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Article ; Online: R-SPONDIN2

Hein, Renee F C / Wu, Joshua H / Holloway, Emily M / Frum, Tristan / Conchola, Ansley S / Tsai, Yu-Hwai / Wu, Angeline / Fine, Alexis S / Miller, Alyssa J / Szenker-Ravi, Emmanuelle / Yan, Kelley S / Kuo, Calvin J / Glass, Ian / Reversade, Bruno / Spence, Jason R

Developmental cell

2022 Volume 57, Issue 13, Page(s) 1598–1614.e8

Abstract: The human respiratory epithelium is derived from a progenitor cell in the distal buds of the developing lung. These "bud tip progenitors" are regulated by reciprocal signaling with surrounding mesenchyme; however, mesenchymal heterogeneity and function ... ...

Abstract	The human respiratory epithelium is derived from a progenitor cell in the distal buds of the developing lung. These "bud tip progenitors" are regulated by reciprocal signaling with surrounding mesenchyme; however, mesenchymal heterogeneity and function in the developing human lung are poorly understood. We interrogated single-cell RNA sequencing data from multiple human lung specimens and identified a mesenchymal cell population present during development that is highly enriched for expression of the WNT agonist RSPO2, and we found that the adjacent bud tip progenitors are enriched for the RSPO2 receptor LGR5. Functional experiments using organoid models, explant cultures, and FACS-isolated RSPO2
MeSH term(s)	Humans ; Lung ; Mesenchymal Stem Cells ; Organogenesis ; Organoids ; Wnt Signaling Pathway
Language	English
Publishing date	2022-06-08
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2054967-2
ISSN	1878-1551 ; 1534-5807
ISSN (online)	1878-1551
ISSN	1534-5807
DOI	10.1016/j.devcel.2022.05.010
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Article ; Online: RLSuite: An Integrative R-Loop Bioinformatics Framework.

Miller, H E / Montemayor, D / Levy, S / Sharma, K / Frost, B / Bishop, A J R

Journal of bioinformatics and systems biology : Open access

2023 Volume 6, Issue 4, Page(s) 364–378

Abstract: We recently described the development of a database of 810 R-loop mapping datasets and used ... this data to conduct a meta-analysis of R-loops. R-loops are three-stranded nucleic acid structures ... containing RNA:DNA hybrids and we were able to verify that 30% of expressed genes have an associated R-loop ...

Abstract	We recently described the development of a database of 810 R-loop mapping datasets and used this data to conduct a meta-analysis of R-loops. R-loops are three-stranded nucleic acid structures containing RNA:DNA hybrids and we were able to verify that 30% of expressed genes have an associated R-loop in a location conserved manner.. Moreover, intergenic R-loops map to enhancers, super enhancers and with TAD domain boundaries. This work demonstrated that R-loop mapping via high-throughput sequencing can reveal novel insight into R-loop biology, however the analysis and quality control of these data is a non-trivial task for which few bioinformatic tools exist. Herein we describe RLSuite, an integrative R-loop bioinformatics framework for pre-processing, quality control, and downstream analysis of R-loop mapping data. RLSuite enables users to compare their data to hundreds of public datasets and generate a user-friendly analysis report for sharing with non-bioinformatician colleagues. Taken together, RLSuite is a novel analysis framework that should greatly benefit the emerging R-loop bioinformatics community in a rapidly expanding aspect of epigenetic control that is still poorly understood.
Language	English
Publishing date	2023-12-21
Publishing country	United States
Document type	Journal Article
ISSN	2688-5107
ISSN (online)	2688-5107
DOI	10.26502/jbsb.5107071
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Article ; Online: Chemoproteomic target deconvolution reveals Histone Deacetylases as targets of (R)-lipoic acid.

Lechner, Severin / Steimbach, Raphael R / Wang, Longlong / Deline, Marshall L / Chang, Yun-Chien / Fromme, Tobias / Klingenspor, Martin / Matthias, Patrick / Miller, Aubry K / Médard, Guillaume / Kuster, Bernhard

Nature communications

2023 Volume 14, Issue 1, Page(s) 3548

Abstract: ... antioxidant properties, racemic (R/S)-lipoic acid is used as a food supplement but is also investigated ... as a pharmaceutical in over 180 clinical trials covering a broad range of diseases. Moreover, (R/S)-lipoic acid is ... of the reduced form of lipoic acid and lipoamide. Importantly, only the naturally occurring (R)-enantiomer ...

Abstract	Lipoic acid is an essential enzyme cofactor in central metabolic pathways. Due to its claimed antioxidant properties, racemic (R/S)-lipoic acid is used as a food supplement but is also investigated as a pharmaceutical in over 180 clinical trials covering a broad range of diseases. Moreover, (R/S)-lipoic acid is an approved drug for the treatment of diabetic neuropathy. However, its mechanism of action remains elusive. Here, we performed chemoproteomics-aided target deconvolution of lipoic acid and its active close analog lipoamide. We find that histone deacetylases HDAC1, HDAC2, HDAC3, HDAC6, HDAC8, and HDAC10 are molecular targets of the reduced form of lipoic acid and lipoamide. Importantly, only the naturally occurring (R)-enantiomer inhibits HDACs at physiologically relevant concentrations and leads to hyperacetylation of HDAC substrates. The inhibition of HDACs by (R)-lipoic acid and lipoamide explain why both compounds prevent stress granule formation in cells and may also provide a molecular rationale for many other phenotypic effects elicited by lipoic acid.
MeSH term(s)	Histone Deacetylase Inhibitors/pharmacology ; Histone Deacetylase Inhibitors/chemistry ; Thioctic Acid/pharmacology ; Histone Deacetylases/metabolism ; Antioxidants/pharmacology
Chemical Substances	Histone Deacetylase Inhibitors ; Thioctic Acid (73Y7P0K73Y) ; Histone Deacetylases (EC 3.5.1.98) ; Antioxidants
Language	English
Publishing date	2023-06-15
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-023-39151-8
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Article ; Online: APOBEC3B regulates R-loops and promotes transcription-associated mutagenesis in cancer.

Nature genetics

2023 Volume 55, Issue 10, Page(s) 1721–1734

Abstract: ... interactions with a surprising number of R-loop factors. Biochemical experiments show APOBEC3B binding to R ... loops in cells and in vitro. Genetic experiments demonstrate R-loop increases in cells lacking APOBEC3B ... landscape of physiological and stimulus-induced R-loops with thousands of differentially altered regions ...

Abstract	The single-stranded DNA cytosine-to-uracil deaminase APOBEC3B is an antiviral protein implicated in cancer. However, its substrates in cells are not fully delineated. Here APOBEC3B proteomics reveal interactions with a surprising number of R-loop factors. Biochemical experiments show APOBEC3B binding to R-loops in cells and in vitro. Genetic experiments demonstrate R-loop increases in cells lacking APOBEC3B and decreases in cells overexpressing APOBEC3B. Genome-wide analyses show major changes in the overall landscape of physiological and stimulus-induced R-loops with thousands of differentially altered regions, as well as binding of APOBEC3B to many of these sites. APOBEC3 mutagenesis impacts genes overexpressed in tumors and splice factor mutant tumors preferentially, and APOBEC3-attributed kataegis are enriched in RTCW motifs consistent with APOBEC3B deamination. Taken together with the fact that APOBEC3B binds single-stranded DNA and RNA and preferentially deaminates DNA, these results support a mechanism in which APOBEC3B regulates R-loops and contributes to R-loop mutagenesis in cancer.
MeSH term(s)	Humans ; R-Loop Structures ; DNA, Single-Stranded/genetics ; Genome-Wide Association Study ; Mutagenesis ; Neoplasms/genetics ; Neoplasms/pathology ; Cytidine Deaminase/genetics ; Minor Histocompatibility Antigens/genetics ; Minor Histocompatibility Antigens/metabolism
Chemical Substances	DNA, Single-Stranded ; Cytidine Deaminase (EC 3.5.4.5) ; Minor Histocompatibility Antigens ; APOBEC3B protein, human (EC 3.5.4.5)
Language	English
Publishing date	2023-09-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1108734-1
ISSN	1546-1718 ; 1061-4036
ISSN (online)	1546-1718
ISSN	1061-4036
DOI	10.1038/s41588-023-01504-w
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Article ; Online: Quality-controlled R-loop meta-analysis reveals the characteristics of R-loop consensus regions.

Miller, Henry E / Montemayor, Daniel / Abdul, Jebriel / Vines, Anna / Levy, Simon A / Hartono, Stella R / Sharma, Kumar / Frost, Bess / Chédin, Frédéric / Bishop, Alexander J R

Nucleic acids research

2022 Volume 50, Issue 13, Page(s) 7260–7286

Abstract: R-loops are three-stranded nucleic acid structures formed from the hybridization of RNA and DNA ... While the pathological consequences of R-loops have been well-studied to date, the locations, classes, and dynamics ... of physiological R-loops remain poorly understood. R-loop mapping studies provide insight into R-loop dynamics ...

Abstract	R-loops are three-stranded nucleic acid structures formed from the hybridization of RNA and DNA. While the pathological consequences of R-loops have been well-studied to date, the locations, classes, and dynamics of physiological R-loops remain poorly understood. R-loop mapping studies provide insight into R-loop dynamics, but their findings are challenging to generalize. This is due to the narrow biological scope of individual studies, the limitations of each mapping modality, and, in some cases, poor data quality. In this study, we reprocessed 810 R-loop mapping datasets from a wide array of biological conditions and mapping modalities. From this data resource, we developed an accurate R-loop data quality control method, and we reveal the extent of poor-quality data within previously published studies. We then identified a set of high-confidence R-loop mapping samples and used them to define consensus R-loop sites called 'R-loop regions' (RL regions). In the process, we identified a stark divergence between RL regions detected by S9.6 and dRNH-based mapping methods, particularly with respect to R-loop size, location, and colocalization with RNA binding factors. Taken together, this work provides a much-needed method to assess R-loop data quality and offers novel context regarding the differences between dRNH- and S9.6-based R-loop mapping approaches.
MeSH term(s)	Consensus ; DNA/chemistry ; Nucleic Acid Hybridization ; R-Loop Structures ; RNA/chemistry ; RNA/genetics
Chemical Substances	RNA (63231-63-0) ; DNA (9007-49-2)
Language	English
Publishing date	2022-06-27
Publishing country	England
Document type	Journal Article ; Meta-Analysis ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	186809-3
ISSN	1362-4962 ; 1362-4954 ; 0301-5610 ; 0305-1048
ISSN (online)	1362-4962 ; 1362-4954
ISSN	0301-5610 ; 0305-1048
DOI	10.1093/nar/gkac537
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Article ; Online: Exploration and analysis of R-loop mapping data with RLBase.

Miller, Henry E / Montemayor, Daniel / Li, Janet / Levy, Simon A / Pawar, Roshan / Hartono, Stella / Sharma, Kumar / Frost, Bess / Chedin, Frédéric / Bishop, Alexander J R

Nucleic acids research

2022 Volume 51, Issue D1, Page(s) D1129–D1137

Abstract: R-loops are three-stranded nucleic acid structures formed from the hybridization of RNA and DNA ... In 2012, Ginno et al. introduced the first R-loop mapping method. Since that time, dozens of R-loop ... mapping studies have been conducted, yielding hundreds of publicly available datasets. Current R-loop ...

Abstract	R-loops are three-stranded nucleic acid structures formed from the hybridization of RNA and DNA. In 2012, Ginno et al. introduced the first R-loop mapping method. Since that time, dozens of R-loop mapping studies have been conducted, yielding hundreds of publicly available datasets. Current R-loop databases provide only limited access to these data. Moreover, no web tools for analyzing user-supplied R-loop datasets have yet been described. In our recent work, we reprocessed 810 R-loop mapping samples, building the largest R-loop data resource to date. We also defined R-loop consensus regions and developed a framework for R-loop data analysis. Now, we introduce RLBase, a user-friendly database that provides the capability to (i) explore hundreds of public R-loop mapping datasets, (ii) explore R-loop consensus regions, (iii) analyze user-supplied data and (iv) download standardized and reprocessed datasets. RLBase is directly accessible via the following URL: https://gccri.bishop-lab.uthscsa.edu/shiny/rlbase/.
MeSH term(s)	DNA/genetics ; DNA/chemistry ; Hybridization, Genetic ; Nucleic Acid Hybridization ; R-Loop Structures ; RNA/genetics ; RNA/chemistry ; Databases, Genetic
Chemical Substances	DNA (9007-49-2) ; RNA (63231-63-0)
Language	English
Publishing date	2022-08-25
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	186809-3
ISSN	1362-4962 ; 1362-4954 ; 0301-5610 ; 0305-1048
ISSN (online)	1362-4962 ; 1362-4954
ISSN	0301-5610 ; 0305-1048
DOI	10.1093/nar/gkac732
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Article ; Online: RNF8 ubiquitylation of XRN2 facilitates R-loop resolution and restrains genomic instability in BRCA1 mutant cells.

Krishnan, Rehna / Lapierre, Mariah / Gautreau, Brandon / Nixon, Kevin C J / El Ghamrasni, Samah / Patel, Parasvi S / Hao, Jun / Yerlici, V Talya / Guturi, Kiran Kumar Naidu / St-Germain, Jonathan / Mateo, Francesca / Saad, Amine / Algouneh, Arash / Earnshaw, Rebecca / Shili, Duan / Seitova, Alma / Miller, Joshua / Khosraviani, Negin / Penn, Adam /

Ho, Brandon / Sanchez, Otto / Hande, M Prakash / Masson, Jean-Yves / Brown, Grant W / Alaoui-Jamali, Moulay / Reynolds, John J / Arrowsmith, Cheryl / Raught, Brian / Pujana, Miguel A / Mekhail, Karim / Stewart, Grant S / Hakem, Anne / Hakem, Razqallah

Nucleic acids research

2023 Volume 51, Issue 19, Page(s) 10484–10505

Abstract: ... cancer cells was found to promote R-loop accumulation and replication fork instability, leading ... which is crucial for transcription termination and R-loop resolution. We report that RNF8 ubiquitylates ... XRN2 to facilitate its recruitment to R-loop-prone genomic loci and that RNF8 deficiency in BRCA1 ...

Abstract	Breast cancer linked with BRCA1/2 mutations commonly recur and resist current therapies, including PARP inhibitors. Given the lack of effective targeted therapies for BRCA1-mutant cancers, we sought to identify novel targets to selectively kill these cancers. Here, we report that loss of RNF8 significantly protects Brca1-mutant mice against mammary tumorigenesis. RNF8 deficiency in human BRCA1-mutant breast cancer cells was found to promote R-loop accumulation and replication fork instability, leading to increased DNA damage, senescence, and synthetic lethality. Mechanistically, RNF8 interacts with XRN2, which is crucial for transcription termination and R-loop resolution. We report that RNF8 ubiquitylates XRN2 to facilitate its recruitment to R-loop-prone genomic loci and that RNF8 deficiency in BRCA1-mutant breast cancer cells decreases XRN2 occupancy at R-loop-prone sites, thereby promoting R-loop accumulation, transcription-replication collisions, excessive genomic instability, and cancer cell death. Collectively, our work identifies a synthetic lethal interaction between RNF8 and BRCA1, which is mediated by a pathological accumulation of R-loops.
MeSH term(s)	Animals ; Female ; Humans ; Mice ; BRCA1 Protein/metabolism ; BRCA2 Protein/genetics ; Breast Neoplasms/genetics ; DNA Damage ; DNA-Binding Proteins/metabolism ; Exoribonucleases/metabolism ; Genomic Instability ; Neoplasm Recurrence, Local ; R-Loop Structures ; Ubiquitin-Protein Ligases/genetics ; Ubiquitin-Protein Ligases/metabolism ; Ubiquitination
Chemical Substances	BRCA1 Protein ; BRCA1 protein, human ; BRCA2 Protein ; BRCA2 protein, human ; DNA-Binding Proteins ; Exoribonucleases (EC 3.1.-) ; RNF8 protein, human ; Ubiquitin-Protein Ligases (EC 2.3.2.27) ; XRN2 protein, human (EC 3.1.13.1) ; Brca1 protein, mouse ; Rnf8 protein, mouse (EC 2.3.2.27) ; Xrn2 protein, mouse (EC 3.1.11.-)
Language	English
Publishing date	2023-09-11
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	186809-3
ISSN	1362-4962 ; 1362-4954 ; 0301-5610 ; 0305-1048
ISSN (online)	1362-4962 ; 1362-4954
ISSN	0301-5610 ; 0305-1048
DOI	10.1093/nar/gkad733
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Article ; Online: Sensitivity to Neutralizing Antibodies and Resistance to Type I Interferons in SARS-CoV-2 R.1 Lineage Variants, Canada.

Jacob, Rajesh Abraham / Zhang, Ali / Ajoge, Hannah O / D'Agostino, Michael R / Nirmalarajah, Kuganya / Shigayeva, Altynay / Demian, Wael L / Baker, Sheridan J C / Derakhshani, Hooman / Rossi, Laura / Nasir, Jalees A / Panousis, Emily M / Draia, Ahmed N / Vermeiren, Christie / Gilchrist, Jodi / Smieja, Nicole / Bulir, David / Smieja, Marek / Surette, Michael G /

McArthur, Andrew G / McGeer, Allison J / Mubareka, Samira / Banerjee, Arinjay / Miller, Matthew S / Mossman, Karen

Emerging infectious diseases

2023 Volume 29, Issue 7, Page(s) 1386–1396

Abstract: ... pathogenesis. In this study, we isolated samples of the SARS-CoV-2 R.1 lineage, categorized as a variant under ... sensitivity. The R.1 isolates were potently neutralized by both the wave 1 and wave 3 convalescent serum ... samples, unlike the B.1.351 (Beta) variant of concern. Of note, the R.1 variant was significantly more ...

Abstract	Isolating and characterizing emerging SARS-CoV-2 variants is key to understanding virus pathogenesis. In this study, we isolated samples of the SARS-CoV-2 R.1 lineage, categorized as a variant under monitoring by the World Health Organization, and evaluated their sensitivity to neutralizing antibodies and type I interferons. We used convalescent serum samples from persons in Canada infected either with ancestral virus (wave 1) or the B.1.1.7 (Alpha) variant of concern (wave 3) for testing neutralization sensitivity. The R.1 isolates were potently neutralized by both the wave 1 and wave 3 convalescent serum samples, unlike the B.1.351 (Beta) variant of concern. Of note, the R.1 variant was significantly more resistant to type I interferons (IFN-α/β) than was the ancestral isolate. Our study demonstrates that the R.1 variant retained sensitivity to neutralizing antibodies but evolved resistance to type I interferons. This critical driving force will influence the trajectory of the pandemic.
MeSH term(s)	Humans ; SARS-CoV-2/genetics ; Interferon Type I/genetics ; Antibodies, Neutralizing ; COVID-19 ; COVID-19 Serotherapy ; Canada/epidemiology ; Antibodies, Viral ; Spike Glycoprotein, Coronavirus
Chemical Substances	Interferon Type I ; Antibodies, Neutralizing ; Antibodies, Viral ; Spike Glycoprotein, Coronavirus ; spike protein, SARS-CoV-2
Language	English
Publishing date	2023-06-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1380686-5
ISSN	1080-6059 ; 1080-6040
ISSN (online)	1080-6059
ISSN	1080-6040
DOI	10.3201/eid2907.230198
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Article ; Online: Clinical and Mechanistic Implications of R-Loops in Human Leukemias.

Lee, Seo-Yun / Miller, Kyle M / Kim, Jae-Jin

International journal of molecular sciences

2023 Volume 24, Issue 6

Abstract: ... with genomic instability. R-loops are three-stranded nucleic acid structures consisting of an RNA-DNA hybrid and a non ... replication, and DSB repair. However, unregulated R-loop formation can cause DNA damage and ... understanding of aberrant R-loop formation and how it influences genomic instability and leukemia development ...

Abstract	Genetic mutations or environmental agents are major contributors to leukemia and are associated with genomic instability. R-loops are three-stranded nucleic acid structures consisting of an RNA-DNA hybrid and a non-template single-stranded DNA. These structures regulate various cellular processes, including transcription, replication, and DSB repair. However, unregulated R-loop formation can cause DNA damage and genomic instability, which are potential drivers of cancer including leukemia. In this review, we discuss the current understanding of aberrant R-loop formation and how it influences genomic instability and leukemia development. We also consider the possibility of R-loops as therapeutic targets for cancer treatment.
MeSH term(s)	Humans ; R-Loop Structures ; Transcription, Genetic ; DNA Repair ; RNA/genetics ; DNA Replication ; Leukemia/genetics ; Genomic Instability
Chemical Substances	RNA (63231-63-0)
Language	English
Publishing date	2023-03-22
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms24065966
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Article ; Online: Meniscal Repair: The R-Factor.

Miller, Mark D

Clinics in sports medicine

2019 Volume 39, Issue 1, Page(s) xiii–xiv

Language	English
Publishing date	2019-11-25
Publishing country	United States
Document type	Editorial
ZDB-ID	779944-5
ISSN	1556-228X ; 0278-5919
ISSN (online)	1556-228X
ISSN	0278-5919
DOI	10.1016/j.csm.2019.10.002
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