Transcription blockage by homopurine DNA sequences: Role of sequence composition and single-strand breaks

Nucleic Acids Research

Volumn 41, Issue 3, 2013, Pages 1817-1828

  Belotserkovskii, Boris P ^a   Neil, Alexander J ^a   Saleh, Syed Shayon ^b   Shin, Jane Hae Soo ^a   Mirkin, Sergei M ^b   Hanawalt, Philip C ^a  

^a STANFORD UNIVERSITY   (United States)

^b TUFTS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; CYTOSINE; DOUBLE STRANDED DNA; GUANINE; PURINE; PYRIMIDINE; THYMINE;

ARTICLE; CONTROLLED STUDY; DNA DETERMINATION; DNA SEQUENCE; DNA TEMPLATE; DNA TRANSCRIPTION; DOWN REGULATION; GENE INSERTION; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SINGLE STRANDED DNA BREAK; TRANSCRIPTION REGULATION; UPREGULATION;

BASE COMPOSITION; BASE SEQUENCE; DNA; DNA BREAKS, SINGLE-STRANDED; DNA-DIRECTED RNA POLYMERASES; GUANINE; NUCLEIC ACID CONFORMATION; NUCLEOTIDES; TRANSCRIPTION, GENETIC;

EID: 84873635660     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1333     Document Type: Article

References (67)

1. Aguilera,A. (2002) The connection between transcription and genomic instability. EMBO J., 21, 195-201.
2. Bacolla,A. and Wells,R.D. (2009) Non-B DNA conformations as determinants of mutagenesis and human disease. Mol. Carcinog., 48, 273-285.
3. Hanawalt,P.C. and Spivak,G. (2008) Transcription-coupled DNA repair: two decades of progress and surprises. Nat. Rev. Mol. Cell. Biol., 9, 958-970.
4. Zhao,J., Bacolla,A., Wang,G. and Vasquez,K.M. (2010) Non-B DNA structure-induced genetic instability and evolution. Cell. Mol. Life. Sci., 67, 43-62.
5. Daniels,G.A. and Lieber,M.R. (1995) RNA:DNA complex formation upon transcription of immunoglobulin switch regions: implications for the mechanism and regulation of class switch recombination. Nucleic Acids Res., 23, 5006-5011.
6. Maizels,N. (2006) Dynamic roles for G4 DNA in the biology of eukaryotic cells. Nat. Struct. Mol. Biol., 13, 1055-1059.
7. 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.
8. 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.
9. Eddy,J. and Maizels,N. (2009) Selection for the G4 DNA motif at the 50 end of human genes. Mol. Carcinog., 48, 319-325.
10. Wongsurawat,T., Jenjaroenpun,P., Kwoh,C.K. and Kuznetsov,V. (2012) Quantitative model of R-loop forming structures reveals a novel level of RNA-DNA interactome complexity. Nucleic Acids Res., 40, e16.
11. Yu,K., Chedin,F., Hsieh,C.L., Wilson,T.E. and Lieber,M.R. (2003) R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Nat. Immunol., 4, 442-451.
12. 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.
13. Reaban,M.E., Lebowitz,J. and Griffin,J.A. (1994) Transcription induces the formation of a stable RNA.DNA hybrid in the immunoglobulin alpha switch region. J. Biol. Chem., 269, 21850-21857.
14. Reaban,M.E. and Griffin,J.A. (1990) Induction of RNA-stabilized DNA conformers by transcription of an immunoglobulin switch region. Nature, 348, 342-344.
15. Grabczyk,E. and Fishman,M.C. (1995) A long purine-pyrimidine homopolymer acts as a transcriptional diode. J. Biol. Chem., 270, 1791-1797.
16. Grabczyk,E. and Usdin,K. (2000) The GA A.*TTC triplet repeat expanded in Friedreich's ataxia impedes transcription elongation by T7 RNA polymerase in a length and supercoil dependent manner. Nucleic Acids Res., 28, 2815-2822.
17. Karamychev,V.N., Panyutin,I.G., Neumann,R.D. and Zhurkin,V.B. (2000) DNA and RNA Folds in Transcription Complex as Evidenced by Iodine-125 Radioprobing. J. Biomol. Struct. Dyn, 17, 155-167.
18. Martianov,I., Ramadass,A., Serra Barros,A., Chow,N. and Akoulitchev,A. (2007) Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript. Nature, 445, 666-670.
19. Roberts,R.W. and Crothers,D.M. (1992) Stability and properties of double and triple helices: dramatic effects of RNA or DNA backbone composition. Science, 258, 1463-1466.
20. Lesnik,E.A. and Freier,S.M. (1995) Relative thermodynamic stability of DNA, RNA, and DNA:RNA hybrid duplexes: relationship with base composition and structure. Biochemistry, 34, 10807-10815.
21. Gyi,J.I., Conn,G.L., Lane,A.N. and Brown,T. (1996) Comparison of the thermodynamic stabilities and solution conformations of DNA.RNA hybrids containing purine-rich and pyrimidine-rich strands with DNA and RNA duplexes. Biochemistry, 35, 12538-12548.
22. Roy,D. and Lieber,M.R. (2009) G clustering is important for the initiation of transcription-induced R-loops in vitro, whereas high G density without clustering is sufficient thereafter. Mol. Cell. Biol., 29, 3124-3133.
23. Roy,D., Yu,K. and Lieber,M.R. (2008) Mechanism of R-loop formation at immunoglobulin class switch sequences. Mol. Cell. Biol., 28, 50-60.
24. Rajagopal,D., Maul,R.W., Ghosh,A., Chakraborty,T., Khamlichi,A.A., Sen,R. and Gearhart,P.J. (2009) Immunoglobulin switch mu sequence causes RNA polymerase II accumulation and reduces dA hypermutation. J. Exp. Med., 206, 1237-1244.
25. Mirkin,E.V. and Mirkin,S.M. (2007) Replication fork stalling at natural impediments. Microbiol. Mol. Biol. Rev., 71, 13-35.
26. Potenski,C.J. and Klein,H.L. (2011) R we there yet? R-loop hazards to finishing the journey. Mol. Cell., 44, 848-850.
27. Krasilnikova,M.M., Samadashwily,G.M., Krasilnikov,A.S. and Mirkin,S.M. (1998) Transcription through a simple DNA repeat blocks replication elongation. EMBO J., 17, 5095-5102.
28. Belotserkovskii,B.P., Liu,R., Tornaletti,S., Krasilnikova,M.M., Mirkin,S.M. and Hanawalt,P.C. (2010) Mechanisms and implications of transcription blockage by guanine-rich DNA sequences. Proc. Natl Acad. Sci. USA, 107, 12816-12821.
29. Belotserkovskii,B.P. and Hanawalt,P.C. (2011) Anchoring nascent RNA to the DNA template could interfere with transcription. Biophys. J., 100, 675-684.
30. Roy,D., Zhang,Z., Lu,Z., Hsieh,C.L. and Lieber,M.R. (2010) Competition between the RNA transcript and the nontemplate DNA strand during R-loop formation in vitro: a nick can serve as a strong R-loop initiation site. Mol. Cell. Biol., 30, 146-159.
31. Tornaletti,S., Patrick,S.M., Turchi,J.J. and Hanawalt,P.C. (2003) Behavior of T7 RNA polymerase and mammalian RNA polymerase II at site-specific cisplatin adducts in the template DNA. J. Biol. Chem., 278, 35791-35797.
32. Belotserkovskii,B.P., De Silva,E., Tornaletti,S., Wang,G., Vasquez,K.M. and Hanawalt,P.C. (2007) A triplex-forming sequence from the human c-MYC promoter interferes with DNA transcription. J. Biol. Chem., 282, 32433-32441.
33. Ditlevson,J.V., Tornaletti,S., Belotserkovskii,B.P., Teijeiro,V., Wang,G., Vasquez,K.M. and Hanawalt,P.C. (2008) Inhibitory effect of a short Z-DNA forming sequence on transcription elongation by T7 RNA polymerase. Nucleic Acids Res., 36, 3163-3170.
34. Zhou,W. and Doetsch,P.W. (1994) Transcription bypass or blockage at single-strand breaks on the DNA template strand: effect of different 3' and 5' flanking groups on the T7 RNA polymerase elongation complex. Biochemistry, 33, 14926-14934.
35. Neil,A.J., Belotserkovskii,B.P. and Hanawalt,P.C. (2012) Transcription blockage by bulky end termini at single-strand breaks in the DNA template: differential effects of 5' and 3' adducts. Biochemistry, 51, 8964-8970.
36. Khobta,A., Lingg,T., Schulz,I., Warken,D., Kitsera,N. and Epe,B. (2010) Mouse CSB protein is important for gene expression in the presence of a single-strand break in the non-transcribed DNA strand. DNA Repair (Amst.), 9, 985-993.
37. Frank-Kamenetskii,M.D. and Mirkin,S.M. (1995) Triplex DNA structures. Annu. Rev. Biochem., 64, 65-95.
38. Mirkin,S.M. and Frank-Kamenetskii,M.D. (1994) H-DNA and related structures. Annu. Rev. Biophys. Biomol. Struct., 23, 541-576.
39. Grabczyk,E., Mancuso,M. and Sammarco,M.C. (2007) A persistent RNA.DNA hybrid formed by transcription of the Friedreich ataxia triplet repeat in live bacteria, and by T7 RNAP in vitro. Nucleic Acids Res., 35, 5351-5359.
40. Rachwal,P.A., Brown,T. and Fox,K.R. (2007) Sequence effects of single base loops in intramolecular quadruplex DNA. FEBS Lett., 581, 1657-1660.
41. sGuedin,A., De Cian,A., Gros,J., Lacroix,L. and Mergny,J.L. (2008) Sequence effects in single-base loops for quadruplexes. Biochimie, 90, 686-696.
42. Gopal,V., Brieba,L.G., Guajardo,R., McAllister,W.T. and Sousa,R. (1999) Characterization of structural features important for T7 RNAP elongation complex stability reveals competing complex conformations and a role for the non-template strand in RNA displacement. J. Mol. Biol., 290, 411-431.
43. Drolet,M. (2006) Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology. Mol. Microbiol., 59, 723-730.
44. Reddy,K., Tam,M., Bowater,R.P., Barber,M., Tomlinson,M., Nichol Edamura,K., Wang,Y.H. and Pearson,C.E. (2011) Determinants of R-loop formation at convergent bidirectionally transcribed trinucleotide repeats. Nucleic Acids Res., 39, 1749-1762.
45. Tous,C. and Aguilera,A. (2007) Impairment of transcription elongation by R-loops in vitro. Biochem. Biophys. Res. Commun., 360, 428-432.
46. Daube,S.S. and von Hippel,P.H. (1994) RNA displacement pathways during transcription from synthetic RNA-DNA bubble duplexes. Biochemistry, 33, 340-347.
47. Yin,Y.W. and Steitz,T.A. (2004) The structural mechanism of translocation and helicase activity in T7 RNA polymerase. Cell, 116, 393-404.
48. Jiang,M., Ma,N., Vassylyev,D.G. and McAllister,W.T. (2004) RNA displacement and resolution of the transcription bubble during transcription by T7 RNA polymerase. Mol. Cell, 15, 777-788.
49. Mentesana,P.E., Chin-Bow,S.T., Sousa,R. and McAllister,W.T. (2000) Characterization of halted T7 RNA polymerase elongation complexes reveals multiple factors that contribute to stability. J. Mol. Biol., 302, 1049-1062.
50. Tomizawa,J. and Masukata,H. (1987) Factor-independent termination of transcription in a stretch of deoxyadenosine residues in the template DNA. Cell, 51, 623-630.
51. Zhou,J., Ha,K.S., La Porta,A., Landick,R. and Block,S.M. (2011) Applied force provides insight into transcriptional pausing and its modulation by transcription factor NusA. Mol. Cell, 44, 635-646.
52. Dalal,R.V., Larson,M.H., Neuman,K.C., Gelles,J., Landick,R. and Block,S.M. (2006) Pulling on the nascent RNA during transcription does not alter kinetics of elongation or ubiquitous pausing. Mol. Cell, 23, 231-239.
53. Zhou,Y. and Martin,C.T. (2006) Observed instability of T7 RNA polymerase elongation complexes can be dominated by collision-induced ''bumping''. J. Biol. Chem., 281, 24441-24448.
54. Nudler,E. (2012) RNA polymerase backtracking in gene regulation and genome instability. Cell, 149, 1438-1445.
55. Eddy,J., Vallur,A.C., Varma,S., Liu,H., Reinhold,W.C., Pommier,Y. and Maizels,N. (2011) G4 motifs correlate with promoter-proximal transcriptional pausing in human genes. Nucleic Acids Res., 39, 4975-4983.
56. Azzalin,C.M. and Lingner,J. (2008) Telomeres: the silence is broken. Cell Cycle, 7, 1161-1165.
57. Marcu,K.B., Bossone,S.A. and Patel,A.J. (1992) myc function and regulation. Annu. Rev. Biochem., 61, 809-860.
58. Lin,Y., Hubert,L. Jr and Wilson,J.H. (2009) Transcription destabilizes triplet repeats. Mol. Carcinog., 48, 350-361.
59. 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.
60. Salinas-Rios,V., Belotserkovskii,B.P. and Hanawalt,P.C. (2011) DNA slip-outs cause RNA polymerase II arrest in vitro: potential implications for genetic instability. Nucleic Acids Res., 39, 7444-7454.
61. Gomez-Gonzalez,B., Garcia-Rubio,M., Bermejo,R., Gaillard,H., Shirahige,K., Marin,A., Foiani,M. and Aguilera,A. (2011) Genome-wide function of THO/TREX in active genes prevents R-loop-dependent replication obstacles. EMBO J., 30, 3106-3119.
62. Kim,N. and Jinks-Robertson,S. (2011) Guanine repeat-containing sequences confer transcription-dependent instability in an orientation-specific manner in yeast. DNA Repair (Amst.), 10, 953-960.
63. Mellon,I., Spivak,G. and Hanawalt,P.C. (1987) Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell, 51, 241-249.
64. Mellon,I. and Hanawalt,P.C. (1989) Induction of the Escherichia coli lactose operon selectively increases repair of its transcribed DNA strand. Nature, 342, 95-98.
65. Hanawalt,P.C. (1994) Transcription-coupled repair and human disease. Science, 266, 1957-1958.
66. Geisler,S., Lojek,L., Khalil,A.M., Baker,K.E. and Coller,J. (2012) Decapping of Long Noncoding RNAs Regulates Inducible Genes. Mol. Cell, 45, 279-291.
67. Liu,C.R., Chang,C.R., Chern,Y., Wang,T.H., Hsieh,W.C., Shen,W.C., Chang,C.Y., Chu,I.C., Deng,N., Cohen,S.N. et al. (2012) Spt4 is selectively required for transcription of extended trinucleotide repeats. Cell, 148, 690-701.