Lipid unsaturation determines the interaction of AFP type I with model membranes during thermotropic phase transitions

Melanie M. Tomczak, L. Vígh, Jeffrey D. Meyer, Mark C. Manning, Dirk K. Hincha, John H. Crowe

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

We have previously shown that antifreeze protein (AFP) type I from winter flounder interacts with the acyl chains of lipids in model membranes containing a mixture of dimyristoylphosphatidylcholine (DMPC) and the plant thylakoid lipid digalactosyldiacylglycerol (DGDG), most likely through hydrophobic interactions. By contrast, in studies with pure phospholipid membranes, no such interaction was seen. DGDG is a highly unsaturated lipid, which renders these studies quite different from the previous studies of AFP-membrane interaction where the lipids were saturated or tranx-unsaturated. Therefore, it seemed possible that either the digalactose headgroups or the unsaturated DGDG acyl chains, or both, may be important for interactions of membranes with AFP type I. To distinguish between these possibilities, we catalytically hydrogenated the DGDG to obtain a galactolipid with completely saturated fatty acyl chains. The results with the hydrogenated DGDG were strikingly different from those obtained previously with the unsaturated DGDG; the clear binding of AFPs to the bilayer appeared to be lost. Nevertheless, the temperature-dependent folding of AFP type I was inhibited in the presence of liposomes containing either the unsaturated or the hydrogenated DGDG. The results indicate that the liposomes and protein still interact, even following hydrogenation of the acyl chains, perhaps at the membrane-solution interface.

Original languageEnglish
Pages (from-to)135-142
Number of pages8
JournalCryobiology
Volume45
Issue number2
DOIs
Publication statusPublished - Oct 2002

Fingerprint

Type I Antifreeze Proteins
Phase Transition
phase transition
Phase transitions
Membranes
Lipids
lipid bodies
lipids
galactolipids
Pseudopleuronectes americanus
hydrogenation
hydrophobic bonding
Liposomes
thylakoids
Galactolipids
Antifreeze Proteins
phospholipids
Dimyristoylphosphatidylcholine
Flounder
Thylakoids

Keywords

  • AFP type I
  • DGDG
  • Lipid phase transitions
  • Protein-lipid interactions
  • Temperature-dependent protein folding

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)

Cite this

Lipid unsaturation determines the interaction of AFP type I with model membranes during thermotropic phase transitions. / Tomczak, Melanie M.; Vígh, L.; Meyer, Jeffrey D.; Manning, Mark C.; Hincha, Dirk K.; Crowe, John H.

In: Cryobiology, Vol. 45, No. 2, 10.2002, p. 135-142.

Research output: Contribution to journalArticle

Tomczak, Melanie M. ; Vígh, L. ; Meyer, Jeffrey D. ; Manning, Mark C. ; Hincha, Dirk K. ; Crowe, John H. / Lipid unsaturation determines the interaction of AFP type I with model membranes during thermotropic phase transitions. In: Cryobiology. 2002 ; Vol. 45, No. 2. pp. 135-142.
@article{6921b654e1dd443a9b912b604c484233,
title = "Lipid unsaturation determines the interaction of AFP type I with model membranes during thermotropic phase transitions",
abstract = "We have previously shown that antifreeze protein (AFP) type I from winter flounder interacts with the acyl chains of lipids in model membranes containing a mixture of dimyristoylphosphatidylcholine (DMPC) and the plant thylakoid lipid digalactosyldiacylglycerol (DGDG), most likely through hydrophobic interactions. By contrast, in studies with pure phospholipid membranes, no such interaction was seen. DGDG is a highly unsaturated lipid, which renders these studies quite different from the previous studies of AFP-membrane interaction where the lipids were saturated or tranx-unsaturated. Therefore, it seemed possible that either the digalactose headgroups or the unsaturated DGDG acyl chains, or both, may be important for interactions of membranes with AFP type I. To distinguish between these possibilities, we catalytically hydrogenated the DGDG to obtain a galactolipid with completely saturated fatty acyl chains. The results with the hydrogenated DGDG were strikingly different from those obtained previously with the unsaturated DGDG; the clear binding of AFPs to the bilayer appeared to be lost. Nevertheless, the temperature-dependent folding of AFP type I was inhibited in the presence of liposomes containing either the unsaturated or the hydrogenated DGDG. The results indicate that the liposomes and protein still interact, even following hydrogenation of the acyl chains, perhaps at the membrane-solution interface.",
keywords = "AFP type I, DGDG, Lipid phase transitions, Protein-lipid interactions, Temperature-dependent protein folding",
author = "Tomczak, {Melanie M.} and L. V{\'i}gh and Meyer, {Jeffrey D.} and Manning, {Mark C.} and Hincha, {Dirk K.} and Crowe, {John H.}",
year = "2002",
month = "10",
doi = "10.1016/S0011-2240(02)00122-0",
language = "English",
volume = "45",
pages = "135--142",
journal = "Cryobiology",
issn = "0011-2240",
publisher = "Academic Press Inc.",
number = "2",

}

TY - JOUR

T1 - Lipid unsaturation determines the interaction of AFP type I with model membranes during thermotropic phase transitions

AU - Tomczak, Melanie M.

AU - Vígh, L.

AU - Meyer, Jeffrey D.

AU - Manning, Mark C.

AU - Hincha, Dirk K.

AU - Crowe, John H.

PY - 2002/10

Y1 - 2002/10

N2 - We have previously shown that antifreeze protein (AFP) type I from winter flounder interacts with the acyl chains of lipids in model membranes containing a mixture of dimyristoylphosphatidylcholine (DMPC) and the plant thylakoid lipid digalactosyldiacylglycerol (DGDG), most likely through hydrophobic interactions. By contrast, in studies with pure phospholipid membranes, no such interaction was seen. DGDG is a highly unsaturated lipid, which renders these studies quite different from the previous studies of AFP-membrane interaction where the lipids were saturated or tranx-unsaturated. Therefore, it seemed possible that either the digalactose headgroups or the unsaturated DGDG acyl chains, or both, may be important for interactions of membranes with AFP type I. To distinguish between these possibilities, we catalytically hydrogenated the DGDG to obtain a galactolipid with completely saturated fatty acyl chains. The results with the hydrogenated DGDG were strikingly different from those obtained previously with the unsaturated DGDG; the clear binding of AFPs to the bilayer appeared to be lost. Nevertheless, the temperature-dependent folding of AFP type I was inhibited in the presence of liposomes containing either the unsaturated or the hydrogenated DGDG. The results indicate that the liposomes and protein still interact, even following hydrogenation of the acyl chains, perhaps at the membrane-solution interface.

AB - We have previously shown that antifreeze protein (AFP) type I from winter flounder interacts with the acyl chains of lipids in model membranes containing a mixture of dimyristoylphosphatidylcholine (DMPC) and the plant thylakoid lipid digalactosyldiacylglycerol (DGDG), most likely through hydrophobic interactions. By contrast, in studies with pure phospholipid membranes, no such interaction was seen. DGDG is a highly unsaturated lipid, which renders these studies quite different from the previous studies of AFP-membrane interaction where the lipids were saturated or tranx-unsaturated. Therefore, it seemed possible that either the digalactose headgroups or the unsaturated DGDG acyl chains, or both, may be important for interactions of membranes with AFP type I. To distinguish between these possibilities, we catalytically hydrogenated the DGDG to obtain a galactolipid with completely saturated fatty acyl chains. The results with the hydrogenated DGDG were strikingly different from those obtained previously with the unsaturated DGDG; the clear binding of AFPs to the bilayer appeared to be lost. Nevertheless, the temperature-dependent folding of AFP type I was inhibited in the presence of liposomes containing either the unsaturated or the hydrogenated DGDG. The results indicate that the liposomes and protein still interact, even following hydrogenation of the acyl chains, perhaps at the membrane-solution interface.

KW - AFP type I

KW - DGDG

KW - Lipid phase transitions

KW - Protein-lipid interactions

KW - Temperature-dependent protein folding

UR - http://www.scopus.com/inward/record.url?scp=12244304185&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=12244304185&partnerID=8YFLogxK

U2 - 10.1016/S0011-2240(02)00122-0

DO - 10.1016/S0011-2240(02)00122-0

M3 - Article

VL - 45

SP - 135

EP - 142

JO - Cryobiology

JF - Cryobiology

SN - 0011-2240

IS - 2

ER -