Separating attoliter-sized compartments using fluid pore-spanning lipid bilayers

ACS Nano

Volumn 5, Issue 9, 2011, Pages 6935-6944

  Lazzara, Thomas D ^a   Carnarius, Christian ^a   Kocun, Marta ^b   Janshoff, Andreas ^b   Steinem, Claudia ^a  

^a Institute of Organic and Biomolecular Chemistry   (Germany)

^b Institute for Physical Chemistry   (Germany)

Author keywords

anodic aluminum oxide; fluorescence microscopy; fluorescence recovery after photobleaching; molecular encapsulation; nanoporous substrates; silane chemistry

Indexed keywords

ANODIC ALUMINUM OXIDE; BARRIER FUNCTIONS; BI-LAYER; BULK SOLUTIONS; CONFOCAL LASER SCANNING; FLUID LIPID BILAYERS; FLUORESCENCE IMAGING; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FUNCTIONALIZED; GIANT UNILAMELLAR VESICLES; LIPID DIFFUSION; MEMBRANE PATCH; MEMBRANE SURFACE; MOLECULAR ENCAPSULATION; NANOPOROUS MATERIALS; NANOPOROUS SUBSTRATE; OPTICAL TRANSPARENCY; SINGLE-LIPID BILAYERS;

ALUMINUM; ANODIC OXIDATION; FLUIDS; FLUORESCENCE; FLUORESCENCE MICROSCOPY; NANOPORES; OXIDES; PHOTOBLEACHING; POROUS MATERIALS; SILICA; SURFACE DIFFUSION;

LIPID BILAYERS;

ALUMINUM OXIDE;

ARTICLE; CHEMISTRY; ELECTRODE; LIPID BILAYER;

ALUMINUM OXIDE; ELECTRODES; LIPID BILAYERS;

EID: 80053309394     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn201266e     Document Type: Article

References (73)

1. Castellana, E. T.; Cremer, P. S. Solid Supported Lipid Bilayers: From Biophysical Studies to Sensor Design Surf. Sci. Rep. 2006, 61, 429-444 (Pubitemid 44634133)
2. Richter, R. P.; Berat, R.; Brisson, A. R. Formation of Solid-Supported Lipid Bilayers: An Integrated View Langmuir 2006, 22, 3497-3505 (Pubitemid 43672517)
3. Sackmann, E. Supported Membranes: Scientific and Practical Applications Science 1996, 271, 43-48 (Pubitemid 26033275)
4. Hubbard, J. B.; Silin, V.; Plant, A. L. Self-Assembly Driven by Hydrophobic Interactions at Alkanethiol Monolayers: Mechanism of Formation of Hybrid Bilayer Membranes Biophys. Chem. 1998, 75, 163-176 (Pubitemid 28558688)
5. Plant, A. L. Supported Hybrid Bilayer Membranes as Rugged Cell Membrane Mimics Langmuir 1999, 15, 5128-5135
6. Sackmann, E.; Tanaka, M. Supported Membranes on Soft Polymer Cushions: Fabrication, Characterization and Applications Trends Biotechnol. 2000, 18, 58-64 (Pubitemid 30084697)
7. Tanaka, M.; Sackmann, E. Polymer-Supported Membranes as Models of the Cell Surface Nature 2005, 437, 656-663 (Pubitemid 41486528)
8. McBee, T. W.; Wang, L. Y.; Ge, C. H.; Beam, B. M.; Moore, A. L.; Gust, D.; Moore, T. A.; Armstrong, N. R.; Saavedra, S. S. Characterization of Proton Transport Across a Waveguide-Supported Lipid Bilayer J. Am. Chem. Soc. 2006, 128, 2184-2185
9. Naumann, R.; Schiller, S. M.; Giess, F.; Grohe, B.; Hartman, K. B.; Karcher, I.; Köper, I.; Lubben, J.; Vasilev, K.; Knoll, W. Tethered Lipid Bilayers on Ultraflat Gold Surfaces Langmuir 2003, 19, 5435-5443
10. Erbe, A.; Bushby, R. J.; Evans, S. D.; Jeuken, L. J. C. Tethered Bilayer Lipid Membranes Studied by Simultaneous Attenuated Total Reflectance Infrared Spectroscopy and Electrochemical Impedance Spectroscopy J. Phys. Chem. B 2007, 111, 3515-3524 (Pubitemid 46656090)
11. Anderson, T. H.; Min, Y. J.; Weirich, K. L.; Zeng, H. B.; Fygenson, D.; Israelachvili, J. N. Formation of Supported Bilayers on Silica Substrates Langmuir 2009, 25, 6997-7005
12. Cremer, P. S.; Boxer, S. G. Formation and Spreading of Lipid Bilayers on Planar Glass Supports J. Phys. Chem. B 1999, 103, 2554-2559 (Pubitemid 129702516)
13. Hamai, C.; Cremer, P. S.; Musser, S. M. Single Giant Vesicle Rupture Events Reveal Multiple Mechanisms of Glass-Supported Bilayer Formation Biophys. J. 2007, 92, 1988-1999 (Pubitemid 46495262)
14. Rädler, J.; Strey, H.; Sackmann, E. Phenomenology and Kinetics of Lipid Bilayer Spreading on Hydrophilic Surfaces Langmuir 1995, 11, 4539-4548
15. Khan, T. R.; Grandin, H. M.; Mashaghi, A.; Textor, M.; Reimhult, E.; Reviakine, I. Lipid Redistribution in Phosphatidylserine-Containing Vesicles Adsorbing on Titania Biointerphases 2008, 3, FA90-FA95
16. Lagerholm, B. C.; Starr, T. E.; Volovyk, Z. N.; Thompson, N. L. Rebinding of IgE Fabs at Haptenated Planar Membranes: Measurement by Total Internal Reflection with Fluorescence Photobleaching Recovery Biochem. 2000, 39, 2042-2051 (Pubitemid 30124012)
17. Tamm, L. K.; McConnell, H. M. Supported Phospholipid-Bilayers Biophys. J. 1985, 47, 105-113
18. 2: Dependence on Vesicle Size J. Chem. Phys. 2002, 117, 7401-7404 (Pubitemid 35354304)
19. 2 Nanobeads Langmuir 2010, 26, 12081-12088
20. Claesson, M.; Cho, N. J.; Frank, C. W.; Andersson, M. Vesicle Adsorption on Mesoporous Silica and Titania Langmuir 2010, 26, 16630-16633
21. Lenz, P.; Ajo-Franklin, C. M.; Boxer, S. G. Patterned Supported Lipid Bilayers and Monolayers on Poly(dimethylsiloxane) Langmuir 2004, 20, 11092-11099
22. Shahal, T.; Melzak, K. A.; Lowe, C. R.; Gizeli, E. Poly(dimethylsiloxane) -Coated Sensor Devices for the Formation of Supported Lipid Bilayers and the Subsequent Study of Membrane Interactions Langmuir 2008, 24, 11268-11275
23. Williams, L. M.; Evans, S. D.; Flynn, T. M.; Marsh, A.; Knowles, P. F.; Bushby, R. J.; Boden, N. Kinetics of the Unrolling of Small Unilamellar Phospholipid Vesicles onto Self-Assembled Monolayers Langmuir 1997, 13, 751-757 (Pubitemid 127592139)
24. 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 (Pubitemid 41071342)
25. Cha, T.; Guo, A.; Zhu, X. Y. Formation of Supported Phospholipid Bilayers on Molecular Surfaces: Role of Surface Charge Density and Electrostatic Interaction Biophys. J. 2006, 90, 1270-1274
26. Steinem, C.; Janshoff, A.; Ulrich, W. P.; Sieber, M.; Galla, H. J. Impedance Analysis of Supported Lipid Bilayer Membranes: A Scrutiny of Different Preparation Techniques Biochim. Biophys. Acta, Biomembr. 1996, 1279, 169-180 (Pubitemid 26080847)
27. Janshoff, A.; Steinem, C. Transport Across Artificial Membranes-An Analytical Perspective Anal. Bioanal.Chem. 2006, 385, 433-451 (Pubitemid 43791931)
28. Gassmann, O.; Kreir, M.; Ambrosi, C.; Pranskevich, J.; Oshima, A.; Roling, C.; Sosinsky, G.; Fertig, N.; Steinem, C. The M34A Mutant of Connexin26 Reveals Active Conductance States in Pore-Suspending Membranes J. Struct. Biol. 2009, 168, 168-176
29. Kleefen, A.; Pedone, D.; Grunwald, C.; Wei, R.; Firnkes, M.; Abstreiter, G.; Rant, U.; Tampé, R. Multiplexed Parallel Single Transport Recordings on Nanopore Arrays Nano Lett. 2010, 10, 5080-5087
30. Schmitt, E. K.; Nurnabi, M.; Bushby, R. J.; Steinem, C. Electrically Insulating Pore-Suspending Membranes on Highly Ordered Porous Alumina Obtained from Vesicle Spreading Soft Matter 2008, 4, 250-253
31. Hennesthal, C.; Steinem, C. Pore-Spanning Lipid Bilayers Visualized by Scanning Force Microscopy J. Am. Chem. Soc. 2000, 122, 8085-8086 (Pubitemid 30659436)
32. Im, H.; Wittenberg, N. J.; Lesuffleur, A.; Lindquist, N. C.; Oh, S. H. Membrane Protein Biosensing with Plasmonic Nanopore Arrays and Pore-Spanning Lipid Membranes Chem. Sci. 2010, 1, 688-696
33. Kresak, S.; Hianik, T.; Naumann, R. L. C. Gigaseal Solvent-Free Bilayer Lipid Membranes: From Single Nanopores to Nanopore Arrays Soft Matter 2009, 5, 4021-4032
34. Sugihara, K.; Voros, J.; Zambelli, T. A Gigaseal Obtained with a Self-Assembled Long-Lifetime Lipid Bilayer on a Single Polyelectrolyte Multilayer-Filled Nanopore ACS Nano 2010, 4, 5047-5054
35. Mager, M. D.; Melosh, N. A. Nanopore-Spanning Lipid Bilayers for Controlled Chemical Release Adv. Mater. 2008, 20, 4423-4427
36. Mager, M. D.; Almquist, B.; Melosh, N. A. Formation and Characterization of Fluid Lipid Bilayers on Alumina Langmuir 2008, 24, 12734-12737
37. Mager, M. D.; Melosh, N. A. Lipid Bilayer Deposition and Patterning via Air Bubble Collapse Langmuir 2007, 23, 9369-9377 (Pubitemid 47383527)
38. Schmitt, E. K.; Vrouenraets, M.; Steinem, C. Channel Activity of OmpF Monitored in Nano-BLMs Biophys. J. 2006, 91, 2163-2171 (Pubitemid 44352399)
39. Weiskopf, D.; Schmitt, E. K.; Klühr, M. H.; Dertinger, S. K.; Steinem, C. Micro-BLMs on Highly Ordered Porous Silicon Substrates: Rupture Process and Lateral Mobility Langmuir 2007, 23, 9134-9139 (Pubitemid 47383495)
40. Han, X. J.; Studer, A.; Sehr, H.; Geissbuhler, I.; Di Berardino, M.; Winkler, F. K.; Tiefenauer, L. X. Nanopore Arrays for Stable and Functional Free-Standing Lipid Bilayers Adv. Mater. 2007, 19, 4466-4470
41. Mey, I.; Stephan, M.; Schmitt, E. K.; Müller, M. M.; Ben Amar, M.; Steinem, C.; Janshoff, A. Local Membrane Mechanics of Pore-Spanning Bilayers J. Am. Chem. Soc. 2009, 131, 7031-7039
42. Jonsson, P.; Jonsson, M. P.; Höök, F. Sealing of Submicrometer Wells by a Shear-Driven Lipid Bilayer Nano Lett. 2010, 10, 1900-1906
43. Worsfold, O.; Voelcker, N. H.; Nishiya, T. Biosensing Using Lipid Bilayers Suspended on Porous Silicon Langmuir 2006, 22, 7078-7083 (Pubitemid 44231454)
44. Cunin, F.; Milhiet, P. E.; Anglin, E.; Sailor, M. J.; Espenel, C.; Le Grimellec, C.; Brunel, D.; Devoisselle, J. M. Continuous Planar Phospholipid Bilayer Supported on Porous Silicon Thin Film Reflector Ultramicroscopy 2007, 107, 1048-1052 (Pubitemid 47103233)
45. Bhattacharya, J.; Kisner, A.; Offenhäusser, A.; Wolfrum, B. Microfluidic Anodization of Aluminum Films for the Fabrication of Nanoporous Lipid Bilayer Support Structures Beilstein J. Nanotechnol. 2011, 2, 104-109
46. Suzuki, K.; Masuhara, H. Groove-Spanning Behavior of Lipid Membranes on Microfabricated Silicon Substrates Langmuir 2005, 21, 6487-6494 (Pubitemid 41006465)
47. Pfeiffer, I.; Seantier, B.; Petronis, S.; Sutherland, D.; Kasemo, B.; Zach, M. Influence of Nanotopography on Phospholipid Bilayer Formation on Silicon Dioxide J. Phys. Chem. B 2008, 112, 5175-5181
48. Pfeiffer, I.; Petronis, S.; Köper, I.; Kasemo, B.; Zach, M. Vesicle Adsorption and Phospholipid Bilayer Formation on Topographically and Chemically Nanostructured Surfaces J. Phys. Chem. B 2010, 114, 4623-4631
49. Simon, A.; Girard-Egrot, A.; Sauter, F.; Pudda, C.; D'Hahan, N. P.; Blum, L.; Chatelain, F.; Fuchs, A. Formation and Stability of a Suspended Biomimetic Lipid Bilayer on Silicon Submicrometer-Sized Pores J. Colloid Interface Sci. 2007, 308, 337-343
50. Knoll, W. Interfaces and Thin Films As Seen by Bound Electromagnetic Waves Annu. Rev. Phys. Chem. 1998, 49, 569-638 (Pubitemid 128436900)
51. Lau, K. H. A.; Tan, L. S.; Tamada, K.; Sander, M. S.; Knoll, W. Highly Sensitive Detection of Processes Occurring Inside Nanoporous Anodic Alumina Templates: A Waveguide Optical Study J. Phys. Chem. B 2004, 108, 10812-10818
52. Lazzara, T. D.; Lau, K. H. A.; Abou-Kandil, A. I.; Caminade, A. M.; Majoral, J. P.; Knoll, W. Polyelectrolyte Layer-by-Layer Deposition in Cylindrical Nanopores ACS Nano 2010, 4, 3909-3920
53. Dai, J. H.; Baker, G. L.; Bruening, M. L. Use of Porous Membranes Modified with Polyelectrolyte Multilayers as Substrates for Protein Arrays with Low Nonspecific Adsorption Anal. Chem. 2006, 78, 135-140 (Pubitemid 43050148)
54. Takmakov, P.; Vlassiouk, I.; Smirnov, S. Application of Anodized Aluminum in Fluorescence Detection of Biological Species Anal. Bioanal. Chem. 2006, 385, 954-958 (Pubitemid 350153373)
55. Casanova, F.; Chiang, C. E.; Li, C. P.; Roshchin, I. V.; Ruminski, A. M.; Sailor, M. J.; Schuller, I. K. Gas Adsorption and Capillary Condensation in Nanoporous Alumina Films Nanotechnology 2008, 19, 315709
56. Janshoff, A.; Dancil, K. P. S.; Steinem, C.; Greiner, D. P.; Lin, V. S. Y.; Gurtner, C.; Motesharei, K.; Sailor, M. J.; Ghadiri, M. R. Macroporous p-Type Silicon Fabry-Perot Layers. Fabrication, Characterization, and Applications in Biosensing J. Am. Chem. Soc. 1998, 120, 12108-12116 (Pubitemid 29012882)
57. 2 Interferometric Biosensor for Quantitative Determination of Protein Interactions: Binding of Protein A to Immunoglobulins Derived from Different Species Anal. Chem. 2007, 79, 327-334 (Pubitemid 46095065)
58. Vasilev, K.; Knoll, W.; Kreiter, M. Fluorescence Intensities of Chromophores in Front of a Thin Metal Film J. Chem. Phys. 2004, 120, 3439-3445
59. Lau, K. H. A.; Knoll, W.; Kim, D. H. Theoretical Optical Waveguide Investigation of Self-Organized Polymer Thin Film Nanostructures with Nanoparticle Incorporation Macromol. Res. 2007, 15, 211-215
60. Ono, S.; Masuko, N. The Duplex Structure of Cell-Walls of Porous Anodic Films Formed on Aluminum Corros. Sci. 1992, 33, 503-505
61. Lazzara, T. D.; Kliesch, T. T.; Janshoff, A.; Steinem, C. Orthogonal Functionalization of Nanoporous Substrates: Control of 3D Surface Functionality ACS Appl. Mater. Interfaces 2011, 3, 1068-1076
62. Aronsson, B. O.; Lausmaa, J.; Kasemo, B. Glow Discharge Plasma Treatment for Surface Cleaning and Modification of Metallic Biomaterials J. Biomed. Mater. Res. 1997, 35, 49-73 (Pubitemid 27143011)
63. Raiber, K.; Terfort, A.; Benndorf, C.; Krings, N.; Strehblow, H. H. Removal of Self-Assembled Monolayers of Alkanethiolates on Gold by Plasma Cleaning Surf. Sci. 2005, 595, 56-63 (Pubitemid 41562875)
64. Axelrod, D.; Koppel, D. E.; Schlessinger, J.; Elson, E.; Webb, W. W. Mobility Measurement by Analysis of Fluorescence Photobleaching Recovery Kinetics Biophys. J. 1976, 16, 1055-1069
65. Stelzle, M.; Miehlich, R.; Sackmann, E. 2-Dimensional Microelectrophoresis in Supported Lipid Bilayers Biophys. J. 1992, 63, 1346-1354 (Pubitemid 23004484)
66. Przybylo, M.; Sykora, J.; Humpolickova, J.; Benda, A.; Zan, A.; Hof, M. Lipid Diffusion in Giant Unilamellar Vesicles is more than 2 Times Faster than in Supported Phospholipid Bilayers under Identical Conditions Langmuir 2006, 22, 9096-9099 (Pubitemid 44818493)
67. Lazzara, T. D.; Mey, I.; Steinem, C.; Janshoff, A. Benefits and Limitations of Porous Substrates as Biosensors for Protein Adsorption Anal. Chem. 2011, 83, 5624-5630
68. Boxer, S. G. Molecular Transport and Organization in Supported Lipid Membranes Curr. Opin. Chem. Biol. 2000, 4, 704-709
69. Nissen, J.; Gritsch, S.; Wiegand, G.; Rädler, J. O. Wetting of Phospholipid Membranes on Hydrophilic Surfaces-Concepts Towards Self-Healing Membranes Eur. Phys. J. B 1999, 10, 335-344 (Pubitemid 129641593)
70. Kocun, M.; Lazzara, T. D.; Steinem, C.; Janshoff, A. Preparation of Solvent-Free, Pore-Spanning Lipid Bilayers: Modeling the Low Tension of Plasma Membranes Langmuir 2011, 27, 7672-7680
71. Guo, P. F.; Wu, S.; Ren, Q. J.; Lu, J.; Chen, Z. H.; Xiao, S. J.; Zhu, Y. Y. Fluorescence Enhancement by Surface Plasmon Polaritons on Metallic Nanohole Arrays J. Phys. Chem. Lett. 2010, 1, 315-318
72. Lazzara, T. D.; Lau, K. H. A.; Knoll, W. Mounted Nanoporous Anodic Alumina Thin Films as Planar Optical Waveguides J. Nanosci. Nanotechnol. 2010, 10, 4293-4299
73. Bagatolli, L. A.; Parasassi, T.; Gratton, E. Giant Phospholipid Vesicles: Comparison Among the Whole Lipid Sample Characteristics using Different Preparation Methods-A Two Photon Fluorescence Microscopy Study Chem. Phys. Lipids 2000, 105, 135-147