A strong endoplasmic reticulum retention signal in the stem-anchor region of envelope glycoprotein of dengue virus type 2 affects the production of virus-like particles

Virology

Volumn 374, Issue 2, 2008, Pages 338-350

  Hsieh, Szu Chia ^a   Liu, I Jung ^b,d   King, Chwan Chuen ^c   Chang, Gwong Jen ^e   Wang, Wei Kung ^a,b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d CARDINAL TIEN COLLEGE OF HEALTHCARE AND MANAGEMENT   (Taiwan)

^e NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

Dengue virus; Endoplasmic reticulum; Stem anchor region; Virus like particles

Indexed keywords

CD4 ANTIGEN; CYTOPLASM PROTEIN; ENDOGLYCOSIDASE H; ENVELOPE PROTEIN; GLYCOPROTEIN; GLYCOSIDASE; MEMBRANE PROTEIN; PROTEIN C;

ARTICLE; CELL FUNCTION; CELL SURFACE; CHIMERA; COMPARATIVE STUDY; DENGUE VIRUS; EMBRYO; ENDOPLASMIC RETICULUM; FLOW CYTOMETRY; HUMAN; HUMAN CELL; JAPANESE ENCEPHALITIS VIRUS; MOLECULAR DYNAMICS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VIRUS LIKE AGENT; VIRUS REPLICATION;

CELL LINE; DENGUE VIRUS; ENDOPLASMIC RETICULUM; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MANNOSYL-GLYCOPROTEIN ENDO-BETA-N-ACETYLGLUCOSAMINIDASE; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; VIRAL ENVELOPE PROTEINS; VIRION;

DENGUE VIRUS; DENGUE VIRUS TYPE 2; JAPANESE ENCEPHALITIS VIRUS;

EID: 43049109558     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2007.12.041     Document Type: Article

References (54)

1. Allison S.L., Stiasny K., Stadler K., Mandl C.W., and Heinz F.X. Mapping of functional elements in the stem-anchor region of tick-borne encephalitis virus envelope protein. E.J. Virol 73 (1999) 5605-5612
2. Bijlmakers M.J., Isobe-Nakamura M., Ruddock L.J., and Marsh M. Intrinsic signals in the unique domain target p56lck to the plasma membrane independently of CD4. J. Cell Biol 137 (1997) 1029-1040
3. Bray M., Men R., Tokimatsu I., and Lai C.J. Genetic determinants responsible for acquisition of dengue type 2 virus mouse neurovirulence. J. Virol. 72 (1998) 1647-1651
4. Chang G.J., Hunt A.R., and Davis B. A single intramuscular injection of recombinant plasmid DNA induces protective immunity and prevents Japanese encephalitis in mice. J. Virol 74 (2000) 4244-4252
5. Chang G.J., Hunt A.R., Holmes D.A., Springfield T., Chiueh T.S., Roehrig J.T., and Gubler D.J. Enhancing biosynthesis and secretion of premembrane and envelope proteins by the chimeric plasmid of dengue virus type 2 and Japanese encephalitis virus. Virology 306 (2003) 170-180
6. Chen C., and Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell Biol. 7 (1987) 2745-2752
7. Cocquerel L., Meunier J.C., Pillez A., Wychowski C., and Dubuisson J. A retention signal necessary and sufficient for endoplasmic reticulum localization maps to the transmembrane domain of hepatitis C virus glycoprotein E2. J. Virol 72 (1998) 2183-2191
8. Cocquerel L., Duvet S., Meunier J.C., Pillez A., Cacan R., Wychowski C., and Dubuisson J. The transmembrane domain of hepatitis C virus glycoprotein E1 is a signal for static retention in the endoplasmic reticulum. J. Virol 73 (1999) 2641-2649
9. Cocquerel L., Wychowski C., Minner F., Penin F., and Dubuisson J. Charged residues in the transmembrane domains of hepatitis C virus glycoproteins play a major role in the processing, subcellular localization, and assembly of these envelope proteins. J. Virol 74 (2000) 3623-3633
10. Davis B.S., Chang G.J., Cropp B., Roehrig J.T., Martin D.A., Mitchell C.J., Bowen R., and Bunning M.L. West Nile virus recombinant DNA vaccine protects mouse and horse from virus challenge and expresses in vitro a noninfectious recombinant antigen that can be used in enzyme-linked immunosorbent assays. J.Virol 75 (2001) 4040-4047
11. Duvet S., Cocquerel L., Pillez A., Cacan R., Verbert A., Moradpour D., Wychowski C., and Dubuisson J. Hepatitis C virus glycoprotein complex localization in the endoplasmic reticulum involves a determinant for retention and not retrieval. J. Biol. Chem 273 (1998) 32088-32095
12. Ferlenghi I., Clarke M., Ruttan T., Allison S.L., Schalich J., Heinz F.X., Harrison S.C., Rey F.A., and Fuller S.D. Molecular organization of a recombinant subviral particle from tick-borne encephalitis virus. Mol. Cell 7 (2001) 593-602
13. Flint M., and McKeating J.A. The C-terminal region of the hepatitis C virus E1 glycoprotein confers localization within the endoplasmic reticulum. J. Gen. Virol. 80 Pt 8 (1999) 1943-1947
14. Green S., and Rothman A. Immunopathological mechanisms in dengue and dengue hemorrhagic fever. Curr. Opin. Infect. Dis 19 (2006) 429-436
15. Gubler D.J. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol 10 (2002) 100-103
16. Guzman M.G., and Kouri G. Dengue: an update. Lancet Infect.Dis 2 (2002) 33-42
17. Halstead S.B. Pathogenesis of dengue: challenges to molecular biology. Science 239 (1988) 476-481
18. Hanna S.L., Pierson T.C., Sanchez M.D., Ahmed A.A., Murtadha M.M., and Doms R.W. N-linked glycosylation of West Nile virus envelope proteins influences particle assembly and infectivity. J. Virol 79 (2005) 13262-13274
19. Henchal E.A., Gentry M.K., McCown J.M., and Brandt W.E. Dengue virus-specific and flavivirus group determinants identified with monoclonal antibodies by indirect immunofluorescence. Am. J. Trop. Med. Hyg 31 (1982) 830-836
20. Hunt A.R., Cropp C.B., and Chang G.J. A recombinant particulate antigen of Japanese encephalitis virus produced in stably-transformed cells is an effective noninfectious antigen and subunit immunogen. J. Virol. Methods 97 (2001) 133-149
21. Irie K., Mohan P.M., Sasaguri Y., Putnak R., and Padmanabhan R. Sequence analysis of cloned dengue virus type 2 genome New Guinea-C strain. Gene 75 (1989) 197-211
22. Ishak R., Tovey D.G., and Howard C.R. Morphogenesis of yellow fever virus 17D in infected cell cultures. J. Gen. Virol. 69 Pt 2 (1988) 325-335
23. Konishi E., and Fujii A. Dengue type 2 virus subviral extracellular particles produced by a stably transfected mammalian cell line and their evaluation for a subunit vaccine. Vaccine 20 (2002) 1058-1067
24. Kroeger M.A., and McMinn P.C. Murray Valley encephalitis virus recombinant subviral particles protect mice from lethal challenge with virulent wild-type virus. Arch. Virol 147 (2002) 1155-1172
25. Kummerer B.M., and Rice C.M. Mutations in the yellow fever virus nonstructural protein NS2A selectively block production of infectious particles. J. Virol 76 (2002) 4773-4784
26. Lin S.R., Hsieh S.C., Yueh Y.Y., Lin T.H., Chao D.Y., Chen W.J., King C.C., and Wang W.K. Study of sequence variation of dengue type 3 virus in naturally infected mosquitoes and human hosts: implications for transmission and evolution. J. Virol 78 (2004) 12717-12721
27. Lindenbach B.D., and Rice C.M. Flaviviridae: the viruses and their replication. In: Knipe D.M., Howley P.M., and Griffin D.E. (Eds). Fields Virology (2001), Philadelphia, Lippincott William and Wilkins 991-1041
28. Liu I.J., Chen P.J., Yeh S.H., Chiang Y.P., Huang L.M., Chang M.F., Chen S.Y., Yang P.C., Chang S.C., and Wang W.K. Immunofluorescence assay for detection of the nucleocapsid antigen of the severe acute respiratory syndrome SARS-associated coronavirus in cells derived from throat wash samples of patients with SARS. J. Clin. Microbiol. 43 (2005) 2444-2448
29. Liu W.J., Chen H.B., and Khromykh A.A. Molecular and functional analyses of Kunjin virus infectious cDNA clones demonstrate the essential roles for NS2A in virus assembly and for a nonconservative residue in NS3 in RNA replication. J. Virol 77 (2003) 7804-7813
30. Liu W.J., Sedlak P.L., Kondratieva N., and Khromykh A.A. Complementation analysis of the flavivirus Kunjin NS3 and NS5 proteins defines the minimal regions essential for formation of a replication complex and shows a requirement of NS3 in cis for virus assembly. J. Virol 76 (2002) 10766-10775
31. Lorenz I.C., Kartenbeck J., Mezzacasa A., Allison S.L., Heinz F.X., and Helenius A. Intracellular assembly and secretion of recombinant subviral particles from tick-borne encephalitis virus. J. Virol 77 (2003) 4370-4382
32. Mackenzie J.M., and Westaway E.G. Assembly and maturation of the flavivirus Kunjin virus appear to occur in the rough endoplasmic reticulum and along the secretory pathway, respectively. J. Virol 75 (2001) 10787-10799
33. Maddon P.J., Dalgleish A.G., McDougal J.S., Clapham P.R., Weiss R.A., and Axel R. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell 47 (1986) 333-348
34. Michelsen K., Yuan H., and Schwappach B. Hide and run. Arginine-based endoplasmic-reticulum-sorting motifs in the assembly of heteromultimeric membrane proteins. . EMBO. Rep 6 (2005) 717-722
35. Modis Y., Ogata S., Clements D., and Harrison S.C. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 6986-6991
36. Modis Y., Ogata S., Clements D., and Harrison S.C. Structure of the dengue virus envelope protein after membrane fusion. Nature 427 (2004) 313-319
37. Mukhopadhyay S., Kuhn R.J., and Rossmann M.G. A structural perspective of the flavivirus life cycle. Nat.Rev.Microbiol 3 (2005) 13-22
38. Nilsson T., and Warren G. Retention and retrieval in the endoplasmic reticulum and the Golgi apparatus. Curr. Opin. Cell Biol. 6 (1994) 517-521
39. Op De Beeck A., Molenkamp R., Caron M., Ben Younes A., Bredenbeek P., and Dubuisson J. Role of the transmembrane domains of prM and E proteins in the formation of yellow fever virus envelope. J. Virol 77 (2003) 813-820
40. Op De Beeck A., Rouille Y., Caron M., Duvet S., and Dubuisson J. The transmembrane domains of the prM and E proteins of yellow fever virus are endoplasmic reticulum localization signals. J. Virol 78 (2004) 12591-12602
41. Pelham H.R. Sorting and retrieval between the endoplasmic reticulum and Golgi apparatus. Curr.Opin.Cell Biol 7 (1995) 530-535
42. Purdy D.E., and Chang G.J. Secretion of noninfectious dengue virus-like particles and identification of amino acids in the stem region involved in intracellular retention of envelope protein. Virology 333 (2005) 239-250
43. Purdy D.E., Noga A.J., and Chang G.J. Noninfectious recombinant antigen for detection of St. Louis encephalitis virus-specific antibodies in serum by enzyme-linked immunosorbent assay. . J. Clin. Microbiol 42 (2004) 4709-4717
44. Rey F.A., Heinz F.X., Mandl C., Kunz C., and Harrison S.C. The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 375 (1995) 291-298
45. Schalich J., Allison S.L., Stiasny K., Mandl C.W., Kunz C., and Heinz F.X. Recombinant subviral particles from tick-borne encephalitis virus are fusogenic and provide a model system for studying flavivirus envelope glycoprotein functions. J.Virol 70 (1996) 4549-4557
46. Shin J., Dunbrack Jr. R.L., Lee S., and Strominger J.L. Signals for retention of transmembrane proteins in the endoplasmic reticulum studied with CD4 truncation mutants. Proc. Natl. Acad. Sci.U. S. A. 88 (1991) 1918-1922
47. Stadler K., Allison S.L., Schalich J., and Heinz F.X. Proteolytic activation of tick-borne encephalitis virus by furin. J.Virol 71 (1997) 8475-8481
48. Stiasny K., Allison S.L., Marchler-Bauer A., Kunz C., and Heinz F.X. Structural requirements for low-pH-induced rearrangements in the envelope glycoprotein of tick-borne encephalitis virus. J.Virol 70 (1996) 8142-8147
49. Szczesna-Skorupa E., and Kemper B. Endoplasmic reticulum retention determinants in the transmembrane and linker domains of cytochrome P450 2C1. J.Biol.Chem 275 (2000) 19409-19415
50. Wang J.J., Liao C.L., Chiou Y.W., Chiou C.T., Huang Y.L., and Chen L.K. Ultrastructure and localization of E proteins in cultured neuron cells infected with Japanese encephalitis virus. Virology 238 (1997) 30-39
51. Wang W.K., Chen H.L., Yang C.F., Hsieh S.C., Juan C.C., Chang S.M., Yu C.C., Lin L.H., Huang J.H., and King C.C. Slower rates of clearance of viral load and virus-containing immune complexes in patients with dengue hemorrhagic fever. Clin.Infect.Dis 43 (2006) 1023-1030
52. Xu Z., Bruss V., and Yen T.S. Formation of intracellular particles by hepatitis B virus large surface protein. J.Virol. 71 (1997) 5487-5494
53. Yang M., Ellenberg J., Bonifacino J.S., and Weissman A.M. The transmembrane domain of a carboxyl-terminal anchored protein determines localization to the endoplasmic reticulum. J.Biol.Chem 272 (1997) 1970-1975
54. Zhang W., Chipman P.R., Corver J., Johnson P.R., Zhang Y., Mukhopadhyay S., Baker T.S., Strauss J.H., Rossmann M.G., and Kuhn R.J. Visualization of membrane protein domains by cryo-electron microscopy of dengue virus. Nat.Struct.Biol 10 (2003) 907-912