Nascent RNA folding mitigates transcriptionassociated mutagenesis

Genome Research

Volumn 26, Issue 1, 2016, Pages 50-59

  Chen, Xiaoshu ^a   Yang, Jian Rong ^a   Zhang, Jianzhi ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA A; RIBONUCLEASE; RNA; AMINO ACID TRANSPORTER; CAN1 PROTEIN, S CEREVISIAE; FUNGAL DNA; RIBONUCLEASE H; RIBONUCLEASE HI; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSCRIPTOME;

ARTICLE; DNA POLYMORPHISM; DNA RNA HYBRIDIZATION; DNA STRAND; DNA TEMPLATE; GENOME; HUMAN; MUTAGENESIS; MUTATION ACCUMULATION; MUTATION RATE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; REPORTER GENE; RNA FOLDING; RNA TRANSCRIPTION; BIOLOGY; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETIC DATABASE; GENETIC TRANSCRIPTION; GENETICS; GENOME-WIDE ASSOCIATION STUDY; METABOLISM; MUTATION; SACCHAROMYCES CEREVISIAE; SINGLE NUCLEOTIDE POLYMORPHISM;

AMINO ACID TRANSPORT SYSTEMS, BASIC; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; DNA, FUNGAL; GENE EXPRESSION REGULATION, FUNGAL; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MUTAGENESIS; MUTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; RIBONUCLEASE H; RNA FOLDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84956698688     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.195164.115     Document Type: Article

References (58)

1. Aguilera A,García-Muse T 2012 R loops: from transcription byproducts to threats to genome stability. Mol Cell 46 115-124.
2. Braberg H, Jin H, Moehl e EA, Chan YA, Wang S, Shales M, Benschop JJ, Morris JH, Qiu C, Hu F, et al. 2013. From structure to systems: high-resolution, quantitative genetic analysis of RNA polymerase II. Cell 154: 775-788.
3. Bürger R, Willensdorfer M, Nowak MA. 2006.Whyare phenotypic mutation rates much higher than genotypic mutation rates? Genetics 172: 197-206.
4. Chan YA, Aristizabal MJ, Lu PY, Luo Z, Hamza A, Kobor MS, Stirling PC, Hieter P. 2014. Genome-wide profiling of yeast DNA:RNA hybrid prone sites with DRIP-chip. PLoS Genet 10: e1004288.
5. Chen X, Zhang J. 2013. No gene-specific optimization of mutation rate in Escherichia coli. Mol Biol Evol 30: 1559-1562.
6. Chen X, Zhang J. 2014. Yeast mutation accumulation experiment supports elevated mutation rates at highly transcribed sites. Proc Natl Acad Sci 111: E4062.
7. Chen X, Chen Z, Chen H, Su Z, Yang J, Lin F, Shi S, He X. 2012. Nucleosomes suppress spontaneous mutations base-specifically in eukaryotes. Science 335: 1235-1238.
8. Churchman LS, Weissman JS. 2011. Nascent transcript sequencing visualizes transcription at nucleotide resolution. Nature 469: 368-373.
9. Core LJ, Waterfall JJ, Lis JT. 2008. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322: 1845-1848.
10. Cunningham F, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho-Silva D, Clapham P, Coates G, Fitzgerald S, et al. 2015. Ensembl 2015. Nucleic Acids Res 43(Database issue): D662-D669.
11. Drummond DA, Wilke CO. 2008. Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134: 341-352.
12. El Hage A, Webb S, Kerr A, Tollervey D. 2014. Genome-wide distribution of RNA-DNA h ybrids identifies RNase H targets in tRNA genes, retrotransposons and mitochondria. PLoS Genet 10: e1004716.
13. Fares MA, Keane OM, Toft C, Carretero-Paulet L, Jones GW. 2013. The roles of whole-genome and small-scale duplications in the functional specialization of Saccharomyces cerevisiae genes. PLoS Genet 9: e1003176.
14. Ginno PA, Lim YW, Lott PL, Korf I, Chédin F. 2013. GC skew at the 5? and 3' ends of human genes links R-loop formation to epigenetic regulation and transcription termination. Genome Res 23: 1590-1600.
15. Gong J. 2008. " A systematic screen of the Saccharomyces cerevisiae deletion mutant collection for novel genes required for DNA damage-induced mutagenesis. " PhD thesis, University of North Texas Health Science Center, Fort Worth.
16. Goodman MF, Woodgate R. 2013. Translesion DNA polymerases. Cold Spring Harb Perspect Biol 5: a010363.
17. Hanawalt PC, Spivak G. 2008. Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol 9: 958-970.
18. Hodgkinson A, Eyre-Walker A. 2011. Variation in the mutation rate across mammalian genomes. Nat Rev Genet 12: 756-766.
19. Hofacker IL. 2009. RNA secondary structure analysis using the Vienna RNA package. Curr Protoc Bioinformatics Chapter 12: Unit12.2.
20. The International HapMap 3 Consortium, Altshuler DM, Gibbs RA, Peltonen L, Altshuler DM, Gibbs RA, Peltonen L, Dermitzakis E, Schaffner SF, Yu F, et al. 2010. Integrating common and rare genetic variation in diverse human populations. Nature 467: 52-58.
21. Kertesz M, Wan Y, Mazor E, Rinn JL, Nutter RC, Chang HY, Segal E. 2010. Genome-wide measurement of RNA secondary structure in yeast. Nature 467: 103-107.
22. Kim N,Jinks-Robertson S 2012 Transcription as a source of genome instability. Nat Rev Genet 13 204-214.
23. Kimura M. 1967. On the evolutionary adjustment of spontaneous mutation rates. Genet Res 9: 23-34.
24. Kimura M. 1983. The neutral theory of molecular evolution. Cambridge University Press, Cambridge, UK.
25. Koren A, Soifer I, Barkai N. 2010. MRC1-dependent scaling of the budding yeast DNA replication timing program. Genome Res 20: 781-790.
26. Lan g GI, Murray AW. 2011. Mutation rates across budding yeast Chromosome VI are correlated with replication timing. Genome Biol Evol 3: 799-811.
27. Lange SJ, Maticzka D, Mö hl M, Gagnon JN, Brown CM, Backofen R. 2012. Global or local? Predicting secondary structure and accessibility in mRNAs. Nucleic Acids Res 40: 5215-5226.
28. Lesnik EA, Freier SM. 1995. Relative thermodynamic stability of DNA, RNA, and DNA:RNA hybrid duplexes: relationship with base composition and structure. Biochemistry 34: 10807-10815.
29. Li R, Li Y, Kristiansen K, Wang J. 2008. SOAP: short oligonucleotide alignment program. Bioinformatics 24: 713-714.
30. Lind PA, Andersson DI. 2008. Whole-genome mutational biases in bacteria. Proc Natl Acad Sci 105: 17878-17883.
31. Lippert MJ, Kim N, Cho JE, Larson RP, Schoenly NE, O'Shea SH, Jinks-Robertson S. 2011. Role for topoisomerase 1 in transcription-Associated mutagenesis in yeast. Proc Natl Acad Sci 108: 698-703.
32. Lorenz R, Hofacker IL, Bernhart SH. 2012. Folding RNA/DNA hybrid duplexes. Bioinformatics 28: 2530-2531.
33. Lynch M. 2010a. Evolution of the mutation rate. Trends Genet 26: 345-352.
34. Lynch M. 2010b. Rate, molecular spectrum, and consequences of human mutation. Proc Natl Acad Sci 107: 961-968.
35. Lynch M. 2011. The lower bound to the evolution of mutation rates. Genome Biol Evol 3: 1107-1118.
36. Lynch M, Sung W, Morris K, Coffey N, Landry CR, Dopman EB, Dickinson WJ, Okamoto K, Kulkarni S, Hartl DL, et al. 2008. A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc Natl Acad Sci 105: 9272-9277.
37. Mathews DH, Disney MD, Childs JL, Schroeder SJ, Zuker M, Turner DH. 2004. Incorporating chemical modification constraints into a dynamic pr ogramming algorithm for prediction of RNA secondary structure. Proc Natl Acad Sci 101: 7287-7292.
38. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. 2008. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.
39. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M. 2008. The transcriptional landscape of the yeast genome defined by RNA se quencing. Science 320: 1344-1349.
40. Pan T, Sosnick T. 2006. RNA folding during transcription. Annu Rev Biophys Biomol Struct 35: 161-175.
41. Park C, Qian W, Zhang J. 201 2. Genomic evidence for elevated mutation rates in highly expressed genes. EMBO Rep 13: 1123-1129.
42. Park C, Chen X, Yang JR, Zhang J. 2013. Differential requirements formRNA folding partially explain why highly expressed proteins evolve slowly. Proc Natl Acad Sci 110: E678-E686.
43. SantaLucia J Jr., Hicks D. 2004. The thermodynamics of DNA structural motifs. Annu Rev Biophys Biomol Struct 33: 415-440.
44. Stamatoyannopoulos JA,Adzhubei I,Thurman RE,Kryukov GV,Mirkin SM,Sunyaev SR. 2009 Human mutation rate associated with DNA replication timing Nat Genet, 41, 393-395.
45. Takahashi T, Burguiere-Slezak G, Van der Kemp PA, Boiteux S. 2011. Topoisomerase 1 provokes the formation of short deletions in repeated sequences upon high transcription in Saccharomyces cerevisiae. Proc Natl Acad Sci 1 08: 692-697.
46. Takahata N. 1993. Allelic genealogy and human evolution. Mol Biol Evol 10: 2-22.
47. Turner DH, Mathews DH. 2010. NNDB: the nearest neighbor parameter database for predicting stability of nucleic acid secondary structure. Nucleic Acids Res 38(Database issue): D280-D282.
48. Wagner A. 2005. Ener gy constraints on the evolution of gene expression. Mol Biol Evol 22: 1365-1374.
49. Wahba L, Amon JD, Koshland D, Vuica-Ross M. 2011. RNaseHand multiple RNA biogenesis factors cooperate to prevent RNA:DNA hybrids from generating genome instability. Mol Cell 44: 978-988.
50. Wan Y, Qu K, Zhang QC, Flynn RA, Manor O, Ouyang Z, Zhang J, Spitale RC, Snyder MP, Segal E, et al. 2014. Lands cape and variation of RNA secondary structure across the human transcriptome. Nature 505: 706-709.
51. Weiner A, Hughes A, Yassour M, Rando OJ, Friedman N. 2010. High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res 20: 90-100.
52. Xia X. 2010. The effect of probe length and GC% on microarray signal intensity: characterizing the functional relationship. Int J Syst Synth Biol 1: 171-183.
53. Yang JR, Liao BY, Zhuang SM, Zhang J. 2012. Protein misinteraction avoidance causes highly expressed proteins to evolve slowly. Proc Natl Acad Sci 109: E831-E840.
54. Yang JR, Chen X, Zhang J. 2014. Codon-by-codon modulation of translational speed and accuracy via mRNA folding. PLoS Biol 12: e1001910.
55. Zamft B, Bintu L, Ishibashi T, Bustamante C. 2012. Nascent RNA structure modulates the transcriptional dynamics of RNA polymerases. Proc Natl Acad Sci 109: 8948-8953.
56. Zhang J, He X. 2005. Significant impact of protein dispensability on the instantaneous rate of protein evolution. Mol Biol Evol 22: 1147-1155.
57. Zhang J, Yang JR. 2015. Determinants of the rate of protein sequence evolution. Nat Rev Genet 16: 409-420.
58. Zur H, Tuller T. 2012. Str ong association between mRNA folding strength and protein abundance in S. cerevisiae. EMBO Rep 13: 272-277.