Graphene-Based Materials for Biosensors: A Review

The advantages conferred by the physical, optical and electrochemical properties of graphene-based nanomaterials have contributed to the current variety of ultrasensitive and selective biosensor devices. In this review, we present the points of view on the intrinsic properties of graphene and its surface engineering concerned with the transduction mechanisms in biosensing applications. We explain practical synthesis techniques along with prospective properties of the graphene-based materials, which include the pristine graphene and functionalized graphene (i.e., graphene oxide (GO), reduced graphene oxide (RGO) and graphene quantum dot (GQD). The biosensing mechanisms based on the utilization of the charge interactions with biomolecules and/or nanoparticle interactions and sensing platforms are also discussed, and the importance of surface functionalization in recent up-to-date biosensors for biological and medical applications.

[1]  R. Maboudian,et al.  Single-layer CVD-grown graphene decorated with metal nanoparticles as a promising biosensing platform. , 2012, Biosensors & bioelectronics.

[2]  Jacek Klinowski,et al.  A new structural model for graphite oxide , 1998 .

[3]  Alina Vasilescu,et al.  Surface Plasmon Resonance based sensing of lysozyme in serum on Micrococcus lysodeikticus-modified graphene oxide surfaces. , 2017, Biosensors & bioelectronics.

[4]  Hanna Trzeciakiewicz,et al.  A protein-based electrochemical biosensor for detection of tau protein, a neurodegenerative disease biomarker. , 2014, The Analyst.

[5]  A. Reina,et al.  Large area, few-layer graphene films on arbitrary substrates by chemical vapor deposition. , 2009, Nano letters.

[6]  M. Pumera,et al.  Electrochemistry of graphene and related materials. , 2014, Chemical reviews.

[7]  P. Ajayan,et al.  Blue photoluminescent carbon nanodots from limeade. , 2016, Materials science & engineering. C, Materials for biological applications.

[8]  N. Peres,et al.  Colloquium: The transport properties of graphene: An introduction , 2010, 1007.2849.

[9]  J. Coleman,et al.  High-yield production of graphene by liquid-phase exfoliation of graphite. , 2008, Nature nanotechnology.

[10]  B. Hong,et al.  Prospects and Challenges of Graphene in Biomedical Applications , 2013, Advanced materials.

[11]  Falah Awwad,et al.  Fabrication and characterization of graphite oxide – nanoparticle composite based field effect transistors for non-enzymatic glucose sensor applications , 2017 .

[12]  Peng Chen,et al.  Electrical Detection of DNA Hybridization with Single‐Base Specificity Using Transistors Based on CVD‐Grown Graphene Sheets , 2010, Advanced materials.

[13]  William Regan,et al.  Graphene as a long-term metal oxidation barrier: worse than nothing. , 2013, ACS nano.

[14]  Xiaoyu Cao,et al.  Ultra-sensitive electrochemical DNA biosensor based on signal amplification using gold nanoparticles modified with molybdenum disulfide, graphene and horseradish peroxidase , 2014, Microchimica Acta.

[15]  Hongju Mao,et al.  Label-free graphene biosensor targeting cancer molecules based on non-covalent modification. , 2017, Biosensors & bioelectronics.

[16]  P. J. Ollivier,et al.  Layer-by-Layer Assembly of Ultrathin Composite Films from Micron-Sized Graphite Oxide Sheets and Polycations , 1999 .

[17]  G. Eda,et al.  Large-area ultrathin films of reduced graphene oxide as a transparent and flexible electronic material. , 2008, Nature nanotechnology.

[18]  Chengzhou Zhu,et al.  Graphene loaded bimetallic Au@Pt nanodendrites enhancing ultrasensitive electrochemical immunoassay of AFP , 2016 .

[19]  S. Iijima,et al.  Low-temperature synthesis of large-area graphene-based transparent conductive films using surface wave plasma chemical vapor deposition , 2011 .

[20]  J. Anzai,et al.  Recent Progress in Nanomaterial-Based Electrochemical Biosensors for Cancer Biomarkers: A Review , 2017, Molecules.

[21]  Yun Wu,et al.  200 GHz Maximum Oscillation Frequency in CVD Graphene Radio Frequency Transistors. , 2016, ACS applied materials & interfaces.

[22]  J. Coleman,et al.  Electrochemical ascorbic acid sensor based on DMF-exfoliated graphene , 2010 .

[23]  Benjamin Collins Brodie,et al.  On the Atomic Weight of Graphite , 1859 .

[24]  Fujita,et al.  Edge state in graphene ribbons: Nanometer size effect and edge shape dependence. , 1996, Physical review. B, Condensed matter.

[25]  Jacek Klinowski,et al.  Solid-State NMR Studies of the Structure of Graphite Oxide , 1996 .

[26]  W. Knoll,et al.  Enzyme-polyelectrolyte multilayer assemblies on reduced graphene oxide field-effect transistors for biosensing applications. , 2017, Biosensors & bioelectronics.

[27]  M. Pumera,et al.  Chemical reduction of graphene oxide: a synthetic chemistry viewpoint. , 2014, Chemical Society reviews.

[28]  A. V. Fedorov,et al.  Substrate-induced bandgap opening in epitaxial graphene. , 2007, Nature materials.

[29]  Yong-Sang Kim,et al.  Highly selective organic transistor biosensor with inkjet printed graphene oxide support system. , 2017, Journal of materials chemistry. B.

[30]  Nan-Fu Chiu,et al.  Carboxyl-functionalized graphene oxide composites as SPR biosensors with enhanced sensitivity for immunoaffinity detection. , 2017, Biosensors & bioelectronics.

[31]  D. Nikolelis,et al.  Biosensors Based on Lipid Modified Graphene Microelectrodes , 2017 .

[32]  Lan Sheng,et al.  Carbon Dots with Continuously Tunable Full-Color Emission and Their Application in Ratiometric pH Sensing , 2014 .

[33]  W. Lu,et al.  Improved synthesis of graphene oxide. , 2010, ACS nano.

[34]  D. Nikolelis,et al.  Development of a Potentiometric Chemical Sensor for the Rapid Detection of Carbofuran Based on Air Stable Lipid Films with Incorporated Calix[4]arene Phosphoryl Receptor Using Graphene Electrodes , 2015 .

[35]  Toshiyuki Kobayashi,et al.  Production of a 100-m-long high-quality graphene transparent conductive film by roll-to-roll chemical vapor deposition and transfer process , 2013 .

[36]  J. Coleman,et al.  Liquid phase production of graphene by exfoliation of graphite in surfactant/water solutions , 2008, 0809.2690.

[37]  F. Miao,et al.  A label-free and portable graphene FET aptasensor for children blood lead detection , 2016, Scientific Reports.

[38]  J. Coleman.  Liquid exfoliation of defect-free graphene. , 2013, Accounts of chemical research.

[39]  Changming Cheng,et al.  A graphene quantum dot@Fe3O4@SiO2 based nanoprobe for drug delivery sensing and dual-modal fluorescence and MRI imaging in cancer cells. , 2017, Biosensors & bioelectronics.

[40]  Yang Yang,et al.  High-throughput solution processing of large-scale graphene. , 2009, Nature nanotechnology.

[41]  Franklin Bien,et al.  Wearable smart sensor systems integrated on soft contact lenses for wireless ocular diagnostics , 2017, Nature Communications.

[42]  Jian Peng,et al.  Enhanced peroxidase-like activity of MoS2/graphene oxide hybrid with light irradiation for glucose detection. , 2017, Biosensors & bioelectronics.

[43]  K. Loh,et al.  Direct voltammetric detection of DNA and pH sensing on epitaxial graphene: an insight into the role of oxygenated defects. , 2010, Analytical chemistry.

[44]  T. Rocha-Santos,et al.  Graphene based sensors and biosensors , 2017 .

[45]  N. Peres.  The transport properties of graphene: an introduction , 2010 .

[46]  Ye Ma,et al.  Highly sensitive electrochemical detection of circulating tumor DNA based on thin-layer MoS2/graphene composites , 2016 .

[47]  Junying Chen,et al.  Tuning photoluminescence and surface properties of carbon nanodots for chemical sensing. , 2016, Nanoscale.

[48]  Yaoqi Zhou,et al.  Real-time reliable determination of binding kinetics of DNA hybridization using a multi-channel graphene biosensor , 2017, Nature Communications.

[49]  Robert H. Hurt,et al.  All in the graphene family - A recommended nomenclature for two-dimensional carbon materials , 2013 .

[50]  Kun Wang,et al.  Fluorescent "on-off-on" switching sensor based on CdTe quantum dots coupled with multiwalled carbon nanotubes@graphene oxide nanoribbons for simultaneous monitoring of dual foreign DNAs in transgenic soybean. , 2017, Biosensors & bioelectronics.

[51]  L. Staudenmaier,et al.  Verfahren zur Darstellung der Graphitsäure , 1898 .

[52]  Rolf Erni,et al.  Determination of the Local Chemical Structure of Graphene Oxide and Reduced Graphene Oxide , 2010, Advanced materials.

[53]  N. Motta,et al.  Graphene growth on silicon carbide: A review , 2016 .

[54]  Hong Zhang,et al.  Synthesis of Luminescent Graphene Quantum Dots with High Quantum Yield and Their Toxicity Study , 2015, PloS one.

[55]  C. M. Li,et al.  Nanoelectronic biosensors based on CVD grown graphene. , 2010, Nanoscale.

[56]  Gang Wei,et al.  When biomolecules meet graphene: from molecular level interactions to material design and applications. , 2016, Nanoscale.

[57]  Jae-Hong Kim,et al.  3D hydrogel scaffold doped with 2D graphene materials for biosensors and bioelectronics. , 2017, Biosensors & bioelectronics.

[58]  M. Willander,et al.  Structural Characterization of Graphene Nanosheets for Miniaturization of Potentiometric Urea Lipid Film Based Biosensors , 2012 .

[59]  Georgia-Paraskevi Nikoleli,et al.  A Selective Immunosensor for D‐dimer Based on Antibody Immobilized on a Graphene Electrode with Incorporated Lipid Films , 2014 .

[60]  W. D. de Heer,et al.  The growth and morphology of epitaxial multilayer graphene , 2008 .

[61]  A. Bourlinos,et al.  Liquid-phase exfoliation of graphite towards solubilized graphenes. , 2009, Small.

[62]  O. Muskens,et al.  Graphene Oxide-Upconversion Nanoparticle Based Optical Sensors for Targeted Detection of mRNA Biomarkers Present in Alzheimer's Disease and Prostate Cancer. , 2017, ACS sensors.

[63]  Md. Shamim Anower,et al.  Modeling of a highly sensitive MoS 2 -Graphene hybrid based fiber optic SPR biosensor for sensing DNA hybridization , 2017 .

[64]  Joseph C Liao,et al.  Advances and challenges in biosensor-based diagnosis of infectious diseases , 2014, Expert review of molecular diagnostics.

[65]  A. Touhami.  Biosensors and Nanobiosensors : Design and Applications , 2015 .

[66]  T. Lin,et al.  Ultra-high sensitivity of the non-immunological affinity of graphene oxide-peptide-based surface plasmon resonance biosensors to detect human chorionic gonadotropin. , 2017, Biosensors & bioelectronics.

[67]  S. Galvagno,et al.  Graphene quantum dots for cancer targeted drug delivery. , 2017, International journal of pharmaceutics.

[68]  Adisorn Tuantranont,et al.  Electrochemical paper-based peptide nucleic acid biosensor for detecting human papillomavirus. , 2017, Analytica chimica acta.

[69]  J.-M. Themlin,et al.  HETEROEPITAXIAL GRAPHITE ON 6H-SIC(0001): INTERFACE FORMATION THROUGH CONDUCTION-BAND ELECTRONIC STRUCTURE , 1998 .

[70]  Taesung Kim,et al.  A sensitive electrochemical sensor for in vitro detection of parathyroid hormone based on a MoS2-graphene composite , 2016, Scientific Reports.

[71]  A. V. Fedorov,et al.  Origin of the energy bandgap in epitaxial graphene , 2008, 0804.1818.

[72]  Kwang S. Kim,et al.  Large-scale pattern growth of graphene films for stretchable transparent electrodes , 2009, Nature.

[73]  Jianguo Tian,et al.  Reduced graphene oxide-based optical sensor for detecting specific protein , 2017 .

[74]  Pradeep Kumar,et al.  Integration of Biosensors and Drug Delivery Technologies for Early Detection and Chronic Management of Illness , 2013, Sensors.

[75]  S. Vigneshvar,et al.  Recent Advances in Biosensor Technology for Potential Applications – An Overview , 2016, Front. Bioeng. Biotechnol..

[76]  Dongmin Chen,et al.  Synthesis and Solid-State NMR Structural Characterization of 13C-Labeled Graphite Oxide , 2008, Science.

[77]  L. C. Clark,et al.  ELECTRODE SYSTEMS FOR CONTINUOUS MONITORING IN CARDIOVASCULAR SURGERY , 1962 .

[78]  Lu Wei,et al.  Bioorthogonal chemical imaging of metabolic activities in live mammalian hippocampal tissues with stimulated Raman scattering , 2016, Scientific Reports.

[79]  Nidhi Chauhan,et al.  Glycated hemoglobin detection with electrochemical sensing amplified by gold nanoparticles embedded N-doped graphene nanosheet. , 2017, Biosensors & bioelectronics.

[80]  Yury V Stebunov,et al.  Highly Sensitive and Selective Sensor Chips with Graphene-Oxide Linking Layer. , 2015, ACS applied materials & interfaces.

[81]  Wei Wang,et al.  Biological applications of carbon dots , 2014, Science China Chemistry.

[82]  Guonan Chen,et al.  Natural carbon-based dots from humic substances , 2015, Scientific Reports.

[83]  Jing Lyu,et al.  A fluorescence turn-on biosensor based on graphene quantum dots (GQDs) and molybdenum disulfide (MoS2) nanosheets for epithelial cell adhesion molecule (EpCAM) detection. , 2017, Biosensors & bioelectronics.

[84]  Guo-Jun Zhang,et al.  Detection of heart failure-related biomarker in whole blood with graphene field effect transistor biosensor. , 2017, Biosensors & bioelectronics.

[85]  Joseph Wang,et al.  Glucose Biosensors : 40 Years of Advances and Challenges , 2001 .

[86]  B. K. Gupta,et al.  Graphene quantum dots derived from carbon fibers. , 2012, Nano letters.

[87]  G. Fudenberg,et al.  Ultrahigh electron mobility in suspended graphene , 2008, 0802.2389.

[88]  L. Brey,et al.  Electronic states of graphene nanoribbons studied with the Dirac equation , 2006 .

[89]  Seungchul Kim,et al.  Origin of anomalous electronic structures of epitaxial graphene on silicon carbide. , 2007, Physical review letters.

[90]  Latha A. Gearheart,et al.  Electrophoretic analysis and purification of fluorescent single-walled carbon nanotube fragments. , 2004, Journal of the American Chemical Society.

[91]  Siyu Zeng,et al.  Fully integrated graphene electronic biosensor for label-free detection of lead (II) ion based on G-quadruplex structure-switching. , 2017, Biosensors & bioelectronics.

[92]  Imre Dékány,et al.  Evolution of surface functional groups in a series of progressively oxidized graphite oxides , 2006 .

[93]  R. Ruoff,et al.  Graphene-based ultracapacitors. , 2008, Nano letters.

[94]  Seokwoo Jeon,et al.  Size and pH dependent photoluminescence of graphene quantum dots with low oxygen content , 2016 .

[95]  Francisco J. Arregui,et al.  Optical Fibre Sensors Using Graphene-Based Materials: A Review , 2017, Sensors.

[96]  Xiaofeng Lin,et al.  Pd-Au@carbon dots nanocomposite: Facile synthesis and application as an ultrasensitive electrochemical biosensor for determination of colitoxin DNA in human serum. , 2017, Biosensors & bioelectronics.

[97]  Hung-Wei Yang,et al.  An electrochemical biosensor to simultaneously detect VEGF and PSA for early prostate cancer diagnosis based on graphene oxide/ssDNA/PLLA nanoparticles. , 2017, Biosensors & bioelectronics.

[98]  Y. Prajapati,et al.  Performance of graphene–MoS2 based surface plasmon resonance sensor using Silicon layer , 2015 .

[99]  A. Geim,et al.  Two-dimensional gas of massless Dirac fermions in graphene , 2005, Nature.

[100]  Ping Wu,et al.  Real-time fluorescence assay of alkaline phosphatase in living cells using boron-doped graphene quantum dots as fluorophores. , 2017, Biosensors & bioelectronics.

[101]  Kwang S. Kim,et al.  Roll-to-roll production of 30-inch graphene films for transparent electrodes. , 2010, Nature nanotechnology.

[102]  W. S. Hummers,et al.  Preparation of Graphitic Oxide , 1958 .

[103]  K. Bolotin,et al.  Graphene: corrosion-inhibiting coating. , 2012, ACS nano.

[104]  U. Hofmann,et al.  Untersuchungen über Graphitoxyd , 1937 .

[105]  Anthony P F Turner,et al.  Biosensors: sense and sensibility. , 2013, Chemical Society reviews.

[106]  Hye Rim Cho,et al.  A graphene-based electrochemical device with thermoresponsive microneedles for diabetes monitoring and therapy. , 2016, Nature nanotechnology.

[107]  Kai Yang,et al.  In vivo NIR fluorescence imaging, biodistribution, and toxicology of photoluminescent carbon dots produced from carbon nanotubes and graphite. , 2012, Small.

[108]  G. Ruess.  Über das Graphitoxyhydroxyd (Graphitoxyd) , 1947 .

[109]  D. Nikolelis,et al.  Development of an Electrochemical Biosensor for the Rapid Detection of Cholera Toxin Using Air Stable Lipid Films with incorporated Ganglioside GM1 , 2011 .

[110]  Lo Gorton,et al.  An Overview of the Latest Graphene-Based Sensors for Glucose Detection: the Effects of Graphene Defects , 2015 .

[111]  H. Boehm.,et al.  Untersuchungen am Graphitoxid. VI. Betrachtungen zur Struktur des Graphitoxids , 1969 .

[112]  X. Qu,et al.  Lighting up left-handed Z-DNA: photoluminescent carbon dots induce DNA B to Z transition and perform DNA logic operations , 2013, Nucleic acids research.

[113]  Andre K. Geim,et al.  Electric Field Effect in Atomically Thin Carbon Films , 2004, Science.

[114]  Georgia-Paraskevi Nikoleli,et al.  Development of an Electrochemical Biosensor for the Rapid Detection of Saxitoxin Based on Air Stable Lipid Films with Incorporated Anti-STX Using Graphene Electrodes , 2017 .

[115]  John A. Rogers,et al.  Transfer of graphene layers grown on SiC wafers to other substrates and their integration into field effect transistors , 2009 .

[116]  Francisco Guinea,et al.  Existence and topological stability of Fermi points in multilayered graphene , 2007 .

[117]  S. Stankovich,et al.  Synthesis of graphene-based nanosheets via chemical reduction of exfoliated graphite oxide , 2007 .

[118]  Bai Yang,et al.  The photoluminescence mechanism in carbon dots (graphene quantum dots, carbon nanodots, and polymer dots): current state and future perspective , 2015, Nano Research.

[119]  Guigen Zhang.  Nanotechnology-Based Biosensors in Drug Delivery , 2009 .

[120]  Wei Wei,et al.  Beyond a Carrier: Graphene Quantum Dots as a Probe for Programmatically Monitoring Anti-Cancer Drug Delivery, Release, and Response. , 2017, ACS applied materials & interfaces.

[121]  Kun Wang,et al.  A novel electrochemical biosensor based on polyadenine modified aptamer for label-free and ultrasensitive detection of human breast cancer cells. , 2017, Talanta.

[122]  Jingyi Xu,et al.  Low-cost synthesis of carbon nanodots from natural products used as a fluorescent probe for the detection of ferrum(III) ions in lake water , 2014 .

[123]  Ulrich Hofmann,et al.  Das Adsorptionsverhalten sehr dünner Kohlenstoff‐Folien , 1962 .

[124]  M Valcárcel,et al.  Semiconductor and carbon-based fluorescent nanodots: the need for consistency. , 2016, Chemical communications.

[125]  Cheol-Woong Yang,et al.  Evidence of graphitic AB stacking order of graphite oxides. , 2008, Journal of the American Chemical Society.

[126]  Zhiming Yu,et al.  High-performance non-enzymatic glucose sensor based on nickel-microcrystalline graphite-boron doped diamond complex electrode , 2017 .

[127]  Kotaro Kajikawa,et al.  Label and Label-Free Detection Techniques for Protein Microarrays , 2015, Microarrays.

[128]  R. Ruoff,et al.  The chemistry of graphene oxide. , 2010, Chemical Society reviews.

[129]  Ata Mahjoubfar,et al.  Deep Learning in Label-free Cell Classification , 2016, Scientific Reports.

[130]  T. K. Maiti,et al.  Simple one-step synthesis of highly luminescent carbon dots from orange juice: application as excellent bio-imaging agents. , 2012, Chemical communications.

[131]  Chongwu Zhou,et al.  Continuous, highly flexible, and transparent graphene films by chemical vapor deposition for organic photovoltaics. , 2010, ACS nano.

[132]  B. Liu,et al.  Graphene Quantum Dots from Polycyclic Aromatic Hydrocarbon for Bioimaging and Sensing of Fe3+ and Hydrogen Peroxide , 2013 .

[133]  Da Chen,et al.  Graphene oxide: preparation, functionalization, and electrochemical applications. , 2012, Chemical reviews.

[134]  E. Alocilja,et al.  Market analysis of biosensors for food safety. , 2003, Biosensors & bioelectronics.

[135]  Huafeng Yang,et al.  Direct electrochemistry of glucose oxidase and biosensing for glucose based on graphene. , 2009, Analytical chemistry.

[136]  H. Dai,et al.  Chemically Derived, Ultrasmooth Graphene Nanoribbon Semiconductors , 2008, Science.

[137]  Jing Zhang,et al.  High Resolution Quantitative Angle-Scanning Widefield Surface Plasmon Microscopy , 2016, Scientific reports.

[138]  Wei Gao,et al.  New insights into the structure and reduction of graphite oxide. , 2009, Nature chemistry.

[139]  Minghong Wu,et al.  Hydrothermal Route for Cutting Graphene Sheets into Blue‐Luminescent Graphene Quantum Dots , 2010, Advanced materials.

[140]  Tsuyoshi Nakajima,et al.  A new structure model of graphite oxide , 1988 .

[141]  Chi‐Man Lawrence Wu,et al.  Label-free detection of 3-nitro-l-tyrosine with nickel-doped graphene localized surface plasmon resonance biosensor. , 2017, Biosensors & bioelectronics.