1887

Abstract

With an expanding geographical range and no specific treatments, human arthritogenic alphaviral disease poses a significant problem worldwide. Previous work with Ross River virus (RRV) demonstrated that alphaviral -linked glycosylation contributes to type I IFN (IFN-αβ) induction in myeloid dendritic cells. This study further evaluated the role of alphaviral -linked glycans , assessing the effect of glycosylation on pathogenesis in a mouse model of RRV-induced disease and on viral infection and dissemination in a common mosquito vector, . A viral mutant lacking the E1-141 glycosylation site was attenuated for virus-induced disease, with reduced myositis and higher levels of IFN-γ induction at peak disease contributing to improved viral clearance, suggesting that glycosylation of the E1 glycoprotein plays a major role in the pathogenesis of RRV. Interestingly, RRV lacking E2-200 glycan had significantly reduced replication in the mosquito vector , whereas loss of either of the E1 or E2-262 glycans had little effect on the competence of the mosquito vector. Overall, these results indicate that glycosylation of the E1 and E2 glycoproteins of RRV provides important determinants of viral virulence and immunopathology in the mammalian host and replication in the mosquito vector.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000412
2016-05-01
2021-08-03
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/5/1094.html?itemId=/content/journal/jgv/10.1099/jgv.0.000412&mimeType=html&fmt=ahah

References

  1. Aaskov J. G., Mataika J. U., Lawrence G. W., Rabukawaqa V., Tucker M. M., Miles J. A., Dalglish D. A. 1981; An epidemic of Ross River virus infection in Fiji, 1979. Am J Trop Med Hyg 30:1053–1059[PubMed]
    [Google Scholar]
  2. Arankalle V. A., Shrivastava S., Cherian S., Gunjikar R. S., Walimbe A. M., Jadhav S. M., Sudeep A. B., Mishra A. C. 2007; Genetic divergence of chikungunya viruses in India (1963–2006) with special reference to the 2005–2006 explosive epidemic. J Gen Virol 88:1967–1976 [View Article][PubMed]
    [Google Scholar]
  3. Ashbrook A. W., Burrack K. S., Silva L. A., Montgomery S. A., Heise M. T., Morrison T. E., Dermody T. S. 2014; Residue 82 of the chikungunya virus E2 attachment protein modulates viral dissemination and arthritis in mice. J Virol 88:12180–12192 [View Article][PubMed]
    [Google Scholar]
  4. Beasley D. W., Whiteman M. C., Zhang S., Huang C. Y., Schneider B. S., Smith D. R., Gromowski G. D., Higgs S., Kinney R. M., Barrett A. D. 2005; Envelope protein glycosylation status influences mouse neuroinvasion phenotype of genetic lineage 1 West Nile virus strains. J Virol 79:8339–8347 [View Article][PubMed]
    [Google Scholar]
  5. Butters T. D., Hughes R. C., Vischer P. 1981; Steps in the biosynthesis of mosquito cell membrane glycoproteins and the effects of tunicamycin. Biochim Biophys Acta 640:672–686 [View Article][PubMed]
    [Google Scholar]
  6. Chen W., Foo S. S., Taylor A., Lulla A., Merits A., Hueston L., Forwood M. R., Walsh N. C., Sims N. A., other authors. 2015; Bindarit, an inhibitor of monocyte chemotactic protein synthesis, protects against bone loss induced by chikungunya virus infection. J Virol 89:581–593 [View Article][PubMed]
    [Google Scholar]
  7. Crispin M., Harvey D. J., Bitto D., Bonomelli C., Edgeworth M., Scrivens J. H., Huiskonen J. T., Bowden T. A. 2014; Structural plasticity of the Semliki Forest virus glycome upon interspecies transmission. J Proteome Res 13:1702–1712 [View Article][PubMed]
    [Google Scholar]
  8. Dalrymple J. M., Schlesinger S., Russell P. K. 1976; Antigenic characterization of two Sindbis envelope glycoproteins separated by isoelectric focusing. Virology 69:93–103 [View Article][PubMed]
    [Google Scholar]
  9. 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 [View Article][PubMed]
    [Google Scholar]
  10. de Lamballerie X., Leroy E., Charrel R. N., Ttsetsarkin K., Higgs S., Gould E. A. 2008; Chikungunya virus adapts to tiger mosquito via evolutionary convergence: a sign of things to come?. Virol J 5:33 [View Article][PubMed]
    [Google Scholar]
  11. Foo S. S., Chen W., Taylor A., Sheng K. C., Yu X., Teng T. S., Reading P. C., Blanchard H., Garlanda C., other authors. 2015; Role of pentraxin 3 in shaping arthritogenic alphaviral disease: from enhanced viral replication to immunomodulation. PLoS Pathog 11:e1004649 [View Article][PubMed]
    [Google Scholar]
  12. Fraser J. R. 1986; Epidemic polyarthritis and Ross River virus disease. Clin Rheum Dis 12:369–388[PubMed]
    [Google Scholar]
  13. Garoff H., Simons K., Renkonen O. 1974; Isolation and characterization of the membrane proteins of Semliki Forest virus. Virology 61:493–504 [View Article][PubMed]
    [Google Scholar]
  14. Garoff H., Frischauf A. M., Simons K., Lehrach H., Delius H. 1980; Nucleotide sequence of cDNA coding for Semliki Forest virus membrane glycoproteins. Nature 288:236–241 [View Article][PubMed]
    [Google Scholar]
  15. Gunn B. M., Morrison T. E., Whitmore A. C., Blevins L. K., Hueston L., Fraser R. J., Herrero L. J., Ramirez R., Smith P. N., other authors. 2012; Mannose binding lectin is required for alphavirus-induced arthritis/myositis. PLoS Pathog 8:e1002586 [View Article][PubMed]
    [Google Scholar]
  16. Hakimi J., Atkinson P. H. 1980; Growth-dependent alterations in oligomannosyl glycopeptides expressed in Sindbis virus glycoproteins. Biochemistry 19:5619–5624 [View Article][PubMed]
    [Google Scholar]
  17. Hardy J. L., Houk E. J., Kramer L. D., Reeves W. C. 1983; Intrinsic factors affecting vector competence of mosquitoes for arboviruses. Annu Rev Entomol 28:229–262 [View Article][PubMed]
    [Google Scholar]
  18. Harley D., Sleigh A., Ritchie S. 2001; Ross River virus transmission, infection, and disease: a cross-disciplinary review. Clin Microbiol Rev 14:909–932 [View Article][PubMed]
    [Google Scholar]
  19. Herrero L. J., Sheng K. C., Jian P., Taylor A., Her Z., Herring B. L., Chow A., Leo Y. S., Hickey M. J., other authors. 2013; Macrophage migration inhibitory factor receptor CD74 mediates alphavirus-induced arthritis and myositis in murine models of alphavirus infection. Arthritis Rheum 65:2724–2736[PubMed]
    [Google Scholar]
  20. Hsieh P., Robbins P. W. 1984; Regulation of asparagine-linked oligosaccharide processing. Oligosaccharide processing in Aedes albopictus mosquito cells. J Biol Chem 259:2375–2382[PubMed]
    [Google Scholar]
  21. Hsieh P., Rosner M. R., Robbins P. W. 1983; Host-dependent variation of asparagine-linked oligosaccharides at individual glycosylation sites of Sindbis virus glycoproteins. J Biol Chem 258:2548–2554[PubMed]
    [Google Scholar]
  22. Jupille H. J., Medina-Rivera M., Hawman D. W., Oko L., Morrison T. E. 2013; A tyrosine-to-histidine switch at position 18 of the Ross River virus E2 glycoprotein is a determinant of virus fitness in disparate hosts. J Virol 87:5970–5984 [View Article][PubMed]
    [Google Scholar]
  23. Keegstra K., Sefton B., Burke D. 1975; Sindbis virus glycoproteins: effect of the host cell on the oligosaccharides. J Virol 16:613–620[PubMed]
    [Google Scholar]
  24. Klimstra W. B., Nangle E. M., Smith M. S., Yurochko A. D., Ryman K. D. 2003; DC-SIGN and L-SIGN can act as attachment receptors for alphaviruses and distinguish between mosquito cell- and mammalian cell-derived viruses. J Virol 77:12022–12032 [View Article][PubMed]
    [Google Scholar]
  25. Knight R. L., Schultz K. L. W., Kent R. J., Venkatesan M., Griffin D. E. 2009; Role of N-linked glycosylation for Sindbis virus infection and replication in vertebrate and invertebrate systems. J Virol 83:5640–5647 [View Article][PubMed]
    [Google Scholar]
  26. Kuhn R. J., Niesters H. G. M., Hong Z., Strauss J. H. 1991; Infectious RNA transcripts from Ross River virus cDNA clones and the construction and characterization of defined chimeras with Sindbis virus. Virology 182:430–441 [View Article][PubMed]
    [Google Scholar]
  27. Leavitt R., Schlesinger S., Kornfeld S. 1977; Tunicamycin inhibits glycosylation and multiplication of Sindbis and vesicular stomatitis viruses. J Virol 21:375–385[PubMed]
    [Google Scholar]
  28. Mayne J. T., Bell J. R., Strauss E. G., Strauss J. H. 1985; Pattern of glycosylation of Sindbis virus envelope proteins synthesized in hamster and chicken cells. Virology 142:121–133 [View Article][PubMed]
    [Google Scholar]
  29. McDowell W., Romero P. A., Datema R., Schwarz R. T. 1987; Glucose trimming and mannose trimming affect different phases of the maturation of Sindbis virus in infected BHK cells. Virology 161:37–44 [View Article][PubMed]
    [Google Scholar]
  30. Morrison T. E., Whitmore A. C., Shabman R. S., Lidbury B. A., Mahalingam S., Heise M. T. 2006; Characterization of Ross River virus tropism and virus-induced inflammation in a mouse model of viral arthritis and myositis. J Virol 80:737–749 [View Article][PubMed]
    [Google Scholar]
  31. Morrison T. E., Simmons J. D., Heise M. T. 2008; Complement receptor 3 promotes severe Ross River virus-induced disease. J Virol 82:11263–11272 [View Article][PubMed]
    [Google Scholar]
  32. Moudy R. M., Zhang B., Shi P. Y., Kramer L. D. 2009; West Nile virus envelope protein glycosylation is required for efficient viral transmission by Culex vectors. Virology 387:222–228 [View Article][PubMed]
    [Google Scholar]
  33. Mylonas A. D., Brown A. M., Carthew T. L., McGrath B., Purdie D. M., Pandeya N., Vecchio P. C., Collins L. G., Gardner I. D., other authors. 2002; Natural history of Ross River virus-induced epidemic polyarthritis. Med J Aust 177:356–360[PubMed]
    [Google Scholar]
  34. Ng L. C., Hapuarachchi H. C. 2010; Tracing the path of chikungunya virus—evolution and adaptation. Infect Genet Evol 10:876–885 [View Article][PubMed]
    [Google Scholar]
  35. Old J. M., Deane E. M. 2005; Antibodies to the Ross River virus in captive marsupials in urban areas of eastern New South Wales, Australia. J Wildl Dis 41:611–614 [View Article][PubMed]
    [Google Scholar]
  36. Renault P., Solet J. L., Sissoko D., Balleydier E., Larrieu S., Filleul L., Lassalle C., Thiria J., Rachou E., other authors. 2007; A major epidemic of chikungunya virus infection on Réunion Island, France, 2005–2006. Am J Trop Med Hyg 77:727–731[PubMed]
    [Google Scholar]
  37. Rice C. M., Strauss J. H. 1981; Nucleotide sequence of the 26S mRNA of Sindbis virus and deduced sequence of the encoded virus structural proteins. Proc Natl Acad Sci U S A 78:2062–2066 [View Article][PubMed]
    [Google Scholar]
  38. Richards S. L., Anderson S. L., Lord C. C., Smartt C. T., Tabachnick W. J. 2012; Relationships between infection, dissemination, and transmission of West Nile virus RNA in Culex pipiens quinquefasciatus (Diptera: Culicidae). J Med Entomol 49:132–142 [View Article][PubMed]
    [Google Scholar]
  39. Rogers K. M., Heise M. 2009; Modulation of cellular tropism and innate antiviral response by viral glycans. J Innate Immun 1:405–412 [View Article][PubMed]
    [Google Scholar]
  40. Rosen L., Gubler D. J., Bennett P. H. 1981; Epidemic polyarthritis (Ross River) virus infection in the Cook Islands. Am J Trop Med Hyg 30:1294–1302[PubMed]
    [Google Scholar]
  41. Rulli N. E., Guglielmotti A., Mangano G., Rolph M. S., Apicella C., Zaid A., Suhrbier A., Mahalingam S. 2009; Amelioration of alphavirus-induced arthritis and myositis in a mouse model by treatment with bindarit, an inhibitor of monocyte chemotactic proteins. Arthritis Rheum 60:2513–2523 [View Article][PubMed]
    [Google Scholar]
  42. Russell R. C. 2002; Ross River virus: ecology and distribution. Annu Rev Entomol 47:1–31 [View Article][PubMed]
    [Google Scholar]
  43. Sam I. C., Chan Y. F., Chan S. Y., Loong S. K., Chin H. K., Hooi P. S., Ganeswrie R., Abubakar S. 2009; Chikungunya virus of Asian and Central/East African genotypes in Malaysia. J Clin Virol 46:180–183 [View Article][PubMed]
    [Google Scholar]
  44. Schlesinger S., Koyama A. H., Malfer C., Gee S. L., Schlesinger M. J. 1985; The effects of inhibitors of glucosidase I on the formation of Sindbis virus. Virus Res 2:139–149 [View Article][PubMed]
    [Google Scholar]
  45. Shabman R. S., Morrison T. E., Moore C., White L., Suthar M. S., Hueston L., Rulli N., Lidbury B., Ting J.P.-Y., other authors. 2007; Differential induction of type I interferon responses in myeloid dendritic cells by mosquito and mammalian-cell-derived alphaviruses. J Virol 81:237–247 [View Article][PubMed]
    [Google Scholar]
  46. Shabman R. S., Rogers K. M., Heise M. T. 2008; Ross River virus envelope glycans contribute to type I interferon production in myeloid dendritic cells. J Virol 82:12374–12383 [View Article][PubMed]
    [Google Scholar]
  47. Shirato K., Miyoshi H., Goto A., Ako Y., Ueki T., Kariwa H., Takashima I. 2004; Viral envelope protein glycosylation is a molecular determinant of the neuroinvasiveness of the New York strain of West Nile virus. J Gen Virol 85:3637–3645 [View Article][PubMed]
    [Google Scholar]
  48. Silva L. A., Khomandiak S., Ashbrook A. W., Weller R., Heise M. T., Morrison T. E., Dermody T. S., Lyles D. S. 2014; A single-amino-acid polymorphism in chikungunya virus E2 glycoprotein influences glycosaminoglycan utilization. J Virol 88:2385–2397 [View Article][PubMed]
    [Google Scholar]
  49. 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 [View Article][PubMed]
    [Google Scholar]
  50. Strauss J. H., Strauss E. G. 1994; The alphaviruses: gene expression, replication, and evolution. Microbiol Rev 58:491–562[PubMed]
    [Google Scholar]
  51. Tesh R. B., McLean R. G., Shroyer D. A., Calisher C. H., Rosen L. 1981; Ross River virus (Togaviridae: Alphavirus) infection (epidemic polyarthritis) in American Samoa. Trans R Soc Trop Med Hyg 75:426–431 [View Article][PubMed]
    [Google Scholar]
  52. Thavara U., Tawatsin A., Pengsakul T., Bhakdeenuan P., Chanama S., Anantapreecha S., Molito C., Chompoosri J., Thammapalo S., other authors. 2009; Outbreak of chikungunya fever in Thailand and virus detection in field population of vector mosquitoes, Aedes aegypti (L.) and Aedes albopictus Skuse (Diptera: Culicidae). Southeast Asian J Trop Med Public Health 40:951–962[PubMed]
    [Google Scholar]
  53. Tsetsarkin K. A., Weaver S. C. 2011; Sequential adaptive mutations enhance efficient vector switching by chikungunya virus and its epidemic emergence. PLoS Pathog 7:e1002412 [View Article][PubMed]
    [Google Scholar]
  54. Van Slyke G. A., Jia Y., Whiteman M. C., Wicker J. A., Barrett A. D., Kramer L. D. 2013; Vertebrate attenuated West Nile virus mutants have differing effects on vector competence in Culex tarsalis mosquitoes. J Gen Virol 94:1069–1072 [View Article][PubMed]
    [Google Scholar]
  55. Weaver S. C., Lecuit M. 2015; Chikungunya virus and the global spread of a mosquito-borne disease. N Engl J Med 372:1231–1239 [View Article][PubMed]
    [Google Scholar]
  56. Whiteman M. C., Li L., Wicker J. A., Kinney R. M., Huang C., Beasley D. W., Chung K. M., Diamond M. S., Solomon T., Barrett A. D. 2010; Development and characterization of non-glycosylated E and NS1 mutant viruses as a potential candidate vaccine for West Nile virus. Vaccine 28:1075–1083 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000412
Loading
/content/journal/jgv/10.1099/jgv.0.000412
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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