Nanobiohybrid Material‐Based Bioelectronic Devices

Biomolecules, especially proteins and nucleic acids, have been widely studied to develop biochips for various applications in scientific fields ranging from bioelectronics to stem cell research. However, restrictions exist due to the inherent characteristics of biomolecules, such as instability and the constraint of granting the functionality to the biochip. Introduction of functional nanomaterials, recently being researched and developed, to biomolecules have been widely researched to develop the nanobiohybrid materials because such materials have the potential to enhance and extend the function of biomolecules on a biochip. The potential for applying nanobiohybrid materials is especially high in the field of bioelectronics. Research in bioelectronics is aimed at realizing electronic functions using the inherent properties of biomolecules. To achieve this, various biomolecules possessing unique properties have been combined with novel nanomaterials to develop bioelectronic devices such as highly sensitive electrochemical‐based bioelectronic sensing platforms, logic gates, and biocomputing systems. In this review, recently reported bioelectronic devices based on nanobiohybrid materials are discussed. The authors believe that this review will suggest innovative and creative directions to develop the next generation of multifunctional bioelectronic devices.

[1]  Chia‐Kuang Tsung,et al.  Integration of Biomolecules with Metal-Organic Frameworks. , 2017, Small.

[2]  Hong Chen,et al.  A supramolecular bioactive surface for specific binding of protein. , 2017, Colloids and surfaces. B, Biointerfaces.

[3]  I. Willner,et al.  Biomaterials integrated with electronic elements: en route to bioelectronics. , 2001, Trends in biotechnology.

[4]  Shaojun Dong,et al.  GOx@ZIF-8(NiPd) Nanoflower: An Artificial Enzyme System for Tandem Catalysis. , 2017, Angewandte Chemie.

[5]  Jeong-Woo Choi,et al.  Nanostructured surfaces for analysis of anticancer drug and cell diagnosis based on electrochemical and SERS tools , 2018, Nano Convergence.

[6]  Wanqin Jin,et al.  Electrochemical mercury biosensors based on advanced nanomaterials , 2019, Journal of Materials Chemistry B.

[7]  Hongbo Wang,et al.  Significance of Nanomaterials in Wearables: A Review on Wearable Actuators and Sensors , 2018, Advanced materials.

[8]  Eric C Lai,et al.  Diverse roles for RNA in gene regulation , 2005, Genome Biology.

[9]  Nurunnabi,et al.  Bioapplication of graphene oxide derivatives: drug/gene delivery, imaging, polymeric modification, toxicology, therapeutics and challenges , 2015 .

[10]  Audrey Sassolas,et al.  Immobilization strategies to develop enzymatic biosensors. , 2012, Biotechnology advances.

[11]  Q. Xie,et al.  Bio-/Nano-Immobilization Platform Based on Bio-Inspired Fibrin-Bone@Polydopamine-Shell Adhesive Composites for Biosensing. , 2019, ACS applied materials & interfaces.

[12]  Nam-Joon Cho,et al.  Graphene‐Functionalized Natural Microcapsules: Modular Building Blocks for Ultrahigh Sensitivity Bioelectronic Platforms , 2016 .

[13]  Donghyun Lee,et al.  Electrochemical Biosensor Composed of Silver Ion-Mediated dsDNA on Au-Encapsulated Bi2 Se3 Nanoparticles for the Detection of H2 O2 Released from Breast Cancer Cells. , 2018, Small.

[14]  Navnath S. Gavande,et al.  DNA repair targeted therapy: The past or future of cancer treatment? , 2016, Pharmacology & therapeutics.

[15]  Pedro J. J. Alvarez,et al.  Nanomaterials in the construction industry: a review of their applications and environmental health and safety considerations. , 2010, ACS nano.

[16]  R. Weiss,et al.  A universal RNAi-based logic evaluator that operates in mammalian cells , 2007, Nature Biotechnology.

[17]  Peixuan Guo,et al.  Construction of RNA-Quantum Dot Chimera for Nanoscale Resistive Biomemory Application. , 2015, ACS nano.

[18]  H. Pei,et al.  Bubble-Mediated Ultrasensitive Multiplex Detection of Metal Ions in Three-Dimensional DNA Nanostructure-Encoded Microchannels. , 2017, ACS applied materials & interfaces.

[19]  S. Ansari,et al.  Potential applications of enzymes immobilized on/in nano materials: A review. , 2012, Biotechnology advances.

[20]  Dmitry Pankratov,et al.  Tear Based Bioelectronics , 2016 .

[21]  Li Wang,et al.  Graphene-based aptasensors: from molecule-interface interactions to sensor design and biomedical diagnostics. , 2018, The Analyst.

[22]  R. Langer,et al.  Biohybrid Design Gets Personal: New Materials for Patient‐Specific Therapy , 2019, Advanced materials.

[23]  Chulhwan Park,et al.  Fabrication of Electrochemical-Based Bioelectronic Device and Biosensor Composed of Biomaterial-Nanomaterial Hybrid , 2018, Advances in experimental medicine and biology.

[24]  Y. Ying,et al.  Recent advances in fabrication strategies and protein preservation application of protein-nanomaterial hybrids: Integration and synergy , 2019, TrAC Trends in Analytical Chemistry.

[25]  Vamsi K Yadavalli,et al.  Flexible Biosensors for the Impedimetric Detection of Protein Targets Using Silk-Conductive Polymer Biocomposites. , 2019, ACS sensors.

[26]  Oh Seok Kwon,et al.  Large‐Scale Graphene Micropattern Nano‐biohybrids: High‐Performance Transducers for FET‐Type Flexible Fluidic HIV Immunoassays , 2013, Advanced materials.

[27]  Yujie Feng,et al.  Nanomaterials for facilitating microbial extracellular electron transfer: Recent progress and challenges. , 2018, Bioelectrochemistry.

[28]  Yong-Ho Chung,et al.  Electrochemical Bioelectronic Device Consisting of Metalloprotein for Analog Decision Making , 2015, Scientific reports.

[29]  J. Lieberman Unveiling the RNA World , 2018, The New England journal of medicine.

[30]  Qiang Wang,et al.  A universal platform for multiple logic operations based on self-assembled a DNA tripod and graphene oxide , 2019, Chemical Engineering Journal.

[31]  N. C. Veitch,et al.  Horseradish peroxidase: a modern view of a classic enzyme. , 2004, Phytochemistry.

[32]  Eon Soo Lee,et al.  Detection of cancer antigens (CA-125) using gold nano particles on interdigitated electrode-based microfluidic biosensor , 2019, Nano Convergence.

[33]  Michael Holzinger,et al.  A synthetic redox biofilm made from metalloprotein-prion domain chimera nanowires. , 2017, Nature chemistry.

[34]  Rupesh K. Mishra,et al.  Wearable Bioelectronics: Enzyme-Based Body-Worn Electronic Devices. , 2018, Accounts of chemical research.

[35]  Harry M. T. Choi,et al.  Programming biomolecular self-assembly pathways , 2008, Nature.

[36]  Guangming Zeng,et al.  How Do Enzymes 'Meet' Nanoparticles and Nanomaterials? , 2017, Trends in biochemical sciences.

[37]  Vamsi K Yadavalli,et al.  Photolithographic Micropatterning of Conducting Polymers on Flexible Silk Matrices , 2016, Advanced materials.

[38]  Christopher M.A. Brett,et al.  Highly sensitive amperometric enzyme biosensor for detection of superoxide based on conducting polymer/CNT modified electrodes and superoxide dismutase , 2016 .

[39]  A. Ashworth,et al.  The DNA damage response and cancer therapy , 2012, Nature.

[40]  Yi Lu,et al.  Biocomputing for Portable, Resettable, and Quantitative Point-of-Care Diagnostics: Making the Glucose Meter a Logic-Gate Responsive Device for Measuring Many Clinically Relevant Targets. , 2018, Angewandte Chemie.

[41]  A. Revzin,et al.  Glucose and lactate biosensors based on redox polymer/oxidoreductase nanocomposite thin films. , 2000, Analytical chemistry.

[42]  Xiao Hu,et al.  Protein-Based Bioelectronics. , 2016, ACS biomaterials science & engineering.

[43]  Igor L. Medintz,et al.  Nanoparticles and DNA - a powerful and growing functional combination in bionanotechnology. , 2016, Nanoscale.

[44]  X. Su,et al.  Nanomaterials‐based biosensors for detection of microorganisms and microbial toxins , 2017, Biotechnology journal.

[45]  Wade W Grabow,et al.  Co-transcriptional assembly of chemically modified RNA nanoparticles functionalized with siRNAs. , 2012, Nano letters.

[46]  M. Sitti,et al.  Biohybrid Microtube Swimmers Driven by Single Captured Bacteria. , 2017, Small.

[47]  Hongyun Liu,et al.  Enzymatic logic calculation systems based on solid-state electrochemiluminescence and molecularly imprinted polymer film electrodes. , 2018, Biosensors & bioelectronics.

[48]  Jing Liu,et al.  Programmable intracellular DNA biocomputing circuits for reliable cell recognitions , 2019, Chemical science.

[49]  Yingshuai Liu,et al.  Oriented immobilization of proteins on solid supports for use in biosensors and biochips: a review , 2015, Microchimica Acta.

[50]  Ziwei Li,et al.  Plasmonics of 2D Nanomaterials: Properties and Applications , 2017, Advanced science.

[51]  E. Park,et al.  High‐Performance Biosensing Systems Based on Various Nanomaterials as Signal Transducers , 2018, Biotechnology journal.

[52]  Yong-Ho Chung,et al.  Control of electrochemical signals from quantum dots conjugated to organic materials by using DNA structure in an analog logic gate. , 2016, Bioelectrochemistry.

[53]  Lorenzo Pasotti,et al.  Multiplexing and demultiplexing logic functions for computing signal processing tasks in synthetic biology. , 2011, Biotechnology journal.

[54]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[55]  A. Panchenko,et al.  Mechanisms of protein oligomerization, the critical role of insertions and deletions in maintaining different oligomeric states , 2010, Proceedings of the National Academy of Sciences.

[56]  M. Moniruzzaman,et al.  Recent advances in exploiting ionic liquids for biomolecules: Solubility, stability and applications , 2016, Biotechnology journal.

[57]  Arben Merkoçi,et al.  Nanomaterials-based enzyme electrochemical biosensors operating through inhibition for biosensing applications. , 2017, Biosensors & bioelectronics.

[58]  Pascal Perriat,et al.  A versatile method for direct and covalent immobilization of DNA and proteins on biochips. , 2007, Angewandte Chemie.

[59]  Shine Augustine,et al.  Microfluidics Based Point‐of‐Care Diagnostics , 2018, Biotechnology journal.

[60]  Ulla Wollenberger,et al.  Cytochrome P450 biosensors-a review. , 2005, Biosensors & bioelectronics.

[61]  T. Torres,et al.  Porphyrinoid biohybrid materials as an emerging toolbox for biomedical light management. , 2018, Chemical Society reviews.

[62]  Antonio Reverter,et al.  A Boolean-based systems biology approach to predict novel genes associated with cancer: Application to colorectal cancer , 2011, BMC Systems Biology.

[63]  A. Eychmüller,et al.  Enzymatic Biofuel Cells on Porous Nanostructures. , 2016, Small.

[64]  Evgeny Katz,et al.  Biomolecular information processing : from logic systems to smart sensors and actuators , 2012 .

[65]  Y. Ying,et al.  Recent advances in nanomaterial-based biosensors for antibiotics detection. , 2017, Biosensors & bioelectronics.

[66]  M. G. Almeida,et al.  Small electron-transfer proteins as mediators in enzymatic electrochemical biosensors , 2013, Analytical and Bioanalytical Chemistry.

[67]  Evgeny Katz,et al.  Enzyme-based logic systems interfaced with signal-responsive materials and electrodes. , 2015, Chemical communications.

[68]  Yongjiu Lei,et al.  Oxygen‐Rich Enzyme Biosensor Based on Superhydrophobic Electrode , 2016, Advanced materials.

[69]  Carla Renata Arciola,et al.  A review of the biomaterials technologies for infection-resistant surfaces. , 2013, Biomaterials.

[70]  M. Win,et al.  Higher-Order Cellular Information Processing with Synthetic RNA Devices , 2008, Science.

[71]  Recombinant azurin-CdSe/ZnS hybrid structures for nanoscale resistive random access memory device. , 2017, Biosensors & bioelectronics.

[72]  Gang Wei,et al.  Designed graphene-peptide nanocomposites for biosensor applications: A review. , 2017, Analytica chimica acta.

[73]  Albert F. Lawrence,et al.  Biomolecular Electronics: Protein-Based Associative Processors and Volumetric Memories , 1999 .

[74]  S. Ramakrishna,et al.  Electrospun Fibers for Recruitment and Differentiation of Stem Cells in Regenerative Medicine , 2017, Biotechnology journal.

[75]  Nan Ma,et al.  Surface modification and endothelialization of biomaterials as potential scaffolds for vascular tissue engineering applications. , 2015, Chemical Society reviews.

[76]  Giovanna Marrazza,et al.  Electrochemical DNA biosensor for environmental monitoring , 2001 .

[77]  Jeong-Woo Choi,et al.  Electrochemical H2O2 biosensor composed of myoglobin on MoS2 nanoparticle-graphene oxide hybrid structure. , 2017, Biosensors & bioelectronics.

[78]  Daria M. Shcherbakova,et al.  Bright monomeric near-infrared fluorescent proteins as tags and biosensors for multiscale imaging , 2016, Nature Communications.

[79]  I. Willner,et al.  Logic gates and elementary computing by enzymes. , 2006, The journal of physical chemistry. A.

[80]  J. Yu,et al.  Complete oxidation of methanol in biobattery devices using a hydrogel created from three modified dehydrogenases. , 2013, Angewandte Chemie.

[81]  A. Turner,et al.  On/Off‐Switchable Zipper‐Like Bioelectronics on a Graphene Interface , 2014, Advanced materials.

[82]  Chao Li,et al.  Enhanced charge transfer by gold nanoparticle at DNA modified electrode and its application to label-free DNA detection. , 2014, ACS applied materials & interfaces.

[83]  Jianding Qiu,et al.  DNA electronic logic gates based on metal-ion-dependent induction of oligonucleotide structural motifs. , 2013, Chemistry.

[84]  Reza M Zadegan,et al.  Nucleic acid memory. , 2016, Nature materials.

[85]  N. Seeman,et al.  A precisely controlled DNA biped walking device , 2004 .

[86]  Emil F. Khisamutdinov,et al.  Fabrication of RNA 3D Nanoprisms for Loading and Protection of Small RNAs and Model Drugs , 2016, Advanced materials.

[87]  James Chappell,et al.  Creating small transcription activating RNAs. , 2015, Nature chemical biology.

[88]  G. Rivas,et al.  Electrochemical biointerfaces based on carbon nanotubes-mesoporous silica hybrid material: Bioelectrocatalysis of hemoglobin and biosensing applications. , 2018, Biosensors & bioelectronics.

[89]  J. Min,et al.  Nanoscale protein-based memory device composed of recombinant azurin. , 2010, Biomaterials.

[90]  J-Pablo Salvador,et al.  Multimodal plasmonic biosensing nanostructures prepared by DNA-directed immobilization of multifunctional DNA-gold nanoparticles. , 2017, Biosensors & bioelectronics.

[91]  T. Tuschl,et al.  Mechanisms of gene silencing by double-stranded RNA , 2004, Nature.

[92]  Peixuan Guo,et al.  Fabrication of pRNA nanoparticles to deliver therapeutic RNAs and bioactive compounds into tumor cells , 2013, Nature Protocols.

[93]  J. Min,et al.  Multifunctional DNA-based biomemory device consisting of ssDNA/Cu heterolayers. , 2011, Biosensors & bioelectronics.

[94]  Peixuan Guo The emerging field of RNA nanotechnology. , 2010, Nature nanotechnology.

[95]  Yanbing Yang,et al.  Aptamer-functionalized carbon nanomaterials electrochemical sensors for detecting cancer relevant biomolecules , 2018 .

[96]  Genxi Li,et al.  Third-Generation Biosensors Based on the Direct Electron Transfer of Proteins , 2004, Analytical sciences : the international journal of the Japan Society for Analytical Chemistry.

[97]  H. Herweijer,et al.  Progress and prospects: naked DNA gene transfer and therapy , 2003, Gene Therapy.

[98]  Ming C. Wu,et al.  Large-scale broadband digital silicon photonic switches with vertical adiabatic couplers , 2016 .

[99]  Magnus Berggren,et al.  Organic bioelectronics in nanomedicine. , 2011, Biochimica et biophysica acta.

[100]  D. Huo,et al.  A sensitive electrochemical DNA biosensor based on three-dimensional nitrogen-doped graphene and Fe3O4 nanoparticles , 2017 .

[101]  W. Peukert,et al.  Impact of the nanoparticle-protein corona on colloidal stability and protein structure. , 2012, Langmuir : the ACS journal of surfaces and colloids.

[102]  Minkyu Shin,et al.  Flexible HIV-1 Biosensor Based on the Au/MoS2 Nanoparticles/Au Nanolayer on the PET Substrate , 2019, Nanomaterials.

[103]  Zhongying Wang,et al.  Environmental Applications of 2D Molybdenum Disulfide (MoS2) Nanosheets. , 2017, Environmental science & technology.

[104]  Xuan Cao,et al.  Highly Sensitive and Wearable In2O3 Nanoribbon Transistor Biosensors with Integrated On-Chip Gate for Glucose Monitoring in Body Fluids. , 2018, ACS nano.

[105]  Jie Gao,et al.  Colorimetric logic gate for alkaline phosphatase based on copper (II)-based metal-organic frameworks with peroxidase-like activity. , 2018, Analytica chimica acta.

[106]  Katherine J Odenthal,et al.  An introduction to electrochemical DNA biosensors. , 2007, The Analyst.

[107]  T. LaBean,et al.  One-pot assembly of a hetero-dimeric DNA origami from chip-derived staples and double-stranded scaffold. , 2013, ACS nano.

[108]  Itamar Willner,et al.  Biomolecule-based nanomaterials and nanostructures. , 2010, Nano letters.

[109]  R. Weiss,et al.  Cancer Cells Multi-Input RNAi-Based Logic Circuit for Identification of Specific , 2011 .

[110]  Robert Penchovsky Engineering integrated digital circuits with allosteric ribozymes for scaling up molecular computation and diagnostics. , 2012, ACS synthetic biology.

[111]  C. Bala,et al.  Electrochemical biosensors for fast detection of food contaminants trends and perspective , 2016 .

[112]  Jiye Shi,et al.  Scaffolded biosensors with designed DNA nanostructures , 2013 .

[113]  Mark Gerstein,et al.  Loregic: A Method to Characterize the Cooperative Logic of Regulatory Factors , 2015, PLoS Comput. Biol..

[114]  E. Bahadır,et al.  Applications of commercial biosensors in clinical, food, environmental, and biothreat/biowarfare analyses. , 2015, Analytical biochemistry.

[115]  Jeong-Woo Choi,et al.  Label-free detection of γ-aminobutyric acid based on silicon nanowire biosensor , 2019, Nano Convergence.

[116]  Lia Stanciu,et al.  Graphene based enzymatic bioelectrodes and biofuel cells. , 2015, Nanoscale.

[117]  Charles M. Lieber,et al.  Nanoscience and the nano-bioelectronics frontier , 2015, Nano Research.

[118]  A. Baeumner,et al.  RNA biosensor for the rapid detection of viable Escherichia coli in drinking water. , 2003, Biosensors & bioelectronics.

[119]  Hye Kyu Choi,et al.  Flexible electrochemical glucose biosensor based on GOx/gold/MoS2/gold nanofilm on the polymer electrode. , 2019, Biosensors & bioelectronics.

[120]  E. Braun,et al.  DNA-Templated Carbon Nanotube Field-Effect Transistor , 2003, Science.

[121]  Yuehe Lin,et al.  Glucose Biosensors Based on Carbon Nanotube Nanoelectrode Ensembles , 2004 .

[122]  N. Seeman,et al.  A nanomechanical device based on the B–Z transition of DNA , 1999, Nature.

[123]  S. Gerson,et al.  Advances in therapeutic targeting of the DNA damage response in cancer. , 2018, DNA repair.

[124]  Hyeon-Yeol Cho,et al.  H2O2 biosensor consisted of hemoglobin-DNA conjugate on nanoporous gold thin film electrode with electrochemical signal enhancement , 2019, Nano Convergence.

[125]  I. Ocsoy,et al.  A new generation approach in enzyme immobilization: Organic-inorganic hybrid nanoflowers with enhanced catalytic activity and stability. , 2016, Enzyme and microbial technology.

[126]  Yong Zhang,et al.  M13 virus-directed synthesis of nanostructured metal oxides for lithium-oxygen batteries. , 2014, Nano letters.

[127]  Applications of Protein Biochips in Biomedical and Biotechnological Research , 2009, Angewandte Chemie.