Advertisement

Coordinating Replication with Transcription

  • Yathish Jagadheesh AcharEmail author
  • Marco Foiani
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1042)

Abstract

DNA topological transitions occur when replication forks encounter other DNA transactions such as transcription. Failure in resolving such conflicts leads to generation of aberrant replication and transcription intermediates that might have adverse effects on genome stability. Cells have evolved numerous surveillance mechanisms to avoid, tolerate, and resolve such replication-transcription conflicts. Defects or non-coordination in such cellular mechanisms might have catastrophic effect on cell viability. In this chapter, we review consequences of replication encounters with transcription and its associated events, topological challenges, and how these inevitable conflicts alter the genome structure and functions.

Keywords

DNA replication Transcription Topology Topoisomerase Chromatin structure Genome instability RNA:DNA hybrids 

Notes

Acknowledgments

We thank Ghadeer Shubassi for helping with manuscript preparations and all the MF-lab members for discussions and valuable inputs. Research in MF-lab is supported by grants from the Associazione Italiana per la Ricerca sul Cancro (AIRC), the European Union and Telethon-Italy. YJA is supported by the European Community’s Seventh Framewok Programme under Grant agreement no.246549 – Train 2009.

References

  1. Aguilera A (2002) The connection between transcription and genomic instability. EMBO J 21(3):195–201. https://doi.org/10.1093/emboj/21.3.195 PubMedPubMedCentralCrossRefGoogle Scholar
  2. Aguilera A, Garcia-Muse T (2012) R loops: from transcription byproducts to threats to genome stability. Mol Cell 46(2):115–124. https://doi.org/10.1016/j.molcel.2012.04.009 PubMedCrossRefGoogle Scholar
  3. Alzu A, Bermejo R, Begnis M, Lucca C, Piccini D, Carotenuto W, Saponaro M, Brambati A, Cocito A, Foiani M, Liberi G (2012) Senataxin associates with replication forks to protect fork integrity across RNA-polymerase-II-transcribed genes. Cell 151(4):835–846. https://doi.org/10.1016/j.cell.2012.09.041 PubMedPubMedCentralCrossRefGoogle Scholar
  4. Ansari A, Hampsey M (2005) A role for the CPF 3′-end processing machinery in RNAP II-dependent gene looping. Genes Dev 19(24):2969–2978. https://doi.org/10.1101/gad.1362305 PubMedPubMedCentralCrossRefGoogle Scholar
  5. Artsimovitch I, Landick R (2000) Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals. Proc Natl Acad Sci U S A 97(13):7090–7095PubMedPubMedCentralCrossRefGoogle Scholar
  6. Azorin F, Nordheim A, Rich A (1983) Formation of Z-DNA in negatively supercoiled plasmids is sensitive to small changes in salt concentration within the physiological range. EMBO J 2(5):649–655PubMedPubMedCentralGoogle Scholar
  7. 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(6):722–734. https://doi.org/10.1016/j.molcel.2009.05.022 PubMedPubMedCentralCrossRefGoogle Scholar
  8. Bacolla A, Collins JR, Gold B, Chuzhanova N, Yi M, Stephens RM, Stefanov S, Olsh A, Jakupciak JP, Dean M, Lempicki RA, Cooper DN, Wells RD (2006) Long homopurine*homopyrimidine sequences are characteristic of genes expressed in brain and the pseudoautosomal region. Nucleic Acids Res 34(9):2663–2675. https://doi.org/10.1093/nar/gkl354 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Baranello L, Wojtowicz D, Cui K, Devaiah BN, Chung HJ, Chan-Salis KY, Guha R, Wilson K, Zhang X, Zhang H, Piotrowski J, Thomas CJ, Singer DS, Pugh BF, Pommier Y, Przytycka TM, Kouzine F, Lewis BA, Zhao K, Levens D (2016) RNA polymerase II regulates topoisomerase 1 activity to favor efficient transcription. Cell 165(2):357–371. https://doi.org/10.1016/j.cell.2016.02.036 PubMedPubMedCentralCrossRefGoogle Scholar
  10. Barlow JH, Faryabi RB, Callen E, Wong N, Malhowski A, Chen HT, Gutierrez-Cruz G, Sun HW, McKinnon P, Wright G, Casellas R, Robbiani DF, Staudt L, Fernandez-Capetillo O, Nussenzweig A (2013) Identification of early replicating fragile sites that contribute to genome instability. Cell 152(3):620–632. https://doi.org/10.1016/j.cell.2013.01.006 PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bates AD, Maxwell A (2005) DNA topology. Oxford University Press, OxfordGoogle Scholar
  12. Bedinger P, Hochstrasser M, Jongeneel CV, Alberts BM (1983) Properties of the T4 bacteriophage DNA replication apparatus: the T4 dda DNA helicase is required to pass a bound RNA polymerase molecule. Cell 34(1):115–123PubMedCrossRefGoogle Scholar
  13. Bermejo R, Doksani Y, Capra T, Katou YM, Tanaka H, Shirahige K, Foiani M (2007) Top1- and Top2-mediated topological transitions at replication forks ensure fork progression and stability and prevent DNA damage checkpoint activation. Genes Dev 21(15):1921–1936. https://doi.org/10.1101/gad.432107 PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bermejo R, Capra T, Gonzalez-Huici V, Fachinetti D, Cocito A, Natoli G, Katou Y, Mori H, Kurokawa K, Shirahige K, Foiani M (2009) Genome-organizing factors Top2 and Hmo1 prevent chromosome fragility at sites of S phase transcription. Cell 138(5):870–884. https://doi.org/10.1016/j.cell.2009.06.022 PubMedCrossRefGoogle Scholar
  15. Bermejo R, Capra T, Jossen R, Colosio A, Frattini C, Carotenuto W, Cocito A, Doksani Y, Klein H, Gomez-Gonzalez B, Aguilera A, Katou Y, Shirahige K, Foiani M (2011) The replication checkpoint protects fork stability by releasing transcribed genes from nuclear pores. Cell 146(2):233–246. https://doi.org/10.1016/j.cell.2011.06.033 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bermejo R, Lai MS, Foiani M (2012) Preventing replication stress to maintain genome stability: resolving conflicts between replication and transcription. Mol Cell 45(6):710–718. https://doi.org/10.1016/j.molcel.2012.03.001 PubMedCrossRefGoogle Scholar
  17. Bermudez I, Garcia-Martinez J, Perez-Ortin JE, Roca J (2010) A method for genome-wide analysis of DNA helical tension by means of psoralen-DNA photobinding. Nucleic Acids Res 38(19):e182. https://doi.org/10.1093/nar/gkq687 PubMedPubMedCentralCrossRefGoogle Scholar
  18. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, Barretina J, Boehm JS, Dobson J, Urashima M, Mc Henry KT, Pinchback RM, Ligon AH, Cho YJ, Haery L, Greulich H, Reich M, Winckler W, Lawrence MS, Weir BA, Tanaka KE, Chiang DY, Bass AJ, Loo A, Hoffman C, Prensner J, Liefeld T, Gao Q, Yecies D, Signoretti S, Maher E, Kaye FJ, Sasaki H, Tepper JE, Fletcher JA, Tabernero J, Baselga J, Tsao MS, Demichelis F, Rubin MA, Janne PA, Daly MJ, Nucera C, Levine RL, Ebert BL, Gabriel S, Rustgi AK, Antonescu CR, Ladanyi M, Letai A, Garraway LA, Loda M, Beer DG, True LD, Okamoto A, Pomeroy SL, Singer S, Golub TR, Lander ES, Getz G, Sellers WR, Meyerson M (2010) The landscape of somatic copy-number alteration across human cancers. Nature 463(7283):899–905. https://doi.org/10.1038/nature08822 PubMedPubMedCentralCrossRefGoogle Scholar
  19. Betous R, Rey L, Wang G, Pillaire MJ, Puget N, Selves J, Biard DS, Shin-ya K, Vasquez KM, Cazaux C, Hoffmann JS (2009) Role of TLS DNA polymerases eta and kappa in processing naturally occurring structured DNA in human cells. Mol Carcinog 48(4):369–378. https://doi.org/10.1002/mc.20509 PubMedPubMedCentralCrossRefGoogle Scholar
  20. Bhatia V, Barroso SI, Garcia-Rubio ML, Tumini E, Herrera-Moyano E, Aguilera A (2014) BRCA2 prevents R-loop accumulation and associates with TREX-2 mRNA export factor PCID2. Nature 511(7509):362–365. https://doi.org/10.1038/nature13374 PubMedCrossRefGoogle Scholar
  21. Biffi G, Tannahill D, McCafferty J, Balasubramanian S (2013) Quantitative visualization of DNA G-quadruplex structures in human cells. Nat Chem 5(3):182–186. https://doi.org/10.1038/nchem.1548 PubMedPubMedCentralCrossRefGoogle Scholar
  22. Bignell GR, Greenman CD, Davies H, Butler AP, Edkins S, Andrews JM, Buck G, Chen L, Beare D, Latimer C, Widaa S, Hinton J, Fahey C, Fu B, Swamy S, Dalgliesh GL, Teh BT, Deloukas P, Yang F, Campbell PJ, Futreal PA, Stratton MR (2010) Signatures of mutation and selection in the cancer genome. Nature 463(7283):893–898. https://doi.org/10.1038/nature08768 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Blattner FR, Plunkett G 3rd, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 277(5331):1453–1462PubMedCrossRefGoogle Scholar
  24. Boubakri H, de Septenville AL, Viguera E, Michel B (2010) The helicases DinG, Rep and UvrD cooperate to promote replication across transcription units in vivo. EMBO J 29(1):145–157. https://doi.org/10.1038/emboj.2009.308 PubMedCrossRefGoogle Scholar
  25. Breier AM, Weier HU, Cozzarelli NR (2005) Independence of replisomes in Escherichia coli chromosomal replication. Proc Natl Acad Sci U S A 102(11):3942–3947. https://doi.org/10.1073/pnas.0500812102 PubMedPubMedCentralCrossRefGoogle Scholar
  26. Brewer BJ (1988) When polymerases collide: replication and the transcriptional organization of the E. coli chromosome. Cell 53(5):679–686PubMedCrossRefGoogle Scholar
  27. Brewer BJ, Fangman WL (1988) A replication fork barrier at the 3′ end of yeast ribosomal RNA genes. Cell 55(4):637–643PubMedCrossRefGoogle Scholar
  28. Brill SJ, DiNardo S, Voelkel-Meiman K, Sternglanz R (1987) Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA. Nature 326(6111):414–416. https://doi.org/10.1038/326414a0 PubMedCrossRefGoogle Scholar
  29. Burns LT, Wente SR (2014) From hypothesis to mechanism: uncovering nuclear pore complex links to gene expression. Mol Cell Biol 34(12):2114–2120. https://doi.org/10.1128/MCB.01730-13 PubMedPubMedCentralCrossRefGoogle Scholar
  30. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, Kodzius R, Shimokawa K, Bajic VB, Brenner SE, Batalov S, Forrest AR, Zavolan M, Davis MJ, Wilming LG, Aidinis V, Allen JE, Ambesi-Impiombato A, Apweiler R, Aturaliya RN, Bailey TL, Bansal M, Baxter L, Beisel KW, Bersano T, Bono H, Chalk AM, Chiu KP, Choudhary V, Christoffels A, Clutterbuck DR, Crowe ML, Dalla E, Dalrymple BP, de Bono B, Della Gatta G, di Bernardo D, Down T, Engstrom P, Fagiolini M, Faulkner G, Fletcher CF, Fukushima T, Furuno M, Futaki S, Gariboldi M, Georgii-Hemming P, Gingeras TR, Gojobori T, Green RE, Gustincich S, Harbers M, Hayashi Y, Hensch TK, Hirokawa N, Hill D, Huminiecki L, Iacono M, Ikeo K, Iwama A, Ishikawa T, Jakt M, Kanapin A, Katoh M, Kawasawa Y, Kelso J, Kitamura H, Kitano H, Kollias G, Krishnan SP, Kruger A, Kummerfeld SK, Kurochkin IV, Lareau LF, Lazarevic D, Lipovich L, Liu J, Liuni S, McWilliam S, Madan Babu M, Madera M, Marchionni L, Matsuda H, Matsuzawa S, Miki H, Mignone F, Miyake S, Morris K, Mottagui-Tabar S, Mulder N, Nakano N, Nakauchi H, Ng P, Nilsson R, Nishiguchi S, Nishikawa S, Nori F, Ohara O, Okazaki Y, Orlando V, Pang KC, Pavan WJ, Pavesi G, Pesole G, Petrovsky N, Piazza S, Reed J, Reid JF, Ring BZ, Ringwald M, Rost B, Ruan Y, Salzberg SL, Sandelin A, Schneider C, Schonbach C, Sekiguchi K, Semple CA, Seno S, Sessa L, Sheng Y, Shibata Y, Shimada H, Shimada K, Silva D, Sinclair B, Sperling S, Stupka E, Sugiura K, Sultana R, Takenaka Y, Taki K, Tammoja K, Tan SL, Tang S, Taylor MS, Tegner J, Teichmann SA, Ueda HR, van Nimwegen E, Verardo R, Wei CL, Yagi K, Yamanishi H, Zabarovsky E, Zhu S, Zimmer A, Hide W, Bult C, Grimmond SM, Teasdale RD, Liu ET, Brusic V, Quackenbush J, Wahlestedt C, Mattick JS, Hume DA, Kai C, Sasaki D, Tomaru Y, Fukuda S, Kanamori-Katayama M, Suzuki M, Aoki J, Arakawa T, Iida J, Imamura K, Itoh M, Kato T, Kawaji H, Kawagashira N, Kawashima T, Kojima M, Kondo S, Konno H, Nakano K, Ninomiya N, Nishio T, Okada M, Plessy C, Shibata K, Shiraki T, Suzuki S, Tagami M, Waki K, Watahiki A, Okamura-Oho Y, Suzuki H, Kawai J, Hayashizaki Y, Consortium F, Group RGER, Genome Science G (2005) The transcriptional landscape of the mammalian genome. Science 309(5740):1559–1563. https://doi.org/10.1126/science.1112014
  31. Casolari JM, Brown CR, Komili S, West J, Hieronymus H, Silver PA (2004) Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117(4):427–439PubMedCrossRefGoogle Scholar
  32. Champoux JJ (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70:369–413. https://doi.org/10.1146/annurev.biochem.70.1.369 PubMedCrossRefGoogle Scholar
  33. Champoux JJ, Been MD (1980) Topoisomerases and the swivel problem. In: Alberts B (ed) Mechanistic studies of DNA replication and genetic recombination. Academic, New York, pp 809–815CrossRefGoogle Scholar
  34. Cheung AC, Cramer P (2011) Structural basis of RNA polymerase II backtracking, arrest and reactivation. Nature 471(7337):249–253. https://doi.org/10.1038/nature09785 PubMedCrossRefGoogle Scholar
  35. Cook PR (1999) The organization of replication and transcription. Science 284(5421):1790–1795PubMedCrossRefGoogle Scholar
  36. Dalgaard JZ, Klar AJ (2001) A DNA replication-arrest site RTS1 regulates imprinting by determining the direction of replication at mat1 in S. pombe. Genes Dev 15(16):2060–2068. https://doi.org/10.1101/gad.200801 PubMedPubMedCentralCrossRefGoogle Scholar
  37. Datta A, Jinks-Robertson S (1995) Association of increased spontaneous mutation rates with high levels of transcription in yeast. Science 268(5217):1616–1619PubMedCrossRefGoogle Scholar
  38. David L, Huber W, Granovskaia M, Toedling J, Palm CJ, Bofkin L, Jones T, Davis RW, Steinmetz LM (2006) A high-resolution map of transcription in the yeast genome. Proc Natl Acad Sci U S A 103(14):5320–5325. https://doi.org/10.1073/pnas.0601091103 PubMedPubMedCentralCrossRefGoogle Scholar
  39. Deem A, Keszthelyi A, Blackgrove T, Vayl A, Coffey B, Mathur R, Chabes A, Malkova A (2011) Break-induced replication is highly inaccurate. PLoS Biol 9(2):e1000594. https://doi.org/10.1371/journal.pbio.1000594 PubMedPubMedCentralCrossRefGoogle Scholar
  40. Deshpande AM, Newlon CS (1996) DNA replication fork pause sites dependent on transcription. Science 272(5264):1030–1033PubMedCrossRefGoogle Scholar
  41. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485(7398):376–380. https://doi.org/10.1038/nature11082 PubMedPubMedCentralCrossRefGoogle Scholar
  42. Dul JL, Drexler H (1988) Transcription stimulates recombination. I. Specialized transduction of Escherichia coli by lambda trp phages. Virology 162(2):466–470PubMedCrossRefGoogle Scholar
  43. Duquette ML, Handa P, Vincent JA, Taylor AF, Maizels N (2004) Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA. Genes Dev 18(13):1618–1629. https://doi.org/10.1101/gad.1200804 PubMedPubMedCentralCrossRefGoogle Scholar
  44. Dutrow N, Nix DA, Holt D, Milash B, Dalley B, Westbroek E, Parnell TJ, Cairns BR (2008) Dynamic transcriptome of Schizosaccharomyces pombe shown by RNA-DNA hybrid mapping. Nat Genet 40(8):977–986. https://doi.org/10.1038/ng.196 PubMedPubMedCentralCrossRefGoogle Scholar
  45. Dutta D, Shatalin K, Epshtein V, Gottesman ME, Nudler E (2011) Linking RNA polymerase backtracking to genome instability in E. coli. Cell 146(4):533–543. https://doi.org/10.1016/j.cell.2011.07.034 PubMedPubMedCentralCrossRefGoogle Scholar
  46. El Hage A, French SL, Beyer AL, Tollervey D (2010) Loss of Topoisomerase I leads to R-loop-mediated transcriptional blocks during ribosomal RNA synthesis. Genes Dev 24(14):1546–1558. https://doi.org/10.1101/gad.573310 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Elias-Arnanz M, Salas M (1997) Bacteriophage phi29 DNA replication arrest caused by codirectional collisions with the transcription machinery. EMBO J 16(18):5775–5783. https://doi.org/10.1093/emboj/16.18.5775 PubMedPubMedCentralCrossRefGoogle Scholar
  48. Elias-Arnanz M, Salas M (1999) Resolution of head-on collisions between the transcription machinery and bacteriophage phi29 DNA polymerase is dependent on RNA polymerase translocation. EMBO J 18(20):5675–5682. https://doi.org/10.1093/emboj/18.20.5675 PubMedPubMedCentralCrossRefGoogle Scholar
  49. Epshtein V, Toulme F, Rahmouni AR, Borukhov S, Nudler E (2003) Transcription through the roadblocks: the role of RNA polymerase cooperation. EMBO J 22(18):4719–4727. https://doi.org/10.1093/emboj/cdg452 PubMedPubMedCentralCrossRefGoogle Scholar
  50. Epshtein V, Kamarthapu V, McGary K, Svetlov V, Ueberheide B, Proshkin S, Mironov A, Nudler E (2014) UvrD facilitates DNA repair by pulling RNA polymerase backwards. Nature 505(7483):372–377. https://doi.org/10.1038/nature12928 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Fachinetti D, Bermejo R, Cocito A, Minardi S, Katou Y, Kanoh Y, Shirahige K, Azvolinsky A, Zakian VA, Foiani M (2010) Replication termination at eukaryotic chromosomes is mediated by Top2 and occurs at genomic loci containing pausing elements. Mol Cell 39(4):595–605. https://doi.org/10.1016/j.molcel.2010.07.024 PubMedPubMedCentralCrossRefGoogle Scholar
  52. Frank-Kamenetskii MD, Mirkin SM (1995) Triplex DNA structures. Annu Rev Biochem 64:65–95. https://doi.org/10.1146/annurev.bi.64.070195.000433 PubMedCrossRefGoogle Scholar
  53. French S (1992) Consequences of replication fork movement through transcription units in vivo. Science 258(5086):1362–1365PubMedCrossRefGoogle Scholar
  54. Gan W, Guan Z, Liu J, Gui T, Shen K, Manley JL, Li X (2011) R-loop-mediated genomic instability is caused by impairment of replication fork progression. Genes Dev 25(19):2041–2056. https://doi.org/10.1101/gad.17010011
  55. Ganesan A, Spivak G, Hanawalt PC (2012) Transcription-coupled DNA repair in prokaryotes. Prog Mol Biol Transl Sci 110:25–40. https://doi.org/10.1016/B978-0-12-387665-2.00002-X PubMedCrossRefGoogle Scholar
  56. Garcia-Muse T, Aguilera A (2016) Transcription-replication conflicts: how they occur and how they are resolved. Nat Rev Mol Cell Biol 17(9):553–563. https://doi.org/10.1038/nrm.2016.88 PubMedCrossRefGoogle Scholar
  57. Gerber JK, Gogel E, Berger C, Wallisch M, Muller F, Grummt I, Grummt F (1997) Termination of mammalian rDNA replication: polar arrest of replication fork movement by transcription termination factor TTF-I. Cell 90(3):559–567PubMedCrossRefGoogle Scholar
  58. Gilbert DM (2002) Replication timing and transcriptional control: beyond cause and effect. Curr Opin Cell Biol 14(3):377–383PubMedCrossRefGoogle Scholar
  59. Glover TW, Berger C, Coyle J, Echo B (1984) DNA polymerase alpha inhibition by aphidicolin induces gaps and breaks at common fragile sites in human chromosomes. Hum Genet 67(2):136–142PubMedCrossRefGoogle Scholar
  60. Gomez-Gonzalez B, Felipe-Abrio I, Aguilera A (2009) The S-phase checkpoint is required to respond to R-loops accumulated in THO mutants. Mol Cell Biol 29(19):5203–5213. https://doi.org/10.1128/MCB.00402-09 PubMedPubMedCentralCrossRefGoogle Scholar
  61. Gomez-Gonzalez B, Garcia-Rubio M, Bermejo R, Gaillard H, Shirahige K, Marin A, Foiani M, Aguilera A (2011) Genome-wide function of THO/TREX in active genes prevents R-loop-dependent replication obstacles. EMBO J 30(15):3106–3119. https://doi.org/10.1038/emboj.2011.206 PubMedPubMedCentralCrossRefGoogle Scholar
  62. Gotta SL, Miller OL Jr, French SL (1991) rRNA transcription rate in Escherichia coli. J Bacteriol 173(20):6647–6649PubMedPubMedCentralCrossRefGoogle Scholar
  63. Gottipati P, Cassel TN, Savolainen L, Helleday T (2008) Transcription-associated recombination is dependent on replication in Mammalian cells. Mol Cell Biol 28(1):154–164. https://doi.org/10.1128/MCB.00816-07 PubMedCrossRefGoogle Scholar
  64. Gray LT, Vallur AC, Eddy J, Maizels N (2014) G quadruplexes are genomewide targets of transcriptional helicases XPB and XPD. Nat Chem Biol 10(4):313–318. https://doi.org/10.1038/nchembio.1475 PubMedPubMedCentralCrossRefGoogle Scholar
  65. Greenfeder SA, Newlon CS (1992) Replication forks pause at yeast centromeres. Mol Cell Biol 12(9):4056–4066PubMedPubMedCentralCrossRefGoogle Scholar
  66. Guy L, Roten CA (2004) Genometric analyses of the organization of circular chromosomes: a universal pressure determines the direction of ribosomal RNA genes transcription relative to chromosome replication. Gene 340(1):45–52. https://doi.org/10.1016/j.gene.2004.06.056 PubMedCrossRefGoogle Scholar
  67. Guy CP, Atkinson J, Gupta MK, Mahdi AA, Gwynn EJ, Rudolph CJ, Moon PB, van Knippenberg IC, Cadman CJ, Dillingham MS, Lloyd RG, McGlynn P (2009) Rep provides a second motor at the replisome to promote duplication of protein-bound DNA. Mol Cell 36(4):654–666. https://doi.org/10.1016/j.molcel.2009.11.009 PubMedPubMedCentralCrossRefGoogle Scholar
  68. Gwynn EJ, Smith AJ, Guy CP, Savery NJ, McGlynn P, Dillingham MS (2013) The conserved C-terminus of the PcrA/UvrD helicase interacts directly with RNA polymerase. PLoS One 8(10):e78141. https://doi.org/10.1371/journal.pone.0078141 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Ha SC, Lowenhaupt K, Rich A, Kim YG, Kim KK (2005) Crystal structure of a junction between B-DNA and Z-DNA reveals two extruded bases. Nature 437(7062):1183–1186. https://doi.org/10.1038/nature04088 PubMedCrossRefGoogle Scholar
  70. Hansel-Hertsch R, Beraldi D, Lensing SV, Marsico G, Zyner K, Parry A, Di Antonio M, Pike J, Kimura H, Narita M, Tannahill D, Balasubramanian S (2016) G-quadruplex structures mark human regulatory chromatin. Nat Genet 48(10):1267–1272. https://doi.org/10.1038/ng.3662 PubMedCrossRefGoogle Scholar
  71. Harada Y, Ohara O, Takatsuki A, Itoh H, Shimamoto N, Kinosita K Jr (2001) Direct observation of DNA rotation during transcription by Escherichia coli RNA polymerase. Nature 409(6816):113–115. https://doi.org/10.1038/35051126 PubMedCrossRefGoogle Scholar
  72. Hatchi E, Skourti-Stathaki K, Ventz S, Pinello L, Yen A, Kamieniarz-Gdula K, Dimitrov S, Pathania S, McKinney KM, Eaton ML, Kellis M, Hill SJ, Parmigiani G, Proudfoot NJ, Livingston DM (2015) BRCA1 recruitment to transcriptional pause sites is required for R-loop-driven DNA damage repair. Mol Cell 57(4):636–647. https://doi.org/10.1016/j.molcel.2015.01.011 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Helmrich A, Ballarino M, Tora L (2011) Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol Cell 44(6):966–977. https://doi.org/10.1016/j.molcel.2011.10.013 PubMedCrossRefGoogle Scholar
  74. Henderson A, Wu Y, Huang YC, Chavez EA, Platt J, Johnson FB, Brosh RM Jr, Sen D, Lansdorp PM (2014) Detection of G-quadruplex DNA in mammalian cells. Nucleic Acids Res 42(2):860–869. https://doi.org/10.1093/nar/gkt957 PubMedCrossRefGoogle Scholar
  75. Herman RK, Dworkin NB (1971) Effect of gene induction on the rate of mutagenesis by ICR-191 in Escherichia coli. J Bacteriol 106(2):543–550PubMedPubMedCentralGoogle Scholar
  76. Hiratani I, Ryba T, Itoh M, Yokochi T, Schwaiger M, Chang CW, Lyou Y, Townes TM, Schubeler D, Gilbert DM (2008) Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol 6(10):e245. https://doi.org/10.1371/journal.pbio.0060245 PubMedPubMedCentralCrossRefGoogle Scholar
  77. Hiratani I, Takebayashi S, Lu J, Gilbert DM (2009) Replication timing and transcriptional control: beyond cause and effect – Part II. Curr Opin Genet Dev 19(2):142–149. https://doi.org/10.1016/j.gde.2009.02.002 PubMedPubMedCentralCrossRefGoogle Scholar
  78. Hirose S, Hiraga S, Okazaki T (1983) Initiation site of deoxyribonucleotide polymerization at the replication origin of the Escherichia coli chromosome. Mol Gen Genet 189(3):422–431PubMedCrossRefGoogle Scholar
  79. Hoyne PR, Maher LJ 3rd (2002) Functional studies of potential intrastrand triplex elements in the Escherichia coli genome. J Mol Biol 318(2):373–386. https://doi.org/10.1016/S0022-2836(02)00041-4 PubMedCrossRefGoogle Scholar
  80. Huang J, Brito IL, Villen J, Gygi SP, Amon A, Moazed D (2006) Inhibition of homologous recombination by a cohesin-associated clamp complex recruited to the rDNA recombination enhancer. Genes Dev 20(20):2887–2901. https://doi.org/10.1101/gad.1472706 PubMedPubMedCentralCrossRefGoogle Scholar
  81. Huertas P, Aguilera A (2003) Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol Cell 12(3):711–721PubMedCrossRefGoogle Scholar
  82. Huppert JL, Balasubramanian S (2005) Prevalence of quadruplexes in the human genome. Nucleic Acids Res 33(9):2908–2916. https://doi.org/10.1093/nar/gki609 PubMedPubMedCentralCrossRefGoogle Scholar
  83. Huvet M, Nicolay S, Touchon M, Audit B, d’Aubenton-Carafa Y, Arneodo A, Thermes C (2007) Human gene organization driven by the coordination of replication and transcription. Genome Res 17(9):1278–1285. https://doi.org/10.1101/gr.6533407 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Iborra FJ, Jackson DA, Cook PR (2001) Coupled transcription and translation within nuclei of mammalian cells. Science 293(5532):1139–1142. https://doi.org/10.1126/science.1061216 PubMedCrossRefGoogle Scholar
  85. Jain A, Wang G, Vasquez KM (2008) DNA triple helices: biological consequences and therapeutic potential. Biochimie 90(8):1117–1130. https://doi.org/10.1016/j.biochi.2008.02.011 PubMedPubMedCentralCrossRefGoogle Scholar
  86. Jeppsson K, Carlborg KK, Nakato R, Berta DG, Lilienthal I, Kanno T, Lindqvist A, Brink MC, Dantuma NP, Katou Y, Shirahige K, Sjogren C (2014) The chromosomal association of the Smc5/6 complex depends on cohesion and predicts the level of sister chromatid entanglement. PLoS Genet 10(10):e1004680. ARTN e1004680. https://doi.org/10.1371/journal.pgen.1004680 CrossRefGoogle Scholar
  87. Joos S, Haluska FG, Falk MH, Henglein B, Hameister H, Croce CM, Bornkamm GW (1992) Mapping chromosomal breakpoints of Burkitt’s t(8;14) translocations far upstream of c-myc. Cancer Res 52(23):6547–6552PubMedGoogle Scholar
  88. Joshi RS, Pina B, Roca J (2012) Topoisomerase II is required for the production of long Pol II gene transcripts in yeast. Nucleic Acids Res 40(16):7907–7915. https://doi.org/10.1093/nar/gks626 PubMedPubMedCentralCrossRefGoogle Scholar
  89. Kanoh Y, Matsumoto S, Fukatsu R, Kakusho N, Kono N, Renard-Guillet C, Masuda K, Iida K, Nagasawa K, Shirahige K, Masai H (2015) Rif1 binds to G quadruplexes and suppresses replication over long distances. Nat Struct Mol Biol 22(11):889–897. https://doi.org/10.1038/nsmb.3102 PubMedCrossRefGoogle Scholar
  90. Kantidakis T, Saponaro M, Mitter R, Horswell S, Kranz A, Boeing S, Aygun O, Kelly GP, Matthews N, Stewart A, Stewart AF, Svejstrup JQ (2016) Mutation of cancer driver MLL2 results in transcription stress and genome instability. Genes Dev 30(4):408–420. https://doi.org/10.1101/gad.275453.115 PubMedPubMedCentralCrossRefGoogle Scholar
  91. Keil RL, Roeder GS (1984) Cis-acting, recombination-stimulating activity in a fragment of the ribosomal DNA of S. cerevisiae. Cell 39(2 Pt 1):377–386PubMedCrossRefGoogle Scholar
  92. Kim E, Deppert W (2003) The complex interactions of p53 with target DNA: we learn as we go. Biochem Cell Biol 81(3):141–150. https://doi.org/10.1139/o03-046 PubMedCrossRefGoogle Scholar
  93. Kim RA, Wang JC (1989) Function of DNA topoisomerases as replication swivels in Saccharomyces cerevisiae. J Mol Biol 208(2):257–267PubMedCrossRefGoogle Scholar
  94. King IF, Yandava CN, Mabb AM, Hsiao JS, Huang HS, Pearson BL, Calabrese JM, Starmer J, Parker JS, Magnuson T, Chamberlain SJ, Philpot BD, Zylka MJ (2013) Topoisomerases facilitate transcription of long genes linked to autism. Nature 501(7465):58–62. https://doi.org/10.1038/nature12504 PubMedPubMedCentralCrossRefGoogle Scholar
  95. Kinniburgh AJ (1989) A cis-acting transcription element of the c-myc gene can assume an H-DNA conformation. Nucleic Acids Res 17(19):7771–7778PubMedPubMedCentralCrossRefGoogle Scholar
  96. Kobayashi T, Horiuchi T (1996) A yeast gene product, Fob1 protein, required for both replication fork blocking and recombinational hotspot activities. Genes Cells 1(5):465–474PubMedCrossRefGoogle Scholar
  97. Kogoma T (1997) Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Microbiol Mol Biol Rev 61(2):212–238PubMedPubMedCentralGoogle Scholar
  98. Kogoma T, Hong X, Cadwell GW, Barnard KG, Asai T (1993) Requirement of homologous recombination functions for viability of the Escherichia coli cell that lacks RNase HI and exonuclease V activities. Biochimie 75(1–2):89–99PubMedCrossRefGoogle Scholar
  99. Kouzine F, Gupta A, Baranello L, Wojtowicz D, Ben-Aissa K, Liu J, Przytycka TM, Levens D (2013) Transcription-dependent dynamic supercoiling is a short-range genomic force. Nat Struct Mol Biol 20(3):396–403. https://doi.org/10.1038/nsmb.2517 PubMedPubMedCentralCrossRefGoogle Scholar
  100. Krings G, Bastia D (2005) Sap1p binds to Ter1 at the ribosomal DNA of Schizosaccharomyces pombe and causes polar replication fork arrest. J Biol Chem 280(47):39135–39142. https://doi.org/10.1074/jbc.M508996200 PubMedCrossRefGoogle Scholar
  101. Kumar A, Mazzanti M, Mistrik M, Kosar M, Beznoussenko GV, Mironov AA, Garre M, Parazzoli D, Shivashankar GV, Scita G, Bartek J, Foiani M (2014) ATR mediates a checkpoint at the nuclear envelope in response to mechanical stress. Cell 158(3):633–646. https://doi.org/10.1016/j.cell.2014.05.046 PubMedPubMedCentralCrossRefGoogle Scholar
  102. Kunst F, Ogasawara N, Moszer I, Albertini AM, Alloni G, Azevedo V, Bertero MG, Bessieres P, Bolotin A, Borchert S, Borriss R, Boursier L, Brans A, Braun M, Brignell SC, Bron S, Brouillet S, Bruschi CV, Caldwell B, Capuano V, Carter NM, Choi SK, Cordani JJ, Connerton IF, Cummings NJ, Daniel RA, Denziot F, Devine KM, Dusterhoft A, Ehrlich SD, Emmerson PT, Entian KD, Errington J, Fabret C, Ferrari E, Foulger D, Fritz C, Fujita M, Fujita Y, Fuma S, Galizzi A, Galleron N, Ghim SY, Glaser P, Goffeau A, Golightly EJ, Grandi G, Guiseppi G, Guy BJ, Haga K, Haiech J, Harwood CR, Henaut A, Hilbert H, Holsappel S, Hosono S, Hullo MF, Itaya M, Jones L, Joris B, Karamata D, Kasahara Y, Klaerr-Blanchard M, Klein C, Kobayashi Y, Koetter P, Koningstein G, Krogh S, Kumano M, Kurita K, Lapidus A, Lardinois S, Lauber J, Lazarevic V, Lee SM, Levine A, Liu H, Masuda S, Mauel C, Medigue C, Medina N, Mellado RP, Mizuno M, Moestl D, Nakai S, Noback M, Noone D, O’Reilly M, Ogawa K, Ogiwara A, Oudega B, Park SH, Parro V, Pohl TM, Portelle D, Porwollik S, Prescott AM, Presecan E, Pujic P, Purnelle B, Rapoport G, Rey M, Reynolds S, Rieger M, Rivolta C, Rocha E, Roche B, Rose M, Sadaie Y, Sato T, Scanlan E, Schleich S, Schroeter R, Scoffone F, Sekiguchi J, Sekowska A, Seror SJ, Serror P, Shin BS, Soldo B, Sorokin A, Tacconi E, Takagi T, Takahashi H, Takemaru K, Takeuchi M, Tamakoshi A, Tanaka T, Terpstra P, Togoni A, Tosato V, Uchiyama S, Vandebol M, Vannier F, Vassarotti A, Viari A, Wambutt R, Wedler H, Weitzenegger T, Winters P, Wipat A, Yamamoto H, Yamane K, Yasumoto K, Yata K, Yoshida K, Yoshikawa HF, Zumstein E, Yoshikawa H, Danchin A (1997) The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390(6657):249–256. https://doi.org/10.1038/36786 PubMedCrossRefGoogle Scholar
  103. Landick R (2006) The regulatory roles and mechanism of transcriptional pausing. Biochem Soc Trans 34(Pt 6):1062–1066. https://doi.org/10.1042/BST0341062 PubMedCrossRefGoogle Scholar
  104. Law MJ, Lower KM, Voon HP, Hughes JR, Garrick D, Viprakasit V, Mitson M, De Gobbi M, Marra M, Morris A, Abbott A, Wilder SP, Taylor S, Santos GM, Cross J, Ayyub H, Jones S, Ragoussis J, Rhodes D, Dunham I, Higgs DR, Gibbons RJ (2010) ATR-X syndrome protein targets tandem repeats and influences allele-specific expression in a size-dependent manner. Cell 143(3):367–378. https://doi.org/10.1016/j.cell.2010.09.023 PubMedCrossRefGoogle Scholar
  105. Li X, Manley JL (2005) Inactivation of the SR protein splicing factor ASF/SF2 results in genomic instability. Cell 122(3):365–378. https://doi.org/10.1016/j.cell.2005.06.008 PubMedCrossRefGoogle Scholar
  106. Li L, Wang X, Stolc V, Li X, Zhang D, Su N, Tongprasit W, Li S, Cheng Z, Wang J, Deng XW (2006) Genome-wide transcription analyses in rice using tiling microarrays. Nat Genet 38(1):124–129. https://doi.org/10.1038/ng1704 PubMedCrossRefGoogle Scholar
  107. Liberi G, Maffioletti G, Lucca C, Chiolo I, Baryshnikova A, Cotta-Ramusino C, Lopes M, Pellicioli A, Haber JE, Foiani M (2005) Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev 19(3):339–350. https://doi.org/10.1101/gad.322605 PubMedPubMedCentralCrossRefGoogle Scholar
  108. Light WH, Brickner DG, Brand VR, Brickner JH (2010) Interaction of a DNA zip code with the nuclear pore complex promotes H2A.Z incorporation and INO1 transcriptional memory. Mol Cell 40(1):112–125. https://doi.org/10.1016/j.molcel.2010.09.007 PubMedPubMedCentralCrossRefGoogle Scholar
  109. Linskens MH, Huberman JA (1988) Organization of replication of ribosomal DNA in Saccharomyces cerevisiae. Mol Cell Biol 8(11):4927–4935PubMedPubMedCentralCrossRefGoogle Scholar
  110. Liu B, Alberts BM (1995) Head-on collision between a DNA replication apparatus and RNA polymerase transcription complex. Science 267(5201):1131–1137PubMedCrossRefGoogle Scholar
  111. Liu LF, Wang JC (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci U S A 84(20):7024–7027PubMedPubMedCentralCrossRefGoogle Scholar
  112. Liu B, Wong ML, Tinker RL, Geiduschek EP, Alberts BM (1993) The DNA replication fork can pass RNA polymerase without displacing the nascent transcript. Nature 366(6450):33–39. https://doi.org/10.1038/366033a0 PubMedCrossRefGoogle Scholar
  113. Lopes M, Cotta-Ramusino C, Pellicioli A, Liberi G, Plevani P, Muzi-Falconi M, Newlon CS, Foiani M (2001) The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412(6846):557–561. https://doi.org/10.1038/35087613 PubMedCrossRefGoogle Scholar
  114. Lopez-estrano C, Schvartzman JB, Krimer DB, Hernandez P (1998) Co-localization of polar replication fork barriers and rRNA transcription terminators in mouse rDNA. J Mol Biol 277(2):249–256. https://doi.org/10.1006/jmbi.1997.1607 PubMedCrossRefGoogle Scholar
  115. Lopez-Estrano C, Schvartzman JB, Krimer DB, Hernandez P (1999) Characterization of the pea rDNA replication fork barrier: putative cis-acting and trans-acting factors. Plant Mol Biol 40(1):99–110PubMedCrossRefGoogle Scholar
  116. Maizels N, Gray LT (2013) The G4 genome. PLoS Genet 9(4):e1003468. https://doi.org/10.1371/journal.pgen.1003468 PubMedPubMedCentralCrossRefGoogle Scholar
  117. Maric C, Levacher B, Hyrien O (1999) Developmental regulation of replication fork pausing in Xenopus laevis ribosomal RNA genes. J Mol Biol 291(4):775–788. https://doi.org/10.1006/jmbi.1999.3017 PubMedCrossRefGoogle Scholar
  118. McHenry CS (2011) DNA replicases from a bacterial perspective. Annu Rev Biochem 80:403–436. https://doi.org/10.1146/annurev-biochem-061208-091655 PubMedCrossRefGoogle Scholar
  119. McKay BC, Becerril C, Spronck JC, Ljungman M (2002) Ultraviolet light-induced apoptosis is associated with S-phase in primary human fibroblasts. DNA Repair (Amst) 1(10):811–820CrossRefGoogle Scholar
  120. Mekhail K, Seebacher J, Gygi SP, Moazed D (2008) Role for perinuclear chromosome tethering in maintenance of genome stability. Nature 456(7222):667–670. https://doi.org/10.1038/nature07460 PubMedPubMedCentralCrossRefGoogle Scholar
  121. Merrikh H, Machon C, Grainger WH, Grossman AD, Soultanas P (2011) Co-directional replication-transcription conflicts lead to replication restart. Nature 470(7335):554–557. https://doi.org/10.1038/nature09758 PubMedPubMedCentralCrossRefGoogle Scholar
  122. Merrikh H, Zhang Y, Grossman AD, Wang JD (2012) Replication-transcription conflicts in bacteria. Nat Rev Microbiol 10(7):449–458. https://doi.org/10.1038/nrmicro2800 PubMedPubMedCentralCrossRefGoogle Scholar
  123. Merrikh CN, Brewer BJ, Merrikh H (2015) The B. subtilis accessory helicase PcrA facilitates DNA replication through transcription units. PLoS Genet 11(6):e1005289. https://doi.org/10.1371/journal.pgen.1005289 PubMedPubMedCentralCrossRefGoogle Scholar
  124. Meryet-Figuiere M, Alaei-Mahabadi B, Ali MM, Mitra S, Subhash S, Pandey GK, Larsson E, Kanduri C (2014) Temporal separation of replication and transcription during S-phase progression. Cell Cycle 13(20):3241–3248. https://doi.org/10.4161/15384101.2014.953876 PubMedPubMedCentralCrossRefGoogle Scholar
  125. Mirkin EV, Mirkin SM (2005) Mechanisms of transcription-replication collisions in bacteria. Mol Cell Biol 25(3):888–895. https://doi.org/10.1128/MCB.25.3.888-895.2005 PubMedPubMedCentralCrossRefGoogle Scholar
  126. Mischo HE, Gomez-Gonzalez B, Grzechnik P, Rondon AG, Wei W, Steinmetz L, Aguilera A, Proudfoot NJ (2011) Yeast Sen1 helicase protects the genome from transcription-associated instability. Mol Cell 41(1):21–32. https://doi.org/10.1016/j.molcel.2010.12.007 PubMedPubMedCentralCrossRefGoogle Scholar
  127. Mok M, Marians KJ (1987) The Escherichia coli preprimosome and DNA B helicase can form replication forks that move at the same rate. J Biol Chem 262(34):16644–16654PubMedGoogle Scholar
  128. Naughton C, Avlonitis N, Corless S, Prendergast JG, Mati IK, Eijk PP, Cockroft SL, Bradley M, Ylstra B, Gilbert N (2013) Transcription forms and remodels supercoiling domains unfolding large-scale chromatin structures. Nat Struct Mol Biol 20(3):387–395. https://doi.org/10.1038/nsmb.2509 PubMedPubMedCentralCrossRefGoogle Scholar
  129. Nickoloff JA (1992) Transcription enhances intrachromosomal homologous recombination in mammalian cells. Mol Cell Biol 12(12):5311–5318PubMedPubMedCentralCrossRefGoogle Scholar
  130. Olavarrieta L, Hernandez P, Krimer DB, Schvartzman JB (2002) DNA knotting caused by head-on collision of transcription and replication. J Mol Biol 322(1):1–6PubMedCrossRefGoogle Scholar
  131. Opalka N, Chlenov M, Chacon P, Rice WJ, Wriggers W, Darst SA (2003) Structure and function of the transcription elongation factor GreB bound to bacterial RNA polymerase. Cell 114(3):335–345PubMedCrossRefGoogle Scholar
  132. Paeschke K, Capra JA, Zakian VA (2011) DNA replication through G-quadruplex motifs is promoted by the Saccharomyces cerevisiae Pif1 DNA helicase. Cell 145(5):678–691. https://doi.org/10.1016/j.cell.2011.04.015 PubMedPubMedCentralCrossRefGoogle Scholar
  133. Park JS, Marr MT, Roberts JW (2002) E. coli transcription repair coupling factor (Mfd protein) rescues arrested complexes by promoting forward translocation. Cell 109(6):757–767PubMedCrossRefGoogle Scholar
  134. Peter BJ, Ullsperger C, Hiasa H, Marians KJ, Cozzarelli NR (1998) The structure of supercoiled intermediates in DNA replication. Cell 94(6):819–827PubMedCrossRefGoogle Scholar
  135. Peter BJ, Arsuaga J, Breier AM, Khodursky AB, Brown PO, Cozzarelli NR (2004) Genomic transcriptional response to loss of chromosomal supercoiling in Escherichia coli. Genome Biol 5(11):R87. https://doi.org/10.1186/gb-2004-5-11-r87 PubMedPubMedCentralCrossRefGoogle Scholar
  136. Pomerantz RT, O’Donnell M (2008) The replisome uses mRNA as a primer after colliding with RNA polymerase. Nature 456(7223):762–766. https://doi.org/10.1038/nature07527 PubMedPubMedCentralCrossRefGoogle Scholar
  137. Postow L, Crisona NJ, Peter BJ, Hardy CD, Cozzarelli NR (2001) Topological challenges to DNA replication: conformations at the fork. Proc Natl Acad Sci U S A 98(15):8219–8226. https://doi.org/10.1073/pnas.111006998 PubMedPubMedCentralCrossRefGoogle Scholar
  138. Prado F, Aguilera A (2005) Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J 24(6):1267–1276. https://doi.org/10.1038/sj.emboj.7600602 PubMedPubMedCentralCrossRefGoogle Scholar
  139. Prado F, Piruat JI, Aguilera A (1997) Recombination between DNA repeats in yeast hpr1delta cells is linked to transcription elongation. EMBO J 16(10):2826–2835. https://doi.org/10.1093/emboj/16.10.2826 PubMedPubMedCentralCrossRefGoogle Scholar
  140. Proshkin S, Rahmouni AR, Mironov A, Nudler E (2010) Cooperation between translating ribosomes and RNA polymerase in transcription elongation. Science 328(5977):504–508. https://doi.org/10.1126/science.1184939 PubMedPubMedCentralCrossRefGoogle Scholar
  141. Raghuraman MK, Winzeler EA, Collingwood D, Hunt S, Wodicka L, Conway A, Lockhart DJ, Davis RW, Brewer BJ, Fangman WL (2001) Replication dynamics of the yeast genome. Science 294(5540):115–121. https://doi.org/10.1126/science.294.5540.115 PubMedCrossRefGoogle Scholar
  142. Rhodes D, Lipps HJ (2015) G-quadruplexes and their regulatory roles in biology. Nucleic Acids Res 43(18):8627–8637. https://doi.org/10.1093/nar/gkv862 PubMedPubMedCentralCrossRefGoogle Scholar
  143. Rich A, Zhang S (2003) Timeline: Z-DNA: the long road to biological function. Nat Rev Genet 4(7):566–572. https://doi.org/10.1038/nrg1115 PubMedCrossRefGoogle Scholar
  144. Rivera-Mulia JC, Gilbert DM (2016) Replication timing and transcriptional control: beyond cause and effect-part III. Curr Opin Cell Biol 40:168–178. https://doi.org/10.1016/j.ceb.2016.03.022 PubMedPubMedCentralCrossRefGoogle Scholar
  145. Roberts RW, Crothers DM (1992) Stability and properties of double and triple helices: dramatic effects of RNA or DNA backbone composition. Science 258(5087):1463–1466PubMedCrossRefGoogle Scholar
  146. Rocha EP, Danchin A (2003) Essentiality, not expressiveness, drives gene-strand bias in bacteria. Nat Genet 34(4):377–378. https://doi.org/10.1038/ng1209 PubMedCrossRefGoogle Scholar
  147. Rodriguez R, Miller KM, Forment JV, Bradshaw CR, Nikan M, Britton S, Oelschlaegel T, Xhemalce B, Balasubramanian S, Jackson SP (2012) Small-molecule-induced DNA damage identifies alternative DNA structures in human genes. Nat Chem Biol 8(3):301–310. https://doi.org/10.1038/nchembio.780 PubMedPubMedCentralCrossRefGoogle Scholar
  148. Roghanian M, Zenkin N, Yuzenkova Y (2015) Bacterial global regulators DksA/ppGpp increase fidelity of transcription. Nucleic Acids Res 43(3):1529–1536. https://doi.org/10.1093/nar/gkv003 PubMedPubMedCentralCrossRefGoogle Scholar
  149. Rossi SE, Ajazi A, Carotenuto W, Foiani M, Giannattasio M (2015) Rad53-mediated regulation of Rrm3 and Pif1 DNA helicases contributes to prevention of aberrant fork transitions under replication stress. Cell Rep 13(1):80–92. https://doi.org/10.1016/j.celrep.2015.08.073 PubMedPubMedCentralCrossRefGoogle Scholar
  150. Roy Chowdhury A, Bakshi R, Wang J, Yildirir G, Liu B, Pappas-Brown V, Tolun G, Griffith JD, Shapiro TA, Jensen RE, Englund PT (2010) The killing of African trypanosomes by ethidium bromide. PLoS Pathog 6(12):e1001226. https://doi.org/10.1371/journal.ppat.1001226 PubMedPubMedCentralCrossRefGoogle Scholar
  151. Roy D, Lieber MR (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(11):3124–3133. https://doi.org/10.1128/MCB.00139-09 PubMedPubMedCentralCrossRefGoogle Scholar
  152. Rudolph CJ, Dhillon P, Moore T, Lloyd RG (2007) Avoiding and resolving conflicts between DNA replication and transcription. DNA Repair (Amst) 6(7):981–993. https://doi.org/10.1016/j.dnarep.2007.02.017 CrossRefGoogle Scholar
  153. Salceda J, Fernandez X, Roca J (2006) Topoisomerase II, not topoisomerase I, is the proficient relaxase of nucleosomal DNA. EMBO J 25(11):2575–2583. https://doi.org/10.1038/sj.emboj.7601142 PubMedPubMedCentralCrossRefGoogle Scholar
  154. Sanchez-Gorostiaga A, Lopez-Estrano C, Krimer DB, Schvartzman JB, Hernandez P (2004) Transcription termination factor reb1p causes two replication fork barriers at its cognate sites in fission yeast ribosomal DNA in vivo. Mol Cell Biol 24(1):398–406PubMedPubMedCentralCrossRefGoogle Scholar
  155. Sankar TS, Wastuwidyaningtyas BD, Dong Y, Lewis SA, Wang JD (2016) The nature of mutations induced by replication-transcription collisions. Nature 535(7610):178–181. https://doi.org/10.1038/nature18316 PubMedPubMedCentralCrossRefGoogle Scholar
  156. Santos-Pereira JM, Aguilera A (2015) R loops: new modulators of genome dynamics and function. Nat Rev Genet 16(10):583–597. https://doi.org/10.1038/nrg3961 PubMedCrossRefGoogle Scholar
  157. Santos-Pereira JM, Herrero AB, Garcia-Rubio ML, Marin A, Moreno S, Aguilera A (2013) The Npl3 hnRNP prevents R-loop-mediated transcription-replication conflicts and genome instability. Genes Dev 27(22):2445–2458. https://doi.org/10.1101/gad.229880.113 PubMedPubMedCentralCrossRefGoogle Scholar
  158. Saponaro M, Kantidakis T, Mitter R, Kelly GP, Heron M, Williams H, Soding J, Stewart A, Svejstrup JQ (2014) RECQL5 controls transcript elongation and suppresses genome instability associated with transcription stress. Cell 157(5):1037–1049. https://doi.org/10.1016/j.cell.2014.03.048 PubMedPubMedCentralCrossRefGoogle Scholar
  159. Sarkies P, Reams C, Simpson LJ, Sale JE (2010) Epigenetic instability due to defective replication of structured DNA. Mol Cell 40(5):703–713. https://doi.org/10.1016/j.molcel.2010.11.009 PubMedPubMedCentralCrossRefGoogle Scholar
  160. Savic DJ, Kanazir DT (1972) The effect of a histidine operator-constitutive mutation on UV-induced mutability within the histidine operon of Salmonella typhimurium. Mol Gen Genet 118(1):45–50PubMedCrossRefGoogle Scholar
  161. Schalbetter SA, Mansoubi S, Chambers AL, Downs JA, Baxter J (2015) Fork rotation and DNA precatenation are restricted during DNA replication to prevent chromosomal instability. Proc Natl Acad Sci U S A 112(33):E4565–E4570. https://doi.org/10.1073/pnas.1505356112 PubMedPubMedCentralCrossRefGoogle Scholar
  162. Selby CP, Drapkin R, Reinberg D, Sancar A (1997) RNA polymerase II stalled at a thymine dimer: footprint and effect on excision repair. Nucleic Acids Res 25(4):787–793PubMedPubMedCentralCrossRefGoogle Scholar
  163. Sen D, Gilbert W (1988) Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis. Nature 334(6180):364–366. https://doi.org/10.1038/334364a0 PubMedCrossRefGoogle Scholar
  164. Smirnov E, Borkovec J, Kovacik L, Svidenska S, Schrofel A, Skalnikova M, Svindrych Z, Krizek P, Ovesny M, Hagen GM, Juda P, Michalova K, Cardoso MC, Cmarko D, Raska I (2014) Separation of replication and transcription domains in nucleoli. J Struct Biol 188(3):259–266. https://doi.org/10.1016/j.jsb.2014.10.001 PubMedCrossRefGoogle Scholar
  165. Song W, Dominska M, Greenwell PW, Petes TD (2014) Genome-wide high-resolution mapping of chromosome fragile sites in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 111(21):E2210–E2218. https://doi.org/10.1073/pnas.1406847111 PubMedPubMedCentralCrossRefGoogle Scholar
  166. Spiesser TW, Diener C, Barberis M, Klipp E (2010) What influences DNA replication rate in budding yeast? PLoS One 5(4):e10203. https://doi.org/10.1371/journal.pone.0010203 PubMedPubMedCentralCrossRefGoogle Scholar
  167. Srivatsan A, Tehranchi A, MacAlpine DM, Wang JD (2010) Co-orientation of replication and transcription preserves genome integrity. PLoS Genet 6(1):e1000810. https://doi.org/10.1371/journal.pgen.1000810 PubMedPubMedCentralCrossRefGoogle Scholar
  168. Stirling PC, Chan YA, Minaker SW, Aristizabal MJ, Barrett I, Sipahimalani P, Kobor MS, Hieter P (2012) R-loop-mediated genome instability in mRNA cleavage and polyadenylation mutants. Genes Dev 26(2):163–175. https://doi.org/10.1101/gad.179721.111 PubMedPubMedCentralCrossRefGoogle Scholar
  169. Stolc V, Gauhar Z, Mason C, Halasz G, van Batenburg MF, Rifkin SA, Hua S, Herreman T, Tongprasit W, Barbano PE, Bussemaker HJ, White KP (2004) A gene expression map for the euchromatic genome of Drosophila melanogaster. Science 306(5696):655–660. https://doi.org/10.1126/science.1101312 PubMedCrossRefGoogle Scholar
  170. Strambio-De-Castillia C, Niepel M, Rout MP (2010) The nuclear pore complex: bridging nuclear transport and gene regulation. Nat Rev Mol Cell Biol 11(7):490–501. https://doi.org/10.1038/nrm2928 PubMedCrossRefGoogle Scholar
  171. Tan-Wong SM, Wijayatilake HD, Proudfoot NJ (2009) Gene loops function to maintain transcriptional memory through interaction with the nuclear pore complex. Genes Dev 23(22):2610–2624. https://doi.org/10.1101/gad.1823209 PubMedPubMedCentralCrossRefGoogle Scholar
  172. Tehranchi AK, Blankschien MD, Zhang Y, Halliday JA, Srivatsan A, Peng J, Herman C, Wang JD (2010) The transcription factor DksA prevents conflicts between DNA replication and transcription machinery. Cell 141(4):595–605. https://doi.org/10.1016/j.cell.2010.03.036 PubMedPubMedCentralCrossRefGoogle Scholar
  173. Thomas BJ, Rothstein R (1989) Elevated recombination rates in transcriptionally active DNA. Cell 56(4):619–630PubMedCrossRefGoogle Scholar
  174. Todd AK, Johnston M, Neidle S (2005) Highly prevalent putative quadruplex sequence motifs in human DNA. Nucleic Acids Res 33(9):2901–2907. https://doi.org/10.1093/nar/gki553 PubMedPubMedCentralCrossRefGoogle Scholar
  175. Tuduri S, Crabbe L, Conti C, Tourriere H, Holtgreve-Grez H, Jauch A, Pantesco V, De Vos J, Thomas A, Theillet C, Pommier Y, Tazi J, Coquelle A, Pasero P (2009) Topoisomerase I suppresses genomic instability by preventing interference between replication and transcription. Nat Cell Biol 11(11):1315–1324. https://doi.org/10.1038/ncb1984 PubMedPubMedCentralCrossRefGoogle Scholar
  176. Usdin K, Woodford KJ (1995) CGG repeats associated with DNA instability and chromosome fragility form structures that block DNA synthesis in vitro. Nucleic Acids Res 23(20):4202–4209PubMedPubMedCentralCrossRefGoogle Scholar
  177. Vilette D, Uzest M, Ehrlich SD, Michel B (1992) DNA transcription and repressor binding affect deletion formation in Escherichia coli plasmids. EMBO J 11(10):3629–3634PubMedPubMedCentralGoogle Scholar
  178. Voelkel-Meiman K, Keil RL, Roeder GS (1987) Recombination-stimulating sequences in yeast ribosomal DNA correspond to sequences regulating transcription by RNA polymerase I. Cell 48(6):1071–1079PubMedCrossRefGoogle Scholar
  179. Wahba L, Amon JD, Koshland D, Vuica-Ross M (2011) RNase H and multiple RNA biogenesis factors cooperate to prevent RNA: DNA hybrids from generating genome instability. Mol Cell 44(6):978–988. https://doi.org/10.1016/j.molcel.2011.10.017 PubMedPubMedCentralCrossRefGoogle Scholar
  180. Wang JC (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 3(6):430–440. https://doi.org/10.1038/nrm831 PubMedCrossRefGoogle Scholar
  181. Wang G, Vasquez KM (2004) Naturally occurring H-DNA-forming sequences are mutagenic in mammalian cells. Proc Natl Acad Sci U S A 101(37):13448–13453. https://doi.org/10.1073/pnas.0405116101 PubMedPubMedCentralCrossRefGoogle Scholar
  182. Wang G, Christensen LA, Vasquez KM (2006) Z-DNA-forming sequences generate large-scale deletions in mammalian cells. Proc Natl Acad Sci U S A 103(8):2677–2682. https://doi.org/10.1073/pnas.0511084103 PubMedPubMedCentralCrossRefGoogle Scholar
  183. Wang JD, Berkmen MB, Grossman AD (2007) Genome-wide coorientation of replication and transcription reduces adverse effects on replication in Bacillus subtilis. Proc Natl Acad Sci U S A 104(13):5608–5613. https://doi.org/10.1073/pnas.0608999104 PubMedPubMedCentralCrossRefGoogle Scholar
  184. Wansink DG, Manders EE, van der Kraan I, Aten JA, van Driel R, de Jong L (1994) RNA polymerase II transcription is concentrated outside replication domains throughout S-phase. J Cell Sci 107(Pt 6):1449–1456PubMedGoogle Scholar
  185. Wei X, Samarabandu J, Devdhar RS, Siegel AJ, Acharya R, Berezney R (1998) Segregation of transcription and replication sites into higher order domains. Science 281(5382):1502–1506PubMedCrossRefGoogle Scholar
  186. Wei PC, Chang AN, Kao J, Du Z, Meyers RM, Alt FW, Schwer B (2016) Long neural genes harbor recurrent DNA break clusters in neural stem/progenitor cells. Cell 164(4):644–655. https://doi.org/10.1016/j.cell.2015.12.039 PubMedPubMedCentralCrossRefGoogle Scholar
  187. Westover KD, Bushnell DA, Kornberg RD (2004) Structural basis of transcription: separation of RNA from DNA by RNA polymerase II. Science 303(5660):1014–1016. https://doi.org/10.1126/science.1090839 PubMedCrossRefGoogle Scholar
  188. Wilda M, Busch K, Klose I, Keller T, Woessmann W, Kreuder J, Harbott J, Borkhardt A (2004) Level of MYC overexpression in pediatric Burkitt’s lymphoma is strongly dependent on genomic breakpoint location within the MYC locus. Genes Chromosomes Cancer 41(2):178–182. https://doi.org/10.1002/gcc.20063 PubMedCrossRefGoogle Scholar
  189. Wilson MD, Harreman M, Taschner M, Reid J, Walker J, Erdjument-Bromage H, Tempst P, Svejstrup JQ (2013) Proteasome-mediated processing of Def1, a critical step in the cellular response to transcription stress. Cell 154(5):983–995. https://doi.org/10.1016/j.cell.2013.07.028 PubMedPubMedCentralCrossRefGoogle Scholar
  190. Wilson TE, Arlt MF, Park SH, Rajendran S, Paulsen M, Ljungman M, Glover TW (2015) Large transcription units unify copy number variants and common fragile sites arising under replication stress. Genome Res 25(2):189–200. https://doi.org/10.1101/gr.177121.114 PubMedPubMedCentralCrossRefGoogle Scholar
  191. Woodford KJ, Howell RM, Usdin K (1994) A novel K(+)-dependent DNA synthesis arrest site in a commonly occurring sequence motif in eukaryotes. J Biol Chem 269(43):27029–27035PubMedGoogle Scholar
  192. Wu HY, Shyy SH, Wang JC, Liu LF (1988) Transcription generates positively and negatively supercoiled domains in the template. Cell 53(3):433–440PubMedCrossRefGoogle Scholar
  193. Wyrick JJ, Aparicio JG, Chen T, Barnett JD, Jennings EG, Young RA, Bell SP, Aparicio OM (2001) Genome-wide distribution of ORC and MCM proteins in S. cerevisiae: high-resolution mapping of replication origins. Science 294(5550):2357–2360. https://doi.org/10.1126/science.1066101 PubMedCrossRefGoogle Scholar
  194. Yunis JJ, Soreng AL (1984) Constitutive fragile sites and cancer. Science 226(4679):1199–1204PubMedCrossRefGoogle Scholar
  195. Zhang Z, Macalpine DM, Kapler GM (1997) Developmental regulation of DNA replication: replication fork barriers and programmed gene amplification in Tetrahymena thermophila. Mol Cell Biol 17(10):6147–6156PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  1. 1.IFOM (Fondazione Istituto FIRC di Oncologia Molecolare)MilanItaly
  2. 2.Istituto FIRC di Oncologia MolecolareMilanItaly

Personalised recommendations