Adsorption of bile salts and pancreatic colipase and lipase onto digalactosyldiacylglycerol and dipalmitoylphosphatidylcholine monolayers

Boon-Seang Chu, A. Patrick Gunning, Gillian T. Rich, Mike J. Ridout, Richard M. Faulks, Martin S. J. Wickham, Victor J. Morris, Peter J. Wilde

Research output: Contribution to journalArticle

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Abstract

It is increasingly recognized that changes in the composition of the oil−water interface can markedly affect pancreatic lipase adsorption and function. To understand interfacial mechanisms determining lipase activity, we investigated the adsorption behavior of bile salts and pancreatic colipase and lipase onto digalactosyldiacylglycerol (DGDG) and dipalmitoylphosphatidylcholine (DPPC) monolayers at the air−water interface. The results from Langmuir trough and pendant drop experiments showed that a DGDG interface was more resistant to the adsorption of bile salts, colipase, and lipase compared to that of DPPC. Atomic force microscopy (AFM) images showed that the adsorption of bile salts into a DPPC monolayer decreased the size of the liquid condensed (LC) domains while there was no visible topographical change for DGDG systems. The results also showed that colipase and lipase adsorbed exclusively onto the mixed DPPC−bile salt regions and not the DPPC condensed phase. When the colipase and lipase were in excess, they fully covered the mixed DPPC−bile salt regions. However, the colipase and lipase coverage on the mixed DGDG−bile salt monolayer was incomplete and discontinuous. It was postulated that bile salts adsorbed into the DPPC monolayers filling the gaps between the lipid headgroups and spacing out the lipid molecules, making the lipid hydrocarbon tails more exposed to the surface. This created hydrophobic patches suitable for the binding of colipase and lipase. In contrast, bile salts adsorbed less easily into the DGDG monolayer because DGDG has a larger headgroup, which has strong intermolecular interactions and the ability to adopt different orientations at the interface. Thus, there are fewer hydrophobic patches that are of sufficient size to accommodate the colipase on the mixed DGDG−bile salt monolayer compared to the mixed DPPC−bile salt regions. The results from this work have reinforced the hypothesis that the interfacial molecular packing of lipids at the oil−water interface influences the adsorption of bile salts, colipase, and lipase, which in turn impacts the rate of lipolysis.
Original languageEnglish
Pages (from-to)9782-9793
Number of pages12
JournalLangmuir
Volume26
Issue number12
DOIs
Publication statusPublished - 2010

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Colipases
1,2-Dipalmitoylphosphatidylcholine
Lipases
Bile Acids and Salts
Lipase
Monolayers
Salts
salts
Adsorption
adsorption
Lipids
lipids
digalactosyldiacylglycerol
Hydrocarbons
Atomic force microscopy
troughs

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Chu, B-S., Gunning, A. P., Rich, G. T., Ridout, M. J., Faulks, R. M., Wickham, M. S. J., ... Wilde, P. J. (2010). Adsorption of bile salts and pancreatic colipase and lipase onto digalactosyldiacylglycerol and dipalmitoylphosphatidylcholine monolayers. Langmuir, 26(12), 9782-9793. https://doi.org/10.1021/la1000446
Chu, Boon-Seang ; Gunning, A. Patrick ; Rich, Gillian T. ; Ridout, Mike J. ; Faulks, Richard M. ; Wickham, Martin S. J. ; Morris, Victor J. ; Wilde, Peter J. / Adsorption of bile salts and pancreatic colipase and lipase onto digalactosyldiacylglycerol and dipalmitoylphosphatidylcholine monolayers. In: Langmuir. 2010 ; Vol. 26, No. 12. pp. 9782-9793.
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abstract = "It is increasingly recognized that changes in the composition of the oil−water interface can markedly affect pancreatic lipase adsorption and function. To understand interfacial mechanisms determining lipase activity, we investigated the adsorption behavior of bile salts and pancreatic colipase and lipase onto digalactosyldiacylglycerol (DGDG) and dipalmitoylphosphatidylcholine (DPPC) monolayers at the air−water interface. The results from Langmuir trough and pendant drop experiments showed that a DGDG interface was more resistant to the adsorption of bile salts, colipase, and lipase compared to that of DPPC. Atomic force microscopy (AFM) images showed that the adsorption of bile salts into a DPPC monolayer decreased the size of the liquid condensed (LC) domains while there was no visible topographical change for DGDG systems. The results also showed that colipase and lipase adsorbed exclusively onto the mixed DPPC−bile salt regions and not the DPPC condensed phase. When the colipase and lipase were in excess, they fully covered the mixed DPPC−bile salt regions. However, the colipase and lipase coverage on the mixed DGDG−bile salt monolayer was incomplete and discontinuous. It was postulated that bile salts adsorbed into the DPPC monolayers filling the gaps between the lipid headgroups and spacing out the lipid molecules, making the lipid hydrocarbon tails more exposed to the surface. This created hydrophobic patches suitable for the binding of colipase and lipase. In contrast, bile salts adsorbed less easily into the DGDG monolayer because DGDG has a larger headgroup, which has strong intermolecular interactions and the ability to adopt different orientations at the interface. Thus, there are fewer hydrophobic patches that are of sufficient size to accommodate the colipase on the mixed DGDG−bile salt monolayer compared to the mixed DPPC−bile salt regions. The results from this work have reinforced the hypothesis that the interfacial molecular packing of lipids at the oil−water interface influences the adsorption of bile salts, colipase, and lipase, which in turn impacts the rate of lipolysis.",
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Chu, B-S, Gunning, AP, Rich, GT, Ridout, MJ, Faulks, RM, Wickham, MSJ, Morris, VJ & Wilde, PJ 2010, 'Adsorption of bile salts and pancreatic colipase and lipase onto digalactosyldiacylglycerol and dipalmitoylphosphatidylcholine monolayers', Langmuir, vol. 26, no. 12, pp. 9782-9793. https://doi.org/10.1021/la1000446

Adsorption of bile salts and pancreatic colipase and lipase onto digalactosyldiacylglycerol and dipalmitoylphosphatidylcholine monolayers. / Chu, Boon-Seang; Gunning, A. Patrick; Rich, Gillian T.; Ridout, Mike J.; Faulks, Richard M.; Wickham, Martin S. J.; Morris, Victor J.; Wilde, Peter J.

In: Langmuir, Vol. 26, No. 12, 2010, p. 9782-9793.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Adsorption of bile salts and pancreatic colipase and lipase onto digalactosyldiacylglycerol and dipalmitoylphosphatidylcholine monolayers

AU - Chu, Boon-Seang

AU - Gunning, A. Patrick

AU - Rich, Gillian T.

AU - Ridout, Mike J.

AU - Faulks, Richard M.

AU - Wickham, Martin S. J.

AU - Morris, Victor J.

AU - Wilde, Peter J.

PY - 2010

Y1 - 2010

N2 - It is increasingly recognized that changes in the composition of the oil−water interface can markedly affect pancreatic lipase adsorption and function. To understand interfacial mechanisms determining lipase activity, we investigated the adsorption behavior of bile salts and pancreatic colipase and lipase onto digalactosyldiacylglycerol (DGDG) and dipalmitoylphosphatidylcholine (DPPC) monolayers at the air−water interface. The results from Langmuir trough and pendant drop experiments showed that a DGDG interface was more resistant to the adsorption of bile salts, colipase, and lipase compared to that of DPPC. Atomic force microscopy (AFM) images showed that the adsorption of bile salts into a DPPC monolayer decreased the size of the liquid condensed (LC) domains while there was no visible topographical change for DGDG systems. The results also showed that colipase and lipase adsorbed exclusively onto the mixed DPPC−bile salt regions and not the DPPC condensed phase. When the colipase and lipase were in excess, they fully covered the mixed DPPC−bile salt regions. However, the colipase and lipase coverage on the mixed DGDG−bile salt monolayer was incomplete and discontinuous. It was postulated that bile salts adsorbed into the DPPC monolayers filling the gaps between the lipid headgroups and spacing out the lipid molecules, making the lipid hydrocarbon tails more exposed to the surface. This created hydrophobic patches suitable for the binding of colipase and lipase. In contrast, bile salts adsorbed less easily into the DGDG monolayer because DGDG has a larger headgroup, which has strong intermolecular interactions and the ability to adopt different orientations at the interface. Thus, there are fewer hydrophobic patches that are of sufficient size to accommodate the colipase on the mixed DGDG−bile salt monolayer compared to the mixed DPPC−bile salt regions. The results from this work have reinforced the hypothesis that the interfacial molecular packing of lipids at the oil−water interface influences the adsorption of bile salts, colipase, and lipase, which in turn impacts the rate of lipolysis.

AB - It is increasingly recognized that changes in the composition of the oil−water interface can markedly affect pancreatic lipase adsorption and function. To understand interfacial mechanisms determining lipase activity, we investigated the adsorption behavior of bile salts and pancreatic colipase and lipase onto digalactosyldiacylglycerol (DGDG) and dipalmitoylphosphatidylcholine (DPPC) monolayers at the air−water interface. The results from Langmuir trough and pendant drop experiments showed that a DGDG interface was more resistant to the adsorption of bile salts, colipase, and lipase compared to that of DPPC. Atomic force microscopy (AFM) images showed that the adsorption of bile salts into a DPPC monolayer decreased the size of the liquid condensed (LC) domains while there was no visible topographical change for DGDG systems. The results also showed that colipase and lipase adsorbed exclusively onto the mixed DPPC−bile salt regions and not the DPPC condensed phase. When the colipase and lipase were in excess, they fully covered the mixed DPPC−bile salt regions. However, the colipase and lipase coverage on the mixed DGDG−bile salt monolayer was incomplete and discontinuous. It was postulated that bile salts adsorbed into the DPPC monolayers filling the gaps between the lipid headgroups and spacing out the lipid molecules, making the lipid hydrocarbon tails more exposed to the surface. This created hydrophobic patches suitable for the binding of colipase and lipase. In contrast, bile salts adsorbed less easily into the DGDG monolayer because DGDG has a larger headgroup, which has strong intermolecular interactions and the ability to adopt different orientations at the interface. Thus, there are fewer hydrophobic patches that are of sufficient size to accommodate the colipase on the mixed DGDG−bile salt monolayer compared to the mixed DPPC−bile salt regions. The results from this work have reinforced the hypothesis that the interfacial molecular packing of lipids at the oil−water interface influences the adsorption of bile salts, colipase, and lipase, which in turn impacts the rate of lipolysis.

U2 - 10.1021/la1000446

DO - 10.1021/la1000446

M3 - Article

VL - 26

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JO - Langmuir

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IS - 12

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