Virus Mutation Frequencies Can Be Greatly Underestimated by Monoclonal Antibody Neutralization of Virions

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 1989 Dec 1

PMID 2479770

Citations 38

Authors

J J Holland

J C de la Torre

D A Steinhauer

D Clarke

E Duarte

E Domingo

Affiliations

Soon will be listed here.

Abstract

Monoclonal antibody-resistant mutants have been widely used to estimate virus mutation frequencies. We demonstrate that standard virion neutralization inevitably underestimates monoclonal antibody-resistant mutant genome frequencies of vesicular stomatitis virus, due to phenotypic masking-mixing when wild-type (wt) virions are present in thousandsfold greater numbers. We show that incorporation of antibody into the plaque overlay medium (after virus penetration at 37 degrees C) can provide accurate estimates of genome frequencies of neutral monoclonal antibody-resistant mutant viruses in wt clones. By using this method, we have observed two adjacent G----A base transition frequencies in the I3 epitope to be of the order of 10(-4) in a wt glycine codon. This appears to be slightly lower than the frequencies observed at other sites for total (viable and nonviable) virus genomes when using a direct sequence approach.

Citing Articles

Sulfonated Nanomaterials with Broad-Spectrum Antiviral Activity Extending beyond Heparan Sulfate-Dependent Viruses.

Cagno V, Gasbarri M, Medaglia C, Gomes D, Clement S, Stellacci F Antimicrob Agents Chemother. 2020; 64(12).

PMID: 32988820 PMC: 7674063. DOI: 10.1128/AAC.02001-20.

Identification of Clotrimazole Derivatives as Specific Inhibitors of Arenavirus Fusion.

Torriani G, Trofimenko E, Mayor J, Fedeli C, Moreno H, Michel S J Virol. 2019; 93(6).

PMID: 30626681 PMC: 6401469. DOI: 10.1128/JVI.01744-18.

Recessive Host Range Mutants and Unsusceptible Cells That Inactivate Virions without Genome Penetration: Ecological and Technical Implications.

Roznowski A, Young R, Love S, Andromita A, Guzman V, Wilch M J Virol. 2018; 93(3).

PMID: 30429341 PMC: 6340031. DOI: 10.1128/JVI.01767-18.

Transmission genetics of drug-resistant hepatitis C virus.

van Buuren N, Tellinghuisen T, Richardson C, Kirkegaard K Elife. 2018; 7.

PMID: 29589830 PMC: 5916564. DOI: 10.7554/eLife.32579.

Discovery and Mechanistic Study of Benzamide Derivatives That Modulate Hepatitis B Virus Capsid Assembly.

Wu S, Zhao Q, Zhang P, Kulp J, Hu L, Hwang N J Virol. 2017; 91(16).

PMID: 28566379 PMC: 5533917. DOI: 10.1128/JVI.00519-17.

References

Holland J, Spindler K, Horodyski F, Grabau E, Nichol S, VandePol S . Rapid evolution of RNA genomes. Science. 1982; 215(4540):1577-85. DOI: 10.1126/science.7041255. View

Steinhauer D, de la Torre J, Holland J . High nucleotide substitution error frequencies in clonal pools of vesicular stomatitis virus. J Virol. 1989; 63(5):2063-71. PMC: 250622. DOI: 10.1128/JVI.63.5.2063-2071.1989. View

Lubeck M, SCHULMAN J, Palese P . Antigenic variants of influenza viruses: marked differences in the frequencies of variants selected with different monoclonal antibodies. Virology. 1980; 102(2):458-62. DOI: 10.1016/0042-6822(80)90114-2. View

Novick A, Szilard L . Virus strains of identical phenotype but different genotype. Science. 1951; 113(2924):34-5. DOI: 10.1126/science.113.2924.34. View

Buonagurio D, Nakada S, FITCH W, Palese P . Epidemiology of influenza C virus in man: multiple evolutionary lineages and low rate of change. Virology. 1986; 153(1):12-21. DOI: 10.1016/0042-6822(86)90003-6. View

Durbin R, Stollar V . 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; 154(1):135-43. DOI: 10.1016/0042-6822(86)90436-8. View

Ledinko N, HIRST G . Mixed infection of HeLa cells with polioviruses types 1 and 2. Virology. 1961; 14:207-19. DOI: 10.1016/0042-6822(61)90196-9. View

Lefrancois L, Lyles D . Antigenic determinants of vesicular stomatitis virus: analysis with antigenic variants. J Immunol. 1983; 130(1):394-8. View

VandePol S, Lefrancois L, Holland J . Sequences of the major antibody binding epitopes of the Indiana serotype of vesicular stomatitis virus. Virology. 1986; 148(2):312-25. DOI: 10.1016/0042-6822(86)90328-4. View

10.

Steinhauer D, Holland J . Rapid evolution of RNA viruses. Annu Rev Microbiol. 1987; 41:409-33. DOI: 10.1146/annurev.mi.41.100187.002205. View

11.

Sedivy J, Capone J, RajBhandary U, Sharp P . An inducible mammalian amber suppressor: propagation of a poliovirus mutant. Cell. 1987; 50(3):379-89. DOI: 10.1016/0092-8674(87)90492-2. View

12.

White B, McGeoch D . Isolation and characterization of conditional lethal amber nonsense mutants of vesicular stomatitis virus. J Gen Virol. 1987; 68 ( Pt 12):3033-44. DOI: 10.1099/0022-1317-68-12-3033. View

13.

Gebauer F, de la Torre J, Gomes I, Mateu M, Barahona H, Tiraboschi B . Rapid selection of genetic and antigenic variants of foot-and-mouth disease virus during persistence in cattle. J Virol. 1988; 62(6):2041-9. PMC: 253289. DOI: 10.1128/JVI.62.6.2041-2049.1988. View

14.

Smith D, Inglis S . The mutation rate and variability of eukaryotic viruses: an analytical review. J Gen Virol. 1987; 68 ( Pt 11):2729-40. DOI: 10.1099/0022-1317-68-11-2729. View

15.

Steinhauer D, de la Torre J, Meier E, Holland J . Extreme heterogeneity in populations of vesicular stomatitis virus. J Virol. 1989; 63(5):2072-80. PMC: 250623. DOI: 10.1128/JVI.63.5.2072-2080.1989. View

16.

Leider J, Palese P, SMITH F . Determination of the mutation rate of a retrovirus. J Virol. 1988; 62(9):3084-91. PMC: 253424. DOI: 10.1128/JVI.62.9.3084-3091.1988. View

17.

Domingo E, Sabo D, Taniguchi T, Weissmann C . Nucleotide sequence heterogeneity of an RNA phage population. Cell. 1978; 13(4):735-44. DOI: 10.1016/0092-8674(78)90223-4. View

18.

FRAENKEL-CONRAT H, Singer B . Virus reconstitution. II. Combination of protein and nucleic acid from different strains. Biochim Biophys Acta. 1957; 24(3):540-8. DOI: 10.1016/0006-3002(57)90244-5. View

19.

Itoh H, Melnick J . Double infections of single cells with ECHO 7 and Coxsackie A9 viruses. J Exp Med. 1959; 109(4):393-406. PMC: 2136956. DOI: 10.1084/jem.109.4.393. View

20.

Domingo E, Martinez-Salas E, Sobrino F, de la Torre J, Portela A, Ortin J . The quasispecies (extremely heterogeneous) nature of viral RNA genome populations: biological relevance--a review. Gene. 1985; 40(1):1-8. DOI: 10.1016/0378-1119(85)90017-4. View