Extracellular Vesicle-Mediated RNA Release in <italic toggle="yes">Histoplasma capsulatum</italic>

ABSTRACT Eukaryotic cells, including fungi, release extracellular vesicles (EVs). These lipid bilayered compartments play essential roles in cellular communication and pathogenesis. EV composition is complex and includes proteins, glycans, pigments, and RNA. RNAs with putative roles in pathogenesis...

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Autores principales: Lysangela R. Alves, Roberta Peres da Silva, David A. Sanchez, Daniel Zamith-Miranda, Marcio L. Rodrigues, Samuel Goldenberg, Rosana Puccia, Joshua D. Nosanchuk
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:21289f20f6804237bec2a3b120f2008e2021-11-15T15:22:22ZExtracellular Vesicle-Mediated RNA Release in <italic toggle="yes">Histoplasma capsulatum</italic>10.1128/mSphere.00176-192379-5042https://doaj.org/article/21289f20f6804237bec2a3b120f2008e2019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00176-19https://doaj.org/toc/2379-5042ABSTRACT Eukaryotic cells, including fungi, release extracellular vesicles (EVs). These lipid bilayered compartments play essential roles in cellular communication and pathogenesis. EV composition is complex and includes proteins, glycans, pigments, and RNA. RNAs with putative roles in pathogenesis have been described in EVs produced by fungi. Here we describe the RNA content in EVs produced by the G186AR and G217B strains of Histoplasma capsulatum, an important human-pathogenic fungal pathogen. A total of 124 mRNAs were identified in both strains. In this set of RNA classes, 93 transcripts were enriched in EVs from the G217B strain, whereas 31 were enriched in EVs produced by the G186AR strain. This result suggests that there are important strain-specific properties in the mRNA composition of fungal EVs. We also identified short fragments (25 to 40 nucleotides in length) that were strain specific, with a greater number identified in EVs produced by the G217B strain. Remarkably, the most highly enriched processes were stress responses and translation. Half of these fragments aligned to the reverse strand of the transcript, suggesting the occurrence of microRNA (miRNA)-like molecules in fungal EVs. We also compared the transcriptome profiles of H. capsulatum with the RNA composition of EVs, and no correlation was observed. Taking the results together, our study provided information about the RNA molecules present in H. capsulatum EVs and about the differences in composition between the strains. In addition, we found no correlation between the most highly expressed transcripts in the cell and their presence in the EVs, reinforcing the idea that the RNAs were directed to the EVs by a regulated mechanism. IMPORTANCE Extracellular vesicles (EVs) play important roles in cellular communication and pathogenesis. The RNA molecules in EVs have been implicated in a variety of processes. EV-associated RNA classes have recently been described in pathogenic fungi; however, only a few reports of studies describing the RNAs in fungal EVs are available. Improved knowledge of EV-associated RNA will contribute to the understanding of their role during infection. In this study, we described the RNA content in EVs produced by two isolates of Histoplasma capsulatum. Our results add this important pathogen to the current short list of fungal species with the ability to use EVs for the extracellular release of RNA.Lysangela R. AlvesRoberta Peres da SilvaDavid A. SanchezDaniel Zamith-MirandaMarcio L. RodriguesSamuel GoldenbergRosana PucciaJoshua D. NosanchukAmerican Society for MicrobiologyarticleHistoplasma capsulatumRNAextracellular vesiclesMicrobiologyQR1-502ENmSphere, Vol 4, Iss 2 (2019)
institution DOAJ
collection DOAJ
language EN
topic Histoplasma capsulatum
RNA
extracellular vesicles
Microbiology
QR1-502
spellingShingle Histoplasma capsulatum
RNA
extracellular vesicles
Microbiology
QR1-502
Lysangela R. Alves
Roberta Peres da Silva
David A. Sanchez
Daniel Zamith-Miranda
Marcio L. Rodrigues
Samuel Goldenberg
Rosana Puccia
Joshua D. Nosanchuk
Extracellular Vesicle-Mediated RNA Release in <italic toggle="yes">Histoplasma capsulatum</italic>
description ABSTRACT Eukaryotic cells, including fungi, release extracellular vesicles (EVs). These lipid bilayered compartments play essential roles in cellular communication and pathogenesis. EV composition is complex and includes proteins, glycans, pigments, and RNA. RNAs with putative roles in pathogenesis have been described in EVs produced by fungi. Here we describe the RNA content in EVs produced by the G186AR and G217B strains of Histoplasma capsulatum, an important human-pathogenic fungal pathogen. A total of 124 mRNAs were identified in both strains. In this set of RNA classes, 93 transcripts were enriched in EVs from the G217B strain, whereas 31 were enriched in EVs produced by the G186AR strain. This result suggests that there are important strain-specific properties in the mRNA composition of fungal EVs. We also identified short fragments (25 to 40 nucleotides in length) that were strain specific, with a greater number identified in EVs produced by the G217B strain. Remarkably, the most highly enriched processes were stress responses and translation. Half of these fragments aligned to the reverse strand of the transcript, suggesting the occurrence of microRNA (miRNA)-like molecules in fungal EVs. We also compared the transcriptome profiles of H. capsulatum with the RNA composition of EVs, and no correlation was observed. Taking the results together, our study provided information about the RNA molecules present in H. capsulatum EVs and about the differences in composition between the strains. In addition, we found no correlation between the most highly expressed transcripts in the cell and their presence in the EVs, reinforcing the idea that the RNAs were directed to the EVs by a regulated mechanism. IMPORTANCE Extracellular vesicles (EVs) play important roles in cellular communication and pathogenesis. The RNA molecules in EVs have been implicated in a variety of processes. EV-associated RNA classes have recently been described in pathogenic fungi; however, only a few reports of studies describing the RNAs in fungal EVs are available. Improved knowledge of EV-associated RNA will contribute to the understanding of their role during infection. In this study, we described the RNA content in EVs produced by two isolates of Histoplasma capsulatum. Our results add this important pathogen to the current short list of fungal species with the ability to use EVs for the extracellular release of RNA.
format article
author Lysangela R. Alves
Roberta Peres da Silva
David A. Sanchez
Daniel Zamith-Miranda
Marcio L. Rodrigues
Samuel Goldenberg
Rosana Puccia
Joshua D. Nosanchuk
author_facet Lysangela R. Alves
Roberta Peres da Silva
David A. Sanchez
Daniel Zamith-Miranda
Marcio L. Rodrigues
Samuel Goldenberg
Rosana Puccia
Joshua D. Nosanchuk
author_sort Lysangela R. Alves
title Extracellular Vesicle-Mediated RNA Release in <italic toggle="yes">Histoplasma capsulatum</italic>
title_short Extracellular Vesicle-Mediated RNA Release in <italic toggle="yes">Histoplasma capsulatum</italic>
title_full Extracellular Vesicle-Mediated RNA Release in <italic toggle="yes">Histoplasma capsulatum</italic>
title_fullStr Extracellular Vesicle-Mediated RNA Release in <italic toggle="yes">Histoplasma capsulatum</italic>
title_full_unstemmed Extracellular Vesicle-Mediated RNA Release in <italic toggle="yes">Histoplasma capsulatum</italic>
title_sort extracellular vesicle-mediated rna release in <italic toggle="yes">histoplasma capsulatum</italic>
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/21289f20f6804237bec2a3b120f2008e
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