ATP11C is a major flippase in human erythrocytes and its defect causes congenital hemolytic anemia

Haematologica. 2016 May;101(5):559-65. doi: 10.3324/haematol.2016.142273. Epub 2016 Mar 4.

Abstract

Phosphatidylserine is localized exclusively to the inner leaflet of the membrane lipid bilayer of most cells, including erythrocytes. This asymmetric distribution is critical for the survival of erythrocytes in circulation since externalized phosphatidylserine is a phagocytic signal for splenic macrophages. Flippases are P-IV ATPase family proteins that actively transport phosphatidylserine from the outer to inner leaflet. It has not yet been determined which of the 14 members of this family of proteins is the flippase in human erythrocytes. Herein, we report that ATP11C encodes a major flippase in human erythrocytes, and a genetic mutation identified in a male patient caused congenital hemolytic anemia inherited as an X-linked recessive trait. Phosphatidylserine internalization in erythrocytes with the mutant ATP11C was decreased 10-fold compared to that of the control, functionally establishing that ATP11C is a major flippase in human erythrocytes. Contrary to our expectations phosphatidylserine was retained in the inner leaflet of the majority of mature erythrocytes from both controls and the patient, suggesting that phosphatidylserine cannot be externalized as long as scramblase is inactive. Phosphatidylserine-exposing cells were found only in the densest senescent cells (0.1% of total) in which scramblase was activated by increased Ca(2+) concentration: the percentage of these phosphatidylserine-exposing cells was increased in the patient's senescent cells accounting for his mild anemia. Furthermore, the finding of similar extents of phosphatidylserine exposure by exogenous Ca(2+)-activated scrambling in both control erythrocytes and the patient's erythrocytes implies that suppressed scramblase activity rather than flippase activity contributes to the maintenance of phosphatidylserine in the inner leaflet of human erythrocytes.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphatases / deficiency
  • Adenosine Triphosphatases / genetics*
  • Adenosine Triphosphatases / metabolism*
  • Adolescent
  • Anemia, Hemolytic, Congenital / diagnosis
  • Anemia, Hemolytic, Congenital / genetics*
  • Anemia, Hemolytic, Congenital / metabolism*
  • Biological Transport, Active
  • Biomarkers
  • Calcium / metabolism
  • Erythrocyte Indices
  • Erythrocytes / drug effects
  • Erythrocytes / metabolism*
  • Humans
  • Male
  • Membrane Transport Proteins / deficiency
  • Membrane Transport Proteins / genetics*
  • Membrane Transport Proteins / metabolism*
  • Mutation
  • Phosphatidylserines / metabolism
  • Phosphatidylserines / pharmacology

Substances

  • Biomarkers
  • Membrane Transport Proteins
  • Phosphatidylserines
  • ATP11C protein, human
  • Adenosine Triphosphatases
  • Calcium