Where does transcription start? 5′-RACE adapted to next-generation sequencing

Nucleic Acids Research

Volumn 44, Issue 6, 2015, Pages 2628-2645

  Leenen, Fleur A D ^a,b   Vernocchi, Sara ^a,b   Hunewald, Oliver E ^a   Schmitz, Stephanie ^a   Molitor, Anne M ^a   Muller, Claude P ^a,b   Turner, Jonathan D ^a  

^a LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

^b UNIVERSITY OF TRIER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AZACITIDINE; DEXAMETHASONE; GAMMA INTERFERON; MESSENGER RNA; 5' UNTRANSLATED REGION; ADRB2 PROTEIN, HUMAN; BETA 2 ADRENERGIC RECEPTOR; CAPPED RNA; GLUCOCORTICOID RECEPTOR; ISOPROTEIN; NR3C1 PROTEIN, HUMAN; OLIGONUCLEOTIDE;

5' UNTRANSLATED REGION; ADRB2R GENE; AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; GENE; GENE AMPLIFICATION; GENE EXPRESSION; GENE FREQUENCY; GENE LOCUS; GR GENE; HUMAN; HUMAN CELL; IN VITRO STUDY; NEXT GENERATION SEQUENCING; NR3C1 GENE; PRIORITY JOURNAL; RAPID AMPLIFICATION OF CDNA END; RNA TRANSLATION; TRANSCRIPTION INITIATION SITE; CHEMISTRY; DRUG EFFECTS; EXON; GENETIC VARIATION; GENETICS; HIGH THROUGHPUT SEQUENCING; INTRON; METABOLISM; NUCLEIC ACID AMPLIFICATION; PROCEDURES; PROMOTER REGION; STAINING; TRANSCRIPTION INITIATION; TUMOR CELL LINE;

5' UNTRANSLATED REGIONS; AZACITIDINE; CELL LINE, TUMOR; DEXAMETHASONE; EXONS; GENETIC LOCI; GENETIC VARIATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INTERFERON-GAMMA; INTRONS; NUCLEIC ACID AMPLIFICATION TECHNIQUES; OLIGONUCLEOTIDES; PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS; RECEPTORS, ADRENERGIC, BETA-2; RECEPTORS, GLUCOCORTICOID; RNA CAPS; STAINING AND LABELING; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION INITIATION, GENETIC;

EID: 84963894303     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1328     Document Type: Article

References (73)

1. Carninci, P., Sandelin, A., Lenhard, B., Katayama, S., Shimokawa, K., Ponjavic, J., Semple, C.A.M., Taylor, M.S., Engstr öm, P.G., Frith, M.C., et al. (2006) Genome-wide analysis of mammalian promoter architecture and evolution. Nat. Genet., 38, 626-635.
2. Ayoubi, T.A.Y. and Van De Ven, W.J.M. (1996) Regulation of gene expression by alternative promoters. FASEB J., 10, 453-460.
3. Hughes, T.A. (2006) Regulation of gene expression by alternative untranslated regions. Trends Genet., 22, 119-122.
4. Pal, S., Gupta, R., Kim, H., Wickramasinghe, P., Baubet, V., Showe, L.C., Dahmane, N. and Davuluri, R. V (2011) Alternative transcription exceeds alternative splicing in generating the transcriptome diversity of cerebellar development. Genome Res., 21, 1260-1272.
5. Shabalina, S.a., Spiridonov, A.N., Spiridonov, N.a. and Koonin, E.V. (2010) Connections between alternative transcription and alternative splicing in mammals. Genome Biol. Evol., 2, 791-799.
6. Zhang, T., Haws, P. and Wu, Q. (2004) Multiple Variable First Exons: A Mechanism for Cell- and Tissue-Specific Gene Regulation. Genome Res., 14, 79-89.
7. Brosius, J. and Gould, S.J. (1992) On 'genomenclature': a comprehensive (and respectful) taxonomy for pseudogenes and other 'junk DNA'. Proc. Natl. Acad. Sci. U.S.A., 89, 10706-10710.
8. Brosius, J. (1999) RNAs from all categories generate retrosequences that may be exapted as novel genes or regulatory elements. Gene, 238, 115-134.
9. Brosius, J. (1999) Many G-protein-coupled receptors are encoded by retrogenes. Trends Genet., 15, 304-305.
10. Merkin, J.J., Chen, P., Alexis, M.S., Hautaniemi, S.K. and Burge, C.B. (2015) Origins and impacts of new mammalian exons. Cell Rep., 10, 1992-2005.
11. Turner, J.D., Vernocchi, S., Schmitz, S. and Muller, C.P. (2014) Role of the 5′-untranslated regions in post-transcriptional regulation of the human Glucocorticoid Receptor. Biochim. Biophys. Acta - Gene Regul. Mech., 1839, 1051-1061.
12. Shabalina, S.a., Ogurtsov, A.Y., Spiridonov, N.a. and Koonin, E.V. (2014) Evolution at protein ends: major contribution of alternative transcription initiation and termination to the transcriptome and proteome diversity in mammals. Nucleic Acids Res., 42, 7132-7144.
13. Schor, I.E., Gómez Acuña, L.I. and Kornblihtt, A.R. (2008) Coupling between transcription and alternative splicing. Bull. Cancer, 95, 33-41.
14. Kornblihtt, A.R., Schor, I.E., All ó, M., Dujardin, G., Petrillo, E. and Muñoz, M.J. (2013) Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nat. Rev. Mol. Cell Biol., 14, 153-65.
15. Irimia, M., Rukov, J.L., Penny, D. and Roy, S.W. (2007) Functional and evolutionary analysis of alternatively spliced genes is consistent with an early eukaryotic origin of alternative splicing. BMC Evol. Biol., 7, 188.
16. Pankratova, E.V. (2008) Alternative promoters in expression of genetic information. Mol. Biol., 42, 371-380.
17. Resch, A.M., Ogurtsov, A.Y., Rogozin, I.B., Shabalina, S.A. and Koonin, E. V (2009) Evolution of alternative and constitutive regions of mammalian 5′ UTRs. BMC Genomics, 10, 162.
18. Siggens, L. and Ekwall, K. (2014) Epigenetics, chromatin and genome organization: recent advances from the ENCODE project. J. Intern. Med., 276, 201-214.
19. Su, A.I., Wiltshire, T., Batalov, S., Lapp, H., Ching, K.A., Block, D., Zhang, J., Soden, R., Hayakawa, M., Kreiman, G., et al. (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. U.S.A., 101, 6062-6067.
20. Breslin, M.B., Geng, C.D. and Vedeckis, W. V (2001) Multiple promoters exist in the human GR gene, one of which is activated by glucocorticoids. Mol. Endocrinol., 15, 1381-1395.
21. Turner, J.D. and Muller, C.P. (2005) Structure of the glucocorticoid receptor (NR3C1) gene 5′ untranslated region: identification, and tissue distribution of multiple new human exon 1. J. Mol. Endocrinol., 35, 283-292.
22. Turner, J.D., Schote, A.B., Macedo, J.A., Pelascini, L.P.L. and Muller, C.P. (2006) Tissue specific glucocorticoid receptor expression, a role for alternative first exon usage? Biochem. Pharmacol., 72, 1529-1537.
23. Presul, E., Schmidt, S., Kofler, R. and Helmberg, A. (2007) Identification, tissue expression, and glucocorticoid responsiveness of alternative first exons of the human glucocorticoid receptor. J. Mol. Endocrinol., 38, 79-90.
24. Turner, J.D., Alt, S.R., Cao, L., Vernocchi, S., Trifonova, S., Battello, N. and Muller, C.P. (2010) Transcriptional control of the glucocorticoid receptor: CpG islands, epigenetics and more. Biochem. Pharmacol., 80, 1860-1868.
25. Cao-Lei, L., Leija, S.C., Kumsta, R., Wüst, S., Meyer, J., Turner, J.D. and Muller, C.P. (2011) Transcriptional control of the human glucocorticoid receptor: identification and analysis of alternative promoter regions. Hum. Genet., 129, 533-543.
26. Cao-Lei, L., Suwansirikul, S., Jutavijittum, P., Mériaux, S.B., Turner, J.D. and Muller, C.P. (2013) Glucocorticoid receptor gene expression and promoter CpG modifications throughout the human brain. J. Psychiatr. Res., 47, 1597-1607.
27. Witzmann, S.R., Turner, J.D., Mériaux, S.B., Meijer, O.C. and Muller, C.P. (2012) Epigenetic regulation of the glucocorticoid receptor promoter 1(7) in adult rats. Epigenetics, 7, 1290-1301.
28. Theisen, L.L. and Muller, C.P. (2012) EPsR7630 (UmckaloaboR) , an extract from Pelargonium sidoides roots, exerts anti-influenza virus activity in vitro and in vivo. Antiviral Res., 94, 147-156.
29. Vernocchi, S., Battello, N., Schmitz, S., Revets, D., Billing, A.M., Turner, J.D. and Muller, C.P. (2013) Membrane glucocorticoid receptor activation induces proteomic changes aligning with classical glucocorticoid effects. Mol. Cell. proteomics, 12, 1764-1779.
30. Maruyama, K. and Sugano, S. (1994) Oligo-capping: a simple method to replace the cap structure of eukaryotic mRNAs with oligoribonucleotides. Gene, 138, 171-174.
31. Volloch, V., Schweitzer, B. and Rits, S. (1994) Ligation-mediated amplification of RNA from murine erythroid cells reveals a novel class of globin mRNA with an extended 5′-untranslated region. Nucleic Acids Res., 22, 2507-2511.
32. Schaefer, B.C. (1995) Revolutions in rapid amplification of cDNA ends: new strategies for polymerase chain reaction cloning of full-length cDNA ends. Anal. Biochem., 227, 255-273.
33. Trapnell, C., Pachter, L. and Salzberg, S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
34. Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D.R., Pimentel, H., Salzberg, S.L., Rinn, J.L. and Pachter, L. (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc., 7, 562-578.
35. Tarzona, S., Garcia-Alcade, F., Dopazo, J., Ferrer, A. and Conesa, A. (2011) Differential expression in RNA-seq: A matter of depth. Genome Biol., 21, 2213-2223.
36. Ritchie, M.E., Phipson, B., Wu, D., Hu, Y., Law, C.W., Shi, W. and Smyth, G.K. (2015) limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res., 43, 1-26.
37. Siepel, A., Bejerano, G., Pedersen, J.S., Hinrichs, A.S., Hou, M., Rosenbloom, K., Clawson, H., Spieth, J., Hillier, L.W., Richards, S., et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res., 15, 1034-1050.
38. Turner, J.D., Pelascini, L.P.L., Macedo, J.a and Muller, C.P. (2008) Highly individual methylation patterns of alternative glucocorticoid receptor promoters suggest individualized epigenetic regulatory mechanisms. Nucleic Acids Res., 36, 7207-7218.
39. Gruber, A.R., Lorenz, R., Bernhart, S.H., Neuböck, R. and Hofacker, I.L. (2008) The Vienna RNA websuite. Nucleic Acids Res., 36, 70-74.
40. Breslin, M.B. and Vedeckis, W. V (1998) The human glucocorticoid receptor promoter upstream sequences contain binding sites for the ubiquitous transcription factor, Yin Yang 1. J. Steroid Biochem. Mol. Biol., 67, 369-381.
41. Stolte, E.H., Verburg van Kemenade, B.M.L., Savelkoul, H.F.J. and Flik, G. (2006) Evolution of glucocorticoid receptors with different glucocorticoid sensitivity. J. Endocrinol., 190, 17-28.
42. Araujo, P.R., Yoon, K., Ko, D., Smith, A.D., Qiao, M., Suresh, U., Burns, S.C. and Penalva, L.O.F. (2012) Before it gets started: regulating translation at the 5′ UTR. Comp. Funct. Genomics, 475731.
43. Turner, J.D., Schote, A.B., Keipes, M. and Muller, C.P. (2007) A new transcript splice variant of the human glucocorticoid receptor: Identification and tissue distribution of hGR-313-338, an alternative exon 2 transactivation domain isoform. Ann. N. Y. Acad. Sci., 1095, 334-341.
44. Roni, V., Carpio, R. and Wissinger, B. (2007) Mapping of transcription start sites of human retina expressed genes. BMC Genomics, 8, 42.
45. Suzuki, Y., Yoshitomo-nakagawa, K., Maruyama, K. and Suyama, A. (1997) Construction and characterization of a full length-enriched and a 5′-end-enriched cDNA library. Gene, 200, 149-156.
46. Coleman, J.E. (1992) Structure and mechanism of alkaline phosphatase. Annu. Rev. Biophys. Biomol. Struct., 21, 441-483.
47. Rittié, L. and Perbal, B. (2008) Enzymes used in molecular biology: a useful guide. J. Cell Commun. Signal., 2, 25-45.
48. Castora, F.J. (1998) Enzymology of Recombinant DNA. In: Greene, JJ and Rao, VB (eds) . Recombinant DNA Principles and Methodologies. CRC Press, p. 768.
49. Alon, S., Vigneault, F., Eminaga, S., Christodoulou, D.C., Seidman, J.G., Church, G.M. and Eisenberg, E. (2011) Barcoding bias in high-throughput multiplex sequencing of miRNA. Genome Res., 21, 1506-1511.
50. Song, Y., Liu, K.J. and Wang, T.-H. (2014) Elimination of ligation dependent artifacts in T4 RNA ligase to achieve high efficiency and low bias microRNA capture. PLoS One, 9, e94619.
51. Berry, D., Ben Mahfoudh, K., Wagner, M. and Loy, A. (2011) Barcoded primers used in multiplex amplicon pyrosequencing bias amplification. Appl. Environ. Microbiol., 77, 7846-7849.
52. Jayaprakash, A.D., Jabado, O., Brown, B.D. and Sachidanandam, R. (2011) Identification and remediation of biases in the activity of RNA ligases in small-RNA deep sequencing. Nucleic Acids Res., 39, e141.
53. Van Nieuwerburgh, F., Soetaert, S., Podshivalova, K., Ay-LinWang, E., Schaffer, L., Deforce, D., Salomon, D.R., Head, S.R. and Ordoukhanian, P. (2011) Quantitative bias in Illumina TruSeq and a novel post amplification barcoding strategy for multiplexed DNA and small RNA deep sequencing. PLoS One, 6, e26969.
54. Hafner, M., Renwick, N., Brown, M. and Mihailović, A. (2011) RNA-ligase-dependent biases in miRNA representation in deep-sequenced small RNA cDNA libraries. RNA, doi:10.1261/rna.2799511.Croce.
55. Zhuang, F., Fuchs, R.T. and Robb, G.B. (2012) Small RNA expression profiling by high-throughput sequencing: implications of enzymatic manipulation. J. Nucleic Acids, 360358.
56. Kodzius, R., Kojima, M., Nishiyori, H., Nakamura, M., Fukuda, S., Tagami, M., Sasaki, D., Imamura, K., Kai, C., Harbers, M., et al. (2006) CAGE: cap analysis of gene expression. Nat. Methods, 3, 211-222.
57. Carninci, P., Kasukawa, T., Katayama, S., Gough, J., Frith, M.C., Maeda, N., Oyama, R., Ravasi, T., Lenhard, B., Wells, C., et al. (2005) The transcriptional landscape of the mammalian genome. Science, 309, 1559-1563.
58. Lu, N.Z. and Cidlowski, J.A. (2005) Translational regulatory mechanisms generate N-terminal glucocorticoid receptor isoforms with unique transcriptional target genes. Mol. Cell, 18, 331-342.
59. Wamboldt, Y., Mohammed, S., Elowsky, C., Wittgren, C., de Paula, W.B.M. and Mackenzie, S.a. (2009) Participation of Leaky Ribosome Scanning in Protein Dual Targeting by Alternative Translation Initiation in Higher Plants. Plant Cell Online, 21, 157-167.
60. Tournillon, A.-S., López, I., Malbert-Colas, L., Naski, N., Olivares-Illana, V. and Fahraeus, R. (2015) The alternative translated MDMX p60 isoform regulates MDM2 activity. Cell Cycle, 14, 449-458.
61. Bohrer, A.-S., Yoshimoto, N., Sekiguchi, A., Rykulski, N., Saito, K. and Takahashi, H. (2015) Alternative translational initiation of ATP sulfurylase underlying dual localization of sulfate assimilation pathways in plastids and cytosol in Arabidopsis thaliana. Front. Plant Sci., 5, 1-10.
62. Zhuo, R.-G., Peng, P., Liu, X.-Y., Zhang, S.-Z., Xu, J.-P., Zheng, J.-Q., Wei, X.-L. and Ma, X.-Y. (2015) The isoforms generated by alternative translation initiation adopt similar conformation in the selectivity filter in TREK-2. J. Physiol. Biochem., doi:10.1007/s13105-015-0422-z.
63. Cagney, G., Amiri, S., Premawaradena, T., Lindo, M. and Emili, A. (2003) In silico proteome analysis to facilitate proteomics experiments using mass spectrometry. Proteome Sci., 1, 5.
64. Ghesquiere, B., Jonckheere, V., Colaert, N., Van Durme, J., Timmerman, E., Goethals, M., Schymkowitz, J., Rousseau, F., Vandekerckhove, J. and Gevaert, K. (2011) Redox Proteomics of Protein-bound Methionine Oxidation. Mol. Cell. Proteomics, 10, M110.006866-M110.006866.
65. Wolf, Y.I., Novichkov, P.S., Karev, G.P., Koonin, E.V. and Lipman, D.J. (2009) The universal distribution of evolutionary rates of genes and distinct characteristics of eukaryotic genes of different apparent ages. Proc. Natl. Acad. Sci. U.S.A., 106, 7273-7280.
66. Hopkins-Donaldson, S., Ziegler, a, Kurtz, S., Bigosch, C., Kandioler, D., Ludwig, C., Zangemeister-Wittke, U. and Stahel, R. (2003) Silencing of death receptor and caspase-8 expression in small cell lung carcinoma cell lines and tumors by DNA methylation. Cell Death Differ., 10, 356-364.
67. Zhang, Z., Chen, C. and Manev, H. (2004) DNA methylation as an epigenetic regulator of neural 5-lipoxygenase expression: evidence in human NT2 and NT2-N cells. J. Neurochem., 88, 1424-1430.
68. Appleton, K., Mackay, H.J., Judson, I., Plumb, J.A., McCormick, C., Strathdee, G., Lee, C., Barrett, S., Reade, S., Jadayel, D., et al. (2007) Phase I and pharmacodynamic trial of the DNA methyltransferase inhibitor decitabine and carboplatin in solid tumors. J. Clin. Oncol., 25, 4603-4609.
69. Breivik, T., Gundersen, Y., Murison, R., Turner, J.D. and Muller, C.P. (2015) Maternal deprivation of Lewis rat pups increases the severity of experimental periodontitis in adulthood. Open Dent. J., 9, 65-78.
70. Weaver, I.C.G., Cervoni, N., Champagne, F.A., D'Alessio, A.C., Sharma, S., Seckl, J.R., Dymov, S., Szyf, M. and Meaney, M.J. (2004) Epigenetic programming by maternal behavior. Nat. Neurosci., 7, 847-854.
71. Moser, D., Molitor, A., Kumsta, R., Tatschner, T., Riederer, P. and Meyer, J. (2007) The glucocorticoid receptor gene exon 1-F promoter is not methylated at the NGFI-A binding site in human hippocampus.World J. Biol. Psychiatry, 8, 262-268.
72. Landry, J.-R., Mager, D.L. and Wilhelm, B.T. (2003) Complex controls: the role of alternative promoters in mammalian genomes. Trends Genet., 19, 640-648.
73. Shabalina, S.a., Ogurtsov, A.Y., Spiridonov, A.N., Novichkov, P.S., Spiridonov, N.a. and Koonin, E.V. (2010) Distinct patterns of expression and evolution of intronless and intron-containing mammalian genes. Mol. Biol. Evol., 27, 1745-1749.