Human cytomegalovirus US9 protein contains an N-terminal signal sequence and a C-terminal mitochondrial localization domain, and does not alter cellular sensitivity to apoptosis

Journal of General Virology

Volumn 90, Issue 5, 2009, Pages 1172-1182

  Mandic, Lana ^a   Miller, Matthew S ^a   Coulter, Corinne ^a   Munshaw, Brian ^a   Hertel, Laura ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BREFELDIN A; CARBONYL CYANIDE CHLOROPHENYLHYDRAZONE; GREEN FLUORESCENT PROTEIN; HYGROMYCIN B; LONIDAMINE; PROTEIN US9; THAPSIGARGIN; TUMOR NECROSIS FACTOR ALPHA; TUNICAMYCIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; MEMBRANE PROTEIN; RNA BINDING PROTEIN; US11 PROTEIN, HERPESVIRUS; US2 PROTEIN, VARICELLOVIRUS; US9 PROTEIN, HUMAN HERPESVIRUS 5; VIRUS ENVELOPE PROTEIN;

AMINO TERMINAL SEQUENCE; APOPTOSIS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL PROTECTION; CELL SURVIVAL; CELLULAR DISTRIBUTION; COMPUTER MODEL; CONTROLLED STUDY; DELETION MUTANT; ENDOPLASMIC RETICULUM; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; VIRUS STRAIN; AMINO ACID SEQUENCE; CELL LINE; CHEMISTRY; CYTOLOGY; CYTOMEGALOVIRUS; GENE EXPRESSION REGULATION; GENETICS; KIDNEY; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; VIRUS GENE;

HUMAN HERPESVIRUS 5;

AMINO ACID SEQUENCE; APOPTOSIS; CELL LINE; CYTOMEGALOVIRUS; GENE EXPRESSION REGULATION, VIRAL; GENES, VIRAL; GREEN FLUORESCENT PROTEINS; HUMANS; KIDNEY; MEMBRANE GLYCOPROTEINS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PROTEIN TRANSPORT; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT; VIRAL ENVELOPE PROTEINS; VIRAL PROTEINS;

EID: 67449094175     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.008466-0     Document Type: Article

References (46)

1. Bendtsen, J. D., Nielsen, H., von Heijne, G. & Brunak, S. (2004). Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340, 783-795.
2. Borgese, N., D'Arrigo, A., De Silvestris, M. & Pietrini, G. (1993). NADH-cytochrome b5 reductase and cytochrome b5. The problem of posttranslational targeting to the endoplasmic reticulum. Subcell Biochem 21, 313-341.
3. Borgese, N., Brambillasca, S. & Colombo, S. (2007). How tails guide tail-anchored proteins to their destinations. Curr Opin Cell Biol 19, 368-375.
4. Bozidis, P., Williamson, C. D. & Colberg-Poley, A. M. (2008). Mitochondrial and secretory human cytomegalovirus UL37 proteins traffic into mitochondrion-associated membranes of human cells. J Virol 82, 2715-2726.
5. Colberg-Poley, A. M., Patel, M. B., Erezo, D. P. & Slater, J. E. (2000). Human cytomegalovirus UL37 immediate-early regulatory proteins traffic through the secretory apparatus and to mitochondria. J Gen Virol 81, 1779-1789.
6. Emanuelsson, O., Nielsen, H., Brunak, S. & von Heijne, G. (2000). Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300, 1005-1016.
7. Falk, C. S., Mach, M., Schendel, D. J., Weiss, E. H., Hilgert, I. & Hahn, G. (2002). NK cell activity during human cytomegalovirus infection is dominated by US2-11-mediated HLA class I down-regulation. J Immunol 169, 3257-3266.
8. Hegde, N. R., Tomazin, R. A., Wisner, T. W., Dunn, C., Boname, J. M., Lewinsohn, D. M. & Johnson, D. C. (2002). 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. J Virol 76, 10929-10941.
9. Hegde, N. R., Chevalier, M. S., Wisner, T. W., Denton, M. C., Shire, K., Frappier, L. & Johnson, D. C. (2006). The role of BiP in endoplasmic reticulum-associated degradation of major histocompatibility complex class I heavy chain induced by cytomegalovirus proteins. J Biol Chem 281, 20910-20919.
10. Hertel, L. & Mocarski, E. S. (2004). Global analysis of host cell gene expression late during cytomegalovirus infection reveals extensive dysregulation of cell cycle gene expression and induction of pseudomitosis independent of US28 function. J Virol 78, 11988-12011.
11. Hertel, L., Lacaille, V. G., Strobl, H., Mellins, E. D. & Mocarski, E. S. (2003). Susceptibility of immature and mature Langerhans cell-type dendritic cells to infection and immunomodulation by human cytomegalovirus. J Virol 77, 7563-7574.
12. Hertel, L., Chou, S. & Mocarski, E. S. (2007). Viral and cell cycle-regulated kinases in cytomegalovirus-induced pseudomitosis and replication. PLoS Pathog 3, e6.
13. Hetz, C. & Glimcher, L. (2008). The daily job of night killers: Alternative roles of the BCL-2 family in organelle physiology. Trends Cell Biol 18, 38-44.
14. Huber, M. T., Tomazin, R., Wisner, T., Boname, J. & Johnson, D. C. (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.
15. Jones, D. T. (2007). Improving the accuracy of transmembrane protein topology prediction using evolutionary information. Bioinformatics 23, 538-544.
16. Jones, T. R. & Muzithras, V. P. (1992). A cluster of dispensable genes within the human cytomegalovirus genome short component: IRS1, US1 through US5, and the US6 family. J Virol 66, 2541-2546.
17. Jones, T. R., Muzithras, V. P. & Gluzman, Y. (1991). Replacement mutagenesis of the human cytomegalovirus genome: US10 and US11 gene products are nonessential. J Virol 65, 5860-5872.
18. Kanaji, S., Iwahashi, J., Kida, Y., Sakaguchi, M. & Mihara, K. (2000). Characterization of the signal that directs Tom20 to the mitochondrial outer membrane. J Cell Biol 151, 277-288.
19. Kollert-Jons, A., Bogner, E. & Radsak, K. (1991). A 15-kilobase-pair region of the human cytomegalovirus genome which includes US1 through US13 is dispensable for growth in cell culture. J Virol 65, 5184-5189.
20. Kutay, U., Hartmann, E. & Rapoport, T. A. (1993). A class of membrane proteins with a C-terminal anchor. Trends Cell Biol 3, 72-75.
21. Kyte, J. & Doolittle, R. F. (1982). A simple method for displaying the hydropathic character of a protein. J Mol Biol 157, 105-132.
22. Lin, A., Xu, H. & Yan, W. (2007). Modulation of HLA expression in human cytomegalovirus immune evasion. Cell Mol Immunol 4, 91-98.
23. Maidji, E., Tugizov, S., Jones, T., Zheng, Z. & Pereira, L. (1996). Accessory human cytomegalovirus glycoprotein US9 in the unique short component of the viral genome promotes cell-to-cell transmission of virus in polarized epithelial cells. J Virol 70, 8402-8410.
24. Maidji, E., Tugizov, S., Abenes, G., Jones, T. & Pereira, L. (1998). A novel human cytomegalovirus glycoprotein, gpUS9, which promotes cell-to-cell spread in polarized epithelial cells, colocalizes with the cytoskeletal proteins E-cadherin and F-actin. J Virol 72, 5717-5727.
25. Martoglio, B. & Dobberstein, B. (1998). Signal sequences: More than just greasy peptides. Trends Cell Biol 8, 410-415.
26. Mavinakere, M. S. & Colberg-Poley, A. M. (2004). Dual targeting of the human cytomegalovirus UL37 exon 1 protein during permissive infection. J Gen Virol 85, 323-329.
27. McCormick, A. L. (2008). Control of apoptosis by human cytomegalovirus. Curr Top Microbiol Immunol 325, 281-295.
28. McCormick, A. L., Smith, V. L., Chow, D. & Mocarski, E. S. (2003). Disruption of mitochondrial networks by the human cytomegalovirus UL37 gene product viral mitochondrion-localized inhibitor of apoptosis. J Virol 77, 631-641.
29. McCormick, A. L., Meiering, C. D., Smith, G. B. & Mocarski, E. S. (2005). Mitochondrial cell death suppressors carried by human and murine cytomegalovirus confer resistance to proteasome inhibitor-induced apoptosis. J Virol 79, 12205-12217.
30. Miller, A. D. & Rosman, G. J. (1989). Improved retroviral vectors for gene transfer and expression. Biotechniques 7, 980-982, 984-986, 989-990.
31. Mocarski, E. S., Shenk, T. & Pass, R. F. (2007). Cytomegaloviruses. In Fields Virology, 5th edn, pp. 2701-2772. Edited by D. M. Knipe & P. M. Howley. Philadelphia, PA: Lippincott Williams & Wilkins.
32. Moorman, N. J., Cristea, I. M., Terhune, S. S., Rout, M. P., Chait, B. T. & Shenk, T. (2008). Human cytomegalovirus protein UL38 inhibits host cell stress responses by antagonizing the tuberous sclerosis protein complex. Cell Host Microbe 3, 253-262.
33. Nakai, K. & Horton, P. (1999). PSORT: A program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24, 34-36.
34. Pelham, H. R. (1990). The retention signal for soluble proteins of the endoplasmic reticulum. Trends Biochem Sci 15, 483-486.
35. Pereira, L., Maidji, E., Tugizov, S. & Jones, T. (1995). Deletion mutants in human cytomegalovirus glycoprotein US9 are impaired in cell-cell transmission and in altering tight junctions of polarized human retinal pigment epithelial cells. Scand J Infect Dis Suppl 99, 82-87.
36. Rapaport, D. (2003). Finding the right organelle. Targeting signals in mitochondrial outer-membrane proteins. EMBO Rep 4, 948-952.
37. Reeves, M. B., Davies, A. A., McSharry, B. P., Wilkinson, G. W. & Sinclair, J. H. (2007). Complex I binding by a virally encoded RNA regulates mitochondria-induced cell death. Science 316, 1345-1348.
38. Sinzger, C., Hahn, G., Digel, M., Katona, R., Sampaio, K. L., Messerle, M., Hengel, H., Koszinowski, U., Brune, W. & Adler, B. (2008). Cloning and sequencing of a highly productive, endotheliotropic virus strain derived from human cytomegalovirus TB40/E. J Gen Virol 89, 359-368.
39. Skaletskaya, A., Bartle, L. M., Chittenden, T., McCormick, A. L., Mocarski, E. S. & Goldmacher, V. S. (2001). A cytomegalovirus-encoded inhibitor of apoptosis that suppresses caspase-8 activation. Proc Natl Acad Sci U S A 98, 7829-7834.
40. Tenney, D. J. & Colberg-Poley, A. M. (1991). Human cytomegalovirus UL36-38 and US3 immediate-early genes: Temporally regulated expression of nuclear, cytoplasmic, and polysome-associated transcripts during infection. J Virol 65, 6724-6734.
41. Terhune, S., Torigoi, E., Moorman, N., Silva, M., Qian, Z., Shenk, T. & Yu, D. (2007). Human cytomegalovirus UL38 protein blocks apoptosis. J Virol 81, 3109-3123.
42. Thomenius, M. J. & Distelhorst, C. W. (2003). Bcl-2 on the endoplasmic reticulum: Protecting the mitochondria from a distance. J Cell Sci 116, 4493-4499.
43. Weston, K. (1988). An enhancer element in the short unique region of human cytomegalovirus regulates the production of a group of abundant immediate early transcripts. Virology 162, 406-416.
44. Weston, K. & Barrell, B. G. (1986). Sequence of the short unique region, short repeats, and part of the long repeats of human cytomegalovirus. J Mol Biol 192, 177-208.
45. Yamanishi, K. & Rapp, F. (1979). Induction of host DNA synthesis and DNA polymerase by DNA-negative temperature-sensitive mutants of human cytomegalovirus. Virology 94, 237-241.
46. Young, J. C., Hoogenraad, N. J. & Hartl, F. U. (2003). Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112, 41-50.