Proteasome, Transporter Associated with Antigen Processing, and Class I Genes in the Nurse Shark<i>Ginglymostoma cirratum</i>: Evidence for a Stable Class I Region and MHC Haplotype Lineages

Ohta, Yuko; McKinney, E. Churchill; Criscitiello, Michael F.; Flajnik, Martin F.

doi:10.4049/jimmunol.168.2.771

Cited by 71 publications

(61 citation statements)

References 56 publications

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“…By contrast, the mammalian MHC has a peculiar organization in which the class I genes are not closely linked to TAP and PSMB genes. The loss of this linkage seems to be accompanied by the loss of the genetic dimorphism of the linked class I/PSMB/TAP genes observed in amphibian, teleosts, and cartilaginous fish (10,64,65,73). Thus, the amphibian seems to be the best model to study evolution of the vertebrate MHC.…”

Section: Discussionmentioning

confidence: 99%

Ancestral Organization of the MHC Revealed in the AmphibianXenopus

Ohta

Goetz

Hossain

et al. 2006

The Journal of Immunology

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With the advent of the Xenopus tropicalis genome project, we analyzed scaffolds containing MHC genes. On eight scaffolds encompassing 3.65 Mbp, 122 MHC genes were found of which 110 genes were annotated. Expressed sequence tag database screening showed that most of these genes are expressed. In the extended class II and class III regions the genomic organization, excluding several block inversions, is remarkably similar to that of the human MHC. Genes in the human extended class I region are also well conserved in Xenopus, excluding the class I genes themselves. As expected from previous work on the Xenopus MHC, the single classical class I gene is tightly linked to immunoproteasome and transporter genes, defining the true class I region, present in all nonmammalian jawed vertebrates studied to date. Surprisingly, the immunoproteasome gene PSMB10 is found in the class III region rather than in the class I region, likely reflecting the ancestral condition. Xenopus DMα, DMβ, and C2 genes were identified, which are not present or not clearly identifiable in the genomes of any teleosts. Of great interest are novel V-type Ig superfamily (Igsf) genes in the class III region, some of which have inhibitory motifs (ITIM) in their cytoplasmic domains. Our analysis indicates that the vertebrate MHC experienced a vigorous rearrangement in the bony fish and bird lineages, and a translocation and expansion of the class I genes in the mammalian lineage. Thus, the amphibian MHC is the most evolutionary conserved MHC so far analyzed.

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Section: Discussionmentioning

confidence: 99%

Ancestral Organization of the MHC Revealed in the AmphibianXenopus

Ohta

Goetz

Hossain

et al. 2006

The Journal of Immunology

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130

120

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“…S1) (29, 30). On the other hand, it is not clear whether there is functional diversification between PSMB8d(V) and PSMB8d(A), because sublineage-specific substitutions were recognized only at two positions, V 31 A and R 67 K (Fig. 2).…”

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confidence: 99%

“…The deduced complete amino acid sequences of the mature peptide of the PSMB8d and PSMB8N allelic lineages identified from these eight Oryzias species, including O. latipes, were aligned, together with dimorphic PSMB8 alleles of Xenopus (29), two paralogous PSMB8 genes of sharks (30,31), and human PSMB8 (Fig. S1).…”

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confidence: 99%

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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“…Throughout vertebrates, gene linkage within the MHC region is highly conserved. For example, MHCI and antigen processing genes remain tightly linked in sharks, members of the oldest vertebrate lineage to maintain an MHC-mediated adaptive immune system (15,16). This tight linkage is also highly conserved in bony fish (17)(18)(19) as well as in additional nonmammalian jawed vertebrates, such as frogs (20).…”

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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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Proteasome, Transporter Associated with Antigen Processing, and Class I Genes in the Nurse SharkGinglymostoma cirratum: Evidence for a Stable Class I Region and MHC Haplotype Lineages

Cited by 71 publications

References 56 publications

Ancestral Organization of the MHC Revealed in the AmphibianXenopus

Ancestral Organization of the MHC Revealed in the AmphibianXenopus

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

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