C-terminus of the P4-ATPase ATP8A2 functions in protein folding and regulation of phospholipid flippase activity

Mol Biol Cell. 2017 Feb 1;28(3):452-462. doi: 10.1091/mbc.E16-06-0453. Epub 2016 Dec 8.

Abstract

ATP8A2 is a P4-ATPase that flips phosphatidylserine and phosphatidylethanolamine across cell membranes. This generates membrane phospholipid asymmetry, a property important in many cellular processes, including vesicle trafficking. ATP8A2 deficiency causes severe neurodegenerative diseases. We investigated the role of the C-terminus of ATP8A2 in its expression, subcellular localization, interaction with its subunit CDC50A, and function as a phosphatidylserine flippase. C-terminal deletion mutants exhibited a reduced tendency to solubilize in mild detergent and exit the endoplasmic reticulum. The solubilized protein, however, assembled with CDC50A and displayed phosphatidylserine flippase activity. Deletion of the C-terminal 33 residues resulted in reduced phosphatidylserine-dependent ATPase activity, phosphatidylserine flippase activity, and neurite extension in PC12 cells. These reduced activities were reversed with 60- and 80-residue C-terminal deletions. Unlike the yeast P4-ATPase Drs2, ATP8A2 is not regulated by phosphoinositides but undergoes phosphorylation on the serine residue within a CaMKII target motif. We propose a model in which the C-terminus of ATP8A2 consists of an autoinhibitor domain upstream of the C-terminal 33 residues and an anti-autoinhibitor domain at the extreme C-terminus. The latter blocks the inhibitory activity of the autoinhibitor domain. We conclude that the C-terminus plays an important role in the efficient folding and regulation of ATP8A2.

MeSH terms

  • Adenosine Triphosphatases / genetics*
  • Adenosine Triphosphatases / metabolism*
  • Adenosine Triphosphatases / physiology*
  • Animals
  • Biological Transport
  • Cell Membrane / metabolism
  • HEK293 Cells
  • Humans
  • Membrane Proteins / metabolism
  • Membrane Proteins / physiology
  • PC12 Cells
  • Phosphatidylethanolamines / metabolism
  • Phosphatidylserines / metabolism
  • Phospholipid Transfer Proteins / genetics*
  • Phospholipid Transfer Proteins / metabolism*
  • Phospholipid Transfer Proteins / physiology*
  • Phospholipids / metabolism
  • Protein Domains
  • Protein Folding
  • Protein Transport
  • Rats

Substances

  • Membrane Proteins
  • Phosphatidylethanolamines
  • Phosphatidylserines
  • Phospholipid Transfer Proteins
  • Phospholipids
  • TMEM30a protein, human
  • phosphatidylethanolamine
  • Adenosine Triphosphatases
  • ATP8A2 protein, human