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Comparative genomic analysis of the proteasome β5t subunit gene: implications for the origin and evolution of thymoproteasomes

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Abstract

The thymoproteasome is a recently discovered, specialized form of 20S proteasomes expressed exclusively in the thymic cortex. Although the precise molecular mechanism by which the thymoproteasome exerts its function remains to be elucidated, accumulating evidence indicates that it plays a crucial role in positive selection of T cells. In the present study, we analyzed the evolution of the β5t subunit, a β-type catalytic subunit uniquely present in thymoproteasomes. The gene coding for the β5t subunit, designated PSMB11, was identified in the cartilaginous fish, the most divergent group of jawed vertebrates compared to the other jawed vertebrates, but not in jawless vertebrates or invertebrates. Interestingly, teleost fish have two copies of apparently functional PSMB11 genes, designated PSMB11a and PSMB11b, that encode β5t subunits with distinct amino acids in the S1 pocket. BLAST searches of genome databases suggest that birds such as chickens, turkey, and zebra finch lost the PSMB11 gene, and have neither thymoproteasomes nor immunoproteasomes. In mammals, reptiles, amphibians, and teleost fishes, the PSMB11 gene (the PSMB11a gene in teleost fish) is located next to the PSMB5 gene coding for the β5 subunit of the standard 20S proteasome, indicating that the PSMB11 gene arose by tandem duplication from the evolutionarily more ancient PSMB5 gene. The general absence of introns in PSMB11 and an unusual exon–intron structure of jawed vertebrate PSMB5 suggest that PSMB5 lost introns and duplicated in tandem in a common ancestor of jawed vertebrates, with PSMB5 subsequently gaining two introns and PSMB11 remaining intronless.

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Acknowledgments

This work was supported by grants from The Ministry of Education, Culture, Sports, Science and Technology of Japan, and National Institutes of Health grant AI027877. Yoichi Sutoh and Mizuho Kondo are supported by the Research Fellowship of the Japan Society for the Promotion of Science.

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  1. Department of Pathology, Hokkaido University Graduate School of Medicine, North-15 West-7, Sapporo, 060-8638, Japan

    Yoichi Sutoh, Mizuho Kondo, Utano Tomaru & Masanori Kasahara

  2. Department of Microbiology and Immunology, University of Maryland, 685 West Baltimore Street, Baltimore, MD, 21201, USA

    Yuko Ohta & Martin F. Flajnik

  3. Department of Evolutionary Studies of Biosystems, The Graduate University for Advanced Studies, Hayama, 240-0193, Japan

    Tatsuya Ota

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Correspondence to Masanori Kasahara.

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Sequence data reported in this paper have been submitted to the DDBJ/EMBL/NCBI databases under accession numbers AB624351 and AB624352.

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Fig. 1S

Amino acid sequence alignment of β5i, β5, and β5t subunits from various species. H1–H5 and β1–β12 stand for helices and β-strands, respectively. The locations of secondary structures are based on the information deposited in the RCSB Protein Data Bank. This alignment was used for the construction of the tree shown in Fig. 1. (PDF 2606 kb)

Fig. 2S

Anolis Ensembl scaffold GL344036.1 encodes MHC class I, TAP1, TAP2, and PSMB8. The MHC class I gene shown here appears to be a classical class I gene as its predicted α1 and α2 domains have eight conserved residues that are involved in the anchoring of peptide termini. The draft genome sequence contains gaps upsteam of the PSMB8 gene (indicated by a broken line) and lacks the presumed exon 1 sequence of PSMB8. (PDF 186 kb)

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Sutoh, Y., Kondo, M., Ohta, Y. et al. Comparative genomic analysis of the proteasome β5t subunit gene: implications for the origin and evolution of thymoproteasomes. Immunogenetics 64, 49–58 (2012). https://doi.org/10.1007/s00251-011-0558-0

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