1887

Abstract

The envelope protein (gp120) of human immunodeficiency virus (HIV) contains highly conserved mannosylated oligosaccharides. These glycoconjugates contribute to resistance to antibody neutralization, and binding to cell surface lectins on macrophages and dendritic cells. Mannose-binding lectin (MBL) binds to gp120 and plays a role in defence against the virus. In this study it is demonstrated that surfactant protein D (SP-D) binds to gp120 and inhibits HIV infectivity at significantly lower concentrations than MBL. The binding of SP-D was mediated by its calcium-dependent carbohydrate-binding activity and was dependent on glycosylation of gp120. Native dodecameric SP-D bound to HIV gp120 more strongly than native trimeric SP-D. Since one common polymorphic form of SP-D is predominantly expressed as trimers and associated with lower blood levels, these individuals may have less effective innate defence against HIV. A chimeric protein containing the N-terminal and collagen domains of SP-D linked to the neck and carbohydrate-recognition domains of MBL (called SP-D/MBL) had greater ability to bind to gp120 and inhibit virus replication than either SP-D or MBL. The enhanced binding of SP-D/MBL was dependent on assembly into higher molecular mass multimers (i.e. a trimeric form of the chimera did not bind to a greater extent than MBL). Hence, the enhanced binding of SP-D compared with MBL results from distinctive properties of its N-terminal and/or collagen domains. SP-D is present in lung and airway fluids, as well as in blood and various mucosal locations, and could, like MBL, play a role in restricting HIV transmission or replication .

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80764-0
2005-11-01
2020-01-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/86/11/3097.html?itemId=/content/journal/jgv/10.1099/vir.0.80764-0&mimeType=html&fmt=ahah

References

  1. Benne, C. A., Kraaijeveld, C. A., van Strijp, J. A. G., Brouwer, E., Harmsen, M., Verhoef, J., van Golde, L. M. G. & van Iwaarden, J. F. ( 1995; ). Interactions of surfactant protein A with influenza A viruses: binding and neutralization. J Infect Dis 171, 335–341.[CrossRef]
    [Google Scholar]
  2. Boniotto, M., Crovella, S., Pirulli, D. & 7 other authors ( 2000; ). Polymorphisms in the MBL2 promoter correlated with risk of HIV-1 vertical transmission and AIDS progression. Genes Immun 1, 346–348.[CrossRef]
    [Google Scholar]
  3. Borron, P., Crouch, E., Lewis, J., Wright, J., Possmayer, F. & Fraher, L. ( 1998; ). Recombinant rat surfactant-associated protein D inhibits human T lymphocyte proliferation and IL-2 production. J Immunol 161, 4599–4603.
    [Google Scholar]
  4. Borron, P. J., Mostaghel, E. A., Doyle, C., Walsh, E. S., McHeyzer-Williams, M. G. & Wright, J. R. ( 2002; ). Pulmonary surfactant proteins A and D directly suppress CD3+/CD4+ cell function: evidence for two shared mechanisms. J Immunol 169, 5844–5850.[CrossRef]
    [Google Scholar]
  5. Brinker, K. G., Martin, E., Borron, P., Mostaghel, E., Doyle, C., Harding, C. V. & Wright, J. R. ( 2001; ). Surfactant protein D enhances bacterial antigen presentation by bone-marrow derived dendritic cells. Am J Physiol 281, L1453–L1463.
    [Google Scholar]
  6. Brown-Augsburger, P., Hartshorn, K., Chang, D., Rust, K., Fliszar, C., Welgus, H. & Crouch, E. ( 1996; ). Site directed mutagenesis of Cys15 and Cys20 of pulmonary surfactant protein D: expression of a trimeric protein with altered anti-viral properties. J Biol Chem 271, 13724–13730.[CrossRef]
    [Google Scholar]
  7. Callahan, M. K., Popernack, P. M., Tsutsui, S., Truong, L., Schlegel, R. A. & Henderson, A. J. ( 2003; ). Phosphatidylserine on HIV envelope is a cofactor for infection of monocytic cells. J Immunol 170, 4840–4845.[CrossRef]
    [Google Scholar]
  8. Clark, H., Palaniyar, N., Strong, P., Edmondson, J., Hawgood, S. & Reid, K. ( 2002; ). Surfactant protein D reduces alveolar macrophage apoptosis in vivo. J Immunol 169, 2892–2899.[CrossRef]
    [Google Scholar]
  9. Crouch, E., Hartshorn, K. & Ofek, I. ( 2000; ). Collectins and pulmonary innate immunity. Immunol Rev 173, 52–65.[CrossRef]
    [Google Scholar]
  10. Ezekowitz, R. A. B., Kuhlman, M., Groopman, J. & 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]
  11. Floros, J., Lin, H., Garcia, A. & 7 other authors ( 2000; ). Surfactant protein marker alleles identify a subgroup of tuberculosis patients in a Mexican population. J Infect Dis 182, 1473–1478.[CrossRef]
    [Google Scholar]
  12. Garred, P., Madsen, H., Balslev, U., Pedersen, C., Gerstoft, J. & Svegaard, A. ( 1997; ). Susceptibility to HIV infection and progression of AIDS in relation to variant alleles of mannose-binding lectin. Lancet 349, 236–240.[CrossRef]
    [Google Scholar]
  13. Haigwood, N. L., Nara, P. L., Brooks, E. & 7 other authors ( 1992; ). Native but not denatured recombinant human immunodeficiency virus type 1 gp120 generates broad-spectrum neutralizing antibodies in baboons. J Virol 66, 172–182.
    [Google Scholar]
  14. Hammer, S. M., Gillis, J. M., Groopman, J. E. & Rose, R. M. ( 1986; ). In vitro modification of human immunodeficiency virus infection by granulocyte–macrophage colony-stimulating factor and γ interferon. Proc Natl Acad Sci U S A 83, 8734–8738.[CrossRef]
    [Google Scholar]
  15. Hart, M., Saifuddin, M. & Spear, G. ( 2003; ). Glycosylation inhibitors and neuraminidase enhance human immunodeficiency virus type 1 binding and neutralization by mannose-binding lectin. J Gen Virol 84, 353–360.[CrossRef]
    [Google Scholar]
  16. Hartshorn, K. L., Neumeyer, D., Vogt, M. V., Schooley, R. T. & Hirsch, M. S. ( 1987; ). Activity of interferons alpha, beta, and gamma against human immunodeficiency virus in vitro. AIDS Res Hum Retroviruses 3, 125–133.[CrossRef]
    [Google Scholar]
  17. Hartshorn, K. L., Collamer, M., Auerbach, M., Myers, J. B., Pavlotsky, N. & Tauber, A. I. ( 1988; ). Effects of influenza A virus on human neutrophil calcium metabolism. J Immunol 141, 1295–1301.
    [Google Scholar]
  18. Hartshorn, K. L., Sastry, K., White, M. R., Anders, E. M., Super, M., Ezekowitz, R. A. & Tauber, A. I. ( 1993; ). Human mannose-binding protein functions as an opsonin for influenza A viruses. J Clin Invest 91, 1414–1420.[CrossRef]
    [Google Scholar]
  19. 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. J Clin Invest 94, 311–319.[CrossRef]
    [Google Scholar]
  20. Hartshorn, K. L., Chang, D., Rust, K., White, M. R., Heuser, J. & Crouch, E. C. ( 1996a; ). Interactions of recombinant human pulmonary surfactant protein D and SP-D multimers with influenza A. Am J Physiol 271, L753–L762.
    [Google Scholar]
  21. Hartshorn, K. L., Reid, K. B. M., White, M. R., Jensenius, J. C., Morris, S. M., Tauber, A. I. & Crouch, E. ( 1996b; ). Neutrophil deactivation by influenza A viruses: mechanisms of protection after viral opsonization with collectins and hemagglutination-inhibiting antibodies. Blood 87, 3450–3461.
    [Google Scholar]
  22. Hartshorn, K. L., White, M. R., Shepherd, V., Reid, K., Jensenius, J. C. & Crouch, E. C. ( 1997; ). Mechanisms of anti-influenza activity of pulmonary surfactant proteins A and D: comparison with other collectins. Am J Physiol 273, L1156–1166.
    [Google Scholar]
  23. Hartshorn, K. L., Crouch, E., White, M. R., Colamussi, M. L., Kakkanatt, A., Tauber, B., Shepherd, V. & Sastry, K. N. ( 1998; ). Pulmonary surfactant proteins A and D enhance neutrophil uptake of bacteria. Am J Physiol 274, L958–L969.
    [Google Scholar]
  24. Hartshorn, K. L., White, M. R., Voelker, D. R., Coburn, J., Zaner, K. & Crouch, E. C. ( 2000; ). Mechanism of binding of surfactant surfactant protein D to influenza A viruses: importance of binding to haemagglutinin to antiviral activity. Biochem J 351, 449–458.[CrossRef]
    [Google Scholar]
  25. Hartshorn. , White, M. R. & Crouch, E. C. ( 2002; ). Contributions of the N- and C-terminal domains of surfactant protein D to the binding, aggregation, and phagocyte uptake of bacteria. Infect Immun 70, 6129–6139.[CrossRef]
    [Google Scholar]
  26. 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]
  27. Hawgood, S., Brown, C., Edmondson, J., Stumbaugh, A., Allen, L., Goerke, J., Clark, H. & Poulain, F. ( 2004; ). Pulmonary collectins modulate strain-specific influenza A virus infection and host responses. J Virol 78, 8565–8572.[CrossRef]
    [Google Scholar]
  28. Hickling, T. P., Bright, H., Wing, K., Gower, D., Martin, S. L., Sim, R. B. & Malhotra, R. ( 1999; ). A recombinant trimeric surfactant protein D carbohydrate recognition domain inhibits respiratory synctitial virus infection in vitro and in vivo. Eur J Immunol 29, 3478–3484.[CrossRef]
    [Google Scholar]
  29. Hong, P. W.-P., Flummerfelt, K. B., de Parseval, A., Gurney, K., Elder, J. H. & Lee, B. ( 2002; ). Human immunodeficiency virus envelope (gp120) binding to DC-SIGN and primary dendritic cells is carbohydrate dependent but does not involve 2G12 or cyanovirin binding sites: implications for structural analysis of gp120-DC-SIGN binding. J Virol 76, 12855–12865.[CrossRef]
    [Google Scholar]
  30. Hoshino, Y., Nakata, K., Hoshino, S., Honda, Y., Tse, D. B., Shioda, T., Rom, W. N. & Weiden, M. ( 2002; ). Maximal HIV-1 replication in alveolar macrophages during tuberculosis requires both lymphocyte contact and cytokines. J Exp Med 195, 495–505.[CrossRef]
    [Google Scholar]
  31. Husby, S., Herskind, A., Jensenius, J. & Holmkov, U. ( 2002; ). Heritability estimates for the constitutional levels of the collectins, mannan-binding lectin and lung surfactant protein D. Immunology 106, 389–394.[CrossRef]
    [Google Scholar]
  32. Lahtl, M., Lofgren, J., Martilla, T., Renko, M., Klaavenuniemi, T., Haataja, R., Ramet, M. & Hallman, M. ( 2002; ). Surfactant protein D gene polymorphism associated with severe respiratory syncytial virus infection. Pediatr Res 51, 696–699.[CrossRef]
    [Google Scholar]
  33. Leonard, C., Spellman, M., Riddle, L., Harris, R., Thomas, J. & Gregory, T. ( 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]
  34. Leth-Larsen, R., Floridon, C., Nielsen, O. & Holmskov, U. ( 2004; ). Surfactant protein D in the female genital tract. Mol Hum Reprod 10, 149–154.[CrossRef]
    [Google Scholar]
  35. Leth-Larsen, R., Garred, P., Jensenius, H. & 8 other authors ( 2005; ). A common polymorphism in the SFTPD gene influences assembly, function, and concentration of surfactant protein D. J Immunol 174, 1532–1538.[CrossRef]
    [Google Scholar]
  36. LeVine, A., Whitsett, J., Hartshorn, K. & Korfhagen, T. ( 2001; ). Surfactant protein D enhances clearance of influenza A virus from the lung in vivo. J Immunol 167, 5868–5873.[CrossRef]
    [Google Scholar]
  37. Lue, J., Hsu, M., Yang, D., Marx, P., Chen, Z. & Cheng-Mayer, C. ( 2002; ). Addition of a single gp120 glycan confers increased binding to dendritic cell-specific ICAM-3-grabbing nonintegrin and neutralization escape to human immunodeficiency virus type 1. J Virol 76, 10299–10306.[CrossRef]
    [Google Scholar]
  38. Madsen, J., Kliem, A., Tornoe, I., Skjolt, K., Koch, C. & Holmskov, U. ( 2000; ). Localization of lung surfactant protein D on mucosal surfaces in human tissues. J Immunol 164, 5866–5870.[CrossRef]
    [Google Scholar]
  39. McBride, M., Fischer, P., Sumiya, M., McClure, M., Turner, M., Skinner, C., Weber, J. & Summerfield, J. ( 1998; ). Mannose-binding protein in HIV-seropositive patients does not contribute to disease progression or bacterial infections. Int J STD AIDS 9, 683–688.[CrossRef]
    [Google Scholar]
  40. Means, R. & Desrosiers, R. ( 2000; ). Resistance of native, oligomeric envelope on simian immunodeficiency virus to digestion by glycosidases. J Virol 74, 11181–11190.[CrossRef]
    [Google Scholar]
  41. Nakata, K., Rom, W. N., Honda, Y., Condos, R., Kanegasaki, S., Cao, Y. & Weiden, M. ( 1997; ). Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication in the lung. Am J Respir Crit Care Med 155, 996–1003.[CrossRef]
    [Google Scholar]
  42. Nguyen, D. & Hildreth, J. ( 2003; ). Involvement of macrophage mannose receptor in the binding and transmission of HIV by macrophages. Eur J Immunol 33, 483–493.[CrossRef]
    [Google Scholar]
  43. Pastinen, T., Liitsola, K., Niini, P., Salminen, M. & Syvanen, A. ( 1998; ). Contribution of CCR5 and MBL genes to susceptibility to HIV type 1 infection in the Finnish population. AIDS Res Hum Retroviruses 14, 695–698.[CrossRef]
    [Google Scholar]
  44. Reading, P. C., Morey, L. S., Crouch, E. C. & Anders, E. ( 1997; ). Collectin-mediated antiviral host defense of the lung: evidence from influenza virus infection of mice. J Virol 71, 8204–8212.
    [Google Scholar]
  45. Saifuddin, M., Hart, M., Gewurz, H., Zhang, Y. & Spear, G. ( 2000; ). Interaction of mannose-binding lectin with primary isolates of human immunodeficiency virus 1. J Gen Virol 81, 949–955.
    [Google Scholar]
  46. Sanders, R., Venturi, M., Schiffner, L., Kalyanaraman, R., Katinger, H., Lloyd, K., Kwong, P. & Moore, J. ( 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]
  47. Spear, G., Zariffard, M., Xin, J. & Saifuddin, M. ( 2003; ). Inhibition of DC-sign mediated trans infection of T cells by mannose-binding lectin. Immunology 110, 80–83.[CrossRef]
    [Google Scholar]
  48. Strong, P. & Kishore, U. ( 1998; ). A novel method of purifying lung surfactant proteins A and D from the lung lavage of alveolar proteinosis patients from pooled amniotic fluid. J Immunol Methods 220, 139–149.[CrossRef]
    [Google Scholar]
  49. Super, M., Gillis, S., Foley, S., Sastry, K., Schweinle, J. E., Silverman, V. J. & Ezekowitz, R. A. B. ( 1992; ). Distinct and overlapping functions of allelic forms of human mannose binding protein. Nat Genet 2, 50–55.[CrossRef]
    [Google Scholar]
  50. Turville, S., Cameron, P., Handley, A., Lin, G., Pohlmann, S., Doms, R. & Cunningham, A. ( 2002; ). Diversity of receptors binding HIV on dendritic cell subsets. Nat Immunol 3, 975–983.[CrossRef]
    [Google Scholar]
  51. Turville, S., Wilkinson, J., Cameron, P., Dable, J. & Cunningham, A. L. ( 2003; ). The role of dendritic cell C-type lectin receptors in HIV pathogenesis. J Leukoc Biol 74, 710–718.[CrossRef]
    [Google Scholar]
  52. van de Wetering, J. K., van Golde, L. M. & Batenburg, J. J. ( 2004; ). Collectins: players of the innate immune system. Eur J Biochem 271, 1229–1249.[CrossRef]
    [Google Scholar]
  53. van Eijk, M., White, M. R., Crouch, E. C., Batenburg, J. J., Vaandrager, A. B., van Golde, L. M., Haagsman, H. P. & Hartshorn, K. L. ( 2003; ). Porcine pulmonary collectins show distinct interactions with influenza A viruses: role of the N-linked oligosaccharides in the carbohydrate recognition domain. J Immunol 171, 1431–1440.[CrossRef]
    [Google Scholar]
  54. van Eijk, M., White, M. R., Batenburg, J. J., Vaandrager, A. B., van Golde, L. M., Haagsman, H. P. & Hartshorn, K. L. ( 2004; ). Interactions of influenza A virus with sialic acids present on porcine surfactant protein D. Am J Respir Cell Mol Biol 30, 871–879.[CrossRef]
    [Google Scholar]
  55. Wei, X., Decker, J., Wang, S. & 12 other authors ( 2003; ). Antibody neutralization and escape by HIV-1. Nature 422, 307–312.[CrossRef]
    [Google Scholar]
  56. Wert, S., Yoshida, M., LeVine, A., Ikegami, M., Jones, T., Ross, G., Fisher, J., Korfhagen, T. & Whitsett, J. ( 2000; ). Increased metalloproteinase activity, oxidant production, and emphysema in surfactant protein D gene-inactivated mice. Proc Natl Acad Sci U S A 97, 5972–5977.[CrossRef]
    [Google Scholar]
  57. White, M., Crouch, E., Chang, D., Sastry, K., Guo, N., Engelich, G., Takahashi, K., Ezekowitz, R. & Hartshorn, K. ( 2000; ). Enhanced antiviral and opsonic activity of a human mannose binding lectin and surfactant protein D fusion protein. J Immunol 165, 2108–2155.[CrossRef]
    [Google Scholar]
  58. White, M., Crouch, E., Chang, D. & Hartshorn, K. ( 2001; ). Increased antiviral and opsonic activity of a highly multimerized collectin chimera. Biochem Biophys Res Commun 286, 206–213.[CrossRef]
    [Google Scholar]
  59. Wright, J. ( 1997; ). Immunomodulatory functions of surfactant. Physiol Rev 77, 931–962.
    [Google Scholar]
  60. Ying, H., Ji, X., Hart, M. L., Gupta, K., Saifuddin, M., Zariffard, M. R. & Spear, G. T. ( 2004; ). Interaction of mannose-binding lectin with HIV type 1 is sufficient for virus opsonization but not neutralization. AIDS Res Hum Retroviruses 20, 327–335.[CrossRef]
    [Google Scholar]
  61. Zhang, Y., Nakata, K., Weiden, M. & Rom, W. N. ( 1995; ). Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication by transcriptional activation at the long terminal repeat. J Clin Invest 95, 2324–2331.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.80764-0
Loading
/content/journal/jgv/10.1099/vir.0.80764-0
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