Potent latency reversal by Tat RNA-containing nanoparticle enables multi-omic analysis of the HIV-1 reservoir

Nat Commun. 2023 Dec 18;14(1):8397. doi: 10.1038/s41467-023-44020-5.

Abstract

The development of latency reversing agents that potently reactivate HIV without inducing global T cell activation would benefit the field of HIV reservoir research and could pave the way to a functional cure. Here, we explore the reactivation capacity of a lipid nanoparticle containing Tat mRNA (Tat-LNP) in CD4 T cells from people living with HIV undergoing antiretroviral therapy (ART). When combined with panobinostat, Tat-LNP induces latency reversal in a significantly higher proportion of latently infected cells compared to PMA/ionomycin (≈ 4-fold higher). We demonstrate that Tat-LNP does not alter the transcriptome of CD4 T cells, enabling the characterization of latently infected cells in their near-native state. Upon latency reversal, we identify transcriptomic differences between infected cells carrying an inducible provirus and non-infected cells (e.g. LINC02964, GZMA, CCL5). We confirm the transcriptomic differences at the protein level and provide evidence that the long non-coding RNA LINC02964 plays a role in active HIV infection. Furthermore, p24+ cells exhibit heightened PI3K/Akt signaling, along with downregulation of protein translation, suggesting that HIV-infected cells display distinct signatures facilitating their long-term persistence. Tat-LNP represents a valuable research tool for in vitro reservoir studies as it greatly facilitates the in-depth characterization of HIV reservoir cells' transcriptome and proteome profiles.

MeSH terms

  • Antiretroviral Therapy, Highly Active
  • CD4 Antigens / genetics
  • CD4 Antigens / metabolism
  • CD4-Positive T-Lymphocytes / drug effects
  • CD4-Positive T-Lymphocytes / virology
  • Cells, Cultured
  • Gene Products, tat* / genetics
  • Gene Products, tat* / metabolism
  • HIV Core Protein p24 / genetics
  • HIV Core Protein p24 / metabolism
  • HIV Infections / drug therapy
  • HIV Infections / genetics
  • HIV Infections / virology
  • HIV-1* / drug effects
  • HIV-1* / genetics
  • Humans
  • Ionomycin / pharmacology
  • Nanoparticles* / administration & dosage
  • Nanoparticles* / chemistry
  • Panobinostat / pharmacology
  • Proviruses / drug effects
  • Proviruses / genetics
  • RNA, Long Noncoding / metabolism
  • RNA, Viral* / administration & dosage
  • RNA, Viral* / genetics
  • RNA, Viral* / metabolism
  • Single-Cell Gene Expression Analysis
  • Virus Latency* / drug effects
  • Virus Latency* / genetics

Substances

  • Gene Products, tat
  • RNA, Viral
  • Panobinostat
  • CD4 Antigens
  • HIV Core Protein p24
  • RNA, Long Noncoding
  • Ionomycin