUTION; LONG NON-CODING RNA; POLYPURINES; SECONDARY STRUCTURE;

ANIMALS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; HUMANS; RNA, ANTISENSE; RNA, LONG NONCODING;

EID: 84890852686     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.10.035     Document Type: Review

References (95)

1. F.S. Collins, E.S. Lander, J. Rogers, R.H. Waterston, and I.H.G.S. Conso Finishing the euchromatic sequence of the human genome Nature 431 2004 931 945 10.1038/Nature03001 (Pubitemid 39434409)
2. S. Djebali et al. Landscape of transcription in human cells Nature 489 2012 101 108 10.1038/Nature11233
3. T. Derrien et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression Genome Res. 22 2012 1775 1789 10.1101/gr.132159.111
4. K. Struhl Transcriptional noise and the fidelity of initiation by RNA polymerase II Nat. Struct. Mol. Biol. 14 2007 103 105 10.1038/Nsmb0207-103
5. M. Guttman et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals Nature 458 2009 223 227 10.1038/Nature07672
6. J. Ponjavic, C.P. Ponting, and G. Lunter Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs Genome Res. 17 2007 556 565 10.1101/Gr.6036807 (Pubitemid 46715505)
7. K.C. Pang, M.C. Frith, and J.S. Mattick Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function Trends Genet. 22 2006 1 5 10.1016/J.Tig.2005.10.003 (Pubitemid 43011990)
8. R.A. Gupta et al. Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis Nature 464 2010 1071 1076 10.1038/nature08975
9. M. Kretz et al. Control of somatic tissue differentiation by the long non-coding RNA TINCR Nature 493 2013 231 235 10.1038/Nature11661
10. P. Johnsson et al. A pseudogene long-noncoding-RNA network regulates PTEN transcription and translation in human cells Nat. Struct. Mol. Biol. 2013 10.1038/nsmb.2516
11. W. Yu et al. Epigenetic silencing of tumour suppressor gene p15 by its antisense RNA Nature 451 2008 202 206 10.1038/nature06468
12. K.V. Morris, S. Santoso, A.M. Turner, C. Pastori, and P.G. Hawkins Bidirectional transcription directs both transcriptional gene activation and suppression in human cells PLoS Genet. 4 2008 e1000258 10.1371/journal.pgen. 1000258
13. L. Lipovich et al. Activity-dependent human brain coding/noncoding gene regulatory networks Genetics 192 2012 1133-+ 10.1534/Genetics.112.145128
14. L. Poliseno et al. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology Nature 465 2010 1033 1038 10.1038/Nature09144
15. G. Bejerano et al. Ultraconserved elements in the human genome Science 304 2004 1321 1325 10.1126/Science.1098119 (Pubitemid 38697428)
16. G.A. Calin et al. Ultraconserved regions encoding ncRNAs are, altered in human leukemias and carcinomas Cancer Cell 12 2007 215 229 10.1016/J.Ccr.2007. 07.027 (Pubitemid 47333418)
17. P. Mestdagh et al. An integrative genomics screen uncovers ncRNA T-UCR functions in neuroblastoma tumours Oncogene 29 2010 3583 3592 10.1038/Onc.2010.106
18. K.S. Pollard et al. An RNA gene expressed during cortical development evolved rapidly in humans Nature 443 2006 167 172 10.1038/Nature05113 (Pubitemid 44387600)
19. K.S. Pollard et al. Forces shaping the fastest evolving regions in the human genome PLoS Genet. 2 2006 1599 1611 10.1371/journal.pgen.0020168 (doi:ARTN e168) (Pubitemid 44656534)
20. A. Beniaminov, E. Westhof, and A. Krol Distinctive structures between chimpanzee and human in a brain noncoding RNA RNA 14 2008 1270 1275 10.1261/rna.1054608 (Pubitemid 351872184)
21. P.G. Engstrom et al. Complex loci in human and mouse genomes PLoS Genet. 2 2006 564 577 10.1371/Journal.Pgen.0020047 (doi:Artn E47)
22. C. Kutter et al. Rapid turnover of long noncoding RNAs and the evolution of gene expression PLoS Genet. 8 2012 10.1371/Journal.Pgen.1002841 (doi:Artn E1002841)
23. E.J. Wood, K. Chin-Inmanu, H. Jia, and L. Lipovich Sense-antisense gene pairs: sequence, transcription, and structure are not conserved between human and mouse Front Genet 4 2013 183 10.3389/fgene.2013.00183
24. I.V. Novikova, S.P. Hennelly, and K.Y. Sanbonmatsu Structural architecture of the human long non-coding RNA, steroid receptor RNA activator Nucleic Acids Res. 40 2012 5034 5051 10.1093/Nar/Gks071
25. R.B. Lanz et al. A steroid receptor coactivator, SRA, functions as an RNA and is present in an SRC-1 complex Cell 97 1999 17 27 10.1016/S0092-8674(00) 80711-4 (Pubitemid 29165886)
26. Y.H. Shi et al. Sharp, an inducible cofactor that integrates nuclear receptor repression and activation Genes Dev. 15 2001 1140 1151 10.1101/Gad.871201 (Pubitemid 32417306)
27. E.C. Hatchell et al. SLIRP, a small SRA binding protein, is a nuclear receptor corepressor Mol. Cell 22 2006 657 668 10.1016/J.Molcel.2006.05.024 (Pubitemid 43817609)
28. S. Hussein-Fikret, and P.J. Fuller Expression of nuclear receptor coregulators in ovarian stromal and epithelial tumours Mol. Cell. Endocrinol. 229 2005 149 160 10.1016/J.Mce.2004.08.005 (Pubitemid 40018093)
29. R.B. Lanz et al. Steroid receptor RNA activator stimulates proliferation as well as apoptosis in vivo Mol. Cell. Biol. 23 2003 7163 7176 10.1128/Mcb.23.20.7163-7176.2003 (Pubitemid 37210999)
30. E. Leygue, H. Dotzlaw, P.H. Watson, and L.C. Murphy Expression of the steroid receptor RNA activator in human breast tumors Cancer Res. 59 1999 4190 4193 (Pubitemid 29418723)
31. L.C. Murphy et al. Altered expression of estrogen receptor coregulators during human breast tumorigenesis Cancer Res. 60 2000 6266 6271
32. C. Schneider, R.M. King, and L. Philipson Genes specifically expressed at growth arrest of mammalian-cells Cell 54 1988 787 793 10.1016/S0092-8674(88) 91065-3
33. C.M. Smith, and J.A. Steitz Classification of gas5 as a multi-small-nucleolar-RNA (snoRNA) host gene and a member of the 5′-terminal oligopyrimidine gene family reveals common features of snoRNA host genes Mol. Cell. Biol. 18 1998 6897 6909 (Pubitemid 28533011)
34. G. Barry et al. The long non-coding RNA Gomafu is acutely regulated in response to neuronal activation and involved in schizophrenia-associated alternative splicing Mol. Psychiatry 2013 10.1038/mp.2013.45
35. T. Kino, D.E. Hurt, T. Ichijo, N. Nader, and G.P. Chrousos Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor Sci. Signal. 3 2010 10.1126/scisignal.2000568 (doi:ARTN ra8)
36. R.A. Dimitrov, and M. Zuker Prediction of hybridization and melting for double-stranded nucleic acids Biophys. J. 87 2004 215 226 10.1529/Biophysj.103. 020743 (Pubitemid 38880079)
37. G.T. Williams, M. Mourtada-Maarabouni, and F. Farzaneh A critical role for non-coding RNA GAS5 in growth arrest and rapamycin inhibition in human T-lymphocytes Biochem. Soc. Trans. 39 2011 482 486 10.1042/Bst0390482
38. M.R. Pickard, M. Mourtada-Maarabouni, and G.T. Williams Long non-coding RNA GAS5 regulates apoptosis in prostate cancer cell lines Biochim. Biophys. Acta Mol. Basis Dis. 1832 2013 1613 1623 10.1016/J.Bbadis.2013.05.005
39. W.T. Powell et al. A Prader-Willi locus lncRNA cloud modulates diurnal genes and energy expenditure Hum. Mol. Genet. 2013 10.1093/hmg/ddt281
40. M.E. Askarian-Amiri et al. SNORD-host RNA Zfas1 is a regulator of mammary development and a potential marker for breast cancer RNA 17 2011 878 891 10.1261/rna.2528811
41. C.J. Brown et al. A gene from the region of the human X-inactivation center is expressed exclusively from the inactive X-chromosome Nature 349 1991 38 44 10.1038/349038a0 (Pubitemid 21912005)
42. G.D. Penny, G.F. Kay, S.A. Sheardown, S. Rastan, and N. Brockdorff Requirement for Xist in X chromosome inactivation Nature 379 1996 131 137 10.1038/379131a0 (Pubitemid 26020194)
43. J.C. Lucchesi, W.G. Kelly, and B. Parming Chromatin remodeling in dosage compensation Annu. Rev. Genet. 39 2005 615 651 10.1146/Annurev.Genet.39.073003. 094210 (Pubitemid 43011128)
44. L.F. Zhang, K.D. Huynh, and J.T. Lee Perinucleolar targeting of the inactive X during S phase: evidence for a role in the maintenance of silencing Cell 129 2007 693 706 10.1016/J.Cell.2007.03.036 (Pubitemid 46802377)
45. Y. Jeon, and J.T. Lee YY1 tethers Xist RNA to the inactive X nucleation center Cell 146 2011 119 133 10.1016/J.Cell.2011.06.026
46. C.J. Brown et al. The human Xist gene - analysis of a 17 kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus Cell 71 1992 527 542 10.1016/0092-8674(92)90520-M
47. N. Brockdorff X-chromosome inactivation: closing in on proteins that bind XistRNA Trends Genet. 18 2002 352 358 10.1016/S0168-9525(02)02717-8 (doi:Pii S0168-9525(02)02717-8) (Pubitemid 34804447)
48. J. Zhao, B.K. Sun, J.A. Erwin, J.J. Song, and J.T. Lee Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome Science 322 2008 750 756 10.1126/Science.1163045
49. S. Maenner et al. 2-D structure of the a region of Xist RNA and its implication for PRC2 association PLoS Biol. 8 2010 10.1371/Journal.Pbio.1000276 (doi:Artn E1000276)
50. A. Wutz, T.P. Rasmussen, and R. Jaenisch Chromosomal silencing and localization are mediated by different domains of Xist RNA Nat. Genet. 30 2002 167 174 10.1038/Ng820
51. A. Romito, and C. Rougeulle Origin and evolution of the long non-coding genes in the X-inactivation center Biochimie 93 2011 1935 1942 10.1016/j.biochi.2011.07.009
52. A.I. Shevchenko, I.S. Zakharova, and S.M. Zakian The evolutionary pathway of X chromosome inactivation in mammals Acta Nat. 5 2013 40 53
53. Y. Ogawa, B.K. Sun, and J.T. Lee Intersection of the RNA interference and X-inactivation pathways Science 320 2008 1336 1341 10.1126/science.1157676 (Pubitemid 351929469)
54. C. Kanellopoulou et al. X chromosome inactivation in the absence of Dicer Proc. Natl. Acad. Sci. U. S. A. 106 2009 1122 1127 10.1073/pnas.0812210106
55. J.L. Rinn et al. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs Cell 129 2007 1311 1323 10.1016/J.Cell.2007.05.022 (Pubitemid 46962090)
56. M.C. Tsai et al. Long noncoding RNA as modular scaffold of histone modification complexes Science 329 2010 689 693 10.1126/Science.1192002
57. Y.J. Shi et al. Histone demethylation mediated by the nuclear arnine oxidase homolog LSD1 Cell 119 2004 941 953 10.1016/J.Cell.2004.12.012 (Pubitemid 40037608)
58. W. Li et al. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation Nature 2013 10.1038/nature12210
59. P. Schorderet, and D. Duboule Structural and functional differences in the long non-coding RNA hotair in mouse and human PLoS Genet. 7 2011 10.1371/Journal.Pgen.1002071 (doi:Artn E1002071)
60. J.N. Hutchinson et al. A screen for nuclear transcripts identifies two linked noncoding RNAs associated with SC35 splicing domains BMC Genomics 8 2007 10.1186/1471-2164-8-39 (doi:Artn 39)
61. A.I. Lamond, and D.L. Spector Nuclear speckles: a model for nuclear organelles Nat. Rev. Mol. Cell Biol. 4 2003 605 612 10.1038/Nrm1172 (Pubitemid 36934962)
62. P. Ji et al. MALAT-1, a novel noncoding RNA, and thymosin beta 4 predict metastasis and survival in early-stage non-small cell lung cancer Oncogene 22 2003 8031 8041 10.1038/Sj.Onc.1206928 (Pubitemid 37175867)
63. R. Lin, S. Maeda, C. Liu, M. Karin, and T.S. Edgington A large noncoding RNA is a marker for murine hepatocellular carcinomas and a spectrum of human carcinomas Oncogene 26 2007 851 858 10.1038/Sj.Onc.1209846
64. J.E. Wilusz, S.M. Freier, and D.L. Spector 3′ end processing of a long nuclear-retained noncoding RNA yields a tRNA-like cytoplasmic RNA Cell 135 2008 919 932 10.1016/J.Cell.2008.10.012
65. J.E. Wilusz et al. A triple helix stabilizes the 3′ ends of long noncoding RNAs that lack poly(A) tails Genes Dev. 26 2012 2392 2407 10.1101/gad.204438.112
66. P.F. Stadler Evolution of the long non-coding RNAs MALAT1 and MEN beta/epsilon Adv. Bioinforma. Comput. Biol. 6268 2010 1 12
67. Y.T.F. Sasaki, T. Ideue, M. Sano, T. Mituyama, and T. Hirose MEN epsilon/beta noncoding RNAs are essential for structural integrity of nuclear paraspeckles Proc. Natl. Acad. Sci. U. S. A. 106 2009 2525 2530 10.1073/Pnas.0807899106
68. M.R. Jacobson et al. Nuclear domains of the RNA subunit of RNase P J. Cell Sci. 110 Pt 7 1997 829 837 (Pubitemid 27196782)
69. A. Vogel, O. Schilling, B. Spath, and A. Marchfelder The tRNase Z family of proteins: physiological functions, substrate specificity and structural properties Biol. Chem. 386 2005 1253 1264 10.1515/BC.2005.142 (Pubitemid 41790808)
70. H. Sunwoo et al. MEN epsilon/beta nuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles Genome Res. 19 2009 347 359 10.1101/Gr.087775.108
71. T. Gutschner, and S. Diederichs The hallmarks of cancer: a long non-coding RNA point of view RNA Biol. 9 2012 703 719 10.4161/rna.20481
72. T. Gutschner, M. Hammerle, and S. Diederichs MALAT1 - a paradigm for long noncoding RNA function in cancer J. Mol. Med. (Berl.) 91 2013 791 801 10.1007/s00109-013-1028-y
73. C. Xu, M. Yang, J. Tian, X. Wang, and Z. Li MALAT-1: a long non-coding RNA and its important 3′ end functional motif in colorectal cancer metastasis Int. J. Oncol. 39 2011 169 175 10.3892/ijo.2011.1007
74. C. Chu, K. Qu, F.L. Zhong, S.E. Artandi, and H.Y. Chang Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions Mol. Cell 44 2011 667 678 10.1016/J.Molcel.2011.08.027
75. A. Ackley et al. An algorithm for generating small RNAs capable of epigenetically modulating transcriptional gene silencing and activation in human cells Mol. Ther. Nucleic Acids 2 2013 e104 10.1038/mtna.2013.33
76. S. Dugre-Brisson et al. Interaction of Staufen1 with the 5′ end of mRNA facilitates translation of these RNAs Nucleic Acids Res. 33 2005 4797 4812 10.1093/Nar/Gki794 (Pubitemid 41418880)
77. C.G. Gong, and L.E. Maquat lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3′ UTRs via Alu elements Nature 470 2011 284-+ 10.1038/Nature09701
78. M.A. Kiebler et al. The mammalian Staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons: implications for its involvement in mRNA transport J. Neurosci. 19 1999 288 297 (Pubitemid 29028969)
79. J.J. Chen et al. Over 20% of human transcripts might form sense-antisense pairs Nucleic Acids Res. 32 2004 4812 4820 10.1093/Nar/Gkh818 (Pubitemid 39429685)
80. S. Katayama et al. Antisense transcription in the mammalian transcriptome Science 309 2005 1564 1566 10.1126/Science.1112009 (Pubitemid 41266482)
81. O.V. Grinchuk, P. Jenjaroenpun, Y.L. Orlov, J. Zhou, and V.A. Kuznetsov Integrative analysis of the human cis-antisense gene pairs, miRNAs and their transcription regulation patterns Nucleic Acids Res. 38 2010 534 547 10.1093/nar/gkp954
82. K.V. Morris The emerging role of RNA in the regulation of gene transcription in human cells Semin. Cell Dev. Biol. 2011 10.1016/j.semcdb.2011. 02.017 (doi:S1084-9521(11)00030-9 [pii])
83. M.A. Faghihi et al. Evidence for natural antisense transcript-mediated inhibition of microRNA function Genome Biol. 11 2010 10.1186/Gb-2010-11-5-R56 (doi:Artn R56)
84. J.T. Kung, D. Colognori, and J.T. Lee Long noncoding RNAs: past, present, and future Genetics 193 2013 651 669 10.1534/genetics.112.146704
85. K. Ohshima et al. Whole-genome screening indicates a possible burst of formation of processed pseudogenes and Alu repeats by particular L1 subfamilies in ancestral primates Genome Biol. 4 2003 10.1186/Gb-2003-4-11-R74 (doi:Artn R74)
86. Z.L. Zhang, N. Carriero, and M. Gerstein Comparative analysis of processed pseudogenes in the mouse and human genomes Trends Genet. 20 2004 62 67 10.1016/J.Tig.2003.12.005 (Pubitemid 38121355)
87. P.G. Hawkins, and K.V. Morris Transcriptional regulation of Oct4 by a long non-coding RNA antisense to Oct4-pseudogene 5 Transcription 1 2010 165 175 10.4161/trns.1.3.13332
88. B.K. Pei et al. The GENCODE pseudogene resource Genome Biol. 13 2012 10.1186/Gb-2012-13-9-R51 (doi:Artn R51)
89. S.K. Tay, J. Blythe, and L. Lipovich Global discovery of primate-specific genes in the human genome Proc. Natl. Acad. Sci. U. S. A. 106 2009 12019 12024 10.1073/pnas.0904569106
90. F. Modarresi et al. Inhibition of natural antisense transcripts in vivo results in gene-specific transcriptional upregulation Nat. Biotechnol. 2012 10.1038/nbt.2158 (doi:nbt.2158 [pii])
91. K.V. Morris Long antisense non-coding RNAs function to direct epigenetic complexes that regulate transcription in human cells Epigenetics 4 2009 (doi:9282 [pii])
92. M. Guttman, and J.L. Rinn Modular regulatory principles of large non-coding RNAs Nature 482 2012 339 346 10.1038/Nature10887
93. Y. Wan et al. Genome-wide measurement of RNA folding energies Mol. Cell 48 2012 169 181 10.1016/J.Molcel.2012.08.008
94. J.G. Underwood et al. FragSeq: transcriptome-wide RNA structure probing using high-throughput sequencing Nat. Methods 7 2010 995 1001 10.1038/nmeth.1529
95. I.V. Novikova, A. Dharap, S.P. Hennelly, and K.Y. Sanbonmatsu 3S: shotgun secondary structure determination of long non-coding RNAs Methods 2013 10.1016/j.ymeth.2013.07.030