A survey of the 2001 to 2005 quartz crystal microbalance biosensor literature: applications of acoustic physics to the analysis of biomolecular interactions

The widespread exploitation of biosensors in the analysis of molecular recognition has its origins in the mid‐1990s following the release of commercial systems based on surface plasmon resonance (SPR). More recently, platforms based on piezoelectric acoustic sensors (principally ‘bulk acoustic wave’ (BAW), ‘thickness shear mode’ (TSM) sensors or ‘quartz crystal microbalances’ (QCM)), have been released that are driving the publication of a large number of papers analysing binding specificities, affinities, kinetics and conformational changes associated with a molecular recognition event. This article highlights salient theoretical and practical aspects of the technologies that underpin acoustic analysis, then reviews exemplary papers in key application areas involving small molecular weight ligands, carbohydrates, proteins, nucleic acids, viruses, bacteria, cells and lipidic and polymeric interfaces. Key differentiators between optical and acoustic sensing modalities are also reviewed. Copyright © 2007 John Wiley & Sons, Ltd.

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[38]  Jianwen Zhao,et al.  A TSM immunosensor for detection of M. tuberculosis with a new membrane material , 2002 .

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[43]  Y. Okahata,et al.  Direct monitoring of DNA cleavages catalyzed by an ATP-dependent deoxyribonuclease on a 27 MHz quartz-crystal microbalance. , 2002, Chemical communications.

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[45]  Yonggui Dong,et al.  Detection of human lung carcinoma cell using quartz crystal microbalance amplified by enlarging Au nanoparticles in vitro , 2002 .

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[48]  Á. Ríos,et al.  Determination of free and total sulphur dioxide in wine by use of an amalgamated piezoelectric sensor , 2005 .

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[51]  E. Lojou,et al.  Buildup of polyelectrolyte-protein multilayer assemblies on gold electrodes. Role of the hydrophobic effect. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[52]  Kazukiyo Kobayashi,et al.  Peptides binding to a Gb3 mimic selected from a phage library. , 2004, Biochimica et biophysica acta.

[53]  Fredrik Höök,et al.  Characterization of DNA immobilization and subsequent hybridization on a 2D arrangement of streptavidin on a biotin-modified lipid bilayer supported on SiO2. , 2003, Analytical chemistry.

[54]  Jing-Min Hwang,et al.  Development of an immunosensor for human ferritin, a nonspecific tumor marker, based on a quartz crystal microbalance , 2002 .

[55]  Piezoelectric Flow Injection Analysis Biosensor for the Detection of Salmonella Typhimurium , 2002 .

[56]  Tetsuya Haruyama,et al.  Micro- and nanobiotechnology for biosensing cellular responses. , 2003, Advanced drug delivery reviews.

[57]  Abdolreza Mirmohseni,et al.  Construction of a sensor for determination of ammonia and aliphatic amines using polyvinylpyrrolidone coated quartz crystal microbalance , 2003 .

[58]  Sara Tombelli,et al.  Piezoelectric biosensors: strategies for coupling nucleic acids to piezoelectric devices. , 2005, Methods.

[59]  Guoquan Liu,et al.  Real time kinetic analysis of the interaction between immunoglobulin G and histidine using quartz crystal microbalance biosensor in solution. , 2003, Biosensors & bioelectronics.

[60]  G. Lonergan,et al.  Application of a quartz crystal microbalance to evaluate biodegradability of starch by Bacillus subtilis , 2004, Biotechnology Letters.

[61]  S. O’Shea,et al.  Antibody/antigen affinity behavior in liquid environment with electrical impedance analysis of quartz crystal microbalances. , 2002, Biophysical chemistry.

[62]  I.D. Avramov,et al.  A 0-phase circuit for QCM-based measurements in highly viscous liquid environments , 2005, IEEE Sensors Journal.

[63]  Marc C Nicklaus,et al.  Small nonphosphorylated Grb2–SH2 domain antagonists evaluated by surface plasmon resonance technology , 2005, Biopolymers.

[64]  K. Tappura,et al.  Interaction between Cellulose and Xylan An Atomic Force Microscope and Quartz Crystal Microbalance Study , 2004 .

[65]  P. Laugier,et al.  Monitoring cell adhesion processes on bioactive polymers with the quartz crystal resonator technique. , 2005, Biomaterials.

[66]  Marcus Textor,et al.  A comparative study of protein adsorption on titanium oxide surfaces using in situ ellipsometry, optical waveguide lightmode spectroscopy, and quartz crystal microbalance/dissipation , 2002 .

[67]  J. Anzai,et al.  Preparation of Multilayer Thin Films Containing Avidin through Sugar−Lectin Interactions and Their Binding Properties , 2002 .

[68]  L. Barnes,et al.  A rapid, non‐destructive method for the determination of Staphylococcus epidermidis adhesion to surfaces using quartz crystal resonant sensor technology , 2001, Letters in applied microbiology.

[69]  G. Hayward,et al.  Mass response of the thickness-shear mode acoustic wave sensor in liquids as a central misleading dogma , 1997, Proceedings of International Frequency Control Symposium.

[70]  H. Galla,et al.  Quantification of the Raf‐C1 Interaction With Solid‐Supported Bilayers , 2002, Chembiochem : a European journal of chemical biology.

[71]  C. Steinem,et al.  Adhesion kinetics of functionalized vesicles and mammalian cells: A comparative study , 2003 .

[72]  S. Wakida,et al.  Conventional diagnosis of Treponema pallidum in serum using latex piezoelectric immunoassay , 2001 .

[73]  R. Larsson,et al.  Characterization of heparin surfaces using photoelectron spectroscopy and quartz crystal microbalance. , 2003, Biomaterials.

[74]  A. Granéli,et al.  DNA-based formation of a supported, three-dimensional lipid vesicle matrix probed by QCM-D and SPR. , 2004, Chemphyschem : a European journal of chemical physics and physical chemistry.

[75]  Itamar Willner,et al.  Amplified detection of telomerase activity using electrochemical and quartz crystal microbalance measurements. , 2004, Biosensors & bioelectronics.

[76]  C. Frank,et al.  Adsorption of disulfide-modified polyacrylamides to gold and silver surfaces as cushions for polymer-supported lipid bilayers , 2003 .

[77]  Yoichi Takakusagi,et al.  Camptothecin binds to a synthetic peptide identified by a T7 phage display screen. , 2005, Bioorganic & medicinal chemistry letters.

[78]  Hirotaka Kaneda,et al.  Development of Beer Taste Sensor Using a Lipid-Coated Quartz-Crystal Microbalance , 2005 .

[79]  D. Shangguan,et al.  QCM-FIA with PGMA coating for dynamic interaction study of heparin and antithrombin III. , 2005, Biosensors & bioelectronics.

[80]  P. Hauptmann,et al.  Disposable HSA QCM-immunosensor for practical measurement in liquid , 2001 .

[81]  B. Kasemo,et al.  Missing mass effect in biosensor's QCM applications. , 2002, Biosensors & bioelectronics.

[82]  H. Chan,et al.  Chiral discrimination of enantiomers with a self-assembled monolayer of functionalized β-cyclodextrins on Au surfaces , 2002 .

[83]  T. Livache,et al.  Reversible oligonucleotide immobilisation based on biotinylated polypyrrole film , 2001 .

[84]  J. Schwarzbauer,et al.  Self-assembled monolayers of alpha,omega-diphosphonic acids on Ti enable complete or spatially controlled surface derivatization. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[85]  G. Lim,et al.  Influence of liquid medium and surface morphology on the response of QCM during immobilization and hybridization of short oligonucleotides. , 2004, Biosensors & bioelectronics.

[86]  K. Pavey,et al.  Quartz crystal resonant sensor (QCRS) model for label-free, small molecules—receptor studies , 2001 .

[87]  Tzong-Zeng Wu,et al.  Piezoelectric immunochip for the detection of dengue fever in viremia phase. , 2005, Biosensors & bioelectronics.

[88]  S. Hattori,et al.  Keratinocyte apoptosis on type I collagen gel caused by lack of laminin 5/10/11 deposition and Akt signaling. , 2002, Experimental cell research.

[89]  N. C. Fawcett,et al.  Determination of chloroplast DNA in a cultured soybean line using a QCM biosensor , 2004, IEEE Sensors Journal.

[90]  Liqun Huang,et al.  Detection of two orchid viruses using quartz crystal microbalance-based DNA biosensors. , 2002, Phytopathology.

[91]  Shawn D. Carrigan,et al.  Real-time QCM-D immunoassay through oriented antibody immobilization using cross-linked hydrogel biointerfaces. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[92]  Hidenobu Aizawa,et al.  Rapid detection of fibrinogen and fibrin degradation products using a smart QCM-sensor , 2004 .

[93]  Stephanus Buettgenbach,et al.  Monolithic fabrication of wireless miniaturized quartz crystal microbalance (QCM-R) arrays and their application for biochemical sensors , 2003 .

[94]  G. Shen,et al.  A Novel Piezoelectric Biosensor for the Detection of Phytohormone β-Indole Acetic Acid , 2002, Analytical sciences : the international journal of the Japan Society for Analytical Chemistry.

[95]  George G. Guilbault,et al.  Development of a quartz crystal microbalance (QCM) immunosensor for the detection of Listeria monocytogenes , 2001 .

[96]  D. Mills,et al.  Comparison of selective attachment and growth of smooth muscle cells on gelatin- and fibronectin-coated micropatterns. , 2005, Journal of nanoscience and nanotechnology.

[97]  Matthew A Cooper,et al.  Advances in membrane receptor screening and analysis , 2004, Journal of molecular recognition : JMR.

[98]  Xiaodi Su,et al.  Serological determination of Helicobacter pylori infection using sandwiched and enzymatically amplified piezoelectric biosensor , 2001 .

[99]  B. Chin,et al.  Specific and selective biosensor for Salmonella and its detection in the environment. , 2003, Journal of microbiological methods.

[100]  Tao Liu,et al.  Particle size effect of the DNA sensor amplified with gold nanoparticles , 2002 .

[101]  Mengsu Yang,et al.  Determination of mode of interactions between novel drugs and calf thymus DNA by using quartz crystal resonator , 2002 .

[102]  V. Prachayasittikul,et al.  Interaction analysis of chimeric metal-binding green fluorescent protein and artificial solid-supported lipid membrane by quartz crystal microbalance and atomic force microscopy. , 2005, Biochemical and biophysical research communications.

[103]  J. Justin Gooding,et al.  Kinetics of irreversible adsorption with diffusion: Application to biomolecule immobilization , 2002 .

[104]  M. Hepel Ion channeling phenomena and Tl-upd induced film dynamics in model biomembranes studied with EQCN and QCI techniques , 2001 .

[105]  Hideo Tanaka,et al.  Conventional diagnosis of C-reactive protein in serum using latex piezoelectric immunoassay , 2001 .

[106]  Jean-Michel Kauffmann,et al.  Biosensors in Drug Discovery and Drug Analysis , 2005 .

[107]  K. Koumoto,et al.  Investigation of Apatite Deposition onto Charged Surfaces in Aqueous Solutions Using a Quartz-Crystal Microbalance , 2003 .

[108]  Bonnie J. Tyler,et al.  Comparison of the Spreeta® surface plasmon resonance sensor and a quartz crystal microbalance for detection of Escherichia coli heat-labile enterotoxin , 2001 .

[109]  M. Serpe,et al.  Doxorubicin uptake and release from microgel thin films. , 2005, Biomacromolecules.

[110]  S. Yao,et al.  Study of bovine serum albumin adsorption onto a silicon dioxide surface using a ring-electrode piezoelectric sensor , 2001 .

[111]  Tse-Chuan Chou,et al.  Determination of albumin concentration by MIP-QCM sensor. , 2004, Biosensors & bioelectronics.

[112]  S. Yao,et al.  Immunosensor for the differentiation and detection of Salmonella species based on a quartz crystal microbalance. , 2002, Biosensors & bioelectronics.

[113]  Thierry Livache,et al.  Electronically conductive polymer grafted with oligonucleotides as electrosensors of DNA: Preliminary study of real time monitoring by in situ techniques , 2001 .

[114]  G McHale,et al.  Molecular-imprinted, polymer-coated quartz crystal microbalances for the detection of terpenes. , 2001, Analytical chemistry.

[115]  C. Domenici,et al.  An integrated approach for the design and synthesis of oligonucleotide probes and their interfacing to a QCM-based RNA biosensor. , 2005, Biosensors & bioelectronics.

[116]  Y. Okahata,et al.  In Vitro Selection of N‐Peptide‐Binding RNA on a Quartz‐Crystal Microbalance to Study a Sequence‐Specific Interaction between the Peptide and Loop RNA , 2003, Chembiochem : a European journal of chemical biology.

[117]  F. Takahashi‐Yanaga,et al.  Cardiac troponin T mutation R141W found in dilated cardiomyopathy stabilizes the troponin T-tropomyosin interaction and causes a Ca2+ desensitization. , 2003, Journal of molecular and cellular cardiology.

[118]  Long Jiang,et al.  Surface modification of nanogold particles in DNA detection with quartz crystal microbalance , 2003 .

[119]  Fernanda F. Rossetti,et al.  Investigating the properties of supported vesicular layers on titanium dioxide by quartz crystal microbalance with dissipation measurements. , 2005, The Journal of chemical physics.

[120]  D. Tai,et al.  Development of immunochips for the detection of dengue viral antigens , 2003 .

[121]  K. Oshima,et al.  Quartz crystal microbalance assay for determination of plasma vitellogenin , 2005 .

[122]  R. Yu,et al.  A reusable piezo-immunosensor with amplified sensitivity for ceruloplasmin based on plasma-polymerized film. , 2004, Talanta.

[123]  Hirotaka Kaneda,et al.  Adsorption and Desorption of Beer and Coffee on a Lipid Membrane as Related to Sensory Bitterness , 2003 .

[124]  E. Lojou,et al.  Quartz crystal microbalance and voltammetry monitoring for layer-by-layer assembly of cytochrome c3 and poly(ester sulfonic acid) films on gold and silver electrodes , 2003 .

[125]  R. Neubert,et al.  Sensing specific adhesion of liposomal and micellar systems with attached carbohydrate recognition structures at lectin surfaces. , 2002, Journal of colloid and interface science.

[126]  J. Vörös,et al.  About the role of water in surface-grafted poly(ethylene glycol) layers. , 2004, Langmuir.

[127]  Wolfgang Knoll,et al.  Detection of point mutation and insertion mutations in DNA using a quartz crystal microbalance and MutS, a mismatch binding protein. , 2004, Analytical chemistry.

[128]  D. Pierce,et al.  Field screening of waterborne petroleum hydrocarbons by thickness shear-mode resonator measurements. , 2004, Environmental science & technology.

[129]  Y. Okahata,et al.  In vitro selection and evaluation of RNA aptamers that recognize arginine-rich-motif model peptide on a quartz-crystal microbalance. , 2002, Chemical communications.

[130]  Rory Stine,et al.  Comparison of glycosphingolipids and antibodies as receptor molecules for ricin detection. , 2005, Analytical chemistry.

[131]  Bo Nilsson,et al.  C3 Adsorbed to a Polymer Surface Can Form an Initiating Alternative Pathway Convertase1 , 2002, The Journal of Immunology.

[132]  Subrayal M Reddy,et al.  Determination of 4-aminophenol using the quartz crystal microbalance sensor. , 2002, The Analyst.

[133]  Fredrik Höök,et al.  Formation of Supported Lipid Bilayer Membranes on SiO2 from Proteoliposomes Containing Transmembrane Proteins , 2003 .

[134]  F. Yin,et al.  Human serum albumin–octadecylamine Langmuir–Blodgett film formed by spreading human serum albumin solution directly on subphase's interface covered with a layer of octadecylamine , 2005 .

[135]  P. Ihalainen,et al.  Immobilization of streptavidin onto biotin-functionalized Langmuir–Schaefer binary monolayers chemisorbed on gold , 2004 .

[136]  Z. Mo,et al.  Highly reproducible hybridization assay of zeptomole DNA based on adsorption of nanoparticle-bioconjugate. , 2005, The Analyst.

[137]  M. Gomes,et al.  The quantification of sodium in mineral waters using a quartz crystal microbalance. , 2003, Talanta.

[138]  G. Borghs,et al.  Simultaneous atomic force microscope and quartz crystal microbalance measurements: Investigation of human plasma fibrinogen adsorption , 2002 .

[139]  F. Höök,et al.  Bivalent-ion-mediated vesicle adsorption and controlled supported phospholipid bilayer formation on molecular phosphate and sulfate layers on gold , 2002 .

[140]  Wanzhi. Wei,et al.  Monitoring, and estimation of kinetic data, by piezoelectric impedance analysis, of the binding of the anticancer drug mitoxantrone to surface-immobilized DNA , 2002, Analytical and bioanalytical chemistry.

[141]  Jianrong Chen,et al.  SELF-ASSEMBLED MONOLAYER BASED QUARTZ CRYSTAL BIOSENSORS FOR THE DETECTION OF ENDOTOXINS , 2002 .

[142]  B. Jakoby,et al.  Novel analog readout electronics for microacoustic thickness shear-mode sensors , 2005, IEEE Sensors Journal.

[143]  A. Mirmohseni,et al.  Application of the quartz crystal microbalance for determination of phenol in solution , 2004 .

[144]  Y. Okahata,et al.  Design and characterization of asparagine- and lysine-containing alanine-based helical peptides that bind selectively to A.T base pairs of oligonucleotides immobilized on a 27 mhz quartz crystal microbalance. , 2001, Biochemistry.

[145]  I. Park,et al.  Development of a direct-binding chloramphenicol sensor based on thiol or sulfide mediated self-assembled antibody monolayers. , 2004, Biosensors & bioelectronics.

[146]  Analytical Applications of QCM-based Nucleic Acid Biosensors , 2006 .

[147]  P. Skládal,et al.  Piezoelectric Immunosensor for Francisella tularensis Detection Using Immunoglobulin M in a Limiting Dilution , 2005 .

[148]  T. Hianik,et al.  Properties of glucose biosensors based on dendrimer layers. Effect of enzyme immobilization , 2002, Analytical and bioanalytical chemistry.

[149]  M. Mascini,et al.  Aptamer-based biosensors for the detection of HIV-1 Tat protein. , 2005, Bioelectrochemistry.

[150]  M. Raje,et al.  Sandwich microgravimetric immunoassay: sensitive and specific detection of low molecular weight analytes using piezoelectric quartz crystal , 2002, Biotechnology Letters.

[151]  T. Osaka,et al.  Chiral discrimination between thalidomide enantiomers using a solid surface with two-dimensional chirality. , 2004, Chirality.

[152]  M. Thompson,et al.  Kinetic characterization of TAR RNA-Tat peptide and neomycin interactions by acoustic wave biosensor. , 2003, Biophysical chemistry.

[153]  I. Maruyama,et al.  Circulating level of α2-macroglobulin–β2-microglobulin complex in hemodialysis patients , 2003 .

[154]  Xiao-li Su,et al.  SURFACE PLASMON RESONANCE AND QUARTZ CRYSTAL MICROBALANCE IMMUNOSENSORS FOR DETECTION OF ESCHERICHIA COLI O157:H7 , 2005 .

[155]  L. Wågberg,et al.  Swelling of model films of cellulose having different charge densities and comparison to the swelling behavior of corresponding fibers , 2003 .

[156]  D. Vautier,et al.  Layer by layer self-assembled polyelectrolyte multilayers with embedded phospholipid vesicles. , 2004, Langmuir : the ACS journal of surfaces and colloids.

[157]  Y. Ando,et al.  Role of VLDL/chylomicron in amyloid formation in familial amyloidotic polyneuropathy. , 2003, Biochemical and biophysical research communications.

[158]  Wolfgang Knoll,et al.  Enzyme immobilization on poly(ethylene-co-acrylic acid) films studied by quartz crystal microbalance with dissipation monitoring. , 2005, Journal of colloid and interface science.

[159]  Jan Přibyl,et al.  Quartz crystal biosensor for detection of sugars and glycated hemoglobin , 2005 .

[160]  C Nicolini,et al.  Cholesterol biosensors prepared by layer-by-layer technique. , 2001, Biosensors & bioelectronics.

[161]  A. Bhunia,et al.  Analysis of environmental Escherichia coli isolates for virulence genes using the TaqMan® PCR system , 2003, Journal of applied microbiology.

[162]  Xiaodi Su,et al.  Piezoelectric quartz crystal based veterinary diagnosis for Salmonella enteritidis infection in chicken and egg , 2001 .

[163]  Y. Okahata,et al.  Direct monitoring kinetic studies of DNA polymerase reactions on a DNA-immobilized quartz-crystal microbalance. , 2001, Chemistry.

[164]  Yukari Sato,et al.  Adsorption Properties and Activities of Lipase on a Gold Substrate Modified by Self-assembled Monolayers , 2001, Bioscience, biotechnology, and biochemistry.

[165]  J. R. Grigera,et al.  The role of hydration on the mechanism of allosteric regulation: in situ measurements of the oxygen-linked kinetics of water binding to hemoglobin. , 2003, Biophysical journal.

[166]  S. Yao,et al.  A sulpha-drug sensitive sensor based on ion-pair complex modified PQC resonator. , 2002, Talanta.

[167]  T. Wärnheim,et al.  Adsorption of liposomes and emulsions studied with a quartz crystal microbalance. , 2001, Advances in colloid and interface science.

[168]  Subrayal M. Reddy,et al.  Quartz crystal microbalance determination of organophosphorus and carbamate pesticides , 2002 .

[169]  Hirotaka Kaneda,et al.  Measuring Astringency of Beverages Using a Quartz-Crystal Microbalance , 2003 .

[170]  Rebecca L Rich,et al.  Higher-throughput, label-free, real-time molecular interaction analysis. , 2007, Analytical biochemistry.

[171]  T. A. Taton,et al.  Metal nanoparticles as labels for heterogeneous, chip-based DNA detection , 2003, Nanotechnology.

[172]  Sara Tombelli,et al.  Direct immobilisation of DNA probes for the development of affinity biosensors. , 2005, Bioelectrochemistry.

[173]  Matthew A Cooper,et al.  Biosensor profiling of molecular interactions in pharmacology. , 2003, Current opinion in pharmacology.

[174]  S. Kuroki,et al.  Piezo Electric Sensor for Endocrine-Disrupting Chemicals Using Receptor–co-factor Interaction , 2003, Analytical sciences : the international journal of the Japan Society for Analytical Chemistry.

[175]  B. Kasemo,et al.  Variations in coupled water, viscoelastic properties, and film thickness of a Mefp-1 protein film during adsorption and cross-linking: a quartz crystal microbalance with dissipation monitoring, ellipsometry, and surface plasmon resonance study. , 2001, Analytical chemistry.

[176]  Franz L. Dickert,et al.  Mass-sensitive detection of cells, viruses and enzymes with artificial receptors , 2003 .

[177]  Virapong Prachayasittikul,et al.  Molecularly imprinted polymer thin films on quartz crystal microbalance using a surface bound photo-radical initiator , 2005 .

[178]  C. Percival,et al.  Molecular imprinted polymer coated QCM for the detection of nandrolone. , 2002, The Analyst.

[179]  G. Bidan,et al.  Investigation by QCM of the Specific and Nonspecific Avidin Interaction onto a Biotinylated Polypyrrole Film , 2004 .

[180]  Miloslav Pravda,et al.  IMMUNOCHEMICAL DETECTION OF POLYCYCLIC AROMATIC HYDROCARBONS (PAHs) , 2002 .

[181]  J. Muthuswamy,et al.  Acoustic biosensor for monitoring antibody immobilization and neurotransmitter GABA in real-time , 2004 .

[182]  J. Najarian,et al.  An immunospecific microbalance. , 1972, Journal of biomedical materials research.

[183]  S. Kurosawa,et al.  Adsorption of anti-C-Reactive Protein Monoclonal Antibody and Its F(ab')2 fragment on Plasma-Polymerized Styrene, Allylamine and Acrylic Acid Coated with Quartz Crystal Microbalance. , 2002 .

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