A monovalent cation acts as structural and catalytic cofactor in translational GTPases

EMBO J. 2014 Nov 3;33(21):2547-63. doi: 10.15252/embj.201488517. Epub 2014 Sep 15.

Abstract

Translational GTPases are universally conserved GTP hydrolyzing enzymes, critical for fidelity and speed of ribosomal protein biosynthesis. Despite their central roles, the mechanisms of GTP-dependent conformational switching and GTP hydrolysis that govern the function of trGTPases remain poorly understood. Here, we provide biochemical and high-resolution structural evidence that eIF5B and aEF1A/EF-Tu bound to GTP or GTPγS coordinate a monovalent cation (M(+)) in their active site. Our data reveal that M(+) ions form constitutive components of the catalytic machinery in trGTPases acting as structural cofactor to stabilize the GTP-bound "on" state. Additionally, the M(+) ion provides a positive charge into the active site analogous to the arginine-finger in the Ras-RasGAP system indicating a similar role as catalytic element that stabilizes the transition state of the hydrolysis reaction. In sequence and structure, the coordination shell for the M(+) ion is, with exception of eIF2γ, highly conserved among trGTPases from bacteria to human. We therefore propose a universal mechanism of M(+)-dependent conformational switching and GTP hydrolysis among trGTPases with important consequences for the interpretation of available biochemical and structural data.

Keywords: GTPase; catalytic mechanism; crystal structure; monovalent cation; translation.

MeSH terms

  • Catalytic Domain
  • Cations, Monovalent / chemistry
  • Cations, Monovalent / metabolism
  • Coenzymes / chemistry*
  • Coenzymes / metabolism
  • Crystallography, X-Ray
  • Eukaryotic Initiation Factor-2 / chemistry*
  • Eukaryotic Initiation Factor-2 / metabolism
  • Eukaryotic Initiation Factors / chemistry*
  • Eukaryotic Initiation Factors / metabolism
  • Guanosine Triphosphate / chemistry
  • Guanosine Triphosphate / metabolism
  • Humans
  • Metals / chemistry*
  • Metals / metabolism
  • Peptide Elongation Factor Tu / chemistry*
  • Peptide Elongation Factor Tu / metabolism

Substances

  • Cations, Monovalent
  • Coenzymes
  • Eukaryotic Initiation Factor-2
  • Eukaryotic Initiation Factors
  • Metals
  • eukaryotic initiation factor-5B
  • Guanosine Triphosphate
  • Peptide Elongation Factor Tu

Associated data

  • PDB/4TMT
  • PDB/4TMV
  • PDB/4TMW
  • PDB/4TMX
  • PDB/4TMZ
  • PDB/4TN1