Macrophage LRP-1 controls plaque cellularity by regulating efferocytosis and Akt activation

Arterioscler Thromb Vasc Biol. 2010 Apr;30(4):787-95. doi: 10.1161/ATVBAHA.109.202051. Epub 2010 Feb 11.

Abstract

Objective: The balance between apoptosis susceptibility and efferocytosis of macrophages is central to plaque remodeling and inflammation. LRP-1 and its ligand, apolipoprotein E, have been implicated in efferocytosis and apoptosis in some cell types. We investigated the involvement of the macrophage LRP-1/apolipoprotein E axis in controlling plaque apoptosis and efferocytosis. Method and Results- LRP-1(-/-) macrophages displayed nearly 2-fold more TUNEL positivity compared to wild-type cells in the presence of DMEM alone or with either lipopolysaccharide or oxidized low-density lipoprotein. The survival kinase, phosphorylated Akt, was barely detectable in LRP-1(-/-) cells, causing decreased phosphorylated Bad and increased cleaved caspase-3. Regardless of the apoptotic stimulation and degree of cell death, LRP-1(-/-) macrophages displayed enhanced inflammation with increased IL-1 beta, IL-6, and tumor necrosis factor-alpha expression. Efferocytosis of apoptotic macrophages was reduced by 60% in LRP-1(-/-) vs wild-type macrophages despite increased apolipoprotein E expression by both LRP-1(-/-) phagocytes and wild-type apoptotic cells. Compared to wild-type macrophage lesions, LRP-1(-/-) lesions had 5.7-fold more necrotic core with more dead cells not associated with macrophages.

Conclusions: Macrophage LRP-1 deficiency increases cell death and inflammation by impairing phosphorylated Akt activation and efferocytosis. Increased apolipoprotein E expression in LRP-1(-/-) macrophages suggests that the LRP-1/apolipoprotein E axis regulates the balance between apoptosis and efferocytosis, thereby preventing necrotic core formation.

Publication types

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

MeSH terms

  • Animals
  • Apolipoproteins E / metabolism*
  • Apoptosis* / drug effects
  • Atherosclerosis / enzymology*
  • Atherosclerosis / pathology
  • Cell Survival
  • Cells, Cultured
  • Enzyme Activation
  • Female
  • In Situ Nick-End Labeling
  • Inflammation / enzymology*
  • Inflammation / pathology
  • Interleukin-1beta / metabolism
  • Interleukin-6 / metabolism
  • Lipopolysaccharides / pharmacology
  • Lipoproteins, LDL / metabolism
  • Low Density Lipoprotein Receptor-Related Protein-1
  • Macrophages, Peritoneal / drug effects
  • Macrophages, Peritoneal / enzymology*
  • Macrophages, Peritoneal / pathology
  • Mice
  • Mice, Knockout
  • Necrosis
  • Phagocytosis* / drug effects
  • Phosphorylation
  • Proto-Oncogene Proteins c-akt / metabolism*
  • Receptors, LDL / deficiency
  • Receptors, LDL / genetics
  • Receptors, LDL / metabolism*
  • Tumor Necrosis Factor-alpha / metabolism
  • Tumor Suppressor Proteins / deficiency
  • Tumor Suppressor Proteins / genetics
  • Tumor Suppressor Proteins / metabolism*

Substances

  • Apolipoproteins E
  • Interleukin-1beta
  • Interleukin-6
  • Lipopolysaccharides
  • Lipoproteins, LDL
  • Low Density Lipoprotein Receptor-Related Protein-1
  • Lrp1 protein, mouse
  • Receptors, LDL
  • Tumor Necrosis Factor-alpha
  • Tumor Suppressor Proteins
  • oxidized low density lipoprotein
  • Proto-Oncogene Proteins c-akt