G4 motifs correlate with promoter-proximal transcriptional pausing in human genes

Nucleic Acids Research

Volumn 39, Issue 12, 2011, Pages 4975-4983

  Eddy, Johanna ^a   Vallur, Aarthy C ^a   Varma, Sudir ^b   Liu, Hongfang ^b,c   Reinhold, William C ^b   Pommier, Yves ^b   Maizels, Nancy ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c GEORGETOWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; RNA; RNA POLYMERASE II; TRANSCRIPTION FACTOR SP1;

ARTICLE; CONTROLLED STUDY; DNA STRAND; DNA STRUCTURE; DNA TEMPLATE; DOWN REGULATION; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HUMAN; INTRON; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN MOTIF; RNA STRUCTURE; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION REGULATION; UPREGULATION;

BINDING SITES; CELL LINE, TUMOR; CPG ISLANDS; GUANINE; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; INTRONS; PROMOTER REGIONS, GENETIC; REGULATORY ELEMENTS, TRANSCRIPTIONAL; RNA POLYMERASE II; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION, GENETIC;

EID: 79960228890     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr079     Document Type: Article

References (47)

1. Barski, A., Cuddapah, S., Cui, K., Roh, T.Y., Schones, D.E., Wang, Z., Wei, G., Chepelev, I. and Zhao, K. (2007) High-resolution profiling of histone methylations in the human genome. Cell, 129, 823-837. (Pubitemid 46802390)
2. Margaritis, T. and Holstege, F.C. (2008) Poised RNA polymerase II gives pause for thought. Cell, 133, 581-584. (Pubitemid 351636308)
3. Gilmour, D.S. (2009) Promoter proximal pausing on genes in metazoans. Chromosoma, 118, 1-10.
4. Eddy, J. and Maizels, N. (2008) Conserved elements with potential to form polymorphic G-quadruplex structures in the first intron of human genes. Nucleic Acids Res., 36, 1321-1333. (Pubitemid 351330947)
5. Eddy, J. and Maizels, N. (2006) Gene function correlates with potential for G4 DNA formation in the human genome. Nucleic Acids Res., 34, 3887-3896. (Pubitemid 44391004)
6. Burge, S., Parkinson, G.N., Hazel, P., Todd, A.K. and Neidle, S. (2006) Quadruplex DNA: sequence, topology and structure. Nucleic Acids Res., 34, 5402-5415. (Pubitemid 44742430)
7. Phan, A.T., Kuryavyi, V. and Patel, D.J. (2006) DNA architecture: from G to Z. Curr. Opin. Struct. Biol., 16, 288-298. (Pubitemid 43831655)
8. Reinhold, W.C., Mergny, J.L., Liu, H., Ryan, M., Pfister, T.D., Kinders, R., Parchment, R., Doroshow, J., Weinstein, J.N. and Pommier, Y. (2010) Exon array analyses across the NCI-60 reveal potential regulation of TOP1 by transcription pausing at guanosine quartets in the first intron. Cancer Res., 70, 2191-2203.
9. Duquette, M.L., Pham, P., Goodman, M.F. and Maizels, N. (2005) AID binds to transcription-induced structures in c-MYC that map to regions associated with translocation and hypermutation. Oncogene, 24, 5791-5798. (Pubitemid 43080070)
10. Duquette, M.L., Handa, P., Vincent, J.A., Taylor, A.F. and Maizels, N. (2004) Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev., 18, 1618-1629. (Pubitemid 38868912)
11. Duquette, M.L., Huber, M.D. and Maizels, N. (2007) G-rich proto-oncogenes are targeted for genomic instability in B-cell lymphomas. Cancer Res., 67, 2586-2594. (Pubitemid 46548944)
12. Vallur, A.C. and Maizels, N. (2008) Activities of human exonuclease 1 that promote cleavage of transcribed immunoglobulin switch regions. Proc. Natl Acad. Sci. USA, 105, 16508-16512.
13. Aguilera, A. (2005) mRNA processing and genomic instability. Nat. Struct. Mol. Biol., 12, 737-738. (Pubitemid 43086246)
14. Li, X. and Manley, J.L. (2006) Cotranscriptional processes and their influence on genome stability. Genes Dev., 20, 1838-1847. (Pubitemid 44079322)
15. Lin, Y., Dent, S.Y., Wilson, J.H., Wells, R.D. and Napierala, M. (2010) R loops stimulate genetic instability of CTG.CAG repeats. Proc. Natl Acad. Sci. USA, 107, 692-697.
16. Sordet, O., Redon, C.E., Guirouilh-Barbat, J., Smith, S., Solier, S., Douarre, C., Conti, C., Nakamura, A.J., Das, B.B., Nicolas, E. et al. (2009) Ataxia telangiectasia mutated activation by transcriptionand topoisomerase I-induced DNA double-strand breaks. EMBO Rep., 10, 887-893.
17. Hubbard, T., Andrews, D., Caccamo, M., Cameron, G., Chen, Y., Clamp, M., Clarke, L., Coates, G., Cox, T., Cunningham, F. et al. (2005) Ensembl 2005. Nucleic Acids Res., 33, D447-453. (Pubitemid 40207913)
18. Durinck, S., Moreau, Y., Kasprzyk, A., Davis, S., De Moor, B., Brazma, A. and Huber, W. (2005) BioMart and bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics, 21, 3439-3440. (Pubitemid 41222455)
19. Irizarry, R.A., Bolstad, B.M., Collin, F., Cope, L.M., Hobbs, B. and Speed, T.P. (2003) Summaries of affymetrix geneChip probe level data. Nucleic Acids Res., 31, e15.
20. Ryan, M.C., Zeeberg, B.R., Caplen, N.J., Cleland, J.A., Kahn, A.B., Liu, H. and Weinstein, J.N. (2008) SpliceCenter: a suite of web-based bioinformatic applications for evaluating the impact of alternative splicing on RT-PCR, RNAi, microarray, and peptide-based studies. BMC Bioinformatics, 9, 313.
21. Scherf, U., Ross, D.T., Waltham, M., Smith, L.H., Lee, J.K., Tanabe, L., Kohn, K.W., Reinhold, W.C., Myers, T.G., Andrews, D.T. et al. (2000) A gene expression database for the molecular pharmacology of cancer. Nat. Genet., 24, 236-244. (Pubitemid 30132190)
22. Weinstein, J.N. and Pommier, Y. (2003) Transcriptomic analysis of the NCI-60 cancer cell lines. C. R. Biol., 326, 909-920. (Pubitemid 38016446)
23. Shoemaker, R.H. (2006) The NCI60 human tumour cell line anticancer drug screen. Nat. Rev. Cancer, 6, 813-823. (Pubitemid 44450469)
24. Bernstein, B.E., Mikkelsen, T.S., Xie, X., Kamal, M., Huebert, D.J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K. et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell, 125, 315-326.
25. Burd, C.G. and Dreyfuss, G. (1994b) RNA binding specificity of hnRNP A1: significance of hnRNP A1 high-affinity binding sites in pre-mRNA splicing. EMBO J., 13, 1197-1204. (Pubitemid 24074726)
26. Caputi, M. and Zahler, A.M. (2001) Determination of the RNA binding specificity of the heterogeneous nuclear ribonucleoprotein (hnRNP) H/H'/F/2H9 family. J. Biol. Chem., 276, 43850-43859.
27. Cahoon, L.A. and Seifert, H.S. (2009) An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae. Science, 325, 764-767.
28. Tornaletti, S., Park-Snyder, S. and Hanawalt, P.C. (2008) G4-forming sequences in the non-transcribed DNA strand pose blocks to T7 RNA polymerase and mammalian RNA polymerase II. J. Biol. Chem., 283, 12756-12762.
29. Woodford, K.J., Howell, R.M. and Usdin, K. (1994) A novel K(+)-dependent DNA synthesis arrest site in a commonly occurring sequence motif in eukaryotes. J. Biol. Chem., 269, 27029-27035. (Pubitemid 24332906)
30. Kumari, S., Bugaut, A., Huppert, J.L. and Balasubramanian, S. (2007) An RNA G-quadruplex in the 50 UTR of the NRAS proto-oncogene modulates translation. Nat. Chem. Biol., 3, 218-221. (Pubitemid 46440536)
31. Arora, A., Dutkiewicz, M., Scaria, V., Hariharan, M., Maiti, S. and Kurreck, J. (2008) Inhibition of translation in living eukaryotic cells by an RNA G-quadruplex motif. RNA, 14, 1290-1296. (Pubitemid 351872187)
32. Toulokhonov, I., Zhang, J., Palangat, M. and Landick, R. (2007) A central role of the RNA polymerase trigger loop in active-site rearrangement during transcriptional pausing. Mol. Cell, 27, 406-419. (Pubitemid 47126936)
33. Stevens, M., De Clercq, E. and Balzarini, J. (2006) The regulation of HIV-1 transcription: molecular targets for chemotherapeutic intervention. Med. Res. Rev., 26, 595-625. (Pubitemid 44230414)
34. El Hage, A., French, S.L., Beyer, A.L. and Tollervey, D. (2010) Loss of Topoisomerase I leads to R-loop-mediated transcriptional blocks during ribosomal RNA synthesis. Genes Dev., 24, 1546-1558.
35. Maizels, N.M. (1973) The nucleotide sequence of the lactose messenger ribonucleic acid transcribed from the UV5 promoter mutant of Escherichia coli. Proc. Natl Acad. Sci. USA, 70, 3585-3589.
36. Maizels, N. (2006) Dynamic roles for G4 DNA in the biology of eukaryotic cells. Nat. Struct. Mol. Biol., 13, 1055-1059. (Pubitemid 44885914)
37. Pavri, R., Gazumyan, A., Jankovic, M., Di Virgilio, M., Klein, I., Ansarah-Sobrinho, C., Resch, W., Yamane, A., San-Martin, B.R., Barreto, V. et al. (2010) Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5. Cell, 143, 122-133.
38. Pauklin, S., Sernandez, I.V., Bachmann, G., Ramiro, A.R. and Petersen-Mahrt, S.K. (2009) Estrogen directly activates AID transcription and function. J. Exp. Med., 206, 99-111.
39. Brassart, B., Gomez, D., De Cian, A., Paterski, R., Montagnac, A., Qui, K.H., Temime-Smaali, N., Trentesaux, C., Mergny, J.L., Gueritte, F. et al. (2007) A new steroid derivative stabilizes g-quadruplexes and induces telomere uncapping in human tumor cells. Mol. Pharmacol., 72, 631-640. (Pubitemid 47347298)
40. De Cian, A. and Mergny, J.L. (2007) Quadruplex ligands may act as molecular chaperones for tetramolecular quadruplex formation. Nucleic Acids Res., 35, 2483-2493.
41. Drygin, D., Siddiqui-Jain, A., O'Brien, S., Schwaebe, M., Lin, A., Bliesath, J., Ho, C.B., Proffitt, C., Trent, K., Whitten, J.P. et al. (2009) Anticancer activity of CX-3543: a direct inhibitor of rRNA biogenesis. Cancer Res., 69, 7653-7661.
42. Sparapani, S., Haider, S.M., Doria, F., Gunaratnam, M. and Neidle, S. (2010) Rational design of acridine-based ligands with selectivity for human telomeric quadruplexes. J. Am. Chem. Soc., 132, 12263-12272.
43. Reyes-Reyes, E.M., Teng, Y. and Bates, P.J. (2010) A new paradigm for aptamer therapeutic AS1411 action: uptake by macropinocytosis and its stimulation by a nucleolin-dependent mechanism. Cancer Res., 70, 8617-8629.
44. Pommier, Y., Leo, E., Zhang, H. and Marchand, C. (2010) DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem. Biol., 17, 421-433.
45. Khobta, A., Ferri, F., Lotito, L., Montecucco, A., Rossi, R. and Capranico, G. (2006) Early effects of topoisomerase I inhibition on RNA polymerase II along transcribed genes in human cells. J. Mol. Biol., 357, 127-138. (Pubitemid 43339319)
46. Hraiky, C., Raymond, M.A. and Drolet, M. (2000) RNase H overproduction corrects a defect at the level of transcription elongation during rRNA synthesis in the absence of DNA topoisomerase I in Escherichia coli. J. Biol. Chem., 275, 11257-11263. (Pubitemid 30212772)
47. Drolet, M., Broccoli, S., Rallu, F., Hraiky, C., Fortin, C., Masse, E. and Baaklini, I. (2003) The problem of hypernegative supercoiling and R-loop formation in transcription. Front. Biosci., 8, d210-d221. (Pubitemid 39069972)