Structure-guided drug design identifies a BRD4-selective small molecule that suppresses HIV

J Clin Invest. 2019 Jul 22;129(8):3361-3373. doi: 10.1172/JCI120633.

Abstract

HIV integrates its provirus into the host genome and establishes latent infection. Antiretroviral therapy (ART) can control HIV viremia, but cannot eradicate or cure the virus. Approaches targeting host epigenetic machinery to repress HIV, leading to an aviremic state free of ART, are needed. Bromodomain and extraterminal (BET) family protein BRD4 is an epigenetic reader involved in HIV transcriptional regulation. Using structure-guided drug design, we identified a small molecule (ZL0580) that induced epigenetic suppression of HIV via BRD4. We showed that ZL0580 induced HIV suppression in multiple in vitro and ex vivo cell models. Combination treatment of cells of aviremic HIV-infected individuals with ART and ZL0580 revealed that ZL0580 accelerated HIV suppression during ART and delayed viral rebound after ART cessation. Mechanistically different from the BET/BRD4 pan-inhibitor JQ1, which nonselectively binds to BD1 and BD2 domains of all BET proteins, ZL0580 selectively bound to BD1 domain of BRD4. We further demonstrate that ZL0580 induced HIV suppression by inhibiting Tat transactivation and transcription elongation as well as by inducing repressive chromatin structure at the HIV promoter. Our findings establish a proof of concept for modulation of BRD4 to epigenetically suppress HIV and provide a promising chemical scaffold for the development of probes and/or therapeutic agents for HIV epigenetic silencing.

Keywords: AIDS/HIV; Drug therapy; Epigenetics.

Publication types

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

MeSH terms

  • Anti-Retroviral Agents* / chemistry
  • Anti-Retroviral Agents* / pharmacology
  • Azepines / chemistry
  • Azepines / pharmacology
  • Cell Cycle Proteins / antagonists & inhibitors*
  • Cell Cycle Proteins / chemistry
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Drug Design
  • Female
  • HIV Infections* / drug therapy
  • HIV Infections* / genetics
  • HIV Infections* / metabolism
  • HIV Infections* / pathology
  • HIV-1 / genetics
  • HIV-1 / metabolism*
  • Humans
  • Male
  • Protein Domains
  • Structure-Activity Relationship
  • Transcription Factors / antagonists & inhibitors*
  • Transcription Factors / chemistry
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Triazoles / chemistry
  • Triazoles / pharmacology
  • tat Gene Products, Human Immunodeficiency Virus / genetics
  • tat Gene Products, Human Immunodeficiency Virus / metabolism

Substances

  • (+)-JQ1 compound
  • Anti-Retroviral Agents
  • Azepines
  • BRD4 protein, human
  • Cell Cycle Proteins
  • Transcription Factors
  • Triazoles
  • tat Gene Products, Human Immunodeficiency Virus