Optimal replication of human cytomegalovirus correlates with endocytosis of glycoprotein gpUL132

Journal of Virology

Volumn 84, Issue 14, 2010, Pages 7039-7052

  Kropff, Barbara ^a   Koedel, Yvonne ^a   Britt, William ^b   Mach, Michael ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN UL132; UNCLASSIFIED DRUG;

ARTICLE; CELL MEMBRANE; CELL SURFACE; CELLULAR DISTRIBUTION; ENDOCYTOSIS; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; MUTAGENESIS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANS GOLGI NETWORK; VIRION; VIRUS RECOMBINANT; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; CYTOMEGALOVIRUS; ENDOCYTOSIS; FIBROBLASTS; HELA CELLS; HUMANS; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; RECOMBINANT FUSION PROTEINS; VIRAL ENVELOPE PROTEINS; VIRION; VIRUS REPLICATION;

HERPESVIRIDAE; HUMAN HERPESVIRUS 5;

EID: 77953770908     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01644-09     Document Type: Article

References (58)

1. Alconada, A., U. Bauer, L. Baudoux, J. Piette, and B. Hoflack. 1998. Intracellular transport of the glycoproteins gE and gI of the varicella-zoster virus. gE accelerates the maturation of gI and determines its accumulation in the trans-Golgi network. J. Biol. Chem. 273:13430-13436.
2. Andreoni, M., M. Faircloth, L. Vugler, and W. J. Britt. 1989. A rapid microneutralization assay for the measurement of neutralizing antibody reactive with human cytomegalovirus. J. Virol. Methods 23:157-167. (Pubitemid 19069993)
3. Beitia Ortiz de Zarate, I., L. Cantero-Aguilar, M. Longo, C. Berlioz-Torrent, and F. Rozenberg. 2007. Contribution of endocytic motifs in the cytoplasmic tail of herpes simplex virus type 1 glycoprotein B to virus replication and cell-cell fusion. J. Virol. 81:13889-13903. (Pubitemid 350247882)
4. Beitia Ortiz de Zarate, I., K. Kaelin, and F. Rozenberg. 2004. Effects of mutations in the cytoplasmic domain of herpes simplex virus type 1 glycoprotein B on intracellular transport and infectivity. J. Virol. 78:1540-1551.
5. Bi, W., and P. J. Stambrook. 1998. Site-directed mutagenesis by combined chain reaction. Anal. Biochem. 256:137-140.
6. Bonifacino, J. S., and L. M. Traub. 2003. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72:395-447.
7. Borst, E. M., G. Hahn, U. H. Koszinowski, and M. Messerle. 1999. Cloning of the human cytomegalovirus (HCMV) genome as an infectious bacterial artificial chromosome in Escherichia coli: a new approach for construction of HCMV mutants. J. Virol. 73:8320-8329.
8. Brideau, A. D., R. T. del, E. J. Wolffe, and L. W. Enquist. 1999. Intracellular trafficking and localization of the pseudorabies virus Us9 type II envelope protein to host and viral membranes. J. Virol. 73:4372-4384.
9. Brideau, A. D., L. W. Enquist, and R. S. Tirabassi. 2000. The role of virion membrane protein endocytosis in the herpesvirus life cycle. J. Clin. Virol. 17:69-82.
10. r human cytomegalovirus protein. J. Gen. Virol. 68:1897-1907.
11. Cherepanov, P. P., and W. Wackernagel. 1995. Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158:9-14.
12. Crump, C. M., C. H. Hung, L. Thomas, L. Wan, and G. Thomas. 2003. Role of PACS-1 in trafficking of human cytomegalovirus glycoprotein B and virus production. J. Virol. 77:11105-11113.
13. Damm, E. M., L. Pelkmans, J. Kartenbeck, A. Mezzacasa, T. Kurzchalia, and A. Helenius. 2005. Clathrin- and caveolin-1-independent endocytosis: entry of simian virus 40 into cells devoid of caveolae. J. Cell Biol. 168:477-488.
14. Fan, Z., M. L. Grantham, M. S. Smith, E. S. Anderson, J. A. Cardelli, and M. I. Muggeridge. 2002. Truncation of herpes simplex virus type 2 glycoprotein B increases its cell surface expression and activity in cell-cell fusion, but these properties are unrelated. J. Virol. 76:9271-9283. (Pubitemid 34919886)
15. Favoreel, H. W., T. C. Mettenleiter, and H. J. Nauwynck. 2004. Copatching and lipid raft association of different viral glycoproteins expressed on the surfaces of pseudorabies virus-infected cells. J. Virol. 78:5279-5287.
16. Favoreel, H. W., M. G. Van, H. J. Nauwynck, L. W. Enquist, and M. B. Pensaert. 2002. A tyrosine-based motif in the cytoplasmic tail of pseudorabies virus glycoprotein B is important for both antibody-induced internalization of viral glycoproteins and efficient cell-to-cell spread. J. Virol. 76: 6845-6851.
17. Ficinska, J., M. G. Van, H. J. Nauwynck, K. Bienkowska-Szewczyk, and H. W. Favoreel. 2005. Pseudorabies virus glycoprotein gD contains a functional endocytosis motif that acts in concert with an endocytosis motif in gB to drive internalization of antibody-antigen complexes from the surface of infected monocytes. J. Virol. 79:7248-7254. (Pubitemid 40677354)
18. Friedman, H. M., L. Wang, N. O. Fishman, J. D. Lambris, R. J. Eisenberg, G. H. Cohen, and J. Lubinski. 1996. Immune evasion properties of herpes simplex virus type 1 glycoprotein gC. J. Virol. 70:4253-4260. (Pubitemid 26187425)
19. Fuchs, W., B. G. Klupp, H. Granzow, C. Hengartner, A. Brack, A. Mundt, L. W. Enquist, and T. C. Mettenleiter. 2002. Physical interaction between envelope glycoproteins E and M of pseudorabies virus and the major tegument protein UL49. J. Virol. 76:8208-8217. (Pubitemid 34809075)
20. Ghosh, P., and S. Kornfeld. 2004. The GGA proteins: key players in protein sorting at the trans-Golgi network. Eur. J. Cell Biol. 83:257-262.
21. Heineman, T. C., and S. L. Hall. 2002. Role of the varicella-zoster virus gB cytoplasmic domain in gB transport and viral egress. J. Virol. 76:591-599.
22. Homman-Loudiyi, M., K. Hultenby, W. Britt, and C. Soderberg-Naucler. 2003. Envelopment of human cytomegalovirus occurs by budding into Golgi-derived vacuole compartments positive for gB, Rab 3, trans-Golgi network 46, and mannosidase II. J. Virol. 77:3191-3203. (Pubitemid 36228103)
23. Jarvis, M. A., K. N. Fish, C. Soderberg-Naucler, D. N. Streblow, H. L. Meyers, G. Thomas, and J. A. Nelson. 2002. Retrieval of human cytomegalovirus glycoprotein B from cell surface is not required for virus envelopment in astrocytoma cells. J. Virol. 76:5147-5155.
24. Kalejta, R. F. 2008. Tegument proteins of human cytomegalovirus. Microbiol. Mol. Biol. Rev. 72:249-265.
25. Krzyzaniak, M., M. Mach, and W. J. Britt. 2007. The cytoplasmic tail of glycoprotein M (gpUL100) expresses trafficking signals required for human cytomegalovirus assembly and replication. J. Virol. 81:10316-10328. (Pubitemid 47463307)
26. Krzyzaniak, M. A., M. Mach, and W. J. Britt. 2009. HCMV-encoded glycoprotein M (UL100) interacts with Rab11 effector protein FIP4. Traffic 10: 1439-1457.
27. Lenac, T., M. Budt, J. Arapovic, M. Hasan, A. Zimmermann, H. Simic, A. Krmpotic, M. Messerle, Z. Ruzsics, U. H. Koszinowski, H. Hengel, and S. Jonjic. 2006. The herpesviral Fc receptor fcr-1 down-regulates the NKG2D ligands MULT-1 and H60. J. Exp. Med. 203:1843-1850.
28. Mach, M., B. Kropff, M. Kryzaniak, and W. Britt. 2005. Complex formation by glycoproteins M and N of human cytomegalovirus: structural and functional aspects. J. Virol. 79:2160-2170. (Pubitemid 40204574)
29. Mach, M., K. Osinski, B. Kropff, U. Schloetzer-Schrehardt, M. Krzyzaniak, and W. Britt. 2007. The carboxy-terminal domain of glycoprotein N of human cytomegalovirus is required for virion morphogenesis. J. Virol. 81: 5212-5224. (Pubitemid 46744431)
30. Maresova, L., T. J. Pasieka, E. Homan, E. Gerday, and C. Grose. 2005. Incorporation of three endocytosed varicella-zoster virus glycoproteins, gE, gH, and gB, into the virion envelope. J. Virol. 79:997-1007. (Pubitemid 40053883)
31. Marsh, H. N., C. I. Dubreuil, C. Quevedo, A. Lee, M. Majdan, G. S. Walsh, S. Hausdorff, F. A. Said, O. Zoueva, M. Kozlowski, K. Siminovitch, B. G. Neel, F. D. Miller, and D. R. Kaplan. 2003. SHP-1 negatively regulates neuronal survival by functioning as a TrkA phosphatase. J. Cell Biol. 163: 999-1010.
32. Maurer, M. E., and J. A. Cooper. 2006. The adaptor protein Dab2 sorts LDL receptors into coated pits independently of AP-2 and ARH. J. Cell Sci. 119:4235-4246.
33. Mettenleiter, T. C. 2002. Herpesvirus assembly and egress. J. Virol. 76:1537-1547.
34. Mettenleiter, T. C., B. G. Klupp, and H. Granzow. 2006. Herpesvirus assembly: a tale of two membranes. Curr. Opin. Microbiol. 9:423-429.
35. Middlemas, D. S., R. A. Lindberg, and T. Hunter. 1991. trkB, a neural receptor protein-tyrosine kinase: evidence for a full-length and two truncated receptors. Mol. Cell. Biol. 11:143-153.
36. Mishra, S. K., P. A. Keyel, M. J. Hawryluk, N. R. Agostinelli, S. C. Watkins, and L. M. Traub. 2002. Disabled-2 exhibits the properties of a cargo-selective endocytic clathrin adaptor. EMBO J. 21:4915-4926.
37. 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. (Pubitemid 39458759)
38. Muyrers, J. P., Y. Zhang, G. Testa, and A. F. Stewart. 1999. Rapid modification of bacterial artificial chromosomes by ET-recombination. Nucleic Acids Res. 27:1555-1557. (Pubitemid 29206301)
39. Naslavsky, N., R. Weigert, and J. G. Donaldson. 2004. Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. Mol. Biol. Cell 15:3542-3552.
40. Nixdorf, R., B. G. Klupp, A. Karger, and T. C. Mettenleiter. 2000. Effects of truncation of the carboxy terminus of pseudorabies virus glycoprotein B on infectivity. J. Virol. 74:7137-7145. (Pubitemid 30470698)
41. Ohno, H., R. C. Aguilar, D. Yeh, D. Taura, T. Saito, and J. S. Bonifacino. 1998. The medium subunits of adaptor complexes recognize distinct but overlapping sets of tyrosine-based sorting signals. J. Biol. Chem. 273:25915-25921.
42. Olson, J. K., and C. Grose. 1997. Endocytosis and recycling of varicellazoster virus Fc receptor glycoprotein gE: internalization mediated by a YXXL motif in the cytoplasmic tail. J. Virol. 71:4042-4054.
43. Pasieka, T. J., L. Maresova, and C. Grose. 2003. A functional YNKI motif in the short cytoplasmic tail of varicella-zoster virus glycoprotein gH mediates clathrin-dependent and antibody-independent endocytosis. J. Virol. 77:4191-4204.
44. Pasieka, T. J., L. Maresova, K. Shiraki, and C. Grose. 2004. Regulation of varicella-zoster virus-induced cell-to-cell fusion by the endocytosis-competent glycoproteins gH and gE. J. Virol. 78:2884-2896.
45. Radsak, K., M. Eickmann, T. Mockenhaupt, E. Bogner, H. Kern, A. Eis- Hubinger, and M. Reschke. 1996. Retrieval of human cytomegalovirus glycoprotein B from the infected cell surface for virus envelopment. Arch. Virol. 141:557-572.
46. 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. (Pubitemid 30036234)
47. Sandvig, K., M. L. Torgersen, H. A. Raa, and D. B. van. 2008. Clathrinin-dependent endocytosis: from nonexisting to an extreme degree of complexity. Histochem. Cell Biol. 129:267-276.
48. Shiba, T., M. Kawasaki, H. Takatsu, T. Nogi, N. Matsugaki, N. Igarashi, M. Suzuki, R. Kato, K. Nakayama, and S. Wakatsuki. 2003. Molecular mechanism of membrane recruitment of GGA by ARF in lysosomal protein transport. Nat. Struct. Biol. 10:386-393.
49. Soppet, D., E. Escandon, J. Maragos, D. S. Middlemas, S. W. Reid, J. Blair, L. E. Burton, B. R. Stanton, D. R. Kaplan, T. Hunter, K. Nikolics, and L. F. Parade. 1991. The neurotrophic factors brain-derived neurotrophic factor and neurotrophin-3 are ligands for the trkB tyrosine kinase receptor. Cell 65:895-903.
50. Spaderna, S., B. Kropff, Y. Kodel, S. Shen, S. Coley, S. Lu, W. Britt, and M. Mach. 2005. Deletion of gpUL132, a structural component of human cytomegalovirus, results in impaired virus replication in fibroblasts. J. Virol. 79:11837-11847.
51. H3 interface of immunoglobulin G. J. Virol. 82: 3490-3499.
52. Sprague, E. R., C. Wang, D. Baker, and P. J. Bjorkman. 2006. Crystal structure of the HSV-1 Fc receptor bound to Fc reveals a mechanism for antibody bipolar bridging. PLoS. Biol. 4:e148.
53. Talbot, P., and J. D. Almeida. 1977. Human cytomegalovirus: purification of enveloped virions and dense bodies. J. Gen. Virol. 36:345-349.
54. Tirabassi, R. S., and L. W. Enquist. 1998. Role of envelope protein gE endocytosis in the pseudorabies virus life cycle. J. Virol. 72:4571-4579.
55. Tirabassi, R. S., and L. W. Enquist. 1999. Mutation of the YXXL endocytosis motif in the cytoplasmic tail of pseudorabies virus gE. J. Virol. 73:2717-2728.
56. Tugizov, S., E. Maidji, J. Xiao, and L. Pereira. 1999. An acidic cluster in the cytosolic domain of human cytomegalovirus glycoprotein B is a signal for endocytosis from the plasma membrane. J. Virol. 73:8677-8688.
57. Van Minnebruggen, G., H. W. Favoreel, and H. J. Nauwynck. 2004. Internalization of pseudorabies virus glycoprotein B is mediated by an interaction between the YQRL motif in its cytoplasmic domain and the clathrin-associated AP-2 adaptor complex. J. Virol. 78:8852-8859.
58. Varnum, S. M., D. N. Streblow, M. E. Monroe, P. Smith, K. J. Auberry, L. Pasa-Tolic, D. Wang, D. G. Camp, K. Rodland, S. Wiley, W. Britt, T. Shenk, R. D. Smith, and J. A. Nelson. 2004. Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J. Virol. 78:10960-10966.