Topoisomerase 1 provokes the formation of short deletions in repeated sequences upon high transcription in Saccharomyces cerevisiae

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 2, 2011, Pages 692-697

  Takahashi, Tomio ^a,b   Burguiere Slezak, Guenaelle ^a,b   Auffret Van Der Kemp, Patricia ^a,b   Boiteux, Serge ^a,b  

^a INSTITUT DE RADIOBIOLOGIE CELLULAIRE ET MOLÉCULAIRE   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME PROTEIN; DNA TOPOISOMERASE; NUCLEIC ACID BINDING PROTEIN; PROTEIN CAN1; PROTEIN MUS81; PROTEIN RAD1; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DINUCLEOTIDE REPEAT; DNA METABOLISM; DNA PROTEIN COMPLEX; DNA REPAIR; GENE DELETION; GENOMIC INSTABILITY; MUTAGENESIS; MUTATION RATE; NONHUMAN; PRIORITY JOURNAL; PROTEIN MICROARRAY; SACCHAROMYCES CEREVISIAE; SPONTANEOUS MUTATION; TRANSCRIPTION ASSOCIATED MUTAGENESIS; TRANSCRIPTION REGULATION; TRINUCLEOTIDE REPEAT;

SACCHAROMYCES CEREVISIAE;

EID: 79551661538     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1012582108     Document Type: Article

References (38)

1. Hanawalt PC (2002) Subpathways of nucleotide excision repair and their regulation. Oncogene 21:8949-8956.
2. Aguilera A (2002) The connection between transcription and genomic instability. EMBO J 21:195-201.
3. Azvolinsky A, Giresi PG, Lieb JD, Zakian VA (2009) Highly transcribed RNA polymerase II genes are impediments to replication fork progression in Saccharomyces cerevisiae. Mol Cell 34:722-734.
4. Ivessa AS, et al. (2003) The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol Cell 12:1525-1536.
5. Huertas P, Aguilera A (2003) Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol Cell 12:711-721.
6. Prado F, Aguilera A (2005) Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J 24:1267-1276.
7. Gottipati P, Cassel TN, Savolainen L, Helleday T (2008) Transcription-associated recombination is dependent on replication in Mammalian cells. Mol Cell Biol 28: 154-164.
8. Beletskii A, Bhagwat AS (1996) Transcription-induced mutations: increase in C to T mutations in the nontranscribed strand during transcription in Escherichia coli. Proc Natl Acad Sci USA 93:13919-13924. (Pubitemid 26424221)
9. Klapacz J, Bhagwat AS (2002) Transcription-dependent increase in multiple classes of base substitution mutations in Escherichia coli. J Bacteriol 184:6866-6872. (Pubitemid 36356122)
10. Beletskii A, Grigoriev A, Joyce S, Bhagwat AS (2000) Mutations induced by bacteriophage T7 RNA polymerase and their effects on the composition of the T7 genome. J Mol Biol 300:1057-1065.
11. Hendriks G, et al. (2008) Gene transcription increases DNA damage-induced mutagenesis in mammalian stem cells. DNA Repair (Amst) 7:1330-1339.
12. Hendriks G, et al. (2010) Transcription-dependent cytosine deamination is a novel mechanism in ultraviolet light-induced mutagenesis. Curr Biol 20:170-175.
13. Datta A, Jinks-Robertson S (1995) Association of increased spontaneous mutation rates with high levels of transcription in yeast. Science 268:1616-1619.
14. Lippert MJ, Freedman JA, Barber MA, Jinks-Robertson S (2004) Identification of a distinctive mutation spectrum associated with high levels of transcription in yeast. Mol Cell Biol 24:4801-4809.
15. Kim N, Abdulovic AL, Gealy R, Lippert MJ, Jinks-Robertson S (2007) Transcription-associated mutagenesis in yeast is directly proportional to the level of gene expression and influenced by the direction of DNA replication. DNA Repair (Amst) 6: 1285-1296. (Pubitemid 47238682)
16. Champoux JJ (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70:369-413.
17. Lynn RM, Bjornsti MA, Caron PR, Wang JC (1989) Peptide sequencing and site-directed mutagenesis identify tyrosine-727 as the active site tyrosine of Saccharomyces cerevisiae DNA topoisomerase I. Proc Natl Acad Sci USA 86:3559-3563.
18. Pouliot JJ, Yao KC, Robertson CA, Nash HA (1999) Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes. Science 286:552-555.
19. Liu C, Pouliot JJ, Nash HA (2002) Repair of topoisomerase I covalent complexes in the absence of the tyrosyl-DNA phosphodiesterase Tdp1. Proc Natl Acad Sci USA 99: 14970-14975.
20. Vance JR, Wilson TE (2002) Yeast Tdp1 and Rad1-Rad10 function as redundant pathways for repairing Top1 replicative damage. Proc Natl Acad Sci USA 99:13669-13674.
21. Deng C, Brown JA, You D, Brown JM (2005) Multiple endonucleases function to repair covalent topoisomerase I complexes in Saccharomyces cerevisiae. Genetics 170:591-600.
22. Nitiss J, Wang JC (1988) DNA topoisomerase-targeting antitumor drugs can be studied in yeast. Proc Natl Acad Sci USA 85:7501-7505.
23. Raymond AC, Staker BL, Burgin ABJ, Jr. (2005) Substrate specificity of tyrosyl-DNA phosphodiesterase I (Tdp1). J Biol Chem 280:22029-22035.
24. Kim N, Jinks-Robertson S (2009) dUTP incorporation into genomic DNA is linked to transcription in yeast. Nature 459:1150-1153.
25. Pourquier P, et al. (1997) Effects of uracil incorporation, DNA mismatches, and abasic sites on cleavage and religation activities of mammalian topoisomerase I. J Biol Chem 272:7792-7796.
26. Lebedeva N, Auffret Vander Kemp P, Bjornsti MA, Lavrik O, Boiteux S (2006) Trapping of DNA topoisomerase I on nick-containing DNA in cell free extracts of Saccharomyces cerevisiae. DNA Repair (Amst) 5:799-809.
27. Tuduri S, et al. (2009) Topoisomerase I suppresses genomic instability by preventing interference between replication and transcription. Nat Cell Biol 11:1315-1324.
28. Wu J, Liu LF (1997) Processing of topoisomerase I cleavable complexes into DNA damage by transcription. Nucleic Acids Res 25:4181-4186.
29. Lippert MJ, et al. (2011) Role for topoisomerase 1 in transcription-associated mutagenesis in yeast. Proc Natl Acad Sci USA 108:698-703.
30. Tanizawa A, Kohn KW, Pommier Y (1993) Induction of cleavage in topoisomerase I c-DNA by topoisomerase I enzymes from calf thymus and wheat germ in the presence and absence of camptothecin. Nucleic Acids Res 21:5157-5166.
31. Takashima H, et al. (2002) Mutation of TDP1, encoding a topoisomerase I-dependent DNA damage repair enzyme, in spinocerebellar ataxia with axonal neuropathy. Nat Genet 32:267-272.
32. Hirano R, et al. (2007) Spinocerebellar ataxia with axonal neuropathy: consequence of a Tdp1 recessive neomorphic mutation? EMBO J 26:4732-4743.
33. Cassier-Chauvat C, Fabre F (1991) A similar defect in UV-induced mutagenesis conferred by the rad6 and rad18 mutations of Saccharomyces cerevisiae. Mutat Res 254:247-253.
34. Longtine MS, et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
35. Bellí G, Garí E, Aldea M, Herrero E (1998) Functional analysis of yeast essential genes using a promoter-substitution cassette and the tetracycline-regulatable dual expression system. Yeast 14:1127-1138.
36. Whelan WL, Gocke E, Manney TR (1979) The CAN1 locus of Saccharomyces cerevisiae: fine-structure analysis and forward mutation rates. Genetics 91:35-51.
37. Lea DE, Coulson CA (1949) The distribution of the numbers of mutants in bacterial populations. J Genet 49:264-285.
38. Guglielmi B, Soutourina J, Esnault C, Werner M (2007) TFIIS elongation factor and Mediator act in conjunction during transcription initiation in vivo. Proc Natl Acad Sci USA 104:16062-16067.