Enhanced Membrane Fluidization and Cholesterol Displacement by 1-Heptanol Inhibit Mast Cell Effector Functions

Cells. 2023 Aug 15;12(16):2069. doi: 10.3390/cells12162069.

Abstract

Signal transduction by the high-affinity IgE receptor (FcεRI) depends on membrane lipid and protein compartmentalization. Recently published data show that cells treated with 1-heptanol, a cell membrane fluidizer, exhibit changes in membrane properties. However, the functional consequences of 1-heptanol-induced changes on mast cell signaling are unknown. This study shows that short-term exposure to 1-heptanol reduces membrane thermal stability and dysregulates mast cell signaling at multiple levels. Cells treated with 1-heptanol exhibited increased lateral mobility and decreased internalization of the FcεRI. However, this did not affect the initial phosphorylation of the FcεRI-β chain and components of the SYK/LAT1/PLCγ1 signaling pathway after antigen activation. In contrast, 1-heptanol inhibited SAPK/JNK phosphorylation and effector functions such as calcium response, degranulation, and cytokine production. Membrane hyperfluidization induced a heat shock-like response via increased expression of the heat shock protein 70, increased lateral diffusion of ORAI1-mCherry, and unsatisfactory performance of STIM1-ORAI1 coupling, as determined by flow-FRET. Furthermore, 1-heptanol inhibited the antigen-induced production of reactive oxygen species and potentiated stress-induced plasma membrane permeability by interfering with heat shock protein 70 activity. The combined data suggest that 1-heptanol-mediated membrane fluidization does not interfere with the earliest biochemical steps of FcεRI signaling, such as phosphorylation of the FcεRI-β chain and components of the SYK/LAT/PLCγ1 signaling pathway, instead inhibiting the FcεRI internalization and mast cell effector functions, including degranulation and cytokine production.

Keywords: FRAP; FcεRI signaling; STIM1-ORAI1 coupling; alkanol; flow-FRET; heat shock response; membrane fluidizer; store-operated calcium entry.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cholesterol
  • Cytokines
  • Heptanol
  • Mast Cells*
  • Signal Transduction*

Substances

  • Heptanol
  • Cholesterol
  • Cytokines

Grants and funding

This research was funded in part by project 23-07736S from the Czech Science Foundation and Institutional project RVO 68378050 from the Czech Academy of Sciences. We acknowledge the CZ-OPENSCREEN (LM2023052) for financial support and Light Microscopy Core Facility, IMG, Prague, Czech Republic, supported by MEYS—LM2023050 and RVO—68378050-KAV-NPUI, for their support with the FRAP analysis.