Effect of antimicrobial peptide on dynamics of phosphocholine membrane: role of cholesterol and physical state of bilayer

Sharma, Veerendra K.; Mamontov, Eugene; Anunciado, Divina B.; O'Neill, Hugh Michael; Urban, Volker S.

doi:10.1039/C5SM01562F

Title: Effect of antimicrobial peptide on dynamics of phosphocholine membrane: role of cholesterol and physical state of bilayer

Journal Article · Wed Jun 24 00:00:00 EDT 2015 · Soft Matter

DOI:https://doi.org/10.1039/C5SM01562F· OSTI ID:1214022

Sharma, Veerendra K. ^[1]; Mamontov, Eugene ^[2]; Anunciado, Divina B. ^[3]; O'Neill, Hugh Michael ^[3]; Urban, Volker S. ^[3]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biology and Soft Matter Div.; Bhabha Atomic Research Centre (BARC), Mumbai (India). Solid State Physics Div.
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical and Engineering Materials Div.
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biology and Soft Matter Div.

Antimicrobial peptides are universal in all forms of life and are well known for their strong interaction with the cell membrane. This makes them a popular target for investigation of peptide-lipid interactions. Here we report the effect of melittin, an important antimicrobial peptide, on the dynamics of membranes based on 1,2-dimyristoyl-sn-glycero-3-phosphocholine (DMPC) lipid in both the solid gel and fluid phases. To probe the phase transition, elastic neutron intensity temperature scans have been carried out on DMPC-based unilamellar vesicles (ULV) with and without melittin. We have found that addition of a small amount (0.2 mol%) melittin eliminates the steep fall in the elastic intensity at 296 K associated with the solid gel to fluid phase transition, which is observed for pure DMPC vesicles. Quasielastic neutron scattering (QENS) experiments have been carried out on DMPC ULV in the solid gel and fluid phases with and without 0.2 mol % melittin. The data analysis invariably shows the presence of lateral and internal motions of the DMPC molecule. We found that melittin does have a profound effect on the dynamics of lipid molecules, especially on the lateral motion, and affects it in a different way, depending on the phase of the bilayers. In the solid gel phase, it acts as a plasticizer, enhancing the lateral motion of DMPC. However, in the fluid phase it acts as a stiffening agent, restricting the lateral motion of the lipid molecules. These observations are consistent with the mean squared displacements extracted from the elastic intensity temperature scans. Cholesterol is a vital component of eukaryotic membrane, which is a natural target for melittin. To investigate the effect of melittin on vesicles supplemented with cholesterol, QENS experiments have also been carried out on DMPC ULV with 20 mol% cholesterol in the presence and absence of 0.2 mol% melittin. Remarkably, the effects of melittin on the membrane dynamics disappear in the presence of 20 mol % cholesterol. Thus, our measurements indicate that the destabilizing effect of the peptide melittin on membranes can be mitigated by the presence of cholesterol.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Spallation Neutron Source (SNS)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1214022

Journal Information:: Soft Matter, Vol. 11, Issue 11; ISSN 1744-683X

Publisher:: Royal Society of ChemistryCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 56 works

Citation information provided by
Web of Science

References (58)

Diffusion in single supported lipid bilayers studied by quasi-elastic neutron scattering Armstrong, Clare L.; Kaye, Martin D.; Zamponi, Michaela Soft Matter, Vol. 6, Issue 23 https://doi.org/10.1039/c0sm00637h	journal	January 2010
Process of inducing pores in membranes by melittin Lee, M. -T.; Sun, T. -L.; Hung, W. -C. Proceedings of the National Academy of Sciences, Vol. 110, Issue 35 https://doi.org/10.1073/pnas.1307010110	journal	August 2013
Incoherent scattering law for neutron quasi-elastic scattering in liquid crystals Dianoux, A. J.; Volino, F.; Hervet, H. Molecular Physics, Vol. 30, Issue 4 https://doi.org/10.1080/00268977500102721	journal	October 1975
The actions of melittin on membranes Dempsey, Christopher E. Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes, Vol. 1031, Issue 2 https://doi.org/10.1016/0304-4157(90)90006-X	journal	May 1990
Role of lipids in the interaction of antimicrobial peptides with membranes Teixeira, Vitor; Feio, Maria J.; Bastos, Margarida Progress in Lipid Research, Vol. 51, Issue 2 https://doi.org/10.1016/j.plipres.2011.12.005	journal	April 2012
Antimicrobial peptides of multicellular organisms Zasloff, Michael Nature, Vol. 415, Issue 6870 https://doi.org/10.1038/415389a	journal	January 2002
Lipid diffusion in planar membranes investigated by fluorescence correlation spectroscopy Macháň, Radek; Hof, Martin Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1798, Issue 7 https://doi.org/10.1016/j.bbamem.2010.02.014	journal	July 2010
How to study proteins by circular dichroism Kelly, Sharon M.; Jess, Thomas J.; Price, Nicholas C. Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1751, Issue 2 https://doi.org/10.1016/j.bbapap.2005.06.005	journal	August 2005
Melittin: a Membrane-active Peptide with Diverse Functions Raghuraman, H.; Chattopadhyay, Amitabha Bioscience Reports, Vol. 27, Issue 4-5 https://doi.org/10.1007/s10540-006-9030-z	journal	August 2007
Lateral diffusion of lipids in model and natural membranes Tocanne, Jean-François; Dupou-Cézanne, Laurence; Lopez, André Progress in Lipid Research, Vol. 33, Issue 3 https://doi.org/10.1016/0163-7827(94)90027-2	journal	January 1994
Phospholipid Reorientation at the Lipid/Water Interface Measured by High Resolution 31P Field Cycling NMR Spectroscopy Roberts, Mary F.; Redfield, Alfred G.; Mohanty, Udayan Biophysical Journal, Vol. 97, Issue 1 https://doi.org/10.1016/j.bpj.2009.03.057	journal	July 2009
A restatement of melittin-induced effects on the thermotropism of zwitterionic phospholipids Dasseux, Jean-Louis; Faucon, Jean-François; Lafleur, Michael Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 775, Issue 1 https://doi.org/10.1016/0005-2736(84)90232-3	journal	August 1984
The dynamical landscape in CTAB micelles Sharma, V. K.; Mitra, S.; Garcia Sakai, V. Soft Matter, Vol. 8, Issue 27 https://doi.org/10.1039/c2sm25515d	journal	January 2012
Measurement of the Lateral Diffusion of Dipalmitoylphosphatidylcholine Adsorbed on Silica Beads in the Absence and Presence of Melittin: A 31P Two-Dimensional Exchange Solid-State NMR Study Picard, Frédéric; Paquet, Marie-Josée; Dufourc, Érick J. Biophysical Journal, Vol. 74, Issue 2 https://doi.org/10.1016/S0006-3495(98)74009-3	journal	February 1998
Nanosecond lipid dynamics in membranes containing cholesterol Armstrong, Clare L.; Häußler, Wolfgang; Seydel, Tilo Soft Matter, Vol. 10, Issue 15 https://doi.org/10.1039/c3sm51757h	journal	January 2014
Peptide-Induced Asymmetric Distribution of Charged Lipids in a Vesicle Bilayer Revealed by Small-Angle Neutron Scattering Qian, Shuo; Heller, William T. The Journal of Physical Chemistry B, Vol. 115, Issue 32 https://doi.org/10.1021/jp204045t	journal	August 2011
Structural and dynamical details of cholesterol-lipid interaction as revealed by deuterium NMR Dufourc, Erick J.; Parish, Edward J.; Chitrakorn, Sarawanee Biochemistry, Vol. 23, Issue 25 https://doi.org/10.1021/bi00320a025	journal	December 1984
Temperature and Size-Dependence of Membrane Molecular Dynamics in Unilamellar Vesicles by Fast Field-Cycling NMR Relaxometry Perlo, Josefina; Meledandri, Carla J.; Anoardo, Esteban The Journal of Physical Chemistry B, Vol. 115, Issue 13 https://doi.org/10.1021/jp2009034	journal	April 2011
Internal Dynamics in SDS Micelles: Neutron Scattering Study Sharma, V. K.; Mitra, S.; Verma, G. The Journal of Physical Chemistry B, Vol. 114, Issue 51 https://doi.org/10.1021/jp108274y	journal	December 2010
Conformation and aggregation of melittin: dependence of pH and concentration Bello, Jake; Bello, Helene R.; Granados, Edward Biochemistry, Vol. 21, Issue 3 https://doi.org/10.1021/bi00532a007	journal	February 1982
Morphological changes of phosphatidylcholine bilayers induced by melittin: vesicularization, fusion, discoidal particles Dufourcq, Jean; Faucon, Jean-Francois; Fourche, Georges Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 859, Issue 1 https://doi.org/10.1016/0005-2736(86)90315-9	journal	July 1986
Differential scanning calorimetric study of the effect of cholesterol on the thermotropic phase behavior of a homologous series of linear saturated phosphatidylcholines McMullen, Todd P. W.; Lewis, Ruthven N. A. H.; McElhaney, Ronald N. Biochemistry, Vol. 32, Issue 2 https://doi.org/10.1021/bi00053a016	journal	January 1993
Cholesterol as a target for toxins de Kruijff, B. Bioscience Reports, Vol. 10, Issue 2 https://doi.org/10.1007/BF01116571	journal	April 1990
Conformational and segmental dynamics in lipid-based vesicles Gerelli, Yuri; Sakai, Victoria García; Ollivier, Jacques Soft Matter, Vol. 7, Issue 8 https://doi.org/10.1039/c0sm01301c	journal	January 2011
Dynamical Features in Cationic Micelles of Varied Chain Length Sharma, V. K.; Mitra, S.; Sakai, V. Garcia The Journal of Physical Chemistry B, Vol. 116, Issue 30 https://doi.org/10.1021/jp304841a	journal	July 2012
Multi-component modeling of quasielastic neutron scattering from phospholipid membranes Wanderlingh, U.; D’Angelo, G.; Branca, C. The Journal of Chemical Physics, Vol. 140, Issue 17 https://doi.org/10.1063/1.4872167	journal	May 2014
Modulation of Tryptophan Environment in Membrane-Bound Melittin by Negatively Charged Phospholipids: Implications in Membrane Organization and Function ^† Ghosh, Anindya K.; Rukmini, R.; Chattopadhyay, Amitabha Biochemistry, Vol. 36, Issue 47 https://doi.org/10.1021/bi971933j	journal	November 1997
Neutron incoherent scattering law for diffusion in a potential of spherical symmetry: general formalism and application to diffusion inside a sphere Volino, F.; Dianoux, A. J. Molecular Physics, Vol. 41, Issue 2 https://doi.org/10.1080/00268978000102761	journal	October 1980
Membranes are more mosaic than fluid Engelman, Donald M. Nature, Vol. 438, Issue 7068 https://doi.org/10.1038/nature04394	journal	November 2005
Peptide-induced bilayer thinning structure of unilamellar vesicles and the related binding behavior as revealed by X-ray scattering Su, Chun-Jen; Wu, Shiuan-Shiaou; Jeng, U-Ser Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1828, Issue 2 https://doi.org/10.1016/j.bbamem.2012.10.027	journal	February 2013
Cholesterol and the cell membrane Yeagle, Philip L. Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes, Vol. 822, Issue 3-4 https://doi.org/10.1016/0304-4157(85)90011-5	journal	December 1985
A time-of-flight backscattering spectrometer at the Spallation Neutron Source, BASIS Mamontov, E.; Herwig, K. W. Review of Scientific Instruments, Vol. 82, Issue 8 https://doi.org/10.1063/1.3626214	journal	August 2011
Estimation of Protein Secondary Structure from Circular Dichroism Spectra: Comparison of CONTIN, SELCON, and CDSSTR Methods with an Expanded Reference Set Sreerama, Narasimha; Woody, Robert W. Analytical Biochemistry, Vol. 287, Issue 2, p. 252-260 https://doi.org/10.1006/abio.2000.4880	journal	December 2000
Partitioning of ethanol into lipid membranes and its effect on fluidity and permeability as seen by X-ray and neutron scattering Toppozini, Laura; Armstrong, Clare L.; Barrett, Matthew A. Soft Matter, Vol. 8, Issue 47 https://doi.org/10.1039/c2sm26546j	journal	January 2012
DAVE: A Comprehensive Software Suite for the Reduction, Visualization, and Analysis of Low Energy Neutron Spectroscopic Data Azuah, Richard Tumanjong; Kneller, Larry R.; Qiu, Yiming Journal of Research of the National Institute of Standards and Technology, Vol. 114, Issue 6 https://doi.org/10.6028/jres.114.025	journal	November 2009
A Molecular View of Melting in Anhydrous Phospholipidic Membranes Doxastakis, M.; Sakai, V. García; Ohtake, S. Biophysical Journal, Vol. 92, Issue 1 https://doi.org/10.1529/biophysj.106.089631	journal	January 2007
Dynamics in Anionic Micelles: Effect of Phenyl Ring Sharma, V. K.; Mitra, S.; Johnson, M. The Journal of Physical Chemistry B, Vol. 117, Issue 20 https://doi.org/10.1021/jp401831y	journal	May 2013
Structure and Dynamics of Ionic Micelles: MD Simulation and Neutron Scattering Study Aoun, B.; Sharma, V. K.; Pellegrini, E. The Journal of Physical Chemistry B, Vol. 119, Issue 15 https://doi.org/10.1021/acs.jpcb.5b00020	journal	April 2015
Nanoscopic Dynamics of Phospholipid in Unilamellar Vesicles: Effect of Gel to Fluid Phase Transition Sharma, V. K.; Mamontov, E.; Anunciado, D. B. The Journal of Physical Chemistry B, Vol. 119, Issue 12 https://doi.org/10.1021/acs.jpcb.5b00220	journal	March 2015
The membrane-induced structure of melittin is correlated with the fluidity of the lipids Andersson, August; Biverståhl, Henrik; Nordin, Jon Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1768, Issue 1 https://doi.org/10.1016/j.bbamem.2006.07.009	journal	January 2007
Effect of cholesterol on the polymorphism of dipalmitoylphosphatidylcholine/melittin complexes: an NMR study Monette, Martine; Van Calsteren, Marie-Rose; Lafleur, Michel Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1149, Issue 2 https://doi.org/10.1016/0005-2736(93)90217-N	journal	July 1993
Inhibition of a plant virus infection by analogs of melittin. Marcos, J. F.; Beachy, R. N.; Houghten, R. A. Proceedings of the National Academy of Sciences, Vol. 92, Issue 26 https://doi.org/10.1073/pnas.92.26.12466	journal	December 1995
Short range ballistic motion in fluid lipid bilayers studied by quasi-elastic neutron scattering Armstrong, C. L.; Trapp, M.; Peters, J. Soft Matter, Vol. 7, Issue 18 https://doi.org/10.1039/c1sm05691c	journal	January 2011
Morphological Behavior of Lipid Bilayers Induced by Melittin near the Phase Transition Temperature Toraya, Shuichi; Nagao, Takashi; Norisada, Kazushi Biophysical Journal, Vol. 89, Issue 5 https://doi.org/10.1529/biophysj.105.059311	journal	November 2005
Thermal Fluctuation and Elasticity of Lipid Vesicles Interacting with Pore-Forming Peptides Lee, Ji-Hwan; Choi, Sung-Min; Doe, Changwoo Physical Review Letters, Vol. 105, Issue 3 https://doi.org/10.1103/PhysRevLett.105.038101	journal	July 2010
Exploring the effect of cholesterol in lipid bilayer membrane on the melittin penetration mechanism Chen, Liang-Yu; Cheng, Chien-Wei; Lin, Jia-Jia Analytical Biochemistry, Vol. 367, Issue 1 https://doi.org/10.1016/j.ab.2007.04.039	journal	August 2007
The interactions of signal sequences with membranes Golding, C.; O'Shea, P. Biochemical Society Transactions, Vol. 23, Issue 4 https://doi.org/10.1042/bst0230971	journal	November 1995
Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Brogden, Kim A. Nature Reviews Microbiology, Vol. 3, Issue 3 https://doi.org/10.1038/nrmicro1098	journal	March 2005
Small-angle X-ray diffraction studies on the effects of melittin on lipid bilayer assemblies Colotto, A.; Lohner, K.; Laggner, P. Journal of Applied Crystallography, Vol. 24, Issue 5 https://doi.org/10.1107/S0021889891003291	journal	October 1991
Molecular Mechanism of Long-Range Diffusion in Phospholipid Membranes Studied by Quasielastic Neutron Scattering Busch, Sebastian; Smuda, Christoph; Pardo, Luis Carlos Journal of the American Chemical Society, Vol. 132, Issue 10 https://doi.org/10.1021/ja907581s	journal	March 2010
Derivation of Mean-Square Displacements for Protein Dynamics from Elastic Incoherent Neutron Scattering Yi, Zheng; Miao, Yinglong; Baudry, Jerome The Journal of Physical Chemistry B, Vol. 116, Issue 16 https://doi.org/10.1021/jp2102868	journal	April 2012
Energetics of Pore Formation Induced by Membrane Active Peptides ^† Lee, Ming-Tao; Chen, Fang-Yu; Huang, Huey W. Biochemistry, Vol. 43, Issue 12 https://doi.org/10.1021/bi036153r	journal	March 2004
Solution Structure of a Polypeptide from the N Terminus of the HIV Protein Nef Barnham, Kevin J.; Monks, Stephen A.; Hinds, Mark G. Biochemistry, Vol. 36, Issue 20 https://doi.org/10.1021/bi9629945	journal	May 1997
Molecular mechanism of antimicrobial peptides: The origin of cooperativity Huang, Huey W. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1758, Issue 9 https://doi.org/10.1016/j.bbamem.2006.02.001	journal	September 2006
The picosecond dynamics of the phospholipid dimyristoylphosphatidylcholine in mono- and bilayers Busch, Sebastian; Pardo, Luis Carlos; Smuda, Christoph Soft Matter, Vol. 8, Issue 13 https://doi.org/10.1039/c2sm07380c	journal	January 2012
Interaction of Melittin with Membrane Cholesterol: A Fluorescence Approach Raghuraman, H.; Chattopadhyay, Amitabha Biophysical Journal, Vol. 87, Issue 4 https://doi.org/10.1529/biophysj.104.043596	journal	October 2004
Melittin-Induced Bilayer Leakage Depends on Lipid Material Properties: Evidence for Toroidal Pores Allende, Daniel; Simon, S. A.; McIntosh, Thomas J. Biophysical Journal, Vol. 88, Issue 3 https://doi.org/10.1529/biophysj.104.049817	journal	March 2005
Molecular recognition between membrane-spanning polypeptides Shai, Yechiel Trends in Biochemical Sciences, Vol. 20, Issue 11 https://doi.org/10.1016/S0968-0004(00)89101-X	journal	November 1995

Cited By (7)

Side chain dynamics in semiconducting polymer MEH‐PPV Osti, Naresh C.; Mamontov, Eugene; Daemen, Luke Journal of Applied Polymer Science https://doi.org/10.1002/app.47394	journal	December 2018
Deciphering interactions of ionic liquids with biomembrane Sharma, V. K.; Mukhopadhyay, R. Biophysical Reviews, Vol. 10, Issue 3 https://doi.org/10.1007/s12551-018-0410-y	journal	March 2018
Dynamical Transitions and Diffusion Mechanism in DODAB Bilayer Dubey, P. S.; Srinivasan, H.; Sharma, V. K. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-19899-6	journal	January 2018
Nano-viscosimetry analysis of the membrane disrupting action of the bee venom peptide melittin Pandidan, Sara; Mechler, Adam Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-019-47325-y	journal	July 2019
High-resolution neutron spectroscopy using backscattering and neutron spin-echo spectrometers in soft and hard condensed matter Gardner, Jason S.; Ehlers, Georg; Faraone, Antonio Nature Reviews Physics, Vol. 2, Issue 2 https://doi.org/10.1038/s42254-019-0128-1	journal	January 2020
Hydrogel degradation triggered by pH for the smart release of antibiotics to combat bacterial infection Lu, Zhentan; Zhang, Jiaqi; Yu, Zhenguo New Journal of Chemistry, Vol. 41, Issue 2 https://doi.org/10.1039/c6nj03260e	journal	January 2017
Novel Naja atra cardiotoxin 1 (CTX-1) derived antimicrobial peptides with broad spectrum activity Sala, Andrea; Cabassi, Clotilde Silvia; Santospirito, Davide PLOS ONE, Vol. 13, Issue 1 https://doi.org/10.1371/journal.pone.0190778	journal	January 2018

Similar Records

Nanoscopic dynamics of phospholipid in unilamellar vesicles: Effect of gel to fluid phase transition

Journal Article · Wed Mar 04 00:00:00 EST 2015 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1214022

Sharma, V. K.; Mamontov, E.; Anunciado, D. B.; +2 more

Dynamical and phase behavior of a phospholipid membrane altered by an antimicrobial peptide at low concentration

Journal Article · Fri May 27 00:00:00 EDT 2016 · Journal of Physical Chemistry Letters · OSTI ID:1214022

Mamontov, Eugene; Tyagi, M.; Qian, Shuo; +3 more

Effect of α-Tocopherol on the Microscopic Dynamics of Dimyristoylphosphatidylcholine Membrane

Journal Article · Wed Dec 16 00:00:00 EST 2015 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry · OSTI ID:1214022

Sharma, V. K.; Mamontov, E.; Tyagi, M.; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Antimicrobial peptides
Melittin
Neutron scattering
DMPC
Cholesterol

Title: Effect of antimicrobial peptide on dynamics of phosphocholine membrane: role of cholesterol and physical state of bilayer

Citation Formats

References (58)

Cited By (7)

Similar Records

Related Subjects