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Article ; Online: In silico analysis of local RNA secondary structure in influenza virus A, B and C finds evidence of widespread ordered stability but little evidence of significant covariation

Jake M. Peterson / Collin A. O’Leary / Walter N. Moss

Scientific Reports, Vol 12, Iss 1, Pp 1-

2022 Volume 10

Abstract: Abstract Influenza virus is a persistent threat to human health; indeed, the deadliest modern pandemic was in 1918 when an H1N1 virus killed an estimated 50 million people globally. The intent of this work is to better understand influenza from an RNA- ... ...

Abstract	Abstract Influenza virus is a persistent threat to human health; indeed, the deadliest modern pandemic was in 1918 when an H1N1 virus killed an estimated 50 million people globally. The intent of this work is to better understand influenza from an RNA-centric perspective to provide local, structural motifs with likely significance to the influenza infectious cycle for therapeutic targeting. To accomplish this, we analyzed over four hundred thousand RNA sequences spanning three major clades: influenza A, B and C. We scanned influenza segments for local secondary structure, identified/modeled motifs of likely functionality, and coupled the results to an analysis of evolutionary conservation. We discovered 185 significant regions of predicted ordered stability, yet evidence of sequence covariation was limited to 7 motifs, where 3—found in influenza C—had higher than expected amounts of sequence covariation.
Keywords	Medicine ; R ; Science ; Q
Language	English
Publishing date	2022-01-01T00:00:00Z
Publisher	Nature Portfolio
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Analysis of a structured intronic region of the LMP2 pre-mRNA from EBV reveals associations with human regulatory proteins and nuclear actin

Nuwanthika Kumarasinghe / Walter N. Moss

BMC Research Notes, Vol 12, Iss 1, Pp 1-

2019 Volume 6

Abstract: Abstract Objective The pre-mRNA of the Epstein–Barr virus LMP2 (latent membrane protein 2) has a region of unusual RNA structure that partially spans two consecutive exons and the entire intervening intron; suggesting RNA folding might affect splicing— ... ...

Abstract	Abstract Objective The pre-mRNA of the Epstein–Barr virus LMP2 (latent membrane protein 2) has a region of unusual RNA structure that partially spans two consecutive exons and the entire intervening intron; suggesting RNA folding might affect splicing—particularly via interactions with human regulatory proteins. To better understand the roles of protein associations with this structured intronic region, we undertook a combined bioinformatics (motif searching) and experimental analysis (biotin pulldowns and RNA immunoprecipitations) of protein binding. Result Characterization of the ribonucleoprotein composition of this region revealed several human proteins as interactors: regulatory proteins hnRNP A1 (heterogeneous nuclear ribonucleoprotein A1), hnRNP U, HuR (human antigen R), and PSF (polypyrimidine tract-binding protein-associated splicing factor), as well as, unexpectedly, the cytoskeletal protein actin. Treatment of EBV-positive cells with drugs that alter actin polymerization specifically showed marked effects on splicing in this region. This suggests a potentially novel role for nuclear actin in regulation of viral RNA splicing.
Keywords	Epstein–Barr virus ; EBV ; LMP2 ; Herpes virus ; RNA ; Splicing ; Medicine ; R ; Biology (General) ; QH301-705.5 ; Science (General) ; Q1-390
Subject code	570 ; 612
Language	English
Publishing date	2019-01-01T00:00:00Z
Publisher	BMC
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Identification of MYC intron 2 regions that modulate expression

Van S. Tompkins / Zheng Xue / Jake M. Peterson / Warren B. Rouse / Collin A. O’Leary / Walter N. Moss

PLoS ONE, Vol 19, Iss

2024 Volume 1

Keywords	Medicine ; R ; Science ; Q
Language	English
Publishing date	2024-01-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Expansion of the RNAStructuromeDB to include secondary structural data spanning the human protein-coding transcriptome

Warren B. Rouse / Collin A. O’Leary / Nicholas J. Booher / Walter N. Moss

Scientific Reports, Vol 12, Iss 1, Pp 1-

2022 Volume 13

Abstract: Abstract RNA plays vital functional roles in almost every component of biology, and these functional roles are often influenced by its folding into secondary and tertiary structures. An important role of RNA secondary structure is in maintaining proper ... ...

Abstract	Abstract RNA plays vital functional roles in almost every component of biology, and these functional roles are often influenced by its folding into secondary and tertiary structures. An important role of RNA secondary structure is in maintaining proper gene regulation; therefore, making accurate predictions of the structures involved in these processes is important. In this study, we have expanded on our previous work that led to the creation of the RNAStructuromeDB. Unlike this previous study that analyzed the human genome at low resolution, we have now scanned the protein-coding human transcriptome at high (single nt) resolution. This provides more robust structure predictions for over 100,000 isoforms of known protein-coding genes. Notably, we also utilize the motif identification tool, ScanFold, to model structures with high propensity for ordered/evolved stability. All data have been uploaded to the RNAStructuromeDB, allowing for easy searching of transcripts, visualization of data tracks (via the Integrative Genomics Viewer or IGV), and download of ScanFold data—including unique highly-ordered motifs. Herein, we provide an example analysis of MAT2A to demonstrate the utility of ScanFold at finding known and novel secondary structures, highlighting regions of potential functionality, and guiding generation of functional hypotheses through use of the data.
Keywords	Medicine ; R ; Science ; Q
Subject code	612
Language	English
Publishing date	2022-08-01T00:00:00Z
Publisher	Nature Portfolio
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Discovery of RNA secondary structural motifs using sequence-ordered thermodynamic stability and comparative sequence analysis

Jake M. Peterson / Collin A. O'Leary / Evelyn C. Coppenbarger / Van S. Tompkins / Walter N. Moss

MethodsX, Vol 11, Iss , Pp 102275- (2023)

2023

Abstract: Major advances in RNA secondary structural motif prediction have been achieved in the last few years; however, few methods harness the predictive power of multiple approaches to deliver in-depth characterizations of local RNA motifs and their potential ... ...

Abstract	Major advances in RNA secondary structural motif prediction have been achieved in the last few years; however, few methods harness the predictive power of multiple approaches to deliver in-depth characterizations of local RNA motifs and their potential functionality. Additionally, most available methods do not predict RNA pseudoknots. This work combines complementary bioinformatic systems into one robust discovery pipeline where: • RNA sequences are folded to search for thermodynamically favorable motifs utilizing ScanFold. • Motifs are expanded and refolded into alternate pseudoknot conformations by Knotty/Iterative HFold. • All conformations are evaluated for covariance via the cm-builder pipeline (Infernal and R-scape).
Keywords	Cobretti ; Science ; Q
Language	English
Publishing date	2023-12-01T00:00:00Z
Publisher	Elsevier
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: A survey of RNA secondary structural propensity encoded within human herpesvirus genomes

Ryan J. Andrews / Collin A. O’Leary / Walter N. Moss

PeerJ, Vol 8, p e

global comparisons and local motifs

2020 Volume 9882

Abstract: There are nine herpesviruses known to infect humans, of which Epstein–Barr virus (EBV) is the most widely distributed (>90% of adults infected). This ubiquitous virus is implicated in a variety of cancers and autoimmune diseases. Previous analyses of the ...

Abstract	There are nine herpesviruses known to infect humans, of which Epstein–Barr virus (EBV) is the most widely distributed (>90% of adults infected). This ubiquitous virus is implicated in a variety of cancers and autoimmune diseases. Previous analyses of the EBV genome revealed numerous regions with evidence of generating unusually stable and conserved RNA secondary structures and led to the discovery of a novel class of EBV non-coding (nc)RNAs: the stable intronic sequence (sis)RNAs. To gain a better understanding of the roles of RNA structure in EBV biology and pathogenicity, we revisit EBV using recently developed tools for genome-wide motif discovery and RNA structural characterization. This corroborated previous results and revealed novel motifs with potential functionality; one of which has been experimentally validated. Additionally, since many herpesviruses increasingly rival the seroprevalence of EBV (VZV, HHV-6 and HHV-7 being the most notable), analyses were expanded to include all sequenced human Herpesvirus RefSeq genomes, allowing for genomic comparisons. In total 10 genomes were analyzed, for EBV (types 1 and 2), HCMV, HHV-6A, HHV-6B, HHV-7, HSV-1, HSV-2, KSHV, and VZV. All resulting data were archived in the RNAStructuromeDB (https://structurome.bb.iastate.edu/herpesvirus) to make them available to a wide array of researchers.
Keywords	RNA ; Herpes viruses ; Motif scan ; RNA structure ; EBV ; KSHV ; Medicine ; R ; Biology (General) ; QH301-705.5
Subject code	500
Language	English
Publishing date	2020-09-01T00:00:00Z
Publisher	PeerJ Inc.
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: ScanFold

Ryan J. Andrews / Julien Roche / Walter N. Moss

PeerJ, Vol 6, p e

an approach for genome-wide discovery of local RNA structural elements—applications to Zika virus and HIV

2018 Volume 6136

Abstract: In addition to encoding RNA primary structures, genomes also encode RNA secondary and tertiary structures that play roles in gene regulation and, in the case of RNA viruses, genome replication. Methods for the identification of functional RNA structures ... ...

Abstract	In addition to encoding RNA primary structures, genomes also encode RNA secondary and tertiary structures that play roles in gene regulation and, in the case of RNA viruses, genome replication. Methods for the identification of functional RNA structures in genomes typically rely on scanning analysis windows, where multiple partially-overlapping windows are used to predict RNA structures and folding metrics to deduce regions likely to form functional structure. Separate structural models are produced for each window, where the step size can greatly affect the returned model. This makes deducing unique local structures challenging, as the same nucleotides in each window can be alternatively base paired. We are presenting here a new approach where all base pairs from analysis windows are considered and weighted by favorable folding. This results in unique base pairing throughout the genome and the generation of local regions/structures that can be ranked by their propensity to form unusually thermodynamically stable folds. We applied this approach to the Zika virus (ZIKV) and HIV-1 genomes. ZIKV is linked to a variety of neurological ailments including microcephaly and Guillain–Barré syndrome and its (+)-sense RNA genome encodes two, previously described, functionally essential structured RNA regions. HIV, the cause of AIDS, contains multiple functional RNA motifs in its genome, which have been extensively studied. Our approach is able to successfully identify and model the structures of known functional motifs in both viruses, while also finding additional regions likely to form functional structures. All data have been archived at the RNAStructuromeDB (www.structurome.bb.iastate.edu), a repository of RNA folding data for humans and their pathogens.
Keywords	RNA ; RNA structure ; Zika virus ; Motif discovery ; Bioinformatics ; Sequence analysis ; Medicine ; R
Subject code	612
Language	English
Publishing date	2018-12-01T00:00:00Z
Publisher	PeerJ Inc.
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Secondary Structure of Influenza A Virus Genomic Segment 8 RNA Folded in a Cellular Environment

Barbara Szutkowska / Klaudia Wieczorek / Ryszard Kierzek / Pawel Zmora / Jake M. Peterson / Walter N. Moss / David H. Mathews / Elzbieta Kierzek

International Journal of Molecular Sciences, Vol 23, Iss 2452, p

2022 Volume 2452

Abstract: Influenza A virus (IAV) is a member of the single-stranded RNA (ssRNA) family of viruses. The most recent global pandemic caused by the SARS-CoV-2 virus has shown the major threat that RNA viruses can pose to humanity. In comparison, influenza has an ... ...

Abstract	Influenza A virus (IAV) is a member of the single-stranded RNA (ssRNA) family of viruses. The most recent global pandemic caused by the SARS-CoV-2 virus has shown the major threat that RNA viruses can pose to humanity. In comparison, influenza has an even higher pandemic potential as a result of its high rate of mutations within its relatively short (<13 kbp) genome, as well as its capability to undergo genetic reassortment. In light of this threat, and the fact that RNA structure is connected to a broad range of known biological functions, deeper investigation of viral RNA (vRNA) structures is of high interest. Here, for the first time, we propose a secondary structure for segment 8 vRNA (vRNA8) of A/California/04/2009 (H1N1) formed in the presence of cellular and viral components. This structure shows similarities with prior in vitro experiments. Additionally, we determined the location of several well-defined, conserved structural motifs of vRNA8 within IAV strains with possible functionality. These RNA motifs appear to fold independently of regional nucleoprotein (NP)-binding affinity, but a low or uneven distribution of NP in each motif region is noted. This research also highlights several accessible sites for oligonucleotide tools and small molecules in vRNA8 in a cellular environment that might be a target for influenza A virus inhibition on the RNA level.
Keywords	influenza A virus ; IAV ; RNA virus ; RNA secondary structure ; RNA chemical mapping ; Biology (General) ; QH301-705.5 ; Chemistry ; QD1-999
Subject code	500
Language	English
Publishing date	2022-02-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Analyses of human cancer driver genes uncovers evolutionarily conserved RNA structural elements involved in posttranscriptional control.

Van S Tompkins / Warren B Rouse / Collin A O'Leary / Ryan J Andrews / Walter N Moss

PLoS ONE, Vol 17, Iss 2, p e

2022 Volume 0264025

Abstract: Experimental breakthroughs have provided unprecedented insights into the genes involved in cancer. The identification of such cancer driver genes is a major step in gaining a fuller understanding of oncogenesis and provides novel lists of potential ... ...

Abstract	Experimental breakthroughs have provided unprecedented insights into the genes involved in cancer. The identification of such cancer driver genes is a major step in gaining a fuller understanding of oncogenesis and provides novel lists of potential therapeutic targets. A key area that requires additional study is the posttranscriptional control mechanisms at work in cancer driver genes. This is important not only for basic insights into the biology of cancer, but also to advance new therapeutic modalities that target RNA-an emerging field with great promise toward the treatment of various cancers. In the current study we performed an in silico analysis on the transcripts associated with 800 cancer driver genes (10,390 unique transcripts) that identified 179,190 secondary structural motifs with evidence of evolutionarily ordered structures with unusual thermodynamic stability. Narrowing to one transcript per gene, 35,426 predicted structures were subjected to phylogenetic comparisons of sequence and structural conservation. This identified 7,001 RNA secondary structures embedded in transcripts with evidence of covariation between paired sites, supporting structure models and suggesting functional significance. A select set of seven structures were tested in vitro for their ability to regulate gene expression; all were found to have significant effects. These results indicate potentially widespread roles for RNA structure in posttranscriptional control of human cancer driver genes.
Keywords	Medicine ; R ; Science ; Q
Subject code	572
Language	English
Publishing date	2022-01-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Structural Context of a Critical Exon of Spinal Muscular Atrophy Gene

Natalia N. Singh / Collin A. O'Leary / Taylor Eich / Walter N. Moss / Ravindra N. Singh

Frontiers in Molecular Biosciences, Vol

2022 Volume 9

Abstract: Humans contain two nearly identical copies of Survival Motor Neuron genes, SMN1 and SMN2. Deletion or mutation of SMN1 causes spinal muscular atrophy (SMA), one of the leading genetic diseases associated with infant mortality. SMN2 is unable to ... ...

Abstract	Humans contain two nearly identical copies of Survival Motor Neuron genes, SMN1 and SMN2. Deletion or mutation of SMN1 causes spinal muscular atrophy (SMA), one of the leading genetic diseases associated with infant mortality. SMN2 is unable to compensate for the loss of SMN1 due to predominant exon 7 skipping, leading to the production of a truncated protein. Antisense oligonucleotide and small molecule-based strategies aimed at the restoration of SMN2 exon 7 inclusion are approved therapies of SMA. Many cis-elements and transacting factors have been implicated in regulation of SMN exon 7 splicing. Also, several structural elements, including those formed by a long-distance interaction, have been implicated in the modulation of SMN exon 7 splicing. Several of these structures have been confirmed by enzymatic and chemical structure-probing methods. Additional structures formed by inter-intronic interactions have been predicted by computational algorithms. SMN genes generate a vast repertoire of circular RNAs through inter-intronic secondary structures formed by inverted Alu repeats present in large number in SMN genes. Here, we review the structural context of the exonic and intronic cis-elements that promote or prevent exon 7 recognition. We discuss how structural rearrangements triggered by single nucleotide substitutions could bring drastic changes in SMN2 exon 7 splicing. We also propose potential mechanisms by which inter-intronic structures might impact the splicing outcomes.
Keywords	RNA structure ; splicing ; small molecule ; spinal muscular atrophy ; SMA ; survival motor neuron ; Biology (General) ; QH301-705.5
Subject code	572
Language	English
Publishing date	2022-07-01T00:00:00Z
Publisher	Frontiers Media S.A.
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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