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Article ; Online: Antiviral responses are shaped by heterogeneity in viral replication dynamics.

Bruurs, Lucas J M / Müller, Micha / Schipper, Jelle G / Rabouw, Huib H / Boersma, Sanne / van Kuppeveld, Frank J M / Tanenbaum, Marvin E

Nature microbiology

2023 Volume 8, Issue 11, Page(s) 2115–2129

Abstract: Antiviral signalling, which can be activated in host cells upon virus infection, restricts virus replication and communicates infection status to neighbouring cells. The antiviral response is heterogeneous, both quantitatively (efficiency of response ... ...

Abstract	Antiviral signalling, which can be activated in host cells upon virus infection, restricts virus replication and communicates infection status to neighbouring cells. The antiviral response is heterogeneous, both quantitatively (efficiency of response activation) and qualitatively (transcribed antiviral gene set). To investigate the basis of this heterogeneity, we combined Virus Infection Real-time IMaging (VIRIM), a live-cell single-molecule imaging method, with real-time readouts of the dsRNA sensing pathway to analyse the response of human cells to encephalomyocarditis virus (EMCV) infection. We find that cell-to-cell heterogeneity in viral replication rates early in infection affect the efficiency of antiviral response activation, with lower replication rates leading to more antiviral response activation. Furthermore, we show that qualitatively distinct antiviral responses can be linked to the strength of the antiviral signalling pathway. Our analyses identify variation in early viral replication rates as an important parameter contributing to heterogeneity in antiviral response activation.
MeSH term(s)	Humans ; Virus Replication ; Signal Transduction ; Encephalomyocarditis virus/physiology ; Antiviral Agents ; Virus Diseases
Chemical Substances	Antiviral Agents
Language	English
Publishing date	2023-10-09
Publishing country	England
Document type	Journal Article
ISSN	2058-5276
ISSN (online)	2058-5276
DOI	10.1038/s41564-023-01501-z
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: The encephalomyocarditis virus Leader promotes the release of virions inside extracellular vesicles via the induction of secretory autophagy.

van der Grein, Susanne G / Defourny, Kyra A Y / Rabouw, Huib H / Goerdayal, Soenita S / van Herwijnen, Martijn J C / Wubbolts, Richard W / Altelaar, Maarten / van Kuppeveld, Frank J M / Nolte-'t Hoen, Esther N M

Nature communications

2022 Volume 13, Issue 1, Page(s) 3625

Abstract: Naked viruses can escape host cells before the induction of lysis via release in extracellular vesicles (EVs). These nanosized EVs cloak the secreted virus particles in a host-derived membrane, which alters virus-host interactions that affect infection ... ...

Abstract	Naked viruses can escape host cells before the induction of lysis via release in extracellular vesicles (EVs). These nanosized EVs cloak the secreted virus particles in a host-derived membrane, which alters virus-host interactions that affect infection efficiency and antiviral immunity. Currently, little is known about the viral and host factors regulating this form of virus release. Here, we assessed the role of the encephalomyocarditis virus (EMCV) Leader protein, a 'viral security protein' that subverts the host antiviral response. EV release upon infection with wildtype virus or a Leader-deficient mutant was characterized at the single particle level using high-resolution flow cytometry. Inactivation of the Leader abolished EV induction during infection and strongly reduced EV-enclosed virus release. We demonstrate that the Leader promotes the release of virions within EVs by stimulating a secretory arm of autophagy. This newly discovered role of the EMCV Leader adds to the variety of mechanisms via which this protein affects virus-host interactions. Moreover, these data provide first evidence for a crucial role of a non-structural viral protein in the non-lytic release of picornaviruses via packaging in EVs.
MeSH term(s)	Antiviral Agents/metabolism ; Autophagy ; Encephalomyocarditis virus/metabolism ; Extracellular Vesicles/metabolism ; Viral Proteins/metabolism ; Virion/metabolism
Chemical Substances	Antiviral Agents ; Viral Proteins
Language	English
Publishing date	2022-06-24
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2553671-0
ISSN	2041-1723 ; 2041-1723
ISSN (online)	2041-1723
ISSN	2041-1723
DOI	10.1038/s41467-022-31181-y
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Article ; Online: The encephalomyocarditis virus Leader promotes the release of virions inside extracellular vesicles via the induction of secretory autophagy

Susanne G. van der Grein / Kyra A. Y. Defourny / Huib H. Rabouw / Soenita S. Goerdayal / Martijn J. C. van Herwijnen / Richard W. Wubbolts / Maarten Altelaar / Frank J. M. van Kuppeveld / Esther N. M. Nolte-‘t Hoen

Nature Communications, Vol 13, Iss 1, Pp 1-

2022 Volume 14

Abstract: Picornaviruses can escape infected cells via packaging in extracellular vesicles (EVs). Here, van der Grein et al. show that the non-structural Leader protein of encephalomyocarditis virus (EMCV) promotes the release of EV-enclosed virus particles and ... ...

Abstract	Picornaviruses can escape infected cells via packaging in extracellular vesicles (EVs). Here, van der Grein et al. show that the non-structural Leader protein of encephalomyocarditis virus (EMCV) promotes the release of EV-enclosed virus particles and provide evidence for a role of secretory autophagy in this process.
Keywords	Science ; Q
Language	English
Publishing date	2022-06-01T00:00:00Z
Publisher	Nature Portfolio
Document type	Article ; Online
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Article ; Online: ACBD3 Is an Essential Pan-enterovirus Host Factor That Mediates the Interaction between Viral 3A Protein and Cellular Protein PI4KB.

Lyoo, Heyrhyoung / van der Schaar, Hilde M / Dorobantu, Cristina M / Rabouw, Huib H / Strating, Jeroen R P M / van Kuppeveld, Frank J M

mBio

2019 Volume 10, Issue 1

Abstract: The enterovirus genus of the picornavirus family includes a large number of important human pathogens such as poliovirus, coxsackievirus, enterovirus A71, and rhinoviruses. Like all other positive-strand RNA viruses, genome replication of enteroviruses ... ...

Abstract	The enterovirus genus of the picornavirus family includes a large number of important human pathogens such as poliovirus, coxsackievirus, enterovirus A71, and rhinoviruses. Like all other positive-strand RNA viruses, genome replication of enteroviruses occurs on rearranged membranous structures called replication organelles (ROs). Phosphatidylinositol 4-kinase IIIβ (PI4KB) is required by all enteroviruses for RO formation. The enteroviral 3A protein recruits PI4KB to ROs, but the exact mechanism remains elusive. Here, we investigated the role of acyl-coenzyme A binding domain containing 3 (ACBD3) in PI4KB recruitment upon enterovirus replication using ACBD3 knockout (ACBD3
MeSH term(s)	Adaptor Proteins, Signal Transducing/genetics ; Adaptor Proteins, Signal Transducing/metabolism ; Cell Line ; Enterovirus A, Human/physiology ; Gene Knockout Techniques ; Genetic Complementation Test ; Host-Pathogen Interactions ; Humans ; Membrane Proteins/genetics ; Membrane Proteins/metabolism ; Phosphotransferases (Alcohol Group Acceptor)/metabolism ; Protein Binding ; Viral Proteins/metabolism ; Virus Replication
Chemical Substances	ACBD3 protein, human ; Adaptor Proteins, Signal Transducing ; Membrane Proteins ; Viral Proteins ; Phosphotransferases (Alcohol Group Acceptor) (EC 2.7.1.-) ; phosphatidylinositol 4-kinase IIIbeta, human (EC 2.7.1.67)
Keywords	covid19
Language	English
Publishing date	2019-02-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2557172-2
ISSN	2150-7511 ; 2161-2129
ISSN (online)	2150-7511
ISSN	2161-2129
DOI	10.1128/mBio.02742-18
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Article ; Online: Essential Role of Enterovirus 2A Protease in Counteracting Stress Granule Formation and the Induction of Type I Interferon.

Visser, Linda J / Langereis, Martijn A / Rabouw, Huib H / Wahedi, Maryam / Muntjewerff, Elke M / de Groot, Raoul J / van Kuppeveld, Frank J M

Journal of virology

2019 Volume 93, Issue 10

Abstract: Most viruses have acquired mechanisms to suppress antiviral alpha/beta interferon (IFN-α/β) and stress responses. Enteroviruses (EVs) actively counteract the induction of IFN-α/β gene transcription and stress granule (SG) formation, which are ... ...

Abstract	Most viruses have acquired mechanisms to suppress antiviral alpha/beta interferon (IFN-α/β) and stress responses. Enteroviruses (EVs) actively counteract the induction of IFN-α/β gene transcription and stress granule (SG) formation, which are increasingly implicated as a platform for antiviral signaling, but the underlying mechanisms remain poorly understood. Both viral proteases (2A
MeSH term(s)	Antigens, Viral/metabolism ; Antiviral Agents/pharmacology ; Cell Line ; Cysteine Endopeptidases/metabolism ; Cytoplasmic Granules/metabolism ; Cytoplasmic Granules/virology ; Encephalomyocarditis virus/genetics ; Enterovirus/metabolism ; Enterovirus A, Human/genetics ; Enterovirus A, Human/metabolism ; Enterovirus A, Human/pathogenicity ; Enterovirus B, Human/genetics ; Enterovirus Infections/virology ; HeLa Cells ; Host-Pathogen Interactions/drug effects ; Humans ; Immune Evasion/drug effects ; Interferon Type I/metabolism ; Interferon-beta/metabolism ; Peptide Hydrolases/metabolism ; Phosphorylation ; Proteolysis ; Signal Transduction/drug effects ; Stress, Physiological/physiology ; Viral Proteins/metabolism
Chemical Substances	Antigens, Viral ; Antiviral Agents ; Interferon Type I ; Viral Proteins ; Interferon-beta (77238-31-4) ; Peptide Hydrolases (EC 3.4.-) ; Cysteine Endopeptidases (EC 3.4.22.-)
Keywords	covid19
Language	English
Publishing date	2019-05-01
Publishing country	United States
Document type	Journal Article ; 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.00222-19
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Article ; Online: Small molecule ISRIB suppresses the integrated stress response within a defined window of activation.

Rabouw, Huib H / Langereis, Martijn A / Anand, Aditya A / Visser, Linda J / de Groot, Raoul J / Walter, Peter / van Kuppeveld, Frank J M

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

2019 Volume 116, Issue 6, Page(s) 2097–2102

Abstract: Activation of the integrated stress response (ISR) by a variety of stresses triggers phosphorylation of the α-subunit of translation initiation factor eIF2. P-eIF2α inhibits eIF2B, the guanine nucleotide exchange factor that recycles inactive eIF2•GDP to ...

Abstract	Activation of the integrated stress response (ISR) by a variety of stresses triggers phosphorylation of the α-subunit of translation initiation factor eIF2. P-eIF2α inhibits eIF2B, the guanine nucleotide exchange factor that recycles inactive eIF2•GDP to active eIF2•GTP. eIF2 phosphorylation thereby represses translation. Persistent activation of the ISR has been linked to the development of several neurological disorders, and modulation of the ISR promises new therapeutic strategies. Recently, a small-molecule ISR inhibitor (ISRIB) was identified that rescues translation in the presence of P-eIF2α by facilitating the assembly of more active eIF2B. ISRIB enhances cognitive memory processes and has therapeutic effects in brain-injured mice without displaying overt side effects. While using ISRIB to investigate the ISR in picornavirus-infected cells, we observed that ISRIB rescued translation early in infection when P-eIF2α levels were low, but not late in infection when P-eIF2α levels were high. By treating cells with varying concentrations of poly(I:C) or arsenite to induce the ISR, we provide additional proof that ISRIB is unable to inhibit the ISR when intracellular P-eIF2α concentrations exceed a critical threshold level. Together, our data demonstrate that the effects of pharmacological activation of eIF2B are tuned by P-eIF2α concentration. Thus, ISRIB can mitigate undesirable outcomes of low-level ISR activation that may manifest neurological disease but leaves the cytoprotective effects of acute ISR activation intact. The insensitivity of cells to ISRIB during acute ISR may explain why ISRIB does not cause overt toxic side effects in vivo.
MeSH term(s)	Acetamides/chemistry ; Acetamides/pharmacology ; Animals ; Arsenites/pharmacology ; Cell Line ; Cyclohexylamines/chemistry ; Cyclohexylamines/pharmacology ; Eukaryotic Initiation Factor-2/antagonists & inhibitors ; Eukaryotic Initiation Factor-2/metabolism ; Humans ; Phosphorylation ; Picornaviridae ; Picornaviridae Infections/metabolism ; Picornaviridae Infections/virology ; Poly I-C/pharmacology ; Stress, Physiological/drug effects
Chemical Substances	2-(4-chlorophenoxy)-N-(4-(2-(4-chlorophenoxy)acetamido)cyclohexyl)acetamide ; Acetamides ; Arsenites ; Cyclohexylamines ; Eukaryotic Initiation Factor-2 ; arsenite (N5509X556J) ; Poly I-C (O84C90HH2L)
Keywords	covid19
Language	English
Publishing date	2019-01-23
Publishing country	United States
Document type	Journal Article ; 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.1815767116
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Article ; Online: Translation and Replication Dynamics of Single RNA Viruses.

Boersma, Sanne / Rabouw, Huib H / Bruurs, Lucas J M / Pavlovič, Tonja / van Vliet, Arno L W / Beumer, Joep / Clevers, Hans / van Kuppeveld, Frank J M / Tanenbaum, Marvin E

Cell

2020 Volume 183, Issue 7, Page(s) 1930–1945.e23

Abstract: RNA viruses are among the most prevalent pathogens and are a major burden on society. Although RNA viruses have been studied extensively, little is known about the processes that occur during the first several hours of infection because of a lack of ... ...

Abstract	RNA viruses are among the most prevalent pathogens and are a major burden on society. Although RNA viruses have been studied extensively, little is known about the processes that occur during the first several hours of infection because of a lack of sensitive assays. Here we develop a single-molecule imaging assay, virus infection real-time imaging (VIRIM), to study translation and replication of individual RNA viruses in live cells. VIRIM uncovered a striking heterogeneity in replication dynamics between cells and revealed extensive coordination between translation and replication of single viral RNAs. Furthermore, using VIRIM, we identify the replication step of the incoming viral RNA as a major bottleneck of successful infection and identify host genes that are responsible for inhibition of early virus replication. Single-molecule imaging of virus infection is a powerful tool to study virus replication and virus-host interactions that may be broadly applicable to RNA viruses.
MeSH term(s)	Cell Line, Tumor ; Cell Survival ; HEK293 Cells ; Host-Pathogen Interactions ; Humans ; Interferons/metabolism ; Protein Biosynthesis ; RNA Transport ; RNA Viruses/physiology ; RNA, Viral/genetics ; Reproducibility of Results ; Single Molecule Imaging ; Time Factors ; Virus Replication/physiology
Chemical Substances	RNA, Viral ; Interferons (9008-11-1)
Keywords	covid19
Language	English
Publishing date	2020-11-13
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	187009-9
ISSN	1097-4172 ; 0092-8674
ISSN (online)	1097-4172
ISSN	0092-8674
DOI	10.1016/j.cell.2020.10.019
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Zs.A 1167: Show issues			Location: Je nach Verfügbarkeit (siehe Angabe bei Bestand) bis Jg. 1994: Bestellungen von Artikeln über das Online-Bestellformular Jg. 1995 - 2021: Lesesall (1.OG) ab Jg. 2022: Lesesaal (EG)
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Article ; Online: Foot-and-Mouth Disease Virus Leader Protease Cleaves G3BP1 and G3BP2 and Inhibits Stress Granule Formation.

Visser, Linda J / Medina, Gisselle N / Rabouw, Huib H / de Groot, Raoul J / Langereis, Martijn A / de Los Santos, Teresa / van Kuppeveld, Frank J M

Journal of virology

2019 Volume 93, Issue 2

Abstract: Like other viruses, the picornavirus foot-and-mouth disease virus (FMDV; ... ...

Abstract	Like other viruses, the picornavirus foot-and-mouth disease virus (FMDV; genus
MeSH term(s)	Animals ; Aphthovirus/enzymology ; Cell Line ; Cricetinae ; Cytoplasmic Granules/metabolism ; Encephalomyocarditis virus/enzymology ; Foot-and-Mouth Disease/metabolism ; Foot-and-Mouth Disease/virology ; Foot-and-Mouth Disease Virus/enzymology ; HEK293 Cells ; HeLa Cells ; Humans ; Peptide Hydrolases/metabolism ; RNA Recognition Motif Proteins/metabolism ; Stress, Physiological ; Viral Proteins/metabolism
Chemical Substances	RNA Recognition Motif Proteins ; Viral Proteins ; Peptide Hydrolases (EC 3.4.-)
Keywords	covid19
Language	English
Publishing date	2019-01-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/JVI.00922-18
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Article ; Online: Knockout of cGAS and STING Rescues Virus Infection of Plasmid DNA-Transfected Cells.

Langereis, Martijn A / Rabouw, Huib H / Holwerda, Melle / Visser, Linda J / van Kuppeveld, Frank J M

Journal of virology

2015 Volume 89, Issue 21, Page(s) 11169–11173

Abstract: It is well known that plasmid DNA transfection, prior to virus infection, negatively affects infection efficiency. Here, we show that cytosolic plasmid DNA activates the cGAS/STING signaling pathway, which ultimately leads to the induction of an ... ...

Abstract	It is well known that plasmid DNA transfection, prior to virus infection, negatively affects infection efficiency. Here, we show that cytosolic plasmid DNA activates the cGAS/STING signaling pathway, which ultimately leads to the induction of an antiviral state of the cells. Using a transient one-plasmid clustered regularly interspaced short palindromic repeat (CRISPR)/Cas9 system, we generated cGAS/STING-knockout cells and show that these cells can be infected after plasmid DNA transfection as efficiently as nontransfected cells.
MeSH term(s)	CRISPR-Cas Systems ; Coxsackievirus Infections/metabolism ; Cytosol/metabolism ; Flow Cytometry ; Gene Knockout Techniques ; Gene Transfer Techniques ; Green Fluorescent Proteins ; HeLa Cells ; Humans ; Luminescent Proteins ; Membrane Proteins/genetics ; Membrane Proteins/metabolism ; Mengovirus/metabolism ; Nucleotidyltransferases/genetics ; Nucleotidyltransferases/metabolism ; Plasmids/genetics ; Plasmids/metabolism ; Signal Transduction/genetics ; Signal Transduction/physiology ; Transfection/methods ; Red Fluorescent Protein
Chemical Substances	Luminescent Proteins ; Membrane Proteins ; STING1 protein, human ; enhanced green fluorescent protein ; Green Fluorescent Proteins (147336-22-9) ; Nucleotidyltransferases (EC 2.7.7.-) ; cGAS protein, human (EC 2.7.7.-)
Language	English
Publishing date	2015-08-26
Publishing country	United States
Document type	Journal Article ; 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.01781-15
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Article ; Online: Picornavirus infection induces temporal release of multiple extracellular vesicle subsets that differ in molecular composition and infectious potential.

van der Grein, Susanne G / Defourny, Kyra A Y / Rabouw, Huib H / Galiveti, Chenna R / Langereis, Martijn A / Wauben, Marca H M / Arkesteijn, Ger J A / van Kuppeveld, Frank J M / Nolte-'t Hoen, Esther N M

PLoS pathogens

2019 Volume 15, Issue 2, Page(s) e1007594

Abstract: Several naked virus species, including members of the Picornaviridae family, have recently been described to escape their host cells and spread infection via enclosure in extracellular vesicles (EV). EV are 50-300 nm sized lipid membrane-enclosed ... ...

Abstract	Several naked virus species, including members of the Picornaviridae family, have recently been described to escape their host cells and spread infection via enclosure in extracellular vesicles (EV). EV are 50-300 nm sized lipid membrane-enclosed particles produced by all cells that are broadly recognized for playing regulatory roles in numerous (patho)physiological processes, including viral infection. Both pro- and antiviral functions have been ascribed to EV released by virus-infected cells. It is currently not known whether this reported functional diversity is a result of the release of multiple virus-containing and non-virus containing EV subpopulations that differ in composition and function. Using encephalomyocarditis virus infection (EMCV, Picornaviridae family), we here provide evidence that EV populations released by infected cells are highly heterogeneous. Virus was contained in two distinct EV populations that differed in physical characteristics, such as sedimentation properties, and in enrichment for proteins indicative of different EV biogenesis pathways, such as the plasma membrane resident proteins Flotillin-1 and CD9, and the autophagy regulatory protein LC3. Additional levels of EV heterogeneity were identified using high-resolution flow cytometric analysis of single EV. Importantly, we demonstrate that EV subsets released during EMCV infection varied largely in potency of transferring virus infection and in their kinetics of release from infected cells. These data support the notion that heterogeneous EV populations released by virus-infected cells can exert diverse functions at distinct time points during infection. Unraveling the compositional, temporal and functional heterogeneity of these EV populations using single EV analysis technologies, as employed in this study, is vital to understanding the role of EV in virus dissemination and antiviral host responses.
MeSH term(s)	Autophagy ; Encephalomyocarditis virus/metabolism ; Extracellular Vesicles/metabolism ; Extracellular Vesicles/physiology ; Extracellular Vesicles/virology ; HeLa Cells ; Humans ; Picornaviridae/metabolism ; Picornaviridae/pathogenicity ; Picornaviridae Infections/metabolism
Language	English
Publishing date	2019-02-19
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7366
ISSN (online)	1553-7374
ISSN	1553-7366
DOI	10.1371/journal.ppat.1007594
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