Promoter analysis reveals globally differential regulation of human long non-coding RNA and protein-coding genes

PLoS ONE

Volumn 9, Issue 10, 2014, Pages

  Alam, Tanvir ^a   Medvedeva, Yulia A ^a,d,e   Jia, Hui ^b   Brown, James B ^c   Lipovich, Leonard ^b   Bajic, Vladimir B ^a  

^a KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

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

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^d Institute of Predictive and Personalized Medicine of Cancer   (Spain)

^e VAVILOV INSTITUTE OF GENERAL GENETICS   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

LONG UNTRANSLATED RNA; MESSENGER RNA; CHROMATIN; PROTEIN; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ARTICLE; BINDING SITE; CHROMATIN; DECISION TREE; DNA SEQUENCE; FEEDBACK SYSTEM; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; LONG NONCODING RNA GENE; PROMOTER REGION; PROTEIN CODING GENE; TRANSCRIPTION FACTOR BINDING SITE; TRANSCRIPTION REGULATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HUMAN GENOME; METABOLISM;

BINDING SITES; CHROMATIN; GENE EXPRESSION REGULATION; GENOME, HUMAN; HUMANS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEINS; RNA, LONG NONCODING; RNA, MESSENGER; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84907536973     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0109443     Document Type: Article

References (80)

1. Lee JT, Davidow LS, Warshawsky D. (1999) Tsix, a gene antisense to Xist at the X-inactivation centre. Nat. Genet. 21: 400-404.
2. Lanz RB, McKenna NJ, Onate S.A., Albrecht U., Wong J, et al. (1999) A steroid receptor coactivator, SRA, functions as an RNA and is present in an SRC-1 complex. Cell 97: 17-27.
3. Lander ES, Linton LM, Birren B, Nusbaum C., Zody MC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860-921.
4. Derrien T, Johnson R, Bussotti G., Tanzer A, Djebali S, et al (2012) The GENCODE v7 catalog of human long noncoding RNAs: Analysis of their gene structure, evolution, and expression. Genome Res. 22: 1775-1789.
5. Jia H, Osak M, Bogu G.K., Stanton LW, Johnson R, et al. (2010) Genome-wide computational identification and manual annotation of human long noncoding RNA genes. RNA 16: 1478-1487.
6. Dunham I, Kundaje A, Aldred S.F., Collins PJ, Davis CA, et al. (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489: 57-74.
7. Lipovich L, Johnson R, Lin C.Y. (2010) MacroRNA underdogs in a microRNA world: evolutionary, regulatory, and biomedical significance of mammalian long non-protein-coding RNA. Biochim. Biophys. Acta 1799: 597-615.
8. Carrieri C, Cimatti L, Biagioli M., Beugnet A, Zucchelli S, et al (2012) Long non-coding antisense RNA controls Uchl1 translation through an embedded SINEB2 repeat. Nature 491: 454-457.
9. Gong C, Maquat L.E. (2011) lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3' UTRs via Alu elements. Nature 470: 284-288.
10. Morey L, Helin K. (2010) Polycomb group protein-mediated repression of transcription. Trends Biochem. Sci. 35: 323-332.
11. Bond AM, VanGompel MJW, Sametsky EA, Clark M.F., Savage JC, et al. (2009) Balanced gene regulation by an embryonic brain ncRNA is critical for adult hippocampal GABA circuitry. Nat. Neurosci. 12: 1020-1027.
12. Kino T, Hurt DE, Ichijo T, Nader N., Chrousos G.P. (2010) Noncoding RNA gas5 is a growth arrest-and starvation-associated repressor of the glucocorticoid receptor. Sci. Signal. 3: ra8.
13. Yang L, Lin C, Jin C., Yang JC, Tanasa B, et al. (2013) lncRNA-dependent mechanisms of androgen-receptor-regulated gene activation programs. Nature 500: 598-602.
14. Sheik Mohamed J., Gaughwin PM, Lim B, Robson P., Lipovich L. (2010) Conserved long noncoding RNAs transcriptionally regulated by Oct4 and Nanog modulate pluripotency in mouse embryonic stem cells. RNA 16: 324-337.
15. Loh YH, Wu Q, Chew J.L., Vega VB, Zhang W, et al. (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet. 38: 431-440.
16. Johnson R, Teh CH-L, Jia H, Vanisri R.R., Pandey T., et al. (2009) Regulation of neural macroRNAs by the transcriptional repressor REST. RNA 15: 85-96.
17. Lipovich L, Dachet F, Cai J., Bagla S, Balan K, et al (2012) Activity-dependent human brain coding/non-coding gene regulatory networks. Genetics 192: 1133-1148.
18. Kong L, Zhang Y, Ye Z.Q., Liu XQ, Zhao SQ, et al. (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res. 35: W345-349.
19. Arrial RT, Togawa RC, Brigido MdeM (2009) Screening non-coding RNAs in transcriptomes from neglected species using PORTRAIT: case study of the pathogenic fungus Paracoccidioides brasiliensis. BMC Bioinformatics 10: 239.
20. Liu J, Gough J, Rost B. (2006) Distinguishing protein-coding from non-coding RNAs through support vector machines. PLoS Genet. 2: e29.
21. Sun K, Chen X, Jiang P., Song X, Wang H, et al (2013) iSeeRNA: identification of long intergenic non-coding RNA transcripts from transcriptome sequencing data. BMC Genomics 14 Suppl 2: S7.
22. Guttman M, Russell P, Ingolia N.T., Weissman JS, Lander E.S. (2013) Ribosome profiling provides evidence that large noncoding RNAs do not encode proteins. Cell 154: 240-251.
23. Banfai B, Jia H, Khatun J., Wood E, Risk B, et al (2012) Long noncoding RNAs are rarely translated in two human cell lines. Genome Res. 22: 1646-1657.
24. Lv J, Liu H, Huang Z., Su J, He H, et al (2013) Long non-coding RNA identification over mouse brain development by integrative modeling of chromatin and genomic features. Nucleic Acids Res. 41: 10044-10061.
25. Santoni FA (2013) EMdeCODE: a novel algorithm capable of reading words of epigenetic code to predict enhancers and retroviral integration sites and to identify H3R2me1 as a distinctive mark of coding versus non-coding genes. Nucleic Acids Res. 41: e48.
26. Saxonov S, Berg P, Brutlag D.L. (2006) A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc. Natl. Acad. Sci. U. S. A. 103: 1412-1417.
27. Lu L, Jia H, Droge P., Li J. (2007) The human genome-wide distribution of DNA palindromes. Funct. Integr. Genomics 7: 221-227.
28. Illingworth RS, Bird A.P. (2009) CpG islands - 'A rough guide'. FEBS Lett. 583: 1713-1720.
29. Medvedeva YA, Fridman MV, Oparina N.J., Malko DB, Ermakova EO, et al. (2010) Intergenic, gene terminal, and intragenic CpG islands in the human genome. BMC Genomics 11: 48.
30. Illingworth RS, Gruenewald-Schneider U, Webb S., Kerr AR, James KD, et al. (2010) Orphan CpG islands identify numerous conserved promoters in the mammalian genome. PLoS Genet. 6: e1001134.
31. Medvedeva YA (2011) Algorithms for CpG Islands Search: New Advantages and Old Problems. In: Mahdavi MA, editor. Bioinformatics - Trends and Methodologies: In Tech. pp. 449-472.
32. Lipovich L, King M.C. (2006) Abundant novel transcriptional units and unconventional gene pairs on human chromosome 22. Genome Res. 16: 45-54.
33. Kulakovskiy IV, Medvedeva YA, Schaefer U, Kasianov A.S., Vorontsov IE, et al. (2012) HOCOMOCO: a comprehensive collection of human transcription factor binding sites models. Nucleic Acids Res. 41: D195-202.
34. Janowski BA, Younger ST, Hardy D.B., Ram R., Huffman KE, et al. (2007) Activating gene expression in mammalian cells with promoter-targeted duplex RNAs. Nat. Chem. Biol. 3: 166-173.
35. Chu Y, Yue X, Younger S.T., Janowski BA, Corey D.R. (2010) Involvement of argonaute proteins in gene silencing and activation by RNAs complementary to a non-coding transcript at the progesterone receptor promoter. Nucleic Acids Res. 38: 7736-7748.
36. Liu JL, Liang XH, Su R.W., Lei W., Jia B, et al. (2012) Combined analysis of microRNome and 3'-UTRome reveals a species-specific regulation of progesterone receptor expression in the endometrium of rhesus monkey. J. Biol. Chem. 287: 13899-13910.
37. Tochitani S, Hayashizaki Y. (2008) Nkx2.2 antisense RNA overexpression enhanced oligodendrocytic differentiation. Biochem. Biophys. Res. Commun. 372: 691-696.
38. Gupta RA, Shah N, Wang K.C., Kim J., Horlings HM, et al. (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464: 1071-1076.
39. Zhao H, Zhang X, Frazao J.B., Condino-Neto A, Newburger P.E. (2013) HOX antisense lincRNA HOXA-AS2 is an apoptosis repressor in all trans retinoic acid treated NB4 promyelocytic leukemia cells. J. Cell. Biochem. 114: 2375-2383.
40. Katayama S, Tomaru Y, Kasukawa T., Waki K, Nakanishi M, et al (2005) Antisense transcription in the mammalian transcriptome. Science 309: 1564-1566.
41. Di Ruscio A., Ebralidze AK, Benoukraf T, Amabile G., Goff LA, et al. (2013) DNMT1-interacting RNAs block gene-specific DNA methylation. Nature 503: 371-376.
42. Necsulea A, Soumillon M, Warnefors M., Liechti A, Daish T, et al (2014) The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 505: 635-640.
43. Vaquerizas JM, Kummerfeld SK, Teichmann S.A., Luscombe N.M. (2009) A census of human transcription factors: function, expression and evolution. Nat. Rev. Genet. 10: 252-263.
44. Marchand B, Bajic V, Kaushik D. (2011) Highly scalable ab initio genomic motif identification. Proceedings of 2011 International Conference for High Performance Computing, Networking, Storage and Analysis: 1-10.
45. Wei GH, Badis G, Berger M.F., Kivioja T., Palin K, et al. (2010) Genome-wide analysis of ETS-family DNA-binding in vitro and in vivo. EMBO J. 29: 2147-2160.
46. Kamanu FK, Medvedeva YA, Schaefer U, Jankovic B.R., Archer JA, et al. (2012) Mutations and binding sites of human transcription factors. Front Genet 3: 100.
47. Boyle AP, Hong EL, Hariharan M, Cheng Y., Schaub MA, et al. (2012) Annotation of functional variation in personal genomes using RegulomeDB. Genome Res. 22: 1790-1797.
48. Ernst J, Kheradpour P, Mikkelsen T.S., Shoresh N., Ward LD, et al. (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473: 43-49.
49. Ørom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, et al. (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell 143: 46-58.
50. Bernstein BE, Mikkelsen TS, Xie X, Kamal M., Huebert DJ, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
51. Voigt P, Tee WW, Reinberg D. (2013) A double take on bivalent promoters. Genes Dev. 27: 1318-1338.
52. Khare SP, Habib F, Sharma R., Gadewal N, Gupta S, et al (2012) HIstome-a relational knowledgebase of human histone proteins and histone modifying enzymes. Nucleic Acids Res. 40: D337-342.
53. Vakoc CR, Mandat SA, Olenchock B.A., Blobel G.A. (2005) Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Mol. Cell 19: 381-391.
54. Rybtsova N, Leimgruber E, Seguin-Estevez Q, Dunand-Sauthier I, Krawczyk M, et al (2007) Transcription-coupled deposition of histone modifications during MHC class II gene activation. Nucleic Acids Res. 35: 3431-3441.
55. Lachner M, O'Sullivan RJ, Jenuwein T. (2003) An epigenetic road map for histone lysine methylation. J. Cell Sci. 116: 2117-2124.
56. Vezzoli A, Bonadies N, Allen M.D., Freund SM, Santiveri CM, et al. (2010) Molecular basis of histone H3K36me3 recognition by the PWWP domain of Brpf1. Nat. Struct. Mol. Biol. 17: 617-619.
57. Wang Z, Zang C, Rosenfeld J.A., Schones DE, Barski A, et al. (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 40: 897-903.
58. Vavouri T, Lehner B. (2012) Human genes with CpG island promoters have a distinct transcription-associated chromatin organization. Genome Biol. 13: R110.
59. Dong X, Greven MC, Kundaje A, Djebali S., Brown JB, et al. (2012) Modeling gene expression using chromatin features in various cellular contexts. Genome Biol. 13: R53.
60. Lercher MJ, Urrutia AO, Pavlicek A, Hurst L.D. (2003) A unification of mosaic structures in the human genome. Hum. Mol. Genet. 12: 2411-2415.
61. Thurman RE, Rynes E, Humbert R., Vierstra J, Maurano MT, et al (2012) The accessible chromatin landscape of the human genome. Nature 489: 75-82.
62. Wang J, Zhuang J, Iyer S., Lin X, Whitfield TW, et al (2012) Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res. 22: 1798-1812.
63. Engstrom PG, Suzuki H, Ninomiya N., Akalin A, Sessa L, et al (2006) Complex Loci in human and mouse genomes. PLoS Genet. 2: e47.
64. Zhang H, Nestor CE, Zhao S, Lentini A., Bohle B, et al. (2013) Profiling of human CD4(+) T-cell subsets identifies the TH2-specific noncoding RNA GATA3-AS1. J. Allergy Clin. Immunol. 132: 1005-1008.
65. Hu G, Tang Q, Sharma S., Yu F, Escobar TM, et al (2013) Expression and regulation of intergenic long noncoding RNAs during T cell development and differentiation. Nat. Immunol. 14: 1190-1198.
66. Maurano MT, Humbert R, Rynes E., Thurman RE, Haugen E, et al. (2012) Systematic localization of common disease-associated variation in regulatory DNA. Science 337: 1190-1195.
67. Cabili MN, Trapnell C, Goff L., Koziol M, Tazon-Vega B, et al. (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 25: 1915-1927.
68. Ernst J, Kheradpour P, Mikkelsen T.S., Shoresh N., Ward LD, et al. (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473: 43-49.
69. Huynh KD, Lee J.T. (2005) X-chromosome inactivation: a hypothesis linking ontogeny and phylogeny. Nat. Rev. Genet. 6: 410-418.
70. Harrow J, Frankish A, Gonzalez J.M., Tapanari E., Diekhans M, et al. (2012) GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res. 22: 1760-1774.
71. Benson DA, Boguski MS, Lipman D.J., Ostell J. (1997) GenBank. Nucleic Acids Res. 25: 1-6.
72. Grinchuk OV, Jenjaroenpun P, Orlov Y.L., Zhou J., Kuznetsov V.A. (2010) Integrative analysis of the human cis-antisense gene pairs, miRNAs and their transcription regulation patterns. Nucleic Acids Res. 38: 534-547.
73. Wood EJ, Chin-Inmanu K, Jia H., Lipovich L. (2013) Sense-antisense gene pairs: sequence, transcription, and structure are not conserved between human and mouse. Front Genet 4: 183.
74. Carninci P, Sandelin A, Lenhard B., Katayama S, Shimokawa K, et al (2006) Genome-wide analysis of mammalian promoter architecture and evolution. Nat. Genet. 38: 626-635.
75. Pardo LM, Rizzu P, Francescatto M., Vitezic M, Leday GG, et al (2013) Regional differences in gene expression and promoter usage in aged human brains. Neurobiol. Aging 34: 1825-1836.
76. Maston GA, Evans SK, Green M.R. (2006) Transcriptional regulatory elements in the human genome. Annu. Rev. Genomics Hum. Genet. 7: 29-59.
77. Breiman L, Friedman JH, Olshen R.A., Stone C.J. (1984) Classification and Regression Trees: Chapman and Hall.
78. Benjamini Y, Hochberg Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol: 289-300.
79. Mortazavi A, Williams BA, McCue K, Schaeffer L., Wold B. (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5: 621-628.
80. Montgomery SB, Sammeth M, Gutierrez-Arcelus M, Lach R.P., Ingle C., et al. (2010) Transcriptome genetics using second generation sequencing in a Caucasian population. Nature 464: 773-777.