1887

Abstract

Mosquito midgut epithelial cells (MEC) play a major role in determining whether an arbovirus can successfully infect and be transmitted by mosquitoes. The Sindbis virus (SINV) strain TR339 efficiently infects MEC but the SINV strain TE/5′2J poorly infects MEC. SINV determinants for MEC infection have been localized to the E2 glycoprotein. The E2 amino acid sequences of TR339 and TE/5′2J differ at two sites, E2-55 and E2-70. We have altered the TE/5′2J virus genome by site-directed mutagenesis to contain two TR339 residues, E2-55 H→Q (histidine to glutamine) and E2-70 K→E (lysine to glutamic acid). We have characterized the growth patterns of derived viruses in cell culture and determined the midgut infection rate (MIR) in mosquitoes. Our results clearly show that the E2-55 H→Q and the E2-70 K→E mutations in the TE/5′2J virus increase MIR both independently and in combination. TE/5′2J virus containing both TR339 E2 residues had MIRs similar to the parental TR339 virus. In addition, SINV propagated in a mammalian cell line had a significantly lower midgut 50 % infectious dose than virus propagated in a mosquito cell line.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.82577-0
2007-05-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/88/5/1545.html?itemId=/content/journal/jgv/10.1099/vir.0.82577-0&mimeType=html&fmt=ahah

References

  1. Agapov E. V., Razumov I. A., Frolov I. V., Kolykhalov A. A., Netesov S. V., Loktev V. B. 1994; Localization of four antigenic sites involved in Venezuelan equine encephalomyelitis virus protection. Arch Virol 139:173–181 [CrossRef]
    [Google Scholar]
  2. Altmann F., Staudacher E., Wilson I. B., Marz L. 1999; Insect cells as hosts for the expression of recombinant glycoproteins. Glycoconj J 16:109–123 [CrossRef]
    [Google Scholar]
  3. Anthony R. P., Brown D. T. 1991; Protein–protein interactions in an alphavirus membrane. J Virol 65:1187–1194
    [Google Scholar]
  4. Bennett K. E., Olson K. E., Munoz M. de L., Fernandez-Salas I., Farfan-Ale J. A., Higgs S., Black W. C. IV, Beaty B. J. 2002; Variation in vector competence for dengue 2 virus among 24 collections of Aedes aegypti from Mexico and the United States. Am J Trop Med Hyg 67:85–92
    [Google Scholar]
  5. Black W. C. IV, Bennett K. E., Gorrochotegui-Escalante N., Barillas-Mury C. V., Fernandez-Salas I., de Lourdes Munoz M., Farfan-Ale J. A., Olson K. E., Beaty B. J. 2002; Flavivirus susceptibility in Aedes aegypti . Arch Med Res 33:379–388 [CrossRef]
    [Google Scholar]
  6. Brault A. C., Powers A. M., Weaver S. C. 2002; Vector infection determinants of Venezuelan equine encephalitis virus reside within the E2 envelope glycoprotein. J Virol 76:6387–6392 [CrossRef]
    [Google Scholar]
  7. Brault A. C., Powers A. M., Ortiz D., Estrada-Franco J. G., Navarro-Lopez R., Weaver S. C. 2004; Venezuelan equine encephalitis emergence: enhanced vector infection from a single amino acid substitution in the envelope glycoprotein. Proc Natl Acad Sci U S A 101:11344–11349 [CrossRef]
    [Google Scholar]
  8. Bretscher M. S., Munro S. 1993; Cholesterol and the Golgi apparatus. Science 261:1280–1281 [CrossRef]
    [Google Scholar]
  9. Byrnes A. P., Griffin D. E. 1998; Binding of Sindbis virus to cell surface heparan sulfate. J Virol 72:7349–7356
    [Google Scholar]
  10. Byrnes A. P., Griffin D. E. 2000; Large-plaque mutants of Sindbis virus show reduced binding to heparan sulfate, heightened viremia, and slower clearance from the circulation. J Virol 74:644–651 [CrossRef]
    [Google Scholar]
  11. Clayton R. B. 1964; The utilization of sterols by insects. J Lipid Res 15:3–19
    [Google Scholar]
  12. Davis N. L., Pence D. F., Meyer W. J., Schmaljohn A. L., Johnston R. E. 1987; Alternative forms of a strain-specific neutralizing antigenic site on the Sindbis virus E2 glycoprotein. Virology 161:101–108 [CrossRef]
    [Google Scholar]
  13. Doherty R. L., Carley J. G., Filippich C., Kay B. H., Gorman B. M., Rajapaksa N. 1977; Isolation of Sindbis (alphavirus) and Leanyer viruses from mosquitoes collected in the Northern Territory of Australia, 1974. Aust J Exp Biol Med Sci 55:485–489 [CrossRef]
    [Google Scholar]
  14. Finn R. D., Mistry J., Schuster-Bockler B., Griffiths-Jones S., Hollich V., Lassmann T., Moxon S., Marshall M., Khanna A. other authors 2006; Pfam: clans, web tools and services. Nucleic Acids Res 34:D247–D251 [CrossRef]
    [Google Scholar]
  15. Hahn C. S., Hahn Y. S., Braciale T. J., Rice C. M. 1992; Infectious Sindbis virus transient expression vectors for studying antigen processing and presentation. Proc Natl Acad Sci U S A 89:2679–2683 [CrossRef]
    [Google Scholar]
  16. Johnson B. J., Brubaker J. R., Roehrig J. T., Trent D. W. 1990; Variants of Venezuelan equine encephalitis virus that resist neutralization define a domain of the E2 glycoprotein. Virology 177:676–683 [CrossRef]
    [Google Scholar]
  17. Karlsson K., Marklund S. L. 1988; Plasma clearance of human extracellular-superoxide dismutase C in rabbits. J Clin Invest 82:762–766 [CrossRef]
    [Google Scholar]
  18. Karlsson K., Sandstrom J., Edlund A., Marklund S. L. 1994; Turnover of extracellular-superoxide dismutase in tissues. Lab Invest 70:705–710
    [Google Scholar]
  19. Klimstra W. B., Ryman K. D., Johnston R. E. 1998; Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J Virol 72:7357–7366
    [Google Scholar]
  20. Lee H., Brown D. T. 1994; Mutations in an exposed domain of Sindbis virus capsid protein result in the production of noninfectious virions and morphological variants. Virology 202:390–400 [CrossRef]
    [Google Scholar]
  21. Lee P., Knight R., Smit J. M., Wilschut J., Griffin D. E. 2002; A single mutation in the E2 glycoprotein important for neurovirulence influences binding of Sindbis virus to neuroblastoma cells. J Virol 76:6302–6310 [CrossRef]
    [Google Scholar]
  22. Levine B., Griffin D. E. 1993; Molecular analysis of neurovirulent strains of Sindbis virus that evolve during persistent infection of scid mice. J Virol 67:6872–6875
    [Google Scholar]
  23. Li M. L., Liao H. J., Simon L. D., Stollar V. 1999; An amino acid change in the exodomain of the E2 protein of Sindbis virus, which impairs the release of virus from chicken cells but not from mosquito cells. Virology 264:187–194 [CrossRef]
    [Google Scholar]
  24. Lu Y. E., Cassese T., Kielian M. 1999; The cholesterol requirement for Sindbis virus entry and exit and characterization of a spike protein region involved in cholesterol dependence. J Virol 73:4272–4278
    [Google Scholar]
  25. Lustig S., Jackson A. C., Hahn C. S., Griffin D. E., Strauss E. G., Strauss J. H. 1988; Molecular basis of Sindbis virus neurovirulence in mice. J Virol 62:2329–2336
    [Google Scholar]
  26. Luukkonen A., Brummer-Korvenkontio M., Renkonen O. 1973; Lipids of cultured mosquito cells ( Aedes albopictus ). Comparison with cultured mammalian fibroblasts (BHK 21 cells). Biochim Biophys Acta 326:256–261 [CrossRef]
    [Google Scholar]
  27. Marchal I., Jarvis D. L., Cacan R., Verbert A. 2001; Glycoproteins from insect cells: sialylated or not?. Biol Chem 382:151–159
    [Google Scholar]
  28. Marquardt M. T., Phalen T., Kielian M. 1993; Cholesterol is required in the exit pathway of Semliki Forest virus. J Cell Biol 123:57–65 [CrossRef]
    [Google Scholar]
  29. McKnight K. L., Simpson D. A., Lin S. C., Knott T. A., Polo J. M., Pence D. F., Johannsen D. B., Heidner H. W., Davis N. L., Johnston R. E. 1996; Deduced consensus sequence of Sindbis virus strain AR339: mutations contained in laboratory strains which affect cell culture and in vivo phenotypes. J Virol 70:1981–1989
    [Google Scholar]
  30. Mendoza Q. P., Stanley J., Griffin D. E. 1988; Monoclonal antibodies to the E1 and E2 glycoproteins of Sindbis virus: definition of epitopes and efficiency of protection from fatal encephalitis. J Gen Virol 69:3015–3022 [CrossRef]
    [Google Scholar]
  31. Miller B. R., Mitchell C. J. 1986; Passage of yellow fever virus: its effect on infection and transmission rates in Aedes aegypti . Am J Trop Med Hyg 35:1302–1309
    [Google Scholar]
  32. Myles K. M., Pierro D. J., Olson K. E. 2003; Deletions in the putative cell receptor-binding domain of Sindbis virus strain MRE16 E2 glycoprotein reduce midgut infectivity in Aedes aegypti . J Virol 77:8872–8881 [CrossRef]
    [Google Scholar]
  33. Myles K. M., Pierro D. J., Olson K. E. 2004; Comparison of the transmission potential of two genetically distinct Sindbis viruses after oral infection of Aedes aegypti (Diptera: Culicidae). J Med Entomol 41:95–106 [CrossRef]
    [Google Scholar]
  34. Paredes A. M., Ferreira D., Horton M., Saad A., Tsuruta H., Johnston R., Klimstra W., Ryman K., Hernandez R. other authors 2004; Conformational changes in Sindbis virions resulting from exposure to low pH and interactions with cells suggest that cell penetration may occur at the cell surface in the absence of membrane fusion. Virology 324:373–386 [CrossRef]
    [Google Scholar]
  35. Pence D. F., Davis N. L., Johnston R. E. 1990; Antigenic and genetic characterization of Sindbis virus monoclonal antibody escape mutants which define a pathogenesis domain on glycoprotein E2. Virology 175:41–49 [CrossRef]
    [Google Scholar]
  36. Pereboev A. V., Razumov I. A., Svyatchenko V. A., Loktev V. B. 1996; Glycoproteins E2 of the Venezuelan and eastern equine encephalomyelitis viruses contain multiple cross-reactive epitopes. Arch Virol 141:2191–2205 [CrossRef]
    [Google Scholar]
  37. Pierro D. J., Myles K. M., Foy B. D., Beaty B. J., Olson K. E. 2003; Development of an orally infectious Sindbis virus transducing system that efficiently disseminates and expresses green fluorescent protein in Aedes aegypti . Insect Mol Biol 12:107–116 [CrossRef]
    [Google Scholar]
  38. Pletnev S. V., Zhang W., Mukhopadhyay S., Fisher B. R., Hernandez R., Brown D. T., Baker T. S., Rossmann M. G., Kuhn R. J. 2001; Locations of carbohydrate sites on alphavirus glycoproteins show that E1 forms an icosahedral scaffold. Cell 105:127–136 [CrossRef]
    [Google Scholar]
  39. Prenner C., Mach L., Glossl J., Marz L. 1992; The antigenicity of the carbohydrate moiety of an insect glycoprotein, honey-bee ( Apis mellifera ) venom phospholipase A2. The role of alpha 1,3-fucosylation of the asparagine-bound N-acetylglucosamine. Biochem J 284:377–380
    [Google Scholar]
  40. Rost B., Yachdav G., Liu J. 2004; The PredictProtein server. Nucleic Acids Res 32:W321–W326 [CrossRef]
    [Google Scholar]
  41. Schlesinger S. 2001; Alphavirus vectors: development and potential therapeutic applications. Expert Opin Biol Ther 1:177–191 [CrossRef]
    [Google Scholar]
  42. Smit J. M., Waarts B. L., Kimata K., Klimstra W. B., Bittman R., Wilschut J. 2002; Adaptation of alphaviruses to heparan sulfate: interaction of Sindbis and Semliki Forest viruses with liposomes containing lipid-conjugated heparin. J Virol 76:10128–10137 [CrossRef]
    [Google Scholar]
  43. Smith T. J., Cheng R. H., Olson N. H., Peterson P., Chase E., Kuhn R. J., Baker T. S. 1995; Putative receptor binding sites on alphaviruses as visualized by cryoelectron microscopy. Proc Natl Acad Sci U S A 92:10648–10652 [CrossRef]
    [Google Scholar]
  44. Stec D. S., Waddell A., Schmaljohn C. S., Cole G. A., Schmaljohn A. L. 1986; Antibody-selected variation and reversion in Sindbis virus neutralization epitopes. J Virol 57:715–720
    [Google Scholar]
  45. Strauss J. H., Strauss E. G. 1994; The alphaviruses: gene expression, replication, and evolution. Microbiol Rev 58:491–562
    [Google Scholar]
  46. Strauss E. G., Stec D. S., Schmaljohn A. L., Strauss J. H. 1991; Identification of antigenically important domains in the glycoproteins of Sindbis virus by analysis of antibody escape variants. J Virol 65:4654–4664
    [Google Scholar]
  47. Takahashi M., Tsuda T., Ikeda Y., Honke K., Taniguchi N. 2004; Role of N-glycans in growth factor signaling. Glycoconj J 20:207–212
    [Google Scholar]
  48. Taylor R. M., Hurlbut H. S., Work T. H., Kingston J. R., Frothingham T. E. 1955; Sindbis virus: a newly recognized arthropod-transmitted virus. Am J Trop Med Hyg 4:844–862
    [Google Scholar]
  49. Tomiya N., Betenbaugh M. J., Lee Y. C. 2003; Humanization of lepidopteran insect-cell-produced glycoproteins. Acc Chem Res 36:613–620 [CrossRef]
    [Google Scholar]
  50. Tomiya N., Narang S., Lee Y. C., Betenbaugh M. J. 2004; Comparing N-glycan processing in mammalian cell lines to native and engineered lepidopteran insect cell lines. Glycoconj J 21:343–360 [CrossRef]
    [Google Scholar]
  51. Tucker P. C., Strauss E. G., Kuhn R. J., Strauss J. H., Griffin D. E. 1993; Viral determinants of age-dependent virulence of Sindbis virus for mice. J Virol 67:4605–4610
    [Google Scholar]
  52. Ubol S., Griffin D. E. 1991; Identification of a putative alphavirus receptor on mouse neural cells. J Virol 65:6913–6921
    [Google Scholar]
  53. Vashishtha M., Phalen T., Marquardt M. T., Ryu J. S., Ng A. C., Kielian M. 1998; A single point mutation controls the cholesterol dependence of Semliki Forest virus entry and exit. J Cell Biol 140:91–99 [CrossRef]
    [Google Scholar]
  54. Vrati S., Kerr P. J., Weir R. C., Dalgarno L. 1996; Entry kinetics and mouse virulence of Ross River virus mutants altered in neutralization epitopes. J Virol 70:1745–1750
    [Google Scholar]
  55. Wang K. S., Strauss J. H. 1991; Use of a λ gt11 expression library to localize a neutralizing antibody-binding site in glycoprotein E2 of Sindbis virus. J Virol 65:7037–7040
    [Google Scholar]
  56. Wang K. S., Schmaljohn A. L., Kuhn R. J., Strauss J. H. 1991; Antiidiotypic antibodies as probes for the Sindbis virus receptor. Virology 181:694–702 [CrossRef]
    [Google Scholar]
  57. Wang K. S., Kuhn R. J., Strauss E. G., Ou S., Strauss J. H. 1992; High-affinity laminin receptor is a receptor for Sindbis virus in mammalian cells. J Virol 66:4992–5001
    [Google Scholar]
  58. Weaver S. C., Anishchenko M., Bowen R., Brault A. C., Estrada-Franco J. G., Fernandez Z., Greene I., Ortiz D., Paessler S., Powers A. M. 2004; Genetic determinants of Venezuelan equine encephalitis emergence. Arch Virol Suppl 18:43–64
    [Google Scholar]
  59. West J., Hernandez R., Ferreira D., Brown D. T. 2006; Mutations in the endodomain of Sindbis virus glycoprotein E2 define sequences critical for virus assembly. J Virol 80:4458–4468 [CrossRef]
    [Google Scholar]
  60. Woodring J. L. H. S., Beaty B. J. 1996; Natural cycles of vector-borne pathogens. In The Biology of Disease Vectors pp 51–72 Edited by Beaty B. J., Marquardt W. Niwot, CO: University of Colorado Press;
    [Google Scholar]
  61. Woodward T. M., Miller B. R., Beaty B. J., Trent D. W., Roehrig J. T. 1991; A single amino acid change in the E2 glycoprotein of Venezuelan equine encephalitis virus affects replication and dissemination in Aedes aegypti mosquitoes. J Gen Virol 72:2431–2435 [CrossRef]
    [Google Scholar]
  62. Zhang W., Mukhopadhyay S., Pletnev S. V., Baker T. S., Kuhn R. J., Rossmann M. G. 2002; Placement of the structural proteins in Sindbis virus. J Virol 76:11645–11658 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.82577-0
Loading
/content/journal/jgv/10.1099/vir.0.82577-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error