Dataset Information

Nanoscale packing differences in sphingomyelin and phosphatidylcholine revealed by BODIPY fluorescence in monolayers: physiological implications.

ABSTRACT: Phosphatidycholines (PC) with two saturated acyl chains (e.g., dipalmitoyl) mimic natural sphingomyelin (SM) by promoting raft formation in model membranes. However, sphingoid-based lipids, such as SM, rather than saturated-chain PCs have been implicated as key components of lipid rafts in biomembranes. These observations raise questions about the physical packing properties of the phase states that can be formed by these two major plasma membrane lipids with identical phosphocholine headgroups. To investigate, we developed a monolayer platform capable of monitoring changes in surface fluorescence by acquiring multiple spectra during measurement of a lipid force-area isotherm. We relied on the concentration-dependent emission changes of 4,4-difluoro-4-bora-3a,4a-diaza-s-indacene (BODIPY)-labeled PC to detect nanoscale alterations in lipid packing and phase state induced by monolayer lateral compression. The BODIPY-PC probe contained an indacene ring with four symmetrically located methyl (Me) substituents to enhance localization to the lipid hydrocarbon region. Surface fluorescence spectra indicated changes in miscibility even when force-area isotherms showed no deviation from ideal mixing behavior in the surface pressure versus cross-sectional molecular area response. We detected slightly better mixing of Me4-BODIPY-8-PC with the fluid-like, liquid expanded phase of 1-palmitoyl-2-oleoyl-PC compared to N-oleoyl-SM. Remarkably, in the gel-like, liquid condensed phase, Me4-BODIPY-8-PC mixed better with N-palmitoyl-SM than dipalmitoyl-PC, suggesting naturally abundant SMs with saturated acyl chains form gel-like lipid phase(s) with enhanced ability to accommodate deeply embedded components compared to dipalmitoyl-PC gel phase. The findings reveal a fundamental difference in the lateral packing properties of SM and PC that occurs even when their acyl chains match.

SUBMITTER: Zhai X

PROVIDER: S-EPMC3983355 | biostudies-literature | 2014 Mar

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Nanoscale packing differences in sphingomyelin and phosphatidylcholine revealed by BODIPY fluorescence in monolayers: physiological implications.

Zhai Xiuhong X Boldyrev Ivan A IA Mizuno Nancy K NK Momsen Maureen M MM Molotkovsky Julian G JG Brockman Howard L HL Brown Rhoderick E RE

Langmuir : the ACS journal of surfaces and colloids 20140311 11

Phosphatidycholines (PC) with two saturated acyl chains (e.g., dipalmitoyl) mimic natural sphingomyelin (SM) by promoting raft formation in model membranes. However, sphingoid-based lipids, such as SM, rather than saturated-chain PCs have been implicated as key components of lipid rafts in biomembranes. These observations raise questions about the physical packing properties of the phase states that can be formed by these two major plasma membrane lipids with identical phosphocholine headgroups. ...[more]

PMID: 24564829

Similar Datasets

Project description:Sphingomyelin, one of the main lipid components of biological membranes, is actively involved in various cellular processes such as protein trafficking and signal transduction. In particular, specific lateral domains enriched in sphingomyelin and cholesterol have been proposed to play an important functional role in biomembranes, although their precise characteristics have remained unclear. A thorough understanding of the functional role of membranes requires detailed knowledge of their individual lipid components. Here, we employ molecular dynamics simulations to conduct a systematic comparison of a palmitoylsphingomyelin (PSM, 16:0-SM) bilayer with a membrane that comprises dipalmitoylphosphatidylcholine (DPPC) above the main phase transition temperature. We clarify atomic-scale properties that are specific to sphingomyelin due to its sphingosine moiety, and further discuss their implications for SM-rich membranes. We find that PSM bilayers, and in particular the dynamics of PSM systems, are distinctly different from those of a DPPC bilayer. When compared with DPPC, the strong hydrogen bonding properties characteristic to PSM are observed to lead to considerable structural changes in the polar headgroup and interface regions. The strong ordering of PSM acyl chains and specific ordering effects in the vicinity of a PSM-water interface reflect this issue clearly. The sphingosine moiety and related hydrogen bonding further play a crucial role in the dynamics of PSM bilayers, as most dynamic properties, such as lateral and rotational diffusion, are strongly suppressed. This is most evident in the rotational motion characterized by spin-lattice relaxation times and the decay of hydrogen bond autocorrelation functions that are expected to be important in complexation of SM with other lipids in many-component bilayers. A thorough understanding of SM bilayers would greatly benefit from nuclear magnetic resonance experiments for acyl chain ordering and dynamics, allowing full comparison of these simulations to experiments.

Dataset Information

Nanoscale packing differences in sphingomyelin and phosphatidylcholine revealed by BODIPY fluorescence in monolayers: physiological implications.

Publications

Nanoscale packing differences in sphingomyelin and phosphatidylcholine revealed by BODIPY fluorescence in monolayers: physiological implications.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets