Evaluation of in vitro antifungal activity of Xylosma prockia (Turcz.) Turcz. (Salicaceae) leaves against Cryptococcus spp

Detalhes bibliográficos
Autor(a) principal: Mariany Lopes da Costa Folly
Data de Publicação: 2020
Outros Autores: Gabriella Freitas Ferreira, Maiara Rodrigues Salvador, Ana A. Sathler, Guilherme F. da Silva, Joice Castelo Branco Santos, Julliana Ribeiro Alves Santos, Wallace Ribeiro Nunes Neto, João Francisco Silva Rodrigues, Elizabeth Soares Fernandes, Luís Cláudio Nascimento da Silva, Gustavo José Cota de Freitas, Ângelo Márcio Leite Denadai, Ivanildes V. Rodrigues, Leonardo M. Mendonça, Andrea Souza Monteiro, Daniel Assis Santos, Gabriela M. Cabrera, Gastón Ezequiel Siless, Karen Luise Lang
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UFMG
Texto Completo: https://doi.org/10.3389/fmicb.2019.03114
http://hdl.handle.net/1843/56339
https://orcid.org/0000-0001-9523-6187
https://orcid.org/0000-0001-6842-1934
https://orcid.org/0000-0003-1677-2817
https://orcid.org/0000-0001-6918-1186
https://orcid.org/0000-0002-4206-0904
https://orcid.org/0000-0001-8259-6933
https://orcid.org/0000-0001-7351-6356
https://orcid.org/0000-0001-6887-8192
https://orcid.org/0000-0002-1108-5666
https://orcid.org/0000-0001-5257-5314
https://orcid.org/0000-0002-1441-6280
Resumo: Cryptococcus species are responsible for important systemic mycosis and are estimated to cause millions of new cases annually. The available therapy is limited due to the high toxicity and the increasing rates of yeast resistance to antifungal drugs. Popularly known as “sucará,” Xylosma prockia (Turcz.) Turcz. (Salicaceae) is a native plant from Brazil with little information on its pharmacological potential. In this work, we evaluated in vitro anticryptococcal effects of the leaf ethanolic extract of X. prockia and its fractions against Cryptococcus gattii and Cryptococcus neoformans. We also evaluated phenotypic alterations caused by ethyl acetate fraction (EAF) (chosen according to its biological results). The liquid chromatography–mass spectrometry (LC-MS) analysis of EAF demonstrated the presence of phenolic metabolites that belong to three structurally related groups as majority compounds: caffeoylquinic acid, coumaroyl-glucoside, and caffeoyl-glucoside/deoxyhexosyl-caffeoyl glucoside derivatives. The minimum inhibitory concentration (MIC) values against C. gattii and C. neoformans ranged from 8 to 64 mg/L and from 0.5 to 8 mg/L, for ethanolic extract and EAF, respectively. The EAF triggered an oxidative burst and promoted lipid peroxidation. EAF also induced a reduction of ergosterol content in the pathogen cell membrane. These effects were not associated with alterations in the cell surface charge or in the thermodynamic fingerprint of the molecular interaction between EAF and the yeasts evaluated. Cytotoxic experiments with peripheral blood mononuclear cells (PBMCs) demonstrated that EAF was more selective for yeasts than was PBMCs. The results may provide evidence that X. prockia leaf extract might indeed be a potential source of antifungal agents.
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spelling 2023-07-14T22:50:34Z2023-07-14T22:50:34Z202010https://doi.org/10.3389/fmicb.2019.031141664-302Xhttp://hdl.handle.net/1843/56339https://orcid.org/0000-0001-9523-6187https://orcid.org/0000-0001-6842-1934https://orcid.org/0000-0003-1677-2817https://orcid.org/0000-0001-6918-1186https://orcid.org/0000-0002-4206-0904https://orcid.org/0000-0001-8259-6933https://orcid.org/0000-0001-7351-6356https://orcid.org/0000-0001-6887-8192https://orcid.org/0000-0002-1108-5666https://orcid.org/0000-0001-5257-5314https://orcid.org/0000-0002-1441-6280Cryptococcus species are responsible for important systemic mycosis and are estimated to cause millions of new cases annually. The available therapy is limited due to the high toxicity and the increasing rates of yeast resistance to antifungal drugs. Popularly known as “sucará,” Xylosma prockia (Turcz.) Turcz. (Salicaceae) is a native plant from Brazil with little information on its pharmacological potential. In this work, we evaluated in vitro anticryptococcal effects of the leaf ethanolic extract of X. prockia and its fractions against Cryptococcus gattii and Cryptococcus neoformans. We also evaluated phenotypic alterations caused by ethyl acetate fraction (EAF) (chosen according to its biological results). The liquid chromatography–mass spectrometry (LC-MS) analysis of EAF demonstrated the presence of phenolic metabolites that belong to three structurally related groups as majority compounds: caffeoylquinic acid, coumaroyl-glucoside, and caffeoyl-glucoside/deoxyhexosyl-caffeoyl glucoside derivatives. The minimum inhibitory concentration (MIC) values against C. gattii and C. neoformans ranged from 8 to 64 mg/L and from 0.5 to 8 mg/L, for ethanolic extract and EAF, respectively. The EAF triggered an oxidative burst and promoted lipid peroxidation. EAF also induced a reduction of ergosterol content in the pathogen cell membrane. These effects were not associated with alterations in the cell surface charge or in the thermodynamic fingerprint of the molecular interaction between EAF and the yeasts evaluated. Cytotoxic experiments with peripheral blood mononuclear cells (PBMCs) demonstrated that EAF was more selective for yeasts than was PBMCs. The results may provide evidence that X. prockia leaf extract might indeed be a potential source of antifungal agents.Espécies de Cryptococcus são responsáveis por importantes micoses sistêmicas e estima-se que causem milhões de novos casos anualmente. A terapia disponível é limitada devido à alta toxicidade e às crescentes taxas de resistência das leveduras aos antifúngicos. Popularmente conhecida como “sucará”, Xylosma prockia (Turcz.) Turcz. (Salicaceae) é uma planta nativa do Brasil com poucas informações sobre seu potencial farmacológico. Neste trabalho, avaliamos os efeitos anticriptocócicos in vitro do extrato etanólico da folha de X. prockia e suas frações contra Cryptococcus gattii e Cryptococcus neoformans. Também avaliamos as alterações fenotípicas causadas pela fração acetato de etila (EAF) (escolhida de acordo com seus resultados biológicos). A análise de cromatografia líquida-espectrometria de massa (LC-MS) de EAF demonstrou a presença de metabólitos fenólicos que pertencem a três grupos estruturalmente relacionados como compostos majoritários: ácido cafeoilquínico, cumaroil-glucosídeo e derivados de cafeoil-glicosídeo/desoxihexosil-cafeoil glicosídeo. Os valores de concentração inibitória mínima (CIM) contra C. gattii e C. neoformans variaram de 8 a 64 mg/L e de 0,5 a 8 mg/L, para extrato etanólico e EAF, respectivamente. O EAF desencadeou uma explosão oxidativa e promoveu a peroxidação lipídica. O EAF também induziu uma redução do conteúdo de ergosterol na membrana celular do patógeno. Esses efeitos não foram associados a alterações na carga da superfície celular ou na impressão digital termodinâmica da interação molecular entre EAF e as leveduras avaliadas. Experimentos citotóxicos com células mononucleares de sangue periférico (PBMCs) demonstraram que EAF foi mais seletivo para leveduras do que PBMCs. Os resultados podem fornecer evidências de que o extrato da folha de X. prockia pode de fato ser uma fonte potencial de agentes antifúngicos.CNPq - Conselho Nacional de Desenvolvimento Científico e TecnológicoFAPEMIG - Fundação de Amparo à Pesquisa do Estado de Minas GeraisengUniversidade Federal de Minas GeraisUFMGBrasilICB - DEPARTAMENTO DE MICROBIOLOGIAFrontiers in MicrobiologyCryptococcus gattiiCryptococcus neoformansSalicaceaeAntifúngicosProdutos biológicosBiodiversidadeCryptococcus sppXylosma prockiaAntifungal agentsNatural productsBiodiversityEvaluation of in vitro antifungal activity of Xylosma prockia (Turcz.) Turcz. (Salicaceae) leaves against Cryptococcus sppAvaliação da atividade antifúngica in vitro que Xylosma prockia (Turcz.) Turcz. (Salicaceae) deixa contra Cryptococcus spp.info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttps://www.frontiersin.org/articles/10.3389/fmicb.2019.03114/fullMariany Lopes da Costa FollyGabriella Freitas FerreiraMaiara Rodrigues SalvadorAna A. SathlerGuilherme F. da SilvaJoice Castelo Branco SantosJulliana Ribeiro Alves SantosWallace Ribeiro Nunes NetoJoão Francisco Silva RodriguesElizabeth Soares FernandesLuís Cláudio Nascimento da SilvaGustavo José Cota de FreitasÂngelo Márcio Leite DenadaiIvanildes V. RodriguesLeonardo M. MendonçaAndrea Souza MonteiroDaniel Assis SantosGabriela M. CabreraGastón Ezequiel SilessKaren Luise Langapplication/pdfinfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da UFMGinstname:Universidade Federal de Minas Gerais (UFMG)instacron:UFMGLICENSELicense.txtLicense.txttext/plain; charset=utf-82042https://repositorio.ufmg.br/bitstream/1843/56339/1/License.txtfa505098d172de0bc8864fc1287ffe22MD51ORIGINALEvaluation of in vitro Antifungal Activity of Xylosma prockia (Turcz.) Turcz. (Salicaceae) Leaves Against Cryptococcus spp.pdfEvaluation of in vitro Antifungal Activity of Xylosma prockia (Turcz.) Turcz. (Salicaceae) Leaves Against Cryptococcus spp.pdfapplication/pdf4003018https://repositorio.ufmg.br/bitstream/1843/56339/2/Evaluation%20of%20in%20vitro%20Antifungal%20Activity%20of%20Xylosma%20prockia%20%28Turcz.%29%20Turcz.%20%28Salicaceae%29%20Leaves%20Against%20Cryptococcus%20spp.pdfab716cc57a27fa2e9cb65f7a5a9ae1feMD521843/563392023-07-14 19:50:34.468oai:repositorio.ufmg.br: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Repositório de PublicaçõesPUBhttps://repositorio.ufmg.br/oaiopendoar:2023-07-14T22:50:34Repositório Institucional da UFMG - Universidade Federal de Minas Gerais (UFMG)false
dc.title.pt_BR.fl_str_mv Evaluation of in vitro antifungal activity of Xylosma prockia (Turcz.) Turcz. (Salicaceae) leaves against Cryptococcus spp
dc.title.alternative.pt_BR.fl_str_mv Avaliação da atividade antifúngica in vitro que Xylosma prockia (Turcz.) Turcz. (Salicaceae) deixa contra Cryptococcus spp.
title Evaluation of in vitro antifungal activity of Xylosma prockia (Turcz.) Turcz. (Salicaceae) leaves against Cryptococcus spp
spellingShingle Evaluation of in vitro antifungal activity of Xylosma prockia (Turcz.) Turcz. (Salicaceae) leaves against Cryptococcus spp
Mariany Lopes da Costa Folly
Cryptococcus spp
Xylosma prockia
Antifungal agents
Natural products
Biodiversity
Cryptococcus gattii
Cryptococcus neoformans
Salicaceae
Antifúngicos
Produtos biológicos
Biodiversidade
title_short Evaluation of in vitro antifungal activity of Xylosma prockia (Turcz.) Turcz. (Salicaceae) leaves against Cryptococcus spp
title_full Evaluation of in vitro antifungal activity of Xylosma prockia (Turcz.) Turcz. (Salicaceae) leaves against Cryptococcus spp
title_fullStr Evaluation of in vitro antifungal activity of Xylosma prockia (Turcz.) Turcz. (Salicaceae) leaves against Cryptococcus spp
title_full_unstemmed Evaluation of in vitro antifungal activity of Xylosma prockia (Turcz.) Turcz. (Salicaceae) leaves against Cryptococcus spp
title_sort Evaluation of in vitro antifungal activity of Xylosma prockia (Turcz.) Turcz. (Salicaceae) leaves against Cryptococcus spp
author Mariany Lopes da Costa Folly
author_facet Mariany Lopes da Costa Folly
Gabriella Freitas Ferreira
Maiara Rodrigues Salvador
Ana A. Sathler
Guilherme F. da Silva
Joice Castelo Branco Santos
Julliana Ribeiro Alves Santos
Wallace Ribeiro Nunes Neto
João Francisco Silva Rodrigues
Elizabeth Soares Fernandes
Luís Cláudio Nascimento da Silva
Gustavo José Cota de Freitas
Ângelo Márcio Leite Denadai
Ivanildes V. Rodrigues
Leonardo M. Mendonça
Andrea Souza Monteiro
Daniel Assis Santos
Gabriela M. Cabrera
Gastón Ezequiel Siless
Karen Luise Lang
author_role author
author2 Gabriella Freitas Ferreira
Maiara Rodrigues Salvador
Ana A. Sathler
Guilherme F. da Silva
Joice Castelo Branco Santos
Julliana Ribeiro Alves Santos
Wallace Ribeiro Nunes Neto
João Francisco Silva Rodrigues
Elizabeth Soares Fernandes
Luís Cláudio Nascimento da Silva
Gustavo José Cota de Freitas
Ângelo Márcio Leite Denadai
Ivanildes V. Rodrigues
Leonardo M. Mendonça
Andrea Souza Monteiro
Daniel Assis Santos
Gabriela M. Cabrera
Gastón Ezequiel Siless
Karen Luise Lang
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.author.fl_str_mv Mariany Lopes da Costa Folly
Gabriella Freitas Ferreira
Maiara Rodrigues Salvador
Ana A. Sathler
Guilherme F. da Silva
Joice Castelo Branco Santos
Julliana Ribeiro Alves Santos
Wallace Ribeiro Nunes Neto
João Francisco Silva Rodrigues
Elizabeth Soares Fernandes
Luís Cláudio Nascimento da Silva
Gustavo José Cota de Freitas
Ângelo Márcio Leite Denadai
Ivanildes V. Rodrigues
Leonardo M. Mendonça
Andrea Souza Monteiro
Daniel Assis Santos
Gabriela M. Cabrera
Gastón Ezequiel Siless
Karen Luise Lang
dc.subject.por.fl_str_mv Cryptococcus spp
Xylosma prockia
Antifungal agents
Natural products
Biodiversity
topic Cryptococcus spp
Xylosma prockia
Antifungal agents
Natural products
Biodiversity
Cryptococcus gattii
Cryptococcus neoformans
Salicaceae
Antifúngicos
Produtos biológicos
Biodiversidade
dc.subject.other.pt_BR.fl_str_mv Cryptococcus gattii
Cryptococcus neoformans
Salicaceae
Antifúngicos
Produtos biológicos
Biodiversidade
description Cryptococcus species are responsible for important systemic mycosis and are estimated to cause millions of new cases annually. The available therapy is limited due to the high toxicity and the increasing rates of yeast resistance to antifungal drugs. Popularly known as “sucará,” Xylosma prockia (Turcz.) Turcz. (Salicaceae) is a native plant from Brazil with little information on its pharmacological potential. In this work, we evaluated in vitro anticryptococcal effects of the leaf ethanolic extract of X. prockia and its fractions against Cryptococcus gattii and Cryptococcus neoformans. We also evaluated phenotypic alterations caused by ethyl acetate fraction (EAF) (chosen according to its biological results). The liquid chromatography–mass spectrometry (LC-MS) analysis of EAF demonstrated the presence of phenolic metabolites that belong to three structurally related groups as majority compounds: caffeoylquinic acid, coumaroyl-glucoside, and caffeoyl-glucoside/deoxyhexosyl-caffeoyl glucoside derivatives. The minimum inhibitory concentration (MIC) values against C. gattii and C. neoformans ranged from 8 to 64 mg/L and from 0.5 to 8 mg/L, for ethanolic extract and EAF, respectively. The EAF triggered an oxidative burst and promoted lipid peroxidation. EAF also induced a reduction of ergosterol content in the pathogen cell membrane. These effects were not associated with alterations in the cell surface charge or in the thermodynamic fingerprint of the molecular interaction between EAF and the yeasts evaluated. Cytotoxic experiments with peripheral blood mononuclear cells (PBMCs) demonstrated that EAF was more selective for yeasts than was PBMCs. The results may provide evidence that X. prockia leaf extract might indeed be a potential source of antifungal agents.
publishDate 2020
dc.date.issued.fl_str_mv 2020
dc.date.accessioned.fl_str_mv 2023-07-14T22:50:34Z
dc.date.available.fl_str_mv 2023-07-14T22:50:34Z
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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dc.identifier.uri.fl_str_mv http://hdl.handle.net/1843/56339
dc.identifier.doi.pt_BR.fl_str_mv https://doi.org/10.3389/fmicb.2019.03114
dc.identifier.issn.pt_BR.fl_str_mv 1664-302X
dc.identifier.orcid.pt_BR.fl_str_mv https://orcid.org/0000-0001-9523-6187
https://orcid.org/0000-0001-6842-1934
https://orcid.org/0000-0003-1677-2817
https://orcid.org/0000-0001-6918-1186
https://orcid.org/0000-0002-4206-0904
https://orcid.org/0000-0001-8259-6933
https://orcid.org/0000-0001-7351-6356
https://orcid.org/0000-0001-6887-8192
https://orcid.org/0000-0002-1108-5666
https://orcid.org/0000-0001-5257-5314
https://orcid.org/0000-0002-1441-6280
url https://doi.org/10.3389/fmicb.2019.03114
http://hdl.handle.net/1843/56339
https://orcid.org/0000-0001-9523-6187
https://orcid.org/0000-0001-6842-1934
https://orcid.org/0000-0003-1677-2817
https://orcid.org/0000-0001-6918-1186
https://orcid.org/0000-0002-4206-0904
https://orcid.org/0000-0001-8259-6933
https://orcid.org/0000-0001-7351-6356
https://orcid.org/0000-0001-6887-8192
https://orcid.org/0000-0002-1108-5666
https://orcid.org/0000-0001-5257-5314
https://orcid.org/0000-0002-1441-6280
identifier_str_mv 1664-302X
dc.language.iso.fl_str_mv eng
language eng
dc.relation.ispartof.pt_BR.fl_str_mv Frontiers in Microbiology
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dc.publisher.none.fl_str_mv Universidade Federal de Minas Gerais
dc.publisher.initials.fl_str_mv UFMG
dc.publisher.country.fl_str_mv Brasil
dc.publisher.department.fl_str_mv ICB - DEPARTAMENTO DE MICROBIOLOGIA
publisher.none.fl_str_mv Universidade Federal de Minas Gerais
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institution UFMG
reponame_str Repositório Institucional da UFMG
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