Ultrastructure of Kunjin virus-infected cells: Colocalization of NS1 and NS3 with double-stranded RNA, and of NS2B with NS3, in virus-induced membrane structures

Journal of Virology

Volumn 71, Issue 9, 1997, Pages 6650-6661

  Westaway, Edwin G ^a   Mackenzie, Jason M ^a   Kenney, Mark T ^a   Jones, Malcolm K ^b   Khromykh, Alexander A ^a  

^a ROYAL CHILDREN'S HOSPITAL   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA;

ANIMAL CELL; ARTICLE; CELLULAR DISTRIBUTION; FLAVIVIRUS; IMMUNOELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; IMMUNOGOLD STAINING; MEMBRANE VESICLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA ANALYSIS; RNA VIRUS INFECTION; VIRUS EXPRESSION;

EID: 0030846512     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.71.9.6650-6661.1997     Document Type: Article

References (60)

1. Adams, S. C., A. K. Broom, L. M. Sammels, A. C. Hartnett, M. J. Howard, R. J. Coelen, J. S. Mackenzie, and R. A. Hall. 1995. Glycosylation and antigenic variation among Kunjin virus isolates. Virology 206:49-56.
2. Arias, C. F., C. F. Preugschat, and J. H. Strauss. 1993. Dengue 2 virus NS2B and NS3 form a stable complex that can cleave NS3 within the helicase domain. Virology 193:888-899.
3. Bartholomeusz, A. I., and P. J. Wright. 1993. Synthesis of dengue virus RNA in vitro:initiation and the involvement of proteins NS3 and NS5. Arch. Virol. 128:111-121.
4. Bensch, K. G., and S. E. Malawista. 1969. Microtubular crystals in mammalian cells. J. Cell Biol. 40:98-107.
5. Bienz, K., D. Egger, M. Troxler, and L. Pasomontes. 1990. Structural organization of poliovirus RNA replication is mediated by viral proteins of the P2 genomic region. J. Virol. 64:1156-1163.
6. Bienz, K., D. Egger, T. Pfister, and M. Troxler. 1992. Structural and functional characterization of the poliovirus replication complex. J. Virol. 66:2740-2747.
7. Buckley, A., S. Gaidamovich, A. Turchinskaya, and E. A. Gould. 1992. Monoclonal antibodies identify the NS5 yellow fever virus non-structural protein in the nuclei of infected cells. J. Gen. Virol. 73:1125-1130.
8. Cahour, A., B. F. Falgout, and C.-J. Lai. 1992. Cleavage of the dengue virus polyprotein at the NS3/NS4A and NS4B/NS5 junction is mediated hy viral protease NS2B-NS3, whereas NS4A/NS4B may be processed by a cellular protease. J. Virol. 66:1535-1542.
9. Cauchi, M. R., E. A. Henchal, and P. J. Wright. 1991. The sensitivity of cell-associated dengue virus proteins and the detection of trypsin-resistant fragments of the nonstructural glycoprotein NS1. Virology 180:659-667.
10. Chambers, T. J., C. S. Hahn, R. Galler, and C. M. Rice. 1990. Flavivirus genome organization, expression, and replication. Annu. Rev. Microbiol. 44:649-688.
11. Chambers, T. J., A. Grakoui, and C. M. Rice. 1991. Processing of the yellow fever virus nonstructural potyprotein:a catulytically active NS3 proteinase domain and NS2B are required for cleavages at dibasic sites. J. Virol. 65: 6042-6050.
12. Chambers, T. J., A. Nestorowicz, S. M. Amberg, and C. M. Rice. 1993. Metagenesis of the yellow fever virus NS2B protein:eff'ects on proteolytic processing. NS2B-NS3 complex formation, and viral replication. J. Virol. 67:6797-6807.
13. Chu, P. W. G., and E. G. Westaway. 1985. Replication strategy of Kunjin virus:evidence for recycling role of replicative form RNA as template in semiconservative and asymmetric replication. Virology 140:68-79.
14. Chu, P. W. G., and E. G. Westaway. 1987. Characterization of Kunjin virus RNA-dependent RNA polymcrase:reinitiation of synthesis in vitro. Virology 157:330-337.
15. Chu, P. W. G., and E. G. Westaway. 1992. Molecular and ultrastructural analysis of heavy membrane fractions associated with the replication of Kunjin virus RNA. Arch. Virol. 125:177-191.
16. Chu, P. W. G., E. G. Westaway, and G. Coia. 1992. Comparison of centrifugation methods for molecular and morphological analysis of membranes associated with RNA replication of the flavivirus Kunjin. J. Virol. Methods 37:219-234.
17. Coia, G., M. D. Parker, G. Speight, M. E. Byrne, and E. G. Westaway. 1988. Nucleotide and complete amino acid sequences of Kunjin virus:definitive gene order and characteristics of the virus-specified proteins. J. Gen. Virol. 69:1-21.
18. Edward, Z., and T. Takegami. 1993. Localization and functions of Japanese encephalitis virus nonstructural proteins NS3 and NS5 for viral RNA synthesis in the infected cells. Microbiol. Immunol. 37:239-243.
19. Egger, D., L. Pasamontes, R. Bolten, V. Boyko, and K. Bienz. 1996. Reversible dissociation of the poliovirus replication complex:functions and interactions of its components in viral RNA synthesis. J. Virol. 70:8675-8683.
20. Falgout, B., M. Pethel, Y. M. Zhang, and C.-J. Lai. 1991. Both nonstructural proteins NS2B and NS3 are required for the proteolytc processing of dengue virus nonstructural proteins. J. Virol. 65:2467-2475.
21. Falgout, B. F., R. H. Miller, and C.-J. Lai. 1993. Deletion analysis of dengue virus type 4 nonstruciural protein NS2B:identification of a domain required for NS2B-NS3 protease activity. J. Virol. 67:2034-2042.
22. Froshauer, S., J. Kartenbeck, and A. Helenius. 1988. Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysomes. J. Cell Biol. 107:2075-2086.
23. Gould, E. A., A. Buckley, N. Cammack. A. D. T. Barrett, J. C. S. Clegg, R. Ishak, and M. G. R. Varma. 1985. Examination of the immunological relationships between flaviviruses using yellow fever virus monoclonal antibodies. J. Gen. Virol. 66:1369-1382.
24. Grun, J. B., and M. A. Brinton. 1987. Dissociation of NS5 from cell fractions containing West Nile virus-specific polymerase activity. J. Virol. 61:3641-3644.
25. Hobman, T. C., L. Woodward, and M. G. Farquhar. 1992. The rubella virus E1 glycoprotein is arrested in a novel post-ER, pre-Golgi compartment. J. Cell. Biol. 118:795-811.
26. Hong, S. S., and M. L. Ng. 1987. Involvement of microtubules in Kunjin virus replication. Brief report. Arch. Virol. 97:115-121.
27. Kapoor, M., L. Zhang, M. Ramachandra, J. Kusukawa, K. E. Ebner, and R. Padmanabhan. 1995. Association between NS3 and NS5 proteins of dengue virus type 2 in the putative RNA replicase is linked to differential phosphorylation of NS5. J. Biol. Chem. 270:19100-19106.
28. Khromykh, A. A., H. Meka, and E. G. Westaway. 1995. Preparation of rocombinant baculovirus hy transfection of a ligated cDNA fragment without prior plasmid amplification in E. coli. Biotechniques 18:357-360.
29. Khromykh, A. A., T. J. Harvey, M. Abedinia, and E. G. Westaway. 1996. Expression and purification of the seven nonstructural proteins of the flavivirus Kunjin in the E. coli and the baculovirus expression systems. J. Virol. Methods 61:47-58.
30. Koonin, E. V. 1993. Computer-assisted identification of a putative methyltransferase domain in NS5 protein of flaviviruses and lambda 2 protein of reovirus. J. Gen. Virol. 74:733-740.
31. Kuo, M.-D., C. Chin, S.-L. Hsu, J.-Y. Shiao, T.-M. Wang, and J.-H. Lin. 1996. Characterization of the NTPase activity of Japanese encephalitis virus NS3 protein. J. Gen. Virol. 77:2077-2084.
32. Leary, K., and C. D. Blair. 1980. Sequential events in the morphogenesis of Japanese encephalitis virus. J. Ultrastruct. Res. 72:123-129.
33. Lee, J.-Y., J. A. Marshall, and D. S. Bowden. 1994. Characterization of rubella virus replication complexes using antibodies to double-stranded RNA. Virology 200:307-312.
34. Lin, C., S. M. Amberg, T. J. Chambers, and C. M. Rice. 1993. Cleavage at a novel site in the NS4A region by the yellow fever virus NS2B-3 proteinase is a prerequisite for processing al the downstream 4A/4B signalase site. J. Virol. 67:2327-2335.
35. Mackenzie, J. M., M. K. Jones, and P. R. Young, 1996. Immunolocaliziition of the dengue virus nonstructural glycoprotein NS1 suggests a role in viral RNA replication. Virology 220:232-240.
36. Mackenzie, J. M., M. K. Jones, and P. R. Young. 1996. Improved membrane preservation of flavivirus-infected cells with cryosectioning. J. Virol. Methods 56:67-75.
37. Muylaert, I. R., T. J. Chambers, R. Galler, and C. M. Rice. 1996. Mutagenesis of the N-linked glycosylation sites of the yellow fever virus NS1 protein:effects on virus replication and mouse neurovirulence. Virology 222:159-168.
38. Muylaert, I. R., R. Caller, and C. M. Rice. 1997. Genetic analysis of the yellow fever NS1 protein:identification of a temperature-sensitive mutation which blocks RNA accumulation. J. Virol. 71:291-298.
39. Ng, M. L. 1987. Ultrastructural studies of Kunjin-virus infected Aedes albopictus cells. J. Gen. Virol. 68:577-582.
40. Ng, M. L., and L. C. Corner. 1989. Detection of some dengue-2 virus antigens in infected cells using immuno-microscopy. Arch. Virol. 104:197-208.
41. Ng, M. L., and S. S. Hong. 1989. Flavivirus infection:essential ultrastructural changes and association of Kunjin virus NS3 protein with microtubules. Arch. Virol. 106:103-120.
42. Ng, M. L., J. S. Pedersen, B. H. Toh, and E. G. Westaway. 1983. Immunofluorescent sites in Vero cells infected wilh the flavivirus Kunjin. Arch. Virol. 78:177-190.
43. Ng, M. L., W. K. P. Choo, and Y. L. Ho. 1992. Detection of flavivirus antigens in purified infected cell membranes. J. Virol. Methods 39:125-138.
44. Ng, M. L., F. M. Yeong, and S. H. Tan. 1994. Cryosubstitution technique reveals new morphology of flavivirus-induccd structures. J. Virol. Methods 49:305-314.
45. Preugschat, F., C. W. Yao, and J. H. Strauss. 1990. In vitro processing of dengue virus type 2 nonstructural proteins NS2A, NS2B, and NS3. J. Virol. 64:4364-4374.
46. Rice, C. M., E. M. Lenches, S. R. Eddy, S. J. Shin, R. L. Sheets, and J. H. Strauss. 1985. Nucleotide sequence of yellow fever virus:implications for flavivirus gene expression and evolution. Science 229:726-733.
47. Speight, G., and E. G. Westaway. 1989. Carboxy-terminal analysis of nine proteins specified by the flavivirus Kunjin:evidence that only the intracellular core protein is truncated. J. Gen. Virol. 70:2209-2214.
48. Speight, G., and E. G. Westaway. 1989. Positive identification of NS4A, the last of the hypothetical nonstructural proteins of flaviviruses. Virology 170:299-301.
49. Speight, G., G. Coia, M. D. Parker, and E. G. West away. 1988. Gene mapping und positive identification of the non-structural proteins NS2A, NS2B, NS3, NS4B and NS5 of the flavivirus Kunjin and their cleavage sites. J. Gen. Virol. 69:23-34.
50. Takegami, T., U, Sakamuro, and T. Furukawa. 1994. Japanese encephalitis virus nonstructural protein NS3 has RNA binding and ATPase activities. Virus Genes 9:105-112.
51. Troxler, M., D. Egger, T. Pfister, and K. Bienz. 1992. Intracellular localization of poliovirus RNA by in situ hybridization at the ultrastructural level using single-stranded riboprobes. Virology 191:687-697.
52. Warrener, P., J. K. Tamura, and M. S. Collett. 1993. RNA-stimulated NTPase activity associated wilh yellow fever virus NS3 protein expressed in bacteria. J. Virol. 67:989-996.
53. Wengler, G., and G. Wengler. 1991. The carboxy-terminal part of the NS3 protein of the West Nile flavivirus can he isolated as a soluble protein after proteolytic cleavage and represents an RNA-stimulated NTPase. Virology 184:707-715.
54. Wengler, G., and G. Wengler. 1993. The NS3 nonstructural protein of flavivirus contains an RNA triphosphatase activity. Virology 197:265-273.
55. Wengler, G., T. Nowak, and E. Castle. 1990. Description of a procedure which allows isolation of viral nonstructural proteins from BHK vertebrate cells infected with the West Nile flavivirus in a state which allows their direct chemical characterization. Virology 177:795-801.
56. Wengler, G., G. Czaya, P. M. Färber, and J. H. Hegemann. 1991. In vitro synthesis of West Nile virus proteins indicates that the amino-terminal segment of the NS3 protein contains the active centre of the protease which cleaves the viral polyprotein after multiple basic amino acids. J. Gen. Virol. 72:300-308.
57. Westaway, E. G. 1973. Proteins specified by group B togaviruses in mammalian cells during productive infections. Virology 51:454-465.
58. Westaway, E. G., and M. R. Goodman. 1987. Variation in distribution of the three flavivirus-specified glycoproteins detected by immunofluorescence in infected Vero cells. Arch. Virol. 94:215-228.
59. Westaway, E. G., A. A. Khromykh, M. T. Kenney, J. M. Mackenzie, and M. K. Jones. Proteins C and NS4B of the flavivirus Kunjin translocate independently into the nucleus. Virology, in press.
60. Wubbolts, R., M. Fernandez-Borja, L. Oomen, D. Venvoerd. H. Janssen, J. Calafat, A. Tulp, S. Dusseljee, and J. Neefjes. 1996. Direct vesicular transport of MHC class II molecules from lysosomal structures to the cell surface. J. Cell Biol. 135:611-622.