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Article ; Online: Flavivirus-host interactions: an expanding network of proviral and antiviral factors.

Schneider, William M / Hoffmann, Hans-Heinrich

2021 Volume 52, Page(s) 71–77

Abstract: Flaviviruses are zoonotic pathogens transmitted by the bite of infected mosquitos and ticks and represent a constant burden to human health. Here we review recent literature aimed at uncovering how flaviviruses interact with the cells that they infect. A ...

Abstract	Flaviviruses are zoonotic pathogens transmitted by the bite of infected mosquitos and ticks and represent a constant burden to human health. Here we review recent literature aimed at uncovering how flaviviruses interact with the cells that they infect. A better understanding of these interactions may ultimately lead to novel therapeutic targets. We highlight several studies that employed low-biased methods to discover new protein-protein, protein-RNA, and genetic interactions, and spotlight recent work characterizing the host protein, TMEM41B, which has been shown to be critical for infection by diverse flaviviruses and coronaviruses.
MeSH term(s)	Animals ; Antiviral Agents/metabolism ; Antiviral Agents/pharmacology ; Antiviral Agents/therapeutic use ; Flavivirus/genetics ; Flavivirus/metabolism ; Flavivirus Infections ; Host-Pathogen Interactions/genetics ; Humans ; Proviruses ; Virus Replication
Chemical Substances	Antiviral Agents
Language	English
Publishing date	2021-12-09
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.2021.11.007
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Article ; Online: DDX60 selectively reduces translation off viral type II internal ribosome entry sites.

Sadic, Mohammad / Schneider, William M / Katsara, Olga / Medina, Gisselle N / Fisher, Ashley / Mogulothu, Aishwarya / Yu, Yingpu / Gu, Meigang / de Los Santos, Teresa / Schneider, Robert J / Dittmann, Meike

EMBO reports

2022 Volume 23, Issue 12, Page(s) e55218

Abstract: Co-opting host cell protein synthesis is a hallmark of many virus infections. In response, certain host defense proteins limit mRNA translation globally, albeit at the cost of the host cell's own protein synthesis. Here, we describe an interferon- ... ...

Abstract	Co-opting host cell protein synthesis is a hallmark of many virus infections. In response, certain host defense proteins limit mRNA translation globally, albeit at the cost of the host cell's own protein synthesis. Here, we describe an interferon-stimulated helicase, DDX60, that decreases translation from viral internal ribosome entry sites (IRESs). DDX60 acts selectively on type II IRESs of encephalomyocarditis virus (EMCV) and foot and mouth disease virus (FMDV), but not by other IRES types or by 5' cap. Correspondingly, DDX60 reduces EMCV and FMDV (type II IRES) replication, but not that of poliovirus or bovine enterovirus 1 (BEV-1; type I IRES). Furthermore, replacing the IRES of poliovirus with a type II IRES is sufficient for DDX60 to inhibit viral replication. Finally, DDX60 selectively modulates the amount of translating ribosomes on viral and in vitro transcribed type II IRES mRNAs, but not 5' capped mRNA. Our study identifies a novel facet in the repertoire of interferon-stimulated effector genes, the selective downregulation of translation from viral type II IRES elements.
MeSH term(s)	Internal Ribosome Entry Sites ; Interferons
Chemical Substances	Internal Ribosome Entry Sites ; Interferons (9008-11-1)
Language	English
Publishing date	2022-10-18
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2020896-0
ISSN	1469-3178 ; 1469-221X
ISSN (online)	1469-3178
ISSN	1469-221X
DOI	10.15252/embr.202255218
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Article ; Online: Interferons and viruses: an evolutionary arms race of molecular interactions.

Hoffmann, Hans-Heinrich / Schneider, William M / Rice, Charles M

Trends in immunology

2015 Volume 36, Issue 3, Page(s) 124–138

Abstract: Over half a century has passed since interferons (IFNs) were discovered and shown to inhibit virus infection in cultured cells. Since then, researchers have steadily brought to light the molecular details of IFN signaling, catalogued their pleiotropic ... ...

Abstract	Over half a century has passed since interferons (IFNs) were discovered and shown to inhibit virus infection in cultured cells. Since then, researchers have steadily brought to light the molecular details of IFN signaling, catalogued their pleiotropic effects on cells, and harnessed their therapeutic potential for a variety of maladies. While advances have been plentiful, several fundamental questions have yet to be answered and much complexity remains to be unraveled. We explore the current knowledge surrounding four main questions: are type I IFN subtypes differentially produced in response to distinct pathogens? How are IFN subtypes distinguished by cells? What are the mechanisms and consequences of viral antagonism? Lastly, how can the IFN response be harnessed to improve vaccine efficacy?
MeSH term(s)	Adaptive Immunity ; Biological Evolution ; Cell Lineage/immunology ; Gene Expression Regulation/immunology ; Humans ; Immune Evasion ; Immunity, Innate ; Interferon Type I/classification ; Interferon Type I/genetics ; Interferon Type I/immunology ; Interleukins/classification ; Interleukins/genetics ; Interleukins/immunology ; Lymphocytes/immunology ; Lymphocytes/virology ; Phylogeny ; Receptors, Pattern Recognition/genetics ; Receptors, Pattern Recognition/immunology ; Signal Transduction ; Viruses/immunology ; Viruses/pathogenicity
Chemical Substances	Interferon Type I ; Interleukins ; Receptors, Pattern Recognition
Language	English
Publishing date	2015-03
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2036831-8
ISSN	1471-4981 ; 1471-4906
ISSN (online)	1471-4981
ISSN	1471-4906
DOI	10.1016/j.it.2015.01.004
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Article ; Online: Interferon-stimulated genes: a complex web of host defenses.

Schneider, William M / Chevillotte, Meike Dittmann / Rice, Charles M

Annual review of immunology

2014 Volume 32, Page(s) 513–545

Abstract: Interferon-stimulated gene (ISG) products take on a number of diverse roles. Collectively, they are highly effective at resisting and controlling pathogens. In this review, we begin by introducing interferon (IFN) and the JAK-STAT signaling pathway to ... ...

Abstract	Interferon-stimulated gene (ISG) products take on a number of diverse roles. Collectively, they are highly effective at resisting and controlling pathogens. In this review, we begin by introducing interferon (IFN) and the JAK-STAT signaling pathway to highlight features that impact ISG production. Next, we describe ways in which ISGs both enhance innate pathogen-sensing capabilities and negatively regulate signaling through the JAK-STAT pathway. Several ISGs that directly inhibit virus infection are described with an emphasis on those that impact early and late stages of the virus life cycle. Finally, we describe ongoing efforts to identify and characterize antiviral ISGs, and we provide a forward-looking perspective on the ISG landscape.
MeSH term(s)	Animals ; Gene Expression Regulation ; Humans ; Immunity/physiology ; Interferons/metabolism ; Janus Kinases/metabolism ; Receptors, Interferon/metabolism ; STAT Transcription Factors/metabolism ; Signal Transduction
Chemical Substances	Receptors, Interferon ; STAT Transcription Factors ; Interferons (9008-11-1) ; Janus Kinases (EC 2.7.10.2)
Keywords	covid19
Language	English
Publishing date	2014-02-06
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	604953-9
ISSN	1545-3278 ; 0732-0582
ISSN (online)	1545-3278
ISSN	0732-0582
DOI	10.1146/annurev-immunol-032713-120231
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Article ; Online: An RNA-based system to study hepatitis B virus replication and evaluate antivirals.

Yu, Yingpu / Schneider, William M / Kass, Maximilian A / Michailidis, Eleftherios / Acevedo, Ashley / Pamplona Mosimann, Ana L / Bordignon, Juliano / Koenig, Alexander / Livingston, Christine M / van Gijzel, Hardeep / Ni, Yi / Ambrose, Pradeep M / Freije, Catherine A / Zhang, Mengyin / Zou, Chenhui / Kabbani, Mohammad / Quirk, Corrine / Jahan, Cyprien / Wu, Xianfang /

Urban, Stephan / You, Shihyun / Shlomai, Amir / de Jong, Ype P / Rice, Charles M

Science advances

2023 Volume 9, Issue 15, Page(s) eadg6265

Abstract: Hepatitis B virus (HBV) chronically infects an estimated 300 million people, and standard treatments are rarely curative. Infection increases the risk of liver cirrhosis and hepatocellular carcinoma, and consequently, nearly 1 million people die each ... ...

Abstract	Hepatitis B virus (HBV) chronically infects an estimated 300 million people, and standard treatments are rarely curative. Infection increases the risk of liver cirrhosis and hepatocellular carcinoma, and consequently, nearly 1 million people die each year from chronic hepatitis B. Tools and approaches that bring insights into HBV biology and facilitate the discovery and evaluation of antiviral drugs are in demand. Here, we describe a method to initiate the replication of HBV, a DNA virus, using synthetic RNA. This approach eliminates contaminating background signals from input virus or plasmid DNA that plagues existing systems and can be used to study multiple stages of HBV replication. We further demonstrate that this method can be uniquely applied to identify sequence variants that confer resistance to antiviral drugs.
MeSH term(s)	Humans ; Hepatitis B virus/genetics ; Antiviral Agents/pharmacology ; Antiviral Agents/therapeutic use ; RNA ; Hepatitis B, Chronic/drug therapy ; Liver Neoplasms/genetics ; Liver Neoplasms/drug therapy ; Virus Replication
Chemical Substances	Antiviral Agents ; RNA (63231-63-0)
Language	English
Publishing date	2023-04-12
Publishing country	United States
Document type	Journal Article
ZDB-ID	2810933-8
ISSN	2375-2548 ; 2375-2548
ISSN (online)	2375-2548
ISSN	2375-2548
DOI	10.1126/sciadv.adg6265
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Article ; Online: Decoupling expression and editing preferences of ADAR1 p150 and p110 isoforms.

Sun, Tony / Yu, Yingpu / Wu, Xianfang / Acevedo, Ashley / Luo, Ji-Dung / Wang, Jiayi / Schneider, William M / Hurwitz, Brian / Rosenberg, Brad R / Chung, Hachung / Rice, Charles M

Proceedings of the National Academy of Sciences of the United States of America

2021 Volume 118, Issue 12

Abstract: Human adenosine deaminase acting on RNA 1 (ADAR1) catalyzes adenosine-to-inosine deamination reactions on double-stranded RNA molecules to regulate cellular responses to endogenous and exogenous RNA. Defective ADAR1 editing leads to disorders such as ... ...

Abstract	Human adenosine deaminase acting on RNA 1 (ADAR1) catalyzes adenosine-to-inosine deamination reactions on double-stranded RNA molecules to regulate cellular responses to endogenous and exogenous RNA. Defective ADAR1 editing leads to disorders such as Aicardi-Goutières syndrome, an autoinflammatory disease that manifests in the brain and skin, and dyschromatosis symmetrica hereditaria, a skin pigmentation disorder. Two ADAR1 protein isoforms, p150 (150 kDa) and p110 (110 kDa), are expressed and can edit RNA, but the contribution of each isoform to the editing landscape remains unclear, largely because of the challenges in expressing p150 without p110. In this study, we demonstrate that p110 is coexpressed with p150 from the canonical p150-encoding mRNA due to leaky ribosome scanning downstream of the p150 start codon. The presence of a strong Kozak consensus context surrounding the p110 start codon suggests the p150 mRNA is optimized to leak p110 alongside expression of p150. To reduce leaky scanning and translation initiation at the p110 start codon, we introduced synonymous mutations in the coding region between the p150 and p110 start codons. Cells expressing p150 constructs with these mutations produced significantly reduced levels of p110. Editing analysis of total RNA from ADAR1 knockout cells reconstituted separately with modified p150 and p110 revealed that more than half of the A-to-I edit sites are selectively edited by p150, and the other half are edited by either p150 or p110. This method of isoform-selective editing analysis, making use of the modified p150, has the potential to be adapted for other cellular contexts.
MeSH term(s)	Adenosine Deaminase/genetics ; Autoimmune Diseases of the Nervous System/genetics ; Disease Susceptibility ; Gene Expression Regulation ; Gene Knockout Techniques ; Genetic Predisposition to Disease ; Humans ; Nervous System Malformations/genetics ; Pigmentation Disorders/congenital ; Pigmentation Disorders/genetics ; Protein Isoforms/genetics ; RNA Editing ; RNA-Binding Proteins/genetics
Chemical Substances	Protein Isoforms ; RNA-Binding Proteins ; ADAR protein, human (EC 3.5.4.37) ; Adenosine Deaminase (EC 3.5.4.4)
Language	English
Publishing date	2021-03-15
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2021757118
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Article ; Online: Diverse Viruses Require the Calcium Transporter SPCA1 for Maturation and Spread.

Hoffmann, H-Heinrich / Schneider, William M / Blomen, Vincent A / Scull, Margaret A / Hovnanian, Alain / Brummelkamp, Thijn R / Rice, Charles M

Cell host & microbe

2017 Volume 22, Issue 4, Page(s) 460–470.e5

Abstract: Respiratory and arthropod-borne viral infections are a global threat due to the lack of effective antivirals and vaccines. A potential strategy is to target host proteins required for viruses but non-essential for the host. To identify such proteins, we ... ...

Abstract	Respiratory and arthropod-borne viral infections are a global threat due to the lack of effective antivirals and vaccines. A potential strategy is to target host proteins required for viruses but non-essential for the host. To identify such proteins, we performed a genome-wide knockout screen in human haploid cells and identified the calcium pump SPCA1. SPCA1 is required by viruses from the Paramyxoviridae, Flaviviridae, and Togaviridae families, including measles, dengue, West Nile, Zika, and chikungunya viruses. Calcium transport activity is required for SPCA1 to promote virus spread. SPCA1 regulates proteases within the trans-Golgi network that require calcium for their activity and are critical for virus glycoprotein maturation. Consistent with these findings, viral glycoproteins fail to mature in SPCA1-deficient cells preventing viral spread, which is evident even in cells with partial loss of SPCA1. Thus, SPCA1 is an attractive antiviral host target for a broad spectrum of established and emerging viral infections.
MeSH term(s)	A549 Cells ; Animals ; Calcium/metabolism ; Calcium-Transporting ATPases/genetics ; Calcium-Transporting ATPases/metabolism ; Chlorocebus aethiops ; Female ; Flaviviridae/physiology ; Gene Knockout Techniques ; Genome-Wide Association Study ; Haploidy ; HeLa Cells ; Host-Pathogen Interactions ; Humans ; Male ; Paramyxoviridae/physiology ; Togaviridae/physiology ; Vero Cells ; Viral Proteins/genetics ; Viral Proteins/metabolism ; trans-Golgi Network/enzymology
Chemical Substances	Viral Proteins ; ATP2C1 protein, human (EC 7.2.2.10) ; Calcium-Transporting ATPases (EC 7.2.2.10) ; Calcium (SY7Q814VUP)
Keywords	covid19
Language	English
Publishing date	2017-10-12
Publishing country	United States
Document type	Journal Article
ZDB-ID	2278004-X
ISSN	1934-6069 ; 1931-3128
ISSN (online)	1934-6069
ISSN	1931-3128
DOI	10.1016/j.chom.2017.09.002
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Article ; Online: Characterization of Novel Splice Variants of Zinc Finger Antiviral Protein (ZAP).

Li, Melody M H / Aguilar, Eduardo G / Michailidis, Eleftherios / Pabon, Jonathan / Park, Paul / Wu, Xianfang / de Jong, Ype P / Schneider, William M / Molina, Henrik / Rice, Charles M / MacDonald, Margaret R

Journal of virology

2019 Volume 93, Issue 18

Abstract: Given the unprecedented scale of the recent Ebola and Zika viral epidemics, it is crucial to understand the biology of host factors with broad antiviral action in order to develop novel therapeutic approaches. Here, we look into one such factor: zinc ... ...

Abstract	Given the unprecedented scale of the recent Ebola and Zika viral epidemics, it is crucial to understand the biology of host factors with broad antiviral action in order to develop novel therapeutic approaches. Here, we look into one such factor: zinc finger antiviral protein (ZAP) inhibits a variety of RNA and DNA viruses. Alternative splicing results in two isoforms that differ at their C termini: ZAPL (long) encodes a poly(ADP-ribose) polymerase (PARP)-like domain that is missing in ZAPS (short). Previously, it has been shown that ZAPL is more antiviral than ZAPS, while the latter is more induced by interferon (IFN). In this study, we discovered and confirmed the expression of two additional splice variants of human ZAP: ZAPXL (extralong) and ZAPM (medium). We also found two haplotypes of human ZAP. Since ZAPL and ZAPS have differential activities, we hypothesize that all four ZAP isoforms have evolved to mediate distinct antiviral and/or cellular functions. By taking a gene-knockout-and-reconstitution approach, we have characterized the antiviral, translational inhibition, and IFN activation activities of individual ZAP isoforms. Our work demonstrates that ZAPL and ZAPXL are more active against alphaviruses and hepatitis B virus (HBV) than ZAPS and ZAPM and elucidates the effects of splice variants on the action of a broad-spectrum antiviral factor.
MeSH term(s)	A549 Cells ; Alphavirus/genetics ; Alternative Splicing ; Cell Line ; HEK293 Cells ; Haplotypes ; HeLa Cells ; Hepatitis B virus/genetics ; Humans ; Protein Isoforms ; RNA Splicing/genetics ; RNA, Viral/genetics ; RNA-Binding Proteins/genetics ; RNA-Binding Proteins/metabolism ; Virus Replication/drug effects ; Zinc Fingers
Chemical Substances	Protein Isoforms ; RNA, Viral ; RNA-Binding Proteins ; ZC3HAV1 protein, human
Language	English
Publishing date	2019-08-28
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/JVI.00715-19
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Article ; Online: A protein-interaction network of interferon-stimulated genes extends the innate immune system landscape.

Hubel, Philipp / Urban, Christian / Bergant, Valter / Schneider, William M / Knauer, Barbara / Stukalov, Alexey / Scaturro, Pietro / Mann, Angelika / Brunotte, Linda / Hoffmann, Heinrich H / Schoggins, John W / Schwemmle, Martin / Mann, Matthias / Rice, Charles M / Pichlmair, Andreas

Nature immunology

2019 Volume 20, Issue 4, Page(s) 493–502

Abstract: Interferon-stimulated genes (ISGs) form the backbone of the innate immune system and are important for limiting intra- and intercellular viral replication and spread. We conducted a mass-spectrometry-based survey to understand the fundamental ... ...

Abstract	Interferon-stimulated genes (ISGs) form the backbone of the innate immune system and are important for limiting intra- and intercellular viral replication and spread. We conducted a mass-spectrometry-based survey to understand the fundamental organization of the innate immune system and to explore the molecular functions of individual ISGs. We identified interactions between 104 ISGs and 1,401 cellular binding partners engaging in 2,734 high-confidence interactions. 90% of these interactions are unreported so far, and our survey therefore illuminates a far wider activity spectrum of ISGs than is currently known. Integration of the resulting ISG-interaction network with published datasets and functional studies allowed us to identify regulators of immunity and processes related to the immune system. Given the extraordinary robustness of the innate immune system, this ISG network may serve as a blueprint for therapeutic targeting of cellular systems to efficiently fight viral infections.
MeSH term(s)	Antigens, Neoplasm/metabolism ; Biomarkers, Tumor/metabolism ; Carrier Proteins/metabolism ; Cell Line ; Gene Expression ; Glycoproteins/metabolism ; HEK293 Cells ; HeLa Cells ; Humans ; Immunity, Innate/genetics ; Interferons/physiology ; Mass Spectrometry ; Protein Interaction Mapping ; Receptors, CCR4/metabolism ; Receptors, Peptide/metabolism ; Ribonucleoproteins/metabolism ; Viral Proteins/metabolism
Chemical Substances	Antigens, Neoplasm ; Biomarkers, Tumor ; CCR4 protein, human ; Carrier Proteins ; Glycoproteins ; LGALS3BP protein, human ; Receptors, CCR4 ; Receptors, Peptide ; Ribonucleoproteins ; Viral Proteins ; annexin II receptor, human ; Interferons (9008-11-1)
Language	English
Publishing date	2019-03-04
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2016987-5
ISSN	1529-2916 ; 1529-2908
ISSN (online)	1529-2916
ISSN	1529-2908
DOI	10.1038/s41590-019-0323-3
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Article: A CRISPR Activation Screen Identifies an Atypical Rho GTPase That Enhances Zika Viral Entry

Viruses. 2021 Oct. 20, v. 13, no. 11

2021

Abstract: Zika virus (ZIKV) is a re-emerging flavivirus that has caused large-scale epidemics. Infection during pregnancy can lead to neurologic developmental abnormalities in children. There is no approved vaccine or therapy for ZIKV. To uncover cellular pathways ...

Abstract	Zika virus (ZIKV) is a re-emerging flavivirus that has caused large-scale epidemics. Infection during pregnancy can lead to neurologic developmental abnormalities in children. There is no approved vaccine or therapy for ZIKV. To uncover cellular pathways required for ZIKV that can be therapeutically targeted, we transcriptionally upregulated all known human coding genes with an engineered CRISPR–Cas9 activation complex in human fibroblasts deficient in interferon (IFN) signaling. We identified Ras homolog family member V (RhoV) and WW domain-containing transcription regulator 1 (WWTR1) as proviral factors, and found them to play important roles during early ZIKV infection in A549 cells. We then focused on RhoV, a Rho GTPase with atypical terminal sequences and membrane association, and validated its proviral effects on ZIKV infection and virion production in SNB-19 cells. We found that RhoV promotes infection of some flaviviruses and acts at the step of viral entry. Furthermore, RhoV proviral effects depend on the complete GTPase cycle. By depleting Rho GTPases and related proteins, we identified RhoB and Pak1 as additional proviral factors. Taken together, these results highlight the positive role of RhoV in ZIKV infection and confirm CRISPR activation as a relevant method to identify novel host–pathogen interactions.
Keywords	CRISPR-Cas systems ; Zika virus ; fibroblasts ; guanosinetriphosphatase ; humans ; interferons ; pregnancy ; therapeutics ; transcription (genetics) ; transcription factors ; vaccines ; virion
Language	English
Dates of publication	2021-1020
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2516098-9
ISSN	1999-4915
ISSN	1999-4915
DOI	10.3390/v13112113
Database	NAL-Catalogue (AGRICOLA)

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