Preferential DNA photocleavage potency of Zn(II) over Ni(II) derivatives of carboxymethyl tetracationic porphyrin: the role of the mode of binding to DNA

Eur Biophys J. 2014 Nov;43(10-11):545-54. doi: 10.1007/s00249-014-0984-7. Epub 2014 Aug 28.

Abstract

The porphyrin-based photosensitizers capable of binding to DNA are perspective drug candidates. Here we report the interactions with calf thymus DNA of 5,10,15,20-tetrakis(N-carboxymethyl-4-pyridinium)porphyrin (P1) and its derivatives containing Zn(II) or Ni(II) in the coordination sphere. These interactions were studied with absorption and circular dichroism spectroscopy. NiP1 and ZnP1 formed different types of complexes with DNA. NiP1 intercalated into the double helix, whereas ZnP1 bound the DNA groove. Compound P1 displayed both binding modes. The ZnP1-DNA binding constant was approximately three times smaller than the respective values for P1-DNA and NiP1-DNA complexes. Light induced degradation of the reactive oxygen species (ROS) trap 1,3-diphenylisobenzofuran in the presence of P1 and its metal derivatives revealed that NiP1 was a weaker photooxidative agent, whereas P1 and ZnP1 generated ROS to similar extents. Nevertheless, the DNA photodamaging effect of ZnP1 was the most pronounced. Illumination of the supercoiled plasmid caused single-strand DNA photocleavage in the presence of P1 and ZnP1; double strand breaks were detectable with micromolar concentrations of ZnP1. The concentration of ZnP1 required for plasmid photonicking was two times smaller than that of P1 and ~20 times lower than that for NiP1. Thus, the modes of P1, NiP1 and ZnP1 binding to DNA determine the differential photodamaging potency of these porphyrins. A greater accessibility to the solvent of the groove binder ZnP1, compared to the shielded intercalator NiP1 and the intercalated P1 molecules, allows for an efficient local generation of ROS followed by DNA photocleavage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • DNA, Single-Stranded / chemistry*
  • DNA, Single-Stranded / metabolism
  • DNA, Single-Stranded / radiation effects
  • Metalloporphyrins / chemical synthesis
  • Metalloporphyrins / chemistry*
  • Metalloporphyrins / pharmacology
  • Metalloporphyrins / radiation effects
  • Molecular Docking Simulation
  • Molecular Sequence Data
  • Nickel / chemistry*
  • Photosensitizing Agents / chemistry*
  • Photosensitizing Agents / pharmacology
  • Photosensitizing Agents / radiation effects
  • Pyridinium Compounds / chemical synthesis
  • Pyridinium Compounds / chemistry*
  • Ultraviolet Rays
  • Zinc / chemistry*

Substances

  • DNA, Single-Stranded
  • Metalloporphyrins
  • Photosensitizing Agents
  • Pyridinium Compounds
  • Nickel
  • Zinc