Download PDF

A DNA sensor based on upconversion nanoparticles and two-dimensional dichalcogenide materials

Frontiers of Chemical Science and Engineering (2021)Cite this article

Abstract

We demonstrate the fabrication of a new DNA sensor that is based on the optical interactions occurring between oligonucleotide-coated NaYF4:Yb3+;Er3+ upconversion nanoparticles and the two-dimensional dichalcogenide materials, MoS2 and WS2. Monodisperse upconversion nanoparticles were functionalized with single-stranded DNA endowing the nanoparticles with the ability to interact with the surface of the two-dimensional materials via van der Waals interactions leading to subsequent quenching of the upconversion fluorescence. By contrast, in the presence of a complementary oligonucleotide target and the formation of double-stranded DNA, the upconversion nanoparticles could not interact with MoS2 and WS2, thus retaining their inherent fluorescence properties. Utilizing this sensor we were able to detect target oligonucleotides with high sensitivity and specificity whilst reaching a concentration detection limit as low as 5 mol·L−1, within minutes.

References

  1. 1.

    Wang J. DNA biosensors based on peptide nucleic acid (PNA) recognition layers. A review. Biosensors & Bioelectronics, 1998, 13 (7–8): 757–762

    CAS  Article  Google Scholar 

  2. 2.

    Leatherbarrow R J, Edwards P R. Analysis of molecular recognition using optical biosensors. Current Opinion in Chemical Biology, 1999, 3(5): 544–547

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  3. 3.

    Akyilmaz E, Yorganci E, Asav E. Do copper ions activate tyrosinase enzyme? A biosensor model for the solution. Bioelectrochemistry, 2010, 78(2): 155–160

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  4. 4.

    Soraya G V, Chan J X, Nguyen T C, Huynh D H, Abeyrathne C D, Chana G, Todaro M, Skafidas E, Kwan P. An interdigitated electrode biosensor platform for rapid HLA-B*15:02 genotyping for prevention of drug hypersensitivity. Biosensors & Bioelectronics, 2018, 111: 174–183

    CAS  Article  Google Scholar 

  5. 5.

    Contag C H, Bachmann M H. Advances in in vivo bioluminescence imaging of gene expression. Annual Review of Biomedical Engineering, 2002, 4(1): 235–260

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  6. 6.

    Heuer Jungemann A, El Sagheer A H, Lackie P M, Brown T, Kanaras A G. Selective killing of cells triggered by their mRNA signature in the presence of smart nanoparticles. Nanoscale, 2016, 8 (38): 16857–16861

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  7. 7.

    Halo T L, McMahon K M, Angeloni N L, Xu Y, Wang W, Chinen A B, Malin D, Strekalova E, Cryns V L, Cheng C, et al. NanoFlares for the detection, isolation, and culture of live tumor cells from human blood. Proceeding of the National Academy of Sciences of the United States of America, 2014, 111(48): 17104–17109

    CAS  Article  Google Scholar 

  8. 8.

    Mobed A, Hasanzadeh M, Ahmadalipour A, Fakhari A. Recent advances in the biosensing of neurotransmitters: material and method overviews towards the biomedical analysis of psychiatric disorders. Analytical Methods, 2020, 12(4): 557–575

    Article  Google Scholar 

  9. 9.

    Blair E O, Corrigan D K. A review of microfabricated electrochemical biosensors for DNA detection. Biosensors & Bioelectronics, 2019, 134: 57–67

    CAS  Article  Google Scholar 

  10. 10.

    Mehrvar M, Abdi M. Recent developments, characteristics, and potential applications of electrochemical biosensors. Analytical Sciences, 2004, 20(8): 1113–1126

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  11. 11.

    Matharu Z, Daggumati P, Wang L, Dorofeeva T S, Li Z D, Seker E. Nanoporous-gold-based electrode morphology libraries for investigating structure-property relationships in nucleic acid based electrochemical biosensors. ACS Applied Materials & Interfaces, 2017, 9(15): 12959–12966

    CAS  Article  Google Scholar 

  12. 12.

    Garcia T, Revenga Parraa M, Anorga L, Arana S, Pariente F, Lorenzo E. Disposable DNA biosensor based on thin-film gold electrodes for selective Salmonella detection. Sensors and Actuators. B, Chemical, 2012, 161(1): 1030–1037

    CAS  Article  Google Scholar 

  13. 13.

    Lange K, Rapp B E, Rapp M. Surface acoustic wave biosensors: a review. Analytical and Bioanalytical Chemistry, 2008, 391(5): 1509–1519

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  14. 14.

    Ten S T, Hashim U, Gopinath S C B, Liu W W, Foo K L, Sam S T, Rahman S F A, Voon C H, Nordin A N. Highly sensitive Escherichia coli shear horizontal surface acoustic wave biosensor with silicon dioxide nanostructures. Biosensors & Bioelectronics, 2017, 93: 146–154

    CAS  Article  Google Scholar 

  15. 15.

    Zhang Y L, Yang F, Sun Z Y, Li Y T, Zhang G J. A surface acoustic wave biosensor synergizing DNA-mediated in situ silver nanoparticle growth for a highly specific and signal-amplified nucleic acid assay. Analyst (London), 2017, 142(18): 3468–3476

    CAS  Article  Google Scholar 

  16. 16.

    Afzal A, Mujahid A, Schirhagl R, Bajwa S Z, Latif U, Feroz S. Gravimetric viral diagnostics: QCM based biosensors for early detection of viruses. Chemosensors, 2017, 5(1): 7

    Article  CAS  Google Scholar 

  17. 17.

    Damborsky P, Svitel J, Katrlik J. Optical biosensors. Essays in Biochemistry, 2016, 60(1): 91–100

    PubMed  PubMed Central  Article  Google Scholar 

  18. 18.

    Dey D, Goswami T. Optical biosensors: a revolution towards quantum nanoscale electronics device fabrication. Journal of Biomedicine & Biotechnology, 2011, 10(5204): 348218

    Google Scholar 

  19. 19.

    Shin Y, Perera A P, Park M K. Label-free DNA sensor for detection of bladder cancer biomarkers in urine. Sensors and Actuators. B, Chemical, 2013, 178: 200–206

    CAS  Article  Google Scholar 

  20. 20.

    Petty J T, Story S P, Hsiang J C, Dickson R M. DNA-templated molecular silver fluorophores. Journal of Physical Chemistry Letters, 2013, 4(7): 1148–1155

    CAS  Article  Google Scholar 

  21. 21.

    Nguyen H H, Park J, Kang S, Kim M. Surface plasmon resonance: a versatile technique for biosensor applications. Sensors (Basel), 2015, 15(5): 10481–10510

    CAS  Article  Google Scholar 

  22. 22.

    Patil P O, Pandey G R, Patil A G, Borse V B, Deshmukh P K, Patil D R, Tade R S, Nangare S N, Khan Z G, Patil A M, et al. Graphene-based nanocomposites for sensitivity enhancement of surface plasmon resonance sensor for biological and chemical sensing: a review. Biosensors & Bioelectronics, 2019, 139: 111324

    CAS  Article  Google Scholar 

  23. 23.

    Shi J Y, Tian F, Lyu J, Yang M. Nanoparticle based fluorescence resonance energy transfer (FRET) for biosensing applications. Journal of Materials Chemistry. B, Materials for Biology and Medicine, 2015, 3(35): 6989–7005

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  24. 24.

    Schuster J, Brabandt J, Von Borczyskowski C. Discrimination of photoblinking and photobleaching on the single molecule level. Journal of Luminescence, 2007, 127(1): 224–229

    CAS  Article  Google Scholar 

  25. 25.

    Frangioni J V. In vivo near-infrared fluorescence imaging. Current Opinion in Chemical Biology, 2003, 7(5): 626–634

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  26. 26.

    Smith A M, Mancini M C, Nie S M. Bioimaging second window for in vivo imaging. Nature Nanotechnology, 2009, 4(11): 710–711

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  27. 27.

    Binnemans K. Lanthanide-based luminescent hybrid materials. Chemical Reviews, 2009, 109(9): 4283–4374

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  28. 28.

    Wang X, Valiev R R, Ohulchanskyy T Y, Agren H, Yang C, Chen G. Dye-sensitized lanthanide-doped upconversion nanoparticles. Chemical Society Reviews, 2017, 46(14): 4150–4167

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  29. 29.

    Wang Y F, Liu G Y, Sun L D, Xiao J W, Zhou J C, Yan C H. Nd3+-sensitized upconversion nanophosphors: efficient in vivo bioimaging probes with minimized heating effect. ACS Nano, 2013, 7(8): 7200–7206

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  30. 30.

    Liu J, Liu Y, Bu W, Bu J, Sun Y, Du J, Shi J. Ultrasensitive nanosensors based on upconversion nanoparticles for selective hypoxia imaging in vivo upon near-infrared excitation. Journal of the American Chemical Society, 2014, 136(27): 9701–9709

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  31. 31.

    Chen Z, Chen H, Hu H, Yu M, Li F, Zhang Q, Zhou Z, Yi T, Huang C. Versatile synthesis strategy for carboxylic acid-functionalized upconverting nanophosphors as biological labels. Journal of the American Chemical Society, 2008, 130(10): 3023–3029

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  32. 32.

    Huang Y X, Shi Y M, Yang H Y, Ai Y. A novel single-layered MoS2 nanosheet based microfluidic biosensor for ultrasensitive detection of DNA. Nanoscale, 2015, 7(6): 2245–2249

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  33. 33.

    Wu M, Kempaiah R, Huang P J J, Maheshwari V, Liu J W. Adsorption and desorption of DNA on graphene oxide studied by fluorescently labeled oligonucleotides. Langmuir, 2011, 27(6): 2731–2738

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  34. 34.

    Alonso Cristobal P, Vilela P, El Sagheer A, Lopez Cabarcos E, Brown T, Muskens O L, Rubio Retama J, Kanaras A G. Highly sensitive DNA sensor based on upconversion nanoparticles and graphene oxide. ACS Applied Materials & Interfaces, 2015, 7(23): 12422–12429

    CAS  Article  Google Scholar 

  35. 35.

    Vilela P, El Sagheer A, Millar T M, Brown T, Muskens O L, Kanaras A G. Graphene oxide-upconversion nanoparticle based optical sensors for targeted detection of mRNA biomarkers present in Alzheimer’s disease and prostate cancer. ACS Sensors, 2017, 2 (1): 52–56

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  36. 36.

    Giust D, Lucio M I, El Sagheer A H, Brown T, Williams L E, Muskens O L, Kanaras A G. Graphene oxide-upconversion nanoparticle based portable sensors for assessing nutritional deficiencies in crops. ACS Nano, 2018, 12(6): 6273–6279

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  37. 37.

    Huang L J, Tian X, Yi J T, Yu R Q, Chu X. A turn-on upconversion fluorescence resonance energy transfer biosensor for ultrasensitive endonuclease detection. Analytical Methods, 2015, 7(18): 7474–7479

    CAS  Article  Google Scholar 

  38. 38.

    Wang F F, Qu X T, Liu D X, Ding C P, Zhang C L, Xian Y Z. Upconversion nanoparticles-MoS2 nanoassembly as a fluorescent turn-on probe for bioimaging of reactive oxygen species in living cells and zebrafish. Sensors and Actuators. B, Chemical, 2018, 274: 180–187

    CAS  Article  Google Scholar 

  39. 39.

    Lu C, Liu Y B, Ying Y B, Liu J W. Comparison of MoS2,WS2, and graphene oxide for DNA adsorption and sensing. Langmuir, 2017, 33(2): 630–637

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  40. 40.

    Kenry G A, Zhang X, Zhang H, Lim C T. Highly sensitive and selective aptamer-based fluorescence detection of a malarial biomarker using single-layer MoS2 nanosheets. ACS Sensors, 2016, 1(11): 1315–1321

    CAS  Article  Google Scholar 

  41. 41.

    Lv J J, Zhao S, Wu S J, Wang Z P. Upconversion nanoparticles grafted molybdenum disulfide nanosheets platform for microcystin-LR sensing. Biosensors & Bioelectronics, 2017, 90: 203–209

    CAS  Article  Google Scholar 

  42. 42.

    Yuan Y, Yu H, Yin Y. A highly sensitive aptasensor for vascular endothelial growth factor based on fluorescence resonance energy transfer from upconversion nanoparticles to MoS2 nanosheets. Analytical Methods: Advancing Methods and Applications, 2020, 12(36): 4466–4472

    CAS  Article  Google Scholar 

  43. 43.

    Li Z Q, Zhang Y. An efficient and user-friendly method for the synthesis of hexagonal-phase NaYF4:Yb, Er/Tm nanocrystals with controllable shape and upconversion fluorescence. Nanotechnology, 2008, 19(34): 345606

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  44. 44.

    Wang F, Deng R R, Liu X G. Preparation of core-shell NaGdF4 nanoparticles doped with luminescent lanthanide ions to be used as upconversion-based probes. Nature Protocols, 2014, 9(7): 1634–1644

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  45. 45.

    Lin W, Fritz K, Guerin G, Bardajee G R, Hinds S, Sukhovatkin V, Sargent E H, Scholes G D, Winnik M A. Highly luminescent lead sulfide nanocrystals in organic solvents and water through ligand exchange with poly(acrylic acid). Langmuir, 2008, 24(15): 8215–8219

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  46. 46.

    Wang M, Abbineni G, Clevenger A, Mao C B, Xu S K. Upconversion nanoparticles: synthesis, surface modification and biological applications. Nanomedicine; Nanotechnology, Biology, and Medicine, 2011, 7(6): 710–729

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. 47.

    Huang X Y, Lin J. Active-core/active-shell nanostructured design: an effective strategy to enhance Nd3+/Yb3+ cascade sensitized upconversion luminescence in lanthanide-doped nanoparticles. Journal of Materials Chemistry. C, Materials for Optical and Electronic Devices, 2015, 3(29): 7652–7657

    CAS  Article  Google Scholar 

  48. 48.

    Nie Z Y, Ke X X, Li D N, Zhao Y L, Zhu L L, Qiao R, Zhang X L. NaYF4:Yb,Er,Nd@NaYF4:Nd upconversion nanocrystals capped with Mn:TiO2 for 808 nm NIR-triggered photocatalytic applications. Journal of Physical Chemistry C, 2019, 123(37): 22959–22970

    CAS  Article  Google Scholar 

  49. 49.

    Neema P M, Tomy A M, Cyriac J. Chemical sensor platforms based on fluorescence resonance energy transfer (FRET) and 2D materials. Trac-Trends in Analytical Chemistry, 2020, 124: 115797

    CAS  Article  Google Scholar 

  50. 50.

    Hu Y L, Huang Y, Tan C L, Zhang X, Lu Q P, Sindoro M, Huang X, Huang W, Wang L H, Zhang H. Two-dimensional transition metal dichalcogenide nanomaterials for biosensing applications. Materials Chemistry Frontiers, 2017, 1(1): 24–36

    CAS  Article  Google Scholar 

Download references

Acknowledgements

Antonios G. Kanaras, Otto L. Muskens and Davide Giust would like to acknowledge funding from BBSRC (Grant No. BB/ N021150/1). Konstantina Alexaki would like to thank the University of Southampton for a Mayflower doctor of philosophy studentship.

Author information

Author notes

  1. These authors contributed equally to this work.

Affiliations

  1. School of Physics and Astronomy, Faculty of Engineering and Physical Sciences, University of Southampton, Southampton, SO17 1BJ, UK

    Konstantina Alexaki, Davide Giust, Maria-Eleni Kyriazi, Otto L. Muskens & Antonios G. Kanaras

  2. Department of Chemistry, University of Oxford, Chemistry Research Laboratory, Oxford, OX1 3TA, UK

    Afaf H. El-Sagheer & Tom Brown

  3. Chemistry Branch, Department of Science and Mathematics, Faculty of Petroleum and Mining Engineering, Suez University, Suez, 43721, Egypt

    Afaf H. El-Sagheer

  4. Institute for Life Sciences, University of Southampton, Southampton, SO17 1BJ, UK

    Otto L. Muskens & Antonios G. Kanaras

Authors
  1. Konstantina Alexaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Davide Giust
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maria-Eleni Kyriazi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Afaf H. El-Sagheer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tom Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Otto L. Muskens
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Antonios G. Kanaras
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Antonios G. Kanaras.

Supporting Information

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Alexaki, K., Giust, D., Kyriazi, ME. et al. A DNA sensor based on upconversion nanoparticles and two-dimensional dichalcogenide materials. Front. Chem. Sci. Eng. (2021). https://doi.org/10.1007/s11705-020-2023-9

Download citation

Keywords

  • upconversion nanoparticles
  • DNA sensor
  • two-dimensional materials
  • MoS2
  • WS2