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Article: Standing your ground to exoribonucleases: Function of Flavivirus long non-coding RNAs

Charley, Phillida A / Jeffrey Wilusz

Virus research. 2016 Jan. 02, v. 212

2016

Abstract: Members of the Flaviviridae (e.g., Dengue virus, West Nile virus, and Hepatitis C virus) contain a positive-sense RNA genome that encodes a large polyprotein. It is now also clear most if not all of these viruses also produce an abundant subgenomic long ... ...

Abstract	Members of the Flaviviridae (e.g., Dengue virus, West Nile virus, and Hepatitis C virus) contain a positive-sense RNA genome that encodes a large polyprotein. It is now also clear most if not all of these viruses also produce an abundant subgenomic long non-coding RNA. These non-coding RNAs, which are called subgenomic flavivirus RNAs (sfRNAs) or Xrn1-resistant RNAs (xrRNAs), are stable decay intermediates generated from the viral genomic RNA through the stalling of the cellular exoribonuclease Xrn1 at highly structured regions. Several functions of these flavivirus long non-coding RNAs have been revealed in recent years. The generation of these sfRNAs/xrRNAs from viral transcripts results in the repression of Xrn1 and the dysregulation of cellular mRNA stability. The abundant sfRNAs also serve directly as a decoy for important cellular protein regulators of the interferon and RNA interference antiviral pathways. Thus the generation of long non-coding RNAs from flaviviruses, hepaciviruses and pestiviruses likely disrupts aspects of innate immunity and may directly contribute to viral replication, cytopathology and pathogenesis.
Keywords	Dengue virus ; Hepatitis C virus ; Pestivirus ; RNA interference ; West Nile virus ; exoribonucleases ; genome ; innate immunity ; interferons ; messenger RNA ; non-coding RNA ; pathogenesis ; polyproteins ; virus replication ; viruses ; covid19
Language	English
Dates of publication	2016-0102
Size	p. 70-77.
Publishing place	Elsevier B.V.
Document type	Article
ZDB-ID	605780-9
ISSN	1872-7492 ; 0168-1702
ISSN (online)	1872-7492
ISSN	0168-1702
DOI	10.1016/j.virusres.2015.09.009
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Standing your ground to exoribonucleases: Function of Flavivirus long non-coding RNAs.

Charley, Phillida A / Wilusz, Jeffrey

Virus research

2015 Volume 212, Page(s) 70–77

Abstract	Members of the Flaviviridae (e.g., Dengue virus, West Nile virus, and Hepatitis C virus) contain a positive-sense RNA genome that encodes a large polyprotein. It is now also clear most if not all of these viruses also produce an abundant subgenomic long non-coding RNA. These non-coding RNAs, which are called subgenomic flavivirus RNAs (sfRNAs) or Xrn1-resistant RNAs (xrRNAs), are stable decay intermediates generated from the viral genomic RNA through the stalling of the cellular exoribonuclease Xrn1 at highly structured regions. Several functions of these flavivirus long non-coding RNAs have been revealed in recent years. The generation of these sfRNAs/xrRNAs from viral transcripts results in the repression of Xrn1 and the dysregulation of cellular mRNA stability. The abundant sfRNAs also serve directly as a decoy for important cellular protein regulators of the interferon and RNA interference antiviral pathways. Thus the generation of long non-coding RNAs from flaviviruses, hepaciviruses and pestiviruses likely disrupts aspects of innate immunity and may directly contribute to viral replication, cytopathology and pathogenesis.
MeSH term(s)	Animals ; Exoribonucleases/genetics ; Exoribonucleases/metabolism ; Flavivirus/genetics ; Flavivirus/metabolism ; Flavivirus Infections/enzymology ; Flavivirus Infections/genetics ; Flavivirus Infections/virology ; Humans ; RNA, Long Noncoding/genetics ; RNA, Long Noncoding/metabolism ; RNA, Viral/genetics ; RNA, Viral/metabolism
Chemical Substances	RNA, Long Noncoding ; RNA, Viral ; Exoribonucleases (EC 3.1.-)
Keywords	covid19
Language	English
Publishing date	2015-09-11
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, U.S. Gov't, Non-P.H.S. ; Review
ZDB-ID	605780-9
ISSN	1872-7492 ; 0168-1702
ISSN (online)	1872-7492
ISSN	0168-1702
DOI	10.1016/j.virusres.2015.09.009
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Article ; Online: Sponging of cellular proteins by viral RNAs.

Charley, Phillida A / Wilusz, Jeffrey

Current opinion in virology

2014 Volume 9, Page(s) 14–18

Abstract: Viral RNAs accumulate to high levels during infection and interact with a variety of cellular factors including miRNAs and RNA-binding proteins. Although many of these interactions exist to directly modulate replication, translation and decay of viral ... ...

Abstract	Viral RNAs accumulate to high levels during infection and interact with a variety of cellular factors including miRNAs and RNA-binding proteins. Although many of these interactions exist to directly modulate replication, translation and decay of viral transcripts, evidence is emerging that abundant viral RNAs may in certain cases serve as a sponge to sequester host non-coding RNAs and proteins. By effectively reducing the ability of cellular RNA binding proteins to regulate host cell gene expression, viral RNAs can alter the response to infection and favor viral replication. This review focuses on the potential contribution that sequestration of cellular proteins by viral RNAs makes to viral replication and cytopathology.
MeSH term(s)	Host-Pathogen Interactions ; Protein Binding ; Proteins/metabolism ; RNA Viruses/physiology ; RNA, Untranslated/metabolism ; RNA, Viral/metabolism ; Virus Replication
Chemical Substances	Proteins ; RNA, Untranslated ; RNA, Viral
Language	English
Publishing date	2014-09-17
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	2611378-8
ISSN	1879-6265 ; 1879-6257
ISSN (online)	1879-6265
ISSN	1879-6257
DOI	10.1016/j.coviro.2014.09.001
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Identification of phlebovirus and arenavirus RNA sequences that stall and repress the exoribonuclease XRN1.

Charley, Phillida A / Wilusz, Carol J / Wilusz, Jeffrey

The Journal of biological chemistry

2017 Volume 293, Issue 1, Page(s) 285–295

Abstract: Regulated mRNA decay plays a vital role in determining both the level and quality of cellular gene expression. Viral RNAs must successfully evade this host RNA decay machinery to establish a productive infection. One way for RNA viruses to accomplish ... ...

Abstract	Regulated mRNA decay plays a vital role in determining both the level and quality of cellular gene expression. Viral RNAs must successfully evade this host RNA decay machinery to establish a productive infection. One way for RNA viruses to accomplish this is to target the cellular exoribonuclease XRN1, because this enzyme is accessible in the cytoplasm and plays a major role in mRNA decay. Members of the Flaviviridae use RNA structures in their 5'- or 3'-untranslated regions to stall and repress XRN1, effectively stabilizing viral RNAs while also causing significant dysregulation of host cell mRNA stability. Here, we use a series of biochemical assays to demonstrate that the 3'-terminal portion of the nucleocapsid (N) mRNA of Rift Valley fever virus, a phlebovirus of the Bunyaviridae family, also can effectively stall and repress XRN1. The region responsible for impeding XRN1 includes a G-rich portion that likely forms a G-quadruplex structure. The 3'-terminal portions of ambisense-derived transcripts of multiple arenaviruses also stalled XRN1. Therefore, we conclude that RNAs from two additional families of mammalian RNA viruses stall and repress XRN1. This observation. emphasizes the importance and commonality of this viral strategy to interfere with the 5'-to-3'-exoribonuclease component of the cytoplasmic RNA decay machinery.
MeSH term(s)	3' Untranslated Regions ; Exoribonucleases/antagonists & inhibitors ; Exoribonucleases/metabolism ; HEK293 Cells ; HeLa Cells ; Host-Pathogen Interactions ; Humans ; Microtubule-Associated Proteins/antagonists & inhibitors ; Microtubule-Associated Proteins/metabolism ; Phlebovirus/genetics ; RNA Stability ; RNA, Messenger/genetics ; RNA, Messenger/metabolism ; RNA, Viral/genetics ; RNA, Viral/metabolism ; Rift Valley fever virus/genetics ; Sequence Analysis, RNA
Chemical Substances	3' Untranslated Regions ; Microtubule-Associated Proteins ; RNA, Messenger ; RNA, Viral ; Exoribonucleases (EC 3.1.-) ; XRN1 protein, human (EC 3.1.13.1)
Keywords	covid19
Language	English
Publishing date	2017-11-08
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	10.1074/jbc.M117.805796
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Article: Engineered viral RNA decay intermediates to assess XRN1-mediated decay

Russo, Joseph / Mundell, Cary T / Charley, Phillida A / Wilusz, Carol / Wilusz, Jeffrey

Methods. 2019 Feb. 15, v. 155

2019

Abstract: Both RNA synthesis and decay must be balanced within a cell to achieve proper gene expression. Additionally, modulation of RNA decay specifically offers the cell an opportunity to rapidly reshape the transcriptome in response to specific stimuli or cues. ...

Abstract	Both RNA synthesis and decay must be balanced within a cell to achieve proper gene expression. Additionally, modulation of RNA decay specifically offers the cell an opportunity to rapidly reshape the transcriptome in response to specific stimuli or cues. Therefore, it is critical to understand the underlying mechanisms through which RNA decay contribute to gene expression homeostasis. Cell-free reconstitution approaches have been used successfully to reveal mechanisms associated with numerous post-transcriptional RNA processes. Historically, it has been difficult to examine all aspects of RNA decay in such an in vitro setting due, in part, to limitations on the ability to resolve larger RNAs through denaturing polyacrylamide gels. Thus, in vitro systems to study RNA decay rely on smaller, less biologically relevant RNA fragments. Herein, we present an approach to more confidently examine RNA decay parameters of large mRNA size transcripts through the inclusion of an engineered XRN1-resistant reporter RNA (xrRNA). By placing a 67 nucleotide xrRNA near the 3′ end of any in vitro transcribed RNA with variable size or sequence context, investigators can observe the accumulation of the xrRNA as a readout of exoribonuclease-mediated 5′-3′ decay. This approach may allow in vitro RNA decay assays to include full biologically relevant mRNA/mRNPs, extending their utility and allow improved experimental design considerations to promote biologically relevant outcomes.
Keywords	experimental design ; gels ; gene expression ; homeostasis ; messenger RNA ; polyacrylamide ; transcription (genetics) ; transcriptome
Language	English
Dates of publication	2019-0215
Size	p. 116-123.
Publishing place	Elsevier Inc.
Document type	Article
ZDB-ID	1066584-5
ISSN	1095-9130 ; 1046-2023
ISSN (online)	1095-9130
ISSN	1046-2023
DOI	10.1016/j.ymeth.2018.11.019
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Article ; Online: Regulatory T cell-like response to SARS-CoV-2 in Jamaican fruit bats (Artibeus jamaicensis) transduced with human ACE2.

Burke, Bradly / Rocha, Savannah M / Zhan, Shijun / Eckley, Miles / Reasoner, Clara / Addetia, Amin / Lewis, Juliette / Fagre, Anna / Charley, Phillida A / Richt, Juergen A / Weiss, Susan R / Tjalkens, Ronald B / Veesler, David / Aboellail, Tawfik / Schountz, Tony

PLoS pathogens

2023 Volume 19, Issue 10, Page(s) e1011728

Abstract: Insectivorous Old World horseshoe bats (Rhinolophus spp.) are the likely source of the ancestral SARS-CoV-2 prior to its spillover into humans and causing the COVID-19 pandemic. Natural coronavirus infections of bats appear to be principally confined to ... ...

Abstract	Insectivorous Old World horseshoe bats (Rhinolophus spp.) are the likely source of the ancestral SARS-CoV-2 prior to its spillover into humans and causing the COVID-19 pandemic. Natural coronavirus infections of bats appear to be principally confined to the intestines, suggesting fecal-oral transmission; however, little is known about the biology of SARS-related coronaviruses in bats. Previous experimental challenges of Egyptian fruit bats (Rousettus aegyptiacus) resulted in limited infection restricted to the respiratory tract, whereas insectivorous North American big brown bats (Eptesicus fuscus) showed no evidence of infection. In the present study, we challenged Jamaican fruit bats (Artibeus jamaicensis) with SARS-CoV-2 to determine their susceptibility. Infection was confined to the intestine for only a few days with prominent viral nucleocapsid antigen in epithelial cells, and mononuclear cells of the lamina propria and Peyer's patches, but with no evidence of infection of other tissues; none of the bats showed visible signs of disease or seroconverted. Expression levels of ACE2 were low in the lungs, which may account for the lack of pulmonary infection. Bats were then intranasally inoculated with a replication-defective adenovirus encoding human ACE2 and 5 days later challenged with SARS-CoV-2. Viral antigen was prominent in lungs for up to 14 days, with loss of pulmonary cellularity during this time; however, the bats did not exhibit weight loss or visible signs of disease. From day 7, bats had low to moderate IgG antibody titers to spike protein by ELISA, and one bat on day 10 had low-titer neutralizing antibodies. CD4+ helper T cells became activated upon ex vivo recall stimulation with SARS-CoV-2 nucleocapsid peptide library and exhibited elevated mRNA expression of the regulatory T cell cytokines interleukin-10 and transforming growth factor-β, which may have limited inflammatory pathology. Collectively, these data show that Jamaican fruit bats are poorly susceptible to SARS-CoV-2 but that expression of human ACE2 in their lungs leads to robust infection and an adaptive immune response with low-titer antibodies and a regulatory T cell-like response that may explain the lack of prominent inflammation in the lungs. This model will allow for insight of how SARS-CoV-2 infects bats and how bat innate and adaptive immune responses engage the virus without overt clinical disease.
MeSH term(s)	Animals ; Humans ; Chiroptera ; SARS-CoV-2 ; Angiotensin-Converting Enzyme 2 ; Pandemics ; Jamaica ; T-Lymphocytes, Regulatory ; COVID-19
Chemical Substances	Angiotensin-Converting Enzyme 2 (EC 3.4.17.23)
Language	English
Publishing date	2023-10-19
Publishing country	United States
Document type	Journal Article
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7374
ISSN (online)	1553-7374
ISSN	1553-7374
DOI	10.1371/journal.ppat.1011728
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Article ; Online: Engineered viral RNA decay intermediates to assess XRN1-mediated decay.

Russo, Joseph / Mundell, Cary T / Charley, Phillida A / Wilusz, Carol / Wilusz, Jeffrey

Methods (San Diego, Calif.)

2018 Volume 155, Page(s) 116–123

Abstract	Both RNA synthesis and decay must be balanced within a cell to achieve proper gene expression. Additionally, modulation of RNA decay specifically offers the cell an opportunity to rapidly reshape the transcriptome in response to specific stimuli or cues. Therefore, it is critical to understand the underlying mechanisms through which RNA decay contribute to gene expression homeostasis. Cell-free reconstitution approaches have been used successfully to reveal mechanisms associated with numerous post-transcriptional RNA processes. Historically, it has been difficult to examine all aspects of RNA decay in such an in vitro setting due, in part, to limitations on the ability to resolve larger RNAs through denaturing polyacrylamide gels. Thus, in vitro systems to study RNA decay rely on smaller, less biologically relevant RNA fragments. Herein, we present an approach to more confidently examine RNA decay parameters of large mRNA size transcripts through the inclusion of an engineered XRN1-resistant reporter RNA (xrRNA). By placing a 67 nucleotide xrRNA near the 3' end of any in vitro transcribed RNA with variable size or sequence context, investigators can observe the accumulation of the xrRNA as a readout of exoribonuclease-mediated 5'-3' decay. This approach may allow in vitro RNA decay assays to include full biologically relevant mRNA/mRNPs, extending their utility and allow improved experimental design considerations to promote biologically relevant outcomes.
MeSH term(s)	Cell-Free System ; Denaturing Gradient Gel Electrophoresis ; Dengue Virus/chemistry ; Dengue Virus/genetics ; Exoribonucleases/genetics ; Exoribonucleases/metabolism ; Genetic Engineering/methods ; Glyceraldehyde-3-Phosphate Dehydrogenase (Phosphorylating)/genetics ; Glyceraldehyde-3-Phosphate Dehydrogenase (Phosphorylating)/metabolism ; Humans ; Microtubule-Associated Proteins/genetics ; Microtubule-Associated Proteins/metabolism ; RNA Stability ; RNA, Messenger/genetics ; RNA, Messenger/metabolism ; RNA, Viral/genetics ; RNA, Viral/metabolism ; Transcription, Genetic
Chemical Substances	Microtubule-Associated Proteins ; RNA, Messenger ; RNA, Viral ; Glyceraldehyde-3-Phosphate Dehydrogenase (Phosphorylating) (EC 1.2.1.12) ; Exoribonucleases (EC 3.1.-) ; XRN1 protein, human (EC 3.1.13.1)
Language	English
Publishing date	2018-12-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1066584-5
ISSN	1095-9130 ; 1046-2023
ISSN (online)	1095-9130
ISSN	1046-2023
DOI	10.1016/j.ymeth.2018.11.019
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Article ; Online: Zika virus noncoding sfRNAs sequester multiple host-derived RNA-binding proteins and modulate mRNA decay and splicing during infection.

Michalski, Daniel / Ontiveros, J Gustavo / Russo, Joseph / Charley, Phillida A / Anderson, John R / Heck, Adam M / Geiss, Brian J / Wilusz, Jeffrey

The Journal of biological chemistry

2019 Volume 294, Issue 44, Page(s) 16282–16296

Abstract: Insect-borne flaviviruses produce a 300-500-base long noncoding RNA, termed subgenomic flavivirus RNA (sfRNA), by stalling the cellular 5'-3'-exoribonuclease 1 (XRN1) via structures located in their 3' UTRs. In this study, we demonstrate that sfRNA ... ...

Abstract	Insect-borne flaviviruses produce a 300-500-base long noncoding RNA, termed subgenomic flavivirus RNA (sfRNA), by stalling the cellular 5'-3'-exoribonuclease 1 (XRN1) via structures located in their 3' UTRs. In this study, we demonstrate that sfRNA production by Zika virus represses XRN1 analogous to what we have previously shown for other flaviviruses. Using protein-RNA reconstitution and a stringent RNA pulldown assay with human choriocarcinoma (JAR) cells, we demonstrate that the sfRNAs from both dengue type 2 and Zika viruses interact with a common set of 21 RNA-binding proteins that contribute to the regulation of post-transcriptional processes in the cell, including splicing, RNA stability, and translation. We found that four of these sfRNA-interacting host proteins, DEAD-box helicase 6 (DDX6) and enhancer of mRNA decapping 3 (EDC3) (two RNA decay factors), phosphorylated adaptor for RNA export (a regulator of the biogenesis of the splicing machinery), and apolipoprotein B mRNA-editing enzyme catalytic subunit 3C (APOBEC3C, a nucleic acid-editing deaminase), inherently restrict Zika virus infection. Furthermore, we demonstrate that the regulations of cellular mRNA decay and RNA splicing are compromised by Zika virus infection as well as by sfRNA alone. Collectively, these results reveal the large extent to which Zika virus-derived sfRNAs interact with cellular RNA-binding proteins and highlight the potential for widespread dysregulation of post-transcriptional control that likely limits the effective response of these cells to viral infection.
MeSH term(s)	3' Untranslated Regions ; Animals ; Chlorocebus aethiops ; DEAD-box RNA Helicases/metabolism ; Exoribonucleases/metabolism ; Flavivirus/genetics ; Genome, Viral/genetics ; HEK293 Cells ; Host-Pathogen Interactions ; Humans ; Microtubule-Associated Proteins/metabolism ; Nucleic Acid Conformation ; Proto-Oncogene Proteins/metabolism ; RNA Splicing/physiology ; RNA Stability/physiology ; RNA, Messenger/metabolism ; RNA, Untranslated/genetics ; RNA, Untranslated/metabolism ; RNA, Viral/metabolism ; RNA-Binding Proteins/metabolism ; Ribonucleoproteins, Small Nuclear/metabolism ; Vero Cells ; Zika Virus/genetics ; Zika Virus/metabolism ; Zika Virus Infection/virology
Chemical Substances	3' Untranslated Regions ; EDC3 protein, human ; Microtubule-Associated Proteins ; Proto-Oncogene Proteins ; RNA, Messenger ; RNA, Untranslated ; RNA, Viral ; RNA-Binding Proteins ; Ribonucleoproteins, Small Nuclear ; Exoribonucleases (EC 3.1.-) ; XRN1 protein, human (EC 3.1.13.1) ; DDX6 protein, human (EC 3.6.1.-) ; DEAD-box RNA Helicases (EC 3.6.4.13)
Language	English
Publishing date	2019-09-13
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2997-x
ISSN	1083-351X ; 0021-9258
ISSN (online)	1083-351X
ISSN	0021-9258
DOI	10.1074/jbc.RA119.009129
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Article ; Online: Beet Necrotic Yellow Vein Virus Noncoding RNA Production Depends on a 5'→3' Xrn Exoribonuclease Activity.

Flobinus, Alyssa / Chevigny, Nicolas / Charley, Phillida A / Seissler, Tanja / Klein, Elodie / Bleykasten-Grosshans, Claudine / Ratti, Claudio / Bouzoubaa, Salah / Wilusz, Jeffrey / Gilmer, David

Viruses

2018 Volume 10, Issue 3

Abstract: The RNA3 species of the beet necrotic yellow vein virus (BNYVV), a multipartite positive-stranded RNA phytovirus, contains the 'core' nucleotide sequence required for its systemic movement ... ...

Abstract	The RNA3 species of the beet necrotic yellow vein virus (BNYVV), a multipartite positive-stranded RNA phytovirus, contains the 'core' nucleotide sequence required for its systemic movement in
MeSH term(s)	Enzyme Activation ; Exoribonucleases/genetics ; Exoribonucleases/metabolism ; Gene Expression ; Gene Expression Regulation, Viral ; Gene Silencing ; Host-Pathogen Interactions ; Mutation ; Plant Diseases/virology ; Plant Viruses/genetics ; Plant Viruses/metabolism ; RNA, Untranslated/chemistry ; RNA, Untranslated/genetics ; Transfection ; Transformation, Genetic ; Virus Replication
Chemical Substances	RNA, Untranslated ; Exoribonucleases (EC 3.1.-) ; 5'-exoribonuclease (EC 3.1.13.-)
Language	English
Publishing date	2018-03-19
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/v10030137
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