A tyrosine-to-histidine switch at position 18 of the ross river virus e2 glycoprotein is a determinant of virus fitness in disparate hosts

Journal of Virology

Volumn 87, Issue 10, 2013, Pages 5970-5984

  Jupille, Henri J ^a   Medina Rivera, Melisa ^a,b   Hawman, David W ^a   Oko, Lauren ^a   Morrison, Thomas E ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PUERTO RICO AT CAYEY   (Puerto Rico)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN E2; HISTIDINE; TYROSINE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CROSS REACTION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; IN VITRO STUDY; MOLECULAR PATHOLOGY; MOUSE; MUSCULOSKELETAL DISEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ROSS RIVER ALPHA VIRUS; UNINDEXED SEQUENCE; VIREMIA; VIRION; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS LOAD; VIRUS REPLICATION; VIRUS VIRULENCE;

ALPHAVIRUS INFECTIONS; AMINO ACID SUBSTITUTION; ANIMALS; CAPSID PROTEINS; CELL LINE; CULICIDAE; DISEASE MODELS, ANIMAL; HISTIDINE; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; ROSS RIVER VIRUS; TYROSINE; VIRAL ENVELOPE PROTEINS; VIRAL LOAD; VIREMIA; VIRULENCE; VIRULENCE FACTORS; VIRUS REPLICATION;

EID: 84877348014     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03326-12     Document Type: Article

References (51)

1. Suhrbier A, Jaffar-Bandjee MC, Gasque P. 2012. Arthritogenic alphaviruses- an overview. Nat. Rev. Rheumatol. 8:420-429.
2. Williams MC, Woodall JP. 1961. O'nyong-nyong fever: an epidemic virus disease in East Africa. II. Isolation and some properties of the virus. Trans. R. Soc. Trop. Med. Hyg. 55:135-141.
3. Harley D, Sleigh A, Ritchie S. 2001. Ross River virus transmission, infection, and disease: a cross-disciplinary review. Clin. Microbiol. Rev. 14:909 -932.
4. Weaver SC, Reisen WK. 2010. Present and future arboviral threats. Antiviral Res. 85:328 -345.
5. Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, Panning M, Cordioli P, Fortuna C, Boros S, Magurano F, Silvi G, Angelini P, Dottori M, Ciufolini MG, Majori GC, Cassone A. 2007. Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet 370:1840 -1846.
6. Grandadam M, Caro V, Plumet S, Thiberge JM, Souares Y, Failloux AB, Tolou HJ, Budelot M, Cosserat D, Leparc-Goffart I, Despres P. 2011. Chikungunya virus, southeastern France. Emerg. Infect. Dis. 17:910 -913.
7. ProMed-mail. 25 May 2011. Chikungunya: New Caledonia. ProMEDmail. Archive no. 20110525.1595. Accessed 3 August 2011. http://www .promedmail.org.
8. Powers AM, Logue CH. 2007. Changing patterns of chikungunya virus: re-emergence of a zoonotic arbovirus. J. Gen. Virol. 88:2363-2377.
9. Dupuis-Maguiraga L, Noret M, Brun S, Le Grand R, Gras G, Roques P. 2012. Chikungunya disease: infection-associated markers from the acute to the chronic phase of arbovirus-induced arthralgia. PLoS Negl. Trop. Dis. 6:e1446. doi:10.1371/journal.pntd.0001446.
10. Morrison TE, Fraser RJ, Smith PN, Mahalingam S, Heise MT. 2007. Complement contributes to inflammatory tissue destruction in a mouse model of Ross River virus-induced disease. J. Virol. 81:5132-5143.
11. Morrison TE, Whitmore AC, Shabman RS, Lidbury BA, Mahalingam S, Heise MT. 2006. Characterization of Ross River virus tropism and virusinduced inflammation in a mouse model of viral arthritis and myositis. J. Virol. 80:737-749.
12. Gunn BM, Morrison TE, Whitmore AC, Blevins LK, Hueston L, Fraser RJ, Herrero LJ, Ramirez R, Smith PN, Mahalingam S, Heise MT. 2012. Mannose binding lectin is required for alphavirus-induced arthritis/ myositis. PLoS Pathog. 8:e1002586. doi:10.1371/journal.ppat.1002586.
13. Hoarau JJ, Jaffar Bandjee MC, Krejbich Trotot P, Das T, Li-Pat-Yuen G, Dassa B, Denizot M, Guichard E, Ribera A, Henni T, Tallet F, Moiton MP, Gauzere BA, Bruniquet S, Jaffar Bandjee Z, Morbidelli P, Martigny G, Jolivet M, Gay F, Grandadam M, Tolou H, Vieillard V, Debre P, Autran B, Gasque P. 2010. Persistent chronic inflammation and infection by Chikungunya arthritogenic alphavirus in spite of a robust host immune response. J. Immunol. 184:5914 -5927.
14. Parola P, de Lamballerie X, Jourdan J, Rovery C, Vaillant V, Minodier P, Brouqui P, Flahault A, Raoult D, Charrel RN. 2006. Novel chikungunya virus variant in travelers returning from Indian Ocean islands. Emerg. Infect. Dis. 12:1493-1499.
15. Fraser JR, Cunningham AL, Clarris BJ, Aaskov JG, Leach R. 1981. Cytology of synovial effusions in epidemic polyarthritis. Aust. N. Z. J. Med. 11:168 -173.
16. Soden M, Vasudevan H, Roberts B, Coelen R, Hamlin G, Vasudevan S, La Brooy J. 2000. Detection of viral ribonucleic acid and histologic analysis of inflamed synovium in Ross River virus infection. Arthritis Rheum. 43:365-369.
17. Hazelton RA, Hughes C, Aaskov JG. 1985. The inflammatory response in the synovium of a patient with Ross River arbovirus infection. Aust. N. Z. J. Med. 15:336 -339.
18. Ozden S, Huerre M, Riviere JP, Coffey LL, Afonso PV, Mouly V, de Monredon J, Roger JC, El Amrani M, Yvin JL, Jaffar MC, Frenkiel MP, Sourisseau M, Schwartz O, Butler-Browne G, Despres P, Gessain A, Ceccaldi PE. 2007. Human muscle satellite cells as targets of Chikungunya virus infection. PLoS One 2:e527. doi:10.1371/journal.pone.0000527.
19. Jupille HJ, Oko L, Stoermer KA, Heise MT, Mahalingam S, Gunn BM, Morrison TE. 2011. Mutations in nsP1 and PE2 are critical determinants of Ross River virus-induced musculoskeletal inflammatory disease in a mouse model. Virology 410:216 -227.
20. Kuhn RJ, Niesters HG, Hong Z, Strauss JH. 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.
21. Dalgarno L, Rice CM, Strauss JH. 1983. Ross River virus 26 s RNA: complete nucleotide sequence and deduced sequence of the encoded structural proteins. Virology 129:170 -187.
22. Lindsay M, Oliveira N, Jasinska E, Johansen C, Harrington S, Wright AE, Smith D. 1996. An outbreak of Ross River virus disease in Southwestern Australia. Emerg. Infect. Dis. 2:117-120.
23. Liao M, Kielian M. 2005. Domain III from class II fusion proteins functions as a dominant-negative inhibitor of virus membrane fusion. J. Cell Biol. 171:111-120.
24. Qin ZL, Zheng Y, Kielian M. 2009. Role of conserved histidine residues in the low-pH dependence of the Semliki Forest virus fusion protein. J. Virol. 83:4670-4677.
25. Liu CY, Kielian M. 2009. E1 mutants identify a critical region in the trimer interface of the Semliki forest virus fusion protein. J. Virol. 83: 11298-11306.
26. Aaskov J, Fokine A, Liu W. 2012. Ross River virus evolution: implications for vaccine development. Future Virol. 7:173-178.
27. Stoermer KA, Burrack A, Oko L, Montgomery SA, Borst LB, Gill RG, Morrison TE. 2012. Genetic ablation of arginase 1 in macrophages and neutrophils enhances clearance of an arthritogenic alphavirus. J. Immunol. 189:4047- 4059.
28. Snyder AJ, Sokoloski KJ, Mukhopadhyay S. 2012. Mutating conserved cysteines in the alphavirus e2 glycoprotein causes virus-specific assembly defects. J. Virol. 86:3100 -3111.
29. Forrester NL, Palacios G, Tesh RB, Savji N, Guzman H, Sherman M, Weaver SC, Lipkin WI. 2012. Genome-scale phylogeny of the alphavirus genus suggests a marine origin. J. Virol. 86:2729 -2738.
30. Tsetsarkin KA, Chen R, Leal G, Forrester N, Higgs S, Huang J, Weaver SC. 2011. Chikungunya virus emergence is constrained in Asia by lineagespecific adaptive landscapes. Proc. Natl. Acad. Sci. U. S. A. 108:7872-7877.
31. Coffey LL, Vignuzzi M. 2011. Host alternation of chikungunya virus increases fitness while restricting population diversity and adaptability to novel selective pressures. J. Virol. 85:1025-1035.
32. Jose J, Snyder JE, Kuhn RJ. 2009. A structural and functional perspective of alphavirus replication and assembly. Future Microbiol. 4:837- 856.
33. Li L, Jose J, Xiang Y, Kuhn RJ, Rossmann MG. 2010. Structural changes of envelope proteins during alphavirus fusion. Nature 468:705-708.
34. Voss JE, Vaney MC, Duquerroy S, Vonrhein C, Girard-Blanc C, Crublet E, Thompson A, Bricogne G, Rey FA. 2010. Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography. Nature 468:709 -712.
35. Thurlkill RL, Grimsley GR, Scholtz JM, Pace CN. 2006. pK values of the ionizable groups of proteins. Protein Sci. 15:1214 -1218.
36. Gorchakov R, Wang E, Leal G, Forrester NL, Plante K, Rossi SL, Partidos CD, Adams AP, Seymour RL, Weger J, Borland EM, Sherman MB, Powers AM, Osorio JE, Weaver SC. 2012. Attenuation of Chikungunya virus vaccine strain 181/clone 25 is determined by two amino acid substitutions in the E2 envelope glycoprotein. J. Virol. 86:6084-6096.
37. Davis NL, Powell N, Greenwald GF, Willis LV, Johnson BJ, Smith JF, Johnston RE. 1991. Attenuating mutations in the E2 glycoprotein gene of Venezuelan equine encephalitis virus: construction of single and multiple mutants in a full-length cDNA clone. Virology 183:20 -31.
38. Klimstra WB, Ryman KD, Johnston RE. 1998. Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J. Virol. 72:7357-7366.
39. Bernard KA, Klimstra WB, Johnston RE. 2000. Mutations in the E2 glycoprotein of Venezuelan equine encephalitis virus confer heparan sulfate interaction, low morbidity, and rapid clearance from blood of mice. Virology 276:93-103.
40. Glasgow GM, Killen HM, Liljestrom P, Sheahan BJ, Atkins GJ. 1994. A single amino acid change in the E2 spike protein of a virulent strain of Semliki Forest virus attenuates pathogenicity. J. Gen. Virol. 75(Part 3): 663-668.
41. Glasgow GM, Sheahan BJ, Atkins GJ, Wahlberg JM, Salminen A, Liljestrom P. 1991. Two mutations in the envelope glycoprotein E2 of Semliki Forest virus affecting the maturation and entry patterns of the virus alter pathogenicity for mice. Virology 185:741-748.
42. Santagati MG, Maatta JA, Itaranta PV, Salmi AA, Hinkkanen AE. 1995. The Semliki Forest virus E2 gene as a virulence determinant. J. Gen. Virol. 76(Part 1):47-52.
43. Tucker PC, Griffin DE. 1991. Mechanism of altered Sindbis virus neurovirulence associated with a single-amino-acid change in the E2 glycoprotein. J. Virol. 65:1551-1557.
44. Lee P, Knight R, Smit JM, Wilschut J, Griffin DE. 2002. A single mutation in the E2 glycoprotein important for neurovirulence influences binding of Sindbis virus to neuroblastoma cells. J. Virol. 76:6302- 6310.
45. Lustig S, Jackson AC, Hahn CS, Griffin DE, Strauss EG, Strauss JH. 1988. Molecular basis of Sindbis virus neurovirulence in mice. J. Virol. 62:2329 -2336.
46. Gardner CL, Burke CW, Higgs ST, Klimstra WB, Ryman KD. 2012. Interferon-alpha/beta deficiency greatly exacerbates arthritogenic disease in mice infected with wild-type chikungunya virus but not with the cell culture-adapted live-attenuated 181/25 vaccine candidate. Virology 425: 103-112.
47. Zhang W, Heil M, Kuhn RJ, Baker TS. 2005. Heparin binding sites on Ross River virus revealed by electron cryo-microscopy. Virology 332:511- 518.
48. Heil ML, Albee A, Strauss JH, Kuhn RJ. 2001. An amino acid substitution in the coding region of the E2 glycoprotein adapts Ross River virus to utilize heparan sulfate as an attachment moiety. J. Virol. 75:6303- 6309.
49. Glomb-Reinmund S, Kielian M. 1998. fus-1, a pH shift mutant of Semliki Forest virus, acts by altering spike subunit interactions via a mutation in the E2 subunit. J. Virol. 72:4281- 4287.
50. Ekstrom M, Liljestrom P, Garoff H. 1994. Membrane protein lateral interactions control Semliki Forest virus budding. EMBO J. 13:1058- 1064.
51. Li ML, Liao HJ, Simon LD, 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.