Early steps of oxidative damage in DNA quadruplexes are position-dependent: Quantum mechanical and molecular dynamics analysis of human telomeric sequence containing ionized guanine

Int J Biol Macromol. 2022 Jan 1:194:882-894. doi: 10.1016/j.ijbiomac.2021.11.143. Epub 2021 Nov 25.

Abstract

Guanine radical cation (G•+) is a key intermediate in many oxidative processes occurring in nucleic acids. Here, by combining mixed Quantum Mechanical/Molecular Mechanics calculations and Molecular Dynamics (MD) simulations, we study how the structural behaviour of a tract GGG(TTAGGG)3 (hereafter Tel21) of the human telomeric sequence, folded in an antiparallel quadruple helix, changes when one of the G bases is ionized to G•+ (Tel21+). Once assessed that the electron-hole is localized on a single G, we perform MD simulations of twelve Tel21+ systems, differing in the position of G•+ in the sequence. When G•+ is located in the tetrad adjacent to the diagonal loop, we observe substantial structural rearrangements, which can decrease the electrostatic repulsion with the inner Na+ ions and increase the solvent exposed surface of G•+. Analysis of solvation patterns of G•+ provides new insights on the main reactions of G•+, i.e. the deprotonation at two different sites and hydration at the C8 atom, the first steps of the processes producing 8oxo-Guanine. We suggest the main structural determinants of the relative reactivity of each position and our conclusions, consistent with the available experimental trends, can help rationalizing the reactivity of other G-quadruplex topologies.

Keywords: DNA structure; Electrostatic repulsion; Guanine quadruplex; Guanine radicals; Solvation.

MeSH terms

  • DNA / chemistry*
  • G-Quadruplexes*
  • Guanine / chemistry*
  • Humans
  • Ions / chemistry*
  • Models, Molecular
  • Molecular Dynamics Simulation*
  • Nucleic Acid Conformation
  • Oxidative Stress*
  • Quantum Theory*
  • Solubility
  • Telomere / chemistry*

Substances

  • Ions
  • Guanine
  • DNA