1887

Abstract

Rotavirus replication occurs in intestinal epithelial cells. Cell lines fully permissive to rotavirus include kidney epithelial (MA104), colonic (Caco-2) and hepatic (HepG2) types. Previously, it has been shown that cellular integrins α2β1, α4β1 and αXβ2 are involved in rotavirus cell entry. As receptor usage is a major determinant of virus tropism, the levels of cell surface expression of these integrins have now been investigated by flow cytometry on cell lines of human (Caco-2, HepG2, RD, K562) and monkey (MA104, COS-7) origin in relation to cellular susceptibility to infection with monkey and human rotaviruses. Cells supporting any replication of human rotaviruses (RD, HepG2, Caco-2, COS-7 and MA104) expressed α2β1 and (when tested) αXβ2, whereas the non-permissive K562 cells did not express α2β1, α4β1 or αXβ2. Only RD cells expressed α4β1. Although SA11 grew to higher titres in RD, HepG2, Caco-2, COS-7 and MA104 cells, this virus still replicated at a low level in K562 cells. In all cell lines tested, SA11 replicated to higher titres than did human strains, consistent with the ability of SA11 to use sialic acids as alternative receptors. Levels of cell surface α2 integrin correlated with levels of rotavirus growth. The α2 integrin relative linear median fluorescence intensity on K562, RD, COS-7, MA104 and Caco-2 cells correlated linearly with the titre of SA11 produced in these cells at 20 h after infection at a multiplicity of 0·1, and the data best fitted a sigmoidal dose–response curve ( =1·00, =0·005). Thus, growth of rotaviruses in these cell lines correlates with their surface expression of α2β1 integrin and is consistent with their expression of αXβ2 and α4β1 integrins.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-81-9-2203
2000-09-01
2019-12-16
Loading full text...

Full text loading...

/deliver/fulltext/jgv/81/9/0812203a.html?itemId=/content/journal/jgv/10.1099/0022-1317-81-9-2203&mimeType=html&fmt=ahah

References

  1. Basson, M. D., Modlin, I. M. & Madri, J. A. ( 1992; ). Human enterocyte (Caco-2) migration is modulated in vitro by extracellular matrix composition and epidermal growth factor. Journal of Clinical Investigation 90, 15-23.[CrossRef]
    [Google Scholar]
  2. Bernstein, C. N., Sargent, M., Gallatin, W. M. & Wilkins, J. ( 1996; ). Beta 2-integrin/intercellular adhesion molecule (ICAM) expression in the normal human intestine. Clinical and Experimental Immunology 106, 160-169.
    [Google Scholar]
  3. Chan, B. M., Matsuura, N., Takada, Y., Zetter, B. R. & Hemler, M. E. ( 1991; ). In vitro and in vivo consequences of VLA-2 expression on rhabdomyosarcoma cells. Science 251, 1600-1602.[CrossRef]
    [Google Scholar]
  4. Ciarlet, M. & Estes, M. K. ( 1999; ). Human and most animal rotavirus strains do not require the presence of sialic acid on the cell surface for efficient infectivity. Journal of General Virology 80, 943-948.
    [Google Scholar]
  5. Clark, S. M., Roth, J. R., Clark, M. L., Barnett, B. B. & Spendlove, R. S. ( 1981; ). Trypsin enhancement of rotavirus infectivity: mechanism of enhancement. Journal of Virology 39, 816-822.
    [Google Scholar]
  6. Coulson, B. S. ( 1993; ). Typing of human rotavirus VP4 by an enzyme immunoassay using monoclonal antibodies. Journal of Clinical Microbiology 31, 1-8.
    [Google Scholar]
  7. Coulson, B. S. ( 1997; ). Effects of Workshop monoclonal antibodies on rotavirus infection of cells. In Leucocyte Typing VI, pp. 391-393. Edited by T. Kishimoto, H. Kikutani, A. E. G. Kr. von dem Borne, S. M. Goyert, D. Y. Mason, M. Miyasaka, L. Moretta, K. Okumura, S. Shaw, T. A. Springer, K. Sugamura & H. Zola. New York: Garland Publishing.
  8. Coulson, B. S., Fowler, K. J., Bishop, R. F. & Cotton, R. G. ( 1985; ). Neutralizing monoclonal antibodies to human rotavirus and indications of antigenic drift among strains from neonates. Journal of Virology 54, 14-20.
    [Google Scholar]
  9. Coulson, B. S., Londrigan, S. L. & Lee, D. J. ( 1997; ). Rotavirus contains integrin ligand sequences and a disintegrin-like domain that are implicated in virus entry into cells. Proceedings of the National Academy of Sciences, USA 94, 5389-5394.[CrossRef]
    [Google Scholar]
  10. Espejo, R. T., Lopez, S. & Arias, C. ( 1981; ). Structural polypeptides of simian rotavirus SA11 and the effect of trypsin. Journal of Virology 37, 156-160.
    [Google Scholar]
  11. Estes, M. K., Graham, D. Y., Gerba, C. P. & Smith, E. M. ( 1979; ). Simian rotavirus SA11 replication in cell cultures. Journal of Virology 31, 810-815.
    [Google Scholar]
  12. Estes, M. K., Graham, D. Y. & Mason, B. B. ( 1981; ). Proteolytic enhancement of rotavirus infectivity: molecular mechanisms. Journal of Virology 39, 879-888.
    [Google Scholar]
  13. Franco, M. A. & Greenberg, H. B. ( 1999; ). Immunity to rotavirus infection in mice. Journal of Infectious Diseases 179 (Suppl. 3), S466–S469.
    [Google Scholar]
  14. Fukudome, K., Yoshie, O. & Konno, T. ( 1989; ). Comparison of human, simian, and bovine rotaviruses for requirement of sialic acid in hemagglutination and cell adsorption. Virology 172, 196-205.[CrossRef]
    [Google Scholar]
  15. Gamble, J. R., Matthias, L. J., Meyer, G., Kaur, P., Russ, G., Faull, R., Berndt, M. C. & Vadas, M. A. ( 1993; ). Regulation of in vitro capillary tube formation by anti-integrin antibodies. Journal of Cell Biology 121, 931-943.[CrossRef]
    [Google Scholar]
  16. Gluzman, Y. ( 1981; ). SV40-transformed simian cells support the replication of early SV40 mutants. Cell 23, 175-182.[CrossRef]
    [Google Scholar]
  17. Hemler, M. E., Huang, C., Takada, Y., Schwarz, L., Strominger, J. L. & Clabby, M. L. ( 1987; ). Characterization of the cell surface heterodimer VLA-4 and related peptides. Journal of Biological Chemistry 262, 11478-11485.
    [Google Scholar]
  18. Hewish, M. J., Takada, Y. & Coulson, B. S. ( 2000; ). Integrins α2β1 and α4β1 can mediate SA11 rotavirus attachment and entry into cells. Journal of Virology 74, 228-236.[CrossRef]
    [Google Scholar]
  19. Hoshino, Y., Saif, L. J., Kang, S. Y., Sereno, M. M., Chen, W. K. & Kapikian, A. Z. ( 1995; ). Identification of group A rotavirus genes associated with virulence of a porcine rotavirus and host range restriction of a human rotavirus in the gnotobiotic piglet model. Virology 209, 274-280.[CrossRef]
    [Google Scholar]
  20. Hussain, L. A., Kelly, C. G., Rodin, A., Jourdan, M. & Lehner, T. ( 1995; ). Investigation of the complement receptor 3 (CD11b/CD18) in human rectal epithelium. Clinical and Experimental Immunology 102, 384-388.
    [Google Scholar]
  21. Jolly, C., Beisner, B. & Holmes, I. (1999). Rotavirus infection of MA104 cells is inhibited by Ricinus lectin and separately expressed single binding domains. In Abstracts of the XIth International Congress of Virology, VW 25.05, p. 149. Sydney, Australia.
  22. Kalica, A. R., Flores, J. & Greenberg, H. B. ( 1983; ). Identification of the rotaviral gene that codes for hemagglutination and protease-enhanced plaque formation. Virology 125, 194-205.[CrossRef]
    [Google Scholar]
  23. Kamata, T., Puzon, W. & Takada, Y. ( 1995; ). Identification of putative ligand-binding sites of the integrin alpha 4 beta 1 (VLA-4, CD49d/CD29). Biochemical Journal 305, 945-951.
    [Google Scholar]
  24. Kirkwood, C. D., Bishop, R. F. & Coulson, B. S. ( 1998; ). Attachment and growth of human rotaviruses RV-3 and S12/85 in Caco-2 cells depend on VP4. Journal of Virology 72, 9348-9352.
    [Google Scholar]
  25. Kitamoto, N., Ramig, R. F., Matson, D. O. & Estes, M. K. ( 1991; ). Comparative growth of different rotavirus strains in differentiated cells (MA104, HepG2, and CaCo-2). Virology 184, 729-737.[CrossRef]
    [Google Scholar]
  26. Komoriya, A., Green, L. J., Mervic, M., Yamada, S. S., Yamada, K. M. & Humphries, M. J. ( 1991; ). The minimal essential sequence for a major cell type-specific adhesion site (CS1) within the alternatively spliced type III connecting segment domain of fibronectin is leucine–aspartic acid–valine. Journal of Biological Chemistry 266, 15075-15079.
    [Google Scholar]
  27. Loike, J. D., Sodeik, B., Cao, L., Leucona, S., Weitz, J. I., Detmers, P. A., Wright, S. D. & Silverstein, S. C. ( 1991; ). CD11c/CD18 on neutrophils recognizes a domain at the N terminus of the A alpha chain of fibrinogen. Proceedings of the National Academy of Sciences, USA 88, 1044-1048.[CrossRef]
    [Google Scholar]
  28. Ludert, J. E., Feng, N., Yu, J. H., Broome, R. L., Hoshino, Y. & Greenberg, H. B. ( 1996; ). Genetic mapping indicates that VP4 is the rotavirus cell attachment protein in vitro and in vivo. Journal of Virology 70, 487-493.
    [Google Scholar]
  29. Mackow, E. R., Barnett, J. W., Chan, H. & Greenberg, H. B. ( 1989; ). The rhesus rotavirus outer capsid protein VP4 functions as a hemagglutinin and is antigenically conserved when expressed by a baculovirus recombinant. Journal of Virology 63, 1661-1668.
    [Google Scholar]
  30. Martin-Villa, J. M., Ferre-Lopez, S., Lopez-Suarez, J. C., Corell, A., Perez-Blas, M. & Arnaiz-Villena, A. ( 1997; ). Cell surface phenotype and ultramicroscopic analysis of purified human enterocytes: a possible antigen-presenting cell in the intestine. Tissue Antigens 50, 586-592.[CrossRef]
    [Google Scholar]
  31. Mendez, E., Arias, C. F. & Lopez, S. ( 1993; ). Binding to sialic acids is not an essential step for the entry of animal rotaviruses to epithelial cells in culture. Journal of Virology 67, 5253-5259.
    [Google Scholar]
  32. O’Connell, P. J., Faull, R., Russ, G. R. & D’Apice, A. J. ( 1991; ). VLA-2 is a collagen receptor on endothelial cells. Immunology and Cell Biology 69, 103-110.[CrossRef]
    [Google Scholar]
  33. Offit, P. A., Blavat, G., Greenberg, H. B. & Clark, H. F. ( 1986; ). Molecular basis of rotavirus virulence: role of gene segment 4. Journal of Virology 57, 46-49.
    [Google Scholar]
  34. Prasad, B. V., Wang, G. J., Clerx, J. P. & Chiu, W. ( 1988; ). Three-dimensional structure of rotavirus. Journal of Molecular Biology 199, 269-275.[CrossRef]
    [Google Scholar]
  35. Prasad, B. V., Burns, J. W., Marietta, E., Estes, M. K. & Chiu, W. ( 1990; ). Localization of VP4 neutralization sites in rotavirus by three-dimensional cryo-electron microscopy. Nature 343, 476-479.[CrossRef]
    [Google Scholar]
  36. Ramig, R. F. & Galle, K. L. ( 1990; ). Rotavirus genome segment 4 determines viral replication phenotype in cultured liver cells (HepG2). Journal of Virology 64, 1044-1049.
    [Google Scholar]
  37. Sato, K., Inaba, Y., Shinozaki, T., Fujii, R. & Matumoto, M. ( 1981; ). Isolation of human rotavirus in cell cultures: brief report. Archives of Virology 69, 155-160.[CrossRef]
    [Google Scholar]
  38. Shibahara, T., Si-Tahar, M., Shaw, S. K. & Madara, J. L. ( 2000; ). Adhesion molecules expressed on homing lymphocytes in model intestinal epithelia. Gastroenterology 118, 289-298.[CrossRef]
    [Google Scholar]
  39. Smart, C. J., Calabrese, A., Oakes, D. J., Howdle, P. D. & Trejdosiewicz, L. K. ( 1991; ). Expression of the LFA-1 beta 2 integrin (CD11a/CD18) and ICAM-1 (CD54) in normal and coeliac small bowel mucosa. Scandinavian Journal of Immunology 34, 299-305.[CrossRef]
    [Google Scholar]
  40. Staatz, W. D., Fok, K. F., Zutter, M. M., Adams, S. P., Rodriguez, B. A. & Santoro, S. A. ( 1991; ). Identification of a tetrapeptide recognition sequence for the alpha 2 beta 1 integrin in collagen. Journal of Biological Chemistry 266, 7363-7367.
    [Google Scholar]
  41. Superti, F. & Donelli, G. ( 1995; ). Characterization of SA-11 rotavirus receptorial structures on human colon carcinoma cell line HT-29. Journal of Medical Virology 47, 421-428.[CrossRef]
    [Google Scholar]
  42. Uciechowski, P. & Schmidt, R. E. ( 1989; ). Cluster report: CD11. In Leucocyte Typing IV, pp. 543-551. Edited by W. Knapp, B. Dorken, W. R. Gilks, E. P. Rieber, R. E. Schmidt, H. Stein & A. E. G. K. von dem Borne. Oxford: Oxford University Press.
  43. Wasserman, K., Subklewe, M., Pothoff, G., Banik, N. & Schell-Frederick, E. ( 1994; ). Expression of surface markers on alveolar macrophages from symptomatic patients with HIV infection as detected by flow cytometry. Chest 105, 1324-1334.[CrossRef]
    [Google Scholar]
  44. Yeager, M., Berriman, J. A., Baker, T. S. & Bellamy, A. R. ( 1994; ). Three-dimensional structure of the rotavirus haemagglutinin VP4 by cryo-electron microscopy and difference map analysis. EMBO Journal 13, 1011-1018.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-81-9-2203
Loading
/content/journal/jgv/10.1099/0022-1317-81-9-2203
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error