Pathophysiological Role and Diagnostic Potential of R-Loops in Cancer and Beyond

R-Loop-Associated Genomic Instability and Implication of WRN and WRNIP1

(2022) Veronica Marabitti et al.   INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES

Proximity labeling identifies a repertoire of site-specific R-loop modulators

(2022) Qingqing Yan et al.   Nature Communications

Aberrant R-loop-induced replication stress in MED12-mutant uterine fibroids

(2022) Sribalasubashini Muralimanoharan et al.   Scientific Reports

The Bidirectional Link Between RNA Cleavage and Polyadenylation and Genome Stability: Recent Insights From a Systematic Screen

(2022) Stefano Spada et al.   Frontiers in Genetics

R-loop Mediated DNA Damage and Impaired DNA Repair in Spinal Muscular Atrophy

(2022) Juliana Cuartas et al.   Frontiers in Cellular Neuroscience

ZFP281-BRCA2 prevents R-loop accumulation during DNA replication

(2022) Yan Wang et al.   Nature Communications

Genomic profiling of native R loops with a DNA-RNA hybrid recognition sensor

(2021) Kang Wang et al.   Science Advances

Molecular mechanisms underlying nucleotide repeat expansion disorders

(2021) Indranil Malik et al.   NATURE REVIEWS MOLECULAR CELL BIOLOGY

Non-Coding RNAs and Splicing Activity in Testicular Germ Cell Tumors

(2021) Marco Barchi et al.   Life-Basel

San1 deficiency leads to cardiomyopathy due to excessive R-loop-associated DNA damage and cardiomyocyte hypoplasia

(2021) Zhiheng Liu et al.   BIOCHIMICA ET BIOPHYSICA ACTA-MOLECULAR BASIS OF DISEASE

R-Loop Tracker: Web Access-Based Tool for R-Loop Detection and Analysis in Genomic DNA Sequences

(2021) Václav Brázda et al.   INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES

R-loopBase: a knowledgebase for genome-wide R-loop formation and regulation

(2021) Ruoyao Lin et al.   NUCLEIC ACIDS RESEARCH

R-loop modulated epigenetic regulation in T helper cells mechanistically associates coronary artery disease and non-small cell lung cancer

(2021) Sudeshna Rakshit et al.   Translational Oncology

Polyglutamine Ataxias: Our Current Molecular Understanding and What the Future Holds for Antisense Therapies

(2021) Craig S. McIntosh et al.   Biomedicines

On the wrong DNA track: Molecular mechanisms of repeat-mediated genome instability

(2020) Alexandra N. Khristich et al.   JOURNAL OF BIOLOGICAL CHEMISTRY

Ultra-Deep Coverage Single-Molecule R-loop Footprinting Reveals Principles of R-loop Formation

(2020) Maika Malig et al.   JOURNAL OF MOLECULAR BIOLOGY

R-Loop Mediated trans Action of the APOLO Long Noncoding RNA

(2020) Federico Ariel et al.   MOLECULAR CELL

Regulatory R-loops as facilitators of gene expression and genome stability

(2020) Christof Niehrs et al.   NATURE REVIEWS MOLECULAR CELL BIOLOGY

The R-loop Atlas of Arabidopsis Development and Responses to Environmental Stimuli

(2020) Wei Xu et al.   PLANT CELL

qDRIP: a method to quantitatively assess RNA–DNA hybrid formation genome-wide

(2020) Magdalena P Crossley et al.   NUCLEIC ACIDS RESEARCH

Emerging Roles of RNA 3′-end Cleavage and Polyadenylation in Pathogenesis, Diagnosis and Therapy of Human Disorders

(2020) Jamie Nourse et al.   Biomolecules

R-Loop Physiology and Pathology: A Brief Review

(2020) Ryan Patrick Mackay et al.   DNA AND CELL BIOLOGY

RecQ helicases in DNA repair and cancer targets

(2020) Joseph A. Newman et al.   Essays in Biochemistry

TREND-DB—a transcriptome-wide atlas of the dynamic landscape of alternative polyadenylation

(2020) Federico Marini et al.   NUCLEIC ACIDS RESEARCH

BRD4 prevents the accumulation of R-loops and protects against transcription–replication collision events and DNA damage

(2020) Fred C. Lam et al.   Nature Communications

Efficient Pre-mRNA Cleavage Prevents Replication-Stress-Associated Genome Instability

(2019) Federico Teloni et al.   MOLECULAR CELL

ATM pathway activation limits R-loop-associated genomic instability in Werner syndrome cells

(2019) Veronica Marabitti et al.   NUCLEIC ACIDS RESEARCH

Interplay between DNA sequence and negative superhelicity drives R-loop structures

(2019) Robert Stolz et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

R-Loops as Cellular Regulators and Genomic Threats

(2019) Madzia P. Crossley et al.   MOLECULAR CELL

High-resolution, strand-specific R-loop mapping via S9.6-based DNA–RNA immunoprecipitation and high-throughput sequencing

(2019) Lionel A. Sanz et al.   Nature Protocols

Drugging the R-loop interactome: RNA-DNA hybrid binding proteins as targets for cancer therapy

(2019) Beáta Boros-Oláh et al.   DNA REPAIR

Mapping Native R-Loops Genome-wide Using a Targeted Nuclease Approach

(2019) Qingqing Yan et al.   Cell Reports

The molecular landscape of ETMR at diagnosis and relapse

(2019) Sander Lambo et al.   NATURE

R-loops cause genomic instability in T helper lymphocytes from patients with Wiskott-Aldrich syndrome

(2018) Koustav Sarkar et al.   JOURNAL OF ALLERGY AND CLINICAL IMMUNOLOGY

The Augmented R-Loop Is a Unifying Mechanism for Myelodysplastic Syndromes Induced by High-Risk Splicing Factor Mutations

(2018) Liang Chen et al.   MOLECULAR CELL

Senataxin Mutation Reveals How R-Loops Promote Transcription by Blocking DNA Methylation at Gene Promoters

(2018) Christopher Grunseich et al.   MOLECULAR CELL

RNA Helicase DDX1 Converts RNA G-Quadruplex Structures into R-Loops to Promote IgH Class Switch Recombination

(2018) Claudia Ribeiro de Almeida et al.   MOLECULAR CELL

Senataxin resolves RNA:DNA hybrids forming at DNA double-strand breaks to prevent translocations

(2018) Sarah Cohen et al.   Nature Communications

Human Rad52 Promotes XPG-Mediated R-loop Processing to Initiate Transcription-Associated Homologous Recombination Repair

(2018) Takaaki Yasuhara et al.   CELL

R-loop generation during transcription: Formation, processing and cellular outcomes

(2018) Boris P. Belotserkovskii et al.   DNA REPAIR

R-Loops in Motor Neuron Diseases

(2018) Martina G. L. Perego et al.   MOLECULAR NEUROBIOLOGY

EWS–FLI1 increases transcription to cause R-loops and block BRCA1 repair in Ewing sarcoma

(2018) Aparna Gorthi et al.   NATURE

GADD45A binds R-loops and recruits TET1 to CpG island promoters

(2018) Khelifa Arab et al.   NATURE GENETICS

Transcriptome 3′end organization by PCF11 links alternative polyadenylation to formation and neuronal differentiation of neuroblastoma

(2018) Anton Ogorodnikov et al.   Nature Communications

BRCA2 controls DNA:RNA hybrid level at DSBs by mediating RNase H2 recruitment

(2018) Giuseppina D’Alessandro et al.   Nature Communications

R Loops and Links to Human Disease

(2017) Patricia Richard et al.   JOURNAL OF MOLECULAR BIOLOGY

R-ChIP Using Inactive RNase H Reveals Dynamic Coupling of R-loops with Transcriptional Pausing at Gene Promoters

(2017) Liang Chen et al.   MOLECULAR CELL

ATM, ATR, and DNA-PK: The Trinity at the Heart of the DNA Damage Response

(2017) Andrew N. Blackford et al.   MOLECULAR CELL

RNase H1 Cooperates with DNA Gyrases to Restrict R-Loops and Maintain Genome Integrity in Arabidopsis Chloroplasts

(2017) Zhuo Yang et al.   PLANT CELL

Telomeres in ICF syndrome cells are vulnerable to DNA damage due to elevated DNA:RNA hybrids

(2017) Shira Sagie et al.   Nature Communications

Defining the location of promoter-associated R-loops at near-nucleotide resolution using bisDRIP-seq

(2017) Jason G Dumelie et al.   eLife

Aquarius is required for proper CtIP expression and homologous recombination repair

(2017) Ryo Sakasai et al.   Scientific Reports

Transient RNA-DNA Hybrids Are Required for Efficient Double-Strand Break Repair

(2016) Corina Ohle et al.   CELL

S1-DRIP-seq identifies high expression and polyA tracts as major contributors to R-loop formation

(2016) Lamia Wahba et al.   GENES & DEVELOPMENT

DEAD Box 1 Facilitates Removal of RNA and Homologous Recombination at DNA Double-Strand Breaks

(2016) Lei Li et al.   MOLECULAR AND CELLULAR BIOLOGY

Prevalent, Dynamic, and Conserved R-Loop Structures Associate with Specific Epigenomic Signatures in Mammals

(2016) Lionel A. Sanz et al.   MOLECULAR CELL

The regulation and functions of the nuclear RNA exosome complex

(2016) Cornelia Kilchert et al.   NATURE REVIEWS MOLECULAR CELL BIOLOGY

R-loopDB: a database for R-loop forming sequences (RLFS) and R-loops

(2016) Piroon Jenjaroenpun et al.   NUCLEIC ACIDS RESEARCH

Increased global transcription activity as a mechanism of replication stress in cancer

(2016) Panagiotis Kotsantis et al.   Nature Communications

XRN2 Links Transcription Termination to DNA Damage and Replication Stress

(2016) Julio C. Morales et al.   PLoS Genetics

Co-transcriptional R-loops are the main cause of estrogen-induced DNA damage

(2016) Caroline Townsend Stork et al.   eLife

The mRNA capping enzyme of Saccharomyces cerevisiae has dual specificity to interact with CTD of RNA Polymerase II

(2016) Akhilendra Pratap Bharati et al.   Scientific Reports

BRCA1 Recruitment to Transcriptional Pause Sites Is Required for R-Loop-Driven DNA Damage Repair

(2015) Elodie Hatchi et al.   MOLECULAR CELL

Senataxin suppresses the antiviral transcriptional response and controls viral biogenesis

(2015) Matthew S Miller et al.   NATURE IMMUNOLOGY

R loops: new modulators of genome dynamics and function

(2015) José M. Santos-Pereira et al.   NATURE REVIEWS GENETICS

R loops regulate promoter-proximal chromatin architecture and cellular differentiation

(2015) Poshen B Chen et al.   NATURE STRUCTURAL & MOLECULAR BIOLOGY

QmRLFS-finder: a model, web server and stand-alone tool for prediction and analysis of R-loop forming sequences

(2015) Piroon Jenjaroenpun et al.   NUCLEIC ACIDS RESEARCH

Head-to-head antisense transcription and R-loop formation promotes transcriptional activation

(2015) Raquel Boque-Sastre et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

Telomere elongation chooses TERRA ALTernatives

(2015) Rajika Arora et al.   RNA Biology

RNA:DNA hybrids in the human genome have distinctive nucleotide characteristics, chromatin composition, and transcriptional relationships

(2015) Julie Nadel et al.   Epigenetics & Chromatin

R loops regulate promoter-proximal chromatin architecture and cellular differentiation

(2015) Poshen B Chen et al.   NATURE STRUCTURAL & MOLECULAR BIOLOGY

Genome-wide DNA hypomethylation and RNA:DNA hybrid accumulation in Aicardi–Goutières syndrome

(2015) Yoong Wearn Lim et al.   eLife

Systematic screening reveals a role for BRCA1 in the response to transcription-associated DNA damage

(2014) Sarah J. Hill et al.   GENES & DEVELOPMENT

The yeast and human FACT chromatin-reorganizing complexes solve R-loop-mediated transcription-replication conflicts

(2014) E. Herrera-Moyano et al.   GENES & DEVELOPMENT

A double-edged sword: R loops as threats to genome integrity and powerful regulators of gene expression

(2014) K. Skourti-Stathaki et al.   GENES & DEVELOPMENT

Transcription-Coupled Nucleotide Excision Repair Factors Promote R-Loop-Induced Genome Instability

(2014) Julie Sollier et al.   MOLECULAR CELL

Arginine Methylation Facilitates the Recruitment of TOP3B to Chromatin to Prevent R Loop Accumulation

(2014) Yanzhong Yang et al.   MOLECULAR CELL

R-loops induce repressive chromatin marks over mammalian gene terminators

(2014) Konstantina Skourti-Stathaki et al.   NATURE

C9orf72 nucleotide repeat structures initiate molecular cascades of disease

(2014) Aaron R. Haeusler et al.   NATURE

BRCA2 prevents R-loop accumulation and associates with TREX-2 mRNA export factor PCID2

(2014) Vaibhav Bhatia et al.   NATURE

Processing of double-R-loops in (CAG)·(CTG) and C9orf72 (GGGGCC)·(GGCCCC) repeats causes instability

(2014) Kaalak Reddy et al.   NUCLEIC ACIDS RESEARCH

DNA damage triggers SAF-A and RNA biogenesis factors exclusion from chromatin coupled to R-loops removal

(2014) Sébastien Britton et al.   NUCLEIC ACIDS RESEARCH

R-Loops in Proliferating Cells but Not in the Brain: Implications for AOA2 and Other Autosomal Recessive Ataxias

(2014) Abrey J. Yeo et al.   PLoS One

RNaseH1 regulates TERRA-telomeric DNA hybrids and telomere maintenance in ALT tumour cells

(2014) Rajika Arora et al.   Nature Communications

Out of Balance: R-loops in Human Disease

(2014) Matthias Groh et al.   PLoS Genetics

R-loops Associated with Triplet Repeat Expansions Promote Gene Silencing in Friedreich Ataxia and Fragile X Syndrome

(2014) Matthias Groh et al.   PLoS Genetics

Genome-Wide Distribution of RNA-DNA Hybrids Identifies RNase H Targets in tRNA Genes, Retrotransposons and Mitochondria

(2014) Aziz El Hage et al.   PLoS Genetics

Transcription-Associated R-Loop Formation across the Human FMR1 CGG-Repeat Region

(2014) Erick W. Loomis et al.   PLoS Genetics

A Novel Mechanism Inducing Genome Instability in Kaposi's Sarcoma-Associated Herpesvirus Infected Cells

(2014) Brian R. Jackson et al.   PLoS Pathogens

The THO complex component Thp2 counteracts telomeric R-loops and telomere shortening

(2013) Verena Pfeiffer et al.   EMBO JOURNAL

The sub-nanomolar binding of DNA-RNA hybrids by the single-chain Fv fragment of antibody S9.6

(2013) Damilola D. Phillips et al.   JOURNAL OF MOLECULAR RECOGNITION

R Loops Are Linked to Histone H3 S10 Phosphorylation and Chromatin Condensation

(2013) Maikel Castellano-Pozo et al.   MOLECULAR CELL

Telomeric RNA-DNA hybrids affect telomere-length dynamics and senescence

(2013) Bettina Balk et al.   NATURE STRUCTURAL & MOLECULAR BIOLOGY

R-loop formation atSnord116mediates topotecan inhibition ofUbe3a-antisenseand allele-specific chromatin decondensation

(2013) Weston T. Powell et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

Senataxin Plays an Essential Role with DNA Damage Response Proteins in Meiotic Recombination and Gene Silencing

(2013) Olivier J. Becherel et al.   PLoS Genetics

Senataxin Associates with Replication Forks to Protect Fork Integrity across RNA-Polymerase-II-Transcribed Genes

(2012) Amaya Alzu et al.   CELL

R-loop-mediated genome instability in mRNA cleavage and polyadenylation mutants

(2012) P. C. Stirling et al.   GENES & DEVELOPMENT

DNA-RNA hybrid formation mediates RNAi-directed heterochromatin formation

(2012) Mina Nakama et al.   GENES TO CELLS

R-Loop Formation Is a Distinctive Characteristic of Unmethylated Human CpG Island Promoters

(2012) Paul A. Ginno et al.   MOLECULAR CELL

R Loops: From Transcription Byproducts to Threats to Genome Stability

(2012) Andrés Aguilera et al.   MOLECULAR CELL

A Programmable Dual-RNA-Guided DNA Endonuclease in Adaptive Bacterial Immunity

(2012) M. Jinek et al.   SCIENCE

Human DHX9 helicase preferentially unwinds RNA-containing displacement loops (R-loops) and G-quadruplexes

(2011) Prasun Chakraborty et al.   DNA REPAIR

Genome-wide function of THO/TREX in active genes prevents R-loop-dependent replication obstacles

(2011) Belén Gómez-González et al.   EMBO JOURNAL

RNase H and Multiple RNA Biogenesis Factors Cooperate to Prevent RNA:DNA Hybrids from Generating Genome Instability

(2011) Lamia Wahba et al.   MOLECULAR CELL

Yeast Sen1 Helicase Protects the Genome from Transcription-Associated Instability

(2011) Hannah E. Mischo et al.   MOLECULAR CELL

Human Senataxin Resolves RNA/DNA Hybrids Formed at Transcriptional Pause Sites to Promote Xrn2-Dependent Termination

(2011) Konstantina Skourti-Stathaki et al.   MOLECULAR CELL

Genome Instability and Transcription Elongation Impairment in Human Cells Depleted of THO/TREX

(2011) María S. Domínguez-Sánchez et al.   PLoS Genetics

Loss of Topoisomerase I leads to R-loop-mediated transcriptional blocks during ribosomal RNA synthesis

(2010) A. El Hage et al.   GENES & DEVELOPMENT

Mechanisms of trinucleotide repeat instability during human development

(2010) Cynthia T. McMurray   NATURE REVIEWS GENETICS

ATR/Mec1: coordinating fork stability and repair

(2009) Anna M Friedel et al.   CURRENT OPINION IN CELL BIOLOGY

Ribonuclease H: the enzymes in eukaryotes

(2009) Susana M. Cerritelli et al.   FEBS Journal

Topoisomerase I suppresses genomic instability by preventing interference between replication and transcription

(2009) Sandie Tuduri et al.   NATURE CELL BIOLOGY

R loops stimulate genetic instability of CTG{middle dot}CAG repeats

(2009) Y. Lin et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

New insights into the biology of Wiskott-Aldrich syndrome (WAS)

(2009) A. J. Thrasher   Hematology-American Society of Hematology Education Program

Molecular recognition of a DNA:RNA hybrid: Sub-nanomolar binding by a neomycin–methidium conjugate

(2008) Nicholas N. Shaw et al.   BIOORGANIC & MEDICINAL CHEMISTRY LETTERS

Biogenesis of mRNPs: integrating different processes in the eukaryotic nucleus

(2008) Rosa Luna et al.   CHROMOSOMA

3′ end mRNA processing: molecular mechanisms and implications for health and disease

(2008) Sven Danckwardt et al.   EMBO JOURNAL