Interaction of sphingomyelinase with sphingomyelin-containing supported membranes

Viviane N. Ngassam, Ann E. Oliver, Phuong N. Dang, Eric L. Kendall, Sean F. Gilmore, Atul N. Parikh

Research output: Contribution to journalArticle

Abstract

We have studied the interaction of the enzyme sphingomyelinase with sphingomyelin-containing supported membranes using quantitative applications of real-time epifluorescence microscopy and imaging optical ellipsometry. The enzymatic action converts sphingomyelin into ceramides by cleaving the phosphodiester bond. Our results confirm previous studies establishing a gross morphological transformation of lipid bilayers involving a multi-step process consisting of lag-burst type of enzyme activation and in-plane reorganization of membrane components attributed to the formation of ceramide-enriched domains. A unique finding of our study is the evidence for the existence of an additional out-of-plane deformation following lateral reorganization resulting in membrane voids disrupting the laterally contiguous bilayer. Taken together, the in-plane and out-of-plane deformations suggest a mechanistic picture in which lateral diffusional processes of translational mobility and phase separation couple with out-of-plane interactions across the membrane leaflet to induce irreversible membrane disruption in response to SMase action. Remarkably, lipid monolayers supported on hydrophobic substrates exhibit no such large-scale deformation despite ceramide generation by enzymatic activity of sphingomyelinase, possibly suggesting the importance of coupling across membrane leaflets in inducing out-of-plane deformations.

Original languageEnglish (US)
Pages (from-to)10413-10420
Number of pages8
JournalSoft Matter
Volume9
Issue number43
DOIs
StatePublished - Nov 21 2013

ASJC Scopus subject areas

  • Chemistry(all)
  • Condensed Matter Physics

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    Ngassam, V. N., Oliver, A. E., Dang, P. N., Kendall, E. L., Gilmore, S. F., & Parikh, A. N. (2013). Interaction of sphingomyelinase with sphingomyelin-containing supported membranes. Soft Matter, 9(43), 10413-10420. https://doi.org/10.1039/c3sm51855h