Structural study of X-ray induced activation of carbonic anhydrase

Proc Natl Acad Sci U S A. 2009 Jun 30;106(26):10609-13. doi: 10.1073/pnas.0904184106. Epub 2009 Jun 11.

Abstract

Carbonic anhydrase, a zinc metalloenzyme, catalyzes the reversible hydration of carbon dioxide to bicarbonate. It is involved in processes connected with acid-base homeostasis, respiration, and photosynthesis. More than 100 distinct human carbonic anhydrase II (HCAII) 3D structures have been generated in last 3 decades [Liljas A, et al. (1972) Nat New Biol 235:131-137], but a structure of an HCAII in complex with CO(2) or HCO(3)(-) has remained elusive. Here, we report previously undescribed structures of HCAII:CO(2) and HCAII:HCO(3)(-) complexes, together with a 3D molecular film of the enzymatic reaction observed successively in the same crystal after extended exposure to X-ray. We demonstrate that the unexpected enzyme activation was caused in an X-ray dose-dependent manner. Although X-ray damage to macromolecular samples has long been recognized [Ravelli RB, Garman EF (2006) Curr Opin Struct Biol 16:624-629], the detailed structural analysis reports on X-ray-driven reactions have been very rare in literature to date. Here, we report on enzyme activation and the associated chemical reaction in a crystal at 100 K. We propose mechanisms based on water photoradiolysis and/or electron radiolysis as the main cause of enzyme activation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bicarbonates / chemistry
  • Bicarbonates / metabolism
  • Carbon Dioxide / chemistry
  • Carbon Dioxide / metabolism
  • Carbonic Anhydrase II / chemistry*
  • Carbonic Anhydrase II / genetics
  • Carbonic Anhydrase II / metabolism
  • Catalysis / radiation effects
  • Catalytic Domain
  • Crystallization
  • Enzyme Activation / radiation effects
  • Histidine / chemistry
  • Humans
  • Hydrogen Bonding
  • Hydrogen-Ion Concentration
  • Kinetics
  • Models, Chemical
  • Models, Molecular
  • Protein Binding
  • Protein Structure, Secondary
  • Protein Structure, Tertiary
  • Recombinant Proteins / chemistry*
  • Recombinant Proteins / metabolism
  • Temperature
  • Water / chemistry
  • X-Ray Diffraction
  • X-Rays*
  • Zinc / chemistry

Substances

  • Bicarbonates
  • Recombinant Proteins
  • Water
  • Carbon Dioxide
  • Histidine
  • Carbonic Anhydrase II
  • Zinc

Associated data

  • PDB/2VVA
  • PDB/2VVB