Phosphorylation of Insig-2 mediates inhibition of fatty acid synthesis by polyunsaturated fatty acids

Proc Natl Acad Sci U S A. 2024 Aug 20;121(34):e2409262121. doi: 10.1073/pnas.2409262121. Epub 2024 Aug 15.

Abstract

Insig-1 and Insig-2 are endoplasmic reticulum (ER) proteins that inhibit lipid synthesis by blocking transport of sterol regulatory element-binding proteins (SREBP-1 and SREBP-2) from ER to Golgi. In the Golgi, SREBPs are processed proteolytically to release their transcription-activating domains, which enhance the synthesis of fatty acids, triglycerides, and cholesterol. Heretofore, the two Insigs have redundant functions, and there is no rationale for two isoforms. The current data identify a specific function for Insig-2. We show that eicosapentaenoic acid (EPA), a polyunsaturated fatty acid, inhibits fatty acid synthesis in human fibroblasts and rat hepatocytes by activating adenylate cyclase, which induces protein kinase A (PKA) to phosphorylate serine-106 in Insig-2. Phosphorylated Insig-2 inhibits the proteolytic processing of SREBP-1, thereby blocking fatty acid synthesis. Phosphorylated Insig-2 does not block the processing of SREBP-2, which activates cholesterol synthesis. Insig-1 lacks serine-106 and is not phosphorylated at this site. EPA inhibition of SREBP-1 processing was reduced by the replacement of serine-106 in Insig-2 with alanine or by treatment with KT5720, a PKA inhibitor. Inhibition did not occur in mutant human fibroblasts that possess Insig-1 but lack Insig-2. These data provide an Insig-2-specific mechanism for the long-known inhibition of fatty acid synthesis by polyunsaturated fatty acids.

Keywords: SREBP-1; cyclic AMP; fatty acid synthesis; mammalian cells; phosphorylated Insig-2.

MeSH terms

  • Animals
  • Cyclic AMP-Dependent Protein Kinases* / metabolism
  • Eicosapentaenoic Acid / pharmacology
  • Fatty Acids / biosynthesis
  • Fatty Acids / metabolism
  • Fatty Acids, Unsaturated / metabolism
  • Fibroblasts* / metabolism
  • Hepatocytes / metabolism
  • Humans
  • Intracellular Signaling Peptides and Proteins* / genetics
  • Intracellular Signaling Peptides and Proteins* / metabolism
  • Membrane Proteins* / genetics
  • Membrane Proteins* / metabolism
  • Phosphorylation
  • Rats
  • Sterol Regulatory Element Binding Protein 1* / genetics
  • Sterol Regulatory Element Binding Protein 1* / metabolism
  • Sterol Regulatory Element Binding Protein 2 / metabolism

Substances

  • Membrane Proteins
  • Sterol Regulatory Element Binding Protein 1
  • Intracellular Signaling Peptides and Proteins
  • Cyclic AMP-Dependent Protein Kinases
  • INSIG2 protein, human
  • Fatty Acids, Unsaturated
  • Fatty Acids
  • Eicosapentaenoic Acid
  • Sterol Regulatory Element Binding Protein 2
  • INSIG1 protein, human
  • SREBF1 protein, human