Abstract
An individual's CD8(+)-cytotoxic-T-lymphocyte (CTL) response to Epstein-Barr virus (EBV) latent cycle antigens focuses on a small number of immunodominant epitopes often presented by just one of the available HLA class I alleles; for example, HLA-A11-positive Caucasians frequently respond to two immunodominant HLA A11 epitopes, IVTDFSVIK (IVT) and AVFDRKSDAK (AVF), within the nuclear antigen EBNA3B. Here, we reexamine the spectrum of EBV strains present in the highly HLA-A11-positive Chinese population for sequence changes in these epitopes relative to the Caucasian type 1 prototype strain B95.8. The IVT epitope was altered in 61 of 64 Chinese type 1 viruses, with four different sequence variants being observed, and the AVF epitope was altered in 46 cases with six different sequence variants; by contrast, all 10 Chinese type 2 viruses retained the prototype 2 epitope sequences. All but one of the type 1 epitope variants were poorly recognized by IVT- or AVF-specific CTLs in pulse-chase assays of peptide-mediated target cell lysis. More importantly, we screened HLA-A11-positive Chinese donors carrying viruses with known epitope mutations for evidence of epitope-specific CTL memory by enzyme-linked immunospot assays: none of the type 1 variants tested, nor the type 2 prototype, appeared to be immunogenic in vivo. The data remain consistent with the possibility that, during virus-host coevolution, pressure from the host CTL-mediated immune response has given A11 epitope-loss viruses a selective advantage.
MeSH Terms
Amino Acid Sequence
Asians
Base Sequence
China
Epitopes, T-Lymphocyte/chemistry,genetics,immunology
Epstein-Barr Virus Infections/genetics,immunology
Epstein-Barr Virus Nuclear Antigens/chemistry,genetics,immunology
Genetic Variation
HLA-A Antigens/genetics,metabolism
HLA-A11 Antigen
Herpesvirus 4, Human/immunology
Humans
Immunodominant Epitopes
Molecular Sequence Data
Polymorphism, Genetic
T-Lymphocytes, Cytotoxic/immunology
Chemicals
EBNA-3B antigen
Epitopes, T-Lymphocyte
Epstein-Barr Virus Nuclear Antigens
HLA-A Antigens
HLA-A11 Antigen
Immunodominant Epitopes
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Midgley R S
CRUK Institute for Cancer Studies, The University of Birmingham, Birmingham, United Kingdom.
Bell A I
Yao Q Y
Croom-Carter D
Hislop A D
Whitney B M
Chan A T C
Johnson P J
Rickinson A B
References (26)
26 references, click to expand
-
Novel intertypic recombinants of epstein-barr virus in the chinese population.
J Virol. 2000 Feb;74(3):1544-8
PMID: 10627567
-
Immunodominance in major histocompatibility complex class I-restricted T lymphocyte responses.
Annu Rev Immunol. 1999;17:51-88
PMID: 10358753
-
Toward a comprehensive phylogeny for mammalian and avian herpesviruses.
J Virol. 2000 Nov;74(22):10401-6
PMID: 11044084
-
Evolution and transmission of stable CTL escape mutations in HIV infection.
Nature. 2001 Jul 19;412(6844):334-8
PMID: 11460164
-
Producing nature's gene-chips: the generation of peptides for display by MHC class I molecules.
Annu Rev Immunol. 2002;20:463-93
PMID: 11861610
-
Latent gene sequencing reveals familial relationships among Chinese Epstein-Barr virus strains and evidence for positive selection of A11 epitope changes.
J Virol. 2003 Nov;77(21):11517-30
PMID: 14557637
-
The polymorphism of HLA antigens in the Chinese.
Tissue Antigens. 1988 Oct;32(4):188-208
PMID: 3217935
-
Epstein-Barr virus types 1 and 2 differ in their EBNA-3A, EBNA-3B, and EBNA-3C genes.
J Virol. 1990 Sep;64(9):4084-92
PMID: 2166806
-
Human immunodeficiency virus genetic variation that can escape cytotoxic T cell recognition.
Nature. 1991 Dec 12;354(6353):453-9
PMID: 1721107
-
Multiple HLA A11-restricted cytotoxic T-lymphocyte epitopes of different immunogenicities in the Epstein-Barr virus-encoded nuclear antigen 4.
J Virol. 1993 Mar;67(3):1572-8
PMID: 7679748
-
An HLA-A11-specific motif in nonamer peptides derived from viral and cellular proteins.
Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2217-21
PMID: 8384718
-
HLA-A11 epitope loss isolates of Epstein-Barr virus from a highly A11+ population.
Science. 1993 Apr 2;260(5104):98-100
PMID: 7682013
-
T cell responses and virus evolution: loss of HLA A11-restricted CTL epitopes in Epstein-Barr virus isolates from highly A11-positive populations by selective mutation of anchor residues.
J Exp Med. 1994 Apr 1;179(4):1297-305
PMID: 7511684
-
Epstein-Barr virus isolates with the major HLA B35.01-restricted cytotoxic T lymphocyte epitope are prevalent in a highly B35.01-positive African population.
Eur J Immunol. 1995 Jan;25(1):102-10
PMID: 7531142
-
Unusually high frequency of Epstein-Barr virus genetic variants in Papua New Guinea that can escape cytotoxic T-cell recognition: implications for virus evolution.
J Virol. 1996 Apr;70(4):2490-6
PMID: 8642677
-
The life span of major histocompatibility complex-peptide complexes influences the efficiency of presentation and immunogenicity of two class I-restricted cytotoxic T lymphocyte epitopes in the Epstein-Barr virus nuclear antigen 4.
J Exp Med. 1996 Mar 1;183(3):915-26
PMID: 8642295
-
Epitope focusing in the primary cytotoxic T cell response to Epstein-Barr virus and its relationship to T cell memory.
J Exp Med. 1996 Nov 1;184(5):1801-13
PMID: 8920868
-
Conserved CTL epitopes within EBV latent membrane protein 2: a potential target for CTL-based tumor therapy.
J Immunol. 1997 Apr 1;158(7):3325-34
PMID: 9120290
-
Epitope-dependent selection of highly restricted or diverse T cell receptor repertoires in response to persistent infection by Epstein-Barr virus.
J Exp Med. 1997 Jul 7;186(1):83-9
PMID: 9207000
-
Rapid effector function in CD8+ memory T cells.
J Exp Med. 1997 Sep 15;186(6):859-65
PMID: 9294140
-
Evolutionary dynamics of genetic variation in Epstein-Barr virus isolates of diverse geographical origins: evidence for immune pressure-independent genetic drift.
J Virol. 1997 Nov;71(11):8340-6
PMID: 9343187
-
Natural variants of the immunodominant HLA A11-restricted CTL epitope of the EBV nuclear antigen-4 are nonimmunogenic due to intracellular dissociation from MHC class I:peptide complexes.
J Immunol. 1997 Dec 1;159(11):5383-90
PMID: 9548478
-
Direct visualization of antigen-specific CD8+ T cells during the primary immune response to Epstein-Barr virus In vivo.
J Exp Med. 1998 May 4;187(9):1395-402
PMID: 9565632
-
HLA-B27 subtype polymorphism and CTL epitope choice: studies with EBV peptides link immunogenicity with stability of the B27:peptide complex.
J Immunol. 1998 Nov 15;161(10):5252-9
PMID: 9820497
-
A re-evaluation of the frequency of CD8+ T cells specific for EBV in healthy virus carriers.
J Immunol. 1999 Feb 1;162(3):1827-35
PMID: 9973448
-
Cytotoxic T-lymphocyte responses to a polymorphic Epstein-Barr virus epitope identify healthy carriers with coresident viral strains.
J Virol. 2000 Feb;74(4):1801-9
PMID: 10644353