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A mechanistic basis for the co-evolution of chicken tapasin and major histocompatibility complex class I (MHC I) proteins

A mechanistic basis for the co-evolution of chicken tapasin and major histocompatibility complex class I (MHC I) proteins
A mechanistic basis for the co-evolution of chicken tapasin and major histocompatibility complex class I (MHC I) proteins
MHC class I molecules display peptides at the cell surface to cytotoxic T cells. The co-factor tapasin functions to ensure MHC I become loaded with high affinity peptides. In most mammals, the tapasin gene appears to have little sequence diversity and few alleles and is located distal to several classical MHC I loci, so tapasin appears to function in a universal way to assist MHC I peptide loading. In contrast the chicken tapasin gene is tightly linked to the single dominantly expressed MHC I locus, is highly polymorphic and moderately diverse in sequence. Therefore tapasin-assisted loading of MHC I in chickens may occur in a haplotype-specific way, via the co-evolution of chicken tapasin and MHC I. Here we demonstrate a mechanistic basis for this co-evolution, revealing differences in the ability of two chicken MHC I alleles to bind and release peptides in the presence or absence of tapasin, where like in mammals efficient self-loading is negatively correlated with tapasin-assisted loading. We found that a polymorphic residue in the MHC I ?3 domain thought to bind tapasin influenced both tapasin function as well as intrinsic peptide-binding properties. Differences were also evident between the MHC alleles in their interactions with tapasin. Lastly we show that a mismatched combination of tapasin and MHC alleles exhibit significantly impaired MHC I maturation in vivo, and that polymorphic MHC residues thought to contact tapasin influence maturation efficiency. Collectively this supports the possibility that tapasin and BF2 proteins have co-evolved resulting in allele-specific peptide-loading in vivo.
antigen presentation, evolution, immunology, major histocompatibility complex (mhc), protein-protein interactions, chicken mhc, co-evolution, peptide selection, tapasin
0021-9258
n/a
Van Hateren, A.
e345fa3c-d89c-4b91-947e-c1d818cc7f71
Carter, R.
840a775a-867e-42ba-a7cb-d131c9fdb9c6
Bailey, A.
541e2cd9-ac72-4058-9293-def64fc2c284
Kontouli, N.
63602628-7753-421d-817e-071cd752b848
Williams, A.P.
973ff46f-46f1-4d7c-b27d-0f53221e4c44
Kaufman, J.
3efdcaaf-f10f-4b98-944f-3fc88f5508c7
Elliott, T.J.
16670fa8-c2f9-477a-91df-7c9e5b453e0e
Van Hateren, A.
e345fa3c-d89c-4b91-947e-c1d818cc7f71
Carter, R.
840a775a-867e-42ba-a7cb-d131c9fdb9c6
Bailey, A.
541e2cd9-ac72-4058-9293-def64fc2c284
Kontouli, N.
63602628-7753-421d-817e-071cd752b848
Williams, A.P.
973ff46f-46f1-4d7c-b27d-0f53221e4c44
Kaufman, J.
3efdcaaf-f10f-4b98-944f-3fc88f5508c7
Elliott, T.J.
16670fa8-c2f9-477a-91df-7c9e5b453e0e

Van Hateren, A., Carter, R., Bailey, A., Kontouli, N., Williams, A.P., Kaufman, J. and Elliott, T.J. (2013) A mechanistic basis for the co-evolution of chicken tapasin and major histocompatibility complex class I (MHC I) proteins The Journal of Biological Chemistry, n/a, n/a. (doi:10.1074/jbc.M113.474031). (PMID:24078633).

Record type: Article

Abstract

MHC class I molecules display peptides at the cell surface to cytotoxic T cells. The co-factor tapasin functions to ensure MHC I become loaded with high affinity peptides. In most mammals, the tapasin gene appears to have little sequence diversity and few alleles and is located distal to several classical MHC I loci, so tapasin appears to function in a universal way to assist MHC I peptide loading. In contrast the chicken tapasin gene is tightly linked to the single dominantly expressed MHC I locus, is highly polymorphic and moderately diverse in sequence. Therefore tapasin-assisted loading of MHC I in chickens may occur in a haplotype-specific way, via the co-evolution of chicken tapasin and MHC I. Here we demonstrate a mechanistic basis for this co-evolution, revealing differences in the ability of two chicken MHC I alleles to bind and release peptides in the presence or absence of tapasin, where like in mammals efficient self-loading is negatively correlated with tapasin-assisted loading. We found that a polymorphic residue in the MHC I ?3 domain thought to bind tapasin influenced both tapasin function as well as intrinsic peptide-binding properties. Differences were also evident between the MHC alleles in their interactions with tapasin. Lastly we show that a mismatched combination of tapasin and MHC alleles exhibit significantly impaired MHC I maturation in vivo, and that polymorphic MHC residues thought to contact tapasin influence maturation efficiency. Collectively this supports the possibility that tapasin and BF2 proteins have co-evolved resulting in allele-specific peptide-loading in vivo.

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More information

e-pub ahead of print date: 27 September 2013
Keywords: antigen presentation, evolution, immunology, major histocompatibility complex (mhc), protein-protein interactions, chicken mhc, co-evolution, peptide selection, tapasin
Organisations: Cancer Sciences

Identifiers

Local EPrints ID: 358904
URI: http://eprints.soton.ac.uk/id/eprint/358904
ISSN: 0021-9258
PURE UUID: c55c2c2b-efca-40ad-8018-5883f173212d
ORCID for A. Bailey: ORCID iD orcid.org/0000-0003-0023-8679
ORCID for T.J. Elliott: ORCID iD orcid.org/0000-0003-1097-0222

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Date deposited: 21 Oct 2013 13:23
Last modified: 18 Jul 2017 03:25

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Contributors

Author: A. Van Hateren
Author: R. Carter
Author: A. Bailey ORCID iD
Author: N. Kontouli
Author: A.P. Williams
Author: J. Kaufman
Author: T.J. Elliott ORCID iD

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