Abstract
Influenza A viruses isolated from the respiratory tract of patients with influenza were cultured in human intestinal epithelium cells (CACO-2 line). The CACO-2 cells were found to be 100-fold more susceptible to the clinical viruses than MDCK cells and chicken embryos. On passaging in CACO-2 cells, clinical isolates of the subtype H3N2 retained the original “human” phenotype and agglutinated human but not chicken erythrocytes, whereas on passaging in MDCK cells the virus phenotype changed to the “avian” one. On comparison with laboratory strains (grown in chicken embryos or MDCK cells), the clinical viruses were characterized by higher stability of the anti-interferon protein NS1 but had a reduced synthesis of the matrix protein M1, and this could facilitate the virus adaptation and escape of the infected cells from immune attack in the human body. The increased tropism to the human CACO-2 cells correlated with higher adsorption of the clinical viruses on cellular receptors. However, in the CACO-2 and MDCK cells the ratio of sialyl-containing glycoreceptors of the 2-3 and 2-6 type was similar. These observations indicated that not only sialic acid residues were involved in the adsorption and penetration of the clinical viruses into human cells, but also the protein moiety of the cellular receptor itself and/or an additional cellular coreceptor. Thus, clinical influenza viruses are shown to possess a specific mechanism of sorption and entry into human epithelial cells, which is responsible for their higher tropism to human cells and is unlike such a mechanism in canine cells.
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Abbreviations
- CACO-2:
-
permanent cell line of human intestinal epithelium
- C-virus:
-
virus passed in CACO-2 cells
- HA:
-
hemagglutinin
- HAA:
-
hemagglutinating activity
- MDCK:
-
permanent cell line of canine kidney
- MMA:
-
lectin isolated from Maackia amurensis
- M-virus:
-
virus passed in MDCK cells
- NA:
-
neuraminidase
- RT-PCR:
-
polymerase chain reaction with reverse transcription
- SNA:
-
lectin isolated from Sambucus nigra
- TMB:
-
tetramethylbenzidine
- VERO:
-
permanent cell line of monkey kidney
References
Klenk, H.-D., Rott, R., Orlich, M., and Blodorn, J. (1975) Virology, 68, 426–439.
Lazarowitz, S. G., and Choppin, P. W. (1975) Virology, 68, 440–454.
Gottchalk, A. (1959) in The Viruses (Burnet, F. M., and Stanley, W. M., eds.) Academic Press, New York, pp. 51–61.
Matrosovich, M. N., Gambaryan, A. S., Teneberg, S., Piskarev, V. E., Yamnikova, S. S., Lvov, D. K., Robertson, J. S., and Karisson, K. A. (1997) Virology, 233, 224–234.
Matrosovich, M. N., Tuzikov, A., Bovin, N., Gambaryan, A., Klimov, A., Castrucci, M. R., Donatelli, I., and Kawaoka, Y. (2000) J. Virol., 74, 8502–8512.
Matrosovich, M. N., Matrosovich, T. Y., Gray, T., Roberts, N. A., and Klenk, H. D. (2004) Proc. Natl. Acad. Sci. USA, 101, 4620–4624.
Pinto, M., Robine-Leon, S., Appay, M. D., Kedinger, M., Triadou, N., Dussaulx, E., Lacroix, B., Simon-Assman, P., Haffen, K., Fogh, J., and Zweibaum, A. (1983) Biol. Cell., 47, 323–330.
Rogers, G. N., Paulson, J. C., Daniels, R. S., Skehel, J. J., Wilson, I. A., and Wiley, D. C. (1983) Nature, 304, 76–78.
Suzuki, Y., Ito, T., Suzuki, T., Holland, R. E., Jr., Chambers, T. M., Kiso, M., Ishida, H., and Kawaoka, Y. (2000) J. Virol., 74, 11825–11831.
Ito, T., Suzuki, Y., Mitnaul, L., Vines, A., Kida, H., and Kawaoka, Y. (1997) Virology, 227, 493–499.
Mederios, R., Escriou, N., Naffakh, N., Manuguerra, J. C., and van der Werf, S. (2001) Virology, 289, 74–85.
Nobusawa, E., Ishihara, H., Morishita, T., Sato, K., and Nakajima, K. (2000) Virology, 278, 587–596.
Ito, T., Siziki, Y., Takada, A., Kawamoto, A., Otsuki, K., Masuda, H., Yamada, M., Suzuki, T., Kida, H., and Kawaoka, Y. (1997) J. Virol., 71, 3357–3362.
Ito, T., Suzuki, Y., Suzuki, T., Tanaka, A., Horimoto, T., Wells, K., Kida, H., Otsuki, K., Kiso, M., Ishida, H., and Kawaoka, Y. (2000) J. Virol., 73, 6743–6751.
Rogers, G. N., and Paulson, J. C. (1983) Virology, 127, 361–373.
Suzuki, H., Saito, R., Masuda, H., Ashitani, H., Sato, M., and Sato, I. (2003) J. Infect. Chemother., 9, 195–200.
Wilson, I. A., Skehel, J. J., and Wiley, D. C. (1981) Nature, 289, 366–373.
Vines, A., Wells, K., Matrosovich, M., Castricci, M. R., Ito, T., and Kawaoka, Y. (1998) J. Virol., 72, 7626–7631.
Wagner, R., Matrosovich, M., and Klenk, H. D. (2002) Rev. Med. Virol., 12, 159–166.
Burnet, F. M. (1948) Aust. J. Exp. Med., 26, 387–391.
Burnet, F. M., and Stone, J. D. (1949) Br. J. Exp. Pathol., 30, 419–425.
Govorkova, E. A., Matrosovich, M. N., Tuzikov, A. B., Bovin, N. V., Gerdil, C., Fanget, B., and Webster, R. G. (1999) Virology, 262, 31–38.
Romanova, J., Katinger, D., Ferko, B., Voglauer, R., Mochalova, L., Bovin, N., Lim, W., Katinger, H., and Egorov, A. (2003) Virology, 307, 90–97.
Yoshino, S., Yamamoto, S., and Kawabata, N. (1998) Kansenshogaku Zassi., 72, 347–351.
Zhirnov, O. P., and Klenk, H. D. (2003) Virology, 313, 198–212.
Hoffmann, E., Stech, J., Guan, Y., Webster, R. G., and Perez, D. R. (2001) Arch. Virol., 146, 2275–2289.
Shibuya, N., Goldstein, I. J., Broeknaert, W. F., Nsimba-Lubaki, M., Peeters, B., and Peumans, W. J. (1987) J. Biol. Chem., 262, 1596–1601.
Wang, W. Ch., and Cummings, R. D. (1988) J. Biol. Chem., 263, 4576–4585.
Klenk, H. D. (1990) in Immunochemistry of Viruses. II. The Basis for Serodiagnosis and Vaccines (van Regenmortel, M. N. V., and Neurath, A. R., eds.) Elsevier, Amsterdam, pp. 25–37.
Vachon, P. H., and Beanlien, J. F. (1992) Gastroenterology, 103, 414–412.
Ollier, L., Caramella, A., Giodanengo, V., and Lefebvre, J. C. (2004) J. Clin. Microbiol., 42, 5861–5865.
Conti, G., Valcavi, P., Natali, A., and Schito, G. C. (1980) Arch. Virol., 66, 309–320.
Ter Meulen, V., and Love, R. (1967) J. Virol., 1, 626–639.
Ivanova, V. T., Burtseva, E. I., Slepushkin, A. N., Oskerko, T. A., Zagorskaya, I. V., Shenchenko, E. S., Mashkova, S. A., and Feodoritova, E. I. (2004) Vopr. Virusol., 49, 12–17.
Azzi, A., Bartolomei-Corsi, O., Zakrzewska, K., Coecoran, T., Newman, R., Robertson, J. S., Yates, P., and Oxford, J. S. (1993) Epidemiol. Infect., 111, 135–142.
Weiss, R. A. (2002) IUBMB Life, 53, 201–205.
Forrest, J. C., and Dermody, T. S. (2003) J. Virol., 77, 9109–9115.
Stray, S., Cummings, R. D., and Air, G. (2000) Glycobiology, 10, 649–658.
Chu, V. C., and Whittaker, G. R. (2004) Proc. Natl. Acad. Sci. USA, 101, 18153–18158.
Gambaryan, A., Yamnikova, S., Lvov, D., Tuzikov, A., Chinarev, A., Pazynina, G., Webster, R. G., Matrosovich, M., and Bovin, N. (2005) Virology, 334, 276–283.
Wagner, R., Herwig, A., Azzouz, N., and Klenk, H. D. (2005) J. Virol., 79, 6449–6458.
Baigent, S. J., and McCauley, J. W. (2001) Virus Res., 79, 177–185.
Gottchalk, A., Belyavin, G., and Biddle, F. (1972) in Glycoproteins: Their Composition, Structure and Function, 2nd Edn., Pt. A (Gottchalk, A., ed.) Elsevier Publishing Company, Amsterdam-London-New York, pp. 1082–1096.
Ohuci, M., Asaoka, N., Sakai, T., and Ohuchi, R. (2006) Microbes Infect., 8, 1287–1293.
Liu, T., and Ye, Z. (2002) J. Virol., 76, 13055–13061.
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Original Russian Text © O. P. Zhirnov, I. V. Vorobjeva, O. A. Saphonova, N. A. Malyshev, A. V. Ovcharenko, H. D. Klenk, 2007, published in Biokhimiya, 2007, Vol. 72, No. 4, pp. 493–505.
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Zhirnov, O.P., Vorobjeva, I.V., Saphonova, O.A. et al. Specific biochemical features of replication of clinical influenza viruses in human intestinal cell culture. Biochemistry Moscow 72, 398–408 (2007). https://doi.org/10.1134/S0006297907040062
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DOI: https://doi.org/10.1134/S0006297907040062