Sequence and expression analysis of rainbow trout CXCR2, CXCR3a and CXCR3b aids interpretation of lineage-specific conversion, loss and expansion of these receptors during vertebrate evolution

Qiaoqing Xu, Ronggai Li, Milena M Monte, Yousheng Jiang, Pin Nie, Jason W Holland, Christopher John Secombes, Tiehui Wang

Research output: Contribution to journalArticle

35 Citations (Scopus)

Abstract

The chemokine receptors CXCR1-3 bind to 11 chemokines (CXCL1-11) that are clustered on the same chromosome in mammals but are largely missing in ray-finned fish. A second CXCR1/2, and a CXCR3a and CXCR3b gene have been cloned in rainbow trout. Analysis of CXCR1-R3 genes in lobe-finned fish, ray-finned fish and tetrapod genomes revealed that the teleostomian ancestor likely possessed loci containing both CXCR1 and CXCR2, and CXCR3a and CXCR3b. Based on this synteny analysis the first trout CXCR1/2 gene was renamed CXCR1, and the new gene CXCR2. The CXCR1/R2 locus was shown to have further expanded in ray-finned fish. In relation to CXCR3, mammals appear to have lost CXCR3b and birds both CXCR3a and CXCR3b during evolution. Trout CXCR1-R3 have distinct tissue expression patterns and are differentially modulated by PAMPs, proinflammatory cytokines and infections. They are highly expressed in macrophages and neutrophils, with CXCR1 and CXCR2 also expressed in B-cells.

Original languageEnglish
Pages (from-to)201-213
Number of pages13
JournalDevelopmental and Comparative Immunology
Volume45
Issue number2
Early online date12 Mar 2014
DOIs
Publication statusPublished - Aug 2014

Fingerprint

Oncorhynchus mykiss
Skates (Fish)
Sequence Analysis
Vertebrates
Trout
Genes
Mammals
Chemokine CXCL1
Synteny
Chemokine Receptors
Birds
Fishes
Neutrophils
B-Lymphocytes
Chromosomes
Macrophages
Genome
Cytokines
Infection

Keywords

  • rainbow trout
  • CXCR2
  • CXCR3a
  • CXCR3b
  • evolution
  • expression

Cite this

@article{594b2e07412f4cbc87a89481e483617c,
title = "Sequence and expression analysis of rainbow trout CXCR2, CXCR3a and CXCR3b aids interpretation of lineage-specific conversion, loss and expansion of these receptors during vertebrate evolution",
abstract = "The chemokine receptors CXCR1-3 bind to 11 chemokines (CXCL1-11) that are clustered on the same chromosome in mammals but are largely missing in ray-finned fish. A second CXCR1/2, and a CXCR3a and CXCR3b gene have been cloned in rainbow trout. Analysis of CXCR1-R3 genes in lobe-finned fish, ray-finned fish and tetrapod genomes revealed that the teleostomian ancestor likely possessed loci containing both CXCR1 and CXCR2, and CXCR3a and CXCR3b. Based on this synteny analysis the first trout CXCR1/2 gene was renamed CXCR1, and the new gene CXCR2. The CXCR1/R2 locus was shown to have further expanded in ray-finned fish. In relation to CXCR3, mammals appear to have lost CXCR3b and birds both CXCR3a and CXCR3b during evolution. Trout CXCR1-R3 have distinct tissue expression patterns and are differentially modulated by PAMPs, proinflammatory cytokines and infections. They are highly expressed in macrophages and neutrophils, with CXCR1 and CXCR2 also expressed in B-cells.",
keywords = "rainbow trout, CXCR2, CXCR3a, CXCR3b, evolution, expression",
author = "Qiaoqing Xu and Ronggai Li and Monte, {Milena M} and Yousheng Jiang and Pin Nie and Holland, {Jason W} and Secombes, {Christopher John} and Tiehui Wang",
note = "Copyright {\circledC} 2014 The Authors. Published by Elsevier Ltd.. All rights reserved. Open Access funded by Biotechnology and Biological Sciences Research Council This work received funding from the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland). MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions. Q.X. and Y.J. were supported financially by the National Scholarship Council of China, J.W.H by the Biotechnology and Biological Sciences Research Council (BB/K009125/1), and M.M.M. by European Commision LIFECYCLE project (222919).",
year = "2014",
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T1 - Sequence and expression analysis of rainbow trout CXCR2, CXCR3a and CXCR3b aids interpretation of lineage-specific conversion, loss and expansion of these receptors during vertebrate evolution

AU - Xu, Qiaoqing

AU - Li, Ronggai

AU - Monte, Milena M

AU - Jiang, Yousheng

AU - Nie, Pin

AU - Holland, Jason W

AU - Secombes, Christopher John

AU - Wang, Tiehui

N1 - Copyright © 2014 The Authors. Published by Elsevier Ltd.. All rights reserved. Open Access funded by Biotechnology and Biological Sciences Research Council This work received funding from the MASTS pooling initiative (The Marine Alliance for Science and Technology for Scotland). MASTS is funded by the Scottish Funding Council (grant reference HR09011) and contributing institutions. Q.X. and Y.J. were supported financially by the National Scholarship Council of China, J.W.H by the Biotechnology and Biological Sciences Research Council (BB/K009125/1), and M.M.M. by European Commision LIFECYCLE project (222919).

PY - 2014/8

Y1 - 2014/8

N2 - The chemokine receptors CXCR1-3 bind to 11 chemokines (CXCL1-11) that are clustered on the same chromosome in mammals but are largely missing in ray-finned fish. A second CXCR1/2, and a CXCR3a and CXCR3b gene have been cloned in rainbow trout. Analysis of CXCR1-R3 genes in lobe-finned fish, ray-finned fish and tetrapod genomes revealed that the teleostomian ancestor likely possessed loci containing both CXCR1 and CXCR2, and CXCR3a and CXCR3b. Based on this synteny analysis the first trout CXCR1/2 gene was renamed CXCR1, and the new gene CXCR2. The CXCR1/R2 locus was shown to have further expanded in ray-finned fish. In relation to CXCR3, mammals appear to have lost CXCR3b and birds both CXCR3a and CXCR3b during evolution. Trout CXCR1-R3 have distinct tissue expression patterns and are differentially modulated by PAMPs, proinflammatory cytokines and infections. They are highly expressed in macrophages and neutrophils, with CXCR1 and CXCR2 also expressed in B-cells.

AB - The chemokine receptors CXCR1-3 bind to 11 chemokines (CXCL1-11) that are clustered on the same chromosome in mammals but are largely missing in ray-finned fish. A second CXCR1/2, and a CXCR3a and CXCR3b gene have been cloned in rainbow trout. Analysis of CXCR1-R3 genes in lobe-finned fish, ray-finned fish and tetrapod genomes revealed that the teleostomian ancestor likely possessed loci containing both CXCR1 and CXCR2, and CXCR3a and CXCR3b. Based on this synteny analysis the first trout CXCR1/2 gene was renamed CXCR1, and the new gene CXCR2. The CXCR1/R2 locus was shown to have further expanded in ray-finned fish. In relation to CXCR3, mammals appear to have lost CXCR3b and birds both CXCR3a and CXCR3b during evolution. Trout CXCR1-R3 have distinct tissue expression patterns and are differentially modulated by PAMPs, proinflammatory cytokines and infections. They are highly expressed in macrophages and neutrophils, with CXCR1 and CXCR2 also expressed in B-cells.

KW - rainbow trout

KW - CXCR2

KW - CXCR3a

KW - CXCR3b

KW - evolution

KW - expression

U2 - 10.1016/j.dci.2014.03.002

DO - 10.1016/j.dci.2014.03.002

M3 - Article

VL - 45

SP - 201

EP - 213

JO - Developmental and Comparative Immunology

JF - Developmental and Comparative Immunology

SN - 0145-305X

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