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

@article{Boudinot2016RestrictingNM,
  title={Restricting nonclassical MHC genes coevolve with TRAV genes used by innate-like T cells in mammals},
  author={Pierre Boudinot and Stanislas Mondot and Luc Jouneau and Luc Teyton and Marie-Paule Lefranc and Olivier Lantz},
  journal={Proceedings of the National Academy of Sciences},
  year={2016},
  volume={113},
  pages={E2983 - E2992}
}
Significance The conservation and cross-reactivity between species of the T-cell receptor (TR)-V regions and restricting major histocompatibility (MH) molecules characterizing innate-like T cells, natural killer T (NKT) and mucosal-associated invariant T (MAIT), indicate important functions for these cells. Yet, we show that the two MAIT-specific genes, TRAV1 and MR1, have been lost at least three times during the evolution of mammals. In the rabbit, which has few NKT cells and no MR1, we found… 

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References

SHOWING 1-10 OF 53 REFERENCES
MR1 antigen presentation to mucosal-associated invariant T cells was highly conserved in evolution
TLDR
It is shown that both mouse and human MAIT cells display a high level of cross-reactivity on mammalian MR1 orthologs, but with differences consistent with limited ligand discrimination, demonstrating that the presentation pathway of MR1 toMAIT cells is highly evolutionarily conserved.
Exceptionally high conservation of the MHC class I-related gene, MR1, among mammals
TLDR
The findings suggest that the MR1 gene might have been established at its present location in a common ancestor of placental and marsupial mammals and that the shape of the putative ligand-binding groove in MR1 has been maintained, probably for presenting highly conserved component(s) of microbes to MAIT cells.
The molecular basis for Mucosal-Associated Invariant T cell recognition of MR1 proteins
TLDR
The elucidation of the MAIT TCR/MR1 complex structure explains how the semi-invariant MAIT-TCR engages the nonpolymorphic MR1 protein, and sheds light onto ligand discrimination by this cell type, a critical link in the understanding of the evolution of αβ T-cell recognition of MHC and MHC-like ligands.
MR1 uses an endocytic pathway to activate mucosal-associated invariant T cells
TLDR
It is demonstrated that MR1 traffics through endocytic compartments, thereby allowing MAIT cells to sample both endocytosed and endogenous antigens, and the importance of the late endosome for MR1 antigen presentation was further corroborated by the localization of MR1 molecules in the multivesicular endosomes.
Patterns of nonclassical MHC antigen presentation
TLDR
It is proposed that another MHC class Ib protein, MR1, which is required for the gut flora–dependent development of mucosa-associated invariant T cells, presents either a microbe-produced or a micro be-induced pattern.
Structure of MHC class I and class II cDNAs and possible immunodeficiency linked to class II expression in the Mexican axolotl
TLDR
The sequence analysis shows that the peptide binding region of this class II β chain is relatively well conserved, but most of all does not present any variability in the β domain in inbred as well as in wild axolotls presuming a limited antigenic presentation of few antigenic epitopes.
Genomics, isoforms, expression, and phylogeny of the MHC class I-related MR1 gene.
TLDR
The molecular identity of all human and murine MR1 isoforms generated through a complex scenario of alternative splicing is defined, some encoding secretory variants lacking the Ig-like alpha3 domain, and ubiquitous transcription of these MR1 variants in several major cell lineages is shown.
An Invariant T Cell Receptor α Chain Defines a Novel TAP-independent Major Histocompatibility Complex Class Ib–restricted α/β T Cell Subpopulation in Mammals
TLDR
A new subset of T cells, found in humans, mice, and cattle, that bear a canonical T cell receptor (TCR) α chain containing hAV7S2 and AJ33 in humans and the homologous AV19-AJ33 in mice and cattle with a CDR3 of constant length are described.
An invariant T cell receptor alpha chain is used by a unique subset of major histocompatibility complex class I-specific CD4+ and CD4-8- T cells in mice and humans
TLDR
The mouse thymus contains a mature T cell subset that is distinguishable from the mainstream thymocytes by several characteristics, and it is found that, whereas the beta chain V-D-J junctions are quite variable, a single invariant alpha chain V alpha 14-J281 is used by a majority of the TCRs.
T-cell activation by transitory neo-antigens derived from distinct microbial pathways
TLDR
It is shown that MAIT-cell activation requires key genes encoding enzymes that form 5-amino-6-d-ribitylaminouracil (5-A-RU), an early intermediate in bacterial riboflavin synthesis, and MR1 is able to capture, stabilize and present chemically unstable pyrimidine intermediates, which otherwise convert to lumazines, as potent antigens to MAIT cells.
...
1
2
3
4
5
...