[en] A mixed phospholipid-cholestrol bilayer, with cholera toxin B (CTB) units attached to the monosialotetrahexosylganglioside (GM1) binding sites in the distal leaflet, was deposited on a Au(111) electrode surface. Polarization modulation infrared reflection absorption spectroscopy (PM-IRRAS) measurements were used to characterize structural and orientational changes in this model biological membrane upon binding CTB and the application of the electrode potential. The data presented in this article show that binding cholera toxin to the membrane leads to an overall increase in the tilt angle of the fatty acid chains; however, the conformation of the bilayer remains relatively constant as indicated by the small decrease in the total number of gauche conformers of acyl tails. In addition, the bound toxin caused a significant decrease in the hydration of the ester group contained within the lipid bilayer. Furthermore, changes in the applied potential had a minimal effect on the overall structure of the membrane. In contrast, our results showed significant voltage-dependent changes in the average orientation of the protein alpha-helices that may correspond to the voltage-gated opening and closing of the central pore that resides within the B subunit of cholera toxin.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Leitch, J. Jay
Brosseau, Christa L.
Roscoe, Sharon G.
Bessonov, Kyrylo ; Université de Liège - ULiège > Dép. d'électric., électron. et informat. (Inst.Montefiore) > Bioinformatique
Dutcher, John R.
Lipkowski, Jacek
Language :
English
Title :
Electrochemical and PM-IRRAS characterization of cholera toxin binding at a model biological membrane.
Publication date :
2013
Journal title :
Langmuir
ISSN :
0743-7463
eISSN :
1520-5827
Publisher :
American Chemical Society, Washington, United States - District of Columbia
Colwell, R.; Anwar, H. Marine Ecosystems and Cholera Hydrobiologia 2001, 460, 141-145
Torgersen, M.; Skretting, G.; Deurs, B.; Sandvig, K. Internalization of Cholera Toxin by Different Endocytic Mechanisms J. Cell Sci. 2001, 114, 3737-3747
Lencer, W.; Saslowsky, D. Raft Trafficking of AB5 Subunit Bacterial Toxins Biochim. Biophys. Acta 2005, 1746, 314-321
Vénien-Bryan, C.; Lenne, P.-F.; Zakri, C.; Renault, A.; Brisson, A.; Legrand, J.-F.; Berge, B. Characterization of the Growth of 2D Protein Crystals on a Lipid Monolayer by Ellipsometry and Rigidity Measurements Coupled to Electron Microscopy Biophys. J. 1998, 74, 2649-2657
Lauer, S.; Goldstein, B.; Nolan, R. L.; Nolan, J. P. Analysis of Cholera Toxin-Ganglioside Interactions by Flow Cytometry Biochemistry. 2002, 41, 1742-1751
Kenworthy, A. K.; Petranova, N.; Edidin, M. High-Resolution FRET Microscopy of Cholera Toxin B-Subunit and GPI-Anchored Proteins in Cell Plasma Membranes Mol. Biol. Cell 2000, 11, 1645-1655
Yuan, C.; Johnston, L. J. Atomic Force Microscopy Studies of Ganglioside GM1 Domains in Phosphatidylcholine and Phosphatidylcholine/Cholesterol Bilayers Biophys. J. 2001, 81, 1059-1069
Forstner, M. B.; Yee, C. K.; Parikh, A. N.; Groves, J. T. Lipid Lateral Mobility and Membrane Phase Structure Modulation by Protein Binding J. Am. Chem. Soc. 2006, 128, 15221-15227
Miller, C. E.; Majewski, J.; Kjær, K.; Weygand, M.; Faller, R.; Satija, S.; Kuhl, T. L. Neutron and X-ray Scattering Studies of Cholera Toxin Interactions with Lipid Monolayers at the Air-Liquid Interface Colloids Surf., B 2005, 40, 159-163
Miller, C. E.; Majewski, J.; Faller, R.; Satija, S.; Kuhl, T. L. Cholera Toxin Assault on Lipid Monolayers Containing Ganglioside GM1 Biophys. J. 2004, 86, 3700-3708
Miller, C. E.; Majewski, J.; Watkins, E. B.; Kuhl, T. L.; Part, I. An X-ray Scattering Study of Cholera Toxin Penetration and Induced Phase Transformations in Lipid Membranes Biophys. J. 2008, 95, 629-640
Krasilnikov, O. V.; Muratkhodjaev, J. N.; Voronov, S. E.; Yezepchuk, Y. V. The Ionic Channels Formed by Cholera Toxin in Planar Bilayer Lipid Membranes Are Entirely Attributable to its B-Subunit Biochim. Biophys. Acta 1991, 1067, 166-170
McCann, J. A.; Mertx, J. A.; Czworkowski, J.; Picking, W. D. The Conformational Changes in Cholera Toxin B Subunit-Gangloside GM1 Complexes are Elicited by Environmental pH and Evoke Changes in Membrane Structure Biochemistry 1991, 36, 9169-9178
Nyquist, R. M.; Eberhardt, A. S.; Silks, L. A., III; Li, Z.; Yang, X.; Swanson, B. I. Characterization of Self-Assembled Monolayers for Biosensor Applications Langmuir 2000, 16, 1793-1800
Sinclair, H. R.; Kemp., F.; de Slegte, J.; Gibson, G. R.; Rastall, R. A. Carbohydrate-Based Anti-Adhesive Inhibition of Vibro Cholerae Toxin Binding to GM1-OS Immobilized into Artificial Planar Lipid Membrane Carbohydr. Res. 2004, 344, 1968-1974
Nullmeier, M.; Koliwer-Brandl, H.; Kelm, S.; Brand, I. Interaction of Siglec Protein with Glycolipids in a Lipid Bilayer Deposited on a Gold Electrode Surface J. Electroanal. Chem. 2010, 649, 177-188
Nullmeier, M.; Koliwer-Brandl, H.; Kelm, S.; Zagel, P.; Koch, K.-W.; Brand, I. Impact of Strong and Weak Lipid-Protein Interactions on the Structure of a Lipid Bilayer on a Gold Electrode Surface ChemPhysChem. 2011, 12, 1066-1079
Zawisza, I.; Bin, X.; Lipkowski, J. Potential-Driven Structural Changes in Langmuir-Blodgett DMPC Bilayers Determined by in Situ Spectroelectrochemical PM IRRAS Langmuir 2007, 23, 5180-5194
Breimer, M. E.; Hansson, G. C.; Karlsson, K.-A.; Larson, G.; Leffler, H. Glycosphingolipid Composition of Epithelial Cells Isolated along the Villus Axis of Small Intestine of a Single Human Individual Glycobiology 2012, 12, 1721-1730
Schuck, S.; Simons, K. Polarized Sorting in Epithelial Cells: Raft Clustering and the Biogenesis of the Apical Membrane J. Cell Sci. 2004, 117, 5955-5964
Spiegel, S.; Blumenthal, R.; Fishman, P. H.; Handler, J. S. Gangliosides Do Not Move from Apical to Basolateral Plasma Membrane in Cultured Epithelial Cells Biochim. Biophys. Acta 1985, 821, 310-318
Torok, Z.; Demel, R. A.; Leenhouts, J. M. de Kruijff, B. Presequence-Mediated Intermembrane Contact Formation and Lipid Flow. A Model Membrane Study Biochemistry 1994, 33, 5589-5594
Zawisza, I.; Bin, X.; Lipkowski, J. Spectroelectrochemical Studies of Bilayers of Phospholipids in Gel and Liquid State on Au(111) Electrode Surface Bioelectrochemistry 2004, 63, 137-147
Richer, J.; Lipkowski, J. Measurement of Physical Adsorption of Organic Species at Solid Electrodes J. Electrochem. Soc. 1986, 133, 121-128
Zamlynny, V.; Zawisza, I.; Lipkowski, J. PM FTIRRAS Studies of Potential Controlled Transformations of a Monolayer and a Bilayer of 4-Pentadecyl Pyridine, a Model Surfactant, Adsorbed on a Au(111) Electrode Surface Langmuir 2003, 19, 132-145
Green, M. J.; Barner, B. J.; Corn, R. M. Real-time Sampling Electronics for Double Modulation Experiments with Fourier Transform Infrared Spectrometers Rev. Sci. Instrum. 1991, 62, 1426-1430
Barner, B. J.; Green, M. J.; Saez, E. I.; Corn, R. M. Polarization Modulation Fourier Transform Infrared Reflectance Measurements of Thin Films and Monolayers at Metal Surfaces Utilizing Real-Time Sampling Electronics Anal. Chem. 1991, 63, 55-60
Buffeteau, T.; Desbat, B.; Blaudez, D.; Turlet, J. M. Calibration Procedure to Derive IRRAS Spectra from PM-IRRAS Spectra Appl. Spectrosc. 2000, 54, 1646-1650
Bin, X.; Lipkowski, J. Electrochemical and PM-IRRAS Studies of the Effect of Cholesterol on the Properties of the Headgroup Region of a DMPC Bilayer Supported at a Au(111) Electrode J. Phys. Chem. B 2006, 110, 26430-26441
Merrit, E. A.; Sarfaty, S.; van der Akker, F.; L'Hoir, C.; Martial, J. A.; Hol, W. G. J. Crystal Structure of Cholera Toxin B-Pentamer Bound to Receptor GM1 Pentasaccharide Protein Sci. 1994, 3, 166-175
Zhang, R. G.; Westbrook, M. L.; Westbrook, E. M.; Scott, D. L.; Otwinowski, Z.; Maulik, P. R.; Reed, R. A.; Shipley, G. G. The 2.4Ǻ Crystal Structure of Cholera Toxin B Subunit Pentamer: Choleragenoid J. Mol. Biol. 1995, 251, 550-562
Hess, B.; Kutzner, C.; Van Der Spoel, D.; Lindahl, E. GROMACS 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation J. Chem. Theory Comput. 2008, 4, 435
Burgess, I.; Li, M.; Horsewell, S.; Szymanski, G.; Lipkowski, J.; Majewski, J.; Satija, S. Electric Field-Driven Transformations of a Supported Model Biological Membrane-an Electrochemical and Neutron Reflectivity Study Biophys. J. 2004, 86, 1763-1776
Spangler, B. D.; Westbrook, E. M. Crystallization of Isoelectrically Homogeneous Cholera Toxin Biochemistry 1989, 28, 1333-1340
Kabir, S. Charge Heterogeneity of Cholera Toxin and its Subunits FEMS Microbiol. Lett. 1986, 37, 155-162
Brosseau, C. L.; Leitch, J.; Bin, X.; Chen, M.; Roscoe, S. G.; Lipkowski, J. Electrochemical and PM-IRRAS a Glycolipid-Containing Biomimetic Membrane Prepared Using Langmuir-Blodgett/Langmuir-Schaefer Deposition Langmuir. 2008, 24, 13058-13067
Lee, D. C.; Durrani, A. A.; Chapman, D. A Difference Infrared Spectroscopy of Gramicidin-A, Alamethicin and Bacteriorhodopisin in Perdeuterated Dimyristol-Phosphatidylcholine Biochim. Biophys. Acta 1984, 766, 49-56
Allara, D. L.; Swalen, J. D. An Infrared Reflection Spectroscopy Study of Oriented Cadmium Arachidate Monolayer Films on Evaporated Silver J. Phys. Chem. 1982, 86, 2700-2704
Umemura, J.; Kamata, T.; Kawai, T.; Takenaka, T. Quantitative Evaluation of Molecular Orientation in Thin Langmuir-Blodgett Films by FT-IR Transmission and Reflection Spectroscopy J. Phys. Chem. 1990, 94, 62-67
Fringeli, U. P. The Structure of Lipids and Proteins Studied by Attenuated Total Reflection (ATR) Infrared Spectroscopy. II. Oriented Layers of a Homologous Series: Phosphatidylethanolamine to Phosphatidylcholine Z. Naturforsch. 1977, 32C, 20-45
Fringeli, U. P.; Günthard, H. H. Infrared Membrane Spectroscopy. In Membrane Spectroscopy; Grell, E., Ed.; Springer-Verlag: New York, 1981; pp 270-332.
Bin, X.; Zawisza, I.; Goddard, J. D.; Lipkowski, J. Electrochemical and PM-IRRAS Studies of the Effect of the Static Electric Field on the Structure of the DMPC Bilayer Supported at a Au(111) Electrode Surface Langmuir 2005, 21, 330-347
Aussenac, F.; Laguerre, M.; Schmitter, J.-M.; Dufourc, E. J. Detailed Structure and Dynamics of Bicelle Phospholipids Using Selectively Deuterated and Perdeuterated Labels. H-2 NMR and Molecular Mechanics Study Langmuir 2003, 19, 10468-10479
Blume, A.; Hübner, W.; Messner, G. Fourier Transform Infrared Spectroscopy of 13C:O Labeled Phospholipids Hydrogen Bonding to Carbonyl Groups Biochemistry 1988, 27, 8239-8249
Hübner, W.; Mantsch, H. H. Orientation of Specifically 13Cî-O Labeled Phosphatidylcholine Multilayers from Polarized attenuated Total Reflection FT-IR Spectroscopy Biophys. J. 1991, 59, 1261-1272
Susi, H.; Byler, D. Resolution-Enhanced Fourier Transform Infrared Spectroscopy of Enzymes Methods Enzymol. 1986, 130, 290-311
Barth, A.; Zscherp, C. What Vibrations Tell Us About Proteins Q. Rev. Biophys. 2002, 35, 369-430
Goormaghtigh, E.; Ruysschaert, J. M.; Raussens, V. Evaluation of the Information Content in Infrared Spectra for Protein Secondary Determination Biophys. J. 2006, 90, 2946-2957
Miura, Y.; Kimura, S.; Imanishi, Y.; Umemura, J. Formation of Oriented Helical Peptide Layers on a Gold Surface Due to the Self-Assembling Properties of Peptides Langmuir 1998, 14, 6935-6940
Tamm, L.; Tatulian, S. A. Infrared Spectroscopy of Proteins and Peptides in Lipid Bilayers Q. Rev. Biophys. 1997, 30, 365-420
Worley, C. G.; Linton, R. W.; Samulski, E. T. Electric-Field-Enhanced Self-Assembly of α-Helical Polypeptides Langmuir 1995, 11, 3805-3810
Gremlich, H. U.; Fringeli, U. P.; Schwyzer, R. Conformational Changes of Adrenocorticotropin Peptides upon Interaction with Lipid Membranes Revealed by Infrared Attenuated Total Reflection Spectroscopy Biochemistry 1983, 22, 4257-4264
Okamura, E.; Umemura, J.; Takenaka, T. Molecular Orientation in Thin Langmuir-Blodgett Films of Dipalmitoylphosphatidylcholine as Studied by FTIR Transmission and Reflection-Absorption Spectroscopy Can. J. Chem. 1991, 69, 1691-1694
Marsh, D.; Müller, M.; Schmitt, F.-J. Orientation of the Infrared Transition Moments for an α-Helix Biophys. J. 2000, 78, 2499-2510
Surewicz, W.; Leddy, J.; Mantsch, H. Structure, Stability and Receptor Interaction of Cholera-Toxin as Studied by Fourier-Transform Infrared Spectroscopy Biochemistry. 1990, 29, 8106-8111
Noda, I.; Dowrey, A. E.; Marcott, C.; Story, G. M.; Ozaki, Y. Generalized Two-Dimensional Correlation Spectroscopy: Theory and Applications Appl. Spectrosc. 2000, 54, 236A-248A
Kong, J. Y. Fourier Transform Infrared Spectroscopic Analysis of Protein Secondary Structures Acta Biochim Biophys Sin. 2007, 39, 549-559
Buffeteau, T.; Le Calvaz, E.; Desbat, B.; Pelletier, I.; Pezolet, M. Quantitative Orientation of α-Helical Polypeptides by Attenuated Total Reflection Infrared Spectroscopy J. Phys. Chem. B. 2001, 105, 1464-1471
Thompson, T. E.; Allietta, M.; Brown, R. E.; Johnson, M. L.; Tillack, T. W. Organization of Ganglioside GM1 in Phosphatidylcholine Bilayers Biochim. Biophys. Acta 1985, 817, 229-237
Mou, J.; Yang, J.; Schao, Z. Atomic Force Microscopy of Cholera Toxin B Oligomer Bound to Bilayers of Biologically Relevant Lipids J. Mol. Biol. 1995, 248, 507-512
