Kinetic mechanism and fidelity of nick sealing by Escherichia coli NAD+-dependent DNA ligase (LigA)

Nucleic Acids Res. 2016 Mar 18;44(5):2298-309. doi: 10.1093/nar/gkw049. Epub 2016 Feb 8.

Abstract

Escherichia coli DNA ligase (EcoLigA) repairs 3'-OH/5'-PO4 nicks in duplex DNA via reaction of LigA with NAD(+) to form a covalent LigA-(lysyl-Nζ)-AMP intermediate (step 1); transfer of AMP to the nick 5'-PO4 to form an AppDNA intermediate (step 2); and attack of the nick 3'-OH on AppDNA to form a 3'-5' phosphodiester (step 3). A distinctive feature of EcoLigA is its stimulation by ammonium ion. Here we used rapid mix-quench methods to analyze the kinetic mechanism of single-turnover nick sealing by EcoLigA-AMP. For substrates with correctly base-paired 3'-OH/5'-PO4 nicks, kstep2 was fast (6.8-27 s(-1)) and similar to kstep3 (8.3-42 s(-1)). Absent ammonium, kstep2 and kstep3 were 48-fold and 16-fold slower, respectively. EcoLigA was exquisitely sensitive to 3'-OH base mispairs and 3' N:abasic lesions, which elicited 1000- to >20000-fold decrements in kstep2. The exception was the non-canonical 3' A:oxoG configuration, which EcoLigA accepted as correctly paired for rapid sealing. These results underscore: (i) how EcoLigA requires proper positioning of the nick 3' nucleoside for catalysis of 5' adenylylation; and (ii) EcoLigA's potential to embed mutations during the repair of oxidative damage. EcoLigA was relatively tolerant of 5'-phosphate base mispairs and 5' N:abasic lesions.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenosine Monophosphate / chemistry*
  • Adenosine Monophosphate / metabolism
  • Ammonium Sulfate / chemistry
  • Ammonium Sulfate / pharmacology
  • Base Pair Mismatch
  • Base Sequence
  • DNA / chemistry*
  • DNA / metabolism
  • DNA Breaks, Double-Stranded / drug effects
  • DNA Ligases / chemistry*
  • DNA Ligases / genetics
  • DNA Repair*
  • Enzyme Assays
  • Escherichia coli / enzymology*
  • Escherichia coli / genetics
  • Escherichia coli Proteins / chemistry*
  • Escherichia coli Proteins / genetics
  • Gene Expression
  • Kinetics
  • Molecular Sequence Data
  • NAD / chemistry*
  • NAD / metabolism
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / genetics
  • Substrate Specificity

Substances

  • Escherichia coli Proteins
  • Recombinant Fusion Proteins
  • NAD
  • Adenosine Monophosphate
  • DNA
  • DNA Ligases
  • LigA protein, E coli
  • Ammonium Sulfate