A DNA sensor based on upconversion nanoparticles and two-dimensional dichalcogenide materials
Konstantina Alexaki1, Davide Giust1, Maria-Eleni Kyriazi1, Afaf H. El-Sagheer2,3, Tom Brown2, Otto L. Muskens1,4, Antonios G. Kanaras1,4()
1. School of Physics and Astronomy, Faculty of Engineering and Physical Sciences, University of Southampton, Southampton SO17 1BJ, UK 2. Department of Chemistry, University of Oxford, Chemistry Research Laboratory, Oxford OX1 3TA, UK 3. Chemistry Branch, Department of Science and Mathematics, Faculty of Petroleum and Mining Engineering, Suez University, Suez 43721, Egypt 4. Institute for Life Sciences, University of Southampton, Southampton SO17 1BJ, UK
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.
. [J]. Frontiers of Chemical Science and Engineering, 2021, 15(4): 935-943.
Konstantina Alexaki, Davide Giust, Maria-Eleni Kyriazi, Afaf H. El-Sagheer, Tom Brown, Otto L. Muskens, Antonios G. Kanaras. A DNA sensor based on upconversion nanoparticles and two-dimensional dichalcogenide materials. Front. Chem. Sci. Eng., 2021, 15(4): 935-943.
J Wang. DNA biosensors based on peptide nucleic acid (PNA) recognition layers. A review. Biosensors & Bioelectronics, 1998, 13(7-8): 757–762 https://doi.org/10.1016/S0956-5663(98)00039-6
2
R J Leatherbarrow, P R Edwards. Analysis of molecular recognition using optical biosensors. Current Opinion in Chemical Biology, 1999, 3(5): 544–547 https://doi.org/10.1016/S1367-5931(99)00006-X
3
E Akyilmaz, E Yorganci, E Asav. Do copper ions activate tyrosinase enzyme? A biosensor model for the solution. Bioelectrochemistry, 2010, 78(2): 155–160 https://doi.org/10.1016/j.bioelechem.2009.09.007
4
G V Soraya, J X Chan, T C Nguyen, D H Huynh, C D Abeyrathne, G Chana, M Todaro, E Skafidas, P Kwan. An interdigitated electrode biosensor platform for rapid HLA-B*15:02 genotyping for prevention of drug hypersensitivity. Biosensors & Bioelectronics, 2018, 111: 174–183 https://doi.org/10.1016/j.bios.2018.01.063
A Heuer Jungemann, A H El Sagheer, P M Lackie, T Brown, A G Kanaras. Selective killing of cells triggered by their mRNA signature in the presence of smart nanoparticles. Nanoscale, 2016, 8(38): 16857–16861 https://doi.org/10.1039/C6NR06154K
7
T L Halo, K M McMahon, N L Angeloni, Y Xu, W Wang, A B Chinen, D Malin, E Strekalova, V L Cryns, C Cheng, 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
8
A Mobed, M Hasanzadeh, A Ahmadalipour, A Fakhari. 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 https://doi.org/10.1039/C9AY02390A
9
E O Blair, D K Corrigan. A review of microfabricated electrochemical biosensors for DNA detection. Biosensors & Bioelectronics, 2019, 134: 57–67 https://doi.org/10.1016/j.bios.2019.03.055
10
M Mehrvar, M Abdi. Recent developments, characteristics, and potential applications of electrochemical biosensors. Analytical Sciences, 2004, 20(8): 1113–1126 https://doi.org/10.2116/analsci.20.1113
11
Z Matharu, P Daggumati, L Wang, T S Dorofeeva, Z D Li, E Seker. 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 https://doi.org/10.1021/acsami.6b15212
12
T Garcia, M Revenga Parraa, L Anorga, S Arana, F Pariente, E Lorenzo. Disposable DNA biosensor based on thin-film gold electrodes for selective Salmonella detection. Sensors and Actuators. B, Chemical, 2012, 161(1): 1030–1037 https://doi.org/10.1016/j.snb.2011.12.002
13
K Lange, B E Rapp, M Rapp. Surface acoustic wave biosensors: a review. Analytical and Bioanalytical Chemistry, 2008, 391(5): 1509–1519 https://doi.org/10.1007/s00216-008-1911-5
14
S T Ten, U Hashim, S C B Gopinath, W W Liu, K L Foo, S T Sam, S F A Rahman, C H Voon, A N Nordin. Highly sensitive Escherichia coli shear horizontal surface acoustic wave biosensor with silicon dioxide nanostructures. Biosensors & Bioelectronics, 2017, 93: 146–154 https://doi.org/10.1016/j.bios.2016.09.035
15
Y L Zhang, F Yang, Z Y Sun, Y T Li, G J Zhang. 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 https://doi.org/10.1039/C7AN00988G
16
A Afzal, A Mujahid, R Schirhagl, S Z Bajwa, U Latif, S Feroz. Gravimetric viral diagnostics: QCM based biosensors for early detection of viruses. Chemosensors, 2017, 5(1): 7 https://doi.org/10.3390/chemosensors5010007
D Dey, T Goswami. Optical biosensors: a revolution towards quantum nanoscale electronics device fabrication. Journal of Biomedicine & Biotechnology, 2011, 10(5204): 348218 https://doi.org/10.1155/2011/348218
19
Y Shin, A P Perera, M K Park. Label-free DNA sensor for detection of bladder cancer biomarkers in urine. Sensors and Actuators. B, Chemical, 2013, 178: 200–206 https://doi.org/10.1016/j.snb.2012.12.057
20
J T Petty, S P Story, J C Hsiang, R M Dickson. DNA-templated molecular silver fluorophores. Journal of Physical Chemistry Letters, 2013, 4(7): 1148–1155 https://doi.org/10.1021/jz4000142
21
H H Nguyen, J Park, S Kang, M Kim. Surface plasmon resonance: a versatile technique for biosensor applications. Sensors (Basel), 2015, 15(5): 10481–10510 https://doi.org/10.3390/s150510481
22
P O Patil, G R Pandey, A G Patil, V B Borse, P K Deshmukh, D R Patil, R S Tade, S N Nangare, Z G Khan, A M Patil, 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 https://doi.org/10.1016/j.bios.2019.111324
23
J Y Shi, F Tian, J Lyu, M Yang. 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 https://doi.org/10.1039/C5TB00885A
24
J Schuster, J Brabandt, C Von Borczyskowski. Discrimination of photoblinking and photobleaching on the single molecule level. Journal of Luminescence, 2007, 127(1): 224–229 https://doi.org/10.1016/j.jlumin.2007.02.028
A M Smith, M C Mancini, S M Nie. Bioimaging second window for in vivo imaging. Nature Nanotechnology, 2009, 4(11): 710–711 https://doi.org/10.1038/nnano.2009.326
27
K Binnemans. Lanthanide-based luminescent hybrid materials. Chemical Reviews, 2009, 109(9): 4283–4374 https://doi.org/10.1021/cr8003983
28
X Wang, R R Valiev, T Y Ohulchanskyy, H Agren, C Yang, G Chen. Dye-sensitized lanthanide-doped upconversion nanoparticles. Chemical Society Reviews, 2017, 46(14): 4150–4167 https://doi.org/10.1039/C7CS00053G
29
Y F Wang, G Y Liu, L D Sun, J W Xiao, J C Zhou, C H Yan. Nd3+-sensitized upconversion nanophosphors: efficient in vivo bioimaging probes with minimized heating effect. ACS Nano, 2013, 7(8): 7200–7206 https://doi.org/10.1021/nn402601d
30
J Liu, Y Liu, W Bu, J Bu, Y Sun, J Du, J Shi. 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 https://doi.org/10.1021/ja5042989
31
Z Chen, H Chen, H Hu, M Yu, F Li, Q Zhang, Z Zhou, T Yi, C Huang. Versatile synthesis strategy for carboxylic acid-functionalized upconverting nanophosphors as biological labels. Journal of the American Chemical Society, 2008, 130(10): 3023–3029 https://doi.org/10.1021/ja076151k
32
Y X Huang, Y M Shi, H Y Yang, Y Ai. A novel single-layered MoS2 nanosheet based microfluidic biosensor for ultrasensitive detection of DNA. Nanoscale, 2015, 7(6): 2245–2249 https://doi.org/10.1039/C4NR07162J
33
M Wu, R Kempaiah, P J J Huang, V Maheshwari, J W Liu. Adsorption and desorption of DNA on graphene oxide studied by fluorescently labeled oligonucleotides. Langmuir, 2011, 27(6): 2731–2738 https://doi.org/10.1021/la1037926
34
P Alonso Cristobal, P Vilela, A El Sagheer, E Lopez Cabarcos, T Brown, O L Muskens, J Rubio Retama, A G Kanaras. Highly sensitive DNA sensor based on upconversion nanoparticles and graphene oxide. ACS Applied Materials & Interfaces, 2015, 7(23): 12422–12429 https://doi.org/10.1021/am507591u
35
P Vilela, A El Sagheer, T M Millar, T Brown, O L Muskens, A G Kanaras. 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 https://doi.org/10.1021/acssensors.6b00651
36
D Giust, M I Lucio, A H El Sagheer, T Brown, L E Williams, O L Muskens, A G Kanaras. Graphene oxide-upconversion nanoparticle based portable sensors for assessing nutritional deficiencies in crops. ACS Nano, 2018, 12(6): 6273–6279 https://doi.org/10.1021/acsnano.8b03261
37
L J Huang, X Tian, J T Yi, R Q Yu, X Chu. A turn-on upconversion fluorescence resonance energy transfer biosensor for ultrasensitive endonuclease detection. Analytical Methods, 2015, 7(18): 7474–7479 https://doi.org/10.1039/C5AY01169H
38
F F Wang, X T Qu, D X Liu, C P Ding, C L Zhang, Y Z Xian. 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 https://doi.org/10.1016/j.snb.2018.07.125
39
C Lu, Y B Liu, Y B Ying, J W Liu. Comparison of MoS2, WS2, and graphene oxide for DNA adsorption and sensing. Langmuir, 2017, 33(2): 630–637 https://doi.org/10.1021/acs.langmuir.6b04502
40
G A Kenry, X Zhang, H Zhang, C T Lim. Highly sensitive and selective aptamer-based fluorescence detection of a malarial biomarker using single-layer MoS2 nanosheets. ACS Sensors, 2016, 1(11): 1315–1321 https://doi.org/10.1021/acssensors.6b00449
41
J J Lv, S Zhao, S J Wu, Z P Wang. Upconversion nanoparticles grafted molybdenum disulfide nanosheets platform for microcystin-LR sensing. Biosensors & Bioelectronics, 2017, 90: 203–209 https://doi.org/10.1016/j.bios.2016.09.110
42
Y Yuan, H Yu, Y Yin. 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 https://doi.org/10.1039/D0AY01067G
43
Z Q Li, Y Zhang. 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 https://doi.org/10.1088/0957-4484/19/34/345606
44
F Wang, R R Deng, X G Liu. 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 https://doi.org/10.1038/nprot.2014.111
45
W Lin, K Fritz, G Guerin, G R Bardajee, S Hinds, V Sukhovatkin, E H Sargent, G D Scholes, M A Winnik. Highly luminescent lead sulfide nanocrystals in organic solvents and water through ligand exchange with poly(acrylic acid). Langmuir, 2008, 24(15): 8215–8219 https://doi.org/10.1021/la800568k
46
M Wang, G Abbineni, A Clevenger, C B Mao, S K Xu. Upconversion nanoparticles: synthesis, surface modification and biological applications. Nanomedicine; Nanotechnology, Biology, and Medicine, 2011, 7(6): 710–729 https://doi.org/10.1016/j.nano.2011.02.013
47
X Y Huang, J Lin. 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 https://doi.org/10.1039/C5TC01438G
48
Z Y Nie, X X Ke, D N Li, Y L Zhao, L L Zhu, R Qiao, X L Zhang. 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 https://doi.org/10.1021/acs.jpcc.9b05234
49
P M Neema, A M Tomy, J Cyriac. Chemical sensor platforms based on fluorescence resonance energy transfer (FRET) and 2D materials. Trac-Trends in Analytical Chemistry, 2020, 124: 115797 https://doi.org/10.1016/j.trac.2019.115797
50
Y L Hu, Y Huang, C L Tan, X Zhang, Q P Lu, M Sindoro, X Huang, W Huang, L H Wang, H Zhang. Two-dimensional transition metal dichalcogenide nanomaterials for biosensing applications. Materials Chemistry Frontiers, 2017, 1(1): 24–36 https://doi.org/10.1039/C6QM00195E