DNA slip-outs cause RNA polymerase II arrest in vitro: Potential implications for genetic instability

Nucleic Acids Research

Volumn 39, Issue 17, 2011, Pages 7444-7455

  Salinas Rios, Viviana ^a   Belotserkovskii, Boris P ^a   Hanawalt, Philip C ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE II; SINGLE STRANDED DNA;

CAG REPEAT; CELL CYCLE ARREST; CELL EXPANSION; CONTROLLED STUDY; DNA TRANSCRIPTION; ENZYME SUBSTRATE; GENE DOSAGE; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN CONFORMATION; REVIEW; RNA SYNTHESIS;

DNA; DNA-DIRECTED RNA POLYMERASES; HELA CELLS; HUMANS; NUCLEIC ACID CONFORMATION; RNA POLYMERASE II; TRANSCRIPTION, GENETIC; TRINUCLEOTIDE REPEAT EXPANSION; TRINUCLEOTIDE REPEATS; VIRAL PROTEINS;

MAMMALIA;

EID: 80053215162     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr429     Document Type: Review

References (42)

1. Wells, R.D. and Ashizawa, T. (2006) Genetic Instabilities and Neurological Diseases, 2nd edn. Elsevier Inc, San Diego, CA.
2. Mirkin, S.M. (2007) Expandable DNA repeats and human disease. Nature, 447, 932-940.
3. Sinden, R.R., Potaman, V.N., Oussatcheva, E.A., Pearson, C.E., Lyubchenko, Y.L. and Shlyakhtenko, L.S. (2002) Triplet repeat DNA structures and human genetic disease: dynamic mutations from dynamic DNA. J. Biosci., 27, 53-65.
4. Usdin, K. and Grabczyk, E. (2000) DNA repeat expansions and human disease. Cell Mol. Life Sci., 57, 914-931.
5. Duyao, M., Ambrose, C., Myers, R., Novelletto, A., Persichetti, F., Frontali, M., Folstein, S., Ross, C., Franz, M., Abbott, M. et al. (1993) Trinucleotide repeat length instability and age of onset in Huntington's disease. Nat. Genet., 4, 387-392.
6. Pearson, C.E., Nichol Edamura, K. and Cleary, J.D. (2005) Repeat instability: mechanisms of dynamic mutations. Nat. Rev. Genet., 6, 729-742.
7. Telenius, H., Kremer, B., Goldberg, Y.P., Theilmann, J., Andrew, S.E., Zeisler, J., Adam, S., Greenberg, C., Ives, E.J., Clarke, L.A. et al. (1994) Somatic and gonadal mosaicism of the Huntington disease gene CAG repeat in brain and sperm. Nat. Genet., 6, 409-414.
8. Kennedy, L., Evans, E., Chen, C.M., Craven, L., Detloff, P.J., Ennis, M. and Shelbourne, P.F. (2003) Dramatic tissue-specific mutation length increases are an early molecular event in Huntington disease pathogenesis. Hum. Mol. Genet., 12, 3359-3367.
9. Ishiguro, H., Yamada, K., Sawada, H., Nishii, K., Ichino, N., Sawada, M., Kurosawa, Y., Matsushita, N., Kobayashi, K., Goto, J. et al. (2001) Age-dependent and tissue-specific CAG repeat instability occurs in mouse knock-in for a mutant Huntington's disease gene. J. Neurosci. Res., 65, 289-297.
10. Kennedy, L. and Shelbourne, P.F. (2000) Dramatic mutation instability in HD mouse striatum: does polyglutamine load contribute to cell-specific vulnerability in Huntington's disease? Hum. Mol. Genet., 9, 2539-2544.
11. Wells, R.D., Dere, R., Hebert, M.L., Napierala, M. and Son, L.S. (2005) Advances in mechanisms of genetic instability related to hereditary neurological diseases. Nucleic Acids Res., 33, 3785-3798.
12. Raghavan, S.C. and Lieber, M.R. (2007) DNA structure and human diseases. Front Biosci., 12, 4402-4408.
13. Petruska, J., Arnheim, N. and Goodman, M.F. (1996) Stability of intrastrand hairpin structures formed by the CAG/CTG class of DNA triplet repeats associated with neurological diseases. Nucleic Acids Res., 24, 1992-1998.
14. Petruska, J., Hartenstine, M.J. and Goodman, M.F. (1998) Analysis of strand slippage in DNA polymerase expansions of CAG/CTG triplet repeats associated with neurodegenerative disease. J. Biol. Chem., 273, 5204-5210.
15. Pearson, C.E., Tam, M., Wang, Y.H., Montgomery, S.E., Dar, A.C., Cleary, J.D. and Nichol, K. (2002) Slipped-strand DNAs formed by long (CAG)*(CTG) repeats: slipped-out repeats and slip-out junctions. Nucleic Acids Res., 30, 4534-4547.
16. Pearson, C.E. and Sinden, R.R. (1996) Alternative structures in duplex DNA formed within the trinucleotide repeats of the myotonic dystrophy and fragile X loci. Biochemistry, 35, 5041-5053.
17. Mirkin, S.M. (2006) DNA structures, repeat expansions and human hereditary disorders. Curr. Opin Struct. Biol., 16, 351-358.
18. Lin, Y. and Wilson, J.H. (2007) Transcription-induced CAG repeat contraction in human cells is mediated in part by transcription-coupled nucleotide excision repair. Mol. Cell Biol., 27, 6209-6217.
19. Lin, Y., Dion, V. and Wilson, J.H. (2006) Transcription promotes contraction of CAG repeat tracts in human cells. Nat. Struct. Mol. Biol., 13, 179-180.
20. Lin, Y., Hubert, L. Jr. and Wilson, J.H. (2009) Transcription destabilizes triplet repeats. Mol. Carcinog., 48, 350-361.
21. Hanawalt, P.C. (1994) Transcription-coupled repair and human disease. Science, 266, 1957-1958.
22. 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.
23. Parsons, M.A., Sinden, R.R. and Izban, M.G. (1998) Transcriptional properties of RNA polymerase II within triplet repeat-containing DNA from the human myotonic dystrophy and fragile X loci. J. Biol. Chem., 273, 26998-27008.
24. 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.
25. 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.
26. Manley, J.L., Fire, A., Samuels, M. and Sharp, P.A. (1983) In vitro transcription: whole-cell extract. Methods Enzymol., 101, 568-582.
27. Pugh, B.F. (1995) Preparation of HeLa nuclear extracts. Methods Mol. Biol., 37, 349-357.
28. Nacheva, G.A. and Berzal-Herranz, A. (2003) Preventing nondesired RNA-primed RNA extension catalyzed by T7 RNA polymerase. Eur. J. Biochem., 270, 1458-1465.
29. Tornaletti, S. (2009) DNA repair in mammalian cells: Transcription- coupled DNA repair: directing your effort where it's most needed. Cell Mol. Life Sci., 66, 1010-1020.
30. Tornaletti, S. (2005) Transcription arrest at DNA damage sites. Mutat. Res., 577, 131-145.
31. 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.
32. 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.
33. 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.
34. 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.
35. Andrecka, J., Treutlein, B., Arcusa, M.A., Muschielok, A., Lewis, R., Cheung, A.C., Cramer, P. and Michaelis, J. (2009) Nano positioning system reveals the course of upstream and nontemplate DNA within the RNA polymerase II elongation complex. Nucleic Acids Res., 37, 5803-5809.
36. Manley, K., Shirley, T.L., Flaherty, L. and Messer, A. (1999) Msh2 deficiency prevents in vivo somatic instability of the CAG repeat in Huntington disease transgenic mice. Nat. Genet., 23, 471-473.
37. Sinden, R.R. (2001) Neurodegenerative diseases. Origins of instability. Nature, 411, 757-758.
38. Aguilera, A. (2002) The connection between transcription and genomic instability. EMBO J., 21, 195-201.
39. Liu, G., Chen, X., Bissler, J.J., Sinden, R.R. and Leffak, M. (2010) Replication-dependent instability at (CTG) x (CAG) repeat hairpins in human cells. Nat. Chem. Biol., 6, 652-659.
40. 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.
41. McIvor, E.I., Polak, U. and Napierala, M. (2010) New insights into repeat instability: role of RNA.DNA hybrids. RNA Biol., 7, 551-558.
42. Reddy, K., Tam, M., Bowater, R.P., Barber, M., Tomlinson, M., Nichol Edamura, K., Wang, Y.H. and Pearson, C.E. (2010) Determinants of R-loop formation at convergent bidirectionally transcribed trinucleotide repeats. Nucleic Acids Res., 39, 1749-1762.