HIV-1 Vpu antagonism of tetherin inhibits antibody-dependent cellular cytotoxic responses by natural killer cells

J Virol. 2014 Jun;88(11):6031-46. doi: 10.1128/JVI.00449-14. Epub 2014 Mar 12.

Abstract

The type I interferon-inducible factor tetherin retains virus particles on the surfaces of cells infected with vpu-deficient human immunodeficiency virus type 1 (HIV-1). While this mechanism inhibits cell-free viral spread, the immunological implications of tethered virus have not been investigated. We found that surface tetherin expression increased the antibody opsonization of vpu-deficient HIV-infected cells. The absence of Vpu also stimulated NK cell-activating FcγRIIIa signaling and enhanced NK cell degranulation and NK cell-mediated antibody-dependent cellular cytotoxicity (ADCC). The deletion of vpu in HIV-1-infected primary CD4(+) T cells enhanced the levels of antibody binding and Fc receptor signaling mediated by HIV-positive-patient-derived antibodies. The magnitudes of antibody binding and Fc signaling were both highly correlated to the levels of tetherin on the surfaces of infected primary CD4 T cells. The affinity of antibody binding to FcγRIIIa was also found to be critical in mediating efficient Fc activation. These studies implicate Vpu antagonism of tetherin as an ADCC evasion mechanism that prevents antibody-mediated clearance of virally infected cells.

Importance: The ability of the HIV-1 accessory factor to antagonize tetherin has been considered to primarily function by limiting the spread of virus by preventing the release of cell-free virus. This study supports the hypothesis that a major function of Vpu is to decrease the recognition of infected cells by anti-HIV antibodies at the cell surface, thereby reducing recognition by antibody-dependent clearance by natural killer cells.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antibody-Dependent Cell Cytotoxicity / immunology*
  • Antigens, CD / immunology*
  • CD4-Positive T-Lymphocytes / immunology
  • CD4-Positive T-Lymphocytes / virology
  • Flow Cytometry
  • GPI-Linked Proteins / antagonists & inhibitors
  • GPI-Linked Proteins / immunology
  • Human Immunodeficiency Virus Proteins / immunology*
  • Humans
  • Jurkat Cells
  • Killer Cells, Natural / immunology*
  • Lysosomal-Associated Membrane Protein 1 / immunology
  • Opsonin Proteins / immunology
  • Receptors, IgG / immunology*
  • Receptors, IgG / metabolism
  • Signal Transduction / immunology*
  • Viral Regulatory and Accessory Proteins / immunology*

Substances

  • Antigens, CD
  • BST2 protein, human
  • FCGR3A protein, human
  • GPI-Linked Proteins
  • Human Immunodeficiency Virus Proteins
  • Lysosomal-Associated Membrane Protein 1
  • Opsonin Proteins
  • Receptors, IgG
  • Viral Regulatory and Accessory Proteins
  • vpu protein, Human immunodeficiency virus 1