Monocytes but Not Lymphocytes Carrying HIV-1 on Their Surface Transmit Infection to Human Tissue Ex Vivo

J Virol. 2016 Oct 14;90(21):9833-9840. doi: 10.1128/JVI.00742-16. Print 2016 Nov 1.

Abstract

Unprotected sexual intercourse with HIV-infected men is the major cause of new infections. HIV virions are released into semen by various cells of the male genital tract, as well as by infected monocytes and lymphocytes present in semen. Some of these virions may attach to the surfaces of cells, infected or uninfected. We investigated whether cells carrying attached HIV on their surfaces can transmit infection. We addressed this question in a model system of human tissue exposed ex vivo to monocytes and lymphocytes carrying HIV on their surfaces. We gamma irradiated the cells to prevent their productive infection. In spite of comparable amounts of HIV attached to monocytes and lymphocytes, only monocytes were capable of transmitting infection and triggering productive infection in tissue. This HIV-1 transmission was mediated by cell-cell contacts. Our experiments suggest that in vivo, HIV attached to infected or uninfected monocytes, which far outnumber lymphocytes in HIV-infected semen, may contribute to sexual transmission of HIV from men to their partners.

Importance: The vast majority of new HIV infections occur through sexual transmission, in which HIV is transferred from the semen of an infected male to an uninfected partner. In semen, HIV-1 particles may exist as free-floating virions; inside infected cells; or attached to the surfaces of cells, whether they are infected or not. Here, we investigated whether HIV attached to the surfaces of monocytes or lymphocytes could transmit infection to human tissue. Incubation of human tissue with monocyte-attached HIV resulted in productive tissue infection. In contrast, there was no infection of tissues when they were incubated with lymphocyte-attached HIV-1. Our results highlight the important role that seminal monocytes may play in HIV transmission in vivo, especially since monocytes far outnumber lymphocytes in the semen of HIV-infected individuals.

MeSH terms

  • Cell Line
  • Cell Line, Tumor
  • Female
  • HIV Infections / transmission*
  • HIV Infections / virology
  • HIV-1
  • Humans
  • Lymphocytes / virology*
  • Monocytes / virology*

Grants and funding

This work, including the efforts of Victor Barreto-de-Souza, Anush Arakelyan, Sonia Zicari, Leonid Margolis, and Christophe Vanpouille, was funded by the NICHD Intramural Program. This work, including the efforts of Victor Barreto-de-Souza, was funded by the Brazilian Ministry of Education and the Brazilian Ministry of Science and Technology.