Inhibition by Marine Algae of Chikungunya Virus Isolated From Patients in a Recent Disease Outbreak in Rio de Janeiro

Detalhes bibliográficos
Autor(a) principal: Cirne-Santos, Claudio Cesar
Data de Publicação: 2019
Outros Autores: Barros, Caroline de Souza, Nogueira, Caio Cesar Richter, Azevedo, Renata Campos, Yamamoto, Kristie Aimi, Meira, Guilherme Louzada Silva, Vasconcelos, Zilton Farias Meira de, Ratcliffe, Norman A., Teixeira, Valéria Laneuville, Schmidt-Chanasit, Jonas, Ferreira, Davis Fernandes, Paixão, Izabel Christina Nunes de Palmer
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da FIOCRUZ (ARCA)
Texto Completo: https://www.arca.fiocruz.br/handle/icict/41511
Resumo: The authors would like to acknowledge for the technical support of Thereza Elizabeth P. P. Garcia.
id CRUZ_7eae744f3cf58b2766412934c498c1bd
oai_identifier_str oai:www.arca.fiocruz.br:icict/41511
network_acronym_str CRUZ
network_name_str Repositório Institucional da FIOCRUZ (ARCA)
repository_id_str 2135
spelling Cirne-Santos, Claudio CesarBarros, Caroline de SouzaNogueira, Caio Cesar RichterAzevedo, Renata CamposYamamoto, Kristie AimiMeira, Guilherme Louzada SilvaVasconcelos, Zilton Farias Meira deRatcliffe, Norman A.Teixeira, Valéria LaneuvilleSchmidt-Chanasit, JonasFerreira, Davis FernandesPaixão, Izabel Christina Nunes de Palmer2020-06-03T19:54:22Z2020-06-03T19:54:22Z2019Cirne-Santos CC, Barros CS, Nogueira CCR, et al. Inhibition by Marine Algae of Chikungunya Virus Isolated From Patients in a Recent Disease Outbreak in Rio de Janeiro. Front Microbiol. 2019;10:2426. Published 2019 Oct 24. doi:10.3389/fmicb.2019.024261664-302Xhttps://www.arca.fiocruz.br/handle/icict/4151110.3389/fmicb.2019.02426The authors would like to acknowledge for the technical support of Thereza Elizabeth P. P. Garcia.A infecção pelo vírus Chikungunya (CHIKV) é uma das doenças reemergentes mais desafiadoras causadas por um vírus e, sem tratamento antiviral específico, tornou-se um grande problema de saúde pública. Nesta investigação, foram coletadas 25 amostras de sangue de pacientes com sintomas característicos de CHIKV e submetidas a um protocolo de isolamento de vírus, que detectou 3 isolados de CHIKV. Essas amostras foram avaliadas por sequenciamento para caracterização das cepas e qualquer homologia com vírus que circulam no Brasil durante um surto recente. Estes vírus foram utilizados para o desenvolvimento de ensaios antivirais. Posteriormente, foram estudados os efeitos inibitórios dos extratos de algas sobre a replicação do CHIKV. As espécies marinhas de algas testadas foram Bryothamnion triquetrum, Caulerpa racemosa, Laurencia dendroidea, Osmundaria obtusiloba, Ulva fasciata e Kappaphycus alvarezii, encontradas em diferentes países, incluindo o Brasil. Os resultados revelaram altos níveis de inibição do CHIKV, incluindo extratos de O. obtusiloba com valores de inibição de 1,25 μg / mL e um índice de seletividade de 420. A inibição viral dependeu do tempo de adição do extrato de O. obtusiloba às células infectadas, com a inibição ideal ocorrendo até 16 horas após a infecção. Avaliações de neurônios com O. obtusiloba foram realizadas e demonstraram baixa toxicidade, e em neurônios infectados observamos alta atividade inibitória de maneira dose-dependente. Estes resultados indicam que os extratos de algas podem ser novos candidatos promissores para o desenvolvimento de agentes terapêuticos contra infecções por CHIKV.Chikungunya virus (CHIKV) infection is one of the most challenging re-emergent diseases caused by a virus, and with no specific antiviral treatment it has now become a major public health concern. In this investigation, 25 blood samples were collected from patients with characteristic CHIKV symptoms and submitted to a virus isolation protocol, which detected 3 CHIKV isolates. These samples were evaluated by sequencing for the characterization of the strains and any homology to viruses circulating in Brazil during a recent outbreak. These viruses were used for the development of antiviral assays. Subsequently, the inhibitory effects of seaweed extracts on CHIKV replication were studied. The marine species of algae tested were Bryothamnion triquetrum, Caulerpa racemosa, Laurencia dendroidea, Osmundaria obtusiloba, Ulva fasciata, and Kappaphycus alvarezii, all of which are found in different countries including Brazil. The results revealed high levels of CHIKV inhibition, including extracts of O. obtusiloba with inhibition values of 1.25 μg/mL and a selectivity index of 420. Viral inhibition was dependent on the time of addition of extract of O. obtusiloba to the infected cells, with the optimal inhibition occurring up to 16 h after infection. Neuron evaluations with O. obtusiloba were performed and demonstrated low toxicity, and in infected neurons we observed high inhibitory activity in a dose-dependent manner. These results indicate that the algal extracts may be promising novel candidates for the development of therapeutic agents against CHIKV infections.The authors are grateful to CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for financial support and for Productivity Fellowships to IP and VT (443930/2014-7 and 304070/2014-9). IP and VT (E-26/201.442/2014) also thank the FAPERJ (Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro) for the Cientista do Nosso Estado Fellowship. CC-S thanks CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for the Postdoc fellowship and CB thanks FAPERJ for the Postdoc fellowship (E-26/201.344/2016). Support also came from the postgraduate program in sciences and biotechnology of UFF (PPBI-UFF).Universidade Federal Fluminense. Programa de Pós-graduação em Ciências e Biotecnologia. Instituto de Biologia. Laboratório de Virologia Molecular e Biotecnologia Marinha. Departamento de Biologia Celular e Molecular. Nterói, RJ. Brasil./ Universidade Salgado de Oliveira. Curso de Farmácia. Departamento de Ensino. Niterói, RJ. Brasil.Universidade Federal Fluminense. Programa de Pós-graduação em Ciências e Biotecnologia. Instituto de Biologia. Laboratório de Virologia Molecular e Biotecnologia Marinha. Departamento de Biologia Celular e Molecular. Niterói, RJ. Brasil.Universidade Federal Fluminense. Programa de Pós-graduação em Ciências e Biotecnologia. Instituto de Biologia. Laboratório de Virologia Molecular e Biotecnologia Marinha. Departamento de Biologia Celular e Molecular. Nterói, RJ. Brasil. / Universidade Federal Fluminense. Instituto de Biologia. Laboratório de Produtos Naturais de Algas Marinhas, Departamento de Biologia Marinha. Niterói, RJ. Brasil.Universidade Federal do Rio de Janeiro. Instituto de Microbiologia Paulo de Góes. Departamento de Virologia. Rio de Janeiro, RJ. Brasil.Universidade Federal do Rio de Janeiro. Instituto de Microbiologia Paulo de Góes. Departamento de Virologia. Rio de Janeiro, RJ. Brasil.Universidade Federal do Rio de Janeiro. Instituto de Microbiologia Paulo de Góes. Departamento de Virologia. Rio de Janeiro, RJ. Brasil.Fundação Oswaldo Cruz. Instituto Nacional de Saúde da Mulher, da Criança e do Adolescente Fernandes Figueira. Rio de Janeiro, RJ. Brasil.Swansea University, College of Science, Department of Biosciences, Swansea, United Kingdom.Universidade Federal Fluminense. Programa de Pós-graduação em Ciências e Biotecnologia. Instituto de Biologia. Laboratório de Virologia Molecular e Biotecnologia Marinha. Departamento de Biologia Celular e Molecular. Niterói, RJ. Brasil. / Universidade Federal do Estado do Rio de Janeiro. Programa de Pós-graduação em Biodiversidade Neotropical. Instituto de Biociencias. Laboratório de Biologia e Taxonomia de Algas. Rio de Janeiro, RJ. Brasil.Bernhard Nocht Institute for Tropical Medicine. WHO Collaborating Centre for Arbovirus and Haemorrhagic Fever Reference and Research .Hamburg, Germany.Universidade Federal do Rio de Janeiro. Instituto de Microbiologia Paulo de Góes. Departamento de Virologia. Rio de Janeiro, RJ. Brasil./ North Carolina State University. Department of Molecular and Structural Biochemistry, Raleigh, NC. United States.Universidade Federal Fluminense. Programa de Pós-graduação em Ciências e Biotecnologia. Instituto de Biologia. Laboratório de Virologia Molecular e Biotecnologia Marinha. Departamento de Biologia Celular e Molecular. Nterói, RJ. Brasil.engFrontiers MediaAntiviralArbovírusChikungunyaExtratos brutosAlgas marinhas.AntiviralArbovirusChikungunyaCrude extractsSeaweed.Inhibition by Marine Algae of Chikungunya Virus Isolated From Patients in a Recent Disease Outbreak in Rio de Janeiroinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleinfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da FIOCRUZ (ARCA)instname:Fundação Oswaldo Cruz (FIOCRUZ)instacron:FIOCRUZLICENSElicense.txtlicense.txttext/plain; charset=utf-82991https://www.arca.fiocruz.br/bitstream/icict/41511/1/license.txt5a560609d32a3863062d77ff32785d58MD51ORIGINALIFF - fmicb-10-02426.pdfIFF - fmicb-10-02426.pdfapplication/pdf3992253https://www.arca.fiocruz.br/bitstream/icict/41511/2/IFF%20-%20fmicb-10-02426.pdf4e7c890a78900e6475c1f5487738e411MD52TEXTIFF - fmicb-10-02426.pdf.txtIFF - fmicb-10-02426.pdf.txtExtracted texttext/plain55057https://www.arca.fiocruz.br/bitstream/icict/41511/3/IFF%20-%20fmicb-10-02426.pdf.txt086ac7cb6d57fb322a71d584ef9dd6fdMD53icict/415112020-06-23 14:28:24.572oai:www.arca.fiocruz.br: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ório InstitucionalPUBhttps://www.arca.fiocruz.br/oai/requestrepositorio.arca@fiocruz.bropendoar:21352020-06-23T17:28:24Repositório Institucional da FIOCRUZ (ARCA) - Fundação Oswaldo Cruz (FIOCRUZ)false
dc.title.pt_BR.fl_str_mv Inhibition by Marine Algae of Chikungunya Virus Isolated From Patients in a Recent Disease Outbreak in Rio de Janeiro
title Inhibition by Marine Algae of Chikungunya Virus Isolated From Patients in a Recent Disease Outbreak in Rio de Janeiro
spellingShingle Inhibition by Marine Algae of Chikungunya Virus Isolated From Patients in a Recent Disease Outbreak in Rio de Janeiro
Cirne-Santos, Claudio Cesar
Antiviral
Arbovírus
Chikungunya
Extratos brutos
Algas marinhas.
Antiviral
Arbovirus
Chikungunya
Crude extracts
Seaweed.
title_short Inhibition by Marine Algae of Chikungunya Virus Isolated From Patients in a Recent Disease Outbreak in Rio de Janeiro
title_full Inhibition by Marine Algae of Chikungunya Virus Isolated From Patients in a Recent Disease Outbreak in Rio de Janeiro
title_fullStr Inhibition by Marine Algae of Chikungunya Virus Isolated From Patients in a Recent Disease Outbreak in Rio de Janeiro
title_full_unstemmed Inhibition by Marine Algae of Chikungunya Virus Isolated From Patients in a Recent Disease Outbreak in Rio de Janeiro
title_sort Inhibition by Marine Algae of Chikungunya Virus Isolated From Patients in a Recent Disease Outbreak in Rio de Janeiro
author Cirne-Santos, Claudio Cesar
author_facet Cirne-Santos, Claudio Cesar
Barros, Caroline de Souza
Nogueira, Caio Cesar Richter
Azevedo, Renata Campos
Yamamoto, Kristie Aimi
Meira, Guilherme Louzada Silva
Vasconcelos, Zilton Farias Meira de
Ratcliffe, Norman A.
Teixeira, Valéria Laneuville
Schmidt-Chanasit, Jonas
Ferreira, Davis Fernandes
Paixão, Izabel Christina Nunes de Palmer
author_role author
author2 Barros, Caroline de Souza
Nogueira, Caio Cesar Richter
Azevedo, Renata Campos
Yamamoto, Kristie Aimi
Meira, Guilherme Louzada Silva
Vasconcelos, Zilton Farias Meira de
Ratcliffe, Norman A.
Teixeira, Valéria Laneuville
Schmidt-Chanasit, Jonas
Ferreira, Davis Fernandes
Paixão, Izabel Christina Nunes de Palmer
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Cirne-Santos, Claudio Cesar
Barros, Caroline de Souza
Nogueira, Caio Cesar Richter
Azevedo, Renata Campos
Yamamoto, Kristie Aimi
Meira, Guilherme Louzada Silva
Vasconcelos, Zilton Farias Meira de
Ratcliffe, Norman A.
Teixeira, Valéria Laneuville
Schmidt-Chanasit, Jonas
Ferreira, Davis Fernandes
Paixão, Izabel Christina Nunes de Palmer
dc.subject.other.pt_BR.fl_str_mv Antiviral
Arbovírus
Chikungunya
Extratos brutos
Algas marinhas.
topic Antiviral
Arbovírus
Chikungunya
Extratos brutos
Algas marinhas.
Antiviral
Arbovirus
Chikungunya
Crude extracts
Seaweed.
dc.subject.en.pt_BR.fl_str_mv Antiviral
Arbovirus
Chikungunya
Crude extracts
Seaweed.
description The authors would like to acknowledge for the technical support of Thereza Elizabeth P. P. Garcia.
publishDate 2019
dc.date.issued.fl_str_mv 2019
dc.date.accessioned.fl_str_mv 2020-06-03T19:54:22Z
dc.date.available.fl_str_mv 2020-06-03T19:54:22Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.citation.fl_str_mv Cirne-Santos CC, Barros CS, Nogueira CCR, et al. Inhibition by Marine Algae of Chikungunya Virus Isolated From Patients in a Recent Disease Outbreak in Rio de Janeiro. Front Microbiol. 2019;10:2426. Published 2019 Oct 24. doi:10.3389/fmicb.2019.02426
dc.identifier.uri.fl_str_mv https://www.arca.fiocruz.br/handle/icict/41511
dc.identifier.issn.pt_BR.fl_str_mv 1664-302X
dc.identifier.doi.none.fl_str_mv 10.3389/fmicb.2019.02426
identifier_str_mv Cirne-Santos CC, Barros CS, Nogueira CCR, et al. Inhibition by Marine Algae of Chikungunya Virus Isolated From Patients in a Recent Disease Outbreak in Rio de Janeiro. Front Microbiol. 2019;10:2426. Published 2019 Oct 24. doi:10.3389/fmicb.2019.02426
1664-302X
10.3389/fmicb.2019.02426
url https://www.arca.fiocruz.br/handle/icict/41511
dc.language.iso.fl_str_mv eng
language eng
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:Repositório Institucional da FIOCRUZ (ARCA)
instname:Fundação Oswaldo Cruz (FIOCRUZ)
instacron:FIOCRUZ
instname_str Fundação Oswaldo Cruz (FIOCRUZ)
instacron_str FIOCRUZ
institution FIOCRUZ
reponame_str Repositório Institucional da FIOCRUZ (ARCA)
collection Repositório Institucional da FIOCRUZ (ARCA)
bitstream.url.fl_str_mv https://www.arca.fiocruz.br/bitstream/icict/41511/1/license.txt
https://www.arca.fiocruz.br/bitstream/icict/41511/2/IFF%20-%20fmicb-10-02426.pdf
https://www.arca.fiocruz.br/bitstream/icict/41511/3/IFF%20-%20fmicb-10-02426.pdf.txt
bitstream.checksum.fl_str_mv 5a560609d32a3863062d77ff32785d58
4e7c890a78900e6475c1f5487738e411
086ac7cb6d57fb322a71d584ef9dd6fd
bitstream.checksumAlgorithm.fl_str_mv MD5
MD5
MD5
repository.name.fl_str_mv Repositório Institucional da FIOCRUZ (ARCA) - Fundação Oswaldo Cruz (FIOCRUZ)
repository.mail.fl_str_mv repositorio.arca@fiocruz.br
_version_ 1798325026152251392