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PMID: 12502850 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Differential N-linked glycosylation of human immunodeficiency virus and Ebola virus envelope glycoproteins modulates interactions with DC-SIGN and DC-SIGNR.

Journal of virology ·Vol. 77 ·No. 2 ·2003-01-00 ·Pages 1337-46

Lin G, Simmons G, Pöhlmann S, Baribaud F, Ni H, Leslie GJ, Haggarty BS, Bates P, Weissman D, Hoxie JA, Doms RW

Abstract

The C-type lectins DC-SIGN and DC-SIGNR [collectively referred to as DC-SIGN(R)] bind and transmit human immunodeficiency virus (HIV) and simian immunodeficiency virus to T cells via the viral envelope glycoprotein (Env). Other viruses containing heavily glycosylated glycoproteins (GPs) fail to interact with DC-SIGN(R), suggesting some degree of specificity in this interaction. We show here that DC-SIGN(R) selectively interact with HIV Env and Ebola virus GPs containing more high-mannose than complex carbohydrate structures. Modulation of N-glycans on Env or GP through production of viruses in different primary cells or in the presence of the mannosidase I inhibitor deoxymannojirimycin dramatically affected DC-SIGN(R) infectivity enhancement. Further, murine leukemia virus, which typically does not interact efficiently with DC-SIGN(R), could do so when produced in the presence of deoxymannojirimycin. We predict that other viruses containing GPs with a large proportion of high-mannose N-glycans will efficiently interact with DC-SIGN(R), whereas those with solely complex N-glycans will not. Thus, the virus-producing cell type is an important factor in dictating both N-glycan status and virus interactions with DC-SIGN(R), which may impact virus tropism and transmissibility in vivo.

MeSH Terms
Cell Adhesion Molecules/metabolism Cell Line Ebolavirus/metabolism Glycosylation HIV/metabolism Humans Lectins, C-Type/metabolism Polysaccharides/metabolism Receptors, Cell Surface/metabolism Viral Envelope Proteins/chemistry,metabolism
Chemicals
CLEC4M protein, human Cell Adhesion Molecules DC-specific ICAM-3 grabbing nonintegrin Lectins, C-Type Polysaccharides Receptors, Cell Surface Viral Envelope Proteins
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Lin George
Hematology-Oncology Division, Department of Medicine, University of Pennsylvania, Philadelphia 19104, USA.
Simmons Graham
Pöhlmann Stefan
Baribaud Frédéric
Ni Houping
Leslie George J
Haggarty Beth S
Bates Paul
Weissman Drew
Hoxie James A
Doms Robert W
References (63)
63 references, click to expand
  1. Identification of gp120 binding sites on CXCR4 by using CD4-independent human immunodeficiency virus type 2 Env proteins.
    J Virol. 2003 Jan;77(2):931-42 PMID: 12502809
  2. Vpr is required for efficient replication of human immunodeficiency virus type-1 in mononuclear phagocytes.
    Virology. 1995 Feb 1;206(2):935-44 PMID: 7531918
  3. Use of a gp120 binding assay to dissect the requirements and kinetics of human immunodeficiency virus fusion events.
    J Virol. 1999 Dec;73(12):10346-58 PMID: 10559353
  4. Oligomeric modeling and electrostatic analysis of the gp120 envelope glycoprotein of human immunodeficiency virus.
    J Virol. 2000 Feb;74(4):1961-72 PMID: 10644369
  5. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses.
    Cell. 2000 Mar 3;100(5):575-85 PMID: 10721994
  6. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells.
    Cell. 2000 Mar 3;100(5):587-97 PMID: 10721995
  7. Crystal structure of the carbohydrate recognition domain of the H1 subunit of the asialoglycoprotein receptor.
    J Mol Biol. 2000 Jul 21;300(4):857-65 PMID: 10891274
  8. Characterization and epitope mapping of neutralizing monoclonal antibodies produced by immunization with oligomeric simian immunodeficiency virus envelope protein.
    J Virol. 2000 Sep;74(17):7922-35 PMID: 10933700
  9. DC-SIGN; a related gene, DC-SIGNR; and CD23 form a cluster on 19p13.
    J Immunol. 2000 Sep 15;165(6):2937-42 PMID: 10975799
  10. Mass spectrometric characterization of the glycosylation pattern of HIV-gp120 expressed in CHO cells.
    Biochemistry. 2000 Sep 19;39(37):11194-204 PMID: 10985765
  11. HIV gag mRNA transfection of dendritic cells (DC) delivers encoded antigen to MHC class I and II molecules, causes DC maturation, and induces a potent human in vitro primary immune response.
    J Immunol. 2000 Oct 15;165(8):4710-7 PMID: 11035115
  12. Co-receptor use by HIV and inhibition of HIV infection by chemokine receptor ligands.
    Immunol Rev. 2000 Oct;177:112-26 PMID: 11138769
  13. Structural study of N-linked oligosaccharides of human intercellular adhesion molecule-3 (CD50).
    Eur J Biochem. 2001 Feb;268(4):1020-9 PMID: 11179968
  14. 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. 2001 Feb 27;98(5):2670-5 PMID: 11226297
  15. 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. 2001 Mar 19;193(6):671-8 PMID: 11257134
  16. Ability of the V3 loop of simian immunodeficiency virus to serve as a target for antibody-mediated neutralization: correlation of neutralization sensitivity, growth in macrophages, and decreased dependence on CD4.
    J Virol. 2001 Apr;75(8):3903-15 PMID: 11264379
  17. DC-SIGN-ICAM-2 interaction mediates dendritic cell trafficking.
    Nat Immunol. 2000 Oct;1(4):353-7 PMID: 11017109
  18. DC-SIGN interactions with human immunodeficiency virus type 1 and 2 and simian immunodeficiency virus.
    J Virol. 2001 May;75(10):4664-72 PMID: 11312337
  19. 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. 2001 Aug 3;276(31):28939-45 PMID: 11384997
  20. Functional and antigenic characterization of human, rhesus macaque, pigtailed macaque, and murine DC-SIGN.
    J Virol. 2001 Nov;75(21):10281-9 PMID: 11581396
  21. The receptor DEC-205 expressed by dendritic cells and thymic epithelial cells is involved in antigen processing.
    Nature. 1995 May 11;375(6527):151-5 PMID: 7753172
  22. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products.
    J Exp Med. 1995 Aug 1;182(2):389-400 PMID: 7629501
  23. Differential glycosylation, virion incorporation, and sensitivity to neutralizing antibodies of human immunodeficiency virus type 1 envelope produced from infected primary T-lymphocyte and macrophage cultures.
    J Virol. 1996 Sep;70(9):6431-6 PMID: 8709276
  24. CD4-independent infection by HIV-2 is mediated by fusin/CXCR4.
    Cell. 1996 Nov 15;87(4):745-56 PMID: 8929542
  25. The CD4-independent tropism of human immunodeficiency virus type 2 involves several regions of the envelope protein and correlates with a reduced activation threshold for envelope-mediated fusion.
    J Virol. 1997 Feb;71(2):1453-65 PMID: 8995671
  26. CD4-independent binding of SIV gp120 to rhesus CCR5.
    Science. 1997 Nov 21;278(5342):1470-3 PMID: 9367961
  27. Host-cell-specific glycosylation of HIV-2 envelope glycoprotein.
    Glycoconj J. 1997 Nov;14(7):785-93 PMID: 9511983
  28. The antigenic structure of the HIV gp120 envelope glycoprotein.
    Nature. 1998 Jun 18;393(6686):705-11 PMID: 9641684
  29. Role of cellular adhesion molecules in HIV type 1 infection and their impact on virus neutralization.
    AIDS Res Hum Retroviruses. 1998 Oct;14 Suppl 3:S247-54 PMID: 9814951
  30. Molecular pathogenesis of filovirus infections: role of macrophages and endothelial cells.
    Curr Top Microbiol Immunol. 1999;235:175-204 PMID: 9893384
  31. HIV-1 attachment: another look.
    Trends Microbiol. 1999 Apr;7(4):144-9 PMID: 10217828
  32. Stable exposure of the coreceptor-binding site in a CD4-independent HIV-1 envelope protein.
    Proc Natl Acad Sci U S A. 1999 May 25;96(11):6359-64 PMID: 10339592
  33. DC-SIGN interactions with human immunodeficiency virus: virus binding and transfer are dissociable functions.
    J Virol. 2001 Nov;75(21):10523-6 PMID: 11581425
  34. HIV gp120 receptors on human dendritic cells.
    Blood. 2001 Oct 15;98(8):2482-8 PMID: 11588046
  35. CD4-independent use of Rhesus CCR5 by human immunodeficiency virus Type 2 implicates an electrostatic interaction between the CCR5 N terminus and the gp120 C4 domain.
    J Virol. 2001 Nov;75(22):10766-78 PMID: 11602718
  36. cis Expression of DC-SIGN allows for more efficient entry of human and simian immunodeficiency viruses via CD4 and a coreceptor.
    J Virol. 2001 Dec;75(24):12028-38 PMID: 11711593
  37. Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR.
    Science. 2001 Dec 7;294(5549):2163-6 PMID: 11739956
  38. Expression of DC-SIGN by dendritic cells of intestinal and genital mucosae in humans and rhesus macaques.
    J Virol. 2002 Feb;76(4):1866-75 PMID: 11799181
  39. DC-SIGN-mediated internalization of HIV is required for trans-enhancement of T cell infection.
    Immunity. 2002 Jan;16(1):135-44 PMID: 11825572
  40. Rhesus macaque dendritic cells efficiently transmit primate lentiviruses independently of DC-SIGN.
    Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1568-73 PMID: 11818554
  41. Ebola virus glycoproteins induce global surface protein down-modulation and loss of cell adherence.
    J Virol. 2002 Mar;76(5):2518-28 PMID: 11836430
  42. The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells.
    J Immunol. 2002 Mar 1;168(5):2118-26 PMID: 11859097
  43. Identification of different binding sites in the dendritic cell-specific receptor DC-SIGN for intercellular adhesion molecule 3 and HIV-1.
    J Biol Chem. 2002 Mar 29;277(13):11314-20 PMID: 11799126
  44. Functional evaluation of DC-SIGN monoclonal antibodies reveals DC-SIGN interactions with ICAM-3 do not promote human immunodeficiency virus type 1 transmission.
    J Virol. 2002 Jun;76(12):5905-14 PMID: 12021323
  45. C-type lectins DC-SIGN and L-SIGN mediate cellular entry by Ebola virus in cis and in trans.
    J Virol. 2002 Jul;76(13):6841-4 PMID: 12050398
  46. Quantitative expression and virus transmission analysis of DC-SIGN on monocyte-derived dendritic cells.
    J Virol. 2002 Sep;76(18):9135-42 PMID: 12186897
  47. Diversity of receptors binding HIV on dendritic cell subsets.
    Nat Immunol. 2002 Oct;3(10):975-83 PMID: 12352970
  48. Carbohydrates of human immunodeficiency virus. Structures of oligosaccharides linked to the envelope glycoprotein 120.
    J Biol Chem. 1988 Aug 25;263(24):11760-7 PMID: 2841333
  49. Carbohydrate structures of the human-immunodeficiency-virus (HIV) recombinant envelope glycoprotein gp120 produced in Chinese-hamster ovary cells.
    Biochem J. 1988 Sep 1;254(2):599-603 PMID: 2845957
  50. Diversity of oligosaccharide structures on the envelope glycoprotein gp 120 of human immunodeficiency virus 1 from the lymphoblastoid cell line H9. Presence of complex-type oligosaccharides with bisecting N-acetylglucosamine residues.
    J Biol Chem. 1990 May 25;265(15):8519-24 PMID: 2341393
  51. 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. 1990 Jun 25;265(18):10373-82 PMID: 2355006
  52. The human immunodeficiency virus type 2 vpr gene is essential for productive infection of human macrophages.
    Proc Natl Acad Sci U S A. 1990 Oct;87(20):8080-4 PMID: 2236020
  53. Glycosylation of the envelope glycoprotein from a polytropic murine retrovirus in two different host cells.
    Eur J Biochem. 1990 Nov 13;193(3):855-62 PMID: 2174368
  54. Regulated expression of foreign genes in vaccinia virus under the control of bacteriophage T7 RNA polymerase and the Escherichia coli lac repressor.
    J Virol. 1992 May;66(5):2934-42 PMID: 1560532
  55. Dendritic cells exposed to human immunodeficiency virus type-1 transmit a vigorous cytopathic infection to CD4+ T cells.
    Science. 1992 Jul 17;257(5068):383-7 PMID: 1352913
  56. 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 U S A. 1992 Sep 1;89(17):8356-60 PMID: 1518869
  57. Molecular cloning of ICAM-3, a third ligand for LFA-1, constitutively expressed on resting leukocytes.
    Nature. 1992 Dec 3;360(6403):481-4 PMID: 1448173
  58. Probing the structure of the human immunodeficiency virus surface glycoprotein gp120 with a panel of monoclonal antibodies.
    J Virol. 1994 Jan;68(1):469-84 PMID: 7504741
  59. Characterization of filoviruses based on differences in structure and antigenicity of the virion glycoprotein.
    Virology. 1994 Mar;199(2):469-73 PMID: 8122375
  60. Glycosidase inhibitors in study of glycoconjugates.
    Methods Enzymol. 1994;230:316-29 PMID: 8139504
  61. Oligosaccharide profiles of HIV-2 external envelope glycoprotein: dependence on host cells and virus isolates.
    Glycobiology. 1994 Aug;4(4):477-84 PMID: 7827409
  62. The asialoglycoprotein receptor is a potential liver-specific receptor for Marburg virus.
    J Gen Virol. 1995 Feb;76 ( Pt 2):393-9 PMID: 7844558
  63. DC-SIGN and DC-SIGNR bind ebola glycoproteins and enhance infection of macrophages and endothelial cells.
    Virology. 2003 Jan 5;305(1):115-23 PMID: 12504546
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2003-01-00
Pages
1337-46
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC140807
Subset
IM
Grants
PHS HHS · R01 35383 · United States
NIAID NIH HHS · R01 AI43455 · United States
NIAID NIH HHS · R01 AI045378 · United States
NIAID NIH HHS · R01 AI043455 · United States
NHLBI NIH HHS · HL62060-04 · United States
NIAID NIH HHS · P30 AI45008 · United States
NIAID NIH HHS · P30 AI045008 · United States
NCI NIH HHS · CA76256 · United States
NCI NIH HHS · R01 CA076256 · United States
PHS HHS · R01 40880 · United States
NIAID NIH HHS · R01 AI45378 · United States
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