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Article ; Online: Visualization of lncRNA and mRNA Structure Models Within the Integrative Genomics Viewer.

Busan, Steven / Weeks, Kevin M

Methods in molecular biology (Clifton, N.J.)

2020 Volume 2254, Page(s) 15–25

Abstract: Every class of RNA forms base-paired structures that impact biological functions. Chemical probing of RNA structure, especially with the advent of strategies such as SHAPE-MaP, vastly expands the scale and quantitative accuracy over which RNA structure ... ...

Abstract	Every class of RNA forms base-paired structures that impact biological functions. Chemical probing of RNA structure, especially with the advent of strategies such as SHAPE-MaP, vastly expands the scale and quantitative accuracy over which RNA structure can be examined. These methods have enabled large-scale structural studies of mRNAs and lncRNAs, but the length and complexity of these RNAs makes interpretation of the data challenging. We have created modules available through the open-source Integrative Genomics Viewer (IGV) for straightforward visualization of RNA structures along with complementary experimental data. Here we present detailed and stepwise strategies for exploring and visualizing complex RNA structures in IGV. Individuals can use these instructions and supplied sample data to become adept at using IGV to visualize RNA structure models in conjunction with useful allied information.
MeSH term(s)	Animals ; Escherichia coli/genetics ; Genomics/methods ; Mice ; Models, Molecular ; Protein Biosynthesis ; RNA, Long Noncoding/chemistry ; RNA, Long Noncoding/genetics ; RNA, Messenger/chemistry ; RNA, Messenger/genetics ; Repetitive Sequences, Nucleic Acid/genetics ; Software
Chemical Substances	RNA, Long Noncoding ; RNA, Messenger
Language	English
Publishing date	2020-12-15
Publishing country	United States
Document type	Journal Article
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-1158-6_2
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Direct detection of RNA modifications and structure using single-molecule nanopore sequencing.

Stephenson, William / Razaghi, Roham / Busan, Steven / Weeks, Kevin M / Timp, Winston / Smibert, Peter

Cell genomics

2022 Volume 2, Issue 2

Abstract: Modifications are present on many classes of RNA, including tRNA, rRNA, and mRNA. These modifications modulate diverse biological processes such as genetic recoding and mRNA export and folding. In addition, modifications can be introduced to RNA ... ...

Abstract	Modifications are present on many classes of RNA, including tRNA, rRNA, and mRNA. These modifications modulate diverse biological processes such as genetic recoding and mRNA export and folding. In addition, modifications can be introduced to RNA molecules using chemical probing strategies that reveal RNA structure and dynamics. Many methods exist to detect RNA modifications by short-read sequencing; however, limitations on read length inherent to short-read-based methods dissociate modifications from their native context, preventing single-molecule modification analysis. Here, we demonstrate direct RNA nanopore sequencing to detect endogenous and exogenous RNA modifications on long RNAs at the single-molecule level. We detect endogenous 2'-
Language	English
Publishing date	2022-02-07
Publishing country	United States
Document type	Journal Article
ISSN	2666-979X
ISSN (online)	2666-979X
DOI	10.1016/j.xgen.2022.100097
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Article ; Online: Visualization of RNA structure models within the Integrative Genomics Viewer.

Busan, Steven / Weeks, Kevin M

RNA (New York, N.Y.)

2017 Volume 23, Issue 7, Page(s) 1012–1018

Abstract: Analyses of the interrelationships between RNA structure and function are increasingly important components of genomic studies. The SHAPE-MaP strategy enables accurate RNA structure probing and realistic structure modeling of kilobase-length noncoding ... ...

Abstract	Analyses of the interrelationships between RNA structure and function are increasingly important components of genomic studies. The SHAPE-MaP strategy enables accurate RNA structure probing and realistic structure modeling of kilobase-length noncoding RNAs and mRNAs. Existing tools for visualizing RNA structure models are not suitable for efficient analysis of long, structurally heterogeneous RNAs. In addition, structure models are often advantageously interpreted in the context of other experimental data and gene annotation information, for which few tools currently exist. We have developed a module within the widely used and well supported open-source Integrative Genomics Viewer (IGV) that allows visualization of SHAPE and other chemical probing data, including raw reactivities, data-driven structural entropies, and data-constrained base-pair secondary structure models, in context with linear genomic data tracks. We illustrate the usefulness of visualizing RNA structure in the IGV by exploring structure models for a large viral RNA genome, comparing bacterial mRNA structure in cells with its structure under cell- and protein-free conditions, and comparing a noncoding RNA structure modeled using SHAPE data with a base-pairing model inferred through sequence covariation analysis.
MeSH term(s)	Base Pairing ; Computational Biology/methods ; Models, Molecular ; Molecular Sequence Annotation ; Nucleic Acid Conformation ; RNA/chemistry ; Software
Chemical Substances	RNA (63231-63-0)
Language	English
Publishing date	2017
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1241540-6
ISSN	1469-9001 ; 1355-8382
ISSN (online)	1469-9001
ISSN	1355-8382
DOI	10.1261/rna.060194.116
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Article ; Online: Accurate detection of chemical modifications in RNA by mutational profiling (MaP) with ShapeMapper 2.

Busan, Steven / Weeks, Kevin M

RNA (New York, N.Y.)

2017 Volume 24, Issue 2, Page(s) 143–148

Abstract: Mutational profiling (MaP) enables detection of sites of chemical modification in RNA as sequence changes during reverse transcription (RT), subsequently read out by massively parallel sequencing. We introduce ShapeMapper 2, which integrates careful ... ...

Abstract	Mutational profiling (MaP) enables detection of sites of chemical modification in RNA as sequence changes during reverse transcription (RT), subsequently read out by massively parallel sequencing. We introduce ShapeMapper 2, which integrates careful handling of all classes of adduct-induced sequence changes, sequence variant correction, basecall quality filters, and quality-control warnings to now identify RNA adduct sites as accurately as achieved by careful manual analysis of electrophoresis data, the prior highest-accuracy standard. MaP and ShapeMapper 2 provide a robust, experimentally concise, and accurate approach for reading out nucleic acid chemical probing experiments.
MeSH term(s)	Base Pairing ; High-Throughput Nucleotide Sequencing/methods ; Mutation ; RNA/chemistry ; Sequence Analysis, RNA/methods ; Software
Chemical Substances	RNA (63231-63-0)
Language	English
Publishing date	2017-11-07
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1241540-6
ISSN	1469-9001 ; 1355-8382
ISSN (online)	1469-9001
ISSN	1355-8382
DOI	10.1261/rna.061945.117
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Article ; Online: Global 5'-UTR RNA structure regulates translation of a SERPINA1 mRNA.

Grayeski, Philip J / Weidmann, Chase A / Kumar, Jayashree / Lackey, Lela / Mustoe, Anthony M / Busan, Steven / Laederach, Alain / Weeks, Kevin M

Nucleic acids research

2022 Volume 50, Issue 17, Page(s) 9689–9704

Abstract: SERPINA1 mRNAs encode the protease inhibitor α-1-antitrypsin and are regulated through post-transcriptional mechanisms. α-1-antitrypsin deficiency leads to chronic obstructive pulmonary disease (COPD) and liver cirrhosis, and specific variants in the 5'- ... ...

Abstract	SERPINA1 mRNAs encode the protease inhibitor α-1-antitrypsin and are regulated through post-transcriptional mechanisms. α-1-antitrypsin deficiency leads to chronic obstructive pulmonary disease (COPD) and liver cirrhosis, and specific variants in the 5'-untranslated region (5'-UTR) are associated with COPD. The NM_000295.4 transcript is well expressed and translated in lung and blood and features an extended 5'-UTR that does not contain a competing upstream open reading frame (uORF). We show that the 5'-UTR of NM_000295.4 folds into a well-defined multi-helix structural domain. We systematically destabilized mRNA structure across the NM_000295.4 5'-UTR, and measured changes in (SHAPE quantified) RNA structure and cap-dependent translation relative to a native-sequence reporter. Surprisingly, despite destabilizing local RNA structure, most mutations either had no effect on or decreased translation. Most structure-destabilizing mutations retained native, global 5'-UTR structure. However, those mutations that disrupted the helix that anchors the 5'-UTR domain yielded three groups of non-native structures. Two of these non-native structure groups refolded to create a stable helix near the translation initiation site that decreases translation. Thus, in contrast to the conventional model that RNA structure in 5'-UTRs primarily inhibits translation, complex folding of the NM_000295.4 5'-UTR creates a translation-optimized message by promoting accessibility at the translation initiation site.
MeSH term(s)	5' Untranslated Regions ; Humans ; Protease Inhibitors ; Protein Biosynthesis ; Pulmonary Disease, Chronic Obstructive/genetics ; RNA, Messenger/metabolism ; alpha 1-Antitrypsin/genetics
Chemical Substances	5' Untranslated Regions ; Protease Inhibitors ; RNA, Messenger ; SERPINA1 protein, human ; alpha 1-Antitrypsin
Language	English
Publishing date	2022-09-15
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/gkac739
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Article ; Online: SHAPE Probing Reveals Human rRNAs Are Largely Unfolded in Solution.

Giannetti, Catherine A / Busan, Steven / Weidmann, Chase A / Weeks, Kevin M

Biochemistry

2019 Volume 58, Issue 31, Page(s) 3377–3385

Abstract: Chemical probing experiments, coupled with empirically determined free energy change relationships, can enable accurate modeling of the secondary structures of diverse and complex RNAs. A current frontier lies in modeling large and structurally ... ...

Abstract	Chemical probing experiments, coupled with empirically determined free energy change relationships, can enable accurate modeling of the secondary structures of diverse and complex RNAs. A current frontier lies in modeling large and structurally heterogeneous transcripts, including complex eukaryotic RNAs. To validate and improve on experimentally driven approaches for modeling large transcripts, we obtained high-quality SHAPE data for the protein-free human 18S and 28S ribosomal RNAs (rRNAs). To our surprise, SHAPE-directed structure models for the human rRNAs poorly matched accepted structures. Analysis of predicted rRNA structures based on low-SHAPE and low-entropy (lowSS) metrics revealed that, whereas ∼75% of
MeSH term(s)	Acylation ; Base Sequence ; Escherichia coli/genetics ; HEK293 Cells ; Humans ; Nucleic Acid Conformation ; RNA, Ribosomal, 18S/chemistry ; RNA, Ribosomal, 18S/genetics ; RNA, Ribosomal, 28S/chemistry ; RNA, Ribosomal, 28S/genetics ; Solutions
Chemical Substances	RNA, Ribosomal, 18S ; RNA, Ribosomal, 28S ; Solutions
Language	English
Publishing date	2019-07-26
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1108-3
ISSN	1520-4995 ; 0006-2960
ISSN (online)	1520-4995
ISSN	0006-2960
DOI	10.1021/acs.biochem.9b00076
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Article ; Online: Guidelines for SHAPE Reagent Choice and Detection Strategy for RNA Structure Probing Studies.

Busan, Steven / Weidmann, Chase A / Sengupta, Arnab / Weeks, Kevin M

Biochemistry

2019 Volume 58, Issue 23, Page(s) 2655–2664

Abstract: Chemical probing is an important tool for characterizing the complex folded structures of RNA molecules, many of which play key cellular roles. Electrophilic SHAPE reagents create adducts at the 2'-hydroxyl position on the RNA backbone of flexible ... ...

Abstract	Chemical probing is an important tool for characterizing the complex folded structures of RNA molecules, many of which play key cellular roles. Electrophilic SHAPE reagents create adducts at the 2'-hydroxyl position on the RNA backbone of flexible ribonucleotides with relatively little dependence on nucleotide identity. Strategies for adduct detection such as mutational profiling (MaP) allow accurate, automated calculation of relative adduct frequencies for each nucleotide in a given RNA or group of RNAs. A number of alternative reagents and adduct detection strategies have been proposed, especially for use in living cells. Here we evaluate five SHAPE reagents: three previously well-validated reagents 1M7 (1-methyl-7-nitroisatoic anhydride), 1M6 (1-methyl-6-nitroisatoic anhydride), and NMIA ( N-methylisatoic anhydride), one more recently proposed NAI (2-methylnicotinic acid imidazolide), and one novel reagent 5NIA (5-nitroisatoic anhydride). We clarify the importance of carefully designed software in reading out SHAPE experiments using massively parallel sequencing approaches. We examine SHAPE modification in living cells in diverse cell lines, compare MaP and reverse transcription-truncation as SHAPE adduct detection strategies, make recommendations for SHAPE reagent choice, and outline areas for future development.
MeSH term(s)	Anhydrides/chemistry ; Animals ; Escherichia coli/chemistry ; High-Throughput Nucleotide Sequencing/methods ; Humans ; Indicators and Reagents/chemistry ; Jurkat Cells ; Mice ; Molecular Probes/chemistry ; Oxazines/chemistry ; RNA, Bacterial/chemistry ; Sequence Analysis, RNA/methods ; ortho-Aminobenzoates/chemistry
Chemical Substances	1-methyl-7-nitroisatoic anhydride ; Anhydrides ; Indicators and Reagents ; Molecular Probes ; Oxazines ; RNA, Bacterial ; ortho-Aminobenzoates ; N-methylisatoic anhydride (10328-92-4)
Language	English
Publishing date	2019-05-30
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1108-3
ISSN	1520-4995 ; 0006-2960
ISSN (online)	1520-4995
ISSN	0006-2960
DOI	10.1021/acs.biochem.8b01218
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Article: SHAPE Probing Reveals Human rRNAs Are Largely Unfolded in Solution

Giannetti, Catherine A / Busan, Steven / Weidmann, Chase A / Weeks, Kevin M

Biochemistry. 2019 July 15, v. 58, no. 31

2019

Abstract	Chemical probing experiments, coupled with empirically determined free energy change relationships, can enable accurate modeling of the secondary structures of diverse and complex RNAs. A current frontier lies in modeling large and structurally heterogeneous transcripts, including complex eukaryotic RNAs. To validate and improve on experimentally driven approaches for modeling large transcripts, we obtained high-quality SHAPE data for the protein-free human 18S and 28S ribosomal RNAs (rRNAs). To our surprise, SHAPE-directed structure models for the human rRNAs poorly matched accepted structures. Analysis of predicted rRNA structures based on low-SHAPE and low-entropy (lowSS) metrics revealed that, whereas ∼75% of Escherichia coli rRNA sequences form well-determined lowSS secondary structure, only ∼40% of the human rRNAs do. Critically, regions of the human rRNAs that specifically fold into well-determined lowSS structures were modeled to high accuracy using SHAPE data. This work reveals that eukaryotic rRNAs are more unfolded than are those of prokaryotic rRNAs and indeed are largely unfolded overall, likely reflecting increased protein dependence for eukaryotic ribosome structure. In addition, those regions and substructures that are well-determined can be identified de novo and successfully modeled by SHAPE-directed folding.
Keywords	Escherichia coli ; Gibbs free energy ; humans ; messenger RNA ; models ; nucleotide sequences ; ribosomal RNA ; ribosomes
Language	English
Dates of publication	2019-0715
Size	p. 3377-3385.
Publishing place	American Chemical Society
Document type	Article
ZDB-ID	1108-3
ISSN	1520-4995 ; 0006-2960
ISSN (online)	1520-4995
ISSN	0006-2960
DOI	10.1021/acs.biochem.9b00076
Database	NAL-Catalogue (AGRICOLA)

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Article: Guidelines for SHAPE Reagent Choice and Detection Strategy for RNA Structure Probing Studies

Busan, Steven / Weidmann, Chase A / Sengupta, Arnab / Weeks, Kevin M

Biochemistry. 2019 May 22, v. 58, no. 23

2019

Abstract: Chemical probing is an important tool for characterizing the complex folded structures of RNA molecules, many of which play key cellular roles. Electrophilic SHAPE reagents create adducts at the 2′-hydroxyl position on the RNA backbone of flexible ... ...

Abstract	Chemical probing is an important tool for characterizing the complex folded structures of RNA molecules, many of which play key cellular roles. Electrophilic SHAPE reagents create adducts at the 2′-hydroxyl position on the RNA backbone of flexible ribonucleotides with relatively little dependence on nucleotide identity. Strategies for adduct detection such as mutational profiling (MaP) allow accurate, automated calculation of relative adduct frequencies for each nucleotide in a given RNA or group of RNAs. A number of alternative reagents and adduct detection strategies have been proposed, especially for use in living cells. Here we evaluate five SHAPE reagents: three previously well-validated reagents 1M7 (1-methyl-7-nitroisatoic anhydride), 1M6 (1-methyl-6-nitroisatoic anhydride), and NMIA (N-methylisatoic anhydride), one more recently proposed NAI (2-methylnicotinic acid imidazolide), and one novel reagent 5NIA (5-nitroisatoic anhydride). We clarify the importance of carefully designed software in reading out SHAPE experiments using massively parallel sequencing approaches. We examine SHAPE modification in living cells in diverse cell lines, compare MaP and reverse transcription–truncation as SHAPE adduct detection strategies, make recommendations for SHAPE reagent choice, and outline areas for future development.
Keywords	Lewis acids ; RNA ; anhydrides ; automation ; cell lines ; computer software ; high-throughput nucleotide sequencing ; ribonucleotides
Language	English
Dates of publication	2019-0522
Size	p. 2655-2664.
Publishing place	American Chemical Society
Document type	Article
ZDB-ID	1108-3
ISSN	1520-4995 ; 0006-2960
ISSN (online)	1520-4995
ISSN	0006-2960
DOI	10.1021/acs.biochem.8b01218
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Role of context in RNA structure: flanking sequences reconfigure CAG motif folding in huntingtin exon 1 transcripts.

Busan, Steven / Weeks, Kevin M

Biochemistry

2013 Volume 52, Issue 46, Page(s) 8219–8225

Abstract: The length of the CAG-repeat region in the huntingtin mRNA is predictive of Huntington's disease. Structural studies of CAG-repeat-containing RNAs suggest that these sequences form simple hairpin structures; however, in the context of the full-length ... ...

Abstract	The length of the CAG-repeat region in the huntingtin mRNA is predictive of Huntington's disease. Structural studies of CAG-repeat-containing RNAs suggest that these sequences form simple hairpin structures; however, in the context of the full-length huntingtin mRNA, CAG repeats may form complex structures that could be targeted for therapeutic intervention. We examined the structures of transcripts spanning the first exon of the huntingtin mRNA with both healthy and disease-prone repeat lengths. In transcripts with 17-70 repeats, the CAG sequences base paired extensively with nucleotides in the 5' UTR and with conserved downstream sequences including a CCG-repeat region. In huntingtin transcripts with healthy numbers of repeats, the previously observed CAG hairpin was either absent or short. In contrast, in transcripts with disease-associated numbers of repeats, a CAG hairpin was present and extended from a three-helix junction. Our findings demonstrate the profound importance of sequence context in RNA folding and identify specific structural differences between healthy and disease-inducing huntingtin alleles that may be targets for therapeutic intervention.
MeSH term(s)	5' Untranslated Regions/physiology ; Exons ; Humans ; Huntingtin Protein ; Huntington Disease/genetics ; Nerve Tissue Proteins/chemistry ; RNA/genetics ; RNA/metabolism ; RNA Folding ; RNA, Messenger/chemistry ; RNA, Messenger/genetics ; Ribonuclease T1/metabolism ; Trinucleotide Repeat Expansion
Chemical Substances	5' Untranslated Regions ; HTT protein, human ; Huntingtin Protein ; Nerve Tissue Proteins ; RNA, Messenger ; RNA (63231-63-0) ; Ribonuclease T1 (EC 3.1.27.3)
Language	English
Publishing date	2013-11-07
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1108-3
ISSN	1520-4995 ; 0006-2960
ISSN (online)	1520-4995
ISSN	0006-2960
DOI	10.1021/bi401129r
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