1887

Journal of General Virology header logo

Volume 87, Issue 9

L-SIGN (CD209L) isoforms differently mediate -infection of hepatoma cells by hepatitis C virus pseudoparticles Free

Abstract

L-SIGN is a C-type lectin that is expressed on liver sinusoidal endothelial cells. Capture of (HCV) by this receptor results in -infection of hepatoma cells. L-SIGN alleles have been identified that encode between three and nine tandem repeats of a 23 residue stretch in the juxtamembrane oligomerization domain. Here, it was shown that these repeat-region isoforms are expressed at the surface of mammalian cells and variably bind HCV envelope glycoprotein E2 and HCV pseudoparticles. Differences in binding were reflected in -infection efficiency, which was highest for isoform 7 and lowest for isoform 3. These findings provide a molecular mechanism whereby L-SIGN polymorphism could influence the establishment and progression of HCV infection.

  • Received:
  • Accepted:
  • Published Online:
SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.82034-0
2006-09-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/jgv/87/9/2571.html?itemId=/content/journal/jgv/10.1099/vir.0.82034-0&mimeType=html&fmt=ahah

References

  1. Alvarez C. P., Lasala F., Carrillo J., Muñiz O., Corbí A. L., 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 [CrossRef]
     [Google Scholar]
  2. Baribaud F., Pöhlmann S., Sparwasser T. & 13 other authors 2001; Functional and antigenic characterization of human, rhesus macaque, pigtailed macaque, and murine DC-SIGN. J Virol 75:10281–10289 [CrossRef]
     [Google Scholar]
  3. Bartosch B., Vitelli A., Granier C. & 7 other authors 2003; Cell entry of hepatitis C virus requires a set of co-receptors that include the CD81 tetraspanin and the SR-B1 scavenger receptor. J Biol Chem 278:41624–41630 [CrossRef]
     [Google Scholar]
  4. Bashirova A. A., Geijtenbeek T. B. H., van Duijnhoven G. C. F. & 10 other authors 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 [CrossRef]
     [Google Scholar]
  5. Bergman M. P., Engering A., Smits H. H. & 7 other authors 2004; Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. J Exp Med 200:979–990 [CrossRef]
     [Google Scholar]
  6. Bernhard O. K., Lai J., Wilkinson J., Sheil M. M., Cunningham A. L. 2004; Proteomic analysis of DC-SIGN on dendritic cells detects tetramers required for ligand binding but no association with CD4. J Biol Chem 279:51828–51835 [CrossRef]
     [Google Scholar]
  7. Boisvert J., He X.-S., Cheung R., Keeffe E. B., Wright T., Greenberg H. B. 2001; Quantitative analysis of hepatitis C virus in peripheral blood and liver: replication detected only in liver. J Infect Dis 184:827–835 [CrossRef]
     [Google Scholar]
  8. Cambi A., Gijzen K., de Vries I. J. M. & 7 other authors 2003; The C-type lectin DC-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur J Immunol 33:532–538 [CrossRef]
     [Google Scholar]
  9. Colmenares M., Puig-Kröger A., Muñiz P. O., Corbí A. L., Rivas L. 2002; Dendritic-cell (DC)-specific intercellular adhesion molecule 3 (ICAM-3)-grabbing nonintegrin (DC-SIGN, CD209), a C-type surface lectin in human dendritic cells, is a receptor for Leishmania amastigotes. J Biol Chem 277:36766–36769 [CrossRef]
     [Google Scholar]
  10. Cooper S., Erickson A. L., Adams E. J., Kansopon J., Weiner A. J., Chien D. Y., Houghton M., Parham P., Walker C. M. 1999; Analysis of a successful immune response against hepatitis C virus. Immunity 10:439–449 [CrossRef]
     [Google Scholar]
  11. Cormier E. G., Durso R. J., Tsamis F., Boussemart L., Manix C., Olson W. C., Gardner J. P., Dragic T. 2004a; L-SIGN (CD209L) and DC-SIGN (CD209) mediate transinfection of liver cells by hepatitis C virus. Proc Natl Acad Sci U S A 101:14067–14072 [CrossRef]
     [Google Scholar]
  12. Cormier E. G., Tsamis F., Kajumo F., Durso R. J., Gardner J. P., Dragic T. 2004b; CD81 is an entry coreceptor for hepatitis C virus. Proc Natl Acad Sci U S A 101:7270–7274 [CrossRef]
     [Google Scholar]
  13. Feinberg H., Guo Y., Mitchell D. A., Drickamer K., Weis W. I. 2005; Extended neck regions stabilize tetramers of the receptors DC-SIGN and DC-SIGNR. J Biol Chem 280:1327–1335 [CrossRef]
     [Google Scholar]
  14. Fournier C., Sureau C., Coste J., Ducos J., Pageaux G., Larrey D., Domergue J., Maurel P. 1998; In vitro infection of adult normal human hepatocytes in primary culture by hepatitis C virus. J Gen Virol 79:2367–2374
     [Google Scholar]
  15. Fry D. E., Flint L. M., Jr. 1997; Hepatitis: an overview of important issues. Bull Am Coll Surg 82:8–13
     [Google Scholar]
  16. Gardner J. P., Durso R. J., Arrigale R. R., Donovan G. P., Maddon P. J., Dragic T., Olson W. C. 2003; L-SIGN (CD209L) is a liver-specific capture receptor for hepatitis C virus. Proc Natl Acad Sci U S A 100:4498–4503 [CrossRef]
     [Google Scholar]
  17. Garry R. F., Dash S. 2003; Proteomics computational analyses suggest that hepatitis C virus E1 and pestivirus E2 envelope glycoproteins are truncated class II fusion proteins. Virology 307:255–265 [CrossRef]
     [Google Scholar]
  18. Geijtenbeek T. B., Torensma R., van Vliet S. J., van Duijnhoven G. C., Adema G. J., van Kooyk Y., Figdor C. G. 2000a; Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100:575–585 [CrossRef]
     [Google Scholar]
  19. Geijtenbeek T. B. H., Kwon D. S., Torensma R. & 9 other authors 2000b; DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans -infection of T cells. Cell 100:587–597 [CrossRef]
     [Google Scholar]
  20. Geijtenbeek T. B. H., van Vliet S. J., Koppel E. A., Sanchez-Hernandez M., Vandenbroucke-Grauls C. M. J. E., Appelmelk B., van Kooyk Y. 2003; Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 197:7–17
     [Google Scholar]
  21. Gramberg T., Zhu T., Chaipan C., Marzi A., Liu H., Wegele A., Andrus T., Hofmann H., Pöhlmann S. 2006; Impact of polymorphisms in the DC-SIGNR neck domain on the interaction with pathogens. Virology 347:354–363 [CrossRef]
     [Google Scholar]
  22. Guo Y., Atkinson C. E., Taylor M. E., Drickamer K. 2006; All but the shortest polymorphic forms of the viral receptor DC-SIGNR assemble into stable homo- and heterotetramers. J Biol Chem 281:16794–16798 [CrossRef]
     [Google Scholar]
  23. Halary F., Amara A., Lortat-Jacob H. & 7 other authors 2002; Human cytomegalovirus binding to DC-SIGN is required for dendritic cell infection and target cell trans -infection. Immunity 17:653–664 [CrossRef]
     [Google Scholar]
  24. Ikeda M., Sugiyama K., Mizutani T., Tanaka T., Tanaka K., Sekihara H., Shimotohno K., Kato N. 1998; Human hepatocyte clonal cell lines that support persistent replication of hepatitis C virus. Virus Res 56:157–167 [CrossRef]
     [Google Scholar]
  25. Klimstra W. B., Nangle E. M., Smith M. S., Yurochko A. D., 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 77:12022–12032 [CrossRef]
     [Google Scholar]
  26. Knolle P. A., Gerken G. 2000; Local control of the immune response in the liver. Immunol Rev 174:21–34 [CrossRef]
     [Google Scholar]
  27. Lavillette D., Tarr A. W., Voisset C. & 7 other authors 2005; Characterization of host-range and cell entry properties of the major genotypes and subtypes of hepatitis C virus. Hepatology 41:265–274 [CrossRef]
     [Google Scholar]
  28. Lechner F., Wong D. K. H., Dunbar P. R. & 7 other authors 2000; Analysis of successful immune responses in persons infected with hepatitis C virus. J Exp Med 191:1499–1512 [CrossRef]
     [Google Scholar]
  29. Lee B., Leslie G., Soilleux E. & 8 other authors 2001; cis Expression of DC-SIGN allows for more efficient entry of human and simian immunodeficiency viruses via CD4 and a coreceptor. J Virol 75:12028–12038 [CrossRef]
     [Google Scholar]
  30. Liu H., Zhu T. 2005; Determination of DC-SIGN and DC-SIGNR repeat region variations. Methods Mol Biol 304:471–481
     [Google Scholar]
  31. Liu H., Hwangbo Y., Holte S. & 8 other authors 2004; Analysis of genetic polymorphisms in CCR5, CCR2, stromal cell-derived factor-1, RANTES, and dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin in seronegative individuals repeatedly exposed to HIV-1. J Infect Dis 190:1055–1058 [CrossRef]
     [Google Scholar]
  32. Liu H., Carrington M., Wang C. & 13 other authors 2006; Repeat-region polymorphisms in the gene for the dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin-related molecule: effects on HIV-1 susceptibility. J Infect Dis 193:698–702 [CrossRef]
     [Google Scholar]
  33. Lozach P.-Y., Lortat-Jacob H., de Lacroix de Lavalette A. & 9 other authors 2003; DC-SIGN and L-SIGN are high affinity binding receptors for hepatitis C virus glycoprotein E2. J Biol Chem 278:20358–20366 [CrossRef]
     [Google Scholar]
  34. Lozach P.-Y., Amara A., Bartosch B., Virelizier J.-L., Arenzana-Seisdedos F., Cosset F.-L., Altmeyer R. 2004; C-type lectins L-SIGN and DC-SIGN capture and transmit infectious hepatitis C virus pseudotype particles. J Biol Chem 279:32035–32045 [CrossRef]
     [Google Scholar]
  35. Martin M. P., Lederman M. M., Hutcheson H. B. & 9 other authors 2004; Association of DC-SIGN promoter polymorphism with increased risk for parenteral, but not mucosal, acquisition of human immunodeficiency virus type 1 infection. J Virol 78:14053–14056 [CrossRef]
     [Google Scholar]
  36. Marzi A., Gramberg T., Simmons G. & 12 other authors 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 78:12090–12095 [CrossRef]
     [Google Scholar]
  37. McKeating J. A., Zhang L. Q., Logvinoff C. & 8 other authors 2004; Diverse hepatitis C virus glycoproteins mediate viral infection in a CD81-dependent manner. J Virol 78:8496–8505 [CrossRef]
     [Google Scholar]
  38. Mitchell D. A., Fadden A. J., 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 276:28939–28945 [CrossRef]
     [Google Scholar]
  39. Mummidi S., Catano G., Lam L., Hoefle A., Telles V., Begum K., Jimenez F., Ahuja S. S., Ahuja S. K. 2001; Extensive repertoire of membrane-bound and soluble dendritic cell-specific ICAM-3-grabbing nonintegrin 1 (DC-SIGN1) and DC-SIGN2 isoforms. Inter-individual variation in expression of DC-SIGN transcripts. J Biol Chem 276:33196–33212 [CrossRef]
     [Google Scholar]
  40. Nattermann J., Ahlenstiel G., Berg T. & 7 other authors 2006; The tandem-repeat polymorphism of the DC-SIGNR gene in HCV infection. J Viral Hepat 13:42–46 [CrossRef]
     [Google Scholar]
  41. Pileri P., Uematsu Y., Campagnoli S. & 8 other authors 1998; Binding of hepatitis C virus to CD81. Science 282:938–941 [CrossRef]
     [Google Scholar]
  42. Pohlmann S., Baribaud F., Lee B., Leslie G. J., Sanchez M. D., Hiebenthal-Millow K., Münch J., Kirchhoff F., Doms R. W. 2001a; DC-SIGN interactions with human immunodeficiency virus type 1 and 2 and simian immunodeficiency virus. J Virol 75:4664–4672 [CrossRef]
     [Google Scholar]
  43. Pöhlmann S., Soilleux E. J., Baribaud F., Leslie G. J., Morris L. S., Trowsdale J., Lee B., Coleman N., Doms R. W. 2001b; DC-SIGNR, a DC-SIGN homologue expressed in endothelial cells, binds to human and simian immunodeficiency viruses and activates infection in trans. Proc Natl Acad Sci U S A 98:2670–2675 [CrossRef]
     [Google Scholar]
  44. Pöhlmann S., Zhang J., Baribaud F. & 7 other authors 2003; Hepatitis C virus glycoproteins interact with DC-SIGN and DC-SIGNR. J Virol 77:4070–4080 [CrossRef]
     [Google Scholar]
  45. Sakuntabhai A., Turbpaiboon C., Casademont I. & 19 other authors 2005; A variant in the CD209 promoter is associated with severity of dengue disease. Nat Genet 37:507–513 [CrossRef]
     [Google Scholar]
  46. Scarselli E., Ansuini H., Cerino R. & 7 other authors 2002; The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J 21:5017–5025 [CrossRef]
     [Google Scholar]
  47. Serrano-Gómez D., Domínguez-Soto A., Ancochea J., Jimenez-Heffernan J. A., Leal J. A., Corbi A. L. 2004; Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin mediates binding and internalization of Aspergillus fumigatus conidia by dendritic cells and macrophages. J Immunol 173:5635–5643 [CrossRef]
     [Google Scholar]
  48. Snyder G. A., Ford J., Torabi-Parizi P., Arthos J. A., Schuck P., Colonna M., Sun P. D. 2005; Characterization of DC-SIGN/R interaction with human immunodeficiency virus type 1 gp120 and ICAM molecules favors the receptor's role as an antigen-capturing rather than an adhesion receptor. J Virol 79:4589–4598 [CrossRef]
     [Google Scholar]
  49. Soilleux E. J., Barten R., Trowsdale J. 2000; DC-SIGN; a related gene, DC-SIGNR; and CD23 form a cluster on 19p13. J Immunol 165:2937–2942 [CrossRef]
     [Google Scholar]
  50. Tassaneetrithep B., Burgess T. H., Granelli-Piperno A. & 10 other authors 2003; DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 197:823–829 [CrossRef]
     [Google Scholar]
  51. Yang Z.-Y., Huang Y., Ganesh L., Leung K., Kong W.-P., Schwartz O., Subbarao K., Nabel G. J. 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 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.82034-0
Loading
L-SIGN (CD209L) isoforms differently mediate trans-infection of hepatoma cells by hepatitis C virus pseudoparticles
J. Gen. Virol. 87, 2571 (2006); https://doi.org/10.1099/vir.0.82034-0
/content/journal/jgv/10.1099/vir.0.82034-0
/content/journal/jgv/10.1099/vir.0.82034-0
Loading

Data & Media loading...

Most cited 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