Skip to main content
SpringerLink
Log in

Achievement and assessment of direct electron transfer of glucose oxidase in electrochemical biosensing using carbon nanotubes, graphene, and their nanocomposites

  • Review Article
  • Published:
Microchimica Acta Aims and scope Submit manuscript

Abstract

Carbon nanotubes, graphenes, and their hybridized composites with nanoparticles have been attempted to establish a direct electrical communication between the recognition biomolecule and its underlying electrode surface. This review (with 133 refs.) focuses on advances, strategies and technical challenges in the development of reagentless electrochemical biosensors for glucose with enhanced detection sensitivity, selectivity, and simplicity. Specifically, the review commences with a discussion of the relevance of direct electron transfer (DET) in biosensing together with the fundamental of electro-enzymology and kinetics. General aspects of glucose oxidase (GOx), the most popular enzyme with a flavin cofactor, are discussed in view of its historical and important role in the development of electrical biosensors for blood glucose. The next section assesses DET of GOx based on the Marcus theory and the Laviron formalism. The reorganizational energy of the Marcus model and the overpotential play an important role in reaction kinetics and affect the rate of electron transfer significantly. The presence of nanomaterials, particularly for graphene oxide, decreases the electron transfer distance between the enzyme redox center and the underlying electrode surface well beyond 15 Å. The improper Marcus-Hush-Chidsey integral is now simplified to estimate the rate of electron transfer with very good accuracy. Critiques, technical challenges, and future possibilities of glucose electrodes with respect to DET are also presented and discussed.

This review (with 133 refs.) focuses on advances, strategies and technical challenges in the development of reagentless electrochemical biosensors for glucose with enhanced detection sensitivity, selectivity, and simplicity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Marcus RA, Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811:265–322

    Article  CAS  Google Scholar 

  2. Page CC, Moser CC, Chen XX, Dutton PL (1999) Natural engineering principles of electron tunneling in biological oxidation-reduction. Nature 402:47–52

    Article  CAS  Google Scholar 

  3. Luong JHT, Male KB, Glennon JD (2008) Biosensor technology: technology push versus market pull. Biotechnol Adv 26(5):492–500

    Article  CAS  Google Scholar 

  4. Heller A, Hellman B (2008) Electrochemical glucose sensors and their applications in diabetes management. Chem Rev 108(7):2482–2505

    Article  CAS  Google Scholar 

  5. Clark LC Jr, Lyons C (1962) Electrode systems for continuous monitoring in cardiovascular surgery. Annals NY. Acad Sci 102:29–45

    Article  CAS  Google Scholar 

  6. Updike SJ, Hicks GP (1967) The enzyme electrode. Nature 214(5092):986–988

    Article  CAS  Google Scholar 

  7. Iijima S (1991) Helical microtubules of graphitic carbon. Nature 354:56–58

    Article  CAS  Google Scholar 

  8. Geim AK, Novoselov KS (2007) The rise of graphene. Nat Mater 6:183–191

    Article  CAS  Google Scholar 

  9. Guiseppi-Elie A, Lei C-H, Baughman RH (2002) Direct electron transfer of glucose oxidase on carbon nanotubes. Nanotechnology 13(5):559–564

    Article  CAS  Google Scholar 

  10. Shan CS, Yang HF, Song JF, Han DX, Ari-Ivaska A, Niu L (2009) Direct electrochemistry of glucose oxidase and biosensing for glucose based on graphene. Anal Chem 81(6):2378–2382

    Article  CAS  Google Scholar 

  11. Katz E, Sheeney-Haj-Ichia L, Willner I (2004) Electrical contacting of glucose oxidase in a redox-active rotaxane configuration. Angew Chem Int Ed 43:3292–3300

    Article  CAS  Google Scholar 

  12. Holland JT, Lau C, Brozik S, Atanassov P, Banta S (2011) Engineering of glucose oxidase for direct electron transfer via site-specific gold nanoparticle conjugation. J Am Chem Soc 133:19262–19265

    Article  CAS  Google Scholar 

  13. Bai Y-F, Xu T-B, Luong JHT, Cui H-F (2014) Direct electron transfer of glucose oxidase-boron doped diamond interface: a new solution for a classical problem. Anal Chem 86(10):4910–4918

    Article  CAS  Google Scholar 

  14. Wooten M, Karra S, Zhang M, Gorski W (2014) On the direct electron transfer, sensing, and enzyme activity in the glucose oxidase/carbon nanotubes system. Anal Chem 86(1):752–757

    Article  CAS  Google Scholar 

  15. Liang B, Guo X-H, Fang L, Hu Y-C, Yang G, Zhu Q, Wei J-W, Ye X-S (2015) Study of direct electron transfer and enzyme activity of glucose oxidase on graphene surface. Electrochem Commun 50:1–5

    Article  CAS  Google Scholar 

  16. Hale JM (1968) The potential-dependence and the upper limits of electrochemical rate constants. J Electroanal Chem 19:315–318

    Article  CAS  Google Scholar 

  17. Chidsey CED (1991) Free-energy and temperature-dependence of electron-transfer at the metal-electrolyte interface. Science 251:919–922

    Article  CAS  Google Scholar 

  18. Heering HA, Hirst J, Armstrong FA (1998) Interpreting the catalytic voltammetry of electroactive enzymes adsorbed on electrodes. J Phys Chem B 102:6889–690219

    Article  CAS  Google Scholar 

  19. Honeychurch MJ (1998) Effect of the interfacial potential distribution on the measurement of the rate constant for electron transfer between electrodes and redox adsorbates. Langmuir 14(21):6291–6296

  20. DeVault D (1984) Quantum mechanical tunneling in biological systems, 2nd edn. Cambridge Univ. Press, Cambridge

    Google Scholar 

  21. Moser CC, Duton PL (2003) Mechanism for electron transfer within and between proteins. Curr Opin Chem Biol 7:551–556

    Article  CAS  Google Scholar 

  22. Moser CC, Keske JM, Warncke K, Farid RS, Dutton PL (1992) Nature of biological electron transfer. Nature 355:796–802

    Article  CAS  Google Scholar 

  23. Farid RS, Moser CC, Dutton PL (1993) Electron transfer in proteins. Curr Opin Struct Biol 3:225–233

    Article  CAS  Google Scholar 

  24. Gray HB, Winkler JR (1996) Electron transfer in proteins. Annu Rev Biochem 65:537–561

    Article  CAS  Google Scholar 

  25. Wohlfahrt G, Witt S, Hendle J, Schomberg D, Kalisz HM, Hecht H-J (1999) 1.8 and 1.9 Å resolution structures of the Penicillium amagasakiense and Aspergillus niger glucose oxidases as a basis for modelling substrate complexes. Acta Crystallogr D Biol Crystallogr 55:969–977

  26. Langen R, Chang I-J, Germanas JP, Richards JH, Winkler JR, Gray HB (1995) Electron tunneling in proteins: coupling through a β strand. Science 268:1733–1735

    Article  CAS  Google Scholar 

  27. Muller D (1928) Studies on enzyme glucoseoxydase. Biochemist 199:136–170

    CAS  Google Scholar 

  28. Courjean O, Gao F, Mano N (2009) Deglycosylation of glucose oxidase for direct and efficient glucose electrooxidation on a glassy carbon electrode. Angew Chem Int Ed Eng 48(32):5897–5899

    Article  CAS  Google Scholar 

  29. Romanos MA, Scorer CA, Clare JJ (1992) Foreign gene expression in yeast: a review. Yeast 8(6):423–488

    Article  CAS  Google Scholar 

  30. Witt S, Singh M, Kalisz HM (1998) Structural and kinetic properties of nonglycosylated recombinant Penicillium amagasakiense glucose oxidase expressed in Escherichia coli. Appl Environ Microbiol 64(4):1405–1411

    CAS  Google Scholar 

  31. Nakamura K, Aizawa M, Miyawaki O (1988) Electro-enzymology: coenzyme regeneration. Sringer-Verlag, Berlin

    Book  Google Scholar 

  32. Gibson QH, Swoboda BE, Massey V (1964) Kinetics and mechanism of action of glucose oxidase. J Biol Chem 239(11):3927–3934

    CAS  Google Scholar 

  33. Tao Z-M, Raffel RA, Souid A-K, Goodisman J (2009) Kinetic studies on enzyme-catalyzed reactions: oxidation of glucose. Biophys J 96:2977–2988

    Article  CAS  Google Scholar 

  34. Laviron E (1979) General expression of the linear potential sweep voltammogram in the case of diffusionless electrochemical systems. J Electroanal Chem 101:19–28

    Article  CAS  Google Scholar 

  35. Xiao Y, Patolsky F, Katz E, Hainfeld JH, Willner I (2003) “Plugging into enzymes”: nanowiring of redox enzymes by gold nanoparticles. Science 299:1877–1881

    Article  CAS  Google Scholar 

  36. Kumar-Krishnan S, Hernandez-Rangel A, Pal U, Ceballos-Sanchez O, Flores-Ruiz FJ, Prokhorov E, Arias De Fuentes O, Esparza R, Meyyappan M (2016) Surface functionalized halloysite nanotubes decorated with silver nanoparticles for enzyme immobilization and biosensing. J Mater Chem B 4(15):2553–2560

    Article  CAS  Google Scholar 

  37. Hidaka H, Nowaki K, Muguruma H (2016) Mechanism of amperometric biosensor with electronic-type-controlled carbon nanotube. Japn J Appl Phys 55(3):03DF01

    Article  CAS  Google Scholar 

  38. Song Y, Lu X, Li Y, Guo Q, Chen S, Mao L, Hou H, Wang L (2016) Nitrogen-doped carbon nanotubes supported by macroporous carbon as an efficient enzymatic biosensing platform for glucose. Anal Chem 88(2):1371–1377

    Article  CAS  Google Scholar 

  39. Amatatongchai M, Sroysee W, Chairam S, Nacapricha D (2015) Amperometric flow injection analysis of glucose using immobilized glucose oxidase on nanocomposite carbon nanotubes-platinum nanoparticles carbon paste electrode. Talanta (in press). doi:10.1016/j.talanta.2015.11.072

  40. Hu H, Feng M, Zhan H (2015) A glucose biosensor based on partially unzipped carbon nanotubes. Talanta 141:66–72

    Article  CAS  Google Scholar 

  41. Liu Y, Dolidze TD, Singhal S, Khoshtariya DE, Wei J (2015) New evidence for a quasi-simultaneous proton-coupled two-electron transfer and direct wiring for glucose oxidase captured by the carbon nanotube-polymer matrix. J Phys Chem C 119(27):14900–14910

    Article  CAS  Google Scholar 

  42. Zhang W, Du Y, Wang ML (2015) On-chip highly sensitive saliva glucose sensing using multilayer films composed of single-walled carbon nanotubes, gold nanoparticles, and glucose oxidase. Sens BioSens Res 4:96–102

    Google Scholar 

  43. Zhao R, Liu X, Zhang J, Zhu J, Wong DKY (2015) Enhancing direct electron transfer of glucose oxidase using a gold nanoparticle titanate nanotube nanocomposite on a biosensor. Electrochim Acta 163:64–70

    Article  CAS  Google Scholar 

  44. Ayato Y, Suganuma T, Seta H, Yamagiwa K, Shiroishi H, Kuwano J (2015) Synthesis and application of carbon nanotubes to glucose biofuel cell with glucose oxidase and p-benzoquinone. J Electrochem Soc 162(14):F1482–F1486

    Article  CAS  Google Scholar 

  45. Chen H-C, Tu Y-M, Hou C-C, Lin Y-C, Chen C-H, Yang K-H (2015) Direct electron transfer of glucose oxidase and dual hydrogen peroxide and glucose detection based on water-dispersible carbon nanotubes derivative. Anal Chim Acta 867:83–91

    Article  CAS  Google Scholar 

  46. Muguruma H, Hoshino T, Nowaki K (2015) Electronically type-sorted carbon nanotube-based electrochemical biosensors with glucose oxidase and dehydrogenase. ACS Appl Mater Interfaces 7(1):584–592

    Article  CAS  Google Scholar 

  47. Hyun K, Han SW, Koh W-G, Kwon Y (2015) Direct electrochemistry of glucose oxidase immobilized on carbon nanotube for improving glucose sensing. Int J Hydrog Energy 40(5):2199–2206

    Article  CAS  Google Scholar 

  48. Tang W, Li L, Wu L, Gong J, Zeng X (2014) Glucose biosensor based on a glassy carbon electrode modified with polythionine and multiwalled carbon nanotubes. PLoS One 9(5):e95030

    Article  CAS  Google Scholar 

  49. Xu X, Yu J, Qian J, Cui D, Liu S (2014) Functionalization of nitrogen-doped carbon nanotubes by 1-pyrenebutyric acid and its application for biosensing. IEEE Sensors J 14(7):2341–2346

    Article  CAS  Google Scholar 

  50. Palanisamy S, Cheemalapati S, Chen S-M (2014) Amperometric glucose biosensor based on glucose oxidase dispersed in multiwalled carbon nanotubes/graphene oxide hybrid biocomposite. Mater Sci Eng C 34(1):207–213

    Article  CAS  Google Scholar 

  51. TermehYousefi A, Bagheri S, Kadri NA, Mahmood MR, Ikeda S (2014) Constant glucose biosensor based on vertically aligned carbon nanotube composites. Int J Electrochem Sci 10(5):4183–4192

    Google Scholar 

  52. Khodadadei F, Ghourchian H, Soltanieh M, Hosseinalipour M, Mortazavi Y (2014) Rapid and clean amine functionalization of carbon nanotubes in a dielectric barrier discharge reactor for biosensor development. Electrochim Acta 115:378–385

    Article  CAS  Google Scholar 

  53. Baghayeri M, Veisi H, Veisi H, Maleki B, Karimi-Maleh H, Beitollahi H (2014) Multi-walled carbon nanotubes decorated with palladium nanoparticles as a novel platform for electrocatalytic sensing applications. RSC Adv 4(91):49595–49604

    Article  CAS  Google Scholar 

  54. Kang X-H, Wang J, Wu H-X, Lin Y-H (2009) Glucose oxidase–graphene–chitosan modified electrode for direct electrochemistry and glucose sensing. Biosens Bioelectron 25(4):901–905

    Article  CAS  Google Scholar 

  55. Mascagni DBT, Miyazaki CM, da Cruz NC, de Moraes ML, Riul A Jr, Ferreira M (2016) Layer-by-layer assembly of functionalized reduced graphene oxide for direct electrochemistry and glucose detection. Mater Sci Eng C 68(1):739–745

    Article  CAS  Google Scholar 

  56. Rafighi P, Tavahodi M, Haghighi B (2016) Fabrication of a third-generation glucose biosensor using graphene-polyethyleneimine-gold nanoparticles hybrid. Sensors Actuators B Chem 232:454–461

    Article  CAS  Google Scholar 

  57. Li Z, Sheng L, Meng A, Xie C, Zhao K (2016) A glassy carbon electrode modified with a composite consisting of reduced graphene oxide, zinc oxide and silver nanoparticles in a chitosan matrix for studying the direct electron transfer of glucose oxidase and for enzymatic sensing of glucose. Microchim Acta 183(5):1625–1632

    Article  CAS  Google Scholar 

  58. Liu Y, Zhang X, He D, Ma F, Fu Q, Hu Y (2016) An amperometric glucose biosensor based on a MnO2/graphene composite modified electrode. RSC Adv 6(22):18654–18661

    Article  CAS  Google Scholar 

  59. Thirumalraj B, Palanisamy S, Chen S-M, Yang C-Y, Periakaruppan P, Lou B-S (2015) Direct electrochemistry of glucose oxidase and sensing of glucose at a glassy carbon electrode modified with a reduced graphene oxide/fullerene-C60 composite. RSC Adv 5(95):77651–77657

    Article  CAS  Google Scholar 

  60. Ye Y, Ding S, Ye Y, Xu H, Cao X, Liu S, Sun H (2015) Enzyme-based sensing of glucose using a glassy carbon electrode modified with a one-pot synthesized nanocomposite consisting of chitosan, reduced graphene oxide and gold nanoparticles. Microchim Acta 182(9–10):1783–1789

    Article  CAS  Google Scholar 

  61. Palanisamy S, Devasenathipathy R, Chen S-M, Ajmal Ali M, Karuppiah C, Balakumar V, Prakash P, Elshikh MS, Al-Hemaid FMA (2015) Direct electrochemistry of glucose oxidase at reduced graphene oxide and β-cyclodextrin composite modified electrode and application for glucose biosensing. Electroanalysis 27(10):2412–2420

    Article  CAS  Google Scholar 

  62. Xia L, Xia J, Wang Z (2015) Direct electrochemical deposition of polyaniline nanowire array on reduced graphene oxide modified graphite electrode for direct electron transfer biocatalysis. RSC Adv 5(113):93209–93214

    Article  CAS  Google Scholar 

  63. Shi Y, Li X, Ye M, Hu C, Shao H, Qu L (2015) An imperata cylindrical flowers-shaped porous graphene microelectrode for direct electrochemistry of glucose oxidase. J Electrochem Soc 162(7):B138–B144

    Article  CAS  Google Scholar 

  64. Yang Z, Cao Y, Li J, Jian Z, Zhang Y, Hu X (2015) Platinum nanoparticles functionalized nitrogen doped graphene platform for sensitive electrochemical glucose biosensing. Anal Chim Acta 871:35–42

    Article  CAS  Google Scholar 

  65. Mani V, Devasenathipathy R, Chen S-M, Subramani B, Govindasamy M (2015) A novel glucose biosensor at glucose oxidase immobilized graphene and bismuth nanocomposite film modified electrode. Int J Electrochem Sci 10(1):691–700

    Google Scholar 

  66. Guo J, Zhang T, Hu C, Fu L (2015) A three-dimensional nitrogen-doped graphene structure: a highly efficient carrier of enzymes for biosensors. Nanoscale 7(4):1290–1295

    Article  CAS  Google Scholar 

  67. Bai X, Shiu K-K (2015) Spontaneous deposition of Prussian blue on reduced graphene oxide-gold nanoparticles composites for the fabrication of electrochemical biosensors. Electroanalysis 27(1):74–83

    Article  CAS  Google Scholar 

  68. Sehat AA, Khodadadi AA, Shemirani F, Mortazavi Y (2015) Fast immobilization of glucose oxidase on graphene oxide for highly sensitive glucose biosensor fabrication. Int J Electrochem Sci 10(1):272–286

    Google Scholar 

  69. Mani V, Devasenathipathy R, Chen S-M, Huang S-T, Vasantha VS (2014) Immobilization of glucose oxidase on graphene and cobalt phthalocyanine composite and its application for the determination of glucose. Enzym Microb Technol 66:60–66

    Article  CAS  Google Scholar 

  70. Martins MVA, Pereira AR, Luz RAS, Iost RM, Crespilho FN (2014) Evidence of short-range electron transfer of a redox enzyme on graphene oxide electrodes. Phys Chem Chem Phys 16(33):17426–17436

  71. Karuppiah C, Palanisamy S, Chen S-M, Veeramani V, Periakaruppan P (2014) A novel enzymatic glucose biosensor and sensitive non-enzymatic hydrogen peroxide sensor based on graphene and cobalt oxide nanoparticles composite modified glassy carbon electrode. Sensors Actuators B Chem 196:450–456

    Article  CAS  Google Scholar 

  72. Bai X, Shiu K-K (2014) Investigation of the optimal weight contents of reduced graphene oxide-gold nanoparticles composites and theirs application in electrochemical biosensors. J Electroanal Chem /721:84–91

    Article  CAS  Google Scholar 

  73. Piao Y, Han DJ, Seo TS (2014) Highly conductive graphite nanoparticle based enzyme biosensor for electrochemical glucose detection. Sensors Actuators B Chem 194:454–459

    Article  CAS  Google Scholar 

  74. Wang Y, Li H, Kong J (2014) Facile preparation of mesocellular graphene foam for direct glucose oxidase electrochemistry and sensitive glucose sensing. Sensors Actuators B Chem 193:708–714

    Article  CAS  Google Scholar 

  75. Zhang X, Liao Q, Chu M, Liu S, Zhang Y (2014) Structure effect on graphene-modified enzyme electrode glucose sensors. Biosens Bioelectron 52:281–287

    Article  CAS  Google Scholar 

  76. Palanisamy S, Karuppiah C, Chen S-M (2014) Direct electrochemistry and electrocatalysis of glucose oxidase immobilized on reduced graphene oxide and silver nanoparticles nanocomposite modified electrode. Colloids Surf B: Biointerfaces 114:164–169

    Article  CAS  Google Scholar 

  77. Vilian ATE, Chen S-M, Ali MA, Al-Hemaid FMA (2014) Direct electrochemistry of glucose oxidase immobilized on ZrO2 nanoparticles-decorated reduced graphene oxide sheets for a glucose biosensor. RSC Adv 4(57):30358–30367

    Article  CAS  Google Scholar 

  78. Leng J, Wang W-M, Lu L-M, Bai L, Qiu X-L (2014) DNA-templated synthesis of PtAu bimetallic nanoparticle/graphene nanocomposites and their application in glucose biosensor. Nanoscale Res Lett 9(1):1–8

    Article  CAS  Google Scholar 

  79. Yu L, Wu H, Wu B, Wang Z, Cao H, Fu C, Jia N (2014) Magnetic Fe3O4-reduced graphene oxide nanocomposites-based electrochemical biosensing. Nano-Micro Lett 6(3):258–267

    Article  Google Scholar 

  80. Terse-Thakoor T, Komori K, Ramnani P, Lee I, Mulchandani A (2015) Electrochemically functionalized seamless three-dimensional graphene-carbon nanotube hybrid for direct electron transfer of glucose oxidase and bioelectrocatalysis. Langmuir 31(47):13054–13061

    Article  CAS  Google Scholar 

  81. Devasenathipathy R, Mani V, Chen S-M, Huang S-T, Huang T-T, Lin C-M, Hwa K-Y, Chen T-Y, Chen B-J (2015) Glucose biosensor based on glucose oxidase immobilized at gold nanoparticles decorated graphene-carbon nanotubes. Enzym Microb Technol 78:40–45

    Article  CAS  Google Scholar 

  82. Yu Y, Chen Z, He S, Zhang B, Li X, Yao M (2014) Direct electron transfer of glucose oxidase and biosensing for glucose based on PDDA-capped gold nanoparticle modified graphene/multi-walled carbon nanotubes electrode. Biosens Bioelectron 52:147–152

    Article  CAS  Google Scholar 

  83. Eskandari K, Kamali M (2014) The investigation of electrochemical parameter for glucose oxidase on graphene, carbon nanotube and gold nanoparticle. Minerva Biotechnologica 26(3):209–214

    Google Scholar 

  84. Palanisamy S, Cheemalapati S, Chen S-M (2014) Amperometric glucose biosensor based on glucose oxidase dispersed in multiwalled carbon nanotubes/graphene oxide hybrid biocomposite. Mater Sci Eng C Mater Biol Appl 34:207–213

    Article  CAS  Google Scholar 

  85. Grosse W, Champavert J, Gambhir S, Wallace GG, Moulton SE (2013) Aqueous dispersions of reduced graphene oxide and multi wall carbon nanotubes for enhanced glucose oxidase bioelectrode performance. Carbon 61:467–475

    Article  CAS  Google Scholar 

  86. Zheng D, Vashist SK, Dykas MM, Saha S, Al-Rubeaan K, Lam E, Luong JHT, Sheu F-S (2013) Materials 6:1011–1027

    Article  CAS  Google Scholar 

  87. Mani V, Devadas B, Chen S-M (2013) Direct electrochemistry of glucose oxidase at electrochemically reduced graphene oxide-multiwalled carbon nanotubes hybrid material modified electrode for glucose biosensor. Biosens Bioelectron 41:309–315

    Article  CAS  Google Scholar 

  88. Chen J-L, Zheng X-L, Miao F-J, Zhang J-N, Cui X-Q, Zheng W-T (2012) Engineering graphene/carbon nanotube hybrid for direct electron transfer of glucose oxidase and glucose biosensor. J Appl Electrochem 42(10):875–881

    Article  CAS  Google Scholar 

  89. Laborda E, Henstridge MC, Batchelor-McAuley C, Compton RG (2013) Asymmetric Marcus-Hush theory for voltammetry. Chem Soc Rev 42:4894–4905

    Article  CAS  Google Scholar 

  90. Oldham KB, Myland JC (2011) On the evaluation and analysis of the Marcus-Hush-Chidsey integral. J Electroanal Chem 655(1):65–72

    Article  CAS  Google Scholar 

  91. Lieber CM, Karas JL, Mayo SL, Albin M, Gray HB (1987) Long range electron transfer in proteins. XXI. Design of enzymes and enzyme models. In: Proceedings of the Robert A. Welch Foundation Conferences on Chemical Research; The Welch Foundation, Houston, pp 9–24.

  92. Heller A (1990) Electrical wiring of redox enzymes. Acc Chem Res 23(5):128–134

  93. Weber K, Creager SE (1994) Voltammetry of redox-active groups irreversibly adsorbed onto electrodes. Treatment using the Marcus relation between rate and overpotential. Anal Chem 66:3164–3172

    Article  CAS  Google Scholar 

  94. Wei H-Z, Omanovic S (2008) Interaction of flavin adenine dinucleotide (FAD) with a glassy carbon electrode surface. Chem Biodivers 5:1622–1639

  95. Bai P, Bazant MZ (2014) Charge transfer kinetics at the solid–solid interface in porous electrodes. Nat Commun 5:3585

    Google Scholar 

  96. Hupp JT, Weaver MJ (1984) The driving-force dependence of rate parameters for electron transfer: further comparisons between theory and experiment. J Phys Chem 88:6128–6135

    Article  CAS  Google Scholar 

  97. Gorton L, Johansson G (1980) Cyclic voltammetry of FAD adsorbed on graphite, glassy carbon, platinum and gold electrodes. J Electrochem Chem 113:151–158

    Article  CAS  Google Scholar 

  98. McGarvey C, Beck S, Quach S, Birss VL, Elzanowska H (1998) Adsorbed lumiflavin at mercury-electrode surfaces. J Electroanal Chem 456:71–82

    Article  CAS  Google Scholar 

  99. Heller A (1992) Electrical connection of enzyme redox centers to electrodes. J Phys Chem 96(9):3579–3587

    Article  CAS  Google Scholar 

  100. Szucs A, Hitchens GD, Bockris JOM (1989) On the adsorption of glucose-oxidase at a gold electrode. J Electrochem Soc 136:3748–3755

    Article  CAS  Google Scholar 

  101. Benavidez TE, Torrente D, Marucho M, Garcia CD (2014) Adsorption and catalytic activity of glucose oxidase accumulated on OTCE upon the application of external potential. J Colloid Interface Sci 435:164–170

    Article  CAS  Google Scholar 

  102. Zhang J-D, Chi Q-J, Dong S-J, Wang E (1996) Orientation and electrocatalysis of riboflavin adsorbed on carbon substrate surfaces. J Chem Soc Faraday Trans 92:1913–1920

    Article  CAS  Google Scholar 

  103. Willner I, Riklin A, Shoham B, Rivenzon D, Katz E (1993) Development of novel enzyme-electrodes: multilayer arrays immobilized onto self-assembled monolayers on electrodes. Adv Mater 5:912–915

    Article  CAS  Google Scholar 

  104. Gregg BA, Heller A (1990) Cross- linked redox gels containing glucose oxidase for amperometric biosensor applications. Anal Chem 62(3):258–263

    Article  CAS  Google Scholar 

  105. Heller A, Feldman B (2010) Electrochemistry in diabetes management. Acc Chem Res 43(7):963–973

    Article  CAS  Google Scholar 

  106. Mano N, Mao F, Heller A (2004) Electro- oxidation of glucose at an increased current density at a reducing potential. Chem Commun 18:2116–2117

    Article  CAS  Google Scholar 

  107. Pishko MV, Michael AC, Heller A (1991) Amperometric glucose microelectrodes prepared through immobilization of glucose oxidase in redox hydrogels. Anal Chem 63(20):2268–2272

    Article  CAS  Google Scholar 

  108. Csoeregi E, Schmidtke DW, Heller A (1995) Design and optimization of a selective subcutaneously implantable glucose electrode based on ‘wired’ glucose oxidase. Anal Chem 67(7):1240–1244

    Article  CAS  Google Scholar 

  109. Heller A (1991) Electrical wiring of redox enzymes. In: Pelizzetti E, Schiavello M (eds) Photochemical conversion and storage of solar energy. Springer, pp 67–87

  110. Gooding JJ, Lai LMH, Goon IY (2009) Nanostructured electrodes with unique properties for biological and other applications. In: Alkire RC, Kolb DM, Lipkowski J, Ross PN (eds) Chemically Modified Electrodes. Advances in Electrochemical Science and Engineering, vol. 11. Wiley-VCH, Weinheim, pp 1–56

  111. Salimi A, Sharifi E, Noorbakhsh A, Saied Soltanian S (2007) Immobilization of glucose oxidase on electrodeposited nickel oxide nanoparticles: direct electron transfer and electrocatalytic activity. Biosens Bioelectron 22:3146–3153

    Article  CAS  Google Scholar 

  112. Badia A, Carlini R, Fernandez A, Battaglini F, Mikkelsen SR, English AM (1993) Intramolecular electron-transfer rates in ferrocene-derivatized glucose oxidase. J Am Chem Soc 115:7053–7060

    Article  CAS  Google Scholar 

  113. Sharma V, Kumar V, Archana G, Kumar GN (2005) Substrate specificity of glucose dehydrogenase (GDH) of Enterobacter asburiae PSI3 and rock phosphate solubilization with GDH substrates as C sources. Can J Microbiol 51(6):477–482

    Article  CAS  Google Scholar 

  114. U.S. Food and Drug Administration (2011) FDA public health notification: potentially fatal errors with GDH-PQQ glucose monitoring technology. http://www.fda.gov/MedicalDevices/Safety/AlertsandNotices/PublicHealthNotifications/ucm176992.htm. Accessed 27 May 2011

  115. Hamamatsu N, Suzumura A, Nomiya Y, Sato M, Aita T, Nakajima M, Husimi Y, Shibanaka Y (2006) Modified substrate specificity of pyrroloquinoline quinone glucose dehydrogenase by biased mutation assembling with optimized amino acid substitution. Appl Microbiol Biotechnol 73(3):607–617

    Article  CAS  Google Scholar 

  116. Igarashi S, Sode K (2003) Stabilization of quaternary structure of watersoluble quinoprotein glucose dehydrogenase. Mol Biotechnol 24(2):97–104

    Article  CAS  Google Scholar 

  117. Halamkova L, Halamek J, Bocharova V, Szczupak A, Alfonta L, Evgeny E (2012) Implanted biofuel cell operating in a living snail. J Am Chem Soc 134:5040–5043

    Article  CAS  Google Scholar 

  118. Koushanpour A, Guz N, Gamella M, Katz E (2016) Biofuel cell based on carbon fiber electrodes functionalized with graphene nanosheets. ECS J Solid State Sci Technol 5(8):2162–8769

    Google Scholar 

  119. Yamaoka H, Yamashita Y, Ferri S, Sode K (2008) Site directed mutagenesis studies of FAD-dependent glucose dehydrogenase catalytic subunit of Burkholderia cepacia. Biotechnol Lett 30(11):1967–1972

    Article  CAS  Google Scholar 

  120. Janssen W, Harff G, Caers M, Schellekens A (1998) Positive interference of icodextrin metabolites in some enzymatic glucose methods. Clin Chem 44(11):2379–2380

    CAS  Google Scholar 

  121. Gooding JJ, Wibowo R, Liu J-Q, Yang W-R, Losic D, Orbons S, Mearns FJ, Shapter JG, Hibbert DB (2003) Protein electrochemistry using aligned carbon nanotube arrays. J Am Chem Soc 125:9006–9007

    Article  CAS  Google Scholar 

  122. Migliore A, Nitzan A (2011) Nonlinear charge transport in redox molecular junctions: a Marcus perspective. ACS Nano 5(8):6669–6685

    Article  CAS  Google Scholar 

  123. Migliore A, Nitzan A (2012) On the evaluation of the Marcus-Hush-Chidsey integral. J Electroanal Chem 671:99–101

    Article  CAS  Google Scholar 

  124. Zeng Z, Smith R, Bai P, Bazant M (2014) Simple formula for Marcus-Hush-Chidsey kinetics. J Electroanal Chem 735:77–83

    Article  CAS  Google Scholar 

  125. Male KB, Hrapovic S, Santini JM, Luong JHT (2007) Biosensor for arsenite using arsenite oxidase and multiwalled carbon nanotube modified electrodes. Anal Chem 79(20):7831–7837

    Article  CAS  Google Scholar 

  126. Rochette JF, Sacher E, Meunier M, Luong JHT (2005) A mediatorless biosensor for putrescine using multiwalled carbon nanotubes. Anal Biochem 336(2):305–311

    Article  CAS  Google Scholar 

  127. Luz RAS, Pereira AR, de Souza JCP, Sales FCPF, Crespilho FN (2014) Enzyme biofuel cells: thermodynamics, kinetics and challenges in applicability. ChemElectroChem 1(1):1–18

    Article  Google Scholar 

  128. Vashist SK, Luong JHT (2015) Recent advances in electrochemical biosensing schemes using graphene and graphene-based nanocomposites. Carbon 84:519–550

    Article  CAS  Google Scholar 

  129. Vashist SK, Zheng D, Al-Rubeaan K, Luong JHT, Sheu F-S (2011) Advances in carbon nanotube based electrochemical sensors for bioanalytical applications. Biotechnol Adv 29(2):169–188

    Article  CAS  Google Scholar 

  130. Eckermann AL, Feld DJ, Shaw JA, Meade TJ (2010) Electrochemistry of redox-active self-assembled monolayers. Coord Chem Rev 254:1769–1802

    Article  CAS  Google Scholar 

  131. Leger C, Bertrand P (2008) Direct electrochemistry of redox enzymes as a tool for mechanistic studies. Chem Rev 108:2379–2438

    Article  CAS  Google Scholar 

  132. Roth JP, Klinman JP (2003) Catalysis of electron transfer during activation of O2 by the flavoprotein glucose oxidase. Proc Natl Acad Sci 100(1):62–67

    Article  CAS  Google Scholar 

  133. Brinkley DW, Roth JP (2005) Determination of a large reorganization energy barrier for hydride abstraction by glucose oxidase. J Am Chem Soc 127:15720–15721

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Innovative Chromatography Group, Irish Separation Science Cluster (ISSC), Department of Chemistry and Analytical, Biological Chemistry Research Facility (ABCRF), University College Cork, Cork, Ireland

    John H.T. Luong & Jeremy D. Glennon

  2. Bar-Ilan Institute for Nanotechnology and Advanced Materials, Department of Chemistry, Bar-Ilan University, 5290002, Ramat-Gan, Israel

    Aharon Gedanken

  3. Vallo Med Health Care GmbH, Bahnhofstr. 200, 44579, Castrop-Rauxel, Germany

    Sandeep K. Vashist

Authors
  1. John H.T. Luong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeremy D. Glennon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aharon Gedanken
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sandeep K. Vashist
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John H.T. Luong.

Ethics declarations

The author(s) declare that they have no competing interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luong, J.H., Glennon, J.D., Gedanken, A. et al. Achievement and assessment of direct electron transfer of glucose oxidase in electrochemical biosensing using carbon nanotubes, graphene, and their nanocomposites. Microchim Acta 184, 369–388 (2017). https://doi.org/10.1007/s00604-016-2049-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00604-016-2049-3

Keywords

Search

Navigation