Expansion of fish CCL20_like chemokines by genome and local gene duplication

Characterisation and expression analysis of 10 CCL20_like chemokines in rainbow trout (Oncorhynchus mykiss)

Fuguo Liu, Tingyu Wang, Yehfang Hu, Guangming Tian, Christopher J. Secombes* (Corresponding Author), Tiehui Wang (Corresponding Author)

*Corresponding author for this work

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Mammalian CCL20, or macrophage inflammatory protein-3α, can function as a homeostatic and inflammatory chemokine. In relation to the latter, it is responsible for the chemoattraction of lymphocytes and dendritic cells to mucosal immune sites under inflammatory and pathological conditions. CK1, CK8A and CK8B are rainbow trout (Oncorhynchus mykiss) CC chemokines that were reported previously to be phylogenetically related to mammalian CCL20. In the current study, an additional seven CCL20_L paralogues in rainbow trout are reported, that are divided into three subgroups and have been designated here as: CCL20_L1a (also referred to as CK1), CCL20_L1b1-2, CCL20_L2a (CK8A), CCL20_L2b (CK8B), CCL20_L3a, and CCL20_L3b1-4. Multiple CCL20_L genes were also identified in other salmonids that arose from both whole genome duplication and local gene duplication. Phylogenetic tree, homology and synteny analysis support that CCL20_L1-3 found in salmonids are also present in most of teleosts that arose from the 3 R whole genome duplication and in some species, local gene duplication. Like mammalian CCL20, rainbow trout CCL20_L molecules possess a high positive net charge with a pI of 9.34–10.16, that is reported to be important for antimicrobial activity. Rainbow trout CCL20_L paralogues are differentially expressed and in general highly expressed in mucosal tissues, such as gills, thymus and intestine. The expression levels of rainbow trout CCL20_L paralogues are increased during development and following PAMP/cytokine stimulation. For example, in RTS-11 cells CCL20_L3b1 and CCL20_L3b2 are highly up-regulated by LPS, Poly I:C, recombinant(r) IFNa and rIL-1β. Trout CCL20_L paralogues are also increased after Yersinia ruckeri infection or Poly I:C stimulation in vivo, with CCL20_L3b1 and CCL20_L3b2 again highly up-regulated. Overall, this is the first report of the complete CCL20 chemokine subfamily in rainbow trout, and the analysis of their expression and modulation in vitro and in vivo. These results suggest that teleosts possess divergent CCL20_L molecules that may have important roles in anti-viral/anti-bacterial defence and in mucosal immunity.
Original languageEnglish
Article number103502
JournalDevelopmental and Comparative Immunology
Volume103
Early online date27 Sep 2019
DOIs
Publication statusE-pub ahead of print - 27 Sep 2019

Fingerprint

Chemokine CCL20
Gene Duplication
Oncorhynchus mykiss
Fishes
Genome
Gene Expression
Salmonidae
Poly I-C
Yersinia ruckeri
Yersinia Infections
Synteny
Macrophage Inflammatory Proteins
CC Chemokines
Mucosal Immunity
Trout
Chemokines
Dendritic Cells
Thymus Gland
Intestines
Mucous Membrane

Keywords

  • Rainbow trout
  • CCL20_L
  • Chemokine
  • Characterisation
  • Expression
  • Mucosal immune response

ASJC Scopus subject areas

  • Immunology
  • Developmental Biology

Cite this

@article{ce7940f7d0f849bfba7569a8116369ab,
title = "Expansion of fish CCL20_like chemokines by genome and local gene duplication: Characterisation and expression analysis of 10 CCL20_like chemokines in rainbow trout (Oncorhynchus mykiss)",
abstract = "Mammalian CCL20, or macrophage inflammatory protein-3α, can function as a homeostatic and inflammatory chemokine. In relation to the latter, it is responsible for the chemoattraction of lymphocytes and dendritic cells to mucosal immune sites under inflammatory and pathological conditions. CK1, CK8A and CK8B are rainbow trout (Oncorhynchus mykiss) CC chemokines that were reported previously to be phylogenetically related to mammalian CCL20. In the current study, an additional seven CCL20_L paralogues in rainbow trout are reported, that are divided into three subgroups and have been designated here as: CCL20_L1a (also referred to as CK1), CCL20_L1b1-2, CCL20_L2a (CK8A), CCL20_L2b (CK8B), CCL20_L3a, and CCL20_L3b1-4. Multiple CCL20_L genes were also identified in other salmonids that arose from both whole genome duplication and local gene duplication. Phylogenetic tree, homology and synteny analysis support that CCL20_L1-3 found in salmonids are also present in most of teleosts that arose from the 3 R whole genome duplication and in some species, local gene duplication. Like mammalian CCL20, rainbow trout CCL20_L molecules possess a high positive net charge with a pI of 9.34–10.16, that is reported to be important for antimicrobial activity. Rainbow trout CCL20_L paralogues are differentially expressed and in general highly expressed in mucosal tissues, such as gills, thymus and intestine. The expression levels of rainbow trout CCL20_L paralogues are increased during development and following PAMP/cytokine stimulation. For example, in RTS-11 cells CCL20_L3b1 and CCL20_L3b2 are highly up-regulated by LPS, Poly I:C, recombinant(r) IFNa and rIL-1β. Trout CCL20_L paralogues are also increased after Yersinia ruckeri infection or Poly I:C stimulation in vivo, with CCL20_L3b1 and CCL20_L3b2 again highly up-regulated. Overall, this is the first report of the complete CCL20 chemokine subfamily in rainbow trout, and the analysis of their expression and modulation in vitro and in vivo. These results suggest that teleosts possess divergent CCL20_L molecules that may have important roles in anti-viral/anti-bacterial defence and in mucosal immunity.",
keywords = "Rainbow trout, CCL20_L, Chemokine, Characterisation, Expression, Mucosal immune response",
author = "Fuguo Liu and Tingyu Wang and Yehfang Hu and Guangming Tian and Secombes, {Christopher J.} and Tiehui Wang",
note = "Acknowledgements Fuguo Liu was supported by a Newton International Fellowship funded by the Academy of Medical Sciences, UK (AMS, NIF004\1036). Tingyu Wang was supported by the Ministry of Science and Technology, Republic of China (Taiwan) (MOST 107-2917-I-564-019). YH was supported by a PhD Studentship from the Ministry of Education, Republic of China. Guangming Tian was supported financially by the State Scholarship Fund organised by the China Scholarship Council (201808420042).",
year = "2019",
month = "9",
day = "27",
doi = "10.1016/j.dci.2019.103502",
language = "English",
volume = "103",
journal = "Developmental and Comparative Immunology",
issn = "0145-305X",
publisher = "Elsevier Limited",

}

TY - JOUR

T1 - Expansion of fish CCL20_like chemokines by genome and local gene duplication

T2 - Characterisation and expression analysis of 10 CCL20_like chemokines in rainbow trout (Oncorhynchus mykiss)

AU - Liu, Fuguo

AU - Wang, Tingyu

AU - Hu, Yehfang

AU - Tian, Guangming

AU - Secombes, Christopher J.

AU - Wang, Tiehui

N1 - Acknowledgements Fuguo Liu was supported by a Newton International Fellowship funded by the Academy of Medical Sciences, UK (AMS, NIF004\1036). Tingyu Wang was supported by the Ministry of Science and Technology, Republic of China (Taiwan) (MOST 107-2917-I-564-019). YH was supported by a PhD Studentship from the Ministry of Education, Republic of China. Guangming Tian was supported financially by the State Scholarship Fund organised by the China Scholarship Council (201808420042).

PY - 2019/9/27

Y1 - 2019/9/27

N2 - Mammalian CCL20, or macrophage inflammatory protein-3α, can function as a homeostatic and inflammatory chemokine. In relation to the latter, it is responsible for the chemoattraction of lymphocytes and dendritic cells to mucosal immune sites under inflammatory and pathological conditions. CK1, CK8A and CK8B are rainbow trout (Oncorhynchus mykiss) CC chemokines that were reported previously to be phylogenetically related to mammalian CCL20. In the current study, an additional seven CCL20_L paralogues in rainbow trout are reported, that are divided into three subgroups and have been designated here as: CCL20_L1a (also referred to as CK1), CCL20_L1b1-2, CCL20_L2a (CK8A), CCL20_L2b (CK8B), CCL20_L3a, and CCL20_L3b1-4. Multiple CCL20_L genes were also identified in other salmonids that arose from both whole genome duplication and local gene duplication. Phylogenetic tree, homology and synteny analysis support that CCL20_L1-3 found in salmonids are also present in most of teleosts that arose from the 3 R whole genome duplication and in some species, local gene duplication. Like mammalian CCL20, rainbow trout CCL20_L molecules possess a high positive net charge with a pI of 9.34–10.16, that is reported to be important for antimicrobial activity. Rainbow trout CCL20_L paralogues are differentially expressed and in general highly expressed in mucosal tissues, such as gills, thymus and intestine. The expression levels of rainbow trout CCL20_L paralogues are increased during development and following PAMP/cytokine stimulation. For example, in RTS-11 cells CCL20_L3b1 and CCL20_L3b2 are highly up-regulated by LPS, Poly I:C, recombinant(r) IFNa and rIL-1β. Trout CCL20_L paralogues are also increased after Yersinia ruckeri infection or Poly I:C stimulation in vivo, with CCL20_L3b1 and CCL20_L3b2 again highly up-regulated. Overall, this is the first report of the complete CCL20 chemokine subfamily in rainbow trout, and the analysis of their expression and modulation in vitro and in vivo. These results suggest that teleosts possess divergent CCL20_L molecules that may have important roles in anti-viral/anti-bacterial defence and in mucosal immunity.

AB - Mammalian CCL20, or macrophage inflammatory protein-3α, can function as a homeostatic and inflammatory chemokine. In relation to the latter, it is responsible for the chemoattraction of lymphocytes and dendritic cells to mucosal immune sites under inflammatory and pathological conditions. CK1, CK8A and CK8B are rainbow trout (Oncorhynchus mykiss) CC chemokines that were reported previously to be phylogenetically related to mammalian CCL20. In the current study, an additional seven CCL20_L paralogues in rainbow trout are reported, that are divided into three subgroups and have been designated here as: CCL20_L1a (also referred to as CK1), CCL20_L1b1-2, CCL20_L2a (CK8A), CCL20_L2b (CK8B), CCL20_L3a, and CCL20_L3b1-4. Multiple CCL20_L genes were also identified in other salmonids that arose from both whole genome duplication and local gene duplication. Phylogenetic tree, homology and synteny analysis support that CCL20_L1-3 found in salmonids are also present in most of teleosts that arose from the 3 R whole genome duplication and in some species, local gene duplication. Like mammalian CCL20, rainbow trout CCL20_L molecules possess a high positive net charge with a pI of 9.34–10.16, that is reported to be important for antimicrobial activity. Rainbow trout CCL20_L paralogues are differentially expressed and in general highly expressed in mucosal tissues, such as gills, thymus and intestine. The expression levels of rainbow trout CCL20_L paralogues are increased during development and following PAMP/cytokine stimulation. For example, in RTS-11 cells CCL20_L3b1 and CCL20_L3b2 are highly up-regulated by LPS, Poly I:C, recombinant(r) IFNa and rIL-1β. Trout CCL20_L paralogues are also increased after Yersinia ruckeri infection or Poly I:C stimulation in vivo, with CCL20_L3b1 and CCL20_L3b2 again highly up-regulated. Overall, this is the first report of the complete CCL20 chemokine subfamily in rainbow trout, and the analysis of their expression and modulation in vitro and in vivo. These results suggest that teleosts possess divergent CCL20_L molecules that may have important roles in anti-viral/anti-bacterial defence and in mucosal immunity.

KW - Rainbow trout

KW - CCL20_L

KW - Chemokine

KW - Characterisation

KW - Expression

KW - Mucosal immune response

UR - http://www.scopus.com/inward/record.url?scp=85073459956&partnerID=8YFLogxK

U2 - 10.1016/j.dci.2019.103502

DO - 10.1016/j.dci.2019.103502

M3 - Article

VL - 103

JO - Developmental and Comparative Immunology

JF - Developmental and Comparative Immunology

SN - 0145-305X

M1 - 103502

ER -