Novel approaches to polynuclear platinum pro-drugs. Selective release of cytotoxic platinum-spermidine species through hydrolytic cleavage of carbamates

Inorg Chem. 2001 Nov 19;40(24):6108-14. doi: 10.1021/ic010509a.

Abstract

BBR3464 is a novel trinuclear platinum drug currently in Phase II clinical trials. Polyamine-bridged dinuclear platinum compounds as represented by [[trans-Pt(NH(3))(2)Cl](2)-mu-spermidine-N(1),N(8)]Cl(3) (1) are highly interesting second-generation analogues of BBR3464 because the hydrogen-bonding and electrostatic contributions of the central platinum-amine group in BBR3464 are replicated by the free, noncoordinated "central" quaternary nitrogens of the linear polyamine linker while the presence of two separate Pt-Cl bonds maintains the bifunctional binding mode on the DNA adducts. Preclinical investigations confirm the potency of these species with cytotoxicity in the nanomolar range. This remarkable potency results in a relatively narrow therapeutic index. To enhance the therapeutic index of these drugs, we investigated the potential for "pro-drug" delivery of less toxic and better tolerated derivatives such as the compounds [[trans-Pt(NH(3))(2)Cl](2)-mu-N(4)-R-spermidine-N(1),N(8)]Cl(2) where N(4)-R represents BOC (tert-butyl), CBz (benzyl), and Fmoc (fluorenylmethyl) carbamate blocking groups, 2-4, respectively. The bulky Fmoc derivative showed evidence for conformational isomers by (1)H NMR spectroscopy due to the inequivalence of the two n-propyl and n-butyl side chains of the spermidine moiety. The rate constants for hydrolysis and release of 1 were calculated. Release of cytotoxic 1 at physiologically relevant pH followed the order 4 > 2 > 3. The calculated values for 4 (pH 5, 6.0(+/-3.9) x 10(-10) s(-1); pH 6, 6.5(+/-0.2) x 10(-9) s(-1); pH 7, 6.0(+/-0.2) x 10(-8) s(-1); pH 8, 1.6(+/-0.1) x 10(-7) s(-1)) show a more pronounced pH dependence compared to 2 (pH 5, 4.6(+/-0.1) x 10(-8) s(-1); pH 6, 4.2(+/-0.1) x 10(-8) s(-1); pH 7, 3.2(+/-0.1) x 10(-8) s(-1)). Preliminary biological assays of cellular uptake and cytotoxicity confirm the utility of the pro-drug concept. While blocked-polyamine compounds such as 2-4 are, in general, 2-3 orders of magnitude less cytotoxic than 1, there is significant cell type variability. Specifically, the Fmoc derivative 4 showed significantly enhanced cytotoxicity warranting further study of the pro-drug concept for greater selectivity and/or oral delivery.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Agents / chemical synthesis*
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology
  • Carbamates / chemistry
  • Catalysis
  • Chromatography, High Pressure Liquid
  • Female
  • Humans
  • Hydrogen-Ion Concentration
  • Hydrolysis
  • Inhibitory Concentration 50
  • Leukemia L1210
  • Mice
  • Molecular Structure
  • Nuclear Magnetic Resonance, Biomolecular
  • Organoplatinum Compounds / chemical synthesis*
  • Organoplatinum Compounds / chemistry
  • Organoplatinum Compounds / pharmacology
  • Ovarian Neoplasms
  • Polyamines / chemical synthesis
  • Polyamines / chemistry
  • Polyamines / pharmacology
  • Prodrugs / chemical synthesis*
  • Prodrugs / chemistry
  • Prodrugs / pharmacology
  • Spermidine / chemistry*
  • Spermidine / pharmacology
  • Spermine / chemistry
  • Spermine / pharmacology
  • Stereoisomerism
  • Structure-Activity Relationship
  • Temperature
  • Tumor Cells, Cultured / drug effects

Substances

  • Antineoplastic Agents
  • Carbamates
  • Organoplatinum Compounds
  • Polyamines
  • Prodrugs
  • Spermine
  • BBR 3464
  • Spermidine