Home LiteratureArticle Details
PMID: 8392602 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Viral determinants of age-dependent virulence of Sindbis virus for mice.

Journal of virology ·Vol. 67 ·No. 8 ·1993-08-00 ·Pages 4605-10

Tucker PC, Strauss EG, Kuhn RJ, Strauss JH, Griffin DE

Abstract

Many alphaviruses cause more severe disease in young animals than in older animals. The age-dependent resistance to severe disease is determined primarily by maturation of the host, but strains of virus can be selected that overcome the increased resistance of mature animals. Sindbis virus (SV) strain AR339 causes fatal encephalitis in newborn mice and nonfatal encephalitis in weanling mice, whereas NSV, a neuroadapted strain of SV, causes fatal encephalitis in weanling as well as newborn mice. We have previously shown that the E2 glycoprotein of NSV contained His-55, whereas AR339 E2 had Gln-55 (S. Lustig, A. C. Jackson, C. S. Hahn, D. E. Griffin, E. G. Strauss, and J. H. Strauss, J. Virol. 62:2329-2336, 1988) and that SV with E2 containing Gly-172 was more virulent for newborn mice than SV with E2 containing Arg-172 (P. C. Tucker and D. E. Griffin, J. Virol. 65:1551-1557, 1991). Here we tested the virulence for both newborn and older mice of SV containing a number of different amino acids at E2 position 55 (His, Gln, Lys, Arg, Glu, Gly) in combination with both Gly-172 and Arg-172. All the viruses were virulent for newborn mice, but the residues at both 55 and 172 influenced the virulence of the virus, and there were differences in virulence observed among the various viruses. However, only viruses with His-55 were fully virulent for 14-day-old mice, and this virulence was independent of the residue at position 172. Virus with Lys-55 was virulent for 7-day-old mice, although slightly attenuated relative to His-55. Viruses with His-55 grew more rapidly and to higher titer in the brains of 7- and 14-day-old mice, in N18 neuroblastoma cells, and in BHK cells. Our data suggest that His-55 is important for neurovirulence in older mice and acts by increasing the efficiency of virus replication.

MeSH Terms
Aging/physiology Animals Animals, Newborn Base Sequence Brain/growth & development,microbiology Cell Line Cloning, Molecular DNA, Viral/genetics,isolation & purification Encephalitis/microbiology,physiopathology Mice Mice, Inbred Strains Molecular Sequence Data Mutagenesis, Site-Directed Neuroblastoma Oligodeoxyribonucleotides Recombination, Genetic Sindbis Virus/genetics,pathogenicity,physiology Togaviridae Infections/physiopathology Tumor Cells, Cultured Virulence/physiology Virus Replication
Chemicals
DNA, Viral Oligodeoxyribonucleotides
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Tucker P C
Department of Medicine, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205.
Strauss E G
Kuhn R J
Strauss J H
Griffin D E
References (34)
34 references, click to expand
  1. Mechanism of altered Sindbis virus neurovirulence associated with a single-amino-acid change in the E2 Glycoprotein.
    J Virol. 1991 Mar;65(3):1551-7 PMID: 1995953
  2. Sequence analysis of the E2 gene of a hyperglycosylated, host restricted mutant of Sindbis virus and estimation of mutation rate from frequency of revertants.
    Virology. 1986 Oct 15;154(1):135-43 PMID: 3750843
  3. Increased expression of T alpha 1 alpha-tubulin mRNA during collateral and NGF-induced sprouting of sympathetic neurons.
    Dev Biol. 1990 Sep;141(1):84-92 PMID: 1975243
  4. Association of sindbis virion glycoproteins and their precursors.
    J Mol Biol. 1982 Jan 15;154(2):325-48 PMID: 7077663
  5. Antigenic characterization of two sindbis envelope glycoproteins separated by isoelectric focusing.
    Virology. 1976 Jan;69(1):93-103 PMID: 54983
  6. Antiidiotypic antibodies as probes for the Sindbis virus receptor.
    Virology. 1991 Apr;181(2):694-702 PMID: 2014644
  7. Molecular analysis of Sindbis virus pathogenesis in neonatal mice by using virus recombinants constructed in vitro.
    J Virol. 1988 Jun;62(6):2124-33 PMID: 2835514
  8. Complete nucleotide sequence of the genomic RNA of Sindbis virus.
    Virology. 1984 Feb;133(1):92-110 PMID: 6322438
  9. Alphavirus neurovirulence: monoclonal antibodies discriminating wild-type from neuroadapted Sindbis virus.
    J Virol. 1985 Oct;56(1):110-9 PMID: 2411947
  10. Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene.
    Nature. 1993 Feb 25;361(6414):739-42 PMID: 8441470
  11. Role of the immune response in age-dependent resistance of mice to encephalitis due to Sindbis virus.
    J Infect Dis. 1976 Apr;133(4):456-64 PMID: 1262711
  12. Japanese encephalitis virus neurotropism is dependent on the degree of neuronal maturity.
    J Virol. 1991 Feb;65(2):880-6 PMID: 1987378
  13. Rapid and efficient site-specific mutagenesis without phenotypic selection.
    Proc Natl Acad Sci U S A. 1985 Jan;82(2):488-92 PMID: 3881765
  14. Location of a major antigenic site involved in Ross River virus neutralization.
    Virology. 1988 Feb;162(2):346-53 PMID: 2448952
  15. Molecular basis of Sindbis virus neurovirulence in mice.
    J Virol. 1988 Jul;62(7):2329-36 PMID: 2836615
  16. Ross River virus mutant with a deletion in the E2 gene: properties of the virion, virus-specific macromolecule synthesis, and attenuation of virulence for mice.
    Virology. 1986 Jun;151(2):222-32 PMID: 3010551
  17. Identification of a putative alphavirus receptor on mouse neural cells.
    J Virol. 1991 Dec;65(12):6913-21 PMID: 1658382
  18. Production of infectious RNA transcripts from Sindbis virus cDNA clones: mapping of lethal mutations, rescue of a temperature-sensitive marker, and in vitro mutagenesis to generate defined mutants.
    J Virol. 1987 Dec;61(12):3809-19 PMID: 3479621
  19. Pathogenesis of encephalitis induced in newborn mice by virulent and avirulent strains of Sindbis virus.
    J Virol. 1990 May;64(5):2041-6 PMID: 1691310
  20. Characterization of Sindbis virus epitopes important for penetration in cell culture and pathogenesis in animals.
    Virology. 1986 Jan 30;148(2):245-54 PMID: 2417415
  21. Specificity of the inflammatory response in viral encephalitis. I. Adoptive immunization of immunosuppressed mice infected with Sindbis virus.
    J Exp Med. 1972 Aug 1;136(2):216-26 PMID: 5043410
  22. Autoradiographic and histological studies of postnatal neurogenesis. 3. Dating the time of production and onset of differentiation of cerebellar microneurons in rats.
    J Comp Neurol. 1969 Jul;136(3):269-93 PMID: 5788129
  23. Persistence of viral RNA in mouse brains after recovery from acute alphavirus encephalitis.
    J Virol. 1992 Nov;66(11):6429-35 PMID: 1383564
  24. Age-dependent resistance to viral encephalitis: studies of infections due to Sindbis virus in mice.
    J Infect Dis. 1972 Mar;125(3):257-62 PMID: 4552644
  25. Age-dependent resistance of mice to sindbis virus infection: viral replication as a function of host age.
    Infect Immun. 1971 Feb;3(2):268-73 PMID: 16557964
  26. Attenuating mutations in glycoproteins E1 and E2 of Sindbis virus produce a highly attenuated strain when combined in vitro.
    J Virol. 1990 Sep;64(9):4438-44 PMID: 2384921
  27. The pathogenesis of spinal cord involvement in the encephalomyelitis of mice caused by neuroadapted Sindbis virus infection.
    Lab Invest. 1987 Apr;56(4):418-23 PMID: 3031369
  28. Protective monoclonal antibodies define maturational and pH-dependent antigenic changes in Sindbis virus E1 glycoprotein.
    Virology. 1983 Oct 15;130(1):144-54 PMID: 6195815
  29. Role of the immune response in recovery from Sindbis virus encephalitis in mice.
    J Immunol. 1977 Mar;118(3):1070-5 PMID: 845432
  30. 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. 1981 Apr;78(4):2062-6 PMID: 6941270
  31. Basis of neurovirulence in Sindbis virus encephalomyelitis of mice.
    Lab Invest. 1988 May;58(5):503-9 PMID: 3367635
  32. Molecular pathogenesis of Sindbis virus encephalitis in experimental animals.
    Adv Virus Res. 1989;36:255-71 PMID: 2544083
  33. A single nucleotide change in the E2 glycoprotein gene of Sindbis virus affects penetration rate in cell culture and virulence in neonatal mice.
    Proc Natl Acad Sci U S A. 1986 Sep;83(18):6771-5 PMID: 3462725
  34. Neurotransmitter synthesis by neuroblastoma clones (neuroblast differentiation-cell culture-choline acetyltransferase-acetylcholinesterase-tyrosine hydroxylase-axons-dendrites).
    Proc Natl Acad Sci U S A. 1972 Jan;69(1):258-63 PMID: 4400294
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1993-08-00
Pages
4605-10
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC237845
Subset
IM
Grants
NIAID NIH HHS · AI01070-01 · United States
NIAID NIH HHS · AI10793 · United States
NINDS NIH HHS · NS18596 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]