Phospholipase C-related catalytically inactive protein (PRIP) regulates lipolysis in adipose tissue by modulating the phosphorylation of hormone-sensitive lipase

PLoS One. 2014 Jun 19;9(6):e100559. doi: 10.1371/journal.pone.0100559. eCollection 2014.

Abstract

Phosphorylation of hormone-sensitive lipase (HSL) and perilipin by protein kinase A (PKA) promotes the hydrolysis of lipids in adipocytes. Although activation of lipolysis by PKA has been well studied, inactivation via protein phosphatases is poorly understood. Here, we investigated whether phospholipase C-related catalytically inactive protein (PRIP), a binding partner for protein phosphatase 1 and protein phosphatase 2A (PP2A), is involved in lipolysis by regulating phosphatase activity. PRIP knockout (PRIP-KO) mice displayed reduced body-fat mass as compared with wild-type mice fed with standard chow ad libitum. Most other organs appeared normal, suggesting that mutant mice had aberrant fat metabolism in adipocytes. HSL in PRIP-KO adipose tissue was highly phosphorylated compared to that in wild-type mice. Starvation of wild-type mice or stimulation of adipose tissue explants with the catabolic hormone, adrenaline, translocated both PRIP and PP2A from the cytosol to lipid droplets, but the translocation of PP2A was significantly reduced in PRIP-KO adipocytes. Consistently, the phosphatase activity associated with lipid droplet fraction in PRIP-KO adipocytes was significantly reduced and was independent of adrenaline stimulation. Lipolysis activity, as assessed by measurement of non-esterified fatty acids and glycerol, was higher in PRIP-KO adipocytes. When wild-type adipocytes were treated with a phosphatase inhibitor, they showed a high lipolysis activity at the similar level to PRIP-KO adipocytes. Collectively, these results suggest that PRIP promotes the translocation of phosphatases to lipid droplets to trigger the dephosphorylation of HSL and perilipin A, thus reducing PKA-mediated lipolysis.

MeSH terms

  • Adipocytes / drug effects
  • Adipocytes / metabolism
  • Adipose Tissue / drug effects
  • Adipose Tissue / metabolism*
  • Animals
  • COS Cells
  • Carrier Proteins / metabolism*
  • Chlorocebus aethiops
  • Cytosol / drug effects
  • Cytosol / metabolism
  • Epinephrine / pharmacology
  • Intracellular Signaling Peptides and Proteins
  • Lipid Droplets / drug effects
  • Lipid Droplets / metabolism
  • Lipolysis* / drug effects
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Models, Biological
  • Perilipin-1
  • Phosphoproteins / metabolism
  • Phosphorylation / drug effects
  • Protein Phosphatase 1 / metabolism
  • Protein Phosphatase 2 / metabolism
  • Protein Transport / drug effects
  • Sterol Esterase / metabolism*
  • Subcellular Fractions / drug effects
  • Subcellular Fractions / metabolism

Substances

  • Carrier Proteins
  • Intracellular Signaling Peptides and Proteins
  • PRIP-1 phospholipase C-related protein, mouse
  • Perilipin-1
  • Phosphoproteins
  • Sterol Esterase
  • Protein Phosphatase 1
  • Protein Phosphatase 2
  • Epinephrine

Grants and funding

This work was supported by funding from the Funding Program for Next Generation World-Leading Researchers (LS087) to T.K., and by JSPS KAKENHI (Grant No. 25861757 to K.H., Grant No. 25861756 to S.A., Grant No. 24229009 to M.H.). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.