Amazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis

Detalhes bibliográficos
Autor(a) principal: Rath, Carolina Torturella
Data de Publicação: 2019
Outros Autores: Schnellrath, Laila Castro, Damaso, Clarissa R, Arruda, Luciana Barros de, Vasconcelos, Pedro Fernando da Costa, Gomes, Claudia Maria de Castro, Laurenti, Márcia Dalastra, Silva, Teresa Cristina Calegari, Vivarini, Áislan de Carvalho, Fasel, Nicolas, Pereira, Renata Meirelles Santos, Lopes, Ulisses Gazos
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Digital do Instituto Evandro Chagas (Patuá)
Texto Completo: https://patua.iec.gov.br/handle/iec/3819
Resumo: BACKGROUND: Leishmania parasites are transmitted to vertebrate hosts by phlebotomine sandflies and, in humans, may cause tegumentary or visceral leishmaniasis. The role of PKR (dsRNA activated kinase) and Toll-like receptor 3 (TLR3) activation in the control of Leishmania infection highlights the importance of the engagement of RNA sensors, which are usually involved in the antiviral cell response, in the fate of parasitism by Leishmania. We tested the hypothesis that Phlebovirus, a subgroup of the Bunyaviridae, transmitted by sandflies, would interfere with Leishmania infection. METHODOLOGY/PRINCIPAL FINDINGS: We tested two Phlebovirus isolates, Icoaraci and Pacui, from the rodents Nectomys sp. and Oryzomys sp., respectively, both natural sylvatic reservoir of Leishmania (Leishmania) amazonensis from the Amazon region. Phlebovirus coinfection with L. (L.) amazonensis in murine macrophages led to increased intracellular growth of L. (L.) amazonensis. Further studies with Icoaraci coinfection revealed the requirement of the PKR/IFN1 axis on the exacerbation of the parasite infection. L. (L.) amazonensis and Phlebovirus coinfection potentiated PKR activation and synergistically induced the expression of IFNβ and IL-10. Importantly, in vivo coinfection of C57BL/6 mice corroborated the in vitro data. The exacerbation effect of RNA virus on parasite infection may be specific because coinfection with dengue virus (DENV2) exerted the opposite effect on parasite load. CONCLUSIONS: Altogether, our data suggest that coinfections with specific RNA viruses shared by vectors or reservoirs of Leishmania may enhance and sustain the activation of host cellular RNA sensors, resulting in aggravation of the parasite infection. The present work highlights new perspectives for the investigation of antiviral pathways as important modulators of protozoan infections.
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spelling Rath, Carolina TorturellaSchnellrath, Laila CastroDamaso, Clarissa RArruda, Luciana Barros deVasconcelos, Pedro Fernando da CostaGomes, Claudia Maria de CastroLaurenti, Márcia DalastraSilva, Teresa Cristina CalegariVivarini, Áislan de CarvalhoFasel, NicolasPereira, Renata Meirelles SantosLopes, Ulisses Gazos2019-08-09T11:53:43Z2019-08-09T11:53:43Z2019RATH, Carolina Torturella et al. Amazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis. PLoS Neglected Tropical Diseases, v. 13, n. 6, e0007500, June 2019. DOI: https://doi.org/10.1371/journal.pntd.0007500.1935-2735https://patua.iec.gov.br/handle/iec/381910.1371/journal.pntd.0007500BACKGROUND: Leishmania parasites are transmitted to vertebrate hosts by phlebotomine sandflies and, in humans, may cause tegumentary or visceral leishmaniasis. The role of PKR (dsRNA activated kinase) and Toll-like receptor 3 (TLR3) activation in the control of Leishmania infection highlights the importance of the engagement of RNA sensors, which are usually involved in the antiviral cell response, in the fate of parasitism by Leishmania. We tested the hypothesis that Phlebovirus, a subgroup of the Bunyaviridae, transmitted by sandflies, would interfere with Leishmania infection. METHODOLOGY/PRINCIPAL FINDINGS: We tested two Phlebovirus isolates, Icoaraci and Pacui, from the rodents Nectomys sp. and Oryzomys sp., respectively, both natural sylvatic reservoir of Leishmania (Leishmania) amazonensis from the Amazon region. Phlebovirus coinfection with L. (L.) amazonensis in murine macrophages led to increased intracellular growth of L. (L.) amazonensis. Further studies with Icoaraci coinfection revealed the requirement of the PKR/IFN1 axis on the exacerbation of the parasite infection. L. (L.) amazonensis and Phlebovirus coinfection potentiated PKR activation and synergistically induced the expression of IFNβ and IL-10. Importantly, in vivo coinfection of C57BL/6 mice corroborated the in vitro data. The exacerbation effect of RNA virus on parasite infection may be specific because coinfection with dengue virus (DENV2) exerted the opposite effect on parasite load. CONCLUSIONS: Altogether, our data suggest that coinfections with specific RNA viruses shared by vectors or reservoirs of Leishmania may enhance and sustain the activation of host cellular RNA sensors, resulting in aggravation of the parasite infection. The present work highlights new perspectives for the investigation of antiviral pathways as important modulators of protozoan infections.UGL- National Council for Scientific and Technological Development (CNPq)- 400063/2017-4. Fundac¸ão Carlos Chagas Filho de Amparo a Pesquisa do Estado do Rio de Janeiro. CNE-09/ 2016 NF- National Council for Scientific and Technological Development. IZRJZ3_164176/1 and FNS grant No 310030_173180.Federal University of Rio de Janeiro. Institute of Biophysics Carlos Chagas Filho. Laboratory of Molecular Parasitology. Rio de Janeiro, RJ, Brazil.Federal University of Rio de Janeiro. Institute of Biophysics Carlos Chagas Filho. Laboratory of Molecular Biology of Virus. Rio de Janeiro, RJ, Brazil.Federal University of Rio de Janeiro. Institute of Biophysics Carlos Chagas Filho. Laboratory of Molecular Biology of Virus. Rio de Janeiro, RJ, Brazil.Universidade Federal do Rio de Janeiro. Instituto de Microbiologia Prof. Paulo de Góes. Departamento de Virologia. Laboratório de Genética e Imunologia das Infecções Virais. Rio de Janeiro, RJ, Brazil.Ministério da Saúde. Secretaria de Vigilância em Saúde. Instituto Evandro Chagas. Ananindeua, PA, Brasil.University of São Paulo. Medical School. Department of Pathology. São Paulo, SP, Brazil.University of São Paulo. Medical School. Department of Pathology. São Paulo, SP, Brazil.Federal University of Rio de Janeiro. Institute of Biophysics Carlos Chagas Filho. Laboratory of Molecular Parasitology. Rio de Janeiro, RJ, Brazil.Federal University of Rio de Janeiro. Institute of Biophysics Carlos Chagas Filho. Laboratory of Molecular Parasitology. Rio de Janeiro, RJ, Brazil.University of Lausanne. Department of Biochemistry. Switzerland.Federal University of Rio de Janeiro. Institute of Microbiology Paulo de Góes. Rio de Janeiro, RJ, Brazil.Federal University of Rio de Janeiro. Institute of Biophysics Carlos Chagas Filho. Laboratory of Molecular Parasitology. Rio de Janeiro, RJ, Brazil.engPublic Library of ScienceAmazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axisinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleArbovirus / isolamento & purificaçãoPhlebovirus / isolamento & purificaçãoLeishmania / isolamento & purificaçãoCoinfecção / virologiaInfecções por Protozoários / transmissãoinfo:eu-repo/semantics/openAccessreponame:Repositório Digital do Instituto Evandro Chagas (Patuá)instname:Instituto Evandro Chagas (IEC)instacron:IECORIGINALAmazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis.pdfAmazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis.pdfapplication/pdf2906493https://patua.iec.gov.br/bitstreams/d61e86a2-79d1-4993-bd6e-0a02a4c55e65/download1238f6fbf58e4f38a0f35227c10ef367MD51LICENSElicense.txtlicense.txttext/plain; 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dc.title.pt_BR.fl_str_mv Amazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis
title Amazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis
spellingShingle Amazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis
Rath, Carolina Torturella
Arbovirus / isolamento & purificação
Phlebovirus / isolamento & purificação
Leishmania / isolamento & purificação
Coinfecção / virologia
Infecções por Protozoários / transmissão
title_short Amazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis
title_full Amazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis
title_fullStr Amazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis
title_full_unstemmed Amazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis
title_sort Amazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis
author Rath, Carolina Torturella
author_facet Rath, Carolina Torturella
Schnellrath, Laila Castro
Damaso, Clarissa R
Arruda, Luciana Barros de
Vasconcelos, Pedro Fernando da Costa
Gomes, Claudia Maria de Castro
Laurenti, Márcia Dalastra
Silva, Teresa Cristina Calegari
Vivarini, Áislan de Carvalho
Fasel, Nicolas
Pereira, Renata Meirelles Santos
Lopes, Ulisses Gazos
author_role author
author2 Schnellrath, Laila Castro
Damaso, Clarissa R
Arruda, Luciana Barros de
Vasconcelos, Pedro Fernando da Costa
Gomes, Claudia Maria de Castro
Laurenti, Márcia Dalastra
Silva, Teresa Cristina Calegari
Vivarini, Áislan de Carvalho
Fasel, Nicolas
Pereira, Renata Meirelles Santos
Lopes, Ulisses Gazos
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Rath, Carolina Torturella
Schnellrath, Laila Castro
Damaso, Clarissa R
Arruda, Luciana Barros de
Vasconcelos, Pedro Fernando da Costa
Gomes, Claudia Maria de Castro
Laurenti, Márcia Dalastra
Silva, Teresa Cristina Calegari
Vivarini, Áislan de Carvalho
Fasel, Nicolas
Pereira, Renata Meirelles Santos
Lopes, Ulisses Gazos
dc.subject.decsPrimary.pt_BR.fl_str_mv Arbovirus / isolamento & purificação
Phlebovirus / isolamento & purificação
Leishmania / isolamento & purificação
Coinfecção / virologia
Infecções por Protozoários / transmissão
topic Arbovirus / isolamento & purificação
Phlebovirus / isolamento & purificação
Leishmania / isolamento & purificação
Coinfecção / virologia
Infecções por Protozoários / transmissão
description BACKGROUND: Leishmania parasites are transmitted to vertebrate hosts by phlebotomine sandflies and, in humans, may cause tegumentary or visceral leishmaniasis. The role of PKR (dsRNA activated kinase) and Toll-like receptor 3 (TLR3) activation in the control of Leishmania infection highlights the importance of the engagement of RNA sensors, which are usually involved in the antiviral cell response, in the fate of parasitism by Leishmania. We tested the hypothesis that Phlebovirus, a subgroup of the Bunyaviridae, transmitted by sandflies, would interfere with Leishmania infection. METHODOLOGY/PRINCIPAL FINDINGS: We tested two Phlebovirus isolates, Icoaraci and Pacui, from the rodents Nectomys sp. and Oryzomys sp., respectively, both natural sylvatic reservoir of Leishmania (Leishmania) amazonensis from the Amazon region. Phlebovirus coinfection with L. (L.) amazonensis in murine macrophages led to increased intracellular growth of L. (L.) amazonensis. Further studies with Icoaraci coinfection revealed the requirement of the PKR/IFN1 axis on the exacerbation of the parasite infection. L. (L.) amazonensis and Phlebovirus coinfection potentiated PKR activation and synergistically induced the expression of IFNβ and IL-10. Importantly, in vivo coinfection of C57BL/6 mice corroborated the in vitro data. The exacerbation effect of RNA virus on parasite infection may be specific because coinfection with dengue virus (DENV2) exerted the opposite effect on parasite load. CONCLUSIONS: Altogether, our data suggest that coinfections with specific RNA viruses shared by vectors or reservoirs of Leishmania may enhance and sustain the activation of host cellular RNA sensors, resulting in aggravation of the parasite infection. The present work highlights new perspectives for the investigation of antiviral pathways as important modulators of protozoan infections.
publishDate 2019
dc.date.accessioned.fl_str_mv 2019-08-09T11:53:43Z
dc.date.available.fl_str_mv 2019-08-09T11:53:43Z
dc.date.issued.fl_str_mv 2019
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
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status_str publishedVersion
dc.identifier.citation.fl_str_mv RATH, Carolina Torturella et al. Amazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis. PLoS Neglected Tropical Diseases, v. 13, n. 6, e0007500, June 2019. DOI: https://doi.org/10.1371/journal.pntd.0007500.
dc.identifier.uri.fl_str_mv https://patua.iec.gov.br/handle/iec/3819
dc.identifier.issn.-.fl_str_mv 1935-2735
dc.identifier.doi.-.fl_str_mv 10.1371/journal.pntd.0007500
identifier_str_mv RATH, Carolina Torturella et al. Amazonian Phlebovirus (Bunyaviridae) potentiates the infection of Leishmania (Leishmania) amazonensis: role of the PKR/IFN1/IL-10 axis. PLoS Neglected Tropical Diseases, v. 13, n. 6, e0007500, June 2019. DOI: https://doi.org/10.1371/journal.pntd.0007500.
1935-2735
10.1371/journal.pntd.0007500
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