Calcium-independent calmodulin binding and two-metal-ion catalytic mechanism of anthrax edema factor

EMBO J. 2005 Mar 9;24(5):929-41. doi: 10.1038/sj.emboj.7600574. Epub 2005 Feb 17.

Abstract

Edema factor (EF), a key anthrax exotoxin, has an anthrax protective antigen-binding domain (PABD) and a calmodulin (CaM)-activated adenylyl cyclase domain. Here, we report the crystal structures of CaM-bound EF, revealing the architecture of EF PABD. CaM has N- and C-terminal domains and each domain can bind two calcium ions. Calcium binding induces the conformational change of CaM from closed to open. Structures of the EF-CaM complex show how EF locks the N-terminal domain of CaM into a closed conformation regardless of its calcium-loading state. This represents a mechanism of how CaM effector alters the calcium affinity of CaM and uncouples the conformational change of CaM from calcium loading. Furthermore, structures of EF-CaM complexed with nucleotides show that EF uses two-metal-ion catalysis, a prevalent mechanism in DNA and RNA polymerases. A histidine (H351) further facilitates the catalysis of EF by activating a water to deprotonate 3'OH of ATP. Mammalian adenylyl cyclases share no structural similarity with EF and they also use two-metal-ion catalysis, suggesting the catalytic mechanism-driven convergent evolution of two structurally diverse adenylyl cyclases.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adenylate Cyclase Toxin / chemistry
  • Adenylate Cyclase Toxin / genetics
  • Adenylate Cyclase Toxin / metabolism
  • Adenylyl Cyclases / chemistry*
  • Adenylyl Cyclases / genetics
  • Adenylyl Cyclases / metabolism*
  • Amino Acid Sequence
  • Antigens, Bacterial
  • Bacillus anthracis / genetics
  • Bacillus anthracis / metabolism
  • Bacillus anthracis / pathogenicity
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Bacterial Toxins
  • Binding Sites
  • Calcium / metabolism
  • Calmodulin / chemistry
  • Calmodulin / metabolism*
  • Catalysis
  • Crystallography, X-Ray
  • Exotoxins / chemistry
  • Exotoxins / genetics
  • Exotoxins / metabolism
  • Glucosyltransferases / chemistry
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism
  • Histidine / chemistry
  • Metals / metabolism
  • Models, Molecular
  • Molecular Sequence Data
  • Multiprotein Complexes
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Sequence Homology, Amino Acid

Substances

  • Adenylate Cyclase Toxin
  • Antigens, Bacterial
  • Bacterial Proteins
  • Bacterial Toxins
  • Calmodulin
  • Exotoxins
  • Metals
  • Multiprotein Complexes
  • Recombinant Proteins
  • anthrax toxin
  • Histidine
  • ExoY protein, bacteria
  • Glucosyltransferases
  • Adenylyl Cyclases
  • Calcium

Associated data

  • PDB/1XFU
  • PDB/1XFV
  • PDB/1XFW
  • PDB/1XFX
  • PDB/1XFY
  • PDB/1XFZ
  • PDB/1Y0V