Skip to main content
SpringerLink
Log in

Biomimetic membranes for sensor and separation applications

  • Review
  • Published:
Analytical and Bioanalytical Chemistry Aims and scope Submit manuscript

Abstract

Biological membranes constitute the set of membranes defining boundaries and organelles in living cells—the structural and functional building blocks of all known living organisms. The integrity of the cell depends on its ability to separate inside from outside and yet at the same time allow massive transport of matter in and out the cell. Nature has elegantly met this challenge by developing membranes in the form of lipid bilayers in which specialized and highly efficient transport proteins are incorporated. This raises the question: is it possible to mimic biological membranes and create membrane-based sensor and/or separation devices? In the development of biomimetic sensor/separation technology, both channels (ion and water channels) and carriers (transporters) are important. Generally, each class of transport proteins conducts specific molecular species in and out of the cell while preventing the passage of others, a property critical for the overall conservation of the cells internal pH and salt concentration. Both ion and water channels are highly efficient membrane pore proteins capable of transporting solutes at very high rates, up to 109 molecules per second. Carrier proteins generally have a lower turnover but are capable of transport against gradients. For both classes of proteins, their unique flux-properties make them interesting as candidates in biomimetic sensor/separation devices. An ideal sensor/separation device requires the supporting biomimetic matrix to be virtually impermeable to anything but the solute in question. In practice, however, a biomimetic support matrix will generally have finite permeabilities to water, electrolytes, and non-electrolytes. The feasibility of a biomimetic device thus depends on the relative transport contribution from both protein and biomimetic support matrix. Also the stability of the incorporated protein must be addressed and the protein-biomimetic matrix must be encapsulated in order to protect it and make it sufficiently stable in a final application. Here I will review and discuss these challenges and how they are met in some current developments of biomimetic sensor/separation devices.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) Molecular biology of the cell, 4th edn. Garland Science, New York

    Google Scholar 

  2. Yeagle PL (ed) (2005) The structure of biological membranes. CRC Press, Boca Raton

    Google Scholar 

  3. Gennis RB (1989) Biomembranes. Molecular structure and function. Springer, New York

    Google Scholar 

  4. Andersen OS (1978) Permeability properties of unmodified lipid bilayer membranes. Membr Transp Biol 1:369–446

    CAS  Google Scholar 

  5. Hille B (1992) Ionic channels of excitable membranes, 2nd edn. Sinauer Associates, Sunderland

    Google Scholar 

  6. Jensen MO, Mouritsen OG (2006) Single-channel water permeabilities of Escherichia coli aquaporins AqpZ and GlpF. Biophys J 90:2270–2284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Stock D, Gibbons C, Arechaga I, Leslie AG, Walker JE (2000) The rotary mechanism of ATP synthase. Curr Opin Struct Biol 10:672–679

    Article  CAS  PubMed  Google Scholar 

  8. Dowhan W (1997) Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu Rev Biochem 66:199–232

    Article  CAS  PubMed  Google Scholar 

  9. Dopico AM, Tigyi GJ (2007) A glance at the structural and functional diversity of membrane lipids. Methods Mol Biol 400:1–13

    Article  CAS  PubMed  Google Scholar 

  10. Pomorski T, Menon AK (2006) Lipid flippases and their biological functions. Cell Mol Life Sci 63:2908–2921

    Article  CAS  PubMed  Google Scholar 

  11. Sackmann E (1984) Physical basis of trigger processes and membrane structures. In: Chapman D (ed) Biological membranes. Academic Press Inc., Ltd., London, pp 105–143

    Google Scholar 

  12. Vind-Kezunovic D, Nielsen CH, Wojewodzka U, Gniadecki R (2008) Line tension at lipid phase boundaries regulates formation of membrane vesicles in living cells. Biochim Biophys Acta 1778:2480–2486

    Article  CAS  PubMed  Google Scholar 

  13. Lundbæk JA (2006) Regulation of membrane protein function by lipid bilayer elasticity - a single molecule technology to measure the bilayer properties experienced by an embedded protein. J Phys Condens Matter 18:S1305–S1344

    Article  CAS  PubMed  Google Scholar 

  14. Nielsen CH (2009) Lipid-protein interactions in biomembranes. In: Bohr HG (ed) Handbook of biophysics. Wiley, Berlin, pp 329–358

    Google Scholar 

  15. Niggli V (2005) Regulation of protein activities by phosphoinositide phosphates. Annu Rev Cell Dev Biol 21:57–79

    Article  CAS  PubMed  Google Scholar 

  16. Andersen OS, Koeppe RE 2nd (2007) Bilayer thickness and membrane protein function: an energetic perspective. Annu Rev Biophys Biomol Struct 36:107–130

    Article  CAS  PubMed  Google Scholar 

  17. Nielsen C, Goulian M, Andersen OS (1998) Energetics of inclusion-induced bilayer deformations. Biophys J 74:1966–1983

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Mueller P, Rudin DO, Tien HT, Wescott WC (1962) Reconstitution of cell membrane structure in vitro and its transformation into an excitable system. Nature 194:979–980

    Article  CAS  PubMed  Google Scholar 

  19. Montal M, Mueller P (1972) Formation of biomolecular membranes from lipid monolayers and a study of their electrical properties. Proc Nat Acad Sci USA 69:3561–3566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. White SH (1978) Formation of “solvent-free” black lipid bilayer membranes from glyceryl monooleate dispersed in squalene. Biophys J 23:337–347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Cruz A, Perez-Gil J (2007) Langmuir films to determine lateral surface pressure on lipid segregation. Methods Mol Biol 400:439–457

    Article  CAS  PubMed  Google Scholar 

  22. Lin WC, Blanchette CD, Ratto TV, Longo ML (2007) Lipid domains in supported lipid bilayer for atomic force microscopy. Methods Mol Biol 400:503–513

    Article  CAS  PubMed  Google Scholar 

  23. Watts TH, Brian AA, Kappler JW, Marrack P, McConnell HM (1984) Antigen presentation by supported planar membranes containing affinity-purified I-Ad. Proc Natl Acad Sci U S A 81:7564–7568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. McConnell HM, Watts TH, Weis RM, Brian AA (1986) Supported planar membranes in studies of cell-cell recognition in the immune system. Biochim Biophys Acta 864:95–106

    Article  CAS  PubMed  Google Scholar 

  25. Lin WC, Blanchette CD, Ratto TV, Longo ML (2006) Lipid asymmetry in DLPC/DSPC-supported lipid bilayers: a combined AFM and fluorescence microscopy study. Biophys J 90:228–237

    Article  CAS  PubMed  Google Scholar 

  26. Elie-Caille C, Fliniaux O, Pantigny J, Maziere JC, Bourdillon C (2005) Self-assembly of solid-supported membranes using a triggered fusion of phospholipid-enriched proteoliposomes prepared from the inner mitochondrial membrane. Langmuir 21:4661–4668

    Article  CAS  PubMed  Google Scholar 

  27. Ti Tien H (1974) Bilayer lipid membranes (BML) theory and practice. Marcel Dekker Inc, New York

    Google Scholar 

  28. Tien HT, Ottova-Leitmannova A (eds) (2003) Planar lipid bilayers (BLMs) and their applications. Elsevier, Amsterdam

    Google Scholar 

  29. Ottova A, Tien HT (2002) The 40th anniversary of bilayer lipid membrane research. Bioelectrochemistry 56:171–173

    Article  CAS  PubMed  Google Scholar 

  30. Mayer M, Kriebel JK, Tosteson MT, Whitesides GM (2003) Microfabricated Teflon membranes for low-noise recordings of ion channels in planar lipid bilayers. Biophys J 85:2684–2695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Suzuki H, Tabata KV, Noji H, Takeuchi S (2006) Highly reproducible method of planar lipid bilayer reconstitution in polymethyl methacrylate microfluidic chip. Langmuir 22:1937–1942

    Article  CAS  PubMed  Google Scholar 

  32. Malmstadt N, Nash MA, Purnell RF, Schmidt JJ (2006) Automated formation of lipid-bilayer membranes in a microfluidic device. Nano Lett 6:1961–1965

    Article  CAS  PubMed  Google Scholar 

  33. Zagnoni M, Sandison ME, Morgan H (2009) Microfluidic array platform for simultaneous lipid bilayer membrane formation. Biosens Bioelectron 24:1235–1240

    Article  CAS  PubMed  Google Scholar 

  34. Sandison ME, Zagnoni M, Abu-Hantash M, Morgan H (2007) Micromachined glass apertures for artificial lipid bilayer formation in a microfluidic system. J Micromech Microeng 17:S189–S196

    Article  CAS  Google Scholar 

  35. Hansen JS, Perry ME, Vogel J, Vissing T, Geschke O, Emneus J, Nielsen CH (2009) Development of an automation technique for the establishment of functional lipid bilayer arrays. J Micromech Microeng 19:025014

    Article  CAS  Google Scholar 

  36. Vogel J, Perry ME, Hansen JS, Bollinger P-Y, Nielsen CH, Geschke O (2009) Support structure for biomimetic applications. J Micromech Microeng 19:025026

    Article  CAS  Google Scholar 

  37. van de Vossenberg JL, Driessen AJ, Konings WN (1998) The essence of being extremophilic: the role of the unique archaeal membrane lipids. Extremophiles 2:163–170

    Article  PubMed  Google Scholar 

  38. Schleper C, Puehler G, Holz I, Gambacorta A, Janekovic D, Santarius U, Klenk HP, Zillig W (1995) Picrophilus gen. nov., fam. nov.: a novel aerobic, heterotrophic, thermoacidophilic genus and family comprising archaea capable of growth around pH 0. J Bacteriol 177:7050–7059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. van de Vossenberg J, Driessen AJ, Zillig W, Konings WN (1998) Bioenergetics and cytoplasmic membrane stability of the extremely acidophilic, thermophilic archaeon Picrophilus oshimae. Extremophiles 2:67–74

    Article  PubMed  Google Scholar 

  40. De Rosa M, Gambacorta A (1988) The lipids of archaebacteria. Prog Lipid Res 27:153–175

    Article  PubMed  Google Scholar 

  41. Dannenmuller O, Arakawa K, Eguchi T, Kakinuma K, Blanc S, Albrecht AM, Schmutz M, Nakatani Y, Ourisson G (2000) Membrane properties of archaeal macrocyclic diether phospholipids. Chemistry 6:645–654

    Article  CAS  PubMed  Google Scholar 

  42. Chang EL (1994) Unusual thermal stability of liposomes made from bipolar tetraether lipids. Biochem Biophys Res Commun 202:673–679

    Article  CAS  PubMed  Google Scholar 

  43. Holland DP, Struts AV, Brown MF, Thompson DH (2008) Bolalipid membrane structure revealed by solid-state 2H NMR spectroscopy. J Am Chem Soc 130:4584–4585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Wiess-Wichert C, Smetazko M, Valina-Saba M, Schalkhammer T (1997) A new analytical device based on gated ion channels: a peptide-channel biosensor. J Biol Screening 2:11–18

    Article  Google Scholar 

  45. Cornell BA, Braach-Maksvytis VL, King LG, Osman PD, Raguse B, Wieczorek L, Pace RJ (1997) A biosensor that uses ion-channel switches. Nature 387:580–583

    Article  CAS  PubMed  Google Scholar 

  46. Febo-Ayala W, Morera-Felix SL, Hrycyna CA, Thompson DH (2006) Functional reconstitution of the integral membrane enzyme, isoprenylcysteine carboxyl methyltransferase, in synthetic bolalipid membrane vesicles. Biochemistry 45:14683–14694

    Article  CAS  PubMed  Google Scholar 

  47. Svenson S, Thompson DH (1998) Facile and efficient synthesis of bolaamphiphilic tetraether phosphocholines. J Org Chem 63:7180–7182

    Article  CAS  PubMed  Google Scholar 

  48. Meier W, Nardin C, Winterhalter M (2000) Reconstitution of channel proteins in (polymerized) ABA triblock copolymer membranes. Angew Chem Int Ed Engl 39:4599–4602

    Article  CAS  PubMed  Google Scholar 

  49. Ho D, Chu B, Lee H, Montemagno C (2004) Protein-driven transduction across polymeric biomembranes. Nanotechnology 15:1084–1094

    Article  CAS  Google Scholar 

  50. Kumar M, Grzelakowski M, Zilles J, Clark M, Meier W (2007) Highly permeable polymeric membranes based on the incorporation of the functional water channel protein Aquaporin Z. Proc Natl Acad Sci U S A 104:20719–20724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Reimhult E, Kumar K (2008) Membrane biosensor platforms using nano- and microporous supports. Trends Biotechnol 26:82–89

    Article  CAS  PubMed  Google Scholar 

  52. Separovic F, Cornell BA (2007) Gated ion channel-based biosensor device. In: Chung SH, Andersen OS, Krishnamurthy V (eds) Biological membrane ion channels. Springer, New York, pp 595–622

    Chapter  Google Scholar 

  53. Eray M, Dogan NS, Reiken SR, Sutisna H, Van Wie BJ, Koch AR, Moffett DF, Silber M, Davis WC (1995) A highly stable and selective biosensor using modified nicotinic acetylcholine receptor (nAChR). Biosystems 35:183–188

    Article  CAS  PubMed  Google Scholar 

  54. Zhang L, Granick S (2006) Dynamical heterogeneity in supported lipid bilayers. MRS Bull 31:527–531

    Article  CAS  Google Scholar 

  55. Tanaka M (2006) Polymer-supported membranes: physical models of cell surfaces. MRS Bull 31:513–520

    Article  CAS  Google Scholar 

  56. Parikh AN, Groves JT (2006) Materials science of supported lipid membranes. MRS Bull 31:507–512

    Article  CAS  Google Scholar 

  57. Sackmann E, Tanaka M (2000) Supported membranes on soft polymer cushions: fabrication, characterization and applications. Trends Biotechnol 18:58–64

    Article  CAS  PubMed  Google Scholar 

  58. Sackmann E (1996) Supported membranes: scientific and practical applications. Science 271:43–48

    Article  CAS  PubMed  Google Scholar 

  59. Rossi C, Chopineau J (2007) Biomimetic tethered lipid membranes designed for membrane-protein interaction studies. Eur Biophys J 36:955–965

    Article  CAS  PubMed  Google Scholar 

  60. Koper I (2007) Insulating tethered bilayer lipid membranes to study membrane proteins. Mol Biosyst 3:651–657

    Article  CAS  PubMed  Google Scholar 

  61. Gagner J, Johnson H, Watkins E, Li Q, Terrones M, Majewski J (2006) Carbon nanotube supported single phospholipid bilayer. Langmuir 22:10909–10911

    Article  CAS  PubMed  Google Scholar 

  62. Castellana ET, Cremer PS (2006) Solid supported lipid bilayers: from biophysical studies to sensor design. Surf Sci Rep 61:429–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Murray DH, Tamm LK, Kiessling V (2009) Supported double membranes. J Struct Biol (in press)

  64. Löfås S, Johnsson BJ (1990) A novel hydrogel matrix on gold surfaces in surface plasmon resonance sensors for fast and efficient covalent immobilization of ligands. Chem Soc Chem Commun 21:1526–1528

    Article  Google Scholar 

  65. Dong Y, Scott Phillips K, Chen Q (2006) Immunosensing of Staphylococcus enterotoxin B (SEB) in milk with PDMS microfluidic systems using reinforced supported bilayer membranes. Lab Chip 6:675–681

    Article  CAS  PubMed  Google Scholar 

  66. Steltze M (1993) On the application of supported bilayers as receptive layers for biosensors with electrical detection. J Phys Chem 97:2974–2981

    Article  Google Scholar 

  67. Becucci L, Leon RR, Moncelli MR, Rovero P, Guidelli R (2006) Electrochemical investigation of melittin reconstituted into a mercury-supported lipid bilayer. Langmuir 22:6644–6650

    Article  CAS  PubMed  Google Scholar 

  68. Becucci L, Moncelli MR, Naumann R, Guidelli R (2005) Potassium ion transport by valinomycin across a Hg-supported lipid bilayer. J Am Chem Soc 127:13316–13323

    Article  CAS  PubMed  Google Scholar 

  69. Becucci L, Moncelli MR, Guidelli R (2006) Impedance spectroscopy of OmpF porin reconstituted into a mercury-supported lipid bilayer. Langmuir 22:1341–1346

    Article  CAS  PubMed  Google Scholar 

  70. Ho D, Chu B, Lee H, Montemagno C (2004) Protein-driven energy transduction across polymeric biomembranes. Nanotechnology 15:1084–1094

    Article  CAS  Google Scholar 

  71. Holden MA, Needham D, Bayley H (2007) Functional bionetworks from nanoliter water droplets. J Am Chem Soc 129:8650–8655

    Article  CAS  PubMed  Google Scholar 

  72. Funakoshi K, Suzuki H, Takeuchi S (2006) Lipid bilayer formation by contacting monolayers in a microfluidic device for membrane protein analysis. Anal Chem 78:8169–8174

    Article  CAS  PubMed  Google Scholar 

  73. Zagnoni M, Sandison ME, Marius P, Morgan H (2009) Bilayer lipid membranes from falling droplets. Anal Bioanal Chem 393:1601–1605

    Article  CAS  PubMed  Google Scholar 

  74. Andersen OS, Green WN, Urban BW (1986) Ion conduction through sodium channels in planar lipid bilayers. Ion Channel Reconstitution 385-404

  75. Benz R, Janko K (1976) Voltage-dependent capacitance relaxation of lipid bilayer membranes. Effects of membrane composition. Biochim Biophys Acta 455:721–738

    Article  CAS  PubMed  Google Scholar 

  76. Jeon TJ, Malmstadt N, Schmidt JJ (2006) Hydrogel-encapsulated lipid membranes. J Am Chem Soc 128:42–43

    Article  CAS  PubMed  Google Scholar 

  77. Jeon TJ, Poulos JL, Schmidt J (2008) Storable and transportable lipid bilayer membrane precursor. Biophys J Abstracts 337a

  78. Shim JW, Gu LQ (2007) Stochastic sensing on a modular chip containing a single-ion channel. Anal Chem 79:2207–2213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Schuster B, Sleytr UB, Diederich A, Bahr G, Winterhalter M (1999) Probing the stability of S-layer-supported planar lipid membranes. Eur Biophys J 28:583–590

    Article  CAS  PubMed  Google Scholar 

  80. Schuster B, Sleytr UB (2002) The effect of hydrostatic pressure on S-layer-supported lipid membranes. Biochim Biophys Acta 1563:29–34

    Article  CAS  PubMed  Google Scholar 

  81. Sleytr UB, Egelseer EM, Ilk N, Pum D, Schuster B (2007) S-Layers as a basic building block in a molecular construction kit. FEBS J 274:323–334

    Article  CAS  PubMed  Google Scholar 

  82. Kang XF, Cheley S, Rice-Ficht AC, Bayley H (2007) A storable encapsulated bilayer chip containing a single protein nanopore. J Am Chem Soc 129:4701–4705

    Article  CAS  PubMed  Google Scholar 

  83. Kaufman Y, Berman A, Freger V (2008) The use of NF membranes as substrates for supported phospholipid bilayers. ICOM 2008 Poster Session Proceedings, International Congress on Membranes and Membrane Processes, Honolulu, Hawaii, July 12–18, p 560

  84. Ndoni S, Vigild ME, Berg RH (2003) Nanoporous materials with spherical and gyroid cavities created by quantitative etching of polydimethylsiloxane in polystyrene-polydimethylsiloxane block copolymers. J Am Chem Soc 125:13366–13367

    Article  CAS  PubMed  Google Scholar 

  85. Hansen MS, Vigild ME, Berg RH, Ndoni S (2004) Nanoporous crosslinked polyisoprene from polyisoprene - Polydimethylsiloxane block copolymer. Polymer Bulletin 51:403–409

    Article  CAS  Google Scholar 

  86. Lodge TP (2003) Block copolymers: past successes and future challenges. Macromol Chem Phys 204:265–273

    Article  CAS  Google Scholar 

  87. Park C, Yoon J, Thomas EL (2003) Enabling nanotechnology with self assembled block copolymer patterns. Polymer 44:6725–6760

    Article  CAS  Google Scholar 

  88. Lian J, Ding S, Cai J, Zhang D, Xu Z, Wang X (2009) Improving aquaporin Z expression in Escherichia coli by fusion partners and subsequent condition optimization. Appl Microbiol Biotechnol 82:463–470

    Article  CAS  PubMed  Google Scholar 

  89. Kiefer H, Krieger J, Olszewski JD, Von Heijne G, Prestwich GD, Breer H (1996) Expression of an olfactory receptor in Escherichia coli: purification, reconstitution, and ligand binding. Biochemistry 35:16077–16084

    Article  CAS  PubMed  Google Scholar 

  90. Tate CG (2001) Overexpression of mammalian integral membrane proteins for structural studies. FEBS Lett 504:94–98

    Article  CAS  PubMed  Google Scholar 

  91. Chen GQ, Gouaux JE (1996) Overexpression of bacterio-opsin in Escherichia coli as a water-soluble fusion to maltose binding protein: efficient regeneration of the fusion protein and selective cleavage with trypsin. Protein Sci 5:456–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. LaVallie ER, DiBlasio EA, Kovacic S, Grant KL, Schendel PF, McCoy JM (1993) A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. coli cytoplasm. Biotechnology (NY) 11:187–193

    Article  CAS  Google Scholar 

  93. Nygren PA, Stahl S, Uhlen M (1994) Engineering proteins to facilitate bioprocessing. Trends Biotechnol 12:184–188

    Article  CAS  PubMed  Google Scholar 

  94. Pryor KD, Leiting B (1997) High-level expression of soluble protein in Escherichia coli using a His6-tag and maltose-binding-protein double-affinity fusion system. Protein Exp Purif 10:309–319

    Article  CAS  Google Scholar 

  95. Samuelsson E, Moks T, Nilsson B, Uhlen M (1994) Enhanced in vitro refolding of insulin-like growth factor I using a solubilizing fusion partner. Biochemistry 33:4207–4211

    Article  CAS  PubMed  Google Scholar 

  96. Power RF, Conneely OM, McDonnell DP, Clark JH, Butt TR, Schrader WT, O’Malley BW (1990) High level expression of a truncated chicken progesterone receptor in Escherichia coli. J Biol Chem 265:1419–1424

    CAS  PubMed  Google Scholar 

  97. Woolley GA, Wallace BA (1992) Model ion channels: gramicidin and alamethicin. J Membrane Biol 129:109–136

    CAS  Google Scholar 

  98. Becucci L, Carbone MV, Biagiotti T, D’Amico M, Olivotto M, Guidelli R (2008) Incorporation of the HERG potassium channel in a mercury supported lipid bilayer. J Phys Chem B 112:1315–1319

    Article  CAS  PubMed  Google Scholar 

  99. Racker E (1972) Reconstitution of cytochrome oxidase vesicles and conferral of sensitivity to energy transfer inhibitors. J Membr Biol 10:221–235

    Article  CAS  PubMed  Google Scholar 

  100. Racker E (1973) A new procedure for the reconstitution of biologically active phospholipid vesicles. Biochem Biophys Res Commun 55:224–230

    Article  CAS  PubMed  Google Scholar 

  101. Hengen P (1995) Purification of His-Tag fusion proteins from Escherichia coli. Trends Biochem Sci 20:285–286

    Article  CAS  PubMed  Google Scholar 

  102. Deniaud A, Rossi C, Berquand A, Homand J, Campagna S, Knoll W, Brenner C, Chopineau J (2007) Voltage-dependent anion channel transports calcium ions through biomimetic membranes. Langmuir 23:3898–3905

    Article  CAS  PubMed  Google Scholar 

  103. Sheibani N (1999) Prokaryotic gene fusion expression systems and their use in structural and functional studies of proteins. Prep Biochem Biotechnol 29:77–90

    Article  CAS  PubMed  Google Scholar 

  104. Terpe K (2003) Overview of tag protein fusions: from molecular and biochemical fundamentals to commercial systems. Appl Microbiol Biotechnol 60:523–533

    Article  CAS  PubMed  Google Scholar 

  105. Nardin C, Thoeni S, Widmer J, Winterhalter M, Meier W (2000) Chem Commun (Camb) 15:1433

    Article  Google Scholar 

  106. Choi HJ, Montemagno CD (2005) Artificial organelle: ATP synthesis from cellular mimetic polymersomes. Nano Lett 5:2538–2542

    Article  CAS  PubMed  Google Scholar 

  107. Choi HJ, Montemagno CD (2005) Nanotechnology 16:1589

    Article  CAS  Google Scholar 

  108. Woodbury DJ, Miller C (1990) Nystatin-induced liposome fusion. A versatile approach to ion channel reconstitution into planar bilayers. Biophys J 58:833–839

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Cass A, Finkelstein A, Krespi V (1970) The ion permeability induced in thin lipid membranes by the polyene antibiotics nystatin and amphotericin B. J Gen Physiol 56:100–124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Moreno-Bello M, Bonilla-Marin M, Gonzalez-Beltran C (1988) Distribution of pore sizes in black lipid membranes treated with nystatin. Biochim Biophys Acta 944:97–100

    Article  CAS  PubMed  Google Scholar 

  111. Woodbury DJ (1999) Nystatin/ergosterol method for reconstituting ion channels into planar lipid bilayers. Methods Enzymol 294:319–339

    Article  CAS  PubMed  Google Scholar 

  112. Kalb E, Frey S, Tamm LK (1992) Formation of supported planar bilayers by fusion of vesicles to supported phospholipid monolayers. Biochim Biophys Acta 1103:307–316

    Article  CAS  PubMed  Google Scholar 

  113. Crane JM, Tamm LK (2007) Fluorescence microscopy to study domains in supported lipid bilayers. Methods Mol Biol 400:481–488

    Article  CAS  PubMed  Google Scholar 

  114. Malinin VS, Frederik P, Lentz BR (2002) Osmotic and curvature stress affect PEG-induced fusion of lipid vesicles but not mixing of their lipids. Biophys J 82:2090–2100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Lentz BR (1994) Polymer-induced membrane fusion: potential mechanism and relation to cell fusion events. Chem Phys Lipids 73:91–106

    Article  CAS  PubMed  Google Scholar 

  116. Simberg D, Weisman S, Talmon Y, Barenholz Y (2004) DOTAP (and other cationic lipids): chemistry, biophysics, and transfection. Crit Rev Ther Drug Carrier Syst 21:257–317

    Article  CAS  PubMed  Google Scholar 

  117. Weber T, Zemelman BV, McNew JA, Westermann B, Gmachl M, Parlati F, Sollner TH, Rothman JE (1998) SNAREpins: minimal machinery for membrane fusion. Cell 92:759–772

    Article  CAS  PubMed  Google Scholar 

  118. Wang T, Smith EA, Chapman ER, Weisshaar JC (2009) Lipid mixing and content release in single-vesicle, SNARE-driven fusion assay with 1–5 ms resolution. Biophys J 96:4122–4131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Van Gelder P, Dumas F, Rosenbusch JP, Winterhalter M (2000) Oriented channels reveal asymmetric energy barriers for sugar translocation through maltoporin of Escherichia coli. Eur J Biochem 267:79–84

    Article  PubMed  Google Scholar 

  120. Dargent B, Hofmann W, Pattus F, Rosenbusch JP (1986) The selectivity filter of voltage-dependent channels formed by phosphoporin (PhoE protein) from E. coli. EMBO J 5:773–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Van Gelder P, Saint N, van Boxtel R, Rosenbusch JP, Tommassen J (1997) Pore functioning of outer membrane protein PhoE of Escherichia coli: mutagenesis of the constriction loop L3. Protein Eng 10:699–706

    Article  PubMed  Google Scholar 

  122. Bonhivers M, Ghazi A, Boulanger P, Letellier L (1996) FhuA, a transporter of the Escherichia coli outer membrane, is converted into a channel upon binding of bacteriophage T5. EMBO J 15:1850–1856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Miedema H, Vrouenraets M, Wierenga J, Gillespie D, Eisenberg B, Meijberg W, Nonner W (2006) Ca2+ selectivity of a chemically modified OmpF with reduced pore volume. Biophys J 91:4392–4400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Miedema H, Vrouenraets M, Wierenga J, Eisenberg B, Schirmer T, Basle A, Meijberg W (2006) Conductance and selectivity fluctuations in D127 mutants of the bacterial porin OmpF. Eur Biophys J 36:13–22

    Article  CAS  PubMed  Google Scholar 

  125. Vrouenraets M, Wierenga J, Meijberg W, Miedema H (2006) Chemical modification of the bacterial porin OmpF: gain of selectivity by volume reduction. Biophys J 90:1202–1211

    Article  CAS  PubMed  Google Scholar 

  126. Fung BK, Hubbell WL (1978) Organization of rhodopsin in photoreceptor membranes. 1. Proteolysis of bovine rhodopsin in native membranes and the distribution of sulfhydryl groups in the fragments. Biochemistry 17:4396–4402

    Article  CAS  PubMed  Google Scholar 

  127. Degrip WJ, Vanoostrum J, Bovee-Geurts PH (1998) Selective detergent-extraction from mixed detergent/lipid/protein micelles, using cyclodextrin inclusion compounds: a novel generic approach for the preparation of proteoliposomes. Biochem J 330(Pt 2):667–674

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Cornelius F (1991) Functional reconstitution of the sodium pump. Kinetics of exchange reactions performed by reconstituted Na/K-ATPase. Biochim Biophys Acta 1071:19–66

    Article  CAS  PubMed  Google Scholar 

  129. Niu L, Kim JM, Khorana HG (2002) Structure and function in rhodopsin: asymmetric reconstitution of rhodopsin in liposomes. Proc Natl Acad Sci U S A 99:13409–13412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Rigaud JL, Paternostre MT, Bluzat A (1988) Mechanisms of membrane protein insertion into liposomes during reconstitution procedures involving the use of detergents. 2. Incorporation of the light-driven proton pump bacteriorhodopsin. Biochemistry 27:2677–2688

    Article  CAS  PubMed  Google Scholar 

  131. Happe M, Teathera RM, Overath P, Knobling A, Oesterhelt D (1977) Direction of proton translocation in proteoliposomes formed from purple membrane and acidic lipids depends on the pH during reconstitution. Biochim Biophys Acta 465:415–420

    Article  CAS  PubMed  Google Scholar 

  132. Wang Z, Bai J, Xu Y (2008) The effect of charged lipids on bacteriorhodopsin membrane reconstitution and its photochemical activities. Biochem Biophys Res Commun 371:814–817

    Article  CAS  PubMed  Google Scholar 

  133. Choi HJ, Germain J, Montemagno CD (2006) Effects of different reconstitution procedures on membrane protein activities in proteopolymerosomes. Nanotechnology 17:1825–1830

    Article  CAS  Google Scholar 

  134. Karlsson OP, Lofas S (2002) Flow-mediated on-surface reconstitution of G-protein coupled receptors for applications in surface plasmon resonance biosensors. Anal Biochem 300:132–138

    Article  CAS  PubMed  Google Scholar 

  135. Stenlund P, Babcock GJ, Sodroski J, Myszka DG (2003) Capture and reconstitution of G protein-coupled receptors on a biosensor surface. Anal Biochem 316:243–250

    Article  CAS  PubMed  Google Scholar 

  136. Bowie JU (2001) Stabilizing membrane proteins. Curr Opin Struct Biol 11:397–402

    Article  CAS  PubMed  Google Scholar 

  137. Finkelstein A (ed) (1987) Water movement through lipid bilayers, pores, and plasma membranes. Theory and reality. Wiley-Interscience, New York

  138. Finkelstein A, Cass A (1967) Effect of cholesterol on the water permeability of thin lipid membranes. Nature 216:717–718

    Article  CAS  PubMed  Google Scholar 

  139. Overton E (1895) Über die osmotischen Eigenschaften der lebenden Pflanzen und Tierzelle. Visch Naturf Ges Zurich 40:159–201

    Google Scholar 

  140. Nagle JF, Tristram-Nagle S (2000) Structure of lipid bilayers. Biochim Biophys Acta 1469:159–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Nagle JF, Mathai JC, Zeidel ML, Tristram-Nagle S (2008) Theory of passive permeability through lipid bilayers. J Gen Physiol 131:77–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Mathai JC, Tristram-Nagle S, Nagle JF, Zeidel ML (2008) Structural determinants of water permeability through the lipid membrane. J Gen Physiol 131:69–76

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Brockman H (1994) Dipole potential of lipid membranes. Chem Phys Lipids 73:57–79

    Article  CAS  PubMed  Google Scholar 

  144. McLaughlin S (1977) Electrostatic potentials at membrane-solution interfaces. Curr Top Membr Transp 9:71–144

    Article  CAS  Google Scholar 

  145. Hladky SB (1979) The carrier mechanism. In: Bronner F, Kleinzeller A (eds) Current topics in membranes and transport. Academic Press, New York, pp 54–164

    Google Scholar 

  146. Barchfeld GL, Deamer DW (1985) The effect of general anaesthetics on the proton and potassium permeabilities of liposomes. Biochim Biophys Acta 819:161–169

    Article  CAS  PubMed  Google Scholar 

  147. Papahadjopoulos D (1971) Na + -K + discrimination by "pure" phospholipid membranes. Biochim Biophys Acta 241:254–259

    Article  CAS  PubMed  Google Scholar 

  148. Papahadjopoulos D, Nir S, Oki S (1972) Permeability properties of phospholipid membranes: effect of cholesterol and temperature. Biochim Biophys Acta 266:561–583

    Article  CAS  PubMed  Google Scholar 

  149. Deamer DW, Volkov AG (1995) Protein permeation of lipid bilayers. In: Disalvo EA, Simon SA (eds) Permeability and stability of lipid bilayers. CRC Press, Boca Raton, pp 161–177

    Google Scholar 

  150. Nagle JF, Morowitz HJ (1978) Molecular mechanisms for proton transport in membranes. Proc Natl Acad Sci U S A 75:298–302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Haines TH (2001) Do sterols reduce proton and sodium leaks through lipid bilayers? Prog Lipid Res 40:299–324

    Article  CAS  PubMed  Google Scholar 

  152. Paula S, Volkov AG, Van Hoek AN, Haines TH, Deamer DW (1996) Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness. Biophys J 70:339–348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Haines TH (1994) Water transport across biological membranes. FEBS Lett 346:115–122

    Article  CAS  PubMed  Google Scholar 

  154. Haines TH, Liebovitch LS (1995) A molecular mechanism for the transport of water across phospholipid bilayer. In: Disalvo EA, Simon SA (eds) Permeability and stability of lipid bilayers. CRC Press, Boca Raton, pp 123–136

    Google Scholar 

  155. Rog T, Pasenkiewicz-Gierula M, Vattulainen I, Karttunen M (2009) Ordering effects of cholesterol and its analogues. Biochim Biophys Acta 1788:97–121

    Article  CAS  PubMed  Google Scholar 

  156. Kleemann G, Kellner R, Poralla K (1994) Purification and properties of the squalene-hopene cyclase from Rhodopseudomonas palustris, a purple non-sulfur bacterium producing hopanoids and tetrahymanol. Biochim Biophys Acta 1210:317–320

    Article  CAS  PubMed  Google Scholar 

  157. Sahm H, Rohmer M, Bringer-Meyer S, Sprenger GA, Welle R (1993) Biochemistry and physiology of hopanoids in bacteria. Adv Microb Physiol 35:247–273

    Article  CAS  PubMed  Google Scholar 

  158. Gliozzi A, Relini A, Lee-Gau Chong P (2002) Structure and permeability properties of biomimetic membranes of archaeal bolaform tetraether lipids. J. Membr. Sci. 206:131–147

    Article  CAS  Google Scholar 

  159. Sikkema J, de Bont JA, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222

    CAS  PubMed  PubMed Central  Google Scholar 

  160. Valtersson C, van Duyn G, Verkleij AJ, Chojnacki T, de Kruijff B, Dallner G (1985) The influence of dolichol, dolichol esters, and dolichyl phosphate on phospholipid polymorphism and fluidity in model membranes. J Biol Chem 260:2742–2751

    CAS  PubMed  Google Scholar 

  161. Monti JA, Christian ST, Schutzbach JS (1987) Effects of dolichol on membrane permeability. Biochim Biophys Acta 905:133–142

    Article  CAS  PubMed  Google Scholar 

  162. Katsikas H, Quinn PJ (1983) Fluorescence probe studies of the distribution of ubiquinone homologues in bilayers of dipalmitoylglycerophosphocholine. Eur J Biochem 131:607–612

    Article  CAS  PubMed  Google Scholar 

  163. Fitch CD, Folkers K (1967) Coenzyme Q and the stability of biological membranes. Biochem Biophys Res Commun 26:128–131

    Article  CAS  PubMed  Google Scholar 

  164. Stillwell W, Dallman T, Dumaual AC, Crump FT, Jenski LJ (1996) Cholesterol versus alpha-tocopherol: effects on properties of bilayers made from heteroacid phosphatidylcholines. Biochemistry 35:13353–13362

    Article  CAS  PubMed  Google Scholar 

  165. Shannon MA, Bohn PW, Elimelech M, Georgiadis JG, Marinas BJ, Mayes AM (2008) Science and technology for water purification in the coming decades. Nature 452:301–310

    Article  CAS  PubMed  Google Scholar 

  166. Skou JC, Esmann M (1992) The Na,K-ATPase. J Bioenerg Biomembr 24:249–261

    CAS  PubMed  Google Scholar 

  167. Seifert K, Fendler K, Bamberg E (1993) Charge transport by ion translocating membrane proteins on solid supported membranes. Biophys J 64:384–391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Pintschovius J, Fendler K, Bamberg E (1999) Charge translocation by the Na+/K+-ATPase investigated on solid supported membranes: cytoplasmic cation binding and release. Biophys J 76:827–836

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Pintschovius J, Fendler K (1999) Charge translocation by the Na+/K+-ATPase investigated on solid supported membranes: rapid solution exchange with a new technique. Biophys J 76:814–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Zebrowska A, Krysinski P (2004) Incorporation of Na(+), K(+)-ATP-ase into the thiolipid biomimetic assemblies via the fusion of proteoliposomes. Langmuir 20:11127–11133

    Article  CAS  PubMed  Google Scholar 

  171. Tadini-Buoninsegni F, Bartolommei G, Moncelli MR, Fendler K (2008) Charge transfer in P-type ATPases investigated on planar membranes. Arch Biochem Biophys 476:75–86

    Article  CAS  PubMed  Google Scholar 

  172. Tadini Buoninsegni F, Bartolommei G, Moncelli MR, Inesi G, Guidelli R (2004) Time-resolved charge translocation by sarcoplasmic reticulum Ca-ATPase measured on a solid supported membrane. Biophys J 86:3671–3686

    Article  CAS  PubMed  Google Scholar 

  173. Nielsen CH, Abdali S, Lundbæk JA, Cornelius F (2005) Raman spectroscopy of conformational changes in membrane-bound sodium potassium ATPase. Spectroscopy 22:52–63

    Google Scholar 

  174. Mulkidjanian AY, Makarova KS, Galperin MY, Koonin EV (2007) Inventing the dynamo machine: the evolution of the F-type and V-type ATPases. Nat Rev Microbiol 5:892–899

    Article  CAS  PubMed  Google Scholar 

  175. Boyer PD (1997) The ATP synthase-a splendid molecular machine. Annu Rev Biochem 66:717–749

    Article  CAS  PubMed  Google Scholar 

  176. Jefferies KC, Cipriano DJ, Forgac M (2008) Function, structure and regulation of the vacuolar (H+)-ATPases. Arch Biochem Biophys 476:33–42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Cipriano DJ, Wang Y, Bond S, Hinton A, Jefferies KC, Qi J, Forgac M (2008) Structure and regulation of the vacuolar ATPases. Biochim Biophys Acta 1777:599–604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Ueno H, Suzuki T, Kinosita K Jr, Yoshida M (2005) ATP-driven stepwise rotation of FoF1-ATP synthase. Proc Natl Acad Sci U S A 102:1333–1338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Tutus M, Rossetti FF, Schneck E, Fragneto G, Förster F, Ricther R, Nawroth T, Tanaka M (2008) Orientation-selective incorporation of transmemrbane F0F1 ATP synthase complex from Micrococcus luteus in polymer-supported membranes. Macromol Biosci 8:1034–1043

    Article  CAS  PubMed  Google Scholar 

  180. Naumann R, Baumgart T, Graber P, Jonczyk A, Offenhausser A, Knoll W (2002) Proton transport through a peptide-tethered bilayer lipid membrane by the H(+)-ATP synthase from chloroplasts measured by impedance spectroscopy. Biosens Bioelectron 17:25–34

    Article  CAS  PubMed  Google Scholar 

  181. Knoll W, Frank CW, Heibel C, Naumann R, Offenhausser A, Ruhe J, Schmidt EK, Shen WW, Sinner A (2000) Functional tethered lipid bilayers. J Biotechnol 74:137–158

    CAS  PubMed  Google Scholar 

  182. Mulkidjanian AY, Dibrov P, Galperin MY (2008) The past and present of sodium energetics: may the sodium-motive force be with you. Biochim Biophys Acta 1777:985–992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Mulkidjanian AY, Galperin MY, Koonin EV (2009) Co-evolution of primordial membranes and membrane proteins. Trends Biochem Sci 34:206–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. LaVan DA, Cha JN (2006) Approaches for biological and biomimetic energy conversion. Proc Natl Acad Sci U S A 103:5251–5255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Oesterhelt D, Stoeckenius W (1973) Functions of a new photoreceptor membrane. Proc Natl Acad Sci U S A 70:2853–2857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Schobert B, Lanyi JK (1982) Halorhodopsin is a light-driven chloride pump. J Biol Chem 257:10306–10313

    CAS  PubMed  Google Scholar 

  187. Essen LO (2002) Halorhodopsin: light-driven ion pumping made simple? Curr Opin Struct Biol 12:516–522

    Article  CAS  PubMed  Google Scholar 

  188. Bamberg E, Tittor J, Oesterhelt D (1993) Light-driven proton or chloride pumping by halorhodopsin. Proc Natl Acad Sci U S A 90:639–643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Kayushin LP, Skulachev VP (1974) Bacteriorhodopsin as an electrogenic proton pump: reconstitution of bacteriorhodopsin proteoliposomes generating delta psi and delta pH. FEBS Lett 39:39–42

    Article  CAS  PubMed  Google Scholar 

  190. Oesterhelt D, Schuhmann L (1974) Reconstitution of bacteriorhodopsin. FEBS Lett 44:262–265

    Article  CAS  PubMed  Google Scholar 

  191. Ganea C, Tittor J, Bamberg E, Oesterhelt D (1998) Chloride- and pH-dependent proton transport by BR mutant D85N. Biochim Biophys Acta 1368:84–96

    Article  CAS  PubMed  Google Scholar 

  192. Horn C, Steinem C (2005) Photocurrents generated by bacteriorhodopsin adsorbed on nano-black lipid membranes. Biophys J 89:1046–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Varo G (2000) Analogies between halorhodopsin and bacteriorhodopsin. Biochim Biophys Acta 1460:220–229

    Article  CAS  PubMed  Google Scholar 

  194. Duschl A, McCloskey MA, Lanyi JK (1988) Functional reconstitution of halorhodopsin. Properties of halorhodopsin-containing proteoliposomes. J Biol Chem 263:17016–17022

    CAS  PubMed  Google Scholar 

  195. Bamberg E, Hegemann P, Oesterhelt D (1984) Reconstitution of halorhodopsin in black lipid membranes. Prog Clin Biol Res 164:73–79

    CAS  PubMed  Google Scholar 

  196. Gruia AD, Bondar AN, Smith JC, Fischer S (2005) Mechanism of a molecular valve in the halorhodopsin chloride pump. Structure 13:617–627

    Article  CAS  PubMed  Google Scholar 

  197. Morth JP, Pedersen BP, Toustrup-Jensen MS, Sorensen TL, Petersen J, Andersen JP, Vilsen B, Nissen P (2007) Crystal structure of the sodium-potassium pump. Nature 450:1043–1049

    Article  CAS  PubMed  Google Scholar 

  198. Shinoda T, Ogawa H, Cornelius F, Toyoshima C (2009) Crystal structure of the sodium-potassium pump at 2.4 A resolution. Nature 459:446–450

    Article  CAS  PubMed  Google Scholar 

  199. Toyoshima C, Nakasako M, Nomura H, Ogawa H (2000) Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 A resolution. Nature 405:647–655

    Article  CAS  PubMed  Google Scholar 

  200. Toyoshima C, Inesi G (2004) Structural basis of ion pumping by Ca2+-ATPase of the sarcoplasmic reticulum. Annu Rev Biochem 73:269–292

    Article  CAS  PubMed  Google Scholar 

  201. Accardi A, Miller C (2004) Secondary active transport mediated by a prokaryotic homologue of ClC Cl- channels. Nature 427:803–807

    Article  CAS  PubMed  Google Scholar 

  202. Scheiner-Bobis G (1998) Ion-transporting ATPases as ion channels. Naunyn Schmiedebergs Arch Pharmacol 357:477–482

    Article  CAS  PubMed  Google Scholar 

  203. Gadsby DC (2009) Ion channels versus ion pumps: the principal difference, in principle. Nat Rev Mol Cell Biol

  204. Ashcroft F, Gadsby D, Miller C (2009) Introduction. The blurred boundary between channels and transporters. Philos Trans R Soc Lond B Biol Sci 364:145–147

    Article  PubMed  Google Scholar 

  205. Kedem O, Katchalsky A (1958) Thermodynamic analysis of the permeability of biological membranes to non-electrolytes. Biochim Biophys Acta 27:229–246

    Article  CAS  PubMed  Google Scholar 

  206. Kedem O, Katchalsky A (1961) A physical interpretation of the phenomenological coefficients of membrane permeability. J Gen Physiol 45:143–179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  207. Goldman DE (1943) Potential, impedance and rectification in membranes. J. Gen. Physiol. 27:37–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  208. Chen D, Eisenberg R (1993) Charges, currents, and potentials in ionic channels of one conformation. Biophys J 64:1405–1421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  209. Chen DP, Eisenberg RS (1993) Flux, coupling, and selectivity in ionic channels of one conformation. Biophys J 65:727–746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  210. Miller C (1999) Ionic hopping defended. J Gen Physiol 113:783–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  211. Chung SH, Kuyucak S (2002) Recent advances in ion channel research. Biochim Biophys Acta 1565:267–286

    Article  CAS  PubMed  Google Scholar 

  212. Roux B (2005) Ion conduction and selectivity in K(+) channels. Annu Rev Biophys Biomol Struct 34:153–171

    Article  CAS  PubMed  Google Scholar 

  213. Edwards S, Corry B, Kuyucak S, Chung SH (2002) Continuum electrostatics fails to describe ion permeation in the gramicidin channel. Biophys J 83:1348–1360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  214. Allen TW, Andersen OS, Roux B (2006) Molecular dynamics - potential of mean force calculations as a tool for understanding ion permeation and selectivity in narrow channels. Biophys Chem 124:251–267

    Article  CAS  PubMed  Google Scholar 

  215. Allen TW, Bastug T, Kuyucak S, Chung SH (2003) Gramicidin A channel as a test ground for molecular dynamics force fields. Biophys J 84:2159–2168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. Andersen OS, Koppe RE II, Roux B (2007) Gramicidin channels: versatile tools. In: Chung SH, Andersen OS, Krishnamurthy V (eds) Biological membrane ion channels. Springer, New York, pp 33–80

    Chapter  Google Scholar 

  217. Cukierman S (2000) Proton mobilities in water and in different stereoisomers of covalently linked gramicidin A channels. Biophys J 78:1825–1834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Koeppe RE II, Andersen OS (1996) Engineering the gramicidin channel. Annu Rev Biophys Biomol Struct 25:231–258

    Article  CAS  PubMed  Google Scholar 

  219. Chung SH, Andersen OS, Krishnamurthy V (eds) (2007) Biological membrane ion channels. Dynamics, Structure and Applications, Springer, New York

  220. Huang L-YM, Catterall WA, Ehrenstein G (1978) Selectivity of cations and nonelectrolytes for acetylcholine-activated channels in cultured muscle cells. J Gen Physiol 71:397–410

    Article  CAS  PubMed  Google Scholar 

  221. Unwin N (2005) Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J Mol Biol 346:967–989

    Article  CAS  PubMed  Google Scholar 

  222. Boheim G, Hanke W, Barrantes FJ, Eibl H, Sakmann B, Fels G, Maelicke A (1981) Agonist-activated ionic channels in acetylcholine receptor reconstituted into planar lipid bilayers. Proc Natl Acad Sci U S A 78:3586–3590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  223. Schmidt EK, Liebermann T, Kreiter M, Jonczyk A, Naumann R, Offenhausser A, Neumann E, Kukol A, Maelicke A, Knoll W (1998) Incorporation of the acetylcholine receptor dimer from Torpedo californica in a peptide supported lipid membrane investigated by surface plasmon and fluorescence spectroscopy. Biosens Bioelectron 13:585–591

    Article  CAS  PubMed  Google Scholar 

  224. Doyle DA, Cabral JM, Pfuetzner RA, Kuo A, Gulbis JM, Cohen SL, Chait BT, MacKinnon R (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280:69–77

    Article  CAS  PubMed  Google Scholar 

  225. Jiang Y, Lee A, Chen J, Cadene M, Chait BT, MacKinnon R (2002) Crystal structure and mechanism of a calcium-gated potassium channel. Nature 417:515–522

    Article  CAS  PubMed  Google Scholar 

  226. Jiang Y, Lee A, Chen J, Ruta V, Cadene M, Chait BT, MacKinnon R (2003) X-ray structure of a voltage-dependent K+ channel. Nature 423:33–41

    Article  CAS  PubMed  Google Scholar 

  227. Kuo A, Gulbis JM, Antcliff JF, Rahman T, Lowe ED, Zimmer J, Cuthbertson J, Ashcroft FM, Ezaki T, Doyle DA (2003) Crystal structure of the potassium channel KirBac1.1 in the closed state. Science 300:1922–1926

    Article  CAS  PubMed  Google Scholar 

  228. MacKinnon R (2003) Potassium channels. FEBS Lett 555:62–65

    Article  CAS  PubMed  Google Scholar 

  229. Sexton LT, Horne LP, Martin CR (2007) Developing synthetic conical nanopores for biosensing applications. Mol Biosyst 3:667–685

    Article  CAS  PubMed  Google Scholar 

  230. Jeon YJ, Kim H, Jon S, Selvapalam N, Oh DH, Seo I, Park CS, Jung SR, Koh DS, Kim K (2004) Artificial ion channel formed by cucurbit[n]uril derivatives with a carbonyl group fringed portal reminiscent of the selectivity filter of K+ channels. J Am Chem Soc 126:15944–15945

    Article  CAS  PubMed  Google Scholar 

  231. Terrettaz S, Follonier S, Makohliso S, Vogel H (2009) A synthetic membrane protein in tethered lipid bilayers for immunosensing in whole blood. J Struct Biol

  232. Gandhi CS, Clark E, Loots E, Pralle A, Isacoff EY (2003) The orientation and molecular movement of a k(+) channel voltage-sensing domain. Neuron 40:515–525

    Article  CAS  PubMed  Google Scholar 

  233. Laine M, Lin MC, Bannister JP, Silverman WR, Mock AF, Roux B, Papazian DM (2003) Atomic proximity between S4 segment and pore domain in Shaker potassium channels. Neuron 39:467–481

    Article  CAS  PubMed  Google Scholar 

  234. Blaustein RO, Miller C (2004) Ion channels: shake, rattle or roll? Nature 427:499–500

    Article  CAS  PubMed  Google Scholar 

  235. Long SB, Campbell EB, Mackinnon R (2005) Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309:897–903

    Article  CAS  PubMed  Google Scholar 

  236. Long SB, Campbell EB, Mackinnon R (2005) Voltage sensor of Kv1.2: structural basis of electromechanical coupling. Science 309:903–908

    Article  CAS  PubMed  Google Scholar 

  237. Dhoke MA, Ladha PJ, Boerio FJ, Lessard LB, Malinowska DH, Cuppoletti J, Wieczorek DS (2005) Porous membranes for reconstitution of ion channels. Biochim Biophys Acta 1716:117–125

    Article  CAS  PubMed  Google Scholar 

  238. Matsuno N, Murawsky M, Ridgeway J, Cuppoletti J (2004) Solid support membranes for ion channel arrays and sensors: application to rapid screening of pharmacological compounds. Biochim Biophys Acta 1665:184–190

    Article  CAS  PubMed  Google Scholar 

  239. Blunck R, McGuire H, Hyde HC, Bezanilla F (2008) Fluorescence detection of the movement of single KcsA subunits reveals cooperativity. Proc Natl Acad Sci U S A 105:20263–20268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  240. DeCoursey TE (2008) Voltage-gated proton channels: what’s next? J Physiol 586:5305–5324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  241. DeCoursey TE (2008) Voltage-gated proton channels. Cell Mol Life Sci 65:2554–2573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  242. Cherny VV, Murphy R, Sokolov V, Levis RA, DeCoursey TE (2003) Properties of single voltage-gated proton channels in human eosinophils estimated by noise analysis and by direct measurement. J Gen Physiol 121:615–628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  243. Demaurex N, Grinstein S, Jaconi M, Schlegel W, Lew DP, Krause KH (1993) Proton currents in human granulocytes: regulation by membrane potential and intracellular pH. J Physiol 466:329–344

    CAS  PubMed  PubMed Central  Google Scholar 

  244. Schilling T, Gratopp A, DeCoursey TE, Eder C (2002) Voltage-activated proton currents in human lymphocytes. J Physiol 545:93–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  245. Tombola F, Ulbrich MH, Isacoff EY (2008) The voltage-gated proton channel Hv1 has two pores, each controlled by one voltage sensor. Neuron 58:546–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  246. Koch HP, Kurokawa T, Okochi Y, Sasaki M, Okamura Y, Larsson HP (2008) Multimeric nature of voltage-gated proton channels. Proc Natl Acad Sci U S A 105:9111–9116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  247. Lee SY, Letts JA, Mackinnon R (2008) Dimeric subunit stoichiometry of the human voltage-dependent proton channel Hv1. Proc Natl Acad Sci U S A 105:7692–7695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  248. Sasaki M, Takagi M, Okamura Y (2006) A voltage sensor-domain protein is a voltage-gated proton channel. Science 312:589–592

    Article  CAS  PubMed  Google Scholar 

  249. Ramsey IS, Moran MM, Chong JA, Clapham DE (2006) A voltage-gated proton-selective channel lacking the pore domain. Nature 440:1213–1216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  250. Starace DM, Bezanilla F (2004) A proton pore in a potassium channel voltage sensor reveals a focused electric field. Nature 427:548–553

    Article  CAS  PubMed  Google Scholar 

  251. Starace DM, Bezanilla F (2001) Histidine scanning mutagenesis of basic residues of the S4 segment of the shaker k+ channel. J Gen Physiol 117:469–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  252. Lee SY, Letts JA, MacKinnon R (2009) Functional reconstitution of purified human Hv1 H+ channels. J Mol Biol 387:1055–1060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  253. Agre P, Sasaki S, Chrispeels MJ (1993) Aquaporins: a family of water channel proteins. Am J Physiol 265:F461

    CAS  PubMed  Google Scholar 

  254. Gonen T, Walz T (2006) The structure of aquaporins. Q Rev Biophys 39:361–396

    Article  CAS  PubMed  Google Scholar 

  255. Fu D, Lu M (2007) The structural basis of water permeation and proton exclusion in aquaporins. Mol Membr Biol 24:366–374

    Article  CAS  PubMed  Google Scholar 

  256. Ishibashi K (2006) Aquaporin subfamily with unusual NPA boxes. Biochim Biophys Acta 1758:989–993

    Article  CAS  PubMed  Google Scholar 

  257. Verkman AS (2005) More than just water channels: unexpected cellular roles of aquaporins. J Cell Sci 118:3225–3232

    Article  CAS  PubMed  Google Scholar 

  258. Nielsen S, Frokiaer J, Marples D, Kwon TH, Agre P, Knepper MA (2002) Aquaporins in the kidney: from molecules to medicine. Physiol Rev 82:205–244

    Article  CAS  PubMed  Google Scholar 

  259. Borgnia MJ, Agre P (2001) Reconstitution and functional comparison of purified GlpF and AqpZ, the glycerol and water channels from Escherichia coli. Proc Natl Acad Sci U S A 98:2888–2893

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  260. Calamita G, Bishai WR, Preston GM, Guggino WB, Agre P (1995) Molecular cloning and characterization of AqpZ, a water channel from Escherichia coli. J Biol Chem 270:29063–29066

    Article  CAS  PubMed  Google Scholar 

  261. Fu D, Libson A, Miercke LJ, Weitzman C, Nollert P, Krucinski J, Stroud RM (2000) Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290:481–486

    Article  CAS  PubMed  Google Scholar 

  262. Nernst W (1909) Zur Theorie des electrischen Reizes. Pfluegers Arch. Physiol 122:275–314

    Article  Google Scholar 

  263. Anthony TL, Brooks HL, Boassa D, Leonov S, Yanochko GM, Regan JW, Yool AJ (2000) Cloned human aquaporin-1 is a cyclic GMP-gated ion channel. Mol Pharmacol 57:576–588

    Article  CAS  PubMed  Google Scholar 

  264. Cooper GJ, Boron WF (1998) Effect of PCMBS on CO2 permeability of Xenopus oocytes expressing aquaporin 1 or its C189S mutant. Am J Physiol 275:C1481–C1486

    Article  CAS  PubMed  Google Scholar 

  265. Herrera M, Hong NJ, Garvin JL (2006) Aquaporin-1 transports NO across cell membranes. Hypertension 48:157–164

    Article  CAS  PubMed  Google Scholar 

  266. Nakhoul NL, Hering-Smith KS, Abdulnour-Nakhoul SM, Hamm LL (2001) Transport of NH(3)/NH in oocytes expressing aquaporin-1. Am J Physiol Renal Physiol 281:F255–F263

    Article  CAS  PubMed  Google Scholar 

  267. Yasui M, Kwon TH, Knepper MA, Nielsen S, Agre P (1999) Aquaporin-6: an intracellular vesicle water channel protein in renal epithelia. Proc Natl Acad Sci U S A 96:5808–5813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  268. Liu Z, Shen J, Carbrey JM, Mukhopadhyay R, Agre P, Rosen BP (2002) Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc Natl Acad Sci U S A 99:6053–6058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  269. Stroud RM, Miercke LJ, O’Connell J, Khademi S, Lee JK, Remis J, Harries W, Robles Y, Akhavan D (2003) Glycerol facilitator GlpF and the associated aquaporin family of channels. Curr Opin Struct Biol 13:424–431

    Article  CAS  PubMed  Google Scholar 

  270. Stroud RM, Savage D, Miercke LJ, Lee JK, Khademi S, Harries W (2003) Selectivity and conductance among the glycerol and water conducting aquaporin family of channels. FEBS Lett 555:79–84

    Article  CAS  PubMed  Google Scholar 

  271. Verkman AS (2002) Does aquaporin-1 pass gas? An opposing view. J Physiol 542:31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  272. Wu B, Beitz E (2007) Aquaporins with selectivity for unconventional permeants. Cell Mol Life Sci 64:2413–2421

    Article  CAS  PubMed  Google Scholar 

  273. Bienert GP, Schussler MD, Jahn TP (2008) Metalloids: essential, beneficial or toxic? Major intrinsic proteins sort it out. Trends Biochem Sci 33:20–26

    Article  CAS  PubMed  Google Scholar 

  274. Khandelia H, Jensen MO, Mouritsen OG (2009) To gate or not to gate: using molecular dynamics simulations to morph gated plant aquaporins into constitutively open conformations. J Phys Chem B 113:5239–5244

    Article  CAS  PubMed  Google Scholar 

  275. Nemeth-Cahalan KL, Hall JE (2000) pH and calcium regulate the water permeability of aquaporin 0. J Biol Chem 275:6777–6782

    Article  CAS  PubMed  Google Scholar 

  276. Nemeth-Cahalan KL, Kalman K, Hall JE (2004) Molecular basis of pH and Ca2+ regulation of aquaporin water permeability. J Gen Physiol 123:573–580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  277. Johansson I, Larsson C, Ek B, Kjellbom P (1996) The major integral proteins of spinach leaf plasma membranes are putative aquaporins and are phosphorylated in response to Ca2+ and apoplastic water potential. Plant Cell 8:1181–1191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  278. Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, Kjellbom P (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10:451–459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  279. Zeuthen T, Klaerke DA (1999) Transport of water and glycerol in aquaporin 3 is gated by H(+). J Biol Chem 274:21631–21636

    Article  CAS  PubMed  Google Scholar 

  280. Yasui M, Hazama A, Kwon TH, Nielsen S, Guggino WB, Agre P (1999) Rapid gating and anion permeability of an intracellular aquaporin. Nature 402:184–187

    Article  CAS  PubMed  Google Scholar 

  281. Nernst W (1904) Theorie der Reaktionsgeschwindigkeit in heterogenen Systemen. Z Phys Chem (Leipzig) 47:52–55

    CAS  Google Scholar 

  282. Schulman JH, Teorell T (1938) On the boundary layer at membrane and monolayer interfaces. Trans Faraday Soc 34:1337

    Article  Google Scholar 

  283. Pearce GK (2008) UF/MF pre-treatment to RO in seawater and wastewater reuse applications: a comparison of energy costs

  284. Byrne W (2002) Reverse osmosis. Tall Oaks Publishing Inc., Littleton, CO

    Google Scholar 

  285. Meltzer TH (1993) High-purity water. Tall Oaks Publishing, Littleton, CO

    Google Scholar 

  286. Macdonald AG (2002) Ion channels under high pressure. Comp Biochem Physiol A Mol Integr Physiol 131:587–593

    Article  CAS  PubMed  Google Scholar 

  287. Griepernau B, Bockmann RA (2008) The influence of 1-alkanols and external pressure on the lateral pressure profiles of lipid bilayers. Biophys J 95:5766–5778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  288. Loeb S, Norman RS (1975) Osmotic power plants. Science 189:654–655

    Article  CAS  PubMed  Google Scholar 

  289. Skilhagen SE, Dugstad JE, Aaberg RJ (2008) Osmotic power - power production based on the osmotic pressure difference between waters with varying salt gradients. Desalination 220:476–482

    Article  CAS  Google Scholar 

  290. Cath TY, Childress AE, Elimelech M (2006) Forward osmosis: principles, applications and recent developments. J Membr Sci 281:70–87

    Article  CAS  Google Scholar 

  291. Kessler JO, Moody CD (1976) Drinking water from sea water by forward osmosis. Desalination 18:297–306

    Article  CAS  Google Scholar 

  292. McCutcheon JR, McGinnis RL, Elimelech M (2006) Desalination by a novel ammonia-carbon dioxide forward osmosis process: influence of draw and feed solution concentrations on process performance. J Membr Sci 278:114–123

    Article  CAS  Google Scholar 

  293. Sleytr U, Bayley H, Sára M, Breitwieser A, Küpcü S, Mader C, Weigert S, Unger F, Messner P, Jahn-Schmid B, Schuster B, Pum D, Douglas K, Clark N, Moore J, Winningham T, Levy S, Frithsen I, Pankovc J, Beale P, Gillis H, Choutov D, Martin KP (1997) Applications of S-layers. FEMS Microbiol Rev 29:151–175

    Article  Google Scholar 

  294. Szewczykowski P (2009) Nano-porous materials from diblock copolymers and their membrane application. PhD Thesis, Department of Chemical and Biochemical Engineering, Technical University of Denmark, Lyngby

  295. Walter A, Gutknecht J (1986) Permeability of small nonelectrolytes through lipid bilayer membranes. J Membrane Biol 77:255–264

    Article  Google Scholar 

  296. Flewelling RF, Hubbell WL (1986) Hydrophobic ion interactions with membranes. Thermodynamic analysis of tetraphenylphosphonium binding to vesicles. Biophys J 49:531–540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  297. Hauser H, Oldani D, Phillips MC (1973) Mechanism of ion escape from phosphatidylcholine and phosphatidylserine single bilayer vesicles. Biochemistry 12:4507–4517

    Article  CAS  PubMed  Google Scholar 

  298. Gutknecht J (1984) Proton/hydroxide conductance through lipid bilayer membranes. J Membr Biol 82:105–112

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported through MEMBAQ, a specific targeted research project (STREP), by the European Commission under the Sixth Framework Programme (NMP4-CT-2006-033234), though Watermembrane, by The Danish National Advanced Technology Foundation (023-2007-1), and by a grant from The Danish National Research Foundation to QuP. I thank my colleagues in MEMBAQ, Watermembrane, QuP, and Aquaporin A/S for helpful discussions and the reviewers for their constructive comments and suggestions.

Author information

Authors and Affiliations

  1. Quantum Protein Center, Department of Physics, Technical University of Denmark, 2800, Lyngby, Denmark

    Claus Hélix Nielsen

  2. Aquaporin /A/S, Diplomvej 377, 2800, Lyngby, Denmark

    Claus Hélix Nielsen

Authors
  1. Claus Hélix Nielsen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claus Hélix Nielsen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nielsen, C.H. Biomimetic membranes for sensor and separation applications. Anal Bioanal Chem 395, 697–718 (2009). https://doi.org/10.1007/s00216-009-2960-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00216-009-2960-0

Keywords

Search

Navigation