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Article ; Online: Correction to "Single-Molecule Correlated Chemical Probing: A Revolution in RNA Structure Analysis".

Mustoe, Anthony M / Weidmann, Chase A / Weeks, Kevin M

2023 Volume 56, Issue 12, Page(s) 1684

Language	English
Publishing date	2023-06-07
Publishing country	United States
Document type	Published Erratum
ZDB-ID	1483291-4
ISSN	1520-4898 ; 0001-4842
ISSN (online)	1520-4898
ISSN	0001-4842
DOI	10.1021/acs.accounts.3c00304
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Article ; Online: Single-Molecule Correlated Chemical Probing: A Revolution in RNA Structure Analysis.

Mustoe, Anthony M / Weidmann, Chase A / Weeks, Kevin M

Accounts of chemical research

2023 Volume 56, Issue 7, Page(s) 763–775

Abstract: RNA molecules convey biological information both in their linear sequence and in their base-paired secondary and tertiary structures. Chemical probing experiments, which involve treating an RNA with a reagent that modifies conformationally dynamic ... ...

Abstract	RNA molecules convey biological information both in their linear sequence and in their base-paired secondary and tertiary structures. Chemical probing experiments, which involve treating an RNA with a reagent that modifies conformationally dynamic nucleotides, have broadly enabled examination of short- and long-range RNA structure in diverse contexts, including in living cells. For decades, chemical probing experiments have been interpreted in a per-nucleotide way, such that the reactivity measured at each nucleotide reports the average structure at a position over all RNA molecules within a sample. However, there are numerous important cases where per-nucleotide chemical probing falls short, including for RNAs that are bound by proteins, RNAs that form complex higher order structures, and RNAs that sample multiple conformations.Recent experimental and computational innovations have started a revolution in RNA structure analysis by transforming chemical probing into a massively parallel, single-molecule experiment. Enabled by a specialized reverse transcription strategy called mutational profiling (MaP), multiple chemical modification events can be measured within individual RNA molecules. Nucleotides that communicate structurally through direct base pairing or large-scale folding-unfolding transitions will react with chemical probes in a correlated manner, thereby revealing structural complexity hidden to conventional approaches. These single-molecule correlated chemical probing (smCCP) experiments can be interpreted to directly identify nucleotides that base pair (the PAIR-MaP strategy) and to reveal long-range, through-space structural communication (RING-MaP). Correlated probing can also define the thermodynamic populations of complex RNA ensembles (DANCE-MaP). Complex RNA-protein networks can be interrogated by cross-linking proteins to RNA and measuring correlations between cross-linked positions (RNP-MaP).smCCP thus visualizes RNA secondary and higher-order structure with unprecedented accuracy, defining novel structures, RNA-protein interaction networks, time-resolved dynamics, and allosteric structural switches. These strategies are not mutually exclusive; in favorable cases, multiple levels of RNA structure ─ base pairing, through-space structural communication, and equilibrium ensembles ─ can be resolved concurrently. The physical experimentation required for smCCP is profoundly simple, and experiments are readily performed in cells on RNAs of any size, including large noncoding RNAs and mRNAs. Single-molecule correlated chemical probing is paving the way for a new generation of biophysical studies on RNA in living systems.
MeSH term(s)	Nucleic Acid Conformation ; RNA/chemistry ; Base Pairing ; RNA, Messenger ; Nucleotides ; Proteins/genetics
Chemical Substances	RNA (63231-63-0) ; RNA, Messenger ; Nucleotides ; Proteins
Language	English
Publishing date	2023-03-14
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't
ZDB-ID	1483291-4
ISSN	1520-4898 ; 0001-4842
ISSN (online)	1520-4898
ISSN	0001-4842
DOI	10.1021/acs.accounts.2c00782
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Article ; Online: Measuring Proximity-Mediated Function of mRNA Regulatory Proteins by Engineered Tethering.

Hatfield, Breanne M / Weidmann, Chase A / Weeks, Kevin M

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

2023 Volume 2723, Page(s) 143–159

Abstract: A powerful approach for studying the functional consequences of site-specific RNA-protein interactions is to artificially tether a protein to a messenger (or noncoding) RNA through a selective, high-affinity interaction. We share a strategy for ... ...

Abstract	A powerful approach for studying the functional consequences of site-specific RNA-protein interactions is to artificially tether a protein to a messenger (or noncoding) RNA through a selective, high-affinity interaction. We share a strategy for evaluating the contribution of protein positioning within an mRNA on gene expression. We introduced an RNA hairpin recognition site for the MS2 coat protein into the untranslated regions or coding sequence of mRNAs expressing a luminescent reporter protein, NanoLuc. Effector proteins fused to the MS2 coat protein could thus be targeted to distinct regions across the mRNA. We illustrate this approach using ZFP36L2, which recruits the CCR4-NOT complex for poly(A) tail deadenylation. Tethering ZFP36L2 to the 3'-UTR decreased NanoLuc expression, as expected, given the known interaction of this adapter protein with adenine uridine-rich elements (AREs). Intriguingly, ZFP36L2 also decreased NanoLuc expression when bound within the coding sequence, revealing that ZFP36L2-and potentially many other mRNA regulatory proteins-can function when targeted to diverse locations within an mRNA. This multi-target tethering strategy enables exploration of the interplay between mRNA-protein proximity and gene expression.
MeSH term(s)	RNA, Messenger/genetics ; RNA, Messenger/metabolism ; Transcription Factors/genetics ; 3' Untranslated Regions/genetics
Chemical Substances	RNA, Messenger ; Transcription Factors ; 3' Untranslated Regions
Language	English
Publishing date	2023-10-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-3481-3_9
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Article ; Online: Structural analysis of MALAT1 long noncoding RNA in cells and in evolution.

Monroy-Eklund, Anais / Taylor, Colin / Weidmann, Chase A / Burch, Christina / Laederach, Alain

RNA (New York, N.Y.)

2023 Volume 29, Issue 5, Page(s) 691–704

Abstract: Although not canonically polyadenylated, the long noncoding RNA MALAT1 (metastasis-associated lung adenocarcinoma transcript 1) is stabilized by a highly conserved 76-nt triple helix structure on its 3' end. The entire MALAT1 transcript is over 8000 nt ... ...

Abstract	Although not canonically polyadenylated, the long noncoding RNA MALAT1 (metastasis-associated lung adenocarcinoma transcript 1) is stabilized by a highly conserved 76-nt triple helix structure on its 3' end. The entire MALAT1 transcript is over 8000 nt long in humans. The strongest structural conservation signal in MALAT1 (as measured by covariation of base pairs) is in the triple helix structure. Primary sequence analysis of covariation alone does not reveal the degree of structural conservation of the entire full-length transcript, however. Furthermore, RNA structure is often context dependent; RNA binding proteins that are differentially expressed in different cell types may alter structure. We investigate here the in-cell and cell-free structures of the full-length human and green monkey (Chlorocebus sabaeus) MALAT1 transcripts in multiple tissue-derived cell lines using SHAPE chemical probing. Our data reveal levels of uniform structural conservation in different cell lines, in cells and cell-free, and even between species, despite significant differences in primary sequence. The uniformity of the structural conservation across the entire transcript suggests that, despite seeing covariation signals only in the triple helix junction of the lncRNA, the rest of the transcript's structure is remarkably conserved, at least in primates and across multiple cell types and conditions.
MeSH term(s)	Animals ; Humans ; Chlorocebus aethiops ; RNA, Long Noncoding/metabolism ; Base Pairing ; Cell Line ; RNA Stability ; Cell Proliferation ; Cell Line, Tumor
Chemical Substances	RNA, Long Noncoding
Language	English
Publishing date	2023-02-15
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; 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.079388.122
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Zs.A 4777: Show issues

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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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Zs.A 1067: Show issues

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Article ; Online: Discovery of a large-scale, cell-state-responsive allosteric switch in the 7SK RNA using DANCE-MaP.

Olson, Samuel W / Turner, Anne-Marie W / Arney, J Winston / Saleem, Irfana / Weidmann, Chase A / Margolis, David M / Weeks, Kevin M / Mustoe, Anthony M

Molecular cell

2022 Volume 82, Issue 9, Page(s) 1708–1723.e10

Abstract: 7SK is a conserved noncoding RNA that regulates transcription by sequestering the transcription factor P-TEFb. 7SK function entails complex changes in RNA structure, but characterizing RNA dynamics in cells remains an unsolved challenge. We developed a ... ...

Abstract	7SK is a conserved noncoding RNA that regulates transcription by sequestering the transcription factor P-TEFb. 7SK function entails complex changes in RNA structure, but characterizing RNA dynamics in cells remains an unsolved challenge. We developed a single-molecule chemical probing strategy, DANCE-MaP (deconvolution and annotation of ribonucleic conformational ensembles), that defines per-nucleotide reactivity, direct base pairing interactions, tertiary interactions, and thermodynamic populations for each state in RNA structural ensembles from a single experiment. DANCE-MaP reveals that 7SK RNA encodes a large-scale structural switch that couples dissolution of the P-TEFb binding site to structural remodeling at distal release factor binding sites. The 7SK structural equilibrium shifts in response to cell growth and stress and can be targeted to modulate expression of P-TEFbresponsive genes. Our study reveals that RNA structural dynamics underlie 7SK function as an integrator of diverse cellular signals to control transcription and establishes the power of DANCE-MaP to define RNA dynamics in cells.
MeSH term(s)	Binding Sites/genetics ; HeLa Cells ; Humans ; Positive Transcriptional Elongation Factor B/genetics ; RNA, Small Nuclear/genetics ; RNA, Untranslated ; RNA-Binding Proteins/genetics
Chemical Substances	RNA, Small Nuclear ; RNA, Untranslated ; RNA-Binding Proteins ; Positive Transcriptional Elongation Factor B (EC 2.7.11.-)
Language	English
Publishing date	2022-03-22
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2022.02.009
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Article: Discovery of a large-scale, cell-state-responsive allosteric switch in the 7SK RNA using DANCE-MaP

Olson, Samuel W. / Turner, Anne-Marie W. / Arney, J. Winston / Saleem, Irfana / Weidmann, Chase A. / Margolis, David M. / Weeks, Kevin M. / Mustoe, Anthony M.

Molecular cell. 2022 Feb. 02,

2022

Abstract	7SK is a conserved noncoding RNA that regulates transcription by sequestering the transcription factor P-TEFb. 7SK function entails complex changes in RNA structure, but characterizing RNA dynamics in cells remains an unsolved challenge. We developed a single-molecule chemical probing strategy, DANCE-MaP (deconvolution and annotation of ribonucleic conformational ensembles), that defines per-nucleotide reactivity, direct base pairing interactions, tertiary interactions, and thermodynamic populations for each state in RNA structural ensembles from a single experiment. DANCE-MaP reveals that 7SK RNA encodes a large-scale structural switch that couples dissolution of the P-TEFb binding site to structural remodeling at distal release factor binding sites. The 7SK structural equilibrium shifts in response to cell growth and stress and can be targeted to modulate expression of P-TEFbresponsive genes. Our study reveals that RNA structural dynamics underlie 7SK function as an integrator of diverse cellular signals to control transcription and establishes the power of DANCE-MaP to define RNA dynamics in cells.
Keywords	cell growth ; non-coding RNA ; thermodynamics ; transcription factors
Language	English
Dates of publication	2022-0202
Publishing place	Elsevier Inc.
Document type	Article
Note	Pre-press version
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2022.02.009
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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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Zs.A 217: Show issues

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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 ; Online: Analysis of RNA-protein networks with RNP-MaP defines functional hubs on RNA.

Weidmann, Chase A / Mustoe, Anthony M / Jariwala, Parth B / Calabrese, J Mauro / Weeks, Kevin M

Nature biotechnology

2020 Volume 39, Issue 3, Page(s) 347–356

Abstract: RNA-protein interaction networks govern many biological processes but are difficult to examine comprehensively. We devised ribonucleoprotein networks analyzed by mutational profiling (RNP-MaP), a live-cell chemical probing strategy that maps cooperative ... ...

Abstract	RNA-protein interaction networks govern many biological processes but are difficult to examine comprehensively. We devised ribonucleoprotein networks analyzed by mutational profiling (RNP-MaP), a live-cell chemical probing strategy that maps cooperative interactions among multiple proteins bound to single RNA molecules at nucleotide resolution. RNP-MaP uses a hetero-bifunctional crosslinker to freeze interacting proteins in place on RNA and then maps multiple bound proteins on single RNA strands by read-through reverse transcription and DNA sequencing. RNP-MaP revealed that RNase P and RMRP, two sequence-divergent but structurally related non-coding RNAs, share RNP networks and that network hubs define functional sites in these RNAs. RNP-MaP also identified protein interaction networks conserved between mouse and human XIST long non-coding RNAs and defined protein communities whose binding sites colocalize and form networks in functional regions of XIST. RNP-MaP enables discovery and efficient validation of functional protein interaction networks on long RNAs in living cells.
MeSH term(s)	Animals ; Humans ; Protein Interaction Maps ; RNA/metabolism ; RNA, Long Noncoding/metabolism ; RNA-Binding Proteins/metabolism ; Reproducibility of Results ; Ribonuclease P/metabolism ; Ribonucleoproteins/metabolism
Chemical Substances	RNA, Long Noncoding ; RNA-Binding Proteins ; Ribonucleoproteins ; XIST non-coding RNA ; RNA (63231-63-0) ; Ribonuclease P (EC 3.1.26.5)
Language	English
Publishing date	2020-10-19
Publishing country	United States
Document type	Journal Article ; 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	1311932-1
ISSN	1546-1696 ; 1087-0156
ISSN (online)	1546-1696
ISSN	1087-0156
DOI	10.1038/s41587-020-0709-7
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