Application of the Enzymatic Electrochemical Biosensors for Monitoring Non-Competitive Inhibition of Enzyme Activity by Heavy Metals
Language English Country Switzerland Media electronic
Document type Journal Article
Grant support
LQ1601
Ministerstvo Školství, Mládeže a Tělovýchovy
PubMed
31277338
PubMed Central
PMC6651500
DOI
10.3390/s19132939
PII: s19132939
Knihovny.cz E-resources
- Keywords
- amperometric biosensor, glucose oxidase, heavy metals, non-competitive inhibition,
- MeSH
- Aspergillus niger enzymology MeSH
- Biosensing Techniques * MeSH
- Electrochemical Techniques instrumentation methods MeSH
- Electrodes MeSH
- Glucose analysis MeSH
- Glucose Oxidase antagonists & inhibitors metabolism MeSH
- Enzyme Inhibitors pharmacology toxicity MeSH
- Calibration MeSH
- Limit of Detection MeSH
- Nanotubes, Carbon MeSH
- Hydrogen Peroxide analysis MeSH
- Ruthenium Compounds chemistry MeSH
- Metals, Heavy pharmacology toxicity MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Glucose MeSH
- Glucose Oxidase MeSH
- Enzyme Inhibitors MeSH
- Nanotubes, Carbon MeSH
- Hydrogen Peroxide MeSH
- ruthenium tetraoxide MeSH Browser
- Ruthenium Compounds MeSH
- Metals, Heavy MeSH
The inhibition effect of the selected heavy metals (Ag+, Cd2+, Cu2+, and Hg2+) on glucose oxidase (GOx) enzyme from Aspergillus niger (EC 1.1.3.4.) was studied using a new amperometric biosensor with an electrochemical transducer based on a glassy carbon electrode (GCE) covered with a thin layer of multi-wall carbon nanotubes (MWCNTs) incorporated with ruthenium(IV) oxide as a redox mediator. Direct adsorption of multi-wall carbon nanotubes (MWCNTs) and subsequent covering with Nafion® layer was used for immobilization of GOx. The analytical figures of merit of the developed glucose (Glc) biosensor are sufficient for determination of Glc in body fluids in clinical analysis. From all tested heavy metals, mercury(II) has the highest inhibition effect. However, it is necessary to remember that cadmium and silver ions also significantly inhibit the catalytic activity of GOx. Therefore, the development of GOx biosensors for selective indirect determination of each heavy metal still represents a challenge in the field of bioelectroanalysis. It can be concluded that amperometric biosensors, differing in the utilized enzyme, could find their application in the toxicity studies of various poisons.
See more in PubMed
Mäntsälä P., Niemi J. Enzymes: The biological catalysts of life. Physiol. Maintanance. 2009;2:1–22.
Woodward J.D., Trompetter I., Sewell B.T., Piotrowski M. Substrate specificity of plant nitrilase complexes is affected by their helical twist. Commun. Biol. 2018;1:186. doi: 10.1038/s42003-018-0186-4. PubMed DOI PMC
Schowen R.L. How an enzyme surmounts the activation energy barrier. Proc. Natl. Acad. Sci. USA. 2003;100:11931–11932. doi: 10.1073/pnas.2235806100. PubMed DOI PMC
Robinson P.K. Enzymes: Principles and biotechnological applications. Essays Biochem. 2015;59:1–41. doi: 10.1042/bse0590001. PubMed DOI PMC
Aledo J.C., Lobo C., del Valle A.E. Energy diagrams for enzyme-catalyzed reactions: Concepts and misconcepts. Biochem. Mol. Biol. Educ. 2003;31:234–236. doi: 10.1002/bmb.2003.494031040240. DOI
Pearce L.L., Bominaar E.L., Hill B.C., Peterson J. Reversal of cyanide inhibition of cytochrome c oxidase by the auxiliary substrate nitric oxide an endogenous antidote to cyanide poisoning? J. Biol. Chem. 2003;278:52139–52145. doi: 10.1074/jbc.M310359200. PubMed DOI
Mizrahi L., Achituv Y. Effect of heavy metals ions on enzyme activity in the mediterranean mussel, donax trunculus. Bull. Environ. Contam. Toxicol. 1989;42:854–859. doi: 10.1007/BF01701626. PubMed DOI
Viarengo A. Biochemical effects of trace metals. Mar. Pollut. Bull. 1985;16:153–158. doi: 10.1016/0025-326X(85)90006-2. DOI
Hodson P.V. The effect of metal metabolism on uptake, disposition and toxicity in fish. Aquat. Toxicol. 1988;11:3–18. doi: 10.1016/0166-445X(88)90003-3. DOI
Martin T., Holdich D. The acute lethal toxicity of heavy metals to peracarid crustaceans (with particular reference to fresh-water asellids and gammarids) Water Res. 1986;20:1137–1147. doi: 10.1016/0043-1354(86)90060-6. DOI
Lu H.P., Xun L., Xie X.S. Single-molecule enzymatic dynamics. Science. 1998;282:1877–1882. doi: 10.1126/science.282.5395.1877. PubMed DOI
Blackmond D.G. Reaction progress kinetic analysis: A powerful methodology for mechanistic studies of complex catalytic reactions. Angew. Chem. Int. Ed. 2005;44:4302–4320. doi: 10.1002/anie.200462544. PubMed DOI
Kirk O., Borchert T.V., Fuglsang C.C. Industrial enzyme applications. Curr. Opin. Biotechnol. 2002;13:345–351. doi: 10.1016/S0958-1669(02)00328-2. PubMed DOI
Hasan F., Shah A.A., Hameed A. Industrial applications of microbial lipases. Enzym. Microb. Technol. 2006;39:235–251. doi: 10.1016/j.enzmictec.2005.10.016. DOI
Vellard M. The enzyme as drug: Application of enzymes as pharmaceuticals. Curr. Opin. Biotechnol. 2003;14:444–450. doi: 10.1016/S0958-1669(03)00092-2. PubMed DOI
Bothner B., Chavez R., Wei J., Strupp C., Phung Q., Schneemann A., Siuzdak G. Monitoring enzyme catalysis with mass spectrometry. J. Biol. Chem. 2000;275:13455–13459. doi: 10.1074/jbc.275.18.13455. PubMed DOI
Cheng S., Wu Q., Xiao H., Chen H. Online monitoring of enzymatic reactions using time-resolved desorption electrospray ionization mass spectrometry. Anal. Chem. 2017;89:2338–2344. doi: 10.1021/acs.analchem.6b03975. PubMed DOI
Xu Z., Yao S., Wei Y., Zhou J., Zhang L., Wang C., Guo Y. Monitoring enzyme reaction and screening of inhibitors of acetylcholinesterase by quantitative matrix-assisted laser desorption/ionization fourier transform mass spectrometry. J. Am. Soc. Mass Spectrom. 2008;19:1849–1855. doi: 10.1016/j.jasms.2008.07.025. PubMed DOI
Westley C., Fisk H., Xu Y., Hollywood K.A., Carnell A.J., Micklefield J., Turner N.J., Goodacre R. Real-time monitoring of enzyme-catalysed reactions using deep UV resonance raman spectroscopy. Chem. A Eur. J. 2017;23:6983–6987. doi: 10.1002/chem.201701388. PubMed DOI PMC
Miller R.B., Karn R.C. A rapid spectrophotometric method for the determination of esterase activity. J. Biochem. Biophys. Methods. 1980;3:345–354. doi: 10.1016/0165-022X(80)90043-3. PubMed DOI
German N., Voronovic J., Ramanavicius A., Ramanaviciene A. Gold nanoparticles and polypyrrole for glucose biosensor design. Procedia Eng. 2012;47:482–485. doi: 10.1016/j.proeng.2012.09.189. DOI
Kim J.-H., Lee D., Bae T.-S., Lee Y.-S. The electrochemical enzymatic glucose biosensor based on mesoporous carbon fibers activated by potassium carbonate. J. Ind. Eng. Chem. 2015;25:192–198. doi: 10.1016/j.jiec.2014.10.034. DOI
Kotzian P., Brázdilová P., Kalcher K., Vytřas K. Determination of hydrogen peroxide, glucose and hypoxanthine using (bio) sensors based on ruthenium dioxide-modified screen-printed electrodes. Anal. Lett. 2005;38:1099–1113. doi: 10.1081/AL-200057205. DOI
Kotzian P., Brázdilová P., Řezková S., Kalcher K., Vytřas K. Amperometric glucose biosensor based on rhodium dioxide-modified carbon ink. Electroanal. Int. J. Devoted Fundam. Pract. Asp. Electroanal. 2006;18:1499–1504. doi: 10.1002/elan.200503549. DOI
Wei A., Sun X.W., Wang J., Lei Y., Cai X., Li C.M., Dong Z., Huang W. Enzymatic glucose biosensor based on ZnO nanorod array grown by hydrothermal decomposition. Appl. Phys. Lett. 2006;89:123902. doi: 10.1063/1.2356307. DOI
Weng W.-H., Wang C.-W., Pang S.-T., Pan T.-M. Enzymatic glucose biosensor based on TbYxOy electrolyte-insulator-semiconductor. J. Electrochem. Soc. 2016;163:B445–B452. doi: 10.1149/2.0641608jes. DOI
Ashrafi A.M., Koudelkova Z., Sedlackova E., Richtera L., Adam V. Electrochemical sensors and biosensors for determination of mercury ions. J. Electrochem. Soc. 2018;165:B824–B834. doi: 10.1149/2.0381816jes. DOI
Wang J. Stripping analysis at bismuth electrodes: A review. Electroanal. Int. J. Devot. Fundam. Pract. Asp. Electroanal. 2005;17:1341–1346. doi: 10.1002/elan.200403270. DOI
Liang M., Jin F., Liu R., Su R., Qi W., Yu Y., Wang L., He Z. Enhanced electrochemical detection performance of multiwall carbon nanotubes functionalized by aspartame. J. Mater. Sci. 2013;48:5624–5632. doi: 10.1007/s10853-013-7357-y. DOI
Scheller F.W., Schubert F., Neumann B., Pfeiffer D., Hintsche R., Dransfeld I., Wollenberger U., Renneberg R., Warsinke A., Johansson G. Second generation biosensors. Biosens. Bioelectron. 1991;6:245–253. doi: 10.1016/0956-5663(91)80010-U. PubMed DOI
Peigney A., Laurent C., Flahaut E., Bacsa R., Rousset A. Specific surface area of carbon nanotubes and bundles of carbon nanotubes. Carbon. 2001;39:507–514. doi: 10.1016/S0008-6223(00)00155-X. DOI
Sýs M., Žabčíková S., Červenka L., Vytřas K. Comparison of adsorptive with extractive stripping voltammetry in electrochemical determination of retinol. Potr. SJF Sci. 2017;11:96–105. doi: 10.5219/713. DOI
Nguyen H., Park J., Kang S., Kim M. Surface plasmon resonance: A versatile technique for biosensor applications. Sensors. 2015;15:10481–10510. doi: 10.3390/s150510481. PubMed DOI PMC
Wolfschmidt H., Baier C., Gsell S., Fischer M., Schreck M., Stimming U. STM, SECPM, AFM and electrochemistry on single crystalline surfaces. Materials. 2010;3:4196–4213. doi: 10.3390/ma3084196. PubMed DOI PMC
Vang R.T., Lauritsen J.V., Laegsgaard E., Besenbacher F. Scanning tunneling microscopy as a tool to study catalytically relevant model systems. Chem. Soc. Rev. 2008;37:2191–2203. doi: 10.1039/b800307f. PubMed DOI
Bard A.J., Fan F.R.F., Kwak J., Lev O. Scanning electrochemical microscopy. Introduction and principles. Anal. Chem. 1989;61:132–138. doi: 10.1021/ac00177a011. DOI
Vahabi S., Salman B.N., Javanmard A. Atomic force microscopy application in biological research: A review study. Iran. J. Med Sci. 2013;38:76. PubMed PMC
Sýs M., Pekec B., Kalcher K., Vytřas K. Amperometric enzyme carbon paste-based biosensor for quantification of hydroquinone and polyphenolic antioxidant capacity. Int. J. Electrochem. Sci. 2013;8:9030–9040.
Pan B., Xing B. Adsorption mechanisms of organic chemicals on carbon nanotubes. Environ. Sci. Technol. 2008;42:9005–9013. doi: 10.1021/es801777n. PubMed DOI
Rasouli H., Naji L., Hosseini M.G. Electrochemical and electromechanical behavior of Nafion-based soft actuators with PPy/CB/MWCNT nanocomposite electrodes. RSC Adv. 2017;7:3190–3203. doi: 10.1039/C6RA25771B. DOI
Bhalla N., Jolly P., Formisano N., Estrela P. Introduction to biosensors. Essays Biochem. 2016;60:1–8. doi: 10.1042/EBC20150001. PubMed DOI PMC
Anojčić J., Guzsvány V., Vajdle O., Madarász D., Rónavári A., Kónya Z., Kalcher K. Hydrodynamic chronoamperometric determination of hydrogen peroxide using carbon paste electrodes coated by multiwalled carbon nanotubes decorated with MnO2 or Pt particles. Sens. Actuators B: Chem. 2016;233:83–92. doi: 10.1016/j.snb.2016.04.005. DOI
Cueni-Villoz N., Devigili A., Delodder F., Cianferoni S., Feihl F., Rossetti A.O., Eggimann P., Vincent J.-L., Taccone F.S., Oddo M. Increased blood glucose variability during therapeutic hypothermia and outcome after cardiac arrest. Crit. Care Med. 2011;39:2225–2231. doi: 10.1097/CCM.0b013e31822572c9. PubMed DOI
Blanco A., Blanco G. Chapter 8—Enzymes. In: Blanco A., Blanco G., editors. Medical Biochemistry. Academic Press; Cambridge, MA, USA: 2017. pp. 153–175.
Ghica M.E., Brett C.M. Glucose oxidase inhibition in poly (neutral red) mediated enzyme biosensors for heavy metal determination. Microchim. Acta. 2008;163:185–193. doi: 10.1007/s00604-008-0018-1. DOI
Malitesta C., Guascito M. Heavy metal determination by biosensors based on enzyme immobilised by electropolymerisation. Biosens. Bioelectron. 2005;20:1643–1647. doi: 10.1016/j.bios.2004.08.003. PubMed DOI
Mugheri A.Q., Tahira A., Sherazi S.T.H., Abro M.I., Willander M., Ibupoto Z.H. An amperometric indirect determination of heavy metal ions through inhibition of glucose oxidase immobilized on cobalt oxide nanostructures. Sens. Lett. 2016;14:1178–1186. doi: 10.1166/sl.2016.3752. DOI
Varjovi M.J., Sabzi R.E., Borghei S.M. Determination of heavy metal ions by an amperometric biosensor based on glucose oxidase immobilized onto single-walled carbon nanotubes/Nile blue nanocomposite. J. Iran. Chem. Soc. 2018;15:1765–1774. doi: 10.1007/s13738-018-1374-3. DOI
Ashrafi A.M., Cerovac S., Mudrić S., Guzsvány V., Husáková L., Urbanová I., Vytřas K. Antimony nanoparticle-multiwalled carbon nanotubes composite immobilized at carbon paste electrode for determination of trace heavy metals. Sens. Actuators B: Chem. 2014;191:320–325. doi: 10.1016/j.snb.2013.08.087. DOI
Ashrafi A.M., Vytřas K. Stripping voltammetric determination of mercury (II) at antimony-coated carbon paste electrode. Talanta. 2011;85:2700–2702. doi: 10.1016/j.talanta.2011.07.078. PubMed DOI
Ashrafi A.M., Vytřas K. New procedures for voltammetric determination of copper (II) using antimony film-coated carbon paste electrodes. Electrochimica Acta. 2012;73:112–117. doi: 10.1016/j.electacta.2011.12.042. DOI
Ashrafi A.M., Vytřas K. Determination of trace bismuth (III) by stripping voltammetry at antimony-coated carbon paste electrode. Int. J. Electrochem. Sci. 2012;7:68–76.
Ashrafi A.M., Vytřas K. Codeposited antimony-bismuth film carbon paste electrodes for electrochemical stripping determination of trace heavy metals. Int. J. Electrochem. Sci. 2013;8:2095–2103.
Bonfil Y., Brand M., Kirowa-Eisner E. Trace determination of mercury by anodic stripping voltammetry at the rotating gold electrode. Analytica Chimica Acta. 2000;424:65–76. doi: 10.1016/S0003-2670(00)01074-6. DOI
Hocevar S.B., Švancara I., Ogorevc B., Vytřas K. Antimony film electrode for electrochemical stripping analysis. Analytical chemistry. 2007;79:8639–8643. doi: 10.1021/ac070478m. PubMed DOI
Perone S. The Application of Stripping Analysis to the Determination of Silver (I) Using Graphite Electrodes. Anal. Chem. 1963;35:2091–2094. doi: 10.1021/ac60206a032. DOI
Švancara I., Vytřas K., Hua C., Smyth M.R. Voltammetric determination of mercury (II) at a carbon paste electrode in aqueous solutions containing tetraphenylborate ion. Talanta. 1992;39:391–396. doi: 10.1016/0039-9140(92)80153-5. PubMed DOI
Svobodová E., Baldrianová L., Hocevar S.B., Svancara I. Electrochemical stripping analysis of selected heavy metals at antimony trioxide-modified carbon paste electrode. Int. J. Electrochem. Sci. 2012;7:197–210.
Yang Y., Wang Z., Yang M., Guo M., Wu Z., Shen G., Yu R. Inhibitive determination of mercury ion using a renewable urea biosensor based on self-assembled gold nanoparticles. Sens. Actuators B Chem. 2006;114:1–8. doi: 10.1016/j.snb.2005.04.005. DOI
D’Souza S.F. Microbial biosensors. Biosens. Bioelectron. 2001;16:337–353. doi: 10.1016/S0956-5663(01)00125-7. PubMed DOI
Chey C., Ibupoto Z., Khun K., Nur O., Willander M.J.S. Indirect determination of mercury ion by inhibition of a glucose biosensor based on ZnO nanorods. Sensors. 2012;12:15063–15077. doi: 10.3390/s121115063. PubMed DOI PMC
Guascito M.R., Malitesta C., Mazzotta E., Turco A. Inhibitive determination of metal ions by an amperometric glucose oxidase biosensor: Study of the effect of hydrogen peroxide decomposition. Sens. Actuators B Chem. 2008;131:394–402. doi: 10.1016/j.snb.2007.11.049. DOI
Samphao A., Rerkchai H., Jitcharoen J., Nacapricha D., Kalcher K. Indirect determination of mercury by inhibition of glucose oxidase immobilized on a carbon paste electrode. Int. J. Electrochem. Sci. 2012;7:1001–1010.
Jung W.K., Koo H.C., Kim K.W., Shin S., Kim S.H., Park Y.H. Antibacterial activity and mechanism of action of the silver ion in Staphylococcus aureus and Escherichia coli. Appl. Environ. Microbiol. 2008;74:2171–2178. doi: 10.1128/AEM.02001-07. PubMed DOI PMC
Colowick S.P., Kaplan N.O., McCormick D.B., Wright L.D. Methods in Enzymology. Volume 1 Academic Press; New York, NY, USA: 1955.
Nečas D., Klapetek P. Gwyddion: An open-source software for SPM data analysis. Open Phys. 2012;10:181–188. doi: 10.2478/s11534-011-0096-2. DOI
Bass M., Berman A., Singh A., Konovalov O., Freger V. Surface structure of Nafion in vapor and liquid. J. Phys. Chem. B. 2010;114:3784–3790. doi: 10.1021/jp9113128. PubMed DOI
Schachl K., Turkušić E., Komersová A., Bartoš M., Moderegger H., Švancara I., Alemu H., Vytřas K., Jimenez-Castro M., Kalcher K. Amperometric determination of glucose with a carbon paste biosensor. Collect. Czechoslov. Chem. Commun. 2002;67:302–313. doi: 10.1135/cccc20020302. DOI
Švancara I., Metelka R., Vytřas K. Piston-driven carbon paste electrode holders for electrochemical measurements. Sens. Electroanal. 2005;1:7–18.
Bis(2,2'-bipyridil)Copper(II) Chloride Complex: Tyrosinase Biomimetic Catalyst or Redox Mediator?