Differential immune gene response in gills, skin, and spleen of rainbow trout Oncorhynchus mykiss infected by Ichthyophthirius multifiliis

Khairul Syahputra; Per W Kania; Azmi Al-Jubury; Huria Marnis; Agung Cahyo Setyawan; Kurt Buchmann

doi:10.1371/journal.pone.0218630

Differential immune gene response in gills, skin, and spleen of rainbow trout Oncorhynchus mykiss infected by Ichthyophthirius multifiliis

Khairul Syahputra, Per W Kania, Azmi Al-Jubury, Huria Marnis, Agung Cahyo Setyawan, Kurt Buchmann

14 Citations (Scopus)

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Abstract

Infection of rainbow trout with the parasitic ciliate Ichthyopthirius multifiliis induces differential responses in gills, skin and spleen. A controlled experimental infection was performed and expression of immune-relevant genes in skin, gills, and spleen were recorded by qPCR at day 1 and 8 after parasite exposure. Infection induced a marked reaction involving regulation of innate and adaptive immune genes in rainbow trout at day 8 post-infection. The expression level of a total of 22 out of 24 investigated genes was significantly higher in gills compared to skin reflecting the more sensitive and delicate structure of gills. Especially pro-inflammatory cytokines IL-6, IL-17 C1, regulatory cytokines IL-4/13A, IL-10, TGFβ, complement factor C5, chemokines CK10, CK12, acute phase proteins (precerebellin, hepcidin) and immunoglobulins (IgM, IgT) displayed differential expression levels. The spleen, a central immune organ with no trace of the parasite, showed elevated expression of IgM, IgT, complement factor C5 and chemokine CK10 (compared to skin and gills directly exposed to the parasite), indicating an interaction between the infected surface sites and central immune organs. This communication could be mediated by chemokines CK10 and CK12 and cytokine IL-4/13A and may at least partly explain the establishment of a systemic response in rainbow trout against the parasite.

Original language	English
Article number	e0218630
Journal	PLoS ONE
Volume	14
Issue number	6
Number of pages	14
ISSN	1932-6203
DOIs	https://doi.org/10.1371/journal.pone.0218630
Publication status	Published - Jun 2019

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Differential immune gene response in gills, skin, and spleen of rainbow trout Oncorhynchus mykiss infected by Ichthyophthirius multifiliisFinal published version, 1.84 MBLicence: CC BY

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@article{cf009f2aa74e4d379e9823bb51e0a9ff,

title = "Differential immune gene response in gills, skin, and spleen of rainbow trout Oncorhynchus mykiss infected by Ichthyophthirius multifiliis",

abstract = "Infection of rainbow trout with the parasitic ciliate Ichthyopthirius multifiliis induces differential responses in gills, skin and spleen. A controlled experimental infection was performed and expression of immune-relevant genes in skin, gills, and spleen were recorded by qPCR at day 1 and 8 after parasite exposure. Infection induced a marked reaction involving regulation of innate and adaptive immune genes in rainbow trout at day 8 post-infection. The expression level of a total of 22 out of 24 investigated genes was significantly higher in gills compared to skin reflecting the more sensitive and delicate structure of gills. Especially pro-inflammatory cytokines IL-6, IL-17 C1, regulatory cytokines IL-4/13A, IL-10, TGFβ, complement factor C5, chemokines CK10, CK12, acute phase proteins (precerebellin, hepcidin) and immunoglobulins (IgM, IgT) displayed differential expression levels. The spleen, a central immune organ with no trace of the parasite, showed elevated expression of IgM, IgT, complement factor C5 and chemokine CK10 (compared to skin and gills directly exposed to the parasite), indicating an interaction between the infected surface sites and central immune organs. This communication could be mediated by chemokines CK10 and CK12 and cytokine IL-4/13A and may at least partly explain the establishment of a systemic response in rainbow trout against the parasite.",

author = "Khairul Syahputra and Kania, {Per W} and Azmi Al-Jubury and Huria Marnis and Setyawan, {Agung Cahyo} and Kurt Buchmann",

year = "2019",

month = jun,

doi = "10.1371/journal.pone.0218630",

language = "English",

volume = "14",

journal = "PLoS ONE",

issn = "1932-6203",

publisher = "Public Library of Science",

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TY - JOUR

T1 - Differential immune gene response in gills, skin, and spleen of rainbow trout Oncorhynchus mykiss infected by Ichthyophthirius multifiliis

AU - Syahputra, Khairul

AU - Kania, Per W

AU - Al-Jubury, Azmi

AU - Marnis, Huria

AU - Setyawan, Agung Cahyo

AU - Buchmann, Kurt

PY - 2019/6

Y1 - 2019/6

N2 - Infection of rainbow trout with the parasitic ciliate Ichthyopthirius multifiliis induces differential responses in gills, skin and spleen. A controlled experimental infection was performed and expression of immune-relevant genes in skin, gills, and spleen were recorded by qPCR at day 1 and 8 after parasite exposure. Infection induced a marked reaction involving regulation of innate and adaptive immune genes in rainbow trout at day 8 post-infection. The expression level of a total of 22 out of 24 investigated genes was significantly higher in gills compared to skin reflecting the more sensitive and delicate structure of gills. Especially pro-inflammatory cytokines IL-6, IL-17 C1, regulatory cytokines IL-4/13A, IL-10, TGFβ, complement factor C5, chemokines CK10, CK12, acute phase proteins (precerebellin, hepcidin) and immunoglobulins (IgM, IgT) displayed differential expression levels. The spleen, a central immune organ with no trace of the parasite, showed elevated expression of IgM, IgT, complement factor C5 and chemokine CK10 (compared to skin and gills directly exposed to the parasite), indicating an interaction between the infected surface sites and central immune organs. This communication could be mediated by chemokines CK10 and CK12 and cytokine IL-4/13A and may at least partly explain the establishment of a systemic response in rainbow trout against the parasite.

AB - Infection of rainbow trout with the parasitic ciliate Ichthyopthirius multifiliis induces differential responses in gills, skin and spleen. A controlled experimental infection was performed and expression of immune-relevant genes in skin, gills, and spleen were recorded by qPCR at day 1 and 8 after parasite exposure. Infection induced a marked reaction involving regulation of innate and adaptive immune genes in rainbow trout at day 8 post-infection. The expression level of a total of 22 out of 24 investigated genes was significantly higher in gills compared to skin reflecting the more sensitive and delicate structure of gills. Especially pro-inflammatory cytokines IL-6, IL-17 C1, regulatory cytokines IL-4/13A, IL-10, TGFβ, complement factor C5, chemokines CK10, CK12, acute phase proteins (precerebellin, hepcidin) and immunoglobulins (IgM, IgT) displayed differential expression levels. The spleen, a central immune organ with no trace of the parasite, showed elevated expression of IgM, IgT, complement factor C5 and chemokine CK10 (compared to skin and gills directly exposed to the parasite), indicating an interaction between the infected surface sites and central immune organs. This communication could be mediated by chemokines CK10 and CK12 and cytokine IL-4/13A and may at least partly explain the establishment of a systemic response in rainbow trout against the parasite.

U2 - 10.1371/journal.pone.0218630

DO - 10.1371/journal.pone.0218630

M3 - Journal article

C2 - 31220151

SN - 1932-6203

VL - 14

JO - PLoS ONE

JF - PLoS ONE

IS - 6

M1 - e0218630

ER -

Differential immune gene response in gills, skin, and spleen of rainbow trout Oncorhynchus mykiss infected by Ichthyophthirius multifiliis

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