The identification of additional zebrafish DICP genes reveals haplotype variation and linkage to MHC class I genes

Abstract

Bony fish encode multiple multi-gene families of membrane receptors that are comprised of immunoglobulin (Ig) domains and are predicted to function in innate immunity. One of these families, the diverse immunoglobulin (Ig) domain-containing protein (DICP) genes, maps to three chromosomal loci in zebrafish. Most DICPs possess one or two Ig ectodomains and include membrane-bound and secreted forms. Membrane-bound DICPs include putative inhibitory and activating receptors. Recombinant DICP Ig domains bind lipids with varying specificity, a characteristic shared with mammalian CD300 and TREM family members. Numerous DICP transcripts amplified from different lines of zebrafish did not match the zebrafish reference genome sequence suggesting polymorphic and haplotypic variation. The expression of DICPs in three different lines of zebrafish has been characterized employing PCR-based strategies. Certain DICPs exhibit restricted expression in adult tissues whereas others are expressed ubiquitously. Transcripts of a subset of DICPs can be detected during embryonic development suggesting roles in embryonic immunity or other developmental processes. Transcripts representing 11 previously uncharacterized DICP sequences were identified. The assignment of two of these sequences to an unplaced genomic scaffold resulted in the identification of an alternative DICP haplotype that is linked to a MHC class I Z lineage haplotype on zebrafish chromosome 3. The linkage of DICP and MHC class I genes also is observable in the genomes of the related grass carp (Ctenopharyngodon idellus) and common carp (Cyprinus carpio) suggesting that this is a shared character with the last common Cyprinidae ancestor.

Spotted Gar and the Evolution of Innate Immune Receptors

“…Definitive DICPs have been identified in cyprinid fishes: zebrafish, grass carp ( Ctenopharyngodon idella ), and common carp ( Cyprinus carpio ) (Rodriguez‐Nunez et al., ). A number of DICPs share many similarities to members of the mammalian CD300 family including the same basic protein structure (Fig.…”

“…Conserved sequence features of gar DICP D1 and D2 domains. Gar ( Lepisosteus oculatus , Leoc) DICP D1 (top) and D2 (bottom) domains were aligned with previously described DICP domains from zebrafish ( Danio rerio , Dare), carp ( Cyprinus carpio , Cyca and Ctenopharyngodon idella , Ctid), pufferfish ( Takifugu rubripes , Teni), salmon ( Salmo salar , Sasa) and coelacanth ( Latimeria chalumnae , Lach) (Haire et al., ; Boudinot et al., ; Rodriguez‐Nunez et al., ). Cysteines representative of Ig domains are indicated with single‐headed arrow below the alignment.…”

“…). The zebrafish DICP gene cluster present on chromosome 3 is adjacent to MHC class I genes (Haire et al., ; Rodriguez‐Nunez et al., ). Similarly, one of the coelacanth DICP sequences also is adjacent to MHC class I sequences (Fig.…”

Holosteans contextualize the role of the teleost genome duplication in promoting the rise of evolutionary novelties in the ray-finned fish innate immune system

“…None of the bowfin DICP transcripts mapped onto the reference genome with 100% accuracy. As the reference genome and transcriptome sequences were derived from different individuals, this observation indicates intraspecific DICP sequence variation in bowfin as described in zebrafish (Rodriguez-Nunez et al 2016). Nevertheless, a phylogenetic comparison of transcript-encoded DICP D1 and D2 domains to genome-encoded D1 and D2 domains revealed multiple similarities (Supplementary Fig.…”

“…nitr3, nitr7, nitr8, nitr13, etc.) Nevertheless, the identification of 34 NITR sequences in bowfin is on par with the 39, 44 and 30 NITR genes identified in zebrafish, medaka and sea bass, respectively (Yoder et al 2004;Desai et al 2008;Ferraresso et al 2009;Rodriguez-Nunez et al 2016) suggesting that the large number of teleost NITRs is not just a result of paralog retention following the TGD.…”