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  • Phylogenetic analysis indicates that in poikilothermic verte

    2019-07-03

    Phylogenetic analysis indicates that in poikilothermic vertebrates CXCR3a and CXCR3b have evolved independently from a common gene possibly after the 2nd round whole genome duplication but before the split of bony fish and tetrapods (Fig. 1 and Supplementary file 3). Owing to the extra round of whole genome duplication in some fish lineages (Danzmann et al., 2008) and random gene duplication events locally, it is possible that more copies of CXCR3 genes could be found, as seen for many other chemokines and chemokine receptors (Bajoghli, 2013, DeVries et al., 2006, Nomiyama et al., 2008, Xu et al., 2014a, Zlotnik and Yoshie, 2012). For example, three CXCR3 genes have been found in zebrafish and medaka (Xu et al., 2014a). The single copy CXCR3 gene retained in mammals is an authentic orthologue of poikilothermic vertebrate CXCR3a from fish, SAR405 and reptiles (Supplementary file 3). It is interesting that phylogenetic tree analysis consistently placed the CXCR3b molecules as an outgroup for CXCR3a and CXCR5 (Fig. 1 and Supplementary files 2 and 3), suggesting a common origin of these receptors that are predominantly SAR405 expressed in B and T lymphocytes. Evidence from gene synteny analysis suggests that the CXCR3a/3b locus had been drastically changed prior to the emergence of homeothermic birds and mammals (Xu et al., 2014a). The cells expressing CXCR3a and 3b have not been fully characterised in fish. Unlike its counterpart in mammals, CXCR3a is constitutively expressed in medaka macrophages and dendritic cells (Aghaallaei et al., 2010), suggesting it may be required for homeostasis of these cell types. These CXCR3a+ cells are likely to be myeloid in origin since they express myeloid-associated markers, such as mpo, csf1r, and l-plastin, but not genes of red blood cell and T cell origin (Aghaallaei et al., 2010). Zebrafish CXCR3a (also referred to as CXCR3.2) expression in macrophages is shown to be controlled by the transcription factor spi1/pu and its expression modulation affects macrophage migration to sites of bacterial infection (Zakrzewska et al., 2010). In grass carp (Ctenopharyngodon idella), CXCR3a+ cells account for 17% of the total peripheral blood leucocytes, as assessed by FACS analysis using a polyclonal antibody against CXCR3a (Chang et al., 2007). In rainbow trout head kidney cells and macrophages, CXCR3a can be significantly induced by inflammatory stimulants (e.g. LPS and peptidoglycan) and cytokines (e.g. IL-1β, TNF and MCSF) (Wang et al., 2008b, Xu et al., 2014a); however, trout CXCR3b expression is not affected. In a separate study, VHSV infection led to a significant increase in CXCR3b transcripts in rainbow trout gills (Aquilino et al., 2014). In addition, the CXCR3a+ cells may play a role in protecting the brain from pathogen infection since a significant number of CXCR3a+ cells are found in different regions of the brain (Chang et al., 2007). In summary, fish CXCR3s are involved in regulating homeostasis, migration and differentiation of immune cells, in particular myeloid cells. Whether they also participate in mediating migration of lymphocytes requires further investigation.
    CXCR4 Among the CXCRs, CXCR4 is the most well studied receptor owing to its critical roles in development. CXCR4 has been discovered as a single copy gene in agnathan and gnathostome vertebrates except for teleosts where duplicated CXCR4 (CXCR4a and 4b), and their ligands CXCL12 (CXCL12a and 12b), are present (Bajoghli, 2013, Baoprasertkul et al., 2005, Chen et al., 2013, DeVries et al., 2006, Huising et al., 2004, Nomiyama et al., 2011, Zlotnik et al., 2006). After binding to CXCL12 (also referred to as SDF-1), CXCR4 functions in a variety of biological processes during development, the immune response and disease. For example, in humans, CXCR4 as well as CXCR5 and CXCR6/Bonzo have been identified as co-receptors of human immunodeficiency virus (HIV) and simian immunodeficiency virus (SIV) for entry into the host cells (Feng et al., 1996, Kanbe et al., 1999, Matloubian et al., 2000). The CXCL12/CXCR4 ligand/receptor system is believed to be the most ancient chemokine system in vertebrates (Bajoghli, 2013, Huising et al., 2003a, Kuroda et al., 2003).