Evolution and comparative analysis of the bat MHC-I region

Ng, Justin H. J.; Tachedjian, Mary; Deakin, Janine E.; Wynne, James W.; Cui, Jie; Häring, Volker; Broz, Ivano; Chen, Honglei; Belov, Katherine; Wang, Lin‐Fa; Baker, Michelle L.

doi:10.1038/srep21256

Cited by 48 publications

(58 citation statements)

References 76 publications

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“…In the microbat, numerous CD1 genes are found, whereas (classic?) MH1 genes (e.g., XP_014304883) contain insertions within their peptide-binding grooves, which would affect the nature and diversity of peptides presented to T cells (42). Notably, the number of CD1 genes and other "recent" MH1Like genes seems to be higher in species lacking MR1 [following Rodgers and Cook (1)]: For instance, the cat harbors five CD1 and 10 other "recent" MH1Like genes, whereas the armadillo has only one CD1 but 49 MH1Like genes.…”

Section: Discussionmentioning

confidence: 99%

Restricting nonclassical MHC genes coevolve with TRAV genes used by innate-like T cells in mammals

Boudinot

Mondot

Jouneau

et al. 2016

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

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Whereas major histocompatibility class-1 (MH1) proteins present peptides to T cells displaying a large T-cell receptor (TR) repertoire, MH1Like proteins, such as CD1D and MR1, present glycolipids and microbial riboflavin precursor derivatives, respectively, to T cells expressing invariant TR-α (iTRA) chains. The groove of such MH1Like, as well as iTRA chains used by mucosal-associated invariant T (MAIT) and natural killer T (NKT) cells, respectively, may result from a coevolution under particular selection pressures. Herein, we investigated the evolutionary patterns of the iTRA of MAIT and NKT cells and restricting MH1Like proteins: MR1 appeared 170 Mya and is highly conserved across mammals, evolving more slowly than other MH1Like. It has been pseudogenized or independently lost three times in carnivores, the armadillo, and lagomorphs. The corresponding TRAV1 gene also evolved slowly and harbors highly conserved complementarity determining regions 1 and 2. TRAV1 is absent exclusively from species in which MR1 is lacking, suggesting that its loss released the purifying selection on MR1. In the rabbit, which has very few NKT and no MAIT cells, a previously unrecognized iTRA was identified by sequencing leukocyte RNA. This iTRA uses TRAV41, which is highly conserved across several groups of mammals. A rabbit MH1Like gene was found that appeared with mammals and is highly conserved. It was independently lost in a few groups in which MR1 is present, like primates and Muridae, illustrating compensatory emergences of new MH1Like/Invariant T-cell combinations during evolution. Deciphering their role is warranted to search similar effector functions in humans.MHC | TCR | MAIT | evolution | mammals

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Section: Discussionmentioning

confidence: 99%

Restricting nonclassical MHC genes coevolve with TRAV genes used by innate-like T cells in mammals

Boudinot

Mondot

Jouneau

et al. 2016

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

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“…RNA extraction was performed using the RNeasy mini kit (Qiagen) including on column DNase digestion to remove traces of genomic DNA and subsequently reverse transcribed into cDNA using SuperScript III (Life Technologies) as per the manufacturer's instructions using random hexamers. To amplify P. alecto MHC class I sequences, 59 and 39 rapid amplification of cDNA ends (RACE) PCR was performed on P. alecto thymus RNA using primers based on MHC class I genes identified in the Pteropus vampyrus genome (Ensembl version pteVam1) (25). The resulting cDNA sequences were used to design specific primers MHC_1_ FORWARD_SHORT (59-ATGCAGGTCATGGGGCCCCGA-39) and MHC_1_REVERSE_SHORT (59-TCATGCTTTAGAAGCTGTGAG-39) for the amplification of full-length genes.…”

Section: Pcr Amplification and Cloningmentioning

confidence: 99%

“…It is unknown whether bat MHC class I molecules imputed from genomic data (24) mature in a similar manner to human and murine MHC and whether they use similar PLC chaperones. Genomic analysis of the MHC class I region of P. alecto has demonstrated that this species has a highly condensed, yet conserved organization across the MHC loci (25). Given the significance of bats as viral reservoirs, we sought to functionally characterize a bat MHC class I homolog and to identify endogenous and viral peptide ligands, if any, bound to this molecule.…”

mentioning

confidence: 99%

Characterization of the Antigen Processing Machinery and Endogenous Peptide Presentation of a Bat MHC Class I Molecule

Wynne

Woon

Dudek

et al. 2016

The Journal of Immunology

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Bats are a major reservoir of emerging and re-emerging infectious diseases, including severe acute respiratory syndrome–like coronaviruses, henipaviruses, and Ebola virus. Although highly pathogenic to their spillover hosts, bats harbor these viruses, and a large number of other viruses, with little or no clinical signs of disease. How bats asymptomatically coexist with these viruses is unknown. In particular, little is known about bat adaptive immunity, and the presence of functional MHC molecules is mostly inferred from recently described genomes. In this study, we used an affinity purification/mass spectrometry approach to demonstrate that a bat MHC class I molecule, Ptal-N*01:01, binds antigenic peptides and associates with peptide-loading complex components. We identified several bat MHC class I–binding partners, including calnexin, calreticulin, protein disulfide isomerase A3, tapasin, TAP1, and TAP2. Additionally, endogenous peptide ligands isolated from Ptal-N*01:01 displayed a relatively broad length distribution and an unusual preference for a C-terminal proline residue. Finally, we demonstrate that this preference for C-terminal proline residues was observed in Hendra virus–derived peptides presented by Ptal-N*01:01 on the surface of infected cells. To our knowledge, this is the first study to identify endogenous and viral MHC class I ligands for any bat species and, as such, provides an important avenue for monitoring and development of vaccines against major bat-borne viruses both in the reservoir and spillover hosts. Additionally, it will provide a foundation to understand the role of adaptive immunity in bat antiviral responses.

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“…Recent genomic studies have offered considerable insights into the evolution of the vertebrate adaptive immune system by comparing phylogenetically divergent species (11)(12)(13)(14). Throughout vertebrates, gene linkage within the MHC region is highly conserved.…”

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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 and comparative analysis of the bat MHC-I region

Cited by 48 publications

References 76 publications

Restricting nonclassical MHC genes coevolve with TRAV genes used by innate-like T cells in mammals

Restricting nonclassical MHC genes coevolve with TRAV genes used by innate-like T cells in mammals

Characterization of the Antigen Processing Machinery and Endogenous Peptide Presentation of a Bat MHC Class I Molecule

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

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