The cytoplasmic domain of rhesus cytomegalovirus Rh178 interrupts translation of major histocompatibility class I leader peptide-containing proteins prior to translocation

Journal of Virology

Volumn 85, Issue 17, 2011, Pages 8766-8776

  Richards, Rebecca ^a,b   Scholz, Isabel ^b   Powers, Colin ^a   Skach, William R ^b   Früh, Klaus ^a,b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEIN RH178; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOMEGALOVIRUS; CYTOSOL; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; HEAVY CHAIN; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN TARGETING; RHESUS MONKEY;

ANIMALS; CELL LINE; CYTOMEGALOVIRUS; ENDOPLASMIC RETICULUM; HISTOCOMPATIBILITY ANTIGENS CLASS I; HOST-PATHOGEN INTERACTIONS; HUMANS; MACACA MULATTA; PROTEIN BIOSYNTHESIS; PROTEIN SORTING SIGNALS; VIRAL PROTEINS;

CERCOPITHECINE HERPESVIRUS 8; CYTOMEGALOVIRUS; HUMAN HERPESVIRUS 5;

EID: 80052279264     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05021-11     Document Type: Article

References (63)

1. Ahn, K., et al. 1997. The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6:613-621.
2. Andrews, D. W., J. C. Young, L. F. Mirels, and G. J. Czarnota. 1992. The role of the N region in signal sequence and signal-anchor function. J. Biol. Chem. 267:7761-7769.
3. Basta, S., and J. R. Bennink. 2003. A survival game of hide and seek: cytomegaloviruses and MHC class I antigen presentation pathways. Viral Immunol. 16:231-242.
4. Besemer, J., et al. 2005. Selective inhibition of cotranslational translocation of vascular cell adhesion molecule 1. Nature 436:290-293.
5. Castillo, J. P., and T. F. Kowalik. 2004. HCMV infection: modulatingthe cell cycle and cell death. Int. Rev. Immunol. 23:113-139.
6. Chang, W. L., V. Kirchoff, G. S. Pari, and P. A. Barry. 2002. Replication of rhesus cytomegalovirus in life-expanded rhesus fibroblasts expressing human telomerase. J. Virol. Methods 104:135-146.
7. Cosman, D., et al. 1997. A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 7:273-282.
8. Cosman, D., et al. 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.
9. Cresswell, P., et al. 1974. Immunological identity of the small subunit of HL-A antigens and beta2-microglobulin and its turnover on the cell membrane. Proc. Natl. Acad. Sci. U. S. A. 71:2123-2127.
10. Cross, B. C., et al. 2009. Eeyarestatin I inhibits Sec61-mediated protein translocation at the endoplasmic reticulum. J. Cell Sci. 122:4393-4400.
11. Daza-Vamenta, R., G. Glusman, L. Rowen, B. Guthrie, and D. E. Geraghty. 2004. Genetic divergence of the rhesus macaque major histocompatibility complex. Genome Res. 14:1501-1515.
12. Deacon, C. F., A. H. Johnsen, and J. J. Holst. 1995. Degradationofglucagon-like peptide-1 by human plasma in vitro yields an N-terminally truncated peptide that is a major endogenous metabolite in vivo. J. Clin. Endocrinol. Metab. 80:952-957.
13. DeFilippis, V. R. 2007. Induction and evasion of the type I interferon response by cytomegaloviruses. Adv. Exp. Med. Biol. 598:309-324.
14. Fiebiger, E., et al. 2004. Dissection of the dislocation pathway for type I membrane proteins with a new small molecule inhibitor, eeyarestatin. Mol. Biol. Cell 15:1635-1646.
15. Garrison, J. L., E. J. Kunkel, R. S. Hegde, and J. Taunton. 2005. Asubstrate-specific inhibitor of protein translocation into the endoplasmic reticulum. Nature 436:285-289.
16. Gewurz, B. E., et al. 2001. 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. 98:6794-6799.
17. Gilmore, R., G. Blobel, and P. Walter. 1982. Proteintranslocationacross the endoplasmic reticulum. I. Detection in the microsomal membrane of a receptor for the signal recognition particle. J. Cell Biol. 95:463-469.
18. Gossen, M., and H. Bujard. 1992. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. U. S. A. 89:5547-5551.
19. Halenius, A., et al. 2006. Physical and functional interactions of the cyto-megalovirus US6 glycoprotein with the transporter associated with antigen processing. J. Biol. Chem. 281:5383-5390.
20. Hansen, S. G., et al. 2010. Evasion of CD8+ T cells is critical for superinfection by cytomegalovirus. Science 328:102-106.
21. Hengel, H., et al. 1997. A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity 6:623-632.
22. Hewitt, E. W., S. S. Gupta, and P. J. Lehner. 2001. The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J. 20:387396.
23. Jackson, M. R., E. S. Song, Y. Yang, and P. A. Peterson. 1992. Empty and peptide-containing conformers of class I major histocompatibility complex molecules expressed in Drosophila melanogaster cells. Proc. Natl. Acad. Sci. U. S. A. 89:12117-12121.
24. Janda, C. Y., et al. 2010. Recognition of a signal peptide by the signal recognition particle. Nature 465:507-510.
25. Jones, T. R., and V. P. Muzithras. 1991. Fine mapping of transcripts expressed from the US6 gene family of human cytomegalovirus strain AD169. J. Virol. 65:2024-2036.
26. Kida, Y., M. Sakaguchi, M. Fukuda, K. Mikoshiba, and K. Mihara. 2000. Membrane topogenesis of a type I signal-anchor protein, mouse synaptotagmin II, on the endoplasmic reticulum. J. Cell Biol. 150:719-730.
27. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
28. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
29. Lakkaraju, A. K., C. Mary, A. Scherrer, A. E. Johnson, and K. Strub. 2008. SRP keeps polypeptides translocation-competent by slowing translation to match limiting ER-targeting sites. Cell 133:440-451.
30. Lee, S., et al. 2000. Structural and functional dissection of human cytomegalovirus US3 in binding major histocompatibility complex class I molecules. J. Virol. 74:11262-11269.
31. Lee, S. O., et al. 2010. Protein disulphide isomerase is required for signal peptide peptidase-mediated protein degradation. EMBO J. 29:363-375.
32. Lee, S. O., et al. 2005. Functional dissection of HCMV US11 in mediating the degradation of MHC class I molecules. Biochem. Biophys. Res. Commun. 330:1262-1267.
33. Lilley, B. N., and H. L. Ploegh. 2004. A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429:834-840.
34. Loenen, W. A., C. A. Bruggeman, and E. J. Wiertz. 2001. Immune evasion by human cytomegalovirus: lessons in immunology and cell biology. Semin. Immunol. 13:41-49.
35. Loureiro, J., et al. 2006. Signal peptide peptidase is required for dislocation from the endoplasmic reticulum. Nature 441:894-897.
36. Meinnel, T., A. Serero, and C. Giglione. 2006. Impact of the N-terminal amino acid on targeted protein degradation. Biol. Chem. 387:839-851.
37. Misaghi, S., et al. 2004. Structural and functional analysis of human cytomegalovirus US3 protein. J. Virol. 78:413-423.
38. Mueller, B., B. N. Lilley, and H. L. Ploegh. 2006. SEL1L, the homologue of yeast Hrd3p, is involved in protein dislocation from the mammalian ER. J. Cell Biol. 175:261-270.
39. Nicchitta, C. V., E. C. Murphy III, R. Haynes, and G. S. Shelness. 1995. Stage- and ribosome-specific alterations in nascent chain-Sec61p interactions accompany translocation across the ER membrane. J. Cell Biol. 129:957970.
40. Okun, M. M., E. M. Eskridge, and D. Shields. 1990. Truncations of a secretory protein define minimum lengths required for binding to signal recognition particle and translocation across the endoplasmic reticulum membrane. J. Biol. Chem. 265:7478-7484.
41. Pande, N. T., C. Powers, K. Ahn, and K. Fruh. 2005. Rhesus cytomegalovirus contains functional homologues of US2, US3, US6, and US11. J. Virol. 79:5786-5798.
42. Park, B., et al. 2004. Human cytomegalovirus inhibits tapasindependent peptide loading and optimization of the MHC class I peptide cargo for immune evasion. Immunity 20:71-85.
43. Park, B., et al. 2006. Redox regulation facilitates optimal peptide selection by MHC class I during antigen processing. Cell 127:369-382.
44. Powers, C., V. DeFilippis, D. Malouli, and K. Fruh. 2008. Cytomegalovirus immune evasion. Curr. Top. Microbiol. Immunol. 325:333-359.
45. Powers, C. J., and K. Fruh. 2008. Signal peptide-dependent inhibition of MHC class I heavy chain translation by rhesus cytomegalovirus. PLoS Pat-hog. 4:e1000150.
46. Rapoport, T. A. 2007. Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450:663-669.
47. Ren, Y., et al. 1995. Topology of prostaglandin H synthase-1 in the endoplasmic reticulum membrane. Arch. Biochem. Biophys. 323:205-214.
48. Saric, T., et al. 2001. Major histocompatibility complex class I-presented antigenic peptides are degraded in cytosolic extracts primarily by thimet oligopeptidase. J. Biol. Chem. 276:36474-36481.
49. Skach, W. R. 2009. Cellular mechanisms of membrane protein folding. Nat. Struct. Mol. Biol. 16:606-612.
50. Skach, W. R. 1998. Topology of P-glycoproteins. Methods Enzymol. 292:265-278.
51. Soetandyo, N., and Y. Ye. 2010. The p97 ATPase dislocates MHC class I heavy chain in US2-expressing cells via a Ufd1-Npl4-independent mechanism. J. Biol. Chem. 285:32352-32359.
52. Tomasec, P., et al. 2000. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287:1031.
53. Tomkinson, B. 1999. Tripeptidyl peptidases: enzymes that count. Trends Biochem. Sci. 24:355-359.
54. 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. 18:861926.
55. Urvater, J. A., et al. 2000. Mamu-I: a novel primate MHC class I B-related locus with unusually low variability. J. Immunol. 164:1386-1398.
56. Wang, E. C., et al. 2002. UL40-mediated NK evasion during productive infection with human cytomegalovirus. Proc. Natl. Acad. Sci. U. S. A. 99:7570-7575.
57. Wang, Q., L. Li, and Y. Ye. 2008. Inhibition of p97-dependent protein degradation by Eeyarestatin I. J. Biol. Chem. 283:7445-7454.
58. Wang, Q., et al. 2010. The ERAD inhibitor Eeyarestatin I is a bifunctional compound with a membrane-binding domain and a p97/VCP inhibitory group. PLoS One 5:e15479.
59. Wiertz, E. J., et al. 1996. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84:769-779.
60. Wiertz, E. J., et al. 1996. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384:432-438.
61. Wilkinson, G. W., et al. 2008. Modulation of natural killer cells by human cytomegalovirus. J. Clin. Virol. 41:206-212.
62. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
63. Yost, C. S., J. Hedgpeth, and V. R. Lingappa. 1983. A stop transfer sequence confers predictable transmembrane orientation to a previously secreted protein in cell-free systems. Cell 34:759-766.