Downregulation of class I major histocompatibility complex surface expression by varicella-zoster virus involves open reading frame 66 protein kinase-dependent and -independent mechanisms

Journal of Virology

Volumn 81, Issue 17, 2007, Pages 9034-9049

  Eisfeld, Amie J ^a   Yee, Michael B ^a   Erazo, Angela ^a   Abendroth, Allison ^b,c   Kinchington, Paul R ^a,d  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b WESTMEAD HOSPITAL   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

^d University of Pittsburgh School of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ENHANCED GREEN FLUORESCENT PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN KINASE;

ADENOVIRUS; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; CELL SURFACE; CONTROLLED STUDY; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME MECHANISM; GENE EXPRESSION REGULATION; GOLGI COMPLEX; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; VARICELLA ZOSTER VIRUS; VIRUS CELL INTERACTION; VIRUS RECOMBINANT; VIRUS REPLICATION;

CELL LINE; DOWN-REGULATION; GOLGI APPARATUS; HERPESVIRUS 3, HUMAN; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; PROTEIN KINASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; VIRAL PROTEINS;

ADENOVIRIDAE; BOVINE HERPESVIRUS 1; HUMAN HERPESVIRUS 3;

EID: 34548157388     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00711-07     Document Type: Article

References (63)

1. Abendroth, A., I. Lin, B. Slobedman, H. Ploegh, and A. M. Arvin. 2001. Varicella-zoster virus retains major histocompatibility complex class I proteins in the Golgi compartment of infected cells. J. Virol. 75:4878-4888.
2. Abendroth, A., G. Morrow, A. L. Cunningham, and B. Slobedman. 2001. Varicella-zoster virus infection of human dendritic cells and transmission to T cells: implications for virus dissemination in the host. J. Virol. 75:6183-6192.
3. Ahn, K., T. H. Meyer, S. Uebel, P. Sempe, H. Djaballah, Y. Yang, P. A. Peterson, K. Fruh, and R. Tampe. 1996. Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47. EMBO J. 15:3247-3255.
4. Arbeit, R. D., J. A. Zaia, M. A. Valerio, and M. J. Levin. 1982. Infection of human peripheral blood mononuclear cells by varicella-zoster virus. Intervirology 18:56-65.
5. Arvin, A. M., M. Sharp, M. Moir, P. R. Kinchington, M. Sadeghi-Zadeh, W. T. Ruyechan, and J. Hay. 2002. Memory cytotoxic T cell responses to viral tegument and regulatory proteins encoded by open reading frames 4, 10, 29, and 62 of varicella-zoster virus. Viral Immunol. 15:507-516.
6. Benetti, L., and B. Roizman. 2004. Herpes simplex virus protein kinase US3 activates and functionally overlaps protein kinase A to block apoptosis. Proc. Natl. Acad. Sci. USA 101:9411-9416.
7. Bennett, E. M., J. R. Bennink, J. W. Yewdell, and F. M. Brodsky. 1999. Cutting edge: adenovirus E19 has two mechanisms for affecting class I MHC expression. J. Immunol. 162:5049-5052.
8. Capps, G. G., and M. C. Zuniga. 2000. Phosphorylation of class I MHC molecules in the absence of phorbol esters is an intracellular event and may be characteristic of trafficking molecules. Mol. Immunol. 37:59-71.
9. Cohen, J. I. 1998. Infection of cells with varicella-zoster virus down-regulates surface expression of class I major histocompatibility complex antigens. J. Infect. Dis. 177:1390-1393.
10. Cohrs, R. J., and D. H. Gilden. 2007. Prevalence and abundance of latently transcribed varicella-zoster virus genes in human ganglia. J. Virol. 81:2950-2956.
11. Cohrs, R. J., D. H. Gilden, P. R. Kinchington, E. Grinfeld, and P. G. Kennedy. 2003. Varicella-zoster virus gene 66 transcription and translation in latently infected human ganglia. J. Virol. 77:6660-6665.
12. Decman, V., P. R. Kinchington, S. A. Harvey, and R. L. Hendricks. 2005. Gamma interferon can block herpes simplex virus type 1 reactivation from latency, even in the presence of late gene expression. J. Virol. 79:10339-10347.
13. de Jong, M. D., J. F. Weel, T. Schuurman, P. M. Wertheim-van Dillen, and R. Boom. 2000. Quantitation of varicella-zoster virus DNA in whole blood, plasma, and serum by PCR and electrochemiluminescence. J. Clin. Microbiol. 38:2568-2573.
14. Eichholtz, T., P. Vossebeld, M. van Overveld, and H. Ploegh. 1992. Activation of protein kinase C accelerates internalization of transferrin receptor but not of major histocompatibility complex class I, independent of their phosphorylation status. J. Biol. Chem. 267:22490-22495.
15. Eisfeld, A. J., S. E. Turse, S. A. Jackson, E. C. Lerner, and P. R. Kinchington. 2006. Phosphorylation of the varicella-zoster virus (VZV) major transcriptional regulatory protein IE62 by the VZV open reading frame 66 protein kinase. J. Virol. 80:1710-1723.
16. Fruh, K., K. Ahn, H. Djaballah, P. Sempe, P. M. van Endert, R. Tampe, P. A. Peterson, and Y. Yang. 1995. A viral inhibitor of peptide transporters for antigen presentation. Nature 375:415-418.
17. Furman, M. H., N. Dey, D. Tortorella, and H. L. Ploegh. 2002. The human cytomegalovirus US10 gene product delays trafficking of major histocompatibility complex class I molecules. J. Virol. 76:11753-11756.
18. Ge, R., X. Liu, and R. P. Ricciardi. 1994. E1A oncogene of adenovirus-12 mediates trans-repression of MHC class I transcription in Ad5/Ad12 somatic hybrid transformed cells. Virology 203:389-392.
19. Gershon, A. A., D. L. Sherman, Z. Zhu, C. A. Gabel, R. T. Ambron, and M. D. Gershon. 1994. Intracellular transport of newly synthesized varicella-zoster virus: final envelopment in the trans-Golgi network. J. Virol. 68:6372-6390.
20. Gilden, D. H., A. R. Hayward, J. Krupp, M. Hunter-Laszlo, J. C. Huff, and A. Vafai. 1987. Varicella-zoster virus infection of human mononuclear cells. Virus Res. 7:117-129.
21. Gopinath, R. S., A. P. Ambagala, S. Hinkley, and S. Srikumaran. 2002. Effects of virion host shut-off activity of bovine herpesvirus 1 on MHC class I expression. Viral Immunol. 15:595-608.
22. Guild, B. C., and J. L. Strominger. 1984. HLA-A2 antigen phosphorylation in vitro by cyclic AMP-dependent protein kinase. Sites of phosphorylation and segmentation in class i major histocompatibility complex gene structure. J. Biol. Chem. 259:13504-13510.
23. Harson, R., and C. Grose. 1995. Egress of varicella-zoster virus from the melanoma cell: a tropism for the melanocyte. J. Virol. 69:4994-5010.
24. Hengel, H., J. O. Koopmann, T. Flohr, W. Muranyi, E. Goulmy, G. J. Hammerling, U. H. Koszinowski, and F. Momburg. 1997. A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity 6:623-632.
25. Hill, A., P. Jugovic, I. York, G. Russ, J. Bennink, J. Yewdell, H. Ploegh, and D. Johnson. 1995. Herpes simplex virus turns off the TAP to evade host immunity. Nature 375:411-415.
26. Hill, A. B., B. C. Barnett, A. J. McMichael, and D. J. McGeoch. 1994. HLA class I molecules are not transported to the cell surface in cells infected with herpes simplex virus types 1 and 2. J. Immunol. 152:2736-2741.
27. Hu, H., and J. I. Cohen. 2005. Varicella-zoster virus open reading frame 47 (ORF47) protein is critical for virus replication in dendritic cells and for spread to other cells. Virology 337:304-311.
28. Hufner, K., T. Derfuss, S. Herberger, K. Sunami, S. Russell, I. Sinicina, V. Arbusow, M. Strupp, T. Brandt, and D. Theil. 2006. Latency of alpha-herpes viruses is accompanied by a chronic inflammation in human trigeminal ganglia but not in dorsal root ganglia. J. Neuropathol. Exp. Neurol. 65:1022-1030.
29. Ishido, S., C. Wang, B. S. Lee, G. B. Cohen, and J. U. Jung. 2000. Down-regulation of major histocompatibility complex class I molecules by Kaposi's sarcoma-associated herpesvirus K3 and K5 proteins. J. Virol. 74:5300-5309.
30. Ito, Y., H. Kimura, S. Hara, S. Kido, T. Ozaki, Y. Nishiyama, and T. Morishima. 2001. Investigation of varicella-zoster virus DNA in lymphocyte subpopulations by quantitative PCR assay. Microbiol. Immunol. 45:267-269.
31. Jons, A., J. M. Dijkstra, and T. C. Mettenleiter. 1998. Glycoproteins M and N of pseudorabies virus form a disulfide-linked complex. J. Virol. 72:550-557.
32. Kasper, M. R., J. F. Roeth, M. Williams, T. M. Filzen, R. I. Fleis, and K. L. Collins. 2005. HIV-1 Nef disrupts antigen presentation early in the secretory pathway. J. Biol. Chem. 280:12840-12848.
33. Kinchington, P. R., K. Fite, A. Seman, and S. E. Turse. 2001. Virion association of IE62, the varicella-zoster virus (VZV) major transcriptional regulatory protein, requires expression of the VZV open reading frame 66 protein kinase. J. Virol. 75:9106-9113.
34. Kinchington, P. R., K. Fite, and S. E. Turse. 2000. Nuclear accumulation of IE62, the varicella-zoster virus (VZV) major transcriptional regulatory protein, is inhibited by phosphorylation mediated by the VZV open reading frame 66 protein kinase. J. Virol. 74:2265-2277.
35. Koenig, A., and M. H. Wolff. 2003. Infectibility of separated peripheral blood mononuclear cell subpopulations by varicella-zoster virus (VZV). J. Med. Virol. 70(Suppl. 1):S59-S63.
36. Koppers-Lalic, D., E. A. Reits, M. E. Ressing, A. D. Lipinska, R. Abele, J. Koch, M. Marcondes Rezende, P. Admiraal, D. van Leeuwen, K. Bienkowska-Szewczyk, T. C. Mettenleiter, F. A. Rijsewijk, R. Tampe, J. Neefjes, and E. J. Wiertz. 2005. Varicelloviruses avoid T cell recognition by UL49.5-mediated inactivation of the transporter associated with antigen processing. Proc. Natl. Acad. Sci. USA 102:5144-5149.
37. Koppers-Lalic, D., F. A. Rijsewijk, S. B. Verschuren, J. A. van Gaans-Van den Brink, A. Neisig, M. E. Ressing, J. Neefjes, and E. J. Wiertz. 2001. The UL41-encoded virion host shutoff (vhs) protein and vhs-independent mechanisms are responsible for down-regulation of MHC class I molecules by bovine herpesvirus 1. J. Gen. Virol. 82:2071-2081.
38. Ku, C. C., J. Besser, A. Abendroth, C. Grose, and A. M. Arvin. 2005. Varicella-zoster virus pathogenesis and immunobiology: new concepts emerging from investigations with the SCIDhu mouse model. J. Virol. 79:2651-2658.
39. + T lymphocytes that express activation, memory, and skin homing markers. J. Virol. 76:11425-11433.
40. Ku, C. C., L. Zerboni, H. Ito, B. S. Graham, M. Wallace, and A. M. Arvin. 2004. Varicella-zoster virus transfer to skin by T Cells and modulation of viral replication by epidermal cell interferon-alpha. J. Exp. Med. 200:917-925.
41. Leader, D. P., A. D. Deana, F. Marchiori, F. C. Purves, and L. A. Pinna. 1991. Further definition of the substrate specificity of the alpha-herpesvirus protein kinase and comparison with protein kinases A and C. Biochim. Biophys. Acta 1091:426-431.
42. Lehner, P. J., 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.
43. Li, Y., L. Salter-Cid, A. Vitiello, T. Preckel, J. D. Lee, A. Angulo, Z. Cai, P. A. Peterson, and Y. Yang. 2000. Regulation of transporter associated with antigen processing by phosphorylation. J. Biol. Chem. 275:24130-24135.
44. Lippe, R., E. Luke, Y. T. Kuah, C. Lomas, and W. A. Jefferies. 1991. Adenovirus infection inhibits the phosphorylation of major histocompatibility complex class I proteins. J. Exp. Med. 174:1159-1166.
45. Mainka, C., B. Fuss, H. Geiger, H. Hofelmayr, and M. H. Wolff. 1998. Characterization of viremia at different stages of varicella-zoster virus infection. J. Med. Virol. 56:91-98.
46. Malmgaard, L. 2004. Induction and regulation of IFNs during viral infections. J. Interferon Cytokine Res. 24:439-454.
47. Mitchell, B. M., D. C. Bloom, R. J. Cohrs, D. H. Gilden, and P. G. Kennedy. 2003. Herpes simplex virus-1 and varicella-zoster virus latency in ganglia. J. Neurovirol. 9:194-204.
48. Moffat, J., C. Mo, J. J. Cheng, M. Sommer, L. Zerboni, S. Stamatis, and A. M. Arvin. 2004. Functions of the C-terminal domain of varicella-zoster virus glycoprotein E in viral replication in vitro and skin and T-cell tropism in vivo. J. Virol. 78:12406-12415.
49. Moffat, J. F., L. Zerboni, M. H. Sommer, T. C. Heineman, J. I. Cohen, H. Kaneshima, and A. M. Arvin. 1998. The ORF47 and ORF66 putative protein kinases of varicella-zoster virus determine tropism for human T cells and skin in the SCID-hu mouse. Proc. Natl. Acad. Sci. USA 95:11969-11974.
50. Morrow, G., B. Slobedman, A. L. Cunningham, and A. Abendroth. 2003. Varicella-zoster virus productively infects mature dendritic cells and alters their immune function. J. Virol. 77:4950-4959.
51. Niizuma, T., L. Zerboni, M. H. Sommer, H. Ito, S. Hinchliffe, and A. M. Arvin. 2003. Construction of varicella-zoster virus recombinants from parent Oka cosmids and demonstration that ORF65 protein is dispensable for infection of human skin and T cells in the SCID-hu mouse model. J. Virol. 77:6062-6065.
52. Park, B., Y. Kim, J. Shin, S. Lee, K. Cho, K. Fruh, S. Lee, and K. Ahn. 2004. Human cytomegalovirus inhibits tapasin-dependent peptide loading and optimization of the MHC class I peptide cargo for immune evasion. Immunity 20:71-85.
53. Pober, J. S., B. C. Guild, and J. L. Strominger. 1978. Phosphorylation in vivo and in vitro of human histocompatibility antigens (HLA-A and HLA-B) in the carboxy-terminal intracellular domain. Proc. Natl. Acad. Sci. USA 75:6002-6006.
54. Proffitt, J. L., E. Sharma, and G. E. Blair. 1994. Adenovirus 12-mediated down-regulation of the major histocompatibility complex (MHC) class I promoter: identification of a negative regulatory element responsive to Ad12 E1A. Nucleic Acids Res. 22:4779-4788.
55. Sato, H., L. D. Callanan, L. Pesnicak, T. Krogmann, and J. I. Cohen. 2002. Varicella-zoster virus (VZV) ORF17 protein induces RNA cleavage and is critical for replication of VZV at 37°C but not 33°C. J. Virol. 76:11012-11023.
56. Schaap-Nutt, A., M. Sommer, X. Che, L. Zerboni, and A. M. Arvin. 2006. Orf66 protein kinase function is required for T cell tropism of varicella-zoster virus in vivo. J. Virol. 80:11806-11816.
57. Schaap, A., J. F. Fortin, M. Sommer, L. Zerboni, S. Stamatis, C. C. Ku, G. P. Nolan, and A. M. Arvin. 2005. T-cell tropism and the role of ORF66 protein in pathogenesis of varicella-zoster virus infection. J. Virol. 79:12921-12933.
58. Soong, W., J. C. Schultz, A. C. Patera, M. H. Sommer, and J. I. Cohen. 2000. Infection of human T lymphocytes with varicella-zoster virus: an analysis with viral mutants and clinical isolates. J. Virol. 74:1864-1870.
59. Storkus, W. J., H. J. Zeh III, R. D. Salter, and M. T. Lotze. 1993. Identification of T-cell epitopes: rapid isolation of class I-presented peptides from viable cells by mild acid elution. J. Immunother. 14:94-103.
60. + CTL clones recognize HSV-2-infected fibroblasts after treatment with IFN-gamma or when virion host shutoff functions are disabled. J. Immunol. 156:3901-3910.
61. Tomazin, R., A. B. Hill, P. Jugovic, I. York, P. van Endert, H. L. Ploegh, D. W. Andrews, and D. C. Johnson. 1996. Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP. EMBO J. 15:3256-3266.
62. Verjans, G. M., R. Q. Hintzen, J. M. van Dun, A. Poot, J. C. Milikan, J. D. Laman, A. W. Langerak, P. R. Kinchington, and A. D. Osterhaus. 2007. Selective retention of herpes simplex virus-specific T cells in latently infected human trigeminal ganglia. Proc. Natl. Acad. Sci. USA 104:3496-3501.
63. Zhao, B., and R. P. Ricciardi. 2006. E1A is the component of the MHC class I enhancer complex that mediates HDAC chromatin repression in adenovirus-12 tumorigenic cells. Virology 352:338-344.