1887

Abstract

Mannose-binding lectin (MBL), a C-type lectin component of the human innate immune system, binds to the gp120 envelope glycoprotein of human immunodeficiency virus type 1 (HIV-1). The objective of this study was to assess the effects of inhibitors of endoplasmic reticulum glucosidases and Golgi mannosidase as well as neuraminidase (NA) on the interaction between HIV and MBL. Production of HIV in the presence of the mannosidase I inhibitor deoxymannojirimycin (dMM) significantly enhanced binding of HIV to MBL and increased MBL neutralization of an M-tropic HIV primary isolate. In contrast, culturing HIV in the presence of α-glucosidase I and II inhibitors castanospermine and deoxynojirimycin only slightly affected virus binding and neutralization by MBL. Removal of sialic acid from HIV by NA also significantly enhanced virus binding and neutralization by MBL. Treatment of virus grown in the presence of dMM with endoglycosidase F1 substantially reduced binding to MBL, indicating that dMM increased MBL binding by increasing high-mannose carbohydrates on the virus. In contrast, endoglycosidase F1 did not decrease the MBL interaction with NA-treated virus, suggesting that NA exposed novel MBL binding sites. Treatment with dMM increased the immunocapture of HIV by monoclonal antibodies 2F5 and 2G12, indicating that altering the glycosylation of viral glycoproteins increases the accessibility or reactivity of some epitopes. This study shows that specific alterations of the -linked carbohydrates on HIV gp120/gp41 can enhance MBL-mediated neutralization of virus by strengthening the interaction of HIV-1 with MBL.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.18734-0
2003-02-01
2020-01-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/2/vir840353.html?itemId=/content/journal/jgv/10.1099/vir.0.18734-0&mimeType=html&fmt=ahah

References

  1. Back, N. K., Smit, L., De Jong, J. J., Keulen, W., Schutten, M., Goudsmit, J. & Tersmette, M. ( 1994; ). An N-glycan within the human immunodeficiency virus type 1 gp120 V3 loop affects virus neutralization. Virology 199, 431–438.[CrossRef]
    [Google Scholar]
  2. Baptista, J. A., Goss, P., Nghiem, M., Krepinsky, J. J., Baker, M. & Dennis, J. W. ( 1994; ). Measuring swainsonine in serum of cancer patients: phase I clinical trial. Clin Chem 40, 426–430.
    [Google Scholar]
  3. Barbas, C. F., III Bjorling, E., Chiodi, F. & 8 others. ( 1992; ). Recombinant human Fab fragments neutralize human type 1 immunodeficiency virus in vitro. Proc Natl Acad Sci U S A 89, 9339–9343.[CrossRef]
    [Google Scholar]
  4. Block, T. M., Lu, X., Mehta, A. S. & 7 other authors ( 1998; ). Treatment of chronic hepadnavirus infection in a woodchuck animal model with an inhibitor of protein folding and trafficking. Nat Med 4, 610–614.[CrossRef]
    [Google Scholar]
  5. Childs, R. A., Drickamer, K., Kawasaki, T., Thiel, S., Mizuochi, T. & Feizi, T. ( 1989; ). Neoglycolipids as probes of oligosaccharide recognition by recombinant and natural mannose-binding proteins of the rat and man. Biochem J 262, 131–138.
    [Google Scholar]
  6. Dedera, D., Vander Heyden, N. & Ratner, L. ( 1990; ). Attenuation of HIV-1 infectivity by an inhibitor of oligosaccharide processing. AIDS Res Hum Retrov 6, 785–794.[CrossRef]
    [Google Scholar]
  7. Ezekowitz, R. A., Kuhlman, M., Groopman, J. E. & Byrn, R. A. ( 1989; ). A human serum mannose-binding protein inhibits in vitro infection by the human immunodeficiency virus. J Exp Med 169, 185–196.[CrossRef]
    [Google Scholar]
  8. Gruters, R. A., Neefjes, J. J., Tersmette, M., de Goede, R. E., Tulp, A., Huisman, H. G., Miedema, F. & Ploegh, H. L. ( 1987; ). Interference with HIV-induced syncytium formation and viral infectivity by inhibitors of trimming glucosidase. Nature 330, 74–77.[CrossRef]
    [Google Scholar]
  9. Haurum, J. S., Thiel, S., Jones, I. M., Fischer, P. B., Laursen, S. B. & Jensenius, J. C. ( 1993; ). Complement activation upon binding of mannan-binding protein to HIV envelope glycoproteins. AIDS 7, 1307–1313.[CrossRef]
    [Google Scholar]
  10. Jack, D. L., Klein, N. J. & Turner, M. W. ( 2001; ). Mannose-binding lectin: targeting the microbial world for complement attack and opsonophagocytosis. Immunol Rev 180, 86–99.[CrossRef]
    [Google Scholar]
  11. Jacob, G. S. ( 1995; ). Glycosylation inhibitors in biology and medicine. Curr Opin Struct Biol 5, 605–611.[CrossRef]
    [Google Scholar]
  12. Karpas, A., Fleet, G. W., Dwek, R. A., Petursson, S., Namgoong, S. K., Ramsden, N. G., Jacob, G. S. & Rademacher, T. W. ( 1988; ). Aminosugar derivatives as potential anti-human immunodeficiency virus agents. Proc Natl Acad Sci U S A 85, 9229–9233.[CrossRef]
    [Google Scholar]
  13. Kawasaki, N., Kawasaki, T. & Yamashina, I. ( 1983; ). Isolation and characterization of a mannan-binding protein from human serum. J Biochem 94, 937–947.
    [Google Scholar]
  14. Leonard, C. K., Spellman, M. W., Riddle, L., Harris, R. J., Thomas, J. N. & Gregory, T. J. ( 1990; ). Assignment of intrachain disulfide bonds and characterization of potential glycosylation sites of the type 1 recombinant human immunodeficiency virus envelope glycoprotein (gp120) expressed in Chinese hamster ovary cells. J Biol Chem 265, 10373–10382.
    [Google Scholar]
  15. Ma, Y., Shida, H. & Kawasaki, T. ( 1997; ). Functional expression of human mannan-binding proteins (MBPs) in human hepatoma cell lines infected by recombinant vaccinia virus: post-translational modification, molecular assembly, and differentiation of serum and liver MBP. J Biochem 122, 810–818.[CrossRef]
    [Google Scholar]
  16. 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. Nat Med 1, 237–243.[CrossRef]
    [Google Scholar]
  17. Means, R. E. & Desrosiers, R. C. ( 2000; ). Resistance of native, oligomeric envelope on simian immunodeficiency virus to digestion by glycosidases. J Virol 74, 11181–11190.[CrossRef]
    [Google Scholar]
  18. Mehta, A., Zitzmann, N., Rudd, P. M., Block, T. M. & Dwek, R. A. ( 1998; ). Alpha-glucosidase inhibitors as potential broad based anti-viral agents. FEBS Lett 430, 17–22.[CrossRef]
    [Google Scholar]
  19. Montefiori, D. C., Robinson, W. E., Jr. & Mitchell, W. M. ( 1988; ). Role of protein N-glycosylation in pathogenesis of human immunodeficiency virus type 1. Proc Natl Acad Sci U S A 85, 9248–9252.[CrossRef]
    [Google Scholar]
  20. Moore, J. P., Wallace, L. A., Follett, E. A. & McKeating, J. A. ( 1989; ). An enzyme-linked immunosorbent assay for antibodies to the envelope glycoproteins of divergent strains of HIV-1. AIDS 3, 155–163.[CrossRef]
    [Google Scholar]
  21. Moore, J. P., Sattentau, Q. J., Wyatt, R. & Sodroski, J. ( 1994; ). Probing the structure of the human immunodeficiency virus surface glycoprotein gp120 with a panel of monoclonal antibodies. J Virol 68, 469–484.
    [Google Scholar]
  22. Muster, T., Steindl, F., Purtscher, M., Trkola, A., Klima, A., Himmler, G., Ruker, F. & Katinger, H. ( 1993; ). A conserved neutralizing epitope on gp41 of human immunodeficiency virus type 1. J Virol 67, 6642–6647.
    [Google Scholar]
  23. Neth, O., Jack, D. L., Dodds, A. W., Holzel, H., Klein, N. J. & Turner, M. W. ( 2000; ). Mannose-binding lectin binds to a range of clinically relevant microorganisms and promotes complement deposition. Infect Immun 68, 688–693.[CrossRef]
    [Google Scholar]
  24. Ohtani, K., Suzuki, Y., Eda, S. & 7 other authors ( 1999; ). High-level and effective production of human mannan-binding lectin (MBL) in Chinese hamster ovary (CHO) cells. J Immunol Methods 222, 135–144.[CrossRef]
    [Google Scholar]
  25. Petersen, S. V., Thiel, S. & Jensenius, J. C. ( 2001; ). The mannan-binding lectin pathway of complement activation: biology and disease association. Mol Immunol 38, 133–149.[CrossRef]
    [Google Scholar]
  26. Purtscher, M., Trkola, A., Gruber, G., Buchacher, A., Predl, R., Steindl, F., Tauer, C., Berger, R., Barrett, N., Jungbauer, A. and others ( 1994; ). A broadly neutralizing human monoclonal antibody against gp41 of human immunodeficiency virus type 1. AIDS Res Hum Retroviruses 10, 1651–1658.[CrossRef]
    [Google Scholar]
  27. Saifuddin, M., Hart, M. L., Gewurz, H., Zhang, Y. & Spear, G. T. ( 2000; ). Interaction of mannose-binding lectin with primary isolates of human immunodeficiency virus type 1. J Gen Virol 81, 949–955.
    [Google Scholar]
  28. Sanders, R. W., Venturi, M., Schiffner, L., Kalyanaraman, R., Katinger, H., Lloyd, K. O., Kwong, P. D. & Moore, J. P. ( 2002; ). The mannose-dependent epitope for neutralizing antibody 2G12 on human immunodeficiency virus type 1 glycoprotein gp120. J Virol 76, 7293–7305.[CrossRef]
    [Google Scholar]
  29. Scanlan, C. N., Pantophlet, R., Wormald, M. R. & 7 other authors ( 2002; ). The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of α1→2 mannose residues on the outer face of gp120. J Virol 76, 7306–7321.[CrossRef]
    [Google Scholar]
  30. Sears, P. & Wong, C. H. ( 1998; ). Enzyme action in glycoprotein synthesis. Cell Mol Life Sci 54, 223–252.[CrossRef]
    [Google Scholar]
  31. Takefman, D. M., Sullivan, B. L., Sha, B. E. & Spear, G. T. ( 1998; ). Mechanisms of resistance of HIV-1 primary isolates to complement-mediated lysis. Virology 246, 370–378.[CrossRef]
    [Google Scholar]
  32. Tierney, M., Pottage, J., Kessler, H. & other authors ( 1995; ). The tolerability and pharmacokinetics of N-butyl-deoxynojirimycin in patients with advanced HIV disease (ACTG 100). The AIDS Clinical Trials Group (ACTG) of the National Institute of Allergy and infectious Diseases. J Acquir Immune Defic Syndr Hum Retrovirol 10, 549–553.[CrossRef]
    [Google Scholar]
  33. Trkola, A., Purtscher, M., Muster, T. & 7 other authors ( 1996; ). Human monoclonal antibody 2G12 defines a distinctive neutralization epitope on the gp120 glycoprotein of human immunodeficiency virus type 1. J Virol 70, 1100–1108.
    [Google Scholar]
  34. van Emmerik, L. C., Kuijper, E. J., Fijen, C. A., Dankert, J. & Thiel, S. ( 1994; ). Binding of mannan-binding protein to various bacterial pathogens of meningitis. Clin Exp Immunol 97, 411–416.
    [Google Scholar]
  35. Walker, B. D., Kowalski, M., Goh, W. C., Kozarsky, K., Krieger, M., Rosen, C., Rohrschneider, L., Haseltine, W. A. & Sodroski, J. ( 1987; ). Inhibition of human immunodeficiency virus syncytium formation and virus replication by castanospermine. Proc Natl Acad Sci U S A 84, 8120–8124.[CrossRef]
    [Google Scholar]
  36. Weis, W. I., Taylor, M. E. & Drickamer, K. ( 1998; ). The C-type lectin superfamily in the immune system. Immunol Rev 163, 19–34.[CrossRef]
    [Google Scholar]
  37. Wyatt, R., Kwong, P. D., Desjardins, E., Sweet, R. W., Robinson, J., Hendrickson, W. A. & Sodroski, J. G. ( 1998; ). The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393, 705–711.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.18734-0
Loading
/content/journal/jgv/10.1099/vir.0.18734-0
Loading

Data & Media loading...

Most cited articles

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