The type IA topoisomerase catalytic cycle: A normal mode analysis and molecular dynamics simulation

Proteins. 2008 Jun;71(4):1984-94. doi: 10.1002/prot.21876.

Abstract

Type IA topoisomerases alter the topological state of DNA to relax the supercoils introduced during the DNA replication and transcription process, giving them critical roles in many cellular functions. To manipulate the DNA, type IA topoisomerases first cleave one DNA strand and form a covalent linkage between a catalytic tyrosine residue and the 5'-phosphoryl of the DNA. This is followed by a movement of domain III of the topoisomerase to accommodate the second DNA strand in the center channel of the topoisomerase. Domain III is then closed for religation of the cleaved DNA and subsequently reopened to release the passing strand. Although numerous biophysical and biochemical studies have examined this catalytic cycle, fundamental questions remain such as how domain III opens and closes during this process. We have used computational simulation methods, namely normal mode analysis and molecular dynamics, to investigate the catalytic cycle of Escherichia coli topoisomerase III as a representative of the type IA topoisomerases. It was found that domain II is intrinsically flexible and may empower the enzyme to perform its function by triggering domain III opening and closing. A molecular dynamics simulation and MM-PBSA analysis shows that topoisomerase III alone cannot overcome the large energy barrier of the conformational transition. A detailed examination of the DNA binding sites suggests that the processing DNA cooperates with the topoisomerase to accomplish this dramatic conformational change. These findings will guide future mutagenesis studies of type IA topoisomerases aimed at dissecting the driving forces and conformations in the catalytic cycle.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoproteins / chemistry
  • Apoproteins / metabolism
  • Binding Sites
  • Catalysis
  • Computer Simulation*
  • Crystallography, X-Ray
  • DNA Topoisomerases, Type I / chemistry
  • DNA Topoisomerases, Type I / metabolism*
  • DNA, Bacterial / metabolism*
  • DNA, Single-Stranded / metabolism
  • Escherichia coli / enzymology*
  • Models, Biological
  • Models, Molecular
  • Protein Binding
  • Protein Structure, Quaternary
  • Protein Structure, Tertiary
  • Temperature
  • Time Factors

Substances

  • Apoproteins
  • DNA, Bacterial
  • DNA, Single-Stranded
  • DNA Topoisomerases, Type I