Arrayed lipid bilayer chambers allow single-molecule analysis of membrane transporter activity

Nature Communications

Volumn 5, Issue , 2014, Pages

  Watanabe, Rikiya ^a,b   Soga, Naoki ^a   Fujita, Daishi ^a   Tabata, Kazuhito V ^a,b   Yamauchi, Lisa ^a,b   Hyeon Kim, Soo ^b,c   Asanuma, Daisuke ^d   Kamiya, Mako ^d   Urano, Yasuteru ^d   Suga, Hiroaki ^a,b   Noji, Hiroyuki ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c INSTITUTE OF INDUSTRIAL SCIENCE   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA HEMOLYSIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; ALEXA 488 HYDRAZIDE; BACTERIAL TOXIN; CARRIER PROTEIN; FLUORESCENT DYE; HEMOLYSIN; HYDRAZINE DERIVATIVE; LIPID BILAYER; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; STAPHYLOCOCCAL ALPHA-TOXIN;

BIOASSAY; LIPID; MEMBRANE; MOLECULAR ANALYSIS; POLYMERASE CHAIN REACTION; PROTEIN; STOCHASTICITY;

AQUEOUS SOLUTION; ARRAYED LIPID BILAYER CHAMBER SYSTEM; ARTICLE; ARTIFICIAL MEMBRANE; LIPID BILAYER; MEMBRANE TRANSPORT; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; STOCHASTIC MODEL; ACTIVE TRANSPORT; BLEACHING; DEVICES; METABOLISM; MICROTECHNOLOGY; MOLECULAR BIOLOGY; NANOTECHNOLOGY; PROCEDURES;

BACTERIAL TOXINS; BIOLOGICAL TRANSPORT, ACTIVE; FLUORESCENT DYES; HEMOLYSIN PROTEINS; HYDRAZINES; LIPID BILAYERS; MEMBRANE TRANSPORT PROTEINS; MICROTECHNOLOGY; MOLECULAR BIOLOGY; NANOTECHNOLOGY; PHOTOBLEACHING; PROTON-TRANSLOCATING ATPASES;

EID: 84904988294     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5519     Document Type: Article

References (41)

1. Saier, Jr M. H. A functional-phylogenetic classification system for transmembrane solute transporters. Microbiol. Mol. Biol. Rev. 64, 354-411 (2000). (Pubitemid 30412678)
2. International Transporter Consortium et al. Membrane transporters in drug development. Nat. Rev. Drug Discov. 9, 215-236 (2010).
3. Kaczorowski, G. J., McManus, O. B., Priest, B. T. & Garcia, M. L. Ion channels as drug targets: the next GPCRs. J. Gen. Physiol. 131, 399-405 (2008). (Pubitemid 351620096)
4. Tschodrich-Rotter, M. & Peters, R. An optical method for recording the activity of single transporters in membrane patches. J. Microsc. 192, 114-125 (1998). (Pubitemid 28539616)
5. Laubinger, W. & Dimroth, P. The sodium ion translocating adenosinetriphosphatase of Propionigenium modestum pumps protons at low sodium ion concentrations. Biochemistry 28, 7194-7198 (1989).
6. Keminer, O., Siebrasse, J. P., Zerf, K. & Peters, R. Optical recording of signalmediated protein transport through single nuclear pore complexes. Proc. Natl Acad. Sci. USA 96, 11842-11847 (1999). (Pubitemid 29502820)
7. Sakakihara, S., Araki, S., Iino, R. & Noji, H. A single-molecule enzymatic assay in a directly accessible femtoliter droplet array. Lab Chip 10, 3355-3362 (2010).
8. Rondelez, Y. et al. Microfabricated arrays of femtoliter chambers allow single molecule enzymology. Nat. Biotechnol. 23, 361-365 (2005). (Pubitemid 41094426)
9. Gorris, H. H., Rissin, D. M. & Walt, D. R. Stochastic inhibitor release and binding from single-enzyme molecules. Proc. Natl Acad. Sci. USA 104, 17680-17685 (2007). (Pubitemid 350210894)
10. Fujiwara, H., Fujihara, M. & Ishiwata, T. Dynamics of the spontaneous formation of a planar phospholipid bilayer: a new approach by simultaneous electrical and optical measurements. J. Chem. Phys. 119, 6768-6775 (2003).
11. Wang, W. et al. Activity monitoring of functional OprM using a biomimetic microfluidic device. Analyst 137, 847-852 (2012).
12. Asanuma, D. et al. Acidic-pH activatable fluorescence probes for visualizing exocytosis dynamics. Angew. Chem. Int. Ed. 53, 6085-6089 (2014).
13. Song, L. et al. Structure of staphylococcal alpha-hemolysin, a heptameric transmembrane pore. Science 274, 1859-1866 (1996). (Pubitemid 26424757)
14. Branton, D. et al. The potential and challenges of nanopore sequencing. Nat. Biotechnol. 26, 1146-1153 (2008).
15. Sumitomo, K. et al. Ca2\+ ion transport through channels formed by alphahemolysin analyzed using a microwell array on a Si substrate. Biosens. Bioelectron. 31, 445-450 (2012).
16. Okuno, D., Iino, R. & Noji, H. Rotation and structure of FoF1-ATP synthase. J. Biochem. 149, 655-664 (2011).
17. Yoshida, M., Muneyuki, E. & Hisabori, T. ATP synthase-a marvellous rotary engine of the cell. Nat. Rev. Mol. Cell. Biol. 2, 669-677 (2001). (Pubitemid 33674070)
18. Dimroth, P., von Ballmoos, C. & Meier, T. Catalytic and mechanical cycles in F-ATP synthases. Fourth in the Cycles Review Series. EMBO Rep. 7, 276-282 (2006).
19. Turina, P., Samoray, D. & Graber, P. H\+/ATP ratio of proton transportcoupled ATP synthesis and hydrolysis catalysed by CFoF1-liposomes. EMBO J. 22, 418-426 (2003). (Pubitemid 36193587)
20. Diez, M. et al. Proton-powered subunit rotation in single membrane-bound FoF1-ATP synthase. Nat. Struct. Mol. Biol. 11, 135-141 (2004). (Pubitemid 38146516)
21. Watanabe, R. et al. Biased Brownian stepping rotation of FoF1-ATP synthase driven by proton motive force. Nat. Commun. 4, 1631 (2013).
22. Weber, J. Structural biology: toward the ATP synthase mechanism. Nat. Chem. Biol. 6, 794-795 (2010).
23. Hermolin, J. & Fillingame, R. H. H\+-ATPase activity of Escherichia coli F1Fo is blocked after reaction of dicyclohexylcarbodiimide with a single proteolipid (subunit c) of the Fo complex. J. Biol. Chem. 264, 3896-3903 (1989). (Pubitemid 19072275)
24. Ueno, H., Suzuki, T., Kinosita, Jr K. & Yoshida, M. ATP-driven stepwise rotation of FoF1-ATP synthase. Proc. Natl Acad. Sci. USA 102, 1333-1338 (2005). (Pubitemid 40209171)
25. van Meer, G., Voelker, D. R. & Feigenson, G. W. Membrane lipids: where they are and how they behave. Nat. Rev. Mol. Cell Biol. 9, 112-124 (2008). (Pubitemid 351158912)
26. Rissin, D. M. et al. Single-molecule enzyme-linked immunosorbent assay detects serum proteins at subfemtomolar concentrations. Nat. Biotechnol. 28, 595-599 (2010).
27. Kim, S. H. et al. Large-scale femtoliter droplet array for digital counting of single biomolecules. Lab Chip 12, 4986-4991 (2012).
28. Eid, J. et al. Real-time DNA sequencing from single polymerase molecules. Science 323, 133-138 (2009).
29. Leiding, T. et al. Precise detection of pH inside large unilamellar vesicles using membrane-impermeable dendritic porphyrin-based nanoprobes. Anal. Biochem. 388, 296-305 (2009).
30. Turina, P. Influence of the transmembrane electrochemical proton gradient on catalysis and regulation of the H\+-ATP synthase from Rhodobacter- capsulatus. Bioelectrochem. Bioenerg. 33, 31-43 (1994). (Pubitemid 24048901)
31. Soga, N., Kinosita, K., Yoshida, M. & Suzuki, T. Kinetic equivalence of transmembrane pH and electrical potential differences in ATP synthesis. J. Biol. Chem. 287, 9633-9639 (2012).
32. Deamer, D. W. & Bramhall, J. Permeability of lipid bilayers to water and ionic solutes. Chem. Phys. Lipids 40, 167-188 (1986).
33. Petrasek, Z. & Schwille, P. Precise measurement of diffusion coefficients using scanning fluorescence correlation spectroscopy. Biophys. J. 94, 1437-1448 (2008).
34. Mamonov, A. B., Kurnikova, M. G. & Coalson, R. D. Diffusion constant of K\+ inside Gramicidin A: a comparative study of four computational methods. Biophys. Chem. 124, 268-278 (2006). (Pubitemid 44692354)
35. Smith, G. R. & Sansom, M. S. P. Effective diffusion coefficients of K\+ and Clions in ion channel models. Biophys. Chem. 79, 129-151 (1999). (Pubitemid 29246098)
36. Burzik, C., Kaim, G., Dimroth, P., Bamberg, E. & Fendler, K. Charge displacements during ATP-hydrolysis and synthesis of the Na\+-transporting FoF1-ATPase of Ilyobacter tartaricus. Biophys. J. 85, 2044-2054 (2003). (Pubitemid 37052284)
37. Mitome, N., Suzuki, T., Hayashi, S. & Yoshida, M. Thermophilic ATP synthase has a decamer c-ring: indication of noninteger 10:3 H\+/ATP ratio and permissive elastic coupling. Proc. Natl Acad. Sci. USA 101, 12159-12164 (2004). (Pubitemid 39145413)
38. Jiang, W., Hermolin, J. & Fillingame, R. H. The preferred stoichiometry of c subunits in the rotary motor sector of Escherichia coli ATP synthase is 10. Proc. Natl Acad. Sci. USA 98, 4966-4971 (2001). (Pubitemid 32397066)
39. Yasuda, R., Noji, H., Kinosita, Jr K. & Yoshida, M. F1-ATPase is a highly efficient molecular motor that rotates with discrete 120 degree steps. Cell 93, 1117-1124 (1998). (Pubitemid 28307417)
40. Iino, R., Hasegawa, R., Tabata, K. V. & Noji, H. Mechanism of inhibition by C-terminal alpha-helices of the epsilon subunit of Escherichia coli FoF1-ATP synthase. J. Biol. Chem. 284, 17457-17464 (2009).
41. Tsunoda, S. P. et al. Observations of rotation within the FoF1-ATP synthase: deciding between rotation of the Foc subunit ring and artifact. FEBS Lett. 470, 244-248 (2000). (Pubitemid 30169272)