Cargando…

Resistance to white spot syndrome virus in the European shore crab is associated with suppressed virion trafficking and heightened immune responses

INTRODUCTION: All decapod crustaceans are considered potentially susceptible to White Spot Syndrome Virus (WSSV) infection, but the degree of White Spot Disease (WSD) susceptibility varies widely between species. The European shore crab Carcinus maenas can be infected with the virus for long periods...

Descripción completa

Detalles Bibliográficos
Autores principales: Millard, Rebecca S., Bickley, Lisa K., Bateman, Kelly S., Verbruggen, Bas, Farbos, Audrey, Lange, Anke, Moore, Karen A., Stentiford, Grant D., Tyler, Charles R., van Aerle, Ronny, Santos, Eduarda M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9831657/
https://www.ncbi.nlm.nih.gov/pubmed/36636327
http://dx.doi.org/10.3389/fimmu.2022.1057421
_version_ 1784867891610386432
author Millard, Rebecca S.
Bickley, Lisa K.
Bateman, Kelly S.
Verbruggen, Bas
Farbos, Audrey
Lange, Anke
Moore, Karen A.
Stentiford, Grant D.
Tyler, Charles R.
van Aerle, Ronny
Santos, Eduarda M.
author_facet Millard, Rebecca S.
Bickley, Lisa K.
Bateman, Kelly S.
Verbruggen, Bas
Farbos, Audrey
Lange, Anke
Moore, Karen A.
Stentiford, Grant D.
Tyler, Charles R.
van Aerle, Ronny
Santos, Eduarda M.
author_sort Millard, Rebecca S.
collection PubMed
description INTRODUCTION: All decapod crustaceans are considered potentially susceptible to White Spot Syndrome Virus (WSSV) infection, but the degree of White Spot Disease (WSD) susceptibility varies widely between species. The European shore crab Carcinus maenas can be infected with the virus for long periods of time without signs of disease. Given the high mortality rate of susceptible species, the differential susceptibility of these resistant hosts offers an opportunity to investigate mechanisms of disease resistance. METHODS: Here, the temporal transcriptional responses (mRNA and miRNA) of C. maenas following WSSV injection were analysed and compared to a previously published dataset for the highly WSSV susceptible Penaeus vannamei to identify key genes, processes and pathways contributing to increased WSD resistance. RESULTS: We show that, in contrast to P. vannamei, the transcriptional response during the first 2 days following WSSV injection in C. maenas is limited. During the later time points (7 days onwards), two groups of crabs were identified, a recalcitrant group where no replication of the virus occurred, and a group where significant viral replication occurred, with the transcriptional profiles of the latter group resembling those of WSSV-susceptible species. We identify key differences in the molecular responses of these groups to WSSV injection. DISCUSSION: We propose that increased WSD resistance in C. maenas may result from impaired WSSV endocytosis due to the inhibition of internal vesicle budding by dynamin-1, and a delay in movement to the nucleus caused by the downregulation of cytoskeletal transcripts required for WSSV cytoskeleton docking, during early stages of the infection. This response allows resistant hosts greater time to fine-tune immune responses associated with miRNA expression, apoptosis and the melanisation cascade to defend against, and clear, invading WSSV. These findings suggest that the initial stages of infection are key to resistance to WSSV in the crab and highlight possible pathways that could be targeted in farmed crustacean to enhance resistance to WSD.
format Online
Article
Text
id pubmed-9831657
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-98316572023-01-11 Resistance to white spot syndrome virus in the European shore crab is associated with suppressed virion trafficking and heightened immune responses Millard, Rebecca S. Bickley, Lisa K. Bateman, Kelly S. Verbruggen, Bas Farbos, Audrey Lange, Anke Moore, Karen A. Stentiford, Grant D. Tyler, Charles R. van Aerle, Ronny Santos, Eduarda M. Front Immunol Immunology INTRODUCTION: All decapod crustaceans are considered potentially susceptible to White Spot Syndrome Virus (WSSV) infection, but the degree of White Spot Disease (WSD) susceptibility varies widely between species. The European shore crab Carcinus maenas can be infected with the virus for long periods of time without signs of disease. Given the high mortality rate of susceptible species, the differential susceptibility of these resistant hosts offers an opportunity to investigate mechanisms of disease resistance. METHODS: Here, the temporal transcriptional responses (mRNA and miRNA) of C. maenas following WSSV injection were analysed and compared to a previously published dataset for the highly WSSV susceptible Penaeus vannamei to identify key genes, processes and pathways contributing to increased WSD resistance. RESULTS: We show that, in contrast to P. vannamei, the transcriptional response during the first 2 days following WSSV injection in C. maenas is limited. During the later time points (7 days onwards), two groups of crabs were identified, a recalcitrant group where no replication of the virus occurred, and a group where significant viral replication occurred, with the transcriptional profiles of the latter group resembling those of WSSV-susceptible species. We identify key differences in the molecular responses of these groups to WSSV injection. DISCUSSION: We propose that increased WSD resistance in C. maenas may result from impaired WSSV endocytosis due to the inhibition of internal vesicle budding by dynamin-1, and a delay in movement to the nucleus caused by the downregulation of cytoskeletal transcripts required for WSSV cytoskeleton docking, during early stages of the infection. This response allows resistant hosts greater time to fine-tune immune responses associated with miRNA expression, apoptosis and the melanisation cascade to defend against, and clear, invading WSSV. These findings suggest that the initial stages of infection are key to resistance to WSSV in the crab and highlight possible pathways that could be targeted in farmed crustacean to enhance resistance to WSD. Frontiers Media S.A. 2022-12-27 /pmc/articles/PMC9831657/ /pubmed/36636327 http://dx.doi.org/10.3389/fimmu.2022.1057421 Text en Copyright © 2022 Millard, Bickley, Bateman, Verbruggen, Farbos, Lange, Moore, Stentiford, Tyler, van Aerle and Santos https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Millard, Rebecca S.
Bickley, Lisa K.
Bateman, Kelly S.
Verbruggen, Bas
Farbos, Audrey
Lange, Anke
Moore, Karen A.
Stentiford, Grant D.
Tyler, Charles R.
van Aerle, Ronny
Santos, Eduarda M.
Resistance to white spot syndrome virus in the European shore crab is associated with suppressed virion trafficking and heightened immune responses
title Resistance to white spot syndrome virus in the European shore crab is associated with suppressed virion trafficking and heightened immune responses
title_full Resistance to white spot syndrome virus in the European shore crab is associated with suppressed virion trafficking and heightened immune responses
title_fullStr Resistance to white spot syndrome virus in the European shore crab is associated with suppressed virion trafficking and heightened immune responses
title_full_unstemmed Resistance to white spot syndrome virus in the European shore crab is associated with suppressed virion trafficking and heightened immune responses
title_short Resistance to white spot syndrome virus in the European shore crab is associated with suppressed virion trafficking and heightened immune responses
title_sort resistance to white spot syndrome virus in the european shore crab is associated with suppressed virion trafficking and heightened immune responses
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9831657/
https://www.ncbi.nlm.nih.gov/pubmed/36636327
http://dx.doi.org/10.3389/fimmu.2022.1057421
work_keys_str_mv AT millardrebeccas resistancetowhitespotsyndromevirusintheeuropeanshorecrabisassociatedwithsuppressedviriontraffickingandheightenedimmuneresponses
AT bickleylisak resistancetowhitespotsyndromevirusintheeuropeanshorecrabisassociatedwithsuppressedviriontraffickingandheightenedimmuneresponses
AT batemankellys resistancetowhitespotsyndromevirusintheeuropeanshorecrabisassociatedwithsuppressedviriontraffickingandheightenedimmuneresponses
AT verbruggenbas resistancetowhitespotsyndromevirusintheeuropeanshorecrabisassociatedwithsuppressedviriontraffickingandheightenedimmuneresponses
AT farbosaudrey resistancetowhitespotsyndromevirusintheeuropeanshorecrabisassociatedwithsuppressedviriontraffickingandheightenedimmuneresponses
AT langeanke resistancetowhitespotsyndromevirusintheeuropeanshorecrabisassociatedwithsuppressedviriontraffickingandheightenedimmuneresponses
AT moorekarena resistancetowhitespotsyndromevirusintheeuropeanshorecrabisassociatedwithsuppressedviriontraffickingandheightenedimmuneresponses
AT stentifordgrantd resistancetowhitespotsyndromevirusintheeuropeanshorecrabisassociatedwithsuppressedviriontraffickingandheightenedimmuneresponses
AT tylercharlesr resistancetowhitespotsyndromevirusintheeuropeanshorecrabisassociatedwithsuppressedviriontraffickingandheightenedimmuneresponses
AT vanaerleronny resistancetowhitespotsyndromevirusintheeuropeanshorecrabisassociatedwithsuppressedviriontraffickingandheightenedimmuneresponses
AT santoseduardam resistancetowhitespotsyndromevirusintheeuropeanshorecrabisassociatedwithsuppressedviriontraffickingandheightenedimmuneresponses