Gene duplication and fragmentation in the zebra finch major histocompatibility complex

Balakrishnan, Christopher N.; Ekblom, Robert; Volker, Martin A.; Westerdahl, Helena; Godinez, Ricardo; Kotkiewicz, Holly; Burt, David W.; Graves, Tina; Griffin, Darren K.; Warren, Wesley C.; Edwards, Scott V.

doi:10.1186/1741-7007-8-29

Cited by 126 publications

(163 citation statements)

References 79 publications

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“…BLAST search approaches in chicken, turkey, quail, black grouse, and zebra finch failed to detect genes for immuno-and thymoproteasome, suggesting that they have been lost in the lineage of birds (Balakrishnan et al 2010;Chaves et al 2009;Shiina et al 2007;Shiina et al 2004;Sutoh et al 2012;Wang et al 2012). While the genes coding for the catalytic subunits β1i and β5i are present in the class II region of the human and murine MHC loci, sequence searches in chicken genome databases revealed that there are no LMP genes in the avian MHC region, and also the immune subunit β2i could not be identified.…”

Section: Introductionmentioning

confidence: 99%

No evidence for immunoproteasomes in chicken lymphoid organs and activated lymphocytes

Erath

Groettrup

2014

Immunogenetics

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The proteasome is the main protein-degrading machine within the cell, producing ligands for MHC class I molecules. It is a cylindrical multicatalytic protease complex, and the catalytic activity is mediated by the three subunits β1, β2, and β5 which possess caspase-, trypsin-, and chymotrypsin-like activities, respectively. By stimulation with interferon (IFN)-γ the replacement of these subunits by β1i, β2i, and β5i is induced leading to formation of immunoproteasomes with altered proteolytic and antigen processing properties. The genes coding for these immunosubunits are restricted to jawed vertebrates but have so far not been found in the genomes of birds, e.g., chicken, turkey, quail, black grouse and zebra finch. However, the chicken genome sequences are not completely assigned; therefore, we investigated the presence of immunoproteasome on protein level. 20S proteasome was purified from the chicken brain, blood, spleen, and bursa of Fabricius, followed by separation via two-dimensional (2D) gel electrophoresis. We analyzed the protein spots derived from the spleen and brain by mass spectrometry and could identify all 14 proteasomal subunits, but there were no differences detectable in the spot patterns. Moreover, we stimulated the chicken spleen cells with phorbol 12-myristate 13-acetate (PMA) and ionomycin aiming at the induction of immunoproteasome, but in spite of the induction of proliferation and IFN-γ, no evidence for immunoproteasome formation in chicken could be obtained. This result was substantiated by the finding that 20S proteasomes isolated from immune and non-immune tissues showed very similar peptidolytic activities. Taken together, our results indicate that chicken lack immunoproteasomes also on protein level.

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Section: Introductionmentioning

confidence: 99%

No evidence for immunoproteasomes in chicken lymphoid organs and activated lymphocytes

Erath

Groettrup

2014

Immunogenetics

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“…However, the Inoko group has since published that only one of these two expressed classical loci is highly expressed (26), much like the chicken. In zebra finch there has also been expansion and fragmentation of the MHC complex (27); however, there is only one functional MHC class I locus, although synteny with TAP2 appears to have been lost. In the Red-Billed gull, four loci were identified in the genome, all transcribed, but using a combination of reference strand conformation analysis, sequencing, and phylogenetic analyses the researchers conclude that only Lasc-UAA is a classical MHC class I gene (28).…”

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confidence: 99%

Extensive Allelic Diversity of MHC Class I in Wild Mallard Ducks

Fleming-Canepa

Jensen

Mesa

et al. 2016

The Journal of Immunology

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MHC class I is critically involved in defense against viruses, and diversity from polygeny and polymorphism contributes to the breadth of the immune response and health of the population. In this article, we examine MHC class I diversity in wild mallard ducks, the natural host and reservoir of influenza A viruses. We previously showed domestic ducks predominantly use UAA, one of five MHC class I genes, but whether biased expression is also true for wild mallards is unknown. Using RT-PCR from blood, we examined expressed MHC class I alleles from 38 wild mallards (Anas platyrhynchos) and identified 61 unique alleles, typically 1 or 2 expressed alleles in each individual. To determine whether expressed alleles correspond to UAA adjacent to TAP2 as in domestic ducks, we cloned and sequenced genomic UAA-TAP2 fragments from all mallards, which matched transcripts recovered and allowed us to assign most alleles as UAA. Allelic differences are primarily located in α1 and α2 domains in the residues known to interact with peptide in mammalian MHC class I, suggesting the diversity is functional. Most UAA alleles have unique residues in the cleft predicting distinct specificity; however, six alleles have an unusual conserved cleft with two cysteine residues. Residues that influence peptide-loading properties and tapasin involvement in chicken are fixed in duck alleles and suggest tapasin independence. Biased expression of one MHC class I gene may make viral escape within an individual easy, but high diversity in the population places continual pressure on the virus in the reservoir species.

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“…Recent studies of the zebra finch ( Taeniopygia guttata ) genome find evidence for gene duplication and fragmentation of the MHC [Balakrishnan et al, 2010]. Here, the sequence associated with the MHC spans a minimum of 739 kb.…”

Section: Discussionmentioning

confidence: 99%

Sequence of a Turkey BAC Clone Identifies MHC Class III Orthologs and Supports Ancient Origins of Immunological Gene Clusters

Chaves

Krueth

Bauer

et al. 2010

Cytogenet Genome Res

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Two genetically unlinked gene clusters currently define the turkey major histocompatibility complex (MHC). Previous studies identified turkey bacterial artificial chromosome (BAC) clones hypothesized as orthologs of the MHC-B and MHC-Y regions of the chicken. Physical mapping assigned these clones to the same microchromosome (MGA18) and sequencing of the MHC-B BAC found near synteny with a portion of the chicken B-locus. This study examines the sequence of the second MHC BAC clone that was hypothesized, based on subclone sequences, to be orthologous to the MHC-Y. Sequencing of this clone identified a class I locus and orthologs of additional genes found in the mammalian class III region. Approximately 50% of the BAC insert is comprised of sequence corresponding to the centromeric repeat, MGASat2. This turkey MHC BAC sequence is unique from sequences assigned to the MHC-Y in the chicken. Based on sequence comparisons, the class I gene appears to be a nonfunctional pseudogene. The class III genes (BAT1, BAT3, STK19, and a G4-like locus) represent the second class III gene cluster identified in the galliform genome. This cluster appears to be of ancient origin and provides insight into the evolution of the avian MHC.

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Gene duplication and fragmentation in the zebra finch major histocompatibility complex

Cited by 126 publications

References 79 publications

No evidence for immunoproteasomes in chicken lymphoid organs and activated lymphocytes

No evidence for immunoproteasomes in chicken lymphoid organs and activated lymphocytes

Extensive Allelic Diversity of MHC Class I in Wild Mallard Ducks

Sequence of a Turkey BAC Clone Identifies MHC Class III Orthologs and Supports Ancient Origins of Immunological Gene Clusters

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