Formation of tubules and helical ribbons by ceramide phosphoethanolamine-containing membranes

Abstract

Ceramide phosphoethanolamine (CPE), a major sphingolipid in invertebrates, is crucial for axonal ensheathment in Drosophila . Darkfield microscopy revealed that an equimolar mixture of bovine buttermilk CPE (milk CPE) and 1,2-dioleoyl- sn -glycero-3-phosphocholine (diC18:1 PC) tends to form tubules and helical ribbons, while pure milk CPE mainly exhibits amorphous aggregates and, at low frequency, straight needles. Negative staining electron microscopy indicated that helices and tubules were composed of multilayered 5–10 nm thick slab-like structures. Using different molecular species of PC and CPE, we demonstrated that the acyl chain length of CPE but not of PC is crucial for the formation of tubules and helices in equimolar mixtures. Incubation of the lipid suspensions at the respective phase transition temperature of CPE facilitated the formation of both tubules and helices, suggesting a dynamic lipid rearrangement during formation. Substituting diC18:1 PC with diC18:1 PE or diC18:1 PS failed to form tubules and helices. As hydrated galactosylceramide (GalCer), a major lipid in mammalian myelin, has been reported to spontaneously form tubules and helices, it is believed that the ensheathment of axons in mammals and Drosophila is based on similar physical processes with different lipids.

Glucosylceramide Associated with Gaucher Disease Forms Amyloid-like Twisted Ribbon Fibrils That Induce α-Synuclein Aggregation

“…45 These structural parameters of GlcCer are also very similar to those reported for in vitro generated GalCer fibrils, where 20:1 Δ11 GalCer aggregates formed helical ribbons that have a right-handed twist with an average width of 30−35 nm and helical pitches of 80−90 nm. 46,47,64 Our combined FTIR and X-ray scattering results indicate that the free GlcCer spontaneously forms a lamellar phase in which the long-chain nonpolar tails of GlcCer monomers interact with each other to organize pairwise in a tail-to-tail configuration, and the polar glycan head groups remain exposed to the aqueous medium. The AFM analysis showed that the average width of the GlcCer fibrils was 29 ± 8 nm.…”

“… 45 These structural parameters of GlcCer are also very similar to those reported for in vitro generated GalCer fibrils, where 20:1 Δ11 GalCer aggregates formed helical ribbons that have a right-handed twist with an average width of 30–35 nm and helical pitches of 80–90 nm. 46 , 47 , 64 …”

Endosomes deliver ceramide phosphoethanolamine with unique acyl chain 2 anchors to the cleavage furrow during male meiotic cytokinesis

“…Previous studies have shown that CPE has an essential role in axonal ensheathment and cortex glial plasma membrane expansion in Drosophila [15,63]. It was hypothesized that the axonal ensheathment in mammals and Drosophila is based on similar physical process with different lipids [62]. We have previously shown that sphingomyelin, a structural analog of CPE, could rescue cortex glial membrane defects in cpes mutants suggesting the head group is not as important as the tail in glial membranes.…”

“…Glycosphingolipids with VLC/ULC PUFAs have been shown to be required for mammalian male meiotic cytokinesis but their actual role has not been delineated [13, 60, 61]. It is interesting to note that CPE mimics certain physical properties of galactosylceramide (GalCer) a major sphingolipid in myelin sheath [62]. Previous studies have shown that CPE has an essential role in axonal ensheathment and cortex glial plasma membrane expansion in Drosophila [15, 63].…”

Endosomes deliver ceramide phosphoethanolamine with unique acyl chain anchors to the cleavage furrow during male meiotic cytokinesis

“…Previous studies have shown that CPE has an essential role in axonal ensheathment and cortex glial plasma membrane expansion in Drosophila [15,50]. It was hypothesized that the axonal ensheathment in mammals and Drosophila is based on similar physical process with different lipids [49]. We have previously shown that sphingomyelin, a structural analogue of CPE, could rescues cortex glial membrane defects in cpes mutants suggesting the head group is not as important as the tail group in glial membranes.…”