Glycovirology Protocols pp 51-68

Part of the Methods in Molecular Biology book series (MIMB, volume 379)

The C Type Lectins DC-SIGN and L-SIGN

Receptors for Viral Glycoproteins
  • Pierre-Yves Lozach
  • Laura Burleigh
  • Isabelle Staropoli
  • Ali Amara

Abstract

DC-SIGN and L-SIGN are C-type lectins that recognize carbohydrate structures present on viral glycoproteins and function as attachment factors for several enveloped viruses. DC-SIGN and L-SIGN enhance viral entry and facilitate infection of cells that express the cognate entry receptor (cis-infection). They are also able to capture viruses and transfer viral infections to other target cells (trans-infection). In this chapter, we will give an overview of protocols used to produce soluble viral glycoproteins at high levels and to study the molecular basis of viruses/DC-SIGN and L-SIGN binding and internalization. We will also describe techniques to investigate the molecular mechanisms by which DC-SIGN or L-SIGN spread viral infections.

Key Words

DC-SIGN L-SIGN dendritic cells endothelial cells viruses envelope glycoproteins endocytosis viral entry infection viral transmission 

References

  1. 1.
    Figdor, C. G., van Kooyk, Y., and Adema, G. J. (2002) C-type lectin receptors on dendritic cells and Langerhans cells. Nat. Rev. Immunol. 2, 77–84.CrossRefPubMedGoogle Scholar
  2. 2.
    Soilleux, E. J., Barten, R., and Trowsdale, J. (2000) DC-SIGN; a related gene, DC-SIGNR; and CD23 form a cluster on 19pl3. J. Immunol. 165, 2937–2942.PubMedGoogle Scholar
  3. 3.
    Van Kooyk, Y. and Geijtenbeek, T. B. (2003) DC-SIGN: escape mechanism for pathogens. Nat. Rev. Immunol. 3, 697–709.CrossRefPubMedGoogle Scholar
  4. 4.
    Soilleux, E. J. (2003) DC-SIGN (dendritic cell-specific ICAM-grabbing non-integrin) and DC-SIGN-related (DC-SIGNR): friend or foe? Clin. Sci. (Lond) 104, 437–446.CrossRefGoogle Scholar
  5. 5.
    Schwartz, A. J., Alvarez, X., and Lackner, A. A. (2002) Distribution and immunophenotype of DC-SIGN-expressing cells in SIV-infected and uninfected macaques. AIDS Res. Hum. Retroviruses 18, 1021–1029.CrossRefPubMedGoogle Scholar
  6. 6.
    Knolle, P. A. and Limmer, A. (2003) Control of immune responses by savenger liver endothelial cells. Swiss Med. Wkly. 133, 501–506.PubMedGoogle Scholar
  7. 7.
    Braet, F. and Wisse, E. (2002) Structural and functional aspects of liver sinusoidal endothelial cell fenestrae: a review. Comp. Hepatol. 1, 1.CrossRefPubMedGoogle Scholar
  8. 8.
    Guo, Y., Feinberg, H., Conroy, E., et al. (2004) Structural basis for distinct ligand-binding and targeting properties of the receptors DC-SIGN and DC-SIGNR. Nat. Struct. Mol. Biol. 11, 591–598.CrossRefPubMedGoogle Scholar
  9. 9.
    Van Liempt, E., Imberty, A., Bank, C. M., et al. (2004) Molecular basis of the differences in binding properties of the highly related C-type lectins DC-SIGN and L-SIGN to Lewis X trisaccharide and schistosoma mansoni egg antigens. J. Biol. Chem. 279, 33,161–33,167.CrossRefPubMedGoogle Scholar
  10. 10.
    Lozach, P. Y., Lortat-Jacob, H., de Lacroix de Lavalette, A., et al. (2003) DC-SIGN and L-SIGN are high affinity binding receptors for hepatitis C virus glycoprotein E2. J. Biol. Chem. 278, 20,358–20,366.CrossRefPubMedGoogle Scholar
  11. 11.
    Feinberg, H., Guo, Y., Mitchell, D. A., Drickamer, K., and Weis, W. I. (2005) Extended neck regions stabilize tetramers of the receptors DC-SIGN and DC-SIGNR. J. Biol. Chem. 280, 1327–1335.CrossRefPubMedGoogle Scholar
  12. 12.
    Mitchell, D. A., Fadden, A. J., and Drickamer, K. (2001) A novel mechanism of carbohydrate recognition by the C-type lectins DC-SIGN and DC-SIGNR. Subunit organization and binding to multivalent ligands. J. Biol. Chem. 276, 28,939–28,945.CrossRefPubMedGoogle Scholar
  13. 13.
    Curtis, B. M., Scharnowske, S., and Watson, A. J. (1992) Sequence and expression of a membrane-associated C-type lectin that exhibits CD4-independent binding of human immunodeficiency virus envelope glycoprotein gp120. Proc. Natl. Acad. Sci. USA 89, 8356–8360.CrossRefPubMedGoogle Scholar
  14. 14.
    Geijtenbeek, T. B., Kwon, D. S., Torensma, R., et al. (2000) DC-SIGN, a dendritic cell-specific HIV1-binding protein that enhances trans-infection of T cells. Cell 100, 587–597.CrossRefPubMedGoogle Scholar
  15. 15.
    Pohlmann, S., Zhang, J., Baribaud, F., et al. (2003) Hepatitis C virus glycoproteins interact with DC-SIGN and DC-SIGNR. J. Virol. 11, 4070–4080.CrossRefGoogle Scholar
  16. 16.
    Lozach, P. Y., Amara, A., Bartosch, B., V et al. (2004) C-type lectins L-SIGN and DC-SIGN capture and transmit infectious hepatitis C virus pseudotype particles. J. Biol. Chem. 279, 32,035–32,045.CrossRefPubMedGoogle Scholar
  17. 17.
    Gardner, J. P., Durso, R. J., Arrigale, R. R., et al. (2003) L-SIGN (CD 209L) is a liver-specific capture receptor for hepatitis C virus. Proc. Natl. Acad. Sci. USA 100, 4498–4503.CrossRefPubMedGoogle Scholar
  18. 18.
    Halary, F., Amara, A., Lortat-Jacob, H., et al. (2002) Human cytomegalovirus binding to DC-SIGN is required for dendritic cell infection and target cell transinfection. Immunity 17, 653–664.CrossRefPubMedGoogle Scholar
  19. 19.
    Klimstra, W. B., Nangle, E. M., Smith, M. S., Yurochko, A. D., and Ryman, K. D. (2003) DC-SIGN and L-SIGN can act as attachment receptors for alphaviruses and distinguish between mosquito cell-and mammalian cell-derived viruses. J. Virol. 77, 12,022–12,032.CrossRefPubMedGoogle Scholar
  20. 20.
    Navarro-Sanchez, E., Altmeyer, R., Amara, A., et al. (2003) Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses. EMBO Rep. 4, 1–6.CrossRefGoogle Scholar
  21. 21.
    Tassaneetrithep, B., Burgess, T. H., Granelli-Piperno, A., et al. (2003) DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197, 823–829.CrossRefPubMedGoogle Scholar
  22. 22.
    Lozach, P. Y., Burleigh, L., Staropoli, L, et al. (2005) Dendritic cell-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN)-mediated enhancement of Dengue virus infection is independent of DC-SIGN internalization signals. J. Biol. Chem. 280, 23,698–23,708.CrossRefPubMedGoogle Scholar
  23. 23.
    Simmons, G., Reeves, J. D., Grogan, C. C., et al. (2003) DC-SIGN and DC-SIGNR bind ebola glycoproteins and enhance infection of macrophages and endothelial cells. Virology 305, 115–123.CrossRefPubMedGoogle Scholar
  24. 24.
    Alvarez, C. P., Lasala, F., Carrillo, J., Muniz, O., Corbi, A. L., and Delgado, R. (2002) C-type lectins DC-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans. J. Virol. 76, 6841–6844.CrossRefPubMedGoogle Scholar
  25. 25.
    Marzi, A., Gramberg, T., Simmons, G., et al. (2004) DC-SIGN and DC-SIGNR interact with the glycoprotein of Marburg virus and the S protein of severe acute respiratory syndrome coronavirus. J. Virol. 78, 12,090–12,095.CrossRefPubMedGoogle Scholar
  26. 26.
    Yang, Z. Y., Huang, Y., Ganesh, L., et al. (2004) pH-Dependent entry of severe acute respiratory syndrome coronavirus is mediated by the spike glycoprotein and enhanced by dendritic cell transfer through DC-SIGN. J. Virol. 78, 5642–5650.CrossRefPubMedGoogle Scholar
  27. 27.
    Jeffers, S. A., Tusell, S. M., Gillim-Ross, L., et al. (2004) CD209L (L-SIGN) is a receptor for severe acute respiratory syndrome coronavirus. Proc. Natl. Acad. Sci. USA 101, 15,748–15,753.CrossRefPubMedGoogle Scholar
  28. 28.
    Moris, A., Nobile, C., Buseyne, F., Porrot, F., Abastado, J. P., and Schwartz, O. (2004) DC-SIGN promotes exogenous MHC-I-restricted HIV-1 antigen presentation. Blood 103, 2648–2654.CrossRefPubMedGoogle Scholar
  29. 29.
    Turville, S. G., Santos, J. J., Frank, I., et al. (2004) Immunodeficiency virus uptake, turnover, and 2-phase transfer in human dendritic cells. Blood 103, 2170–2179.CrossRefPubMedGoogle Scholar
  30. 30.
    Lee, B., Leslie, G., Soilleux, E., et al. (2001) cis Expression of DC-SIGN allows for more efficient entry of human and simian immunodeficiency viruses via CD4 and a coreceptor. J. Virol. 75, 12,028–12,038.CrossRefPubMedGoogle Scholar
  31. 31.
    Bashirova, A. A., Geijtenbeek, T. B., van Duijnhoven, G. C., et al. (2001) A dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin (DC-SIGN)-related protein is highly expressed on human liver sinusoidal endothelial cells and promotes HIV-1 infection. J. Exp. Med. 193, 671–678.CrossRefPubMedGoogle Scholar
  32. 32.
    Larsson, M., Beignon, A. S., and Bhardwaj, N. (2004) DC-virus interplay: a double edged sword. Semin. Immunol. 16, 147–161.CrossRefPubMedGoogle Scholar
  33. 33.
    Breiner, K. M., Schaller, H., and Knolle, P. A. (2001) Endothelial cell-mediated uptake of a hepatitis B virus: a new concept of liver targeting of hepatotropic microorganisms. Hepatology 34, 803–808.CrossRefPubMedGoogle Scholar
  34. 34.
    Guidotti, L. G., Borrow, P., Brown, A., McClary, H., Koch, R., and Chisari, F. V. (1999) Noncytopathic clearance of lymphocytic choriomeningitis virus from the hepatocyte. J. Exp. Med. 189, 1555–1564.CrossRefPubMedGoogle Scholar
  35. 35.
    Berglund, P., Sjoberg, M., Garoff, H., Atkins, G. J., Sheahan, B. J., and Liljestrom, P. (1993) Semliki Forest virus expression system: production of conditionally infectious recombinant particles. Biotechnology (NY) 11, 916–920.CrossRefGoogle Scholar
  36. 36.
    Liljestrom, P. and Garoff, H. (1991) A new generation of animal cell expression vectors based on the Semliki Forest virus replicon. Biotechnology (NY) 9, 1356–1361.CrossRefGoogle Scholar
  37. 37.
    Meanger, J., Peroulis, I., and Mills, J. (1997) Modified semliki forest virus expression vector that facilitates cloning. Biotechniques 23, 432–434, 436.PubMedGoogle Scholar
  38. 38.
    Staropoli, I., Chanel, C., Girard, M., and Altmeyer, R. (2000) Processing, stability, and receptor binding properties of oligomeric envelope glycoprotein from a primary HIV-1 isolate. J. Biol. Chem. 275, 35,137–35,145.CrossRefPubMedGoogle Scholar
  39. 39.
    Kwon, D. S., Gregorio, G., Bitton, N., Hendrickson, W. A., and Littman, D. R. (2002) DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection. Immunity 16, 135–144.CrossRefPubMedGoogle Scholar
  40. 40.
    Rappocciolo, G., Jenkins, F. J., Hensler, H. R., et al. (2006) DC-SIGN is a receptor for human herpesvirus 8 on dendritic cells and macrophages. J. Immunol. 176, 1741–1749.PubMedGoogle Scholar
  41. 41.
    Davis, C. W., Nguyen, H. Y., Hanna, S. L., Sanchez, M. D., Doms, R. W., and Pierson, T. C. (2006) West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J. Virol. 80, 1290–1301.CrossRefPubMedGoogle Scholar
  42. 42.
    Garcia-Pineres, A. J., Hildesheim, A., Trivett, M., et al. (2006) Role of DC-SIGN in the activation of dendritic cells by HPV-16 L1 virus-like particle vaccine. Eur. J. Immunol. 36, 437–445.CrossRefPubMedGoogle Scholar
  43. 43.
    Burleigh, L., Lozach, P. Y., Schiffer, C., et al. (2006) Infection of dendritic cells (DCs), not DC-SIGN-mediated internalization of human immunodeficiency virus, is required for long-term transfer of virus to T cells. J. Virol. 80, 2949–2957.CrossRefPubMedGoogle Scholar

Copyright information

© Humana Press Inc., Totowa, NJ 2007

Authors and Affiliations

  • Pierre-Yves Lozach
    • 1
    • 2
  • Laura Burleigh
    • 1
  • Isabelle Staropoli
    • 1
  • Ali Amara
    • 1
  1. 1.Laboratoire de Pathogénie Virale MoléculaireInstitut PasteurParisFrance
  2. 2.UMR de Virologie Moléculaire et StructuraleCNRS 2472-INRA 1157Gif-sur-Yvette CedexFrance

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