Functional role of TrIL-1β in Takifugu rubripes defense against Cryptocaryon irritans infection.

The Japanese puffer, Takifugu rubripes, is a commercially important fish species in China that is under serious threat from white spot disease (cyptocaryoniasis), which leads to heavy economic losses. We previously found that interleukin-1β (IL-1β), an important cytokine with a potential role in res...

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Published in:International Journal of Biological Macromolecules
Main Authors: Cheng, Jian-Xin, Liu, Peng-Fei, Yang, Yi, Liu, Yan-Yun, Xia, Yu-Qing
Format: Article in Journal/Newspaper
Language:English
Published: Elsevier Science 2024
Subjects:
Online Access:https://doi.org/10.1016/j.ijbiomac.2024.132167
https://pubmed.ncbi.nlm.nih.gov/38729479
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spelling ftpubmed:38729479 2024-06-09T07:44:50+00:00 Functional role of TrIL-1β in Takifugu rubripes defense against Cryptocaryon irritans infection. Cheng, Jian-Xin Liu, Peng-Fei Yang, Yi Liu, Yan-Yun Xia, Yu-Qing 2024 May 08 https://doi.org/10.1016/j.ijbiomac.2024.132167 https://pubmed.ncbi.nlm.nih.gov/38729479 eng eng Elsevier Science https://doi.org/10.1016/j.ijbiomac.2024.132167 https://pubmed.ncbi.nlm.nih.gov/38729479 Copyright © 2024 Elsevier B.V. All rights reserved. Int J Biol Macromol ISSN:1879-0003 Volume:269 Issue:Pt 2 Cryptocaryon irritans Cytokines Immunofluorescence experiments Recombinant IL-1β Takifugu rubripes Transmission electron microscopy Journal Article 2024 ftpubmed https://doi.org/10.1016/j.ijbiomac.2024.132167 2024-05-16T16:03:00Z The Japanese puffer, Takifugu rubripes, is a commercially important fish species in China that is under serious threat from white spot disease (cyptocaryoniasis), which leads to heavy economic losses. We previously found that interleukin-1β (IL-1β), an important cytokine with a potential role in resistance against pathogens, was one of the most significantly differentially up-regulated proteins in the gills and spleen of T. rubripes infected by the protozoan parasite Cryptocaryon irritans. In this study, we assessed the potential function of T. rubripes IL-1β (TrIL-1β) in fish infected with C. irritans. Phylogenetic analysis indicated that the TrIL-1β protein sequence was most closely related to that of Atlantic salmon (Salmo salar) (67.2 %). The incubation experiments revealed that TrIL-1β may reduce trophont activity by destroying membranes. Immunofluorescence experiments showed that recombinant TrIL-1β promoted the expression of endogenous IL-1β, which penetrated and disrupted the cell membranes of trophonts. Transmission electron microscopy showed that the IL-1β group had less tissue damage compared with control groups of fish. IL-1β-small interfering RNA and IL-1β overexpression experiments were performed in head kidney primary cells, and challenge experiments were performed in vitro. Quantitative RT-PCR results showed that TrIL-1β regulated and activated MyD88/NF-κB and MyD88/MAPK/p38 signaling pathways during C. irritans infection. TrIL-1β also promoted the differential expression of IgM, showing that it was involved in humoral immunity of T. rubripes. The cumulative mortality experiment show that TrIL-1β could protect fish against C. irritans infection. These results enrich current knowledge about the molecular structure of TrIL-1β. They also suggested that recombinant TrIL-1β could be used as an adjuvant in a subunit vaccine against C. irritans infection, which is of profound importance for the prevention and control of parasitic diseases in T. rubripes. Article in Journal/Newspaper Atlantic salmon Salmo salar PubMed Central (PMC) International Journal of Biological Macromolecules 269 132167
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Cryptocaryon irritans
Cytokines
Immunofluorescence experiments
Recombinant IL-1β
Takifugu rubripes
Transmission electron microscopy
spellingShingle Cryptocaryon irritans
Cytokines
Immunofluorescence experiments
Recombinant IL-1β
Takifugu rubripes
Transmission electron microscopy
Cheng, Jian-Xin
Liu, Peng-Fei
Yang, Yi
Liu, Yan-Yun
Xia, Yu-Qing
Functional role of TrIL-1β in Takifugu rubripes defense against Cryptocaryon irritans infection.
topic_facet Cryptocaryon irritans
Cytokines
Immunofluorescence experiments
Recombinant IL-1β
Takifugu rubripes
Transmission electron microscopy
description The Japanese puffer, Takifugu rubripes, is a commercially important fish species in China that is under serious threat from white spot disease (cyptocaryoniasis), which leads to heavy economic losses. We previously found that interleukin-1β (IL-1β), an important cytokine with a potential role in resistance against pathogens, was one of the most significantly differentially up-regulated proteins in the gills and spleen of T. rubripes infected by the protozoan parasite Cryptocaryon irritans. In this study, we assessed the potential function of T. rubripes IL-1β (TrIL-1β) in fish infected with C. irritans. Phylogenetic analysis indicated that the TrIL-1β protein sequence was most closely related to that of Atlantic salmon (Salmo salar) (67.2 %). The incubation experiments revealed that TrIL-1β may reduce trophont activity by destroying membranes. Immunofluorescence experiments showed that recombinant TrIL-1β promoted the expression of endogenous IL-1β, which penetrated and disrupted the cell membranes of trophonts. Transmission electron microscopy showed that the IL-1β group had less tissue damage compared with control groups of fish. IL-1β-small interfering RNA and IL-1β overexpression experiments were performed in head kidney primary cells, and challenge experiments were performed in vitro. Quantitative RT-PCR results showed that TrIL-1β regulated and activated MyD88/NF-κB and MyD88/MAPK/p38 signaling pathways during C. irritans infection. TrIL-1β also promoted the differential expression of IgM, showing that it was involved in humoral immunity of T. rubripes. The cumulative mortality experiment show that TrIL-1β could protect fish against C. irritans infection. These results enrich current knowledge about the molecular structure of TrIL-1β. They also suggested that recombinant TrIL-1β could be used as an adjuvant in a subunit vaccine against C. irritans infection, which is of profound importance for the prevention and control of parasitic diseases in T. rubripes.
format Article in Journal/Newspaper
author Cheng, Jian-Xin
Liu, Peng-Fei
Yang, Yi
Liu, Yan-Yun
Xia, Yu-Qing
author_facet Cheng, Jian-Xin
Liu, Peng-Fei
Yang, Yi
Liu, Yan-Yun
Xia, Yu-Qing
author_sort Cheng, Jian-Xin
title Functional role of TrIL-1β in Takifugu rubripes defense against Cryptocaryon irritans infection.
title_short Functional role of TrIL-1β in Takifugu rubripes defense against Cryptocaryon irritans infection.
title_full Functional role of TrIL-1β in Takifugu rubripes defense against Cryptocaryon irritans infection.
title_fullStr Functional role of TrIL-1β in Takifugu rubripes defense against Cryptocaryon irritans infection.
title_full_unstemmed Functional role of TrIL-1β in Takifugu rubripes defense against Cryptocaryon irritans infection.
title_sort functional role of tril-1β in takifugu rubripes defense against cryptocaryon irritans infection.
publisher Elsevier Science
publishDate 2024
url https://doi.org/10.1016/j.ijbiomac.2024.132167
https://pubmed.ncbi.nlm.nih.gov/38729479
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source Int J Biol Macromol
ISSN:1879-0003
Volume:269
Issue:Pt 2
op_relation https://doi.org/10.1016/j.ijbiomac.2024.132167
https://pubmed.ncbi.nlm.nih.gov/38729479
op_rights Copyright © 2024 Elsevier B.V. All rights reserved.
op_doi https://doi.org/10.1016/j.ijbiomac.2024.132167
container_title International Journal of Biological Macromolecules
container_volume 269
container_start_page 132167
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