Three-dimensional structure of the human cytomegalovirus cytoplasmic virion assembly complex includes a reoriented secretory apparatus

Journal of Virology

Volumn 81, Issue 21, 2007, Pages 11861-11869

  Das, Subhendu ^a   Vasanji, Amit ^a   Pellett, Philip E ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; EARLY ENDOSOME ANTIGEN 1; UNCLASSIFIED DRUG;

ARTICLE; CELL INCLUSION; CELL STRUCTURE; COMPLEX FORMATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; ELECTRON MICROSCOPY; ENDOSOME; EXOCYTOSIS; GOLGI COMPLEX; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SECRETORY VESICLE; THREE DIMENSIONAL IMAGING; VIRION; VIRUS ASSEMBLY; VIRUS MORPHOLOGY; VIRUS MUTATION;

CELL LINE; CYTOMEGALOVIRUS; CYTOPLASM; ENDOSOMES; EXOCYTOSIS; GOLGI APPARATUS; HUMANS; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON; MODELS, BIOLOGICAL; PROTEIN CONFORMATION; TIME FACTORS; TRANS-GOLGI NETWORK; VIRION; VIRUS ASSEMBLY;

HUMAN HERPESVIRUS 5;

EID: 35448968369     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01077-07     Document Type: Article

References (60)

1. AuCoin, D. P., G. B. Smith, C. D. Metering, and E. S. Mocarski. 2006. Betaherpesvirus-conserved cytomegalovirus tegument protein ppUL32 (pp150) controls cytoplasmic events during virion maturation. J. Virol. 80:8199-8210.
2. Azzeh, M., A. Honigman, A. Taraboulos, A. Rouvinski, and D. G. Wolf. 2006. Structural changes in human cytomegalovirus cytoplasmic assembly sites in the absence of UL97 kinase activity. Virology 354:69-79.
3. Barr, F. A. 1999. A novel Rab6-interacting domain defines a family of Golgi-targeted coiled-coil proteins. Curr. Biol. 9:381-384.
4. Barr, F. A., and B. Short. 2003. Golgins in the structure and dynamics of the Golgi apparatus. Curr. Opin. Cell Biol. 15:405-413.
5. Benboudjema, L., M. Mulvey, Y. Gao, S. W. Pimplikar, and I. Mohr. 2003. Association of the herpes simplex virus type 1 Us11 gene product with the cellular kinesin light-chain-related protein PAT1 results in the redistribution of both polypeptides. J. Virol. 77:9192-9203.
6. Cha, T. A., E. Tom, G. W. Kemble, G. M. Duke, E. S. Mocarski, and R. R. Spaete. 1996. Human cytomegalovirus clinical isolates carry at least 19 genes not found in laboratory strains. J. Virol. 70:78-83.
7. Coumailleau, F., V. Das, A. Alcover, G. Raposo, S. Vandormael-Pournin, S. Le Bras, P. Baldacci, A. Dautry-Varsat, C. Babinet, and M. Cohen-Tannoudji. 2004. Over-expression of Rififylin, a new RING finger and FYVE-like domain-containing protein, inhibits recycling from the endocytic recycling compartment. Mol. Biol. Cell 15:4444-4456.
8. 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.
9. Das, S., and P. E. Pellett. 2007. Members of the HCMV US12 family of predicted heptaspanning membrane proteins have unique intracellular distributions, including association with the cytoplasmic virion assembly complex. Virology 361:263-273.
10. Das, S., Y. Skomorovska-Prokvolit, F. Z. Wang, and P. E. Pellett. 2006. Infection-dependent nuclear localization of US17, a member of the US12 family of human cytomegalovirus-encoded seven-transmembrane proteins. J. Virol. 80:1191-1203.
11. Diefenbach, R. J., M. Miranda-Saksena, E. Diefenbach, D. J. Holland, R. A. Boadle, P. J. Armati, and A. L. Cunningham. 2002. Herpes simplex virus tegument protein US11 interacts with conventional kinesin heavy chain. J. Virol. 76:3282-3291.
12. Dohner, K., K. Radtke, S. Schmidt, and B. Sodeik. 2006. Eclipse phase of herpes simplex virus type 1 infection: efficient dynein-mediated capsid transport without the small capsid protein VP26. J. Virol. 80:8211-8224.
13. Dohner, K., A. Wolfstein, U. Prank, C. Echeverri, D. Dujardin, R. Vallee, and B. Sodeik. 2002. Function of dynein and dynactin in herpes simplex virus capsid transport. Mol. Biol. Cell 13:2795-2809.
14. Dolan, A., C. Cunningham, R. D. Hector, A. F. Hassan-Walker, L. Lee, C. Addison, D. J. Dargan, D. J. McGeoch, D. Gatherer, V. C. Emery, P. D. Griffiths, C. Sinzger, B. P. McSharry, G. W. Wilkinson, and A. J. Davison. 2004. Genetic content of wild-type human cytomegalovirus. J. Gen. Virol. 85:1301-1312.
15. Donnellan, W. L., S. Chantra-Umporn, and J. M. Kidd. 1966. The cytomegalic inclusion cell: an electron microscopic study. Arch. Pathol. 82:336-348.
16. Enquist, L. W., P. J. Husak, B. W. Banfield, and G. A. Smith. 1998. Infection and spread of alphaherpesviruses in the nervous system. Adv. Virus Res. 51:237-347.
17. Foster, L. J., C. L. de Hoog, Y. Zhang, Y. Zhang, X. Xie, V. K. Mootha, and M. Mann. 2006. A mammalian organelle map by protein correlation profiling. Cell 125:187-199.
18. Fraile-Ramos, A., A. Pelchen-Matthews, T. N. Kledal, H. Browne, T. W. Schwartz, and M. Marsh. 2002. Localization of HCMV UL33 and US27 in endocytic compartments and viral membranes. Traffic 3:218-232.
19. Gaspar, M., and T. Shenk. 2006. Human cytomegalovirus inhibits a DNA damage response by mislocalizing checkpoint proteins. Proc. Natl. Acad. Sci. USA 103:2821-2826.
20. Gilloteaux, J., and M. R. Nassiri. 2000. Human bone marrow fibroblasts infected by cytomegalovirus: ultrastructural observations. J. Submicrosc. Cytol. Pathol. 32:17-45.
21. Grefte, A., N. Blom, M. van der Giessen, W. van Son, and T. H. The. 1993. Ultrastructural analysis of circulating cytomegalic cells in patients with active cytomegalovirus infection: evidence for virus production and endothelial origin. J. Infect. Dis. 168:1110-1118.
22. Guo, Y. W., and E. S. Huang. 1993. Characterization of a structurally tricistronic gene of human cytomegalovirus composed of U(s)18, U(s)19, and U(s)20. J. Virol. 67:2043-2054.
23. Hertel, L., and E. S. Mocarski. 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.
24. 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 11. J. Virol. 77:3191-3203.
25. Iwasaki, Y., T. Furukawa, S. Plotkin, and H. Koprowski. 1973. Ultrastructural study on the sequence of human cytomegalovirus infection in human diploid cells. Arch. Gesamte Virusforsch. 40:311-324.
26. 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.
27. Jesionek and Kiolemenoglou. 1904. Über einen befund von protozoenartigen gebilden in den Organen eines feten. Munch. Med. Wochenschr. 51:1905-1907.
28. Kimura, A., T. Tamura, and T. Nakao. 1976. Intracytoplasmic uncoated capsids of human cytomegalovirus. Tohoku J. Exp. Med. 119:223-236.
29. Kjer-Nielsen, L., R. D. Teasdale, C. van Vliet, and P. A. Gleeson. 1999. A novel Golgi-localization domain shared by a class of coiled-coil peripheral membrane proteins. Curr. Biol. 9:385-388.
30. Koshizuka, T., Y. Kawaguchi, and Y. Nishiyama. 2005. Herpes simplex virus type 2 membrane protein UL56 associates with the kinesin motor protein KIF1A. J. Gen. Virol. 86:527-533.
31. Lee, G. E., J. W. Murray, A. W. Wolkoff, and D. W. Wilson. 2006. Reconstitution of herpes simplex virus microtubule-dependent trafficking in vitro. J. Virol. 80:4264-4275.
32. Lu, L., G. Tai, and W. Hong. 2004. Autoantigen Golgin-97, an effector of Ar11 GTPase, participates in traffic from the endosome to the trans-Golgi network. Mol. Biol. Cell 15:4426-4443.
33. Matsumoto, A., and P. C. Hanawalt. 2000. Histone H3 and heat shock protein GRP78 are selectively cross-linked to DNA by photoactivated gilvocarcin V in human fibroblasts. Cancer Res. 60:3921-3926.
34. McGavran, M. H., and M. G. Smith. 1965. Ultrastructural, cytochemical, and microchemical observations on cytomegalovirus (salivary gland virus) infection of human cells in tissue culture. Exp. Mol. Pathol. 76:1-10.
35. Mettenleiter, T. C. 2005. Intriguing interplay between viral proteins during herpesvirus assembly or: the herpesvirus assembly puzzle. Vet. Microbiol. 113:163-169.
36. Munro, S., and B. J. Nichols. 1999. The GRIP domain: a novel Golgi-targeting domain found in several coiled-coil proteins. Curr. Biol. 9:377-380.
37. Murphy, E., D. Yu, J. Grimwood, J. Schmutz, M. Dickson, M. A. Jarvis, G. Hahn, J. A. Nelson, R. M. Myers, and T. E. Shenk. 2003. Coding potential of laboratory and clinical strains of human cytomegalovirus. Proc. Natl. Acad. Sci. USA 100:14976-14981.
38. Ogawa-Goto, K., K. Tanaka, W. Gibson, E. Moriishi, Y. Miura, T. Kurata, S. Irie, and T. Sata. 2003. Microtubule network facilitates nuclear targeting of human cytomegalovirus capsid. J. Virol. 77:8541-8547.
39. Pignatelli, S., P. Dal Monte, M. P. Landini, B. Seven, R. Nassiri, J. Gilloteaux, J. M. Papadimitriou, G. R. Shellam, T. Mertens, C. Buser, D. Michel, and P. Walther. 2007. Cytomegalovirus primary envelopment at large nuclear membrane infoldings: what's new? J. Virol. 81:7320-7321.
40. Prichard, M. N., W. J. Britt, S. L. Daily, C. B. Hartline, and E. R. Kern. 2005. Human cytomegalovirus UL97 kinase is required for the normal intranuclear distribution of pp65 and virion morphogenesis. J. Virol. 79:15494-15502.
41. Prichard, M. N., N. Gao, S. Jairath, G. Mulamba, P. Krosky, D. M. Coen, B. O. Parker, and G. S. Pari. 1999. A recombinant human cytomegalovirus with a large deletion in UL97 has a severe replication deficiency. J. Virol. 73:5663-5670.
42. Prichard, M. N., M. E. Penfold, G. M. Duke, R. R. Spaete, and G. W. Kemble. 2001. A review of genetic differences between limited and extensively passaged human cytomegalovirus strains. Rev. Med. Virol. 11:191-200.
43. Radtke, K., K. Dohner, and B. Sodeik. 2006. Viral interactions with the cytoskeleton: a hitchhiker's guide to the cell. Cell Microbiol. 8:387-400.
44. Resnik, K. S., M. DiLeonardo, and M. Maillet. 2000. Histopathologic findings in cutaneous cytomegalovirus infection. Am. J. Dermatopathol. 22:397-407.
45. Ruebner, B. H., T. Hirano, R. J. Slusser, and D. N. Medearis, Jr. 1965 Human cytomegalovirus infection, electron microscopic and histochemical changes in cultures of human fibroblasts. Am. J. Pathol. 46:477-496.
46. Sampaio, K. L., Y. Cavignac, Y. D. Stierhof, and C. Sinzger. 2005. Human cytomegalovirus labeled with green fluorescent protein for live analysis of intracellular particle movements. J. Virol. 79:2754-2767.
47. 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.
48. Satpute-Krishnan, P., J. A. DeGiorgis, and E. L. Bearer. 2003. Fast anterograde transport of herpes simplex virus: role for the amyloid precursor protein of Alzheimer's disease. Aging Cell 2:305-318.
49. Seo, J. Y., and W. J. Britt. 2006. Sequence requirements for localization of human cytomegalovirus tegument protein pp28 to the virus assembly compartment and for assembly of infectious virus. J. Virol. 80:5611-5626.
50. Severi, B., M. P. Landini, and E. Govoni. 1988. Human cytomegalovirus morphogenesis: an ultrastructural study of the late cytoplasmic phases. Arch. Virol. 98:51-64.
51. Severi, B., M. P. Landini, M. Musiani, and M. Zerbini. 1979. A study of the passage of human cytomegalovirus from the nucleus to the cytoplasm. Microbiologica 2:265-273.
52. Silva, M. C., Q. C. Yu, L. Enquist, and T. Shenk. 2003. Human cytomegalovirus UL99-encoded pp28 is required for the cytoplasmic envelopment of tegument-associated capsids. J. Virol. 77:10594-10605.
53. Smith, G. A., S. P. Gross, and L. W. Enquist. 2001. Herpesviruses use bidirectional fast-axonal transport to spread in sensory neurons. Proc. Natl. Acad. Sci. USA 98:3466-3470.
54. Smith, J. D., and E. De Harven. 1973. Herpes simplex virus and human cytomegalovirus replication in WI-38 cells 1. Sequence of viral replication. J. Virol. 12:919-930.
55. Smith, M. G. 1959. The salivary gland viruses of man and animals (cytomegalic inclusion disease). Prog. Med. Virol. 2:171-202.
56. Stackpole, C. W. 1969. Herpes-type virus of the frog renal adenocarcinoma. I. Virus development in tumor transplants maintained at low temperature. J. Virol. 4:75-93.
57. Tooze, J., M. Hollinshead, B. Reis, K. Radsak, and H. Kern. 1993. Progeny vaccinia and human cytomegalovirus particles utilize early endosomal cisternae for their envelopes. Eur. J. Cell Biol. 60:163-178.
58. Turcotte, S., J. Letellier, and R. Lippe. 2005. Herpes simplex virus type 1 capsids transit by the trans-Golgi network, where viral glycoproteins accumulate independently of capsid egress. J. Virol. 79:8847-8860.
59. Wright, H. T., Jr., F. H. Kasten, and R. M. McAllister. 1968. Human cytomegalovirus, observations of intracellular lesion development as revealed by phase contrast, time-lapse cinematography. Proc. Soc. Exp. Biol. Med. 127:1032-1036.
60. Yoshino, A., B. M. Bieler, D. C. Harper, D. A. Cowan, S. Sutterwala, D. M. Gay, N. B. Cole, J. M. McCaffery, and M. S. Marks. 2003. A role for GRIP domain proteins and/or their ligands in structure and function of the trans-Golgi network. J. Cell Sci. 116:4441-4454.