Engineered ion channels as emerging tools for chemical biology

Accounts of Chemical Research

Volumn 46, Issue 12, 2013, Pages 2998-3008

  Mayer, Michael ^a   Yang, Jerry ^b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ION CHANNEL;

ARTICLE; BIOCHEMISTRY; CHEMISTRY; GENETIC ENGINEERING;

BIOCHEMISTRY; GENETIC ENGINEERING; ION CHANNELS;

EID: 84890600403     PISSN: 00014842     EISSN: 15204898     Source Type: Journal    
DOI: 10.1021/ar400129t     Document Type: Article

References (60)

1. Verger, R. Interfacial enzyme kinetics of lipolysis Annu. Rev. Biophys. Bioeng. 1976, 5, 77-117
2. Majd, S.; Yusko, E. C.; Billeh, Y. N.; Macrae, M. X.; Yang, J.; Mayer, M. Applications of biological pores in nanomedicine, sensing, and nanoelectronics Curr. Opin. Biotechnol. 2010, 21, 439-476
3. Futaki, S.; Zhang, Y.; Kiwada, T.; Nakase, I.; Yagami, T.; Oiki, S.; Sugiura, Y. Gramicidin-based channel systems for the detection of protein-ligand interaction Bioorg. Med. Chem. 2004, 12, 1343-1350 (Pubitemid 38296524)
4. Majd, S.; Yusko, E. C.; MacBriar, A. D.; Yang, J.; Mayer, M. Gramicidin pores report the activity of membrane-active enzymes J. Am. Chem. Soc. 2009, 131, 16119-16126
5. Bayley, H.; Cremer, P. S. Stochastic sensors inspired by biology Nature 2001, 413, 226-230 (Pubitemid 32867888)
6. Pastrana, E. Optogenetics: Controlling cell function with light Nat. Methods 2011, 8, 24-25
7. Banghart, M.; Borges, K.; Isacoff, E.; Trauner, D.; Kramer, R. H. Light-activated ion channels for remote control of neuronal firing Nat. Neurosci. 2004, 7, 1381-1386 (Pubitemid 41057762)
8. Manrao, E. A.; Derrington, I. M.; Laszlo, A. H.; Langford, K. W.; Hopper, M. K.; Gillgren, N.; Pavlenok, M.; Niederweis, M.; Gundlach, J. H. Reading DNA at single-nucleotide resolution with a mutant MspA nanopore and phi29 DNA polymerase Nat. Biotechnol. 2012, 30, 349-353
9. Macrae, M. X.; Blake, S.; Jiang, X. Y.; Capone, R.; Estes, D. J.; Mayer, M.; Yang, J. A semi-synthetic ion channel platform for detection of phosphatase and protease activity ACS Nano 2009, 3, 3567-3580
10. Capone, R.; Blake, S.; Restrepo, M. R.; Yang, J.; Mayer, M. Designing nanosensors based on charged derivatives of gramicidin A J. Am. Chem. Soc. 2007, 129, 9737-9745 (Pubitemid 47237487)
11. Mayer, M.; Semetey, V.; Gitlin, I.; Yang, J.; Whitesides, G. M. Using ion channel-forming peptides to quantify protein-ligand interactions J. Am. Chem. Soc. 2008, 130, 1453-1465 (Pubitemid 351171024)
12. Astier, Y.; Bayley, H.; Howorka, S. Protein components for nanodevices Curr. Opin. Chem. Biol. 2005, 9, 576-584 (Pubitemid 41612185)
13. Szobota, S.; Gorostiza, P.; Del Bene, F.; Wyart, C.; Fortin, D. L.; Kolstad, K. D.; Tulyathan, O.; Volgraf, M.; Numano, R.; Aaron, H. L.; Scott, E. K.; Kramer, R. H.; Flannery, J.; Baier, H.; Trauner, D.; Isacoff, E. Y. Remote control of neuronal activity with a light-gated glutamate receptor Neuron 2007, 54, 535-545 (Pubitemid 46756151)
14. Litvinchuk, S.; Bollot, G.; Mareda, J.; Som, A.; Ronan, D.; Shah, M. R.; Perrottet, P.; Sakai, N.; Matile, S. Thermodynamic and kinetic stability of synthetic multifunctional rigid-rod beta-barrel pores: Evidence for supramolecular catalysis J. Am. Chem. Soc. 2004, 126, 10067-10075 (Pubitemid 39079429)
15. Matile, S.; Jentzsch, A. V.; Montenegro, J.; Fin, A. Recent synthetic transport systems Chem. Soc. Rev. 2011, 40, 2453-2474
16. Prangkio, P.; Rao, D. K.; Lance, K. D.; Rubinshtein, M.; Yang, J.; Mayer, M. Self-assembled, cation-selective ion channels from an oligo(ethylene glycol) derivative of benzothiazole aniline Biochim. Biophys. Acta 2011, 1808, 2877-2885
17. Lu, S. R.; Li, W. W.; Rotem, D.; Mikhailova, E.; Bayley, H. A primary hydrogen-deuterium isotope effect observed at the single-molecule level Nat. Chem. 2010, 2, 921-928
18. Bayley, H.; Jayasinghe, L. Functional engineered channels and pores (Review) Mol. Membr. Biol. 2004, 21, 209-220 (Pubitemid 39208296)
19. Apell, H. J.; Bamberg, E.; Lauger, P. Effects of surface charge on the conductance of the gramicidin channel Biochim. Biophys. Acta 1979, 552, 369-78
20. Howorka, S.; Siwy, Z. Nanopore analytics: Sensing of single molecules Chem. Soc. Rev. 2009, 38, 2360-2384
21. Lundbaek, J. A.; Collingwood, S. A.; Ingolfsson, H. I.; Kapoor, R.; Andersen, O. S. Lipid bilayer regulation of membrane protein function: Gramicidin channels as molecular force probes J. R. Soc. Interface 2010, 7, 373-395
22. Xie, X.; Al-Momani, L.; Reiss, P.; Griesinger, C.; Koert, U. An asymmetric ion channel derived from gramicidin A. Synthesis, function and NMR structure FEBS J. 2005, 272, 975-986 (Pubitemid 40282579)
23. Borisenko, V.; Lougheed, T.; Hesse, J.; Fureder-Kitzmuller, E.; Fertig, N.; Behrends, J. C.; Woolley, G. A.; Schutz, G. J. Simultaneous optical and electrical recording of single gramicidin channels Biophys. J. 2003, 84, 612-622 (Pubitemid 36026429)
24. Cornell, B. A.; Braach-Maksvytis, V. L.; King, L. G.; Osman, P. D.; Raguse, B.; Wieczorek, L.; Pace, R. J. A biosensor that uses ion-channel switches Nature 1997, 387, 580-583 (Pubitemid 27248758)
25. Blake, S.; Capone, R.; Mayer, M.; Yang, J. Chemically reactive derivatives of gramicidin A for developing ion channel-based nanoprobes Bioconjugate Chem. 2008, 19, 1614-1624
26. Ambudkar, S. V.; Lelong, I. H.; Zhang, J.; Cardarelli, C. Purification and reconstitution of human P-glycoprotein Methods Enzymol. 1998, 292, 492-504 (Pubitemid 29343910)
27. Terrettaz, S.; Mayer, M.; Vogel, H. Highly electrically insulating tethered lipid bilayers for probing the function of ion channel proteins Langmuir 2003, 19, 5567-5569
28. Mayer, M.; Kriebel, J. K.; Tosteson, M. T.; Whitesides, G. M. Microfabricated Teflon membranes for low-noise recordings of ion channels in planar lipid bilayers Biophys. J. 2003, 85, 2684-2695 (Pubitemid 37210814)
29. Gross, L. C.; Castell, O. K.; Wallace, M. I. Dynamic and reversible control of 2D membrane protein concentration in a droplet interface bilayer Nano Lett. 2011, 11, 3324-3328
30. Joshi, P. R.; Suryanarayanan, A.; Schulte, M. K. A vertical flow chamber for Xenopus oocyte electrophysiology and automated drug screening J. Neurosci. Methods 2004, 132, 69-79 (Pubitemid 37543752)
31. Blake, S.; Mayer, T.; Mayer, M.; Yang, J. Monitoring chemical reactions by using ion-channel-forming peptides ChemBioChem 2006, 7, 433-435
32. Macrae, M. X.; Blake, S.; Mayer, M.; Yang, J. Nanoscale ionic diodes with tunable and switchable rectifying behavior J. Am. Chem. Soc. 2010, 132, 1766-1767
33. Hladky, S. B.; Haydon, D. A. Ion transfer across lipid-membranes in the presence of gramicidin A. 1. Studies of the unit conductance channel Biochim. Biophys. Acta 1972, 274, 294-312
34. Rokitskaya, T. I.; Macrae, M. X.; Blake, S.; Egorova, N. S.; Kotova, E. A.; Yang, J.; Antonenko, Y. N. Mechanistic insight into gramicidin-based detection of protein-ligand interactions via sensitized photoinactivation J. Phys.: Condens. Matter 2010, 22 454118
35. Holden, M. A.; Needham, D.; Bayley, H. Functional bionetworks from nanoliter water droplets J. Am. Chem. Soc. 2007, 129, 8650-8655 (Pubitemid 47066529)
36. Kocer, A.; Walko, M.; Meijberg, W.; Feringa, B. L. A light-actuated nanovalve derived from a channel protein Science 2005, 309, 755-758 (Pubitemid 41077318)
37. Macrae, M. X.; Schlamadinger, D.; Kim, J. E.; Mayer, M.; Yang, J. Using charge to control the functional properties of self-assembled nanopores in membranes Small 2011, 7, 2016-2020
38. Fehrentz, T.; Schonberger, M.; Trauner, D. Optochemical genetics Angew. Chem., Int. Ed. 2011, 50, 12156-12182
39. Fenno, L.; Yizhar, O.; Deisseroth, K. The development and application of optogenetics Annu. Rev. Neurosci. 2011, 34, 389-412
40. Kasianowicz, J. J.; Brandin, E.; Branton, D.; Deamer, D. W. Characterization of individual polynucleotide molecules using a membrane channel Proc. Natl. Acad. Sci. U. S. A. 1996, 93, 13770-13773 (Pubitemid 26424195)
41. Hornblower, B.; Coombs, A.; Whitaker, R. D.; Kolomeisky, A.; Picone, S. J.; Meller, A.; Akeson, M. Single-molecule analysis of DNA-protein complexes using nanopores Nat. Methods 2007, 4, 315-317 (Pubitemid 46766974)
42. Renner, S.; Bessonov, A.; Gerland, U.; Simmel, F. C. Sequence-dependent unfolding kinetics of DNA hairpins studied by nanopore force spectroscopy J. Phys.: Condens. Matter 2010, 22 454119
43. Mohammad, M. M.; Prakash, S.; Matouschek, A.; Movileanu, L. Controlling a single protein in a nanopore through electrostatic traps J. Am. Chem. Soc. 2008, 130, 4081-4088 (Pubitemid 351429878)
44. Bezrukov, S. M.; Vodyanoy, I.; Parsegian, V. A. Counting polymers moving through a single ion channel Nature 1994, 370, 279-281 (Pubitemid 24250118)
45. Eisenstein, M. Oxford Nanopore announcement sets sequencing sector abuzz Nat. Biotechnol. 2012, 30, 295-296
46. Derrington, I. M.; Butler, T. Z.; Collins, M. D.; Manrao, E.; Pavlenok, M.; Niederweis, M.; Gundlach, J. H. Nanopore DNA sequencing with MspA Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 16060-16065
47. Wang, F.; Qin, L. H.; Pace, C. J.; Wong, P.; Malonis, R.; Gao, J. M. Solubilized gramicidin A as potential systemic antibiotics ChemBioChem 2012, 13, 51-55
48. Macrae, M. X.; Blake, S.; Mayer, T.; Mayer, M.; Yang, J. Reactive derivatives of gramicidin enable light-and ion-modulated ion channels Proc. SPIE 2009, 7397 739709
49. Langecker, M.; Arnaut, V.; Martin, T. G.; List, J.; Renner, S.; Mayer, M.; Dietz, H.; Simmel, F. C. Synthetic lipid membrane channels formed by designed dna nanostructures Science 2012, 338, 932-936
50. Hernandez-Ainsa, S.; Bell, N. A.; Thacker, V. V.; Gopfrich, K.; Misiunas, K.; Fuentes-Perez, M. E.; Moreno-Herrero, F.; Keyser, U. F. DNA origami nanopores for controlling DNA translocation ACS Nano 2013, 7, 6024-6030
51. Burns, J. R.; Stulz, E.; Howorka, S. Self-assembled DNA nanopores that span lipid bilayers Nano Lett 2013, 13, 2351-2356
52. Fan, Z.; Liu, H.; Mayer, M.; Deng, C. X. Spatiotemporally controlled single cell sonoporation Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 16486-16491
53. Reneer, M. C.; Estes, D. J.; Velez-Ortega, A. C.; Norris, A.; Mayer, M.; Marti, F. Peripherally induced human regulatory T cells uncouple Kv1.3 activation from TCR-associated signaling Eur. J. Immunol. 2011, 41, 3170-3175
54. Estes, D. J.; Memarsadeghi, S.; Lundy, S. K.; Marti, F.; Mikol, D. D.; Fox, D. A.; Mayer, M. High-throughput profiling of ion channel activity in primary human lymphocytes Anal. Chem. 2008, 80, 3728-3735 (Pubitemid 351705874)
55. Wulff, H.; Beeton, C.; Chandy, K. G. Potassium channels as therapeutic targets for autoimmune disorders Curr. Opin. Drug Discovery Dev. 2003, 6, 640-647 (Pubitemid 37287933)
56. Milligan, C. J.; Moller, C. Automated planar patch-clamp Methods Mol. Biol. 2013, 998, 171-187
57. Haythornthwaite, A.; Stoelzle, S.; Hasler, A.; Kiss, A.; Mosbacher, J.; George, M.; Bruggemann, A.; Fertig, N. Characterizing human ion channels in induced pluripotent stem cell-derived neurons J. Biomol. Screening 2012, 17, 1264-1272
58. Capone, R.; Quiroz, F. G.; Prangkio, P.; Saluja, I.; Sauer, A. M.; Bautista, M. R.; Turner, R. S.; Yang, J.; Mayer, M. Amyloid-beta-induced ion flux in artificial lipid bilayers and neuronal cells: Resolving a controversy Neurotox. Res. 2009, 16, 1-13
59. Jeon, T. J.; Malmstadt, N.; Poulos, J. L.; Schmidt, J. J. Black lipid membranes stabilized through substrate conjugation to a hydrogel Biointerphases 2008, 3, FA96-FA100
60. Majd, S.; Yusko, E. C.; Yang, J.; Sept, D.; Mayer, M. A model for the interfacial kinetics of phospholipase D activity on long-chain lipids Biophys. J. 2013, 105, 146-153