Differential Recognition of Clinically Relevant <i>Sporothrix</i> Species by Human Mononuclear Cells

Sporotrichosis is a human and animal fungal infection distributed worldwide that is caused by the thermodimorphic species of the <i>Sporothrix</i> pathogenic clade, which includes <i>Sporothrix brasiliensis</i>, <i>Sporothrix schenckii</i>, and <i>Sporothrix...

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Main Authors: Laura C. García-Carnero, Iván Martínez-Duncker, Manuela Gómez-Gaviria, Héctor M. Mora-Montes
Format: Article
Language:English
Published: MDPI AG 2023-04-01
Series:Journal of Fungi
Subjects:
Online Access:https://www.mdpi.com/2309-608X/9/4/448
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author Laura C. García-Carnero
Iván Martínez-Duncker
Manuela Gómez-Gaviria
Héctor M. Mora-Montes
author_facet Laura C. García-Carnero
Iván Martínez-Duncker
Manuela Gómez-Gaviria
Héctor M. Mora-Montes
author_sort Laura C. García-Carnero
collection DOAJ
description Sporotrichosis is a human and animal fungal infection distributed worldwide that is caused by the thermodimorphic species of the <i>Sporothrix</i> pathogenic clade, which includes <i>Sporothrix brasiliensis</i>, <i>Sporothrix schenckii</i>, and <i>Sporothrix globosa</i>. The cell wall composition and the immune response against the <i>Sporothrix</i> species have been studied mainly in <i>S. brasiliensis</i> and <i>S. schenckii</i>, whilst little is known about the <i>S. globosa</i> cell wall and the immune response that its components trigger. Therefore, in this study, we aimed to analyze the cell wall composition of <i>S. globosa</i> in three morphologies (germlings, conidia, and yeast-like cells) and the differences in cytokine production when human peripheral blood mononuclear cells (PBMCs) interact with these morphotypes, using <i>S. schenckii</i> and <i>S. brasiliensis</i> as a comparison. We found that <i>S. globosa</i> conidia and yeast-like cells have a higher cell wall chitin content, while all three morphologies have a higher β-1,3-glucan content, which was found most exposed at the cell surface when compared to <i>S. schenckii</i> and <i>S. brasiliensis</i>. In addition, <i>S. globosa</i> has lower levels of mannose- and rhamnose-based glycoconjugates, as well as of <i>N</i>- and <i>O</i>-linked glycans, indicating that this fungal cell wall has species-specific proportions and organization of its components. When interacting with PBMCs, <i>S. brasiliensis</i> and <i>S. globosa</i> showed a similar cytokine stimulation profile, but with a higher stimulation of IL-10 by <i>S. globosa</i>. Additionally, when the inner cell wall components of <i>S. globosa</i> were exposed at the surface or <i>N</i>- and <i>O</i>-glycans were removed, the cytokine production profile of this species in its three morphotypes did not significantly change, contrasting with the <i>S. schenckii</i> and <i>S. brasiliensis</i> species that showed different cytokine profiles depending on the treatment applied to the walls. In addition, it was found that the anti-inflammatory response stimulated by <i>S. globosa</i> was dependent on the activation of dectin-1, mannose receptor, and TLR2, but not TLR4. All of these results indicate that the cell wall composition and structure of the three <i>Sporothrix</i> species in the three morphologies are different, affecting their interaction with human PBMCs and generating species-specific cytokine profiles.
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spelling doaj.art-0a0cd9009d304e7896c2d38c1e92f0b32023-11-17T19:58:17ZengMDPI AGJournal of Fungi2309-608X2023-04-019444810.3390/jof9040448Differential Recognition of Clinically Relevant <i>Sporothrix</i> Species by Human Mononuclear CellsLaura C. García-Carnero0Iván Martínez-Duncker1Manuela Gómez-Gaviria2Héctor M. Mora-Montes3Departamento de Biología, División de Ciencias Naturales y Exactas, Campus Guanajuato, Universidad de Guanajuato, Noria Alta s/n, col. Noria Alta, C.P., Guanajuato 36050, Gto., MexicoLaboratorio de Glicobiología Humana y Diagnóstico Molecular, Centro de Investigación en Dinámica Celular, Instituto de Investigación en Ciencias Básicas y Aplicadas, Universidad Autónoma del Estado de Morelos, Cuernavaca 62209, Mor., MexicoDepartamento de Biología, División de Ciencias Naturales y Exactas, Campus Guanajuato, Universidad de Guanajuato, Noria Alta s/n, col. Noria Alta, C.P., Guanajuato 36050, Gto., MexicoDepartamento de Biología, División de Ciencias Naturales y Exactas, Campus Guanajuato, Universidad de Guanajuato, Noria Alta s/n, col. Noria Alta, C.P., Guanajuato 36050, Gto., MexicoSporotrichosis is a human and animal fungal infection distributed worldwide that is caused by the thermodimorphic species of the <i>Sporothrix</i> pathogenic clade, which includes <i>Sporothrix brasiliensis</i>, <i>Sporothrix schenckii</i>, and <i>Sporothrix globosa</i>. The cell wall composition and the immune response against the <i>Sporothrix</i> species have been studied mainly in <i>S. brasiliensis</i> and <i>S. schenckii</i>, whilst little is known about the <i>S. globosa</i> cell wall and the immune response that its components trigger. Therefore, in this study, we aimed to analyze the cell wall composition of <i>S. globosa</i> in three morphologies (germlings, conidia, and yeast-like cells) and the differences in cytokine production when human peripheral blood mononuclear cells (PBMCs) interact with these morphotypes, using <i>S. schenckii</i> and <i>S. brasiliensis</i> as a comparison. We found that <i>S. globosa</i> conidia and yeast-like cells have a higher cell wall chitin content, while all three morphologies have a higher β-1,3-glucan content, which was found most exposed at the cell surface when compared to <i>S. schenckii</i> and <i>S. brasiliensis</i>. In addition, <i>S. globosa</i> has lower levels of mannose- and rhamnose-based glycoconjugates, as well as of <i>N</i>- and <i>O</i>-linked glycans, indicating that this fungal cell wall has species-specific proportions and organization of its components. When interacting with PBMCs, <i>S. brasiliensis</i> and <i>S. globosa</i> showed a similar cytokine stimulation profile, but with a higher stimulation of IL-10 by <i>S. globosa</i>. Additionally, when the inner cell wall components of <i>S. globosa</i> were exposed at the surface or <i>N</i>- and <i>O</i>-glycans were removed, the cytokine production profile of this species in its three morphotypes did not significantly change, contrasting with the <i>S. schenckii</i> and <i>S. brasiliensis</i> species that showed different cytokine profiles depending on the treatment applied to the walls. In addition, it was found that the anti-inflammatory response stimulated by <i>S. globosa</i> was dependent on the activation of dectin-1, mannose receptor, and TLR2, but not TLR4. All of these results indicate that the cell wall composition and structure of the three <i>Sporothrix</i> species in the three morphologies are different, affecting their interaction with human PBMCs and generating species-specific cytokine profiles.https://www.mdpi.com/2309-608X/9/4/448fungal cell wallprotein glycosylation<i>N</i>-linked glycans<i>O</i>-linked glycansinnate immune sensing
spellingShingle Laura C. García-Carnero
Iván Martínez-Duncker
Manuela Gómez-Gaviria
Héctor M. Mora-Montes
Differential Recognition of Clinically Relevant <i>Sporothrix</i> Species by Human Mononuclear Cells
Journal of Fungi
fungal cell wall
protein glycosylation
<i>N</i>-linked glycans
<i>O</i>-linked glycans
innate immune sensing
title Differential Recognition of Clinically Relevant <i>Sporothrix</i> Species by Human Mononuclear Cells
title_full Differential Recognition of Clinically Relevant <i>Sporothrix</i> Species by Human Mononuclear Cells
title_fullStr Differential Recognition of Clinically Relevant <i>Sporothrix</i> Species by Human Mononuclear Cells
title_full_unstemmed Differential Recognition of Clinically Relevant <i>Sporothrix</i> Species by Human Mononuclear Cells
title_short Differential Recognition of Clinically Relevant <i>Sporothrix</i> Species by Human Mononuclear Cells
title_sort differential recognition of clinically relevant i sporothrix i species by human mononuclear cells
topic fungal cell wall
protein glycosylation
<i>N</i>-linked glycans
<i>O</i>-linked glycans
innate immune sensing
url https://www.mdpi.com/2309-608X/9/4/448
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