Applications of tunable resistive pulse sensing.

Tunable resistive pulse sensing (TRPS) is an experimental technique that has been used to study and characterise colloidal particles ranging from approximately 50 nm in diameter up to the size of cells. The primary aim of this Review is to provide a guide to the characteristics and roles of TRPS in recent applied research. Relevant studies reflect both the maturation of the technique and the growing importance of submicron colloids in fields such as nanomedicine and biotechnology. TRPS analysis of extracellular vesicles is expanding particularly swiftly, while TRPS studies also extend to on-bead assays using DNA and aptamers, drug delivery particles, viruses and bacteria, food and beverages, and superparamagnetic beads. General protocols for TRPS measurement of particle size, concentration and charge have been developed, and a summary of TRPS technology and associated analysis techniques is included in this Review.

[1]  M. Trau,et al.  Simultaneous size and ζ-potential measurements of individual nanoparticles in dispersion using size-tunable pore sensors. , 2012, ACS nano.

[2]  Nathalie Tufenkji,et al.  Characterizing manufactured nanoparticles in the environment: multimethod determination of particle sizes. , 2009, Environmental science & technology.

[3]  Warren K. Mino,et al.  A method for reproducibly preparing synthetic nanopores for resistive-pulse biosensors. , 2007, Small.

[4]  Q. Pankhurst,et al.  Applications of magnetic nanoparticles in biomedicine , 2003 .

[5]  Omar A Alsager,et al.  Small molecule detection in solution via the size contraction response of aptamer functionalized nanoparticles. , 2014, Biosensors & bioelectronics.

[6]  G. Willmott,et al.  Co-ordinated detection of microparticles using tunable resistive pulse sensing and fluorescence spectroscopy. , 2015, Biomicrofluidics.

[7]  Lesley Cheng,et al.  Exosomes provide a protective and enriched source of miRNA for biomarker profiling compared to intracellular and cell-free blood , 2014, Journal of extracellular vesicles.

[8]  J. Giérak,et al.  Dynamics of colloids in single solid-state nanopores. , 2011, The journal of physical chemistry. B.

[9]  Characterization of a Nanoparticulate Drug Delivery System Using Scanning Ion Occlusion Sensing , 2012, Pharmaceutical Research.

[10]  Michelle Low,et al.  Investigative Study of Nucleic Acid-Gold Nanoparticle Interactions Using Laser-based Techniques, Electron Microscopy, and Resistive Pulse Sensing with a Nanopore , 2011 .

[11]  I. Chourpa,et al.  Nanovectors for anticancer agents based on superparamagnetic iron oxide nanoparticles , 2007, International journal of nanomedicine.

[12]  L. Lagae,et al.  Measuring the electric charge and zeta potential of nanometer-sized objects using pyramidal-shaped nanopores. , 2012, Analytical Chemistry.

[13]  Analysis and Finite Element Modelling of Resizable Nanopores , 2009 .

[14]  E. C. Gregg,et al.  Electrical counting and sizing of mammalian cells in suspension. , 1965, Biophysical journal.

[15]  D. Devos,et al.  Platelet microparticles: detection and assessment of their paradoxical functional roles in disease and regenerative medicine. , 2014, Blood reviews.

[16]  M. Trau,et al.  Tunable nano/micropores for particle detection and discrimination: scanning ion occlusion spectroscopy. , 2010, Small.

[17]  P. Déjardin,et al.  Nanopore sensors: from hybrid to abiotic systems. , 2012, Biosensors & bioelectronics.

[18]  Emily R. Billinge,et al.  Monitoring aptamer-protein interactions using tunable resistive pulse sensing. , 2014, Analytical chemistry.

[19]  L. Steinbock,et al.  Sensing DNA-coatings of microparticles using micropipettes. , 2009, Biosensors & bioelectronics.

[20]  Imre Mäger,et al.  Extracellular vesicles: biology and emerging therapeutic opportunities , 2013, Nature Reviews Drug Discovery.

[21]  Société de mathématiques appliquées et industrielles,et al.  ESAIM. Probability and statistics , 1997 .

[22]  Lu-Yi Yu,et al.  Polymer–Liposome Complexes with a Functional Hydrogen-Bond Cross-Linker for Preventing Protein Adsorption and Improving Tumor Accumulation , 2013 .

[23]  R. Horváth,et al.  Label-free optical monitoring of surface adhesion of extracellular vesicles by grating coupled interferometry , 2013 .

[24]  Lydia L. Sohn,et al.  An Artificial Nanopore for Molecular Sensing , 2003 .

[25]  G. Willmott,et al.  Size and charge characterisation of a submicrometre oil-in-water emulsion using resistive pulse sensing with tunable pores. , 2013, Journal of colloid and interface science.

[26]  Richard M Crooks,et al.  Simultaneous determination of the size and surface charge of individual nanoparticles using a carbon nanotube-based Coulter counter. , 2003, Analytical chemistry.

[27]  Geoff R. Willmott,et al.  Quantitative sizing of nano/microparticles with a tunable elastomeric pore sensor. , 2011, Analytical chemistry.

[28]  G. Willmott,et al.  Fast piezoelectric actuation of an elastomeric micropore , 2013 .

[29]  Shanshan Wu,et al.  Lithography-free formation of nanopores in plastic membranes using laser heating. , 2006, Nano letters.

[30]  Richard M Crooks,et al.  The resurgence of Coulter counting for analyzing nanoscale objects. , 2004, The Analyst.

[31]  T. Rades,et al.  Exploring the fate of liposomes in the intestine by dynamic in vitro lipolysis. , 2012, International journal of pharmaceutics.

[32]  Jin-Wook Yoo,et al.  Enzyme/pH dual sensitive polymeric nanoparticles for targeted drug delivery to the inflamed colon. , 2014, Colloids and surfaces. B, Biointerfaces.

[33]  L. Lagae,et al.  Measuring mass of nanoparticles and viruses in liquids with nanometer-scale pores. , 2014, Analytical chemistry.

[34]  Zuzanna S Siwy,et al.  Detecting single porphyrin molecules in a conically shaped synthetic nanopore. , 2005, Nano letters.

[35]  H. White,et al.  Pressure-Driven Nanoparticle Transport across Glass Membranes Containing a Conical-Shaped Nanopore , 2011 .

[36]  A. Aksimentiev,et al.  Modeling thermophoretic effects in solid-state nanopores , 2014, Journal of computational electronics.

[37]  Scott N. Dean,et al.  Chitinases Are Negative Regulators of Francisella novicida Biofilms , 2014, PloS one.

[38]  Z. Siwy,et al.  Particle deformation and concentration polarization in electroosmotic transport of hydrogels through pores. , 2013, ACS nano.

[39]  C. Metzner,et al.  Quantitative real-time single particle analysis of virions , 2014, Virology.

[40]  G R Willmott,et al.  Comment on 'Modeling the conductance and DNA blockade of solid-state nanopores'. , 2012, Nanotechnology.

[41]  G. Willmott,et al.  Magnetic microbead transport during resistive pulse sensing. , 2013, Biomicrofluidics.

[42]  Richard M Crooks,et al.  A carbon nanotube-based coulter nanoparticle counter. , 2004, Accounts of chemical research.

[43]  K. Ladell,et al.  Lipoprotein-apheresis reduces circulating microparticles in individuals with familial hypercholesterolemia[S] , 2014, Journal of Lipid Research.

[44]  M. Trau,et al.  Tuning Particle Velocity and Measurement Sensitivity by Changing Pore Sensor Dimensions , 2012 .

[45]  Long Luo,et al.  Resistive-pulse analysis of nanoparticles. , 2014, Annual review of analytical chemistry.

[46]  Wen-Jie Lan,et al.  Diffusional motion of a particle translocating through a nanopore. , 2012, ACS nano.

[47]  Mark Platt,et al.  Resistive pulse sensing of analyte-induced multicomponent rod aggregation using tunable pores. , 2012, Small.

[48]  M. Trau,et al.  Modeling Elastic Pore Sensors for Quantitative Single Particle Sizing. , 2012, The journal of physical chemistry. C, Nanomaterials and interfaces.

[49]  M. Krumrey,et al.  Towards traceable size determination of extracellular vesicles , 2014, Journal of extracellular vesicles.

[50]  Bo Zhang,et al.  Electrostatic-gated transport in chemically modified glass nanopore electrodes. , 2006, Journal of the American Chemical Society.

[51]  S. Saxena,et al.  Influence of microgel packing on raspberry-like heteroaggregate assembly. , 2015, Journal of colloid and interface science.

[52]  Matt Trau,et al.  A comparative study of submicron particle sizing platforms: accuracy, precision and resolution analysis of polydisperse particle size distributions. , 2013, Journal of colloid and interface science.

[53]  H. Ho,et al.  Detection of Panton-Valentine Leukocidin DNA from methicillin-resistant Staphylococcus aureus by resistive pulse sensing and loop-mediated isothermal amplification with gold nanoparticles. , 2013, Analytica chimica acta.

[54]  H. Ishitobi,et al.  Exosome-formed synthetic microRNA-143 is transferred to osteosarcoma cells and inhibits their migration. , 2014, Biochemical and biophysical research communications.

[55]  J. Lahann,et al.  Amphiphilic colloidal surfactants based on electrohydrodynamic co-jetting. , 2013, ACS applied materials & interfaces.

[56]  T G van Leeuwen,et al.  Optical and non‐optical methods for detection and characterization of microparticles and exosomes , 2010, Journal of thrombosis and haemostasis : JTH.

[57]  Philip Demokritou,et al.  High Resolution Characterization of Engineered Nanomaterial Dispersions in Complex Media Using Tunable Resistive Pulse Sensing Technology , 2014, ACS nano.

[58]  Lydia L. Sohn,et al.  Direct detection of antibody–antigen binding using an on-chip artificial pore , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Bo Zhang,et al.  Nanoparticle transport in conical-shaped nanopores. , 2011, Analytical chemistry.

[60]  M. Burns,et al.  Nanopore sequencing technology: nanopore preparations. , 2007, Trends in biotechnology.

[61]  G. Willmott,et al.  Nanoparticle ζ-potential measurements using tunable resistive pulse sensing with variable pressure. , 2014, Journal of colloid and interface science.

[62]  F. Kiessling,et al.  Drug targeting to tumors: principles, pitfalls and (pre-) clinical progress. , 2012, Journal of controlled release : official journal of the Controlled Release Society.

[63]  E. Uzgiris,et al.  Comparative measurements of size and polydispersity of several insect viruses. , 1978, Analytical biochemistry.

[64]  X. Banquy,et al.  Assessment of PEG on polymeric particles surface, a key step in drug carrier translation. , 2014, Journal of controlled release : official journal of the Controlled Release Society.

[65]  Kevin Ke,et al.  Submicrometer pore-based characterization and quantification of antibody-virus interactions. , 2006, Small.

[66]  C. Melief,et al.  B lymphocytes secrete antigen-presenting vesicles , 1996, The Journal of experimental medicine.

[67]  J. Hall.  Access resistance of a small circular pore , 1975, The Journal of general physiology.

[68]  S. Kong,et al.  Monitoring bacterial growth using tunable resistive pulse sensing with a pore-based technique , 2013, Applied Microbiology and Biotechnology.

[69]  Lynne T. Bemis,et al.  Standardization of sample collection, isolation and analysis methods in extracellular vesicle research , 2013, Journal of extracellular vesicles.

[70]  Jonathan R. McDaniel,et al.  Noncanonical Self-Assembly of Highly Asymmetric Genetically Encoded Polypeptide Amphiphiles into Cylindrical Micelles , 2014, Nano letters.

[71]  L. L. Yung,et al.  Rapid and label-free single-nucleotide discrimination via an integrative nanoparticle-nanopore approach. , 2012, ACS nano.

[72]  B. Pan,et al.  Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: Selective externalization of the receptor , 1983, Cell.

[73]  Matt Trau,et al.  Advances in Resistive Pulse Sensors: Devices bridging the void between molecular and microscopic detection. , 2011, Nano today.

[74]  P. Fürjes,et al.  Calibration-less sizing and quantitation of polymeric nanoparticles and viruses with quartz nanopipets. , 2014, Analytical chemistry.

[75]  I. Sargent,et al.  Particle size distribution of exosomes and microvesicles determined by transmission electron microscopy, flow cytometry, nanoparticle tracking analysis, and resistive pulse sensing , 2014, Journal of thrombosis and haemostasis : JTH.

[76]  Jadranka Travas-Sejdic,et al.  Detection of target-probe oligonucleotide hybridization using synthetic nanopore resistive pulse sensing. , 2013, Biosensors & bioelectronics.

[77]  G. Willmott,et al.  A variable pressure method for characterizing nanoparticle surface charge using pore sensors. , 2012, Analytical chemistry.

[78]  Andreas Bund,et al.  Effect of Surface Charge on the Resistive Pulse Waveshape during Particle Translocation through Glass Nanopores , 2014 .

[79]  Raymond M. Schiffelers,et al.  Possibilities and limitations of current technologies for quantification of biological extracellular vesicles and synthetic mimics , 2015, Journal of controlled release : official journal of the Controlled Release Society.

[80]  K. Healy.  Nanopore-based single-molecule DNA analysis. , 2007, Nanomedicine.

[81]  C. Ringhofer,et al.  Hierarchies of transport equations for nanopores , 2014 .

[82]  Jiwook Shim,et al.  Single molecule sensing by nanopores and nanopore devices. , 2010, The Analyst.

[83]  L. Ruff,et al.  Antigen-loaded pH-sensitive hydrogel microparticles are taken up by dendritic cells with no requirement for targeting antibodies. , 2013, Integrative biology : quantitative biosciences from nano to macro.

[84]  Gil U. Lee,et al.  Resistive pulse sensing of magnetic beads and supraparticle structures using tunable pores. , 2012, Biomicrofluidics.

[85]  R. Vogel,et al.  High resolution particle characterization to expedite development and regulatory acceptance of nanomedicines. , 2015, Current drug delivery.

[86]  Lesley Cheng,et al.  Characterization and deep sequencing analysis of exosomal and non-exosomal miRNA in human urine. , 2014, Kidney international.

[87]  R W DeBlois,et al.  Sizes and concentrations of several type C oncornaviruses and bacteriophage T2 by the resistive-pulse technique , 1977, Journal of virology.

[88]  Matt Trau,et al.  Analysis of exosome purification methods using a model liposome system and tunable-resistive pulse sensing , 2015, Scientific Reports.

[89]  S. Tóth,et al.  Critical role of extracellular vesicles in modulating the cellular effects of cytokines , 2014, Cellular and Molecular Life Sciences.

[90]  G. Willmott,et al.  Resistive pulse asymmetry for nanospheres passing through tunable submicron pores , 2011 .

[91]  Ronald W Davis,et al.  Label-free biosensing with functionalized nanopipette probes , 2009, Proceedings of the National Academy of Sciences.

[92]  Emily R. Billinge,et al.  Tunable resistive pulse sensing as a tool to monitor analyte induced particle aggregation , 2013 .

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

[94]  D. Branton,et al.  Characterization of nucleic acids by nanopore analysis. , 2002, Accounts of chemical research.

[95]  A Gel Filtration-Based Method for the Purification of Infectious Rotavirus Particles for Environmental Research Applications , 2013, Food and Environmental Virology.

[96]  A. Mitra,et al.  Role of antifeeding prophage (Afp) protein Afp16 in terminating the length of the Afp tailocin and stabilizing its sheath , 2013, Molecular microbiology.

[97]  R. Crooks,et al.  Comparison of nanoparticle size and electrophoretic mobility measurements using a carbon-nanotube-based coulter counter, dynamic light scattering, transmission electron microscopy, and phase analysis light scattering. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[98]  G. Willmott,et al.  Use of tunable nanopore blockade rates to investigate colloidal dispersions , 2010, Journal of physics. Condensed matter : an Institute of Physics journal.

[99]  C. R. Martin,et al.  Developing synthetic conical nanopores for biosensing applications. , 2007, Molecular bioSystems.

[100]  M. Lenz,et al.  Colloidal properties of nanoparticular biogenic selenium govern environmental fate and bioremediation effectiveness. , 2013, Environmental science & technology.

[101]  S. Brar,et al.  Measurement of nanoparticles by light-scattering techniques , 2011 .

[102]  M. Yeh,et al.  Clinical development of liposome-based drugs: formulation, characterization, and therapeutic efficacy , 2011, International journal of nanomedicine.

[103]  W. Kuo,et al.  Alternative Methods for Characterization of Extracellular Vesicles , 2012, Front. Physio..

[104]  J. Stap,et al.  Active caspase-3 is removed from cells by release of caspase-3-enriched vesicles. , 2013, Biochimica et biophysica acta.

[105]  R. Schiffelers,et al.  Toward routine detection of extracellular vesicles in clinical samples , 2014, International journal of laboratory hematology.

[106]  E. Oosterwijk,et al.  Specific targeting of tumor cells by lyophilisomes functionalized with antibodies. , 2014, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[107]  Graça Raposo,et al.  Extracellular vesicles: Exosomes, microvesicles, and friends , 2013, The Journal of cell biology.

[108]  G. Willmott,et al.  Actuation of Tunable Elastomeric Pores: Resistance Measurements and Finite Element Modelling , 2014 .

[109]  Long Luo,et al.  Controlling Nanoparticle Dynamics in Conical Nanopores , 2013 .

[110]  D. Deamer.  Nanopore analysis of nucleic acids bound to exonucleases and polymerases. , 2010, Annual review of biophysics.

[111]  Peixuan Guo,et al.  Solid-State and Biological Nanopore for Real-Time Sensing of Single Chemical and Sequencing of DNA. , 2013, Nano today.

[112]  M. Grinstaff,et al.  Microscopy and tunable resistive pulse sensing characterization of the swelling of pH-responsive, polymeric expansile nanoparticles. , 2013, Nanoscale.

[113]  Z. Siwy,et al.  Charged Particles Modulate Local Ionic Concentrations and Cause Formation of Positive Peaks in Resistive-Pulse-Based Detection , 2014 .

[114]  G. Willmott,et al.  MODELLING OF RESISTIVE PULSE SENSING: FLEXIBLE METHODS FOR SUBMICRON PARTICLES , 2014, The ANZIAM Journal.

[115]  G. B. Petersen,et al.  Dynamically resizable nanometre-scale apertures for molecular sensing , 2007 .

[116]  C. P. Bean,et al.  Electrokinetic measurements with submicron particles and pores by the resistive pulse technique , 1977 .

[117]  C. Harding,et al.  Endocytosis and intracellular processing of transferrin and colloidal gold-transferrin in rat reticulocytes: demonstration of a pathway for receptor shedding. , 1984, European journal of cell biology.

[118]  K. Takagaki,et al.  Human adipose tissue-derived mesenchymal stem cells secrete functional neprilysin-bound exosomes , 2013, Scientific Reports.

[119]  Egbert Oosterwijk,et al.  Lyophilisomes as a new generation of drug delivery capsules. , 2012, International journal of pharmaceutics.

[120]  A. K. Yang,et al.  Quantitative detection of eryptosis in human erythrocytes using tunable resistive pulse sensing and annexin-V-beads. , 2015, The Analyst.

[121]  J. Reiner,et al.  Nanoscopic porous sensors. , 2008, Annual review of analytical chemistry.

[122]  Alidad Amirfazli,et al.  Magnetic nanoparticles hit the target , 2007, Nature Nanotechnology.

[123]  Liping Pang,et al.  Biotin- and glycoprotein-coated microspheres: potential surrogates for studying filtration of cryptosporidium parvum in porous media. , 2012, Environmental science & technology.

[124]  R. Renneberg,et al.  Bioinspired protein microparticles fabrication by peptide mediated disulfide interchange , 2014 .

[125]  M. Krumrey,et al.  Innovation in detection of microparticles and exosomes , 2013, Journal of thrombosis and haemostasis : JTH.

[126]  A. Morrison,et al.  Solid-state nanopore technologies for nanopore-based DNA analysis. , 2007, Nanomedicine.

[127]  V. Torchilin,et al.  Micellar Nanocarriers: Pharmaceutical Perspectives , 2006, Pharmaceutical Research.

[128]  E. Waters,et al.  Roles of proteins, polysaccharides, and phenolics in haze formation in white wine via reconstitution experiments. , 2012, Journal of agricultural and food chemistry.

[129]  T. V. van Leeuwen,et al.  Reproducible extracellular vesicle size and concentration determination with tunable resistive pulse sensing , 2014, Journal of extracellular vesicles.

[130]  D. Branton,et al.  The potential and challenges of nanopore sequencing , 2008, Nature Biotechnology.

[131]  S. Rome,et al.  Endometrial Exosomes/Microvesicles in the Uterine Microenvironment: A New Paradigm for Embryo-Endometrial Cross Talk at Implantation , 2013, PloS one.

[132]  G. Willmott,et al.  Reversible mechanical actuation of elastomeric nanopores , 2008, Nanotechnology.

[133]  M. Mayer,et al.  Noise and bandwidth of current recordings from submicrometer pores and nanopores. , 2008, ACS nano.

[134]  Mark E. Davis,et al.  Nanoparticle therapeutics: an emerging treatment modality for cancer , 2008, Nature Reviews Drug Discovery.

[135]  Martin A. M. Gijs,et al.  Magnetic bead handling on-chip: new opportunities for analytical applications , 2004 .

[136]  Kevin Ke,et al.  Ultrafast laser fabrication of submicrometer pores in borosilicate glass. , 2008, Optics letters.

[137]  A. Koster,et al.  Quantification of nanosized extracellular membrane vesicles with scanning ion occlusion sensing. , 2013, Nanomedicine.

[138]  A. Biance,et al.  Osmotic flow through fully permeable nanochannels. , 2014, Physical Review Letters.

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

[140]  H. White,et al.  Resistive-pulse detection of multilamellar liposomes. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[141]  P. Renaud,et al.  Transport phenomena in nanofluidics , 2008 .

[142]  C. R. Martin,et al.  Electrophoretic capture and detection of nanoparticles at the opening of a membrane pore using scanning electrochemical microscopy. , 2004, Analytical chemistry.

[143]  R. Bashir,et al.  Nanopore sensors for nucleic acid analysis. , 2011, Nature nanotechnology.

[144]  L. Steinbock,et al.  Modeling of colloidal transport in capillaries , 2009 .

[145]  Molly M. Stevens,et al.  Emerging techniques for submicrometer particle sizing applied to Stöber silica. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[146]  G. Babcock,et al.  Protocol Standardization Reveals MV Correlation to Healthy Donor BMI , 2014, Journal of Circulating Biomarkers.

[147]  Mark W Grinstaff,et al.  Tunable pores for measuring concentrations of synthetic and biological nanoparticle dispersions. , 2012, Biosensors & bioelectronics.

[148]  M. Nilsson,et al.  Digital quantification of rolling circle amplified single DNA molecules in a resistive pulse sensing nanopore. , 2015, Biosensors & bioelectronics.

[149]  C. P. Bean,et al.  Counting and Sizing of Submicron Particles by the Resistive Pulse Technique , 1970 .

[150]  Daniela Traini,et al.  Magnetised Thermo Responsive Lipid Vehicles for Targeted and Controlled Lung Drug Delivery , 2012, Pharmaceutical Research.

[151]  Physicochemical characterization techniques for solid lipid nanoparticles: principles and limitations , 2014, Drug development and industrial pharmacy.