A gigaseal obtained with a self-assembled long-lifetime lipid bilayer on a single polyelectrolyte multilayer-filled nanopore

ACS Nano

Volumn 4, Issue 9, 2010, Pages 5047-5054

  Sugihara, Kaori ^a   Vörös, János ^a   Zambelli, Tomaso ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

impedance spectroscopy; melittin; planar lipid bilayers; polyelectrolyte multilayers; single channel monitoring

Indexed keywords

IMPEDANCE SPECTROSCOPY; MELITTIN; PLANAR LIPID BILAYERS; POLYELECTROLYTE MULTILAYERS; SINGLE CHANNELS;

LIPOSOMES; MULTILAYERS; NANOPORES; PHOSPHOLIPIDS; POLYELECTROLYTES;

LIPID BILAYERS;

ELECTROLYTE; MELITTIN; POLYMER; SILICON; SILICON DERIVATIVE; SILICON NITRIDE;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; IMPEDANCE; LIPID BILAYER; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; NANOPORE; NANOTECHNOLOGY; POROSITY;

AMINO ACID SEQUENCE; ELECTRIC IMPEDANCE; ELECTROLYTES; LIPID BILAYERS; MELITTEN; MOLECULAR SEQUENCE DATA; NANOPORES; NANOTECHNOLOGY; POLYMERS; POROSITY; SILICON; SILICON COMPOUNDS;

EID: 77957292389     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn100773q     Document Type: Article

References (65)

1. Mueller, P.; Rudin, D. O.; Ti Tien, H.; Wescott, W. C. Reconstitution of Cell Membrane Structure In Vitro and Its Transformation into an Excitable System Nature 1962, 194, 979-980
2. Ogier, S. D.; Bushby, R. J.; Cheng, Y.; Evans, S. D.; Evans, S. W.; Jenkins, A. T. A.; Knowles, P. F.; Miles, R. E. Suspended Planar Phospholipid Bilayers on Micromachined Supports Langmuir 2000, 16, 5696-5701
3. Bradley, R. J.; Urry, D. W.; Okamoto, K.; Rapaka, R. Channel Structures of Gramicidin-Characterization of Succinyl Derivatives Science 1978, 200, 435-437
4. Pawlak, M.; Stankowski, S.; Schwarz, G. Melittin Induced Voltage-Dependent Conductance in DOPC Lipid Bilayers Biochim. Biophys. Acta 1991, 1062, 94-102
5. Gomezlagunas, F.; Pena, A.; Lievano, A.; Darszon, A. Incorporation of Ionic Channels from Yeast Plasma-Membranes into Black Lipid-Membranes Biophys. J. 1989, 56, 115-119
6. Cornell, B. A.; BraachMaksvytis, V. L. B.; King, L. G.; Osman, P. D. J.; Raguse, B.; Wieczorek, L.; Pace, R. J. A Biosensor That Uses Ion-Channel Switches Nature 1997, 387, 580-583
7. Priscilla Kailian, A.; Kian Ping, L.; Thorsten, W.; Milos, N.; Emile Van, H. Supported Lipid Bilayer on Nanocrystalline Diamond: Dual Optical and Field-Effect Sensor for Membrane Disruption Adv. Funct. Mater. 2009, 19, 109-116
8. Yang, T.-H.; Yee, C. K.; Amweg, M. L.; Singh, S.; Kendall, E. L.; Dattelbaum, A. M.; Shreve, A. P.; Brinker, C. J.; Parikh, A. N. Optical Detection of Ion-Channel-Induced Proton Transport in Supported Phospholipid Bilayers Nano Lett. 2007, 7, 2446-2451
9. Zhou, X. J.; Moran-Mirabal, J. M.; Craighead, H. G.; McEuen, P. L. Supported Lipid Bilayer/Carbon Nanotube Hybrids Nat. Nanotechnol. 2007, 2, 185-190
10. Andersson, M.; Keizer, H. M.; Zhu, C.; Fine, D.; Dodabalapur, A.; Duran, R. S. Detection of Single Ion Channel Activity on a Chip Using Tethered Bilayer Membranes Langmuir 2007, 23, 2924-2927
11. 2 Langmuir 2006, 22, 3313-3319
12. Schmitt, E. K.; Weichbrodt, C.; Steinem, C. Impedance Analysis of Gramicidin D in Pore-Suspending Membranes Soft Matter 2009, 5, 3347-3353
13. Han, X.; Studer, A.; Sehr, H.; Geissbühler, 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
14. Simon, A.; Girard-Egrot, A.; Sauter, F.; Pudda, C.; DHahan, 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
15. Kresak, S.; Hianik, T.; Naumann, R. L. C. Giga-seal Solvent-Free Bilayer Lipid Membranes: From Single Nanopores to Nanopore Arrays Soft Matter 2009, 5, 4021-4032
16. Jeon, T. J.; Malmstadt, N.; Schmidt, J. J. Hydrogel-Encapsulated Lipid Membranes J. Am. Chem. Soc. 2006, 128, 42-43
17. Tanaka, M.; Sackmann, E. Polymer-Supported Membranes As Models of the Cell Surface Nature 2005, 437, 656-663
18. Wong, J. Y.; Majewski, J.; Seitz, M.; Park, C. K.; Israelachvili, J. N.; Smith, G. S. Polymer-Cushioned Bilayers. I. A Structural Study of Various Preparation Methods Using Neutron Reflectometry Biophys. J. 1999, 77, 1445-1457
19. Merzlyakov, M.; Li, E.; Gitsov, I.; Hristova, K. Surface-Supported Bilayers with Transmembrane Proteins: Role of the Polymer Cushion Revisited Langmuir 2006, 22, 10145-10151
20. Kohli, N.; Vaidya, S.; Ofoli, R. Y.; Worden, R. M.; Lee, I. Arrays of Lipid Bilayers and Liposomes on Patterned Polyelectrolyte Templates J. Colloid Interface Sci. 2006, 301, 461-469
21. Kang, X. f.; Cheley, S.; Rice-Ficht, A. C.; Bayley, H. A Storable Encapsulated Bilayer Chip Containing a Single Protein Nanopore J. Am. Chem. Soc. 2007, 129, 4701-4705
22. Shim, J. W.; Gu, L. Q. Stochastic Sensing on a Modular Chip Containing a Single-Ion Channel Anal. Chem. 2007, 79, 2207-2213
23. Decher, G. Fuzzy Nanoassemblies: Toward Layered Polymeric Multicomposites Science 1997, 277, 1232-1237
24. Sullivan, D. M.; Bruening, M. L. Ultrathin, Ion-Selective Polyimide Membranes Prepared from Layered Polyelectrolytes J. Am. Chem. Soc. 2001, 123, 11805-11806
25. Tang, Z.; Wang, Y.; Podsiadlo, P.; Kotov, N. A. Biomedical Applications of Layer-by-Layer Assembly: From Biomimetics to Tissue Engineering Adv. Mater. 2006, 18, 3203-3224
26. Xianghui, L.; Jingtao, Z.; David, M. L. Ultrathin Multilayered Films That Promote the Release of Two DNA Constructs with Separate and Distinct Release Profiles Adv. Mater. 2008, 20, 4148-4153
27. Tanaka, M.; Kaufmann, S.; Nissen, J.; Hochrein, M. Orientation Selective Immobilization of Human Erythrocyte Membranes on Ultrathin Cellulose Films Phys. Chem. Chem. Phys. 2001, 3, 4091-4095
28. Vockenroth, I. K.; Fine, D.; Dodobalapur, A.; Jenkins, A. T. A.; Köper, I. Tethered Bilayer Lipid Membranes with Giga-Ohm Resistances Electrochem. Commun. 2008, 10, 323-328
29. Moya, S.; Donath, E.; Sukhorukov, G. B.; Auch, M.; Baumler, H.; Lichtenfeld, H.; Mohwald, H. Lipid Coating on Polyelectrolyte Surface Modified Colloidal Particles and Polyelectrolyte Capsules Macromolecules 2000, 33, 4538-4544
30. Cassier, T.; Sinner, A.; Offenhäuser, A.; Möhwald, H. Homogeneity, Electrical Resistivity and Lateral Diffusion of Lipid Bilayers Coupled to Polyelectrolyte Multilayers Colloids Surf., B 1999, 15, 215-225
31. Volodkin, D.; Mohwald, H.; Voegel, J.-C.; Ball, V. Coating of Negatively Charged Liposomes by Polylysine: Drug Release Study J. Controlled Release 2007, 117, 111-120
32. Michel, A.; Izquierdo, A.; Decher, G.; Voegel, J. C.; Schaaf, P.; Ball, V. Layer by Layer Self-Assembled Polyelectrolyte Multilayers with Embedded Phospholipid Vesicles Obtained by Spraying: Integrity of the Vesicles Langmuir 2005, 21, 7854-7859
33. Schlenoff, J. B.; Dubas, S. T.; Farhat, T. Sprayed Polyelectrolyte Multilayers Langmuir 2000, 16, 9968-9969
34. Izquierdo, A.; Ono, S. S.; Voegel, J. C.; Schaaf, P.; Decher, G. Dipping versus Spraying: Exploring the Deposition Conditions for Speeding up Layer-by-Layer Assembly Langmuir 2005, 21, 7558-7567
35. Caruso, F.; Niikura, K.; Furlong, D. N.; Okahata, Y. Ultrathin Multilayer Polyelectrolyte Films on Gold: Construction and Thickness Determination. 1 Langmuir 1997, 13, 3422-3426
36. Lavalle, P.; Gergely, C.; Cuisinier, F. J. G.; Decher, G.; Schaaf, P.; Voegel, J. C.; Picart, C. Comparison of the Structure of Polyelectrolyte Multilayer Films Exhibiting a Linear and an Exponential Growth Regime: An In Situ Atomic Force Microscopy Study Macromolecules 2002, 35, 4458-4465
37. Fischlechner, M.; Zaulig, M.; Meyer, S.; Estrela-Lopis, I.; Cuellar, L.; Irigoyen, J.; Pescador, P.; Brumen, M.; Messner, P.; Moya, S.; Donath, E. Lipid Layers on Polyelectrolyte Multilayer Supports Soft Matter 2008, 4, 2245-2258
38. Ai, S.; He, Q.; Tao, C.; Zheng, S.; Li, J. Conductive Polypyrrole and Poly(allylamine hydrochloride) Nanotubes Fabricated with Layer-by-Layer Assembly Macromol. Rapid Commun. 2005, 26, 1965-1969
39. Ai, S.; Lu, G.; He, Q.; Li, J. Highly Flexible Polyelectrolyte Nanotubes J. Am. Chem. Soc. 2003, 125, 11140-11141
40. Lee, D.; Nolte, A. J.; Kunz, A. L.; Rubner, M. F.; Cohen, R. E. pH-Induced Hysteretic Gating of Track-Etched Polycarbonate Membranes: Swelling/Deswelling Behavior of Polyelectrolyte Multilayers in Confined Geometry J. Am. Chem. Soc. 2006, 128, 8521-8529
41. Alem, H.; Blondeau, F.; Glinel, K.; Demoustier-Champagne, S.; Jonas, A. M. Layer-by-Layer Assembly of Polyelectrolytes in Nanopores Macromolecules 2007, 40, 3366-3372
42. Roy, C. J.; Dupont-Gillain, C.; Demoustier-Champagne, S.; Jonas, A. M.; Landoulsi, J. Growth Mechanism of Confined Polyelectrolyte Multilayers in Nanoporous Templates Langmuir 2009, 26, 3350-3355
43. Soumpasis, D. M. Theoretical Analysis of Fluorescence Photobleaching Recovery Experiments Biophys. J. 1983, 41, 95-97
44. Stanton, B. W.; Harris, J. J.; Miller, M. D.; Bruening, M. L. Ultrathin, Multilayered Polyelectrolyte Films as Nanofiltration Membranes Langmuir 2003, 19, 7038-7042
45. Lubke, L. L.; Garon, C. F. The Antimicrobial Agent Melittin Exhibits Powerful In Vitro Inhibitory Effects on the Lyme Disease Spirochete Clin. Infect. Dis. 1997, 25, S48-S51
46. Klotz, S. A.; Gaur, N. K.; Rauceo, J.; Lake, D. F.; Park, Y.; Hahm, K. S.; Lipke, P. N. Inhibition of Adherence and Killing of Candida albicans with a 23-Mer Peptide (Fn/23) with Dual Antifungal Properties Antimicrob. Agents Chemother. 2004, 48, 4337-4341
47. Lazarev, V. N.; Parfenova, T. M.; Gularyan, S. K.; Misyurina, O. Y.; Akopian, T. A.; Govorun, V. M. Induced Expression of Melittin, An Antimicrobial Peptide, Inhibits Infection by Chlamydia trachomatis and Mycoplasma hominis in a HeLa Cell Line Int. J. Antimicrob. Agents 2002, 19, 133-137
48. Raghuraman, H.; Chattopadhyay, A. Melittin: A Membrane-Active Peptide with Diverse Functions Biosci. Rep. 2007, 27, 189-223
49. Studer, A.; Han, X.; Winkler, F. K.; Tiefenauer, L. X. Formation of Individual Protein Channels in Lipid Bilayers Suspended in Nanopores Colloids Surf., B 2009, 73, 325-331
50. Tosteson, M. T.; Tosteson, D. C. The Sting. Melittin Forms Channels in Lipid Bilayers Biophys. J. 1981, 36, 109-116
51. Hanke, W.; Methfessel, C.; Wilmsen, H.-U.; Katz, E.; Jung, G.; Boheim, G. Melittin and a Chemically Modified Trichotoxin Form Alamethicin-Type Multi-State Pores Biochim. Biophys. Acta 1983, 727, 108-114
52. Stankowski, S.; Pawlak, M.; Kaisheva, E.; Robert, C. H.; Schwarz, G. A Combined Study of Aggregation, Membrane Affinity and Pore Activity of Natural and Modified Melittin Biochim. Biophys. Acta 1991, 1069, 77-86
53. Dubas, S. T.; Schlenoff, J. B. Swelling and Smoothing of Polyelectrolyte Multilayers by Salt Langmuir 2001, 17, 7725-7727
54. Steitz, R.; Jaeger, W.; von Klitzing, R. Influence of Charge Density and Ionic Strength on the Multilayer Formation of Strong Polyelectrolytes Langmuir 2001, 17, 4471-4474
55. Ladam, G.; Schaad, P.; Voegel, J. C.; Schaaf, P.; Decher, G.; Cuisinier, F. In Situ Determination of the Structural Properties of Initially Deposited Polyelectrolyte Multilayers Langmuir 1999, 16, 1249-1255
56. One may hypothesize the continuous increase of the current is because of the change in the thickness of the lipid bilayer due to the adsorption of melittin since recent works have revealed that adsorption of melittin onto the lipid bilayer stretches the bilayer and makes the bilayer thinner to induce a mechanical stress. (47) However, the hypothesis can be rejected because the thickness change by 60% is unreasonable compared to the reported change rate by 5% in PC systems.
57. Becucci, L.; Leon, R. R.; Moncelli, M. R.; Rovero, P.; Guidelli, R. Electrochemical Investigation of Melittin Reconstituted into a Mercury-Supported Lipid Bilayer Langmuir 2006, 22, 6644-6650 (Pubitemid 44146900)
58. Hincha, D. K.; Crowe, J. H. The Lytic Activity of the Bee Venom Peptide Melittin Is Strongly Reduced by the Presence of Negatively Charged Phospholipids or Chloroplast Galactolipids in the Membranes of Phosphatidylcholine Large Unilamellar Vesicles Biochim. Biophys. Acta 1996, 1284, 162-170
59. Benachir, T.; Lafleur, M. Study of Vesicle Leakage Induced by Melittin Biochim. Biophys. Acta 1995, 1235, 452-460
60. Talbot, J. C.; Dufourcq, J.; de Bony, J.; Faucon, J. F.; Lussan, C. Conformational Change and Self Association of Monomeric Melittin FEBS Lett. 1979, 102, 191-193
61. Rex, S. Pore Formation Induced by the Peptide Melittin in Different Lipid Vesicle Membranes Biophys. Chem. 1996, 58, 75-85
62. Matsuzaki, K.; Yoneyama, S.; Miyajima, K. Pore Formation and Translocation of Melittin Biophys. J. 1997, 73, 831-838
63. Ladokhin, A. S.; Selsted, M. E.; White, S. H. Sizing Membrane Pores in Lipid Vesicles by Leakage of Co-encapsulated Markers: Pore Formation by Melittin Biophys. J. 1997, 72, 1762-1766
64. Lee, M.-T.; Hung, W.-C.; Chen, F.-Y.; Huang, H. W. Mechanism and Kinetics of Pore Formation in Membranes by Water-Soluble Amphipathic Peptides Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 5087-5092
65. Heyderman, L. J.; Ketterer, B.; Bachle, D.; Glaus, F.; Haas, B.; Schift, H.; Vogelsang, K.; Gobrecht, J.; Tiefenauer, L.; Dubochet, O.; Surbled, P.; Hessler, T. High Volume Fabrication of Customised Nanopore Membrane Chips Microelectron. Eng. 2003, 67-8, 208-213