Experimental and theoretical study for miR-155 detection through resveratrol interaction with nucleic acids using magnetic core-shell nanoparticles

Abstract

A novel electrochemical nanobiosensor for the detection of miR-155 (as breast cancer biomarker) is introduced . Fe3O4NPs@Ag core-shell nanoparticles were synthesized and their shape and characteristics were confirmed by scanning electron microscope (SEM) imaging, Fourier-transform infrared spectroscopy (FTIR), and X-ray diffraction (XRD) methods. Synthesized nanoparticles were applied onto the magnetic bar carbon paste electrode and then the amine-modified anti-miR-155 (single-stranded probes) was applied on the modified electrode surface and upon hybridization with target miR-155, resveratrol (RSV) was eventually applied as an electrochemical label on the double-strand oligonucleotide. Differential pulse voltammetry (DPV) of the oxidation peak of RSV was assumed as the final signal by sweeping potential from 0 to 0.6 V (vs. Ag/AgCl). The fabrication process was optimized through a series of experiments and the optimized process was confirmed using cyclic voltammetry (CV) and electrochemical impedance spectroscopy (EIS). The linear range of the fabricated nanobiosensor was 0.5 fM to 1.0 nM and the detection limit was 0.15 fM. The nanobiosensor was able to pass reproducibility and specificity tests using different types of mismatched target sequences.Spiked real samples of human serum were used to confirm that the nanobiosensor enables detection of miR-155 without any significant interferences from other moieties and molecules. Finally, the molecular dynamics simulation of the RSV interaction with single- and double-stranded oligonucleotide was performed and confirmed the preferential binding of RSV to double-stranded DNA; therefore, it can be used as the electrochemical label of DNA and/or miRNA hybridization–based biosensors.

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References

  1. 1.

    Siegel R, Ma J, Zou Z, Jemal A (2014) Cancer statistic, 2014. CA Cancer J Clin 64:9–29

    Article  Google Scholar 

  2. 2.

    Yazdanparast S, Benvidi A, Banaei M, Nikukar H, Dehghani M, Azimzadeh M (2018) Dual-aptamer based electrochemical sandwich biosensor for MCF-7 human breast cancer cells using silver nanoparticle labels and a poly (glutamic acid)/MWNT nanocomposite. Microchim Acta 185:405

    Article  CAS  Google Scholar 

  3. 3.

    Chang J, Wang X, Wang J, Li H, Li F (2019) Nucleic acid-functionalized metal–organic framework-based homogeneous electrochemical biosensor for simultaneous detection of multiple tumor biomarkers. Anal Chem 91:3604–3610

    Article  CAS  Google Scholar 

  4. 4.

    Liu S, Su W, Li Z, Ding X (2015) Electrochemical detection of lung cancer specific microRNAs using 3D DNA origami nanostructures. Biosens Bioelectron 71:57–61

    Article  CAS  Google Scholar 

  5. 5.

    Azimzadeh M, Nasirizadeh N, Rahaie M, Naderi-Manesh H (2017) Early detection of Alzheimer’s disease using a biosensor based on electrochemically-reduced graphene oxide and gold nanowires for the quantification of serum microRNA-137. RSC Adv 7:55709–55719

    Article  CAS  Google Scholar 

  6. 6.

    Wu X, Chai Y, Zhang P, Yuan R (2015) An electrochemical biosensor for sensitive detection of MicroRNA-155: combining target recycling with cascade catalysis for signal amplification. ACS Appl Mater Interfaces 7:713–720

    Article  CAS  Google Scholar 

  7. 7.

    Labute P (2008) Molecular operating environment. Chemical Computing Group. Inc, Montreal

    Google Scholar 

  8. 8.

    Wu L, Qu X (2015) Cancer biomarker detection: recent achievements and challenges. Chem Soc Rev 44:2963–2997

    Article  CAS  Google Scholar 

  9. 9.

    Gerber PR, Müller K (1995) MAB a generally applicable molecular force field for structure modelling in medicinal chemistry. J Comput Aid Mol Des 9:251–268

    Article  CAS  Google Scholar 

  10. 10.

    Stewart JJ (1990) MOPAC: a semiempirical molecular orbital program. J Comput aid mol des 4:1–103

    Article  Google Scholar 

  11. 11.

    Naïm M, Bhat S, Rankin KN, Dennis S, Chowdhury SF, Siddiqi I, Drabik P, Sulea T, Bayly C, Jakalian A, Purisima E (2007) Solvated interaction energy (SIE) for scoring protein− ligand binding affinities. 1. Exploring the parameter space. J Chem Inf Model 47:122–133

    Article  CAS  Google Scholar 

  12. 12.

    Corbeil CR, Williams CI, Labute P (2012) Variability in docking success rates due to dataset preparation. J Comput Aid Mol Des 26:775–786

    Article  CAS  Google Scholar 

  13. 13.

    Kong D, Bi S, Wang Z, Xia J, Zhang F (2016) In situ growth of three-dimensional graphene films for signal-on electrochemical biosensing of various analytes. Anal Chem 88:10667–10674

    Article  CAS  Google Scholar 

  14. 14.

    Akbarnia A, Zare H (2018) A voltammetric assay for microRNA-25 based on the use of amino-functionalized graphene quantum dots and ss- and ds-DNAs as gene probes. Microchim Acta 185:503

    Article  CAS  Google Scholar 

  15. 15.

    Jou AFJ, Chen YJ, Li Y, Chang YF, Lee JJ, Liao AT, Ho JA (2017) Target-triggered, dual amplification strategy for sensitive electrochemical detection of a lymphoma-associated MicroRNA. Electrochim Acta 236:190–197

    Article  CAS  Google Scholar 

  16. 16.

    Mohammadniaei M, Yoon J, Lee T, Choi J-W (2018) Spectroelectrochemical detection of microRNA-155 based on functional RNA immobilization onto ITO/GNP nanopattern. Search Results Featured snippet from the web J Biotechnol 274:40–46

  17. 17.

    Peng Y, Yi G, Gao Z (2010) A highly sensitive microRNA biosensor based on ruthenium oxide nanoparticle-initiated polymerization of aniline. Chem Commun 46:9131–9133

    Article  CAS  Google Scholar 

  18. 18.

    Baraldi PG, Bovero A, Fruttarolo F, Preti D, Tabrizi MA, Pavani MG, Romagnoli R (2004) DNA minor groove binders as potential antitumor and antimicrobial agents. Med Res Rev 24:475–528

    Article  CAS  Google Scholar 

  19. 19.

    Turner PR, Denny WA (1996) The mutagenic properties of DNA minor-groove binding ligands. Mutation research/fundamental and molecular mechanisms of mutagenesis. Mutat Res 355:141–169

    Article  Google Scholar 

  20. 20.

    Martinez R, Chacon-Garcia L (2005) The search of DNA-intercalators as antitumoral drugs: what it worked and what did not work. Curr Med Chem 12:127–151

    Article  CAS  Google Scholar 

  21. 21.

    Wheate NJ, Brodie CR, Collins JG, Kemp S, Aldrich-Wright JR (2007) DNA intercalators in cancer therapy: organic and inorganic drugs and their spectroscopic tools of analysis. Mini-Rev Med Chem 7:627–648

    Article  CAS  Google Scholar 

  22. 22.

    Rafiee-Pour H-A, Behpour M, Keshavarz M (2016) A novel labelfree electrochemical miRNA biosensor using methylene blue as redox indicator: application to breast cancer biomarker miRNA-21. Biosens Bioelectron 77:202–207

    Article  CAS  Google Scholar 

  23. 23.

    Xia N, Wang X, Deng D, Wang G, Zhai H, Li S-J (2013) Label-free electrochemical sensor for MicroRNAs detection with ferroceneboronic acids as redox probes. Int J Electrochem Sci 8:9714–9722

    CAS  Google Scholar 

  24. 24.

    Azimzadeh M, Rahaie M, Nasirizadeh N, Ashtari K, Naderi-Manesh H (2016) An electrochemical nanobiosensor for plasma miRNA-155, based on graphene oxide and gold nanorod, for early detection of breast cancer. Biosens Bioelectron 77:99–106

    Article  CAS  Google Scholar 

  25. 25.

    Lopez-Hernández J, Paseiro-Losada P, Sanches-Silva AT, Lange-Yusty MA (2007) Study of the changes of trans-resveratrol caused by ultraviolet light and determination of trans- and cis-resveratrol in Spanish white wines. Eur Food Res Technol 225:789–796

    Article  CAS  Google Scholar 

  26. 26.

    Chen LZ, Yao L, Jiao MM, Shi JB, Tan Y, Ruan BF, Liu XH (2019) Novel resveratrol-based flavonol derivatives: synthesis and anti-inflammatory activity in vitro and in vivo. Eur J Med Chem 175:114–128

    Article  CAS  Google Scholar 

  27. 27.

    Zhang SH, Sun X, Jing ZH, Qu F (2011) Spectroscopic analysis on the resveratrol–DNA binding interactions at physiological pH. Spectrochim Acta A 82:213–216

    Article  CAS  Google Scholar 

  28. 28.

    Tran HV, Piro B, Reisberg S, Huy Nguyen L, Dung Nguyen T, Duc HT, Pham MC (2014) An electrochemical ELISA-like immunosensor for miRNAs detection based on screen-printed gold electrodes modified with reduced graphene oxide and carbon nanotubes. Biosens Bioelectron 62:25–30

    Article  CAS  Google Scholar 

  29. 29.

    Huang YL, Mo S, Gao ZF, Chen JR, Lei JL, Luo HQ, Li NB (2017) Amperometric biosensor for microRNA based on the use of tetrahedral DNA nanostructure probes and guanine nanowire amplification. Microchim Acta 184:2597–2604

    Article  CAS  Google Scholar 

  30. 30.

    Wu X, Chai Y, Yuan R, Su H, Han J (2013) A novel label-free electrochemical microRNA biosensor using Pd nanoparticles as enhancer and linker. Analyst 138:1060–1066

    Article  CAS  Google Scholar 

  31. 31.

    Wu X, Chai Y, Yuan R, Zhuo Y, Chen Y (2014) Dual signal amplification strategy for enzyme-free electrochemical detection of microRNAs. Sens Actuators B: Chemical 203:296–302

    Article  CAS  Google Scholar 

  32. 32.

    Farzin L, Shamsipur M, Samandari L, Sheibani SH (2018) Signalling probe displacement electrochemical aptasensor for malignant cell surface nucleolin as a breast cancer biomarker based on gold nanoparticle decorated hydroxyapatite nanorods and silver nanoparticle labels. Microchim Acta 154

  33. 33.

    Liu G, Jiang W, Wang Y, Zhong S, Sun D, Liu J, Li F (2015) One-pot synthesis of Ag@Fe3O4/reduced graphene oxide composite with excellent electromagnetic absorption properties. Ceram Int 41:4982–4988

    Article  CAS  Google Scholar 

  34. 34.

    Benvidi A, Jahanbani SH (2016) Self-assembled monolayer of SH-DNA strand on a magnetic bar carbon paste electrode modified with Fe3O4@Ag nanoparticles for detection of breast cancer mutation. J Electroanal Chem 768:47–54

    Article  CAS  Google Scholar 

  35. 35.

    Ahmadian Fard-Finia SH, Salavati-Niasaria M, Ghanbari D (2018) Hydrothermal green synthesis of magnetic Fe3O4-carbon dots by lemon and grape fruit extracts and as a photoluminescence sensor for detecting of E. coli bacteria. Spectrochim Acta A 203:481–493

    Article  CAS  Google Scholar 

  36. 36.

    Salimi A, Kavosia B, Navaeea A (2019) Amine-functionalized graphene as an effective electrochemical platform toward easily miRNA hybridization detection. Measurment 143:191–198

    Google Scholar 

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Correspondence to Ali Benvidi or Mostafa Azimzadeh.

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Yazdanparast, S., Benvidi, A., Azimzadeh, M. et al. Experimental and theoretical study for miR-155 detection through resveratrol interaction with nucleic acids using magnetic core-shell nanoparticles. Microchim Acta 187, 479 (2020). https://doi.org/10.1007/s00604-020-04447-9

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Keywords

  • Breast cancer
  • Electrochemical nanobiosensors
  • Differential pulse voltammetrymiR-155, Magnetic nanoparticle
  • Resveratrol indicator
  • Molecular docking