Page Header

Home > ONLINE FIRST > Farahdina

Electrochemical Characterization of Thin Film/Nanodots Electrodes of Silver and Gold for Biosensing CCRF-CEM Leukemia Cells

Ulya Farahdina, Miftakhul Firdhaus, Putri Wulandari, Agus Rubiyanto, Nasori Nasori, Ihwanul Aziz, Hari Suprihatin, Nurul Jadid, Rini Khamimatul Ula

Abstract


This study presents a novel biosensor for detecting CCRF-CEM cells, derived from a T lymphoblastoid cell line, featuring intricate surface modification techniques. The fabrication process involves thin film deposition, electropolishing and dual anodization to create an anodic aluminum oxide template, followed by DC sputtering deposition to produce gold (Au) thin film/silver (Ag) nanodots and an Ag thin film/Au nanodots electrodes. Characterization using scanning electron microscopes (SEM), energy-dispersive X-ray spectroscopy (EDX), and X-ray diffraction (XRD) confirms electrode suitability for biosensing applications. Surface modification with aptamer Sgc8c and bovine serum albumin enables specific binding of CCRF-CEM cells while minimizing non-specific interactions. Electrochemical characterization via cyclic voltammetry (CV) and electrochemical impedance spectroscopy (EIS) reveals the biosensor's sensitivity, selectivity, and reproducibility. The Au thin film/Ag nanodots electrode emerges as the most promising choice, exhibiting exceptional sensitivity (limit of detection (LOD) = 16 cell/10 mL), reproducibility, and selectivity for CCRF-CEM cells. This work highlights the importance of tailored surface development in biosensor design and lays the groundwork for highly sensitive and selective biosensors with potential applications in disease diagnosis and therapeutic monitoring.

Keywords



[1]    M. Abramovitz, Leukemia. New York: Greenhaven Publishing, 2010.

[2]    The Leukemia & Lymphoma Society, “Facts: Updated Data on Blood Cancers | Leukemia and Lymphoma Society,” 2023. [Online]. Available: https://www.lls.org/booklet/facts-updated-data-blood-cancers

[3]    American Cancer Society, “Cancer Facts and Statistics,” 2023. [Online]. Available: https://www. cancer.org/research/cancer-facts-statistics.html

[4]    M. P. Coleman, M. Quaresma, F. Berrino, J. M. Lutz, R. De Angelis, R. Capocaccia, P. Baili, B. Rachet, G. Gatta, T. Hakulinen, A. Micheli, M. Sant, H. K. Weir, J. M. Elwood, H. Tsukuma, S. Koifman, G. A. E. Silva, S. Francisci, M. Santaquilani, A. Verdecchia, H. H. Storm, J. L. Young, “Cancer survival in five continents: A worldwide population-based study (CONCORD),” The Lancet Oncology, vol. 9, no. 8, pp. 730–756, 2008, doi: 10.1016/S1470-2045(08)70179-7.

[5]    J. Song, H.-J. Kim, C. Lee, S. J. Kim, S. Hwang, and T. S. Kim, “Identification of gene expression signatures for molecular classification in human leukemia cells,” International Journal of Oncology, vol. 29, no. 1, pp. 57–64, 2006, doi: 10.3892/ IJO.29.1.57.

[6]    T. Lightfoot and E. Roman, “Causes of childhood leukaemia and lymphoma,” Toxicology and Applied Pharmacology, vol. 199, no. 2, pp. 104–117, 2004, doi: 10.1016/J.TAAP.2003.12.032.

[7]    P. Dörge, B. Meissner, M. Zimmermann, A. Möricke, A. Schrauder, J. P. Bouquin, D. Schewe, J. Harbott, A. T. Schlegel, R. Ratei, W. D. Ludwig, R. Koehler, C. R. Bartram, M. Schrappe, M. Stanulla, and G. Cario, “IKZF1 deletion is an independent predictor of outcome in pediatric acute lymphoblastic leukemia treated according to the ALL-BFM 2000 protocol,” Haematologica, vol. 98, pp. 428–432, 2010, doi: 10.3324/haematol.2011.056135.

[8]    P. Das, V. A. Diya, S. Meher, R. Panda, and A. Abraham, “A systematic review on recent advancements in deep and machine learning based detection and classification of acute lymphoblastic leukemia,” IEEE Access, vol. 10, pp. 81741–81763, 2022, doi: 10.1109/access. 2022.3196037.

[9]    U. Farahdina, T. Amrillah, M. Mashuri, V. Lee, and N. Nasori, “A novel nanobiosensor for electrochemical and optical diagnosis of leukemia: challenge and opportunity,” Journal of Innovative Optical Health Sciences, vol. 17, no. 04, 2024, Art. no. 2430003, doi: 10.1142/ S1793545824300039.

[10]  J. Wang, “Electrochemical biosensors: Towards point-of-care cancer diagnostics,” Biosensors & Bioelectronics, vol. 21, no. 10, pp. 1887–1892, 2006, doi: 10.1016/J.BIOS.2005.10.027.

[11]  M. A. Tabrizi, M. Shamsipur, R. Saber, and S. Sarkar, “Isolation of HL-60 cancer cells from the human serum sample using MnO2-PEI/Ni/Au/aptamer as a novel nanomotor and electrochemical determination of thereof by aptamer/gold nanoparticles-poly(3,4-ethylene dioxythiophene) modified GC electrode,” Biosensors and Bioelectronics, vol. 110, pp. 141–146, 2018, doi: 10.1016/j.bios.2018.03.034.

[12]  Y. Sun, Q. Ren, B. Liu, Y. Qin, and S. Zhao, “Enzyme-free and sensitive electrochemical determination of the FLT3 gene based on a dual signal amplified strategy: Controlled nanomaterial multilayers and a target-catalyzed hairpin assembly,” Biosensors and Bioelectronics, vol. 78, pp. 7–13, 2016, doi: 10.1016/j.bios. 2015.11.014.

[13]  T. Hianik, “Advances in electrochemical and acoustic aptamer-based biosensors and immunosensors in diagnostics of leukemia,” Biosensors, vol. 11, no. 6, pp. 177, 2021, doi: 10.3390/bios11060177.

[14]  A. Malysheva, A. Ivask, C. L. Doolette, N. H. Voelcker, and E. Lombi, “Cellular binding, uptake and biotransformation of silver nanoparticles in human T lymphocytes,” Nature Nanotechnology, vol. 16, no. 8, pp. 926–932, 2021, doi: 10.1038/s41565-021-00914-3.

[15]  C. Salvo-Comino, F. Martín-Pedrosa, C. García-Cabezón, and M. L. Rodriguez-Mendez, “Silver nanowires as electron transfer mediators in electrochemical catechol biosensors,” Sensors, vol. 21, no. 3, p. 899, 2021, doi: 10.3390/ s21030899.

[16]  Y. Liu, D. Zhang, E. Alocilja, and S. Chakrabartty, “Biomolecules detection using a silver-enhanced gold nanoparticle-based biochip,” Nanoscale Research Letters, vol. 5, pp. 533–538, 2010, doi: 10.1007/s11671-010-9542-0.

[17]  X. Ren, X. Meng, D. Chen, F. Tang, and J. Jiao, “Using silver nanoparticle to enhance current response of biosensor,” Biosensors & Bioelectronics, vol. 21 3, pp. 433–7, 2005, doi: 10.1016/ J.BIOS.2004.08.052.

[18]  D. V. Sotnikov, A. N. Berlina, V. S. Ivanov, A. V. Zherdev, and B. B. Dzantiev, “Adsorption of proteins on gold nanoparticles: One or more layers?,” Colloids and Surfaces B: Biointerfaces, vol. 173, pp. 557–563, 2019, doi: 10.1016/ j.colsurfb.2018.10.025.

[19]  PubChem, “Glycerin,” 2024. [Online]. Available: https://pubchem.ncbi.nlm.nih.gov/compound/753

[20]  A. Rutz, J. Bisson, and P.-M. Allard, “The LOTUS initiative for open natural products research: Frozen dataset union wikidata (with metadata),” 2023, doi: 10.5281/zenodo.5794106.

[21]  C. Liu, J. Lin, C. Langevine, D. Smith, J. Li, J. S. Tokarski, J. Khan, M. Ruzanov, J. Strnad, A. Z. Fernandez, L. Cheng, K. M. Gillooly, D. Shuster, Y. Zhang, A. Thankappan, K. W. McIntyre, C. Chaudhry, P. A. Elzinga, M. Chiney, A. Chimalakonda, L. J. Lombardo, J.  E. Macor, P. H. Carter, J. R. Burke, and D. S. Weinstein, “Discovery of BMS-986202: A clinical Tyk2 inhibitor that binds to Tyk2 JH2,” Journal of Medicinal Chemistry, vol. 64, no. 1, pp. 677–694, 2021, doi: 10.1021/acs.jmedchem. 0c01698.

[22]  F. Briganti, S. Mangani, A. Scozzafava, G. Vernaglione, and C. T. Supuran, “Carbonic anhydrase catalyzes cyanamide hydration to urea: Is it mimicking the physiological reaction?,” Journal of Biological Inorganic Chemistry, vol. 4, no. 5, pp. 528–536, 1999, doi: 10.1007/s007750050375.

[23]  K. A. Majorek, P. J. Porebski, A. Dayal, M. D. Zimmerman, K. Jablonska, A. J. Stewart, M. Chruszcz, and W. Minor, “Structural and immunologic characterization of bovine, horse, and rabbit serum albumins,” Molecular Immunology, vol. 52, no. 3–4, pp. 174–182, 2012, doi: 10.1016/j.molimm.2012.05.011.

[24]  D. Kozakov, D. R. Hall, B. Xia, K. A. Porter, D. Padhorny, C. Yueh, D. Beglov, and S. Vajda, “The ClusPro web server for protein–protein docking,” Nature Protocols, vol. 12, no. 2, pp. 255–278, 2017, doi: 10.1038/nprot.2016.169.

[25]  M. A. Khan, Y. Zhu, Y. Yao, P. Zhang, A. Agrawal, and P. J. Reece, “Impact of metal crystallinity-related morphologies on the sensing performance of plasmonic nanohole arrays,” Nanoscale, vol. 12, no. 14, pp. 7577–7585, 2020, doi: 10.1039/D0NR00619J.

[26]  X. Yan, P. Lin, X. Qi, and L. Yang, “Finnis–Sinclair potentials for fcc Au–Pd and Ag–Pt alloys,” International Journal of Materials Research, vol. 102, no. 4, pp. 381–388, 2011, doi: 10.3139/146.110488.

[27]  K. Fu, J.-W. Seo, V. Kesler, N. Maganzini, B. D. Wilson, M. Eisenstein, B. Murmann, and H. T. Soh, “Accelerated electron transfer in nanostructured electrodes improves the sensitivity of electrochemical biosensors,” Advanced Science, vol. 8, 2021, Art. no. 2102495, doi: 10.1002/advs.202102495.

[28]  E. Randviir, “A cross examination of electron transfer rate constants for carbon screen-printed electrodes using electrochemical impedance spectroscopy and cyclic voltammetry,” Electrochimica Acta, vol. 286, pp. 179–186, 2018, doi: 10.1016/J.ELECTACTA.2018.08.021.

[29]  M. Yaşa, S. Surmeli, T. Depci, L. Toppare, and S. Hacioglu, “Synthesis of a multifunctional quinoxaline and benzodithiophene bearing polymer and its electrochromic device applications,” Macromolecular Chemistry and Physics, vol. 221, 2020, Art. no. 1900470, doi: 10.1002/macp.201900470.

[30]  X. Yang and Z. Gao, “Enzyme-catalysed deposition of ultrathin silver shells on gold nanorods: a universal and highly efficient signal amplification strategy for translating immunoassay into a litmus-type test,” Chemical Communications, vol. 51, no. 32, pp. 6928–6931, 2015, doi: 10.1039/c5cc01286d.

[31]  X. Pang, C. Cui, M. Su, Y. Wang, Q. Wei, and W. Tan, “Construction of self-powered cytosensing device based on ZnO nanodisks@g-C3N4 quantum dots and application in the detection of CCRF-CEM cells,” Nano Energy, vol. 46, pp. 101–109, 2018, doi: 10.1016/j. nanoen.2018.01.018.

[32]  J. Lee, I.-S. Park, H. Kim, J.-S. Woo, B.-S. Choi, and D.-H. Min, “BSA as additive: A simple strategy for practical applications of PNA in bioanalysis,” Biosensors and Bioelectronics, vol. 69, pp. 167–173,  2015, doi: 10.1016/j.bios.2015. 02.030.

[33]  Y. Kim, H.-S. Jung, T. Matsuura, H.-Y. Lee, T. Kawai, and M. Gu, “Electrochemical detection of 17beta-estradiol using DNA aptamer immobilized gold electrode chip,” Biosensors & bioelectronics, vol. 22, no. 11, pp. 2525–2531, 2007, doi: 10.1016/J.BIOS.2006.10.004.

[34]  F. A. Armstrong, R. Camba, H. A. Heering, J. Hirst, L. J. C. Jeuken, A. K. Jones, C. Léger, and J. P. McEvoy, “Fast voltammetric studies of the kinetics and energetics of coupled electron-transfer reactions in proteins,” Faraday Discussions, vol. 116, pp. 191–203, 2000, doi: 10.1039/B002290J.

[35]  M. Cohen-Atiya and D. Mandler, “Studying electron transfer through alkanethiol self-assembled monolayers on a hanging mercury drop electrode using potentiometric measurements,” Physical Chemistry Chemical Physics, vol. 8,  no. 38, pp. 4405–4409, 2006, doi: 10.1039/ B609560G.

[36]  Y. Jin, “Label-free monitoring of site-specific DNA cleavage by EcoRI endonuclease using cyclic voltammetry and electrochemical impedance,” Analytica Chimica Acta, vol. 634, no. 1, pp. 44–48, 2009, doi: 10.1016/j.aca.2008. 12.005.

[37]  K. Kaniewska, W. Hyk, Z. Stojek, and M. Karbarz, “Diffusional and migrational transport of ionic species affected by electrostatic interactions with an oppositely charged hydrogel layer attached to an electrode surface,” Electrochemistry Communications, vol. 88, pp. 97–100, 2018, doi: 10.1016/J.ELECOM.2018.02.004.

[38]  P. St-Pierre and N. Petersen, “Relative ligand binding to small or large aggregates measured by scanning correlation spectroscopy,” Biophysical Journal, vol. 58, no. 2, pp. 503–511, 1990, doi: 10.1016/S0006-3495(90)82395-X.

[39]  S. Peng, D.-W. Liang, P. Diao, Y. Liu, F. Lan, Y. Yang, S. Lu, and Y. Xiang, “Nernst-ping-pong model for evaluating the effects of the substrate concentration and anode potential on the kinetic characteristics of bioanode,” Bioresource Technology, vol. 136, pp. 610–616, 2013, doi: 10.1016/j.biortech.2013.03.073.

[40]  U. Farahdina, A. S. Muliawati, V. Z. Zulfa, M. Firdhaus, I. Aziz, H. Suprihatin, D. Darsono, N. Nasori, and A. Rubiyanto, “Electrochemical and optical analysis of various compositions of Au and Ag layers for blood cancer prognosis,” Coatings, vol. 13, no. 1, 2023, doi: 10.3390/ coatings13010186.

[41]  R. Misra, “Biosensors,” Materials Technology, vol. 30, pp. 139–139, 2015, doi: 10.1179/b15z. 00000000024.

[42]  L. Soleymani, Z. Fang, E. Sargent, and S. Kelley, “Programming the detection limits of biosensors through controlled nanostructuring,” Nature Nanotechnology, vol. 4, no. 12, pp. 844–848, 2009, doi: 10.1038/nnano.2009.276.

[43]  A. H. Suroviec, “Introduction to electrochemistry,” Journal of Laboratory Chemical Education, vol. 1, no. 3, pp. 45–48, 2013, doi: 10.5923/j.jlce. 20130103.02.

[44]  O. Dračka, “Theory of current elimination in linear scan voltammetry,” Journal of Electroanalytical Chemistry, vol. 402, pp. 19–28, 1996, doi: 10.1016/0022-0728(95)04257-1.

[45]  S. Tanimoto and A. Ichimura, “Discrimination of inner- and outer-sphere electrode reactions by cyclic voltammetry experiments,” Journal of Chemical Education, vol. 90, pp. 778–781, 2013, doi: 10.1021/ED200604M.

[46]  K. Aoki and N. Kato, “Analysis of the cyclic voltammograms associated with deposition or precipitation of the electrochemical product,” Journal of Electroanalytical Chemistry, vol. 245, pp. 51–60, 1988, doi: 10.1016/0022-0728(88) 80058-5.

[47]  R. N. Moman, N. Gupta, and M. Varacallo, “Physiology, Albumin,” 2024. [Online]. Available: http://www.ncbi.nlm.nih.gov/books/NBK459198/

[48]  J. Feher, “9.4 - the endocrine pancreas and control of blood glucose,” in Quantitative Human Physiology, J. Feher, Ed. Boston: Academic Press, 2012, pp. 799–809.

[49]  A. O. Hosten, “BUN and Creatinine,” in Clinical Methods: The History, Physical, and Laboratory Examinations, H. K. Walker, W. D. Hall, and J. W. Hurst, Eds. Boston: Butterworths, 1990.

[50]  E. C. C. Lin, “Glycerol utilization and its regulation in mammals,” Annual Review of Biochemistry, vol. 46, pp. 765–795, 1977, doi: 10.1146/annurev.bi.46.070177.004001.

[51]  S. Albright, M. Cacace, Y. Tivon, and A. Deiters, “Cell surface labeling and detection of protein tyrosine kinase 7 via covalent aptamers,” Journal of the American Chemical Society, vol. 145, no. 30, pp. 16458–16463, 2023, doi: 10.1021/jacs.3c02752.

[52]  M. Leitner, A. Poturnayova, C. Lamprecht, S. Weich, M. Snejdarkova, I. Karpisova, T. Hianik, and A. Ebner, “Characterization of the specific interaction between the DNA aptamer sgc8c and protein tyrosine kinase-7 receptors at the surface of T-cells by biosensing AFM,” Analytical and Bioanalytical Chemistry, vol. 409, pp. 2767–2776, 2017, doi: 10.1007/s00216 -017-0238-5.

[53]  P. Aiemderm, K. Monkhang, S. Wongjard, K. Choowongkomon, N. Mongkoldhumrongkul Swainson, C. Prasittichai, C. Kraiya, “Advantages of electro-deposited gold on carbon electrodes for NT-proBNP immunosensor for development of heart failure test kit,” Applied Science and Engineering Progress, vol. 17, no. 2, 2024, doi: 10.14416/j.asep.2023.10.004.

[54]  S. S. Patil, V. N. Narwade, K. S. Sontakke, T. Hianik, and M. D. Shirsat, “Layer-by-layer immobilization of DNA aptamers on Ag-incorporated co-succinate metal–organic framework for Hg(II) detection,” Sensors, vol. 24, no. 2, 2024, doi: 10.3390/s24020346.

[55]  W. Guo, C. Zhang, T. Ma, X. Liu, Z. Chen, S. Li, and Y. Deng, “Advances in aptamer screening and aptasensors’ detection of heavy metal ions,” Journal of Nanobiotechnology, vol. 19, no. 1, p. 166, 2021, doi: 10.1186/s12951-021-00914-4.

[56]  B. Chatterjee, N. Kalyani, A. Anand, E. Khan, S. Das, V. Bansal, A. Kumar, and T. K. Sharma, “GOLD SELEX: A novel SELEX approach for the development of high-affinity aptamers against small molecules without residual activity,” Microchimica Acta, vol. 187, no. 11, p. 618, 2020, doi: 10.1007/s00604-020-04577-0.

[57]  J. Li, H. Xi, C. Kong, Q. Liu, and Z. Chen, “‘Aggregation-to-deaggregation’ colorimetric signal amplification strategy for Ag+ detection at the femtomolar level with dark-field microscope observation,” Analytical Chemistry, vol. 90, no. 19, pp. 11723–11727, 2018, doi: 10.1021/ acs.analchem.8b03739.

[58]  M. H. Akhtar, K. K. Hussain, N. G. Gurudatt, and Y.-B. Shim, “Detection of Ca2+-induced acetylcholine released from leukemic T-cells using an amperometric microfluidic sensor,” Biosensors and Bioelectronics, vol. 98, pp. 364–370, 2017, doi: 10.1016/j.bios.2017.07.003.

[59]  J. Li, X. Lin, Z. Zhang, W. Tu, and Z. Dai, “Red light-driven photoelectrochemical biosensing for ultrasensitive and scatheless assay of tumor cells based on hypotoxic AgInS2 nanoparticles,” Biosensors and Bioelectronics, vol. 126, pp. 332–338, 2019, doi: 10.1016/j.bios.2018.09.096.

[60]  M. Mazloum-Ardakani, B. Barazesh, A. Khoshroo, M. Moshtaghiun, and M. H. Sheikhha, “A new composite consisting of electrosynthesized conducting polymers, graphene sheets and biosynthesized gold nanoparticles for biosensing acute lymphoblastic leukemia,” Bioelectrochemistry, vol. 121, pp. 38–45, 2018, doi: 10.1016/j.bioelechem.2017.12.010.

[61]  M. A. Tabrizi, M. Shamsipur, R. Saber, and S. Sarkar, “Flow injection amperometric sandwich-type aptasensor for the determination of human leukemic lymphoblast cancer cells using MWCNTs-Pdnano/PTCA/aptamer as labeled aptamer for the signal amplification,” Analytica Chimica Acta, vol. 985, pp. 61–68, 2017, doi: 10.1016/j.aca.2017.07.054.

[62]  M. Su, L. Ge, S. Ge, N. Li, J. Yu, M. Yan, J. Huang, “Paper-based electrochemical cyto-device for sensitive detection of cancer cells and in situ anticancer drug screening,” Analytica Chimica Acta, vol. 847, pp. 1–9, 2014, doi: 10.1016/j.aca.2014.08.013.

[63]  B. Dou, L. Xu, B. Jiang, R. Yuan, and Y. Xiang, “Aptamer-functionalized and gold nanoparticle array-decorated magnetic graphene nanosheets enable multiplexed and sensitive electrochemical detection of rare circulating tumor cells in whole blood,” Analytical Chemistry, vol. 91, no. 16, pp. 10792–10799, 2019, doi: 10.1021/acs.analchem. 9b02403.

[64]  S. Ismail‐Hamdi, M. N. Romdane, and S. Ben Romdhane, “Comparison of a human portable blood glucose meter and automated chemistry analyser for measurement of blood glucose concentrations in healthy dogs,” Veterinary Medicine and Science, vol. 7, no. 6, pp. 2185–2190, 2021, doi: 10.1002/vms3.594.

[65]  G. Abdul-Hamid, “Classification of acute leukemia,” in Acute Leukemia - The Scientist’s Perspective and Challenge. London, UK: IntechOpen, 2011.

Full Text: PDF

DOI: 10.14416/j.asep.2024.09.003

Refbacks

  • There are currently no refbacks.


Copyright © 2024 by King Mongkut’s University of Technology North Bangkok. All rights reserved.