Co-evolution of rat Tap transporters and MHC class I RT1.A molecules

Joly, Etienne; Stevens, James; Rölle, Alexander; González, A.L.; Mehling, B.; Clarkson, C A; Howard, Jonathan; Butcher, Geoffrey W.

doi:10.1016/s0165-2478(97)85019-5

Cited by 12 publications

(20 citation statements)

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“…Alternatively, there may be subtle changes in the peptide-binding groove in the class I A and B lineages that show a preference for binding to particular types of peptide pools. For example, in rats, the 'restrictive' TAP2B gene is linked to particular class I genes encoding molecules with acidic F-pocket and load longer peptides [13,34]. However, in Xenopus class I, we have not detected obvious sequence signatures that distinguish the two class Ia lineages.…”

Section: Discussionmentioning

confidence: 61%

“…Distinctive allelic lineages of TAP2 and linkage disequilibrium between class Ia and TAP2 genes were previously reported in rats [8,9] and chickens [10]. Peptides transported by the 'restrictive' rat TAP2B presumably can be loaded onto TAP2B-linked class I molecules more efficiently [11][12][13]. A similar phenomenon is believed to occur in chickens, in which there is extremely tight genetic linkage between class Ia and TAP1/2 [10,14], and TAP1 lineages have also been described in hamsters [15].…”

Section: Introductionmentioning

confidence: 67%

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Two highly divergent ancient allelic lineages of the transporter associated with antigen processing (TAP) gene in Xenopus: further evidence for co‐evolution among MHC class I region genes

et al. 2003

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In the frog Xenopus, MHC class I antigen presentation and processing genes (the immunoproteasome LMP2 and LMP7 and the transporter TAP1 and TAP2) seem to be closely linked in a primordial organization. Two distinct lineages of class Ia and LMP7 loci were previously identified, thus strongly suggesting co-evolution among 'class I region' genes. We now show that the Xenopus MHC 'class I region' lies between class II and class III genes and we have isolated two distinct alleles at both the TAP1 and TAP2 loci. The alleles at each locus are remarkably divergent from each other and phylogenetic tree analysis revealed in both cases that they diverged from each other 60-100 million years ago (MYA). For lineage-frequency and linkage analysis, 25 wild-caught X. laevis and 16 X. tropicalis were examined. The two lineages were present in different frequencies for X. laevis and X. tropicalis. Nevertheless, in all cases, the LMP7, TAP1, and TAP2 lineages were found in a set comprising one of the two lineages. Furthermore, like the LMP7 lineages, the TAP lineages were detected in most Xenopus species that diverged from a common ancestor 80-100 MYA, suggesting that the 'class I region' biallelic lineages are under balancing selection.

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Section: Discussionmentioning

confidence: 61%

Section: Introductionmentioning

confidence: 67%

Two highly divergent ancient allelic lineages of the transporter associated with antigen processing (TAP) gene in Xenopus: further evidence for co‐evolution among MHC class I region genes

et al. 2003

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“…Based on our discovery that the transporter associated with antigen presentation (TAP) genes are located between the class I genes in chicken (1, 2), we proposed that the coevolution of linked polymorphic genes could be the explanation (1, 2, 8-11). This concept was first developed for mouse class II genes and then used to explain the relationship of rat class I and TAP2 genes (14)(15)(16).…”

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confidence: 99%

The dominantly expressed class I molecule of the chicken MHC is explained by coevolution with the polymorphic peptide transporter (TAP) genes

Walker

Hunt

Sowa

et al. 2011

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

129

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In most mammals, the MHC class I molecules are polymorphic and determine the specificity of peptide presentation, whereas the transporter associated with antigen presentation (TAP) heterodimers are functionally monomorphic. In chickens, there are two classical class I genes but only one is expressed at a high level, which can result in strong MHC associations with resistance to particular infectious pathogens. However, the basis for having a single dominantly expressed class I molecule has been unclear. Here we report TAP1 and TAP2 sequences from 16 chicken lines, and show that both genes have high allelic polymorphism and moderate sequence diversity, with variation in positions expected for peptide binding. We analyze peptide translocation in two MHC haplotypes, showing that chicken TAPs specify translocation at three peptide positions, matching the peptide motif of the single dominantly expressed class I molecule. These results show that coevolution between class I and TAP genes can explain the presence of a single dominantly expressed class I molecule in common chicken MHC haplotypes. Moreover, such coevolution in the primordial MHC may have been responsible for the appearance of the antigen presentation pathways at the birth of the adaptive immune system. avian | evolution | bird

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“…Such coevolution requires close genetic linkage (13)(14)(15) and, in fact, no recombination between the serologically defined class I and class II B genes has been observed in thousands of experimental matings (16 -19).…”

mentioning

confidence: 99%

Different Evolutionary Histories of the Two Classical Class I Genes BF1 and BF2 Illustrate Drift and Selection within the Stable MHC Haplotypes of Chickens

Shaw

Powell

Marston

et al. 2007

The Journal of Immunology

108

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Compared with the MHC of typical mammals, the chicken MHC (BF/BL region) of the B12 haplotype is smaller, simpler, and rearranged, with two classical class I genes of which only one is highly expressed. In this study, we describe the development of long-distance PCR to amplify some or all of each class I gene separately, allowing us to make the following points. First, six other haplotypes have the same genomic organization as B12, with a poorly expressed (minor) BF1 gene between DMB2 and TAP2 and a well-expressed (major) BF2 gene between TAP2 and C4. Second, the expression of the BF1 gene is crippled in three different ways in these haplotypes: enhancer A deletion (B12, B19), enhancer A divergence and transcription start site deletion (B2, B4, B21), and insertion/rearrangement leading to pseudogenes (B14, B15). Third, the three kinds of alterations in the BF1 gene correspond to dendrograms of the BF1 and poorly expressed class II B (BLB1) genes reflecting mostly neutral changes, while the dendrograms of the BF2 and well-expressed class II (BLB2) genes each have completely different topologies reflecting selection. The common pattern for the poorly expressed genes reflects the fact the BF/BL region undergoes little recombination and allows us to propose a pattern of descent for these chicken MHC haplotypes from a common ancestor. Taken together, these data explain how stable MHC haplotypes predominantly express a single class I molecule, which in turn leads to striking associations of the chicken MHC with resistance to infectious pathogens and response to vaccines.

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Co-evolution of rat Tap transporters and MHC class I RT1.A molecules

Cited by 12 publications

References 0 publications

Two highly divergent ancient allelic lineages of the transporter associated with antigen processing (TAP) gene in Xenopus: further evidence for co‐evolution among MHC class I region genes

Two highly divergent ancient allelic lineages of the transporter associated with antigen processing (TAP) gene in Xenopus: further evidence for co‐evolution among MHC class I region genes

The dominantly expressed class I molecule of the chicken MHC is explained by coevolution with the polymorphic peptide transporter (TAP) genes

Different Evolutionary Histories of the Two Classical Class I Genes BF1 and BF2 Illustrate Drift and Selection within the Stable MHC Haplotypes of Chickens

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