Bicontinuous microemulsions as a biomembrane mimetic system for melittin

Hayes, Douglas G.; Ye, Ran; Dunlap, Rachel N.; Anunciado, Divina B.; Pingali, Sai Venkatesh; O'Neill, Hugh M.; Urban, Volker S.

doi:10.1016/j.bbamem.2017.11.005

Title: Bicontinuous microemulsions as a biomembrane mimetic system for melittin

Abstract

Antimicrobial peptides effectively kill antibiotic-resistant bacteria by forming pores in prokaryotes' biomembranes via penetration into the biomembranes' interior. Bicontinuous microemulsions, consisting of interdispersed oil and water nanodomains separated by flexible surfactant monolayers, are potentially valuable for hosting membrane-associated peptides and proteins due to their thermodynamic stability, optical transparency, low viscosity, and high interfacial area. Here, we show that bicontinuous microemulsions formed by negatively-charged surfactants are a robust biomembrane mimetic system for the antimicrobial peptide melittin. When encapsulated in bicontinuous microemulsions formed using three-phase (Winsor-III) systems, melittin's helicity increases greatly due to penetration into the surfactant monolayers, mimicking its behavior in biomembranes. But, the threshold melittin concentration required to achieve these trends is lower for the microemulsions. The extent of penetration was decreased when the interfacial fluidity of the microemulsions was increased. In conclusion, these results suggest the utility of bicontinuous microemulsions for isolation, purification, delivery, and host systems for antimicrobial peptides.

Authors:: Hayes, Douglas G.; Ye, Ran; Dunlap, Rachel N.; Anunciado, Divina B.; Pingali, Sai Venkatesh; O'Neill, Hugh M.; Urban, Volker S.

Publication Date:: Thu Feb 01 00:00:00 EST 2018

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:: 1549058

Alternate Identifier(s):: OSTI ID: 1413610

Grant/Contract Number:: 6552; 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: 1860 Journal Issue: 2; Journal ID: ISSN 0005-2736

Publisher:: Elsevier

Country of Publication:: Netherlands

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; Aerosol-OT; Bicontinuous microemulsions; Melittin; Antimicrobial peptides; Small-angle neutron scattering; Winsor-III microemulsion systems; Biomembrane mimetic systems

Citation Formats


                    Hayes, Douglas G., Ye, Ran, Dunlap, Rachel N., Anunciado, Divina B., Pingali, Sai Venkatesh, O'Neill, Hugh M., and Urban, Volker S. Bicontinuous microemulsions as a biomembrane mimetic system for melittin.  Netherlands: N. p., 2018. 
Web.  doi:10.1016/j.bbamem.2017.11.005.

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                    Hayes, Douglas G., Ye, Ran, Dunlap, Rachel N., Anunciado, Divina B., Pingali, Sai Venkatesh, O'Neill, Hugh M., & Urban, Volker S. Bicontinuous microemulsions as a biomembrane mimetic system for melittin.  Netherlands.  https://doi.org/10.1016/j.bbamem.2017.11.005

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                    Hayes, Douglas G., Ye, Ran, Dunlap, Rachel N., Anunciado, Divina B., Pingali, Sai Venkatesh, O'Neill, Hugh M., and Urban, Volker S. Thu .  
"Bicontinuous microemulsions as a biomembrane mimetic system for melittin".  Netherlands.  https://doi.org/10.1016/j.bbamem.2017.11.005.

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@article{osti_1549058,

  title        = {Bicontinuous microemulsions as a biomembrane mimetic system for melittin},

  author       = {Hayes, Douglas G. and Ye, Ran and Dunlap, Rachel N. and Anunciado, Divina B. and Pingali, Sai Venkatesh and O'Neill, Hugh M. and Urban, Volker S.},

  abstractNote = {Antimicrobial peptides effectively kill antibiotic-resistant bacteria by forming pores in prokaryotes' biomembranes via penetration into the biomembranes' interior. Bicontinuous microemulsions, consisting of interdispersed oil and water nanodomains separated by flexible surfactant monolayers, are potentially valuable for hosting membrane-associated peptides and proteins due to their thermodynamic stability, optical transparency, low viscosity, and high interfacial area. Here, we show that bicontinuous microemulsions formed by negatively-charged surfactants are a robust biomembrane mimetic system for the antimicrobial peptide melittin. When encapsulated in bicontinuous microemulsions formed using three-phase (Winsor-III) systems, melittin's helicity increases greatly due to penetration into the surfactant monolayers, mimicking its behavior in biomembranes. But, the threshold melittin concentration required to achieve these trends is lower for the microemulsions. The extent of penetration was decreased when the interfacial fluidity of the microemulsions was increased. In conclusion, these results suggest the utility of bicontinuous microemulsions for isolation, purification, delivery, and host systems for antimicrobial peptides.},

  doi          = {10.1016/j.bbamem.2017.11.005},

  journal      = {Biochimica et Biophysica Acta. Biomembranes},

  number       = 2,

  volume       = 1860,

  place        = {Netherlands},

  year         = {Thu Feb 01 00:00:00 EST 2018},

  month        = {Thu Feb 01 00:00:00 EST 2018}

}

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Title: Bicontinuous microemulsions as a biomembrane mimetic system for melittin

Abstract

Citation Formats

Process of inducing pores in membranes by melittin journal, August 2013

Gating charge displacement in voltage-gated ion channels involves limited transmembrane movement journal, August 2005

Characterization of Microemulsion Systems Formed by a Mixed 1,3-Dioxolane Ethoxylate/Octyl Glucoside Surfactant System journal, April 2009

The actions of melittin on membranes journal, May 1990

Synthesis of pH-Degradable Nonionic Surfactants and Their Applications in Microemulsions journal, October 2001

Recommended Liquid–Liquid Equilibrium Data. Part 4. 1-Alkanol–Water Systems journal, September 2006

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

Confinement Effects in Block Copolymer Modified Bicontinuous Microemulsions journal, April 2013

Multidrug-resistant organisms, wounds and topical antimicrobial protection journal, May 2012

Protective effects of melittin on transforming growth factor-β1 injury to hepatocytes via anti-apoptotic mechanism journal, October 2011

The economic burden of community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) journal, June 2013

Detergent-like actions of linear amphipathic cationic antimicrobial peptides journal, September 2006

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Small‐angle neutron scattering from microemulsions near the disorder line in water/formamide–octane‐C i E j systems journal, December 1991

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Effects of Sweet Bee Venom Pharmacopuncture Treatment for Chemotherapy-Induced Peripheral Neuropathy: A Case Series journal, June 2011

Protein extraction into the bicontinuous microemulsion phase of a Water/SDS/pentanol/dodecane winsor-III system: Effect on nanostructure and protein conformation journal, December 2017

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Effect of Protein Incorporation on the Nanostructure of the Bicontinuous Microemulsion Phase of Winsor-III Systems: A Small-Angle Neutron Scattering Study journal, February 2015

Liquid Interface Functionalized by an Ion Extractant: The Case of Winsor III Microemulsions journal, March 2011

Flexibility, persistence length and bicontinuous microstructures in microemulsions journal, January 2009

Small angle neutron scattering near Lifshitz lines: Transition from weakly structured mixtures to microemulsions journal, September 1994

Amphipathic, α-helical antimicrobial peptides journal, January 2000

Partitioning behavior of an acid-cleavable, 1,3-dioxolane alkyl ethoxylate, surfactant in single and binary surfactant mixtures for 2- and 3-phase microemulsion systems according to ethoxylate head group size journal, December 2010

Molecular mechanism of antimicrobial peptides: The origin of cooperativity journal, September 2006

The sting. Melittin forms channels in lipid bilayers journal, October 1981

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

Surgical site infection: Incidence and impact on hospital utilization and treatment costs journal, June 2009

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

Antiarthritic effect of bee venom: Inhibition of inflammation mediator generation by suppression of NF-?B through interaction with the p50 subunit journal, November 2004

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

Melittin restores proteasome function in an animal model of ALS journal, January 2011

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journal, August 2005

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journal, April 2009

The actions of melittin on membranes
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Synthesis of pH-Degradable Nonionic Surfactants and Their Applications in Microemulsions
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Recommended Liquid–Liquid Equilibrium Data. Part 4. 1-Alkanol–Water Systems
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Role of lipids in the interaction of antimicrobial peptides with membranes
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Confinement Effects in Block Copolymer Modified Bicontinuous Microemulsions
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Protective effects of melittin on transforming growth factor-β1 injury to hepatocytes via anti-apoptotic mechanism
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The economic burden of community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA)
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Nanoscopic dynamics of bicontinous microemulsions: effect of membrane associated protein
journal, January 2017

Small‐angle neutron scattering from microemulsions near the disorder line in water/formamide–octane‐C _i E _j systems
journal, December 1991

Measuring bending rigidity and spatial renormalization in bicontinuous microemulsions
journal, December 2001

Melittin inhibits inflammatory target gene expression and mediator generation via interaction with IκB kinase
journal, January 2007

Structure of biodiesel based bicontinuous microemulsions for environmentally compatible decontamination: A small angle neutron scattering and freeze fracture electron microscopy study
journal, September 2008

Microemulsion Efficiency Boosting and the Complementary Effect. 1. Structural Properties
journal, November 2004

Dual secured nano-melittin for the safe and effective eradication of cancer cells
journal, January 2015

Protein extraction by Winsor-III microemulsion systems
journal, June 2011

Ordered porous materials for emerging applications
journal, June 2002

Triacylglycerol microemulsions stabilized by alkyl ethoxylate surfactants—A basic study
journal, August 2007

Antimicrobials and Non-Healing Wounds. Evidence, controversies and suggestions—key messages
journal, October 2014

Emerging roles for lipids in shaping membrane-protein function
journal, May 2009

Experimental determination of bending rigidity and saddle splay modulus in bicontinuous microemulsions
journal, January 2013

Bee venom and melittin reduce proinflammatory mediators in lipopolysaccharide-stimulated BV2 microglia
journal, August 2007

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

Reduction and analysis of SANS and USANS data using IGOR Pro
journal, November 2006

Effects of Sweet Bee Venom Pharmacopuncture Treatment for Chemotherapy-Induced Peripheral Neuropathy: A Case Series
journal, June 2011

Protein extraction into the bicontinuous microemulsion phase of a Water/SDS/pentanol/dodecane winsor-III system: Effect on nanostructure and protein conformation
journal, December 2017

Removal of non-ionic organic pollutants from water via liquid–liquid extraction
journal, May 2005

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

Effect of Protein Incorporation on the Nanostructure of the Bicontinuous Microemulsion Phase of Winsor-III Systems: A Small-Angle Neutron Scattering Study
journal, February 2015

Liquid Interface Functionalized by an Ion Extractant: The Case of Winsor III Microemulsions
journal, March 2011

Flexibility, persistence length and bicontinuous microstructures in microemulsions
journal, January 2009

Small angle neutron scattering near Lifshitz lines: Transition from weakly structured mixtures to microemulsions
journal, September 1994

Amphipathic, α-helical antimicrobial peptides
journal, January 2000

Partitioning behavior of an acid-cleavable, 1,3-dioxolane alkyl ethoxylate, surfactant in single and binary surfactant mixtures for 2- and 3-phase microemulsion systems according to ethoxylate head group size
journal, December 2010

Molecular mechanism of antimicrobial peptides: The origin of cooperativity
journal, September 2006

The sting. Melittin forms channels in lipid bilayers
journal, October 1981

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

Surgical site infection: Incidence and impact on hospital utilization and treatment costs
journal, June 2009

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

Antiarthritic effect of bee venom: Inhibition of inflammation mediator generation by suppression of NF-?B through interaction with the p50 subunit
journal, November 2004

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

Melittin restores proteasome function in an animal model of ALS
journal, January 2011

Incorporation of antimicrobial peptides in nanostructured lipid membrane mimetic bilayer cubosomes
journal, April 2017