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

Abstract

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 resultsmore »« less

Authors:

; Heller, William T.

Publication Date:: Thu Oct 01 00:00:00 EDT 2015

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

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

OSTI Identifier:: 1328240

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

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

Resource Type:: Published Article

Journal Name:: Biochimica et Biophysica Acta. Biomembranes

Additional Journal Information:: Journal Name: Biochimica et Biophysica Acta. Biomembranes Journal Volume: 1848 Journal Issue: 10 PA; Journal ID: ISSN 0005-2736

Publisher:: Elsevier

Country of Publication:: Netherlands

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; membrane active peptides; lipid bilayers; small-angle neutron scattering; melittin; cholesterol

Citation Formats


                    Qian, Shuo, and Heller, William T. Melittin-induced cholesterol reorganization in lipid bilayer membranes.  Netherlands: N. p., 2015. 
Web.  doi:10.1016/j.bbamem.2015.06.012.

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                    Qian, Shuo, & Heller, William T. Melittin-induced cholesterol reorganization in lipid bilayer membranes.  Netherlands.  https://doi.org/10.1016/j.bbamem.2015.06.012

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                    Qian, Shuo, and Heller, William T. Thu .  
"Melittin-induced cholesterol reorganization in lipid bilayer membranes".  Netherlands.  https://doi.org/10.1016/j.bbamem.2015.06.012.

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@article{osti_1328240,

  title        = {Melittin-induced cholesterol reorganization in lipid bilayer membranes},

  author       = {Qian, Shuo and Heller, William T.},

  abstractNote = {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.},

  doi          = {10.1016/j.bbamem.2015.06.012},

  journal      = {Biochimica et Biophysica Acta. Biomembranes},

  number       = 10 PA,

  volume       = 1848,

  place        = {Netherlands},

  year         = {Thu Oct 01 00:00:00 EDT 2015},

  month        = {Thu Oct 01 00:00:00 EDT 2015}

}

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Title: Melittin-induced cholesterol reorganization in lipid bilayer membranes

Abstract

Citation Formats

Mantid—Data analysis and visualization package for neutron scattering and μ SR experiments journal, November 2014

The actions of melittin on membranes journal, May 1990

Interaction of melittin with lipid membranes journal, September 1994

Role of lipids in the interaction of antimicrobial peptides with membranes journal, April 2012

Molecular details of melittin-induced lysis of phospholipid membranes as revealed by deuterium and phosphorus NMR journal, October 1986

Melittin-induced leakage from phosphatidylcholine vesicles is modulated by cholesterol: a property used for membrane targeting journal, January 1997

Melittin-Lipid Bilayer Interactions and the Role of Cholesterol journal, November 2008

Melittin: a Membrane-active Peptide with Diverse Functions journal, August 2007

Thermomechanical and transition properties of dimyristoylphosphatidylcholine/cholesterol bilayers journal, June 1988

Location of Cholesterol in DMPC Membranes. A Comparative Study by Neutron Diffraction and Molecular Mechanics Simulation † journal, March 2001

Barrel-Stave Model or Toroidal Model? A Case Study on Melittin Pores journal, September 2001

Aggregation state of melittin in lipid vesicle membranes journal, August 1991

ELLSTAT : shape modeling for solution small-angle scattering of proteins and protein complexes with automated statistical characterization journal, September 2006

Peptide-Induced Asymmetric Distribution of Charged Lipids in a Vesicle Bilayer Revealed by Small-Angle Neutron Scattering journal, August 2011

Action of Antimicrobial Peptides: Two-State Model † journal, July 2000

Mode of action of membrane active antimicrobial peptides 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 journal, September 1987

Effect of cholesterol on viscoelastic properties of dipalmitoylphosphatidylcholine multibilayers as measured by a laser-induced ultrasonic probe journal, August 1986

The extended Q -range small-angle neutron scattering diffractometer at the SNS journal, July 2010

ORNL_SAS : software for calculation of small-angle scattering intensities of proteins and protein complexes journal, July 2007

Structure and Functions of Channel-Forming Peptides: Magainins, Cecropins, Melittin and Alamethicin journal, April 1997

Cholesterol Shows Preference for the Interior of Polyunsaturated Lipid Membranes journal, January 2008

The structure of melittin. II. Interpretation of the structure. journal, June 1982

Circular dichroism of oriented α helices. I. Proof of the exciton theory journal, August 1988

Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective journal, August 1991

Alamethicin Disrupts the Cholesterol Distribution in Dimyristoyl Phosphatidylcholine–Cholesterol Lipid Bilayers journal, September 2014

Effect of cholesterol on the structure of a phospholipid bilayer journal, February 2009

Mechanisms of membrane fusion: disparate players and common principles journal, May 2008

Liquid-ordered phases induced by cholesterol: A compendium of binary phase diagrams journal, March 2010

Effect of cholesterol on the polymorphism of dipalmitoylphosphatidylcholine/melittin complexes: an NMR study journal, July 1993

Action of melittin on the DPPC-cholesterol liquid-ordered phase: a solid state 2H-and 31P-NMR study journal, March 1995

Method of oriented circular dichroism journal, April 1990

Three-Dimensional Structure of Membrane and Surface Proteins journal, June 1984

Effect of changing the size of lipid headgroup on peptide insertion into membranes journal, July 1997

Reversible disc-micellization of dimyristoylphosphatidylcholine bilayers induced by melittin and [Ala-14]melittin journal, January 1991

Antibacterial peptides: basic facts and emerging concepts journal, September 2003

Mechanism of alamethicin insertion into lipid bilayers journal, November 1996

Molecular Simulation of the DMPC-Cholesterol Phase Diagram journal, August 2010

The structure of melittin in the form I crystals and its implication for melittin's lytic and surface activities journal, January 1982

Humidity fixed points of binary saturated aqueous solutions journal, January 1977

Amphipathic, α-helical antimicrobial peptides journal, January 2000

Structure of the Alamethicin Pore Reconstructed by X-Ray Diffraction Analysis journal, May 2008

The Bio-SANS instrument at the High Flux Isotope Reactor of Oak Ridge National Laboratory journal, June 2014

The structure of melittin. I. Structure determination and partial refinement. journal, June 1982

Evidence for Membrane Thinning Effect as the Mechanism for Peptide-Induced Pore Formation journal, June 2003

Dynamical order and disorder in lipid bilayers journal, September 1994

Membrane Thinning Effect of the β-Sheet Antimicrobial Protegrin † journal, January 2000

Interaction of Melittin with Membrane Cholesterol: A Fluorescence Approach journal, October 2004

The secondary structure of bacteriorhodopsin determined by Raman and circular dichroism spectroscopy. journal, August 1987

The Condensing Effect of Cholesterol in Lipid Bilayers journal, June 2007

The structure of melittin in lipid bilayer membranes journal, August 1979

Cholesterol Is Found To Reside in the Center of a Polyunsaturated Lipid Membrane journal, July 2008

Small-angle neutron scattering and contrast variation: a powerful combination for studying biological structures journal, October 2010

Mantid—Data analysis and visualization package for neutron scattering and $μ$ SR experiments
journal, November 2014

The actions of melittin on membranes
journal, May 1990

Interaction of melittin with lipid membranes
journal, September 1994

Role of lipids in the interaction of antimicrobial peptides with membranes
journal, April 2012

Molecular details of melittin-induced lysis of phospholipid membranes as revealed by deuterium and phosphorus NMR
journal, October 1986

Melittin-induced leakage from phosphatidylcholine vesicles is modulated by cholesterol: a property used for membrane targeting
journal, January 1997

Melittin-Lipid Bilayer Interactions and the Role of Cholesterol
journal, November 2008

Melittin: a Membrane-active Peptide with Diverse Functions
journal, August 2007

Thermomechanical and transition properties of dimyristoylphosphatidylcholine/cholesterol bilayers
journal, June 1988

Location of Cholesterol in DMPC Membranes. A Comparative Study by Neutron Diffraction and Molecular Mechanics Simulation ^†
journal, March 2001

Barrel-Stave Model or Toroidal Model? A Case Study on Melittin Pores
journal, September 2001

Aggregation state of melittin in lipid vesicle membranes
journal, August 1991

ELLSTAT : shape modeling for solution small-angle scattering of proteins and protein complexes with automated statistical characterization
journal, September 2006

Peptide-Induced Asymmetric Distribution of Charged Lipids in a Vesicle Bilayer Revealed by Small-Angle Neutron Scattering
journal, August 2011

Action of Antimicrobial Peptides: Two-State Model ^†
journal, July 2000

Mode of action of membrane active antimicrobial peptides
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
journal, September 1987

Effect of cholesterol on viscoelastic properties of dipalmitoylphosphatidylcholine multibilayers as measured by a laser-induced ultrasonic probe
journal, August 1986

The extended Q -range small-angle neutron scattering diffractometer at the SNS
journal, July 2010

ORNL_SAS : software for calculation of small-angle scattering intensities of proteins and protein complexes
journal, July 2007

Structure and Functions of Channel-Forming Peptides: Magainins, Cecropins, Melittin and Alamethicin
journal, April 1997

Cholesterol Shows Preference for the Interior of Polyunsaturated Lipid Membranes
journal, January 2008

The structure of melittin. II. Interpretation of the structure.
journal, June 1982

Circular dichroism of oriented α helices. I. Proof of the exciton theory
journal, August 1988

Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective
journal, August 1991

Alamethicin Disrupts the Cholesterol Distribution in Dimyristoyl Phosphatidylcholine–Cholesterol Lipid Bilayers
journal, September 2014

Effect of cholesterol on the structure of a phospholipid bilayer
journal, February 2009

Mechanisms of membrane fusion: disparate players and common principles
journal, May 2008

Liquid-ordered phases induced by cholesterol: A compendium of binary phase diagrams
journal, March 2010

Effect of cholesterol on the polymorphism of dipalmitoylphosphatidylcholine/melittin complexes: an NMR study
journal, July 1993

Action of melittin on the DPPC-cholesterol liquid-ordered phase: a solid state 2H-and 31P-NMR study
journal, March 1995

Method of oriented circular dichroism
journal, April 1990

Three-Dimensional Structure of Membrane and Surface Proteins
journal, June 1984

Effect of changing the size of lipid headgroup on peptide insertion into membranes
journal, July 1997

Reversible disc-micellization of dimyristoylphosphatidylcholine bilayers induced by melittin and [Ala-14]melittin
journal, January 1991

Antibacterial peptides: basic facts and emerging concepts
journal, September 2003

Mechanism of alamethicin insertion into lipid bilayers
journal, November 1996

Molecular Simulation of the DMPC-Cholesterol Phase Diagram
journal, August 2010

The structure of melittin in the form I crystals and its implication for melittin's lytic and surface activities
journal, January 1982

Humidity fixed points of binary saturated aqueous solutions
journal, January 1977

Amphipathic, α-helical antimicrobial peptides
journal, January 2000

Structure of the Alamethicin Pore Reconstructed by X-Ray Diffraction Analysis
journal, May 2008

The Bio-SANS instrument at the High Flux Isotope Reactor of Oak Ridge National Laboratory
journal, June 2014

The structure of melittin. I. Structure determination and partial refinement.
journal, June 1982

Evidence for Membrane Thinning Effect as the Mechanism for Peptide-Induced Pore Formation
journal, June 2003

Dynamical order and disorder in lipid bilayers
journal, September 1994

Membrane Thinning Effect of the β-Sheet Antimicrobial Protegrin ^†
journal, January 2000

Interaction of Melittin with Membrane Cholesterol: A Fluorescence Approach
journal, October 2004

The secondary structure of bacteriorhodopsin determined by Raman and circular dichroism spectroscopy.
journal, August 1987

The Condensing Effect of Cholesterol in Lipid Bilayers
journal, June 2007

The structure of melittin in lipid bilayer membranes
journal, August 1979

Cholesterol Is Found To Reside in the Center of a Polyunsaturated Lipid Membrane
journal, July 2008

Small-angle neutron scattering and contrast variation: a powerful combination for studying biological structures
journal, October 2010