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Article ; Online: Mammalian and Avian Host Cell Influenza A Restriction Factors.

McKellar, Joe / Rebendenne, Antoine / Wencker, Mélanie / Moncorgé, Olivier / Goujon, Caroline

2021 Volume 13, Issue 3

Abstract: The threat of a new influenza pandemic is real. With past pandemics claiming millions of lives, finding new ways to combat this virus is essential. Host cells have developed a multi-modular system to detect incoming pathogens, a phenomenon called sensing. ...

Abstract	The threat of a new influenza pandemic is real. With past pandemics claiming millions of lives, finding new ways to combat this virus is essential. Host cells have developed a multi-modular system to detect incoming pathogens, a phenomenon called sensing. The signaling cascade triggered by sensing subsequently induces protection for themselves and their surrounding neighbors, termed interferon (IFN) response. This response induces the upregulation of hundreds of interferon-stimulated genes (ISGs), including antiviral effectors, establishing an antiviral state. As well as the antiviral proteins induced through the IFN system, cells also possess a so-called intrinsic immunity, constituted of antiviral proteins that are constitutively expressed, creating a first barrier preceding the induction of the interferon system. All these combined antiviral effectors inhibit the virus at various stages of the viral lifecycle, using a wide array of mechanisms. Here, we provide a review of mammalian and avian influenza A restriction factors, detailing their mechanism of action and in vivo relevance, when known. Understanding their mode of action might help pave the way for the development of new influenza treatments, which are absolutely required if we want to be prepared to face a new pandemic.
MeSH term(s)	Animals ; Birds ; Host-Pathogen Interactions ; Humans ; Immunity, Innate ; Influenza A virus/immunology ; Influenza A virus/physiology ; Influenza in Birds/immunology ; Influenza in Birds/virology ; Influenza, Human/immunology ; Influenza, Human/virology ; Poultry ; Virus Replication
Language	English
Publishing date	2021-03-22
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v13030522
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Article ; Online: Phagocytose : les professionnels dictent leur loi.

Rebendenne, Antoine / Amiar, Olivia / Hemmi, Audrey / Dupré, Sophie

Medecine sciences : M/S

2017 Volume 33, Issue 8-9, Page(s) 738–740

Title translation	Phagocytosis: professionals make their own law.
MeSH term(s)	Apoptosis/physiology ; Humans ; Hypersensitivity/pathology ; Hypersensitivity/physiopathology ; Inflammation/pathology ; Inflammation/physiopathology ; Insulin-Like Growth Factor I/physiology ; Macrophages, Alveolar/physiology ; Organ Specificity ; Phagocytosis/physiology ; Respiratory Mucosa/cytology ; Respiratory Mucosa/physiology ; Signal Transduction/physiology
Chemical Substances	Insulin-Like Growth Factor I (67763-96-6)
Language	French
Publishing date	2017-09-18
Publishing country	France
Document type	News
ZDB-ID	632733-3
ISSN	1958-5381 ; 0767-0974
ISSN (online)	1958-5381
ISSN	0767-0974
DOI	10.1051/medsci/20173308017
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Article: Mammalian and Avian Host Cell Influenza A Restriction Factors

McKellar, Joe / Rebendenne, Antoine / Wencker, Mélanie / Moncorgé, Olivier / Goujon, Caroline

Viruses. 2021 Mar. 22, v. 13, no. 3

2021

Abstract	The threat of a new influenza pandemic is real. With past pandemics claiming millions of lives, finding new ways to combat this virus is essential. Host cells have developed a multi-modular system to detect incoming pathogens, a phenomenon called sensing. The signaling cascade triggered by sensing subsequently induces protection for themselves and their surrounding neighbors, termed interferon (IFN) response. This response induces the upregulation of hundreds of interferon-stimulated genes (ISGs), including antiviral effectors, establishing an antiviral state. As well as the antiviral proteins induced through the IFN system, cells also possess a so-called intrinsic immunity, constituted of antiviral proteins that are constitutively expressed, creating a first barrier preceding the induction of the interferon system. All these combined antiviral effectors inhibit the virus at various stages of the viral lifecycle, using a wide array of mechanisms. Here, we provide a review of mammalian and avian influenza A restriction factors, detailing their mechanism of action and in vivo relevance, when known. Understanding their mode of action might help pave the way for the development of new influenza treatments, which are absolutely required if we want to be prepared to face a new pandemic.
Keywords	avian influenza ; birds ; immunity ; interferons ; mammals ; mechanism of action ; pandemic ; viruses
Language	English
Dates of publication	2021-0322
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
Note	NAL-light
ZDB-ID	2516098-9
ISSN	1999-4915
ISSN	1999-4915
DOI	10.3390/v13030522
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: SARS-CoV-2 triggers an MDA-5-dependent interferon response which is unable to control replication in lung epithelial cells.

Rebendenne, Antoine / Valadão, Ana Luiza Chaves / Tauziet, Marine / Maarifi, Ghizlane / Bonaventure, Boris / McKellar, Joe / Planès, Rémi / Nisole, Sébastien / Arnaud-Arnould, Mary / Moncorgé, Olivier / Goujon, Caroline

Journal of virology

2021 Volume 95, Issue 8

Abstract: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is the etiologic agent of coronavirus disease 19 (COVID-19), which ranges from mild respiratory symptoms to acute respiratory distress syndrome, and death in the most severe cases. Immune ... ...

Abstract	Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is the etiologic agent of coronavirus disease 19 (COVID-19), which ranges from mild respiratory symptoms to acute respiratory distress syndrome, and death in the most severe cases. Immune dysregulation with altered innate cytokine responses is thought to contribute to disease severity. Here, we characterized in depth host cell responses against SARS-CoV-2 in primary human airway epithelia (HAE) and immortalized cell lines. Our results demonstrate that primary HAE and model cells elicit a robust induction of type I and III interferons (IFNs). Importantly, we show for the first time that melanoma differentiation associated gene (MDA)-5 is the main sensor of SARS-CoV-2 in lung cells. IFN exposure strongly inhibited viral replication and
Language	English
Publishing date	2021-01-29
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.02415-20
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Article ; Online: Bidirectional genome-wide CRISPR screens reveal host factors regulating SARS-CoV-2, MERS-CoV and seasonal HCoVs.

Rebendenne, Antoine / Roy, Priyanka / Bonaventure, Boris / Chaves Valadão, Ana Luiza / Desmarets, Lowiese / Arnaud-Arnould, Mary / Rouillé, Yves / Tauziet, Marine / Giovannini, Donatella / Touhami, Jawida / Lee, Yenarae / DeWeirdt, Peter / Hegde, Mudra / Urbach, Serge / Koulali, Khadija El / de Gracia, Francisco Garcia / McKellar, Joe / Dubuisson, Jean / Wencker, Mélanie /

Belouzard, Sandrine / Moncorgé, Olivier / Doench, John G / Goujon, Caroline

Nature genetics

2022 Volume 54, Issue 8, Page(s) 1090–1102

Abstract: CRISPR knockout (KO) screens have identified host factors regulating severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) replication. Here, we conducted a meta-analysis of these screens, which showed a high level of cell-type specificity of the ... ...

Abstract	CRISPR knockout (KO) screens have identified host factors regulating severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) replication. Here, we conducted a meta-analysis of these screens, which showed a high level of cell-type specificity of the identified hits, highlighting the necessity of additional models to uncover the full landscape of host factors. Thus, we performed genome-wide KO and activation screens in Calu-3 lung cells and KO screens in Caco-2 colorectal cells, followed by secondary screens in four human cell lines. This revealed host-dependency factors, including AP1G1 adaptin and ATP8B1 flippase, as well as inhibitors, including mucins. Interestingly, some of the identified genes also modulate Middle East respiratory syndrome coronavirus (MERS-CoV) and seasonal human coronavirus (HCoV) (HCoV-NL63 and HCoV-229E) replication. Moreover, most genes had an impact on viral entry, with AP1G1 likely regulating TMPRSS2 activity at the plasma membrane. These results demonstrate the value of multiple cell models and perturbational modalities for understanding SARS-CoV-2 replication and provide a list of potential targets for therapeutic interventions.
MeSH term(s)	COVID-19/genetics ; Caco-2 Cells ; Clustered Regularly Interspaced Short Palindromic Repeats/genetics ; Humans ; Middle East Respiratory Syndrome Coronavirus/genetics ; SARS-CoV-2/genetics ; Seasons
Language	English
Publishing date	2022-07-25
Publishing country	United States
Document type	Journal Article ; Meta-Analysis ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	1108734-1
ISSN	1546-1718 ; 1061-4036
ISSN (online)	1546-1718
ISSN	1061-4036
DOI	10.1038/s41588-022-01110-2
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Article ; Online: Structure of the zinc-finger antiviral protein in complex with RNA reveals a mechanism for selective targeting of CG-rich viral sequences.

Meagher, Jennifer L / Takata, Matthew / Gonçalves-Carneiro, Daniel / Keane, Sarah C / Rebendenne, Antoine / Ong, Heley / Orr, Victoria K / MacDonald, Margaret R / Stuckey, Jeanne A / Bieniasz, Paul D / Smith, Janet L

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

2019 Volume 116, Issue 48, Page(s) 24303–24309

Abstract: Infection of animal cells by numerous viruses is detected and countered by a variety of means, including recognition of nonself nucleic acids. The zinc finger antiviral protein (ZAP) depletes cytoplasmic RNA that is recognized as foreign in mammalian ... ...

Abstract	Infection of animal cells by numerous viruses is detected and countered by a variety of means, including recognition of nonself nucleic acids. The zinc finger antiviral protein (ZAP) depletes cytoplasmic RNA that is recognized as foreign in mammalian cells by virtue of its elevated CG dinucleotide content compared with endogenous mRNAs. Here, we determined a crystal structure of a protein-RNA complex containing the N-terminal, 4-zinc finger human (h) ZAP RNA-binding domain (RBD) and a CG dinucleotide-containing RNA target. The structure reveals in molecular detail how hZAP is able to bind selectively to CG-rich RNA. Specifically, the 4 zinc fingers create a basic patch on the hZAP RBD surface. The highly basic second zinc finger contains a pocket that selectively accommodates CG dinucleotide bases. Structure guided mutagenesis, cross-linking immunoprecipitation sequencing assays, and RNA affinity assays show that the structurally defined CG-binding pocket is not required for RNA binding per se in human cells. However, the pocket is a crucial determinant of high-affinity, specific binding to CG dinucleotide-containing RNA. Moreover, variations in RNA-binding specificity among a panel of CG-binding pocket mutants quantitatively predict their selective antiviral activity against a CG-enriched HIV-1 strain. Overall, the hZAP RBD RNA structure provides an atomic-level explanation for how ZAP selectively targets foreign, CG-rich RNA.
MeSH term(s)	Binding Sites ; Crystallography, X-Ray ; Fluorescence Polarization ; GC Rich Sequence ; HEK293 Cells ; HIV-1/genetics ; Humans ; Models, Molecular ; Mutagenesis ; Mutation ; Protein Domains ; RNA, Viral/chemistry ; RNA, Viral/metabolism ; RNA-Binding Proteins/chemistry ; RNA-Binding Proteins/genetics ; RNA-Binding Proteins/metabolism ; Repressor Proteins/chemistry ; Repressor Proteins/genetics ; Repressor Proteins/metabolism ; Zinc Fingers
Chemical Substances	RNA, Viral ; RNA-Binding Proteins ; Repressor Proteins ; YLPM1 protein, human
Language	English
Publishing date	2019-11-12
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.1913232116
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Article: Bidirectional genome-wide CRISPR screens reveal host factors regulating SARS-CoV-2, MERS-CoV and seasonal coronaviruses.

bioRxiv : the preprint server for biology

2021

Abstract: Several genome-wide CRISPR knockout screens have been conducted to identify host factors regulating SARS-CoV-2 replication, but the models used have often relied on overexpression of ACE2 receptor. Additionally, such screens have yet to identify the ... ...

Abstract	Several genome-wide CRISPR knockout screens have been conducted to identify host factors regulating SARS-CoV-2 replication, but the models used have often relied on overexpression of ACE2 receptor. Additionally, such screens have yet to identify the protease TMPRSS2, known to be important for viral entry at the plasma membrane. Here, we conducted a meta-analysis of these screens and showed a high level of cell-type specificity of the identified hits, arguing for the necessity of additional models to uncover the full landscape of SARS-CoV-2 host factors. We performed genome-wide knockout and activation CRISPR screens in Calu-3 lung epithelial cells, as well as knockout screens in Caco-2 intestinal cells. In addition to identifying ACE2 and TMPRSS2 as top hits, our study reveals a series of so far unidentified and critical host-dependency factors, including the Adaptins AP1G1 and AP1B1 and the flippase ATP8B1. Moreover, new anti-SARS-CoV-2 proteins with potent activity, including several membrane-associated Mucins, IL6R, and CD44 were identified. We further observed that these genes mostly acted at the critical step of viral entry, with the notable exception of ATP8B1, the knockout of which prevented late stages of viral replication. Exploring the pro- and anti-viral breadth of these genes using highly pathogenic MERS-CoV, seasonal HCoV-NL63 and -229E and influenza A orthomyxovirus, we reveal that some genes such as AP1G1 and ATP8B1 are general coronavirus cofactors. In contrast, Mucins recapitulated their known role as a general antiviral defense mechanism. These results demonstrate the value of considering multiple cell models and perturbational modalities for understanding SARS-CoV-2 replication and provide a list of potential new targets for therapeutic interventions.
Language	English
Publishing date	2021-05-21
Publishing country	United States
Document type	Preprint
DOI	10.1101/2021.05.19.444823
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Article: Bidirectional genome-wide CRISPR screens reveal host factors regulating SARS-CoV-2, MERS-CoV and seasonal HCoVs.

Research square

2021

Abstract	Several genome-wide CRISPR knockout screens have been conducted to identify host factors regulating SARS-CoV-2 replication, but the models used have often relied on overexpression of ACE2 receptor. Additionally, such screens have yet to identify the protease TMPRSS2, known to be important for viral entry at the plasma membrane. Here, we conducted a meta-analysis of these screens and showed a high level of cell-type specificity of the identified hits, arguing for the necessity of additional models to uncover the full landscape of SARS-CoV-2 host factors. We performed genome-wide knockout and activation CRISPR screens in Calu-3 lung epithelial cells, as well as knockout screens in Caco-2 intestinal cells. In addition to identifying ACE2 and TMPRSS2 as top hits, our study reveals a series of so far unidentified and critical host-dependency factors, including the Adaptins AP1G1 and AP1B1 and the flippase ATP8B1. Moreover, new anti-SARS-CoV-2 proteins with potent activity, including several membrane-associated Mucins, IL6R, and CD44 were identified. We further observed that these genes mostly acted at the critical step of viral entry, with the notable exception of ATP8B1, the knockout of which prevented late stages of viral replication. Exploring the pro- and anti-viral breadth of these genes using highly pathogenic MERS-CoV, seasonal HCoV-NL63 and -229E and influenza A orthomyxovirus, we reveal that some genes such as AP1G1 and ATP8B1 are general coronavirus cofactors. In contrast, Mucins recapitulated their known role as a general antiviral defense mechanism. These results demonstrate the value of considering multiple cell models and perturbational modalities for understanding SARS-CoV-2 replication and provide a list of potential new targets for therapeutic interventions.
Language	English
Publishing date	2021-05-27
Publishing country	United States
Document type	Preprint
DOI	10.21203/rs.3.rs-555275/v1
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Article ; Online: The DEAD box RNA helicase DDX42 is an intrinsic inhibitor of positive-strand RNA viruses.

Bonaventure, Boris / Rebendenne, Antoine / Chaves Valadão, Ana Luiza / Arnaud-Arnould, Mary / Gracias, Ségolène / Garcia de Gracia, Francisco / McKellar, Joe / Labaronne, Emmanuel / Tauziet, Marine / Vivet-Boudou, Valérie / Bernard, Eric / Briant, Laurence / Gros, Nathalie / Djilli, Wassila / Courgnaud, Valérie / Parrinello, Hugues / Rialle, Stéphanie / Blaise, Mickaël / Lacroix, Laurent /

Lavigne, Marc / Paillart, Jean-Christophe / Ricci, Emiliano P / Schulz, Reiner / Jouvenet, Nolwenn / Moncorgé, Olivier / Goujon, Caroline

EMBO reports

2022 Volume 23, Issue 11, Page(s) e54061

Abstract: Genome-wide screens are powerful approaches to unravel regulators of viral infections. Here, a CRISPR screen identifies the RNA helicase DDX42 as an intrinsic antiviral inhibitor of HIV-1. Depletion of endogenous DDX42 increases HIV-1 DNA accumulation ... ...

Abstract	Genome-wide screens are powerful approaches to unravel regulators of viral infections. Here, a CRISPR screen identifies the RNA helicase DDX42 as an intrinsic antiviral inhibitor of HIV-1. Depletion of endogenous DDX42 increases HIV-1 DNA accumulation and infection in cell lines and primary cells. DDX42 overexpression inhibits HIV-1 infection, whereas expression of a dominant-negative mutant increases infection. Importantly, DDX42 also restricts LINE-1 retrotransposition and infection with other retroviruses and positive-strand RNA viruses, including CHIKV and SARS-CoV-2. However, DDX42 does not impact the replication of several negative-strand RNA viruses, arguing against an unspecific effect on target cells, which is confirmed by RNA-seq analysis. Proximity ligation assays show DDX42 in the vicinity of viral elements, and cross-linking RNA immunoprecipitation confirms a specific interaction of DDX42 with RNAs from sensitive viruses. Moreover, recombinant DDX42 inhibits HIV-1 reverse transcription in vitro. Together, our data strongly suggest a direct mode of action of DDX42 on viral ribonucleoprotein complexes. Our results identify DDX42 as an intrinsic viral inhibitor, opening new perspectives to target the life cycle of numerous RNA viruses.
MeSH term(s)	Humans ; DEAD-box RNA Helicases/genetics ; DEAD-box RNA Helicases/metabolism ; HIV-1/physiology ; Positive-Strand RNA Viruses/physiology ; SARS-CoV-2/physiology ; Virus Replication
Chemical Substances	DEAD-box RNA Helicases (EC 3.6.4.13) ; DDX42 protein, human (EC 3.6.1-)
Language	English
Publishing date	2022-09-26
Publishing country	England
Document type	Journal Article
ZDB-ID	2020896-0
ISSN	1469-3178 ; 1469-221X
ISSN (online)	1469-3178
ISSN	1469-221X
DOI	10.15252/embr.202154061
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Article ; Online: SARS-CoV-2 replication triggers an MDA-5-dependent interferon production which is unable to efficiently control replication

Rebendenne, Antoine / Chaves Valadão, Ana Luiza / Tauziet, Marine / Maarifi, Ghizlane / Bonaventure, Boris / Planès, Rémi / McKellar, Joe / Nisole, Sébastien / Arnaud-Arnould, Mary / Moncorgé, Olivier / Goujon, Caroline

bioRxiv

Abstract: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is the third highly pathogenic coronavirus to spill over to humans in less than 20 years, after SARS-CoV-1 in 2002-2003 and Middle East respiratory syndrome (MERS)-CoV in 2012. SARS-CoV-2 is ... ...

Abstract	Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is the third highly pathogenic coronavirus to spill over to humans in less than 20 years, after SARS-CoV-1 in 2002-2003 and Middle East respiratory syndrome (MERS)-CoV in 2012. SARS-CoV-2 is the etiologic agent of coronavirus disease 19 (COVID-19), which ranges from mild respiratory symptoms to severe lung injury and death in the most severe cases. The COVID-19 pandemic is currently a major health issue worldwide. Immune dysregulation characterized by altered innate cytokine responses is thought to contribute to the pathology of COVID-19 patients, which is a testimony of the fundamental role of the innate immune response against SARS-CoV-2. Here, we further characterized the host cell antiviral response against SARS-CoV-2 by using primary human airway epithelia and immortalized model cell lines. We mainly focused on the type I and III interferon (IFN) responses, which lead to the establishment of an antiviral state through the expression of IFN-stimulated genes (ISGs). Our results demonstrate that both primary airway epithelial cells and model cell lines elicit a robust immune response characterized by a strong induction of type I and III IFN through the detection of viral pathogen molecular patterns (PAMPs) by melanoma differentiation associated gene (MDA)-5. However, despite the high levels of type I and III IFNs produced in response to SARS-CoV-2 infection, the IFN response was unable to control viral replication, whereas IFN pre-treatment strongly inhibited viral replication and de novo production of infectious virions. Taken together, these results highlight the complex and ambiguous interplay between viral replication and the timing of IFN responses.
Keywords	covid19
Language	English
Publishing date	2020-10-28
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2020.10.28.358945
Database	COVID19

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