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PMID: 11861847 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Physical association of the K3 protein of gamma-2 herpesvirus 68 with major histocompatibility complex class I molecules with impaired peptide and beta(2)-microglobulin assembly.

Journal of virology ·Vol. 76 ·No. 6 ·2002-03-00 ·Pages 2796-803

Yu YY, Harris MR, Lybarger L, Kimpler LA, Myers NB, Virgin HW, Hansen TH

Abstract

To persist in the presence of an active immune system, viruses encode proteins that decrease expression of major histocompatibility complex class I molecules by using a variety of mechanisms. For example, murine gamma-2 herpesvirus 68 expresses the K3 protein, which causes the rapid turnover of nascent class I molecules. In this report we show that certain mouse class I alleles are more susceptible than others to K3-mediated down regulation. Prior to their rapid degradation, class I molecules in K3-expressing cells exhibit impaired assembly with beta(2)-microglobulin. Furthermore, K3 is detected predominantly in association with class I molecules lacking assembly with high-affinity peptides, including class I molecules associated with the peptide loading complex TAP/tapasin/calreticulin. The detection of K3 with class I assembly intermediates raises the possibility that molecular chaperones involved in class I assembly are involved in K3-mediated class I regulation.

MeSH Terms
Animals Down-Regulation Gammaherpesvirinae/pathogenicity,physiology Herpesviridae Infections/virology Histocompatibility Antigens Class I/chemistry,genetics,physiology L Cells Mice Peptides/metabolism Protein Folding Viral Proteins/physiology beta 2-Microglobulin/metabolism
Chemicals
Histocompatibility Antigens Class I Peptides Viral Proteins beta 2-Microglobulin
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Yu Y Y Lawrence
Department of Genetics, Washington University School of Medicine, St. Louis, Missouri 63110, USA.
Harris Michael R
Lybarger Lonnie
Kimpler Lisa A
Myers Nancy B
Virgin Herbert W
Hansen Ted H
References (51)
51 references, click to expand
  1. Calnexin and calreticulin promote folding, delay oligomerization and suppress degradation of influenza hemagglutinin in microsomes.
    EMBO J. 1996 Jun 17;15(12):2961-8 PMID: 8670797
  2. Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin.
    Science. 1995 May 5;268(5211):726-31 PMID: 7732382
  3. Cytomegalovirus selectively blocks antigen processing and presentation of its immediate-early gene product.
    Nature. 1996 Oct 24;383(6602):720-2 PMID: 8878482
  4. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction.
    Nature. 1996 Dec 5;384(6608):432-8 PMID: 8945469
  5. The HCMV gene products US11 and US2 differ in their ability to attack allelic forms of murine major histocompatibility complex (MHC) class I heavy chains.
    J Exp Med. 1997 Jan 20;185(2):363-6 PMID: 9016885
  6. Prominence of beta 2-microglobulin, class I heavy chain conformation, and tapasin in the interactions of class I heavy chain with calreticulin and the transporter associated with antigen processing.
    J Immunol. 1997 Mar 1;158(5):2236-41 PMID: 9036970
  7. A mouse cytomegalovirus glycoprotein retains MHC class I complexes in the ERGIC/cis-Golgi compartments.
    Immunity. 1997 Jan;6(1):57-66 PMID: 9052837
  8. Human cytomegalovirus US2 destabilizes major histocompatibility complex class I heavy chains.
    J Virol. 1997 Apr;71(4):2970-9 PMID: 9060656
  9. The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP.
    Immunity. 1997 May;6(5):613-21 PMID: 9175839
  10. Complete sequence and genomic analysis of murine gammaherpesvirus 68.
    J Virol. 1997 Aug;71(8):5894-904 PMID: 9223479
  11. The effect of the proteasome inhibitor lactacystin on the presentation of transporter associated with antigen processing (TAP)-dependent and TAP-independent peptide epitopes by class I molecules.
    J Immunol. 1997 Sep 1;159(5):2139-46 PMID: 9278300
  12. Inhibition of ubiquitin/proteasome-dependent protein degradation by the Gly-Ala repeat domain of the Epstein-Barr virus nuclear antigen 1.
    Proc Natl Acad Sci U S A. 1997 Nov 11;94(23):12616-21 PMID: 9356498
  13. Viral strategies of immune evasion.
    Science. 1998 Apr 10;280(5361):248-53 PMID: 9535648
  14. Mechanisms of MHC class I--restricted antigen processing.
    Annu Rev Immunol. 1998;16:323-58 PMID: 9597133
  15. Immune evasion by cytomegalovirus--survival strategies of a highly adapted opportunist.
    Trends Microbiol. 1998 May;6(5):190-7 PMID: 9614343
  16. Nef--an adaptor adaptor?
    Trends Cell Biol. 1998 Aug;8(8):302-5 PMID: 9704405
  17. Definition and transfer of a serological epitope specific for peptide-empty forms of MHC class I.
    Int Immunol. 1999 Dec;11(12):1897-906 PMID: 10590255
  18. The luminal part of the murine cytomegalovirus glycoprotein gp40 catalyzes the retention of MHC class I molecules.
    EMBO J. 2000 Mar 1;19(5):870-81 PMID: 10698929
  19. Herpes simplex virus turns off the TAP to evade host immunity.
    Nature. 1995 Jun 1;375(6530):411-5 PMID: 7760935
  20. A viral inhibitor of peptide transporters for antigen presentation.
    Nature. 1995 Jun 1;375(6530):415-8 PMID: 7760936
  21. TAP associates with a unique class I conformation, whereas calnexin associates with multiple class I forms in mouse and man.
    J Immunol. 1995 Nov 15;155(10):4726-33 PMID: 7594473
  22. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol.
    Cell. 1996 Mar 8;84(5):769-79 PMID: 8625414
  23. Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein.
    Nat Med. 1996 Mar;2(3):338-42 PMID: 8612235
  24. Viral effects on antigen processing.
    Curr Opin Immunol. 1999 Feb;11(1):94-9 PMID: 10047534
  25. HIV-1 Nef protein binds to the cellular protein PACS-1 to downregulate class I major histocompatibility complexes.
    Nat Cell Biol. 2000 Mar;2(3):163-7 PMID: 10707087
  26. Downregulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins.
    J Virol. 2000 Jun;74(11):5300-9 PMID: 10799607
  27. Kaposi's sarcoma-associated herpesvirus encodes two proteins that block cell surface display of MHC class I chains by enhancing their endocytosis.
    Proc Natl Acad Sci U S A. 2000 Jul 5;97(14):8051-6 PMID: 10859362
  28. Inhibition of MHC class I-restricted antigen presentation by gamma 2-herpesviruses.
    Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8455-60 PMID: 10890918
  29. Kb, Kd, and Ld molecules share common tapasin dependencies as determined using a novel epitope tag.
    J Immunol. 2000 Nov 15;165(10):5656-63 PMID: 11067922
  30. Selective export of MHC class I molecules from the ER after their dissociation from TAP.
    Immunity. 2000 Dec;13(6):841-51 PMID: 11163199
  31. Association of ERp57 with mouse MHC class I molecules is tapasin dependent and mimics that of calreticulin and not calnexin.
    J Immunol. 2001 Jun 1;166(11):6686-92 PMID: 11359824
  32. Antigen presentation subverted: Structure of the human cytomegalovirus protein US2 bound to the class I molecule HLA-A2.
    Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6794-9 PMID: 11391001
  33. Tapasin enhances peptide-induced expression of H2-M3 molecules, but is not required for the retention of open conformers.
    J Immunol. 2001 Aug 15;167(4):2097-105 PMID: 11489993
  34. Interactions of HLA-B27 with the peptide loading complex as revealed by heavy chain mutations.
    Int Immunol. 2001 Oct;13(10):1275-82 PMID: 11581172
  35. Properties of monoclonal antibodies to mouse Ig allotypes, H-2, and Ia antigens.
    Curr Top Microbiol Immunol. 1978;81:115-20 PMID: 567555
  36. Biology of simian virus 40 (SV40) transplantation antigen (TrAg). V In vitro demonstration of SV40 TrAg in SV40 infected nonpermissive mouse cells by the lymphocyte mediated cytotoxicity assay.
    Virology. 1979 Aug;97(1):32-41 PMID: 224580
  37. Hybridoma cell lines secreting monoclonal antibodies to mouse H-2 and Ia antigens.
    J Immunol. 1980 Feb;124(2):533-40 PMID: 7188699
  38. An adenovirus type 2 glycoprotein blocks cell surface expression of human histocompatibility class I antigens.
    Cell. 1985 Jul;41(3):987-97 PMID: 3924414
  39. Intracellular transport of membrane glycoproteins: two closely related histocompatibility antigens differ in their rates of transit to the cell surface.
    J Cell Biol. 1985 Sep;101(3):725-34 PMID: 3928633
  40. Impaired intracellular transport of class I MHC antigens as a possible means for adenoviruses to evade immune surveillance.
    Cell. 1985 Nov;43(1):215-22 PMID: 2934137
  41. Slower processing, weaker beta 2-M association, and lower surface expression of H-2Ld are influenced by its amino terminus.
    J Immunol. 1986 Aug 1;137(3):916-23 PMID: 3522739
  42. H-2-restricted cytolytic T cells specific for HLA can recognize a synthetic HLA peptide.
    Nature. 1986 Dec 11-17;324(6097):578-9 PMID: 3491326
  43. A pentapeptide as minimal antigenic determinant for MHC class I-restricted T lymphocytes.
    Nature. 1989 Feb 16;337(6208):651-3 PMID: 2465495
  44. The specific binding of peptide ligand to Ld class I major histocompatibility complex molecules determines their antigenic structure.
    J Exp Med. 1991 Feb 1;173(2):449-59 PMID: 1703208
  45. Participation of a novel 88-kD protein in the biogenesis of murine class I histocompatibility molecules.
    J Cell Biol. 1991 Mar;112(6):1099-115 PMID: 1999467
  46. Disparate interaction of peptide ligand with nascent versus mature class I major histocompatibility complex molecules: comparisons of peptide binding to alternative forms of Ld in cell lysates and the cell surface.
    J Exp Med. 1992 Jan 1;175(1):191-202 PMID: 1730917
  47. Model for the in vivo assembly of nascent Ld class I molecules and for the expression of unfolded Ld molecules at the cell surface.
    J Exp Med. 1993 Dec 1;178(6):2035-46 PMID: 8245780
  48. MHC class I/beta 2-microglobulin complexes associate with TAP transporters before peptide binding.
    Nature. 1994 Apr 28;368(6474):864-7 PMID: 8159247
  49. A cytosolic herpes simplex virus protein inhibits antigen presentation to CD8+ T lymphocytes.
    Cell. 1994 May 20;77(4):525-35 PMID: 8187174
  50. Species-specific differences in chaperone interaction of human and mouse major histocompatibility complex class I molecules.
    J Exp Med. 1995 Jan 1;181(1):327-37 PMID: 7807012
  51. Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains.
    Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11327-33 PMID: 8876135
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2002-03-00
Pages
2796-803
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC135993
Subset
IM
Grants
NIAID NIH HHS · R01 AI042793 · United States
NHLBI NIH HHS · R01 HL060090 · United States
NIAID NIH HHS · AI01498 · United States
NIAID NIH HHS · AI16789 · United States
NIAID NIH HHS · AI46553 · United States
NIAID NIH HHS · AI45019 · United States
NCI NIH HHS · CA74730 · United States
NHLBI NIH HHS · HL60090 · United States
NIAID NIH HHS · T32 AI007163 · United States
NIAID NIH HHS · AI07163 · United States
NCI NIH HHS · R01 CA074730 · United States
NIAID NIH HHS · R01 AI046553 · United States
NIAID NIH HHS · R21 AI042793 · United States
NIAID NIH HHS · AI42793 · United States
NIAID NIH HHS · R01 AI045019 · United States
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