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Intermolecular interaction of phosphatidylinositol with the lipid raft molecules sphingomyelin and cholesterol

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ABSTRACT

Diacylphosphatidylinositol (PI) is the starting reactant in the process of phosphatidylinositide-related signal transduction mediated through the lipid raft domain. We investigated intermolecular interactions of PI with major raft components, sphingomyelin (SM) and cholesterol (Chol), using surface pressure–molecular area (π–A) isotherm measurements. The classical mean molecular area versus composition plot showed that the measured mean molecular areas are smaller in PI/Chol mixed monolayers and larger in PI/SM mixed monolayers than those calculated on the basis of the ideal additivity. These results indicate that PI interacts attractively with Chol and repulsively with SM. In addition, we energetically evaluated the interaction of PI with SM/Chol mixtures and found that the mixing energy of PI/SM/Chol ternary monolayers decreased as the molar ratio of Chol to SM increased. In order to quantitatively analyze the distribution of PI we calculated the chemical potentials of mixing of PI into the SM/Chol mixed monolayer and into the dioleoylphosphatidylcholine (DOPC) monolayer, which was used as a model for the fluid matrix, on the basis of partial molecular area analysis. Analysis using the chemical potential of mixing of PI suggested that partition of PI molecules between these two monolayers can be changed by a factor of about 1.7 in response to change in Chol molar fraction in the SM/Chol mixed monolayer from 0.3 to 0.6 when the concentration of PI in the DOPC monolayer is kept constant at 7 mol%.

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Chol-induced redistribution of PI molecules between the SCm and the fluid matrix, speculated from the results obtained in the model monolayer systems. When rChol∼0.3, PI may be equally distributed between the fluid matrix and the SCm (upper). The PI molecules will be gradually transferred from the fluid matrix to the SCm as rChol increases (lower).
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f7-4_1: Chol-induced redistribution of PI molecules between the SCm and the fluid matrix, speculated from the results obtained in the model monolayer systems. When rChol∼0.3, PI may be equally distributed between the fluid matrix and the SCm (upper). The PI molecules will be gradually transferred from the fluid matrix to the SCm as rChol increases (lower).

Mentions: Our results suggested that PI concentration in the SCm (model raft) can be controlled by a factor of about 1.7 (0.12/0.07) as rChol is changed between 0.3 and 0.6 (Fig. 7). Furthermore, the behavior of ΔμPI in the range of small XPI suggested that the condensation rate is much larger than 1.7 if the molar fraction of PI in the fluid DOPC matrix is much smaller than 0.07. If the results obtained for PI molecules are applicable to phospatidylinositides such as PIP2, whose concentration in the membrane is quite low, they might be concentrated in the SCm domain at a high rate. Thus, these static analyses showed fairly good agreement with the characteristics of PI distribution in biomembranes notwithstanding the difference between artificial monolayers and biomembranes; in addition to the structural difference as mentioned above the processes in biological membranes are dynamical. Although the results obtained in an artificial system should not be applied straightforwardly to the biological system and further studies with bilayer systems are needed, analysis based on the partial-specific area will be a useful tool for quantitative understanding of incorporation of various molecules into the raft domain.


Intermolecular interaction of phosphatidylinositol with the lipid raft molecules sphingomyelin and cholesterol
Chol-induced redistribution of PI molecules between the SCm and the fluid matrix, speculated from the results obtained in the model monolayer systems. When rChol∼0.3, PI may be equally distributed between the fluid matrix and the SCm (upper). The PI molecules will be gradually transferred from the fluid matrix to the SCm as rChol increases (lower).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC5036605&req=5

f7-4_1: Chol-induced redistribution of PI molecules between the SCm and the fluid matrix, speculated from the results obtained in the model monolayer systems. When rChol∼0.3, PI may be equally distributed between the fluid matrix and the SCm (upper). The PI molecules will be gradually transferred from the fluid matrix to the SCm as rChol increases (lower).
Mentions: Our results suggested that PI concentration in the SCm (model raft) can be controlled by a factor of about 1.7 (0.12/0.07) as rChol is changed between 0.3 and 0.6 (Fig. 7). Furthermore, the behavior of ΔμPI in the range of small XPI suggested that the condensation rate is much larger than 1.7 if the molar fraction of PI in the fluid DOPC matrix is much smaller than 0.07. If the results obtained for PI molecules are applicable to phospatidylinositides such as PIP2, whose concentration in the membrane is quite low, they might be concentrated in the SCm domain at a high rate. Thus, these static analyses showed fairly good agreement with the characteristics of PI distribution in biomembranes notwithstanding the difference between artificial monolayers and biomembranes; in addition to the structural difference as mentioned above the processes in biological membranes are dynamical. Although the results obtained in an artificial system should not be applied straightforwardly to the biological system and further studies with bilayer systems are needed, analysis based on the partial-specific area will be a useful tool for quantitative understanding of incorporation of various molecules into the raft domain.

View Article: PubMed Central - PubMed

ABSTRACT

Diacylphosphatidylinositol (PI) is the starting reactant in the process of phosphatidylinositide-related signal transduction mediated through the lipid raft domain. We investigated intermolecular interactions of PI with major raft components, sphingomyelin (SM) and cholesterol (Chol), using surface pressure–molecular area (π–A) isotherm measurements. The classical mean molecular area versus composition plot showed that the measured mean molecular areas are smaller in PI/Chol mixed monolayers and larger in PI/SM mixed monolayers than those calculated on the basis of the ideal additivity. These results indicate that PI interacts attractively with Chol and repulsively with SM. In addition, we energetically evaluated the interaction of PI with SM/Chol mixtures and found that the mixing energy of PI/SM/Chol ternary monolayers decreased as the molar ratio of Chol to SM increased. In order to quantitatively analyze the distribution of PI we calculated the chemical potentials of mixing of PI into the SM/Chol mixed monolayer and into the dioleoylphosphatidylcholine (DOPC) monolayer, which was used as a model for the fluid matrix, on the basis of partial molecular area analysis. Analysis using the chemical potential of mixing of PI suggested that partition of PI molecules between these two monolayers can be changed by a factor of about 1.7 in response to change in Chol molar fraction in the SM/Chol mixed monolayer from 0.3 to 0.6 when the concentration of PI in the DOPC monolayer is kept constant at 7 mol%.

No MeSH data available.