Development of a multi-targeted chemotherapeutic approach based on G-quadruplex stabilisation and carbonic anhydrase inhibition

J Enzyme Inhib Med Chem. 2024 Dec;39(1):2366236. doi: 10.1080/14756366.2024.2366236. Epub 2024 Jun 18.

Abstract

A novel class of compounds designed to hit two anti-tumour targets, G-quadruplex structures and human carbonic anhydrases (hCAs) IX and XII is proposed. The induction/stabilisation of G-quadruplex structures by small molecules has emerged as an anticancer strategy, disrupting telomere maintenance and reducing oncogene expression. hCAs IX and XII are well-established anti-tumour targets, upregulated in many hypoxic tumours and contributing to metastasis. The ligands reported feature a berberine G-quadruplex stabiliser scaffold connected to a moiety inhibiting hCAs IX and XII. In vitro experiments showed that our compounds selectively stabilise G-quadruplex structures and inhibit hCAs IX and XII. The crystal structure of a telomeric G-quadruplex in complex with one of these ligands was obtained, shedding light on the ligand/target interaction mode. The most promising ligands showed significant cytotoxicity against CA IX-positive HeLa cancer cells in hypoxia, and the ability to stabilise G-quadruplexes within tumour cells.

Keywords: G-Quadruplex; carbonic anhydrase; multitarget-directed ligands; tumours.

MeSH terms

  • Antigens, Neoplasm / metabolism
  • Antineoplastic Agents* / chemical synthesis
  • Antineoplastic Agents* / chemistry
  • Antineoplastic Agents* / pharmacology
  • Carbonic Anhydrase IX* / antagonists & inhibitors
  • Carbonic Anhydrase IX* / metabolism
  • Carbonic Anhydrase Inhibitors* / chemical synthesis
  • Carbonic Anhydrase Inhibitors* / chemistry
  • Carbonic Anhydrase Inhibitors* / pharmacology
  • Carbonic Anhydrases* / metabolism
  • Cell Proliferation / drug effects
  • Dose-Response Relationship, Drug*
  • Drug Screening Assays, Antitumor*
  • G-Quadruplexes* / drug effects
  • HeLa Cells
  • Humans
  • Ligands
  • Models, Molecular
  • Molecular Structure
  • Structure-Activity Relationship

Substances

  • Carbonic Anhydrase Inhibitors
  • Antineoplastic Agents
  • Carbonic Anhydrase IX
  • Carbonic Anhydrases
  • Ligands
  • CA9 protein, human
  • Antigens, Neoplasm
  • carbonic anhydrase XII

Grants and funding

The authors acknowledge the financial support from: (i) Fondazione Intesa San Paolo [B/2021/0168] to PG; (ii) Fondazione Italiana per la Ricerca sul Cancro [IG 26313] and Ministero dell’Università e della Ricerca [PRIN P2022EPH87] to AR; Ministero dell’Università e della Ricerca [PRIN 2022HMJLN] to AN. ADP is the recipient of a postdoc fellowship from Fondazione Italiana per la Ricerca sul Cancro [26644]. SB acknowledges the Research Institute of the University of Bucharest for the ICUB Fellowship for Young Researchers.