Characterization of the early events in dengue virus cell entry by biochemical assays and single-virus tracking

Journal of Virology

Volumn 81, Issue 21, 2007, Pages 12019-12028

  Van Der Schaar, Hilde M ^a   Rust, Michael J ^c,e   Waarts, Barry Lee ^a   Van Der Ende Metselaar, Heidi ^a   Kuhn, Richard J ^b   Wilschut, Jan ^a   Zhuang, Xiaowei ^c,d,e   Smit, Jolanda M ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b PURDUE UNIVERSITY   (United States)

^c HARVARD UNIVERSITY   (United States)

^d HARVARD UNIVERSITY   (United States)

^e HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,1' DIOCTADECYL 3,3,3',3' TETRAMETHYLINDOCARBOCYANINE; 4 CHLOROBENZENESULFONATE; AMMONIUM CHLORIDE; CHLOROBENZOIC ACID DERIVATIVE; SULFONIC ACID DERIVATIVE; UNCLASSIFIED DRUG; VIRUS RECEPTOR;

ACIDITY; ARTICLE; BIOASSAY; CELL STRAIN BHK; DENGUE VIRUS; ENDOSOME; FLUORESCENCE MICROSCOPY; MEMBRANE FUSION; MOSQUITO; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; VIRUS CELL INTERACTION; VIRUS CHARACTERIZATION; VIRUS ENVELOPE; VIRUS INFECTIVITY; VIRUS PARTICLE;

AMMONIUM CHLORIDE; ANIMALS; BIOCHEMISTRY; CELL LINE; CELL MEMBRANE; CRICETINAE; DENGUE; DENGUE VIRUS; KINETICS; MEMBRANE FUSION; MICROSCOPY, FLUORESCENCE; POLYMERASE CHAIN REACTION; VIROLOGY; VIRUS DISEASES; VIRUS INTERNALIZATION;

DENGUE VIRUS; DENGUE VIRUS TYPE 2;

EID: 35448960873     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00300-07     Document Type: Article

References (51)

1. Allison, S. L., J. Schalich, K. Stiasny, C. W. Mandl, and F. X. Heinz. 2001. Mutational evidence for an internal fusion peptide in flavivirus envelope protein E. J. Virol. 75:4268-4275.
2. Allison, S. L., J. Schalich, K. Stiasny, C. W. Mandl, C. Kunz, and F. X. Heinz. 1995. Oligomeric rearrangement of tick-borne encephalitis virus envelope proteins induced by an acidic pH. J. Virol. 69:695-700.
3. Anderson, R., S. Wang, C. Osiowy, and A. C. Issekutz. 1997. Activation of endothelial cells via antibody-enhanced dengue virus infection of peripheral blood monocytes. J. Virol. 71:4226-4232.
4. Bae, H. G., A. Nitsche, A. Teichmann, S. S. Biel, and M. Niedrig. 2003. Detection of yellow fever virus: a comparison of quantitative real-time PCR and plaque assay. J. Virol. Methods 110:185-191.
5. Chen, Y., T. Maguire, R. E. Hileman, J. R. Fromm, J. D. Esko, R. J. Linhardt, and R. M. Marks. 1997. Dengue virus infectivity depends on envelope protein binding to target cell heparan sulfate. Nat. Med. 3:866-871.
6. Chen, Y., T. Maguire, and R. M. Marks. 1996. Demonstration of binding of dengue virus envelope protein to target cells. J. Virol. 70:8765-8772.
7. Crill, W. D., and J. T. Roehrig. 2001. Monoclonal antibodies that bind to domain III of dengue virus E glycoprotein are the most efficient blockers of virus adsorption to Vero cells. J. Virol. 75:7769-7773.
8. Diamond, M. S., D. Edgil, T. G. Roberts, B. Lu, and E. Harris. 2000. Infection of human cells by dengue virus is modulated by different cell types and viral strains. J. Virol. 74:7814-7823.
9. Ferlenghi, I., M. Clarke, T. Ruttan, S. L. Allison, J. Schalich, F. X. Heinz, S. C. Harrison, F. A. Rey, and S. D. Fuller. 2001. Molecular organization of a recombinant subviral particle from tick-borne encephalitis virus. Mol. Cell 7:593-602.
10. Germi, R., J. M. Crance, D. Garin, J. Guimet, H. Lortat-Jacob, R. W. Ruigrok, J. P. Zarski, and E. Drouet. 2002. Heparan sulfate-mediated binding of infectious dengue virus type 2 and yellow fever virus. Virology 292:162-168.
11. Gollins, S. W., and J. S. Porterfield. 1984. Flavivirus infection enhancement in macrophages: radioactive and biological studies on the effect of antibody on viral fate. J. Gen. Virol. 65:1261-1272.
12. Hahn, Y. S., R. Galler, T. Hunkapiller, J. M. Dalrymple, J. H. Strauss, and E. G. Strauss. 1988. Nucleotide sequence of dengue 2 RNA and comparison of the encoded proteins with those of other flaviviruses. Virology 162:167-180.
13. He, R. T., B. L. Innis, A. Nisalak, W. Usawattanakul, S. Wang, S. Kalayanarooj, and R. Anderson. 1995. Antibodies that block virus attachment to Vero cells are a major component of the human neutralizing antibody response against dengue virus type 2. J. Med. Virol. 45:451-461.
14. Heinz, F. X., K. Stiasny, and S. L. Allison. 2004. The entry machinery of flaviviruses. Arch. Virol. Suppl. 2004:133-137.
15. Heinz, F. X., K. Stiasny, G. Puschner-Auer, H. Holzmann, S. L. Allison, C. W. Mandl, and C. Kunz. 1994. Structural changes and functional control of the tick-borne encephalitis virus glycoprotein E by the heterodimeric association with protein prM. Virology 198:109-117.
16. Henchal, E. A., J. M. McCown, D. S. Burke, M. C. Seguin, and W. E. Brandt. 1985. Epitopic analysis of antigenic determinants on the surface of dengue-2 virions using monoclonal antibodies. Am. J. Trop. Med. Hyg. 34:162-169.
17. Hilgard, P., and R. Stockert. 2000. Heparan sulfate proteoglycans initiate dengue virus infection of hepatocytes. Hepatology 32:1069-1077.
18. Huang, K. J., Y. C. Yang, Y. S. Lin, J. H. Huang, H. S. Liu, T. M. Yeh, S. H. Chen, C. C. Liu, and H. Y. Lei. 2006. The dual-specific binding of dengue virus and target cells for the antibody-dependent enhancement of dengue virus infection. J. Immunol. 176:2825-2832.
19. Ishak, R., D. G. Tovey, and C. R. Howard. 1988. Morphogenesis of yellow fever virus 17D in infected cell cultures. J. Gen. Virol. 69:325-335.
20. Keelapang, P., R. Sriburi, S. Supasa, N. Panyadee, A. Songjaeng, A. Jairungsri, C. Puttikhunt, W. Kasinrerk, P. Malasit, and N. Sittisombut. 2004. Alterations of pr-M cleavage and virus export in pr-M junction chimeric dengue viruses. J. Virol. 78:2367-2381.
21. Kuhn, R. J., W. Zhang, M. G. Rossmann, S. V. Pletnev, J. Corver, E. Lenches, C. T. Jones, S. Mukhopadhyay, P. R. Chipman, E. G. Strauss, T. S. Baker, and J. H. Strauss. 2002. Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108:717-725.
22. Lakadamyali, M., M. J. Rust, H. P. Babcock, and X. Zhuang. 2003. Visualizing infection of individual influenza viruses. Proc. Natl. Acad. Sci. USA 100:9280-9285.
23. Lakadamyali, M., M. J. Rust, and X. Zhuang. 2006. Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes. Cell 124:997-1009.
24. Lambeth, C. R., L. J. White, R. E. Johnston, and A. M. de Silva. 2005. Flow cytometry-based assay for titrating dengue virus. J. Clin. Microbiol. 43:3267-3272.
25. Lee, E., M. Pavy, N. Young, C. Freeman, and M. Lobigs. 2006. Antiviral effect of the heparan sulfate mimetic, PI-88, against dengue and encephalitic flaviviruses. Antivir. Res. 69:31-38.
26. Lindenbach, D., and C. M. Rice. 2001. Flaviviridae: the viruses and their replication, p. 991-1041. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, and S. E. Straus (ed.), Fields virology, 4th ed. Lippincott Williams and Wilkins, Philadelphia, PA.
27. Lorenz, I. C., S. L. Allison, F. X. Heinz, and A. Helenius. 2002. Folding and dimerization of tick-borne encephalitis virus envelope proteins prM and E in the endoplasmic reticulum. J. Virol. 76:5480-5491.
28. Lozach, P. Y., L. Burleigh, I. Staropoli, E. Navarro-Sanchez, J. Harriague, J. L. Virelizier, F. A. Rey, P. Despres, F. Arenzana-Seisdedos, and A. Amara. 2005. Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin (DC-SIGN)-mediated enhancement of dengue virus infection is independent of DC-SIGN internalization signals. J. Biol. Chem. 280:23698-23708.
29. Marsh, M., and R. Bron. 1997. SFV infection in CHO cells: cell-type specific restrictions to productive virus entry at the cell surface. J. Cell Sci. 110:95-103.
30. Modis, Y., S. Ogata, D. Clements, and S. C. Harrison. 2004. Structure of the dengue virus envelope protein after membrane fusion. Nature 427:313-319.
31. Mukhopadhyay, S., R. J. Kuhn, and M. G. Rossmann. 2005. A structural perspective of the flavivirus life cycle. Nat. Rev. Microbiol. 3:13-22.
32. Murray, J. M., J. G. Aaskov, and P. J. Wright. 1993. Processing of the dengue virus type 2 proteins prM and C-prM. J. Gen. Virol. 74:175-182.
33. Navarro-Sanchez, E., R. Altmeyer, A. Amara, O. Schwartz, F. Fieschi, J. L. Virelizier, F. Arenzana-Seisdedos, and P. Despres. 2003. Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses. EMBO Rep. 4:723-728.
34. Peterson, G. L. 1977. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83:346-356.
35. Pokidysheva, E., Y. Zhang, A. J. Battisti, C. M. Bator-Kelly, P. R. Chipman, C. Xiao, G. G. Gregorio, W. A. Hendrickson, R. J. Kuhn, and M. G. Rossmann. 2006. Cryo-EM reconstruction of dengue virus in complex with the carbohydrate recognition domain of DC-SIGN. Cell 124:485-493.
36. Putnak, R., D. A. Barvir, J. M. Burrous, D. R. Dubois, V. M. D'Andrea, C. H. Hoke, J. C. Sadoff, and K. H. Eckels. 1996. Development of a purified, inactivated, dengue-2 virus vaccine prototype in Vero cells: immunogenicity and protection in mice and rhesus monkeys. J. Infect. Dis. 174:1176-1184.
37. Randolph, V. B., and V. Stellar. 1990. Low pH-induced cell fusion in flavivirus-infected Aedes albopictus cell cultures. J. Gen. Virol. 71:1845-1850.
38. Randolph, V. B., G. Winkler, and V. Stollar. 1990. Acidotropic amines inhibit proteolytic processing of flavivirus prM protein. Virology 174:450-458.
39. Rey, F. A., F. X. Heinz, C. Mandl, C. Kunz, and S. C. Harrison. 1995. The envelope glycoprotein from tick-borne encephalitis virus at 2 Å resolution. Nature 375:291-298.
40. Richardson, J., A. Molina-Cruz, M. I. Salazar, and W. Black. 2006. Quantitative analysis of dengue-2 virus RNA during the extrinsic incubation period in individual Aedes aegypti. Am. J. Trop. Med. Hyg. 74:132-141.
41. Roche, R. R., M. Alvarez, M. G. Guzman, L. Morier, and G. Kouri. 2000. Comparison of rapid centrifugation assay with conventional tissue culture method for isolation of dengue 2 virus in C6/36-HT cells. J. Clin. Microbiol. 38:3508-3510.
42. Russell, P. K., W. E. Brandt, and J. M. Dalrymple. 1980. Chemical and antigenic structure of flaviviruses, p. 503-529. In R. W. Schlesinger (ed.), The togaviruses: biology, structure, replication. Academic Press, New York, NY.
43. Sieczkarski, S. B., and G. R. Whittaker. 2002. Dissecting virus entry via endocytosis. J. Gen. Virol. 83:1535-1545.
44. Smit, J. M., R. Bittman, and J. Wilschut. 1999. Low-pH-dependent fusion of Sindbis virus with receptor-free cholesterol- and sphingolipid- containing liposomes. J. Virol. 73:8476-8484.
45. Stegmann, T., H. W. Morselt, J. Scholma, and J. Wilschut. 1987. Fusion of influenza virus in an intracellular acidic compartment measured by fluorescence dequenching. Biochim. Biophys. Acta 904:165-170.
46. Tassaneetrithep, B., T. H. Burgess, A. Granelli-Piperno, C. Trumpfheller, J. Finke, W. Sun, M. A. Eller, K. Pattanapanyasat, S. Sarasombath, D. L. Birx, R. M. Steinman, S. Schlesinger, and M. A. Marovich. 2003. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197:823-829.
47. Thomas, G. 2002. Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell. Biol. 3:753-766.
48. Thomas, J. A., D. E. Ott, and R. J. Gorelick. 2007. Efficiency of human immunodeficiency virus type 1 postentry infection processes: evidence against disproportionate numbers of defective virions. J. Virol. 81:4367-4370.
49. Vonderheit, A., and A. Helenius. 2005. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLOS Biol. 3:e233.
50. Wang, S., R. He, and R. Anderson. 1999. PrM- and cell-binding domains of the dengue virus E protein. J. Virol. 73:2547-2551.
51. Zhang, Y., J. Corver, P. R. Chipman, W. Zhang, S. V. Pletnev, D. Sedlak, T. S. Baker, J. H. Strauss, R. J. Kuhn, and M. G. Rossmann. 2003. Structures of immature flavivirus particles. EMBO J. 22:2604-2613.