Differential miRNA Expression in Human Macrophage-Like Cells Infected with <i>Histoplasma capsulatum</i> Yeasts Cultured in Planktonic and Biofilm Forms

<i>Histoplasma capsulatum</i> affects healthy and immunocompromised individuals, sometimes causing a severe disease. This fungus has two morphotypes, the mycelial (infective) and the yeast (parasitic) phases. MicroRNAs (miRNAs) are small RNAs involved in the regulation of several cellula...

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Main Authors: Nayla de Souza Pitangui, Junya de Lacorte Singulani, Janaina de Cássia Orlandi Sardi, Paula Carolina de Souza, Gabriela Rodríguez-Arellanes, Blanca Estela García-Pérez, Francisco Javier Enguita, Fernando R. Pavan, Maria Lucia Taylor, Maria José Soares Mendes-Giannini, Ana Marisa Fusco-Almeida
Format: Article
Language:English
Published: MDPI AG 2021-01-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/7/1/60
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author Nayla de Souza Pitangui
Junya de Lacorte Singulani
Janaina de Cássia Orlandi Sardi
Paula Carolina de Souza
Gabriela Rodríguez-Arellanes
Blanca Estela García-Pérez
Francisco Javier Enguita
Fernando R. Pavan
Maria Lucia Taylor
Maria José Soares Mendes-Giannini
Ana Marisa Fusco-Almeida
author_facet Nayla de Souza Pitangui
Junya de Lacorte Singulani
Janaina de Cássia Orlandi Sardi
Paula Carolina de Souza
Gabriela Rodríguez-Arellanes
Blanca Estela García-Pérez
Francisco Javier Enguita
Fernando R. Pavan
Maria Lucia Taylor
Maria José Soares Mendes-Giannini
Ana Marisa Fusco-Almeida
author_sort Nayla de Souza Pitangui
collection DOAJ
description <i>Histoplasma capsulatum</i> affects healthy and immunocompromised individuals, sometimes causing a severe disease. This fungus has two morphotypes, the mycelial (infective) and the yeast (parasitic) phases. MicroRNAs (miRNAs) are small RNAs involved in the regulation of several cellular processes, and their differential expression has been associated with many disease states. To investigate miRNA expression in host cells during <i>H. capsulatum</i> infection, we studied the changes in the miRNA profiles of differentiated human macrophages infected with yeasts from two fungal strains with different virulence, EH-315 (high virulence) and 60I (low virulence) grown in planktonic cultures, and EH-315 grown in biofilm form. MiRNA profiles were evaluated by means of reverse transcription-quantitative polymerase chain reaction using a commercial human miRNome panel. The target genes of the differentially expressed miRNAs and their corresponding signaling pathways were predicted using bioinformatics analyses. Here, we confirmed biofilm structures were present in the EH-315 culture whose conditions facilitated producing insoluble exopolysaccharide and intracellular polysaccharides. In infected macrophages, bioinformatics analyses revealed especially increased (hsa-miR-99b-3p) or decreased (hsa-miR-342-3p) miRNAs expression levels in response to infection with biofilms or both growth forms of <i>H. capsulatum</i> yeasts, respectively. The results of miRNAs suggested that infection by <i>H. capsulatum</i> can affect important biological pathways of the host cell, targeting two genes: one encoding a protein that is important in the cortical cytoskeleton; the other, a protein involved in the formation of stress granules. Expressed miRNAs in the host’s response could be proposed as new therapeutic and/or diagnostic tools for histoplasmosis.
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spelling doaj.art-99824a7c270347c38844e1d6908588e52023-12-03T13:36:44ZengMDPI AGJournal of Fungi2309-608X2021-01-01716010.3390/jof7010060Differential miRNA Expression in Human Macrophage-Like Cells Infected with <i>Histoplasma capsulatum</i> Yeasts Cultured in Planktonic and Biofilm FormsNayla de Souza Pitangui0Junya de Lacorte Singulani1Janaina de Cássia Orlandi Sardi2Paula Carolina de Souza3Gabriela Rodríguez-Arellanes4Blanca Estela García-Pérez5Francisco Javier Enguita6Fernando R. Pavan7Maria Lucia Taylor8Maria José Soares Mendes-Giannini9Ana Marisa Fusco-Almeida10School of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, São Paulo 14800-903, BrazilSchool of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, São Paulo 14800-903, BrazilSchool of Pharmaceutical Sciences, Food and Nutrition, Federal University of Mato Grosso do Sul, Campo Grande, Mato Grosso do Sul 79070-900, BrazilSchool of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, São Paulo 14800-903, BrazilUnidad de Micología, Departamento de Microbiología y Parasitología, Facultad de Medicina, UNAM-Universidad Nacional Autónoma de México, Mexico City 04510, MexicoDepartamento de Microbiología, Escuela Nacional de Ciencias Biológicas, IPN–Instituto Politécnico Nacional, Mexico City 11340, MexicoInstituto de Medicina Molecular, Faculdade de Medicina, Universidade de Lisboa, Lisboa 1649-028, PortugalSchool of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, São Paulo 14800-903, BrazilUnidad de Micología, Departamento de Microbiología y Parasitología, Facultad de Medicina, UNAM-Universidad Nacional Autónoma de México, Mexico City 04510, MexicoSchool of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, São Paulo 14800-903, BrazilSchool of Pharmaceutical Sciences, São Paulo State University (UNESP), Araraquara, São Paulo 14800-903, Brazil<i>Histoplasma capsulatum</i> affects healthy and immunocompromised individuals, sometimes causing a severe disease. This fungus has two morphotypes, the mycelial (infective) and the yeast (parasitic) phases. MicroRNAs (miRNAs) are small RNAs involved in the regulation of several cellular processes, and their differential expression has been associated with many disease states. To investigate miRNA expression in host cells during <i>H. capsulatum</i> infection, we studied the changes in the miRNA profiles of differentiated human macrophages infected with yeasts from two fungal strains with different virulence, EH-315 (high virulence) and 60I (low virulence) grown in planktonic cultures, and EH-315 grown in biofilm form. MiRNA profiles were evaluated by means of reverse transcription-quantitative polymerase chain reaction using a commercial human miRNome panel. The target genes of the differentially expressed miRNAs and their corresponding signaling pathways were predicted using bioinformatics analyses. Here, we confirmed biofilm structures were present in the EH-315 culture whose conditions facilitated producing insoluble exopolysaccharide and intracellular polysaccharides. In infected macrophages, bioinformatics analyses revealed especially increased (hsa-miR-99b-3p) or decreased (hsa-miR-342-3p) miRNAs expression levels in response to infection with biofilms or both growth forms of <i>H. capsulatum</i> yeasts, respectively. The results of miRNAs suggested that infection by <i>H. capsulatum</i> can affect important biological pathways of the host cell, targeting two genes: one encoding a protein that is important in the cortical cytoskeleton; the other, a protein involved in the formation of stress granules. Expressed miRNAs in the host’s response could be proposed as new therapeutic and/or diagnostic tools for histoplasmosis.https://www.mdpi.com/2309-608X/7/1/60<i>Histoplasma capsulatum</i>biofilmsmacrophagesmicroRNAsfungal-host interactions
spellingShingle Nayla de Souza Pitangui
Junya de Lacorte Singulani
Janaina de Cássia Orlandi Sardi
Paula Carolina de Souza
Gabriela Rodríguez-Arellanes
Blanca Estela García-Pérez
Francisco Javier Enguita
Fernando R. Pavan
Maria Lucia Taylor
Maria José Soares Mendes-Giannini
Ana Marisa Fusco-Almeida
Differential miRNA Expression in Human Macrophage-Like Cells Infected with <i>Histoplasma capsulatum</i> Yeasts Cultured in Planktonic and Biofilm Forms
Journal of Fungi
<i>Histoplasma capsulatum</i>
biofilms
macrophages
microRNAs
fungal-host interactions
title Differential miRNA Expression in Human Macrophage-Like Cells Infected with <i>Histoplasma capsulatum</i> Yeasts Cultured in Planktonic and Biofilm Forms
title_full Differential miRNA Expression in Human Macrophage-Like Cells Infected with <i>Histoplasma capsulatum</i> Yeasts Cultured in Planktonic and Biofilm Forms
title_fullStr Differential miRNA Expression in Human Macrophage-Like Cells Infected with <i>Histoplasma capsulatum</i> Yeasts Cultured in Planktonic and Biofilm Forms
title_full_unstemmed Differential miRNA Expression in Human Macrophage-Like Cells Infected with <i>Histoplasma capsulatum</i> Yeasts Cultured in Planktonic and Biofilm Forms
title_short Differential miRNA Expression in Human Macrophage-Like Cells Infected with <i>Histoplasma capsulatum</i> Yeasts Cultured in Planktonic and Biofilm Forms
title_sort differential mirna expression in human macrophage like cells infected with i histoplasma capsulatum i yeasts cultured in planktonic and biofilm forms
topic <i>Histoplasma capsulatum</i>
biofilms
macrophages
microRNAs
fungal-host interactions
url https://www.mdpi.com/2309-608X/7/1/60
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