DNA Torsion As a Feedback Mediator of Transcription and Chromatin Dynamics

Overview

Journal Nucleus

Date 2014 May 14

PMID 24819949

Citations 32

Authors

Sheila S Teves

Steven Henikoff

Affiliations

Soon will be listed here.

Abstract

The double helical structure of DNA lends itself to topological constraints. Many DNA-based processes alter the topological state of DNA, generating torsional stress, which is efficiently relieved by topoisomerases. Maintaining this topological balance is crucial to cell survival, as excessive torsional strain risks DNA damage. Here, we review the mechanisms that generate and modulate DNA torsion within the cell. In particular, we discuss how transcription-generated torsional stress affects Pol II kinetics and chromatin dynamics, highlighting an emerging role of DNA torsion as a feedback mediator of torsion-generating processes.

Citing Articles

RNA interacts with topoisomerase I to adjust DNA topology.

Bhola M, Abe K, Orozco P, Rahnamoun H, Avila-Lopez P, Taylor E Mol Cell. 2024; 84(17):3192-3208.e11.

PMID: 39173639 PMC: 11380577. DOI: 10.1016/j.molcel.2024.07.032.

Downstream-of-gene (DoG) transcripts contribute to an imbalance in the cancer cell transcriptome.

Abe K, Maunze B, Lopez P, Xu J, Muhammad N, Yang G Sci Adv. 2024; 10(27):eadh9613.

PMID: 38959318 PMC: 11221514. DOI: 10.1126/sciadv.adh9613.

Type I toxin-antitoxin systems in bacteria: from regulation to biological functions.

Shore S, Leinberger F, Fozo E, Berghoff B EcoSal Plus. 2024; 12(1):eesp00252022.

PMID: 38767346 PMC: 11636113. DOI: 10.1128/ecosalplus.esp-0025-2022.

DNA topoisomerase 1 represses HIV-1 promoter activity through its interaction with a guanine quadruplex present in the LTR sequence.

Lista M, Jousset A, Cheng M, Saint-Andre V, Perrot E, Rodrigues M Retrovirology. 2023; 20(1):10.

PMID: 37254203 PMC: 10228017. DOI: 10.1186/s12977-023-00625-8.

The viral packaging motor potentiates Kaposi's sarcoma-associated herpesvirus gene expression late in infection.

McCollum C, Didychuk A, Liu D, Murray-Nerger L, Cristea I, Glaunsinger B PLoS Pathog. 2023; 19(4):e1011163.

PMID: 37068108 PMC: 10138851. DOI: 10.1371/journal.ppat.1011163.

References

Gupta P, Zlatanova J, Tomschik M . Nucleosome assembly depends on the torsion in the DNA molecule: a magnetic tweezers study. Biophys J. 2009; 97(12):3150-7. PMC: 2793352. DOI: 10.1016/j.bpj.2009.09.032. View

Khadka D, Cho W . Topoisomerase inhibitors as anticancer agents: a patent update. Expert Opin Ther Pat. 2013; 23(8):1033-56. DOI: 10.1517/13543776.2013.790958. View

Pommier Y . Drugging topoisomerases: lessons and challenges. ACS Chem Biol. 2012; 8(1):82-95. PMC: 3549721. DOI: 10.1021/cb300648v. View

Brill S, Sternglanz R . Transcription-dependent DNA supercoiling in yeast DNA topoisomerase mutants. Cell. 1988; 54(3):403-11. DOI: 10.1016/0092-8674(88)90203-6. View

Viard T, Bouthier de la Tour C . Type IA topoisomerases: a simple puzzle?. Biochimie. 2006; 89(4):456-67. DOI: 10.1016/j.biochi.2006.10.013. View

Kimura K, Hirano T . ATP-dependent positive supercoiling of DNA by 13S condensin: a biochemical implication for chromosome condensation. Cell. 1997; 90(4):625-34. DOI: 10.1016/s0092-8674(00)80524-3. View

Kouzine F, Gupta A, Baranello L, Wojtowicz D, Ben-Aissa K, Liu J . Transcription-dependent dynamic supercoiling is a short-range genomic force. Nat Struct Mol Biol. 2013; 20(3):396-403. PMC: 3594045. DOI: 10.1038/nsmb.2517. View

Baxter J, Sen N, Martinez V, De Carandini M, Schvartzman J, Diffley J . Positive supercoiling of mitotic DNA drives decatenation by topoisomerase II in eukaryotes. Science. 2011; 331(6022):1328-32. DOI: 10.1126/science.1201538. View

Salceda J, Fernandez X, Roca J . Topoisomerase II, not topoisomerase I, is the proficient relaxase of nucleosomal DNA. EMBO J. 2006; 25(11):2575-83. PMC: 1478187. DOI: 10.1038/sj.emboj.7601142. View

10.

Matsumoto K, Hirose S . Visualization of unconstrained negative supercoils of DNA on polytene chromosomes of Drosophila. J Cell Sci. 2004; 117(Pt 17):3797-805. DOI: 10.1242/jcs.01225. View

11.

Naughton C, Avlonitis N, Corless S, Prendergast J, Mati I, Eijk P . Transcription forms and remodels supercoiling domains unfolding large-scale chromatin structures. Nat Struct Mol Biol. 2013; 20(3):387-95. PMC: 3689368. DOI: 10.1038/nsmb.2509. View

12.

Dixon J, Selvaraj S, Yue F, Kim A, Li Y, Shen Y . Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012; 485(7398):376-80. PMC: 3356448. DOI: 10.1038/nature11082. View

13.

Luger K, Mader A, Richmond R, Sargent D, Richmond T . Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997; 389(6648):251-60. DOI: 10.1038/38444. View

14.

Liu L, Liu C, Alberts B . Type II DNA topoisomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. Cell. 1980; 19(3):697-707. DOI: 10.1016/s0092-8674(80)80046-8. View

15.

Piruat J, Chavez S, Aguilera A . The yeast HRS1 gene is involved in positive and negative regulation of transcription and shows genetic characteristics similar to SIN4 and GAL11. Genetics. 1997; 147(4):1585-94. PMC: 1208333. DOI: 10.1093/genetics/147.4.1585. View

16.

Huang W . Bacterial diversity based on type II DNA topoisomerase genes. Annu Rev Genet. 1996; 30:79-107. DOI: 10.1146/annurev.genet.30.1.79. View

17.

Kahn J . Topological effects of the TATA box binding protein on minicircle DNA and a possible thermodynamic linkage to chromatin remodeling. Biochemistry. 2000; 39(13):3520-4. DOI: 10.1021/bi992263f. View

18.

Nolis I, McKay D, Mantouvalou E, Lomvardas S, Merika M, Thanos D . Transcription factors mediate long-range enhancer-promoter interactions. Proc Natl Acad Sci U S A. 2009; 106(48):20222-7. PMC: 2779200. DOI: 10.1073/pnas.0902454106. View

19.

Koster D, Croquette V, Dekker C, Shuman S, Dekker N . Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB. Nature. 2005; 434(7033):671-4. DOI: 10.1038/nature03395. View

20.

Kouzine F, Sanford S, Elisha-Feil Z, Levens D . The functional response of upstream DNA to dynamic supercoiling in vivo. Nat Struct Mol Biol. 2008; 15(2):146-54. DOI: 10.1038/nsmb.1372. View