Dual Inhibitors of P-gp and Carbonic Anhydrase XII (hCA XII) against Tumor Multidrug Resistance with Piperazine Scaffold

Molecules. 2024 Jul 11;29(14):3290. doi: 10.3390/molecules29143290.

Abstract

A new series of piperazine derivatives were synthesized and studied with the aim of obtaining dual inhibitors of P-glycoprotein (P-gp) and carbonic anhydrase XII (hCA XII) to synergistically overcome the P-gp-mediated multidrug resistance (MDR) in cancer cells expressing the two proteins, P-gp and hCA XII. Indeed, these hybrid compounds contain both P-gp and hCA XII binding groups on the two nitrogen atoms of the heterocyclic ring. All compounds showed good inhibitory activity on each protein (P-gp and hCA XII) studied individually, and many of them showed a synergistic effect in the resistant HT29/DOX and A549/DOX cell lines which overexpress both the target proteins. In particular, compound 33 displayed the best activity by enhancing the cytotoxicity and intracellular accumulation of doxorubicin in HT29/DOX and A549/DOX cells, thus resulting as promising P-gp-mediated MDR reverser with a synergistic mechanism. Furthermore, compounds 13, 27 and 32 induced collateral sensitivity (CS) in MDR cells, as they were more cytotoxic in resistant cells than in the sensitive ones; their CS mechanisms were extensively investigated.

Keywords: A549/DOX; CA XII inhibitors; HT29/DOX; K562/DOX; MDR reversers; P-gp modulators; dual P-gp/CA XII inhibitory activity; hybrid compounds; multitarget ligands; selective chemosensitizers.

MeSH terms

  • A549 Cells
  • ATP Binding Cassette Transporter, Subfamily B, Member 1* / antagonists & inhibitors
  • ATP Binding Cassette Transporter, Subfamily B, Member 1* / metabolism
  • Antineoplastic Agents / chemical synthesis
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology
  • Carbonic Anhydrase Inhibitors* / chemical synthesis
  • Carbonic Anhydrase Inhibitors* / chemistry
  • Carbonic Anhydrase Inhibitors* / pharmacology
  • Carbonic Anhydrases* / metabolism
  • Cell Line, Tumor
  • Doxorubicin / chemistry
  • Doxorubicin / pharmacology
  • Drug Resistance, Multiple* / drug effects
  • Drug Resistance, Neoplasm* / drug effects
  • HT29 Cells
  • Humans
  • Molecular Structure
  • Piperazine / chemistry
  • Piperazine / pharmacology
  • Piperazines* / chemical synthesis
  • Piperazines* / chemistry
  • Piperazines* / pharmacology
  • Structure-Activity Relationship

Substances

  • carbonic anhydrase XII
  • ATP Binding Cassette Transporter, Subfamily B, Member 1
  • Piperazines
  • Carbonic Anhydrase Inhibitors
  • Carbonic Anhydrases
  • Doxorubicin
  • Piperazine
  • Antineoplastic Agents

Grants and funding

This project was supported by grants from the University of Florence (Fondo Ricerca Ateneo RICATEN21, RICATEN22 and RICATEN23) and Compagnia di San Paolo (Fondo EX-POST 2021 to University of Torino).