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Article ; Online: The inflammasome pathway is activated by dengue virus non-structural protein 1 and is protective during dengue virus infection.

Wong, Marcus P / Juan, Evan Y W / Pahmeier, Felix / Chelluri, Sai S / Wang, Phoebe / Castillo-Rojas, Bryan / Blanc, Sophie F / Biering, Scott B / Vance, Russell E / Harris, Eva

PLoS pathogens

2024 Volume 20, Issue 4, Page(s) e1012167

Abstract: Dengue virus (DENV) is a medically important flavivirus causing an estimated 50-100 million dengue cases annually, some of whom progress to severe disease. DENV non-structural protein 1 (NS1) is secreted from infected cells and has been implicated as a ... ...

Abstract	Dengue virus (DENV) is a medically important flavivirus causing an estimated 50-100 million dengue cases annually, some of whom progress to severe disease. DENV non-structural protein 1 (NS1) is secreted from infected cells and has been implicated as a major driver of dengue pathogenesis by inducing endothelial barrier dysfunction. However, less is known about how DENV NS1 interacts with immune cells and what role these interactions play. Here we report that DENV NS1 can trigger activation of inflammasomes, a family of cytosolic innate immune sensors that respond to infectious and noxious stimuli, in mouse and human macrophages. DENV NS1 induces the release of IL-1β in a caspase-1 dependent manner. Additionally, we find that DENV NS1-induced inflammasome activation is independent of the NLRP3, Pyrin, and AIM2 inflammasome pathways, but requires CD14. Intriguingly, DENV NS1-induced inflammasome activation does not induce pyroptosis and rapid cell death; instead, macrophages maintain cellular viability while releasing IL-1β. Lastly, we show that caspase-1/11-deficient, but not NLRP3-deficient, mice are more susceptible to lethal DENV infection. Together, these results indicate that the inflammasome pathway acts as a sensor of DENV NS1 and plays a protective role during infection.
Language	English
Publishing date	2024-04-25
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.1012167
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Article ; Online: Identification of host dependency factors involved in SARS-CoV-2 replication organelle formation through proteomics and ultrastructural analysis.

Pahmeier, Felix / Lavacca, Teresa-Maria / Goellner, Sarah / Neufeldt, Christopher J / Prasad, Vibhu / Cerikan, Berati / Rajasekharan, Sreejith / Mizzon, Giulia / Haselmann, Uta / Funaya, Charlotta / Scaturro, Pietro / Cortese, Mirko / Bartenschlager, Ralf

Journal of virology

2023 Volume 97, Issue 11, Page(s) e0087823

Abstract: Importance: Remodeling of the cellular endomembrane system by viruses allows for efficient and coordinated replication of the viral genome in distinct subcellular compartments termed replication organelles. As a critical step in the viral life cycle, ... ...

Abstract	Importance: Remodeling of the cellular endomembrane system by viruses allows for efficient and coordinated replication of the viral genome in distinct subcellular compartments termed replication organelles. As a critical step in the viral life cycle, replication organelle formation is an attractive target for therapeutic intervention, but factors central to this process are only partially understood. In this study, we corroborate that two viral proteins, nsp3 and nsp4, are the major drivers of membrane remodeling in SARS-CoV-2 infection. We further report a number of host cell factors interacting with these viral proteins and supporting the viral replication cycle, some of them by contributing to the formation of the SARS-CoV-2 replication organelle.
MeSH term(s)	Humans ; COVID-19 ; Organelles/metabolism ; Proteomics ; SARS-CoV-2/physiology ; Viral Nonstructural Proteins/genetics ; Viral Nonstructural Proteins/metabolism ; Virus Replication
Chemical Substances	Viral Nonstructural Proteins
Language	English
Publishing date	2023-10-31
Publishing country	United States
Document type	Journal Article
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/jvi.00878-23
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Article: The Inflammasome Pathway is Activated by Dengue Virus Non-structural Protein 1 and is Protective During Dengue Virus Infection.

Wong, Marcus P / Juan, Evan Y W / Chelluri, Sai S / Wang, Phoebe / Pahmeier, Felix / Castillo-Rojas, Bryan / Blanc, Sophie F / Biering, Scott B / Vance, Russell E / Harris, Eva

bioRxiv : the preprint server for biology

2023

Abstract	Dengue virus (DENV) is a medically important flavivirus causing an estimated 50-100 million dengue cases annually, some of whom progress to severe disease. DENV non-structural protein 1 (NS1) is secreted from infected cells and has been implicated as a major driver of dengue pathogenesis by inducing endothelial barrier dysfunction. However, less is known about how DENV NS1 interacts with immune cells and what role these interactions play. Here we report that DENV NS1 can trigger activation of inflammasomes, a family of cytosolic innate immune sensors that respond to infectious and noxious stimuli, in mouse and human macrophages. DENV NS1 induces the release of IL-1β in a caspase-1 dependent manner. Additionally, we find that DENV NS1-induced inflammasome activation is independent of the NLRP3, Pyrin, and AIM2 inflammasome pathways, but requires CD14. Intriguingly, DENV NS1-induced inflammasome activation does not induce pyroptosis and rapid cell death; instead, macrophages maintain cellular viability while releasing IL-1β. Lastly, we show that caspase-1/11-deficient, but not NLRP3-deficient, mice are more susceptible to lethal DENV infection. Together, these results indicate that the inflammasome pathway acts as a sensor of DENV NS1 and plays a protective role during infection.
Language	English
Publishing date	2023-09-21
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.09.21.558875
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Article ; Online: N-Phenylpyridine-3-Carboxamide and 6-Acetyl-1H-Indazole Inhibit the RNA Replication Step of the Dengue Virus Life Cycle.

Sow, Aïssatou Aïcha / Pahmeier, Felix / Ayotte, Yann / Anton, Anaïs / Mazeaud, Clément / Charpentier, Tania / Angelo, Léna / Woo, Simon / Cerikan, Berati / Falzarano, Darryl / Abrahamyan, Levon / Lamarre, Alain / Labonté, Patrick / Cortese, Mirko / Bartenschlager, Ralf / LaPlante, Steven R / Chatel-Chaix, Laurent

Antimicrobial agents and chemotherapy

2023 Volume 67, Issue 2, Page(s) e0133122

Abstract: Dengue virus (DENV) is ... ...

Abstract	Dengue virus (DENV) is a
MeSH term(s)	Animals ; Humans ; Antiviral Agents/pharmacology ; Antiviral Agents/therapeutic use ; Dengue/drug therapy ; Dengue Virus/genetics ; Flavivirus ; Life Cycle Stages ; RNA Replication ; RNA, Viral/genetics ; Virus Replication ; Zika Virus/genetics ; Zika Virus Infection ; Subgenomic RNA/genetics
Chemical Substances	Antiviral Agents ; RNA, Viral ; Subgenomic RNA
Language	English
Publishing date	2023-01-26
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	217602-6
ISSN	1098-6596 ; 0066-4804
ISSN (online)	1098-6596
ISSN	0066-4804
DOI	10.1128/aac.01331-22
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Article ; Online: The Biogenesis of Dengue Virus Replication Organelles Requires the ATPase Activity of Valosin-Containing Protein.

Mazeaud, Clément / Anton, Anaïs / Pahmeier, Felix / Sow, Aïssatou Aïcha / Cerikan, Berati / Freppel, Wesley / Cortese, Mirko / Bartenschlager, Ralf / Chatel-Chaix, Laurent

Viruses

2021 Volume 13, Issue 10

Abstract: The dengue virus (DENV) causes the most prevalent arthropod-borne viral disease worldwide. While its incidence is increasing in many countries, there is no approved antiviral therapy currently available. In infected cells, the DENV induces extensive ... ...

Abstract	The dengue virus (DENV) causes the most prevalent arthropod-borne viral disease worldwide. While its incidence is increasing in many countries, there is no approved antiviral therapy currently available. In infected cells, the DENV induces extensive morphological alterations of the endoplasmic reticulum (ER) to generate viral replication organelles (vRO), which include convoluted membranes (CM) and vesicle packets (VP) hosting viral RNA replication. The viral non-structural protein NS4B localizes to vROs and is absolutely required for viral replication through poorly defined mechanisms, which might involve cellular protein partners. Previous interactomic studies identified the ATPase valosin-containing protein (VCP) as a DENV NS4B-interacting host factor in infected cells. Using both pharmacological and dominant-negative inhibition approaches, we show, in this study, that VCP ATPase activity is required for efficient DENV replication. VCP associates with NS4B when expressed in the absence of other viral proteins while in infected cells, both proteins colocalize within large DENV-induced cytoplasmic structures previously demonstrated to be CMs. Consistently, VCP inhibition dramatically reduces the abundance of DENV CMs in infected cells. Most importantly, using a recently reported replication-independent plasmid-based vRO induction system, we show that
MeSH term(s)	Adenosine Triphosphatases/genetics ; Cell Line ; Dengue/virology ; Dengue Virus/genetics ; Dengue Virus/metabolism ; Dengue Virus/pathogenicity ; Endoplasmic Reticulum/virology ; Humans ; RNA, Viral/genetics ; Valosin Containing Protein/genetics ; Valosin Containing Protein/metabolism ; Viral Nonstructural Proteins/genetics ; Viral Replication Compartments/physiology ; Virus Replication/physiology
Chemical Substances	RNA, Viral ; Viral Nonstructural Proteins ; Adenosine Triphosphatases (EC 3.6.1.-) ; VCP protein, human (EC 3.6.4.6) ; Valosin Containing Protein (EC 3.6.4.6)
Language	English
Publishing date	2021-10-18
Publishing country	Switzerland
Document type	Journal Article ; 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/v13102092
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Article ; Online: A Versatile Reporter System To Monitor Virus-Infected Cells and Its Application to Dengue Virus and SARS-CoV-2.

Pahmeier, Felix / Neufeldt, Christopher J / Cerikan, Berati / Prasad, Vibhu / Pape, Costantin / Laketa, Vibor / Ruggieri, Alessia / Bartenschlager, Ralf / Cortese, Mirko

Journal of virology

2021 Volume 95, Issue 4

Abstract: Positive-strand RNA viruses have been the etiological agents in several major disease outbreaks over the last few decades. Examples of this include flaviviruses, such as dengue virus and Zika virus, which cause millions of yearly infections around the ... ...

Abstract	Positive-strand RNA viruses have been the etiological agents in several major disease outbreaks over the last few decades. Examples of this include flaviviruses, such as dengue virus and Zika virus, which cause millions of yearly infections around the globe, and coronaviruses, such as SARS-CoV-2, the source of the current pandemic. The severity of outbreaks caused by these viruses stresses the importance of research aimed at determining methods to limit virus spread and to curb disease severity. Such studies require molecular tools to decipher virus-host interactions and to develop effective treatments. Here, we describe the generation and characterization of a reporter system that can be used to visualize and identify cells infected with dengue virus or SARS-CoV-2. This system is based on viral protease activity that mediates cleavage and nuclear translocation of an engineered fluorescent protein stably expressed in cells. We show the suitability of this system for live cell imaging, for visualization of single infected cells, and for screening and testing of antiviral compounds. With the integrated modular building blocks, this system is easy to manipulate and can be adapted to any virus encoding a protease, thus offering a high degree of flexibility.
MeSH term(s)	A549 Cells ; Animals ; COVID-19/diagnosis ; COVID-19/metabolism ; COVID-19/pathology ; COVID-19/virology ; Cell Line ; Chlorocebus aethiops ; Dengue/diagnosis ; Dengue/metabolism ; Dengue/pathology ; Dengue/virology ; Dengue Virus/genetics ; Dengue Virus/isolation & purification ; Dengue Virus/metabolism ; Genes, Reporter ; Green Fluorescent Proteins/metabolism ; HEK293 Cells ; Humans ; Nuclear Localization Signals/metabolism ; SARS-CoV-2/genetics ; SARS-CoV-2/isolation & purification ; SARS-CoV-2/metabolism ; Vero Cells ; Viral Nonstructural Proteins/metabolism ; Virus Replication
Chemical Substances	Nuclear Localization Signals ; Viral Nonstructural Proteins ; Green Fluorescent Proteins (147336-22-9)
Language	English
Publishing date	2021-01-28
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.01715-20
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Article ; Online: Enhanced SARS-CoV-2 entry via UPR-dependent AMPK-related kinase NUAK2.

Molecular cell

2023 Volume 83, Issue 14, Page(s) 2559–2577.e8

Abstract: Severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) remodels the endoplasmic reticulum (ER) to form replication organelles, leading to ER stress and unfolded protein response (UPR). However, the role of specific UPR pathways in infection remains ...

Abstract	Severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) remodels the endoplasmic reticulum (ER) to form replication organelles, leading to ER stress and unfolded protein response (UPR). However, the role of specific UPR pathways in infection remains unclear. Here, we found that SARS-CoV-2 infection causes marginal activation of signaling sensor IRE1α leading to its phosphorylation, clustering in the form of dense ER-membrane rearrangements with embedded membrane openings, and XBP1 splicing. By investigating the factors regulated by IRE1α-XBP1 during SARS-CoV-2 infection, we identified stress-activated kinase NUAK2 as a novel host-dependency factor for SARS-CoV-2, HCoV-229E, and MERS-CoV entry. Reducing NUAK2 abundance or kinase activity impaired SARS-CoV-2 particle binding and internalization by decreasing cell surface levels of viral receptors and viral trafficking likely by modulating the actin cytoskeleton. IRE1α-dependent NUAK2 levels were elevated in SARS-CoV-2-infected and bystander non-infected cells, promoting viral spread by maintaining ACE2 cell surface levels and facilitating virion binding to bystander cells.
MeSH term(s)	Humans ; AMP-Activated Protein Kinase Kinases ; AMP-Activated Protein Kinases/metabolism ; COVID-19/metabolism ; COVID-19/pathology ; COVID-19/virology ; Endoribonucleases/genetics ; Endoribonucleases/metabolism ; Protein Serine-Threonine Kinases/genetics ; Protein Serine-Threonine Kinases/metabolism ; SARS-CoV-2/physiology ; Unfolded Protein Response ; Virus Internalization
Chemical Substances	AMP-Activated Protein Kinase Kinases (EC 2.7.11.3) ; AMP-Activated Protein Kinases (EC 2.7.11.31) ; Endoribonucleases (EC 3.1.-) ; NUAK2 protein, human (EC 2.7.11.1) ; Protein Serine-Threonine Kinases (EC 2.7.11.1)
Language	English
Publishing date	2023-07-07
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	1415236-8
ISSN	1097-4164 ; 1097-2765
ISSN (online)	1097-4164
ISSN	1097-2765
DOI	10.1016/j.molcel.2023.06.020
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Article ; Online: Novel Toscana Virus Reverse Genetics System Establishes NSs as an Antagonist of Type I Interferon Responses.

Woelfl, Franziska / Léger, Psylvia / Oreshkova, Nadia / Pahmeier, Felix / Windhaber, Stefan / Koch, Jana / Stanifer, Megan / Roman Sosa, Gleyder / Uckeley, Zina M / Rey, Felix A / Boulant, Steeve / Kortekaas, Jeroen / Wichgers Schreur, Paul J / Lozach, Pierre-Yves

Viruses

2020 Volume 12, Issue 4

Abstract: The sand fly-borne Toscana virus (TOSV) is the major cause of human meningoencephalitis in the Mediterranean basin during the summer season. In this work, we have developed a T7 RNA polymerase-driven reverse genetics system to recover infectious ... ...

Abstract	The sand fly-borne Toscana virus (TOSV) is the major cause of human meningoencephalitis in the Mediterranean basin during the summer season. In this work, we have developed a T7 RNA polymerase-driven reverse genetics system to recover infectious particles of a lineage B strain of TOSV. The viral protein pattern and growth properties of the rescued virus (rTOSV) were found to be similar to those of the corresponding wild-type (wt) virus. Using this system, we genetically engineered a TOSV mutant lacking expression of the non-structural protein NSs (rTOSVɸNSs). Unlike rTOSV and the wt virus, rTOSVɸNSs was unable to (i) suppress interferon (IFN)-b messenger RNA induction; and (ii) grow efficiently in cells producing IFN-b. Together, our results highlight the importance of NSs for TOSV in evading the IFN response and provide a comprehensive toolbox to investigate the TOSV life cycle in mammalian and insect host cells, including several novel polyclonal antibodies.
MeSH term(s)	A549 Cells ; Animals ; Antibodies, Viral/immunology ; Cell Line ; Chlorocebus aethiops ; Cricetinae ; DNA-Directed RNA Polymerases/genetics ; Genome, Viral ; Humans ; Insecta ; Interferon-beta/antagonists & inhibitors ; Interferon-beta/immunology ; Kidney/cytology ; Mutation ; Reverse Genetics ; Sandfly fever Naples virus/genetics ; Sandfly fever Naples virus/immunology ; Vero Cells ; Viral Nonstructural Proteins/genetics ; Viral Nonstructural Proteins/immunology ; Viral Proteins/genetics
Chemical Substances	Antibodies, Viral ; Viral Nonstructural Proteins ; Viral Proteins ; Interferon-beta (77238-31-4) ; bacteriophage T7 RNA polymerase (EC 2.7.7.-) ; DNA-Directed RNA Polymerases (EC 2.7.7.6)
Language	English
Publishing date	2020-04-04
Publishing country	Switzerland
Document type	Journal Article ; 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/v12040400
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Article: The Biogenesis of Dengue Virus Replication Organelles Requires the ATPase Activity of Valosin-Containing Protein

Mazeaud, Clément / Anton, Anaïs / Pahmeier, Felix / Sow, Aïssatou Aïcha / Cerikan, Berati / Freppel, Wesley / Cortese, Mirko / Bartenschlager, Ralf / Chatel-Chaix, Laurent

Viruses. 2021 Oct. 18, v. 13, no. 10

2021

Abstract	The dengue virus (DENV) causes the most prevalent arthropod-borne viral disease worldwide. While its incidence is increasing in many countries, there is no approved antiviral therapy currently available. In infected cells, the DENV induces extensive morphological alterations of the endoplasmic reticulum (ER) to generate viral replication organelles (vRO), which include convoluted membranes (CM) and vesicle packets (VP) hosting viral RNA replication. The viral non-structural protein NS4B localizes to vROs and is absolutely required for viral replication through poorly defined mechanisms, which might involve cellular protein partners. Previous interactomic studies identified the ATPase valosin-containing protein (VCP) as a DENV NS4B-interacting host factor in infected cells. Using both pharmacological and dominant-negative inhibition approaches, we show, in this study, that VCP ATPase activity is required for efficient DENV replication. VCP associates with NS4B when expressed in the absence of other viral proteins while in infected cells, both proteins colocalize within large DENV-induced cytoplasmic structures previously demonstrated to be CMs. Consistently, VCP inhibition dramatically reduces the abundance of DENV CMs in infected cells. Most importantly, using a recently reported replication-independent plasmid-based vRO induction system, we show that de novo VP biogenesis is dependent on VCP ATPase activity. Overall, our data demonstrate that VCP ATPase activity is required for vRO morphogenesis and/or stability. Considering that VCP was shown to be required for the replication of other flaviviruses, our results argue that VCP is a pan-flaviviral host dependency factor. Given that new generation VCP-targeting drugs are currently evaluated in clinical trials for cancer treatment, VCP may constitute an attractive broad-spectrum antiviral target in drug repurposing approaches.
Keywords	Dengue virus ; RNA replication ; adenosinetriphosphatase ; biogenesis ; cancer therapy ; drugs ; endoplasmic reticulum ; morphogenesis ; viral nonstructural proteins ; virus replication
Language	English
Dates of publication	2021-1018
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2516098-9
ISSN	1999-4915
ISSN	1999-4915
DOI	10.3390/v13102092
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: A versatile reporter system to monitor virus infected cells and its application to dengue virus and SARS-CoV-2

Pahmeier, Felix / Neufeldt, Christopher John / Cerikan, Berati / Prasad, Vibhu / Pape, Constantin / Laketa, Vibor / Ruggieri, Alessia / Bartenschlager, Ralf / Cortese, Mirko

bioRxiv

Abstract: Positive-strand RNA viruses have been the etiological agents in several major disease outbreaks over the last few decades. Examples of that are flaviviruses, such as dengue virus and Zika virus that cause millions of yearly infections and spread around ... ...

Abstract	Positive-strand RNA viruses have been the etiological agents in several major disease outbreaks over the last few decades. Examples of that are flaviviruses, such as dengue virus and Zika virus that cause millions of yearly infections and spread around the globe, and coronaviruses, such as SARS-CoV-2, which is the cause of the current pandemic. The severity of outbreaks caused by these viruses stresses the importance of virology research in determining mechanisms to limit virus spread and to curb disease severity. Such studies require molecular tools to decipher virus-host interactions and to develop effective interventions. Here, we describe the generation and characterization of a reporter system to visualize dengue virus and SARS-CoV-2 replication in live cells. The system is based on viral protease activity causing cleavage and nuclear translocation of an engineered fluorescent protein that is expressed in the infected cells. We show the suitability of the system for live cell imaging and visualization of single infected cells as well as for screening and testing of antiviral compounds. Given the modular building blocks, the system is easy to manipulate and can be adapted to any virus encoding a protease, thus offering a high degree of flexibility.
Keywords	covid19
Language	English
Publishing date	2020-09-01
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2020.08.31.276683
Database	COVID19

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