R-Loops at Chromosome Ends: From Formation, Regulation, and Cellular Consequence

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

(2022) Qingqing Yan et al.   Nature Communications

Regulation of Replication Stress in Alternative Lengthening of Telomeres by Fanconi Anaemia Protein

(2022) Duda Li et al.   Genes

Walking a tightrope: The complex balancing act of R-loops in genome stability

(2022) Joshua R. Brickner et al.   MOLECULAR CELL

Sources, resolution and physiological relevance of R-loops and RNA–DNA hybrids

(2022) Eva Petermann et al.   NATURE REVIEWS MOLECULAR CELL BIOLOGY

ADAR1 and its implications in cancer development and treatment

(2022) Allison R. Baker et al.   TRENDS IN GENETICS

Telomere Interacting Proteins and TERRA Regulation

(2022) Lara Pérez-Martínez et al.   Frontiers in Genetics

RAD51AP1 regulates ALT-HDR through chromatin-directed homeostasis of TERRA

(2022) Nicole Kaminski et al.   MOLECULAR CELL

TERRA and RAD51AP1 promote alternative lengthening of telomeres through an R- to D-loop switch

(2022) Tribhuwan Yadav et al.   MOLECULAR CELL

METTL3-mediated m6A modification stabilizes TERRA and maintains telomere stability

(2022) Liping Chen et al.   NUCLEIC ACIDS RESEARCH

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

(2022) Essak S. Khan et al.   Genes

ADAR1 RNA editing enzyme regulates R-loop formation and genome stability at telomeres in cancer cells

(2021) Yusuke Shiromoto et al.   Nature Communications

TERRA G-quadruplex RNA interaction with TRF2 GAR domain is required for telomere integrity

(2021) Yang Mei et al.   Scientific Reports

RNA transcripts stimulate homologous recombination by forming DR-loops

(2021) Jian Ouyang et al.   NATURE

The SWI/SNF chromatin remodeling complex helps resolve R-loop-mediated transcription–replication conflicts

(2021) Aleix Bayona-Feliu et al.   NATURE GENETICS

RTEL1 influences the abundance and localization of TERRA RNA

(2021) Fiorella Ghisays et al.   Nature Communications

BRCA1 binds TERRA RNA and suppresses R-Loop-based telomeric DNA damage

(2021) Jekaterina Vohhodina et al.   Nature Communications

The Ultimate (Mis)match: When DNA Meets RNA

(2021) Benoit Palancade et al.   Cells

Keeping Balance Between Genetic Stability and Plasticity at the Telomere and Subtelomere of Trypanosoma brucei

(2021) Bibo Li   Frontiers in Cell and Developmental Biology

Human subtelomeric DNA methylation: regulation and roles in telomere function

(2020) Shir Toubiana et al.   CURRENT OPINION IN GENETICS & DEVELOPMENT

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

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

TRF1 averts chromatin remodelling, recombination and replication dependent-break induced replication at mouse telomeres

(2020) Rosa Maria Porreca et al.   eLife

RTEL1 suppresses G-quadruplex-associated R-loops at difficult-to-replicate loci in the human genome

(2020) Wei Wu et al.   NATURE STRUCTURAL & MOLECULAR BIOLOGY

Alternative lengthening of telomeres: from molecular mechanisms to therapeutic outlooks

(2020) Jia-Min Zhang et al.   Cell and Bioscience

Human RTEL1 associates with Poldip3 to facilitate responses to replication stress and R-loop resolution

(2020) Andrea Björkman et al.   GENES & DEVELOPMENT

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

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

TRF2 recruits nucleolar protein TCOF1 to coordinate telomere transcription and replication

(2020) Xin Nie et al.   CELL DEATH AND DIFFERENTIATION

Re‐equilibration of imbalanced NAD metabolism ameliorates the impact of telomere dysfunction

(2020) Chongkui Sun et al.   EMBO JOURNAL

RAD51-dependent recruitment of TERRA lncRNA to telomeres through R-loops

(2020) Marianna Feretzaki et al.   NATURE

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

RTEL1 Regulates G4/R-Loops to Avert Replication-Transcription Collisions

(2020) Panagiotis Kotsantis et al.   Cell Reports

SFPQ and NONO suppress RNA:DNA-hybrid-related telomere instability

(2019) Eleonora Petti et al.   Nature Communications

R-Loops as Cellular Regulators and Genomic Threats

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

Targeted and Persistent 8-Oxoguanine Base Damage at Telomeres Promotes Telomere Loss and Crisis

(2019) Elise Fouquerel 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

BRCA1-associated R-loop affects transcription and differentiation in breast luminal epithelial cells

(2019) Huai-Chin Chiang et al.   NUCLEIC ACIDS RESEARCH

The mitochondrial R-loop

(2019) Ian J Holt   NUCLEIC ACIDS RESEARCH

The FANCM-BLM-TOP3A-RMI complex suppresses alternative lengthening of telomeres (ALT)

(2019) Robert Lu et al.   Nature Communications

FANCM limits ALT activity by restricting telomeric replication stress induced by deregulated BLM and R-loops

(2019) Bruno Silva et al.   Nature Communications

TERRA regulate the transcriptional landscape of pluripotent cells through TRF1-dependent recruitment of PRC2

(2019) Rosa María Marión et al.   eLife

R Loops: From Physiological to Pathological Roles

(2019) Tatiana García-Muse et al.   CELL

DNA methylation in disease: Immunodeficiency, Centromeric instability, Facial anomalies syndrome

(2019) Maja Vukic et al.   Essays in Biochemistry

Systematic bromodomain protein screens identify homologous recombination and R-loop suppression pathways involved in genome integrity

(2019) Jae Jin Kim et al.   GENES & DEVELOPMENT

An R-loop-initiated CSB–RAD52–POLD3 pathway suppresses ROS-induced telomeric DNA breaks

(2019) Jun Tan et al.   NUCLEIC ACIDS RESEARCH

FANCM suppresses DNA replication stress at ALT telomeres by disrupting TERRA R-loops

(2019) Xiaolei Pan et al.   Scientific Reports

A-to-I RNA editing — immune protector and transcriptome diversifier

(2018) Eli Eisenberg et al.   NATURE REVIEWS GENETICS

TRF1 participates in chromosome end protection by averting TRF2-dependent telomeric R loops

(2018) Yong Woo Lee et al.   NATURE STRUCTURAL & MOLECULAR BIOLOGY

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

(2018) Sarah Cohen et al.   Nature Communications

TRF1 participates in chromosome end protection by averting TRF2-dependent telomeric R loops

(2018) Yong Woo Lee et al.   NATURE STRUCTURAL & MOLECULAR BIOLOGY

RNA/DNA Hybrid Interactome Identifies DXH9 as a Molecular Player in Transcriptional Termination and R-Loop-Associated DNA Damage

(2018) Agnese Cristini et al.   Cell Reports

Shelterin-Mediated Telomere Protection

(2018) Titia de Lange   Annual Review of Genetics

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

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

Human proteins that interact with RNA/DNA hybrids

(2018) Isabel X. Wang et al.   GENOME RESEARCH

The DEAD-box protein Dbp2p is linked to non-coding RNAs, the helicase Sen1p, and R-loops

(2018) Frank A. Tedeschi et al.   RNA

Loss of ADAR1 in tumours overcomes resistance to immune checkpoint blockade

(2018) Jeffrey J. Ishizuka et al.   NATURE

DHX9 helicase promotes R-loop formation in cells with impaired RNA splicing

(2018) Prasun Chakraborty et al.   Nature Communications

Non-random length distribution of individual telomeres in immunodeficiency, centromeric instability and facial anomalies syndrome, type I

(2017) Shira Sagie et al.   HUMAN MOLECULAR GENETICS

Trypanosoma brucei RAP1 maintains telomere and subtelomere integrity by suppressing TERRA and telomeric RNA:DNA hybrids

(2017) Vishal Nanavaty et al.   NUCLEIC ACIDS RESEARCH

FANCM, BRCA1, and BLM cooperatively resolve the replication stress at the ALT telomeres

(2017) Xiaolei Pan et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

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

(2017) Shira Sagie et al.   Nature Communications

Attenuation of RNA polymerase II pausing mitigates BRCA1-associated R-loop accumulation and tumorigenesis

(2017) Xiaowen Zhang et al.   Nature Communications

Life and cancer without telomerase: ALT and other strategies for making sure ends (don’t) meet

(2016) Manasi S. Apte et al.   CRITICAL REVIEWS IN BIOCHEMISTRY AND MOLECULAR BIOLOGY

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

(2016) Lamia Wahba et al.   GENES & DEVELOPMENT

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

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

Break-induced telomere synthesis underlies alternative telomere maintenance

(2016) Robert L. Dilley et al.   NATURE

Transcription–replication conflicts: how they occur and how they are resolved

(2016) Tatiana García-Muse et al.   NATURE REVIEWS MOLECULAR CELL BIOLOGY

The DBHS proteins SFPQ, NONO and PSPC1: a multipurpose molecular scaffold

(2016) Gavin J. Knott et al.   NUCLEIC ACIDS RESEARCH

Alternative lengthening of telomeres and loss of ATRX are frequent events in pleomorphic and dedifferentiated liposarcomas

(2015) Jen-Chieh Lee et al.   MODERN PATHOLOGY

The Fanconi Anemia Pathway Maintains Genome Stability by Coordinating Replication and Transcription

(2015) Rebekka A. Schwab et al.   MOLECULAR CELL

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

(2015) Elodie Hatchi et al.   MOLECULAR CELL

A-to-I editing of coding and non-coding RNAs by ADARs

(2015) Kazuko Nishikura   NATURE REVIEWS MOLECULAR CELL BIOLOGY

Alternative lengthening of telomeres renders cancer cells hypersensitive to ATR inhibitors

(2015) R. L. Flynn et al.   SCIENCE

Homologous Recombination and Human Health: The Roles of BRCA1, BRCA2, and Associated Proteins

(2015) Rohit Prakash et al.   Cold Spring Harbor Perspectives in Biology

Frequent ATRX, CIC, FUBP1 and IDH1 mutations refine the classification of malignant gliomas

(2015) Yuchen Jiao et al.   Oncotarget

Whole-exome sequencing identifies ATRX mutation as a key molecular determinant in lower-grade glioma

(2015) Kasthuri Kannan et al.   Oncotarget

Mechanism and regulation of incisions during DNA interstrand cross-link repair

(2014) Jieqiong Zhang et al.   DNA REPAIR

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

Induced pluripotent stem cells as a model for telomeric abnormalities in ICF type I syndrome

(2014) Shira Sagie et al.   HUMAN MOLECULAR GENETICS

Multiple Interactions of the Intrinsically Disordered Region between the Helicase and Nuclease Domains of the Archaeal Hef Protein

(2014) Sonoko Ishino et al.   JOURNAL OF BIOLOGICAL CHEMISTRY

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

(2014) Julie Sollier et al.   MOLECULAR CELL

Alternative Lengthening of Telomeres is characterized by reduced compaction of telomeric chromatin

(2014) Harikleia Episkopou et al.   NUCLEIC ACIDS RESEARCH

Association of BLM and BRCA1 during Telomere Maintenance in ALT Cells

(2014) Samir Acharya et al.   PLoS One

The differential processing of telomeres in response to increased telomeric transcription and RNA–DNA hybrid accumulation

(2014) Bettina Balk et al.   RNA Biology

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

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

(2013) Verena Pfeiffer et al.   EMBO JOURNAL

Heterogeneous clinical presentation in ICF syndrome: correlation with underlying gene defects

(2013) Corry MR Weemaes et al.   EUROPEAN JOURNAL OF HUMAN GENETICS

GC skew at the 5' and 3' ends of human genes links R-loop formation to epigenetic regulation and transcription termination

(2013) P. A. Ginno et al.   GENOME RESEARCH

Fanconi anaemia and the repair of Watson and Crick DNA crosslinks

(2013) Molly C. Kottemann et al.   NATURE

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

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

BRCA1 in the DNA damage response and at telomeres

(2013) Eliot M. Rosen   Frontiers in Genetics

Characterization and rescue of telomeric abnormalities in ICF syndrome type I fibroblasts

(2013) Shiran Yehezkel et al.   Frontiers in Oncology

Association of Age at Diagnosis and Genetic Mutations in Patients With Neuroblastoma

(2012) Nai-Kong V. Cheung   JAMA-JOURNAL OF THE AMERICAN MEDICAL ASSOCIATION

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

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

Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma

(2012) Jeremy Schwartzentruber et al.   NATURE

Loss of Wild-Type ATRX Expression in Somatic Cell Hybrids Segregates with Activation of Alternative Lengthening of Telomeres

(2012) Kylie Bower et al.   PLoS One

FANCM Limits Meiotic Crossovers

(2012) W. Crismani et al.   SCIENCE

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

(2012) M. Jinek et al.   SCIENCE

Loss of ATRX, Genome Instability, and an Altered DNA Damage Response Are Hallmarks of the Alternative Lengthening of Telomeres Pathway

(2012) Courtney A. Lovejoy et al.   PLoS Genetics

Prevalence of the Alternative Lengthening of Telomeres Telomere Maintenance Mechanism in Human Cancer Subtypes

(2011) Christopher M. Heaphy et al.   AMERICAN JOURNAL OF PATHOLOGY

TERRA, CpG methylation, and telomere heterochromatin: Lessons from ICF syndrome cells

(2011) Zhong Deng et al.   CELL CYCLE

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

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

R-loop-mediated genomic instability is caused by impairment of replication fork progression

(2011) W. Gan et al.   GENES & DEVELOPMENT

Collisions between Replication and Transcription Complexes Cause Common Fragile Site Instability at the Longest Human Genes

(2011) Anne Helmrich 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

Telomere dysfunction induces metabolic and mitochondrial compromise

(2011) Ergün Sahin et al.   NATURE

Combinatorial readout of histone H3 modifications specifies localization of ATRX to heterochromatin

(2011) Sebastian Eustermann et al.   NATURE STRUCTURAL & MOLECULAR BIOLOGY

Quantitative model of R-loop forming structures reveals a novel level of RNA-DNA interactome complexity

(2011) T. Wongsurawat et al.   NUCLEIC ACIDS RESEARCH

Altered Telomeres in Tumors with ATRX and DAXX Mutations

(2011) C. M. Heaphy et al.   SCIENCE

The p53/p21WAF/CIP Pathway Mediates Oxidative Stress and Senescence in Dyskeratosis Congenita Cells with Telomerase Insufficiency

(2010) Erik R. Westin et al.   ANTIOXIDANTS & REDOX SIGNALING

Distinct Factors Control Histone Variant H3.3 Localization at Specific Genomic Regions

(2010) Aaron D. Goldberg et al.   CELL

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

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

Reactive species and DNA damage in chronic inflammation: reconciling chemical mechanisms and biological fates

(2010) Pallavi Lonkar et al.   INTERNATIONAL JOURNAL OF CANCER

Molecular Dissection of Telomeric Repeat-Containing RNA Biogenesis Unveils the Presence of Distinct and Multiple Regulatory Pathways

(2010) A. Porro et al.   MOLECULAR AND CELLULAR BIOLOGY

Telomeres: protecting chromosomes against genome instability

(2010) Roderick J. O'Sullivan et al.   NATURE REVIEWS MOLECULAR CELL BIOLOGY

Daxx is an H3.3-specific histone chaperone and cooperates with ATRX in replication-independent chromatin assembly at telomeres

(2010) P. W. Lewis et al.   PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA

Characterization of Oxidative Guanine Damage and Repair in Mammalian Telomeres

(2010) Zhilong Wang et al.   PLoS Genetics

Ribonuclease H: the enzymes in eukaryotes

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

Fancm-deficient mice reveal unique features of Fanconi anemia complementation group M

(2009) Sietske T. Bakker et al.   HUMAN MOLECULAR GENETICS

BRCA1 Localization to the Telomere and Its Loss from the Telomere in Response to DNA Damage

(2009) Rahul D. Ballal et al.   JOURNAL OF BIOLOGICAL CHEMISTRY

G Clustering Is Important for the Initiation of Transcription-Induced R-Loops In Vitro, whereas High G Density without Clustering Is Sufficient Thereafter

(2009) D. Roy et al.   MOLECULAR AND CELLULAR BIOLOGY

TERRA RNA Binding to TRF2 Facilitates Heterochromatin Formation and ORC Recruitment at Telomeres

(2009) Zhong Deng et al.   MOLECULAR CELL

FANCM Connects the Genome Instability Disorders Bloom's Syndrome and Fanconi Anemia

(2009) Andrew J. Deans et al.   MOLECULAR CELL

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

(2009) Sandie Tuduri et al.   NATURE CELL BIOLOGY

Telomerase activity is associated with an increase in DNA methylation at the proximal subtelomere and a reduction in telomeric transcription

(2009) Laura J. Ng et al.   NUCLEIC ACIDS RESEARCH

CpG-island promoters drive transcription of human telomeres

(2009) S. G. Nergadze et al.   RNA

Hypomethylation of subtelomeric regions in ICF syndrome is associated with abnormally short telomeres and enhanced transcription from telomeric regions

(2008) Shiran Yehezkel et al.   HUMAN MOLECULAR GENETICS