Building membrane nanopores.

Membrane nanopores-hollow nanoscale barrels that puncture biological or synthetic membranes-have become powerful tools in chemical- and biosensing, and have achieved notable success in portable DNA sequencing. The pores can be self-assembled from a variety of materials, including proteins, peptides, synthetic organic compounds and, more recently, DNA. But which building material is best for which application, and what is the relationship between pore structure and function? In this Review, I critically compare the characteristics of the different building materials, and explore the influence of the building material on pore structure, dynamics and function. I also discuss the future challenges of developing nanopore technology, and consider what the next-generation of nanopore structures could be and where further practical applications might emerge.

[1]  S. Howorka,et al.  Self-assembled DNA nanopores that span lipid bilayers. , 2013, Nano letters.

[2]  T. Heimburg,et al.  Lipid ion channels and the role of proteins. , 2013, Accounts of chemical research.

[3]  G. Rummel,et al.  Crystal structures explain functional properties of two E. coli porins , 1992, Nature.

[4]  I. Izzo,et al.  Ion transport through lipid bilayers by synthetic ionophores: modulation of activity and selectivity. , 2013, Accounts of chemical research.

[5]  C. Montemagno,et al.  Incorporation of a viral DNA-packaging motor channel in lipid bilayers for real-time, single-molecule sensing of chemicals and double-stranded DNA , 2013, Nature Protocols.

[6]  Cees Dekker,et al.  Graphene nanodevices for DNA sequencing. , 2016, Nature nanotechnology.

[7]  Friedrich C. Simmel,et al.  Membrane-Assisted Growth of DNA Origami Nanostructure Arrays , 2015, ACS nano.

[8]  Jingmin Jin,et al.  Rapid electronic detection of probe-specific microRNAs using thin nanopore sensors. , 2010, Nature nanotechnology.

[9]  L. Tamm,et al.  Structure of outer membrane protein G by solution NMR spectroscopy , 2007, Proceedings of the National Academy of Sciences.

[10]  Liang Wang,et al.  Nanopore stochastic detection: diversity, sensitivity, and beyond. , 2013, Accounts of chemical research.

[11]  A. Brik,et al.  Expanding the chemical toolbox for the synthesis of large and uniquely modified proteins. , 2016, Nature chemistry.

[12]  M. Ghadiri,et al.  Ion channel models based on self-assembling cyclic peptide nanotubes. , 2013, Accounts of chemical research.

[13]  H. Bayley,et al.  Semisynthetic protein nanoreactor for single-molecule chemistry , 2015, Proceedings of the National Academy of Sciences.

[14]  Sergey M Bezrukov,et al.  On 'three decades of nanopore sequencing' , 2016, Nature Biotechnology.

[15]  Stuart Lindsay,et al.  The promises and challenges of solid-state sequencing. , 2016, Nature nanotechnology.

[16]  L. A. Baker,et al.  Nanopore Sensing. , 2017, Analytical chemistry.

[17]  H. Bayley,et al.  Photoisomerization of an individual azobenzene molecule in water: an on-off switch triggered by light at a fixed wavelength. , 2006, Journal of the American Chemical Society.

[18]  C. Robinson,et al.  Membrane proteins bind lipids selectively to modulate their structure and function , 2014, Nature.

[19]  D C Rees,et al.  Structure of the MscL homolog from Mycobacterium tuberculosis: a gated mechanosensitive ion channel. , 1998, Science.

[20]  Robert C. Wolpert,et al.  A Review of the , 1985 .

[21]  William L. Hwang,et al.  Droplet networks with incorporated protein diodes show collective properties. , 2009, Nature nanotechnology.

[22]  Pekka Orponen,et al.  DNA rendering of polyhedral meshes at the nanoscale , 2015, Nature.

[23]  Jochen W. Klingelhoefer,et al.  Functional truncated membrane pores , 2014, Proceedings of the National Academy of Sciences.

[24]  G. Kochendoerfer,et al.  Total chemical synthesis and electrophysiological characterization of mechanosensitive channels from Escherichia coli and Mycobacterium tuberculosis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Olaf S Andersen,et al.  Bilayer thickness and membrane protein function: an energetic perspective. , 2007, Annual review of biophysics and biomolecular structure.

[26]  Friedrich C Simmel,et al.  Molecular transport through large-diameter DNA nanopores , 2016, Nature Communications.

[27]  I. Derrington,et al.  Detection and mapping of 5-methylcytosine and 5-hydroxymethylcytosine with nanopore MspA , 2013, Proceedings of the National Academy of Sciences.

[28]  H. W. Lam,et al.  Catalytic 1,4-Rhodium(III) Migration Enables 1,3-Enynes to Function as One-Carbon Oxidative Annulation Partners in C–H Functionalizations , 2014, Angewandte Chemie.

[29]  B. Cornell,et al.  A biosensor that uses ion-channel switches , 1997, Nature.

[30]  Tae-Joon Jeon,et al.  Hydrogel-encapsulated lipid membranes. , 2006, Journal of the American Chemical Society.

[31]  P. Rothemund.  Folding DNA to create nanoscale shapes and patterns , 2006, Nature.

[32]  S. Howorka,et al.  Membrane-Spanning DNA Nanopores with Cytotoxic Effect , 2014, Angewandte Chemie.

[33]  B. Chait,et al.  The structure of the potassium channel: molecular basis of K+ conduction and selectivity. , 1998, Science.

[34]  L Kochevar,et al.  Form Follows Function , 1997, AAOHN journal : official journal of the American Association of Occupational Health Nurses.

[35]  E. Isacoff,et al.  Light-activated ion channels for remote control of neuronal firing , 2004, Nature Neuroscience.

[36]  H. Bayley,et al.  Continuous observation of the stochastic motion of an individual small-molecule walker , 2014, Nature nanotechnology.

[37]  Matthew A Watson,et al.  Man-made molecular machines: membrane bound. , 2016, Chemical Society reviews.

[38]  J. Lipkowski,et al.  Direct visualization of the alamethicin pore formed in a planar phospholipid matrix , 2012, Proceedings of the National Academy of Sciences.

[39]  Mathias Winterhalter,et al.  Giant Free-Standing ABA Triblock Copolymer Membranes , 2000 .

[40]  Jejoong Yoo,et al.  Modeling and simulation of ion channels. , 2012, Chemical reviews.

[41]  Tim Liedl,et al.  DNA-Tile Structures Induce Ionic Currents through Lipid Membranes. , 2015, Nano letters.

[42]  H. Bayley,et al.  An engineered dimeric protein pore that spans adjacent lipid bilayers , 2013, Nature Communications.

[43]  Ben L Feringa,et al.  A Light-Actuated Nanovalve Derived from a Channel Protein , 2005, Science.

[44]  Friedrich C. Simmel,et al.  DNA nanostructures interacting with lipid bilayer membranes. , 2014, Accounts of chemical research.

[45]  M. Niederweis,et al.  Reading DNA at single-nucleotide resolution with a mutant MspA nanopore and phi29 DNA polymerase , 2012, Nature Biotechnology.

[46]  H. Bayley,et al.  Formation of a chiral center and pyrimidal inversion at the single-molecule level. , 2007, Angewandte Chemie.

[47]  Kyunghoon Kim,et al.  Ultrafast proton transport in sub-1-nm diameter carbon nanotube porins. , 2016, Nature nanotechnology.

[48]  G. Schneider,et al.  Designing antimicrobial peptides: form follows function , 2011, Nature Reviews Drug Discovery.

[49]  S. Howorka,et al.  Sequence-specific detection of individual DNA strands using engineered nanopores , 2001, Nature Biotechnology.

[50]  Z. Siwy,et al.  Nanopore analytics: sensing of single molecules. , 2009, Chemical Society reviews.

[51]  Hao Yan,et al.  DNA-cholesterol barges as programmable membrane-exploring agents. , 2014, ACS nano.

[52]  T. Fyles.  How do amphiphiles form ion-conducting channels in membranes? Lessons from linear oligoesters. , 2013, Accounts of chemical research.

[53]  H. Sitte,et al.  Nanopharmacological Force Sensing to Reveal Allosteric Coupling in Transporter Binding Sites. , 2016, Angewandte Chemie.

[54]  S. Buchanan,et al.  The structure of the β-barrel assembly machinery complex , 2016, Science.

[55]  W. Hendrickson.  Atomic-level analysis of membrane-protein structure , 2016, Nature Structural &Molecular Biology.

[56]  G. Whitesides,et al.  Using ion channel-forming peptides to quantify protein-ligand interactions. , 2008, Journal of the American Chemical Society.

[57]  Marcus Mueller,et al.  The structure of a cytolytic α-helical toxin pore reveals its assembly mechanism , 2009, Nature.

[58]  S. Matile,et al.  Ion channels and pores, made from scratch. , 2007, Molecular bioSystems.

[59]  Ulrich Koert,et al.  Synthetic ion channels. , 2004, Bioorganic & medicinal chemistry.

[60]  N. Seeman,et al.  Programmable materials and the nature of the DNA bond , 2015, Science.

[61]  H. Bayley,et al.  Capture of a single molecule in a nanocavity. , 2001, Science.

[62]  Luvena L. Ong,et al.  Three-Dimensional Structures Self-Assembled from DNA Bricks , 2012, Science.

[63]  Mark Akeson,et al.  Unfoldase-mediated protein translocation through an α-hemolysin nanopore , 2013, Nature Biotechnology.

[64]  Gabriel Waksman,et al.  Secretion systems in Gram-negative bacteria: structural and mechanistic insights , 2015, Nature Reviews Microbiology.

[65]  N. Voyer,et al.  A Synthetic Transmembrane Channel Active in Lipid Bilayers , 1997 .

[66]  G. Bainbridge.  Energetic perspective , 1975, Nature.

[67]  Svetlana Litvinchuk,et al.  AFM snapshots of synthetic multifunctional pores with polyacetylene blockers: pseudorotaxanes and template effects. , 2005, Angewandte Chemie.

[68]  H. Bayley,et al.  Temperature-responsive protein pores. , 2006, Journal of the American Chemical Society.

[69]  Jejoong Yoo,et al.  Large-Conductance Transmembrane Porin Made from DNA Origami , 2016, ACS nano.

[70]  Hao Yan,et al.  Challenges and opportunities for structural DNA nanotechnology. , 2011, Nature nanotechnology.

[71]  U. Keyser,et al.  Ion Channels Made from a Single Membrane-Spanning DNA Duplex , 2016, Nano letters.

[72]  P. J. Focke,et al.  Studies of ion channels using expressed protein ligation. , 2010, Current opinion in chemical biology.

[73]  Yazan N. Billeh,et al.  Applications of biological pores in nanomedicine, sensing, and nanoelectronics. , 2010, Current opinion in biotechnology.

[74]  O. Andersen,et al.  On the supramolecular organization of gramicidin channels. The elementary conducting unit is a dimer. , 1992, Biophysical journal.

[75]  C Raillon,et al.  Detecting the translocation of DNA through a nanopore using graphene nanoribbons. , 2013, Nature nanotechnology.

[76]  N. Seeman.  Nanomaterials based on DNA. , 2010, Annual review of biochemistry.

[77]  S. Matile,et al.  Artificial β-Barrels , 2009 .

[78]  H. Bayley,et al.  Engineered transmembrane pores. , 2016, Current opinion in chemical biology.

[79]  Ulrich F. Keyser,et al.  Digitally encoded DNA nanostructures for multiplexed, single-molecule protein sensing with nanopores. , 2016, Nature nanotechnology.

[80]  G. Gokel,et al.  Synthetic ion channels: from pores to biological applications. , 2013, Accounts of chemical research.

[81]  N. Shinohara,et al.  Total synthesis of the large non-ribosomal peptide polytheonamide B. , 2010, Nature chemistry.

[82]  Shawn M. Douglas,et al.  Folding DNA into Twisted and Curved Nanoscale Shapes , 2009, Science.

[83]  Nicholas A. W. Bell,et al.  Nanopores formed by DNA origami: A review , 2014, FEBS letters.

[84]  G. Gokel,et al.  Pore formation in phospholipid bilayers by branched-chain pyrogallol[4]arenes. , 2011, Journal of the American Chemical Society.

[85]  Robert Tampé,et al.  Highly Parallel Transport Recordings on a Membrane-on-Nanopore Chip at Single Molecule Resolution , 2014, Nano letters.

[86]  Adam H. Marblestone,et al.  Rapid prototyping of 3D DNA-origami shapes with caDNAno , 2009, Nucleic acids research.

[87]  S. Howorka,et al.  Structural and mechanistic insights into the bacterial amyloid secretion channel CsgG , 2014, Nature.

[88]  Patrick Couvreur,et al.  Stimuli-responsive nanocarriers for drug delivery. , 2013, Nature materials.

[89]  S. Howorka,et al.  A biomimetic DNA-based channel for the ligand-controlled transport of charged molecular cargo across a biological membrane. , 2016, Nature nanotechnology.

[90]  S. Howorka,et al.  A protein pore with a single polymer chain tethered within the lumen , 2000 .

[91]  Benjamien Moeyaert,et al.  An engineered ClyA nanopore detects folded target proteins by selective external association and pore entry. , 2012, Nano letters.

[92]  Yong Wang,et al.  Nanopore-based detection of circulating microRNAs in lung cancer patients , 2011, Nature nanotechnology.

[93]  C. Steinem,et al.  A DNA-inspired synthetic ion channel based on G-C base pairing. , 2015, Journal of the American Chemical Society.

[94]  T. Martin Schmeing,et al.  Synthetic cycle of the initiation module of a formylating nonribosomal peptide synthetase , 2016, Nature.

[95]  Syma Khalid,et al.  Outer membrane protein G: Engineering a quiet pore for biosensing , 2008, Proceedings of the National Academy of Sciences.

[96]  Oliver K Castell,et al.  High-throughput optical sensing of nucleic acids in a nanopore array , 2015, Nature nanotechnology.

[97]  G. Robillard,et al.  A biological porin engineered into a molecular, nanofluidic diode. , 2007, Nano letters.

[98]  M. Dunstone,et al.  Packing a punch: the mechanism of pore formation by cholesterol dependent cytolysins and membrane attack complex/perforin-like proteins. , 2012, Current opinion in structural biology.

[99]  Jerry Yang,et al.  Engineered ion channels as emerging tools for chemical biology. , 2013, Accounts of chemical research.

[100]  Joseph E. Goose,et al.  MemProtMD: Automated Insertion of Membrane Protein Structures into Explicit Lipid Membranes , 2015, Structure.

[101]  Stefan Howorka,et al.  Bilayer-Spanning DNA Nanopores with Voltage-Switching between Open and Closed State , 2014, ACS nano.

[102]  Joshua B Edel,et al.  Single molecule sensing with solid-state nanopores: novel materials, methods, and applications. , 2013, Chemical Society reviews.

[103]  H. Sleiman,et al.  Site-specific positioning of dendritic alkyl chains on DNA cages enables their geometry-dependent self-assembly. , 2013, Nature chemistry.

[104]  Jiwook Shim,et al.  Stochastic sensing on a modular chip containing a single-ion channel. , 2007, Analytical chemistry.

[105]  H. Bayley,et al.  Protein Detection by Nanopores Equipped with Aptamers , 2012, Journal of the American Chemical Society.

[106]  Costas P. Grigoropoulos,et al.  Stochastic transport through carbon nanotubes in lipid bilayers and live cell membranes , 2014, Nature.

[107]  S. Hussain,et al.  Efficient, non-toxic anion transport by synthetic carriers in cells and epithelia , 2015, Nature Chemistry.

[108]  Mathias Winterhalter,et al.  Reconstitution of Channel Proteins in (Polymerized) ABA Triblock Copolymer Membranes , 2000 .

[109]  Gevorg Grigoryan,et al.  De novo design of a transmembrane Zn2+-transporting four-helix bundle , 2014, Science.

[110]  David Needham,et al.  Functional bionetworks from nanoliter water droplets. , 2007, Journal of the American Chemical Society.

[111]  Christopher D Spicer,et al.  Selective chemical protein modification , 2014, Nature Communications.

[112]  S. Matile,et al.  Synthetic ion channels with rigid-rod pi-stack architecture that open in response to charge-transfer complex formation. , 2005, Journal of the American Chemical Society.

[113]  Sheereen Majd,et al.  Controlling protein translocation through nanopores with bio-inspired fluid walls , 2011 .

[114]  J. Gouaux,et al.  Designed protein pores as components for biosensors. , 1997, Chemistry & biology.

[115]  Georg E. Schulz,et al.  The Structure of a Mycobacterial Outer-Membrane Channel , 2004, Science.

[116]  Hao Yan,et al.  DNA Origami with Complex Curvatures in Three-Dimensional Space , 2011, Science.

[117]  Gabriel Villar,et al.  A Tissue-Like Printed Material , 2013, Science.

[118]  Jonathan K. W. Chui,et al.  Ionic conductance of synthetic channels: analysis, lessons, and recommendations. , 2012, Chemical Society reviews.

[119]  L. Movileanu,et al.  Interrogating single proteins through nanopores: challenges and opportunities. , 2009, Trends in biotechnology.

[120]  H. Bayley,et al.  Stochastic detection of enantiomers. , 2006, Journal of the American Chemical Society.

[121]  Jacob J. Schmidt.  Membrane platforms for biological nanopore sensing and sequencing. , 2016, Current opinion in biotechnology.

[122]  Richard A. Muscat,et al.  DNA nanotechnology from the test tube to the cell. , 2015, Nature nanotechnology.

[123]  Vivek V. Thacker,et al.  Lipid-Bilayer-Spanning DNA Nanopores with a Bifunctional Porphyrin Anchor , 2013, Angewandte Chemie.

[124]  James H. Naismith,et al.  Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein , 2006, Nature.

[125]  Jing Wang,et al.  Self-assembly of size-controlled liposomes on DNA nanotemplates , 2016, Nature chemistry.

[126]  Kazuhiko Kinosita,et al.  Direct observation of the rotation of F1-ATPase , 1997, Nature.

[127]  S. Matile,et al.  Artificial beta-barrels. , 2008, Accounts of chemical research.

[128]  M. Barboiu,et al.  Highly Selective Artificial K(+) Channels: An Example of Selectivity-Induced Transmembrane Potential. , 2016, Journal of the American Chemical Society.

[129]  A. Gavin,et al.  The systematic analysis of protein–lipid interactions comes of age , 2015, Nature Reviews Molecular Cell Biology.

[130]  Ruoshan Wei,et al.  Stochastic sensing of proteins with receptor-modified solid-state nanopores. , 2012, Nature nanotechnology.

[131]  David A. Matthews,et al.  Real-time, portable genome sequencing for Ebola surveillance , 2016, Nature.

[132]  A. Aksimentiev,et al.  Molecular Dynamics of Membrane-Spanning DNA Channels: Conductance Mechanism, Electro-Osmotic Transport, and Mechanical Gating. , 2015, The journal of physical chemistry letters.

[133]  Daniel J. Estes,et al.  A semi-synthetic ion channel platform for detection of phosphatase and protease activity. , 2009, ACS nano.

[134]  Hao Yan,et al.  Complex wireframe DNA origami nanostructures with multi-arm junction vertices. , 2015, Nature nanotechnology.

[135]  T. G. Martin,et al.  DNA origami gatekeepers for solid-state nanopores. , 2012, Angewandte Chemie.

[136]  J. Dupuis,et al.  Coupling ion channels to receptors for biomolecule sensing. , 2008, Nature nanotechnology.

[137]  T. Fyles,et al.  Synthetic ion channels in bilayer membranes. , 2007, Chemical Society reviews.

[138]  R. MacKinnon,et al.  Ion Selectivity in a Semisynthetic K+ Channel Locked in the Conductive Conformation , 2006, Science.

[139]  Jonathan K. Williams,et al.  Solid-State NMR Investigation of the Conformation, Proton Conduction, and Hydration of the Influenza B Virus M2 Transmembrane Proton Channel. , 2016, Journal of the American Chemical Society.

[140]  Colin Nuckolls,et al.  Translocation of Single-Stranded DNA Through Single-Walled Carbon Nanotubes , 2010, Science.

[141]  Sheshanath V. Bhosale,et al.  Photoproduction of Proton Gradients with π-Stacked Fluorophore Scaffolds in Lipid Bilayers , 2006, Science.

[142]  S. Saavedra,et al.  Fractional polymerization of a suspended planar bilayer creates a fluid, highly stable membrane for ion channel recordings. , 2010, Journal of the American Chemical Society.

[143]  Petra Schwille,et al.  Amphipathic DNA origami nanoparticles to scaffold and deform lipid membrane vesicles. , 2015, Angewandte Chemie.

[144]  J. Gouaux,et al.  Structure of Staphylococcal α-Hemolysin, a Heptameric Transmembrane Pore , 1996, Science.

[145]  U. Koert,et al.  Ion-channels: goals for function-oriented synthesis. , 2013, Accounts of chemical research.

[146]  David M. Treiman,et al.  Changing of the guard , 2012, Epilepsy Research.

[147]  Richard B. Sessions,et al.  Computational design of water-soluble α-helical barrels , 2014, Science.

[148]  Sergey M Bezrukov,et al.  Single polymer molecules in a protein nanopore in the limit of a strong polymer-pore attraction. , 2006, Physical review letters.

[149]  Stefan Howorka,et al.  Detecting protein analytes that modulate transmembrane movement of a polymer chain within a single protein pore , 2000, Nature Biotechnology.

[150]  Shoji Takeuchi,et al.  Lipid bilayer formation by contacting monolayers in a microfluidic device for membrane protein analysis. , 2006, Analytical chemistry.

[151]  J. Kasianowicz,et al.  Conductance and ion selectivity of a mesoscopic protein nanopore probed with cysteine scanning mutagenesis. , 2005, Biophysical journal.

[152]  Daniel H Stoloff,et al.  Recent trends in nanopores for biotechnology. , 2013, Current opinion in biotechnology.

[153]  Aleksei Aksimentiev,et al.  Highly permeable artificial water channels that can self-assemble into two-dimensional arrays , 2015, Proceedings of the National Academy of Sciences.

[154]  Cees Dekker,et al.  Hybrid pore formation by directed insertion of α-haemolysin into solid-state nanopores. , 2010, Nature nanotechnology.

[155]  He Tian,et al.  Discrimination of oligonucleotides of different lengths with a wild-type aerolysin nanopore. , 2016, Nature nanotechnology.

[156]  R. Capone,et al.  Chemically reactive derivatives of gramicidin A for developing ion channel-based nanoprobes. , 2008, Bioconjugate chemistry.

[157]  Stefan Howorka,et al.  Stability and dynamics of membrane-spanning DNA nanopores , 2017, Nature Communications.

[158]  E. Isacoff,et al.  Allosteric control of an ionotropic glutamate receptor with an optical switch , 2006, Nature chemical biology.

[159]  Juan R. Granja,et al.  Antibacterial agents based on the cyclic d,l-α-peptide architecture , 2001, Nature.

[160]  H. Bayley,et al.  A primary hydrogen-deuterium isotope effect observed at the single-molecule level. , 2010, Nature chemistry.

[161]  Gevorg Grigoryan,et al.  Computational design and experimental characterization of peptides intended for pH-dependent membrane insertion and pore formation. , 2015, ACS chemical biology.

[162]  G. Maglia,et al.  A nanopore machine promotes the vectorial transport of DNA across membranes , 2013, Nature Communications.

[163]  H. Saibil,et al.  Atomic force microscopy of membrane pore formation by cholesterol dependent cytolysins. , 2016, Current opinion in structural biology.

[164]  T. G. Martin,et al.  Synthetic Lipid Membrane Channels Formed by Designed DNA Nanostructures , 2012, Science.

[165]  J. Tait,et al.  Challenges and opportunities. , 1996, Journal of psychiatric and mental health nursing.

[166]  William M. Shih,et al.  Virus-Inspired Membrane Encapsulation of DNA Nanostructures To Achieve In Vivo Stability , 2014, ACS nano.

[167]  George M Whitesides,et al.  Microfabricated teflon membranes for low-noise recordings of ion channels in planar lipid bilayers. , 2003, Biophysical journal.

[168]  Randal R Ketchem,et al.  High-resolution conformation of gramicidin A in a lipid bilayer by solid-state NMR. , 1993, Science.

[169]  Dumitru Dumcenco,et al.  Identification of single nucleotides in MoS2 nanopores. , 2015, Nature nanotechnology.

[170]  Derek N. Woolfson,et al.  Installing hydrolytic activity into a completely de novo protein framework. , 2016, Nature chemistry.

[171]  Svetlana Litvinchuk,et al.  Synthetic pores with reactive signal amplifiers as artificial tongues. , 2007, Nature materials.

[172]  Stefan Howorka,et al.  Gating-like Motions and Wall Porosity in a DNA Nanopore Scaffold Revealed by Molecular Simulations. , 2015, ACS nano.

[173]  Nicholas A W Bell,et al.  DNA origami nanopores. , 2012, Nano letters.

[174]  Sean Conlan,et al.  Stochastic sensing of organic analytes by a pore-forming protein containing a molecular adapter , 1999, Nature.

[175]  Michael Famulok,et al.  Pseudo-complementary PNA actuators as reversible switches in dynamic DNA nanotechnology , 2013, Nucleic acids research.

[176]  C. Dekker.  Solid-state nanopores. , 2007, Nature nanotechnology.

[177]  Mihail Barboiu,et al.  From Natural to Bioassisted and Biomimetic Artificial Water/Ion Channel Systems , 2014 .

[178]  B. Wallace,et al.  Circular dichroism spectroscopy of membrane proteins. , 2016, Chemical Society reviews.

[179]  Jason Campbell,et al.  Disease detection and management via single nanopore-based sensors. , 2012, Chemical reviews.

[180]  H. Bayley,et al.  Enhanced translocation of single DNA molecules through α-hemolysin nanopores by manipulation of internal charge , 2008, Proceedings of the National Academy of Sciences.

[181]  C. Vágvölgyi,et al.  The History of Alamethicin: A Review of the Most Extensively Studied Peptaibol , 2007, Chemistry & biodiversity.

[182]  H. Bayley,et al.  Stochastic sensors inspired by biology , 2001, Nature.

[183]  Junqiu Liu,et al.  Biomimetic Transmembrane Channels with High Stability and Transporting Efficiency from Helically Folded Macromolecules. , 2016, Angewandte Chemie.