Assessment of antimicrobial activity of melittin encapsulated in bicontinuous microemulsions prepared using renewable oils

Oehler, Madison A.; Hayes, Douglas G.; D'Souza, Doris H.; Senanayake, Manjula; Gurumoorthy, Viswanathan; Pingali, Sai Venkatesh; O'Neill, Hugh M.; Bras, Wim; Urban, Volker S.

doi:10.1002/jsde.12654

Title: Assessment of antimicrobial activity of melittin encapsulated in bicontinuous microemulsions prepared using renewable oils

Abstract

Abstract The objective of this study is to demonstrate that melittin, a well‐studied antimicrobial peptide (AMP), can be solubilized in an active form in bicontinuous microemulsions (BMEs) that employ biocompatible oils. The systems investigated consisted of Winsor‐III and ‐IV BME phases composed of Water/Aerosol‐OT (AOT)/Polysorbate 85/isopropyl myristate and a Winsor‐IV BME employing Polysorbate 80 and limonene. We found that melittin resided in an α‐helix‐rich configuration and was in an apolar environment for the AOT/Polysorbate 85 Winsor‐III system, suggesting that melittin interacted with the surfactant monolayer and was in an active conformation. An apolar environment was also detected for melittin in the two Winsor‐IV systems, but to a lesser extent than the Winsor‐III system. Small‐angle X‐ray scattering analysis indicated that melittin at a concentration of 1.0 g/L _aq in the aqueous subphase of the Winsor‐IV systems led to the greatest impact on the BME structure (e.g., decrease of quasi‐periodic repeat distance and correlation length and induction of interfacial fluidity). The antimicrobial activity of the Polysorbate 80 Winsor‐IV system was evaluated against several bacteria prominent in chronic wounds and surgical site infections (SSIs). Melittin‐free BMEs inhibited the growth of all tested bacteria due to its oil, limonene, while the inclusion of 1.0 g/L _aqmore »« less

Authors:

^[1];

^[1]; D'Souza, Doris H. ^[2];

^[3];

^[3]

Department of Biosystems Engineering and Soil Science University of Tennessee Knoxville Tennessee USA
Department of Food Science University of Tennessee Knoxville Tennessee USA
Neutron Scattering Division Oak Ridge National Laboratory Oak Ridge Tennessee USA

Publication Date:: Wed Dec 28 00:00:00 EST 2022

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

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

OSTI Identifier:: 1907025

Alternate Identifier(s):: OSTI ID: 1983554; OSTI ID: 1984346

Grant/Contract Number:: AC05-00OR22725; 5R03AI154314-02

Resource Type:: Published Article

Journal Name:: Journal of Surfactants and Detergents

Additional Journal Information:: Journal Name: Journal of Surfactants and Detergents Journal Volume: 26 Journal Issue: 3; Journal ID: ISSN 1097-3958

Publisher:: Wiley Blackwell (John Wiley & Sons)

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; antimicrobial activity; antimicrobial peptides; bicontinuous microemulsions; melittin; small-angle X-ray scattering

Citation Formats


                    Oehler, Madison A., Hayes, Douglas G., D'Souza, Doris H., Senanayake, Manjula, Gurumoorthy, Viswanathan, Pingali, Sai Venkatesh, O'Neill, Hugh M., Bras, Wim, and Urban, Volker S. Assessment of antimicrobial activity of melittin encapsulated in bicontinuous microemulsions prepared using renewable oils.  United States: N. p., 2022. 
Web.  doi:10.1002/jsde.12654.

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                    Oehler, Madison A., Hayes, Douglas G., D'Souza, Doris H., Senanayake, Manjula, Gurumoorthy, Viswanathan, Pingali, Sai Venkatesh, O'Neill, Hugh M., Bras, Wim, & Urban, Volker S. Assessment of antimicrobial activity of melittin encapsulated in bicontinuous microemulsions prepared using renewable oils.  United States.  https://doi.org/10.1002/jsde.12654

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                    Oehler, Madison A., Hayes, Douglas G., D'Souza, Doris H., Senanayake, Manjula, Gurumoorthy, Viswanathan, Pingali, Sai Venkatesh, O'Neill, Hugh M., Bras, Wim, and Urban, Volker S. Wed .  
"Assessment of antimicrobial activity of melittin encapsulated in bicontinuous microemulsions prepared using renewable oils".  United States.  https://doi.org/10.1002/jsde.12654.

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@article{osti_1907025,

  title        = {Assessment of antimicrobial activity of melittin encapsulated in bicontinuous microemulsions prepared using renewable oils},

  author       = {Oehler, Madison A. and Hayes, Douglas G. and D'Souza, Doris H. and Senanayake, Manjula and Gurumoorthy, Viswanathan and Pingali, Sai Venkatesh and O'Neill, Hugh M. and Bras, Wim and Urban, Volker S.},

  abstractNote = {Abstract The objective of this study is to demonstrate that melittin, a well‐studied antimicrobial peptide (AMP), can be solubilized in an active form in bicontinuous microemulsions (BMEs) that employ biocompatible oils. The systems investigated consisted of Winsor‐III and ‐IV BME phases composed of Water/Aerosol‐OT (AOT)/Polysorbate 85/isopropyl myristate and a Winsor‐IV BME employing Polysorbate 80 and limonene. We found that melittin resided in an α‐helix‐rich configuration and was in an apolar environment for the AOT/Polysorbate 85 Winsor‐III system, suggesting that melittin interacted with the surfactant monolayer and was in an active conformation. An apolar environment was also detected for melittin in the two Winsor‐IV systems, but to a lesser extent than the Winsor‐III system. Small‐angle X‐ray scattering analysis indicated that melittin at a concentration of 1.0 g/L aq in the aqueous subphase of the Winsor‐IV systems led to the greatest impact on the BME structure (e.g., decrease of quasi‐periodic repeat distance and correlation length and induction of interfacial fluidity). The antimicrobial activity of the Polysorbate 80 Winsor‐IV system was evaluated against several bacteria prominent in chronic wounds and surgical site infections (SSIs). Melittin‐free BMEs inhibited the growth of all tested bacteria due to its oil, limonene, while the inclusion of 1.0 g/L aq of melittin in the BMEs enhanced the activity against several bacteria. A further increase of melittin concentration in the BMEs had no further enhancement. These results demonstrate the potential utility of BMEs as a delivery platform for AMPs and other hydrophilic and lipophilic drugs to inhibit antibiotic‐resistant microorganisms in chronic wounds and SSIs.},

  doi          = {10.1002/jsde.12654},

  journal      = {Journal of Surfactants and Detergents},

  number       = 3,

  volume       = 26,

  place        = {United States},

  year         = {Wed Dec 28 00:00:00 EST 2022},

  month        = {Wed Dec 28 00:00:00 EST 2022}

}

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Title: Assessment of antimicrobial activity of melittin encapsulated in bicontinuous microemulsions prepared using renewable oils

Abstract

Citation Formats

Surgical-site infection journal, October 2009

Antimicrobial Peptide-Driven Colloidal Transformations in Liquid-Crystalline Nanocarriers journal, August 2016

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

Protein helical structure determination using CD spectroscopy for solutions with strong background absorbance from 190 to 230nm journal, December 2014

Influence of polysorbates (Tweens) on structural and antimicrobial properties for microemulsions journal, November 2020

Challenges in the Treatment of Chronic Wounds journal, September 2015

Microemulsions — phase equilibria characterization, structures, applications and chemical reactions journal, May 1996

Effect of multiple scattering on SANS spectra from bicontinuous microemulsions journal, January 2003

Bicontinuous Cyclosporin a Loaded Water-AOT/Tween 85-Isopropylmyristate Microemulsion: Structural Characterization and Dermal Pharmacokinetics In Vivo journal, March 2009

Formulating Alcohol-Free Microemulsions Using Rhamnolipid Biosurfactant and Rhamnolipid Mixtures journal, December 2008

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

Review: Lessons Learned From Clinical Trials Using Antimicrobial Peptides (AMPs) journal, February 2021

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

Antimicrobial Peptides journal, November 2013

How Melittin Inserts into Cell Membrane: Conformational Changes, Inter-Peptide Cooperation, and Disturbance on the Membrane journal, May 2019

Detergency of Vegetable Oils and Semi‐Solid Fats Using Microemulsion Mixtures of Anionic Extended Surfactants: The HLD Concept and Cold Water Applications journal, December 2014

Incorporation of Melittin Enhances Interfacial Fluidity of Bicontinuous Microemulsions journal, February 2019

Sequenzanalyse des Melittins aus den tryptischen und peptischen Spaltstücken journal, January 1967

Characterization of phase and diffusion behaviors of oil, surfactant, and co-surfactant ternary systems for lipid-based delivery carriers journal, October 2021

Incorporation of Membrane Proteins Into Bicontinuous Microemulsions Through Winsor‐III System‐Based Extraction journal, March 2021

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

Rosmarinus officinalis L. essential oil encapsulated in new microemulsion formulations for enhanced antimicrobial activity journal, September 2021

A review on antimicrobial peptides databases and the computational tools journal, March 2022

Optimized Microemulsion Systems for Detergency of Vegetable Oils at Low Surfactant Concentration and Bath Temperature journal, April 2017

Antimicrobial Peptides: Classification, Design, Application and Research Progress in Multiple Fields journal, October 2020

Anionic-Surfactant-Stabilized Hydrophobic Ionic-Liquid-Based Bicontinuous Microemulsion as a Medium for Enzymatic Oxidative Polymerization of Aniline journal, July 2021

Essential oil microemulsions inactivate antibiotic-resistant Salmonella Newport and spoilage bacterium Lactobacillus casei on Iceberg lettuce during 28-day storage at 4°C journal, December 2021

Organization and Dynamics of Melittin in Environments of Graded Hydration: A Fluorescence Approach journal, October 2003

Antimicrobial activity of a food-grade fully dilutable microemulsion against Escherichia coli and Staphylococcus aureus journal, November 2009

Topical antimicrobial peptide formulations for wound healing: Current developments and future prospects journal, February 2020

The influence of the structure and the composition of water/AOT-Tween 85/IPM microemulsion system on transdermal delivery of 5-fluorouracil journal, February 2012

Five-component food-grade microemulsions: structural characterization by SANS journal, June 2004

Health Care–Associated Infections: A Meta-analysis of Costs and Financial Impact on the US Health Care System journal, December 2013

Mixed micelles and bicontinuous microemulsions: Promising media for enzymatic reactions journal, January 2022

Three Valuable Peptides from Bee and Wasp Venoms for Therapeutic and Biotechnological Use: Melittin, Apamin and Mastoparan journal, April 2015

Applications and evolution of melittin, the quintessential membrane active peptide journal, November 2021

Bicontinuous microemulsions as a biomembrane mimetic system for melittin journal, February 2018

Delivery systems for antimicrobial peptides journal, April 2017

Characterization and Emulsification Properties of Rhamnolipid and Sophorolipid Biosurfactants and Their Applications journal, February 2011

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

Nanoscopic dynamics of bicontinous microemulsions: effect of membrane associated protein journal, January 2017

The Burden of Methicillin Resistant Staphylococcus aureus in Surgical Site Infections: A Review journal, January 2021

Surgical-site infection journal, September 2010

Preparation of water-in-oil (W/O) cinnamaldehyde microemulsion loaded with epsilon-polylysine and its antibacterial properties journal, April 2022

Porous gold nanomesh films electrodeposited in toluene-based dynamic soft template journal, September 2022

Effects of Triglyceride Molecular Structure on Optimum Formulation of Surfactant-Oil-Water Systems journal, August 2009

Characterizing oil mixture and surfactant mixture via hydrophilic-lipophilic deviation (HLD) principle: An insight in consumer products development journal, February 2022

A study of melittin, motilin and galanin in reversed micellar environments, using circular dichroism spectroscopy journal, March 1996

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

New Interfacial Rheology Characteristics Measured Using a Spinning Drop Rheometer at the Optimum Formulation. Part 2. Surfactant–Oil–Water Systems with a High Volume of Middle‐Phase Microemulsion journal, January 2019

Mechanism of Bacterial Inactivation by (+)-Limonene and Its Potential Use in Food Preservation Combined Processes journal, February 2013

Mechanism of the Extraction of Proteins into Tween 85 Nonionic Microemulsions journal, January 1996

Bicontinuous microemulsions containing Melaleuca alternifolia essential oil as a therapeutic agent for cutaneous wound healing journal, September 2020

Antimicrobial activity and mechanism of limonene against Staphylococcus aureus journal, August 2021

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

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

Gelled non-toxic bicontinuous microemulsions as promising transdermal drug carriers journal, February 2021

DRAMP 2.0, an updated data repository of antimicrobial peptides journal, August 2019

Using circular dichroism spectra to estimate protein secondary structure journal, January 2007

Impact of Composition and Placement of Hydrogen-Bonding Groups along Polymer Chains on Blend Phase Behavior: Coarse-Grained Molecular Dynamics Simulation Study journal, March 2022

Surgical-site infection
journal, October 2009

Antimicrobial Peptide-Driven Colloidal Transformations in Liquid-Crystalline Nanocarriers
journal, August 2016

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

Protein helical structure determination using CD spectroscopy for solutions with strong background absorbance from 190 to 230nm
journal, December 2014

Influence of polysorbates (Tweens) on structural and antimicrobial properties for microemulsions
journal, November 2020

Challenges in the Treatment of Chronic Wounds
journal, September 2015

Microemulsions — phase equilibria characterization, structures, applications and chemical reactions
journal, May 1996

Effect of multiple scattering on SANS spectra from bicontinuous microemulsions
journal, January 2003

Bicontinuous Cyclosporin a Loaded Water-AOT/Tween 85-Isopropylmyristate Microemulsion: Structural Characterization and Dermal Pharmacokinetics In Vivo
journal, March 2009

Formulating Alcohol-Free Microemulsions Using Rhamnolipid Biosurfactant and Rhamnolipid Mixtures
journal, December 2008

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

Review: Lessons Learned From Clinical Trials Using Antimicrobial Peptides (AMPs)
journal, February 2021

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

Antimicrobial Peptides
journal, November 2013

How Melittin Inserts into Cell Membrane: Conformational Changes, Inter-Peptide Cooperation, and Disturbance on the Membrane
journal, May 2019

Detergency of Vegetable Oils and Semi‐Solid Fats Using Microemulsion Mixtures of Anionic Extended Surfactants: The HLD Concept and Cold Water Applications
journal, December 2014

Incorporation of Melittin Enhances Interfacial Fluidity of Bicontinuous Microemulsions
journal, February 2019

Sequenzanalyse des Melittins aus den tryptischen und peptischen Spaltstücken
journal, January 1967

Characterization of phase and diffusion behaviors of oil, surfactant, and co-surfactant ternary systems for lipid-based delivery carriers
journal, October 2021

Incorporation of Membrane Proteins Into Bicontinuous Microemulsions Through Winsor‐III System‐Based Extraction
journal, March 2021

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

Rosmarinus officinalis L. essential oil encapsulated in new microemulsion formulations for enhanced antimicrobial activity
journal, September 2021

A review on antimicrobial peptides databases and the computational tools
journal, March 2022

Optimized Microemulsion Systems for Detergency of Vegetable Oils at Low Surfactant Concentration and Bath Temperature
journal, April 2017

Antimicrobial Peptides: Classification, Design, Application and Research Progress in Multiple Fields
journal, October 2020

Anionic-Surfactant-Stabilized Hydrophobic Ionic-Liquid-Based Bicontinuous Microemulsion as a Medium for Enzymatic Oxidative Polymerization of Aniline
journal, July 2021

Essential oil microemulsions inactivate antibiotic-resistant Salmonella Newport and spoilage bacterium Lactobacillus casei on Iceberg lettuce during 28-day storage at 4°C
journal, December 2021

Organization and Dynamics of Melittin in Environments of Graded Hydration: A Fluorescence Approach
journal, October 2003

Antimicrobial activity of a food-grade fully dilutable microemulsion against Escherichia coli and Staphylococcus aureus
journal, November 2009

Topical antimicrobial peptide formulations for wound healing: Current developments and future prospects
journal, February 2020

The influence of the structure and the composition of water/AOT-Tween 85/IPM microemulsion system on transdermal delivery of 5-fluorouracil
journal, February 2012

Five-component food-grade microemulsions: structural characterization by SANS
journal, June 2004

Health Care–Associated Infections: A Meta-analysis of Costs and Financial Impact on the US Health Care System
journal, December 2013

Mixed micelles and bicontinuous microemulsions: Promising media for enzymatic reactions
journal, January 2022

Three Valuable Peptides from Bee and Wasp Venoms for Therapeutic and Biotechnological Use: Melittin, Apamin and Mastoparan
journal, April 2015

Applications and evolution of melittin, the quintessential membrane active peptide
journal, November 2021

Bicontinuous microemulsions as a biomembrane mimetic system for melittin
journal, February 2018

Delivery systems for antimicrobial peptides
journal, April 2017

Characterization and Emulsification Properties of Rhamnolipid and Sophorolipid Biosurfactants and Their Applications
journal, February 2011

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

Nanoscopic dynamics of bicontinous microemulsions: effect of membrane associated protein
journal, January 2017

The Burden of Methicillin Resistant Staphylococcus aureus in Surgical Site Infections: A Review
journal, January 2021

Surgical-site infection
journal, September 2010

Preparation of water-in-oil (W/O) cinnamaldehyde microemulsion loaded with epsilon-polylysine and its antibacterial properties
journal, April 2022

Porous gold nanomesh films electrodeposited in toluene-based dynamic soft template
journal, September 2022

Effects of Triglyceride Molecular Structure on Optimum Formulation of Surfactant-Oil-Water Systems
journal, August 2009

Characterizing oil mixture and surfactant mixture via hydrophilic-lipophilic deviation (HLD) principle: An insight in consumer products development
journal, February 2022

A study of melittin, motilin and galanin in reversed micellar environments, using circular dichroism spectroscopy
journal, March 1996

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

New Interfacial Rheology Characteristics Measured Using a Spinning Drop Rheometer at the Optimum Formulation. Part 2. Surfactant–Oil–Water Systems with a High Volume of Middle‐Phase Microemulsion
journal, January 2019

Mechanism of Bacterial Inactivation by (+)-Limonene and Its Potential Use in Food Preservation Combined Processes
journal, February 2013

Mechanism of the Extraction of Proteins into Tween 85 Nonionic Microemulsions
journal, January 1996

Bicontinuous microemulsions containing Melaleuca alternifolia essential oil as a therapeutic agent for cutaneous wound healing
journal, September 2020

Antimicrobial activity and mechanism of limonene against Staphylococcus aureus
journal, August 2021

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

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

Gelled non-toxic bicontinuous microemulsions as promising transdermal drug carriers
journal, February 2021

DRAMP 2.0, an updated data repository of antimicrobial peptides
journal, August 2019

Using circular dichroism spectra to estimate protein secondary structure
journal, January 2007

Impact of Composition and Placement of Hydrogen-Bonding Groups along Polymer Chains on Blend Phase Behavior: Coarse-Grained Molecular Dynamics Simulation Study
journal, March 2022