Further insights on the structural aspects of PLA(2) inhibition by gamma-hydroxybutenolide-containing natural products: a comparative study on petrosaspongiolides M-R

Bioorg Med Chem. 2004 Mar 15;12(6):1467-74. doi: 10.1016/j.bmc.2003.12.038.

Abstract

Petrosaspongiolides M-R (PM-PR, 1-5) are marine sesterterpenes structurally characterised by a gamma-hydroxybutenolide moiety. They have shown an in vitro and in vivo potent anti-inflammatory activity, mediated by specific inhibition of secretory phospholipase A(2) (sPLA(2) enzymes). The molecular mechanism underlying the sub-micromolar irreversible inhibition of the bee-venom PLA(2) (bvPLA(2)) by PM has been clarified combining mass spectrometry (MS) and molecular modelling approaches. The N-terminal amino group (Ile-1 residue), recently identified as the unique PM covalent binding site on this enzyme, selectively delivers a nucleophilic attack onto the masked aldehyde at C-25 of the pharmacophoric gamma-hydroxybutenolide ring of PM, giving rise to a Schiff base. In the attempt of broadening the knowledge of the mechanism at molecular level of PLA(2) inactivation by this family of compounds, we performed a comparative analysis on petrosaspongiolides M-R, whose results are discussed in this paper. Firstly, the amount of bvPLA(2) enzyme covalently modified after incubation with each of petrosaspongiolides M-R was measured and resulted to be in good agreement with pharmacological in vitro data. Then, a full characterisation of the bvPLA(2) adduct with PR, one of the least active and most structurally different among petrosaspongiolides, by LC-MS, MS(n), and computational methods, confirmed the same inhibition mechanism and covalent binding site already found for PM. Finally, extensive molecular docking studies performed in comparison on the PM-PLA(2) and PR-PLA(2) complexes provided critical insight on how the balance between non-covalent and covalent inhibitor-enzyme interactions may affect the final potency exhibited by the various compounds of the petrosaspongiolide family.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • 4-Butyrolactone / analogs & derivatives
  • Animals
  • Bee Venoms / enzymology*
  • Binding Sites
  • Biological Products*
  • Chromatography, High Pressure Liquid
  • Computational Biology
  • Enzyme Inhibitors / chemistry
  • Enzyme Inhibitors / pharmacology*
  • Furans / chemistry*
  • Furans / pharmacology
  • Immunosuppressive Agents / chemistry
  • Immunosuppressive Agents / pharmacology
  • Mass Spectrometry
  • Models, Molecular
  • Molecular Structure
  • Oleanolic Acid / analogs & derivatives*
  • Oleanolic Acid / chemistry*
  • Oleanolic Acid / pharmacology*
  • Phospholipases A / antagonists & inhibitors*
  • Phospholipases A / chemistry

Substances

  • Bee Venoms
  • Biological Products
  • Enzyme Inhibitors
  • Furans
  • Immunosuppressive Agents
  • petrosaspongiolide m
  • Oleanolic Acid
  • butenolide
  • Phospholipases A
  • 4-Butyrolactone