Neutrophil Extracellular Traps Effectively Control Acute Chikungunya Virus Infection
The Chikungunya virus (CHIKV) is a re-emerging arbovirus, in which its infection causes a febrile illness also commonly associated with severe joint pain and myalgia. Although the immune response to CHIKV has been studied, a better understanding of the virus-host interaction mechanisms may lead to m...
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| Published in | Frontiers in immunology Vol. 10; p. 3108 |
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| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
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31.01.2020
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| Abstract | The Chikungunya virus (CHIKV) is a re-emerging arbovirus, in which its infection causes a febrile illness also commonly associated with severe joint pain and myalgia. Although the immune response to CHIKV has been studied, a better understanding of the virus-host interaction mechanisms may lead to more effective therapeutic interventions. In this context, neutrophil extracellular traps (NETs) have been described as a key mediator involved in the control of many pathogens, including several bacteria and viruses, but no reports of this important protective mechanism were documented during CHIKV infection. Here we demonstrate that the experimental infection of mouse-isolated neutrophils with CHIKV resulted in NETosis (NETs release) through a mechanism dependent on TLR7 activation and reactive oxygen species generation.
, mouse-isolated neutrophils stimulated with phorbol 12-myristate 13-acetate release NETs that once incubated with CHIKV, resulting in further virus capture and neutralization.
, NETs inhibition by the treatment of the mice with DNase resulted in the enhanced susceptibility of IFNAR
mice to CHIKV experimental acute infection. Lastly, by accessing the levels of MPO-DNA complex on the acutely CHIKV-infected patients, we found a correlation between the levels of NETs and the viral load in the blood, suggesting that NETs are also released in natural human infection cases. Altogether our findings characterize NETosis as a contributing natural process to control CHIKV acute infection, presenting an antiviral effect that helps to control systemic virus levels. |
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| AbstractList | The Chikungunya virus (CHIKV) is a re-emerging arbovirus, in which its infection causes a febrile illness also commonly associated with severe joint pain and myalgia. Although the immune response to CHIKV has been studied, a better understanding of the virus-host interaction mechanisms may lead to more effective therapeutic interventions. In this context, neutrophil extracellular traps (NETs) have been described as a key mediator involved in the control of many pathogens, including several bacteria and viruses, but no reports of this important protective mechanism were documented during CHIKV infection. Here we demonstrate that the experimental infection of mouse-isolated neutrophils with CHIKV resulted in NETosis (NETs release) through a mechanism dependent on TLR7 activation and reactive oxygen species generation.
, mouse-isolated neutrophils stimulated with phorbol 12-myristate 13-acetate release NETs that once incubated with CHIKV, resulting in further virus capture and neutralization.
, NETs inhibition by the treatment of the mice with DNase resulted in the enhanced susceptibility of IFNAR
mice to CHIKV experimental acute infection. Lastly, by accessing the levels of MPO-DNA complex on the acutely CHIKV-infected patients, we found a correlation between the levels of NETs and the viral load in the blood, suggesting that NETs are also released in natural human infection cases. Altogether our findings characterize NETosis as a contributing natural process to control CHIKV acute infection, presenting an antiviral effect that helps to control systemic virus levels. The Chikungunya virus (CHIKV) is a re-emerging arbovirus, in which its infection causes a febrile illness also commonly associated with severe joint pain and myalgia. Although the immune response to CHIKV has been studied, a better understanding of the virus-host interaction mechanisms may lead to more effective therapeutic interventions. In this context, neutrophil extracellular traps (NETs) have been described as a key mediator involved in the control of many pathogens, including several bacteria and viruses, but no reports of this important protective mechanism were documented during CHIKV infection. Here we demonstrate that the experimental infection of mouse-isolated neutrophils with CHIKV resulted in NETosis (NETs release) through a mechanism dependent on TLR7 activation and reactive oxygen species generation. In vitro, mouse-isolated neutrophils stimulated with phorbol 12-myristate 13-acetate release NETs that once incubated with CHIKV, resulting in further virus capture and neutralization. In vivo, NETs inhibition by the treatment of the mice with DNase resulted in the enhanced susceptibility of IFNAR−/− mice to CHIKV experimental acute infection. Lastly, by accessing the levels of MPO-DNA complex on the acutely CHIKV-infected patients, we found a correlation between the levels of NETs and the viral load in the blood, suggesting that NETs are also released in natural human infection cases. Altogether our findings characterize NETosis as a contributing natural process to control CHIKV acute infection, presenting an antiviral effect that helps to control systemic virus levels. The Chikungunya virus (CHIKV) is a re-emerging arbovirus, in which its infection causes a febrile illness also commonly associated with severe joint pain and myalgia. Although the immune response to CHIKV has been studied, a better understanding of the virus-host interaction mechanisms may lead to more effective therapeutic interventions. In this context, neutrophil extracellular traps (NETs) have been described as a key mediator involved in the control of many pathogens, including several bacteria and viruses, but no reports of this important protective mechanism were documented during CHIKV infection. Here we demonstrate that the experimental infection of mouse-isolated neutrophils with CHIKV resulted in NETosis (NETs release) through a mechanism dependent on TLR7 activation and reactive oxygen species generation. In vitro , mouse-isolated neutrophils stimulated with phorbol 12-myristate 13-acetate release NETs that once incubated with CHIKV, resulting in further virus capture and neutralization. In vivo , NETs inhibition by the treatment of the mice with DNase resulted in the enhanced susceptibility of IFNAR −/− mice to CHIKV experimental acute infection. Lastly, by accessing the levels of MPO-DNA complex on the acutely CHIKV-infected patients, we found a correlation between the levels of NETs and the viral load in the blood, suggesting that NETs are also released in natural human infection cases. Altogether our findings characterize NETosis as a contributing natural process to control CHIKV acute infection, presenting an antiviral effect that helps to control systemic virus levels. |
| Author | Franca, Rafael F O Fumagalli, Marcilio J Toller-Kawahisa, Juliana E Hiroki, Carlos H Fonseca, Bendito A L D Colon, David F Figueiredo, Luiz T M Cunha, Fernando Q |
| AuthorAffiliation | 4 Department of Virology and Experimental Therapy, Institute Aggeu Magalhaes, Oswaldo Cruz Foundation , Recife , Brazil 3 Virology Research Center, School of Medicine of Ribeirao Preto, University of São Paulo , Ribeirao Preto , Brazil 1 Department of Pharmacology, School of Medicine of Ribeirao Preto, University of São Paulo , Ribeirao Preto , Brazil 2 Department of Biochemistry and Immunology, School of Medicine of Ribeirao Preto, University of São Paulo , Ribeirao Preto , Brazil |
| AuthorAffiliation_xml | – name: 4 Department of Virology and Experimental Therapy, Institute Aggeu Magalhaes, Oswaldo Cruz Foundation , Recife , Brazil – name: 3 Virology Research Center, School of Medicine of Ribeirao Preto, University of São Paulo , Ribeirao Preto , Brazil – name: 2 Department of Biochemistry and Immunology, School of Medicine of Ribeirao Preto, University of São Paulo , Ribeirao Preto , Brazil – name: 1 Department of Pharmacology, School of Medicine of Ribeirao Preto, University of São Paulo , Ribeirao Preto , Brazil |
| Author_xml | – sequence: 1 givenname: Carlos H surname: Hiroki fullname: Hiroki, Carlos H organization: Department of Pharmacology, School of Medicine of Ribeirao Preto, University of São Paulo, Ribeirao Preto, Brazil – sequence: 2 givenname: Juliana E surname: Toller-Kawahisa fullname: Toller-Kawahisa, Juliana E organization: Department of Pharmacology, School of Medicine of Ribeirao Preto, University of São Paulo, Ribeirao Preto, Brazil – sequence: 3 givenname: Marcilio J surname: Fumagalli fullname: Fumagalli, Marcilio J organization: Department of Biochemistry and Immunology, School of Medicine of Ribeirao Preto, University of São Paulo, Ribeirao Preto, Brazil – sequence: 4 givenname: David F surname: Colon fullname: Colon, David F organization: Department of Biochemistry and Immunology, School of Medicine of Ribeirao Preto, University of São Paulo, Ribeirao Preto, Brazil – sequence: 5 givenname: Luiz T M surname: Figueiredo fullname: Figueiredo, Luiz T M organization: Virology Research Center, School of Medicine of Ribeirao Preto, University of São Paulo, Ribeirao Preto, Brazil – sequence: 6 givenname: Bendito A L D surname: Fonseca fullname: Fonseca, Bendito A L D organization: Virology Research Center, School of Medicine of Ribeirao Preto, University of São Paulo, Ribeirao Preto, Brazil – sequence: 7 givenname: Rafael F O surname: Franca fullname: Franca, Rafael F O organization: Department of Virology and Experimental Therapy, Institute Aggeu Magalhaes, Oswaldo Cruz Foundation, Recife, Brazil – sequence: 8 givenname: Fernando Q surname: Cunha fullname: Cunha, Fernando Q organization: Department of Pharmacology, School of Medicine of Ribeirao Preto, University of São Paulo, Ribeirao Preto, Brazil |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32082301$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright © 2020 Hiroki, Toller-Kawahisa, Fumagalli, Colon, Figueiredo, Fonseca, Franca and Cunha. Copyright © 2020 Hiroki, Toller-Kawahisa, Fumagalli, Colon, Figueiredo, Fonseca, Franca and Cunha. 2020 Hiroki, Toller-Kawahisa, Fumagalli, Colon, Figueiredo, Fonseca, Franca and Cunha |
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| Keywords | Chikungunya NETs viral infection neutrophils innate response |
| Language | English |
| License | Copyright © 2020 Hiroki, Toller-Kawahisa, Fumagalli, Colon, Figueiredo, Fonseca, Franca and Cunha. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by: Lisa F. P. Ng, Singapore Immunology Network (A*STAR), Singapore This article was submitted to Viral Immunology, a section of the journal Frontiers in Immunology Reviewed by: E. Ashley Moseman, Duke University School of Medicine, United States; Pierre Roques, CEA Saclay, France |
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| Title | Neutrophil Extracellular Traps Effectively Control Acute Chikungunya Virus Infection |
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