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Article ; Online: Structural and Functional RNA Motifs of SARS-CoV-2 and Influenza A Virus as a Target of Viral Inhibitors.

Szczesniak, Izabela / Baliga-Gil, Agnieszka / Jarmolowicz, Aleksandra / Soszynska-Jozwiak, Marta / Kierzek, Elzbieta

International journal of molecular sciences

2023 Volume 24, Issue 2

Abstract: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is responsible for the COVID-19 pandemic, whereas the influenza A virus (IAV) causes seasonal epidemics and occasional pandemics. Both viruses lead to widespread infection and death. SARS-CoV-2 ...

Abstract	Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is responsible for the COVID-19 pandemic, whereas the influenza A virus (IAV) causes seasonal epidemics and occasional pandemics. Both viruses lead to widespread infection and death. SARS-CoV-2 and the influenza virus are RNA viruses. The SARS-CoV-2 genome is an approximately 30 kb, positive sense, 5' capped single-stranded RNA molecule. The influenza A virus genome possesses eight single-stranded negative-sense segments. The RNA secondary structure in the untranslated and coding regions is crucial in the viral replication cycle. The secondary structure within the RNA of SARS-CoV-2 and the influenza virus has been intensively studied. Because the whole of the SARS-CoV-2 and influenza virus replication cycles are dependent on RNA with no DNA intermediate, the RNA is a natural and promising target for the development of inhibitors. There are a lot of RNA-targeting strategies for regulating pathogenic RNA, such as small interfering RNA for RNA interference, antisense oligonucleotides, catalytic nucleic acids, and small molecules. In this review, we summarized the knowledge about the inhibition of SARS-CoV-2 and influenza A virus propagation by targeting their RNA secondary structure.
MeSH term(s)	Humans ; SARS-CoV-2 ; COVID-19 ; Influenza A virus/genetics ; Nucleotide Motifs ; Pandemics ; Orthomyxoviridae ; RNA ; RNA, Viral/genetics ; RNA, Viral/chemistry
Chemical Substances	RNA (63231-63-0) ; RNA, Viral
Language	English
Publishing date	2023-01-08
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/ijms24021232
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Secondary Structure of Subgenomic RNA M of SARS-CoV-2

Soszynska-Jozwiak, Marta / Ruszkowska, Agnieszka / Kierzek, Ryszard / O’Leary, Collin A. / Moss, Walter N. / Kierzek, Elzbieta

Viruses. 2022 Feb. 04, v. 14, no. 2

2022

Abstract: SARS-CoV-2 belongs to the Coronavirinae family. Like other coronaviruses, SARS-CoV-2 is enveloped and possesses a positive-sense, single-stranded RNA genome of ~30 kb. Genomic RNA is used as the template for replication and transcription. During these ... ...

Abstract	SARS-CoV-2 belongs to the Coronavirinae family. Like other coronaviruses, SARS-CoV-2 is enveloped and possesses a positive-sense, single-stranded RNA genome of ~30 kb. Genomic RNA is used as the template for replication and transcription. During these processes, positive-sense genomic RNA (gRNA) and subgenomic RNAs (sgRNAs) are created. Several studies presented the importance of the genomic RNA secondary structure in SARS-CoV-2 replication. However, the structure of sgRNAs has remained largely unsolved so far. In this study, we probed the sgRNA M model of SARS-CoV-2 in vitro. The presented model molecule includes 5′UTR and a coding sequence of gene M. This is the first experimentally informed secondary structure model of sgRNA M, which presents features likely to be important in sgRNA M function. The knowledge of sgRNA M structure provides insights to better understand virus biology and could be used for designing new therapeutics.
Keywords	Severe acute respiratory syndrome coronavirus 2 ; genes ; genomics ; models ; therapeutics ; viruses
Language	English
Dates of publication	2022-0204
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2516098-9
ISSN	1999-4915
ISSN	1999-4915
DOI	10.3390/v14020322
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Secondary structure of subgenomic RNA M of SARS-CoV-2

Soszynska-Jozwiak, Marta / Kierzek, Ryszard / Kierzek, Elzbieta

bioRxiv

Abstract: SARS-CoV-2 belongs the Coronavirinae family. As other coronaviruses, SARS-CoV-2 is enveloped and possesses positive-sense, single-stranded RNA genome of ~30 kb. Genome RNA is used as the template for replication and transcription. During these processes, ...

Abstract	SARS-CoV-2 belongs the Coronavirinae family. As other coronaviruses, SARS-CoV-2 is enveloped and possesses positive-sense, single-stranded RNA genome of ~30 kb. Genome RNA is used as the template for replication and transcription. During these processes, positive-sense genomic RNA (gRNA) and subgenomic RNAs (sgRNAs) are created. Several studies showed importance of genomic RNA secondary structure in SARS-CoV-2 replication. However, the structure of sgRNAs have remained largely unsolved so far. In this study, we performed probing of sgRNA M of SARS-CoV-2 in vitro. This is the first experimentally informed secondary structure model of sgRNA M, which presents features likely to be important in sgRNA M function. The knowledge about sgRNA M provides insights to better understand virus biology and could be used for designing new therapeutics.
Keywords	covid19
Language	English
Publishing date	2021-10-12
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2021.10.11.463917
Database	COVID19

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Article ; Online: Secondary Structure of Subgenomic RNA M of SARS-CoV-2.

Soszynska-Jozwiak, Marta / Ruszkowska, Agnieszka / Kierzek, Ryszard / O'Leary, Collin A / Moss, Walter N / Kierzek, Elzbieta

Viruses

2022 Volume 14, Issue 2

Abstract: SARS-CoV-2 belongs to ... ...

Abstract	SARS-CoV-2 belongs to the
MeSH term(s)	5' Untranslated Regions ; COVID-19/virology ; Genome, Viral ; Genomics ; Humans ; Open Reading Frames ; RNA, Viral/chemistry ; RNA, Viral/genetics ; SARS-CoV-2/genetics ; Transcription, Genetic
Chemical Substances	5' Untranslated Regions ; RNA, Viral
Language	English
Publishing date	2022-02-04
Publishing country	Switzerland
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v14020322
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Universal and strain specific structure features of segment 8 genomic RNA of influenza A virus-application of 4-thiouridine photocrosslinking.

Soszynska-Jozwiak, Marta / Pszczola, Maciej / Piasecka, Julita / Peterson, Jake M / Moss, Walter N / Taras-Goslinska, Katarzyna / Kierzek, Ryszard / Kierzek, Elzbieta

The Journal of biological chemistry

2021 Volume 297, Issue 6, Page(s) 101245

Abstract: RNA structure in the influenza A virus (IAV) has been the focus of several studies that have shown connections between conserved secondary structure motifs and their biological function in the virus replication cycle. Questions have arisen on how to best ...

Abstract	RNA structure in the influenza A virus (IAV) has been the focus of several studies that have shown connections between conserved secondary structure motifs and their biological function in the virus replication cycle. Questions have arisen on how to best recognize and understand the pandemic properties of IAV strains from an RNA perspective, but determination of the RNA secondary structure has been challenging. Herein, we used chemical mapping to determine the secondary structure of segment 8 viral RNA (vRNA) of the pandemic A/California/04/2009 (H1N1) strain of IAV. Additionally, this long, naturally occurring RNA served as a model to evaluate RNA mapping with 4-thiouridine (4sU) crosslinking. We explored 4-thiouridine as a probe of nucleotides in close proximity, through its incorporation into newly transcribed RNA and subsequent photoactivation. RNA secondary structural features both universal to type A strains and unique to the A/California/04/2009 (H1N1) strain were recognized. 4sU mapping confirmed and facilitated RNA structure prediction, according to several rules: 4sU photocross-linking forms efficiently in the double-stranded region of RNA with some flexibility, in the ends of helices, and across bulges and loops when their structural mobility is permitted. This method highlighted three-dimensional properties of segment 8 vRNA secondary structure motifs and allowed to propose several long-range three-dimensional interactions. 4sU mapping combined with chemical mapping and bioinformatic analysis could be used to enhance the RNA structure determination as well as recognition of target regions for antisense strategies or viral RNA detection.
MeSH term(s)	Base Pairing ; Base Sequence ; Cross-Linking Reagents/chemistry ; Humans ; Influenza A virus/chemistry ; Influenza, Human/virology ; Nucleic Acid Conformation ; RNA, Viral/chemistry ; Thiouridine/chemistry
Chemical Substances	Cross-Linking Reagents ; RNA, Viral ; Thiouridine (13957-31-8)
Language	English
Publishing date	2021-10-22
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2997-x
ISSN	1083-351X ; 0021-9258
ISSN (online)	1083-351X
ISSN	0021-9258
DOI	10.1016/j.jbc.2021.101245
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: RNA Secondary Structure Motifs of the Influenza A Virus as Targets for siRNA-Mediated RNA Interference.

Piasecka, Julita / Lenartowicz, Elzbieta / Soszynska-Jozwiak, Marta / Szutkowska, Barbara / Kierzek, Ryszard / Kierzek, Elzbieta

Molecular therapy. Nucleic acids

2019 Volume 19, Page(s) 627–642

Abstract: The influenza A virus is a human pathogen that poses a serious public health threat due to rapid antigen changes and emergence of new, highly pathogenic strains with the potential to become easily transmitted in the human population. The viral genome is ... ...

Abstract	The influenza A virus is a human pathogen that poses a serious public health threat due to rapid antigen changes and emergence of new, highly pathogenic strains with the potential to become easily transmitted in the human population. The viral genome is encoded by eight RNA segments, and all stages of the replication cycle are dependent on RNA. In this study, we designed small interfering RNA (siRNA) targeting influenza segment 5 nucleoprotein (NP) mRNA structural motifs that encode important functions. The new criterion for choosing the siRNA target was the prediction of accessible regions based on the secondary structure of segment 5 (+)RNA. This design led to siRNAs that significantly inhibit influenza virus type A replication in Madin-Darby canine kidney (MDCK) cells. Additionally, chemical modifications with the potential to improve siRNA properties were introduced and systematically validated in MDCK cells against the virus. A substantial and maximum inhibitory effect was achieved at concentrations as low as 8 nM. The inhibition of viral replication reached approximately 90% for the best siRNA variants. Additionally, selected siRNAs were compared with antisense oligonucleotides targeting the same regions; this revealed that effectiveness depends on both the target accessibility and oligonucleotide antiviral strategy. Our new approach of target-site preselection based on segment 5 (+)RNA secondary structure led to effective viral inhibition and a better understanding of the impact of RNA structural motifs on the influenza replication cycle.
Language	English
Publishing date	2019-12-24
Publishing country	United States
Document type	Journal Article
ZDB-ID	2662631-7
ISSN	2162-2531
ISSN	2162-2531
DOI	10.1016/j.omtn.2019.12.018
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Secondary structure of the segment 5 genomic RNA of influenza A virus and its application for designing antisense oligonucleotides.

Michalak, Paula / Soszynska-Jozwiak, Marta / Biala, Ewa / Moss, Walter N / Kesy, Julita / Szutkowska, Barbara / Lenartowicz, Elzbieta / Kierzek, Ryszard / Kierzek, Elzbieta

Scientific reports

2019 Volume 9, Issue 1, Page(s) 3801

Abstract: Influenza virus causes seasonal epidemics and dangerous pandemic outbreaks. It is a single stranded (-)RNA virus with a segmented genome. Eight segments of genomic viral RNA (vRNA) form the virion, which are then transcribed and replicated in host cells. ...

Abstract	Influenza virus causes seasonal epidemics and dangerous pandemic outbreaks. It is a single stranded (-)RNA virus with a segmented genome. Eight segments of genomic viral RNA (vRNA) form the virion, which are then transcribed and replicated in host cells. The secondary structure of vRNA is an important regulator of virus biology and can be a target for finding new therapeutics. In this paper, the secondary structure of segment 5 vRNA is determined based on chemical mapping data, free energy minimization and structure-sequence conservation analysis for type A influenza. The revealed secondary structure has circular folding with a previously reported panhandle motif and distinct novel domains. Conservations of base pairs is 87% on average with many structural motifs that are highly conserved. Isoenergetic microarray mapping was used to additionally validate secondary structure and to discover regions that easy bind short oligonucleotides. Antisense oligonucleotides, which were designed based on modeled secondary structure and microarray mapping, inhibit influenza A virus proliferation in MDCK cells. The most potent oligonucleotides lowered virus titer by ~90%. These results define universal for type A structured regions that could be important for virus function, as well as new targets for antisense therapeutics.
MeSH term(s)	Genome, Viral ; Influenza A virus/genetics ; Oligonucleotides, Antisense ; Protein Structure, Secondary
Chemical Substances	Oligonucleotides, Antisense
Language	English
Publishing date	2019-03-07
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-019-40443-7
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Influenza virus segment 5 (+)RNA - secondary structure and new targets for antiviral strategies.

Soszynska-Jozwiak, Marta / Michalak, Paula / Moss, Walter N / Kierzek, Ryszard / Kesy, Julita / Kierzek, Elzbieta

Scientific reports

2017 Volume 7, Issue 1, Page(s) 15041

Abstract: Influenza A virus is a threat for humans due to seasonal epidemics and occasional pandemics. This virus can generate new strains that are dangerous through nucleotide/amino acid changes or through segmental recombination of the viral RNA genome. It is ... ...

Abstract	Influenza A virus is a threat for humans due to seasonal epidemics and occasional pandemics. This virus can generate new strains that are dangerous through nucleotide/amino acid changes or through segmental recombination of the viral RNA genome. It is important to gain wider knowledge about influenza virus RNA to create new strategies for drugs that will inhibit its spread. Here, we present the experimentally determined secondary structure of the influenza segment 5 (+)RNA. Two RNAs were studied: the full-length segment 5 (+)RNA and a shorter construct containing only the coding region. Chemical mapping data combined with thermodynamic energy minimization were used in secondary structure prediction. Sequence/structure analysis showed that the determined secondary structure of segment 5 (+)RNA is mostly conserved between influenza virus type A strains. Microarray mapping and RNase H cleavage identified accessible sites for oligonucleotides in the revealed secondary structure of segment 5 (+)RNA. Antisense oligonucleotides were designed based on the secondary structure model and tested against influenza virus in cell culture. Inhibition of influenza virus proliferation was noticed, identifying good targets for antisense strategies. Effective target sites fall within two domains, which are conserved in sequence/structure indicating their importance to the virus.
MeSH term(s)	Animals ; Antiviral Agents/therapeutic use ; Base Sequence ; Dogs ; Humans ; Influenza A Virus, H5N1 Subtype/drug effects ; Influenza A Virus, H5N1 Subtype/genetics ; Influenza, Human/prevention & control ; Influenza, Human/virology ; Madin Darby Canine Kidney Cells ; Models, Molecular ; Nucleic Acid Conformation ; Oligonucleotides, Antisense/genetics ; Open Reading Frames/genetics ; RNA, Viral/chemistry ; RNA, Viral/genetics ; RNA, Viral/metabolism ; Ribonuclease H/metabolism ; Virus Replication/drug effects ; Virus Replication/genetics
Chemical Substances	Antiviral Agents ; Oligonucleotides, Antisense ; RNA, Viral ; Ribonuclease H (EC 3.1.26.4)
Language	English
Publishing date	2017-11-08
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2615211-3
ISSN	2045-2322 ; 2045-2322
ISSN (online)	2045-2322
ISSN	2045-2322
DOI	10.1038/s41598-017-15317-5
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: A Conserved Secondary Structural Element in the Coding Region of the Influenza A Virus Nucleoprotein (NP) mRNA Is Important for the Regulation of Viral Proliferation.

Soszynska-Jozwiak, Marta / Michalak, Paula / Moss, Walter N / Kierzek, Ryszard / Kierzek, Elzbieta

PloS one

2015 Volume 10, Issue 10, Page(s) e0141132

Abstract: Influenza A virus is a threat to humans due to seasonal epidemics and infrequent, but dangerous, pandemics that lead to widespread infection and death. Eight segments of RNA constitute the genome of this virus and they encode greater than eight proteins ... ...

Abstract	Influenza A virus is a threat to humans due to seasonal epidemics and infrequent, but dangerous, pandemics that lead to widespread infection and death. Eight segments of RNA constitute the genome of this virus and they encode greater than eight proteins via alternative splicing of coding (+)RNAs generated from the genomic (-)RNA template strand. RNA is essential in its life cycle. A bioinformatics analysis of segment 5, which encodes nucleoprotein, revealed a conserved structural motif in the (+)RNA. The secondary structure proposed by energy minimization and comparative analysis agrees with structure predicted based on experimental data using a 121 nucleotide in vitro RNA construct comprising an influenza A virus consensus sequence and also an entire segment 5 (+)RNA (strain A/VietNam/1203/2004 (H5N1)). The conserved motif consists of three hairpins with one being especially thermodynamically stable. The biological importance of this conserved secondary structure is supported in experiments using antisense oligonucleotides in cell line, which found that disruption of this motif led to inhibition of viral fitness. These results suggest that this conserved motif in the segment 5 (+)RNA might be a candidate for oligonucleotide-based antiviral therapy.
MeSH term(s)	Alternative Splicing/genetics ; Animals ; Cell Line ; Dogs ; Influenza A Virus, H5N1 Subtype/genetics ; Madin Darby Canine Kidney Cells ; Nucleic Acid Conformation ; Open Reading Frames/genetics ; Protein Binding/genetics ; RNA, Messenger/genetics ; RNA, Viral/genetics ; Viral Proteins/genetics ; Virus Replication/genetics
Chemical Substances	RNA, Messenger ; RNA, Viral ; Viral Proteins
Language	English
Publishing date	2015-10-21
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.
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0141132
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Secondary structure of the segment 5 genomic RNA of influenza A virus and its application for designing antisense oligonucleotides

Paula Michalak / Marta Soszynska-Jozwiak / Ewa Biala / Walter N. Moss / Julita Kesy / Barbara Szutkowska / Elzbieta Lenartowicz / Ryszard Kierzek / Elzbieta Kierzek

Scientific Reports, Vol 9, Iss 1, Pp 1-

2019 Volume 16

Abstract: Abstract Influenza virus causes seasonal epidemics and dangerous pandemic outbreaks. It is a single stranded (−)RNA virus with a segmented genome. Eight segments of genomic viral RNA (vRNA) form the virion, which are then transcribed and replicated in ... ...

Abstract	Abstract Influenza virus causes seasonal epidemics and dangerous pandemic outbreaks. It is a single stranded (−)RNA virus with a segmented genome. Eight segments of genomic viral RNA (vRNA) form the virion, which are then transcribed and replicated in host cells. The secondary structure of vRNA is an important regulator of virus biology and can be a target for finding new therapeutics. In this paper, the secondary structure of segment 5 vRNA is determined based on chemical mapping data, free energy minimization and structure-sequence conservation analysis for type A influenza. The revealed secondary structure has circular folding with a previously reported panhandle motif and distinct novel domains. Conservations of base pairs is 87% on average with many structural motifs that are highly conserved. Isoenergetic microarray mapping was used to additionally validate secondary structure and to discover regions that easy bind short oligonucleotides. Antisense oligonucleotides, which were designed based on modeled secondary structure and microarray mapping, inhibit influenza A virus proliferation in MDCK cells. The most potent oligonucleotides lowered virus titer by ~90%. These results define universal for type A structured regions that could be important for virus function, as well as new targets for antisense therapeutics.
Keywords	Medicine ; R ; Science ; Q
Subject code	500
Language	English
Publishing date	2019-03-01T00:00:00Z
Publisher	Nature Publishing Group
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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