Signal peptide-dependent inhibition of MHC class I heavy chain translation by rhesus cytomegalovirus

PLoS Pathogens

Volumn 4, Issue 10, 2008, Pages

  Powers, Colin J ^a   Früh, Klaus ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PROTEASOME INHIBITOR; PROTEIN RH178; SIGNAL PEPTIDE; UNCLASSIFIED DRUG; VIRUS PROTEIN; GLYCOPROTEIN; HLA ANTIGEN CLASS 1; MESSENGER RNA;

ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS; ENDOPLASMIC RETICULUM; FIBROBLAST; GENE DELETION; HEAVY CHAIN; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RIBOSOME; RNA TRANSCRIPTION; VIRUS RECOMBINANT; ANIMAL; BIOSYNTHESIS; CELL LINE; CYTOMEGALOVIRUS INFECTION; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; MACACA; METABOLISM; MOUSE; PROTEIN TRANSPORT; VIROLOGY; VIRUS GENOME;

CERCOPITHECINE HERPESVIRUS 8; MURINAE;

ANIMALS; CELL LINE, TRANSFORMED; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; ENDOPLASMIC RETICULUM; FIBROBLASTS; GENE DELETION; GENE EXPRESSION REGULATION; GENOME, VIRAL; GLYCOPROTEINS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MACACA MULATTA; MICE; PROTEIN BIOSYNTHESIS; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RNA, MESSENGER; VIRAL PROTEINS;

EID: 55449101387     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000150     Document Type: Article

References (50)

1. Pass RF (2001) Cytomegalovirus. In: David MKnipe PMH, Diane EGriffin, Robert ALamb, Malcolm AMartin, BernardRoizman, Stephen EStraus, eds. Fields Virology. 4th ed. Philadelphia: Lippincott Williams & Wilkins. pp 2675-2705.
2. Sylwester AW, Mitchell BL, Edgar JB, Taormina C, Pelte C, et al. (2005) Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J Exp Med 202: 673-685.
3. Boppana SB, Rivera LB, Fowler KB, Mach M, Britt WJ (2001) Intrauterine transmission of cytomegalovirus to infants of women with preconceptional immunity. N Engl J Med 344: 1366-1371.
4. Yu D, Silva MC, Shenk T (2003) Functional map of human cytomegalovirus AD169 defined by global mutational analysis. Proc Natl Acad Sci U S A 100: 12396-12401.
5. Dunn W, Chou C, Li H, Hai R, Patterson D, et al. (2003) Functional profiling of a human cytomegalovirus genome. Proc Natl Acad Sci U S A 100: 14223-14228.
6. Castillo JP, Kowalik TF (2004) HCMV infection: modulating the cell cycle and cell death. Int Rev Immunol 23: 113-139.
7. Loenen WA, Bruggeman CA, Wiertz EJ (2001) Immune evasion by human cytomegalovirus: lessons in immunology and cell biology. Semin Immunol 13: 41-49.
8. Wilkinson GW, Tomasec P, Stanton RJ, Armstrong M, Prod'homme V, et al. (2007) Modulation of natural killer cells by human cytomegalovirus. J Clin Virol.
9. DeFilippis VR (2007) Induction and evasion of the type I interferon response by cytomegaloviruses. Adv Exp Med Biol 598: 309-324.
10. McGeoch DJ, Cook S, Dolan A, Jamieson FE, Telford EA (1995) Molecular phylogeny and evolutionary timescale for the family of mammalian herpesviruses. J Mol Biol 247: 443-458.
11. Davison AJ, Dolan A, Akter P, Addison C, Dargan DJ, et al. (2003) The human cytomegalovirus genome revisited: comparison with the chimpanzee cytomegalovirus genome. J Gen Virol 84: 17-28.
12. Hansen SG, Strelow LI, Franchi DC, Anders DG, Wong SW (2003) Complete sequence and genomic analysis of rhesus cytomegalovirus. J Virol 77: 6620-6636.
13. Rivailler P, Kaur A, Johnson RP, Wang F (2006) Genomic sequence of rhesus cytomegalovirus 180.92: insights into the coding potential of rhesus cytomegalovirus. J Virol 80: 4179-4182.
14. van der Wal FJ, Kikkert M, Wiertz E (2002) The HCMV gene products US2 and US11 target MHC class I molecules for degradation in the cytosol. Curr Top Microbiol Immunol 269: 37-55.
15. Gruhler A, Fruh K (2000) Control of MHC class I traffic from the endoplasmic reticulum by cellular chaperones and viral anti-chaperones. Traffic 1: 306-311.
16. Momburg F, Hengel H (2002) Corking the bottleneck: the transporter associated with antigen processing as a target for immune subversion by viruses. Curr Top Microbiol Immunol 269: 57-74.
17. Gewurz BE, Gaudet R, Tortorella D, Wang EW, Ploegh HL, 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.
18. Barel MT, Hassink GC, van Voorden S, Wiertz EJ (2006) Human cytomegalovirus-encoded US2 and US11 target unassembled MHC class I heavy chains for degradation. Mol Immunol 43: 1258-1266.
19. Wiertz EJ, Jones TR, Sun L, Bogyo M, Geuze HJ, 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.
20. Park B, Lee S, Kim E, Cho K, Riddell SR, et al. (2006) Redox regulation facilitates optimal peptide selection by MHC class I during antigen processing. Cell 127: 369-382.
21. Pande NT, Powers C, Ahn K, Fruh K (2005) Rhesus Cytomegalovirus Contains Functional Homologues of US2, US3, US6, and US11. J Virol 79: 5786-5798.
22. Jones TR, Hanson LK, Sun L, Slater JS, Stenberg RM, et al. (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.
23. Chang WL, Barry PA (2003) Cloning of the full-length rhesus cytomegalovirus genome as an infectious and self-excisable bacterial artificial chromosome for analysis of viral pathogenesis. J Virol 77: 5073-5083.
24. Andersson M, Paabo S, Nilsson T, Peterson PA (1985) Impaired intracellular transport of class I MHC antigens as a possible means for adenoviruses to evade immune surveillance. Cell 43: 215-222.
25. Stam NJ, Vroom TM, Peters PJ, Pastoors EB, Ploegh HL (1990) HLA-A- and HLA-B-specific monoclonal antibodies reactive with free heavy chains in western blots, in formalin-fixed, paraffin-embedded tissue sections and in cryoimmunoelectron microscopy. Int Immunol 2: 113-125.
26. Turner GC, Varshavsky A (2000) Detecting and measuring cotranslational protein degradation in vivo. Science 289: 2117-2120.
27. Cha TA, Tom E, Kemble GW, Duke GM, Mocarski ES, et al. (1996) Human cytomegalovirus clinical isolates carry at least 19 genes not found in laboratory strains. J Virol 70: 78-83.
28. Chang WL, Tarantal AF, Zhou SS, Borowsky AD, Barry PA (2002) A recombinant rhesus cytomegalovirus expressing enhanced green fluorescent protein retains the wild-type phenotype and pathogenicity in fetal macaques. J Virol 76: 9493-9504.
29. Lodish HF (1971) Alpha and beta globin messenger ribonucleic acid. Different amounts and rates of initiation of translation. J Biol Chem 246: 7131-7138.
30. Nottrott S, Simard MJ, Richter JD (2006) Human let-7a miRNA blocks protein production on actively translating polyribosomes. Nat Struct Mol Biol 13: 1108-1114.
31. Song W, Raden D, Mandon EC, Gilmore R (2000) Role of Sec61alpha in the regulated transfer of the ribosome-nascent chain complex from the signal recognition particle to the translocation channel. Cell 100: 333-343.
32. Goodman M, Porter CA, Czelusniak J, Page SL, Schneider H, et al. (1998) Toward a phylogenetic classification of Primates based on DNA evidence complemented by fossil evidence. Mol Phylogenet Evol 9: 585-598.
33. Daza-Vamenta R, Glusman G, Rowen L, Guthrie B, Geraghty DE (2004) Genetic divergence of the rhesus macaque major histocompatibility complex. Genome Res 14: 1501-1515.
34. Kulski JK, Anzai T, Shiina T, Inoko H (2004) Rhesus macaque class I duplicon structures, organization, and evolution within the alpha block of the major histocompatibility complex. Mol Biol Evol 21: 2079-2091.
35. Barel MT, Pizzato N, Le Bouteiller P, Wiertz EJ, Lenfant F (2006) Subtle sequence variation among MHC class I locus products greatly influences sensitivity to HCMV US2- and US11-mediated degradation. Int Immunol 18: 173-182.
36. Machold RP, Wiertz EJ, Jones TR, Ploegh HL (1997) 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 185: 363-366.
37. Tortorella D, Gewurz B, Schust D, Furman M, Ploegh H (2000) Down-regulation of MHC class I antigen presentation by HCMV; lessons for tumor immunology. Immunol Invest 29: 97-100.
38. Wagner M, Gutermann A, Podlech J, Reddehase MJ, Koszinowski UH (2002) Major histocompatibility complex class I allele-specific cooperative and competitive interactions between immune evasion proteins of cytomegalovirus. J Exp Med 196: 805-816.
39. Hengel H, Reusch U, Gutermann A, Ziegler H, Jonjic S, et al. (1999) Cytomegaloviral control of MHC class I function in the mouse. Immunol Rev 168: 167-176.
40. Urvater JA, Otting N, Loehrke JH, Rudersdorf R, Slukvin II, et al. (2000) Mamu-I: a novel primate MHC class I B-related locus with unusually low variability. J Immunol 164: 1386-1398.
41. Lopez-Botet M, Llano M, Navarro F, Bellon T (2000) NK cell recognition of non-classical HLA class I molecules. Semin Immunol 12: 109-119.
42. Tomasec P, Braud VM, Rickards C, Powell MB, McSharry BP, et al. (2000) Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 287: 1031.
43. Ulbrecht M, Martinozzi S, Grzeschik M, Hengel H, Ellwart JW, et al. (2000) Cutting edge: the human cytomegalovirus UL40 gene product contains a ligand for HLA-E and prevents NK cell-mediated lysis. J Immunol 164: 5019-5022.
44. Bacher G, Pool M, Dobberstein B (1999) The ribosome regulates the GTPase of the beta-subunit of the signal recognition particle receptor. J Cell Biol 146: 723-730.
45. Garrison JL, Kunkel EJ, Hegde RS, Taunton J (2005) A substrate-specific inhibitor of protein translocation into the endoplasmic reticulum. Nature 436: 285-289.
46. Oyadomari S, Yun C, Fisher EA, Kreglinger N, Kreibich G, et al. (2006) Cotranslocational degradation protects the stressed endoplasmic reticulum from protein overload. Cell 126: 727-739.
47. Ito-Harashima S, Kuroha K, Tatematsu T, Inada T (2007) Translation of the poly(A) tail plays crucial roles in nonstop mRNA surveillance via translation repression and protein destabilization by proteasome in yeast. Genes Dev 21: 519-524.
48. Stern-Ginossar N, Elefant N, Zimmermann A, Wolf DG, Saleh N, et al. (2007) Host immune system gene targeting by a viral miRNA. Science 317: 376-381.
49. Chang WL, Kirchoff V, Pari GS, Barry PA (2002) Replication of rhesus cytomegalovirus in life-expanded rhesus fibroblasts expressing human telomerase. J Virol Methods 104: 135-146.
50. Atalay R, Zimmermann A, Wagner M, Borst E, Benz C, et al. (2002) Identification and expression of human cytomegalovirus transcription units coding for two distinct Fcgamma receptor homologs. J Virol 76: 8596-8608.