Effects of the antifungal agent ciclopirox in HPV-positive cancer cells: Repression of viral E6/E7 oncogene expression and induction of senescence and apoptosis

Int J Cancer. 2020 Jan 15;146(2):461-474. doi: 10.1002/ijc.32709. Epub 2019 Oct 31.

Abstract

The malignant growth of human papillomavirus (HPV)-positive cancer cells is dependent on the continuous expression of the viral E6/E7 oncogenes. Here, we examined the effects of iron deprivation on the phenotype of HPV-positive cervical cancer cells. We found that iron chelators, such as the topical antifungal agent ciclopirox (CPX), strongly repress HPV E6/E7 oncogene expression, both at the transcript and protein level. CPX efficiently blocks the proliferation of HPV-positive cancer cells by inducing cellular senescence. Although active mTOR signaling is considered to be critical for the cellular senescence response towards a variety of prosenescent agents, CPX-induced senescence occurs under conditions of severely impaired mTOR signaling. Prolonged CPX treatment leads to p53-independent Caspase-3/7 activation and induction of apoptosis. CPX also eliminates HPV-positive cancer cells under hypoxic conditions through induction of apoptosis. Taken together, these results show that iron deprivation exerts profound antiviral and antiproliferative effects in HPV-positive cancer cells and suggest that iron chelators, such as CPX, possess therapeutic potential as HPV-inhibitory, prosenescent and proapoptotic agents in both normoxic and hypoxic environments.

Keywords: cervical cancer; human papillomavirus; iron; mTOR; tumor virus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antifungal Agents / pharmacology
  • Antifungal Agents / therapeutic use
  • Apoptosis / drug effects
  • Cellular Senescence / drug effects
  • Ciclopirox / pharmacology*
  • Ciclopirox / therapeutic use
  • DNA-Binding Proteins / antagonists & inhibitors*
  • DNA-Binding Proteins / metabolism
  • Female
  • HCT116 Cells
  • HeLa Cells
  • Humans
  • Iron Chelating Agents / pharmacology
  • Iron Chelating Agents / therapeutic use
  • Oncogene Proteins, Viral / antagonists & inhibitors*
  • Oncogene Proteins, Viral / metabolism
  • Papillomavirus E7 Proteins / antagonists & inhibitors*
  • Papillomavirus E7 Proteins / metabolism
  • Papillomavirus Infections / drug therapy*
  • Papillomavirus Infections / pathology
  • Papillomavirus Infections / virology
  • Repressor Proteins / antagonists & inhibitors*
  • Repressor Proteins / metabolism
  • Spheroids, Cellular
  • Uterine Cervical Neoplasms / drug therapy*
  • Uterine Cervical Neoplasms / pathology
  • Uterine Cervical Neoplasms / virology

Substances

  • Antifungal Agents
  • DNA-Binding Proteins
  • E6 protein, Human papillomavirus type 16
  • E6 protein, Human papillomavirus type 18
  • E7 protein, Human papillomavirus type 18
  • Iron Chelating Agents
  • Oncogene Proteins, Viral
  • Papillomavirus E7 Proteins
  • Repressor Proteins
  • oncogene protein E7, Human papillomavirus type 16
  • Ciclopirox