Classical MHC Class I Genes Composed of Highly Divergent Sequence Lineages Share a Single Locus in Rainbow Trout (<i>Oncorhynchus mykiss</i>)

Aoyagi, Kazuhiko; Dijkstra, Johannes M.; Xia, Chun; Denda, Ikuo; Ototake, Mitsuru; Hashimoto, Keiichiro; Nakanishi, Teruyuki

doi:10.4049/jimmunol.168.1.260

Cited by 89 publications

(131 citation statements)

References 38 publications

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“…Unlike the sturgeon in which the four ␤ 2 m alleles sort into two pairs of more closely related alleles (19), there is no indication for diploidization of the rainbow trout ␤ 2 m locus. This is in contrast with MHC class I of rainbow trout, for which a maximum of two Onmy UBA alleles can be detected in an individual (29,30).…”

Section: Discussionmentioning

confidence: 66%

The β2-Microglobulin Locus of Rainbow Trout (Oncorhynchus mykiss) Contains Three Polymorphic Genes

Magor

Shum

Parham

2004

The Journal of Immunology

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β2-microglobulin (β2m) associates with MHC and related class I H chains to form cell surface glycoproteins that mediate a variety of functions in defense. In humans, monomorphism of a single β2m gene contrasts with the diversity and polymorphism of the class I H chain genes, and a similar picture was seen in almost all other species examined. In this regard, rainbow trout (Oncorhynchus mykiss) appeared unusual: trout β2m genes gave a complicated and polymorphic pattern in Southern blots, and a minimum of 10 different mRNA encoding two distinct types of β2m were expressed by a single fish. Characterization of genomic clones from the same fish now shows that the rainbow trout β2m locus consists of two expressed genes and one partial gene that are closely linked. Four copies of the locus were identified and allelic variants of each gene defined, largely through comparison of the noncoding regions. A dramatic variation in the lengths of introns is caused by variable repetitive elements and accounts for the complex pattern seen in Southern blots. By comparison to noncoding sequences, the coding regions are conserved but the three loci differ within a cluster of codons that encode residues of β2m that do not interact with class I H chains. Additional diversity in the trout β2m genes appears to be due to somatic mutation that might be facilitated by the abundance of repetitive DNA elements within the 12 β2m genes of an individual rainbow trout.

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Section: Discussionmentioning

confidence: 66%

The β2-Microglobulin Locus of Rainbow Trout (Oncorhynchus mykiss) Contains Three Polymorphic Genes

Magor

Shum

Parham

2004

The Journal of Immunology

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“…Presumably there has been a whole genome duplication event early in the salmonid lineage (Allendorf and Thorgaard, 1984), resulting in two similar MHC class I region copies on two different chromosomes, each encoding MHC class I genes plus a set of genes involved in MHC class I loading (Phillips et al, 2003;Shiina et al, 2005). One re-gion (RT-16) may only encode the single MHC class Ia locus Onmy-UBA (Aoyagi et al, 2002), whereas the other region (RT-3) does not encode Ia but encodes a set of at least three intact class Ib loci-Onmy-UCA, Onmy-UDA, and Onmy-UEA (Shiina et al, 2005)-and likely additional class I genes as well (Hansen, personal communication). The loci Onmy-UCA, Onmy-UDA, and Onmy-UEA are located together within a stretch of only 50 kb, and therefore the Onmy-UEA mapping performed in the present study simultaneously mapped Onmy-UCA and Onmy-UDA.…”

Section: Discussionmentioning

confidence: 99%

“…Segregation of Onmy-UBA alleles in the 97-K2-2 backcross family was studied by separately applying two UBA-a1 primer sets, namely p601-A1-F1 (5¢-AACAAGGCAGCAGAAACACTG-3¢) in combination with pA1-1-R1 (5¢-TCCACTTTGGTTAA-AACGCTG-3¢), which amplifies a UBA fragment from the YN-RT201 resistant strain, and A1-3-F1 (5¢-ACTG-CAACTTCCGGAGTACCAG-3¢) in conjunction with pA1-3-R1 (5¢-CTCGTCACCAATGGAGTTCTGA-3¢), which amplifies a UBA fragment from the YK-RT101 susceptible strain. PCR analysis was performed for 35 cycles at an annealing temperature of 55∞C and an extension time of 30 s. The fragments that were amplified with p601-A1-F1/pA1-1-R1 and pA1-3-F1/pA3-3-R1 were sequenced and found identical to the alleles Onmy-UBA*601 (Aoyagi et al, 2002) and Onmy-UBA*05 (Shum et al, 2001), respectively; the a1 domains encoded by Onmy-UBA*601 and Onmy-UBA*0501 share only 63% identity.…”

Section: Mapping Of Tyrosinase and Mhc Genesmentioning

confidence: 99%

“…Mapping of the classical MHC class I locus Onmy-UBA: Because the Onmy-UBA gene has very large introns (~18 kb; Shiina et al, 2005), we investigated its a1 exon only, for which widely divergent allelic lineages have been described (Shum et al, 2001;Aoyagi et al, 2002;Kiryu et al, 2005). Segregation of Onmy-UBA alleles in the 97-K2-2 backcross family was studied by separately applying two UBA-a1 primer sets, namely p601-A1-F1 (5¢-AACAAGGCAGCAGAAACACTG-3¢) in combination with pA1-1-R1 (5¢-TCCACTTTGGTTAA-AACGCTG-3¢), which amplifies a UBA fragment from the YN-RT201 resistant strain, and A1-3-F1 (5¢-ACTG-CAACTTCCGGAGTACCAG-3¢) in conjunction with pA1-3-R1 (5¢-CTCGTCACCAATGGAGTTCTGA-3¢), which amplifies a UBA fragment from the YK-RT101 susceptible strain.…”

Section: Mapping Of Tyrosinase and Mhc Genesmentioning

confidence: 99%

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Identification of Additional Quantitative Trait Loci (QTL) Responsible for Susceptibility to Infectious Pancreatic Necrosis Virus in Rainbow Trout

et al. 2007

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ABSTRACT-Previous typing of microsatellite markers in a BC 1 F 1 backcross rainbow trout Oncorhynchus mykiss revealed two quantitative trait loci (QTL) with a significant impact on susceptibility to infectious pancreatic necrosis. In the present study, additional genetic markers were mapped using the same strain in order to increase QTL resolution. A total of 199 individuals were screened at 226 marker loci (106 microsatellites, 116 amplified fragment length polymorphism markers, classical major histocompatibility complex molecules [MHC class I, nonclassical MHC class I, MHC class II] and tyrosinase) and the QTL were determined by single-point and interval mappings. Seven QTL were distinguished in the linkage groups 12, 17, 23, 26, 29 and 31, in addition to the two already known in RT-3 and 22. The major QTL were those in RT-3, 12 and 22; whereas the classical MHC class I locus Onmy-UBA and the MHC class II locus Onmy-DAB were not associated with any of the QTL, a nonclassical MHC class I region with Onmy-UCA, Onmy-UDA, and Onmy-UEA mapped to the major QTL on RT-3.

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“…Starting with this diversity, balancing selection preserves polymorphism within populations during conditions when no single allele is optimized for all environments, with a disproportionate impact on immune loci (6). Some nonmammalian vertebrates, such as bony fish, frogs, and sharks, maintain MHC polymorphism at even higher levels than mammals (7)(8)(9)(10), implying preservation of ancient alleles across different species.…”

mentioning

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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Classical MHC Class I Genes Composed of Highly Divergent Sequence Lineages Share a Single Locus in Rainbow Trout (Oncorhynchus mykiss)

Cited by 89 publications

References 38 publications

The β2-Microglobulin Locus of Rainbow Trout (Oncorhynchus mykiss) Contains Three Polymorphic Genes

The β2-Microglobulin Locus of Rainbow Trout (Oncorhynchus mykiss) Contains Three Polymorphic Genes

Identification of Additional Quantitative Trait Loci (QTL) Responsible for Susceptibility to Infectious Pancreatic Necrosis Virus in Rainbow Trout

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

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