Dichotomous Haplotypic Lineages of the Immunoproteasome Subunit Genes, PSMB8 and PSMB10, in the MHC Class I Region of a Teleost Medaka, Oryzias latipes

Tsukamoto, Keizou; Sakaizumi, Mitsuru; Hata, Masayoshi; Sawara, Yuji; Eah, Jaeyoung; Kim, Chang Bae; Nonaka, Masaru

doi:10.1093/molbev/msn305

Cited by 14 publications

(8 citation statements)

References 39 publications

(45 reference statements)

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“…the NP and SP clarified that all PSMB8 alleles were clearly classified into the dichotomous allelic lineages, PSMB8N or PSMB8d (24). Both PSMB8d and PSMB8N lineages were retained in NP and SP although the allelic frequency of the PSMB8d lineage (73-100%) was much higher than that of the PSMB8N lineage (0-27%) in all the populations we analyzed.…”

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confidence: 71%

“…S1 and was used in the following analyses. There are two sublineages, PSMB8d(V) and PSMB8d(A), in thePSMB8d lineage of medaka, having valine and alanine, respectively, at the 31st amino acid position, respectively (24). These two sublineages were present in all the wild populations of Oryzias species we analyzed.…”

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confidence: 90%

“…The PSMB8N lineage was not identified in wild populations of O. minutillus and O. dancena. However, because the frequency of the PSMB8N lineage was less than 0.01 in certain populations of O. latipes (24), it still is unclear whether the PSMB8N lineage is missing or is present at an extremely low frequency in these populations.…”

Section: Comparison Of Nucleotide Sequences Of Exons and Introns Amonmentioning

confidence: 99%

“…Two to eight bands with distinct sizes were detected in each species. All bands amplified from all individuals were sequenced directly, and the lineage was determined based on the 31st amino acid residue of the mature peptide encoded by exon 3 (24). One homozygous individual for each distinctive band was selected for another round of PCR amplification from exon 1 to exon 6 (the last exon), and nucleotide sequences were determined by direct sequencing.…”

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confidence: 99%

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Transspecies dimorphic allelic lineages of the proteasome subunit β-type 8 gene ( PSMB8 ) in the teleost genus Oryzias

Miura

Tsukamoto

Mehta

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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The proteasome subunit β-type 8 (PSMB8) gene in the jawed vertebrate MHC genomic region encodes a catalytic subunit of the immunoproteasome involved in the generation of peptides to be presented by the MHC class I molecules. A teleost, the medaka (Oryzias latipes), has highly diverged dimorphic allelic lineages of the PSMB8 gene with only about 80% amino acid identity, termed "PSMB8d" and "PSMB8N," which have been retained by most wild populations analyzed. To elucidate the evolutionary origin of these two allelic lineages, seven species of the genus Oryzias were analyzed for their PSMB8 allelic sequences using a large number of individuals from wild populations. All the PSMB8 alleles of these species were classified into one of these two allelic lineages based on their nucleotide sequences of exons and introns, indicating that the Oryzias PSMB8 gene has a truly dichotomous allelic lineage. Retention of both allelic lineages was confirmed except for one species. The PSMB8d lineage showed a higher frequency than the PSMB8N lineage in all seven species. The two allelic lineages showed curious substitutions at the 31st and 53rd residues of the mature peptide, probably involved in formation of the S1 pocket, suggesting that these allelic lineages show a functional difference in cleavage specificity. These results indicate that the PSMB8 dimorphism was established before speciation within the genus Oryzias and has been maintained for more than 30-60 million years under a strict and asymmetric balancing selection through several speciation events.long-term balancing selection | antigen processing | transspecies polymorphism T ransspecies polymorphism (TSP) is the passage of allelic lineages from ancestral to descendent species (1), and the underlying selective mechanism is referred to as balancing selection caused by "overdominant selection," "frequency-dependent selection," or "selection that varies in time and space" (2). The vertebrate MHC class I and II genes with a large number of alleles and wide allelic differences provide a classical example of TSP (3, 4), most probably arising by overdominant selection (5). TSP of the MHC genes sometimes persists for very long periods. Certain HLA-DRB alleles are reported to have persisted for 50-60 million years (6). Another well-characterized TSP has been reported for the rabbit Ig heavy-chain variable-region genes; its persistence has been estimated at 50 million years based on molecular phylogenetic analysis (7,8). Except for these genes encoding molecules showing high degree of binding specificity, information for long-term balancing selection resulting in TSP is limited (9-11). Moreover, all TSP reported thus far involve only a few species, and the possible presence of a long-lasting TSP surviving through many speciation events is still to be clarified by systematic phylogenetic analysis.The MHC class I molecules deliver the peptides derived from cytosolic proteins to the cell surface for recognition by cytotoxic T cells. The proteins are degraded proteolytically into s...

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confidence: 71%

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confidence: 90%

Section: Comparison Of Nucleotide Sequences Of Exons and Introns Amonmentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Transspecies dimorphic allelic lineages of the proteasome subunit β-type 8 gene ( PSMB8 ) in the teleost genus Oryzias

Miura

Tsukamoto

Mehta

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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“…Furthermore, the antigen processing gene psmb8 has also been shown to retain ancient sequence lineages in teleosts that are hundreds of millions of years old (28). Finally, an additional set of unique and perhaps teleost-specific proteasome subunit genes was previously linked to teleost MHCI genes (17)(18)(19)29), and one of these genes referred to as psmb10 displayed limited (believed nonfunctional) polymorphism (30). However, few other studies have examined these genes in detail.…”

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confidence: 99%

Alternative haplotypes of antigen processing genes in zebrafish diverged early in vertebrate evolution

McConnell

Hernandez

Wcisel

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Antigen processing and presentation genes found within the MHC are among the most highly polymorphic genes of vertebrate genomes, providing populations with diverse immune responses to a wide array of pathogens. Here, we describe transcriptome, exome, and whole-genome sequencing of clonal zebrafish, uncovering the most extensive diversity within the antigen processing and presentation genes of any species yet examined. Our CG2 clonal zebrafish assembly provides genomic context within a remarkably divergent haplotype of the core MHC region on chromosome 19 for six expressed genes not found in the zebrafish reference genome: mhc1uga, proteasome-β 9b (psmb9b), psmb8f, and previously unknown genes psmb13b, tap2d, and tap2e. We identify ancient lineages for Psmb13 within a proteasome branch previously thought to be monomorphic and provide evidence of substantial lineage diversity within each of three major trifurcations of catalytic-type proteasome subunits in vertebrates: Psmb5/Psmb8/Psmb11, Psmb6/ Psmb9/Psmb12, and Psmb7/Psmb10/Psmb13. Strikingly, nearby tap2 and MHC class I genes also retain ancient sequence lineages, indicating that alternative lineages may have been preserved throughout the entire MHC pathway since early diversification of the adaptive immune system ∼500 Mya. Furthermore, polymorphisms within the three MHC pathway steps (antigen cleavage, transport, and presentation) are each predicted to alter peptide specificity. Lastly, comparative analysis shows that antigen processing gene diversity is far more extensive than previously realized (with ancient coelacanth psmb8 lineages, shark psmb13, and tap2t and psmb10 outside the teleost MHC), implying distinct immune functions and conserved roles in shaping MHC pathway evolution throughout vertebrates.comparative genomics | proteasome and TAP evolution | major histocompatibility | MHC class I pathway | CG2 clonal zebrafish

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Evolution of the Major Histocompatibility Complex: A Lesson from the Oryzias Species

Nonaka

Tsukamoto

2011

Medaka

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Dichotomous Haplotypic Lineages of the Immunoproteasome Subunit Genes, PSMB8 and PSMB10, in the MHC Class I Region of a Teleost Medaka, Oryzias latipes

Cited by 14 publications

References 39 publications

Transspecies dimorphic allelic lineages of the proteasome subunit β-type 8 gene ( PSMB8 ) in the teleost genus Oryzias

Transspecies dimorphic allelic lineages of the proteasome subunit β-type 8 gene ( PSMB8 ) in the teleost genus Oryzias

Alternative haplotypes of antigen processing genes in zebrafish diverged early in vertebrate evolution

Evolution of the Major Histocompatibility Complex: A Lesson from the Oryzias Species

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