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

Fingerprint

Sphingomyelin Phosphodiesterase
Sphingomyelins
membranes
Membranes
Ceramides
interactions
lipids
enzymes
disrupting
Lipid bilayers
Ellipsometry
Enzymes
Phase separation
ellipsometry
voids
Monolayers
bursts
Microscopic examination
time lag
Chemical activation

ASJC Scopus subject areas

  • Chemistry(all)
  • Condensed Matter Physics

Cite this

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

Interaction of sphingomyelinase with sphingomyelin-containing supported membranes. / Ngassam, Viviane N.; Oliver, Ann E.; Dang, Phuong N.; Kendall, Eric L.; Gilmore, Sean F.; Parikh, Atul N.

In: Soft Matter, Vol. 9, No. 43, 21.11.2013, p. 10413-10420.

Research output: Contribution to journalArticle

Ngassam, VN, Oliver, AE, Dang, PN, Kendall, EL, Gilmore, SF & Parikh, AN 2013, 'Interaction of sphingomyelinase with sphingomyelin-containing supported membranes', Soft Matter, vol. 9, no. 43, pp. 10413-10420. https://doi.org/10.1039/c3sm51855h
Ngassam VN, Oliver AE, Dang PN, Kendall EL, Gilmore SF, Parikh AN. Interaction of sphingomyelinase with sphingomyelin-containing supported membranes. Soft Matter. 2013 Nov 21;9(43):10413-10420. https://doi.org/10.1039/c3sm51855h
Ngassam, Viviane N. ; Oliver, Ann E. ; Dang, Phuong N. ; Kendall, Eric L. ; Gilmore, Sean F. ; Parikh, Atul N. / Interaction of sphingomyelinase with sphingomyelin-containing supported membranes. In: Soft Matter. 2013 ; Vol. 9, No. 43. pp. 10413-10420.
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