Human Immunodeficiency Virus Tat Protein Aids V Region Somatic Hypermutation in Human B Cells

mBio. 2018 Apr 17;9(2):e02315-17. doi: 10.1128/mBio.02315-17.

Abstract

Long-term survivors of human immunodeficiency virus (HIV) infection have been shown to have a greatly increased incidence of B cell lymphomas. This increased lymphomagenesis suggests some link between HIV infection and the destabilization of the host B cell genome, a phenomenon also suggested by the extraordinary high frequency of mutation, insertion, and deletion in the broadly neutralizing HIV antibodies. Since HIV does not infect B cells, the molecular mechanisms of this genomic instability remain to be fully defined. Here, we demonstrate that the cell membrane-permeable HIV Tat proteins enhance activation-induced deaminase (AID)-mediated somatic hypermutation (SHM) of antibody V regions through their modulation of the endogenous polymerase II (Pol II) transcriptional process. Extremely small amounts of Tat that could come from bystander HIV-infected cells were sufficient to promote SHM. Our data suggest HIV Tat is one missing link between HIV infection and the overall B cell genomic instability in AIDS patients.IMPORTANCE Although the introduction of antiretroviral therapy (ART) has successfully controlled primary effects of human immunodeficiency virus (HIV) infection, such as HIV proliferation and HIV-induced immune deficiency, it did not eliminate the increased susceptibility of HIV-infected patients to B cell lymphomas. We find that a secreted HIV protein, Tat, enhances the intrinsic antibody diversification mechanism by increasing the AID-induced somatic mutations at the heavy-chain variable (VH) regions in human B cells. This could contribute to the high rate of mutation in the variable regions of broadly neutralizing anti-HIV antibodies and the genomewide mutations leading to B cell malignancies in HIV carriers.

Keywords: AID; AIDS; B cell; HIV; Tat; somatic hypermutation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acquired Immunodeficiency Syndrome / pathology*
  • B-Lymphocytes / immunology*
  • HIV-1 / immunology*
  • Humans
  • Immunoglobulin Variable Region / genetics*
  • RNA Polymerase II / metabolism*
  • Somatic Hypermutation, Immunoglobulin*
  • tat Gene Products, Human Immunodeficiency Virus / metabolism*

Substances

  • Immunoglobulin Variable Region
  • tat Gene Products, Human Immunodeficiency Virus
  • RNA Polymerase II