Nucleated Teleost Erythrocytes Play an Nk-Lysin- and Autophagy-Dependent Role in Antiviral Immunity

With the exception of mammals, vertebrate erythrocytes are nucleated. Nevertheless, these cells are usually considered as mere carriers of hemoglobin. In this work, however, we describe for the first time an unrecognized role of teleost red blood cells (RBCs). We found that Nk-lysin (Nkl), an antimi...

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Main Authors: Patricia Pereiro, Alejandro Romero, Patricia Díaz-Rosales, Amparo Estepa, Antonio Figueras, Beatriz Novoa
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-11-01
Series:Frontiers in Immunology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fimmu.2017.01458/full
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author Patricia Pereiro
Alejandro Romero
Patricia Díaz-Rosales
Amparo Estepa
Antonio Figueras
Beatriz Novoa
author_facet Patricia Pereiro
Alejandro Romero
Patricia Díaz-Rosales
Amparo Estepa
Antonio Figueras
Beatriz Novoa
author_sort Patricia Pereiro
collection DOAJ
description With the exception of mammals, vertebrate erythrocytes are nucleated. Nevertheless, these cells are usually considered as mere carriers of hemoglobin. In this work, however, we describe for the first time an unrecognized role of teleost red blood cells (RBCs). We found that Nk-lysin (Nkl), an antimicrobial peptide produced by NK-cells and cytotoxic T-lymphocytes, was also expressed in flatfish turbot (Scophthalmus maximus) erythrocytes. Although the antiviral role of Nkl remains to be elucidated, we found a positive correlation between the transcription of nkl and the resistance to an infection with Rhabdovirus in a teleost fish. Surprisingly, Nkl was found to be present in the autophagolysosomes of erythrocytes, and therefore this higher resistance provided by Nkl could be related to autophagy. The organelles of RBCs are degraded through autophagy during the maturation process of these cells. In this work, we observed that the blockage of autophagy increased the replication of viral hemorrhagic septicemia virus in nucleated teleost erythrocytes, which suggests that this mechanism may also be a key process in the defense against viruses in these cells. Nkl, which possesses membrane-perturbing ability and was affected by this modulation of RBC autophagy, could also participate in this process. For the first time, autophagy has been described not only as a life cycle event during the maturation of erythrocytes but also as a pivotal antiviral mechanism in nucleated erythrocytes. These results suggest a role of erythrocytes and Nkl in the antiviral immunity of fish and other vertebrates with nucleated RBCs.
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spelling doaj.art-9f0e1d73446f4b42bb84489992108fd62022-12-22T01:48:18ZengFrontiers Media S.A.Frontiers in Immunology1664-32242017-11-01810.3389/fimmu.2017.01458304502Nucleated Teleost Erythrocytes Play an Nk-Lysin- and Autophagy-Dependent Role in Antiviral ImmunityPatricia Pereiro0Alejandro Romero1Patricia Díaz-Rosales2Amparo Estepa3Antonio Figueras4Beatriz Novoa5Instituto de Investigaciones Marinas, Consejo Superior de Investigaciones Científicas (CSIC), Vigo, SpainInstituto de Investigaciones Marinas, Consejo Superior de Investigaciones Científicas (CSIC), Vigo, SpainInstituto de Investigaciones Marinas, Consejo Superior de Investigaciones Científicas (CSIC), Vigo, SpainInstituto de Biología Molecular y Celular (IBMC), Universidad Miguel Hernández, Elche, SpainInstituto de Investigaciones Marinas, Consejo Superior de Investigaciones Científicas (CSIC), Vigo, SpainInstituto de Investigaciones Marinas, Consejo Superior de Investigaciones Científicas (CSIC), Vigo, SpainWith the exception of mammals, vertebrate erythrocytes are nucleated. Nevertheless, these cells are usually considered as mere carriers of hemoglobin. In this work, however, we describe for the first time an unrecognized role of teleost red blood cells (RBCs). We found that Nk-lysin (Nkl), an antimicrobial peptide produced by NK-cells and cytotoxic T-lymphocytes, was also expressed in flatfish turbot (Scophthalmus maximus) erythrocytes. Although the antiviral role of Nkl remains to be elucidated, we found a positive correlation between the transcription of nkl and the resistance to an infection with Rhabdovirus in a teleost fish. Surprisingly, Nkl was found to be present in the autophagolysosomes of erythrocytes, and therefore this higher resistance provided by Nkl could be related to autophagy. The organelles of RBCs are degraded through autophagy during the maturation process of these cells. In this work, we observed that the blockage of autophagy increased the replication of viral hemorrhagic septicemia virus in nucleated teleost erythrocytes, which suggests that this mechanism may also be a key process in the defense against viruses in these cells. Nkl, which possesses membrane-perturbing ability and was affected by this modulation of RBC autophagy, could also participate in this process. For the first time, autophagy has been described not only as a life cycle event during the maturation of erythrocytes but also as a pivotal antiviral mechanism in nucleated erythrocytes. These results suggest a role of erythrocytes and Nkl in the antiviral immunity of fish and other vertebrates with nucleated RBCs.http://journal.frontiersin.org/article/10.3389/fimmu.2017.01458/fullteleosterythrocytesred blood cellsautophagyautophagolysosomeNk-lysin
spellingShingle Patricia Pereiro
Alejandro Romero
Patricia Díaz-Rosales
Amparo Estepa
Antonio Figueras
Beatriz Novoa
Nucleated Teleost Erythrocytes Play an Nk-Lysin- and Autophagy-Dependent Role in Antiviral Immunity
Frontiers in Immunology
teleost
erythrocytes
red blood cells
autophagy
autophagolysosome
Nk-lysin
title Nucleated Teleost Erythrocytes Play an Nk-Lysin- and Autophagy-Dependent Role in Antiviral Immunity
title_full Nucleated Teleost Erythrocytes Play an Nk-Lysin- and Autophagy-Dependent Role in Antiviral Immunity
title_fullStr Nucleated Teleost Erythrocytes Play an Nk-Lysin- and Autophagy-Dependent Role in Antiviral Immunity
title_full_unstemmed Nucleated Teleost Erythrocytes Play an Nk-Lysin- and Autophagy-Dependent Role in Antiviral Immunity
title_short Nucleated Teleost Erythrocytes Play an Nk-Lysin- and Autophagy-Dependent Role in Antiviral Immunity
title_sort nucleated teleost erythrocytes play an nk lysin and autophagy dependent role in antiviral immunity
topic teleost
erythrocytes
red blood cells
autophagy
autophagolysosome
Nk-lysin
url http://journal.frontiersin.org/article/10.3389/fimmu.2017.01458/full
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AT patriciadiazrosales nucleatedteleosterythrocytesplayannklysinandautophagydependentroleinantiviralimmunity
AT amparoestepa nucleatedteleosterythrocytesplayannklysinandautophagydependentroleinantiviralimmunity
AT antoniofigueras nucleatedteleosterythrocytesplayannklysinandautophagydependentroleinantiviralimmunity
AT beatriznovoa nucleatedteleosterythrocytesplayannklysinandautophagydependentroleinantiviralimmunity