Skip to main content
SpringerLink
Log in

Cantilever Nanobiosensor Functionalized with Tyrosinase for Detection of Estrone and β-estradiol in Water

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

This work aimed to develop cantilever nanobiosensor functionalized with tyrosinase enzyme to detect 17β-estradiol and estrone hormones. In this system, the tyrosinase enzyme was covalently immobilized by self-assembled monolayer onto the cantilever sensor surface. It was possible to verify that the high hormone concentration investigated resulted in high voltage response. The nanobiosensor presented a distinction between the concentrations evaluated and was verified sensitivities of 0.497 and 0.101 V/μg, limit of detection of 0.1 and 0.4 ng/L for the hormones 17β-estradiol and estrone, respectively. The device showed good reversibility and during 30 days of storage maintained about 99% of the original signal. The cantilever nanobiosensor applied in different water samples (ultrapure, river, tap, and mineral) showed good performance, so could be readily extended toward the on-site monitoring of the other trace small molecular pollutants in environmental water matrices.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Li, Y., Zhu, Y., Wang, C., He, M., & Lin, Q. (2019). Selective detection of water pollutants using a differential aptamer-based graphene biosensor. Biosensors and Bioelectronics, 126, 59–67. https://doi.org/10.1016/j.bios.2018.10.047.

    Article  CAS  PubMed  Google Scholar 

  2. Kase, R., Javurkova, B., Simon, E., Swart, K., Buchinger, S., Könemann, S., et al. (2018). Screening and risk management solutions for steroidal estrogens in surface and wastewater. TrAC Trends in Analytical Chemistry, 102, 343–358. https://doi.org/10.1016/j.trac.2018.02.013.

    Article  CAS  Google Scholar 

  3. Vigneshvar, S., Sudhakumari, C. C., Senthilkumaran, B., & Prakash, H. (2016). Recent advances in biosensor technology for potential applications – an overview. Frontiers in Bioengineering and Biotechnology, 4. https://doi.org/10.3389/fbioe.2016.00011.

  4. Liu, S., Cheng, R., Chen, Y., Shi, H., & Zhao, G. (2018). A simple one-step pretreatment, highly sensitive and selective sensing of 17β-estradiol in environmental water samples using surface-enhanced Raman spectroscopy. Sensors and Actuators B: Chemical, 254, 1157–1164. https://doi.org/10.1016/j.snb.2017.08.003.

    Article  CAS  Google Scholar 

  5. Busayapongchai, P., & Siri, S. (2017). Sensitive detection of estradiol based on ligand binding domain of estrogen receptor and gold nanoparticles. Analytical Biochemistry, 518, 60–68. https://doi.org/10.1016/j.ab.2016.11.003.

    Article  CAS  PubMed  Google Scholar 

  6. Alonso, J. M., Bielen, A. A. M., Olthuis, W., Kengen, S. W. M., Zuilhof, H., & Franssen, M. C. R. (2016). Self-assembled monolayers of 1-alkenes on oxidized platinum surfaces as platforms for immobilized enzymes for biosensing. Applied Surface Science. https://doi.org/10.1016/j.apsusc.2016.05.006.

  7. Della Ventura, B., Iannaccone, M., Funari, R., Pica Ciamarra, M., Altucci, C., Capparelli, R., & Velotta, R. (2017). Effective antibodies immobilization and functionalized nanoparticles in a quartz-crystal microbalance-based immunosensor for the detection of parathion. PLoS One, 12(2), e0171754. https://doi.org/10.1371/journal.pone.0171754.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Sýs, M., & Vytřas, K. (2018). Tyrosinase electrochemical biosensors monitoring medicinally significant substances. Current Medicinal Chemistry, 25(33), 3988–4006. https://doi.org/10.2174/0929867324666170727121327.

    Article  CAS  PubMed  Google Scholar 

  9. El Harrad, L., Bourais, I., Mohammadi, H., & Amine, A. (2018). Recent advances in electrochemical biosensors based on enzyme inhibition for clinical and pharmaceutical applications. Sensors, 18(2), 164. https://doi.org/10.3390/s18010164.

    Article  CAS  Google Scholar 

  10. Varmira, K., Mohammadi, G., Mahmoudi, M., Khodarahmi, R., Rashidi, K., Hedayati, M., & Jalalvand, A. R. (2018). Fabrication of a novel enzymatic electrochemical biosensor for determination of tyrosine in some food samples. Talanta, 183, 1–10. https://doi.org/10.1016/j.talanta.2018.02.053.

    Article  CAS  PubMed  Google Scholar 

  11. Camargo, J. R., Baccarin, M., Raymundo-Pereira, P. A., Campos, A. M., Oliveira, G. G., Fatibello-Filho, O., & Janegitz, B. C. (2018). Electrochemical biosensor made with tyrosinase immobilized in a matrix of nanodiamonds and potato starch for detecting phenolic compounds. Analytica Chimica Acta, 1034, 137–143. https://doi.org/10.1016/j.aca.2018.06.001.

    Article  CAS  PubMed  Google Scholar 

  12. Zaidi, K. U., Ali, A. S., Ali, S. A., & Naaz, I. (2014). Microbial tyrosinases: promising enzymes for pharmaceutical, food bioprocessing, and environmental industry. Biochemistry Research International, 2014, 1–16. https://doi.org/10.1155/2014/854687.

    Article  CAS  Google Scholar 

  13. Marques De Oliveira, R., Ferreira, J., Santos, M. J. L., Faria, R. M., & Oliveira, O. N. (2011). Probing the functionalization of gold surfaces and protein adsorption by PM-IRRAS. ChemPhysChem. https://doi.org/10.1002/cphc.201100080.

  14. Tagliazucchi, M., De Leo, L. P. M., Cadranel, A., Baraldo, L. M., Völker, E., Bonazzola, C., & Zamlynny, V. (2010). PM IRRAS spectroelectrochemistry of layer-by-layer self-assembled polyelectrolyte multilayers. Journal of Electroanalytical Chemistry. https://doi.org/10.1016/j.jelechem.2010.02.013.

  15. Muenchen, D. K., Martinazzo, J., Brezolin, A. N., de Cezaro, A. M., Rigo, A. A., Mezarroba, M. N., Manzoli, A., Steffens, J., & Steffens, C. (2018). Cantilever functionalization using peroxidase extract of low cost for glyphosate detection. Applied Biochemistry and Biotechnology, 186(4), 1061–1073. https://doi.org/10.1007/s12010-018-2799-y.

    Article  CAS  PubMed  Google Scholar 

  16. Martinazzo, J., Muenchen, D. K., Brezolin, A. N., Cezaro, A. M., Rigo, A. A., Manzoli, A., et al. (2018). Cantilever nanobiosensor using tyrosinase to detect atrazine in liquid medium. Journal of Environmental Science and Health - Part B Pesticides, Food Contaminants, and Agricultural Wastes, 53(4), 229–236. https://doi.org/10.1080/03601234.2017.1421833.

    Article  CAS  Google Scholar 

  17. Lu, L., Zhang, L., Zhang, X., Huan, S., Shen, G., & Yu, R. (2010). A novel tyrosinase biosensor based on hydroxyapatite–chitosan nanocomposite for the detection of phenolic compounds. Analytica Chimica Acta, 665(2), 146–151. https://doi.org/10.1016/j.aca.2010.03.033.

    Article  CAS  PubMed  Google Scholar 

  18. Lavrik, N. V., Sepaniak, M. J., & Datskos, P. G. (2004). Cantilever transducers as a platform for chemical and biological sensors. Review of Scientific Instruments, 75(7), 2229–2253. https://doi.org/10.1063/1.1763252.

    Article  CAS  Google Scholar 

  19. Datskos, P. G., & Sauers, I. (1999). Detection of 2-mercaptoethanol using gold-coated micromachined cantilevers. Sensors and Actuators B: Chemical, 61(1–3), 75–82. https://doi.org/10.1016/S0925-4005(99)00251-8.

    Article  CAS  Google Scholar 

  20. CONAMA. (2005). Resolução n° 357, DE 17 DE MARÇO DE 2005.

  21. European Commission. (2012). Directive of the European parliament and of the council amending Directives 2000/60/EC and 2008/105/EC as regards priority substances in the field of water policy, COM (2011).

  22. Daniel, M. D. S., & De Lima, E. C. (2014). Determinação simultânea de estriol, β-estradiol, 17α-etinilestradiol e estrona empregando-se extração em fase sólida (SPE) e cromatografia líquida de alta eficiência (HPLC). Ambiente e Agua - An Interdisciplinary Journal of Applied Science, 9(4). https://doi.org/10.4136/ambi-agua.1346.

  23. Manickum, T., John, W., & Mlambo, Z. D. (2016). Development and validation of a gas chromatography-mass spectrometry test method for screening and quantitation of steroid estrogens (endocrine disruptor compounds) in water and wastewater using large volume injection. Annals of Chromatography and Separation Techniques, 2(2473–0696).

  24. Sodré, F. F., Locatelli, M. A. F., & Jardim, W. F. (2010). Occurrence of emerging contaminants in Brazilian drinking waters: a sewage-to-tap issue. Water, Air, and Soil Pollution, 206(1–4), 57–67. https://doi.org/10.1007/s11270-009-0086-9.

    Article  CAS  Google Scholar 

  25. Moreira, M., Aquino, S., Coutrim, M., Silva, J., & Afonso, R. (2011). Determination of endocrine-disrupting compounds in waters from Rio das Velhas, Brazil, by liquid chromatography/high resolution mass spectrometry (ESI-LC-IT-TOF/MS). Environmental Technology, 32(12), 1409–1417. https://doi.org/10.1080/09593330.2010.537829.

    Article  CAS  PubMed  Google Scholar 

  26. Torres, N. H., Aguiar, M. M., Ferreira, L. F. R., Américo, J. H. P., Machado, Â. M., Cavalcanti, E. B., & Tornisielo, V. L. (2015). Detection of hormones in surface and drinking water in Brazil by LC-ESI-MS/MS and ecotoxicological assessment with Daphnia magna. Environmental Monitoring and Assessment, 187(6), 379. https://doi.org/10.1007/s10661-015-4626-z.

    Article  CAS  PubMed  Google Scholar 

  27. Stredansky, M. (2017). Multienzyme amperometric gluconic acid biosensor based on nanocomposite planar electrodes for analysis in musts and wines. International Journal of Electrochemical Science, 1183–1192. https://doi.org/10.20964/2017.02.31.

  28. Welch, C. M., & Compton, R. G. (2006). The use of nanoparticles in electroanalysis: a review. Analytical and Bioanalytical Chemistry, 384(3), 601–619. https://doi.org/10.1007/s00216-005-0230-3.

    Article  CAS  PubMed  Google Scholar 

  29. Yogeswaran, U., & Chen, S.-M. (2008). A review on the electrochemical sensors and biosensors composed of nanowires as sensing material. Sensors, 8(1), 290–313. https://doi.org/10.3390/s8010290.

    Article  CAS  PubMed  Google Scholar 

  30. Sassolas, A., Blum, L. J., & Leca-Bouvier, B. D. (2012). Immobilization strategies to develop enzymatic biosensors. Biotechnology Advances, 30(3), 489–511. https://doi.org/10.1016/j.biotechadv.2011.09.003.

    Article  CAS  PubMed  Google Scholar 

  31. Silvério, M. D. O., Castro, C. F. S., & Miranda, A. R. (2013). Avaliação da atividade antioxidante e inibitÃ\textthreesuperiorria da tirosinase das folhas de Dipteryx alata Vogel (Baru). Revista Brasileira de Plantas Medicinais, 15, 59–65 Retrieved from http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1516-05722013000100008&nrm=iso.

    Article  Google Scholar 

  32. Zolghadri, S., Bahrami, A., Hassan Khan, M. T., Munoz-Munoz, J., Garcia-Molina, F., Garcia-Canovas, F., & Saboury, A. A. (2019). A comprehensive review on tyrosinase inhibitors. Journal of Enzyme Inhibition and Medicinal Chemistry. https://doi.org/10.1080/14756366.2018.1545767.

  33. Lee, K. E., Bharadwaj, S., Yadava, U., & Kang, S. G. (2019). Evaluation of caffeine as inhibitor against collagenase, elastase and tyrosinase using in silico and in vitro approach. Journal of Enzyme Inhibition and Medicinal Chemistry, 34(1), 927–936. https://doi.org/10.1080/14756366.2019.1596904.

    Article  CAS  Google Scholar 

  34. Liu, X., Wang, X., Zhang, J., Feng, H., Liu, X., & Wong, D. K. Y. (2012). Detection of estradiol at an electrochemical immunosensor with a Cu UPD|DTBP–Protein G scaffold. Biosensors and Bioelectronics, 35(1), 56–62. https://doi.org/10.1016/j.bios.2012.02.002.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank URI Erechim for the infrastructure.

Funding

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 00,1, Cnpq, Fapergs, and Finep.

Author information

Authors and Affiliations

  1. Department of Food Engineering, URI Erechim, Av. Sete de Setembro, 1621, Erechim, RS, 99709-910, Brazil

    Alana Marie de Cezaro, Aline Andressa Rigo, Janine Martinazzo, Daniela Kunkel Muenchen, Alexandra Manzoli, Juliana Steffens & Clarice Steffens

  2. Nanotechnology National Laboratory for Agriculture (LNNA), Embrapa Instrumentação, P.O. Box 741, São Carlos, SP, 13560-970, Brazil

    Daniel Souza Correa

Authors
  1. Alana Marie de Cezaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aline Andressa Rigo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Janine Martinazzo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniela Kunkel Muenchen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexandra Manzoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Daniel Souza Correa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Juliana Steffens
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Clarice Steffens
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Clarice Steffens.

Ethics declarations

Conflicts of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Cezaro, A.M., Rigo, A.A., Martinazzo, J. et al. Cantilever Nanobiosensor Functionalized with Tyrosinase for Detection of Estrone and β-estradiol in Water. Appl Biochem Biotechnol 190, 1512–1524 (2020). https://doi.org/10.1007/s12010-019-03195-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-019-03195-8

Keywords

Search

Navigation