The Interaction of Melittin with Dimyristoyl Phosphatidylcholine-Dimyristoyl Phosphatidylserine Lipid Bilayer Membranes

Rai, Durgesh K.; Qian, Shuo; Heller, William T.

doi:10.1016/j.bbamem.2016.08.006

Title: The Interaction of Melittin with Dimyristoyl Phosphatidylcholine-Dimyristoyl Phosphatidylserine Lipid Bilayer Membranes

Abstract

We report that membrane-active peptides (MAPs), which interact directly with the lipid bilayer of a cell and include toxins and host defense peptides, display lipid composition-dependent activity. Phosphatidylserine (PS) lipids are anionic lipids that are found throughout the cellular membranes of most eukaryotic organisms where they serve as both a functional component and as a precursor to phosphatidylethanolamine lipids. The inner leaflet of the plasma membrane contains more PS than the outer one, and the asymmetry is actively maintained. Here, the impact of the MAP melittin on the structure of lipid bilayer vesicles made of a mixture of phosphatidylcholine and phosphatidylserine was studied. Small-angle neutron scattering of the MAP associated with selectively deuterium-labeled lipid bilayer vesicles revealed how the thickness and lipid composition of phosphatidylserine-containing vesicles change in response to melittin. The peptide thickens the lipid bilayer for concentrations up to P/L = 1/500, but membrane thinning results when P/L = 1/200. The thickness transition is accompanied by a large change in the distribution of DMPS between the leaflets of the bilayer. The change in composition is driven by electrostatic interactions, while the change in bilayer thickness is driven by changes in the interaction of the peptide with the headgroupmore »« less

Authors:: Rai, Durgesh K.; Qian, Shuo; Heller, William T.

Publication Date:: Tue Nov 01 00:00:00 EDT 2016

Research Org.:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Spallation Neutron Source (SNS); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). Center for Structural Molecular Biology (CSMB)

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

OSTI Identifier:: 1406384

Alternate Identifier(s):: OSTI ID: 1311221; OSTI ID: 1397552

Grant/Contract Number:: LDRD-6436; 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: 1858 Journal Issue: 11; Journal ID: ISSN 0005-2736

Publisher:: Elsevier

Country of Publication:: Netherlands

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; membrane-active peptide; melittin; small-angle neutron scattering; phosphatidylserine; membrane asymmetry

Citation Formats


                    Rai, Durgesh K., Qian, Shuo, and Heller, William T. The Interaction of Melittin with Dimyristoyl Phosphatidylcholine-Dimyristoyl Phosphatidylserine Lipid Bilayer Membranes.  Netherlands: N. p., 2016. 
Web.  doi:10.1016/j.bbamem.2016.08.006.

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                    Rai, Durgesh K., Qian, Shuo, & Heller, William T. The Interaction of Melittin with Dimyristoyl Phosphatidylcholine-Dimyristoyl Phosphatidylserine Lipid Bilayer Membranes.  Netherlands.  https://doi.org/10.1016/j.bbamem.2016.08.006

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                    Rai, Durgesh K., Qian, Shuo, and Heller, William T. Tue .  
"The Interaction of Melittin with Dimyristoyl Phosphatidylcholine-Dimyristoyl Phosphatidylserine Lipid Bilayer Membranes".  Netherlands.  https://doi.org/10.1016/j.bbamem.2016.08.006.

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@article{osti_1406384,

  title        = {The Interaction of Melittin with Dimyristoyl Phosphatidylcholine-Dimyristoyl Phosphatidylserine Lipid Bilayer Membranes},

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

  abstractNote = {We report that membrane-active peptides (MAPs), which interact directly with the lipid bilayer of a cell and include toxins and host defense peptides, display lipid composition-dependent activity. Phosphatidylserine (PS) lipids are anionic lipids that are found throughout the cellular membranes of most eukaryotic organisms where they serve as both a functional component and as a precursor to phosphatidylethanolamine lipids. The inner leaflet of the plasma membrane contains more PS than the outer one, and the asymmetry is actively maintained. Here, the impact of the MAP melittin on the structure of lipid bilayer vesicles made of a mixture of phosphatidylcholine and phosphatidylserine was studied. Small-angle neutron scattering of the MAP associated with selectively deuterium-labeled lipid bilayer vesicles revealed how the thickness and lipid composition of phosphatidylserine-containing vesicles change in response to melittin. The peptide thickens the lipid bilayer for concentrations up to P/L = 1/500, but membrane thinning results when P/L = 1/200. The thickness transition is accompanied by a large change in the distribution of DMPS between the leaflets of the bilayer. The change in composition is driven by electrostatic interactions, while the change in bilayer thickness is driven by changes in the interaction of the peptide with the headgroup region of the lipid bilayer. Lastly, the results provide new information about lipid-specific interactions that take place in mixed composition lipid bilayer membranes.},

  doi          = {10.1016/j.bbamem.2016.08.006},

  journal      = {Biochimica et Biophysica Acta. Biomembranes},

  number       = 11,

  volume       = 1858,

  place        = {Netherlands},

  year         = {Tue Nov 01 00:00:00 EDT 2016},

  month        = {Tue Nov 01 00:00:00 EDT 2016}

}

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Title: The Interaction of Melittin with Dimyristoyl Phosphatidylcholine-Dimyristoyl Phosphatidylserine Lipid Bilayer Membranes

Abstract

Citation Formats

Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network journal, January 1993

Lipid–protein interactions in blood coagulation journal, November 1998

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

Interaction of melittin with lipid membranes journal, September 1994

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

Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides journal, September 1976

Phospholipid Composition of Bacillus subtilis journal, January 1969

Investigation on lipid asymmetry using lipid probes journal, June 2002

Phospholipid Component Volumes: Determination and Application to Bilayer Structure Calculations journal, August 1998

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

Lipid compositions in Escherichia coli and Bacillus subtilis during growth as determined by MALDI-TOF and TOF/TOF mass spectrometry journal, June 2009

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

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

Neutron scattering lengths and cross sections journal, January 1992

Mode of action of membrane active antimicrobial peptides journal, January 2002

Detection of asymmetric distribution of phospholipids by fluorescence resonance energy transfer journal, April 2012

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

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

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

Loss of Phospholipid Asymmetry and Surface Exposure of Phosphatidylserine Is Required for Phagocytosis of Apoptotic Cells by Macrophages and Fibroblasts journal, January 2001

Modulation of Tryptophan Environment in Membrane-Bound Melittin by Negatively Charged Phospholipids: Implications in Membrane Organization and Function † journal, November 1997

Structure and Fluctuations of Charged Phosphatidylserine Bilayers in the Absence of Salt journal, March 2004

Membranes are more mosaic than fluid journal, November 2005

Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl journal, November 1995

CD Spectroscopy of Peptides and Proteins Bound to Large Unilamellar Vesicles journal, August 2010

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

Direct measurement of the interaction between phosphatidylglycerol bilayers in aqueous electrolyte solutions journal, November 1986

Interaction of melittin with mixed phospholipid membranes composed of dimyristoylphosphatidylcholine and dimyristoylphosphatidylserine studied by deuterium NMR journal, August 1989

Lipid outward translocation by ABC proteins journal, April 2010

Method of separated form factors for polydisperse vesicles journal, May 2006

An Antimicrobial Peptide, Magainin 2, Induced Rapid Flip-Flop of Phospholipids Coupled with Pore Formation and Peptide Translocation † journal, January 1996

Modulation of melittin-induced lysis by surface charge density of membranes journal, January 1995

Electrostatic Induction of Lipid Asymmetry journal, June 2011

Melittin-induced cholesterol reorganization in lipid bilayer membranes journal, October 2015

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

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

Phosphatidic acid- and phosphatidylserine-binding proteins journal, August 2006

A phosphatidylserine binding site in factor Va C1 domain regulates both assembly and activity of the prothrombinase complex journal, October 2008

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

Phospholipid flip-flop modulated by transmembrane peptides WALP and melittin journal, October 2009

Mechanism of alamethicin insertion into lipid bilayers journal, November 1996

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Amphipathic, α-helical antimicrobial peptides journal, January 2000

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

Understanding inelastically scattered neutrons from water on a time-of-flight small-angle neutron scattering (SANS) instrument journal, February 2014

Pore-Forming Peptides Induce Rapid Phospholipid Flip-Flop in Membranes journal, May 1994

Multiple States of β-Sheet Peptide Protegrin in Lipid Bilayers † journal, December 1998

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

Static and dynamic lipid asymmetry in cell membranes journal, February 1991

Evaluation of secondary structure of proteins from UV circular dichroism spectra using an unsupervised learning neural network
journal, January 1993

Lipid–protein interactions in blood coagulation
journal, November 1998

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

Interaction of melittin with lipid membranes
journal, September 1994

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

Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides
journal, September 1976

Phospholipid Composition of Bacillus subtilis
journal, January 1969

Investigation on lipid asymmetry using lipid probes
journal, June 2002

Phospholipid Component Volumes: Determination and Application to Bilayer Structure Calculations
journal, August 1998

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

Lipid compositions in Escherichia coli and Bacillus subtilis during growth as determined by MALDI-TOF and TOF/TOF mass spectrometry
journal, June 2009

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

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

Neutron scattering lengths and cross sections
journal, January 1992

Mode of action of membrane active antimicrobial peptides
journal, January 2002

Detection of asymmetric distribution of phospholipids by fluorescence resonance energy transfer
journal, April 2012

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

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

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

Loss of Phospholipid Asymmetry and Surface Exposure of Phosphatidylserine Is Required for Phagocytosis of Apoptotic Cells by Macrophages and Fibroblasts
journal, January 2001

Modulation of Tryptophan Environment in Membrane-Bound Melittin by Negatively Charged Phospholipids: Implications in Membrane Organization and Function ^†
journal, November 1997

Structure and Fluctuations of Charged Phosphatidylserine Bilayers in the Absence of Salt
journal, March 2004

Membranes are more mosaic than fluid
journal, November 2005

Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl
journal, November 1995

CD Spectroscopy of Peptides and Proteins Bound to Large Unilamellar Vesicles
journal, August 2010

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

Direct measurement of the interaction between phosphatidylglycerol bilayers in aqueous electrolyte solutions
journal, November 1986

Interaction of melittin with mixed phospholipid membranes composed of dimyristoylphosphatidylcholine and dimyristoylphosphatidylserine studied by deuterium NMR
journal, August 1989

Lipid outward translocation by ABC proteins
journal, April 2010

Method of separated form factors for polydisperse vesicles
journal, May 2006

An Antimicrobial Peptide, Magainin 2, Induced Rapid Flip-Flop of Phospholipids Coupled with Pore Formation and Peptide Translocation ^†
journal, January 1996

Modulation of melittin-induced lysis by surface charge density of membranes
journal, January 1995

Electrostatic Induction of Lipid Asymmetry
journal, June 2011

Melittin-induced cholesterol reorganization in lipid bilayer membranes
journal, October 2015

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

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

Phosphatidic acid- and phosphatidylserine-binding proteins
journal, August 2006

A phosphatidylserine binding site in factor Va C1 domain regulates both assembly and activity of the prothrombinase complex
journal, October 2008

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

Phospholipid flip-flop modulated by transmembrane peptides WALP and melittin
journal, October 2009

Mechanism of alamethicin insertion into lipid bilayers
journal, November 1996

X-ray diffraction study of lipid bilayer membranes interacting with amphiphilic helical peptides: diphytanoyl phosphatidylcholine with alamethicin at low concentrations
journal, June 1995

Amphipathic, α-helical antimicrobial peptides
journal, January 2000

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

Understanding inelastically scattered neutrons from water on a time-of-flight small-angle neutron scattering (SANS) instrument
journal, February 2014

Pore-Forming Peptides Induce Rapid Phospholipid Flip-Flop in Membranes
journal, May 1994

Multiple States of β-Sheet Peptide Protegrin in Lipid Bilayers ^†
journal, December 1998

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

Static and dynamic lipid asymmetry in cell membranes
journal, February 1991