Nitric oxide inhibits topoisomerase II activity and induces resistance to topoisomerase II-poisons in human tumor cells

Biochim Biophys Acta. 2016 Jul;1860(7):1519-27. doi: 10.1016/j.bbagen.2016.04.009. Epub 2016 Apr 17.

Abstract

Background: Etoposide and doxorubicin, topoisomerase II poisons, are important drugs for the treatment of tumors in the clinic. Topoisomerases contain several free sulfhydryl groups which are important for their activity and are also potential targets for nitric oxide (NO)-induced nitrosation. NO, a physiological signaling molecule nitrosates many cellular proteins, causing altered protein and cellular functions.

Methods: Here, we have evaluated the roles of NO/NO-derived species in the activity/stability of topo II both in vitro and in human tumor cells, and in the cytotoxicity of topo II-poisons, etoposide and doxorubicin.

Results: Treatment of purified topo IIα with propylamine propylamine nonoate (PPNO), an NO donor, resulted in inhibition of both the catalytic and relaxation activity in vitro, and decreased etoposide-dependent cleavable complex formation in both human HT-29 colon and MCF-7 breast cancer cells. PPNO treatment also induced significant nitrosation of topo IIα protein in these human tumor cells. These events, taken together, caused a significant resistance to etoposide in both cell lines. However, PPNO had no effect on doxorubicin-induced cleavable complex formation, or doxorubicin cytotoxicity in these cell lines.

Conclusion: Inhibition of topo II function by NO/NO-derived species induces significant resistance to etoposide, without affecting doxorubicin cytotoxicity in human tumor cells.

General significance: As tumors express inducible nitric oxide synthase and generate significant amounts of NO, modulation of topo II functions by NO/NO-derived species could render tumors resistant to certain topo II-poisons in the clinic.

Keywords: Cytotoxicity; Doxorubicin; Nitric oxide; Resistance; Topoisomerase II; VP-16.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Intramural

MeSH terms

  • Breast Neoplasms / drug therapy*
  • Breast Neoplasms / enzymology
  • Breast Neoplasms / pathology
  • Catalysis
  • Colorectal Neoplasms / drug therapy*
  • Colorectal Neoplasms / enzymology
  • Colorectal Neoplasms / pathology
  • DNA / chemistry
  • DNA / metabolism
  • DNA Topoisomerases, Type II / metabolism*
  • Dose-Response Relationship, Drug
  • Doxorubicin / pharmacology
  • Drug Resistance, Neoplasm / drug effects*
  • Enzyme Stability
  • Etoposide / pharmacology*
  • Female
  • HT29 Cells
  • Humans
  • MCF-7 Cells
  • Nitric Oxide / metabolism*
  • Nitric Oxide Donors / pharmacology*
  • Nucleic Acid Conformation
  • Protein Conformation
  • Topoisomerase II Inhibitors / pharmacology*

Substances

  • Nitric Oxide Donors
  • Topoisomerase II Inhibitors
  • Nitric Oxide
  • Etoposide
  • Doxorubicin
  • DNA
  • DNA Topoisomerases, Type II