Rainbow Trout Red Blood Cells Exposed to Viral Hemorrhagic Septicemia Virus Up-Regulate Antigen-Processing Mechanisms and MHC I&II, CD86, and CD83 Antigen-presenting Cell Markers

Nucleated teleost red blood cells (RBCs) are known to express molecules from the major histocompatibility complex and peptide-generating processes such as autophagy and proteasomes, but the role of RBCs in antigen presentation of viruses have not been studied yet. In this study, RBCs exposed ex vivo...

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Main Authors: Ivan Nombela, Ricardo Requena-Platek, Byron Morales-Lange, Veronica Chico, Sara Puente-Marin, Sergio Ciordia, Maria Carmen Mena, Julio Coll, Luis Perez, Luis Mercado, Maria del Mar Ortega-Villaizan
Format: Article
Language:English
Published: MDPI AG 2019-04-01
Series:Cells
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Online Access:https://www.mdpi.com/2073-4409/8/5/386
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author Ivan Nombela
Ricardo Requena-Platek
Byron Morales-Lange
Veronica Chico
Sara Puente-Marin
Sergio Ciordia
Maria Carmen Mena
Julio Coll
Luis Perez
Luis Mercado
Maria del Mar Ortega-Villaizan
author_facet Ivan Nombela
Ricardo Requena-Platek
Byron Morales-Lange
Veronica Chico
Sara Puente-Marin
Sergio Ciordia
Maria Carmen Mena
Julio Coll
Luis Perez
Luis Mercado
Maria del Mar Ortega-Villaizan
author_sort Ivan Nombela
collection DOAJ
description Nucleated teleost red blood cells (RBCs) are known to express molecules from the major histocompatibility complex and peptide-generating processes such as autophagy and proteasomes, but the role of RBCs in antigen presentation of viruses have not been studied yet. In this study, RBCs exposed ex vivo to viral hemorrhagic septicemia virus (VHSV) were evaluated by means of transcriptomic and proteomic approaches. Genes and proteins related to antigen presentation molecules, proteasome degradation, and autophagy were up-regulated. VHSV induced accumulation of ubiquitinated proteins in ex vivo VHSV-exposed RBCs and showed at the same time a decrease of proteasome activity. Furthermore, induction of autophagy was detected by evaluating LC3 protein levels. Sequestosome-1/p62 underwent degradation early after VHSV exposure, and it may be a link between ubiquitination and autophagy activation. Inhibition of autophagosome degradation with niclosamide resulted in intracellular detection of N protein of VHSV (NVHSV) and p62 accumulation. In addition, antigen presentation cell markers, such as major histocompatibility complex (MHC) class I & II, CD83, and CD86, increased at the transcriptional and translational level in rainbow trout RBCs exposed to VHSV. In summary, we show that nucleated rainbow trout RBCs can degrade VHSV while displaying an antigen-presenting cell (APC)-like profile.
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spelling doaj.art-3877ba66c7974e6a8df1ec84b5fa608e2023-09-02T06:06:46ZengMDPI AGCells2073-44092019-04-018538610.3390/cells8050386cells8050386Rainbow Trout Red Blood Cells Exposed to Viral Hemorrhagic Septicemia Virus Up-Regulate Antigen-Processing Mechanisms and MHC I&II, CD86, and CD83 Antigen-presenting Cell MarkersIvan Nombela0Ricardo Requena-Platek1Byron Morales-Lange2Veronica Chico3Sara Puente-Marin4Sergio Ciordia5Maria Carmen Mena6Julio Coll7Luis Perez8Luis Mercado9Maria del Mar Ortega-Villaizan10Instituto de Investigación, Desarrollo e Innovación en Biotecnología Sanitaria de Elche (IDiBE) and Instituto de Biología Molecular y Celular (IBMC), Universidad Miguel Hernández (UMH), 03202 Elche, SpainInstituto de Investigación, Desarrollo e Innovación en Biotecnología Sanitaria de Elche (IDiBE) and Instituto de Biología Molecular y Celular (IBMC), Universidad Miguel Hernández (UMH), 03202 Elche, SpainInstituto de Biología, Pontificia Universidad Católica de Valparaiso, 2373223 Valparaiso, ChileInstituto de Investigación, Desarrollo e Innovación en Biotecnología Sanitaria de Elche (IDiBE) and Instituto de Biología Molecular y Celular (IBMC), Universidad Miguel Hernández (UMH), 03202 Elche, SpainInstituto de Investigación, Desarrollo e Innovación en Biotecnología Sanitaria de Elche (IDiBE) and Instituto de Biología Molecular y Celular (IBMC), Universidad Miguel Hernández (UMH), 03202 Elche, SpainUnidad de Proteómica, Centro Nacional de Biotecnología (CNB- CSIC), 28049 Madrid, SpainUnidad de Proteómica, Centro Nacional de Biotecnología (CNB- CSIC), 28049 Madrid, SpainInstituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), 28040 Madrid, SpainInstituto de Investigación, Desarrollo e Innovación en Biotecnología Sanitaria de Elche (IDiBE) and Instituto de Biología Molecular y Celular (IBMC), Universidad Miguel Hernández (UMH), 03202 Elche, SpainInstituto de Biología, Pontificia Universidad Católica de Valparaiso, 2373223 Valparaiso, ChileInstituto de Investigación, Desarrollo e Innovación en Biotecnología Sanitaria de Elche (IDiBE) and Instituto de Biología Molecular y Celular (IBMC), Universidad Miguel Hernández (UMH), 03202 Elche, SpainNucleated teleost red blood cells (RBCs) are known to express molecules from the major histocompatibility complex and peptide-generating processes such as autophagy and proteasomes, but the role of RBCs in antigen presentation of viruses have not been studied yet. In this study, RBCs exposed ex vivo to viral hemorrhagic septicemia virus (VHSV) were evaluated by means of transcriptomic and proteomic approaches. Genes and proteins related to antigen presentation molecules, proteasome degradation, and autophagy were up-regulated. VHSV induced accumulation of ubiquitinated proteins in ex vivo VHSV-exposed RBCs and showed at the same time a decrease of proteasome activity. Furthermore, induction of autophagy was detected by evaluating LC3 protein levels. Sequestosome-1/p62 underwent degradation early after VHSV exposure, and it may be a link between ubiquitination and autophagy activation. Inhibition of autophagosome degradation with niclosamide resulted in intracellular detection of N protein of VHSV (NVHSV) and p62 accumulation. In addition, antigen presentation cell markers, such as major histocompatibility complex (MHC) class I & II, CD83, and CD86, increased at the transcriptional and translational level in rainbow trout RBCs exposed to VHSV. In summary, we show that nucleated rainbow trout RBCs can degrade VHSV while displaying an antigen-presenting cell (APC)-like profile.https://www.mdpi.com/2073-4409/8/5/386rainbow trouterythrocytesred blood cellsVHSVtranscriptomeproteomeantigen presentationautophagyubiquitination
spellingShingle Ivan Nombela
Ricardo Requena-Platek
Byron Morales-Lange
Veronica Chico
Sara Puente-Marin
Sergio Ciordia
Maria Carmen Mena
Julio Coll
Luis Perez
Luis Mercado
Maria del Mar Ortega-Villaizan
Rainbow Trout Red Blood Cells Exposed to Viral Hemorrhagic Septicemia Virus Up-Regulate Antigen-Processing Mechanisms and MHC I&II, CD86, and CD83 Antigen-presenting Cell Markers
Cells
rainbow trout
erythrocytes
red blood cells
VHSV
transcriptome
proteome
antigen presentation
autophagy
ubiquitination
title Rainbow Trout Red Blood Cells Exposed to Viral Hemorrhagic Septicemia Virus Up-Regulate Antigen-Processing Mechanisms and MHC I&II, CD86, and CD83 Antigen-presenting Cell Markers
title_full Rainbow Trout Red Blood Cells Exposed to Viral Hemorrhagic Septicemia Virus Up-Regulate Antigen-Processing Mechanisms and MHC I&II, CD86, and CD83 Antigen-presenting Cell Markers
title_fullStr Rainbow Trout Red Blood Cells Exposed to Viral Hemorrhagic Septicemia Virus Up-Regulate Antigen-Processing Mechanisms and MHC I&II, CD86, and CD83 Antigen-presenting Cell Markers
title_full_unstemmed Rainbow Trout Red Blood Cells Exposed to Viral Hemorrhagic Septicemia Virus Up-Regulate Antigen-Processing Mechanisms and MHC I&II, CD86, and CD83 Antigen-presenting Cell Markers
title_short Rainbow Trout Red Blood Cells Exposed to Viral Hemorrhagic Septicemia Virus Up-Regulate Antigen-Processing Mechanisms and MHC I&II, CD86, and CD83 Antigen-presenting Cell Markers
title_sort rainbow trout red blood cells exposed to viral hemorrhagic septicemia virus up regulate antigen processing mechanisms and mhc i amp ii cd86 and cd83 antigen presenting cell markers
topic rainbow trout
erythrocytes
red blood cells
VHSV
transcriptome
proteome
antigen presentation
autophagy
ubiquitination
url https://www.mdpi.com/2073-4409/8/5/386
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