Selection and characterization of a novel DNA aptamer for label-free fluorescence biosensing of ochratoxin A

Toxins

Volumn 6, Issue 8, 2014, Pages 2435-2452

  McKeague, Maureen ^a,b   Velu, Ranganathan ^b   Hill, Kayla ^b   Bardóczy, Viola ^c   Mészáros, Tamás ^d,e   DeRosa, Maria C ^b  

^a Stanford University   (United States)

^b CARLETON UNIVERSITY   (Canada)

^c BUDAPEST UNIVERSITY OF TECHNOLOGY AND ECONOMICS   (Hungary)

^d SEMMELWEIS UNIVERSITY   (Hungary)

^e INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Aptamer; Aptasensor; Biosensing; Fluorescent assay; In vitro selection; Mycotoxins; Ochratoxin A; SELEX; SYBR green I

Indexed keywords

APTAMER; OCHRATOXIN;

ANALYTICAL PARAMETERS; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; GENETIC PROCEDURES; LIMIT OF DETECTION; LINEARITY; ROBUSTNESS; SELECTIVITY; SENSITIVITY; COMBINATORIAL CHEMISTRY; FLUORESCENCE; FOOD CONTAMINATION; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE;

APTAMERS, NUCLEOTIDE; BASE SEQUENCE; BIOSENSING TECHNIQUES; FLUORESCENCE; FOOD CONTAMINATION; MOLECULAR SEQUENCE DATA; OCHRATOXINS; SELEX APTAMER TECHNIQUE;

EID: 84927171253     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins6082435     Document Type: Article

References (71)

1. Van Der Merwe, K.J.; Steyn, P.S.; Fourie, L.; Scott, D.B.; Theron, J.J. Ochratoxin A, A toxic metabolite produced by aspergillus ochraceus wilh. Nature 1965, 205, 1112-1113.
2. Duarte, S.C.; Lino, C.M.; Pena, A. Mycotoxin food and feed regulation and the specific case of ochratoxin A: A review of the worldwide status. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 2010, 27, 1440-1450.
3. Tittlemier, S.A.; Varga, E.; Scott, P.M.; Krska, R. Sampling of cereals and cereal-based foods for the determination of ochratoxin A: An overview. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 2011, 28, 775-785.
4. Mayura, K.; Parker, R.; Berndt, W.O.; Phillips, T.D. Ochratoxin A-induced teratogenesis in rats: Partial protection by phenylalanine. Appl. Environ. Microbiol. 1984, 48, 1186-1188.
5. Creppy, E.E.; Chiarappa, P.; Baudrimont, I.; Borracci, P.; Moukha, S.; Carratù, M.R. Synergistic effects of fumonisin B1 and ochratoxin A: Are In vitro cytotoxicity data predictive of In vivo acute toxicity? Toxicology 2004, 201, 115-123.
6. Pitout, M.J. The effect of ochratoxin A on glycogen storage in the rat liver. Toxicol. Appl. Pharmacol. 1968, 13, 299-306.
7. Creppy, E.E.; Stormer, F.C.; Roschenthaler, R.; Dirheimer, G. Effects of two metabolites of ochratoxin A, (4R)-4-hydroxyochratoxin A and ochratoxin alpha, on immune response in mice. Infect. Immun. 1983, 39, 1015-1018.
8. Pfohl-Leszkowicz, A.; Manderville, R.A. Ochratoxin A: An overview on toxicity and carcinogenicity in animals and humans. Mol. Nutr. Food Res. 2007, 51, 61-99.
9. Creppy, E.E.; Lugnier, A.A.J.; Fasiolo, F.; Heller, K.; Röschenthaler, R.; Dirheimer, G. In vitro inhibition of yeast phenylalanyl-tRNA synthetase by ochratoxin A. Chem.-Biol. Interact. 1979, 24, 257-261.
10. European Union. Commission regulation (Ec) No. 123/2005 Of 26 January 2005 amending regulation (Ec) No. 466/2001 as regards ochratoxin A. Off. J. Eur. Union 2005, L25, 3-5.
11. Entwisle, A.C.; Williams, A.C.; Mann, P.J.; Russell, J.; Slack, P.T.; Gilbert, J. Combined phenyl silane and immunoaffinity column cleanup with liquid chromatography for determination of ochratoxin A in roasted coffee: Collaborative study. J. AOAC Int. 2001, 84, 444-450.
12. Visconti, A.; de Girolamo, A. Fitness for purpose-Ochratoxin A analytical developments. Food Addit. Contam. 2005, 22 (Suppl. 1), 37-44.
13. Tuerk, C.; Gold, L. Systematic evolution of ligands by exponential enrichment: RNA ligands to bacteriophage T4 DNA polymerase. Science 1990, 249, 505-510.
14. Ellington, A.D.; Szostak, J.W. In vitro selection of RNA molecules that bind specific ligands. Nature 1990, 346, 818-822.
15. Cho, E.J.; Lee, J.W.; Ellington, A.D. Applications of aptamers as sensors. Annu. Rev. Anal. Chem. 2009, 2, 241-264.
16. Mckeague, M.; Giamberardino, A.; DeRosa, M.C. Advances in aptamer-based biosensors for food safety. In Environmental Biosensors; Somerset, V., Ed.; Intech: Rijeka, Croatia, 2011; pp. 17-42.
17. Mckeague, M.; DeRosa, M.C. Challenges and opportunities for small molecule aptamer development. J. Nucleic Acids 2012, 2012, 748913.
18. Stead, S.L.; Ashwin, H.; Johnston, B.; Dallas, A.; Kazakov, S.A.; Tarbin, J.A.; Sharman, M.; Kay, J.; Keely, B.J. An RNA-aptamer-based assay for the detection and analysis of malachite green and leucomalachite green residues in fish tissue. Anal. Chem. 2010, 82, 2652-2660.
19. Cruz-Aguado, J.A.; Penner, G. Determination of ochratoxin A with a DNA aptamer. J. Agric. Food Chem. 2008, 56, 10456-10461.
20. Sheng, L.; Ren, J.; Miao, Y.; Wang, J.; Wang, E. Pvp-coated graphene oxide for selective determination of ochratoxin A via quenching fluorescence of free aptamer. Biosens. Bioelectron. 2011, 26, 3494-3499.
21. Huizenga, D.E.; Szostak, J.W. A DNA aptamer that binds adenosine and Atp. Biochemistry 1995, 34, 656-665.
22. Barthelmebs, L.; Jonca, J.; Hayat, A.; Prieto-Simon, B.; Marty, J.-L. Enzyme-linked aptamer assays (Elaas), based on a competition format for a rapid and sensitive detection of ochratoxin A in wine. Food Control 2011, 22, 737-743.
23. Silverman, S.K. Artificial functional nucleic acids: Aptamers, ribozymes, and deoxyribozymes identified by in vitro selection. Funct. Nucleic Acids Anal. Appl. 2009, 1, 47-108.
24. Rhouati, A.; Yang, C.; Hayat, A.; Marty, J.-L. Aptamers: A promosing tool for ochratoxin A detection in food analysis. Toxins 2013, 5, 1988-2008.
25. De Girolamo, A.; Mckeague, M.; Miller, J.D.; DeRosa, M.C.; Visconti, A. Determination of ochratoxin A in wheat after clean-up through a DNA aptamer-based solid phase extraction column. Food Chem. 2011, 127, 1378-1384.
26. Wang, L.; Chen, W.; Ma, W.; Liu, L.; Ma, W.; Zhao, Y.; Zhu, Y.; Xu, L.; Kuang, H.; Xu, C. Fluorescent strip sensor for rapid determination of toxins. Chem. Commun. 2011, 47, 1574-1576.
27. Guo, Z.; Ren, J.; Wang, J.; Wang, E. Single-walled carbon nanotubes based quenching of free fam-aptamer for selective determination of ochratoxin A. Talanta 2011, 85, 2517-2521.
28. Chen, J.; Fang, Z.; Liu, J.; Zeng, L. A simple and rapid biosensor for ochratoxin A based on a structure-switching signaling aptamer. Food Control 2012, 25, 555-560.
29. Zhang, J.; Zhang, X.; Yang, G.; Chen, J.; Wang, S. A signal-on fluorescent aptasensor based on Tb3+ and structure-switching aptamer for label-free detection of ochratoxin A in wheat. Biosens. Bioelectron. 2013, 41, 704-709.
30. Zhao, Q.; Geng, X.; Wang, H. Fluorescent sensing ochratoxin A with single fluorophore-labeled aptamer. Anal. Bioanal. Chem. 2013, 405, 6281-6286.
31. Yang, C.; Lates, V.; Prieto-Simon, B.; Marty, J.L.; Yang, X. Aptamer-dnazyme hairpins for biosensing of ochratoxin A. Biosens. Bioelectron. 2012, 32, 208-212.
32. Yang, C.; Lates, V.; Prieto-Simon, B.; Marty, J.L.; Yang, X. Rapid high-throughput analysis of ochratoxin A by the self-assembly of dnazyme-aptamer conjugates in wine. Talanta 2013, 116, 520-526.
33. Wang, Z.; Duan, N.; Hun, X.; Wu, S. Electrochemiluminescent aptamer biosensor for the determination of ochratoxin A at a gold-nanoparticles-modified gold electrode using N-(aminobutyl)-N-ethylisoluminol as a luminescent label. Anal. Bioanal. Chem. 2010, 398, 2125-2132.
34. Kuang, H.; Chen, W.; Xu, D.; Xu, L.; Zhu, Y.; Liu, L.; Chu, H.; Peng, C.; Xu, C.; Zhu, S. Fabricated aptamer-based electrochemical "signal-off" sensor of ochratoxin A. Biosens. Bioelectron. 2010, 26, 710-716.
35. Prabhakar, N.; Matharu, Z.; Malhotra, B.D. Polyaniline langmuir-blodgett film based aptasensor for ochratoxin A detection. Biosens. Bioelectron. 2011, 26, 4006-4011.
36. Bonel, L.; Vidal, J.C.; Duato, P.; Castillo, J.R. An electrochemical competitive biosensor for ochratoxin A based on a DNA biotinylated aptamer. Biosens. Bioelectron. 2011, 26, 3254-3259.
37. Rhouati, A.; Hayat, A.; Hernandez, D.B.; Meraihi, Z.; Munoz, R.; Marty, J.-L. Development of an automated flow-based electrochemical aptasensor for on-line detection of ochratoxin A. Sens. Actuators B 2013, 176, 1160-1166.
38. Wu, J.; Chu, H.; Mei, Z.; Deng, Y.; Xue, F.; Zheng, L.; Chen, W. Ultrasensitive one-step rapid detection of ochratoxin A by the folding-based electrochemical aptasensor. Anal. Chim. Acta 2012, 753, 27-31.
39. Castillo, G.; Lamberti, I.; Mosiello, L.; Hianik, T. Impedimetric DNA aptasensor for sensitive detection of ochratoxin A in food. Electroanalysis 2012, 24, 512-520.
40. Tong, P.; Zhang, L.; Xu, J.J.; Chen, H.Y. Simply amplified electrochemical aptasensor of ochratoxin A based on exonuclease-catalyzed target recycling. Biosens. Bioelectron. 2011, 29, 97-101.
41. Tong, P.; Zhao, W.W.; Zhang, L.; Xu, J.J.; Chen, H.Y. Double-probe signal enhancing strategy for toxin aptasensing based on rolling circle amplification. Biosens. Bioelectron. 2012, 33, 146-151.
42. Hayat, A.; Sassolas, A.; Marty, J.L.; Radi, A.E. Highly sensitive ochratoxin A impedimetric aptasensor based on the immobilization of azido-aptamer onto electrografted binary film via click chemistry. Talanta 2013, 103, 14-19.
43. Zhu, Z.; Yang, C.; Zhou, X.; Qin, J. Label-free aptamer-based sensors for L-argininamide by using nucleic acid minor groove binding dyes. Chem. Commun. 2011, 47, 3192-3194.
44. Tan, Y.; Zhang, X.; Xie, Y.; Zhao, R.; Tan, C.; Jiang, Y. Label-free fluorescent assays based on aptamer-target recognition. Analyst 2012, 137, 2309-2312.
45. Babendure, J.R.; Adams, S.R.; Tsien, R.Y. Aptamers switch on fluorescence of triphenylmethane dyes. J. Am. Chem. Soc. 2003, 125, 14716-14717.
46. Jin, Y.; Bai, J.; Li, H. Label-free protein recognition using aptamer-based fluorescence assay. Analyst 2010, 135, 1731-1735.
47. Huang, C.C.; Chang, H.T. Aptamer-based fluorescence sensor for rapid detection of potassium ions in urine. Chem. Commun. 2008, 1461-1463.
48. Cruz-Toledo, J.; Mckeague, M.; Zhang, X.; Giamberardino, A.; Mcconnell, E.; Francis, T.; Derosa, M.C.; Dumontier, M. Aptamer base: A collaborative knowledge base to describe aptamers and selex experiments. Database: J. Biol. Databases Curation 2012, 2012, Bas006.
49. Tok, J.B.; Fischer, N.O. Single microbead selex for efficient ssdna aptamer generation against botulinum neurotoxin. Chem. Commun. 2008, 1883-1885.
50. Bock, L.C.; Griffin, L.C.; Latham, J.A.; Vermaas, E.H.; Toole, J.J. Selection of single-stranded DNA molecules that bind and inhibit human thrombin. Nature 1992, 355, 564-566.
51. Mathews, D.H.; Disney, M.D.; Childs, J.L.; Schroeder, S.J.; Zuker, M.; Turner, D.H. Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc. Natl. Acad. Sci. USA 2004, 101, 7287-7292.
52. Luo, X.; Mckeague, M.; Pitre, S.; Dumontier, M.; Green, J.; Golshani, A.; DeRosa, M.C.; Dehne, F. Computational approaches toward the design of pools for the in vitro selection of complex aptamers. RNA (N. Y.) 2010, 16, 2252-2262.
53. Kikin, O.; D'antonio, L.; Bagga, P.S. Qgrs mapper: A web-based server for predicting G-quadruplexes in nucleotide sequences. Nucleic Acids Res. 2006, 34, W676-W682.
54. Mergny, J.L.; Phan, A.T.; Lacroix, L. Following G-quartet formation by Uv-spectroscopy. FEBS Lett. 1998, 435, 74-78.
55. Darty, K.; Denise, A.; Ponty, Y. Varna: Interactive drawing and editing of the RNA secondary structure. Bioinformatics 2009, 25, 1974-1975.
56. Mckeague, M.; Bradley, C.R.; de Girolamo, A.; Visconti, A.; Miller, J.D.; DeRosa, M.C. Screening and initial binding assessment of fumonisin B1 aptamers. Int. J. Mol. Sci. 2010, 11, 4864-4881.
57. Mckeague, M.; Foster, A.; Miguel, Y.; Giamberardino, A.; Verdin, C.; Chan, J.Y.S.; DeRosa, M.C. Development of a DNA aptamer for direct and selective homocysteine detection in human serum. RSC Adv. 2013, 3, 24415-24422.
58. Chang, A.L.; Mckeague, M.; Liang, J.C.; Smolke, C.D. Kinetic and equilibrium binding characterization of aptamers to small molecules using a label-free, sensitive, and scalable platform. Anal. Chem. 2014, 86, 3273-3278.
59. Carothers, J.M.; Goler, J.A.; Kapoor, Y.; Lara, L.; Keasling, J.D. Selecting RNA aptamers for synthetic biology: Investigating magnesium dependence and predicting binding affinity. Nucleic Acids Res. 2010, 38, 2736-2747.
60. Zipper, H.; Brunner, H.; Bernhagen, J.; Vitzthum, F. Investigations on DNA intercalation and surface binding by sybr green I, its structure determination and methodological implications. Nucleic Acids Res. 2004, 32, E103.
61. Schmidt, D.M.; Ernst, J.D. A fluorometric assay for the quantification of RNA in solution with nanogram sensitivity. Anal. Biochem. 1995, 232, 144-146.
62. Wittwer, C.T.; Herrmann, M.G.; Gundry, C.N.; Elenitoba-Johnson, K.S. Real-time multiplex pcr assays. Methods 2001, 25, 430-442.
63. Wittwer, C.T.; Ririe, K.M.; Andrew, R.V.; David, D.A.; Gundry, R.A.; Balis, U.J. The lightcycler: A microvolume multisample fluorimeter with rapid temperature control. Biotechniques 1997, 22, 176-181.
64. Suzuki, T.; Fujikura, K.; Higashiyama, T.; Takata, K. DNA staining for fluorescence and laser confocal microscopy. J. Histochem. Cytochem.: Off. J. Histochem. Soc. 1997, 45, 49-53.
65. Sarpong, K.; Datta, B. Nucleic-acid-binding chromophores as efficient indicators of aptamer-target interactions. J. Nucleic Acids 2012, 2012, 247-280.
66. Kong, L.; Xu, J.; Xu, Y.; Xiang, Y.; Yuan, R.; Chai, Y. A universal and label-free aptasensor for fluorescent detection of ATP and thrombin based on SYBR green I dye. Biosens. Bioelectron. 2013, 42, 193-197.
67. Xu, Y.; Xu, J.; Xiang, Y.; Yuan, R.; Chai, Y. Target-induced structure switching of hairpin aptamers for label-free and sensitive fluorescent detection of ATP via exonuclease-catalyzed target recycling amplification. Biosens. Bioelectron. 2014, 51, 293-296.
68. Armbruster, D.A.; Pry, T. Limit of blank, limit of detection and limit of quantitation. Clin. Biochem. Rev./Aust. Assoc. Clin. Biochem. 2008, 29 (Suppl. 1), S49-S52.
69. Carothers, J.M.; Oestreich, S.C.; Szostak, J.W. Aptamers selected for higher-affinity binding are not more specific for the target ligand. J. Am. Chem. Soc. 2006, 128, 7929-7937.
70. Murphy, M.B.; Fuller, S.T.; Richardson, P.M.; Doyle, S.A. An improved method for the in vitro evolution of aptamers and applications in protein detection and purification. Nucleic Acids Res. 2003, 31, E110.
71. Rosenthal, A.; Coutelle, O.; Craxton, M. Large-scale production of DNA sequencing templates by microtitre format Pcr. Nucleic Acids Res. 1993, 21, 173-174.