Confocal Raman Microscopy of Hybrid-Supported Phospholipid Bilayers within Individual C18-Functionalized Chromatographic Particles

Kitt, Jay P.; Harris, Joel M.

doi:10.1021/acs.langmuir.6b02309

Confocal Raman Microscopy of Hybrid-Supported Phospholipid Bilayers within Individual C₁₈-Functionalized Chromatographic Particles

Journal Article · Fri Aug 05 00:00:00 EDT 2016 · Langmuir

DOI:https://doi.org/10.1021/acs.langmuir.6b02309· OSTI ID:2480567

Kitt, Jay P. ^[1]; Harris, Joel M. ^[2]

University of Utah, Salt Lake City, UT (United States); University of Utah
University of Utah, Salt Lake City, UT (United States)

Measuring lipid-membrane partitioning of small molecules is critical to predicting bioavailability and investigating molecule-membrane interactions. A stable model membrane for such studies has been developed through assembly of a phospholipid monolayer on n-alkane-modified surfaces. These hybrid-bilayers have recently been generated within n-alkyl-chain (C₁₈) modified porous silica and used in chromatographic retention studies of small molecules. Despite their successful application, determining the structure of hybrid-bilayers within chromatographic silica is challenging, because they reside at buried interfaces within the porous structure. In this work, we employ confocal Raman microscopy to investigate the formation and temperature-dependent structure of hybrid-phospholipid bilayers in C₁₈-modified, porous-silica chromato¬graphic particles. Porous silica provides sufficient surface area within a confocal probe volume centered in an individual particle to readily measure, with Raman microscopy, the formation of an ordered hybrid-bilayer of 1,2-dimyristoyl-sn-glycero-3-phospho¬choline (DMPC) with the surface C₁₈ chains. The DMPC surface density was quantified from the relative Raman scattering intensities of C₁₈ and phospholipid acyl chains and found to be ~40% of a DMPC vesicle membrane. By monitoring Raman spectra acquired versus temperature, the bilayer main phase transition was observed to be broadened and shifted to higher temperature compared to a DMPC vesicle, in agreement with differential scanning calorimetry (DSC) results. Raman scattering of deuterated phospholipid was resolved from protonated C₁₈-chain scattering, showing that the lipid-acyl and C₁₈ chains melt simultaneously in a single phase transition. The surface-density of lipid in the hybrid bilayer, the ordering of both C₁₈ and lipid acyl chains upon bilayer formation, and decoupling of C₁₈ methylene C–H vibrations by deuterated lipid acyl chains all suggest an interdigitated acyl-chain structure. Furthermore, the simultaneous melting of both layers is also consistent with an interdigitated structure, where immobility of surface-grafted C₁₈-chains decreases the cooperativity and increases the melting temperature compared to a vesicle bilayer.

View Accepted Manuscript (DOE)

Research Organization:: University of Utah, Salt Lake City, UT (United States)

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

Grant/Contract Number:: FG03-93ER14333

OSTI ID:: 2480567

Journal Information:: Langmuir, Journal Name: Langmuir Journal Issue: 35 Vol. 32; ISSN 0743-7463

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (64)

Beiträge zur Optik trüber Medien, speziell kolloidaler Metallösungen Mie, Gustav Annalen der Physik, Vol. 330, Issue 3 https://doi.org/10.1002/andp.19083300302	journal	January 1908
Drug Membrane Interaction and the Importance for Drug Transport, Distribution, Accumulation, Efficacy and Resistance Seydel, Joachim K.; Coats, Eugene A.; Cordes, Hans Peter Archiv der Pharmazie, Vol. 327, Issue 10 https://doi.org/10.1002/ardp.19943271002	journal	January 1994
Confocal Raman microscopy for simultaneous monitoring of partitioning and disordering of tricyclic antidepressants in phospholipid vesicle membranes: Confocal Raman microscopy of tricyclic antidepressants in vesicle membranes Fox, Christopher B.; Harris, Joel M. Journal of Raman Spectroscopy, Vol. 41, Issue 5 https://doi.org/10.1002/jrs.2483	journal	September 2009
Characterization of Flavonoid–Biomembrane Interactions Ollila, Fredrik; Halling, Katrin; Vuorela, Pia Archives of Biochemistry and Biophysics, Vol. 399, Issue 1 https://doi.org/10.1006/abbi.2001.2759	journal	March 2002
Phospholipid/Alkanethiol Bilayers for Cell-Surface Receptor Studies by Surface Plasmon Resonance Plant, A. L.; Brighamburke, M.; Petrella, E. C. Analytical Biochemistry, Vol. 226, Issue 2 https://doi.org/10.1006/abio.1995.1234	journal	April 1995
Membrane Spectroscopy Grell, Ernst Molecular Biology Biochemistry and Biophysics https://doi.org/10.1007/978-3-642-81537-9	book	January 1981
Lipophilicity and Its Relationship with Passive Drug Permeation Liu, Xiangli; Testa, Bernard; Fahr, Alfred Pharmaceutical Research, Vol. 28, Issue 5 https://doi.org/10.1007/s11095-010-0303-7	journal	October 2010
Raman active vibrations in long-chain fatty acids and phospholipid sonicates Lippert, J. L.; Peticolas, W. L. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 282 https://doi.org/10.1016/0005-2736(72)90306-9	journal	September 1972
Evidence for acyl chain trans/gauche isomerization during the thermal pretransition of dipalmitoyl phosphatidylcholine bilayer dispersions Levin, Ira W.; Bush, S. Fowler Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 640, Issue 3 https://doi.org/10.1016/0005-2736(81)90106-1	journal	February 1981
Molecular interaction of aromatic hydrocarbons in lipid monolayers Snart, Ronald S. Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, Vol. 144, Issue 1 https://doi.org/10.1016/0005-2760(67)90072-0	journal	August 1967
Raman spectra and vibrational assignments for dipalmitoyl phosphatidylcholine and structurally related molecules Spiker, Robert C.; Levin, Ira W. Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism, Vol. 388, Issue 3 https://doi.org/10.1016/0005-2760(75)90095-8	journal	June 1975
Studies on lysosomes—X Weissmann, Gerald; Troll, Walter; van Duuren, Benjamin L. Biochemical Pharmacology, Vol. 17, Issue 12 https://doi.org/10.1016/0006-2952(68)90132-9	journal	December 1968
Effect of lateral chain-chain spacing on the Raman spectrum of dipalmitoyl phosphatidylcholine bilayers Cirák, J.; Horváth, L. I. Chemistry and Physics of Lipids, Vol. 49, Issue 3 https://doi.org/10.1016/0009-3084(88)90007-2	journal	December 1988
Application of laser Raman and infrared spectroscopy to the analysis of membrane structure Wallach, Donald F. H.; Verma, Surendra P.; Fookson, Jeffrey Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes, Vol. 559, Issue 2-3 https://doi.org/10.1016/0304-4157(79)90001-7	journal	August 1979
Vibrational spectra in the CH stretching region and the structure of the polymethylene chain Snyder, R. G.; Hsu, S. L.; Krimm, S. Spectrochimica Acta Part A: Molecular Spectroscopy, Vol. 34, Issue 4 https://doi.org/10.1016/0584-8539(78)80167-6	journal	January 1978
Neutron reflection from a dimyristoylphosphatidylcholine monolayer adsorbed on a hydrophobised silicon support Hollinshead, C. M.; Hanna, M.; Barlow, D. J. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1511, Issue 1 https://doi.org/10.1016/S0005-2736(00)00380-1	journal	March 2001
Analysis of antimicrobial peptide interactions with hybrid bilayer membrane systems using surface plasmon resonance Mozsolits, Henriette; Wirth, Hans-Jürgen; Werkmeister, Jerome Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1512, Issue 1 https://doi.org/10.1016/S0005-2736(01)00303-0	journal	May 2001
Structure of Gel Phase DMPC Determined by X-Ray Diffraction Tristram-Nagle, Stephanie; Liu, Yufeng; Legleiter, Justin Biophysical Journal, Vol. 83, Issue 6 https://doi.org/10.1016/S0006-3495(02)75333-2	journal	December 2002
Deuterated phospholipids as nonperturbing components for Raman studies of biomembranes Gaber, B. P.; Yager, P.; Peticolas, W. L. Biophysical Journal, Vol. 22, Issue 2 https://doi.org/10.1016/S0006-3495(78)85484-8	journal	May 1978
Interpretation of biomembrane structure by Raman difference spectroscopy. Nature of the endothermic transitions in phosphatidylcholines Gaber, B. P.; Yager, P.; Peticolas, W. L. Biophysical Journal, Vol. 21, Issue 2 https://doi.org/10.1016/S0006-3495(78)85516-7	journal	February 1978
Hybrid Bilayer Membranes in Air and Water: Infrared Spectroscopy and Neutron Reflectivity Studies Meuse, Curtis W.; Krueger, Susan; Majkrzak, Charles F. Biophysical Journal, Vol. 74, Issue 3 https://doi.org/10.1016/S0006-3495(98)77851-8	journal	March 1998
Characterization of dynamically prepared phospholipid-modified reversed-phase columns Tsirkin, Irena; Grushka, Eli Journal of Chromatography A, Vol. 919, Issue 2 https://doi.org/10.1016/S0021-9673(01)00824-X	journal	June 2001
Noncovalent immobilized artificial membrane chromatography, an improved method for describing peptide–lipid bilayer interactions Krause, Eberhard; Dathe, Margitta; Wieprecht, Torsten Journal of Chromatography A, Vol. 849, Issue 1 https://doi.org/10.1016/S0021-9673(99)00528-2	journal	July 1999
Studying the length of trans conformational sequences in polyethylene using Raman spectroscopy: a computational study Meier, Robert J. Polymer, Vol. 43, Issue 2 https://doi.org/10.1016/S0032-3861(01)00416-5	journal	January 2002
Immobilized liposome and biomembrane partitioning chromatography of drugs for prediction of drug transport Beigi, Farideh; Gottschalk, Ingo; Lagerquist Hägglund, Christine International Journal of Pharmaceutics, Vol. 164, Issue 1-2 https://doi.org/10.1016/S0378-5173(97)00398-0	journal	April 1998
Effects of non-steroid anti-inflammatory drugs in membrane bilayers Kyrikou, I.; Hadjikakou, S. K.; Kovala-Demertzi, D. Chemistry and Physics of Lipids, Vol. 132, Issue 2 https://doi.org/10.1016/j.chemphyslip.2004.06.005	journal	December 2004
The phase transition behavior of 1,2-dipalmitoyl-sn-glycero-3-phosphocholine (DPPC) model membrane influenced by 2,4-dichlorophenol—an FT-Raman Spectroscopy Study Csiszár, Agnes; Koglin, Eckhard; Meier, Robert J. Chemistry and Physics of Lipids, Vol. 139, Issue 2 https://doi.org/10.1016/j.chemphyslip.2005.11.005	journal	February 2006
Characterization of hybrid bilayer membranes on silver electrodes as biocompatible SERS substrates to study membrane–protein interactions Millo, Diego; Bonifacio, Alois; Moncelli, Maria Rosa Colloids and Surfaces B: Biointerfaces, Vol. 81, Issue 1 https://doi.org/10.1016/j.colsurfb.2010.07.010	journal	November 2010
Confocal Raman Microscopy for Monitoring Chemical Reactions on Single Optically Trapped, Solid-Phase Support Particles Houlne, Michael P.; Sjostrom, Christopher M.; Uibel, Rory H. Analytical Chemistry, Vol. 74, Issue 17 https://doi.org/10.1021/ac020325t	journal	July 2002
Structure−Function Relationships in High-Density Octadecylsilane Stationary Phases by Raman Spectroscopy. 1. Effects of Temperature, Surface Coverage, and Preparation Procedure Ducey,, Michael W.; Orendorff, Christopher J.; Pemberton, Jeanne E. Analytical Chemistry, Vol. 74, Issue 21 https://doi.org/10.1021/ac0203488	journal	October 2002
Optical-Trapping Raman Microscopy Detection of Single Unilamellar Lipid Vesicles Cherney, Daniel P.; Conboy, John C.; Harris, Joel M. Analytical Chemistry, Vol. 75, Issue 23 https://doi.org/10.1021/ac034838r	journal	December 2003
Optical Trapping of Unilamellar Phospholipid Vesicles: Investigation of the Effect of Optical Forces on the Lipid Membrane Shape by Confocal-Raman Microscopy Cherney, Daniel P.; Bridges, Travis E.; Harris, Joel M. Analytical Chemistry, Vol. 76, Issue 17 https://doi.org/10.1021/ac0492620	journal	September 2004
Quantitative Confocal Raman Microscopy Study of Ion-Interaction Retention at Reversed-Phase Chromatographic Interfaces Gasser-Ramirez, Jennifer L.; Harris, Joel M. Analytical Chemistry, Vol. 82, Issue 13 https://doi.org/10.1021/ac100781p	journal	June 2010
Confocal Raman Microscopy for in Situ Detection of Solid-Phase Extraction of Pyrene into Single C ₁₈ –Silica Particles Kitt, Jay P.; Harris, Joel M. Analytical Chemistry, Vol. 86, Issue 3 https://doi.org/10.1021/ac403514r	journal	January 2014
Confocal Raman Microscopy Investigation of the Wetting of Reversed-Phase Liquid Chromatographic Stationary Phase Particles Gasser-Ramirez, Jennifer L.; Harris, Joel M. Analytical Chemistry, Vol. 81, Issue 18 https://doi.org/10.1021/ac901037d	journal	August 2009
Confocal Raman Microscopy for in Situ Measurement of Octanol–Water Partitioning within the Pores of Individual C ₁₈ -Functionalized Chromatographic Particles Kitt, Jay P.; Harris, Joel M. Analytical Chemistry, Vol. 87, Issue 10 https://doi.org/10.1021/acs.analchem.5b00634	journal	May 2015
Direct determination by Raman scattering of the conformation of the choline group in phospholipid bilayers Akutsu, Hideo Biochemistry, Vol. 20, Issue 26 https://doi.org/10.1021/bi00529a006	journal	December 1981
Hydrocarbon chain trans-gauche isomerization in phospholipid bilayer gel assemblies Yellin, Nehama; Levin, Ira W. Biochemistry, Vol. 16, Issue 4 https://doi.org/10.1021/bi00623a014	journal	February 1977
Temperature Dependence of Polypeptide Partitioning between Water and Phospholipid Bilayers Russell, Charles J.; Thorgeirsson, Thorgeir Elís; Shin, Yeon-Kyun Biochemistry, Vol. 35, Issue 29 https://doi.org/10.1021/bi960614+	journal	January 1996
Carbon-hydrogen stretching modes and the structure of n-alkyl chains. 1. Long, disordered chains Snyder, R. G.; Strauss, H. L.; Elliger, C. A. The Journal of Physical Chemistry, Vol. 86, Issue 26 https://doi.org/10.1021/j100223a018	journal	December 1982
Deuterium isotope effect on the stability of molecules: phospholipids Guard-Friar, Deborah; Chen, Chang Hwei; Engle, Adam S. The Journal of Physical Chemistry, Vol. 89, Issue 9 https://doi.org/10.1021/j100255a054	journal	April 1985
Carbon-hydrogen stretching modes and the structure of n-alkyl chains. 2. Long, all-trans chains MacPhail, R. A.; Strauss, H. L.; Snyder, R. G. The Journal of Physical Chemistry, Vol. 88, Issue 3 https://doi.org/10.1021/j150647a002	journal	February 1984
Quantitative Correlation of Raman Spectral Indicators in Determining Conformational Order in Alkyl Chains Orendorff, Christopher J.; Ducey, Michael W.; Pemberton, Jeanne E. The Journal of Physical Chemistry A, Vol. 106, Issue 30 https://doi.org/10.1021/jp014311n	journal	July 2002
Detecting Phase Transitions in Phosphatidylcholine Vesicles by Raman Microscopy and Self-Modeling Curve Resolution Fox, Christopher B.; Uibel, Rory H.; Harris, Joel M. The Journal of Physical Chemistry B, Vol. 111, Issue 39 https://doi.org/10.1021/jp0735886	journal	October 2007
Self-assembled phospholipid/alkanethiol biomimetic bilayers on gold Plant, Anne L. Langmuir, Vol. 9, Issue 11 https://doi.org/10.1021/la00035a004	journal	November 1993
Infrared Spectroscopic Characterization of Lipid−Alkylsiloxane Hybrid Bilayer Membranes at Oxide Substrates Parikh, Atul N.; Beers, Jaime D.; Shreve, Andrew P. Langmuir, Vol. 15, Issue 16 https://doi.org/10.1021/la9813679	journal	July 1999
Synthetic Lecithin Monolayers on Hydrophobized Silica Supports Interdigitate with the Surface-Attached Alkyl Chains under Gel Phase Conditions Käsbauer, M.; Bayerl, T. M. Langmuir, Vol. 15, Issue 7 https://doi.org/10.1021/la981500x	journal	March 1999
Supported Hybrid Bilayer Membranes as Rugged Cell Membrane Mimics Plant, Anne L. Langmuir, Vol. 15, Issue 15 https://doi.org/10.1021/la981662t	journal	July 1999
Real-time monitoring of lipid transfer between vesicles and hybrid bilayers on Au nanoshells using surface enhanced Raman scattering (SERS) Kundu, Janardan; Levin, Carly S.; Halas, Naomi J. Nanoscale, Vol. 1, Issue 1 https://doi.org/10.1039/b9nr00063a	journal	January 2009
Exchange dephasing and motional narrowing of vibrational modes Abbott, Richard J.; Oxtoby, David W. The Journal of Chemical Physics, Vol. 70, Issue 10 https://doi.org/10.1063/1.437257	journal	May 1979
Vibrational spectra and carbon–hydrogen stretching mode assignments for a series of n-alkyl carboxylic acids Hill, Ian R.; Levin, Ira W. The Journal of Chemical Physics, Vol. 70, Issue 2 https://doi.org/10.1063/1.437517	journal	January 1979
Effect of anesthetics and pressure on the thermotropic behavior of multilamellar dipalmitoylphosphatidylcholine liposomes. Mountcastle, D. B.; Biltonen, R. L.; Halsey, M. J. Proceedings of the National Academy of Sciences, Vol. 75, Issue 10 https://doi.org/10.1073/pnas.75.10.4906	journal	October 1978
A scanning calorimetric study of small molecule-lipid bilayer mixtures. Sturtevant, J. M. Proceedings of the National Academy of Sciences, Vol. 79, Issue 13 https://doi.org/10.1073/pnas.79.13.3963	journal	July 1982
Self Modeling Curve Resolution Lawton, William H.; Sylvestre, Edward A. Technometrics, Vol. 13, Issue 3 https://doi.org/10.1080/00401706.1971.10488823	journal	August 1971
Vibrational Spectroscopy of Biomembranes Schultz, Zachary D.; Levin, Ira W. Annual Review of Analytical Chemistry, Vol. 4, Issue 1 https://doi.org/10.1146/annurev-anchem-061010-114048	journal	July 2011
Raman Spectroscopy of Thermotropic and High-Pressure Phases of Aqueous Phospholipid Dispersions Wong, P. T. T. Annual Review of Biophysics and Bioengineering, Vol. 13, Issue 1 https://doi.org/10.1146/annurev.bb.13.060184.000245	journal	June 1984
Theory of the Main Lipid Bilayer Phase Transition Nagle, J. F. Annual Review of Physical Chemistry, Vol. 31, Issue 1 https://doi.org/10.1146/annurev.pc.31.100180.001105	journal	October 1980
Biochemical Applications of Differential Scanning Calorimetry Sturtevant, J. M. Annual Review of Physical Chemistry, Vol. 38, Issue 1 https://doi.org/10.1146/annurev.pc.38.100187.002335	journal	October 1987
Calorimetry-Derived Composition Vectors to Resolve Component Raman Spectra in Phospholipid Phase Transitions Kitt, Jay P.; Bryce, David A.; Harris, Joel M. Applied Spectroscopy, Vol. 70, Issue 7 https://doi.org/10.1177/0003702816652359	journal	June 2016
Temperature-Controlled Confocal Raman Microscopy to Detect Phase Transitions in Phospholipid Vesicles Fox, Christopher B.; Myers, Grant A.; Harris, Joel M. Applied Spectroscopy, Vol. 61, Issue 5 https://doi.org/10.1366/000370207780807786	journal	May 2007
Confocal Raman Microspectroscopy Using a Stigmatic Spectrograph and CCD Detector Williams, K. P. J.; Pitt, G. D.; Batchelder, D. N. Applied Spectroscopy, Vol. 48, Issue 2 https://doi.org/10.1366/0003702944028407	journal	February 1994
Spatial Filtering of a Diode Laser Beam for Confocal Raman Microscopy Kitt, Jay P.; Bryce, David A.; Harris, Joel M. Applied Spectroscopy, Vol. 69, Issue 4 https://doi.org/10.1366/14-07671	journal	April 2015
Lipid Microdomain Formation: Characterization by Infrared Spectroscopy and Ultrasonic Velocimetry Schultz, Zachary D.; Levin, Ira W. Biophysical Journal, Vol. 94, Issue 8 https://doi.org/10.1529/biophysj.107.119735	journal	April 2008
Biomembrane models and drug-biomembrane interaction studies: Involvement in drug design and development Pignatello, R.; Musumeci, T.; Basile, L. Journal of Pharmacy and Bioallied Sciences, Vol. 3, Issue 1 https://doi.org/10.4103/0975-7406.76461	journal	January 2011

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36 MATERIALS SCIENCE
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
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Confocal Raman Microscopy of Hybrid-Supported Phospholipid Bilayers within Individual C18-Functionalized Chromatographic Particles

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Confocal Raman Microscopy of Hybrid-Supported Phospholipid Bilayers within Individual C₁₈-Functionalized Chromatographic Particles