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Conservation of sequence motifs suggests that the nonclassical MHC class I lineages CD1/PROCR and UT were established before the emergence of tetrapod species

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Abstract

Humans have a number of nonclassical major histocompatibility complex (MHC) class I molecules that are quite divergent from the classical ones, and that may have separated from the classical lineage in pre-mammalian times. To estimate when in evolution the respective nonclassical lineages separated from the classical lineage, we first identified “phylogenetic marker motifs” within the evolution of classical MHC class I; the selected motifs are rather specific for and rather stably inherited within clades of species. Distribution of these motifs in nonclassical MHC class I molecules indicates that the lineage including the nonclassical MHC class I molecules CD1 and PROCR separated from the classical lineage before the emergence of tetrapod species, and that the human nonclassical MHC class I molecules FCGRT, MIC/ULBP/RAET, HFE, MR1, and ZAG show similarity with classical MHC class I at the avian/reptilian level. An MR1-like α1 exon sequence was identified in turtle. Our system furthermore indicates that the lineage UT, hitherto only found in non-eutherian mammals, predates tetrapod existence, and we identified UT genes in reptiles. If only accepting wide distribution of a lineage among extant species as true evidence for ancientness, the oldest identified nonclassical MHC class I lineage remains the fish-specific lineage Z, which was corroborated in the present study by finding both Z and classical-type MHC class I sequences in a primitive fish, the bichir. In short, we gained important new insights into the evolution of classical MHC class I motifs and the probable time of origin of nonclassical MHC class I lineages.

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Acknowledgements

This work was supported by JSPS KAKENHI Grant Number 22580213 for Johannes M. Dijkstra, and by Internal funding from the Norwegian Veterinary Institute for Unni Grimholt. UG collected most of the sequences, analyzed their genomic organization, and made Supplementary text 1, Supplementary Fig. 1, and Supplementary Table 1, and assisted in writing the paper. TY retrieved and assembled MHC class I sequences of primitive fishes using SRA datasets. JMD made the sequence alignments, analyzed the phylogeny, established the marker motif system, and wrote the paper.

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Authors and Affiliations

  1. Institute for Comprehensive Medical Science, Fujita Health University, Dengaku-gakubo 1-98, Toyoake, Aichi-ken, 470-1192, Japan

    Johannes M. Dijkstra

  2. Laboratory of Fish Immunology, Institute of Infectology, Friedrich-Loeffler-Institut, Südufer 10, 17493, Greifswald-Insel Riems, Germany

    Takuya Yamaguchi

  3. Fish Research Group, Norwegian Veterinary Institute, Ullevaalsveien 68, 0454, Oslo, Norway

    Unni Grimholt

Authors
  1. Johannes M. Dijkstra
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  2. Takuya Yamaguchi
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  3. Unni Grimholt
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Correspondence to Johannes M. Dijkstra or Unni Grimholt.

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Dijkstra, J.M., Yamaguchi, T. & Grimholt, U. Conservation of sequence motifs suggests that the nonclassical MHC class I lineages CD1/PROCR and UT were established before the emergence of tetrapod species. Immunogenetics 70, 459–476 (2018). https://doi.org/10.1007/s00251-017-1050-2

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