Morphology-induced defects enhance lipid transfer rates

Xia, Yan; Charubin, Kamil; Marquardt, Drew; Heberle, Frederick A.; Katsaras, John; Tian, Jianhui; Cheng, Xiaolin; Liu, Ying; Nieh, Mu -Ping

doi:10.1021/acs.langmuir.6b02099

Title: Morphology-induced defects enhance lipid transfer rates

Journal Article · Thu Aug 25 00:00:00 EDT 2016 · Langmuir

DOI:https://doi.org/10.1021/acs.langmuir.6b02099· OSTI ID:1327689

Xia, Yan ^[1]; Charubin, Kamil ^[1]; Marquardt, Drew ^[2]; Heberle, Frederick A. ^[3]; Katsaras, John ^[3]; Tian, Jianhui ^[3]; Cheng, Xiaolin ^[3]; Liu, Ying ^[1]; Nieh, Mu -Ping ^[1]

Univ. of Connecticut, Storrs, CT (United States)
Univ. of Graz, Graz (Austria); Brock Univ., St. Catharines, ON (Canada)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Molecular transfer between nanoparticles has been considered to have important implications regarding nanoparticle stability. Recently, the interparticle spontaneous lipid transfer rate constant for discoidal bicelles was found to be very different from spherical, unilamellar vesicles (ULVs). Here, we investigate the mechanism responsible for this discrepancy. Analysis of the data indicates that lipid transfer is entropically favorable, but enthalpically unfavorable with an activation energy that is independent of bicelle size and long- to short-chain lipid molar ratio. Moreover, molecular dynamics simulations reveal a lower lipid dissociation energy cost in the vicinity of interfaces (“defects”) induced by the segregation of the long- and short-chain lipids in bicelles; these defects are not present in ULVs. Taken together, these results suggest that the enhanced lipid transfer observed in bicelles arises from interfacial defects as a result of the hydrophobic mismatch between the long- and short-chain lipid species. In conclusion, the observed lipid transfer rate is found to be independent of nanoparticle stability.

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

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1327689

Journal Information:: Langmuir, Vol. 32, Issue 38; ISSN 0743-7463

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 10 works

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References (48)

Membrane transport in the endocytic pathway Gruenberg, Jean; Maxfield, Frederick R. Current Opinion in Cell Biology, Vol. 7, Issue 4 https://doi.org/10.1016/0955-0674(95)80013-1	journal	January 1995
HDL Metabolism and Atheroprotection: Predictive Value of Lipid Transfers Maranhão, Raul C.; Freitas, Fatima R. Advances in Clinical Chemistry https://doi.org/10.1016/B978-0-12-800141-7.00001-2	book	January 2014
START ships lipids across interorganelle space Alpy, Fabien; Tomasetto, Catherine Biochimie, Vol. 96 https://doi.org/10.1016/j.biochi.2013.09.015	journal	January 2014
Structure of LIMP-2 provides functional insights with implications for SR-BI and CD36 Neculai, Dante; Schwake, Michael; Ravichandran, Mani Nature, Vol. 504, Issue 7478 https://doi.org/10.1038/nature12684	journal	October 2013
Effect of Obesity on High-density Lipoprotein Metabolism** Rashid, Shirya; Genest, Jacques Obesity, Vol. 15, Issue 12 https://doi.org/10.1038/oby.2007.342	journal	December 2007
Phosphoinositides: Tiny Lipids With Giant Impact on Cell Regulation Balla, Tamas Physiological Reviews, Vol. 93, Issue 3 https://doi.org/10.1152/physrev.00028.2012	journal	July 2013
The molecular structure of a phosphatidylserine bilayer determined by scattering and molecular dynamics simulations Pan, Jianjun; Cheng, Xiaolin; Monticelli, Luca Soft Matter, Vol. 10, Issue 21 https://doi.org/10.1039/c4sm00066h	journal	January 2014
Bilayer Thickness Mismatch Controls Domain Size in Model Membranes Heberle, Frederick A.; Petruzielo, Robin S.; Pan, Jianjun Journal of the American Chemical Society, Vol. 135, Issue 18 https://doi.org/10.1021/ja3113615	journal	February 2013
The Magic of Bicelles Lights Up Membrane Protein Structure Dürr, Ulrich H. N.; Gildenberg, Melissa; Ramamoorthy, Ayyalusamy Chemical Reviews, Vol. 112, Issue 11 https://doi.org/10.1021/cr300061w	journal	August 2012
Direct Measurement of the Membrane Dipole Field in Bicelles Using Vibrational Stark Effect Spectroscopy Hu, Wenhui; Webb, Lauren J. The Journal of Physical Chemistry Letters, Vol. 2, Issue 15 https://doi.org/10.1021/jz200729a	journal	July 2011
Physicochemical Profiling of Surfactant-Induced Membrane Dynamics in a Cell-Sized Liposome Hamada, Tsutomu; Hagihara, Hideyuki; Morita, Masamune The Journal of Physical Chemistry Letters, Vol. 3, Issue 3 https://doi.org/10.1021/jz2016044	journal	January 2012
Magnetically-oriented phospholipid micelles as a tool for the study of membrane-associated molecules Sanders, Charles R.; Hare, Brian J.; Howard, Kathleen P. Progress in Nuclear Magnetic Resonance Spectroscopy, Vol. 26 https://doi.org/10.1016/0079-6565(94)80012-X	journal	January 1994
Bicelles: a model membrane system for all seasons? Sanders, Charles R.; Prosser, R. Scott Structure, Vol. 6, Issue 10 https://doi.org/10.1016/S0969-2126(98)00123-3	journal	October 1998
Customizing model membranes and samples for NMR spectroscopic studies of complex membrane proteins11This review is dedicated to the fond memory of Professor Gitte Vold of the University of California, San Diego, CA, USA. Sanders, Charles R.; Oxenoid, Kirill Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1508, Issue 1-2 https://doi.org/10.1016/S0005-2736(00)00308-4	journal	November 2000
Bicelles as model membranes for solid- and solution-state NMR studies of membrane peptides and proteins Marcotte, Isabelle; Auger, Mich�le Concepts in Magnetic Resonance Part A, Vol. 24A, Issue 1 https://doi.org/10.1002/cmr.a.20025	journal	January 2005
Bicelles and Other Membrane Mimics: Comparison of Structure, Properties, and Dynamics from MD Simulations Vestergaard, Mikkel; Kraft, Johan F.; Vosegaard, Thomas The Journal of Physical Chemistry B, Vol. 119, Issue 52 https://doi.org/10.1021/acs.jpcb.5b08463	journal	December 2015
Coarse-Grained Model for PEGylated Lipids: Effect of PEGylation on the Size and Shape of Self-Assembled Structures Lee, Hwankyu; Pastor, Richard W. The Journal of Physical Chemistry B, Vol. 115, Issue 24 https://doi.org/10.1021/jp2020148	journal	June 2011
Lipid-based nanodiscs as models for studying mesoscale coalescence – a transport limited case Hu, Andrew; Fan, Tai-Hsi; Katsaras, John Soft Matter, Vol. 10, Issue 28 https://doi.org/10.1039/c3sm51761f	journal	January 2014
A time-resolved study on the interaction of oppositely charged bicelles – implications on the charged lipid exchange kinetics Yang, Po-Wei; Lin, Tsang-Lang; Hu, Yuan Soft Matter, Vol. 11, Issue 11 https://doi.org/10.1039/C4SM02886D	journal	January 2015
Micelle Stabilization via Entropic Repulsion: Balance of Force Directionality and Geometric Packing of Subunit Dong, He; Lund, Reidar; Xu, Ting Biomacromolecules, Vol. 16, Issue 3 https://doi.org/10.1021/bm501659w	journal	January 2015
Effect of the Lipid Chain Melting Transition on the Stability of DSPE-PEG(2000) Micelles Kastantin, Mark; Ananthanarayanan, Badriprasad; Karmali, Priya Langmuir, Vol. 25, Issue 13 https://doi.org/10.1021/la900310k	journal	July 2009
3-Helix Micelles Stabilized by Polymer Springs Dong, He; Shu, Jessica Y.; Dube, Nikhil Journal of the American Chemical Society, Vol. 134, Issue 28 https://doi.org/10.1021/ja3048128	journal	July 2012
Consequences of Nonergodicity in Aqueous Binary PEO−PB Micellar Dispersions Jain, Sumeet; Bates, Frank S. Macromolecules, Vol. 37, Issue 4 https://doi.org/10.1021/ma035467j	journal	February 2004
Molecular Exchange in Diblock Copolymer Micelles: Bimodal Distribution in Core-Block Molecular Weights Lu, J.; Choi, S.; Bates, F. S. ACS Macro Letters, Vol. 1, Issue 8 https://doi.org/10.1021/mz300285x	journal	July 2012
Effects of Nanoparticle Morphology and Acyl Chain Length on Spontaneous Lipid Transfer Rates Xia, Yan; Li, Ming; Charubin, Kamil Langmuir, Vol. 31, Issue 47 https://doi.org/10.1021/acs.langmuir.5b03291	journal	November 2015
Equilibrium Chain Exchange Kinetics of Diblock Copolymer Micelles: Tuning and Logarithmic Relaxation Lund, Reidar; Willner, Lutz; Richter, Dieter Macromolecules, Vol. 39, Issue 13 https://doi.org/10.1021/ma060328y	journal	June 2006
Mechanism of Molecular Exchange in Diblock Copolymer Micelles: Hypersensitivity to Core Chain Length Choi, Soo-Hyung; Lodge, Timothy P.; Bates, Frank S. Physical Review Letters, Vol. 104, Issue 4 https://doi.org/10.1103/PhysRevLett.104.047802	journal	January 2010
Equilibrium exchange kinetics in n-alkyl–PEO polymeric micelles: single exponential relaxation and chain length dependence Zinn, Thomas; Willner, Lutz; Lund, Reidar Soft Matter, Vol. 8, Issue 3 https://doi.org/10.1039/C1SM06809A	journal	January 2012
Determination of Interbilayer and Transbilayer Lipid Transfers by Time-Resolved Small-Angle Neutron Scattering Nakano, Minoru; Fukuda, Masakazu; Kudo, Takayuki Physical Review Letters, Vol. 98, Issue 23 https://doi.org/10.1103/PhysRevLett.98.238101	journal	June 2007
Kinetics of symmetric and asymmetric phospholipid transfer between small sonicated vesicles studied by high-sensitivity differential scanning calorimetry, NMR, electron microscopy, and dynamic light scattering Bayerl, Thomas M.; Schmidt, Christoph F.; Sackmann, Erich Biochemistry, Vol. 27, Issue 16 https://doi.org/10.1021/bi00416a037	journal	August 1988
Hybrid and Nonhybrid Lipids Exert Common Effects on Membrane Raft Size and Morphology Heberle, Frederick A.; Doktorova, Milka; Goh, Shih Lin Journal of the American Chemical Society, Vol. 135, Issue 40 https://doi.org/10.1021/ja407624c	journal	September 2013
Polyelectrolyte solutions: Intrachain and interchain correlations observed by SANS Williams, C. E.; Nierlich, M.; Cotton, J. P. Journal of Polymer Science: Polymer Letters Edition, Vol. 17, Issue 6 https://doi.org/10.1002/pol.1979.130170608	journal	June 1979
Structure factor of a polymer in a complex system by small-angle neutron scattering Benoît, H.; Picot, C.; Benmouna, M. Journal of Polymer Science: Polymer Physics Edition, Vol. 22, Issue 8 https://doi.org/10.1002/pol.1984.180220817	journal	August 1984
GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit Pronk, Sander; Páll, Szilárd; Schulz, Roland Bioinformatics, Vol. 29, Issue 7 https://doi.org/10.1093/bioinformatics/btt055	journal	February 2013
Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types Klauda, Jeffery B.; Venable, Richard M.; Freites, J. Alfredo The Journal of Physical Chemistry B, Vol. 114, Issue 23 https://doi.org/10.1021/jp101759q	journal	June 2010
Structure of fully hydrated bilayer dispersions Nagle, J. F.; Wiener, M. C. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 942, Issue 1 https://doi.org/10.1016/0005-2736(88)90268-4	journal	July 1988
Transbilayer diffusion of phospholipids: dependence on headgroup structure and acyl chain length Homan, Reynold; Pownall, Henry J. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 938, Issue 2 https://doi.org/10.1016/0005-2736(88)90155-1	journal	February 1988
Theory of the kinetics of micellar equilibria and quantitative interpretation of chemical relaxation studies of micellar solutions of ionic surfactants Aniansson, E. A. G.; Wall, S. N.; Almgren, M. The Journal of Physical Chemistry, Vol. 80, Issue 9 https://doi.org/10.1021/j100550a001	journal	April 1976
Kinetics of phosphatidylcholine and lysophosphatidylcholine exchange between unilamellar vesicles McLean, Larry R.; Phillips, Michael C. Biochemistry, Vol. 23, Issue 20 https://doi.org/10.1021/bi00315a017	journal	September 1984
Static and Dynamic Properties of Phospholipid Bilayer Nanodiscs Nakano, Minoru; Fukuda, Masakazu; Kudo, Takayuki Journal of the American Chemical Society, Vol. 131, Issue 23 https://doi.org/10.1021/ja9017013	journal	June 2009
Kinetic pathway of the bilayered-micelle to perforated-lamellae transition Wang, H.; Nieh, M. P.; Hobbie, E. K. Physical Review E, Vol. 67, Issue 6 https://doi.org/10.1103/PhysRevE.67.060902	journal	June 2003
Growth kinetics of lipid-based nanodiscs to unilamellar vesicles—A time-resolved small angle neutron scattering (SANS) study Mahabir, Suanne; Small, Darcy; Li, Ming Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1828, Issue 3 https://doi.org/10.1016/j.bbamem.2012.11.002	journal	March 2013
Concentration-Independent Spontaneously Forming Biomimetric Vesicles Nieh, M. -P.; Harroun, T. A.; Raghunathan, V. A. Physical Review Letters, Vol. 91, Issue 15 https://doi.org/10.1103/PhysRevLett.91.158105	journal	October 2003
Lipid Exchange and Transfer on Nanoparticle Supported Lipid Bilayers: Effect of Defects, Ionic Strength, and Size Drazenovic, Jelena; Ahmed, Selver; Tuzinkiewicz, Nicole-Marie Langmuir, Vol. 31, Issue 2 https://doi.org/10.1021/la503967m	journal	January 2015
The effects of temperature, salinity, concentration and PEGylated lipid on the spontaneous nanostructures of bicellar mixtures Liu, Ying; Li, Ming; Yang, Yongkun Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1838, Issue 7 https://doi.org/10.1016/j.bbamem.2014.02.004	journal	July 2014
Phospholipid phase transitions in homogeneous nanometer scale bilayer discs Shaw, Andrew W.; McLean, Mark A.; Sligar, Stephen G. FEBS Letters, Vol. 556, Issue 1-3, p. 260-264 https://doi.org/10.1016/S0014-5793(03)01400-5	journal	December 2003
Cooperativity of the phase transition in single- and multibilayer lipid vesicles Marsh, D.; Watts, A.; Knowles, P. F. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 465, Issue 3 https://doi.org/10.1016/0005-2736(77)90268-1	journal	March 1977
Effect of Core Crystallization and Conformational Entropy on the Molecular Exchange Kinetics of Polymeric Micelles Zinn, Thomas; Willner, Lutz; Pipich, Vitaliy ACS Macro Letters, Vol. 4, Issue 6 https://doi.org/10.1021/acsmacrolett.5b00197	journal	May 2015

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