Strand-specific RNA-Seq provides greater resolution of transcriptome profiling

Current Genomics

Volumn 14, Issue 3, 2013, Pages 173-181

  Mills, James Dominic ^a   Kawahara, Yoshihiro ^b   Janitz, Michael ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

Author keywords

Antisense RNA; Next generation sequencing; Non coding; Pervasive transcription; RNA; Transcriptome

Indexed keywords

AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; COMPLEMENTARY DNA; COMPLEMENTARY RNA; MESSENGER RNA; MICRORNA; PRIMER DNA; RIBOSOME RNA; RNA POLYMERASE; TRANSCRIPTOME; UNTRANSLATED RNA;

ALTERNATIVE RNA SPLICING; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA FRAGMENTATION; DNA LIBRARY; GENE EXPRESSION; HUMAN; NONHUMAN; NUCLEOSOME; PROMOTER REGION; PROTEIN MODIFICATION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; RNA HYBRIDIZATION; RNA SEQUENCE; RNA TRANSCRIPTION; RNA TRANSLATION; SEQUENCE ALIGNMENT; X CHROMOSOME INACTIVATION;

FUNGI; INVERTEBRATA; MAMMALIA; PROTOZOA;

EID: 84878637612     PISSN: 13892029     EISSN: 18755488     Source Type: Journal    
DOI: 10.2174/1389202911314030003     Document Type: Article

References (66)

1. Meinke D.W.; Cherry J.M.; Dean C.; Rounsley S.D. Koornneef M.; Arabidopsis thaliana: a model plant for genome analysis. Science 1998, 282, 662, 79-82.
2. Orgel L.E. Crick F.H.; Selfish DNA: the ultimate parasite. Nature 1980, 284, 604-607.
3. Rubin G.M.; Yandell M.D.; Wortman J.R.; Gabor Miklos G.L.; Nelson C.R.; Hariharan I.K.; Fortini M.E.; Li P.W.; Apweiler R.; Fleischmann W.; Cherry J.M.; Henikoff S.; Skupski M.P.; Misra S.; Ashburner M.; Birney E.; Boguski M.S.; Brody T.; Brokstein P.; Celniker S.E.; Chervitz S.A.; Coates D.; Cravchik A.; Gabrielian A.; Galle R.F.; Gelbart W.M.; George R.A.; Goldstein L.S.; Gong F.; Guan P.; Harris N.L.; Hay B.A.; Hoskins R.A.; Li J.; Li Z.; Hynes R.O.; Jones S.J.; Kuehl P.M.; Lemaitre B.; Littleton J.T.; Morrison D.K.; Mungall C.; O'Farrell P.H.; Pickeral O.K.; Shue C.; Vosshall L.B.; Zhang J.; Zhao Q.; Zheng X.H. Lewis S.; Comparative genomics of the eukaryotes. Science, 2000, 287, 2204-2215.
4. Venter J.C.; Adams M.D.; Myers E.W.; Li P.W.; Mural R.J.; Sutton G.G.; Smith H.O.; Yandell M.; Evans C.A.; Holt R.A.; Gocayne J.D.; Amanatides P.; Ballew R.M.; Huson D.H.; Wortman J.R.; Zhang Q.; Kodira C.D.; Zheng X.H.; Chen L.; Skupski M.; Subramanian G.; Thomas P.D.; Zhang J.; Gabor Miklos G.L.; Nelson C.; Broder S.; Clark A.G.; Nadeau J.; McKusick V.A.; Zinder N.; Levine A.J.; Roberts R.J.; Simon M.; Slayman C.; Hunkapiller M.; Bolanos R.; Delcher A.; Dew I.; Fasulo D.; Flanigan M.; Florea L.; Halpern A.; Hannenhalli S.; Kravitz S.; Levy S.; Mobarry C.; Reinert K.; Remington K.; Abu-Threideh J.; Beasley E.; Biddick K.; Bonazzi V.; Brandon R.; Cargill M.; Chandramouliswaran I.; Charlab R.; Chaturvedi K.; Deng Z.; Di Francesco V.; Dunn P.; Eilbeck K.; Evangelista C.; Gabrielian A.E.; Gan W.; Ge W.; Gong F.; Gu Z.; Guan P.; Heiman T.J.; Higgins M.E.; Ji R.R.; Ke Z.; Ketchum K.A.; Lai Z.; Lei Y.; Li Z.; Li J.; Liang Y.; Lin X.; Lu F.; Merkulov G.V.; Milshina N.; Moore H.M.; Naik A.K.; Narayan V.A.; Neelam B.; Nusskern D.; Rusch D.B.; Salzberg S.; Shao W.; Shue B.; Sun J.; Wang Z.; Wang A.; Wang X.; Wang J.; Wei M.; Wides R.; Xiao C.; Yan C.; Yao A.; Ye J.; Zhan M.; Zhang W.; Zhang H.; Zhao Q.; Zheng L.; Zhong F.; Zhong W.; Zhu S.; Zhao S.; Gilbert D.; Baumhueter S.; Spier G.; Carter C.; Cravchik A.; Woodage T.; Ali F.; An H.; Awe A.; Baldwin D.; Baden H.; Barnstead M.; Barrow I.; Beeson K.; Busam D.; Carver A.; Center A.; Cheng M.L.; Curry L.; Danaher S.; Davenport L.; Desilets R.; Dietz S.; Dodson K.; Doup L.; Ferriera S.; Garg N.; Gluecksmann A.; Hart B.; Haynes J.; Haynes C.; Heiner C.; Hladun S.; Hostin D.; Houck J.; Howland T.; Ibegwam C.; Johnson J.; Kalush F.; Kline L.; Koduru S.; Love A.; Mann F.; May D.; McCawley S.; McIntosh T.; McMullen I.; Moy M.; Moy L.; Murphy B.; Nelson K.; Pfannkoch C.; Pratts E.; Puri V.; Qureshi H.; Reardon M.; Rodriguez R.; Rogers Y.H.; Romblad D.; Ruhfel B.; Scott R.; Sitter C.; Smallwood M.; Stewart E.; Strong R.; Suh E.; Thomas R.; Tint N.N.; Tse S.; Vech C.; Wang G.; Wetter J.; Williams S.; Williams M.; Windsor S.; Winn-Deen E.; Wolfe K.; Zaveri J.; Zaveri K.; Abril J.F.; Guigo R.; Campbell M.J.; Sjolander K.V.; Karlak B.; Kejariwal A.; Mi H.; Lazareva B.; Hatton T.; Narechania A.; Diemer K.; Muruganujan A.; Guo N.; Sato S.; Bafna V.; Istrail S.; Lippert R.; Schwartz R.; Walenz B.; Yooseph S.; Allen D.; Basu A.; Baxendale J.; Blick L.; Caminha M.; Carnes-Stine J.; Caulk P.; Chiang Y.H.; Coyne M.; Dahlke C.; Mays A.; Dombroski M.; Donnelly M.; Ely D.; Esparham S.; Fosler C.; Gire H.; Glanowski S.; Glasser K.; Glodek A.; Gorokhov M.; Graham K.; Gropman B.; Harris M.; Heil J.; Henderson S.; Hoover J.; Jennings D.; Jordan C.; Jordan J.; Kasha J.; Kagan L.; Kraft C.; Levitsky A.; Lewis M.; Liu X.; Lopez J.; Ma D.; Majoros W.; McDaniel J.; Murphy S.; Newman M.; Nguyen T.; Nguyen N.; Nodell M.; Pan S.; Peck J.; Peterson M.; Rowe W.; Sanders R.; Scott J.; Simpson M.; Smith T.; Sprague A.; Stockwell T.; Turner R.; Venter E.; Wang M.; Wen M.; Wu D.; Wu M.; Xia A.; Zandieh A., Zhu X.; The sequence of the human genome. Science, 2001, 291, 1304-1351.
5. Mattick J.S.; Non-coding RNAs: the architects of eukaryotic complexity. EMBO Rep, 2001, 2, 986-991.
6. Mattick J.S.; The genetic signatures of noncoding RNAs. PLoS Genet, 2009, 5, e1000459.
7. Mattick J.S. Gagen M.J.; The evolution of controlled multitasked gene networks: the role of introns and other noncoding RNAs in the development of complex organisms. Mol. Biol. Evol, 2001, 18, 1611-1630.
8. Mattick J.S. Makunin I.V.; Non-coding RNA. Hum. Mol. Genet, 2006, 15 Spec No 1, R17-29.
9. Katayama S.; Tomaru Y.; Kasukawa T.; Waki K.; Nakanishi M.; Nakamura M.; Nishida H.; Yap C.C.; Suzuki M.; Kawai J.; Suzuki H.; Carninci P.; Hayashizaki Y.; Wells C.; Frith M.; Ravasi T.; Pang K.C.; Hallinan J.; Mattick J.; Hume D.A.; Lipovich L.; Batalov S.; Engstrom P.G.; Mizuno Y.; Faghihi M.A.; Sandelin A.; Chalk A.M.; Mottagui-Tabar S.; Liang Z.; Lenhard B. Wahlestedt C.; Antisense transcription in the mammalian transcriptome. Science, 2005, 309, 1564-1566.
10. Faghihi M.A. Wahlestedt C.; Regulatory roles of natural antisense transcripts. Nat. Rev. Mol. Cell. Biol, 2009, 10, 637-643.
11. Lopez-Barragan M.J.; Lemieux J.; Quinones M.; Williamson K.C.; Molina-Cruz A.; Cui K.; Barillas-Mury C.; Zhao K., Su X.Z.; Directional gene expression and antisense transcripts in sexual and asexual stages of Plasmodium falciparum. BMC Genomics, 2011, 12, 587.
12. Lu T.; Zhu C.; Lu G.; Guo Y.; Zhou Y.; Zhang Z.; Zhao Y.; Li W.; Lu Y.; Tang W.; Feng Q. Han B.; Strand-specific RNA-seq reveals widespread occurrence of novel cis-natural antisense transcripts in rice. BMC Genomics, 2012, 13, 721.
13. Passalacqua K.D.; Varadarajan A.; Weist C.; Ondov B.D.; Byrd B.; Read T.D. Bergman N.H.; Strand-specific RNA-seq reveals ordered patterns of sense and antisense transcription in Bacillus anthracis. PloS One, 2012, 7, e43350.
14. Costa V.; Angelini C.; De Feis I. Ciccodicola A.; Uncovering the complexity of transcriptomes with RNA-Seq. J. Biomed. Biotechnol, 2010, 2010, 853916.
15. Mills J.D. Janitz M.; Alternative splicing of mRNA in the molecular pathology of neurodegenerative diseases. Neurobiol. Aging, 2012, 33, 1012 e11-24.
16. Levin J.Z.; Yassour M.; Adiconis X.; Nusbaum C.; Thompson D.A.; Friedman N.; Gnirke A. Regev A.; Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat. Methods, 2010, 7, 709-715.
17. Core L.J.; Waterfall J.J. Lis J.T.; Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science, 2008, 322, 1845-1848.
18. Dornenburg J.E.; Devita A.M.; Palumbo M.J., Wade J.T.; Widespread antisense transcription in Escherichia coli. mBio, 2010, 1.
19. He Y.; Vogelstein B.; Velculescu V.E.; Papadopoulos N. Kinzler K.W.; The antisense transcriptomes of human cells. Science, 2008, 322, 1855-1857.
20. Lindberg J. Lundeberg J.; The plasticity of the mammalian transcriptome. Genomics, 2010, 95, 1-6.
21. Wagner E.G., Simons R.W.; Antisense RNA control in bacteria, phages, and plasmids. Annu. Rev. Microbiol, 1994, 48, 713-742.
22. Preker P.; Nielsen J.; Kammler S.; Lykke-Andersen S.; Christensen M.S.; Mapendano C.K.; Schierup M.H. Jensen T.H.; RNA exosome depletion reveals transcription upstream of active human promoters. Science, 2008, 322, 1851-1854.
23. Seila A.C.; Calabrese J.M.; Levine S.S.; Yeo G.W.; Rahl P.B.; Flynn R.A.; Young R.A. Sharp P.A.; Divergent transcription from active promoters. Science, 2008, 322, 1849-1851.
24. Lapidot M. Pilpel Y.; Genome-wide natural antisense transcription: coupling its regulation to its different regulatory mechanisms. EMBO Rep, 2006, 7, 1216-1222.
25. Osato N.; Suzuki Y.; Ikeo K. Gojobori T.; Transcriptional interferences in cis natural antisense transcripts of humans and mice. Genetics, 2007, 176, 1299-1306.
26. Prescott E.M. Proudfoot N.J.; Transcriptional collision between convergent genes in budding yeast. Proc. Natl. Acad. Sci. U. S. A, 2002, 99, 8796-8801.
27. Matlin A.J.; Clark F. Smith C.W.; Understanding alternative splicing: towards a cellular code. Nat. Rev. Mol. Cell. Biol, 2005, 6, 386-398.
28. Hastings M.L.; Milcarek C.; Martincic K.; Peterson M.L. Munroe S.H.; Expression of the thyroid hormone receptor gene, erbAalpha, in B lymphocytes: alternative mRNA processing is independent of differentiation but correlates with antisense RNA levels. Nucleic Acids Res, 1997, 25, 4296-4300.
29. Ebralidze A.K.; Guibal F.C.; Steidl U.; Zhang P.; Lee S.; Bartholdy B.; Jorda M.A.; Petkova V.; Rosenbauer F.; Huang G.; Dayaram T.; Klupp J.; O'Brien K.B.; Will B.; Hoogenkamp M.; Borden K.L.; Bonifer C. Tenen D.G.; PU.1 expression is modulated by the balance of functional sense and antisense RNAs regulated by a shared cis-regulatory element. Genes Dev, 2008, 22, 2085-2092.
30. Tanahashi H., Tabira T.; Three novel alternatively spliced isoforms of the human beta-site amyloid precursor protein cleaving enzyme (BACE) and their effect on amyloid beta-peptide production. Neurosci. Lett, 2001, 307, 9-12.
31. Faghihi M.A.; Modarresi F.; Khalil A.M.; Wood D.E.; Sahagan B.G.; Morgan T.E.; Finch C.E.; St Laurent G., 3rd; Kenny P.J., Wahlestedt C.; Expression of a noncoding RNA is elevated in Alzheimer's disease and drives rapid feed-forward regulation of beta-secretase. Nat. Med, 2008, 14, 723-730.
32. Luger K.; Mader A.W.; Richmond R.K.; Sargent D.F. Richmond T.J.; Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 1997, 389, 251-260.
33. Tremethick D.J.; Higher-order structures of chromatin: the elusive 30 nm fiber. Cell, 2007, 128, 651-654.
34. Luger K.; Dechassa M.L. Tremethick D.J.; New insights into nucleosome and chromatin structure: an ordered state or a disordered affair? Nat. Rev. Mol. Cell. Biol, 2012, 13, 436-447.
35. Filion G.J.; van Bemmel J.G.; Braunschweig U.; Talhout W.; Kind J.; Ward L.D.; Brugman W.; de Castro I.J.; Kerkhoven R.M.; Bussemaker H.J. van Steensel B.; Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell, 2010, 143, 212-224.
36. Magistri M.; Faghihi M.A.; St Laurent G., 3rd Wahlestedt C.; Regulation of chromatin structure by long noncoding RNAs: focus on natural antisense transcripts. Trends Genet., Genet, 2012, 28, 389-396.
37. Bernstein E. Allis C.D.; RNA meets chromatin. Genes Dev, 2005, 19, 1635-1655.
38. Lee J.T.; Davidow L.S., Warshawsky D.; Tsix, a gene antisense to Xist at the X-inactivation centre. Nat. Genet, 1999, 21, 400-404.
39. Brown C.J.; Hendrich B.D.; Rupert J.L.; Lafreniere R.G.; Xing Y.; Lawrence J. Willard H.F.; 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, 1992, 71, 527-542.
40. Clemson C.M.; McNeil J.A.; Willard H.F. Lawrence J.B.; XIST RNA paints the inactive X chromosome at interphase: evidence for a novel RNA involved in nuclear/chromosome structure. J. Cell. Biol, 1996, 132, 259-275.
41. Ohhata T.; Hoki Y.; Sasaki H. Sado T.; Crucial role of antisense transcription across the Xist promoter in Tsix-mediated Xist chromatin modification. Development, 2008, 135, 227-235.
42. Mercer T.R.; Dinger M.E. Mattick J.S.; Long non-coding RNAs: insights into functions. Nat. Rev. Genet, 2009, 10, 155-159.
43. Wang Z.; Gerstein M. Snyder M.; RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet, 2009, 10, 57-63.
44. Janitz M.; Next-Generation Genome Sequencing-Towards Persona lised Medicine. Wiley-VCH, Weinheim, Germany, 2008.
45. Trapnell C.; Roberts A.; Goff L.; Pertea G.; Kim D.; Kelley D.R.; Pimentel H.; Salzberg S.L.; Rinn J.L. Pachter L.; Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc, 2012, 7, 562-578.
46. Blankenberg D.; Von Kuster G.; Coraor N.; Ananda G.; Lazarus R.; Mangan M.; Nekrutenko A. Taylor J.; Galaxy: a web-based genome analysis tool for experimentalists. Current protocols in molecular biology / edited by Frederick M Ausubel, 2010, Chapter 19, Unit 19.10.1-21.
47. Giardine B.; Riemer C.; Hardison R.C.; Burhans R.; Elnitski L.; Shah P.; Zhang Y.; Blankenberg D.; Albert I.; Taylor J.; Miller W.; Kent W.J. Nekrutenko A.; Galaxy: a platform for interactive largescale genome analysis. Genome Res, 2005, 15, 1451-1455.
48. Goecks J.; Nekrutenko A. Taylor J.; Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol, 2010, 11, R86.
49. Morin R.; Bainbridge M.; Fejes A.; Hirst M.; Krzywinski M.; Pugh T.; McDonald H.; Varhol R.; Jones S. Marra M.; Profiling the HeLa S3 transcriptome using randomly primed cDNA and massively parallel short-read sequencing. Biotechniques, 2008, 45, 81-94.
50. Marioni J.C.; Mason C.E.; Mane S.M.; Stephens M. Gilad Y.; RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res, 2008, 18, 1509-1517.
51. Schadt E.E.; Linderman M.D.; Sorenson J.; Lee L., Nolan G.P.; Computational solutions to large-scale data management and analysis. Nat. Rev. Genet, 2010, 11, 647-657.
52. Chen Z. Duan X.; Ribosomal RNA depletion for massively parallel bacterial RNA-sequencing applications. Methods Mol. Biol. 2011, 733, 93-103.
53. Chatterjee A.; Johnson C.M.; Shu C.C.; Kaznessis Y.N.; Ramkrishna D.; Dunny G.M., Hu W.S.; Convergent transcription confers a bistable switch in Enterococcus faecalis conjugation. Proc. Natl. Acad. Sci. U. S. A, 2011, 108, 9721-9726.
54. Yoon O.K., Brem R.B.; Noncanonical transcript forms in yeast and their regulation during environmental stress. RNA, 2010, 16, 1256-1267.
55. Tupy J.L.; Bailey A.M.; Dailey G.; Evans-Holm M.; Siebel C.W.; Misra S.; Celniker S.E. Rubin G.M.; Identification of putative noncoding polyadenylated transcripts in Drosphila melanogaster. Proc. Natl. Acad. Sci. U. S. A, 2005, 102, 5495-5000.
56. Croucher N.J.; Fookes M.C.; Perkins T.T.; Turner D.J.; Marguerat S.B.; Keane T.; Quail M.A.; He M.; Assefa S.; Bahler J.; Kingsley R.A.; Parkhill J.; Bentley S.D.; Dougan G. Thomson N.R.; A simple method for directional transcriptome sequencing using Illumina technology. Nucleic Acids Res, 2009, 37, e148.
57. Kuhn H. Frank-Kamenetskii M.D.; Template-independent ligation of single-stranded DNA by T4 DNA ligase. FEBS J, 2005, 272, 5991-6000.
58. Mamanova L.; Andrews R.M.; James K.D.; Sheridan E.M.; Ellis P.D.; Langford C.F.; Ost T.W.; Collins J.E. Turner D.J.; FRT-seq: amplification-free, strand-specific transcriptome sequencing. Nat. Methods, 2010, 7, 130-132.
59. Mamanova L., Turner D.J.; Low-bias, strand-specific transcriptome Illumina sequencing by on-flowcell reverse transcription (FRTseq). Nat. Protoc, 2011, 6, 1736-1747.
60. Vivancos A.P.; Guell M.; Dohm J.C.; Serrano L. Himmelbauer H.; Strand-specific deep sequencing of the transcriptome. Genome Res, 2010, 20, 989-999.
61. Schaefer M.; Pollex T.; Hanna K. Lyko F.; RNA cytosine methylation analysis by bisulfite sequencing. Nucleic Acids Res, 2009, 37, e12.
62. Borodina T.; Adjaye J. Sultan M.; A strand-specific library preparation protocol for RNA sequencing. Methods Enzymol, 2011, 500, 79-98.
63. Parkhomchuk D.; Borodina T.; Amstislavskiy V.; Banaru M.; Hallen L.; Krobitsch S.; Lehrach H. Soldatov A.; Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res, 2009, 37, e123.
64. Sultan M.; Dokel S.; Amstislavskiy V.; Wuttig D.; Sultmann H.; Lehrach H., Yaspo M.L.; A simple strand-specific RNA-Seq library preparation protocol combining the Illumina TruSeq RNA and the dUTP methods. Biochem. Biophys. Res. Commun, 2012, 422, 643-646.
65. Wang L.; Si Y.; Dedow L.K.; Shao Y.; Liu P. Brutnell T.P.; A lowcost library construction protocol and data analysis pipeline for Illumina-based strand-specific multiplex RNA-seq. PloS One, 2011, 6, e26426.
66. Zhang Z.; Theurkauf W.E.; Weng Z. Zamore P.D.; Strand-specific libraries for high throughput RNA sequencing (RNA-Seq) prepared without poly(A) selection. Silence, 2012, 3, 9.