Department of Bacteriology, Yamagata University School of Medicine, Iida-Nishi, Yamagata 990-9585, Japan1
Virus Research Center, Clinical Research Division, Sendai National Hospital, Sendai 983-8520, Japan2
Department of Public Health, Niigata University School of Medicine, Asahi-Machi Dori, Niigata 951-8510, Japan3
Author for correspondence: Yoko Matsuzaki. Fax +81 23 628 5250. e-mail matuzaki{at}med.id.yamagata-u.ac.jp
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Abstract |
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The surveillance of influenza C virus infections initiated in Yamagata City in 1988 and in the adjacent Sendai City in 1990 has succeeded in isolating a large number of viruses, almost all of which have been shown to possess HE genes belonging to one of the three lineages described above (Matsuzaki et al., 1994 ; Peng et al., 1996
; Kimura et al., 1997
). We noticed, however, that three virus strains [Yamagata/1/92 (YA/1/92), Yamagata/1/93 (YA/1/93) and Miyagi/5/93 (MI/5/93)] isolated between June 1992 and May 1993 were closely similar to one another in both antigenic and genetic structures but dissimilar to any of the 60 strains isolated in Japan before June 1992, raising the possibility that an influenza C variant, belonging to an evolutionary lineage distinct from any identified previously, had been newly introduced into Japan shortly before June 1992 and then circulated in the country up to at least May 1993.
In this communication, to obtain information about the origin of the 1992/1993 isolates from Yamagata and Sendai, we compared their antigenic and genetic properties with those of eight foreign isolates from France [Paris/1/67 (PA/67)], the Republic of South Africa [Johannesburg/4/67 (JHG/67)], the United States [Georgia/1/69 (GA/69), NewJersey/1/76 (NJ/76), Kansas/1/79 (KAN/1/79) and Kansas/2/79 (KAN/2/79)], Greece [Greece/1/79 (GR/79)] and Brazil [SaoPaulo/378/82 (SP/82)] that have not as yet been well characterized. The results show that the 1992/1993 isolates are closely related to the Brazilian isolate (SP/82) and that these viruses (including SP/82) emerged through a reassortment event from a YA/26/81-like parent and another parent that has not yet been identified, having acquired the PB1 and NP genes from the former and the remaining five genes from the latter.
Strains YA/1/92, YA/1/93 and MI/5/93 were isolated from throat swab specimens collected on 4 June 1992, 30 April 1993 and 6 May 1993, respectively, from paediatric patients with acute respiratory illness by inoculating the strains into the amniotic cavity of 9-day-old embryonated hens eggs. The viruses were each cloned by means of the limiting dilution method and then propagated in eggs. The eight foreign isolates used for comparison, all of which were kindly provided by N. J. Cox (CDC, Atlanta, USA), were also cloned and propagated in eggs.
A total of 14 influenza C strains were isolated between June 1992 and May 1993 from patients living in Yamagata or Sendai Cities. Antigenic analysis with monoclonal antibodies (MAbs) to the HE glycoprotein showed that 11 of the 14 isolates belonged to one of the three known antigenic groups represented by YA/26/81, AI/81 and MS/80 (Peng et al., 1996 ; Kimura et al., 1997
). The remaining three (YA/1/92, YA/1/93 and MI/5/93), on the other hand, displayed antigenicities that were identical to one another but were clearly different from that of any of the reference strains (YA/26/81, AI/81 and MS/80), as shown in Table 1
. Table 1
summarizes the results of antigenic analysis performed by haemagglutination-inhibition (HI) tests (Matsuzaki et al., 1994
), utilizing four different anti-HE MAbs characterized previously (Sugawara et al., 1988
, 1993
). The reactivity patterns of the three 1992/1993 strains were also dissimilar to those of nine strains isolated outside Japan [Taylor/47 (TAY/47), AnnArbor/1/50 (AA/50), GreatLakes/54 (GL/54), Johannesburg/1/66 (JHG/66), California/78 (CAL/78), Pig/Beijing/10/81, Pig/Beijing/115/81 (P/B/115/81), Pig/Beijing/439/82 and England/83 (EG/83)] (data not shown), the HE antigenicity of which had been characterized previously (Matsuzaki et al., 1994
; our unpublished results). The additional eight foreign isolates (listed in Table 1
) were therefore examined for reactivity with anti-HE MAbs and their reactivity patterns were compared with those of the three 1992/1993 strains. The results showed that six of the eight isolates belonged to one of the three known antigenic groups: NJ/76 fell within the YA/26/81 virus group; JHG/67, GA/69, KAN/1/79 and KAN/2/79 within the AI/81 virus group; and GR/79 within the MS/80 virus group. In contrast, the patterns of PA/67 and SP/82 were clearly different from that of any of the three reference strains. It was evident, however, that strain SP/82 had a remarkably similar antigenicity to that of the three 1992/1993 isolates.
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In order to clarify the results of antigenic analysis, the nucleotide sequence of the HE gene was determined for one of the three 1992/1993 isolates (YA/1/93) as well as for all of the eight foreign isolates by sequencing PCR products directly according to procedures described elsewhere (Kimura et al., 1997 ). A phylogenetic tree was then constructed by the neighbour-joining method (Saitou & Nei, 1987
), utilizing these nine sequences as well as 33 sequences reported previously, including those of two prototype strains, TAY/47 and AA/50. In our previous phylogenetic studies (Muraki et al., 1996
; Kimura et al., 1997
), these latter two strains were excluded from the analysis, since numerous passages in embryonated eggs may have introduced many additional mutations not present in the original isolates. As expected from the results of antigenic analysis, six of the eight foreign isolates were found to belong to one of the three lineages: NJ/76 was within the YA/26/81-related lineage, JHG/67, GA/69, KAN/1/79 and KAN/2/79 within the AI/81-related lineage and GR/79 within the MS/80-related lineage (Fig. 1
). Strain PA/67, together with two oldest strains (TAY/47 and AA/50), formed a lineage (designated the TAY/47-related lineage) that was separate from the four lineages identified previously. More importantly, the HE gene sequence of YA/1/93 showed a much higher degree of identity to SP/82 (99·1%) than to any of the other 40 strains (92·396·9%), and strains YA/1/93 and SP/82 made up a separate sixth lineage (designated the SP/82-related lineage). Furthermore, comparison of the predicted amino acid sequence showed that the HE protein of YA/1/93 differed from that of SP/82 by only two amino acids (residues 134 and 331), yet it differed from those of the other seven foreign isolates by as many as 1723 amino acids.
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Acknowledgments |
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Footnotes |
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b Present address: Yamagata Prefectural Institute of Public Health, Toka-Machi, Yamagata 990-0031, Japan.
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References |
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Received 13 December 1999;
accepted 15 February 2000.