Structural basis of R-loop recognition by the S9.6 monoclonal antibody

Bou-Nader, Charles; Bothra, Ankur; Garboczi, David N.; Leppla, Stephen H.; Zhang, Jinwei

doi:10.1038/s41467-022-29187-7

Structural basis of R-loop recognition by the S9.6 monoclonal antibody

Journal Article · Mon Mar 28 00:00:00 EDT 2022 · Nature Communications

DOI:https://doi.org/10.1038/s41467-022-29187-7· OSTI ID:1861863

^[1]; Bothra, Ankur ^[2]; Garboczi, David N. ^[2]; Leppla, Stephen H. ^[2]; ^[1]

National Institutes of Health (NIH), Bethesda, MD (United States). National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK)
National Institutes of Health (NIH), Bethesda, MD (United States). National Institute of Allergy and Infectious Diseases (NIAID)

R-loops are ubiquitous, dynamic nucleic-acid structures that play fundamental roles in DNA replication and repair, chromatin and transcription regulation, as well as telomere maintenance. The DNA-RNA hybrid–specific S9.6 monoclonal antibody is widely used to map R-loops. Here, we report crystal structures of a S9.6 antigen-binding fragment (Fab) free and bound to a 13-bp hybrid duplex. We demonstrate that S9.6 exhibits robust selectivity in binding hybrids over double-stranded (ds) RNA and in categorically rejecting dsDNA. S9.6 asymmetrically recognizes a compact epitope of two consecutive RNA nucleotides via their 2'-hydroxyl groups and six consecutive DNA nucleotides via their backbone phosphate and deoxyribose groups. Recognition is mediated principally by aromatic and basic residues of the S9.6 heavy chain, which closely track the curvature of the hybrid minor groove. These findings reveal the molecular basis for S9.6 recognition of R-loops, detail its binding specificity, identify a new hybrid-recognition strategy, and provide a framework for S9.6 protein engineering.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institute of Allergy and Infectious Diseases (NIAID); National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK); National Institutes of Health (NIH); USDOE Office of Science (SC)

Grant/Contract Number:: W-31109-ENG-38

OSTI ID:: 1861863

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 13; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (81)

The sub-nanomolar binding of DNA-RNA hybrids by the single-chain Fv fragment of antibody S9.6: ANTIBODY RECOGNITION OF DNA-RNA HYBRIDS Phillips, Damilola D.; Garboczi, David N.; Singh, Kavita Journal of Molecular Recognition, Vol. 26, Issue 8 https://doi.org/10.1002/jmr.2284	journal	June 2013
Characterization of monoclonal antibody to DNA · RNA and its application to immunodetection of hybrids Boguslawski, Sophie J.; Smith, Dennis E.; Michalak, Mary A. Journal of Immunological Methods, Vol. 89, Issue 1 https://doi.org/10.1016/0022-1759(86)90040-2	journal	May 1986
Impairment of transcription elongation by R-loops in vitro Tous, Cristina; Aguilera, Andrés Biochemical and Biophysical Research Communications, Vol. 360, Issue 2 https://doi.org/10.1016/j.bbrc.2007.06.098	journal	August 2007
Structural Flexibility of DNA-RNA Hybrid Duplex: Stretching and Twist-Stretch Coupling Liu, Ju-Hui; Xi, Kun; Zhang, Xi Biophysical Journal, Vol. 117, Issue 1 https://doi.org/10.1016/j.bpj.2019.05.018	journal	July 2019
Crystal Structures of RNase H Bound to an RNA/DNA Hybrid: Substrate Specificity and Metal-Dependent Catalysis Nowotny, Marcin; Gaidamakov, Sergei A.; Crouch, Robert J. Cell, Vol. 121, Issue 7 https://doi.org/10.1016/j.cell.2005.04.024	journal	July 2005
Structural Basis of Transcription: Role of the Trigger Loop in Substrate Specificity and Catalysis Wang, Dong; Bushnell, David A.; Westover, Kenneth D. Cell, Vol. 127, Issue 5 https://doi.org/10.1016/j.cell.2006.11.023	journal	December 2006
Structural Basis for dsRNA Recognition, Filament Formation, and Antiviral Signal Activation by MDA5 Wu, Bin; Peisley, Alys; Richards, Claire Cell, Vol. 152, Issue 1-2 https://doi.org/10.1016/j.cell.2012.11.048	journal	January 2013
R Loops: From Physiological to Pathological Roles García-Muse, Tatiana; Aguilera, Andrés Cell, Vol. 179, Issue 3 https://doi.org/10.1016/j.cell.2019.08.055	journal	October 2019
Human DHX9 helicase preferentially unwinds RNA-containing displacement loops (R-loops) and G-quadruplexes Chakraborty, Prasun; Grosse, Frank DNA Repair, Vol. 10, Issue 6 https://doi.org/10.1016/j.dnarep.2011.04.013	journal	June 2011
RNases H: Structure and mechanism Hyjek, Malwina; Figiel, Małgorzata; Nowotny, Marcin DNA Repair, Vol. 84 https://doi.org/10.1016/j.dnarep.2019.102672	journal	December 2019
Defining R-loop classes and their contributions to genome instability Castillo-Guzman, Daisy; Chédin, Frédéric DNA Repair, Vol. 106 https://doi.org/10.1016/j.dnarep.2021.103182	journal	October 2021
Ultra-deep Coverage Single-molecule R-loop Footprinting Reveals Principles of R-loop Formation Malig, Maika; Hartono, Stella R.; Giafaglione, Jenna M. Journal of Molecular Biology, Vol. 432, Issue 7 https://doi.org/10.1016/j.jmb.2020.02.014	journal	March 2020
Cotranscriptionally Formed DNA:RNA Hybrids Mediate Transcription Elongation Impairment and Transcription-Associated Recombination Huertas, Pablo; Aguilera, Andrés Molecular Cell, Vol. 12, Issue 3 https://doi.org/10.1016/j.molcel.2003.08.010	journal	September 2003
Structure of Human RNase H1 Complexed with an RNA/DNA Hybrid: Insight into HIV Reverse Transcription Nowotny, Marcin; Gaidamakov, Sergei A.; Ghirlando, Rodolfo Molecular Cell, Vol. 28, Issue 2 https://doi.org/10.1016/j.molcel.2007.08.015	journal	October 2007
Human Senataxin Resolves RNA/DNA Hybrids Formed at Transcriptional Pause Sites to Promote Xrn2-Dependent Termination Skourti-Stathaki, Konstantina; Proudfoot, Nicholas J.; Gromak, Natalia Molecular Cell, Vol. 42, Issue 6 https://doi.org/10.1016/j.molcel.2011.04.026	journal	June 2011
R-Loop Formation Is a Distinctive Characteristic of Unmethylated Human CpG Island Promoters Ginno, Paul A.; Lott, Paul L.; Christensen, Holly C. Molecular Cell, Vol. 45, Issue 6 https://doi.org/10.1016/j.molcel.2012.01.017	journal	March 2012
Regulated Formation of lncRNA-DNA Hybrids Enables Faster Transcriptional Induction and Environmental Adaptation Cloutier, Sara C.; Wang, Siwen; Ma, Wai Kit Molecular Cell, Vol. 61, Issue 3 https://doi.org/10.1016/j.molcel.2015.12.024	journal	February 2016
Prevalent, Dynamic, and Conserved R-Loop Structures Associate with Specific Epigenomic Signatures in Mammals Sanz, Lionel A.; Hartono, Stella R.; Lim, Yoong Wearn Molecular Cell, Vol. 63, Issue 1 https://doi.org/10.1016/j.molcel.2016.05.032	journal	July 2016
Senataxin Mutation Reveals How R-Loops Promote Transcription by Blocking DNA Methylation at Gene Promoters Grunseich, Christopher; Wang, Isabel X.; Watts, Jason A. Molecular Cell, Vol. 69, Issue 3 https://doi.org/10.1016/j.molcel.2017.12.030	journal	February 2018
R-Loops as Cellular Regulators and Genomic Threats Crossley, Madzia P.; Bocek, Michael; Cimprich, Karlene A. Molecular Cell, Vol. 73, Issue 3 https://doi.org/10.1016/j.molcel.2019.01.024	journal	February 2019
R-Loops Promote Antisense Transcription across the Mammalian Genome Tan-Wong, Sue Mei; Dhir, Somdutta; Proudfoot, Nick J. Molecular Cell, Vol. 76, Issue 4 https://doi.org/10.1016/j.molcel.2019.10.002	journal	November 2019
SEDPHAT – A platform for global ITC analysis and global multi-method analysis of molecular interactions Zhao, Huaying; Piszczek, Grzegorz; Schuck, Peter Methods, Vol. 76 https://doi.org/10.1016/j.ymeth.2014.11.012	journal	April 2015
Relative Thermodynamic Stability of DNA, RNA, and DNA:RNA Hybrid Duplexes: Relationship with Base Composition and Structure Lesnik, Elena A.; Freier, Susan M. Biochemistry, Vol. 34, Issue 34 https://doi.org/10.1021/bi00034a013	journal	August 1995
Sequence Specific Thermodynamic and Structural Properties for DNA.cntdot.RNA Duplexes Ratmeyer, Lynda; Vinayak, Ravi; Zhong, Yi Yi Biochemistry, Vol. 33, Issue 17 https://doi.org/10.1021/bi00183a037	journal	May 1994
Comparison of the Thermodynamic Stabilities and Solution Conformations of DNA·RNA Hybrids Containing Purine-Rich and Pyrimidine-Rich Strands with DNA and RNA Duplexes Gyi, Jeffrey I.; Conn, Graeme L.; Lane, Andrew N. Biochemistry, Vol. 35, Issue 38 https://doi.org/10.1021/bi960948z	journal	January 1996
Mechanical Identities of RNA and DNA Double Helices Unveiled at the Single-Molecule Level Herrero-Galán, Elías; Fuentes-Perez, Maria Eugenia; Carrasco, Carolina Journal of the American Chemical Society, Vol. 135, Issue 1 https://doi.org/10.1021/ja3054755	journal	December 2012
Specific recognition of RNA/DNA hybrid and enhancement of human RNase H1 activity by HBD Nowotny, Marcin; Cerritelli, Susana M.; Ghirlando, Rodolfo The EMBO Journal, Vol. 27, Issue 7 https://doi.org/10.1038/emboj.2008.44	journal	March 2008
Structural basis for substrate loading in bacterial RNA polymerase Vassylyev, Dmitry G.; Vassylyeva, Marina N.; Zhang, Jinwei Nature, Vol. 448, Issue 7150 https://doi.org/10.1038/nature05931	journal	June 2007
Effects of cytosine modifications on DNA flexibility and nucleosome mechanical stability Ngo, Thuy T. M.; Yoo, Jejoong; Dai, Qing Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms10813	journal	February 2016
Dynamic transcriptome of Schizosaccharomyces pombe shown by RNA-DNA hybrid mapping Dutrow, Natalie; Nix, David A.; Holt, Derick Nature Genetics, Vol. 40, Issue 8 https://doi.org/10.1038/ng.196	journal	July 2008
m6A promotes R-loop formation to facilitate transcription termination Yang, Xin; Liu, Qian-Lan; Xu, Wei Cell Research, Vol. 29, Issue 12 https://doi.org/10.1038/s41422-019-0235-7	journal	October 2019
Crystal structure of an adenovirus virus-associated RNA Hood, Iris V.; Gordon, Jackson M.; Bou-Nader, Charles Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10752-6	journal	June 2019
A conserved RNA structural motif for organizing topology within picornaviral internal ribosome entry sites Koirala, Deepak; Shao, Yaming; Koldobskaya, Yelena Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11585-z	journal	August 2019
The R-loop is a common chromatin feature of the Arabidopsis genome Xu, Wei; Xu, Hui; Li, Kuan Nature Plants, Vol. 3, Issue 9 https://doi.org/10.1038/s41477-017-0004-x	journal	August 2017
Regulatory R-loops as facilitators of gene expression and genome stability Niehrs, Christof; Luke, Brian Nature Reviews Molecular Cell Biology, Vol. 21, Issue 3 https://doi.org/10.1038/s41580-019-0206-3	journal	January 2020
New insights into the role of antinuclear antibodies in systemic lupus erythematosus Pisetsky, David S.; Lipsky, Peter E. Nature Reviews Rheumatology, Vol. 16, Issue 10 https://doi.org/10.1038/s41584-020-0480-7	journal	September 2020
RAD51-dependent recruitment of TERRA lncRNA to telomeres through R-loops Feretzaki, Marianna; Pospisilova, Michaela; Valador Fernandes, Rita Nature, Vol. 587, Issue 7833 https://doi.org/10.1038/s41586-020-2815-6	journal	October 2020
GADD45A binds R-loops and recruits TET1 to CpG island promoters Arab, Khelifa; Karaulanov, Emil; Musheev, Michael Nature Genetics, Vol. 51, Issue 2 https://doi.org/10.1038/s41588-018-0306-6	journal	January 2019
N6-methyladenosine regulates the stability of RNA:DNA hybrids in human cells Abakir, Abdulkadir; Giles, Tom C.; Cristini, Agnese Nature Genetics, Vol. 52, Issue 1 https://doi.org/10.1038/s41588-019-0549-x	journal	December 2019
R-ChIP for genome-wide mapping of R-loops by using catalytically inactive RNASEH1 Chen, Jia-Yu; Zhang, Xuan; Fu, Xiang-Dong Nature Protocols, Vol. 14, Issue 5 https://doi.org/10.1038/s41596-019-0154-6	journal	April 2019
High-resolution, strand-specific R-loop mapping via S9.6-based DNA–RNA immunoprecipitation and high-throughput sequencing Sanz, Lionel A.; Chédin, Frédéric Nature Protocols, Vol. 14, Issue 6 https://doi.org/10.1038/s41596-019-0159-1	journal	May 2019
Activation-induced cytidine deaminase action is strongly stimulated by mutations of the THO complex Gómez-González, Belén; Aguilera, Andrés Proceedings of the National Academy of Sciences, Vol. 104, Issue 20 https://doi.org/10.1073/pnas.0702836104	journal	May 2007
Synthetic antibodies for specific recognition and crystallization of structured RNA Ye, J. -D.; Tereshko, V.; Frederiksen, J. K. Proceedings of the National Academy of Sciences, Vol. 105, Issue 1 https://doi.org/10.1073/pnas.0709082105	journal	December 2007
Preconfiguration of the antigen-binding site during affinity maturation of a broadly neutralizing influenza virus antibody Schmidt, A. G.; Xu, H.; Khan, A. R. Proceedings of the National Academy of Sciences, Vol. 110, Issue 1 https://doi.org/10.1073/pnas.1218256109	journal	November 2012
Hybridization of RNA to double-stranded DNA: formation of R-loops. Thomas, M.; White, R. L.; Davis, R. W. Proceedings of the National Academy of Sciences, Vol. 73, Issue 7 https://doi.org/10.1073/pnas.73.7.2294	journal	July 1976
Mechanism of polypurine tract primer generation by HIV-1 reverse transcriptase Figiel, Małgorzata; Krepl, Miroslav; Park, Sangwoo Journal of Biological Chemistry, Vol. 293, Issue 1 https://doi.org/10.1074/jbc.M117.798256	journal	January 2018
Recognition of RNA by the S9.6 antibody creates pervasive artifacts when imaging RNA:DNA hybrids Smolka, John A.; Sanz, Lionel A.; Hartono, Stella R. Journal of Cell Biology, Vol. 220, Issue 6 https://doi.org/10.1083/jcb.202004079	journal	April 2021
Catalytically inactive, purified RNase H1: A specific and sensitive probe for RNA–DNA hybrid imaging Crossley, Magdalena P.; Brickner, Joshua R.; Song, Chenlin Journal of Cell Biology, Vol. 220, Issue 9 https://doi.org/10.1083/jcb.202101092	journal	July 2021
Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA:DNA Sarafianos, Stefan G.; Das, Kalyan; Tantillo, Chris The EMBO Journal, Vol. 20, Issue 6 https://doi.org/10.1093/emboj/20.6.1449	journal	March 2001
A monoclonal antibody to triplex DNA binds to eucaryotic chromosomes Lee, Jeremy S.; Burkholder, Gary D.; Latimer, Laura J. P. Nucleic Acids Research, Vol. 15, Issue 3 https://doi.org/10.1093/nar/15.3.1047	journal	January 1987
Monoclonal antibodies to double-stranded RNA as probes of RNA structure in crude nucleic acid extracts Schonborn, J.; Oberstraβ, J.; Breyel, E. Nucleic Acids Research, Vol. 19, Issue 11 https://doi.org/10.1093/nar/19.11.2993	journal	January 1991
Double-stranded RNA bending by AU-tract sequences Marin-Gonzalez, Alberto; Aicart-Ramos, Clara; Marin-Baquero, Mikel Nucleic Acids Research, Vol. 48, Issue 22 https://doi.org/10.1093/nar/gkaa1128	journal	November 2020
RNase H2 roles in genome integrity revealed by unlinking its activities Chon, Hyongi; Sparks, Justin L.; Rychlik, Monika Nucleic Acids Research, Vol. 41, Issue 5 https://doi.org/10.1093/nar/gkt027	journal	January 2013
DNA–protein π-interactions in nature: abundance, structure, composition and strength of contacts between aromatic amino acids and DNA nucleobases or deoxyribose sugar Wilson, Katie A.; Kellie, Jennifer L.; Wetmore, Stacey D. Nucleic Acids Research, Vol. 42, Issue 10 https://doi.org/10.1093/nar/gku269	journal	April 2014
Crystal structure of RNase H3–substrate complex reveals parallel evolution of RNA/DNA hybrid recognition Figiel, Małgorzata; Nowotny, Marcin Nucleic Acids Research, Vol. 42, Issue 14 https://doi.org/10.1093/nar/gku615	journal	July 2014
Viable RNaseH1 knockout mice show RNaseH1 is essential for R loop processing, mitochondrial and liver function Lima, Walt F.; Murray, Heather M.; Damle, Sagar S. Nucleic Acids Research, Vol. 44, Issue 11 https://doi.org/10.1093/nar/gkw350	journal	April 2016
RNase H sequence preferences influence antisense oligonucleotide efficiency Kiełpiński, Łukasz J.; Hagedorn, Peter H.; Lindow, Morten Nucleic Acids Research, Vol. 45, Issue 22 https://doi.org/10.1093/nar/gkx1073	journal	November 2017
Affinity maturation of a portable Fab–RNA module for chaperone-assisted RNA crystallography Koirala, Deepak; Shelke, Sandip A.; Dupont, Marcel Nucleic Acids Research, Vol. 46, Issue 5 https://doi.org/10.1093/nar/gkx1292	journal	January 2018
R-loop-mediated genomic instability is caused by impairment of replication fork progression Gan, W.; Guan, Z.; Liu, J. Genes & Development, Vol. 25, Issue 19 https://doi.org/10.1101/gad.17010011	journal	October 2011
S1-DRIP-seq identifies high expression and polyA tracts as major contributors to R-loop formation Wahba, Lamia; Costantino, Lorenzo; Tan, Frederick J. Genes & Development, Vol. 30, Issue 11 https://doi.org/10.1101/gad.280834.116	journal	June 2016
Human proteins that interact with RNA/DNA hybrids Wang, Isabel X.; Grunseich, Christopher; Fox, Jennifer Genome Research, Vol. 28, Issue 9 https://doi.org/10.1101/gr.237362.118	journal	August 2018
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Macromolecular structure determination using X-rays, neutrons and electrons: recent developments in Phenix Liebschner, Dorothee; Afonine, Pavel V.; Baker, Matthew L. Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10 https://doi.org/10.1107/S2059798319011471	journal	October 2019
The Positional Influence of the Helical Geometry of the Heteroduplex Substrate on Human RNase H1 Catalysis Lima, Walt F.; Rose, John B.; Nichols, Josh G. Molecular Pharmacology, Vol. 71, Issue 1 https://doi.org/10.1124/mol.106.025429	journal	October 2006
Genomic profiling of native R loops with a DNA-RNA hybrid recognition sensor Wang, Kang; Wang, Honghong; Li, Conghui Science Advances, Vol. 7, Issue 8 https://doi.org/10.1126/sciadv.abe3516	journal	February 2021
Crystal Structure of the Catalytic Core of an RNA-Polymerase Ribozyme Shechner, David M.; Grant, Robert A.; Bagby, Sarah C. Science, Vol. 326, Issue 5957 https://doi.org/10.1126/science.1174676	journal	November 2009
Stability and properties of double and triple helices: dramatic effects of RNA or DNA backbone composition Roberts, R.; Crothers, D. Science, Vol. 258, Issue 5087 https://doi.org/10.1126/science.1279808	journal	November 1992
Structures of a CRISPR-Cas9 R-loop complex primed for DNA cleavage Jiang, F.; Taylor, D. W.; Chen, J. S. Science, Vol. 351, Issue 6275 https://doi.org/10.1126/science.aad8282	journal	January 2016
DNA Topoisomerase I differentially modulates R-loops across the human genome Manzo, Stefano G.; Hartono, Stella R.; Sanz, Lionel A. Genome Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s13059-018-1478-1	journal	July 2018
The search for a PKR code—differential regulation of protein kinase R activity by diverse RNA and protein regulators Bou-Nader, Charles; Gordon, Jackson M.; Henderson, Frances E. RNA, Vol. 25, Issue 5 https://doi.org/10.1261/rna.070169.118	journal	February 2019
Out of Balance: R-loops in Human Disease Groh, Matthias; Gromak, Natalia PLoS Genetics, Vol. 10, Issue 9 https://doi.org/10.1371/journal.pgen.1004630	journal	September 2014
The monoclonal S9.6 antibody exhibits highly variable binding affinities towards different R-loop sequences König, Fabian; Schubert, Thomas; Längst, Gernot PLOS ONE, Vol. 12, Issue 6 https://doi.org/10.1371/journal.pone.0178875	journal	June 2017
Best practices for the visualization, mapping, and manipulation of R‐loops Chédin, Frédéric; Hartono, Stella R.; Sanz, Lionel A. The EMBO Journal, Vol. 40, Issue 4 https://doi.org/10.15252/embj.2020106394	journal	January 2021
Antibodies specific for nucleic acids and applications in genomic detection and clinical diagnostics Hu, Zonglin; Leppla, Stephen H.; Li, Baoguang Expert Review of Molecular Diagnostics, Vol. 14, Issue 7 https://doi.org/10.1586/14737159.2014.931810	journal	June 2014
Reverse Turns in Peptides and Protein Smith, John A.; Pease, Lila G.; Kopple, Kenneth D. Critical Reviews in Biochemistry, Vol. 8, Issue 4 https://doi.org/10.3109/10409238009105470	journal	January 1980
Strengths and Weaknesses of the Current Strategies to Map and Characterize R-Loops Vanoosthuyse, Vincent Non-Coding RNA, Vol. 4, Issue 2 https://doi.org/10.3390/ncrna4020009	journal	March 2018
Crystal structure of RNA-DNA duplex provides insight into conformational changes induced by RNase H binding Davis, Ryan R.; Shaban, Nadine M.; Perrino, Fred W. Cell Cycle, Vol. 14, Issue 4 https://doi.org/10.4161/15384101.2014.994996	journal	February 2015
Genome-wide DNA hypomethylation and RNA:DNA hybrid accumulation in Aicardi–Goutières syndrome Lim, Yoong Wearn; Sanz, Lionel A.; Xu, Xiaoqin eLife, Vol. 4 https://doi.org/10.7554/eLife.08007	journal	July 2015
Defining the location of promoter-associated R-loops at near-nucleotide resolution using bisDRIP-seq Dumelie, Jason G.; Jaffrey, Samie R. eLife, Vol. 6 https://doi.org/10.7554/eLife.28306	journal	October 2017
A nuclease- and bisulfite-based strategy captures strand-specific R-loops genome-wide Wulfridge, Phillip; Sarma, Kavitha eLife, Vol. 10 https://doi.org/10.7554/eLife.65146	journal	February 2021

Similar Records

Specific recognition of RNA/DNA hybrid and enhancement of human RNase H1 activity by HBD

Journal Article · Wed Jul 09 00:00:00 EDT 2008 · EMBO J. · OSTI ID:1006648

Insights into RNA/DNA hybrid recognition and processing by RNase H from the crystal structure of a non-specific enzyme-dsDNA complex

Journal Article · Wed Jun 17 00:00:00 EDT 2009 · Cell Cycle · OSTI ID:1007083

Catalytically inactive, purified RNase H1: A specific and sensitive probe for RNA–DNA hybrid imaging

Journal Article · Tue Jul 06 20:00:00 EDT 2021 · Journal of Cell Biology · OSTI ID:2470862

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
applied immunology
non-coding RNAs
nucleic acids
x-ray crystallography

Structural basis of R-loop recognition by the S9.6 monoclonal antibody

Citation Formats

References (81)

Similar Records

Related Subjects