Ceramide 1-phosphate acts as a positive allosteric activator of group IVA cytosolic phospholipase A2 alpha and enhances the interaction of the enzyme with phosphatidylcholine

J Biol Chem. 2005 May 6;280(18):17601-7. doi: 10.1074/jbc.M414173200. Epub 2005 Mar 1.

Abstract

Previous findings from our laboratory have demonstrated that cPLA(2)alpha is directly activated by the emerging bioactive sphingolipid, ceramide 1-phosphate (C-1-P) (1). In this study, a Triton X-100/phosphatidylcholine (PC) mixed micelle assay was utilized to determine the kinetics and specificity of this lipid-enzyme interaction. Using this assay, the addition of C-1-P induced a dramatic increase in the activity of cPLA(2)alpha (>15-fold) with a K(a) of 2.4 mol % C-1-P/Triton X-100 micelle. This activation was highly specific as the addition of other lipids had insignificant effects on cPLA(2)alpha activity. Studies using surface-dilution kinetics revealed that C-1-P had no effect on the Michaelis-Menten constant, K(m)(B), but decreased the dissociation constant (K (A)(s)) value by 87%. Thus, C-1-P not only increases the membrane affinity of cPLA(2)alpha but also may act as an allosteric activator of the enzyme. Surface plasmon resonance analysis of the C-1-P/cPLA(2)alpha interaction verified a decrease in the dissociation constant, demonstrating that cPLA(2)alpha bound PC vesicles containing C-1-P with increased affinity (5-fold) compared with PC vesicles alone. The effect on the dissociation rate of cPLA(2)alpha was also found to be lipid-specific with the exception of phosphatidylinositol 4,5-bisphosphate, which caused a modest increase in vesicle affinity (2-fold). Lastly, the binding site for C-1-P was determined to be within the C2-domain of cPLA(2)alpha, unlike phosphatidylinositol 4,5-bisphosphate. These data demonstrate a novel interaction site for C-1-P and suggest that C-1-P may function to recruit cPLA(2)alpha to intracellular membranes as well as allosterically activate the membrane-associated enzyme.

Publication types

  • Research Support, N.I.H., Extramural
  • 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

  • Allosteric Regulation / physiology
  • Animals
  • Ceramides / physiology*
  • Drug Synergism
  • Enzyme Activation / physiology
  • Group IV Phospholipases A2
  • Humans
  • Insecta
  • Isoenzymes / metabolism
  • Phosphatidylcholines / metabolism*
  • Phospholipases A / metabolism*
  • Phospholipases A2
  • Protein Binding / physiology

Substances

  • Ceramides
  • Isoenzymes
  • Phosphatidylcholines
  • ceramide 1-phosphate
  • Phospholipases A
  • Group IV Phospholipases A2
  • PLA2G4A protein, human
  • Phospholipases A2