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

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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.

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Acknowledgment

We thank Hayley Dirscherl (NC State University) for helpful discussions and zebrafish genomic DNA samples, John Whitesides and Patti McDermott (Duke Human Vaccine Institute, Duke University School of Medicine) for assistance with cell sorting, Diana Skapura (All Children’s Hospital) for assistance with DNA sequencing, and Barbara Pryor for editorial assistance. The authors are supported by the National Institutes of Health (R01 AI057559 to G.W.L. and J.A.Y. and R01 AI23337 to G.W.L.) and the National Evolutionary Synthesis Center (NESCent), NSF #EF‐0905606 (D.J.W.).

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Correspondence to Jeffrey A. Yoder.

Electronic Supplementary Material

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ESM 1

Online Resource 1. Table S1. Complete DICP amplicon sequence data including cDNA source, DNA polymerase, nucleotide and amino acid sequence, and GenBank accession numbers. (XLSX 45 kb)

ESM 2

Online Resource 2. Table S2. Percent (nucleotide) identity between DICP amplicons generated with a high-fidelity DNA polymerase and previously described DICP sequences. (XLSX 17 kb)

ESM 3

Online Resource 3. DICP sequence variation; DICP exon-intron architecture Figures S1–S14; Tables S3–S4. (PDF 2796 kb)

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Rodriguez-Nunez, I., Wcisel, D.J., Litman, R.T. et al. The identification of additional zebrafish DICP genes reveals haplotype variation and linkage to MHC class I genes. Immunogenetics 68, 295–312 (2016). https://doi.org/10.1007/s00251-016-0901-6

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  • DOI: https://doi.org/10.1007/s00251-016-0901-6

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