Macrophage-Associated Lipin-1 Enzymatic Activity Contributes to Modified Low-Density Lipoprotein-Induced Proinflammatory Signaling and Atherosclerosis

Arterioscler Thromb Vasc Biol. 2018 Feb;38(2):324-334. doi: 10.1161/ATVBAHA.117.310455. Epub 2017 Dec 7.

Abstract

Objective: Macrophage proinflammatory responses induced by modified low-density lipoproteins (modLDL) contribute to atherosclerotic progression. How modLDL causes macrophages to become proinflammatory is still enigmatic. Macrophage foam cell formation induced by modLDL requires glycerolipid synthesis. Lipin-1, a key enzyme in the glycerolipid synthesis pathway, contributes to modLDL-elicited macrophage proinflammatory responses in vitro. The objective of this study was to determine whether macrophage-associated lipin-1 contributes to atherogenesis and to assess its role in modLDL-mediated signaling in macrophages.

Approach and results: We developed mice lacking lipin-1 in myeloid-derived cells and used adeno-associated viral vector 8 expressing the gain-of-function mutation of mouse proprotein convertase subtilisin/kexin type 9 (adeno-associated viral vector 8-proprotein convertase subtilisin/kexin type 9) to induce hypercholesterolemia and plaque formation. Mice lacking myeloid-associated lipin-1 had reduced atherosclerotic burden compared with control mice despite similar plasma lipid levels. Stimulation of bone marrow-derived macrophages with modLDL activated a persistent protein kinase Cα/βII-extracellular receptor kinase1/2-jun proto-oncogene signaling cascade that contributed to macrophage proinflammatory responses that was dependent on lipin-1 enzymatic activity.

Conclusions: Our data demonstrate that macrophage-associated lipin-1 is atherogenic, likely through persistent activation of a protein kinase Cα/βII-extracellular receptor kinase1/2-jun proto-oncogene signaling cascade that contributes to foam cell proinflammatory responses. Taken together, these results suggest that modLDL-induced foam cell formation and modLDL-induced macrophage proinflammatory responses are not independent consequences of modLDL stimulation but rather are both directly influenced by enhanced lipid synthesis.

Keywords: atherosclerosis; foam cells; inflammation; macrophages.

Publication types

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

MeSH terms

  • Animals
  • Aorta / enzymology*
  • Aorta / pathology
  • Aortic Diseases / enzymology*
  • Aortic Diseases / genetics
  • Aortic Diseases / pathology
  • Atherosclerosis / enzymology*
  • Atherosclerosis / genetics
  • Atherosclerosis / pathology
  • Cyclic AMP-Dependent Protein Kinase Catalytic Subunits / metabolism
  • Disease Models, Animal
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Foam Cells / enzymology
  • Foam Cells / pathology
  • Inflammation / enzymology*
  • Inflammation / genetics
  • Inflammation / pathology
  • Inflammation Mediators / metabolism*
  • Lipoproteins, LDL / blood*
  • Macrophages / enzymology*
  • Macrophages / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nuclear Proteins / deficiency
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Phosphatidate Phosphatase / deficiency
  • Phosphatidate Phosphatase / genetics
  • Phosphatidate Phosphatase / metabolism*
  • Plaque, Atherosclerotic
  • Protein Kinase C beta / metabolism
  • Proto-Oncogene Proteins c-jun / metabolism
  • RAW 264.7 Cells
  • Signal Transduction

Substances

  • Inflammation Mediators
  • Lipoproteins, LDL
  • Nuclear Proteins
  • Proto-Oncogene Proteins c-jun
  • Cyclic AMP-Dependent Protein Kinase Catalytic Subunits
  • Prkaca protein, mouse
  • Protein Kinase C beta
  • Extracellular Signal-Regulated MAP Kinases
  • Lpin1 protein, mouse
  • Phosphatidate Phosphatase