Enhancing the anticancer efficacy of camptothecin using biotinylated poly(ethylene glycol) conjugates in sensitive and multidrug-resistant human ovarian carcinoma cells

Cancer Chemother Pharmacol. 2002 Aug;50(2):143-50. doi: 10.1007/s00280-002-0463-1. Epub 2002 Jun 11.

Abstract

Background: Camptothecin (CPT) is an anticancer agent that kills cells by converting DNA topoisomerase I into a DNA-damaging agent. Although CPT and its derivatives are now being used to treat tumors in a variety of clinical protocols, the low water solubility of the drug and its unique pharmacodynamics and reactivity in vivo limit its delivery to cancer cells. To increase the anticancer efficacy of CPT a special drug delivery system is needed.

Purpose: To synthesize a novel camptothecin-poly(ethylene glycol) conjugate (CPT-PEG) which includes biotin as a moiety to enhance nonspecific and/or targeted uptake via the sodium-dependent multivitamin transporter (SMVT) and to evaluate its anticancer activity and apoptosis induction.

Methods: CPT-PEG and CPT-PEG-biotin conjugates were synthesized and studied in vitro in A2780 sensitive and A2780/AD multidrug-resistant human ovarian carcinoma cells. Cytotoxicity, apoptosis induction, expression of genes encoding BCL-2 and apoptotic protease-activating factor 1 (APAF-1) proteins and caspases 3 and 9 as well as caspase activity were measured.RESULTS. We found that the conjugation of CPT with a simple linear PEG polymer led to a more than 12-fold enhancement of CPT toxicity in both sensitive and multidrug-resistant cells. Biotinylation of the PEG led to a further increase in CPT toxicity (5.2 times in sensitive and 2.1 times in multidrug-resistant cells) compared to the nonbiotinylated CPT-PEG conjugate. As a result, the cytotoxicity of the CPT-PEG-biotin conjugate increased more than 60 times in sensitive and almost 30 times in resistant cells, probably by enhancing nonspecific passive and/or SMVT-mediated uptake. In contrast, the same amounts of PEG and PEG-biotin conjugates without CPT did not induce cell death in either sensitive or resistant cells. Further analysis showed that the biotinylated CPT-PEG conjugate induced apoptosis more significantly than the same equivalent concentrations of free CPT or nonbiotinylated CPT-PEG. The enhancement of proapoptotic activity was achieved by the overexpression of genes encoding the APAF-1, and caspases 3 and 9, increasing caspase activity and simultaneously downregulating the BCL-2 gene.

Conclusions: The results obtained demonstrate that the binding of CPT to PEG/PEG-biotin polymers increases its cytotoxicity, ability to induce apoptosis by the activation of caspase-dependent cell death signaling pathway and simultaneous suppression of antiapoptotic cellular defense. This suggests that the targeting approach utilizing transporters such as SMVT may substantially improve the delivery of CPT and its anticancer activity by enhancing cellular permeability and possibly retention of CPT.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Antineoplastic Agents, Phytogenic / administration & dosage*
  • Antineoplastic Agents, Phytogenic / pharmacokinetics
  • Antineoplastic Agents, Phytogenic / pharmacology
  • Apoptosis / drug effects
  • Apoptotic Protease-Activating Factor 1
  • Biological Transport
  • Biotinylation
  • Camptothecin / administration & dosage*
  • Camptothecin / pharmacokinetics
  • Camptothecin / pharmacology
  • Carrier Proteins / metabolism
  • Caspases / biosynthesis
  • Caspases / genetics
  • Drug Resistance, Multiple*
  • Drug Resistance, Neoplasm*
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Genes, bcl-2
  • Humans
  • Membrane Glycoproteins / metabolism
  • Multidrug Resistance-Associated Proteins / metabolism
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / metabolism
  • Ovarian Neoplasms / pathology*
  • Polyethylene Glycols / administration & dosage
  • Polyethylene Glycols / pharmacology
  • Protein Biosynthesis
  • Proteins / genetics
  • Proto-Oncogene Proteins c-bcl-2 / biosynthesis
  • Signal Transduction
  • Solubility
  • Symporters*
  • Tumor Cells, Cultured / drug effects

Substances

  • APAF1 protein, human
  • Antineoplastic Agents, Phytogenic
  • Apoptotic Protease-Activating Factor 1
  • Carrier Proteins
  • Membrane Glycoproteins
  • Multidrug Resistance-Associated Proteins
  • Neoplasm Proteins
  • Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • Symporters
  • biotin transporter
  • Polyethylene Glycols
  • Caspases
  • Camptothecin