1887

Abstract

The antiviral activity against rotaviruses of three bovine collectins, conglutinin, collectin-43 (CL-43) and bovine SP-D, was examined. As shown by ELISA and Western blot, all three collectins bound to the Nebraska calf diarrhoea virus bovine strain of rotavirus, and specifically to the VP7 glycoprotein. Inhibition by mannose or EDTA confirmed that binding was mediated through the lectin domains of the collectins. Binding resulted in haemagglutination inhibition and neutralization of rotavirus in-fectivity, CL-43 displaying the highest activity in both types of assay. In contrast, conglutinin was the most potent of the three collectins against influenza virus A/HKx31. Neutralization of rotaviruses by the lectins was dependent on glycosylation of VP7. Furthermore, rotaviruses adapted to growth in Madin-Darby bovine kidney cells, and thus bearing carbohydrate of bovine origin, remained sensitive to neutralization, although slightly less so than virus stocks propagated in the monkey kidney cell line MA104. These findings provide the first description of antiviral activity of collectins against a non-enveloped virus and may indicate a potential role for collectins in host defence against bovine rotavirus infection.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-79-9-2255
1998-09-01
2022-05-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/79/9/9747736.html?itemId=/content/journal/jgv/10.1099/0022-1317-79-9-2255&mimeType=html&fmt=ahah

References

  1. Anders E. M., Hartley C. A., Jackson D. C. 1990; Bovine and mouse serum β inhibitors of influenza A viruses are mannose-binding lectins. Proceedings of the National Academy of Sciences, USA 87:4485–4489
    [Google Scholar]
  2. Anders E. M., Hartley C. A., Reading P. C., Ezekowitz R. A. B. 1994; Complement-dependent neutralization of infuenza virus by a serum mannose-binding lectin. Journal of General Virology 75:615–622
    [Google Scholar]
  3. Andersen O., Sorensen A.-M., Svehag S.-E., Fenouillet E. 1991; Conglutinin binds the HIV-1 envelope glycoprotein gp160 and inhibits its interaction with cell membrane CD4. Scandinavian Journal of Immunology 33:81–88
    [Google Scholar]
  4. Both G. W., Mattick J. S., Bellamy A. R. 1983; The serotype- specific glycoprotein of simian-11 rotavirus: coding assignment and gene sequence. Proceedings of the National Academy of Sciences, USA 80:3091–3095
    [Google Scholar]
  5. Bridger J. C. 1994; A definition of rotavirus virulence. Journal of General Virology 75:2807–2812
    [Google Scholar]
  6. Burke B., Desselberger U. 1996; Rotavirus pathogenicity. Virology 218:299–305
    [Google Scholar]
  7. Caust J., Dyall-Smith M. L., Lazdins I. H., Holmes I. H. 1987; Glycosylation, an important modifier of rotavirus antigenicity. Archives of Virology 96:123–134
    [Google Scholar]
  8. Chen C. C., Baylor M., Bass D. M. 1993; Murine intestinal mucins inhibit rotavirus infection. Gastroenterology 105:84–92
    [Google Scholar]
  9. Colman P. M., Ward C. W. 1985; Structure and diversity of influenza virus neuraminidase. Current Topics in Microbiology and Immunology 114:177–255
    [Google Scholar]
  10. 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
    [Google Scholar]
  11. Crouch E., Parghi D., Kuan S. F., Persson A. 1992; Surfactant protein D : subcellular localisation in nonciliated bronchiolar epithelial cells. American Journal of Physiology 263, L60-L66
    [Google Scholar]
  12. Eliakim R., Becich M. J., Green K., Alpers D. H. 1991; Developmental expression of intestinal surfactant-like particles in rats. American Journal of Physiology 261:G269–G279
    [Google Scholar]
  13. Estes M. K. 1996; Rotaviruses and their replication. In Fields Virology, 3rd edn. pp 1625–1655 Fields B. N., Knipe D. M., Howely P. M. Edited by Philadelphia: Lippincott-Raven;
    [Google Scholar]
  14. Estes M. K., Cohen J. 1989; Rotavirus gene structure and function. Microbiological Reviews 53:410–449
    [Google Scholar]
  15. Estes M. K., Graham D. Y., Ramig R. F., Ericson B. L. 1982; Heterogeneity in the structural glycoprotein (VP7) of simian rotavirus SA11. Virology 122:8–14
    [Google Scholar]
  16. Ezekowitz R. A. B., Kuhlman M., Groopman J. E., Byrn R. A. 1989; A human serum mannose-binding protein inhibits in vitro infection by the human immunodeficiency virus. Journal of Experimental Medicine 169:185–196
    [Google Scholar]
  17. Ezekowitz R. A. B., Sastry K. W., Reid K. B. M.editors 1996 Collectins and Innate Immunity Austin, Texas: R. G. Landes;
    [Google Scholar]
  18. Fischer P. B., Ellermann-Eriksen S., Thiel S., Jensenius J. C., Mogensen S. C. 1994; Mannan-binding protein and bovine con- glutinin mediate enhancement of herpes simplex type 2 infection in mice. Scandinavian Journal of Immunology 39:439–445
    [Google Scholar]
  19. Fisher J. H., Mason R. 1995; Expression of pulmonary surfactant protein D in rat gastric mucosa. American Journal of Respiratory Cell and Molecular Biology 12:13–18
    [Google Scholar]
  20. Glass R. I., Keith J., Nakagomi O., Nakagomi T., Askaa J., Kapikian A. Z., Chanock R. M., Flores J. 1985; Nucleotide sequence of the structural glycoprotein VP7 gene of Nebraska calf diarrhea virus rotavirus : comparison with homologous genes from four strains of human and animal rotaviruses. Virology 141:292–298
    [Google Scholar]
  21. Hartley C. A., Jackson D. C., Anders E. M. 1992; Two distinct serum mannose-binding lectins function as β inhibitors of influenza virus: identification of bovine serum β inhibitor as conglutinin. Journal of Virology 66:4358–4363
    [Google Scholar]
  22. Hartshorn K. L., Sastry K., Brown D., White M. R., Okarma T. B., Lee Y.-M., Tauber A. I. 1993a; Conglutinin acts as an opsonin for influenza A viruses. Journal of Immunology 151:6265–6273
    [Google Scholar]
  23. Hartshorn K. L., Sastry K., White M. R., Anders E. M., super M., Ezekowitz R. A. B., Tauber A. I. 1993b; Human mannose-binding protein functions as an opsonin for influenza A viruses. Journal of Clinical Investigation 91:1414–1420
    [Google Scholar]
  24. Hartshorn K. L., Crouch E. C., White M. R., Eggleton P., Tauber A. I., Chang D., Sastry K. 1994; Evidence for a protective role of pulmonary surfactant protein D (SP-D) against influenza A viruses. Journal of Clinical Investigation 94:311–319
    [Google Scholar]
  25. Holmskov U., Teisner B., Pedersen N. T., Laursen S. B., Rasmussen H. B., Jensenius J. C. 1992; Tissue localization of conglutinin, a bovine C-type lectin. Immunology 76:169–173
    [Google Scholar]
  26. Holmskov U., Teisner B., Willis A. C., Reid K. B. M., Jensenius J. C. 1993; Purification and characterization of a bovine serum lectin (CL-43) with structural homology to conglutinin and SP-D and carbohydrate specificity similar to mannan-binding protein. Journal of Biological Chemistry 268:10120–10125
    [Google Scholar]
  27. Holmskov U., Malhotra R., Sim R. B., Jensenius J. 1994; Collectins : collagenous C-type lectins of the innate immune defense system. Immunology Today 15:67–74
    [Google Scholar]
  28. Holmskov U., Laursen S. B., Malhotra R., Wiedemann H., Timpl R., Stuart G. R., Tornøe A., Madsen P. S., Reid K. B. M., Jensenius J. C. 1995; Comparative study of the structural and functional properties of a bovine C-type lectin, collectin-43, with other collectins. Biochemical Journal 305:889–896
    [Google Scholar]
  29. Hoppe H.-J., Reid K. B. M. 1994; Collectins - soluble proteins containing collagenous regions and lectin domains - and their role in innate immunity. Protein Science 3:1143–1158
    [Google Scholar]
  30. Huang J., Nagesha H. S., Snodgrass D. R., Holmes I. H. 1992; Molecular and serological analyses of two bovine rotaviruses (B-ll and B-60) causing calf scours in Australia. Journal of Clinical Microbiology 30:85–92
    [Google Scholar]
  31. Ingram D. G., Mitchell W. R. 1970; Conglutinin levels in dairy cattle: changes associated with parturition. American Journal of Veterinary Research 31:487–492
    [Google Scholar]
  32. Kabcenell A. K., Atkinson P. H. 1985; Processing of the rough endoplasmic reticulum membrane glycoproteins of rotavirus SAll. Journal of Cell Biology 101:l270–l280
    [Google Scholar]
  33. 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
    [Google Scholar]
  34. Kilbourne E. D. 1969; Future influenza vaccines and the use of genetic recombinants. Bulletin of the World Health Organization 41:643–645
    [Google Scholar]
  35. Kornfeld R., Kornfeld S. 1985; Assembly of asparagine-linked oligosaccharides. Annual Review of Biochemistry 54:631–664
    [Google Scholar]
  36. Kouvelos K., Petric M., Middleton P. J. 1984; Oligosaccharide composition of calf rotavirus. Journal of General Virology 65:1159–1164
    [Google Scholar]
  37. Lardins I., Coulson B. S., Kirkwood C., Dyall-Smith M., Masendycz P. J., Sonza S., Holmes I. H. 1995; Rotavirus antigenicity is affected by the genetic context and glycosylation of VP7. Virology 209:80–89
    [Google Scholar]
  38. Lim B., Willis A. C., Reid K. B. M., Lu J., Laursen S. B., Jensenius J. C., Holmskov U. 1994; Primary structure of bovine collectin-43 (CL-43). Comparison with conglutinin and lung surfactant protein-D. Journal of Biological Chemistry 269:11820–11824
    [Google Scholar]
  39. Loveless R. W., Holmskov U., Feizl T. 1995; Collectin-43 is a serum lectin with a distinct pattern of carbohydrate recognition. Immunology 85:651–659
    [Google Scholar]
  40. 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]
  41. Malherbe H. H., Strickland-Cholmley M. 1967; Simian virus SA-11 and the related O agent. Archiv für die Gesamte Virusforschung 22:235–245
    [Google Scholar]
  42. Malhotra R., Haurum J. S., Thiel S., Sim R. B. 1994; Binding of human collectins (SP-A and MBP) to influenza virus. Biochemical Journal 304:455–461
    [Google Scholar]
  43. Malhotra R., Wormald M. R., Rudd P. M., Fischer P. B., Dwek R. A., Sim R. B. 1995; Glycosylation changes of IgG associated with rheumatoid arthritis can activate complement via the mannose-binding protein. Nature Medicine 1:207–208
    [Google Scholar]
  44. Matsui S. M., Mackow E. R., Greenberg H. B. 1989; Molecular determinant of rotavirus neutralization and protection. Advances in Virus Research 36:181–214
    [Google Scholar]
  45. Mebus C. A., Kono M., Underdahl N. R., Twiehaus M. J. 1971; Cell culture propagation of neonatal calf diarrhea (scours) virus. Canadian Veterinary Journal 12:69–72
    [Google Scholar]
  46. Motwani M., White R. A., Guo N., Dowler L. L., Tauber A. I., Sastry K. N. 1995; Mouse surfactant protein-D. cDNA cloning, characterisation, and gene localisation to chromosome 14. Journal of Immunology 155:5671–5677
    [Google Scholar]
  47. Nishimura S., Ushijima H., Nishimura S., Shiraiishi H., Kanazawa C., Abe T., Kaneko K., Fukuyama Y. 1993; Detection of rotavirus in cerebrospinal fluid and blood from patients with convulsions and gastroenteritis by means of reverse transcription polymerase chain reaction. Brain & Development 15:457–459
    [Google Scholar]
  48. Palmer D. F., Coleman M. T., Dowdle W. R., Schild G. C. 1975 Laboratory Techniques for Influenza Diagnosis Atlanta, Georgia: US Department of Health, Education and Welfare;
    [Google Scholar]
  49. Reading P. C., Morey L. S., Crouch E. C., Anders E. M. 1997; Collectin-mediated antiviral host defence of the lung: evidence from influenza virus infection of mice. Journal of Virology 71:8204–8212
    [Google Scholar]
  50. Riepenhoff-Talty M., Lee P., Carmody P. J., Barrett H. J., Ogra P. L. 1982; Age-dependent rotavirus-enterocyte interactions. Pro-ceedings of the Society for Experimental Biology and Medicine 170:146–154
    [Google Scholar]
  51. Ruggeri F. M., Greenberg H. B. 1991; Antibodies to the trypsin cleavage peptide VP8 neutralize rotavirus by inhibiting binding of virions to target cells in culture. Journal of Virology 65:2211–2219
    [Google Scholar]
  52. Solís D., Feizi T., Yuen C., Lawson A. M., Harrison R. A., Loveless R. W. 1994; Differential recognition of conglutinin and mannan- binding protein of N-glycans presented on neoglycolipids and glycoproteins with special reference to complement glycoprotein C3 and ribonuclease B. Journal of Biological Chemistry 269:11555–11562
    [Google Scholar]
  53. Sonza S., Breschkin A. M., Holmes I. H. 1984; The major surface glycoprotein of simian rotavirus (SA11) contains distinct epitopes. Virology 134:318–327
    [Google Scholar]
  54. Thiel S., Reid K. B. M. 1989; Structures and functions associated with the group of mammalian lectins containing collagen-like sequences. FEBS Letters 250:78–84
    [Google Scholar]
  55. Tzipori S. R., Makin T. J., Smith M. L., Krautil F. L. 1981; Clinical manifestations of diarrhea in calves infected with rotavirus and enterotoxigenic Escherichia coli. Journal of Clinical Microbiology 13:1011–1016
    [Google Scholar]
  56. Ward C. W., Dopheide T. A. 1981; Amino acid sequence and oligosaccharide distribution of the haemagglutinin of an early Hong Kong influenza virus variant A/Aichi/2/68 (X-31). Biochemical Journal 193:953–962
    [Google Scholar]
  57. Woode G. N., Kelso N. E., Simpson T. F., Gaul S. K., Evans L. E., Babiuk L. 1983; Antigenic relationships among some bovine rotaviruses : serum neutralization and cross protection in gnotobiotic calves. Journal of Clinical Microbiology 18:358–364
    [Google Scholar]
  58. Xu L., Harbour D., McCrae M. A. 1991; Sequence of the gene encoding the major neutralization antigen (VP7) of serotype 10 rotavirus. Journal of General Virology 72:177–180
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-79-9-2255
Loading
/content/journal/jgv/10.1099/0022-1317-79-9-2255
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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