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; Chris J. Secombes; Tiehui Wang

doi:10.1016/j.dci.2014.03.002

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, Chris J. Secombes^*, Tiehui Wang

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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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 OCCR1 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. (C) 2014 The Authors. Published by Elsevier Ltd.

Original language	English
Pages (from-to)	201-213
Number of pages	13
Journal	Developmental and Comparative Immunology
Volume	45
Issue number	2
Early online date	12 Mar 2014
DOIs	https://doi.org/10.1016/j.dci.2014.03.002
Publication status	Published - Aug 2014

Bibliographical note

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).

Keywords

Rainbow trout
OCCR2
OCCR3a
CXCR3b
Evolution
Expression
PROLIFERATIVE KIDNEY-DISEASE
ONCORHYNCHUS-MYKISS
CHEMOKINE RECEPTORS
TELEOST FISH
MOLECULAR-CLONING
SALMO-GAIRDNERI
GENE
INTERLEUKIN-8
NEUTROPHILS
PROTEIN

UN SDGs

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

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This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/)
Final published version, 1.86 MBLicence: CC BY

Jason Holland
- Biological Sciences, Aberdeen Centre For Environmental Sustainability - Lecturer
- Biological Sciences, Scottish Fish Immunology Research Centre
Person: Academic

Cite this

Xu, Q., Li, R., Monte, M. M., Jiang, Y., Nie, P., Holland, J. W., Secombes, C. J., & Wang, T. (2014). 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. Developmental and Comparative Immunology, 45(2), 201-213. https://doi.org/10.1016/j.dci.2014.03.002

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. / Xu, Qiaoqing; Li, Ronggai; Monte, Milena M. et al.
In: Developmental and Comparative Immunology, Vol. 45, No. 2, 08.2014, p. 201-213.

Research output: Contribution to journal › Article › peer-review

Xu, Q, Li, R, Monte, MM, Jiang, Y, Nie, P, Holland, JW , Secombes, CJ & Wang, T 2014, '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', Developmental and Comparative Immunology, vol. 45, no. 2, pp. 201-213. https://doi.org/10.1016/j.dci.2014.03.002

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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 OCCR1 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. (C) 2014 The Authors. Published by Elsevier Ltd.",

keywords = "Rainbow trout, OCCR2, OCCR3a, CXCR3b, Evolution, Expression, PROLIFERATIVE KIDNEY-DISEASE, ONCORHYNCHUS-MYKISS, CHEMOKINE RECEPTORS, TELEOST FISH, MOLECULAR-CLONING, SALMO-GAIRDNERI, GENE, INTERLEUKIN-8, NEUTROPHILS, PROTEIN",

author = "Qiaoqing Xu and Ronggai Li and Monte, {Milena M.} and Yousheng Jiang and Pin Nie and Holland, {Jason W.} and Secombes, {Chris J.} and Tiehui Wang",

note = "Copyright {\textcopyright} 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).",

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AU - Xu, Qiaoqing

AU - Li, Ronggai

AU - Monte, Milena M.

AU - Jiang, Yousheng

AU - Nie, Pin

AU - Holland, Jason W.

AU - Secombes, Chris J.

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

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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 OCCR1 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. (C) 2014 The Authors. Published by Elsevier Ltd.

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 OCCR1 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. (C) 2014 The Authors. Published by Elsevier Ltd.

KW - Rainbow trout

KW - OCCR2

KW - OCCR3a

KW - CXCR3b

KW - Evolution

KW - Expression

KW - PROLIFERATIVE KIDNEY-DISEASE

KW - ONCORHYNCHUS-MYKISS

KW - CHEMOKINE RECEPTORS

KW - TELEOST FISH

KW - MOLECULAR-CLONING

KW - SALMO-GAIRDNERI

KW - GENE

KW - INTERLEUKIN-8

KW - NEUTROPHILS

KW - PROTEIN

U2 - 10.1016/j.dci.2014.03.002

DO - 10.1016/j.dci.2014.03.002

M3 - Article

C2 - 24613851

SN - 0145-305X

VL - 45

SP - 201

EP - 213

JO - Developmental and Comparative Immunology

JF - Developmental and Comparative Immunology

IS - 2

ER -

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

Bibliographical note

Keywords

UN SDGs

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Jason Holland

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