Inhibition of HLA-DR assembly, transport, and loading by human cytomegalovirus glycoprotein US3: A novel mechanism for evading major histocompatibility complex class II antigen presentation

Journal of Virology

Volumn 76, Issue 21, 2002, Pages 10929-10941

  Hegde, Nagendra R ^a   Tomazin, Roman A ^a   Wisner, Todd W ^a   Dunn, Claire ^a   Boname, Jessica M ^a   Lewinsohn, David M ^a   Johnson, David C ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CD4 ANTIGEN; CD8 ANTIGEN; GLYCOPROTEIN US11; GLYCOPROTEIN US2; GLYCOPROTEIN US3; GLYCOPROTEIN US6; HLA DR ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; UNCLASSIFIED DRUG; VIRUS ANTIGEN; VIRUS GLYCOPROTEIN;

ANTIGEN PRESENTATION; ANTIGEN RECOGNITION; ARTICLE; CONTROLLED STUDY; GENE CASSETTE; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; IMMUNITY; MAJOR HISTOCOMPATIBILITY COMPLEX; NONHUMAN; PERSISTENT INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; T LYMPHOCYTE; VIRUS GENE; VIRUS REPLICATION;

ANTIGEN PRESENTATION; BIOLOGICAL TRANSPORT; CD4-POSITIVE T-LYMPHOCYTES; CYTOMEGALOVIRUS; DIMERIZATION; ENDOPLASMIC RETICULUM; GLYCOPROTEINS; GOLGI APPARATUS; HISTOCOMPATIBILITY ANTIGENS CLASS II; HLA-DR ANTIGENS; HUMANS; IMMEDIATE-EARLY PROTEINS; LYSOSOMES; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; PEPTIDES; RNA-BINDING PROTEINS; SUBCELLULAR FRACTIONS; TUMOR CELLS, CULTURED; VIRAL PROTEINS;

EID: 0036838715     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.76.21.10929-10941.2002     Document Type: Article

References (65)

1. Adorini, L., S. J. Ullrich, E. Appella, and S. Fuchs. 1990. Inhibition by brefeldin A of presentation of exogenous protein antigens to MHC class II-restricted T cells. Nature 346:63-66.
2. Ahn, K., A. Angulo, P. Ghazal, P. A. Peterson, Y. Yang, and K. Fruh. 1996. Human cytomegalovirus inhibits antigen presentation by a sequential multistep process. Proc. Natl. Acad. Sci. USA 93:10990-10995.
3. , Ahn, K., A. Gruhler, B. Galocha, T. R. Jones, E. J. Wiertz, H. L. Ploegh, P. A. Peterson, Y. Yang, and K. Fruh. 1997. The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6:613-621.
4. Beersma, M. F., M. J. Bijlmakers, and H. L. Ploegh. 1993. Human cytomegalovirus down-regulates HLA class I expression by reducing the stability of class I H chains. J. Immunol. 151:4455-4464.
5. Ben-Arieh, S. V., B. Zimerman, N. I. Smorodinsky, M. Yaacubovicz, C. Schechter, I. Bacik, J. Gibbs, J. R. Bennink, J. W. Yewdell, J. E. Coligan, H. Firat, F. Lemonnier, and R. Ehrlich. 2001. Human cytomegalovirus protein US2 interferes with the expression of human HFE, a nonclassical class I major histocompatibility complex molecule that regulates iron homeostasis. J. Virol. 75:10557-10562.
6. Britt, W. J., and C. A. Alford. 1996. Cytomegalovirus, p. 2493-2523. In B. N. Fields, D. M. Knipe, P. M. Howley, R. M. Chanock, J. L. Melnick, T. P. Monath, B. Roizman, and S. E. Strauss (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa.
7. Calafat, J., M. Nijenhuis, H. Janssen, A. Tulp, S. Dusseljee, R. Wubbolts, and J. Neefjes. 1994. Major histocompatibility complex class II molecules induce the formation of endocytic MIIC-like structures. J. Cell Biol. 126:967-977.
8. a. Chevalier, M. S., G. M. Daniels, and D. C. Johnson. 2002. Binding of human cytomegalovirus US2 to major histocompatibility complex class I and II proteins is not sufficient for their degradation. J. Virol. 76:8265-8275.
9. Clark, E. A., and R. Yakoshi. 1984. Leucocyte typing. Springer-Verlag, Berlin, Germany.
10. Coscoy, L., and D. Ganem. 2000. Kaposis sarcoma-associated herpesvirus encodes two proteins that block cell surface display of MHC class I chains by enhancing their endocytosis. Proc. Natl. Acad. Sci. USA 97:8051-8056.
11. Cosman, D., J. Mullberg, C. L. Sutherland, W. Chin, R. Armitage, W. Fanslow, M. Kubin, and N. J. Chalupny. 2001. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14:123-133.
12. Cresswell, P. 1996. Invarian chain structure and MHC class II function. Cell 84:505-507.
13. Davidson, H. W., P. A. Reid, A. Lanzavecehia, and C. Watts. 1991. Processed antigen binds to newly synthesized MHC class II molecules in antigen-specific B lymphocytes. Cell 67:105-116.
14. Denzin, L. K., N. F. Robbins, C. Carboy-Newcomb, and P. Cresswell. 1994. Assembly and intracellular transport of HLA-DM and correction of the class Il antigen-processing defect in T2 cells. Immunity 1:595-606.
15. Dillon, D. C., M. R. Alderson, C. H. Day, D. M. Lewinsohn, R. Coler, T. Bement, A. Campos-Neto, Y. A. Skeiky, I. M. Orme, A. Roberts, S. Steen, W. Dalemans, R. Badaro, and S. G. Reed. 1999. Molecular characterization and human T-cell responses to a member of a novel Mycobacterium tuberculosis mtb39 gene family. Infect. Immun. 67:2941-2950.
16. Farrell, H., M. Degli-Esposti, E. Densley, E. Cretney, M. Smyth, and N. Davis-Poynter. 2000. Cytomegalovirus MHC class I homologues and natural killer cells: an overview. Microbes Infect. 2:521-532.
17. Fish, K. N., C. Soderberg-Naucler, and J. A. Nelson. 1998. Steady-state plasma membrane expression of human cytomegalovirus gB is determined by the phosphorylation of state of Sergo. J. Virol. 72:6657-6664.
18. Germain, R. N., and L. R. Hendrix. 1991. MHC class II structure, occupancy and surface expression determined by post-endoplasmic reticulum antigen binding. Nature 353:134-139.
19. Gilbert, M. J., S. R. Riddell, B. Plachter, and P. D. Greenberg. 1996. Cytomegalovirus selectively blocks antigen processing and presentation of its immediate-early gene product. Nature 383:720-722.
20. Gruhler, A., P. A. Peterson, and K. Fruh. 2000. Human cytomegalovirus immediate early glycoprotein US3 retains MHC class I molecules by transient association. Traffic 1:318-325.
21. Gruhler, A., and K. Fruh. 2000. Control of MHC class I traffic from the endoplasmic reticulum by cellular chaperones and viral anti-chaperones. Traffic 1:306-311.
22. Guerra, C. B., R. Busch, R. C. Doebele, W. Liu, T. Sawada, W. W. Kwok, M. D. Chang, and E. D. Mellins. 1998. Novel glycosylation of HLA-DRα disrupts antigen presentation without altering endosomal localization. J. Immunol. 160:4289-4297.
23. Guy, K., V. Van Heyningen, B. B. Cohen, D. L. Deane, and C. M. Steel. 1982. Differential expression and serologically distinct subpopulations of human Ia antigens detected with monoclonal antibodies to Ia α and β chains. Eur. J. Immunol. 12:942-948.
24. Hammond, C., L. K. Denzin, M. Pan, J. M. Griffith, H. J. Geuze, and P. Cresswell. 1998. The tetraspan protein CD82 is a resident of MHC class II compartments where it associates with HLA-DR, -DM, and -DO molecules. J. Immunol. 161:3282-3291.
25. Harlow, E., and D. Lane. 1999. Using antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
26. Hengel, H., T. Flohr, G. J. Hammerling, U. H. Koszinowski, and F. Momburg. 1996. Human cytomegalovirus inhibits peptide translocation into the endoplasmic reticulum for MHC class I assembly. J. Gen. Virol. 77:2287-2296.
27. Hewitt, E. W., S. S. Gupta, and P. J. Lehner. 2001. The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J. 20:387-396.
28. Huber, M. T., R. Tomazin, T. Wisner, J. Boname, and D. C. Johnson. 2002. Human cytomegalovirus US7, US8, US9, and US10 are cytoplasmic glycoproteins, not found at cell surfaces, and US9 does not mediate cell-to-cell spread. J. Virol. 76:5748-5758.
29. Johnson, D. C., and N. R. Hegde. 2002. Inhibition of the MHC class II antigen presentation pathway by human cytomegalovirus. Curr. Top. Microbiol. Immunol. 269:101-115.
30. Johnson, D. C., and M. T. Huber. 2002. Directed egress of animal viruses promotes cell-to-cell spread. J. Virol. 76:1-8.
31. Johnson, D. C., and G. McFadden. 2002. Viral immune evasion p357-377. In S. H. E. Kaufmann, A. Sher, and R. Ahmed (ed.), Immunology of infectious diseases. American Society for Microbiology, Washington, D.C.
32. Jones, T. R., V. P. Muzithras, and Y. Gluzman. 1991. Replacement mutagenesis of the human cytomegalovirus genome: US10 and US11 gene products are nonessential. J. Virol. 65:5860-5872.
33. Jones, T. R., E. J. Wiertz, L. Sun, K. N. Fish, J. A. Nelson, and H. L. Ploegh. 1996. Human cytomegalovirus US3 impairs transport and maturation of major histocompatibility complex class I heavy chains. Proc. Natl. Acad. Sci. USA 93:11327-11333.
34. Jones, T. R., L. K. Hanson, L. Sun, J. S. Slater, R. M. Stenberg, and A. E. Campbell. 1995. Multiple independent loci within the human cytomegalovirus unique short region down-regulate expression of major histocompatibility complex class I heavy chains. J. Virol. 69:4830-4841.
35. Kyristis, C., S. Gorbulev, S. Hutschenreiter, K. Pawlitschko, R. Abele, and R. Tampe. 2001. Molecular mechanism and structural aspects of transporter associated with antigen processing inhibition by the cytomegalovirus US6. J. Biol. Chem. 276:48031-48039.
36. Lamb, C. A., J. W. Yewdell, J. R. Bennink, and P. Cresswell. 1991. Invariant chain targets HLA class II molecules to acidic endosomes containing internalized influenza virus. Proc. Natl. Acad. Sci. USA 88:5998-6002.
37. Lampson, L. A., and R. Levy. 1980. Two populations of Ia-like molecules on a human B cell line. J. Immunol. 125:293-299.
38. Lehner, P., J. T. Karttunen, G. W. Wilkinson, and P. Cresswell. 1997. The human cytomegalovirus US6 glycoprotein inhibits transporter associated with antigen processing-dependent peptide translocation. Proc. Natl. Acad. Sci. USA 94:6904-6909.
39. + T-cell response is mediated by repression of gamma interferon-induced class II transactivator expression. J. Virol. 73:6582-6589.
40. Lotteau, V., L. Teyton, A. Peleraux, T. Nilsson, L. Karlsson, S. L. Schmid, V. Quaranta, and P. A. Peterson. 1990. Intracellular transport of class II MHC molecules directed by invariant chain. Nature 348:600-605.
41. Miller, D. M., B. M. Rahill, J. M. Boss, M. D. Lairmore, J. E. Durbin, W. J. Waldman, and D. D. Sedmak. 1998. Human cytomegalovirus inhibits major histocompatibility complex class II expression by disruption of the jak/stat pathway. J. Exp. Med. 187:675-683.
42. Ng, P., and F. L. Graham. 2001. Construction of first-generation adenoviral vectors, p. 389-413. In J. R. Morgan (ed.), Gene therapy protocols. Humana Press Inc., Totowa, N.J.
43. Pieters, J. 2000. MHC class lI-restricted antigen processing and presentation. Adv. Immunol. 75:159-208.
44. Pulliam, L. 1991. Cytomegalovirus preferentially infects a monocyte-derived macrophage/microglial cell in human brain cultures: neuropathology differs between strains. J. Neuropathol. Exp. Neurol. 50:432-440.
45. Raftery, M. J., M. Schwab, S. M. Eibert, Y. Samstag, H. Walczak, and G. Schonrich. 2001. Targeting the function of mature dendritic cells by human cytomegalovirus: a multilayered viral defense strategy. Immunity 15:997-1009.
46. Rehm, A., A. Engelsberg, D. Tortorella, I. J. Korner, I. Lehmann, H. L. Ploegh, and U. E. Hopken. 2002. Human cytomegalovirus gene products US2 and USII differ in their ability to attack major histocompatibility class I heavy chains in dendritic cells. J. Virol. 76:5043-5050.
47. Riegler, S., H. Hebart, H. Einsele, P. Brossart, G. Jahn, and C. Sinzger. 2000. Monocyte-derived dendritic cells are permissive to the complete replicative cycle of human cytomegalovirus. J. Gen. Virol. 81:393-399.
48. Reyburn, H. T., O. Mandelboim, M. Vales-Gomez, D. M. Davis, L. Pazmany, and J. L. Strominger. 1997. The class I MHC homologue of human cytomegalovirus inhibits attack by natural killer cells. Nature 386:514-517.
49. Roche, P. A., M. S. Marks, and P. Cresswell. 1991. Formation of a ninesubunit complex by HLA class II glycoproteins and the invariant chain. Nature 354:392-394.
50. Sanchez, V., K. D. Greis, E. Sztul, and W. J. Britt. 2000. Accumulation of virion tegument and envelope proteins in a stable cytoplasmic compartment during human cytomegalovirus replication: characterization of a potential site of virus assembly. J. Virol. 74:975-986.
51. Sanderson, F., C. Thomas, J. Neefjes, and J. Trowsdale. 1996. Association between HLA-DM and HLA-DR in vivo. Immunity 4:87-96.
52. Schaiff, W. T., K. A. Hruska, Jr., D. W. McCourt, M. Green, and B. D. Schwartz. 1992. HLA-DR associates with specific stress proteins and is retained in the endoplasmic reticulum in invariant chain negative cells. J. Exp. Med. 176:657-666.
53. Sekaly, R. P., C. Tonnelle, M. Strubin, B. Mach, and E. O. Long. 1986. Cell surface expression of class II histocompatibility antigens occurs in the absence of the invariant chain. J. Exp. Med. 164:1490-1504.
54. Soderberg-Naucler, C., K. N. Fish, and J. A. Nelson. 1997. Reactivation of latent human cytomegalovirus by allogeneic stimulation of blood cells from healthy donors. Cell 91:119-126.
55. Soderberg-Naucler, C., K. Fish, and J. A. Nelson. 1999. Cytomegalovirus, p. 209-242. In R. Ahmed and I. Chen (ed.), Persistent viral infections. John Wiley & Sons, New York, N.Y.
56. Stern, L. J., and D. C. Wiley. 1992. The human class II MHC protein HLA-DR1 assembles as empty αβ heterodimers in the absence of antigenic peptide. Cell 68:465-477.
57. Streblow, D. N., C. Soderberg-Naucler, J. Vieira, P. Smith, E. Wakabayashi, F. Ruchti, K. Mattison, Y. Altschuler, and J. A. Nelson. 1999. The human cytomegalovirus chemokine receptor US28 mediates vascular smooth muscle cell migration. Cell 99:511-520.
58. Sun, Y., E. Kim, M. Jin, H. C. Sung, H. Han, D. E. Geraghty, and K. Ahn. 2000. Human cytomegalovirus gene products US3 and US6 down-regulate trophoblast class I MHC molecules. J. Immunol. 164:805-811.
59. + T cells. Nat. Med. 5:1039-1043.
60. Tooze, J., M. Hollinshead, B. Reis, K. Radsak, and H. Kern. 1993. Progeny vaccinia and human cytomegalovirus particles utilize early endosomal cisternae for their envelopes. Eur. J. Cell Biol. 60:163-178.
61. Tortorella, D., B. E. Gewurz, M. H. Furman, D. J. Schust, and H. L. Ploegh. 2000. Viral subversion of the immune system. Annu. Rev. Immunol. 18:861-926.
62. van den Pol, A. N., E. Mocarski, N. Saederup, J. Vieira, and T. J. Meier. 1999. Cytomegalovirus cell tropism, replication, and gene transfer in brain. J. Neurosci. 19:10948-10965.
63. Wiertz, E. J., T. R. Jones, L. Sun, M. Bogyo, H. J. Geuze, and H. L. Ploegh. 1996. The human cytomegalovirus USII gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84:769-779.
64. Wiertz, E. J., D. Tortorella, M. Bogyo, J. Yu, W. Mothes, T. R. Jones, T. A. Rapoport, and H. L. Ploegh. 1996. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384:432-438.
65. Wiley, C. A., R. D. Schrier, F. J. Denaro, J. A. Nelson, P. W. Lampert, and M. B. Oldstone. 1986. Localization of cytomegalovirus proteins and genome during fulminant central nervous system infection in an AIDS patient. J. Neuropathol. Exp. Neurol. 45:127-139.