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; Mira Monte, Milenaet al.
2014 • In Developmental and Comparative Immunology, 45 (2), p. 201-13
Amino Acid Sequence; Animals; Evolution, Molecular; Fish Diseases/immunology/microbiology/parasitology; Fish Proteins/genetics/immunology; Head Kidney/immunology; Humans; Infection/immunology/microbiology/parasitology/veterinary; Macrophages/immunology; Molecular Sequence Data; Oncorhynchus mykiss/genetics/immunology; Organ Specificity; Phylogeny; Receptors, CXCR/genetics/immunology; Sequence Alignment; CXCR2; CXCR3a; CXCR3b; Evolution; Expression; Rainbow trout
Abstract :
[en] 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.
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.
Publication date :
2014
Journal title :
Developmental and Comparative Immunology
ISSN :
0145-305X
Publisher :
Elsevier, United Kingdom
Volume :
45
Issue :
2
Pages :
201-13
Peer reviewed :
Peer Reviewed verified by ORBi
Commentary :
Copyright (c) 2014 The Authors. Published by Elsevier Ltd.. All rights reserved.
Aghaallaei N., Bajoghli B., Schwarz H., Schorpp M., Boehm T. Characterization of mononuclear phagocytic cells in medaka fish transgenic for a cxcr3a:gfp reporter. Proc. Natl. Acad. Sci. USA 2010, 107:18079-18084.
Alejo A., Tafalla C. Chemokines in teleost fish species. Dev. Comp. Immunol. 2011, 35:1215-1222.
Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
Amemiya C.T., Alföldi J., Lee A.P., Fan S., Philippe H., Maccallum I., Braasch I., Manousaki T., Schneider I., Rohner N., et al. The African coelacanth genome provides insights into tetrapod evolution. Nature 2013, 496:311-316.
Bajoghli B. Evolution and function of chemokine receptors in the immune system of lower vertebrates. Eur. J. Immunol. 2013, 43:1686-1692.
Campanella J.J., Bitincka L., Smalley J. MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics. 2003, 4:29.
Chang M.X., Sun B.J., Nie P. The first non-mammalian CXCR3 in a teleost fish: gene and expression in blood cells and central nervous system in the grass carp (Ctenopharyngodon idella). Mol. Immunol. 2007, 44:1123-1134.
Chen C., Li Z., Zhou Z., Yin Z., Chan S.M., Yu X.Q., Weng S., He J. Cloning, characterization and expression analysis of a CXCR1-like gene from mandarin fish Siniperca chuatsi. Fish Physiol. Biochem. 2009, 35:489-499.
Chen J., Xu Q., Wang T., Collet B., Corripio-Miyar Y., Bird S., Xie P., Nie P., Secombes C.J., Zou J. Phylogenetic analysis of vertebrate CXC chemokines reveals novel lineage specific groups in teleost fish. Dev. Comp. Immunol. 2013, 41:137-152.
Chenna R., Sugawara H., Koike T., Lopez R., Gibson T.J., Higgins D.G., Thompson J.D. Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res. 2003, 31:3497-3500.
Clifton-Hadley R.S., Bucke D., Richards R.H. A study of the sequential clinical and pathological changes during proliferative kidney disease in rainbow trout, Salmo gairdneri Richardson. J. Fish Dis. 1987, 10:335-352.
Coelho F.M., Pinho V., Amaral F.A., Sachs D., Costa V.V., Rodrigues D.H., Vieira A.T., Silva T.A., Souza D.G., Bertini R., Teixeira A.L., Teixeira M.M. The chemokine receptors CXCR1/CXCR2 modulate antigen-induced arthritis by regulating adhesion of neutrophils to the synovial microvasculature. Arthritis Rheum. 2008, 58:2329-2337.
Costa M.M., Maehr T., Diaz-Rosales P., Secombes C.J., Wang T. Bioactivity studies of rainbow trout (Oncorhynchus mykiss) interleukin-6: effects on macrophage growth and antimicrobial peptide gene expression. Mol. Immunol. 2011, 48:1903-1916.
DeLuca D., Wilson M., Warr G.W. Lymphocyte heterogeneity in the trout, Salmo gairdneri, defined with monoclonal antibodies to IgM. Eur. J. Immunol. 1983, 13:546-551.
Deng Q., Sarris M., Bennin D.A., Green J.M., Herbomel P., Huttenlocher A. Localized bacterial infection induces systemic activation of neutrophils through Cxcr2 signaling in zebrafish. J. Leukoc. Biol. 2013, 93:761-769.
DeVries M.E., Kelvin A.A., Xu L., Ran L., Robinson J., Kelvin D.J. Defining the origins and evolution of the chemokine/chemokine receptor system. J. Immunol. 2006, 176:401-415.
Forlenza M., Walker P.D., de Vries B.J., Wendelaar Bonga S.E., Wiegertjes G.F. Transcriptional analysis of the common carp (Cyprinus carpio L.) immune response to the fish louse Argulus japonicus Thiele (Crustacea: Branchiura). Fish Shellfish Immunol. 2008, 25:76-83.
Frydelund-Larsen L., Penkowa M., Akerstrom T., Zankari A., Nielsen S., Pedersen B.K. Exercise induces interleukin-8 receptor (CXCR2) expression in human skeletal muscle. Exp. Physiol. 2007, 92:233-240.
Fujiki K., Shin D.H., Nakao M., Yano T. Molecular cloning of carp (Cyprinus carpio) CC chemokine, CXC chemokine receptors, allograft inflammatory factor-1, and natural killer cell enhancing factor by use of suppression subtractive hybridization. Immunogenetics 1999, 49:909-914.
Ganassin R.C., Bols N.C. Development of a monocyte/macrophage-like cell line, RTS11, from rainbow trout spleen. Fish Shellfish Immunol. 1998, 8:457-476.
Gonzalez S.F., Buchmann K., Nielsen M.E. Real-time gene expression analysis in carp (Cyprinus carpio L.) skin: inflammatory responses caused by the ectoparasite Ichthyophthirius multifiliis. Fish Shellfish Immunol. 2007, 22:641-650.
Gorgoglione B., Wang T., Secombes C.J., Holland J.W. Immune gene expression profiling of Proliferative Kidney Disease in rainbow trout Oncorhynchus mykiss reveals a dominance of anti-inflammatory, antibody and T helper cell-like activities. Vet. Res. 2013, 44:55. 10.1186/1297-9716-44-55.
Groom J.R., Luster A.D. CXCR3 in T cell function. Exp. Cell Res. 2011, 317:620-631.
Harun N.O., Wang T., Secombes C.J. Gene expression profiling in naïve and vaccinated rainbow trout after Yersinia ruckeri infection: insights into the mechanisms of protection seen in vaccinated fish. Vaccine 2011, 29:4388-4399.
Hong S., Zou J., Crampe M., Peddie S., Scapigliati G., Bols N., Cunningham C., Secombes C.J. The production and bioactivity of rainbow trout (Oncorhynchus mykiss) recombinant IL-1 beta. Vet. Immunol. Immunopathol. 2001, 81:1-14.
Hong S., Li R., Xu Q., Secombes C.J., Wang T. Two types of TNF-α exist in teleost fish: Phylogeny, expression and bioactivity analysis of Type II TNF-a3 in rainbow trout Oncorhynchus mykiss. J. Immunol. 2013, 191:5959-5972.
Huising M.O., Stolte E., Flik G., Savelkoul H.F., Verburg-van Kemenade B.M.L. CXC chemokines and leukocyte chemotaxis in common carp (Cyprinus carpio L.). Dev. Comp. Immunol. 2003, 27:875-888.
Husain M., Bird S., van Zwieten R., Secombes C.J., Wang T. Cloning of the IL-1β3 gene and IL-1β4 pseudogene in salmonids uncovers a second type of IL-1β gene in teleost fish. Dev. Comp. Immunol. 2012, 38:431-446.
Johansson P., Corripio-Miyar Y., Wang T., Collet B., Secombes C.J., Zou J. Characterisation and expression analysis of the rainbow trout (Oncorhynchus mykiss) homologue of the human dendritic cell marker CD208/lysosomal associated membrane protein 3. Dev. Comp. Immunol. 2012, 37:402-413.
Khabar K.S. Post-transcriptional control during chronic inflammation and cancer: a focus on AU-rich elements. Cell Mol. Life Sci. 2010, 67:2937-2955.
Laing K.J., Bols N., Secombes C.J. A CXC chemokine sequence isolated from the rainbow trout Oncorhynchus mykiss resembles the closely related interferon-gamma-inducible chemokines CXCL9, CXCL10 and CXCL11. Eur. Cytokine Netw. 2002, 13:462-473.
Laing K.J., Zou J.J., Wang T., Bols N., Hirono I., Aoki T., Secombes C.J. Identification and analysis of an interleukin 8-like molecule in rainbow trout Oncorhynchus mykiss. Dev. Comp. Immunol. 2002, 26:433-444.
Letunic I., Doerks T., Bork P. SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 2012, 40:D302-D305. (Database issue).
Limatola C., Di Bartolomeo S., Catalano M., Trettel F., Fucile S., Castellani L., Eusebi F. Cysteine residues are critical for chemokine receptor CXCR2 functional properties. Exp. Cell Res. 2005, 307:65-75.
Morohashi H., Miyawaki T., Nomura H., Kuno K., Murakami S., Matsushima K., Mukaida N. Expression of both types of human interleukin-8 receptors on mature neutrophils, monocytes, and natural killer cells. J. Leukoc. Biol. 1995, 57:180-187.
Muffato M., Louis A., Poisnel C.E., Roest Crollius H. Genomicus: a database and a browser to study gene synteny in modern and ancestral genomes. Bioinformatics 2010, 26:1119-1121.
Nomiyama H., Osada N., Yoshie O. The evolution of mammalian chemokine genes. Cytokine Growth Factor Rev. 2010, 21:253-262.
Nomiyama H., Osada N., Yoshie O. A family tree of vertebrate chemokine receptors for a unified nomenclature. Dev. Comp. Immunol. 2011, 35:705-715.
Nomiyama H., Osada N., Yoshie O. Systematic classification of vertebrate chemokines based on conserved synteny and evolutionary history. Genes Cells 2013, 18:1-16.
Oehlers S.H., Flores M.V., Hall C.J., O'Toole R., Swift S., Crosier K.E., Crosier P.S. Expression of zebrafish cxcl8 (interleukin-8) and its receptors during development and in response to immune stimulation. Dev. Comp. Immunol. 2010, 34:352-359.
Raida M.K., Holten-Andersen L., Buchmann K. Association between Yersinia ruckeri infection, cytokine expression and survival in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 2011, 30:1257-1264.
Saha N.R., Bei J.X., Suetake H., Araki K., Kai W., Kikuchi K., Lin H.R., Suzuki Y. Description of a fugu CXC chemokine and two CXC receptor genes, and characterization of the effects of different stimulators on their expression. Fish Shellfish Immunol. 2007, 23:1324-1332.
Sasaki Y., Maita M., Okamoto N. Rainbow trout neutrophils are responsible for non-specific cytotoxicity. Fish Shell Immunol. 2002, 12:243-252.
Shields D.C. Gene conversion among chemokine receptors. Gene 2000, 246:239-245.
Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
Verbeke H., Struyf S., Laureys G., Van Damme J. The expression and role of CXC chemokines in colorectal cancer. Cytokine Growth Factor Rev. 2011, 22:345-358.
Wang T., Secombes C.J. Complete sequencing and expression of three complement components, C1r, C4 and C1 inhibitor, of the classical activation pathway of the complement system in rainbow trout Oncorhynchus mykiss. Immunogenetics 2003, 55:615-628.
Wang T., Hanington P.C., Belosevic M., Secombes C.J. Two macrophage colony-stimulating factor genes exist in fish that differ in gene organization and are differentially expressed. J. Immunol. 2008, 181:3310-3322.
Wang T., Bird S., Koussounadis A., Holland J.W., Carrington A., Zou J., Secombes C.J. Identification of a novel IL-1 cytokine family member in teleost fish. J. Immunol. 2009, 183:962-974.
Wang T., Holland J.W., Martin S.A., Secombes C.J. Sequence and expression analysis of two T helper master transcription factors, T-bet and GATA3, in rainbow trout Oncorhynchus mykiss and analysis of their expression during bacterial and parasitic infection. Fish Shellfish Immunol. 2010, 29:705-715.
Wang T., Diaz-Rosales P., Costa M.M., Campbell S., Snow M., Collet B., Martin S.A., Secombes C.J. Functional characterization of a nonmammalian IL-21: rainbow trout Oncorhynchus mykiss IL-21 upregulates the expression of the Th cell signature cytokines IFN-gamma, IL-10, and IL-22. J. Immunol. 2011, 186:708-721.
Wang T., Huang W., Costa M.M., Martin S.A., Secombes C.J. Two copies of the genes encoding the subunits of putative interleukin (IL)-4/IL-13 receptors, IL-4Rα, IL-13Rα1 and IL-13Rα2, have been identified in rainbow trout (Oncorhynchus mykiss) and have complex patterns of expression and modulation. Immunogenetics 2011, 63:235-253.
Xu T., Zhu Z., Sun Y., Ren L., Wang R. Characterization and expression of the CXCR1 and CXCR4 in miiuy croaker and evolutionary analysis shows the strong positive selection pressures imposed in mammal CXCR1. Dev. Comp. Immunol. 2013, 44:133-144.
Zhang H., Thorgaard G.H., Ristow S.S. Molecular cloning and genomic structure of an interleukin-8 receptor-like gene from homozygous clones of rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol. 2002, 13:251-258.
Zlotnik A., Yoshie O. The chemokine superfamily revisited. Immunity 2012, 36:705-716.