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Sensitivity of single membrane-spanning alpha-helical peptides to hydrophobic mismatch with a lipid bilayer: Effects on backbone structure, orientation, and extent of membrane incorporation

Sensitivity of single membrane-spanning alpha-helical peptides to hydrophobic mismatch with a lipid bilayer: Effects on backbone structure, orientation, and extent of membrane incorporation
Sensitivity of single membrane-spanning alpha-helical peptides to hydrophobic mismatch with a lipid bilayer: Effects on backbone structure, orientation, and extent of membrane incorporation
The extent of matching of membrane hydrophobic thickness with the hydrophobic length of transmembrane protein segments potentially constitutes a major director of membrane organization. Therefore, the extent of mismatch that can be compensated, and the types of membrane rearrangements that result, can provide valuable insight into membrane functionality. In the present study, a large family of synthetic peptides and lipids is used to investigate a range of mismatch situations. Peptide conformation, orientation, and extent of incorporation are assessed by infrared spectroscopy, tryptophan fluorescence, circular dichroism, and sucrose gradient centrifugation. It is shown that peptide backbone structure is not significantly affected by mismatch, even when the extent of mismatch is large. Instead, this study demonstrates that for tryptophan-flanked peptides the dominant response of a membrane to large mismatch is that the extent of incorporation is reduced, when the peptide is both too short and too long. With increasing mismatch, a smaller fraction of peptide is incorporated into the lipid bilayer, and a larger fraction is present in extramembranous aggregates. Relatively long peptides that remain incorporated in the bilayer have a small tilt angle with respect to the membrane normal. The observed effects depend on the nature of the flanking residues: long tryptophan-flanked peptides do not associate well with thin bilayers, while equisized lysine-flanked peptides associate completely, thus supporting the notion that tryptophan and lysine interact differently with membrane-water interfaces. The different properties that aromatic and charged flanking residues impart on transmembrane protein segments are discussed in relation to protein incorporation in biological systems.
0006-2960
5000-5010
de Planque, M.R.R.
a1d33d13-f516-44fb-8d2c-c51d18bc21ba
Goormaghtigh, E.
e5e7c35a-3a13-465f-ae3c-3aee5c2d2514
Greathouse, D.V.
d3a9f257-6d8b-418c-8ed0-29c18432c1ca
Koeppe II, R.E.
172c9a8d-70ca-4539-b677-fbe4456bf82e
Kruijtzer, J.A.W.
18bdd913-8d9a-4de4-b98b-3f91c2b357ba
Liskamp, R.M.J.
c101a850-1064-404b-ae73-8d0d31cd079d
de Kruijff, B.
c6a1a2d0-ec5d-4210-bd08-6d3afad45734
Killian, J.A.
86f7f502-8cbf-4950-bcad-153f5745aa66
de Planque, M.R.R.
a1d33d13-f516-44fb-8d2c-c51d18bc21ba
Goormaghtigh, E.
e5e7c35a-3a13-465f-ae3c-3aee5c2d2514
Greathouse, D.V.
d3a9f257-6d8b-418c-8ed0-29c18432c1ca
Koeppe II, R.E.
172c9a8d-70ca-4539-b677-fbe4456bf82e
Kruijtzer, J.A.W.
18bdd913-8d9a-4de4-b98b-3f91c2b357ba
Liskamp, R.M.J.
c101a850-1064-404b-ae73-8d0d31cd079d
de Kruijff, B.
c6a1a2d0-ec5d-4210-bd08-6d3afad45734
Killian, J.A.
86f7f502-8cbf-4950-bcad-153f5745aa66

de Planque, M.R.R., Goormaghtigh, E., Greathouse, D.V., Koeppe II, R.E., Kruijtzer, J.A.W., Liskamp, R.M.J., de Kruijff, B. and Killian, J.A. (2001) Sensitivity of single membrane-spanning alpha-helical peptides to hydrophobic mismatch with a lipid bilayer: Effects on backbone structure, orientation, and extent of membrane incorporation. Biochemistry, 40 (16), 5000-5010. (doi:10.1021/bi000804r).

Record type: Article

Abstract

The extent of matching of membrane hydrophobic thickness with the hydrophobic length of transmembrane protein segments potentially constitutes a major director of membrane organization. Therefore, the extent of mismatch that can be compensated, and the types of membrane rearrangements that result, can provide valuable insight into membrane functionality. In the present study, a large family of synthetic peptides and lipids is used to investigate a range of mismatch situations. Peptide conformation, orientation, and extent of incorporation are assessed by infrared spectroscopy, tryptophan fluorescence, circular dichroism, and sucrose gradient centrifugation. It is shown that peptide backbone structure is not significantly affected by mismatch, even when the extent of mismatch is large. Instead, this study demonstrates that for tryptophan-flanked peptides the dominant response of a membrane to large mismatch is that the extent of incorporation is reduced, when the peptide is both too short and too long. With increasing mismatch, a smaller fraction of peptide is incorporated into the lipid bilayer, and a larger fraction is present in extramembranous aggregates. Relatively long peptides that remain incorporated in the bilayer have a small tilt angle with respect to the membrane normal. The observed effects depend on the nature of the flanking residues: long tryptophan-flanked peptides do not associate well with thin bilayers, while equisized lysine-flanked peptides associate completely, thus supporting the notion that tryptophan and lysine interact differently with membrane-water interfaces. The different properties that aromatic and charged flanking residues impart on transmembrane protein segments are discussed in relation to protein incorporation in biological systems.

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Published date: 24 April 2001

Identifiers

Local EPrints ID: 48608
URI: http://eprints.soton.ac.uk/id/eprint/48608
ISSN: 0006-2960
PURE UUID: 6c014bf2-73a0-48fd-ae5b-d4611a1c2f78
ORCID for M.R.R. de Planque: ORCID iD orcid.org/0000-0002-8787-0513

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Date deposited: 03 Oct 2007
Last modified: 15 Mar 2024 09:48

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Contributors

Author: M.R.R. de Planque ORCID iD
Author: E. Goormaghtigh
Author: D.V. Greathouse
Author: R.E. Koeppe II
Author: J.A.W. Kruijtzer
Author: R.M.J. Liskamp
Author: B. de Kruijff
Author: J.A. Killian

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