Impedimetric Detection of Cancer Markers Based on Nanofiber Copolymers
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Instrumentation
2.3. Fabrication of NFs
2.4. Preparation of the Biosensor and FR Biosensing Assay
Detection in Human Plasma
2.5. Analytical Procedure of the Electrochemical Biosensor
3. Results and Discussion
3.1. Preparation of SA-PEO/FA NFs
3.2. Morphological, Structural, and Electrochemical Characterizations of the Biosensor
3.2.1. Morphological Characterization
3.2.2. Structural Characterization
3.2.3. Electrochemical Characterization of SA-PEO/FA NFs
Biosensors Optimization
3.3. Biosensors Properties Regarding FRs
3.4. Selectivity of the Biosensor
3.5. Reproducibility, Reusability, and Stability of the Biosensor
3.6. Detection in the Plasma Samples
3.7. Risk Scenario Related to the Process, Sampling, and Detection
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA A Cancer J. Clin. 2021, 71, 209–249. [Google Scholar] [CrossRef]
- Correia, A.R.; Sampaio, I.; Comparetti, E.J.; Vieira, N.C.S.; Zucolotto, V. Detecting cancer cells with a highly sensitive LbL-based biosensor. Talanta 2021, 233, 122506. [Google Scholar] [CrossRef]
- Andreou, C.; Weissleder, R.; Kircher, M.F. Multiplexed imaging in oncology. Nat. Biomed. Eng. 2022, 6, 527–540. [Google Scholar] [CrossRef]
- Hussain, S.; Mubeen, I.; Ullah, N.; Shah, S.S.U.D.; Khan, B.A.; Zahoor, M.; Ullah, R.; Khan, F.A.; Sultan, M.A. Modern diagnostic imaging technique applications and risk factors in the medical field: A review. BioMed Res. Int. 2022, 2022, 5164970. [Google Scholar] [CrossRef] [PubMed]
- Vaghashiya, R.; Shin, S.; Chauhan, V.; Kapadiya, K.; Sanghavi, S.; Seo, S.; Roy, M. Machine Learning Based Lens-Free Shadow Imaging Technique for Field-Portable Cytometry. Biosensors 2022, 12, 144. [Google Scholar] [CrossRef] [PubMed]
- Rajput, G.; Agrawal, S.; Raut, G.; Vishvakarma, S.K. An accurate and noninvasive skin cancer screening based on imaging technique. Int. J. Imaging Syst. Technol. 2022, 32, 354–368. [Google Scholar] [CrossRef]
- Varoquaux, G.; Cheplygina, V. Machine learning for medical imaging: Methodological failures and recommendations for the future. NPJ Digit. Med. 2022, 5, 48. [Google Scholar] [CrossRef]
- Farran, B.; Albayrak, S.; Abrams, J.; Tainsky, M.A.; Levin, N.K.; Morris, R.; Matherly, L.H.; Ratnam, M.; Winer, I. Serum folate receptor α (sFR) in ovarian cancer diagnosis and surveillance. Cancer Med. 2019, 8, 920–927. [Google Scholar] [CrossRef]
- Leung, F.-R.; Dimitromanolakis, A.; Kobayashi, H.; Diamandis, E.; Kulasingam, V. Folate-receptor 1 (FOLR1) protein is elevated in the serum of ovarian cancer patients. Clin. Biochem. 2013, 46, 1462–1468. [Google Scholar] [CrossRef]
- Bax, H.J.; Chauhan, J.; Stavraka, C.; Santaolalla, A.; Osborn, G.; Khiabany, A.; Grandits, M.; López-Abente, J.; Palhares, L.C.; Chan Wah Hak, C. Folate receptor alpha in ovarian cancer tissue and patient serum is associated with disease burden and treatment outcomes. Br. J. Cancer 2023, 128, 342–353. [Google Scholar] [CrossRef]
- Çelikkol, A.; Şeber, E.S.; Güzel, S.; Yolcu, A.; Yetişyiğit, T.; Yilmaz, A. Investigation of Serum Folate-Receptor-1 Levels in Patients with Non-Small Cell Lung Cancer. Konuralp Med. J. 2022, 14, 526–532. [Google Scholar] [CrossRef]
- van Zijl, F.; Krupitza, G.; Mikulits, W. Initial steps of metastasis: Cell invasion and endothelial transmigration. Mutat. Res./Rev. Mutat. Res. 2011, 728, 23–34. [Google Scholar] [CrossRef] [PubMed]
- Du, L.; Chen, W.; Wang, J.; Cai, W.; Kong, S.; Wu, C. Folic acid-functionalized zirconium metal-organic frameworks based electrochemical impedance biosensor for the cancer cell detection. Sens. Actuators B Chem. 2019, 301, 127073. [Google Scholar] [CrossRef]
- Soleymani, J.; Hasanzadeh, M.; Somi, M.H.; Shadjou, N.; Jouyban, A. Probing the specific binding of folic acid to folate receptor using amino-functionalized mesoporous silica nanoparticles for differentiation of MCF 7 tumoral cells from MCF 10A. Biosens. Bioelectron. 2018, 115, 61–69. [Google Scholar] [CrossRef]
- Hu, C.; Wei, G.; Zhu, F.; Wu, A.; Luo, L.; Shen, S.; Zhang, J. Platinum-Based Nanocomposite Pt@ BSA as an Efficient Electrochemical Biosensing Interface for Rapid and Ultrasensitive Determination of Folate Receptor-Positive Tumor Cells. ACS Appl. Bio Mater. 2022, 5, 3038–3048. [Google Scholar] [CrossRef] [PubMed]
- Verdin, A.; Sloan-Dennison, S.; Malherbe, C.; Graham, D.; Eppe, G. SERS nanotags for folate receptor α detection at the single cell level: Discrimination of overexpressing cells and potential for live cell applications. Analyst 2022, 147, 3328–3339. [Google Scholar] [CrossRef] [PubMed]
- Yang, T.; Xu, F.; Fang, D.; Chen, Y. Targeted proteomics enables simultaneous quantification of folate receptor isoforms and potential isoform-based diagnosis in breast cancer. Sci. Rep. 2015, 5, 16733. [Google Scholar] [CrossRef] [PubMed]
- Ishiwata, T.; Hiraishi, Y.; Bernards, N.; Sata, Y.; Gregor, A.; Aragaki, M.; Yasufuku, K. Transbronchial real-time lung tumor localization with folate receptor–targeted near-infrared molecular imaging: A proof of concept study in animal models. J. Thorac. Cardiovasc. Surg. 2023, 165, e240–e251. [Google Scholar] [CrossRef]
- Dong, S.; Teo, J.D.W.; Chan, L.Y.; Lee, C.-L.K.; Sou, K. Far-red fluorescent liposomes for folate receptor-targeted bioimaging. ACS Appl. Nano Mater. 2018, 1, 1009–1013. [Google Scholar] [CrossRef]
- Wagner, L.; Kenzhebayeva, B.; Dhaini, B.; Boukhlef, S.; Moussaron, A.; Mordon, S.; Frochot, C.; Collet, C.; Acherar, S. Folate-based radiotracers for nuclear imaging and radionuclide therapy. Coord. Chem. Rev. 2022, 470, 214702. [Google Scholar] [CrossRef]
- Tian, A.; Lin, R.; Yu, J.; Zhang, F.; Zheng, Q.; Yuan, X.; Sun, Z.; Zhong, Z. The differential diagnostic value of dual-phase 18F-DCFPyL PET/CT in prostate carcinoma. Prostate Cancer Prostatic Dis. 2022, 25, 351–358. [Google Scholar] [CrossRef] [PubMed]
- Correia, A.R.; Sampaio, I.; Comparetti, E.J.; Vieira, N.C.S.; Zucolotto, V. Optimized PAH/Folic acid layer-by-layer films as an electrochemical biosensor for the detection of folate receptors. Bioelectrochemistry 2021, 137, 107685. [Google Scholar] [CrossRef] [PubMed]
- Agrahari, S.; Gautam, R.K.; Singh, A.K.; Tiwari, I. Nanoscale materials-based hybrid frameworks modified electrochemical biosensors for early cancer diagnostics: An overview of current trends and challenges. Microchem. J. 2022, 172, 106980. [Google Scholar] [CrossRef]
- Mostafa, I.M.; Tian, Y.; Anjum, S.; Hanif, S.; Hosseini, M.; Lou, B.; Xu, G. Comprehensive review on the electrochemical biosensors of different breast cancer biomarkers. Sens. Actuators B Chem. 2022, 365, 131944. [Google Scholar] [CrossRef]
- Anusha, T.; Bhavani, K.S.; Kumar, J.S.; Brahman, P.K.; Hassan, R.Y. Fabrication of electrochemical immunosensor based on GCN-β-CD/Au nanocomposite for the monitoring of vitamin D deficiency. Bioelectrochemistry 2022, 143, 107935. [Google Scholar] [CrossRef] [PubMed]
- Magar, H.S.; Hassan, R.Y.; Mulchandani, A. Electrochemical impedance spectroscopy (EIS): Principles, construction, and biosensing applications. Sensors 2021, 21, 6578. [Google Scholar] [CrossRef] [PubMed]
- Ni, J.; Wang, Q.; Yang, W.; Zhao, M.; Zhang, Y.; Guo, L.; Qiu, B.; Lin, Z.; Yang, H.-H. Immobilization free electrochemical biosensor for folate receptor in cancer cells based on terminal protection. Biosens. Bioelectron. 2016, 86, 496–501. [Google Scholar] [CrossRef]
- Geetha Bai, R.; Muthoosamy, K.; Tuvikene, R.; Nay Ming, H.; Manickam, S. Highly sensitive electrochemical biosensor using folic acid-modified reduced graphene oxide for the detection of cancer biomarker. Nanomaterials 2021, 11, 1272. [Google Scholar] [CrossRef]
- Soares, A.L.; Hryniewicz, B.M.; Deller, A.E.; Volpe, J.; Marchesi, L.F.; Souto, D.E.; Vidotti, M. Electrodes based on PEDOT nanotubes decorated with gold nanoparticles for biosensing and energy storage. ACS Appl. Nano Mater. 2021, 4, 9945–9956. [Google Scholar] [CrossRef]
- Damiati, S.; Peacock, M.; Mhanna, R.; Søpstad, S.; Sleytr, U.B.; Schuster, B. Bioinspired detection sensor based on functional nanostructures of S-proteins to target the folate receptors in breast cancer cells. Sens. Actuators B Chem. 2018, 267, 224–230. [Google Scholar] [CrossRef]
- Ruiyi, L.; Fangchao, C.; Haiyan, Z.; Xiulan, S.; Zaijun, L. Electrochemical sensor for detection of cancer cell based on folic acid and octadecylamine-functionalized graphene aerogel microspheres. Biosens. Bioelectron. 2018, 119, 156–162. [Google Scholar] [CrossRef]
- Dodero, A.; Alberti, S.; Gaggero, G.; Ferretti, M.; Botter, R.; Vicini, S.; Castellano, M. An Up-to-Date Review on Alginate Nanoparticles and Nanofibers for Biomedical and Pharmaceutical Applications. Adv. Mater. Interfaces 2021, 8, 2100809. [Google Scholar] [CrossRef]
- Song, L.; Zhu, L.; Liu, Y.; Zhou, X.; Shi, H. A disposable cobalt-based phosphate sensor based on screen printing technology. Sci. China Chem. 2014, 57, 1283–1290. [Google Scholar] [CrossRef]
- Zhou, X.-H.; Liu, L.-H.; Bai, X.; Shi, H.-C. A reduced graphene oxide based biosensor for high-sensitive detection of phenols in water samples. Sens. Actuators B Chem. 2013, 181, 661–667. [Google Scholar] [CrossRef]
- Mercante, L.A.; Pavinatto, A.; Pereira, T.S.; Migliorini, F.L.; dos Santos, D.M.; Correa, D.S. Nanofibers interfaces for biosensing: Design and applications. Sens. Actuators Rep. 2021, 3, 100048. [Google Scholar] [CrossRef]
- Mokhena, T.C.; Mochane, M.J.; Mtibe, A.; John, M.J.; Sadiku, E.R.; Sefadi, J.S. Electrospun alginate nanofibers toward various applications: A review. Materials 2020, 13, 934. [Google Scholar] [CrossRef] [PubMed]
- Taemeh, M.A.; Shiravandi, A.; Korayem, M.A.; Daemi, H. Fabrication challenges and trends in biomedical applications of alginate electrospun nanofibers. Carbohydr. Polym. 2020, 228, 115419. [Google Scholar] [CrossRef] [PubMed]
- Sheldon, R.A.; Norton, M. Green chemistry and the plastic pollution challenge: Towards a circular economy. Green Chem. 2020, 22, 6310–6322. [Google Scholar] [CrossRef]
- Fang, D.; Liu, Y.; Jiang, S.; Nie, J.; Ma, G. Effect of intermolecular interaction on electrospinning of sodium alginate. Carbohydr. Polym. 2011, 85, 276–279. [Google Scholar] [CrossRef]
- Saquing, C.D.; Tang, C.; Monian, B.; Bonino, C.A.; Manasco, J.L.; Alsberg, E.; Khan, S.A. Alginate–polyethylene oxide blend nanofibers and the role of the carrier polymer in electrospinning. Ind. Eng. Chem. Res. 2013, 52, 8692–8704. [Google Scholar] [CrossRef]
- Lowe, S.; O’Brien-Simpson, N.M.; Connal, L.A. Antibiofouling polymer interfaces: Poly (ethylene glycol) and other promising candidates. Polym. Chem. 2015, 6, 198–212. [Google Scholar] [CrossRef]
- Pillay, V.; Dott, C.; Choonara, Y.E.; Tyagi, C.; Tomar, L.; Kumar, P.; du Toit, L.C.; Ndesendo, V.M. A review of the effect of processing variables on the fabrication of electrospun nanofibers for drug delivery applications. J. Nanomater. 2013, 2013, 789289. [Google Scholar] [CrossRef]
- Kalluri, L.; Duan, Y. Role of Electrospun Nanofibers in Cancer Detection and Treatment. In Nanomaterials for Cancer Detection Using Imaging Techniques and Their Clinical Applications; Springer: Cham, Switzerland, 2022; pp. 261–275. [Google Scholar]
- Sanfelice, R.C.; Mercante, L.A.; Pavinatto, A.; Tomazio, N.B.; Mendonça, C.R.; Ribeiro, S.J.; Mattoso, L.H.; Correa, D.S. Hybrid composite material based on polythiophene derivative nanofibers modified with gold nanoparticles for optoelectronics applications. J. Mater. Sci. 2017, 52, 1919–1929. [Google Scholar] [CrossRef]
- Caykara, T.; Demirci, S.; Eroğlu, M.S.; Güven, O. Poly (ethylene oxide) and its blends with sodium alginate. Polymer 2005, 46, 10750–10757. [Google Scholar] [CrossRef]
- Babeli, I.; Ruano, G.; Casanovas, J.; Ginebra, M.-P.; García-Torres, J.; Alemán, C. Conductive, self-healable and reusable poly (3, 4-ethylenedioxythiophene)-based hydrogels for highly sensitive pressure arrays. J. Mater. Chem. C 2020, 8, 8654–8667. [Google Scholar] [CrossRef]
- Wongkanya, R.; Chuysinuan, P.; Pengsuk, C.; Techasakul, S.; Lirdprapamongkol, K.; Svasti, J.; Nooeaid, P. Electrospinning of alginate/soy protein isolated nanofibers and their release characteristics for biomedical applications. J. Sci. Adv. Mater. Devices 2017, 2, 309–316. [Google Scholar] [CrossRef]
- Nie, H.; He, A.; Wu, W.; Zheng, J.; Xu, S.; Li, J.; Han, C.C. Effect of poly (ethylene oxide) with different molecular weights on the electrospinnability of sodium alginate. Polymer 2009, 50, 4926–4934. [Google Scholar] [CrossRef]
- Parın, F.N.; Aydemir, Ç.İ.; Taner, G.; Yıldırım, K. Co-electrospun-electrosprayed PVA/folic acid nanofibers for transdermal drug delivery: Preparation, characterization, and in vitro cytocompatibility. J. Ind. Text. 2022, 51, 1323S–1347S. [Google Scholar] [CrossRef]
- İnce, İ.; Yıldırım, Y.; Güler, G.; Medine, E.İ.; Ballıca, G.; Kuşdemir, B.C.; Göker, E. Synthesis and characterization of folic acid-chitosan nanoparticles loaded with thymoquinone to target ovarian cancer cells. J. Radioanal. Nucl. Chem. 2020, 324, 71–85. [Google Scholar] [CrossRef]
- Lee, S.; Lee, K. pH-sensitive folic acid conjugated alginate nanoparticle for induction of cancer-specific fluorescence imaging. Pharmaceutics 2020, 12, 537. [Google Scholar] [CrossRef]
- Baibarac, M.; Smaranda, I.; Nila, A.; Serbschi, C. Optical properties of folic acid in phosphate buffer solutions: The influence of pH and UV irradiation on the UV-VIS absorption spectra and photoluminescence. Sci. Rep. 2019, 9, 14278. [Google Scholar] [CrossRef]
- Randviir, E.P. A cross examination of electron transfer rate constants for carbon screen-printed electrodes using Electrochemical Impedance Spectroscopy and cyclic voltammetry. Electrochim. Acta 2018, 286, 179–186. [Google Scholar] [CrossRef]
- Castillo, J.J.; Svendsen, W.E.; Rozlosnik, N.; Escobar, P.; Martínez, F.; Castillo-León, J. Detection of cancer cells using a peptide nanotube–folic acid modified graphene electrode. Analyst 2013, 138, 1026–1031. [Google Scholar] [CrossRef]
- Ghalehkhondabi, V.; Fazlali, A.; Soleymani, M. Folic acid-conjugated pH-responsive poly (methacrylic acid) nanospheres for targeted delivery of anticancer drugs to breast cancer cells. J. Mol. Liq. 2022, 348, 118028. [Google Scholar] [CrossRef]
- Haider, A.; Haider, S.; Kang, I.-K. A comprehensive review summarizing the effect of electrospinning parameters and potential applications of nanofibers in biomedical and biotechnology. Arab. J. Chem. 2018, 11, 1165–1188. [Google Scholar] [CrossRef]
- Brett, C.M. Electrochemical Impedance Spectroscopy in the Characterisation and Application of Modified Electrodes for Electrochemical Sensors and Biosensors. Molecules 2022, 27, 1497. [Google Scholar] [CrossRef]
- Fan, B.; Fan, Q.; Hu, L.; Cui, M.; Wang, X.; Ma, H.; Wei, Q. Polydopamine-PEG–folic acid conjugate film engineered TiO2 nanotube arrays for photoelectrochemical sensing of folate binding protein. ACS Appl. Mater. Interfaces 2019, 12, 1877–1884. [Google Scholar] [CrossRef]
- Wang, G.; He, X.; Wang, L.; Zhang, X. A folate receptor electrochemical sensor based on terminal protection and supersandwich DNAzyme amplification. Biosens. Bioelectron. 2013, 42, 337–341. [Google Scholar] [CrossRef] [PubMed]
- Wei, X.; Lin, W.; Ma, N.; Luo, F.; Lin, Z.; Guo, L.; Qiu, B.; Chen, G. Sensitive fluorescence biosensor for folate receptor based on terminal protection of small-molecule-linked DNA. Chem. Commun. 2012, 48, 6184–6186. [Google Scholar] [CrossRef] [PubMed]
- Li, R.; Wang, C.; Hu, Y.; Zheng, O.; Guo, L.; Lin, Z.; Qiu, B.; Chen, G. Electrochemiluminescence biosensor for folate receptor based on terminal protection of small-molecule-linked DNA. Biosens. Bioelectron. 2014, 58, 226–231. [Google Scholar] [CrossRef] [PubMed]
- Kwon, B.; Park, J.; Jeong, W.; Jeong, G.; Ryu, H.S.; Paoprasert, P.; Park, S.Y.; In, I. Assembly of chemically reduced graphene oxide with folic acid functionalized with pyrene moieties and electrochemical sensing of folate receptors. Carbon Lett. 2018, 27, 26–34. [Google Scholar]
- Burke, L.D.; Blackwood, K.A.; Zomer Volpato, F. Reproducibility and robustness in electrospinning with a view to medical device manufacturing. In Electrospun Biomaterials and Related Technologies; Springer: Cham, Switzerland, 2017; pp. 1–19. [Google Scholar]
Formulations | Zeta Potential (mV) | St Dev (mV) |
---|---|---|
NFs SA-PEO | −21.4 | ±3.80 |
NFs SA-PEO/FA | −33.2 | ±7.86 |
Element | Rct (Ω) | Ks (k0/cm s−1) | Electroactive Surface Area |
---|---|---|---|
SPCE | 674.76 | 1.48 × 10−3 | 10.2 mm2 |
SPCE/SA-PEO NFs | 381.96 | 2.61 × 10−3 | 13.5 mm2 |
SPCE/SA-PEO/FA NFs | 298.07 | 3.35 × 10−3 | 14.8 mm2 |
Sensing Material | Working Electrode | FR Range of Detection | Limit of Detection (FR Conc) | Method | Reference |
---|---|---|---|---|---|
PDA–PEG–FA | ITO | FR (1 × 10−3–5 × 102 ng/mL) | (2 × 10−4 ng/mL) | EIS | [58] |
FA-DNA | Au | FR (1.0–20.0 ng/mL) | 0.3 ng/mL | CV | [59] |
PNT–FA | G | FR (8–13 nM) | 8 nM | CV | [60] |
DNA–FA | Au | FR (0.66–26.31 nM/L) | 0.1204 nM/L | CV | [61] |
PAH/FA | ITO | FR (10–40 nM) | 0.7 nM, 1.5 nM | CV, EIS | [22] |
rGO/FA-Py | G | FR (1–50 nM) | 3.07 nM | CV | [62] |
SA-PEO/FA NFs | SPE | FR (0.1 pM–100 nM) | 2.5 pM | EIS | This work |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Elnagar, N.; Elgiddawy, N.; El Rouby, W.M.A.; Farghali, A.A.; Korri-Youssoufi, H. Impedimetric Detection of Cancer Markers Based on Nanofiber Copolymers. Biosensors 2024, 14, 77. https://doi.org/10.3390/bios14020077
Elnagar N, Elgiddawy N, El Rouby WMA, Farghali AA, Korri-Youssoufi H. Impedimetric Detection of Cancer Markers Based on Nanofiber Copolymers. Biosensors. 2024; 14(2):77. https://doi.org/10.3390/bios14020077
Chicago/Turabian StyleElnagar, Noha, Nada Elgiddawy, Waleed M. A. El Rouby, Ahmed A. Farghali, and Hafsa Korri-Youssoufi. 2024. "Impedimetric Detection of Cancer Markers Based on Nanofiber Copolymers" Biosensors 14, no. 2: 77. https://doi.org/10.3390/bios14020077
APA StyleElnagar, N., Elgiddawy, N., El Rouby, W. M. A., Farghali, A. A., & Korri-Youssoufi, H. (2024). Impedimetric Detection of Cancer Markers Based on Nanofiber Copolymers. Biosensors, 14(2), 77. https://doi.org/10.3390/bios14020077