Biomimetic potassium-selective nanopores

Acar, Elif Turker; Buchsbaum, Steven F.; Combs, Cody; Fornasiero, Francesco; Siwy, Zuzanna S.

doi:10.1126/sciadv.aav2568

Title: Biomimetic potassium-selective nanopores

Journal Article · Fri Feb 08 00:00:00 EST 2019 · Science Advances

DOI:https://doi.org/10.1126/sciadv.aav2568· OSTI ID:1513132

^[1];

^[2];

^[3];

^[2];

^[4]

Univ. of California, Irvine, CA (United States). Dept. of Physics and Astronomy; Istanbul Univ. Cerrahpasa, Avcılar-Istanbul (Turkey). Dept. of Chemistry
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Univ. of California, Irvine, CA (United States). Dept. of Physics and Astronomy
Univ. of California, Irvine, CA (United States). Dept. of Physics and Astronomy, Dept. of Chemistry, Dept. of Biomedical Engineering

Reproducing the exquisite ion selectivity displayed by biological ion channels in artificial nanopore systems has proven to be one of the most challenging tasks undertaken by the nanopore community, yet a successful achievement of this goal offers immense technological potential. Here, we show a strategy to design solid-state nanopores that selectively transport potassium ions and show negligible conductance for sodium ions. The nanopores contain walls decorated with 4'-aminobenzo-18-crown-6 ether and single-stranded DNA (ssDNA) molecules located at one pore entrance. The ionic selectivity stems from facilitated transport of potassium ions in the pore region containing crown ether, while the highly charged ssDNA plays the role of a cation filter. Achieving potassium selectivity in solid-state nanopores opens new avenues toward advanced separation processes, more efficient biosensing technologies, and novel biomimetic nanopore systems.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: AC52-07NA27344

OSTI ID:: 1513132

Report Number(s):: LLNL-JRNL-760930; 949836

Journal Information:: Science Advances, Vol. 5, Issue 2; ISSN 2375-2548

Publisher:: AAASCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 87 works

Citation information provided by
Web of Science

References (40)

Thermodynamic and Kinetic Data for Macrocycle Interaction with Cations, Anions, and Neutral Molecules Izatt, Reed M.; Pawlak, Krystyna.; Bradshaw, Jerald S. Chemical Reviews, Vol. 95, Issue 7 https://doi.org/10.1021/cr00039a010	journal	November 1995
Thickness-dependent dielectric breakdown and nanopore creation on sub-10-nm-thick SiN membranes in solution Yanagi, Itaru; Fujisaki, Koji; Hamamura, Hirotaka Journal of Applied Physics, Vol. 121, Issue 4 https://doi.org/10.1063/1.4974286	journal	January 2017
Biomimetic smart nanopores and nanochannels Hou, Xu; Guo, Wei; Jiang, Lei Chemical Society Reviews, Vol. 40, Issue 5 https://doi.org/10.1039/c0cs00053a	journal	January 2011
DNA-Modified Polymer Pores Allow pH- and Voltage-Gated Control of Channel Flux Buchsbaum, Steven F.; Nguyen, Gael; Howorka, Stefan Journal of the American Chemical Society, Vol. 136, Issue 28 https://doi.org/10.1021/ja505302q	journal	July 2014
Novel Resorcin[4]arenes as Potassium-Selective Ion-Channel and Transporter Mimics Wright, Angela J.; Matthews, Susan E.; Fischer, Wolfgang B. Chemistry - A European Journal, Vol. 7, Issue 16 https://doi.org/10.1002/1521-3765(20010817)7:16<3474::AID-CHEM3474>3.0.CO;2-6	journal	August 2001
Highly Selective Artificial K ⁺ Channels: An Example of Selectivity-Induced Transmembrane Potential Gilles, Arnaud; Barboiu, Mihail Journal of the American Chemical Society, Vol. 138, Issue 1 https://doi.org/10.1021/jacs.5b11743	journal	December 2015
Fabrication of multiple nanopores in a SiNx membrane via controlled breakdown Wang, Yunlong; Ying, Cuifeng; Zhou, Wenyuan Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-19450-7	journal	January 2018
Dynamic hybrid materials for constitutional self-instructed membranes Cazacu, A.; Legrand, Y. -M.; Pasc, A. Proceedings of the National Academy of Sciences, Vol. 106, Issue 20 https://doi.org/10.1073/pnas.0813257106	journal	April 2009
Stochastic sensing of proteins with receptor-modified solid-state nanopores Wei, Ruoshan; Gatterdam, Volker; Wieneke, Ralph Nature Nanotechnology, Vol. 7, Issue 4 https://doi.org/10.1038/nnano.2012.24	journal	March 2012
Nanopore Fabrication by Controlled Dielectric Breakdown Kwok, Harold; Briggs, Kyle; Tabard-Cossa, Vincent PLoS ONE, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pone.0092880	journal	March 2014
Crown ethers in graphene Guo, Junjie; Lee, Jaekwang; Contescu, Cristian I. Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6389	journal	November 2014
Potassium Channels and the Atomic Basis of Selective Ion Conduction (Nobel Lecture) MacKinnon, Roderick Angewandte Chemie International Edition, Vol. 43, Issue 33 https://doi.org/10.1002/anie.200400662	journal	August 2004
Voltage-Gated Hydrophobic Nanopores Smirnov, Sergei N.; Vlassiouk, Ivan V.; Lavrik, Nickolay V. ACS Nano, Vol. 5, Issue 9 https://doi.org/10.1021/nn202392d	journal	August 2011
Host–guest supramolecular chemistry in solid-state nanopores: potassium-driven modulation of ionic transport in nanofluidic diodes Pérez-Mitta, Gonzalo; Albesa, Alberto G.; Knoll, Wolfgang Nanoscale, Vol. 7, Issue 38 https://doi.org/10.1039/C5NR04645A	journal	January 2015
DNA−Nanotube Artificial Ion Channels Harrell, C. Chad; Kohli, Punit; Siwy, Zuzanna Journal of the American Chemical Society, Vol. 126, Issue 48 https://doi.org/10.1021/ja044948v	journal	December 2004
Ionic Blockage of Sodium Channels in Nerve Woodhull, A. M. The Journal of General Physiology, Vol. 61, Issue 6 https://doi.org/10.1085/jgp.61.6.687	journal	June 1973
Fabrication of Carboxylated Silicon Nitride Sensor Chips for Detection of Antigen–Antibody Reaction Using Microfluidic Reflectometric Interference Spectroscopy Kurihara, Yoshikazu; Takama, Masaaki; Sekiya, Tadanobu Langmuir, Vol. 28, Issue 38 https://doi.org/10.1021/la302221y	journal	September 2012
Fundamental studies and practical applications of bio-inspired smart solid-state nanopores and nanochannels Zhang, Huacheng; Tian, Ye; Jiang, Lei Nano Today, Vol. 11, Issue 1 https://doi.org/10.1016/j.nantod.2015.11.001	journal	February 2016
Protein Biosensors Based on Biofunctionalized Conical Gold Nanotubes Siwy, Zuzanna; Trofin, Lacramioara; Kohli, Punit Journal of the American Chemical Society, Vol. 127, Issue 14 https://doi.org/10.1021/ja043910f	journal	April 2005
The Structure of the Potassium Channel: Molecular Basis of K+ Conduction and Selectivity Doyle, D. A. Science, Vol. 280, Issue 5360 https://doi.org/10.1126/science.280.5360.69	journal	April 1998
Thermally Switchable Aligned Nanopores by Magnetic-Field Directed Self-Assembly of Block Copolymers Gopinadhan, Manesh; Deshmukh, Prashant; Choo, Youngwoo Advanced Materials, Vol. 26, Issue 30 https://doi.org/10.1002/adma.201401569	journal	June 2014
Highly Selective Artificial Cholesteryl Crown Ether K ⁺ -Channels Sun, Zhanhu; Barboiu, Mihail; Legrand, Yves-Marie Angewandte Chemie International Edition, Vol. 54, Issue 48 https://doi.org/10.1002/anie.201506430	journal	October 2015
Concentration-Polarization-Induced Precipitation and Ionic Current Oscillations with Tunable Frequency Acar, Elif Turker; Hinkle, Preston; Siwy, Zuzanna S. The Journal of Physical Chemistry C, Vol. 122, Issue 6 https://doi.org/10.1021/acs.jpcc.7b12265	journal	January 2018
From Natural to Bioassisted and Biomimetic Artificial Water Channel Systems Barboiu, Mihail; Gilles, Arnaud Accounts of Chemical Research, Vol. 46, Issue 12 https://doi.org/10.1021/ar400025e	journal	January 2013
Biomimetic nanopores: learning from and about nature Kowalczyk, Stefan W.; Blosser, Timothy R.; Dekker, Cees Trends in Biotechnology, Vol. 29, Issue 12 https://doi.org/10.1016/j.tibtech.2011.07.006	journal	December 2011
Electric-field-induced wetting and dewetting in single hydrophobic nanopores Powell, Matthew R.; Cleary, Leah; Davenport, Matthew Nature Nanotechnology, Vol. 6, Issue 12 https://doi.org/10.1038/nnano.2011.189	journal	October 2011
Combinatorial Evolution of Fast-Conducting Highly Selective K ⁺ -Channels via Modularly Tunable Directional Assembly of Crown Ethers Ren, Changliang; Shen, Jie; Zeng, Huaqiang Journal of the American Chemical Society, Vol. 139, Issue 36 https://doi.org/10.1021/jacs.7b04335	journal	August 2017
Thermodynamic and kinetic data for cation-macrocycle interaction Izatt, Reed M.; Bradshaw, Jerald S.; Nielsen, Steven A. Chemical Reviews, Vol. 85, Issue 4 https://doi.org/10.1021/cr00068a003	journal	August 1985
Highly Selective Artificial Cholesteryl Crown Ether K ⁺ -Channels Sun, Zhanhu; Barboiu, Mihail; Legrand, Yves-Marie Angewandte Chemie, Vol. 127, Issue 48 https://doi.org/10.1002/ange.201506430	journal	October 2015
Self-assembling subnanometer pores with unusual mass-transport properties Zhou, Xibin; Liu, Guande; Yamato, Kazuhiro Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms1949	journal	January 2012
Transport mechanisms in nanopores and nanochannels: can we mimic nature? Tagliazucchi, Mario; Szleifer, Igal Materials Today, Vol. 18, Issue 3 https://doi.org/10.1016/j.mattod.2014.10.020	journal	April 2015
Access resistance of a small circular pore Hall, J. E. The Journal of General Physiology, Vol. 66, Issue 4 https://doi.org/10.1085/jgp.66.4.531	journal	October 1975
Bis-15-crown-5-ether-pillar[5]arene K ⁺ -Responsive Channels Feng, Wei-Xu; Sun, Zhanhu; Zhang, Yan Organic Letters, Vol. 19, Issue 6 https://doi.org/10.1021/acs.orglett.7b00352	journal	March 2017
Gating of Single Synthetic Nanopores by Proton-Driven DNA Molecular Motors Xia, Fan; Guo, Wei; Mao, Youdong Journal of the American Chemical Society, Vol. 130, Issue 26 https://doi.org/10.1021/ja800266p	journal	July 2008
Nanopore Fabrication by Controlled Dielectric Breakdown Kwok, Harold; Briggs, Kyle; Tabard-Cossa, Vincent arXiv https://doi.org/10.48550/arxiv.1310.5126	text	January 2013
Single-molecule analysis of DNA-protein complexes using nanopores Hornblower, Breton; Coombs, Amy; Whitaker, Richard D. Nature Methods, Vol. 4, Issue 4 https://doi.org/10.1038/nmeth1021	journal	March 2007
Engineered voltage-responsive nanopores Siwy, Zuzanna S.; Howorka, Stefan Chem. Soc. Rev., Vol. 39, Issue 3 https://doi.org/10.1039/B909105J	journal	January 2010
Facilitated Target Location in Biological Systems von Hippel, P. H.; Berg, O. G. Journal of Biological Chemistry, Vol. 264, Issue 2 https://doi.org/10.1016/S0021-9258(19)84994-3	journal	January 1989
Molecular simulation studies of hydrophobic gating in nanopores and ion channels Trick, Jemma L.; Aryal, Prafulla; Tucker, Stephen J. Biochemical Society Transactions, Vol. 43, Issue 2 https://doi.org/10.1042/bst20140256	journal	April 2015
Salt dependence of the radius of gyration and flexibility of single-stranded DNA in solution probed by small-angle x-ray scattering Sim, Adelene Y. L.; Lipfert, Jan; Herschlag, Daniel Physical Review E, Vol. 86, Issue 2 https://doi.org/10.1103/physreve.86.021901	journal	August 2012

Cited By (11)

Self‐Assembled Gold Arrays That Allow Rectification by Nanoscale Selectivity Cai, Jiarong; Ma, Wei; Xu, Liguang Angewandte Chemie International Edition, Vol. 58, Issue 48 https://doi.org/10.1002/anie.201909447	journal	November 2019
Ion current rectification: from nanoscale to microscale Xiong, Tianyi; Zhang, Kailin; Jiang, Yanan Science China Chemistry, Vol. 62, Issue 10 https://doi.org/10.1007/s11426-019-9526-4	journal	September 2019
Electrokinetic ion transport in an asymmetric double-gated nanochannel with a pH-tunable zwitterionic surface Hsu, Jyh-Ping; Chen, Yu-Min; Lin, Chih-Yuan Physical Chemistry Chemical Physics, Vol. 21, Issue 15 https://doi.org/10.1039/c9cp00266a	journal	January 2019
Controlled Focused Ion Beam Milling of Composite Solid State Nanopore Arrays for Molecule Sensing Fürjes, Péter Micromachines, Vol. 10, Issue 11 https://doi.org/10.3390/mi10110774	journal	November 2019
Engineering Smart Nanofluidic Systems for Artificial Ion Channels and Ion Pumps: From Single‐Pore to Multichannel Membranes Zhang, Zhen; Huang, Xiaodong; Qian, Yongchao Advanced Materials, Vol. 32, Issue 4 https://doi.org/10.1002/adma.201904351	journal	December 2019
Rod‐Cell‐Mimetic Photochromic Layered Ion Channels with Multiple Switchable States for Controllable Ion Transport Xiao, Tianliang; Ma, Jing; Jiang, Jiaqiao Chemistry – A European Journal, Vol. 25, Issue 55 https://doi.org/10.1002/chem.201902450	journal	September 2019
Application of a bipolar nanopore as a sensor: rectification as an additional device function Mádai, Eszter; Valiskó, Mónika; Boda, Dezső Physical Chemistry Chemical Physics, Vol. 21, Issue 36 https://doi.org/10.1039/c9cp03821c	journal	January 2019
A nanofluidic osmotic power generator demonstrated in polymer gel electrolytes with substantially enhanced performance Yeh, Li-Hsien; Huang, Zih-Ying; Liu, Yi-Cheng Journal of Materials Chemistry A, Vol. 7, Issue 47 https://doi.org/10.1039/c9ta10028h	journal	January 2019
A pyrophosphate-activated nanochannel inspired by a TRP ion channel Zhu, Fei; Yang, Guanxing; Dhinakaran, Manivannan Kalavathi Chemical Communications, Vol. 55, Issue 85 https://doi.org/10.1039/c9cc06615b	journal	January 2019
Self‐Assembled Gold Arrays That Allow Rectification by Nanoscale Selectivity Cai, Jiarong; Ma, Wei; Xu, Liguang Angewandte Chemie, Vol. 131, Issue 48 https://doi.org/10.1002/ange.201909447	journal	November 2019
Ionic amplifying circuits inspired by electronics and biology Lucas, Rachel A.; Lin, Chih-Yuan; Baker, Lane A. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15398-3	journal	March 2020