Transcription Regulatory Elements Are Punctuation Marks for DNA Replication

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2006 May 4

PMID 16670199

Citations 35

Authors

Ekaterina V Mirkin

Daniel Castro Roa

Evgeny Nudler

Sergei M Mirkin

Affiliations

Soon will be listed here.

Abstract

Collisions between DNA replication and transcription significantly affect genome organization, regulation, and stability. Previous studies have described collisions between replication forks and elongating RNA polymerases. Although replication collisions with the transcription-initiation or -termination complexes are potentially even more important because most genes are not actively transcribed during DNA replication, their existence and mechanisms remained unproven. To address this matter, we have designed a bacterial promoter that binds RNA polymerase and maintains it in the initiating mode by precluding the transition into the elongation mode. By using electrophoretic analysis of replication intermediates, we have found that this steadfast transcription-initiation complex inhibits replication fork progression in an orientation-dependent manner during head-on collisions. Transcription terminators also appeared to attenuate DNA replication, but in the opposite, codirectional orientation. Thus, transcription regulatory signals may serve as "punctuation marks" for DNA replication in vivo.

Citing Articles

Endogenous DNA damage at sites of terminated transcripts.

Liu J, Perren J, Rogers C, Nimer S, Wen A, Halliday J Nature. 2025; .

PMID: 39972147 DOI: 10.1038/s41586-024-08578-4.

Genome-wide mapping of spontaneous DNA replication error-hotspots using mismatch repair proteins in rapidly proliferating Escherichia coli.

Hasenauer F, Barreto H, Lotton C, Matic I Nucleic Acids Res. 2024; 53(2.

PMID: 39660654 PMC: 11754648. DOI: 10.1093/nar/gkae1196.

High-resolution landscape of an antibiotic binding site.

Yang K, Cameranesi M, Gowder M, Martinez C, Shamovsky Y, Epshtein V Nature. 2023; 622(7981):180-187.

PMID: 37648864 PMC: 10550828. DOI: 10.1038/s41586-023-06495-6.

The in vivo measurement of replication fork velocity and pausing by lag-time analysis.

Huang D, Johnson A, Sim B, Lo T, Merrikh H, Wiggins P Nat Commun. 2023; 14(1):1762.

PMID: 36997519 PMC: 10063678. DOI: 10.1038/s41467-023-37456-2.

Mitogenome-wise codon usage pattern from comparative analysis of the first mitogenome of Blepharipa sp. (Muga uzifly) with other Oestroid flies.

Kabiraj D, Chetia H, Nath A, Sharma P, Mosahari P, Singh D Sci Rep. 2022; 12(1):7028.

PMID: 35487927 PMC: 9054809. DOI: 10.1038/s41598-022-10547-8.

References

Takeuchi Y, Horiuchi T, Kobayashi T . Transcription-dependent recombination and the role of fork collision in yeast rDNA. Genes Dev. 2003; 17(12):1497-506. PMC: 196080. DOI: 10.1101/gad.1085403. View

Liu B, Alberts B . Head-on collision between a DNA replication apparatus and RNA polymerase transcription complex. Science. 1995; 267(5201):1131-7. DOI: 10.1126/science.7855590. View

Liu B, Wong M, Tinker R, Geiduschek E, Alberts B . The DNA replication fork can pass RNA polymerase without displacing the nascent transcript. Nature. 1993; 366(6450):33-9. DOI: 10.1038/366033a0. View

Courcelle J, Hanawalt P . RecA-dependent recovery of arrested DNA replication forks. Annu Rev Genet. 2003; 37:611-46. DOI: 10.1146/annurev.genet.37.110801.142616. View

Gusarov I, Nudler E . The mechanism of intrinsic transcription termination. Mol Cell. 1999; 3(4):495-504. DOI: 10.1016/s1097-2765(00)80477-3. View

Huerta A, Collado-Vides J . Sigma70 promoters in Escherichia coli: specific transcription in dense regions of overlapping promoter-like signals. J Mol Biol. 2003; 333(2):261-78. DOI: 10.1016/j.jmb.2003.07.017. View

Salas M . Bacteriophage phi29 DNA replication arrest caused by codirectional collisions with the transcription machinery. EMBO J. 1997; 16(18):5775-83. PMC: 1170208. DOI: 10.1093/emboj/16.18.5775. View

Hsu L, Vo N, CHAMBERLIN M . Escherichia coli transcript cleavage factors GreA and GreB stimulate promoter escape and gene expression in vivo and in vitro. Proc Natl Acad Sci U S A. 1995; 92(25):11588-92. PMC: 40447. DOI: 10.1073/pnas.92.25.11588. View

Nudler E, Avetissova E, Markovtsov V, Goldfarb A . Transcription processivity: protein-DNA interactions holding together the elongation complex. Science. 1996; 273(5272):211-7. DOI: 10.1126/science.273.5272.211. View

10.

Higgins N, Kato K, Strauss B . A model for replication repair in mammalian cells. J Mol Biol. 1976; 101(3):417-25. DOI: 10.1016/0022-2836(76)90156-x. View

11.

Rocha E, Danchin A . Essentiality, not expressiveness, drives gene-strand bias in bacteria. Nat Genet. 2003; 34(4):377-8. DOI: 10.1038/ng1209. View

12.

Blattner F, Plunkett 3rd G, Bloch C, Perna N, Burland V, Riley M . The complete genome sequence of Escherichia coli K-12. Science. 1997; 277(5331):1453-62. DOI: 10.1126/science.277.5331.1453. View

13.

Krasilnikova M, Samadashwily G, Krasilnikov A, Mirkin S . Transcription through a simple DNA repeat blocks replication elongation. EMBO J. 1998; 17(17):5095-102. PMC: 1170837. DOI: 10.1093/emboj/17.17.5095. View

14.

Cha R, Kleckner N . ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science. 2002; 297(5581):602-6. DOI: 10.1126/science.1071398. View

15.

Ivessa A, Lenzmeier B, Bessler J, Goudsouzian L, Schnakenberg S, Zakian V . The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol Cell. 2003; 12(6):1525-36. DOI: 10.1016/s1097-2765(03)00456-8. View

16.

Olavarrieta L, Hernandez P, Krimer D, Schvartzman J . DNA knotting caused by head-on collision of transcription and replication. J Mol Biol. 2002; 322(1):1-6. DOI: 10.1016/s0022-2836(02)00740-4. View

17.

Myung K, Datta A, Kolodner R . Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell. 2001; 104(3):397-408. DOI: 10.1016/s0092-8674(01)00227-6. View

18.

Mohanty B, Bairwa N, Bastia D . The Tof1p-Csm3p protein complex counteracts the Rrm3p helicase to control replication termination of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 2006; 103(4):897-902. PMC: 1347974. DOI: 10.1073/pnas.0506540103. View

19.

Brewer B, FANGMAN W . The localization of replication origins on ARS plasmids in S. cerevisiae. Cell. 1987; 51(3):463-71. DOI: 10.1016/0092-8674(87)90642-8. View

20.

Cleary J, Nichol K, Wang Y, Pearson C . Evidence of cis-acting factors in replication-mediated trinucleotide repeat instability in primate cells. Nat Genet. 2002; 31(1):37-46. DOI: 10.1038/ng870. View