Tumor-targeting efficacy of a BF211 prodrug through hydrolysis by fibroblast activation protein-α

Acta Pharmacol Sin. 2018 Mar;39(3):415-424. doi: 10.1038/aps.2017.121. Epub 2017 Nov 9.

Abstract

BF211, a bufalin (BF) derivative, exhibits stronger anti-cancer activity than BF but with potential cardiotoxicity. Fibroblast activation protein-α (FAPα) is a membrane-bound protease specifically expressed by carcinoma-associated fibroblasts, thus has been used for the selective delivery of anticancer agents. In this study, we used a FAPα-based prodrug strategy to synthesize a dipeptide (Z-Gly-Pro)-conjugated BF211 prodrug named BF211-03. BF211-03 was hydrolyzed by recombinant human FAPα (rhFAPα) and cleaved by homogenates of human colon cancer HCT-116 or human gastric cancer MGC-803 xenografts. In contrast, BF211-03 showed good stability in plasma and in the homogenates of FAPα-negative normal tissues, such as heart and kidney. In HCT-116 and MGC-803 cells with low levels of FAPα expression, BF211-03 displayed a lower in vitro cytotoxicity than BF211 with approximately 30 to 40-fold larger IC50 values, whereas in human breast cancer MDA-MB-435 cells with high levels of FAPα expression, the IC50 value difference between BF211-03 and BF211 was small (approximately 4-fold). Although the cytotoxicity of BF211-03 against tumor cells was dramatically decreased by the chemical decoration, it was restored after cleavage of BF211-03 by rhFAPα or tumor homogenate. In HCT-116 tumor-bearing nude mice, doubling the dose of BF211-03, compared with BF211, caused less weight loss, but showing similar inhibitive effects on tumor growth. Our results suggest that BF211-03 is converted to active BF211 in tumor tissues and exhibits anti-tumor activities in tumor-bearing nude mice. FAPα-targeted BF211-03 displays tumor selectivity and may be useful as a targeting agent to improve the safety profile of cytotoxic natural products for use in cancer therapy.

MeSH terms

  • Animals
  • Bufanolides / chemistry
  • Bufanolides / metabolism*
  • Bufanolides / pharmacology
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Dipeptides / chemistry
  • Dipeptides / metabolism*
  • Dipeptides / pharmacology
  • Endopeptidases
  • Gelatinases / metabolism*
  • Humans
  • Hydrolysis
  • Membrane Proteins / metabolism*
  • Mice
  • Piperazines / chemistry
  • Piperazines / metabolism*
  • Piperazines / pharmacology
  • Prodrugs / chemistry
  • Prodrugs / metabolism*
  • Prodrugs / pharmacology
  • Serine Endopeptidases / metabolism*
  • Xenograft Model Antitumor Assays

Substances

  • BF211 compound
  • Bufanolides
  • Dipeptides
  • Membrane Proteins
  • Piperazines
  • Prodrugs
  • Endopeptidases
  • Serine Endopeptidases
  • fibroblast activation protein alpha
  • Gelatinases