Molecular determinants of the N-terminal acetyltransferase Naa60 anchoring to the Golgi membrane

J Biol Chem. 2017 Apr 21;292(16):6821-6837. doi: 10.1074/jbc.M116.770362. Epub 2017 Feb 14.

Abstract

Nα-Acetyltransferase 60 (Naa60 or NatF) was recently identified as an unconventional N-terminal acetyltransferase (NAT) because it localizes to organelles, in particular the Golgi apparatus, and has a preference for acetylating N termini of the transmembrane proteins. This knowledge challenged the prevailing view of N-terminal acetylation as a co-translational ribosome-associated process and suggested a new mechanistic functioning for the enzymes responsible for this increasingly recognized protein modification. Crystallography studies on Naa60 were unable to resolve the C-terminal tail of Naa60, which is responsible for the organellar localization. Here, we combined modeling, in vitro assays, and cellular localization studies to investigate the secondary structure and membrane interacting capacity of Naa60. The results show that Naa60 is a peripheral membrane protein. Two amphipathic helices within the Naa60 C terminus bind the membrane directly in a parallel position relative to the lipid bilayer via hydrophobic and electrostatic interactions. A peptide corresponding to the C terminus was unstructured in solution and only folded into an α-helical conformation in the presence of liposomes. Computational modeling and cellular mutational analysis revealed the hydrophobic face of two α-helices to be critical for membranous localization. Furthermore, we found a strong and specific binding preference of Naa60 toward membranes containing the phosphatidylinositol PI(4)P, thus possibly explaining the primary residency of Naa60 at the PI(4)P-rich Golgi. In conclusion, we have defined the mode of cytosolic Naa60 anchoring to the Golgi apparatus, most likely occurring post-translationally and specifically facilitating post-translational N-terminal acetylation of many transmembrane proteins.

Keywords: Golgi; N-terminal acetylation; NAT; Naa60; NatF; PI(4)P; acetylation; acetyltransferase; lipid binding protein; membrane enzyme.

MeSH terms

  • Calorimetry
  • Circular Dichroism
  • Crystallography, X-Ray
  • Cytosol / enzymology
  • DNA Mutational Analysis
  • Golgi Apparatus / metabolism*
  • Green Fluorescent Proteins / chemistry
  • HeLa Cells
  • Humans
  • Hydrogen Bonding
  • Lipid Bilayers / chemistry
  • Liposomes / chemistry
  • Molecular Dynamics Simulation
  • Mutagenesis, Site-Directed
  • N-Terminal Acetyltransferase F / chemistry*
  • Peptides / chemistry
  • Protein Binding
  • Protein Domains
  • Protein Structure, Secondary
  • Ribosomes / chemistry
  • Static Electricity
  • Tryptophan / chemistry

Substances

  • Lipid Bilayers
  • Liposomes
  • NAA60 protein, human
  • Peptides
  • Green Fluorescent Proteins
  • Tryptophan
  • N-Terminal Acetyltransferase F

Associated data

  • PDB/5ICV