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
-
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
-
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
-
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
-
Association of sindbis virion glycoproteins and their precursors.
J Mol Biol. 1982 Jan 15;154(2):325-48
PMID: 7077663
-
Antigenic characterization of two sindbis envelope glycoproteins separated by isoelectric focusing.
Virology. 1976 Jan;69(1):93-103
PMID: 54983
-
Antiidiotypic antibodies as probes for the Sindbis virus receptor.
Virology. 1991 Apr;181(2):694-702
PMID: 2014644
-
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
-
Complete nucleotide sequence of the genomic RNA of Sindbis virus.
Virology. 1984 Feb;133(1):92-110
PMID: 6322438
-
Alphavirus neurovirulence: monoclonal antibodies discriminating wild-type from neuroadapted Sindbis virus.
J Virol. 1985 Oct;56(1):110-9
PMID: 2411947
-
Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene.
Nature. 1993 Feb 25;361(6414):739-42
PMID: 8441470
-
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
-
Japanese encephalitis virus neurotropism is dependent on the degree of neuronal maturity.
J Virol. 1991 Feb;65(2):880-6
PMID: 1987378
-
Rapid and efficient site-specific mutagenesis without phenotypic selection.
Proc Natl Acad Sci U S A. 1985 Jan;82(2):488-92
PMID: 3881765
-
Location of a major antigenic site involved in Ross River virus neutralization.
Virology. 1988 Feb;162(2):346-53
PMID: 2448952
-
Molecular basis of Sindbis virus neurovirulence in mice.
J Virol. 1988 Jul;62(7):2329-36
PMID: 2836615
-
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
-
Identification of a putative alphavirus receptor on mouse neural cells.
J Virol. 1991 Dec;65(12):6913-21
PMID: 1658382
-
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
-
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
-
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
-
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
-
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
-
Persistence of viral RNA in mouse brains after recovery from acute alphavirus encephalitis.
J Virol. 1992 Nov;66(11):6429-35
PMID: 1383564
-
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
-
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
-
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
-
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
-
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
-
Role of the immune response in recovery from Sindbis virus encephalitis in mice.
J Immunol. 1977 Mar;118(3):1070-5
PMID: 845432
-
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
-
Basis of neurovirulence in Sindbis virus encephalomyelitis of mice.
Lab Invest. 1988 May;58(5):503-9
PMID: 3367635
-
Molecular pathogenesis of Sindbis virus encephalitis in experimental animals.
Adv Virus Res. 1989;36:255-71
PMID: 2544083
-
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
-
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