Formation and characterization of supported lipid bilayers containing phosphatidylinositol-4,5-bisphosphate and cholesterol as functional surfaces

Langmuir

Volumn 30, Issue 49, 2014, Pages 14877-14886

  Drücker, Patrick ^a   Grill, David ^a   Gerke, Volker ^a   Galla, Hans Joachim ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC FORCE MICROSCOPY; BIOCHEMISTRY; CHOLESTEROL; CRYSTALS; CYTOLOGY; MIXTURES; PHASE SEPARATION; PROTEINS; QUARTZ; QUARTZ CRYSTAL MICROBALANCES;

BIOPHYSICAL PROPERTIES; FUNCTIONAL SURFACES; LIPID-PROTEIN INTERACTIONS; LONG TERM STABILITY; NEGATIVELY CHARGED; PHOSPHATIDYLINOSITOL; SOLID SUPPORTED LIPID BILAYERS; SUPPORTED LIPID BILAYERS;

LIPID BILAYERS;

CHOLESTEROL; LIPID BILAYER; PHOSPHATIDYLINOSITOL;

ATOMIC FORCE MICROSCOPY; BIOLOGICAL MODEL; CHEMISTRY; LIPID BILAYER;

CHOLESTEROL; LIPID BILAYERS; MICROSCOPY, ATOMIC FORCE; MODELS, BIOLOGICAL; PHOSPHATIDYLINOSITOLS;

EID: 84918811036     PISSN: 07437463     EISSN: 15205827     Source Type: Journal    
DOI: 10.1021/la503203a     Document Type: Article

References (61)

1. Lingwood, D.; Simons, K. Lipid rafts as a membrane-organizing principle. Science 2010, 327, 46-50.
2. Ross, M.; Steinem, C.; Galla, H.-J.; Janshoff, A. Visualization of chemical and physical properties of calcium-induced domains in DPPC/DPPS Langmuir-Blodgett layers. Langmuir 2001, 17, 2437-2445.
3. Simons, K.; Ikonen, E. Functional rafts in cell membranes. Nature 1997, 387, 569-572.
4. Menke, M.; Gerke, V.; Steinem, C. Phosphatidylserine membrane domain clustering induced by Annexin A2/S100A10 heterotetramer. Biochemistry 2005, 44, 15296-15303.
5. Drücker, P.; Pejic, M.; Galla, H.-J.; Gerke, V. Lipid segregation and membrane budding induced by the peripheral membrane binding protein Annexin A2. J. Biol. Chem. 2013, 288, 24764-24776.
6. Kiessling, V.; Wan, C.; Tamm, L. K. Domain coupling in asymmetric lipid bilayers. Biochim. Biophys. Acta 2009, 1788, 64-71.
7. van Meer, G.; Voelker, D. R.; Feigenson, G. W. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 2008, 9, 112-124.
8. Maxfield, F. R.; Tabas, I. Role of cholesterol and lipid organization in disease. Nature 2005, 438, 612-621.
9. McMullen, T. P. W.; Lewis, R. N. A. H.; McElhaney, R. N. Cholesterol-phospholipid interactions, the liquid-ordered phase and lipid rafts in model and biological membranes. Curr. Opin. Colloid Interface Sci. 2004, 8, 459-468.
10. Jiang, Z.; Redfern, R. E.; Isler, Y.; Ross, A. H.; Gericke, A. Cholesterol stabilizes fluid phosphoinositide domains. Chem. Phys. Lipids 2014, 182, 52-61.
11. Delage, E.; Puyaubert, J.; Zachowski, A.; Ruelland, E. Signal transduction pathways involving phosphatidylinositol 4-phosphate and phosphatidylinositol 4,5-bisphosphate: Convergences and divergences among eukaryotic kingdoms. Prog. Lipid Res. 2013, 52, 1-14.
12. 2 and proteins: Interactions, organization, and information flow. Annu. Rev. Biophys. Biomater. 2002, 31, 151-175.
13. Baumann, M.; Amstad, E.; Mashaghi, A.; Textor, M.; Reimhult, E. Characterization of supported lipid bilayers incorporating and phosphoinositol-3,4,5-triphosphate by complementary techniques. Biointerphases 2010, 5, 114-119.
14. Braunger, J. A.; Kramer, C.; Morick, D.; Steinem, C. Solid supported membranes doped with PIP2: Influence of ionic strength and pH on bilayer formation and membrane organization. Langmuir 2013, 29, 14204-14213.
15. Richter, R. P.; Bérat, R.; Brisson, A. R. Formation of solid-supported lipid bilayers: An integrated view. Langmuir 2006, 22, 3497-3505.
16. Richter, R.; Mukhopadhyay, A.; Brisson, A. Pathways of lipid vesicle deposition on solid surfaces: A combined QCM-D and AFM study. Biophys. J. 2003, 85, 3035-3047.
17. El Kirat, K.; Morandat, S.; Dufrêne, Y. F. Nanoscale analysis of supported lipid bilayers using atomic force microscopy. Biochim. Biophys. Acta 2010, 1798, 750-765.
18. Wang, J.; Gambhir, A.; Hangyás-Mihályné, G.; Murray, D.; Golebiewska, U.; McLaughlin, S. Lateral sequestration of phosphatidylinositol 4,5-bisphosphate by the basic effector domain of myristoylated alanine-rich C kinase substrate is due to nonspecific electrostatic interactions. J. Biol. Chem. 2002, 277, 34401-34412.
19. Urban, M.; Kleefen, A.; Mukherjee, N.; Seelheim, P.; Windschiegl, B.; Vor der Brüggen, M.; Koc¸er, A.; Tampé, R. Highly parallel transport recordings on a membrane-on-nanopore chip at single molecule resolution. Nano Lett. 2014, 14, 1674-1680.
20. Reimhult, E.; Kumar, K. Membrane biosensor platforms using nano-and microporous supports. Trends Biotechnol. 2008, 26, 82-89.
21. Rydberg, H.; Kunze, A.; Carlsson, N.; Altgärde, N.; Svedhem, S.; Nordén, B. Peptide-membrane interactions of arginine-tryptophan peptides probed using quartz crystal microbalance with dissipation monitoring. Eur. Biophys J. 2014, 43, 241-253.
22. Tamm, L. K. Lateral membrane diffusion corralled. Biophys. J. 2013, 104, 1399-1400.
23. 2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 2005, 6, 449-461.
24. Zhuang, T.; Tamm, L. K. Control of the conductance of engineered protein nanopores through concerted loop motions. Angew. Chem., Int. Ed. 2014, 53, 5897-5902.
25. Castellana, E. T.; Cremer, P. S. Solid supported lipid bilayers: From biophysical studies to sensor design. Surf. Sci. Rep. 2006, 61, 429-444.
26. Kunze, A.; Zhao, F.; Marel, A.-K.; Svedhem, S.; Kasemo, B. Ion-mediated changes of supported lipid bilayers and their coupling to the substrate. A case of bilayer slip? Soft Matter 2011, 7, 8582-8591.
27. 2+-dependent binding and activation of dormant ezrin by dimeric S100P. Mol. Biol. Cell 2003, 14, 2372-2384.
28. 2: Dependence on vesicle size. J. Chem. Phys. 2002, 117, 7401-7404.
29. Sauerbrey, G. Verwendung von Schwingquarzen zur Wägung dünner Schichten und zur Mikrowägung. Z. Phys. A 1959, 155, 206-222.
30. Janshoff, A.; Galla, H.-J.; Steinem, C. Piezoelectric mass-sensing devices as biosensors-An alternative to optical biosensors? Angew. Chem., Int. Ed. 2000, 39, 4004-4032.
31. Fatisson, J.; Azari, F.; Tufenkji, N. Real-time QCM-D monitoring of cellular responses to different cytomorphic agents. Biosens. Bioelectron. 2011, 26, 3207-3212.
32. Graber, Z. T.; Gericke, A.; Kooijman, E. E. Phosphatidylinositol-4,5-bisphosphate ionization in the presence of cholesterol, calcium or magnesium ions. Chem. Phys. Lipids 2014, 182, 62-72.
33. Graber, Z. T.; Jiang, Z.; Gericke, A.; Kooijman, E. E. Phosphatidylinositol-4,5-bisphosphate ionization and domain formation in the presence of lipids with hydrogen bond donor capabilities. Chem. Phys. Lipids 2012, 165, 696-704.
34. Richter, R. P.; Brisson, A. R. Following the formation of supported lipid bilayers on mica: A study combining AFM, QCM-D, and Ellipsometry. Biophys. J. 2005, 88, 3422-3433.
35. Keller, C. A.; Kasemo, B. Surface specific kinetics of lipid vesicle adsorption measured with a Quartz Crystal Microbalance. Biophys. J. 1998, 75, 1397-1402.
36. Richter, R. P.; Brisson, A. QCM-D on Mica for parallel QCM-D AFM studies. Langmuir 2004, 20, 4609-4613.
37. Ohvo-Rekilä, H.; Ramstedt, B.; Leppimäki, P.; Peter Slotte, J. Cholesterol interactions with phospholipids in membranes. Prog. Lipid Res. 2002, 41, 66-97.
38. Simons, K.; Sampaio, J. L. Membrane organization and lipid rafts. Cold Spring Harb. Perspect. Biol. 2011, 3, a004697.
39. Höök, F.; Rodahl, M.; Brzezinski, P.; Kasemo, B. Energy dissipation kinetics for protein and antibody-antigen adsorption under shear oscillation on a quartz crystal microbalance. Langmuir 1998, 14, 729-734.
40. Höök, F. Development of a Novel QCM Technique for Protein Adsorption Studies. Ph.D. Dissertation, Calmers University of Technology and Göteborg University, December 16, 1997.
41. Kant, R.; Singh, M. B. Generalization of the Gouy-Chapman-Stern model of an electric double layer for a morphologically complex electrode: Deterministic and stochastic morphologies. Phys. Rev. E 2013, 88, 052303.
42. Van der Heyden, F. H. J.; Bonthuis, D. J.; Stein, D.; Meyer, C.; Dekker, C. Electrokinetic energy conversion efficiency in nanofluidic channels. Nano Lett. 2006, 6, 2232-2237.
43. Reimhult, E.; Höök, F.; Kasemo, B. Intact vesicle adsorption and supported biomembrane formation from vesicles in solution: Influence of surface chemistry, vesicle size, temperature and osmotic pressure. Langmuir 2002, 19, 1681-1691.
44. Seeger, H. M.; Cerbo, A. D.; Alessandrini, A.; Facci, P. Supported lipid bilayers on mica and silicon oxide: Comparison of the main phase transition behavior. J. Phys. Chem. B 2010, 114, 8926-8933.
45. Leonenko, Z.; Cramb, D. T.; Amrein, M.; Finot, E. Atomic Force Microscopy: Interaction Forces Measured in Phospholipid Monolayers, Bilayers and Cell Membranes; Tomitori, M., Bhushan, B., Fuchs, H., Eds.; Springer: Berlin, 2008; pp 207-234.
46. Butt, H.-J.; Cappella, B.; Kappl, M. Force measurements with the atomic force microscope: Technique, interpretation and applications. Surf. Sci. Rep. 2005, 59, 1-152.
47. Pera, I.; Stark, R.; Kappl, M.; Butt, H.-J.; Benfenati, F. Using the Atomic Force Microscope to study the interaction between two solid supported lipid bilayers and the influence of Synapsin I. Biophys. J. 2004, 87, 2446-2455.
48. Canale, C.; Jacono, M.; Diaspro, A.; Dante, S. Force spectroscopy as a tool to investigate the properties of supported lipid membranes. Microsc. Res. Tech. 2010, 73, 965-972.
49. Drücker, P.; Pejic, M.; Grill, D.; Galla, H. J.; Gerke, V. Cooperative binding of annexin A2 to cholesterol-and phosphatidylinositol-4,5-bisphosphate-containing bilayers. Biophys. J. 2014, 107, 2070-2081.
50. Levental, I.; Christian, D. A.; Wang, Y.-H.; Madara, J. J.; Discher, D. E.; Janmey, P. A. Calcium-dependent lateral organization in phosphatidylinositol 4,5-bisphosphate (PIP2)-and cholesterol-containing monolayers. Biochemistry 2009, 48, 8241-8248.
51. Wang, Y.-H.; Collins, A.; Guo, L.; Smith-Dupont, K. B.; Gai, F.; Svitkina, T.; Janmey, P. A. Divalent cation induced cluster formation by polyphosphoinositides in model membranes. J. Am. Chem. Soc. 2012, 134, 3387-3395.
52. Salvemini, I. L.; Gau, D. M.; Reid, J.; Bagatolli, L. A.; Macmillan, A.; Moens, P. D. J. Low PIP2 molar fractions induce nanometer size clustering in giant unilamellar vesicles. Chem. Phys. Lipids 2014, 177, 51-63.
53. Ngwa, W.; Chen, K.; Sahgal, A.; Stepanov, E. V.; Luo, W. Nanoscale mechanics of solid-supported multilayered lipid films by force measurement. Thin Solid Films 2008, 516, 5039-5045.
54. Glazier, S. A.; Vanderah, D. J.; Plant, A. L.; Bayley, H.; Valincius, G.; Kasianowicz, J. J. Reconstitution of the pore-forming toxin α-Hemolysin in phospholipid/18-octadecyl-1-thiahexa(ethylene oxide) and phospholipid/n-octadecanethiol supported bilayer membranes. Langmuir 2000, 16, 10428-10435.
55. Maniti, O.; Khalifat, N.; Goggia, K.; Dalonneau, F.; Guérin, C.; Blanchoin, L.; Ramos, L.; Picart, C. Binding of moesin and ezrin to membranes containing phosphatidylinositol (4,5) bisphosphate: A comparative study of the affinity constants and conformational changes. Biochim. Biophys. Acta 2012, 1818, 2839-2849.
56. Bosk, S.; Braunger, J. A.; Gerke, V.; Steinem, C. Activation of F-actin binding capacity of Ezrin: Synergism of PIP2 interaction and phosphorylation. Biophys. J. 2011, 100, 1708-1717.
57. 2-containing membranes. Biochemistry 2006, 45, 13025-13034.
58. Höök, F.; Rodahl, M.; Kasemo, B.; Brzezinski, P. Structural changes in hemoglobin during adsorption to solid surfaces: Effects of pH, ionic strength, and ligand binding. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 12271-12276.
59. Contreras, F. X.; Sánchez-Magraner, L.; Alonso, A.; Goñi, F. M. Transbilayer (flip-flop) lipid motion and lipid scrambling in membranes. FEBS Lett. 2010, 584, 1779-1786.
60. Chiantia, S.; Klymchenko, A. S.; London, E. A novel leaflet-selective fluorescence labeling technique reveals differences between inner and outer leaflets at high bilayer curvature. Biochim. Biophys. Acta 2012, 1818, 1284-1290.
61. Cullis, P. R.; Hope, M. J.; Bally, M. B.; Madden, T. D.; Mayer, L. D.; Fenske, D. B. Influence of pH gradients on the transbilayer transport of drugs, lipids, peptides and metal ions into large unilamellar vesicles. Biochim. Biophys. Acta 1997, 1331, 187-211.