Discovery of a Series of Acridinones as Mechanism-Based Tubulin Assembly Inhibitors with Anticancer Activity

PLoS One. 2016 Aug 10;11(8):e0160842. doi: 10.1371/journal.pone.0160842. eCollection 2016.

Abstract

Microtubules play critical roles in vital cell processes, including cell growth, division, and migration. Microtubule-targeting small molecules are chemotherapeutic agents that are widely used in the treatment of cancer. Many of these compounds are structurally complex natural products (e.g., paclitaxel, vinblastine, and vincristine) with multiple stereogenic centers. Because of the scarcity of their natural sources and the difficulty of their partial or total synthesis, as well as problems related to their bioavailability, toxicity, and resistance, there is an urgent need for novel microtubule binding agents that are effective for treating cancer but do not have these disadvantages. In the present work, our lead discovery effort toward less structurally complex synthetic compounds led to the discovery of a series of acridinones inspired by the structure of podophyllotoxin, a natural product with important microtubule assembly inhibitory activity, as novel mechanism-based tubulin assembly inhibitors with potent anticancer properties and low toxicity. The compounds were evaluated in vitro by wound healing assays employing the metastatic and triple negative breast cancer cell line MDA-MB-231. Four compounds with IC50 values between 0.294 and 1.7 μM were identified. These compounds showed selective cytotoxicity against MDA-MB-231 and DU-145 cancer cell lines and promoted cell cycle arrest in G2/M phase and apoptosis. Consistent with molecular modeling results, the acridinones inhibited tubulin assembly in in vitro polymerization assays with IC50 values between 0.9 and 13 μM. Their binding to the colchicine-binding site of tubulin was confirmed through competitive assays.

MeSH terms

  • Acridines / chemistry
  • Antineoplastic Agents / chemistry*
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects
  • Binding Sites
  • Binding, Competitive
  • Cell Cycle / drug effects
  • Cell Line, Tumor
  • Cell Movement / drug effects
  • Colchicine / metabolism
  • Drug Design
  • Drug Screening Assays, Antitumor
  • Humans
  • Models, Molecular
  • Molecular Structure
  • Podophyllotoxin / chemistry
  • Tubulin / metabolism
  • Tubulin Modulators / chemistry
  • Tubulin Modulators / pharmacology*

Substances

  • Acridines
  • Antineoplastic Agents
  • Tubulin
  • Tubulin Modulators
  • Podophyllotoxin
  • Colchicine

Grants and funding

The work was supported by the following: The State of São Paulo Research Foundation (FAPESP, grant # 2013/07600-3 – CEPID-CIBFar); The National Council for Scientific and Technological Development (CNPq, grant # 474879/2012-7 - Universal); The Coordination for the Improvement of Higher Education Personnel (CAPES); and The Carlos Chagas Filho Research Support Foundation of the State of Rio de Janeiro (FAPERJ, grants # E-26/111.474/2011 and # E-26/111.357/2014).