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Title: Interaction of a short antimicrobial peptide on charged lipid bilayer: A case study on aurein 1.2 peptide

Abstract

Aurein 1.2 (aurein) is a short but active α-helical antimicrobial peptide discovered in Australian tree frogs (Litoria aurea). It shows inhibition on a broad spectrum of bacteria and cancer cells. With well-defined helicity, amphipathicity, and cationic charges, it readily binds to membranes and causes membrane change and disruption. This study provides details on how aurein interacts with charged lipid membranes by using neutron membrane diffraction (NMD) and neutron spin echo (NSE) spectroscopy on complex peptide-membrane systems. NMD provides higher resolution lipid bilayer structures than solution scattering. NMD revealed the peptide is mostly associated in the lipid headgroup region. Even at moderately high concentrations (e.g., peptide:lipid ratio of 1:30), aurein is located at the acyl chain-headgroup region without deep penetration into the hydrophobic acyl chain. However, it does reduce the elasticity of the membrane at that concentration, which was corroborated by the NSE results. Furthermore, NSE shows that aurein first softens the membrane, like many other α-helical peptides at low concentration, but then makes the membrane much more rigid, even without membrane pore formation. Combining our previous studies, the evidence shows that aurein at relatively low concentrations still modifies lipid distribution significantly and can cause membrane thinning and lateral segregation ofmore » charged lipids. At the same time, the membrane's mechanical properties are modified with much slower lipid diffusion. This suggests that aurein can attack the microbial membrane without the need to form membrane pores or disintegrate membranes; instead, it promotes the formation of domains at low concentration.« less

Authors:
;
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Spallation Neutron Source (SNS)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; USDOE Office of Science (SC), Nuclear Physics (NP)
OSTI Identifier:
1845945
Alternate Identifier(s):
OSTI ID: 1847522
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Published Article
Journal Name:
BBA Advances
Additional Journal Information:
Journal Name: BBA Advances Journal Volume: 2 Journal Issue: C; Journal ID: ISSN 2667-1603
Publisher:
Elsevier
Country of Publication:
Netherlands
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Antimicrobial peptide; Membrane interaction; Membrane modulus; Neutron diffraction; Neutron spin echo

Citation Formats

Qian, Shuo, and Zolnierczuk, Piotr A. Interaction of a short antimicrobial peptide on charged lipid bilayer: A case study on aurein 1.2 peptide. Netherlands: N. p., 2022. Web. doi:10.1016/j.bbadva.2022.100045.
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Qian, Shuo, & Zolnierczuk, Piotr A. Interaction of a short antimicrobial peptide on charged lipid bilayer: A case study on aurein 1.2 peptide. Netherlands. https://doi.org/10.1016/j.bbadva.2022.100045
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Qian, Shuo, and Zolnierczuk, Piotr A. Sat . "Interaction of a short antimicrobial peptide on charged lipid bilayer: A case study on aurein 1.2 peptide". Netherlands. https://doi.org/10.1016/j.bbadva.2022.100045.
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@article{osti_1845945,
title = {Interaction of a short antimicrobial peptide on charged lipid bilayer: A case study on aurein 1.2 peptide},
author = {Qian, Shuo and Zolnierczuk, Piotr A.},
abstractNote = {Aurein 1.2 (aurein) is a short but active α-helical antimicrobial peptide discovered in Australian tree frogs (Litoria aurea). It shows inhibition on a broad spectrum of bacteria and cancer cells. With well-defined helicity, amphipathicity, and cationic charges, it readily binds to membranes and causes membrane change and disruption. This study provides details on how aurein interacts with charged lipid membranes by using neutron membrane diffraction (NMD) and neutron spin echo (NSE) spectroscopy on complex peptide-membrane systems. NMD provides higher resolution lipid bilayer structures than solution scattering. NMD revealed the peptide is mostly associated in the lipid headgroup region. Even at moderately high concentrations (e.g., peptide:lipid ratio of 1:30), aurein is located at the acyl chain-headgroup region without deep penetration into the hydrophobic acyl chain. However, it does reduce the elasticity of the membrane at that concentration, which was corroborated by the NSE results. Furthermore, NSE shows that aurein first softens the membrane, like many other α-helical peptides at low concentration, but then makes the membrane much more rigid, even without membrane pore formation. Combining our previous studies, the evidence shows that aurein at relatively low concentrations still modifies lipid distribution significantly and can cause membrane thinning and lateral segregation of charged lipids. At the same time, the membrane's mechanical properties are modified with much slower lipid diffusion. This suggests that aurein can attack the microbial membrane without the need to form membrane pores or disintegrate membranes; instead, it promotes the formation of domains at low concentration.},
doi = {10.1016/j.bbadva.2022.100045},
journal = {BBA Advances},
number = C,
volume = 2,
place = {Netherlands},
year = {Sat Jan 01 00:00:00 EST 2022},
month = {Sat Jan 01 00:00:00 EST 2022}
}
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Works referenced in this record:

The antibiotic and anticancer active aurein peptides from the Australian Bell Frogs Litoria aurea and Litoria raniformis: The solution structure of aurein 1.2
journal, September 2000

A novel, rationally designed, hybrid antimicrobial peptide, inspired by cathelicidin and aurein, exhibits membrane-active mechanisms against Pseudomonas aeruginosa
journal, June 2020

  • Klubthawee, Natthaporn; Adisakwattana, Poom; Hanpithakpong, Warunee
  • Scientific Reports, Vol. 10, Issue 1
  • DOI: 10.1038/s41598-020-65688-5

Neutron diffraction studies of the interaction between amphotericin B and lipid-sterol model membranes
journal, October 2012

  • Foglia, Fabrizia; Lawrence, M. Jayne; Demė, Bruno
  • Scientific Reports, Vol. 2, Issue 1
  • DOI: 10.1038/srep00778

Antimicrobial peptides
journal, January 2016

Specific and Selective Peptide-Membrane Interactions Revealed Using Quartz Crystal Microbalance
journal, December 2007

Grazing-Angle Neutron Diffraction Study of the Water Distribution in Membrane Hemifusion: From the Lamellar to Rhombohedral Phase
journal, August 2018

Interaction of cationic antimicrobial peptides from Australian frogs with lipid membranes
journal, March 2018

  • Zhu, Shiying; Sani, Marc‐Antoine; Separovic, Frances
  • Peptide Science, Vol. 110, Issue 3
  • DOI: 10.1002/pep2.24061

Antimicrobial peptides of multicellular organisms
journal, January 2002

Probing Elastic and Viscous Properties of Phospholipid Bilayers Using Neutron Spin Echo Spectroscopy
journal, September 2017

  • Nagao, Michihiro; Kelley, Elizabeth G.; Ashkar, Rana
  • The Journal of Physical Chemistry Letters, Vol. 8, Issue 19
  • DOI: 10.1021/acs.jpclett.7b01830

Data Analysis and Background Subtraction in Neutron Spin Echo Spectroscopy
journal, February 2021

Molecular Mechanism of Peptide-Induced Pores in Membranes
journal, May 2004

Interaction of the Antimicrobial Peptide Aurein 1.2 and Charged Lipid Bilayer
journal, June 2017

Insertion of TAT peptide and perturbation of negatively charged model phospholipid bilayer revealed by neutron diffraction
journal, August 2013

  • Chen, Xiaochao; Sa'adedin, Farid; Deme, Bruno
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1828, Issue 8
  • DOI: 10.1016/j.bbamem.2013.04.022

Effect of Chain Length and Unsaturation on Elasticity of Lipid Bilayers
journal, July 2000

Direct Visualization of Membrane Leakage Induced by the Antibiotic Peptides: Maculatin, Citropin, and Aurein
journal, September 2005

Incorporation of β-Amino Acids Enhances the Antifungal Activity and Selectivity of the Helical Antimicrobial Peptide Aurein 1.2
journal, November 2017

Viscosity of deuterium oxide and water in the range 5 to 125 C
journal, June 1949

  • Hardy, Robert C.; Cottington, Robert L.
  • Journal of Research of the National Bureau of Standards, Vol. 42, Issue 6
  • DOI: 10.6028/jres.042.049

Lipid domains in bacterial membranes and the action of antimicrobial agents
journal, January 2009

  • Epand, Richard M.; Epand, Raquel F.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1788, Issue 1
  • DOI: 10.1016/j.bbamem.2008.08.023

Structure of transmembrane pore induced by Bax-derived peptide: Evidence for lipidic pores
journal, November 2008

  • Qian, S.; Wang, W.; Yang, L.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 45
  • DOI: 10.1073/pnas.0807764105

Real-time quantitative analysis of lipid disordering by aurein 1.2 during membrane adsorption, destabilisation and lysis
journal, October 2010

  • Lee, Tzong-Hsien; Heng, Christine; Swann, Marcus J.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1798, Issue 10
  • DOI: 10.1016/j.bbamem.2010.06.023

Understanding the Structure and Dynamics of Complex Biomembrane Interactions by Neutron Scattering Techniques
journal, December 2020

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

  • Qian, Shuo; Heller, William T.
  • The Journal of Physical Chemistry B, Vol. 115, Issue 32
  • DOI: 10.1021/jp204045t

Controls and constrains of the membrane disrupting action of Aurein 1.2
journal, November 2015

  • Shahmiri, Mahdi; Enciso, Marta; Mechler, Adam
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep16378

Dimerization of aurein 1.2: effects in structure, antimicrobial activity and aggregation of Cândida albicans cells
journal, March 2013

Interaction of the antimicrobial peptides caerin 1.1 and aurein 1.2 with intact bacteria by 2 H solid-state NMR
journal, December 2016

  • Laadhari, Marwa; Arnold, Alexandre A.; Gravel, Andrée E.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1858, Issue 12
  • DOI: 10.1016/j.bbamem.2016.09.009

The antimicrobial peptide aurein 1.2 disrupts model membranes via the carpet mechanism
journal, January 2012

  • Fernandez, David I.; Le Brun, Anton P.; Whitwell, Thomas C.
  • Physical Chemistry Chemical Physics, Vol. 14, Issue 45
  • DOI: 10.1039/c2cp43099a

Atomic Force Microscopy Study on the Stiffness of Nanosized Liposomes Containing Charged Lipids
journal, June 2018

Dynamics of liposomes in the fluid phase
journal, August 2019

  • Gupta, Sudipta; De Mel, Judith U.; Schneider, Gerald J.
  • Current Opinion in Colloid & Interface Science, Vol. 42
  • DOI: 10.1016/j.cocis.2019.05.003

Amyloid β-Peptide Interaction with Membranes: Can Chaperones Change the Fate?
journal, December 2018

  • Ricci, Caterina; Maccarini, Marco; Falus, Peter
  • The Journal of Physical Chemistry B, Vol. 123, Issue 3
  • DOI: 10.1021/acs.jpcb.8b11719

Beyond structural models for the mode of action: How natural antimicrobial peptides affect lipid transport
journal, January 2021

  • Nielsen, Josefine Eilsø; Bjørnestad, Victoria Ariel; Pipich, Vitaliy
  • Journal of Colloid and Interface Science, Vol. 582
  • DOI: 10.1016/j.jcis.2020.08.094

The in vivo structure of biological membranes and evidence for lipid domains
journal, May 2017

The therapeutic applications of antimicrobial peptides (AMPs): a patent review
journal, December 2016

Design and characterization of new antimicrobial peptides derived from aurein 1.2 with enhanced antibacterial activity
journal, February 2021

Membrane Tension in Negatively Charged Lipid Bilayers in a Buffer under Osmotic Pressure
journal, June 2020

  • Saha, Samiron Kumar; Alam Shibly, Sayed Ul; Yamazaki, Masahito
  • The Journal of Physical Chemistry B, Vol. 124, Issue 27
  • DOI: 10.1021/acs.jpcb.0c03681

The relationship between water vapor absorption and desorption by phospholipids and bilayer phase transitions
journal, February 2007

  • Mansour, Heidi M.; Zografi, George
  • Journal of Pharmaceutical Sciences, Vol. 96, Issue 2
  • DOI: 10.1002/jps.20810

Collective dynamics in lipid membranes containing transmembrane peptides
journal, January 2021

  • Kelley, Elizabeth G.; Butler, Paul D.; Nagao, Michihiro
  • Soft Matter, Vol. 17, Issue 23
  • DOI: 10.1039/D1SM00314C

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

The helix-to-sheet transition of an HIV-1 fusion peptide derivative changes the mechanical properties of lipid bilayer membranes
journal, March 2019

  • Heller, William T.; Zolnierczuk, Piotr A.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1861, Issue 3
  • DOI: 10.1016/j.bbamem.2018.12.004

Chain Packing in the Inverted Hexagonal Phase of Phospholipids:  A Study by X-ray Anomalous Diffraction on Bromine-labeled Chains
journal, March 2006

  • Pan, Deng; Wang, Wangchen; Liu, Wenhan
  • Journal of the American Chemical Society, Vol. 128, Issue 11
  • DOI: 10.1021/ja058045t

Thermal Fluctuation and Elasticity of Lipid Vesicles Interacting with Pore-Forming Peptides
journal, July 2010

Undulations and Dynamic Structure Factor of Membranes
journal, December 1996

Effect of dimerization on the mechanism of action of aurein 1.2
journal, June 2016

  • Lorenzón, E. N.; Riske, K. A.; Troiano, G. F.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1858, Issue 6
  • DOI: 10.1016/j.bbamem.2016.02.010

Efficient data extraction from neutron time-of-flight spin-echo raw data
journal, August 2019

  • Zolnierczuk, P. A.; Holderer, O.; Pasini, S.
  • Journal of Applied Crystallography, Vol. 52, Issue 5
  • DOI: 10.1107/S1600576719010847

Influence of charge density on bilayer bending rigidity in lipid vesicles: A combined dynamic light scattering and neutron spin-echo study
journal, July 2013

Location of hexane in lipid bilayers determined by neutron diffraction
journal, March 1981

  • White, Stephen H.; King, Glen I.; Cain, James E.
  • Nature, Vol. 290, Issue 5802
  • DOI: 10.1038/290161a0

NMR studies of aurein 1.2 analogs
journal, September 2006

  • Li, Xia; Li, Yifeng; Peterkofsky, Alan
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1758, Issue 9
  • DOI: 10.1016/j.bbamem.2006.03.032

The spin-echo spectrometer at the Spallation Neutron Source (SNS)
journal, December 2012

  • Ohl, M.; Monkenbusch, M.; Arend, N.
  • Nuclear Instruments and Methods in Physics Research Section A: Accelerators, Spectrometers, Detectors and Associated Equipment, Vol. 696
  • DOI: 10.1016/j.nima.2012.08.059

Alamethicin influence on the membrane bending elasticity
journal, October 2005

  • Vitkova, Victoria; Méléard, Philippe; Pott, Tanja
  • European Biophysics Journal, Vol. 35, Issue 3
  • DOI: 10.1007/s00249-005-0019-5

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

New insights into water–phospholipid model membrane interactions
journal, May 2004

Distorted Hexagonal Phase Studied by Neutron Diffraction:  Lipid Components Demixed in a Bent Monolayer
journal, January 2005

  • Ding, Lai; Weiss, Thomas M.; Fragneto, Giovanna
  • Langmuir, Vol. 21, Issue 1
  • DOI: 10.1021/la047876u

Entropy-Driven Softening of Fluid Lipid Bilayers by Alamethicin
journal, October 2007

  • Pabst, Georg; Danner, Sabine; Podgornik, Rudi
  • Langmuir, Vol. 23, Issue 23
  • DOI: 10.1021/la701586c

Interpreting Membrane Scattering Experiments at the Mesoscale: The Contribution of Dissipation within the Bilayer
journal, March 2010

A Novel Phase of Compressed Bilayers That Models the Prestalk Transition State of Membrane Fusion
journal, January 2012

Increasing complexity in small-angle X-ray and neutron scattering experiments: from biological membrane mimics to live cells
journal, January 2021

  • Semeraro, Enrico F.; Marx, Lisa; Frewein, Moritz P. K.
  • Soft Matter, Vol. 17, Issue 2
  • DOI: 10.1039/C9SM02352F
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