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A molecule in teleost fish, related with human MHC-encoded G6F, has a cytoplasmic tail with ITAM and marks the surface of thrombocytes and in some fishes also of erythrocytes

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Abstract

In teleost fish, a novel gene G6F-like was identified, encoding a type I transmembrane molecule with four extracellular Ig-like domains and a cytoplasmic tail with putative tyrosine phosphorylation motifs including YxN and an immunoreceptor tyrosine-based activation motif (ITAM). G6F-like maps to a teleost genomic region where stretches corresponding to human chromosomes 6p (with the MHC), 12p (with CD4 and LAG-3), and 19q are tightly linked. This genomic organization resembles the ancestral “Ur-MHC” proposed for the jawed vertebrate ancestor. The deduced G6F-like molecule shows sequence similarity with members of the CD4/LAG-3 family and with the human major histocompatibility complex-encoded thrombocyte marker G6F. Despite some differences in molecular organization, teleost G6F-like and tetrapod G6F seem orthologous as they map to similar genomic location, share typical motifs in transmembrane and cytoplasmic regions, and are both expressed by thrombocytes/platelets. In the crucian carps goldfish (Carassius auratus auratus) and ginbuna (Carassius auratus langsdorfii), G6F-like was found expressed not only by thrombocytes but also by erythrocytes, supporting that erythroid and thromboid cells in teleost fish form a hematopoietic lineage like they do in mammals. The ITAM-bearing of G6F-like suggests that the molecule plays an important role in cell activation, and G6F-like expression by erythrocytes suggests that these cells have functional overlap potential with thrombocytes.

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Acknowledgments

This work was supported by grants-in-aid for Scientific Research, 19580220, from the Japan Society for the Promotion of Science (JSPS) to JMD. We thank Dr. Mitsuru Ototake, National Research Institute of Aquaculture, Tamaki, Japan, for providing clonal rainbow trout; Dr. Bernd Köllner, FLI, Insel Riems, Germany, for providing the mAb 42 antibody; and Dr. Taei Matsui, FHU, Toyoake, Japan and Dr. Makoto Kobayashi, University of Tsukuba, Japan for carefully reading the manuscript.

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  1. Laboratory of Fish Pathology, Department of Veterinary Medicine, Nihon University, 1866 Kameino, Fujisawa, Kanagawa, 252-8510, Japan

    Ken Ohashi, Fumio Takizawa, Hideaki Toda, Tadaaki Moritomo & Teruyuki Nakanishi

  2. Friedrich-Loeffler-Institute, Federal Research Institute for Animal Health, Institute for Infectiology, Insel Riems, 17498, Germany

    Fumio Takizawa & Uwe Fischer

  3. Institute for Comprehensive Medical Science, Fujita Health University, Toyoake, Aichi, 470-1192, Japan

    Norihiro Tokumaru, Keiichiro Hashimoto & Johannes Martinus Dijkstra

  4. Pathogen Research Group, Aquatic Animal Health Division, National Research Institute of Aquaculture, Tamaki, Mie, 519-0423, Japan

    Chihaya Nakayasu

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Electronic Supplementary Materials

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Supplementary Fig. 1

Synteny between medaka chromosomes 11/16 and human chromosomes 6, 12, and 19 (PDF 272 kb)

Supplementary Fig. 2

G6F-like nucleotide sequences (PDF 448 kb)

Supplementary Fig. 3

Best 20 matches of blastp-queries with teleost G6F-like against the UniProt Knowledgebase (PDF 395 kb)

Supplementary Fig. 4

Best 20 matches of a blastp-query with human G6F against the UniProt Knowledgebase (PDF 143 kb)

Supplementary Fig. 5

G6B and G6F loci in green anole lizard (Anolis carolinensis) (PDF 151 kb)

Supplementary Fig. 6

Alignment of deduced G6B amino acid sequences (PDF 120 kb)

Supplementary Fig. 7

Alignment of deduced G6F amino acid sequences (PDF 126 kb)

Supplementary Fig. 8

Establishment of monoclonal antibodies against ginbuna G6F-like (PDF 140 kb)

Supplementary Fig. 9

Expression of G6F-like in goldfish (PDF 212 kb)

Supplementary Fig. 10

Expression of G6F-like in rainbow trout (PDF 712 kb)

Supplementary Table 1

Primer sequences (PDF 135 kb)

Supplementary Table 2

Orthologous pairs between the human MHC and medaka chromosomes 11 and 16 (PDF 117 kb)

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Ohashi, K., Takizawa, F., Tokumaru, N. et al. A molecule in teleost fish, related with human MHC-encoded G6F, has a cytoplasmic tail with ITAM and marks the surface of thrombocytes and in some fishes also of erythrocytes. Immunogenetics 62, 543–559 (2010). https://doi.org/10.1007/s00251-010-0460-1

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