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Article ; Online: R-Propranolol Has Broad-Spectrum Anti-Coronavirus Activity and Suppresses Factors Involved in Pathogenic Angiogenesis.

Thaler, Melissa / Salgado-Benvindo, Clarisse / Leijs, Anouk / Tas, Ali / Ninaber, Dennis K / Arbiser, Jack L / Snijder, Eric J / van Hemert, Martijn J

International journal of molecular sciences

2023 Volume 24, Issue 5

Abstract: The SARS-CoV-2 pandemic highlighted the need for broad-spectrum antivirals to increase our preparedness. Patients often require treatment by the time that blocking virus replication is less effective. Therefore, therapy should not only aim to inhibit the ...

Abstract	The SARS-CoV-2 pandemic highlighted the need for broad-spectrum antivirals to increase our preparedness. Patients often require treatment by the time that blocking virus replication is less effective. Therefore, therapy should not only aim to inhibit the virus, but also to suppress pathogenic host responses, e.g., leading to microvascular changes and pulmonary damage. Clinical studies have previously linked SARS-CoV-2 infection to pathogenic intussusceptive angiogenesis in the lungs, involving the upregulation of angiogenic factors such as ANGPTL4. The β-blocker propranolol is used to suppress aberrant ANGPTL4 expression in the treatment of hemangiomas. Therefore, we investigated the effect of propranolol on SARS-CoV-2 infection and the expression of ANGPTL4. SARS-CoV-2 upregulated ANGPTL4 in endothelial and other cells, which could be suppressed with R-propranolol. The compound also inhibited the replication of SARS-CoV-2 in Vero-E6 cells and reduced the viral load by up to ~2 logs in various cell lines and primary human airway epithelial cultures. R-propranolol was as effective as S-propranolol but lacks the latter's undesired β-blocker activity. R-propranolol also inhibited SARS-CoV and MERS-CoV. It inhibited a post-entry step of the replication cycle, likely via host factors. The broad-spectrum antiviral effect and suppression of factors involved in pathogenic angiogenesis make R-propranolol an interesting molecule to further explore for the treatment of coronavirus infections.
MeSH term(s)	Animals ; Chlorocebus aethiops ; Humans ; COVID-19 ; Propranolol/pharmacology ; SARS-CoV-2 ; Vero Cells ; Cell Line ; Antiviral Agents/pharmacology ; Virus Replication
Chemical Substances	Propranolol (9Y8NXQ24VQ) ; Antiviral Agents
Language	English
Publishing date	2023-02-27
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms24054588
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Honokiol Inhibits SARS-CoV-2 Replication in Cell Culture at a Post-Entry Step.

Salgado-Benvindo, Clarisse / Leijs, Anouk A / Thaler, Melissa / Tas, Ali / Arbiser, Jack L / Snijder, Eric J / van Hemert, Martijn J

Microbiology spectrum

2023 Volume 11, Issue 3, Page(s) e0327322

Abstract: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) emerged in 2019, and the resulting pandemic has already caused the death of over 6 million people. There are currently few antivirals approved for treatment of the 2019 coronavirus disease ( ... ...

Abstract	Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) emerged in 2019, and the resulting pandemic has already caused the death of over 6 million people. There are currently few antivirals approved for treatment of the 2019 coronavirus disease (COVID-19), and more options would be beneficial, not only now but also to increase our preparedness for future coronavirus outbreaks. Honokiol is a small molecule from magnolia trees for which several biological effects have been reported, including anticancer and anti-inflammatory activities. Honokiol has also been shown to inhibit several viruses in cell culture. In this study, we determined that honokiol protected Vero E6 cells from SARS-CoV-2-mediated cytopathic effect, with a 50% effective concentration of 7.8 μM. In viral load reduction assays, honokiol decreased viral RNA copies as well as viral infectious progeny titers. The compound also inhibited SARS-CoV-2 replication in the more relevant human A549 cells expressing angiotensin converting enzyme 2 and transmembrane protease serine 2. Time-of-addition and other assays showed that honokiol inhibited virus replication at a post-entry step of the replication cycle. Honokiol was also effective against more recent variants of SARS-CoV-2, including Omicron, and it inhibited other human coronaviruses as well. Our study suggests that honokiol is an interesting molecule to be evaluated further in animal studies and, when successful, maybe even in clinical trials to investigate its effect on virus replication and pathogenic (inflammatory) host responses.
MeSH term(s)	Animals ; Humans ; SARS-CoV-2 ; COVID-19 ; Antiviral Agents/pharmacology ; Cell Culture Techniques
Chemical Substances	honokiol (11513CCO0N) ; Antiviral Agents
Language	English
Publishing date	2023-05-04
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2807133-5
ISSN	2165-0497 ; 2165-0497
ISSN (online)	2165-0497
ISSN	2165-0497
DOI	10.1128/spectrum.03273-22
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: SARS-CoV-2-infected human airway epithelial cell cultures uniquely lack interferon and immediate early gene responses caused by other coronaviruses.

Wang, Ying / Thaler, Melissa / Salgado-Benvindo, Clarisse / Ly, Nathan / Leijs, Anouk A / Ninaber, Dennis K / Hansbro, Philip M / Boedijono, Fia / van Hemert, Martijn J / Hiemstra, Pieter S / van der Does, Anne M / Faiz, Alen

Clinical & translational immunology

2024 Volume 13, Issue 4, Page(s) e1503

Abstract: Objectives: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a member of a class of highly pathogenic coronaviruses. The large family of coronaviruses, however, also includes members that cause only mild symptoms, like human coronavirus- ... ...

Abstract	Objectives: Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is a member of a class of highly pathogenic coronaviruses. The large family of coronaviruses, however, also includes members that cause only mild symptoms, like human coronavirus-229E (HCoV-229E) or OC43 (HCoV-OC43). Unravelling how molecular (and cellular) pathophysiology differs between highly and low pathogenic coronaviruses is important for the development of therapeutic strategies. Methods: Here, we analysed the transcriptome of primary human bronchial epithelial cells (PBEC), differentiated at the air-liquid interface (ALI) after infection with SARS-CoV-2, SARS-CoV, Middle East Respiratory Syndrome (MERS)-CoV and HCoV-229E using bulk RNA sequencing. Results: ALI-PBEC were efficiently infected by all viruses, and SARS-CoV, MERS-CoV and HCoV-229E infection resulted in a largely similar transcriptional response. The response to SARS-CoV-2 infection differed markedly as it uniquely lacked the increase in expression of immediate early genes, including Conclusion: Our results demonstrate a previously unknown suppression of a host response gene set by SARS-CoV-2 and confirm a difference in interferon-related gene expression between highly pathogenic and low pathogenic coronaviruses.
Language	English
Publishing date	2024-04-15
Publishing country	Australia
Document type	Journal Article
ZDB-ID	2694482-0
ISSN	2050-0068
ISSN	2050-0068
DOI	10.1002/cti2.1503
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Article ; Online: Impact of Changes in Human Airway Epithelial Cellular Composition and Differentiation on SARS-CoV-2 Infection Biology.

Thaler, Melissa / Wang, Ying / van der Does, Anne M / Faiz, Alen / Ninaber, Dennis K / Ogando, Natacha S / Beckert, Hendrik / Taube, Christian / Salgado-Benvindo, Clarisse / Snijder, Eric J / Bredenbeek, Peter J / Hiemstra, Pieter S / van Hemert, Martijn J

Journal of innate immunity

2023 Volume 15, Issue 1, Page(s) 562–580

Abstract: The consequences of infection with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) can range from asymptomatic to fatal disease. Variations in epithelial susceptibility to SARS-CoV-2 infection depend on the anatomical location from the ... ...

Abstract	The consequences of infection with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) can range from asymptomatic to fatal disease. Variations in epithelial susceptibility to SARS-CoV-2 infection depend on the anatomical location from the proximal to distal respiratory tract. However, the cellular biology underlying these variations is not completely understood. Thus, air-liquid interface cultures of well-differentiated primary human tracheal and bronchial epithelial cells were employed to study the impact of epithelial cellular composition and differentiation on SARS-CoV-2 infection by transcriptional (RNA sequencing) and immunofluorescent analyses. Changes of cellular composition were investigated by varying time of differentiation or by using specific compounds. We found that SARS-CoV-2 primarily infected not only ciliated cells but also goblet cells and transient secretory cells. Viral replication was impacted by differences in cellular composition, which depended on culturing time and anatomical origin. A higher percentage of ciliated cells correlated with a higher viral load. However, DAPT treatment, which increased the number of ciliated cells and reduced goblet cells, decreased viral load, indicating the contribution of goblet cells to infection. Cell entry factors, especially cathepsin L and transmembrane protease serine 2, were also affected by differentiation time. In conclusion, our study demonstrates that viral replication is affected by changes in cellular composition, especially in cells related to the mucociliary system. This could explain in part the variable susceptibility to SARS-CoV-2 infection between individuals and between anatomical locations in the respiratory tract.
MeSH term(s)	Humans ; COVID-19 ; SARS-CoV-2 ; Respiratory System ; Epithelial Cells ; Biology
Language	English
Publishing date	2023-03-25
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2454158-8
ISSN	1662-8128 ; 1662-811X
ISSN (online)	1662-8128
ISSN	1662-811X
DOI	10.1159/000530374
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: R-Propranolol Has Broad-Spectrum Anti-Coronavirus Activity and Suppresses Factors Involved in Pathogenic Angiogenesis

Melissa Thaler / Clarisse Salgado-Benvindo / Anouk Leijs / Ali Tas / Dennis K. Ninaber / Jack L. Arbiser / Eric J. Snijder / Martijn J. van Hemert

International Journal of Molecular Sciences, Vol 24, Iss 4588, p

2023 Volume 4588

Abstract	The SARS-CoV-2 pandemic highlighted the need for broad-spectrum antivirals to increase our preparedness. Patients often require treatment by the time that blocking virus replication is less effective. Therefore, therapy should not only aim to inhibit the virus, but also to suppress pathogenic host responses, e.g., leading to microvascular changes and pulmonary damage. Clinical studies have previously linked SARS-CoV-2 infection to pathogenic intussusceptive angiogenesis in the lungs, involving the upregulation of angiogenic factors such as ANGPTL4. The β-blocker propranolol is used to suppress aberrant ANGPTL4 expression in the treatment of hemangiomas. Therefore, we investigated the effect of propranolol on SARS-CoV-2 infection and the expression of ANGPTL4. SARS-CoV-2 upregulated ANGPTL4 in endothelial and other cells, which could be suppressed with R-propranolol. The compound also inhibited the replication of SARS-CoV-2 in Vero-E6 cells and reduced the viral load by up to ~2 logs in various cell lines and primary human airway epithelial cultures. R-propranolol was as effective as S-propranolol but lacks the latter’s undesired β-blocker activity. R-propranolol also inhibited SARS-CoV and MERS-CoV. It inhibited a post-entry step of the replication cycle, likely via host factors. The broad-spectrum antiviral effect and suppression of factors involved in pathogenic angiogenesis make R-propranolol an interesting molecule to further explore for the treatment of coronavirus infections.
Keywords	propranolol ; R-propranolol ; antiviral ; coronavirus ; SARS-CoV-2 ; angiogenesis ; Biology (General) ; QH301-705.5 ; Chemistry ; QD1-999
Subject code	570
Language	English
Publishing date	2023-02-01T00:00:00Z
Publisher	MDPI AG
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Honokiol inhibits SARS-CoV-2 replication in cell culture

Salgado-Benvindo, Clarisse / Leijs, Anouk A. / Thaler, Melissa / Tas, Ali / Arbiser, Jack L. / Snijder, Eric J. / van Hemert, Martijn J.

bioRxiv

Abstract: SARS-CoV-2 emerged in 2019 and since its global spread has caused the death of over 6 million people. There are currently few antiviral options for treatment of COVID-19. Repurposing of known drugs can be a fast route to obtain molecules that inhibit ... ...

Abstract	SARS-CoV-2 emerged in 2019 and since its global spread has caused the death of over 6 million people. There are currently few antiviral options for treatment of COVID-19. Repurposing of known drugs can be a fast route to obtain molecules that inhibit viral infection and/or modulate pathogenic host responses. Honokiol is a small molecule from Magnolia trees, for which several biological effects have been reported, including anticancer and anti-inflammatory activity. Honokiol has also been shown to inhibit several viruses in cell culture. In this study, we show that honokiol protected Vero E6 cells from SARS-CoV-2-mediated cytopathic effect with an EC50 of 7.8 µM. In viral load reduction assays we observed that honokiol decreased viral RNA copies as well as viral infectious progeny titers. The compound also inhibited SARS-CoV-2 replication in the more relevant A549 cells, expressing ACE2 and TMPRSS2. A time-of-addition assay showed that honokiol inhibited virus replication even when added post infection, suggesting it acts at a post-entry step of the replication cycle. Honokiol was also effective against more recent variants of SARS-CoV-2, including omicron and it inhibited other human coronaviruses as well. Our study suggests that honokiol is an interesting molecule to evaluate in animal studies and clinical trials to investigate its effect on virus replication and pathogenic (inflammatory) host responses.
Keywords	covid19
Language	English
Publishing date	2022-07-27
Publisher	Cold Spring Harbor Laboratory
Document type	Article ; Online
DOI	10.1101/2022.07.26.501656
Database	COVID19

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Article ; Online: Impact of changes in human airway epithelial cellular composition and differentiation on SARS-CoV-2 infection biology

Melissa Thaler / Ying Wang / Anne M. van der Does / Alen Faiz / Dennis K. Ninaber / Natacha S. Ogando / Hendrik Beckert / Christian Taube / Clarisse Salgado-Benvindo / Eric J. Snijder / Peter J. Bredenbeek / Pieter S. Hiemstra / Martijn J. van Hemert

Journal of Innate Immunity (2023)

2023

Abstract	The consequences of infection with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) can range from asymptomatic to fatal disease. Variations in epithelial susceptibility to SARS-CoV-2 infection depend on the anatomical location from the proximal to distal respiratory tract. However, the cellular biology underlying these variations is not completely understood. Thus, air-liquid interface (ALI) cultures of well-differentiated primary human tracheal and bronchial epithelial cells were employed to study the impact of epithelial cellular composition and differentiation on SARS-CoV-2 infection by transcriptional (RNA sequencing) and immunofluorescent analyses. Changes of cellular composition were investigated by varying time of differentiation or by using specific compounds. We found that SARS-CoV-2 primarily infected ciliated cells but also goblet cells and transient secretory cells. Viral replication was impacted by differences in cellular composition, which depended on culturing time and anatomical origin. A higher percentage of ciliated cells correlated with a higher viral load. However, DAPT-treatment, which increased number of ciliated cells and reduced goblet cells, decreased viral load, indicating the contribution of goblet cells to infection. Cell-entry factors, especially cathepsin L and transmembrane protease serine 2, were also affected by differentiation time. In conclusion, our study demonstrates that viral replication is affected by changes in cellular composition, especially in cells related to the mucociliary system. This could explain in part the variable susceptibility to SARS-CoV-2 infection between individuals and between anatomical locations in the respiratory tract.
Keywords	Medicine ; R ; Internal medicine ; RC31-1245
Subject code	570
Language	English
Publishing date	2023-03-01T00:00:00Z
Publisher	Karger Publishers
Document type	Article ; Online
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: Suramin Inhibits SARS-CoV-2 Infection in Cell Culture by Interfering with Early Steps of the Replication Cycle.

Salgado-Benvindo, Clarisse / Thaler, Melissa / Tas, Ali / Ogando, Natacha S / Bredenbeek, Peter J / Ninaber, Dennis K / Wang, Ying / Hiemstra, Pieter S / Snijder, Eric J / van Hemert, Martijn J

Antimicrobial agents and chemotherapy

2020 Volume 64, Issue 8

Abstract: The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic that originated in Wuhan, China, in December 2019 has impacted public health, society, the global economy, and the daily lives of billions of people in an unprecedented manner. ... ...

Abstract	The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic that originated in Wuhan, China, in December 2019 has impacted public health, society, the global economy, and the daily lives of billions of people in an unprecedented manner. There are currently no specific registered antiviral drugs to treat or prevent SARS-CoV-2 infections. Therefore, drug repurposing would be the fastest route to provide at least a temporary solution while better, more specific drugs are being developed. Here, we demonstrate that the antiparasitic drug suramin inhibits SARS-CoV-2 replication, protecting Vero E6 cells with a 50% effective concentration (EC
MeSH term(s)	Animals ; Antiviral Agents/pharmacology ; Betacoronavirus/drug effects ; Cell Line ; Chlorocebus aethiops ; Coronavirus Infections/drug therapy ; Drug Evaluation, Preclinical ; Drug Repositioning ; Humans ; Pandemics ; Pneumonia, Viral/drug therapy ; Suramin/pharmacology ; Vero Cells ; Viral Load/drug effects ; Virus Replication/drug effects
Chemical Substances	Antiviral Agents ; Suramin (6032D45BEM)
Keywords	covid19
Language	English
Publishing date	2020-07-22
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.00900-20
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article ; Online: Epidemiological and genomic investigation of chikungunya virus in Rio de Janeiro state, Brazil, between 2015 and 2018.

Moreira, Filipe Romero Rebello / Menezes, Mariane Talon de / Salgado-Benvindo, Clarisse / Whittaker, Charles / Cox, Victoria / Chandradeva, Nilani / Paula, Hury Hellen Souza de / Martins, André Frederico / Chagas, Raphael Rangel das / Brasil, Rodrigo Decembrino Vargas / Cândido, Darlan da Silva / Herlinger, Alice Laschuk / Ribeiro, Marisa de Oliveira / Arruda, Monica Barcellos / Alvarez, Patricia / Tôrres, Marcelo Calado de Paula / Dorigatti, Ilaria / Brady, Oliver / Voloch, Carolina Moreira /

Tanuri, Amilcar / Iani, Felipe / Souza, William Marciel de / Cardozo, Sergian Vianna / Faria, Nuno Rodrigues / Aguiar, Renato Santana

PLoS neglected tropical diseases

2023 Volume 17, Issue 9, Page(s) e0011536

Abstract: Since 2014, Brazil has experienced an unprecedented epidemic caused by chikungunya virus (CHIKV), with several waves of East-Central-South-African (ECSA) lineage transmission reported across the country. In 2018, Rio de Janeiro state, the third most ... ...

Abstract	Since 2014, Brazil has experienced an unprecedented epidemic caused by chikungunya virus (CHIKV), with several waves of East-Central-South-African (ECSA) lineage transmission reported across the country. In 2018, Rio de Janeiro state, the third most populous state in Brazil, reported 41% of all chikungunya cases in the country. Here we use evolutionary and epidemiological analysis to estimate the timescale of CHIKV-ECSA-American lineage and its epidemiological patterns in Rio de Janeiro. We show that the CHIKV-ECSA outbreak in Rio de Janeiro derived from two distinct clades introduced from the Northeast region in mid-2015 (clade RJ1, n = 63/67 genomes from Rio de Janeiro) and mid-2017 (clade RJ2, n = 4/67). We detected evidence for positive selection in non-structural proteins linked with viral replication in the RJ1 clade (clade-defining: nsP4-A481D) and the RJ2 clade (nsP1-D531G). Finally, we estimate the CHIKV-ECSA's basic reproduction number (R0) to be between 1.2 to 1.6 and show that its instantaneous reproduction number (Rt) displays a strong seasonal pattern with peaks in transmission coinciding with periods of high Aedes aegypti transmission potential. Our results highlight the need for continued genomic and epidemiological surveillance of CHIKV in Brazil, particularly during periods of high ecological suitability, and show that selective pressures underline the emergence and evolution of the large urban CHIKV-ECSA outbreak in Rio de Janeiro.
MeSH term(s)	Humans ; Chikungunya virus/genetics ; Brazil/epidemiology ; Phylogeny ; Chikungunya Fever ; Genomics ; Disease Outbreaks
Language	English
Publishing date	2023-09-28
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2429704-5
ISSN	1935-2735 ; 1935-2735
ISSN (online)	1935-2735
ISSN	1935-2735
DOI	10.1371/journal.pntd.0011536
Database	MEDical Literature Analysis and Retrieval System OnLINE

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Article: Suramin Inhibits SARS-CoV-2 Infection in Cell Culture by Interfering with Early Steps of the Replication Cycle

Salgado-Benvindo, Clarisse / Thaler, Melissa / Tas, Ali / Ogando, Natacha S / Bredenbeek, Peter J / Ninaber, Dennis K / Wang, Ying / Hiemstra, Pieter S / Snijder, Eric J / van Hemert, Martijn J

Abstract	The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic that originated in Wuhan, China, in December 2019 has impacted public health, society, the global economy, and the daily lives of billions of people in an unprecedented manner. There are currently no specific registered antiviral drugs to treat or prevent SARS-CoV-2 infections. Therefore, drug repurposing would be the fastest route to provide at least a temporary solution while better, more specific drugs are being developed. Here, we demonstrate that the antiparasitic drug suramin inhibits SARS-CoV-2 replication, protecting Vero E6 cells with a 50% effective concentration (EC50) of â¼20 µM, which is well below the maximum attainable level in human serum. Suramin also decreased the viral load by 2 to 3 logs when Vero E6 cells or cells of a human lung epithelial cell line (Calu-3 2B4 [referred to here as "Calu-3"]) were treated. Time-of-addition and plaque reduction assays performed on Vero E6 cells showed that suramin acts on early steps of the replication cycle, possibly preventing binding or entry of the virus. In a primary human airway epithelial cell culture model, suramin also inhibited the progression of infection. The results of our preclinical study warrant further investigation and suggest that it is worth evaluating whether suramin provides any benefit for COVID-19 patients, which obviously requires safety studies and well-designed, properly controlled randomized clinical trials.
Keywords	covid19
Publisher	WHO
Document type	Article
Note	WHO #Covidence: #574704
Database	COVID19

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