Benzo(a)pyrene in Cigarette Smoke Enhances HIV-1 Replication through NF-κB Activation via CYP-Mediated Oxidative Stress Pathway

Sci Rep. 2018 Jul 10;8(1):10394. doi: 10.1038/s41598-018-28500-z.

Abstract

Smoking aggravates HIV-1 pathogenesis and leads to decreased responses to antiretroviral therapy. In this study, we aim to find a molecular mechanism that would explain smoking-induced HIV-1 replication. Benzo(a)pyrene (BaP), a major carcinogen in cigarette, requires metabolic activation through cytochrome P450s (CYPs) to exert its toxic effects. We hypothesized that CYP-mediated BaP metabolism generates reactive oxygen species (ROS), and the resultant oxidative stress aggravates HIV-1 replication. As expected, we observed ~3 to 4-fold increase in HIV-1 replication in U1 cells and human primary macrophages after chronic BaP exposure. We also observed ~30-fold increase in the expression of CYP1A1 at mRNA level, ~2.5-fold increase in its enzymatic activity as well as elevated ROS and cytotoxicity in U1 cells. The knock-down of the CYP1A1 gene using siRNA and treatment with selective CYP inhibitors and antioxidants significantly reduced HIV-1 replication. Further, we observed a nuclear translocation of NF-κB subunits (p50 and p65) after chronic BaP exposure, which was reduced by treatment with siRNA and antioxidants/CYP inhibitors. Suppression of NF-κB pathway using specific NF-κB inhibitors also significantly reduced HIV-1 replication. Altogether, our results suggest that BaP enhances HIV-1 replication in macrophages by a CYP-mediated oxidative stress pathway followed by the NF-κB pathway.

Publication types

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

MeSH terms

  • Antioxidants / pharmacology
  • Benzo(a)pyrene / chemistry
  • Benzo(a)pyrene / toxicity*
  • Carcinogens / toxicity
  • Cigarette Smoking / adverse effects
  • Cytochrome P-450 CYP1A1 / antagonists & inhibitors
  • Cytochrome P-450 CYP1A1 / genetics*
  • Gene Expression Regulation / drug effects
  • HIV-1 / drug effects*
  • Humans
  • Macrophages / drug effects
  • Macrophages / virology
  • NF-kappa B / genetics
  • Oxidative Stress / drug effects
  • Primary Cell Culture
  • RNA, Small Interfering / genetics
  • Reactive Oxygen Species / chemistry
  • Signal Transduction / drug effects
  • Virus Replication / drug effects*

Substances

  • Antioxidants
  • Carcinogens
  • NF-kappa B
  • RNA, Small Interfering
  • Reactive Oxygen Species
  • Benzo(a)pyrene
  • Cytochrome P-450 CYP1A1