Model Biological Membranes and Possibilities of Application of Electrochemical Impedance Spectroscopy for their Characterization
Štěpánka Skalová
J. Heyrovský Institute of Physical Chemistry of the Czech Academy of Sciences, Dolejškova 3, 182 23 Prague 8, Czech Republic
Charles University, Faculty of Science, Department of Analytical Chemistry, UNESCO Laboratory of Environmental Electrochemistry, Hlavova 2030/8, 128 43 Prague 2 Czech Republic
Search for more papers by this authorVlastimil Vyskočil
Charles University, Faculty of Science, Department of Analytical Chemistry, UNESCO Laboratory of Environmental Electrochemistry, Hlavova 2030/8, 128 43 Prague 2 Czech Republic
Search for more papers by this authorJiří Barek
Charles University, Faculty of Science, Department of Analytical Chemistry, UNESCO Laboratory of Environmental Electrochemistry, Hlavova 2030/8, 128 43 Prague 2 Czech Republic
Search for more papers by this authorCorresponding Author
Tomáš Navrátil
J. Heyrovský Institute of Physical Chemistry of the Czech Academy of Sciences, Dolejškova 3, 182 23 Prague 8, Czech Republic
Search for more papers by this authorŠtěpánka Skalová
J. Heyrovský Institute of Physical Chemistry of the Czech Academy of Sciences, Dolejškova 3, 182 23 Prague 8, Czech Republic
Charles University, Faculty of Science, Department of Analytical Chemistry, UNESCO Laboratory of Environmental Electrochemistry, Hlavova 2030/8, 128 43 Prague 2 Czech Republic
Search for more papers by this authorVlastimil Vyskočil
Charles University, Faculty of Science, Department of Analytical Chemistry, UNESCO Laboratory of Environmental Electrochemistry, Hlavova 2030/8, 128 43 Prague 2 Czech Republic
Search for more papers by this authorJiří Barek
Charles University, Faculty of Science, Department of Analytical Chemistry, UNESCO Laboratory of Environmental Electrochemistry, Hlavova 2030/8, 128 43 Prague 2 Czech Republic
Search for more papers by this authorCorresponding Author
Tomáš Navrátil
J. Heyrovský Institute of Physical Chemistry of the Czech Academy of Sciences, Dolejškova 3, 182 23 Prague 8, Czech Republic
Search for more papers by this authorAbstract
Biological membranes are essential parts of living systems. They represent an interface between intracellular and extracellular space. Depending on their structure, they often perform very complex functions and play an important role in the transport of both charged and uncharged particles in any organism. Structure of the biological membranes, which play very important role in electrochemical processes inside living organisms, is very complicated and still not precisely defined and explained. Model lipid membranes are used to gain detail information about properties of real biological membranes and about associated electrochemical processes. Electrochemistry, especially electrochemical impedance spectroscopy (EIS), can play a useful role in the characterization of properties of model lipid membranes (planar and supported lipid bilayers, tethered lipid membranes, liposomes, etc.). This review is focused on model biological membranes and the possibilities and limitations of electrochemical methods and namely of EIS in this field.
References
- 1K. Novakova, Chem. Listy 2015, 109, 166.
- 2T. Navratil, I. Sestakova, V. Marecek, K. Stulik, in XXX Moderni Elektrochemicke Metody (Modern Electrochemical Methods XXX) (Eds: ), BEST Servis, Jetrichovice 2010, pp. 119.
- 3J. Jaklova Dytrtova, M. Jakl, K. Novakova, T. Navratil, V. Sadek, Monatsh. Chem. 2015, 146, 831.
- 4T. Navratil, I. Sestakova, K. Stulik, V. Marecek, Electroanalysis 2010, 22, 2043.
- 5J. Jaklova Dytrtova, I. Sestakova, M. Jakl, T. Navratil, Electroanalysis 2009, 21, 573.
- 6J. Jaklova Dytrtova, M. Jakl, I. Sestakova, E. L. Zins, D. Schroder, T. Navratil, Anal. Chim. Acta 2011, 693, 100.
10.1016/j.aca.2011.03.028 Google Scholar
- 7J. Jaklova Dytrtova, M. Jakl, D. Schroder, T. Navratil, Curr. Org. Chem. 2011, 15, 2970.
- 8I. Sestakova, S. Skalova, T. Navratil, J. Electroanal. Chem. 2017, doi:10.1016/j.jelechem.2017.11.052, In press.
- 9M. Casal, S. Paiva, O. Queiros, I. Soares-Silva, FEMS Microbiol. Rev. 2008, 32, 974.
- 10J. Jaklova Dytrtova, T. Navratil, V. Marecek, Collect. Czech. Chem. Commun. 2011, 76, 1917.
- 11T. Navratil, I. Sestakova, V. Marecek, Int. J. Electrochem. Sci. 2011, 6, 6032.
- 12K. Novakova, T. Navratil, I. Sestakova, V. Marecek, J. Chylkova, Chem. Listy 2014, 108, 219.
- 13M. Naumowicz, A. D. Petelska, J. Electroanal. Chem. 2016, 782, 233.
10.1016/j.jelechem.2016.10.046 Google Scholar
- 14I. Sestakova, K. Novakova, B. Josypcuk, T. Navratil, in XXXIV Moderni Elektrochemicke Metody (Modern Electrochemial Methods XXXIV) (Eds: T. Navratil and J. Barek), Best Servis, Jetrichovice 2014, pp. 190.
- 15T. Navratil, K. Novakova, B. Josypcuk, R. Sokolova, I. Sestakova, Monatsh. Chem. 2016, 147, 165.
- 16M. Naumowicz, Z. Figaszewski, Bioelectrochemistry 2003, 61, 21.
- 17M. Naumowicz, Z. A. Figaszewski, Biophys. J. 2005, 89, 3174.
- 18J. Navarro-Laboulais, J. Trijueque, J. J. Garcia-Jareno, D. Benito, F. Vicente, J. Electroanal. Chem. 1998, 444, 173.
- 19M. Parisova, T. Navratil, I. Sestakova, J. Jaklova Dytrtova, V. Marecek, Int. J. Electrochem. Sci. 2013, 8, 27.
- 20M. Traube, Arch. Anat. Physiol. Wiss. Med. 1867, 87, 129.
- 21G. Quincke, Über die Physikalischen Eigenschaften Dünner, Fester Lamellen, Akademie der Wissenschaften, Berlin 1888.
- 22O. Hertwig, M. Campbell, H. J. Campbell, The Cell: Outlines of General Anatomy and Physiology, Macmillan and Co., New York 1895.
- 23A. Kleinzeller, News Physiol. Sci. 1997, 12, 49.
- 24C. E. Overton, Studien der Narkose (Studies of Narcosis), Gustav Fischer, Jena, Germany 1901.
- 25C. S. Helrich, Aims Biophysics 2017, 4, 415.
- 26E. Gorter, F. Grendel, J. Exp. Med. 1925, 41, 439.
- 27J. F. Danielli, H. Davson, J. Cell. Comp. Physiol. 1935, 5, 495.
- 28J. D. Robertson, Prog. Biophys. Mol. Biol. 1960, 10, 343.
- 29A. A. Benson, Annu. Rev. Plant Physiol. Plant Mol. Biol. 1964, 15, 1.
- 30D. E. Green, Tzagolof. A, J. Lipid Res. 1966, 7, 587.
- 31P. Mueller, D. O. Rudin, H. T. Tien, W. C. Wescott, Nature 1962, 194, 979.
- 32P. Mueller, D. O. Rudin, H. T. Tien, W. C. Wescott, J. Phys. Chem. 1963, 67, 534.
- 33H. T. Tien, S. Carbone, E. A. Dawidowi, Nature 1966, 212, 718.
- 34H. T. Tien, A. L. Diana, Nature 1967, 215, 1199.
- 35S. J. Singer, G. L. Nicolson, Science 1972, 175, 720.
- 36R. K. Murray, D. Bender, K. M. Botham, P. J. Kennelly, V. W. Rodwell, P. A. Weil, Harper's Illustrated Biochemistry, McGraw-Hill Lange, Columbus 2012.
- 37Z. Aminipour, M. Khorshid, M. Bayoumi, P. Losada-Perez, R. Thoelen, S. Bonakdar, H. Keshvari, G. Maglia, P. Wagner, B. Van der Bruggen, Phys. Status Solidi A 2017, 214, 1700104.
10.1002/pssa.201700104 Google Scholar
- 38A. J. Heron, J. R. Thompson, A. E. Mason, M. I. Wallace, J. Am. Chem. Soc. 2007, 129, 16042.
- 39H. Bayley, O. Braha, L. Q. Gu, Adv. Mater. 2000, 12, 139.
- 40H. Bayley, P. S. Cremer, Nature 2001, 413, 226.
- 41J. J. Kasianowicz, E. Brandin, D. Branton, D. W. Deamer, Proc. Natl. Acad. Sci. USA 1996, 93, 13770.
- 42S. Howorka, S. Cheley, H. Bayley, Nat. Biotechnol. 2001, 19, 636.
- 43Y. Astier, O. Braha, H. Bayley, J. Am. Chem. Soc. 2006, 128, 1705.
- 44M. Montal, P. Mueller, Proc. Natl. Acad. Sci. USA 1972, 69, 3561.
- 45I. Prudovsky, T. K. S. Kumar, S. Sterling, D. Neivandt, Int. J. Mol. Med. Sci. 2013, 14, 3734.
- 46P. Kramar, D. Miklavcic, M. Kotulska, A. M. Lebar, in Advances in Planar Lipid Bilayers Liposomes, Vol. 11, (Ed: ), Academic Press, Oxford 2010, pp. 29.
- 47K. A. Melzak, S. A. Melzak, E. Gizeli, J. L. Toca-Herrera, Materials 2012, 5, 2306.
- 48D. Bach, E. Wachtel, BBA-Biomembranes 2003, 1610, 187.
- 49T. Rog, M. Pasenkiewicz-Gierula, I. Vattulainen, M. Karttunen, BBA-Biomembranes 2009, 1788, 97.
- 50P. L. Yeagle, Biochim. Biophys. Acta 1985, 822, 267.
- 51P. L. Yeagle, Biochimie 1991, 73, 1303.
- 52T. P. W. McMullen, R. N. McElhaney, Curr. Opin. Colloid Interface Sci. 1996, 1, 83.
- 53O. Edholm, A. M. Nyberg, Biophys. J. 1992, 63, 1081.
- 54S. W. Chiu, E. Jakobsson, R. J. Mashl, H. L. Scott, Biophys. J. 2002, 83, 1842.
- 55E. Falck, M. Patra, M. Karttunen, M. T. Hyvonen, I. Vattulainen, J. Chem. Phys. 2004, 121, 12676.
- 56W. K. Subczynski, J. S. Hyde, A. Kusumi, Proc. Natl. Acad. Sci. USA 1989, 86, 4474.
- 57W. K. Subczynski, A. Wisniewska, J. J. Yin, J. S. Hyde, A. Kusumi, Biochemistry 1994, 33, 7670.
- 58L. J. Pike, J. Lipid Res. 2003, 44, 655.
- 59H. J. Risselada, S. J. Marrink, Proc. Natl. Acad. Sci. USA 2008, 105, 17367.
- 60C. L. Wennberg, D. van der Spoel, J. S. Hub, J. Am. Chem. Soc. 2012, 134, 5351.
- 61J. M. Boggs, J. C. Hsia, Biochim. Biophys. Acta 1972, 290, 32.
- 62M. C. Blok, L. L. M. Vandeenen, J. Degier, Biochim. Biophys. Acta 1977, 464, 509.
- 63T. J. Mcintosh, Biochim. Biophys. Acta 1978, 513, 43.
- 64A. A. Brian, H. M. Mcconnell, Proc. Natl. Acad. Sci. USA 1984, 81, 6159.
- 65L. K. Tamm, H. M. Mcconnell, Biophys. J. 1985, 47, 105.
- 66V. Kiessling, M. K. Domanska, D. Murray, C. Wan, L. K. Tamm, in Wiley Encyclopedia of Chemical Biology, Vol. 4, (Ed: ), Wiley-InterScience, Hoboken, 2009, pp. 411.
- 67E. T. Castellana, P. S. Cremer, Surf. Sci. Rep. 2006, 61, 429.
- 68S. J. Johnson, T. M. Bayerl, D. C. Mcdermott, G. W. Adam, A. R. Rennie, R. K. Thomas, E. Sackmann, Biophys. J. 1991, 59, 289.
- 69E. B. Watkins, C. E. Miller, D. J. Mulder, T. L. Kuhl, J. Majewski, Phys. Rev. Lett. 2009, 102, 238101.
- 70J. M. Crane, V. Kiessling, L. K. Tamm, Langmuir 2005, 21, 1377.
- 71J. Kim, G. Kim, P. S. Cremer, Langmuir 2001, 17, 7255.
- 72R. P. Richter, A. R. Brisson, Biophys. J. 2005, 88, 3422.
- 73H. Schonherr, J. M. Johnson, P. Lenz, C. W. Frank, S. G. Boxer, Langmuir 2004, 20, 11600.
- 74E. Reimhult, M. Zach, F. Hook, B. Kasemo, Langmuir 2006, 22, 3313.
- 75S. Nirasay, A. Badia, G. Leclair, J. P. Claverie, I. Marcotte, Materials 2012, 5, 2621.
- 76E. Sackmann, Science 1996, 271, 43.
- 77B. Kasemo, Surf. Sci. 2002, 500, 656.
- 78M. Tanaka, E. Sackmann, Nature 2005, 437, 656.
- 79E. K. Sinner, W. Knoll, Curr. Opin. Chem. Biol. 2001, 5, 705.
- 80I. Koper, Mol. BioSyst. 2007, 3, 651.
- 81R. Glazier, K. Salaita, BBA-Biomembranes 2017, 1859, 1465.
- 82Z. Zhang, M. Sohgawa, K. Yamashita, M. Noda, Electroanalysis 2016, 28, 620.
- 83H. Baghirov, S. Melikishvili, Y. Morch, E. Sulheim, A. K. O. Aslund, T. Hianik, C. D. Davies, Colloids Surf. B 2017, 150, 373.
10.1016/j.colsurfb.2016.10.051 Google Scholar
- 84B. A. Cornell, V. L. B. Braach-Maksvytis, L. G. King, P. D. J. Osman, B. Raguse, L. Wieczorek, R. J. Pace, Nature 1997, 387, 580.
- 85O. Worsfold, N. H. Voelcker, T. Nishiya, Langmuir 2006, 22, 7078.
- 86M. A. Mohsin, F. G. Banica, T. Oshima, T. Hianik, Electroanalysis 2011, 23, 1229.
- 87G.-P. Nikoleli, D. P. Nikolelis, G. Evtugyn, T. Hianik, TrAC Trends Anal. Chem. 2016, 79, 210.
10.1016/j.trac.2016.01.021 Google Scholar
- 88J. W. Liu, A. Stace-Naughton, X. M. Jiang, C. J. Brinker, J. Am. Chem. Soc. 2009, 131, 1354.
- 89V. Cauda, H. Engelke, A. Sauer, D. Arcizet, C. Brauchle, J. Radler, T. Bein, Nano Lett. 2010, 10, 2484.
- 90M. Ionov, K. Ciepluch, Z. Garaiova, S. Melikishvili, S. Michlewska, L. Balcerzak, S. Glinska, K. Milowska, R. Gomez-Ramirez, F. J. de la Mata, D. Shcharbin, I. Waczulikova, M. Bryszewska, T. Hianik, BBA-Biomembranes 2015, 1848, 907.
10.1016/j.bbamem.2014.12.025 Google Scholar
- 91D. Afanasenkau, A. Offenhausser, Langmuir 2012, 28, 13387.
- 92C. W. Hollars, R. C. Dunn, Biophys. J. 1998, 75, 342.
- 93K. Morigaki, T. Baumgart, U. Jonas, A. Offenhausser, W. Knoll, Langmuir 2002, 18, 4082.
- 94J. Radler, H. Strey, E. Sackmann, Langmuir 1995, 11, 4539.
- 95K. Furukawa, H. Nakashima, Y. Kashimura, K. Torimitsu, Lab Chip 2006, 6, 1001.
- 96K. Furukawa, T. Aiba, Langmuir 2011, 27, 7341.
- 97K. Furukawa, H. Hibino, Chem. Lett. 2012, 41, 1259.
- 98D. Axelrod, Traffic 2001, 2, 764.
- 99T. Fukuma, M. J. Higgins, S. P. Jarvis, Biophys. J. 2007, 92, 3603.
- 100R. Tero, Materials 2012, 5, 2658.
- 101J. Yang, J. Appleyard, J. Phys. Chem. B 2000, 104, 8097.
- 102A. Charrier, F. Thibaudau, Biophys. J. 2005, 89, 1094.
- 103Z. V. Feng, T. A. Spurlin, A. A. Gewirth, Biophys. J. 2005, 88, 2154.
- 104S. Stanglmaier, S. Hertrich, K. Fritz, J. F. Moulin, M. Haese-Seiller, J. O. Radler, B. Nickel, Langmuir 2012, 28, 10818.
- 105A. P. Shreve, M. C. Howland, A. R. Sapuri-Butti, T. W. Allen, A. N. Parikh, Langmuir 2008, 24, 13250.
- 106F. F. Rossetti, M. Textor, I. Reviakine, Langmuir 2006, 22, 3467.
- 107J. T. Groves, N. Ulman, S. G. Boxer, Science 1997, 275, 651.
- 108M. C. Howland, A. R. Sapuri-Butti, S. S. Dixit, A. M. Dattelbaum, A. P. Shreve, A. N. Parikh, J. Am. Chem. Soc. 2005, 127, 6752.
- 109T. Okazaki, T. Inaba, Y. Tatsu, R. Tero, T. Urisu, K. Morigaki, Langmuir 2009, 25, 345.
- 110J. P. Overington, B. Al-Lazikani, A. L. Hopkins, Nat. Rev. Drug Discov. 2006, 5, 993.
- 111J. Y. Wong, C. K. Park, M. Seitz, J. Israelachvili, Biophys. J. 1999, 77, 1458.
- 112J. A. Jackman, W. Knoll, N. J. Cho, Materials 2012, 5, 2637.
- 113R. Naumann, S. M. Schiller, F. Giess, B. Grohe, K. B. Hartman, I. Karcher, I. Koper, J. Lubben, K. Vasilev, W. Knoll, Langmuir 2003, 19, 5435.
- 114B. Raguse, V. Braach-Maksvytis, B. A. Cornell, L. G. King, P. D. J. Osman, R. J. Pace, L. Wieczorek, Langmuir 1998, 14, 648.
- 115S. M. Schiller, R. Naumann, K. Lovejoy, H. Kunz, W. Knoll, Angew. Chem. Int. Ed. 2003, 42, 208.
- 116S. Terrettaz, M. Mayer, H. Vogel, Langmuir 2003, 19, 5567.
- 117M. Chadli, S. Rebaud, O. Maniti, B. Tillier, S. Cortes, A. Girard-Egrot, Langmuir 2017, 33, 10385.
- 118T. Ragaliauskas, M. Mickevicius, B. Rakovska, T. Penkauskas, D. J. Vanderah, F. Heinrich, G. Valincius, BBA-Biomembranes 2017, 1859, 669.
10.1016/j.bbamem.2017.01.015 Google Scholar
- 119H. Lang, C. Duschl, H. Vogel, Langmuir 1994, 10, 197.
- 120V. Vontscharner, H. M. McConnell, Biophys. J. 1981, 36, 421.
- 121A. L. Plant, Langmuir 1993, 9, 2764.
- 122R. Guidelli, L. Becucci, A. Dolfi, M. R. Moncelli, F. T. Buoninsegni, Solid State Ionics 2002, 150, 13.
- 123J. C. Love, L. A. Estroff, J. K. Kriebel, R. G. Nuzzo, G. M. Whitesides, Chem. Rev. 2005, 105, 1103.
- 124A. Demoz, D. J. Harrison, Langmuir 1993, 9, 1046.
- 125V. I. Silin, H. Wieder, J. T. Woodward, G. Valincius, A. Offenhausser, A. L. Plant, J. Am. Chem. Soc. 2002, 124, 14676.
- 126J. T. Buboltz, G. W. Feigenson, BBA-Biomembranes 1999, 1417, 232.
- 127C. A. Naumann, O. Prucker, T. Lehmann, J. Ruhe, W. Knoll, C. W. Frank, Biomacromolecules 2002, 3, 27.
- 128R. Kugler, W. Knoll, Bioelectrochemistry 2002, 56, 175.
- 129R. Naumann, E. K. Schmidt, A. Jonczyk, K. Fendler, B. Kadenbach, T. Liebermann, A. Offenhausser, W. Knoll, Biosens. Bioelectron. 1999, 14, 651.
- 130E. K. Schmidt, T. Liebermann, M. Kreiter, A. Jonczyk, R. Naumann, A. Offenhausser, E. Neumann, A. Kukol, A. Maelicke, W. Knoll, Biosens. Bioelectron. 1998, 13, 585.
- 131R. Naumann, T. Baumgart, P. Graber, A. Jonczyk, A. Offenhausser, W. Knoll, Biosens. Bioelectron. 2002, 17, 25.
- 132V. Atanasov, P. P. Atanasova, I. K. Vockenroth, N. Knorr, I. Koper, Bioconjugate Chem. 2006, 17, 631.
- 133I. Koeper, N. Knorr, V. Atanasov, J. R. Long, P. A. V. Anderson, R. Duran, W. Knoll, Abstr. Pap. Am. Chem. Soc. 2005, 229, U 657.
- 134R. F. Roskamp, I. K. Vockenroth, N. Eisenmenger, J. Braunagel, I. Koper, ChemPhysChem 2008, 9, 1920.
- 135B. A. Cornell, G. Krishna, P. D. Osman, R. D. Pace, L. Wieczorek, Biochem. Soc. Trans. 2001, 29, 613.
- 136G. Krishna, J. Schulte, B. A. Cornell, R. Pace, L. Wieczorek, P. D. Osman, Langmuir 2001, 17, 4858.
- 137C. Soto, A. Del Valle, P. A. Valiente, U. Ros, M. E. Lanio, A. M. Hernandez, C. Alvarez, Biochimie 2017, 138, 20.
- 138L. Redondo-Morata, R. Lea Sanford, O. S. Andersen, S. Scheuring, Biophys. J. 2016, 111, 363.
10.1016/j.bpj.2016.06.016 Google Scholar
- 139I. K. Vockenroth, C. Rossi, M. R. Shah, I. Koper, Biointerphases 2009, 4, 19.
- 140H. T. Tien, A. Ottova-Leitmannova, Advances in Planar Lipid Bilayers Liposomes, Vol. 11, (Ed: ), Academic Press, Oxford 2010, pp. 29.
- 141C. G. Siontorou, G. P. Nikoleli, D. P. Nikolelis, S. K. Karapetis, Membranes 2017, 7, 38.
- 142H. A. H. Rongen, A. Bult, W. P. van Bennekom, J. Immunol. Methods 1997, 204, 105.
- 143K. A. Edwards, A. J. Baeumner, Talanta 2006, 68, 1432.
- 144R. Bittman, L. Blau, Biochemistry 1972, 11, 4831.
- 145R. A. Demel, S. C. Kinsky, C. B. Kinsky, L. L. van Deene, Biochim. Biophys. Acta 1968, 150, 655.
- 146C. M. Bailey, A. Tripathi, A. Shukla, Langmuir 2017, 33, 11986.
- 147Z. Y. Zhang, Y. Murakami, T. Taniguchi, M. Sohgawa, K. Yamashita, M. Noda, Electroanalysis 2017, 29, 722.
- 148L. Zhang, F. X. Gu, J. M. Chan, A. Z. Wang, R. S. Langer, O. C. Farokhzad, Clin. Pharmacol. Ther. 2008, 83, 761.
- 149D. Peer, J. M. Karp, S. Hong, O. C. Farokhzad, R. Margalit, R. Langer, Nat. Nanotechnol. 2007, 2, 751.
- 150Gregoria. G, B. E. Ryman, Biochem. J. 1971, 124, P 58.
- 151M. L. Immordino, F. Dosio, L. Cattel, Int. J. Nanomed. 2006, 1, 297.
- 152H. Barani, M. Montazer, J. Liposome Res. 2008, 18, 249.
- 153L. A. Meure, R. Knott, N. R. Foster, F. Dehghani, Langmuir 2009, 25, 326.
- 154K. Novakova, T. Navratil, I. Sestakova, M. P. Le, H. Vodickova, B. Zamecnikova, R. Sokolova, J. Bulickova, M. Gal, Monatsh. Chem. 2015, 146, 819.
- 155M. Kanduser, M. Sentjurc, D. Miklavcic, Eur. Biophys. J. 2006, 35, 196.
- 156G. C. Troiano, L. Tung, V. Sharma, K. J. Stebe, Biophys. J. 1998, 75, 880.
- 157J. Kolek, K. Sedlar, I. Provaznik, P. Patakova, Biotechnol. Biofuels 2016, 9, 14.
- 158T. Kotnik, D. Miklavcic, Biophys. J. 2006, 90, 480.
- 159Y. Hanyu, T. Yamada, G. Matsumoto, Biochemistry 1998, 37, 15376.
- 160H. Yamaguchi, H. Nakanishi, BBA-Biomembranes 1993, 1148, 179.
- 161T. F. Eibert, M. Alaydrus, F. Wilczewski, V. W. Hansen, IEEE Trans. Biomed. Eng. 1999, 46, 1013.
- 162J. R. Macdonald, W. B. Johnson, Impedance Spectroscopy: Theory, Experiment, and Applications, 2nd Editionk (Eds. ), Wiley-InterScience, Hoboken, 2006, pp. 1.
- 163C. Steinem, A. Janshoff, H. J. Galla, M. Sieber, Bioelectrochem. Bioenerg. 1997, 42, 213.
- 164A. E. Vallejo, C. A. Gervasi, Bioelectrochemistry 2002, 57, 1.
- 165L. J. C. Jeuken, S. A. Weiss, P. J. F. Henderson, S. D. Evans, R. J. Bushby, Anal. Chem. 2008, 80, 9084.
- 166G. Laputkova, M. Legin, J. Sabo, Chem. Listy 2010, 104, 353.
- 167T. Navratil, I. Sestakova, J. Jaklova Dytrtova, M. Jakl, V. Marecek, WSEAS Trans. Environ. Dev. 2010, 6, 208.
- 168T. Navratil, I. Sestakova, V. Marecek, in XXXI Moderni Elektrochemicke Metody (Modern Electrochemical Methods XXXI) (Eds: ), BEST Servis, Jetrichovice 2011, pp. 91.
- 169T. Navratil, I. Sestakova, V. Marecek, Int. J. Energy Environ. 2011, 5, 337.
- 170K. Novakova, T. Navratil, I. Sestakova, J. Langmaier, M. Heyrovsky, B. Zamecnikova, H. Vodickova, in XXXIV Moderni Elektrochemicke Metody (Modern Electrochemical Methods XXXIV) (Eds: ), Best Servis, Jetrichovice 2014, pp. 114.
- 171K. Novakova, T. Navratil, I. Sestakova, V. Marecek, J. Chylkova, in XXXIII Moderni Elektrochemicke Metody (Modern Electrochemical Methods XXXIII) (Eds: ), Best Servis, Jetrichovice 2013, pp. 128.
- 172C. Steinem, A. Janshoff, W. P. Ulrich, M. Sieber, H. J. Galla, BBA-Biomembranes 1996, 1279, 169.
- 173A. Lundgren, J. Hedlund, O. Andersson, M. Branden, A. Kunze, H. Elwing, F. Hook, Anal. Chem. 2011, 83, 7800.
- 174Z. Salamon, G. Lindblom, G. Tollin, Biophys. J. 2003, 84, 1796.
- 175P. Diao, D. L. Jiang, X. L. Cui, D. P. Gu, R. T. Tong, B. Zhong, Bioelectrochem. Bioenerg. 1999, 48, 469.
- 176P. E. Alvarez, C. A. Gervasi, A. E. Vallejo, J. Biol. Phys. 2007, 33, 421.
10.1007/s10867-008-9072-5 Google Scholar
- 177S. Gritsch, P. Nollert, F. Jahnig, E. Sackmann, Langmuir 1998, 14, 3118.
- 178T. N. Tun, P. J. Cameron, A. T. A. Jenkins, Biosens. Bioelectron. 2011, 28, 227.
- 179K. Kannisto, L. Murtomaki, T. Viitala, Colloids Surf. B 2011, 86, 298.
- 180S. Jaksch, O. Holderer, M. Gvaramia, M. Ohl, M. Monkenbusch, H. Frielinghaus, Sci. Rep. 2017, 7, 4417.
- 181C. Satriano, G. Lupo, C. Motta, C. D. Anfuso, P. Di Pietro, B. Kasemo, Colloids Surf. B 2017, 149, 48.
10.1016/j.colsurfb.2016.10.004 Google Scholar
- 182G. B. Soriano, R. da Silva Oliveira, F. F. Camilo, L. Caseli, J. Colloid Interface Sci. 2017, 496, 111.
10.1016/j.jcis.2017.02.017 Google Scholar
- 183F. Berthier, J. P. Diard, L. Pronzato, E. Walter, Automatica 1996, 32, 973.
- 184D. M. Miller, H. E. Findlay, O. Ces, R. H. Templer, P. J. Booth, Nanotechnology 2016, 27, 494004.
- 185M. Przybylo, D. Drabik, K. Szostak, T. Borowik, B. Klosgen, J. Dobrucki, A. F. Sikorski, M. Langner, Biochim. Biophys Acta 2017, 1859, 1301.
10.1016/j.bbamem.2017.04.025 Google Scholar
- 186M. M. Nerurkar, N. F. H. Ho, P. S. Burton, T. J. Vidmar, R. T. Borchardt, J. Pharm. Sci. 1997, 86, 813.
- 187H. L. Wu, H. K. Tsao, Y. J. Sheng, J. Chem. Phys. 2016, 144, 154904.
- 188T. Hianik, J. Biotechnol. 2000, 74, 189.
- 189T. Hianik, in Bioelectrochemistry. Fundamentals, Experimental Techniques and Applications (Ed: ), Wiley, Chichester, 2008, pp. 87.
- 190A. Janshoff, C. Steinem, Anal. Bioanal. Chem. 2006, 385, 433.
- 191S. Terrettaz, H. Vogel, MRS Bull. 2005, 30, 207.
- 192I. K. Vockenroth, D. Fine, A. Dodobalapur, A. T. A. Jenkins, I. Koper, Electrochem. Commun. 2008, 10, 323.
- 193G. Valincius, T. Meskauskas, F. Ivanauskas, Langmuir 2012, 28, 977.
- 194K. Lum, H. I. Ingolfsson, R. E. Koeppe, 2nd, O. S. Andersen, Biophys. J. 2017, 113, 1757.
- 195L. Q. Gu, S. Cheley, H. Bayley, J. Gen. Physiol. 2001, 118, 481.
- 196S. Cheley, M. S. Malghani, L. Z. Song, M. Hobaugh, J. E. Gouaux, J. Yang, H. Bayley, Protein Eng. 1997, 10, 1433.
- 197I. Sestakova, T. Navratil, B. Josypcuk, Electroanalysis 2016, 28, 2754.
- 198J. T. Connelly, S. Kondapalli, M. Skoupi, J. S. L. Parker, B. J. Kirby, A. J. Baeumner, Anal. Bioanal. Chem. 2012, 402, 315.
- 199K. A. Edwards, O. R. Bolduc, A. J. Baeumner, Curr. Opin. Chem. Biol. 2012, 16, 444.
- 200S. R. Nugen, P. J. Asiello, J. T. Connelly, A. J. Baeumner, Biosens. Bioelectron. 2009, 24, 2428.
- 201M. C. Sandstrom, L. M. Ickenstein, L. D. Mayer, K. Edwards, J. Control. Release 2005, 107, 131.
- 202D. Volodkin, H. Mohwald, J. C. Voegel, V. Ball, J. Controlled Release 2007, 117, 111.
- 203X. M. Liu, B. Yang, Y. L. Wang, J. Y. Wang, BBA-Biomembranes 2005, 1720, 28.
- 204G. L. Damhorst, C. E. Smith, E. M. Salm, M. M. Sobieraj, H. K. Ni, H. Kong, R. Bashir, Biomed. Microdevices 2013, 15, 895.
- 205F. Bordi, C. Cametti, S. Sennato, D. Viscomi, J. Colloid Interface Sci. 2006, 304, 512.
10.1016/j.jcis.2006.09.009 Google Scholar
- 206G. M. Chen, Z. W. Jiang, M. Yoshimoto, Y. L. Wei, Colloids Surf. B 2009, 74, 32.
10.1016/j.colsurfb.2009.06.026 Google Scholar
- 207J. Wegener, C. R. Keese, I. Giaever, Exp. Cell Res. 2000, 259, 158.