Bilayer nanotubes and helical ribbons formed by hydrated galactosylceramides: acyl chain and headgroup effects

V. S. Kulkarni, W. H. Anderson, Rhoderick E Brown

Research output: Contribution to journalArticlepeer-review

56 Scopus citations

Abstract

The molecular basis of bilayer tubule formation in hydrated galactosylceramide (GalCer) dispersions has been investigated by synthesizing different chain-pure GalCers and examining their aqueous mesomorphic phase structure by freeze fracture and negative-stain electron microscopy. Thermotropic characterization of the GalCer species by differential scanning calorimetry provided supplementary information that verified the phase state under which morphological observations were carried out. Under aqueous conditions and at room temperature, N-24:1 delta 15(cis) GalSph, the predominant monounsaturated, nonhydroxy acyl species of bovine brain GalCer (NFA-GalCer), formed cylindrical mesomorphic self-assemblies consisting almost exclusively of "nanotubes," i.e., lipid bilayer tubules of relatively uniform length and diameter (length, 250–400 nm; diameter, 25–30 nm). In contrast, N-24:0 GalSph, the major saturated, nonhydroxy acyl species of bovine brain GalCer, displayed no tendency to form these relatively small "nanotubes." Rather, N-24:0 GalSph formed larger, variable-length ribbon-like structures (length, 5,000–10,000 nm) that often appeared to undulate and, occasionally, appeared to be helically twisted. Interestingly, bovine brain GalCer, which contains high levels of the N-24:1 delta 15(cis) and N-24:0 species as well as 2-hydroxy acyl chains, formed multilamellar liposomes of variable size and showed little tendency to form cylindrical structures. This result suggested that changes to the polar interface/headgroup region imparted by the 2-hydroxy acyl species strongly influenced bilayer tubule and cylinder formation in GalCer. To define this influence more clearly, other sphingoid-based and glycerol-based lipids were investigated. Morphological characterization of N-24:1 delta 15(cis) sphingosylphosphorylcholine (24:1 SM) revealed no evidence of bilayer cylinder or tubule formation. Similar results were obtained with aqueous dispersions of 1-palmitoyl-2-nervonoyl phosphatidylcholine (16:0, 24:1 PC). Hence, the bulkier, more hydrated, zwitterionic phosphocholine headgroup inhibited the formation of bilayer nanotubes and cylinders under physiological saline conditions.

Original languageEnglish (US)
Pages (from-to)1976-1986
Number of pages11
JournalBiophysical journal
Volume69
Issue number5
DOIs
StatePublished - 1995

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