Skip to main content

Advertisement

Log in

Specific biochemical features of replication of clinical influenza viruses in human intestinal cell culture

  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

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

  1. Klenk, H.-D., Rott, R., Orlich, M., and Blodorn, J. (1975) Virology, 68, 426–439.

    Article  PubMed  CAS  Google Scholar 

  2. Lazarowitz, S. G., and Choppin, P. W. (1975) Virology, 68, 440–454.

    Article  PubMed  CAS  Google Scholar 

  3. Gottchalk, A. (1959) in The Viruses (Burnet, F. M., and Stanley, W. M., eds.) Academic Press, New York, pp. 51–61.

    Google Scholar 

  4. 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.

    Article  PubMed  CAS  Google Scholar 

  5. 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.

    Article  PubMed  CAS  Google Scholar 

  6. Matrosovich, M. N., Matrosovich, T. Y., Gray, T., Roberts, N. A., and Klenk, H. D. (2004) Proc. Natl. Acad. Sci. USA, 101, 4620–4624.

    Article  PubMed  CAS  Google Scholar 

  7. 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.

    Google Scholar 

  8. Rogers, G. N., Paulson, J. C., Daniels, R. S., Skehel, J. J., Wilson, I. A., and Wiley, D. C. (1983) Nature, 304, 76–78.

    Article  PubMed  CAS  Google Scholar 

  9. 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.

    Article  PubMed  CAS  Google Scholar 

  10. Ito, T., Suzuki, Y., Mitnaul, L., Vines, A., Kida, H., and Kawaoka, Y. (1997) Virology, 227, 493–499.

    Article  PubMed  CAS  Google Scholar 

  11. Mederios, R., Escriou, N., Naffakh, N., Manuguerra, J. C., and van der Werf, S. (2001) Virology, 289, 74–85.

    Article  CAS  Google Scholar 

  12. Nobusawa, E., Ishihara, H., Morishita, T., Sato, K., and Nakajima, K. (2000) Virology, 278, 587–596.

    Article  PubMed  CAS  Google Scholar 

  13. 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.

    PubMed  CAS  Google Scholar 

  14. 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.

    Google Scholar 

  15. Rogers, G. N., and Paulson, J. C. (1983) Virology, 127, 361–373.

    Article  PubMed  CAS  Google Scholar 

  16. Suzuki, H., Saito, R., Masuda, H., Ashitani, H., Sato, M., and Sato, I. (2003) J. Infect. Chemother., 9, 195–200.

    Article  PubMed  CAS  Google Scholar 

  17. Wilson, I. A., Skehel, J. J., and Wiley, D. C. (1981) Nature, 289, 366–373.

    Article  PubMed  CAS  Google Scholar 

  18. Vines, A., Wells, K., Matrosovich, M., Castricci, M. R., Ito, T., and Kawaoka, Y. (1998) J. Virol., 72, 7626–7631.

    PubMed  CAS  Google Scholar 

  19. Wagner, R., Matrosovich, M., and Klenk, H. D. (2002) Rev. Med. Virol., 12, 159–166.

    Article  PubMed  CAS  Google Scholar 

  20. Burnet, F. M. (1948) Aust. J. Exp. Med., 26, 387–391.

    Google Scholar 

  21. Burnet, F. M., and Stone, J. D. (1949) Br. J. Exp. Pathol., 30, 419–425.

    PubMed  CAS  Google Scholar 

  22. 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.

    Article  PubMed  CAS  Google Scholar 

  23. Romanova, J., Katinger, D., Ferko, B., Voglauer, R., Mochalova, L., Bovin, N., Lim, W., Katinger, H., and Egorov, A. (2003) Virology, 307, 90–97.

    Article  PubMed  CAS  Google Scholar 

  24. Yoshino, S., Yamamoto, S., and Kawabata, N. (1998) Kansenshogaku Zassi., 72, 347–351.

    CAS  Google Scholar 

  25. Zhirnov, O. P., and Klenk, H. D. (2003) Virology, 313, 198–212.

    Article  PubMed  CAS  Google Scholar 

  26. Hoffmann, E., Stech, J., Guan, Y., Webster, R. G., and Perez, D. R. (2001) Arch. Virol., 146, 2275–2289.

    Article  PubMed  CAS  Google Scholar 

  27. Shibuya, N., Goldstein, I. J., Broeknaert, W. F., Nsimba-Lubaki, M., Peeters, B., and Peumans, W. J. (1987) J. Biol. Chem., 262, 1596–1601.

    PubMed  CAS  Google Scholar 

  28. Wang, W. Ch., and Cummings, R. D. (1988) J. Biol. Chem., 263, 4576–4585.

    PubMed  CAS  Google Scholar 

  29. 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.

    Google Scholar 

  30. Vachon, P. H., and Beanlien, J. F. (1992) Gastroenterology, 103, 414–412.

    PubMed  CAS  Google Scholar 

  31. Ollier, L., Caramella, A., Giodanengo, V., and Lefebvre, J. C. (2004) J. Clin. Microbiol., 42, 5861–5865.

    Article  PubMed  Google Scholar 

  32. Conti, G., Valcavi, P., Natali, A., and Schito, G. C. (1980) Arch. Virol., 66, 309–320.

    Article  PubMed  CAS  Google Scholar 

  33. Ter Meulen, V., and Love, R. (1967) J. Virol., 1, 626–639.

    PubMed  CAS  Google Scholar 

  34. 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.

    CAS  Google Scholar 

  35. 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.

    Article  PubMed  CAS  Google Scholar 

  36. Weiss, R. A. (2002) IUBMB Life, 53, 201–205.

    Article  PubMed  CAS  Google Scholar 

  37. Forrest, J. C., and Dermody, T. S. (2003) J. Virol., 77, 9109–9115.

    Article  PubMed  CAS  Google Scholar 

  38. Stray, S., Cummings, R. D., and Air, G. (2000) Glycobiology, 10, 649–658.

    Article  PubMed  CAS  Google Scholar 

  39. Chu, V. C., and Whittaker, G. R. (2004) Proc. Natl. Acad. Sci. USA, 101, 18153–18158.

    Article  PubMed  CAS  Google Scholar 

  40. 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.

    Article  PubMed  CAS  Google Scholar 

  41. Wagner, R., Herwig, A., Azzouz, N., and Klenk, H. D. (2005) J. Virol., 79, 6449–6458.

    Article  PubMed  CAS  Google Scholar 

  42. Baigent, S. J., and McCauley, J. W. (2001) Virus Res., 79, 177–185.

    Article  PubMed  CAS  Google Scholar 

  43. 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.

    Google Scholar 

  44. Ohuci, M., Asaoka, N., Sakai, T., and Ohuchi, R. (2006) Microbes Infect., 8, 1287–1293.

    Article  CAS  Google Scholar 

  45. Liu, T., and Ye, Z. (2002) J. Virol., 76, 13055–13061.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. P. Zhirnov.

Additional information

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.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297907040062

Key words

Navigation