Trifunctional sphingomyelin derivatives enable nanoscale resolution of sphingomyelin turnover in physiological and infection processes via expansion microscopy

Marcel Rühling, Louise Kersting, Fabienne Wagner, Fabian Schumacher, Dominik Wigger, Dominic A. Helmerich, Tom Pfeuffer, Robin Elflein, Christian Kappe, Markus Sauer, Christoph Arenz, Burkhard Kleuser, Thomas Rudel, Martin Fraunholz and Jürgen Seibel ()
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Marcel Rühling: Julius-Maximilians-University Würzburg
Louise Kersting: Julius-Maximilians-University Würzburg
Fabienne Wagner: Julius-Maximilians-University Würzburg
Fabian Schumacher: Freie Universität Berlin
Dominik Wigger: Freie Universität Berlin
Dominic A. Helmerich: Julius-Maximilians-University Würzburg
Tom Pfeuffer: Julius-Maximilians-University Würzburg
Robin Elflein: Julius-Maximilians-University Würzburg
Christian Kappe: Brook-Taylor-Str 2
Markus Sauer: Julius-Maximilians-University Würzburg
Christoph Arenz: Brook-Taylor-Str 2
Burkhard Kleuser: Freie Universität Berlin
Thomas Rudel: Julius-Maximilians-University Würzburg
Martin Fraunholz: Julius-Maximilians-University Würzburg
Jürgen Seibel: Julius-Maximilians-University Würzburg

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract Sphingomyelin is a key molecule of sphingolipid metabolism, and its enzymatic breakdown is associated with various infectious diseases. Here, we introduce trifunctional sphingomyelin derivatives that enable the visualization of sphingomyelin distribution and sphingomyelinase activity in infection processes. We demonstrate this by determining the activity of a bacterial sphingomyelinase on the plasma membrane of host cells using a combination of Förster resonance energy transfer and expansion microscopy. We further use our trifunctional sphingomyelin probes to visualize their metabolic state during infections with Chlamydia trachomatis and thereby show that chlamydial inclusions primarily contain the cleaved forms of the molecules. Using expansion microscopy, we observe that the proportion of metabolized molecules increases during maturation from reticulate to elementary bodies, indicating different membrane compositions between the two chlamydial developmental forms. Expansion microscopy of trifunctional sphingomyelins thus provides a powerful microscopy tool to analyze sphingomyelin metabolism in cells at nanoscale resolution.

Date: 2024
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DOI: 10.1038/s41467-024-51874-w

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