Melittin-induced cholesterol reorganization in lipid bilayer membranes

Qian, Shuo; Heller, William T.

doi:10.1016/j.bbamem.2015.06.012

Title: Melittin-induced cholesterol reorganization in lipid bilayer membranes

Journal Article · Thu Oct 01 00:00:00 EDT 2015 · Biochimica et Biophysica Acta. Biomembranes

DOI:https://doi.org/10.1016/j.bbamem.2015.06.012· OSTI ID:1328240

; Heller, William T.

The peptide melittin, a 26 amino acid, cationic peptide from honey bee (Apis mellifera) venom, disrupts lipid bilayer membranes in a concentration-dependent manner. Rather than interacting with a specific receptor, the peptide interacts directly with the lipid matrix of the membrane in a manner dependent on the lipid composition. Here, a small-angle neutron scattering study of the interaction of melittin with lipid bilayers made of mixtures of dimyristoylphosphatidylcholine (DMPC) and cholesterol (Chol) is presented. Through the use of deuterium-labeled DMPC, changes in the distribution of the lipid and cholesterol in unilamellar vesicles were observed for peptide concentrations below those that cause pores to form. In addition to disrupting the in-plane organization of Chol, melittin produces vesicles having inner and outer leaflet compositions that depend on the lipid–Chol molar ratio and on the peptide concentration. The changes seen at high cholesterol and low peptide concentration are similar to those produced by alamethicin (Qian, S. et al., J. Phys. Chem. B 2014, 118, 11200–11208), which points to an underlying physical mechanism driving the redistribution of Chol, but melittin displays an additional effect not seen with alamethicin. Furthermore, a model for how the peptide drives the redistribution of Chol is proposed. The results suggest that redistribution of the lipids in a target cell membrane by membrane active peptides takes places as a prelude to the lysis of the cell.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FWP ERKP291; AC05-00OR22725

OSTI ID:: 1328240

Alternate ID(s):: OSTI ID: 1195805; OSTI ID: 1249637

Journal Information:: Biochimica et Biophysica Acta. Biomembranes, Journal Name: Biochimica et Biophysica Acta. Biomembranes Vol. 1848 Journal Issue: 10 PA; ISSN 0005-2736

Publisher:: ElsevierCopyright Statement

Country of Publication:: Netherlands

Language:: English

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Cited by: 25 works

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References (53)

Mantid—Data analysis and visualization package for neutron scattering and $μ$ SR experiments Arnold, O.; Bilheux, J. C.; Borreguero, J. M. Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 764 https://doi.org/10.1016/j.nima.2014.07.029	journal	November 2014
The actions of melittin on membranes Dempsey, Christopher E. Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes, Vol. 1031, Issue 2 https://doi.org/10.1016/0304-4157(90)90006-X	journal	May 1990
Interaction of melittin with lipid membranes Ohki, Shinpei; Marcus, Emil; Sukumaran, Dinesh K. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1194, Issue 2 https://doi.org/10.1016/0005-2736(94)90303-4	journal	September 1994
Role of lipids in the interaction of antimicrobial peptides with membranes Teixeira, Vitor; Feio, Maria J.; Bastos, Margarida Progress in Lipid Research, Vol. 51, Issue 2 https://doi.org/10.1016/j.plipres.2011.12.005	journal	April 2012
Molecular details of melittin-induced lysis of phospholipid membranes as revealed by deuterium and phosphorus NMR Dufourc, Erick J.; Smith, Ian C. P.; Dufourcq, Jean Biochemistry, Vol. 25, Issue 21 https://doi.org/10.1021/bi00369a016	journal	October 1986
Melittin-induced leakage from phosphatidylcholine vesicles is modulated by cholesterol: a property used for membrane targeting Benachir, Toni; Monette, M.; Grenier, Julie European Biophysics Journal, Vol. 25, Issue 3 https://doi.org/10.1007/s002490050032	journal	January 1997
Melittin-Lipid Bilayer Interactions and the Role of Cholesterol Wessman, Per; Strömstedt, Adam A.; Malmsten, Martin Biophysical Journal, Vol. 95, Issue 9 https://doi.org/10.1529/biophysj.108.130559	journal	November 2008
Melittin: a Membrane-active Peptide with Diverse Functions Raghuraman, H.; Chattopadhyay, Amitabha Bioscience Reports, Vol. 27, Issue 4-5 https://doi.org/10.1007/s10540-006-9030-z	journal	August 2007
Thermomechanical and transition properties of dimyristoylphosphatidylcholine/cholesterol bilayers Needham, D.; McIntosh, T. J.; Evans, E. Biochemistry, Vol. 27, Issue 13 https://doi.org/10.1021/bi00413a013	journal	June 1988
Location of Cholesterol in DMPC Membranes. A Comparative Study by Neutron Diffraction and Molecular Mechanics Simulation ^† Léonard, Alain; Escrive, Céline; Laguerre, Michel Langmuir, Vol. 17, Issue 6 https://doi.org/10.1021/la001382p	journal	March 2001
Barrel-Stave Model or Toroidal Model? A Case Study on Melittin Pores Yang, Lin; Harroun, Thad A.; Weiss, Thomas M. Biophysical Journal, Vol. 81, Issue 3 https://doi.org/10.1016/S0006-3495(01)75802-X	journal	September 2001
Aggregation state of melittin in lipid vesicle membranes John, Edgar; Jähnig, Fritz Biophysical Journal, Vol. 60, Issue 2 https://doi.org/10.1016/S0006-3495(91)82056-2	journal	August 1991
ELLSTAT : shape modeling for solution small-angle scattering of proteins and protein complexes with automated statistical characterization Heller, William T. Journal of Applied Crystallography, Vol. 39, Issue 5 https://doi.org/10.1107/S0021889806029591	journal	September 2006
Peptide-Induced Asymmetric Distribution of Charged Lipids in a Vesicle Bilayer Revealed by Small-Angle Neutron Scattering Qian, Shuo; Heller, William T. The Journal of Physical Chemistry B, Vol. 115, Issue 32 https://doi.org/10.1021/jp204045t	journal	August 2011
Action of Antimicrobial Peptides: Two-State Model ^† Huang, Huey W. Biochemistry, Vol. 39, Issue 29 https://doi.org/10.1021/bi000946l	journal	July 2000
Mode of action of membrane active antimicrobial peptides Shai, Yechiel Biopolymers, Vol. 66, Issue 4 https://doi.org/10.1002/bip.10260	journal	January 2002
A deuterium and phosphorus-31 nuclear magnetic resonance study of the interaction of melittin with dimyristoylphosphatidylcholine bilayers and the effects of contaminating phospholipase A2 Dempsey, Christopher E.; Watts, Anthony Biochemistry, Vol. 26, Issue 18 https://doi.org/10.1021/bi00392a033	journal	September 1987
Effect of cholesterol on viscoelastic properties of dipalmitoylphosphatidylcholine multibilayers as measured by a laser-induced ultrasonic probe El-Sayed, M. Y.; Guion, T. A.; Fayer, M. D. Biochemistry, Vol. 25, Issue 17 https://doi.org/10.1021/bi00365a016	journal	August 1986
The extended Q -range small-angle neutron scattering diffractometer at the SNS Zhao, J. K.; Gao, C. Y.; Liu, D. Journal of Applied Crystallography, Vol. 43, Issue 5 https://doi.org/10.1107/S002188981002217X	journal	July 2010
ORNL_SAS : software for calculation of small-angle scattering intensities of proteins and protein complexes Tjioe, Elina; Heller, William T. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S002188980702420X	journal	July 2007
Structure and Functions of Channel-Forming Peptides: Magainins, Cecropins, Melittin and Alamethicin Bechinger, B. Journal of Membrane Biology, Vol. 156, Issue 3 https://doi.org/10.1007/s002329900201	journal	April 1997
Cholesterol Shows Preference for the Interior of Polyunsaturated Lipid Membranes Marrink, Siewert J.; de Vries, Alex H.; Harroun, Thad. A. Journal of the American Chemical Society, Vol. 130, Issue 1 https://doi.org/10.1021/ja076641c	journal	January 2008
The structure of melittin. II. Interpretation of the structure. Terwilliger, T. C.; Eisenberg, D. Journal of Biological Chemistry, Vol. 257, Issue 11 https://doi.org/10.1016/S0021-9258(20)65098-0	journal	June 1982
Circular dichroism of oriented α helices. I. Proof of the exciton theory Olah, Glenn A.; Huang, Huey W. The Journal of Chemical Physics, Vol. 89, Issue 4 https://doi.org/10.1063/1.455047	journal	August 1988
Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective Bloom, Myer; Evans, Evan; Mouritsen, Ole G. Quarterly Reviews of Biophysics, Vol. 24, Issue 3 https://doi.org/10.1017/S0033583500003735	journal	August 1991
Alamethicin Disrupts the Cholesterol Distribution in Dimyristoyl Phosphatidylcholine–Cholesterol Lipid Bilayers Qian, Shuo; Rai, Durgesh; Heller, William T. The Journal of Physical Chemistry B, Vol. 118, Issue 38 https://doi.org/10.1021/jp504886u	journal	September 2014
Effect of cholesterol on the structure of a phospholipid bilayer de Meyer, F.; Smit, B. Proceedings of the National Academy of Sciences, Vol. 106, Issue 10 https://doi.org/10.1073/pnas.0809959106	journal	February 2009
Mechanisms of membrane fusion: disparate players and common principles Martens, Sascha; McMahon, Harvey T. Nature Reviews Molecular Cell Biology, Vol. 9, Issue 7 https://doi.org/10.1038/nrm2417	journal	May 2008
Liquid-ordered phases induced by cholesterol: A compendium of binary phase diagrams Marsh, Derek Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1798, Issue 3 https://doi.org/10.1016/j.bbamem.2009.12.027	journal	March 2010
Effect of cholesterol on the polymorphism of dipalmitoylphosphatidylcholine/melittin complexes: an NMR study Monette, Martine; Van Calsteren, Marie-Rose; Lafleur, Michel Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1149, Issue 2 https://doi.org/10.1016/0005-2736(93)90217-N	journal	July 1993
Action of melittin on the DPPC-cholesterol liquid-ordered phase: a solid state 2H-and 31P-NMR study Pott, T.; Dufourc, E. J. Biophysical Journal, Vol. 68, Issue 3 https://doi.org/10.1016/S0006-3495(95)80272-9	journal	March 1995
Method of oriented circular dichroism Wu, Y.; Huang, H. W.; Olah, G. A. Biophysical Journal, Vol. 57, Issue 4 https://doi.org/10.1016/S0006-3495(90)82599-6	journal	April 1990
Three-Dimensional Structure of Membrane and Surface Proteins Eisenberg, D. Annual Review of Biochemistry, Vol. 53, Issue 1 https://doi.org/10.1146/annurev.bi.53.070184.003115	journal	June 1984
Effect of changing the size of lipid headgroup on peptide insertion into membranes Heller, W. T.; He, K.; Ludtke, S. J. Biophysical Journal, Vol. 73, Issue 1 https://doi.org/10.1016/S0006-3495(97)78064-0	journal	July 1997
Reversible disc-micellization of dimyristoylphosphatidylcholine bilayers induced by melittin and [Ala-14]melittin Dempsey, Christopher E.; Sternberg, Brigitte Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1061, Issue 2 https://doi.org/10.1016/0005-2736(91)90283-E	journal	January 1991
Antibacterial peptides: basic facts and emerging concepts Boman, H. G. Journal of Internal Medicine, Vol. 254, Issue 3 https://doi.org/10.1046/j.1365-2796.2003.01228.x	journal	September 2003
Mechanism of alamethicin insertion into lipid bilayers He, K.; Ludtke, S. J.; Heller, W. T. Biophysical Journal, Vol. 71, Issue 5 https://doi.org/10.1016/S0006-3495(96)79458-4	journal	November 1996
Molecular Simulation of the DMPC-Cholesterol Phase Diagram de Meyer, Frédérick J. -M.; Benjamini, Ayelet; Rodgers, Jocelyn M. The Journal of Physical Chemistry B, Vol. 114, Issue 32 https://doi.org/10.1021/jp103903s	journal	August 2010
The structure of melittin in the form I crystals and its implication for melittin's lytic and surface activities Terwilliger, T. C.; Weissman, L.; Eisenberg, D. Biophysical Journal, Vol. 37, Issue 1 https://doi.org/10.1016/S0006-3495(82)84683-3	journal	January 1982
Humidity fixed points of binary saturated aqueous solutions Greenspan, Lewis Journal of Research of the National Bureau of Standards Section A: Physics and Chemistry, Vol. 81A, Issue 1 https://doi.org/10.6028/jres.081A.011	journal	January 1977
Amphipathic, α-helical antimicrobial peptides Tossi, Alessandro; Sandri, Luca; Giangaspero, Anna Biopolymers, Vol. 55, Issue 1 https://doi.org/10.1002/1097-0282(2000)55:1<4::AID-BIP30>3.0.CO;2-M	journal	January 2000
Structure of the Alamethicin Pore Reconstructed by X-Ray Diffraction Analysis Qian, Shuo; Wang, Wangchen; Yang, Lin Biophysical Journal, Vol. 94, Issue 9 https://doi.org/10.1529/biophysj.107.126474	journal	May 2008
The Bio-SANS instrument at the High Flux Isotope Reactor of Oak Ridge National Laboratory Heller, William T.; Urban, Volker S.; Lynn, Gary W. Journal of Applied Crystallography, Vol. 47, Issue 4 https://doi.org/10.1107/S1600576714011285	journal	June 2014
The structure of melittin. I. Structure determination and partial refinement. Terwilliger, T. C.; Eisenberg, D. Journal of Biological Chemistry, Vol. 257, Issue 11 https://doi.org/10.1016/S0021-9258(20)65097-9	journal	June 1982
Evidence for Membrane Thinning Effect as the Mechanism for Peptide-Induced Pore Formation Chen, Fang-Yu; Lee, Ming-Tao; Huang, Huey W. Biophysical Journal, Vol. 84, Issue 6 https://doi.org/10.1016/S0006-3495(03)75103-0	journal	June 2003
Dynamical order and disorder in lipid bilayers Mouritsen, Ole G.; Jørgensen, Kent Chemistry and Physics of Lipids, Vol. 73, Issue 1-2 https://doi.org/10.1016/0009-3084(94)90171-6	journal	September 1994
Membrane Thinning Effect of the β-Sheet Antimicrobial Protegrin ^† Heller, William T.; Waring, Alan J.; Lehrer, Robert I. Biochemistry, Vol. 39, Issue 1 https://doi.org/10.1021/bi991892m	journal	January 2000
Interaction of Melittin with Membrane Cholesterol: A Fluorescence Approach Raghuraman, H.; Chattopadhyay, Amitabha Biophysical Journal, Vol. 87, Issue 4 https://doi.org/10.1529/biophysj.104.043596	journal	October 2004
The secondary structure of bacteriorhodopsin determined by Raman and circular dichroism spectroscopy. Vogel, H.; Gärtner, W. Journal of Biological Chemistry, Vol. 262, Issue 24 https://doi.org/10.1016/S0021-9258(18)60829-4	journal	August 1987
The Condensing Effect of Cholesterol in Lipid Bilayers Hung, Wei-Chin; Lee, Ming-Tao; Chen, Fang-Yu Biophysical Journal, Vol. 92, Issue 11 https://doi.org/10.1529/biophysj.106.099234	journal	June 2007
The structure of melittin in lipid bilayer membranes Drake, A. F.; Hider, R. C. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 555, Issue 2 https://doi.org/10.1016/0005-2736(79)90178-0	journal	August 1979
Cholesterol Is Found To Reside in the Center of a Polyunsaturated Lipid Membrane Harroun, Thad A.; Katsaras, John; Wassall, Stephen R. Biochemistry, Vol. 47, Issue 27 https://doi.org/10.1021/bi800123b	journal	July 2008
Small-angle neutron scattering and contrast variation: a powerful combination for studying biological structures Heller, William T. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 11 https://doi.org/10.1107/S0907444910017658	journal	October 2010

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59 BASIC BIOLOGICAL SCIENCES
membrane active peptides
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small-angle neutron scattering
melittin
cholesterol

Title: Melittin-induced cholesterol reorganization in lipid bilayer membranes

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