Biosensors based on graphene oxide and its biomedical application

Advanced Drug Delivery Reviews

Volumn 105, Issue , 2016, Pages 275-287

  Lee, Jieon ^a   Kim, Jungho ^a   Kim, Seongchan ^a   Min, Dal Hee ^a,b  

^a Seoul National University   (South Korea)

^b Lemonex Inc   (South Korea)

Author keywords

Biomolecule; Biosensor; Electrochemistry; FRET; Graphene oxide; Hybrid nanomaterial; LDI MS; SERS

Indexed keywords

BIOCOMPATIBILITY; BIOMOLECULES; BIOSENSORS; CHEMICAL DETECTION; DESORPTION; ELECTROCHEMISTRY; ENERGY TRANSFER; FLUORESCENCE; MASS SPECTROMETRY; MEDICAL APPLICATIONS; MOLECULAR BIOLOGY; RAMAN SPECTROSCOPY;

FRET; GRAPHENE OXIDES; HYBRID NANOMATERIALS; LDI-MS; SERS;

GRAPHENE;

GRAPHENE OXIDE; GRAPHITE; OXIDE;

ANALYTIC METHOD; BIOSENSOR; CHEMICAL STRUCTURE; DNA PROBE; ELECTROCHEMICAL ANALYSIS; ENZYME ACTIVITY; ENZYME ASSAY; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT BIOSENSOR; HIGH THROUGHPUT SCREENING; HUMAN; LIVING CELL IMAGING; MATERIAL COATING; MATRIX-ASSISTED LASER DESORPTION-IONIZATION MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; RAMAN SPECTROMETRY; REVIEW; SIGNAL DETECTION; SIGNAL PROCESSING; SOLID; SURFACE ENHANCED RAMAN SPECTROSCOPY; TISSUE IMAGING; ANIMAL; GENETIC PROCEDURES;

ANIMALS; BIOSENSING TECHNIQUES; ENZYME ASSAYS; GRAPHITE; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; OXIDES;

EID: 84977576369     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2016.06.001     Document Type: Review

References (152)

1. [1] Novoselov, K.S., Geim, A.K., Morozov, S.V., Jiang, D., Zhang, Y., Dubonos, S.V., Grigorieva, I.V., Firsov, A.A., Electric field effect in atomically thin carbon films. Science 306 (2004), 666–669.
2. [2] Allen, M.J., Tung, V.C., Kaner, R.B., Honeycomb carbon: a review of graphene. Chem. Rev. 110 (2010), 132–146.
3. [3] Yin, P.T., Shah, S., Chhowalla, M., Lee, K.B., Design, synthesis, and characterization of graphene-nanoparticle hybrid materials for bioapplications. Chem. Rev. 115 (2015), 2483–2531.
4. [4] Kim, K.S., Zhao, Y., Jang, H., Lee, S.Y., Kim, J.M., Kim, K.S., Ahn, J.H., Kim, P., Choi, J.Y., Hong, B.H., Large-scale pattern growth of graphene films for stretchable transparent electrodes. Nature 457 (2009), 706–710.
5. [5] Bogue, R., Graphene sensors: a review of recent developments. Sensor Rev. 34 (2014), 233–238.
6. [6] Ge, S., Lan, F., Yuc, F., Yu, J., Applications of graphene and related nanomaterials in analytical chemistry. New J. Chem. 39 (2015), 2380–2395.
7. [7] Hummers, W.S., Offeman, R.E., Preparation of graphitic oxide. J. Am. Chem. Soc., 80, 1958, 1339.
8. [8] Botas, C., Alvarez, P., Blanco, P., Granda, M., Blanco, C., Santamaría, R., Romasanta, L.J., Verdejo, R., Lopez-Manchado, M.A., Menendez, R., Graphene materials with different structures prepared from the same graphite by the Hummers and Brodie methods. Carbon 65 (2013), 156–164.
9. [9] Marcano, D.C., Kosynkin, D.V., Berlin, J.M., Sinitskii, A., Sun, Z., Slesarev, A., Alemany, L.B., Lu, W., Tour, J.M., Improved synthesis of graphene oxide. ACS Nano 4 (2010), 4806–4814.
10. [10] Li, D., Muller, M.B., Gilje, S., Kaner, R.B., Wallace, G.G., Processable aqueous dispersions of graphene nanosheets. Nat. Nanotechnol. 3 (2009), 101–105.
11. [11] Zhu, Y., Murali, S., Cai, W., Li, X., Suk, J.W., Potts, J.R., Ruoff, R.S., Graphene and graphene oxide: synthesis, properties, and applications. Adv. Mater. 22 (2010), 3906–3924.
12. [12] Loh, K.P., Bao, Q., Eda, G., Chhowalla, M., Graphene oxide as a chemically tunable platform for optical applications. Nat. Chem. 2 (2010), 1015–1024.
13. [13] Hunt, A., Dikin, D.A., Kurmaev, E.Z., Boyko, T.D., Bazylewski, P., Chang, G.S., Moewes, A., Epoxide speciation and functional group distribution in graphene oxide paper-like materials. Adv. Funct. Mater. 22 (2012), 3950–3957.
14. [14] Gao, W., Alemany, L.B., Ci, L., Ajayan, P.M., New insights into the structure and reduction of graphite oxide. Nat. Chem. 1 (2009), 403–408.
15. [15] Liu, Y., Dong, X., Chen, P., Biological and chemical sensors based on graphene materials. Chem. Soc. Rev. 41 (2012), 2283–2307.
16. [16] Zhang, Y., Wu, C., Guo, S., Zhang, J., Interactions of graphene and graphene oxide with proteins and peptides. Nanotechnol. Rev. 2 (2013), 27–45.
17. [17] Wang, Y., Li, Z., Wang, J., Li, J., Lin, Y., Graphene and graphene oxide: biofunctionalization and applications in biotechnology. Trends Biotechnol. 29 (2011), 205–212.
18. [18] Chung, C., Kim, Y.K., Shin, D., Ryoo, S.R., Hong, B.H., Min, D.-H., Biomedical applications of graphene and graphene oxide. Acc. Chem. Res. 46 (2013), 2211–2224.
19. [19] Huang, X., Yin, Z., Wu, S., Qi, X., He, Q., Zhang, Q., Yan, Q., Boey, F., Zhang, H., Graphene-based materials: synthesis, characterization, properties, and applications. Small 7 (2011), 1876–1902.
20. [20] Park, S., An, J., Jung, I., Piner, R.D., An, S.J., Li, X., Velamakanni, A., Ruoff, R.S., Colloidal suspensions of highly reduced graphene oxide in a wide variety of organic solvents. Nano Lett. 9 (2009), 1593–1597.
21. [21] Si, Y., Samulski, E.T., Synthesis of water soluble graphene. Nano Lett. 8 (2008), 1679–1682.
22. [22] Shen, J., Hu, Y., Shi, M., Lu, X., Qin, C., Li, C., Ye, M., Fast and facile preparation of graphene oxide and reduced graphene oxide nanoplatelets. Chem. Mater. 21 (2009), 3514–3520.
23. [23] Pei, S., Cheng, H.-M., The reduction of graphene oxide. Carbon 50 (2012), 3210–3228.
24. [24] Bai, S., Shen, X., Graphene-inorganic nanocomposites. RSC Adv. 2 (2012), 64–98.
25. [25] Kim, Y.K., Kim, M.H., Min, D.-H., Biocompatible reduced graphene oxide prepared by using dextran as a multifunctional reducing agent. Chem. Commun. 47 (2011), 3195–3197.
26. [26] Vashist, S.K., Luong, J.H.T., Recent advances in electrochemical biosensing schemes using graphene and graphene-based nanocomposites. Carbon 84 (2015), 519–550.
27. [27] Kim, J., Cote, L.J., Kim, F., Yuan, W., Shull, K.R., Huang, J., Graphene oxide sheets at interfaces. J. Am. Chem. Soc. 132 (2010), 8180–8186.
28. [28] Shao, J.J., Lv, W., Yang, Q.H., Self-assembly of graphene oxide at interfaces. Adv. Mater. 26 (2014), 5586–5612.
29. [29] Swathi, R.S., Sebastian, K.L., Resonance energy transfer from a dye molecule to graphene. J. Chem. Phys., 129, 2008, 054703.
30. [30] Swathi, R.S., Sebastian, K.L., Long range resonance energy transfer from a dye molecule to graphene has (distance)(− 4) dependence. J. Chem. Phys., 130, 2009, 186010.
31. [31] Kim, J., Cote, L.J., Kim, F., Huang, J., Visualizing graphene based sheets by fluorescence quenching microscopy. J. Am. Chem. Soc. 132 (2010), 260–267.
32. [32] Morales-Narvaez, E., Merkoci, A., Graphene oxide as an optical biosensing platform. Adv. Mater. 24 (2012), 3298–3308.
33. [33] de Miguel, M., Alvaro, M., García, H., Graphene as a quencher of electronic excited states of photochemical probes. Langmuir 28 (2012), 2849–2857.
34. [34] Morales-Narváez, E., Pérez-López, B., Pires, L.B., Merkoçi, A., Simple Förster resonance energy transfer evidence for the ultrahigh quantum dot quenching efficiency by graphene oxide compared to other carbon structures. Carbon 50 (2012), 2987–2993.
35. [35] Wu, M., Kempaiah, R., Huang, P.J., Maheshwari, V., Liu, J., Adsorption and desorption of DNA on graphene oxide studied by fluorescently labeled oligonucleotides. Langmuir 27 (2011), 2731–2738.
36. [36] Liu, B., Sun, Z., Zhang, X., Liu, J., Mechanisms of DNA sensing on graphene oxide. Anal. Chem. 85 (2013), 7987–7993.
37. [37] Zhang, H., Jia, S., Lv, M., Shi, J., Zuo, X., Su, S., Wang, L., Huang, W., Fan, C., Huang, Q., Size-dependent programming of the dynamic range of graphene oxide-DNA interaction-based ion sensors. Anal. Chem. 86 (2014), 4047–4051.
38. [38] Lee, J., Yim, Y., Kim, S., Choi, M.-H., Choi, B.-S., Lee, Y., Min, D.-H., In-depth investigation of the interaction between DNA and nano-sized graphene oxide. Carbon 97 (2016), 92–98.
39. [39] Kong, X., Huang, Y., Applications of graphene in mass spectrometry. J. Nanosci. Nanotechnol. 14 (2014), 4719–4732.
40. [40] De, M., Chou, S.S., Dravid, V.P., Graphene oxide as an enzyme inhibitor: modulation of activity of α-chymotrypsin. J. Am. Chem. Soc. 33 (2011), 17524–17527.
41. [41] Tang, L.A.L., Wang, J., Loh, K.P., Graphene-based SELDI probe with ultrahigh extraction and sensitivity for DNA oligomer. J. Am. Chem. Soc. 132 (2010), 10976–10977.
42. [42] Ling, X., Xie, L., Fang, Y., Xu, H., Zhang, H., Kong, J., Dresselhaus, M.S., Zhang, J., Liu, Z., Can graphene be used as a substrate for Raman enhancement?. Nano Lett. 10 (2009), 553–561.
43. [43] Xie, L., Ling, X., Fang, Y., Zhang, J., Liu, Z., Graphene as a substrate to suppress fluorescence in resonance raman spectroscopy. J. Am. Chem. Soc. 131 (2009), 9890–9891.
44. [44] Xu, W., Mao, N., Zhang, J., Graphene: a platform for surface-enhanced Raman spectroscopy. Small 9 (2013), 1206–1224.
45. [45] Xu, W., Ling, X., Xiao, J., Dresselhaus, M.S., Kong, J., Xu, H., Liu, Z., Zhang, J., Surface enhanced Raman spectroscopy on a flat graphene surface. Proc. Natl. Acad. Sci. 109 (2012), 9281–9286.
46. [46] Sharma, B., Frontiera, R.R., Henry, A.-I., Ringe, E., Duyne, R.P.V., SERS: materials, applications, and the future. Mater. Today 15 (2012), 16–25.
47. [47] Lu, C.H., Yang, H.H., Zhu, C.L., Chen, X., Chen, G.N., A graphene platform for sensing biomolecules. Angew. Chem. Int. Ed. 48 (2009), 4785–4787.
48. [48] He, S.J., Song, B., Li, D., Zhu, C.F., Qi, W.P., Wen, Y.Q., Wang, L.H., Song, S.P., Fang, H.P., Fan, C.H., A graphene nanoprobe for rapid, sensitive, and multicolor fluorescent DNA analysis. Adv. Funct. Mater. 20 (2010), 453–459.
49. [49] Li, F., Huang, Y., Yang, Q., Zhong, Z., Li, D., Wang, L., Song, S., Fan, C., A graphene-enhanced molecular beacon for homogeneous DNA detection. Nanoscale 2 (2010), 1021–1026.
50. [50] Yi, J.W., Park, J., Singh, N.J., Lee, I.J., Kim, K.S., Kim, B.H., Quencher-free molecular beacon: enhancement of the signal-to-background ratio with graphene oxide, Bioorg. Med. Chem. Lett. 21 (2011), 704–706.
51. [51] Dong, H., Zhang, J., Ju, H., Lu, H., Wang, S., Jin, S., Hao, K., Du, H., Zhang, X., Highly sensitive multiple microRNA detection based on fluorescence quenching of graphene oxide and isothermal strand-displacement polymerase reaction. Anal. Chem. 84 (2012), 4587–4593.
52. [52] Cao, L., Cheng, L., Zhang, Z., Wang, Y., Zhang, X., Chen, H., Liu, B., Zhang, S., Kong, J., Visual and high-throughput detection of cancer cells using a graphene oxide-based FRET aptasensing microfluidic chip. Lab Chip 12 (2012), 4864–4869.
53. [53] Chang, H., Tang, L., Wang, Y., Jiang, J., Li, J., Graphene fluorescence resonance energy transfer aptasensor for the thrombin detection. Anal. Chem. 82 (2010), 2341–2346.
54. [54] Wen, Y., Xing, F., He, S., Song, S., Wang, L., Long, Y., Li, D., Fan, C., A graphene-based fluorescent nanoprobe for silver(I) ions detection by using graphene oxide and a silver-specific oligonucleotide. Chem. Commun. 46 (2010), 2596–2598.
55. [55] He, Y., Wang, Z.G., Tang, H.W., Pang, D.W., Low background signal platform for the detection of ATP: when a molecular aptamer beacon meets graphene oxide. Biosens. Bioelectron. 29 (2011), 76–81.
56. [56] Pei, H., Li, J., Lv, M., Wang, J., Gao, J., Lu, J., Li, Y., Huang, Q., Hu, J., Fan, C., A graphene-based sensor array for high-precision and adaptive target identification with ensemble aptamers. J. Am. Chem. Soc. 134 (2012), 13843–13849.
57. [57] Lu, Z., Zhang, L., Deng, Y., Li, S., He, N., Graphene oxide for rapid microRNA detection. Nanoscale 4 (2012), 5840–5842.
58. [58] Dong, H.F., Gao, W., Yan, F., Ji, H., Ju, H., Fluorescence resonance energy transfer between quantum dots and graphene oxide for sensing biomolecules. Anal. Chem. 82 (2010), 5511–5517.
59. [59] Liu, C., Wang, Z., Jia, H., Li, Z., Efficient fluorescence resonance energy transfer between upconversion nanophosphors and graphene oxide: a highly sensitive biosensing platform. Chem. Commun. 47 (2011), 4661–4663.
60. [60] Tao, Y., Lin, Y., Huang, Z., Ren, J., Qu, X., DNA-templated silver nanoclusters-graphene oxide nanohybrid materials: a platform for label-free and sensitive fluorescence turn-on detection of multiple nucleic acid targets. Analyst 137 (2012), 2588–2592.
61. [61] Liu, X., Wang, F., Aizen, R., Yehezkeli, O., Willner, I., Graphene oxide/nucleic-acid-stabilized silver nanoclusters: functional hybrid materials for optical aptamer sensing and multiplexed analysis of pathogenic DNAs. J. Am. Chem. Soc. 135 (2013), 11832–11839.
62. [62] Guo, S., Du, D., Tang, L., Ning, Y., Yao, Q., Zhang, G.J., PNA-assembled graphene oxide for sensitive and selective detection of DNA. Analyst 138 (2013), 3216–3220.
63. [63] Lee, J., Park, I.S., Jung, E., Lee, Y., Min, D.-H., Direct, sequence-specific detection of dsDNA based on peptide nucleic acid and graphene oxide without requiring denaturation. Biosens. Bioelectron. 62 (2014), 140–144.
64. [64] Lee, J., Park, G., Min, D.-H., A biosensor for the detection of single base mismatches in microRNA. Chem. Commun. 51 (2015), 14597–14600.
65. [65] Lee, J., Park, I.S., Kim, H., Woo, J.S., Choi, B.S., Min, D.-H., BSA as additive: a simple strategy for practical applications of PNA in bioanalysis. Biosens. Bioelectron. 69 (2015), 167–173.
66. [66] Dong, X.L., Cheng, J., Li, J., Wang, Y., Graphene as a novel matrix for the analysis of small molecules by MALDI-TOF MS. Anal. Chem. 82 (2010), 6208–6214.
67. [67] Gulbakan, B., Yasun, E., Shukoor, M., Zhu, Z., You, M., Tan, X., Sanchez, H., Powell, D.H., Dai, H., Tan, W., A dual platform for selective analyte enrichment and ionization in mass spectrometry using aptamer-conjugated graphene oxide. J. Am. Chem. Soc. 132 (2010), 17408–17410.
68. [68] Liu, Y., Liu, J., Yin, P., Gao, M., Deng, C., Zhang, X., High throughput identification of components from traditional Chinese medicine herbs by utilizing graphene or graphene oxide as MALDI-TOF-MS matrix. J. Mass Spectrom. 46 (2011), 804–815.
69. [69] Liu, C., Chien, M.W., Su, C.Y., Chen, H.Y., Li, L.J., Lai, C.C., Analysis of flavonoids by graphene-based surface-assisted laser desorption/ionization time-of-flight mass spectrometry. Analyst 137 (2012), 5809–5816.
70. [70] Liu, Q., Cheng, M., Jiang, G., Mildly oxidized graphene: facile synthesis, characterization, and application as a matrix in MALDI mass spectrometry. Chem. Eur. J. 19 (2013), 5561–5565.
71. [71] Cheng, G., Wang, Z.G., Liu, Y.L., Zhang, J.L., Sun, D.H., Ni, J.Z., A graphene-based multifunctional affinity probe for selective capture and sequential identification of different biomarkers from biosamples. Chem. Commun. 48 (2012), 10240–10242.
72. [72] Kawasaki, H., Nakai, K., Arakawa, R., Athanassiou, E.K., Grass, R.N., Stark, W.J., Wang, Functionalized graphene-coated cobalt nanoparticles for highly efficient surface-assisted laser desorption/ionization mass spectrometry analysis. Anal. Chem. 84 (2012), 9268–9275.
73. 2 multifunctional composite for highly selective and sensitive enrichment of phosphopeptides. RSC Adv. 4 (2014), 18132–18135.
74. [74] Huang, R.C., Chiu, W.J., Po-Jung Lai, I., Huang, C.C., Multivalent aptamer/gold nanoparticle-modified graphene oxide for mass spectrometry-based tumor tissue imaging. Sci. Rep., 5, 2015, 10292.
75. [75] Kim, Y.K., Na, H.K., Kwack, S.J., Ryoo, S.R., Lee, Y., Hong, S., Hong, S., Jeong, Y., Min, D.-H., Synergistic effect of graphene oxide/MWCNT films in laser desorption/ionization mass spectrometry of small molecules and tissue imaging. ACS Nano 5 (2011), 4550–4561.
76. [76] Kim, Y.K., Min, D.-H., Fabrication of alternating multilayer films of graphene oxide and carbon nanotube and its application in mechanistic study of laser desorption/ionization of small molecules. ACS Appl. Mater. Interfaces 4 (2012), 2088–2095.
77. [77] Kim, Y.K., Min, D.-H., Preparation of the hybrid film of poly(allylamine hydrochloride)-functionalized graphene oxide and gold nanoparticle and its application for laser-induced desorption/ionization of small molecules. Langmuir 28 (2012), 4453–4458.
78. [78] Qian, K., Zhou, L., Liu, J., Yang, J., Xu, H., Yu, M., Nouwens, A., Zou, J., Monteiro, M.J., Yu, C., Laser engineered graphene paper for mass spectrometry imaging. Sci. Rep., 3, 2013, 1415.
79. [79] Zhou, M., Zhai, Y., Dong, S., Electrochemical sensing and biosensing platform based on chemically reduced graphene oxide. Anal. Chem. 81 (2009), 5603–5613.
80. [80] Feng, L., Wu, L., Wang, J., Ren, J., Miyoshi, D., Sugimoto, N., Qu, X., Detection of a prognostic indicator in early stage cancer using functionalized graphene based peptide sensors. Adv. Mater. 23 (2012), 125–131.
81. [81] Bonanni, A., Chua, C.K., Zhao, G., Sofer, Z., Pumera, M., Inherently electroactive graphene oxide nanoplatelets as labels for single nucleotide polymorphism detection. ACS Nano 6 (2012), 8546–8551.
82. [82] He, L., Wang, Q., Mandler, D., Li, M., Boukherroub, R., Szunerits, S., Detection of folic acid protein in human serum using reduced graphene oxide electrodes modified by folic-acid. Biosens. Bioelectron. 75 (2016), 389–395.
83. [83] Choi, D., Jeong, H., Kim, K., Electrochemical thrombin detection based on the direct interaction of target proteins and graphene oxide as an indicator. Analyst 139 (2014), 1331–1333.
84. [84] Liu, J., Kong, N., Li, A., Luo, X., Cui, L., Wang, R., Feng, S., Graphene bridged enzyme electrodes for glucose biosensing application. Analyst 138 (2013), 2567–2575.
85. [85] Wang, Z.J., Zhou, X., Zhang, J., Boey, F., Zhang, H., Direct electrochemical reduction of single-layer graphene oxide and subsequent functionalization with glucose oxidase. J. Phys. Chem. C 113 (2009), 14071–14075.
86. [86] Srivastava, S., Abraham, S., Singh, C., Ali, M.A., Srivastava, A., Sumanaa, G., Malhotra, B.D., Protein conjugated carboxylated gold@reduced graphene oxide for aflatoxin B1 detection. RSC Adv. 5 (2015), 5406–5414.
87. [87] Li, J., Guo, S., Zhai, Y., Wang, E., High-sensitivity determination of lead and cadmium based on the nafion-graphene composite film. Anal. Chim. Acta 649 (2009), 196–201.
88. [88] Gong, J., Zhou, T., Song, D., Zhang, L., Monodispersed Au nanoparticles decorated graphene as an enhanced sensing platform for ultrasensitive stripping voltammetric detection of mercury(II). Sensors Actuators B 150 (2010), 491–497.
89. [89] Guo, C.X., Zheng, X.T., Lu, Z.S., Lou, X.W., Li, C.M., Biointerface by cell growth on layered graphene-artificial peroxidase–protein nanostructure for in situ quantitative molecular detection. Adv. Mater. 22 (2010), 5164–5167.
90. [90] Feng, L., Chen, Y., Ren, J., Qu, X., A graphene functionalized electrochemical aptasensor for selective label-free detection of cancer cells. Biomaterials 32 (2011), 2930–2937.
91. [91] Khoshfetrat, S.M., Mehrgardi, M.A., Amplified electrochemical genotyping of single-nucleotide polymorphisms using a graphene–gold nanoparticles modified glassy carbon platform. RSC Adv. 5 (2015), 29285–29293.
92. [92] Wang, Z.J., Zhang, J., Chen, P., Zhou, X., Yang, Y., Wu, S., Niu, L., Han, Y., Wang, L., Chen, P., Boey, F., Zhang, Q., Liedberg, B., Zhang, H., Label-free, electrochemical detection of methicillin-resistant Staphylococcus aureus DNA with reduced graphene oxide-modified electrodes. Biosens. Bioelectron. 26 (2011), 3881–3886.
93. [93] Du, Y., Guo, S., Dong, S., Wang, E., An integrated sensing system for detection of DNA using new parallel-motif DNA triplex system and graphene-mesoporous silica-gold nanoparticle hybrids. Biomaterials 32 (2011), 8584–8592.
94. [94] Roy, S., Soin, N., Bajpai, R., Misra, D.S., McLaughlinb, J.A., Roy, S.S., Graphene oxide for electrochemical sensing applications. J. Mater. Chem. 21 (2011), 14725–14731.
95. [95] Loo, A.H., Bonanni, A., Pumera, M., Impedimetric thrombin aptasensor based on chemically modified graphenes. Nanoscale 4 (2012), 143–147.
96. [96] Ren, W., Fang, Y., Wang, E., A binary functional substrate for enrichment and ultrasensitive SERS spectroscopic detection of folic acid using graphene oxide/Ag nanoparticle hybrids. ACS Nano 5 (2011), 6425–6433.
97. [97] Fan, Z., Kanchanapally, R., Ray, P.C., Hybrid graphene oxide based ultrasensitive SERS probe for label-free biosensing. J. Phys. Chem. Lett. 4 (2013), 3813–3818.
98. [98] Xie, Y., Li, Y., Niu, L., Wang, H., Qian, H., Yao, W., A novel surface-enhanced Raman scattering sensor to detect prohibited colorants in food by graphene/silver nanocomposite. Talanta 100 (2012), 32–37.
99. [99] Zhang, Y., Liu, S., Wang, L., Qin, X., Tian, J., Lu, W., Changa, G., Sun, X., One-pot green synthesis of Ag nanoparticles-graphene nanocomposites and their applications in SERS, H2O2, and glucose sensing. RSC Adv. 2 (2012), 538–545.
100. [100] Li, Y., Qu, L.L., Li, D.W., Song, Q.X., Fathi, F., Long, Y.T., Rapid and sensitive in-situ detection of polar antibiotics in water using a disposable Ag–graphene sensor based on electrophoretic preconcentration and surface-enhanced Raman spectroscopy. Biosen. Bioelectron. 43 (2013), 94–100.
101. [101] Lin, T.-W., Wu, H.-Y., Tasi, T.-T., Laia, Y.-H., Shen, H.-H., Surface-enhanced Raman spectroscopy for DNA detection by the self-assembly of Ag nanoparticles onto Ag nanoparticle-graphene oxide nanocomposites. Phys. Chem. Chem. Phys. 17 (2015), 18443–18448.
102. [102] Hu, C., Liu, Y., Qin, J., Nie, G., Lei, B., Xiao, Y., Zheng, M., Rong, J., Fabrication of reduced graphene oxide and sliver nanoparticle hybrids for Raman detection of absorbed folic acid: a potential cancer diagnostic probe. ACS Appl. Mater. Interfaces 5 (2013), 4760–4768.
103. [103] Zhang, Z., Liu, Q., Gao, D., Luo, D., Niu, Y., Yang, J., Li, Y., Graphene Oxide as a Multifunctional Platform for Raman and Fluorescence Imaging of Cells. Small 11 (2015), 3000–3005.
104. [104] Y. K. Kim, S. W. Han, D.-H. Min, Graphene oxide sheath on Ag nanoparticle/graphene hybrid films as an antioxidative coating and enhancer of surface-enhanced Raman scattering, ACS Appl. Mater. Interfaces 4 (1021) 6545–6551.
105. [105] Gao, N., Yang, T., Liu, T., Zoua, Y., Jiang, J., Graphene oxide wrapped individual silver nanocomposites with improved stability for surface-enhanced Raman scattering. RSC Adv. 5 (2015), 55801–55807.
106. [106] Cui, L., Lin, X., Lin, N., Song, Y., Zhu, Z., Chen, X., Yang, C.J., Graphene oxide-protected DNA probes for multiplex microRNA analysis in complex biological samples based on a cyclic enzymatic amplification method. Chem. Commun. 48 (2012), 194–196.
107. [107] Pu, Y., Zhu, Z., Han, D., Liu, H., Liu, J., Liao, J., Zhang, K., Tan, W., Insulin-binding aptamer-conjugated graphene oxide for insulin detection. Analyst 136 (2011), 4138–4140.
108. [108] Liu, X., Aizen, R., Freeman, R., Yehezkeli, O., Willner, I., Multiplexed aptasensors and amplified DNA sensors using functionalized graphene oxide: application for logic gate operations. ACS Nano 6 (2012), 3553–3563.
109. [109] Huang, R.C., Chiu, W.J., Li, Y.J., Huang, C.C., Detection of microRNA in tumor cells using exonuclease III and graphene oxide-regulated signal amplification. ACS Appl. Mater. Interfaces 6 (2014), 21780–21787.
110. [110] Liu, Y., Luo, M., Xiang, X., Chen, C., Ji, X., Chen, L., He, Z., A graphene oxide and exonuclease-aided amplification immuno-sensor for antigen detection. Chem. Commun. 50 (2014), 2679–2681.
111. [111] Lu, C.H., Li, J., Lin, M.H., Wang, Y.W., Yang, H.H., Chen, X., Chen, G.N., Amplified aptamer-based assay through catalytic recycling of the analyte. Angew. Chem. Int. Ed. 49 (2010), 8454–8457.
112. [112] Li, X., Ding, X., Fan, J., Nicking endonuclease-assisted signal amplification of a split molecular aptamer beacon for biomolecule detection using graphene oxide as a sensing platform. Analyst 140 (2015), 7918–7925.
113. [113] Li, Z., Zhu, W., Zhang, J., Jiang, J., Shen, G., Yu, R., A label-free amplified fluorescence DNA detection based on isothermal circular strand-displacement polymerization reaction and graphene oxide. Analyst 138 (2013), 3616–3620.
114. [114] Hu, K., Liu, J., Chen, J., Huang, Y., Zhao, S., Tian, J., Zhang, G., An amplified graphene oxide-based fluorescence aptasensor based on target-triggered aptamer hairpin switch and strand-displacement polymerization recycling forbioassays. Biosens. Bioelectron. 42 (2013), 598–602.
115. [115] Liu, H., Li, L., Wang, Q., Duan, L., Tang, B., Graphene fluorescence switch-based cooperative amplification: a sensitive and accurate method to detection microRNA. Anal. Chem. 86 (2014), 5487–5493.
116. [116] Wang, T., Zhang, Z., Lib, Y., Xie, G., Amplified electrochemical detection of mecA gene in methicillin-resistant Staphylococcus aureus based on target recycling amplification and isothermal strand-displacement polymerization reaction. Sensors Actuators B Chem. 221 (2015), 148–154.
117. [117] Liu, M., Song, J., Shuang, S., Dong, C., Brennan, J.D., Li, Y., A graphene-based biosensing platform based on the release of DNA probes and rolling circle amplification. ACS Nano 8 (2014), 5564–5573.
118. [118] Zhao, X., Kong, R.M., Zhang, X.B., Meng, H.M., Liu, W.N., Tan, W., Shen, G.L., Yu, R.Q., Graphene-DNAzyme based biosensor for amplified fluorescence “turn-on” detection of Pb2 + with a high selectivity. Anal. Chem. 83 (2011), 5062–5066.
119. [119] Liu, M., Zhao, H., Chen, S., Yu, H., Zhang, Y., Quan, X., A “turn-on” fluorescent copper biosensor based on DNA cleavage-dependent graphene-quenched DNAzyme. Biosens. Bioelectron. 26 (2011), 4111–4116.
120. [120] Yang, L., Liu, C., Ren, W., Li, Z., Graphene surface-anchored fluorescence sensor for sensitive detection of microRNA coupled with enzyme-free signal amplification of hybridization chain reaction. ACS Appl. Mater. Interfaces 4 (2012), 6450–6453.
121. [121] Zhang, Z., Liu, Y., Ji, X., Xiang, X., He, Z., A graphene oxide-based enzyme-free signal amplification platform for homogeneous DNA detection. Analyst 139 (2014), 4806–4809.
122. [122] Ge, J., Huang, Z.M., Xi, Q., Yu, R.Q., Jiang, J.H., Chu, X., A novel graphene oxide based fluorescent nanosensing strategy with hybridization chain reaction signal amplification for highly sensitive biothiol detection. Chem. Commun. 50 (2014), 11879–11882.
123. [123] Li, L., Feng, J., Liu, H., Li, Q., Tong, L., Tang, B., Two-color imaging of microRNA with enzyme-free signal amplification via hybridization chain reactions in living cells. Chem. Sci. 7 (2016), 1940–1945.
124. [124] Jang, H., Kim, Y.K., Kwon, H.M., Yeo, W.S., Kim, D.E., Min, D.-H., A graphene-based platform for the assay of duplex-DNA unwinding by helicase. Angew. Chem. Int. Ed. 49 (2010), 5703–5707.
125. [125] Lin, L., Liu, Y., Zhao, X., Li, J., Sensitive and rapid screening of T4 polynucleotide kinase activity and inhibition based on coupled exonuclease reaction and graphene oxide platform. Anal. Chem. 83 (2011), 8396–8402.
126. [126] Lee, J., Kim, Y.K., Min, D.-H., A new assay for endonuclease/methyltransferase activities based on graphene oxide. Anal. Chem. 83 (2011), 8906–8912.
127. [127] Park, J.S., Baek, A., Park, I.S., Jun, B.H., Kim, D.E., A graphene oxide-based platform for the assay of RNA synthesis by RNA polymerase using a fluorescent peptide nucleic acid probe. Chem. Commun. 49 (2013), 9203–9205.
128. [128] Lee, J., Min, D.-H., A simple fluorometric assay for DNA exonuclease activity based on graphene oxide. Analyst 137 (2012), 2024–2026.
129. [129] Zhou, D.M., Xi, Q., Liang, M.F., Chen, C.H., Tang, L.J., Jiang, J.H., Graphene oxide-hairpin probe nanocomposite as a homogeneous assay platform for DNA base excision repair screening, Biosens. Bioelectron 41 (2013), 359–365.
130. [130] Peng, L., Zhu, Z., Chen, Y., Han, D., Tan, W., An exonuclease III and graphene oxide-aided assay for DNA detection. Biosens. Bioelectron. 35 (2012), 475–478.
131. [131] Zhang, M., Yin, B.C., Wang, X.F., Ye, B.C., Interaction of peptides with graphene oxide and its application for real-time monitoring of protease activity. Chem. Commun. 47 (2011), 2399–2401.
132. [132] Zhou, J., Xu, X., Liu, W., Liu, X., Nie, Z., Qing, M., Nie, L., Yao, S., Graphene oxide-peptide nanocomplex as a versatile fluorescence probe of protein kinase activity based on phosphorylation protection against carboxypeptidase digestion. Anal. Chem. 85 (2013), 5746–5754.
133. [133] Wang, F., Liu, C., Fan, Y., Wang, Y., Li, Z., Robust detection of tyrosine phosphatase activity by coupling chymotrypsin-assisted selective peptide cleavage and a graphene oxide-based fluorescent platform. Chem. Commun. 50 (2014), 8161–8163.
134. [134] Li, J., Lu, C.H., Yao, Q.H., Zhang, X.L., Liu, J.J., Yang, H.H., Chen, G.N., A graphene oxide platform for energy transfer-based detection of protease activity. Biosens. Bioelectron. 26 (2011), 3894–3899.
135. [135] Song, E., Cheng, D., Song, Y., Jiang, M., Yu, J., Wang, Y., A graphene oxide-based FRET sensor for rapid and sensitive detection of matrix metalloproteinase 2 in human serum sample. Biosens. Bioelectron. 47 (2013), 445–450.
136. [136] Liu, Y., Li, Y., Liu, J., Deng, C., Zhang, X., High throughput enzyme inhibitor screening by functionalized magnetic carbonaceous microspheres and graphene oxide-based MALDI-TOF-MS. J. Am. Soc. Mass. Spectr. 22 (2011), 2188–2198.
137. [137] Lee, J., Kim, Y.K., Min, D.-H., Laser desorption/ionization mass spectrometric assay for phospholipase activity based on graphene oxide/carbon nanotube double-layer films. J. Am. Chem. Soc. 132 (2010), 14714–14717.
138. [138] Shan, C.S., Yang, H., Song, J., Han, D., Ivaska, A., Niu, L., Direct electrochemistry of glucose oxidase and biosensing for glucose based on graphene. Anal. Chem. 81 (2009), 2378–2382.
139. [139] Li, W., Wu, P., Zhang, H., Cai, C., Signal amplification of graphene oxide combining with restriction endonuclease for site-specific determination of DNA methylation and assay of methyltransferase activity. Anal. Chem. 84 (2012), 7583–7590.
140. [140] Wu, L., Wang, J., Feng, L., Ren, J., Wei, W., Qu, X., Label-free ultrasensitive detection of human telomerase activity using porphyrin-functionalized graphene and electrochemiluminescence technique. Adv. Mater. 24 (2012), 2447–2452.
141. [141] Zhang, L., Liang, J., Huang, Y., Ma, Y., Wang, Y., Chen, Y., Size-controlled synthesis of graphene oxide sheets on a large scale using chemical exfoliation. Carbon 47 (2009), 3365–3368.
142. [142] Luo, J., Cote, L.J., Tung, V.C., Tan, A.T.L., Goins, P.E., Wu, J., Huang, J., Graphene oxide nanocolloids. J. Am. Chem. Soc. 132 (2010), 17667–17669.
143. [143] Wang, X., Bai, H., Shi, G., Size fractionation of graphene oxide sheets by pH-assisted selective sedimentation. J. Am. Chem. Soc. 133 (2011), 6338–6342.
144. [144] Wang, Y., Li, Z., Hu, D., Lin, C.T., Li, J., Lin, Y., Aptamer/graphene oxide nanocomplex for in situ molecular probing in living cells. J. Am. Chem. Soc. 132 (2010), 9274–9276.
145. [145] Wang, H.B., Zhang, Q., Chu, X., Chen, T., Ge, J., Yu, R., Graphene oxide-peptide conjugate as an intracellular protease sensor for caspase-3 activation imaging in live cells. Angew. Chem. Int. Ed. 50 (2011), 7065–7069.
146. [146] Ryoo, S.R., Lee, J., Yeo, J., Na, H.K., Kim, Y.K., Jang, H., Lee, J.H., Han, S.W., Lee, Y., Kim, V.N., Min, D.-H., Quantitative and multiplexed microRNA sensing in living cells based on peptide nucleic acid and nano graphene oxide (PANGO). ACS Nano 7 (2013), 5882–5891.
147. [147] Kim, S., Ryoo, S.R., Na, H.K., Kim, Y.K., Choi, B.S., Lee, Y., Kim, D.E., Min, D.-H., Deoxyribozyme-loaded nano-graphene oxide for simultaneous sensing and silencing of the hepatitis C virus gene in liver cells. Chem. Commun. 49 (2013), 8241–8243.
148. [148] Wang, Y., Li, Z., Weber, T.J., Hu, D., Lin, C.T., Li, J., Lin, Y., In situ live cell sensing of multiple nucleotides exploiting DNA/RNA aptamers and graphene oxide nanosheets. Anal. Chem. 85 (2013), 6775–6782.
149. [149] Wang, Y., Tang, L., Li, Z., Lin, Y., Li, J., In situ simultaneous monitoring of ATP and GTP using a graphene oxide nanosheet–based sensing platform in living cells. Nat. Protoc. 9 (2014), 1944–1955.
150. [150] Liu, Z., Hu, C., Li, S., Zhang, W., Guo, Z., Rapid intracellular growth of gold nanostructures assisted by functionalized graphene oxide and its application for surface-enhanced Raman spectroscopy. Anal. Chem. 84 (2012), 10338–10344.
151. [151] Liu, Q.H., Wei, L., Wang, J., Peng, F., Luo, D., Cui, R., Niu, Y., Qin, X., Liu, Y., Sun, H., Yang, J., Li, Y., Cell imaging by graphene oxide based on surface enhanced Raman scattering. Nanoscale 4 (2012), 7084–7089.
152. [152] Jang, H., Ryoo, S.R., Kim, Y.K., Yoon, S., Kim, H., Han, S.W., Choi, B.S., Kim, D.E., Min, D.-H., Discovery of hepatitis C virus NS3 helicase inhibitors by a multiplexed, high-throughput helicase activity assay based on graphene oxide. Angew. Chem. Int. Ed. 52 (2013), 2340–2344.