Genomic organization of duplicated major histocompatibility complex class I regions in Atlantic salmon (Salmo salar)

Lukacs, Morten; Harstad, Håvard; Grimholt, Unni; Beetz-Sargent, Marianne; Cooper, Glenn A.; Reid, Linda; Bakke, Hege G.; Phillips, Ruth B.; Miller, Kristina M.; Davidson, William S.; Koop, Ben F.

doi:10.1186/1471-2164-8-251

Cited by 66 publications

(83 citation statements)

References 62 publications

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“…Similar to the other Tap2 subunits in zebrafish, Tap2t conserves key residues within a specificity loop predicted to interact with peptides (SI Appendix, Table S3). In summary, this zebrafish proteasome and TAP gene nomenclature remains consistent with that in humans as well as additional vertebrates (44). We believe that this proposal will help further promote nomenclature consistency across species, facilitating future comparative studies.…”

Section: Methodsmentioning

confidence: 97%

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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Section: Methodsmentioning

confidence: 97%

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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“…Three additional microsatellites linked to MHC loci (adaptive SSRs), and first described in Atlantic salmon (Salmo salar; Grimholt 1997; Grimholt et al 2002;Gharbi et al 2009) were amplified in a 3-plex reaction: (1) Satr-UBA is a tightly linked microsatellite in the 3′-untranslated region of the MHC I locus Satr-UBA and has been applied in brown trout (Coughlan et al 2006;O'Farrell et al 2012). (2) SatrTAP2b (nomenclature of Lukacs et al 2007, corresponding to TAP2A of; Grimholt et al 2002) is located in intron 5 of the TAP2A gene. The TAP protein is involved in transporting peptides into the endoplasmic reticulum, where they bind to MHC class I molecules.…”

Section: Microsatellite (Ssr) Typingmentioning

confidence: 99%

Selection and genetic drift in captive versus wild populations: an assessment of neutral and adaptive (MHC-linked) genetic variation in wild and hatchery brown trout (Salmo trutta) populations

Schenekar

Weiss

2017

Conserv Genet

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“…In this study, the classical class I gene was termed Ctid-UBA, and a hallmark of Ctid-UBA is that it flanks TAP-associated glycoprotein (TAPBP). The organization here is similar to that of MHC I-UDA in zebrafish (42, 48), Orla-UBA in medaka (16,50), and Sasa-UCA in Atlantic salmon (73). Because TAPBP is a key member of class I Ag-loading complexes (9,15), it was first considered that the TAPBP had an opportunity to coevolve to function in coordination with MHC class I in bony fish.…”

Section: Discussionmentioning

confidence: 90%

“…Rainbow trout and Atlantic salmon genomes encode only one classical MHC class I locus designated UBA (72,73), although the species have multiple U-lineage genes, such as the class I-like lineages of ZE and L (74)(75)(76). In rainbow trout, the a2 domain amino acid sequence of Onmy-UA-C32 is more closely related to that of zebrafish and carp than to that of other salmonid species (77).…”

Section: Discussionmentioning

confidence: 99%

MHC Class I Presentation and Regulation by IFN in Bony Fish Determined by Molecular Analysis of the Class I Locus in Grass Carp

Chen

Jia

Zhang

et al. 2010

The Journal of Immunology

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Beyond their sequences, little is known regarding MHC class I presentation and regulation by IFN in bony fish. In this work, the class I locus (Ctid-UBA) was isolated from a grass carp fosmid library, and its polymorphisms and tissue expression were investigated. The Ctid-UBA and Ctid-β2–microglobulin genes then were expressed and refolded, and tetramer techniques were used to identify the CTL response. The interaction between grass carp type I IFN and Ctid-UBA genes was investigated. Two fosmids coding for Ctid-UBA *0101 and Ctid-UBA *0201 genes were sequenced. The SXY box and IFN-stimulated regulatory element motifs were located from the start codons to −800 bp in Ctid-UBA. A Southern blot showed three to four bands, suggesting that grass carp contains at least three class I loci. In addition, the Ctid-UBA allelic genes are expressed in all tissue of grass carp. The three-dimensional structure of Ctid-UBA *0102 showed that the peptide-binding domain was formed by the α1 and α2 domains, which could bind several nonapeptides of grass carp hemorrhagic virus. There were 1.60% more PE-positive cells in P1(QPNEAIRSL)-immunized fish than in blank and adjuvant control groups. Additionally, recombinant grass carp IFN could regulate the expression of Ctid-UBA. These results characterize the class I presentation, CTL response, and regulation by type I IFN in bony fish.

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Genomic organization of duplicated major histocompatibility complex class I regions in Atlantic salmon (Salmo salar)

Cited by 66 publications

References 62 publications

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

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

Selection and genetic drift in captive versus wild populations: an assessment of neutral and adaptive (MHC-linked) genetic variation in wild and hatchery brown trout (Salmo trutta) populations

MHC Class I Presentation and Regulation by IFN in Bony Fish Determined by Molecular Analysis of the Class I Locus in Grass Carp

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