Native low-density lipoprotein induces endothelial nitric oxide synthase dysfunction: role of heat shock protein 90 and caveolin-1

Free Radic Biol Med. 2002 Jul 1;33(1):52-62. doi: 10.1016/s0891-5849(02)00851-1.

Abstract

Although native LDL (n-LDL) is well recognized for inducing endothelial cell (EC) dysfunction, the mechanisms remain unclear. One hypothesis is n-LDL increases caveolin-1 (Cav-1), which decreases nitric oxide (*NO) production by binding endothelial nitric oxide synthase (eNOS) in an inactive state. Another is n-LDL increases superoxide anion (O(2)(*-)), which inactivates *NO. To test these hypotheses, EC were incubated with n-LDL and then analyzed for *NO, O(2)(*-), phospho-eNOS (S1179), eNOS, Cav-1, calmodulin (CaM), and heat shock protein 90 (hsp90). n-LDL increased NOx by more than 4-fold while having little effect on A23187-stimulated nitrite production. In contrast, n-LDL decreased cGMP under basal and A23187-stimulated conditions and increased O(2)(*-) by a mechanism that could be inhibited by L-nitroargininemethylester (L-NAME) and BAPTA/AM. n-LDL increased phospho-eNOS by 149%, eNOS by approximately 34%, and Cav-1 by 28%, and decreased the association of hsp90 with eNOS by 49%. n-LDL did not appear to alter eNOS distribution between membrane fractions (approximately 85%) and cytosol (approximately 15%). Only 3-6% of eNOS in membrane fractions was associated with Cav-1. These data support the hypothesis that n-LDL increases O(2)(*-), which scavenges *NO, and suggest that n-LDL uncouples eNOS activity by decreasing the association of hsp90 as an initial step in signaling eNOS to generate O(2)(*-).

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Biological Transport
  • Blotting, Western
  • Calmodulin / metabolism
  • Cattle
  • Caveolin 1
  • Caveolins / metabolism*
  • Cells, Cultured
  • Chelating Agents / pharmacology
  • Cyclic GMP / metabolism
  • Egtazic Acid / analogs & derivatives*
  • Egtazic Acid / pharmacology
  • Endothelium, Vascular / drug effects*
  • Endothelium, Vascular / enzymology
  • Enzyme Activation
  • Enzyme Inhibitors / pharmacology
  • HSP90 Heat-Shock Proteins / metabolism*
  • Humans
  • Lipoproteins, LDL / pharmacology*
  • NG-Nitroarginine Methyl Ester / pharmacology
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase / antagonists & inhibitors
  • Nitric Oxide Synthase / metabolism*
  • Nitric Oxide Synthase Type III
  • Nitrites / metabolism
  • Phosphorylation
  • Superoxides / metabolism

Substances

  • CAV1 protein, human
  • Calmodulin
  • Caveolin 1
  • Caveolins
  • Chelating Agents
  • Enzyme Inhibitors
  • HSP90 Heat-Shock Proteins
  • Lipoproteins, LDL
  • Nitrites
  • Superoxides
  • Nitric Oxide
  • Egtazic Acid
  • NOS3 protein, human
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type III
  • Cyclic GMP
  • 1,2-bis(2-aminophenoxy)ethane-N,N,N',N'-tetraacetic acid
  • NG-Nitroarginine Methyl Ester