Tuberous sclerosis complex 2 loss increases lysophosphatidylcholine synthesis in lymphangioleiomyomatosis

Am J Respir Cell Mol Biol. 2015 Jul;53(1):33-41. doi: 10.1165/rcmb.2014-0379RC.

Abstract

Lymphangioleiomyomatosis (LAM) is a destructive lung disease affecting women. LAM is caused by mutations in the tuberous sclerosis complex (TSC) genes. The TSC protein complex inhibits the mechanistic/mammalian target of rapamycin complex 1 (mTORC1), which is a master regulator of cellular metabolism. Using mass spectrometry-based lipid profiling, we analyzed plasma from patients with LAM and discovered elevated levels of four lysophosphatidylcholine (LPC) species (C16:0, C18:0, C18:1, and C20:4) compared with those in healthy control women. To investigate whether these lipids are generated in a TSC2-dependent manner, we profiled in vitro preclinical models of TSC/LAM and found significant LPC accumulation in TSC2-deficient cells relative to TSC2-expressing control cells. These lysoglycerophospholipid changes occurred alongside changes in other phospholipid and neutral lipid species. Treatment with rapamycin or torin1 or down-regulation of sterol regulatory element-binding protein (SREBP), a lipogenic transcription factor, did not suppress LPC in TSC2-deficient cells. Inhibition of distinct isoforms of phospholipase A2 decreased the proliferation of TSC2-deficient cells. Collectively, these results demonstrate that TSC2-deficient cells have enhanced choline phospholipid metabolism and reveal a novel function of the TSC proteins in choline lysoglycerophospholipid metabolism, with implications for disease pathogenesis and targeted therapeutic strategies.

Keywords: lipidomics; mTORC1; mass spectrometry; phospholipase.

Publication types

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

MeSH terms

  • Animals
  • Antibiotics, Antineoplastic / pharmacology
  • Cell Line, Tumor
  • Female
  • Humans
  • Lipid Metabolism*
  • Lymphangioleiomyomatosis / genetics
  • Lymphangioleiomyomatosis / metabolism*
  • Lymphangioleiomyomatosis / pathology
  • Lysophosphatidylcholines / biosynthesis*
  • Lysophosphatidylcholines / genetics
  • Mass Spectrometry
  • Mechanistic Target of Rapamycin Complex 1
  • Mice
  • Mice, Knockout
  • Multiprotein Complexes / genetics
  • Multiprotein Complexes / metabolism
  • Naphthyridines / pharmacology
  • Phospholipases A2 / genetics
  • Phospholipases A2 / metabolism
  • Rats
  • Sirolimus / pharmacology
  • Sterol Regulatory Element Binding Proteins / genetics
  • Sterol Regulatory Element Binding Proteins / metabolism
  • TOR Serine-Threonine Kinases / genetics
  • TOR Serine-Threonine Kinases / metabolism
  • Tuberous Sclerosis Complex 2 Protein
  • Tumor Suppressor Proteins / deficiency*

Substances

  • 1-(4-(4-propionylpiperazin-1-yl)-3-(trifluoromethyl)phenyl)-9-(quinolin-3-yl)benzo(h)(1,6)naphthyridin-2(1H)-one
  • Antibiotics, Antineoplastic
  • Lysophosphatidylcholines
  • Multiprotein Complexes
  • Naphthyridines
  • Sterol Regulatory Element Binding Proteins
  • TSC2 protein, human
  • Tsc2 protein, mouse
  • Tsc2 protein, rat
  • Tuberous Sclerosis Complex 2 Protein
  • Tumor Suppressor Proteins
  • Mechanistic Target of Rapamycin Complex 1
  • TOR Serine-Threonine Kinases
  • Phospholipases A2
  • Sirolimus