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Long non-coding RNA: its evolutionary relics and biological implications in mammals: a review

  • Dhanoa, Jasdeep Kaur (School of Animal Biotechnology, Guru Angad Dev Veterinary and Animal Sciences University) ;
  • Sethi, Ram Saran (School of Animal Biotechnology, Guru Angad Dev Veterinary and Animal Sciences University) ;
  • Verma, Ramneek (School of Animal Biotechnology, Guru Angad Dev Veterinary and Animal Sciences University) ;
  • Arora, Jaspreet Singh (School of Animal Biotechnology, Guru Angad Dev Veterinary and Animal Sciences University) ;
  • Mukhopadhyay, Chandra Sekhar (School of Animal Biotechnology, Guru Angad Dev Veterinary and Animal Sciences University)
  • Received : 2018.08.23
  • Accepted : 2018.10.05
  • Published : 2018.10.31

Abstract

The central dogma of gene expression propounds that DNA is transcribed to mRNA and finally gets translated into protein. Only 2-3% of the genomic DNA is transcribed to protein-coding mRNA. Interestingly, only a further minuscule part of genomic DNA encodes for long non-coding RNAs (lncRNAs) which are characteristically more than 200 nucleotides long and can be transcribed from both protein-coding (e.g. H19 and TUG1) as well as non-coding DNA by RNA polymerase II. The lncRNAs do not have open reading frames (with some exceptions), 3`-untranslated regions (3'-UTRs) and necessarily these RNAs lack any translation-termination regions, however, these can be spliced, capped and polyadenylated as mRNA molecules. The flexibility of lncRNAs confers them specific 3D-conformations that eventually enable the lncRNAs to interact with proteins, DNA or other RNA molecules via base pairing or by forming networks. The lncRNAs play a major role in gene regulation, cell differentiation, cancer cell invasion and metastasis and chromatin remodeling. Deregulation of lncRNA is also responsible for numerous diseases in mammals. Various studies have revealed their significance as biomarkers for prognosis and diagnosis of cancer. The aim of this review is to overview the salient features, evolution, biogenesis and biological importance of these molecules in the mammalian system.

Keywords

References

  1. Anguera MC, Ma W, Clift D, Namekawa S, Kelleher RJ, Lee JT. Tsxproduces a long noncoding RNA and has general functions in the germline, stem cells,and brain. PLoS Genet. 2011;7:e1002248. https://doi.org/10.1371/journal.pgen.1002248.
  2. Ayers D. Long noncoding RNAs: novel emergent biomarkers for Cancer diagnostics. J Cancer Res Treat. 2013;1(2):31-5.
  3. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007;447:799-816. https://doi.org/10.1038/nature05874
  4. Bolha L, Ravnik-Glavac M, Glavac D. Long noncoding RNAs as biomarkers in Cancer. Dis Markers. 2017;2017:7243968. https://doi.org/10.1155/2017/7243968.
  5. Cao J. The functional role of long non-coding RNAs and epigenetics. Biol Proced Online. 2014;16:11.
  6. Carrieri C, Cimatti L, Biagioli M, Beugnet A, Zucchelli S, Fedele S, Pesce E, Ferrer I, Collavin L, Santoro C, et al. Long noncoding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature. 2012;491:454-7. https://doi.org/10.1038/nature11508
  7. Castellanos-Rubio A, Fernandez-Jimenez N, Kratchmarov R, Luo X, Bhagat G, Green PH, Schneider R, Kiledjian M, Bilbao JR, Ghosh S. A long noncoding RNA associatedwith susceptibility to celiac disease. Science. 2016;352:91-5. https://doi.org/10.1126/science.aad0467
  8. Chen B, Yu M, Chang Q, et al. Mdig de-represses H19 large intergenic noncoding RNA (lincRNA) by down-regulating H3K9me3 and heterochromatin. Oncotarget. 2013a;4:1427-37.
  9. Chen G, Wang Z, Wang D, Qiu C, Liu M, Chen X, et al. The lncRNA disease: a database for long-noncoding RNA-associated diseases. Nucleic Acids Res. 2013b;41:D983-6.
  10. Chen J, Shishkin AA, Zhu X, Kadri S, Maza I, Guttman M, Hanna JH, et al. Evolutionary analysis across mammals reveals distinct classes of long noncoding RNAs. Genome Biol. 2016;17:19. https://doi.org/10.1186/s13059-016-0880-9.
  11. Chen W, Bocker W, Brosius J, Tiedge H. Expression of neural BC200 RNA in human tumours. J Pathol. 1997;183(3):345-51. https://doi.org/10.1002/(SICI)1096-9896(199711)183:3<345::AID-PATH930>3.0.CO;2-8
  12. Chen Z, Jia S, Li D, Cai J, Tu J, Geng B, Guan Y, Cui Q, Yang J. Silencing of long noncoding RNA AK139328 attenuates ischemia/reperfusion injury in mouse livers. PLoS One. 2013;8(11):e80817. https://doi.org/10.1371/journal.pone.0080817
  13. Dai Y, Liang Z, Li Y, Li C, Chen L. Circulating long noncoding RNAs as potential biomarkers of Sepsis: a preliminary study. Genet Test Mol Biomarkers. 2017. https://doi.org/10.1089/gtmb.2017.0061.
  14. Dempsey JL, Cui JY. Long noncoding RNAs: a novel paradigm for toxicology. Toxicol Sci. 2017;155(1):1-21. https://doi.org/10.1093/toxsci/kfw232
  15. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H et al. The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution and expression. Genome Research. 2012;22:1775-89. https://doi.org/10.1101/gr.132159.111
  16. Dinger ME, Amaral PP, Mercer TR, Pang KC, Bruce SJ, et al. Long noncoding RNAs in mouse embryonic stem cell pluripotency and differentiation. Genome Res. 2008;18:1433-45. https://doi.org/10.1101/gr.078378.108
  17. Dinger ME, Gascoigne DK, Mattick JS. The evolution of RNAs with multiple functions. Biochimie. 2011;93:2013-2018. https://doi.org/10.1016/j.biochi.2011.07.018
  18. Dinger ME, Pang KC, Mercer TR, Crowe ML, Grimmond SM, Mattick JS. NRED: a database of long noncoding RNA expression. Nucleic Acids Res. 2009;37:D122-6. https://doi.org/10.1093/nar/gkn617
  19. Fang Y, Fullwood MJ. Roles, functions, and mechanisms of long noncoding RNAs in Cancer. Genomics Proteomics Bioinformatics. 2016;14:42-54. https://doi.org/10.1016/j.gpb.2015.09.006
  20. Forterre P. Origin of DNA and DNA genomes. Curr Opin Microbiol. 2002;5:525-32. https://doi.org/10.1016/S1369-5274(02)00360-0
  21. Friedlander MR, Lizano E, Houben AJS, Bezdan D, Banez-Coronel M, Kudla G, Mateu-Huertas E, Kagerbauer B, Gonzalez J, et al. Evidence for the biogenesis of more than 1,000 novel human microRNAs. Genome Biol. 2014;15:R57. https://doi.org/10.1186/gb-2014-15-4-r57
  22. Fu LL, Li CJ, Xu Y, Li LY, Zhou X, Li DD, Chen SX, et al. Role of lncRNAs as novel biomarkers and therapeutic targets in ovarian Cancer. Crit Rev Eukaryot Gene Expr. 2017;27(2):183-95. https://doi.org/10.1615/CritRevEukaryotGeneExpr.2017019244.
  23. Ganesan G, Rao SM. A novel noncoding RNA processed by Drosha is restricted to the nucleus in the mouse. RNA. 2008;14:1399-410. https://doi.org/10.1261/rna.838308.
  24. Gardini A, Shiekhattar R. The many faces of long noncoding RNAs. FEBS J. 2015;282(9):1647-57. https://doi.org/10.1111/febs.13101.
  25. Gomes AQ, Nolasco S, Soares H. Noncoding RNAs: multi-tasking molecules in the cell. Int J Mol Sci. 2013;14:16010-39. https://doi.org/10.3390/ijms140816010.
  26. Gonzalez I, Munita R, Agirre E, Dittmer TA, Gysling K, Misteli T, Luco RF. A lncRNA regulates alternative splicing via the establishment of a splicingspecific chromatin signature. Nat Struct Mol Biol. 2015;22:370-6. https://doi.org/10.1038/nsmb.3005
  27. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, et al. Long noncoding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature. 2010;464:1071-6. https://doi.org/10.1038/nature08975
  28. Gutschner T, Diederichs S. The hallmarks of cancer: a long noncoding RNA point of view. RNA Biol. 2012;9:703-19. https://doi.org/10.4161/rna.20481
  29. Gutschner T, Hammerle M, Eissmann M, Hsu J, Kim Y, Hung G, et al. The noncoding RNA MALAT1 is a critical regulator of the metastasis phenotype of lung cancer cells. Cancer Res. 2013;73(3):1180-9. https://doi.org/10.1158/0008-5472.CAN-12-2850
  30. Guttman M, Russell P, Ingolia NT, Weissman JX, Lander ES. Ribosome profiling provides evidence that large noncoding RNAs do not encode proteins. Cell. 2013;154:240-251. https://doi.org/10.1016/j.cell.2013.06.009
  31. Haerty W, Ponting CP. Mutations within lncRNAs are effectively selected against in fruitfly but not in human. Genome Biol. 2013;14:R49. https://doi.org/10.1186/gb-2013-14-5-r49
  32. Hajjari M, Behmanesh M, Sadeghizadeh M, Zeinoddini M. Up-regulation of HOTAIR long noncoding RNA in human gastric adenocarcinoma tissues. Med Oncol Northwood Lond Engl. 2013;30(3):670. https://doi.org/10.1007/s12032-013-0670-0
  33. Han P, Chang C-P. Long noncoding RNA and chromatin remodeling. RNA Biol. 2015;12(10):1094-8. https://doi.org/10.1080/15476286.2015.1063770
  34. Hangauer MJ, Vaughn IW, McManus MT. Pervasive transcription of the human genome produces thousands of previously unidentified long intergenic noncoding RNAs. PLoS Genet. 2013;9:e1003569. https://doi.org/10.1371/journal.pgen.1003569
  35. Hawkins PG, Morris KV. Transcriptional regulation of Oct4 by a long noncoding RNA antisense to Oct4-pseudogene 5. Transcr. 2010;1(3):165-75. https://doi.org/10.4161/trns.1.3.13332
  36. Hezroni H, Koppstein D, Schwart MG, Avrutin A, Bartel DP, Ulitsky I. Principles of long noncoding RNA evolution derived from a direct comparison of transcriptomes in 17 species. Cell Rep. 2015;11(7):1110-22. https://doi.org/10.1016/j.celrep.2015.04.023.
  37. Hu K, Zhang J, The LM. lncRNA AK015322 promotes proliferation of spermatogonial stem cell C18-4 by acting as a decoy for microRNA-19b-3p. In Vitro Cell Dev Biol Anim. 2017;53(3):277-84. https://doi.org/10.1007/s11626-016-0102-5.
  38. Hung T, Wang Y, Lin MF, Koegel AK, KotakeY GGD, Horlings HM, et al. Extensive and coordinated transcription of noncoding sRNAs within cellcycle promoters. Nat Genet. 2011;43(7):621-9. https://doi.org/10.1038/ng.848
  39. Ishibashi M, Kogo R, Shibata K, Sawada G, Takahashi Y, Kurashige J, Akiyoshi S, et al. Clinical significance of the expression of long noncoding RNA HOTAIR in primary hepatocellular carcinoma. Oncol Rep. 2013;29:946-50. https://doi.org/10.3892/or.2012.2219
  40. Iyer MK, Niknafs YS, Malik R, Singhal U, Sahu A, Hosono Y, Barrette TR, et al. The landscape of long noncoding RNAs in the human transcriptome. Nat Genet. 2015;47:199-208. https://doi.org/10.1038/ng.3192
  41. Jalali S, Jayaraj GG, Scaria V. Integrative transcriptome analysis suggests processing of a subset of long noncoding RNAs to small RNAs. Biol Direct. 2012;7:25. https://doi.org/10.1186/1745-6150-7-25
  42. Jelinic P, Shaw P. Loss of imprinting and cancer. J Pathol. 2007;211:261-8. https://doi.org/10.1002/path.2116
  43. Juan V, Crain C, Wilson C. Evidence for evolutionarily conserved secondary structure in the H19 tumor suppressor RNA. Nucleic Acids Res. 2000;28: 1221-7. https://doi.org/10.1093/nar/28.5.1221
  44. Kanduri C. Long noncoding RNAs: lessons from genomic imprinting. Biochim Biophys Acta (BBA) Gene Regulatory Mechanisms. 2016;1859(1): 102-11. https://doi.org/10.1016/j.bbagrm.2015.05.006
  45. Keniry A, Oxley D, Monnier P, Kyba M, Dandolo L, Smits G, Reik W. The H19 lincRNA is a developmental reservoir of miR-675 that suppresses growth and Igf1r. Nat Cell Biol. 2012;14(7):659-65. https://doi.org/10.1038/ncb2521
  46. Kim JH, Lee BB, Oh YM, Zhu C, Steinmetz LM, Lee Y, Kim WK, Lee SB, Buratowski S, Kim T. Modulation of mRNA and lncRNA expression dynamics by the Set2-Rpd3S pathway. Nat Commun. 2016;7:13534. https://doi.org/10.1038/ncomms13534.
  47. Kiss T. Biogenesis of small nuclear RNPs. J Cell Sci. 2004;117:5949-51. https://doi.org/10.1242/jcs.01487
  48. Kogo R, Shimamura T, Mimori K, Kawahara K, Imoto S, Sudo T, et al. Long noncoding RNA HOTAIR regulates polycomb-dependent chromatin modification and is associated with poor prognosis in colorectal cancers. Cancer Res. 2011;71(20):6320-6. https://doi.org/10.1158/0008-5472.CAN-11-1021
  49. Kono T, Sotomaru Y, Katsuzawa Y, Dandolo L. Mouse parthenogenetic embryos with monoallelic H19 expression can develop to day 17.5 of gestation. Dev Biol. 2002;243:294-300. https://doi.org/10.1006/dbio.2001.0561
  50. Kung JTY, Colognori D, Lee JT. Long noncoding RNAs: past, present, and future. Genetics. 2013;193:651-69. https://doi.org/10.1534/genetics.112.146704
  51. Lapidot M, Pilpel Y. Genome-wide natural antisense transcription: coupling its regulation to its different regulatory mechanisms. EMBO Rep. 2006;7:1216-22. https://doi.org/10.1038/sj.embor.7400857
  52. Johnsson P, Lipovich L, Grander D, Morris KV. Evolutionary conservation of long noncoding RNAs; sequence, structure, function. Biochim Biophys Acta. 2014;1840:1063-71. https://doi.org/10.1016/j.bbagen.2013.10.035.
  53. Quinn JJ, Zhang QC, Georgiev P, Ilik IA, Akhtar A, Chang HY. Rapid evolutionary turnover underlies conserved lncRNA-genome interactions. Genes Dev. 2016;30(2):191-207. https://doi.org/10.1101/gad.272187.115.
  54. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, Cabili MN, Jaenisch R, Mikkelsen TS, Jacks T, Hacohen N, Bernstein BE, Kellis M, Regev A, Rinn JL, Lander ES. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature. 2009;458(7235):223-7. https://doi.org/10.1038/nature07672.
  55. Ponjavic J, Ponting CP, Lunter G. Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res. 2007;17:556-65. https://doi.org/10.1101/gr.6036807
  56. Pang KC, Frith MC, Mattick JS. Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function. Trends Genet. 2006;22:1-5. https://doi.org/10.1016/j.tig.2005.10.003
  57. Leighton PA, Ingram RS, Eggenschwiler J, Efstratiadis A, Tilghman SM. Disruption of imprinting caused by deletion of the H19 gene region in mice. Nature. 1995;375(6526):34-9. https://doi.org/10.1038/375034a0
  58. Li L, Wang M, Wang M, Wu X, Geng L, Xue Y, Wei X, Jia Y, Wu X. A long noncoding RNA interacts with Gfra1 and maintains the survival of mouse spermatogonial stem cells. Cell Death Dis. 2016a;7:e2140. https://doi.org/10.1038/cddis.2016.24
  59. Li R, Zhu H, Luo Y. Understanding the functions of long noncoding RNAs through their higher-order structures. Int J Mol Sci. 2016b;17:702. https://doi.org/10.3390/ijms17050702.
  60. Losko M, Kotlinowski J, Jura J. Long Noncoding RNAs in Metabolic Syndrome Related Disorders. Mediators of Inflammation. 2016;2016:1-12. https://doi.org/10.1155/2016/5365209.
  61. Louro R, Smirnova AS, Verjovski-Almeida S. Long intronic noncoding RNA transcription: expression noise or expression choice? Genomics. 2008; 93(2009):291-8.
  62. Luk AC-S, Chan W-Y, Rennert OM, Lee T-L. Long noncoding RNAs in spermatogenesis: insights from recent high-throughput transcriptome studies. Reproduction. 2014;147:R131-41. https://doi.org/10.1530/REP-13-0594
  63. Ma H, Hao Y, Dong X, Gong Q, Chen J, Zhang J, Tian W. Molecular mechanisms and function prediction of long noncoding RNA. Sci World J. 2012;2012:1-11. https://doi.org/10.1100/2012/541786.
  64. Mariner PD, Walters RD, Espinoza CA, Drullinger LF, Wagner SD, Kugel JF, Goodrich JA. HumanAlu RNA is a modular transacting repressor of mRNA transcription during heat shock. Mol Cell. 2008;29:499-509. https://doi.org/10.1016/j.molcel.2007.12.013
  65. Mayama T, Marr AK, Kino T. Differential expression of glucocorticoid receptor noncoding RNA repressorGas5 in autoimmune and inflammatory diseases. HormMetab Res. 2016;48:550-7.
  66. Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS. Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci U S A. 2008;105:716-21. https://doi.org/10.1073/pnas.0706729105
  67. Mohammad F, Mondal T, Guseva N, Pandey GK, Kanduri C. Kcnq1ot1 noncoding RNA mediates transcriptional gene silencing by interacting with Dnmt1. Development (Cambridge, England). 2010;137(15):2493-9. https://doi.org/10.1242/dev.048181.
  68. Monnier P, Martineta C, Pontisc J, Stanchevad I, Ait-Si-Alic S, Dandoloa L. H19 lncRNA controls gene expression of the imprinted gene network by recruiting MBD1. PNAS. 2013;110(51):20693-8. https://doi.org/10.1073/pnas.1310201110
  69. Mukhopadhyay CS, Singh J. MicroRNAs: Basics, Implications,and Modulation in Improving Disease Resistance. DBT Sponsored Short Term Training Course on Molecular Tools and Bioinformatics Approaches for Livestock Genome Analysis, delivered on 13th September' 2014 at Central Institute for Research on Cattle, Grass Farm Road, Meerut, UP, organized during 10th to 30th September' 2014;67-73.
  70. Ni MJ, Hu ZH, Liu Q, Liu MF, Lu MH, Zhang JS, Zhang L, Zhang YL. Identification and characterization of a novel noncoding RNA involved in sperm maturation. PLoS One. 2011;6:e26053. https://doi.org/10.1371/journal.pone.0026053.
  71. Niu D-K, Jiang L. Can ENCODE tell us how much junk DNA we carry in our genome? Biochem Biophys Res Commun. 2013;430:1340-3. https://doi.org/10.1016/j.bbrc.2012.12.074
  72. Novikova IV, Hennelly SP, Sanbonmatsu KY. Structural architecture of the human long noncoding RNA, steroid receptor RNA activator. Nucleic Acids Res. 2012;40:5034-51. https://doi.org/10.1093/nar/gks071
  73. Ohno S. So much “junk” DNA in our genome. Brookhaven Symp Biol. 1972; 23:366-70.
  74. Olsen GJ, Woese CR. Archaeal genomics: an overview. Cell. 1997;89:991-4. https://doi.org/10.1016/S0092-8674(00)80284-6
  75. Orgel LE, Crick FH. Selfish DNA: the ultimate parasite. Nature. 1980; 284(5757):604-7. https://doi.org/10.1038/284604a0.
  76. Ottolenghi C, Veitia R, Barbieri M, Fellous M, McElreavey K. The human doublesex-related gene, DMRT2, is homologous to a gene involved in somitogenesis and encodes a potential bicistronic transcript. Genomics. 2000;64:179-86. https://doi.org/10.1006/geno.2000.6120.
  77. Palazzo AF, Lee ES. Non-coding RNA: what is functional and what is junk? Front Genet. 2015;6:2. https://doi.org/10.3389/fgene.2015.00002.
  78. Paraskevopoulou MD, Hatzigeorgiou AG. Analyzing miRNA-the lncRNA interactions- Long Non-Coding RNAs. Methods Mol Biol. 2016;1402:271-86. https://doi.org/10.1007/978-1-4939-3378-5_21.
  79. Patil VS, Zhou R, Rana TM. Gene regulation by noncoding RNAs. Crit Rev Biochem Mol Biol. 2014;49(1):16-32. https://doi.org/10.3109/10409238.2013.844092.
  80. Peschansky VJ, Wahlestedt C. Noncoding RNAs as direct and indirect modulators of epigenetic regulation. Epigenetics. 2014;9:3-12 doi.org/10.4161/epi.27473.
  81. Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell. 2009;136:629-41. https://doi.org/10.1016/j.cell.2009.02.006
  82. Prensner JR, Chinnaiyan AM. The emergence of lncRNAs in cancer biology. Cancer Discovery. 2011;1(5):391-407. https://doi.org/10.1158/2159-8290.CD-11-0209
  83. Prensner JR, Iyer MK, Balbin OA, Dhanasekaran SM, Cao Q, et al. Transcriptome sequencing across a prostate cancer cohort identifies PCAT-1, an unannotated lincRNA implicated in disease progression. Nat Biotechnol. 2011;29:742-9. https://doi.org/10.1038/nbt.1914
  84. Quek XC, Thomson DW, Maag JL, Bartonicek N, Signal B, Clark MB, et al. lncRNAdb v2.0: expanding the reference database for functional longnoncoding RNAs. Nucleic Acids Res. 2015;43:D168-73. https://doi.org/10.1093/nar/gku988
  85. Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem. 2012;81:145-66. https://doi.org/10.1146/annurev-biochem-051410-092902.
  86. Roberts TC, Morris KV, Wood MJA. The role of long non-coding RNAs in neurodevelopment, brain function and neurological disease. Phil Trans R Soc B. 2014;369:20130507 https://doi.org/10.1098/rstb.2013.0507.
  87. Romero-Barrios N, Legascue MF, Benhamed M, Ariel F, Crespi M. Splicing regulation by long noncoding RNAs. Nucleic Acids Res. 2018;46(5):2169-84 https://doi.org/10.1093/nar/gky095.
  88. Satpathy AT, Chang HY. Long noncoding RNA in hematopoiesis and immunity. Immunity. 2015;42:792-804 https://doi.org/10.1016/j.immuni.2015.05.004.
  89. Schmitt AM, Chang HY. Long noncoding RNAs in Cancer pathways. Cancer Cell. 2016;29(4):452-63. https://doi.org/10.1016/j.ccell.2016.03.010
  90. Schutt C, Nothiger R. Structure, function and evolution of sex-determining systems in dipteran insects. Development (Cambridge, England). 2000; 127(4):667-77.
  91. Shamovsky I, Ivannikov M, Kandel ES, Gershon D, Nudler E. RNA-mediated response to heat shock in mammalian cells. Nature. 2006;440:556-60. https://doi.org/10.1038/nature04518
  92. Shi X, Sun M, Liu H, Yao Y, Kong R, Chen F, Song Y. A critical role for the long noncoding RNA GAS5 in proliferation and apoptosis in nonsmallcell lung cancer. MolCarcinog. 2015;54(1):E1-E12. https://doi.org/10.1002/mc.22120.
  93. Singh J, Mukhopadhyay CS, Dhanoa JK, Arora JS, Kaur S. miRNA repertoire of bubaline PBMC obtained from disease tolerant vis-a-vis susceptible buffaloes. Poster presentation (Poster No. AH-14) and abstract publication (Abstract No. ASC2015ABS1418031523) in XII Agricultural Science Congress and Silver Jubilee of National Academy of Agricultural Science, India, organized during 3-6th February 2015, at National Dairy Research Institute, Karnal; pp. 180.
  94. Sun J, Ding C, Yang Z, Liu T, Zhang X, Zhao C, Wang J. The long noncoding RNA TUG1 indicates a poor prognosis for colorectal cancer and promotes metastasis by affecting epithelial-mesenchymal transition. J Transl Med. 2016;14:42. https://doi.org/10.1186/s12967-016-0786-z.
  95. Sun M, Kraus WL. From discovery to function: the expanding roles of long NonCoding RNAs in physiology and disease. Endocr Rev. 2015;36(1):25-64. https://doi.org/10.1210/er.2014-1034.
  96. Sun M, Liu XH, Wang KM, et al. Down-regulation of BRAF activated noncoding RNA is associated with poor prognosis for non-small cell lung cancer and promotes metastasis by affecting epithelial-mesenchymal transition. Mol Cancer. 2014;13:68. https://doi.org/10.1186/1476-4598-13-68
  97. Sun Y, Zou X, He J, Mao Y. Identification of long noncoding RNAs biomarkers associated with progression of endometrial carcinoma and patient outcomes. Oncotarget. 2017;8(32):52604-13.
  98. Tano K, Mizuno R, Okada T, Rakwal R, Shibato J, et al. MALAT-1 enhances cell motility of lung adenocarcinoma cells by influencing the expression of motility-related genes. FEBS Lett. 2010;584:4575-80. https://doi.org/10.1016/j.febslet.2010.10.008
  99. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY. Long noncoding RNA as modular scaffold of histone modification complexes. Science. 2010;329:689-93. https://doi.org/10.1126/science.1192002
  100. Wan LB, Bartolomei MS. Regulation of imprinting in clusters: noncoding RNAs vs insulators. Adv Genet. 2008;61:207-23.
  101. Wang J, Du S, Wang J, Fan W, Wang P, Zhang Z, Xu P, Tang S, Deng Q, Yang W, Yu M. The prognostic value of abnormally expressed lncRNAs in colorectal cancer: a meta-analysis. PLoSOne. 2017a;12(6):e0179670. https://doi.org/10.1371/journal.pone.0179670.
  102. Wang J, Ye C, Xiong H, Shen Y, Lu Y, Zhou J, Wang L. Dysregulation of long noncoding RNA in breast cancer: an overview of mechanism and clinical implication. Oncotarget. 2017b;8(3):5508-22.
  103. Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. MolCell. 2011;43(6):904-14. https://doi.org/10.1016/j.molcel.2011.08.018.
  104. Wang P, Ren Z, Sun P. Overexpression of the long noncoding RNA MEG3 impairs in vitro glioma cell proliferation. J Cell Biochem. 2012;113(6):1868-74. https://doi.org/10.1002/jcb.24055
  105. Wang W, Zhuang Q, Ji K, Wen B, Lin P, Zhao Y, Li L, Yan C. Identification of miRNA, lncRNA and mRNA-associated ceRNA networks and a potential biomarker for MELAS with mitochondrial DNA A3243G mutation. Sci Rep. 2017c;7:41639. https://doi.org/10.1038/srep41639.
  106. Wang X, Arai S, Song X, Reichart D, Du K, Pascual G, Tempst P, Rosenfeld MG, Glass CK, Kurokawa R. Induced ncRNAsallosterically modify RNA-binding proteins in cis to inhibit transcription. Nature. 2008;454:126-30. https://doi.org/10.1038/nature06992
  107. White NM, Cabanski CR, Silva-Fisher JM, Dang HX, Govindan R, Maher CA. Transcriptome sequencing reveals altered long intergenic noncoding RNAs in lung cancer. Genome Biol. 2014;15:429. https://doi.org/10.1186/s13059-014-0429-8
  108. Wight M, Werner A. The functions of natural antisense transcripts. Essays Biochem. 2015;54:91-101.
  109. Wilusz JE, Sunwoo H, Spector DL. Long noncoding RNAs: functional surprises from the RNA world. Genes Dev. 2009;23:1494-504. https://doi.org/10.1101/gad.1800909
  110. Wucherpfennig KW, Strominger JL. Molecular mimicry in T cell-mediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein. Cell. 1995;80(5):695-705. https://doi.org/10.1016/0092-8674(95)90348-8
  111. Yang C, Chapman AG, Kelsey AD, Minks J, Cotton AM, Brown CJ. Xchromosome inactivation: molecular mechanisms from the human perspective. Hum Genet. 2011;130:175-85. https://doi.org/10.1007/s00439-011-0994-9
  112. Yang JH, Li JH, Jiang S, Zhou H, Qu LH. ChIPBase: a database for decoding the transcriptional regulation of long noncoding RNA and microRNA genes from ChIP-Seq data. Nucleic Acids Res. 2013;41:D177-87. https://doi.org/10.1093/nar/gks1060
  113. Yap KL, Li S, Munoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ, Zhou MM. Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell. 2010;38(5):662-74. https://doi.org/10.1016/j.molcel.2010.03.021
  114. Zhang C, Gao L, Xu EYT. lncRNA, a new component of expanding RNAprotein regulatory network important for animal sperm development. Semin Cell Dev Biol. 2016;59:110-7. https://doi.org/10.1016/j.semcdb.2016.06.013
  115. Zhang Q, Geng PL, Yin P, Wang XL, Jia JP, Yao J. Down-regulation of long noncoding RNA TUG1 inhibits osteosarcoma cell proliferation and promotes apoptosis. Asian Pac J Cancer Prev. 2013;1:2311-5.

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