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Nanoscale Packing Differences in Sphingomyelin and Phosphatidylcholine Revealed by BODIPY Fluorescence in Monolayers: Physiological Implications
[Image: see text] 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...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American
Chemical Society
2014
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3983355/ https://www.ncbi.nlm.nih.gov/pubmed/24564829 http://dx.doi.org/10.1021/la4047098 |
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author | Zhai, Xiuhong Boldyrev, Ivan A. Mizuno, Nancy K. Momsen, Maureen M. Molotkovsky, Julian G. Brockman, Howard L. Brown, Rhoderick E. |
author_facet | Zhai, Xiuhong Boldyrev, Ivan A. Mizuno, Nancy K. Momsen, Maureen M. Molotkovsky, Julian G. Brockman, Howard L. Brown, Rhoderick E. |
author_sort | Zhai, Xiuhong |
collection | PubMed |
description | [Image: see text] 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 Me(4)-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, Me(4)-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. |
format | Online Article Text |
id | pubmed-3983355 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2014 |
publisher | American
Chemical Society |
record_format | MEDLINE/PubMed |
spelling | pubmed-39833552015-02-24 Nanoscale Packing Differences in Sphingomyelin and Phosphatidylcholine Revealed by BODIPY Fluorescence in Monolayers: Physiological Implications Zhai, Xiuhong Boldyrev, Ivan A. Mizuno, Nancy K. Momsen, Maureen M. Molotkovsky, Julian G. Brockman, Howard L. Brown, Rhoderick E. Langmuir [Image: see text] 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 Me(4)-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, Me(4)-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. American Chemical Society 2014-02-24 2014-03-25 /pmc/articles/PMC3983355/ /pubmed/24564829 http://dx.doi.org/10.1021/la4047098 Text en Copyright © 2014 American Chemical Society |
spellingShingle | Zhai, Xiuhong Boldyrev, Ivan A. Mizuno, Nancy K. Momsen, Maureen M. Molotkovsky, Julian G. Brockman, Howard L. Brown, Rhoderick E. Nanoscale Packing Differences in Sphingomyelin and Phosphatidylcholine Revealed by BODIPY Fluorescence in Monolayers: Physiological Implications |
title | Nanoscale Packing Differences in Sphingomyelin and
Phosphatidylcholine Revealed by BODIPY Fluorescence in Monolayers:
Physiological Implications |
title_full | Nanoscale Packing Differences in Sphingomyelin and
Phosphatidylcholine Revealed by BODIPY Fluorescence in Monolayers:
Physiological Implications |
title_fullStr | Nanoscale Packing Differences in Sphingomyelin and
Phosphatidylcholine Revealed by BODIPY Fluorescence in Monolayers:
Physiological Implications |
title_full_unstemmed | Nanoscale Packing Differences in Sphingomyelin and
Phosphatidylcholine Revealed by BODIPY Fluorescence in Monolayers:
Physiological Implications |
title_short | Nanoscale Packing Differences in Sphingomyelin and
Phosphatidylcholine Revealed by BODIPY Fluorescence in Monolayers:
Physiological Implications |
title_sort | nanoscale packing differences in sphingomyelin and
phosphatidylcholine revealed by bodipy fluorescence in monolayers:
physiological implications |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3983355/ https://www.ncbi.nlm.nih.gov/pubmed/24564829 http://dx.doi.org/10.1021/la4047098 |
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