The evolutionary relationships of epidemic influenza A (H1N1) viruses isolated between 1982 and 1986 have been examined by oligonucleotide mapping and partial DNA sequencing. The T1 mapping studies confirmed our previous report that the evolution of the influenza virus genome generally results in an average of four to six oligonucleotide changes per year. Between 1982 and 1986, however, two apparent exceptions to this finding occurred. H1N1 antigenic variants (including the A/Chile/83 and A/Victoria/83 reference strains) that caused influenza outbreaks and epidemics from 1983 to 1984 differed by 20 to 30 oligonucleotides from viruses isolated during the previous influenza season. T1 mapping of individual RNA segments and sequencing revealed that all six internal genes of a representative 1983 A/Chile-like virus were more closely related to genes of non-reassortant H1N1 viruses that circulated from 1977 to 1982 than to genes of H3N2 viruses. Therefore, the 1983 variant viruses were not H1N1-H3N2 reassortants. The A/Taiwan/86-like H1N1 antigenic variants that emerged in south-east Asia in the spring of 1986 and caused epidemic activity the following winter also exhibited changes of 20 to 30 oligonucleotides from the A/Chile/83-like or A/Victoria/83-like H1N1 viruses that circulated during the previous influenza season. Fewer oligonucleotide changes were observed between the 1986 A/Taiwan/86-like and H1N1 viruses isolated before 1983, however, suggesting that the former evolved from viruses that circulated before the 1983 antigenic variants became the predominant H1N1 epidemic virus strains. This was confirmed by sequencing the HA1 domain of the haemagglutinin genes of three A/Taiwan/86-like viruses. These studies provide evidence that other genes of influenza A viruses, in addition to the haemagglutinin gene, may evolve concurrently along two or more separate pathways.
AaronsonR. P.,
YoungI. F.,
PaleseP.1982; Oligonucleotide mapping: evaluation of its sensitivity by computer-simulation. Nucleic Acids Research 10:237–246
AirG. M.1979; Nucleotide sequence coding for the ‘signal peptide’ and N terminus of the hemagglutinin from an Asian (H2N2) strain of influenza virus. Virology 97:468–472
BishopD. H. L.,
HuddlestonJ. A.,
BrownleeG. G.1982a; The complete sequence of RNA segment 2 of influenza A/NT/60/68 and its encoded P1 protein. Nucleic Acids Research 10:1335–1343
BishopD. H. L.,
JonesK. L.,
HuddlestonJ. A.,
BrownleeG. G.1982b; Influenza A virus evolution: complete sequences of influenza A/NT/60/68 RNA segment 3 and its predicted acidic P polypeptide compared with those of influenza A/PR/8/34. Virology 120:481–489
BothG. W.,
SleighM. J.,
CoxN. J.,
KendalA. P.1983; Antigenic drift in influenza virus H3 hemagglutinin from 1968 to 1980: multiple evolutionary pathways and sequential amino acid changes at key antigenic sites. Journal of Virology 48:52–60
BrownE. G.1988; Genetic variants of influenza A/Taiwan/1/86 cocirculating in Canada during the winter of 1986 to 1987. Journal of Clinical Microbiology 26:313–318
BuonagurioD. A.,
NakadaS.,
ParvinI. D.,
KrystalM.,
PaleseP.,
FitchW. M.1986; Evolution of human influenza A viruses over 50 years: rapid, uniform rate of change in the NS gene. Science 232:980–982
Centers For Disease Control1987; Update on influenza activity in the United States, availability of influenza vaccines and recommendations for the use of vaccines and amantidine. Morbidity and Mortality Weekly Report 35:805–807
CoxN. J.,
KendalA. P.1984; Genetic stability of A/Ann Arbor/6/60 cold-mutant (temperature-sensitive) live influenza virus genes: analysis by oligonucleotide mapping of recombinant vaccine strains before and after replication in volunteers. Journal of Infectious Diseases 149:194–200
CoxN. J.,
BaiZ. S.,
KendalA. P.1983; Laboratory-based surveillance of influenza A(H1N1) and A(H3N2) viruses in 1980–1981: antigenic and genomic analyses. Bulletin of the World Health Organization 61:143–152
CoxN. J.,
KendalA. P.,
ShilovA. A.,
AlexandrovaG. I.,
GhendonY. Z.,
KlimovA. I.1985; Comparative studies of A/Leningrad/134/57 wild-type and 47-times passaged cold-adapted mutant influenza viruses; oligonucleotide mapping and RNA-RNA hybridization studies. Journal of General Virology 66:1697–1704
CoxN. J.,
KitameF.,
KlimovA.,
KoenneckeI.,
KendalA. P.1986; Comparative studies of wild-type and cold-mutant (temperature-sensitive) influenza virus: detection of mutations in all genes of the A/Ann Arbor/6/60 (H2N2) mutant vaccine donor strain. Microbial Pathogenesis 1:387–397
DanielsR. S.,
DouglasA. R.,
SkehelJ. J.,
WileyD. C.1985; Antigenic and amino acid sequence analysis of influenza viruses of the H1N1 subtype isolated between 1982 and 1984. Bulletin of the World Health Organization 63:273–277
HuddlestonJ. A.,
BrownleeG. G.1982; The sequence of the nucleoprotein gene of human influenza A virus, strain A/NT/60/68. Nucleic Acids Research 10:1029–1038
JonesK. L.,
HuddlestonJ. A.,
BrownleeG. G.1983; The sequence of RNA segment 1 of influenza virus A/NT/60/68 and its comparison with the corresponding segment of strains A/PR/8/34 and A/WSN/33. Nucleic Acids Research 11:1555–1566
KendalA. P.,
NobleG. R.,
SkehelJ. J.,
DowdleW. R.1978; Antigenic similarity of influenza A(H1N1) viruses from epidemics in 1977-1978 to “Scandinavian” strains isolated in epidemics of 1950-1951. Virology 89:632–636
KendalA. P.,
LeeD. T.,
ParishH. S.,
RainesD.,
NobleG. R.,
DowdleW. R.1979a; Laboratory-based surveillance of influenza virus in the United States during the winter of 1977 1978.I. Periods of prevalence of H1N1 and H3N2 influenza A strains, their relative rates of isolation in different age groups, and detection of antigenic variants. American Journal of Epidemiology 111:449–461
KendalA. P.,
LeeD. T.,
ParishH. S.,
RainesD.,
nobleG. r.,
dowdleW. R.1979b; Laboratory-based surveillance of influenza virus in the United States during the winter of 1977 1978. II. Isolation of a mixture of A/Victoria and A/USSR-like viruses during an epidemic in Wyoming, U.S.A., January 1978. American Journal of Epidemiology 110:462–468
KrystalM.,
BuonagurioD.,
YoungJ. F.,
PaleseP.1983; Sequential mutations in the NS genes of influenza virus field strains. Journal of Virology 45:547–554
LambR. A.,
LaiC. J.1980; Sequence of interrupted and uninterrupted mRNAs and cloned DNA coding for two overlapping nonstructural proteins of influenza virus. Cell 21:475–485
LambR. A.,
LaiC.-J.1981; Conservation of the influenza virus membrane protein (M1) amino acid sequence and an open reading frame of RNA segment 7 encoding a second protein (M2) in H1N1 and H3N2 strains. Virology 112:746–751
NakajimaK.,
DesselbergerU.,
PaleseP.1978; Recent human influenza A(H1N1) viruses are closely related genetically to strains isolated in 1950. Nature, London 274:334–339
NakajimaS.,
CoxN. J.,
KendalA. P.1981; Antigenic and genomic analyses of influenza A(H1N1) viruses from different regions of the world, February 1978-March 1980. Infection and Immunity 32:287–294
OrtinJ.,
MartinezC.,
Del RioL.,
DavilaM.,
Lopez-GalindezC.,
VillanuevaN.,
DomingoE.1983; Genetic variability of Hong Kong (H3N2) influenza viruses: spontaneous mutations and their location in the viral genome. Gene 23:233–239
PaleseP.,
BrandC.,
YoungJ. A.,
BaezM.,
SixH. R.,
KaselJ. A.1981; Molecular epidemiology of influenza viruses. In Perspectives in VirologyXI115–127PollardM.
New York: Alan R. Liss;
RaymondF. L.,
CatonA. J.,
CoxN. J.,
KendalA. P.,
BrownleeG. G.1986; The antigenicity and evolution of influenza HI hemagglutinin, from 1950–1957 and 1977–1983: two pathways from one gene. Virology 148:275–287
RobertsonJ. s.1987; Sequence analysis of the haemagglutinin of A/Taiwan/1/86, a new variant of human influenza A(H1N1). Journal of General Virology 68:1205–1208
RobertsonJ. S.,
BootmanJ. A.,
NewmanR.,
OxfordI. S.,
DanielsR. S.,
WebsterR. G.,
SchildG. C.1987; Structural changes in the hemagglutinin which accompany egg adaptation of an influenza A (H1N1) virus. Virology 160:31–37
SangerF.,
NicklenS.,
CoulsonA. R.1977; DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of SciencesU.S.A 74:5463–5467
ScholtissekC.,
Von HoyningenV.,
RottR.1978; Genetic relatedness between the new 1977 epidemic strains (H1N1) of influenza and human influenza strains isolated between 1947 and 1957. Virology 89:613–617
YoungJ. F.,
PaleseP.1979; Evolution of human influenza A viruses in nature: recombination contributes to genetic variation of H1N1 strains. Proceedings of the National Academy of SciencesU.S.A 76:6547–6551
YoungJ. F.,
DesselbergerU.,
PaleseP.1979; Evolution of human influenza A viruses in nature: sequential mutations in the genomes of new H1N1 isolates. cell 18:73–83