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PMID: 17609281 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Phase-dependent immune evasion of herpesviruses.

Journal of virology ·Vol. 81 ·No. 17 ·2007-09-00 ·Pages 9536-45

Vider-Shalit T, Fishbain V, Raffaeli S, Louzoun Y

Abstract

Viruses employ various modes to evade immune detection. Two possible evasion modes are a reduction of the number of epitopes presented and the mimicry of host epitopes. The immune evasion efforts are not uniform among viral proteins. The number of epitopes in a given viral protein and the similarity of the epitopes to host peptides can be used as a measure of the viral attempts to hide this protein. Using bioinformatics tools, we here present a genomic analysis of the attempts of four human herpesviruses (herpes simplex virus type 1-human herpesvirus 1, Epstein-Barr virus-human herpesvirus 4, human cytomegalovirus-human herpesvirus 5, and Kaposi's sarcoma-associated herpesvirus-human herpesvirus 8) and one murine herpesvirus (murine herpesvirus 68) to escape from immune detection. We determined the full repertoire of CD8 T-lymphocyte epitopes presented by each viral protein and show that herpesvirus proteins present many fewer epitopes than expected. Furthermore, the epitopes that are presented are more similar to host epitopes than are random viral epitopes, minimizing the immune response. We defined a score for the size of the immune repertoire (the SIR score) based on the number of epitopes in a protein. The numbers of epitopes in proteins expressed in the latent and early phases of infection were significantly smaller than those in proteins expressed in the lytic phase in all tested viruses. The latent and immediate-early epitopes were also more similar to host epitopes than were lytic epitopes. A clear trend emerged from the analysis. In general, herpesviruses demonstrated an effort to evade immune detection. However, within a given herpesvirus, proteins expressed in phases critical to the fate of infection (e.g., early lytic and latent) evaded immune detection more than all others. The application of the SIR score to specific proteins allows us to quantify the importance of immune evasion and to detect optimal targets for immunotherapy and vaccine development.

MeSH Terms
Computational Biology Cytomegalovirus/genetics,immunology Epitopes, T-Lymphocyte/genetics,immunology Genome, Viral Herpesviridae/genetics,immunology Herpesvirus 1, Human/genetics,immunology Herpesvirus 4, Human/genetics,immunology Herpesvirus 8, Human/genetics,immunology Immediate-Early Proteins/immunology Rhadinovirus/genetics,immunology Viral Proteins/genetics,immunology Virus Latency/immunology
Chemicals
Epitopes, T-Lymphocyte Immediate-Early Proteins Viral Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Vider-Shalit Tal
Math Department, Bar Ilan University, Ramat Gan, Israel.
Fishbain Vered
Raffaeli Shai
Louzoun Yoram
References (42)
42 references, click to expand
  1. Large-scale sequencing of human influenza reveals the dynamic nature of viral genome evolution.
    Nature. 2005 Oct 20;437(7062):1162-6 PMID: 16208317
  2. Functional genomic analysis of herpes simplex virus type 1 counteraction of the host innate response.
    J Virol. 2006 Aug;80(15):7600-12 PMID: 16840339
  3. Sequence motifs important for peptide binding to the human MHC class I molecule, HLA-A2.
    J Immunol. 1992 Dec 1;149(11):3580-7 PMID: 1331239
  4. MPID: MHC-Peptide Interaction Database for sequence-structure-function information on peptides binding to MHC molecules.
    Bioinformatics. 2003 Jan 22;19(2):309-10 PMID: 12538264
  5. Escape of human immunodeficiency virus from immune control.
    Annu Rev Immunol. 1997;15:271-96 PMID: 9143689
  6. MHCBN: a comprehensive database of MHC binding and non-binding peptides.
    Bioinformatics. 2003 Mar 22;19(5):665-6 PMID: 12651731
  7. Herpesviruses--immune escape artists?
    Clin Infect Dis. 1992 Apr;14(4):933-41 PMID: 1315587
  8. CD8+ immunodominance among Epstein-Barr virus lytic cycle antigens directly reflects the efficiency of antigen presentation in lytically infected cells.
    J Exp Med. 2005 Feb 7;201(3):349-60 PMID: 15684323
  9. MHCPEP, a database of MHC-binding peptides: update 1997.
    Nucleic Acids Res. 1998 Jan 1;26(1):368-71 PMID: 9399876
  10. Population of the HLA ligand database.
    Tissue Antigens. 2003 Jan;61(1):12-9 PMID: 12622773
  11. An overview of Ensembl.
    Genome Res. 2004 May;14(5):925-8 PMID: 15078858
  12. Protein degradation and the generation of MHC class I-presented peptides.
    Adv Immunol. 2002;80:1-70 PMID: 12078479
  13. SYFPEITHI: database for MHC ligands and peptide motifs.
    Immunogenetics. 1999 Nov;50(3-4):213-9 PMID: 10602881
  14. IMGT/HLA Database--a sequence database for the human major histocompatibility complex.
    Nucleic Acids Res. 2001 Jan 1;29(1):210-3 PMID: 11125094
  15. Population biology of antigen presentation by MHC class I molecules.
    Science. 1996 Apr 5;272(5258):67-74 PMID: 8600539
  16. JenPep: a novel computational information resource for immunobiology and vaccinology.
    J Chem Inf Comput Sci. 2003 Jul-Aug;43(4):1276-87 PMID: 12870921
  17. Preventing transfusion-transmitted infections: issues related to migrating populations and increasing world travel.
    Haematologia (Budap). 1991;24(4):197-210 PMID: 1688227
  18. The role of perforin in infections and tumour surveillance.
    Exp Physiol. 2000 Nov;85(6):681-5 PMID: 11187963
  19. In vitro selection of lymphocytic choriomeningitis virus escape mutants by cytotoxic T lymphocytes.
    Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11047-51 PMID: 1722316
  20. Concurrent expression of latent and a limited number of lytic genes with immune modulation and antiapoptotic function by Kaposi's sarcoma-associated herpesvirus early during infection of primary endothelial and fibroblast cells and subsequent decline of lytic gene expression.
    J Virol. 2004 Apr;78(7):3601-20 PMID: 15016882
  21. Molecular genetics of Kaposi's sarcoma-associated herpesvirus (human herpesvirus-8) epidemiology and pathogenesis.
    Microbiol Mol Biol Rev. 2003 Jun;67(2):175-212, table of contents PMID: 12794189
  22. The human cytomegalovirus UL94 open reading frame encodes a conserved herpesvirus capsid/tegument-associated virion protein that is expressed with true late kinetics.
    J Virol. 1996 Jun;70(6):3339-45 PMID: 8648663
  23. Optimization by simulated annealing.
    Science. 1983 May 13;220(4598):671-80 PMID: 17813860
  24. Epstein-barr virus nuclear antigen 1: from immunologically invisible to a promising T cell target.
    J Exp Med. 2004 May 17;199(10):1301-4 PMID: 15148332
  25. Identifying MHC class I epitopes by predicting the TAP transport efficiency of epitope precursors.
    J Immunol. 2003 Aug 15;171(4):1741-9 PMID: 12902473
  26. Varicella-zoster virus immune evasion.
    Immunol Rev. 1999 Apr;168:143-56 PMID: 10399071
  27. The myristylated virion proteins of herpes simplex virus type 1: investigation of their role in the virus life cycle.
    J Gen Virol. 1992 Mar;73 ( Pt 3):539-47 PMID: 1312117
  28. Immune evasion mechanisms of varicella-zoster virus.
    Arch Virol Suppl. 2001;(17):99-107 PMID: 11339556
  29. Mutational escape from CD8+ T cell immunity: HCV evolution, from chimpanzees to man.
    J Exp Med. 2005 Jun 6;201(11):1709-14 PMID: 15939787
  30. Strategies and mechanisms for host and pathogen survival in acute and persistent viral infections.
    Proc Natl Acad Sci U S A. 2004 Oct 5;101 Suppl 2:14560-6 PMID: 15297608
  31. Transcription program of murine gammaherpesvirus 68.
    J Virol. 2003 Oct;77(19):10488-503 PMID: 12970434
  32. Herpes simplex virus evades natural killer T cell recognition by suppressing CD1d recycling.
    Nat Immunol. 2006 Aug;7(8):835-42 PMID: 16845396
  33. Transcriptome profile of murine gammaherpesvirus-68 lytic infection.
    J Gen Virol. 2003 Jan;84(Pt 1):99-109 PMID: 12533705
  34. Viral mimicry of cytokines, chemokines and their receptors.
    Nat Rev Immunol. 2003 Jan;3(1):36-50 PMID: 12511874
  35. Selection of the T cell repertoire.
    Annu Rev Immunol. 1999;17:829-74 PMID: 10358775
  36. T-cell epitope repertoire as predicted from human and viral genomes.
    Mol Immunol. 2006 Feb;43(6):559-69 PMID: 15927255
  37. Human cytomegalovirus-encoded US2 and US11 target unassembled MHC class I heavy chains for degradation.
    Mol Immunol. 2006 Mar;43(8):1258-66 PMID: 16098592
  38. Database resources of the National Center for Biotechnology Information.
    Nucleic Acids Res. 2005 Jan 1;33(Database issue):D39-45 PMID: 15608222
  39. Dominant influence of HLA-B in mediating the potential co-evolution of HIV and HLA.
    Nature. 2004 Dec 9;432(7018):769-75 PMID: 15592417
  40. JenPep: a database of quantitative functional peptide data for immunology.
    Bioinformatics. 2002 Mar;18(3):434-9 PMID: 11934742
  41. Human cytomegalovirus persists in its host and attacks and avoids elimination by the immune system.
    Crit Rev Immunol. 2006;26(3):231-64 PMID: 16928188
  42. The human cytomegalovirus.
    Pharmacol Ther. 2003 Jun;98(3):269-97 PMID: 12782241
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2007-09-00
Epub
2007-00-03
Pages
9536-45
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC1951411
Subset
IM
Grants
NIAID NIH HHS · R01 AI061062 · United States
NIAID NIH HHS · 1 R01 AI61062-01 · United States
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