Induction of IL-22 protein and IL-22-producing cells in rainbow trout Oncorhynchus mykiss

Yehfang Hu; Yamila Carpio; Callum Scott; Ayham Alnabulsi; Abdo Alnabulsi; Tingyu Wang; Fuguo Liu; Milena Monte; Tiehui Wang; Christopher Secombes

doi:10.1016/j.dci.2019.103449

Induction of IL-22 protein and IL-22-producing cells in rainbow trout Oncorhynchus mykiss

Yehfang Hu, Yamila Carpio, Callum Scott, Ayham Alnabulsi, Abdo Alnabulsi, Tingyu Wang, Fuguo Liu, Milena Monte, Tiehui Wang, Christopher Secombes^* (Corresponding Author)

^*Corresponding author for this work

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Abstract

IL-22 is a critical cytokine which is involved in modulating tissue responses during inflammation, and is produced mainly by T cells and innate leucocytes. In mammals, IL-22 is a key component in mucosal defences, tissue repair, epithelial cell survival and proliferation. In teleosts, IL-22 has been cloned and studied in several species, and the transcript is highly expressed in mucosal tissues and induced by pathogen associated molecular patterns (PAMPs), suggesting IL-22 also functions as an important component of the innate immune response in fish. To investigate these immune responses further, we have validated and characterised two monoclonal antibodies (mAbs) which were raised against two different peptide immunogens of salmonid IL-22. Our results show that both mAbs specifically react to their own peptide immunogens and recombinant IL-22, and are able to detect the induction of native protein expression after stimulation. In flow cytometry, an increase in IL-22 positive cells was detected after stimulation in vitro with cytokines and PAMPs and in vivo after bacterial challenge. The immunohistochemistry results showed that IL-22 is highly upregulated in the gills after challenge, both in cells within the gill filaments and in the interbranchial lymphoid tissue. Such results suggest IL-22 may have a role in triggering local antimicrobial defences in fish that may facilitate efficient microbial clearance. Hence monitoring IL-22 producing cells/protein secretion may provide an alternative mean to assess the effectiveness of mucosal vaccines.

Original language	English
Article number	103449
Number of pages	12
Journal	Developmental and Comparative Immunology
Volume	101
Early online date	25 Jul 2019
DOIs	https://doi.org/10.1016/j.dci.2019.103449
Publication status	Published - Dec 2019

Bibliographical note

This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC, BB/N024052/1 and BB/R008442/1). This research was also funded by the European Commission under the 7th Framework Programme for Research and Technological Development (FP7) of the European Union (grant agreement No. 311993 TARGETFISH). YH was supported by a PhD Studentship from the Ministry of Education, Republic of China (Taiwan). Tingyu Wang was supported by the Ministry of Science and Technology, Republic of China (Taiwan) (MOST 107-2917-I-564-019). Fuguo Liu was supported by a Newton International Fellowship funded by the Academy of Medical Sciences, UK (AMS, NIF004\1036). Thanks also go to Dr. Dawn Shewring for excellent technical assistance and to Dr. Alex Douglas and Ms. Anna Harte for statistical advice.

Keywords

rainbow trout
interleukin-22
transcript expression
protein expression
monoclonal antibody
molecular characterization
aeromonas-salmonicida
functional-characterization
IMMUNE GENE-EXPRESSION
inflammation
YERSINIA-RUCKERI INFECTION
host-defense
fish
INTERLEUKIN (IL)-22
Atlantic salmon

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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@article{c9e72b68d8b0452cad959e61ad729e36,

title = "Induction of IL-22 protein and IL-22-producing cells in rainbow trout Oncorhynchus mykiss",

abstract = "IL-22 is a critical cytokine which is involved in modulating tissue responses during inflammation, and is produced mainly by T cells and innate leucocytes. In mammals, IL-22 is a key component in mucosal defences, tissue repair, epithelial cell survival and proliferation. In teleosts, IL-22 has been cloned and studied in several species, and the transcript is highly expressed in mucosal tissues and induced by pathogen associated molecular patterns (PAMPs), suggesting IL-22 also functions as an important component of the innate immune response in fish. To investigate these immune responses further, we have validated and characterised two monoclonal antibodies (mAbs) which were raised against two different peptide immunogens of salmonid IL-22. Our results show that both mAbs specifically react to their own peptide immunogens and recombinant IL-22, and are able to detect the induction of native protein expression after stimulation. In flow cytometry, an increase in IL-22 positive cells was detected after stimulation in vitro with cytokines and PAMPs and in vivo after bacterial challenge. The immunohistochemistry results showed that IL-22 is highly upregulated in the gills after challenge, both in cells within the gill filaments and in the interbranchial lymphoid tissue. Such results suggest IL-22 may have a role in triggering local antimicrobial defences in fish that may facilitate efficient microbial clearance. Hence monitoring IL-22 producing cells/protein secretion may provide an alternative mean to assess the effectiveness of mucosal vaccines.",

keywords = "rainbow trout, interleukin-22, transcript expression, protein expression, monoclonal antibody, molecular characterization, aeromonas-salmonicida, functional-characterization, IMMUNE GENE-EXPRESSION, inflammation, YERSINIA-RUCKERI INFECTION, host-defense, fish, INTERLEUKIN (IL)-22, Atlantic salmon",

author = "Yehfang Hu and Yamila Carpio and Callum Scott and Ayham Alnabulsi and Abdo Alnabulsi and Tingyu Wang and Fuguo Liu and Milena Monte and Tiehui Wang and Christopher Secombes",

note = "This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC, BB/N024052/1 and BB/R008442/1). This research was also funded by the European Commission under the 7th Framework Programme for Research and Technological Development (FP7) of the European Union (grant agreement No. 311993 TARGETFISH). YH was supported by a PhD Studentship from the Ministry of Education, Republic of China (Taiwan). Tingyu Wang was supported by the Ministry of Science and Technology, Republic of China (Taiwan) (MOST 107-2917-I-564-019). Fuguo Liu was supported by a Newton International Fellowship funded by the Academy of Medical Sciences, UK (AMS, NIF004\1036). Thanks also go to Dr. Dawn Shewring for excellent technical assistance and to Dr. Alex Douglas and Ms. Anna Harte for statistical advice.",

year = "2019",

month = dec,

doi = "10.1016/j.dci.2019.103449",

language = "English",

volume = "101",

journal = "Developmental and Comparative Immunology",

issn = "0145-305X",

publisher = "Elsevier Limited",

}

TY - JOUR

T1 - Induction of IL-22 protein and IL-22-producing cells in rainbow trout Oncorhynchus mykiss

AU - Hu, Yehfang

AU - Carpio, Yamila

AU - Scott, Callum

AU - Alnabulsi, Ayham

AU - Alnabulsi, Abdo

AU - Wang, Tingyu

AU - Liu, Fuguo

AU - Monte, Milena

AU - Wang, Tiehui

AU - Secombes, Christopher

N1 - This work was funded by the Biotechnology and Biological Sciences Research Council (BBSRC, BB/N024052/1 and BB/R008442/1). This research was also funded by the European Commission under the 7th Framework Programme for Research and Technological Development (FP7) of the European Union (grant agreement No. 311993 TARGETFISH). YH was supported by a PhD Studentship from the Ministry of Education, Republic of China (Taiwan). Tingyu Wang was supported by the Ministry of Science and Technology, Republic of China (Taiwan) (MOST 107-2917-I-564-019). Fuguo Liu was supported by a Newton International Fellowship funded by the Academy of Medical Sciences, UK (AMS, NIF004\1036). Thanks also go to Dr. Dawn Shewring for excellent technical assistance and to Dr. Alex Douglas and Ms. Anna Harte for statistical advice.

PY - 2019/12

Y1 - 2019/12

N2 - IL-22 is a critical cytokine which is involved in modulating tissue responses during inflammation, and is produced mainly by T cells and innate leucocytes. In mammals, IL-22 is a key component in mucosal defences, tissue repair, epithelial cell survival and proliferation. In teleosts, IL-22 has been cloned and studied in several species, and the transcript is highly expressed in mucosal tissues and induced by pathogen associated molecular patterns (PAMPs), suggesting IL-22 also functions as an important component of the innate immune response in fish. To investigate these immune responses further, we have validated and characterised two monoclonal antibodies (mAbs) which were raised against two different peptide immunogens of salmonid IL-22. Our results show that both mAbs specifically react to their own peptide immunogens and recombinant IL-22, and are able to detect the induction of native protein expression after stimulation. In flow cytometry, an increase in IL-22 positive cells was detected after stimulation in vitro with cytokines and PAMPs and in vivo after bacterial challenge. The immunohistochemistry results showed that IL-22 is highly upregulated in the gills after challenge, both in cells within the gill filaments and in the interbranchial lymphoid tissue. Such results suggest IL-22 may have a role in triggering local antimicrobial defences in fish that may facilitate efficient microbial clearance. Hence monitoring IL-22 producing cells/protein secretion may provide an alternative mean to assess the effectiveness of mucosal vaccines.

AB - IL-22 is a critical cytokine which is involved in modulating tissue responses during inflammation, and is produced mainly by T cells and innate leucocytes. In mammals, IL-22 is a key component in mucosal defences, tissue repair, epithelial cell survival and proliferation. In teleosts, IL-22 has been cloned and studied in several species, and the transcript is highly expressed in mucosal tissues and induced by pathogen associated molecular patterns (PAMPs), suggesting IL-22 also functions as an important component of the innate immune response in fish. To investigate these immune responses further, we have validated and characterised two monoclonal antibodies (mAbs) which were raised against two different peptide immunogens of salmonid IL-22. Our results show that both mAbs specifically react to their own peptide immunogens and recombinant IL-22, and are able to detect the induction of native protein expression after stimulation. In flow cytometry, an increase in IL-22 positive cells was detected after stimulation in vitro with cytokines and PAMPs and in vivo after bacterial challenge. The immunohistochemistry results showed that IL-22 is highly upregulated in the gills after challenge, both in cells within the gill filaments and in the interbranchial lymphoid tissue. Such results suggest IL-22 may have a role in triggering local antimicrobial defences in fish that may facilitate efficient microbial clearance. Hence monitoring IL-22 producing cells/protein secretion may provide an alternative mean to assess the effectiveness of mucosal vaccines.

KW - rainbow trout

KW - interleukin-22

KW - transcript expression

KW - protein expression

KW - monoclonal antibody

KW - molecular characterization

KW - aeromonas-salmonicida

KW - functional-characterization

KW - IMMUNE GENE-EXPRESSION

KW - inflammation

KW - YERSINIA-RUCKERI INFECTION

KW - host-defense

KW - fish

KW - INTERLEUKIN (IL)-22

KW - Atlantic salmon

U2 - 10.1016/j.dci.2019.103449

DO - 10.1016/j.dci.2019.103449

M3 - Article

SN - 0145-305X

VL - 101

JO - Developmental and Comparative Immunology

JF - Developmental and Comparative Immunology

M1 - 103449

ER -

Induction of IL-22 protein and IL-22-producing cells in rainbow trout Oncorhynchus mykiss

Abstract

Bibliographical note

Keywords

UN SDGs

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