Variable Inhibition of DNA Unwinding Rates Catalyzed by the SARS-CoV-2 Helicase Nsp13 by Structurally Distinct Single DNA Lesions

Int J Mol Sci. 2024 Jul 19;25(14):7930. doi: 10.3390/ijms25147930.

Abstract

The SARS-CoV-2 helicase, non-structural protein 13 (Nsp13), plays an essential role in viral replication, translocating in the 5' → 3' direction as it unwinds double-stranded RNA/DNA. We investigated the impact of structurally distinct DNA lesions on DNA unwinding catalyzed by Nsp13. The selected lesions include two benzo[a]pyrene (B[a]P)-derived dG adducts, the UV-induced cyclobutane pyrimidine dimer (CPD), and the pyrimidine (6-4) pyrimidone (6-4PP) photolesion. The experimentally observed unwinding rate constants (kobs) and processivities (P) were examined. Relative to undamaged DNA, the kobs values were diminished by factors of up to ~15 for B[a]P adducts but only by factors of ~2-5 for photolesions. A minor-groove-oriented B[a]P adduct showed the smallest impact on P, which decreased by ~11% compared to unmodified DNA, while an intercalated one reduced P by ~67%. However, the photolesions showed a greater impact on the processivities; notably, the CPD, with the highest kobs value, exhibited the lowest P, which was reduced by ~90%. Our findings thus show that DNA unwinding efficiencies are lesion-dependent and most strongly inhibited by the CPD, leading to the conclusion that processivity is a better measure of DNA lesions' inhibitory effects than unwinding rate constants.

Keywords: 6–4PP; CPD; Nsp13 helicase; SARS-CoV-2; SF1 helicase; UV photolesions; benzo[a]pyrene diol epoxide–DNA adducts; crosslinked thymine dimer; processivity; protein–DNA interactions; unwinding.

MeSH terms

  • COVID-19 / virology
  • DNA / chemistry
  • DNA / metabolism
  • DNA Damage
  • DNA Helicases* / chemistry
  • DNA Helicases* / metabolism
  • Humans
  • Kinetics
  • Methyltransferases
  • RNA Helicases
  • SARS-CoV-2* / metabolism
  • Viral Nonstructural Proteins* / chemistry
  • Viral Nonstructural Proteins* / metabolism

Substances

  • Viral Nonstructural Proteins
  • DNA Helicases
  • Nsp13 protein, SARS-CoV
  • DNA
  • Methyltransferases
  • RNA Helicases