SPTLC3 regulates plasma membrane sphingolipid composition to facilitate hepatic gluconeogenesis

Cell Rep. 2024 Dec 24;43(12):115054. doi: 10.1016/j.celrep.2024.115054. Epub 2024 Dec 10.

Abstract

SPTLC3, an inducible subunit of the serine palmitoyltransferase (SPT) complex, causes production of alternative sphingoid bases, including a 16-carbon dihydrosphingosine, whose biological function is only beginning to emerge. High-fat feeding induced SPTLC3 in the liver, prompting us to produce a liver-specific knockout mouse line. Following high-fat feeding, knockout mice showed decreased fasting blood glucose, and knockout primary hepatocytes showed suppressed glucose production, a core function of hepatocytes. Stable isotope tracing revealed suppression of the gluconeogenic pathway, finding that SPTLC3 was required to maintain expression of key gluconeogenic genes via adenylate cyclase/cyclic AMP (cAMP)/cAMP response element binding protein (CREB) signaling. Additionally, by employing a combination of a recently developed lipidomics methodology, exogenous C14/C16 fatty acid treatment, and in situ adenylate cyclase activity, we implicated a functional interaction between sphingomyelin with a d16 backbone and adenylate cyclase at the plasma membrane. This work pinpoints a specific sphingolipid-protein functional interaction with broad implications for understanding sphingolipid signaling and metabolic disease.

Keywords: CP: Metabolism; MAFLD; SPT; SPTLC3; adenylate cylcase; ceramide; cyclic-AMP; gluconeogenesis; metabolic disease; sphingolipid; sphingomyelin.

MeSH terms

  • Adenylyl Cyclases / metabolism
  • Animals
  • Cell Membrane* / metabolism
  • Cyclic AMP / metabolism
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Gluconeogenesis*
  • Hepatocytes* / metabolism
  • Liver* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout*
  • Serine C-Palmitoyltransferase* / genetics
  • Serine C-Palmitoyltransferase* / metabolism
  • Signal Transduction
  • Sphingolipids* / metabolism
  • Sphingomyelins / metabolism

Substances

  • Sphingolipids
  • Serine C-Palmitoyltransferase
  • Cyclic AMP Response Element-Binding Protein
  • Adenylyl Cyclases
  • Cyclic AMP
  • Sphingomyelins