Ensuring food safety is nowadays a top priority of authorities and professional players in the food supply chain. One of the key challenges to determine the safety of food and guarantee a high level of consumer protection is the availability of fast, sensitive and reliable analytical methods to identify specific hazards associated to food before they become a health problem. The limitations of existing methods have encouraged the development of new technologies, among them biosensors. Success in biosensor design depends largely on the development of novel receptors with enhanced affinity to the target, while being stable and economical. Aptamers fulfill these characteristics, and thus have surfaced as promising alternatives to natural receptors. This Review describes analytical strategies developed so far using aptamers for the control of pathogens, allergens, adulterants, toxins and other forbidden contaminants to ensure food safety. The main progresses to date are presented, highlighting potential prospects for the future.
References
[1]
Garcia-Canas, V.; Simo, C.; Herrero, M.; Iba？ez, E.; Cifuentes, A. Present and future challenges in food analysis: Foodomics. Anal. Chem. 2012, 84, 10150–10159.
Citartan, M.; Gopinath, S.C.B.; Tominaga, J.; Tan, S.C.; Tang, T.H. Assays for aptamer-based platforms. Biosens. Bioelectron. 2012, 34, 1–11.
[4]
Pathogens and Toxins in Foods: Challenges and Interventions; Juneja, V.K., Sofos, J.N., Eds.; ASM Press: Washington, DC, USA, 2010.
[5]
Principles of Bacterial Detection: Biosensors, Recognition Receptors and Microsystems; Zourob, M., Elwary, S., Turner, A., Eds.; Springer Science+Business Media LLC: New York, NY, USA, 2008.
[6]
Hamula, C.; Zhang, H.; Li, F.; Wang, Z.; Le, X.; Li, X. Selection and analytical applications of aptamers binding microbial pathogens. TrAC Trends Anal. Chem. 2011, 30, 1587–1597.
[7]
Torres-Chavolla, E.; Alocilja, E.C. Aptasensors for detection of microbial and viral pathogens. Biosens. Bioelectron. 2009, 24, 3175–3182.
[8]
Vivekananda, J.; Kiel, J.L. Anti-Francisella tularensis DNA aptamers detect tularemia antigen from different subspecies by aptamer-linked immobilized sorbent assay. Lab. Investig. 2006, 86, 610–618.
[9]
Duan, N.; Ding, X.; He, L.; Wu, S.; Wei, Y.; Wang, Z. Selection, identification and application of a DNA aptamer against Listeria monocytogenes. Food Control 2013, 33, 239–243.
[10]
Bruno, J.G.; Phillips, T.; Carrillo, M.P.; Crowell, R. Plastic-adherent DNA aptamer-magnetic bead and quantum dot sandwich assay for Campylobacter detection. J. Fluoresc. 2009, 19, 427–435.
Yang, M.; Peng, Z.; Ning, Y.; Chen, Y.; Zhou, Q.; Deng, L. Highly specific and cost-efficient detection of Salmonella Paratyphi A combining aptamers with single-walled carbon nanotubes. Sensors 2013, 13, 6865–6881.
[13]
Lee, H.-J.; Kim, B.C.; Kim, K.-W.; Kim, Y.K.; Kim, J.; Oh, M.-K. A sensitive method to detect Escherichia coli based on immunomagnetic separation and real-time PCR amplification of aptamers. Biosens. Bioelectron. 2009, 24, 3550–3555.
[14]
Zelada-Guillen, G.A.; Riu, J.; Duezguen, A.; Rius, F.X. Immediate detection of living bacteria at ultralow concentrations using a carbon nanotube based potentiometric aptasensor. Angew. Chem. Int. Ed. 2009, 48, 7334–7337.
[15]
Zelada-Guillen, G.A.; Bhosale, S.V.; Riu, J.; Xavier Rius, F. Real-time potentiometric detection of bacteria in complex samples. Anal. Chem. 2010, 82, 9254–9260.
Ohk, S.H.; Koo, O.K.; Sen, T.; Yamamoto, C.M.; Bhunia, A.K. Antibody-aptamer functionalized fibre-optic biosensor for specific detection of Listeria monocytogenes from food. J. Appl. Microbiol. 2010, 109, 808–817.
[18]
Luo, C.; Lei, Y.; Yan, L.; Yu, T.; Li, Q.; Zhang, D.; Ding, S.; Ju, H. A rapid and sensitive aptamer-based electrochemical biosensor for direct detection of Escherichia Coli O111. Electroanalysis 2012, 24, 1186–1191.
Duan, N.; Wu, S.; Zhu, C.; Ma, X.; Wang, Z.; Yu, Y.; Jiang, Y. Dual-color upconversion fluorescence and aptamer-functionalized magnetic nanoparticles-based bioassay for the simultaneous detection of Salmonella Typhimurium and Staphylococcus aureus. Anal. Chim. Acta. 2012, 723, 1–6.
[21]
Zuo, P.; Li, X.; Dominguez, D.C.; Ye, B.-C. A PDMS/paper/glass hybrid microfluidic biochip integrated with aptamer-functionalized graphene oxide nano-biosensors for one-step multiplexed pathogen detection. Lab Chip 2013, 13, 3921–3928.
[22]
Xiao, S.J.; Hu, P.P.; Wu, X.D.; Zou, Y.L.; Chen, L.Q.; Peng, L.; Ling, J.; Zhen, S.J.; Zhan, L.; Li, Y.F.; et al. Sensitive discrimination and detection of prion disease-associated isoform with a dual-aptamer strategy by developing a sandwich structure of magnetic microparticles and Quantum Dots. Anal. Chem. 2010, 82, 9736–9742.
Lauridsen, L.H.; Veedu, R.N. Nucleic acid aptamers against biotoxins: A new paradigm toward the treatment and diagnostic approach. Nucleic Acid Ther. 2012, 22, 371–379.
[25]
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.
[26]
Cruz-Aguado, J.A.; Penner, G. Fluorescence polarization based displacement assay for the determination of small molecules with aptamers. Anal. Chem. 2008, 80, 8853–8855.
Wu, S.; Duan, N.; Wang, Z.; Wang, H. Aptamer-functionalized magnetic nanoparticle-based bioassay for the detection of ochratoxin a using upconversion nanoparticles as labels. Analyst 2011, 136, 2306–2314.
[29]
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.
[30]
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.
[31]
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.
[32]
Duan, N.; Wu, S.; Ma, X.; Chen, X.; Huang, Y.; Wang, Z. Gold nanoparticle-based fluorescence resonance energy transfer aptasensor for ochratoxin A detection. Anal. Lett. 2012, 45, 714–723.
[33]
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.
[34]
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.
[35]
Zhang, J.; Chen, J.; Zhang, X.; Zeng, Z.; Chen, M.; Wang, S. An electrochemical biosensor based on hairpin-DNA aptamer probe and restriction endonuclease for ochratoxin A detection. Electrochem. Commun. 2012, 25, 5–7.
[36]
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.
[37]
Ma, W.; Yin, H.; Xu, L.; Xu, Z.; Kuang, H.; Wang, L.; Xu, C. Femtogram ultrasensitive aptasensor for the detection of Ochratoxin A. Biosens. Bioelectron. 2013, 42, 545–549.
Wu, S.; Duan, N.; Ma, X.; Xia, Y.; Wang, H.; Wang, Z.; Zhang, Q. Multiplexed fluorescence resonance energy transfer aptasensor between upconversion nanoparticles and graphene oxide for the simultaneous determination of mycotoxins. Anal. Chem. 2012, 84, 6263–6270.
[40]
Binh, H.N.; Lam, D.T.; Quan, P.D.; Huy, L.N.; Ngoc, H.T.; Phuc, X.N. Label-free detection of aflatoxin M1 with electrochemical Fe3O4/polyaniline-based aptasensor. Mater. Sci. Eng. C 2013, 33, 2229–2234.
[41]
Prabhakar, N.; Matharu, Z.; Malhotra, B.D. Polyaniline langmuir-blodgett film based aptasensor for ochratoxin A detection. Biosens. Bioelectron. 2011, 26, 4006–4011.
[42]
Tang, J.; Yu, T.; Guo, L.; Xie, J.; Shao, N.; He, Z. In vitro selection of DNA aptamer against abrin toxin and aptamer-based abrin direct detection. Biosens. Bioelectron. 2007, 22, 2456–2463.
[43]
Lamont, E.A.; He, L.; Warriner, K.; Labuza, T.P.; Sreevatsan, S. A single DNA aptamer functions as a biosensor for ricin. Analyst 2011, 136, 3884–3895.
[44]
Koppelman, S.J.; Hefle, S.L. Detecting Allergens in Food, 1st ed. ed.; Woodhead Publishing Ltd and CRC Press LLC: Boca Raton, FL, USA, 2006.
[45]
Opinion of the Scientific Panel on Dietetic Products, Nutrition and Allergies on a request from the Commission relating to the evaluation of allergenic foods for labelling purposes. EFSA J. 2004, 32, 1–197.
[46]
Directive 2003/89/EC of the European Parliament and of the Council. Available online: http://eur-ex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2003:308:0015:0018:EN:PDF (accessed on 28 November 2013).
[47]
Commision Directive 2007/68/EC. vailable online: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=CELEX:32007L0068:EN:NOT (accessed on 28 November 2013).
[48]
Regulation (EU) 1169/2011 of the European Parliament and of the Council. Available online: http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=CELEX:32011R1169:EN:NOT (accessed on 28 November 2013).
[49]
Van Hengel, A.J. Food allergen detection methods and the challenge to protect food-allergic consumers. Anal. Bioanal. Chem. 2007, 389, 111–118.
[50]
Nadal, P.; Pinto, A.; Svobodova, M.; Canela, N.; O'Sullivan, C.K. DNA aptamers against the lup an 1 food allergen. PLoS One 2012, 7, e35253.
[51]
Tran, D.T.; Knez, K.; Janssen, K.P.; Pollet, J.; Spasic, D.; Lammertyn, J. Selection of aptamers against Ara h 1 protein for FO-SPR biosensing of peanut allergens in food matrices. Biosens. Bioelectron. 2013, 43, 245–251.
[52]
Amaya-Gonzalez, S.; de-los-Santos-Alvarez, N.; Miranda-Ordieres, A.J.; Lobo-Casta？ón, M.J. Aptámeros Específicos Contra el Gluten y Método de Detección del Gluten Asociado (in Spanish). International Patent Application PCT/ES2013/000133, 28 June 2013.
[53]
Amaya-Gonzalez, S.; de-los-Santos-Alvarez, N.; Miranda-Ordieres, A.J.; Lobo-Casta？ón, M.J. Aptamer binding to coelic disease-triggering hydrophobic proteins: Towards a sensitive gluten detection system. Anal. Chem. 2013. submitted.
[54]
La Farre, M.; Perez, S.; Kantiani, L.; Barcelo, D. Fate and toxicity of emerging pollutants, their metabolites and transformation products in the aquatic environment. TrAC Trends Anal. Chem. 2008, 27, 991–1007.
[55]
De-los-Santos-álvarez, N.; Lobo-Casta？ón, M.J.; Miranda-Ordieres, A.J.; Tu？ón-Blanco, P. Modified-RNA aptamer-based sensor for competitive impedimetric assay of neomycin B. J. Am. Chem. Soc. 2007, 129, 3808–3809.
[56]
Yan, L.; Luo, C.; Cheng, W.; Mao, W.; Zhang, D.; Ding, S. A simple and sensitive electrochemical aptasensor for determination of chloramphenicol in honey based on target-induced strand release. J. Electroanal. Chem. 2012, 687, 89–94.
[57]
Zhou, L.; Li, D.J.; Gai, L.; Wang, J.P.; Li, Y.B. Electrochemical aptasensor for the detection of tetracycline with multi-walled carbon nanotubes amplification. Sens. Actuators B: Chem. 2012, 162, 201–208.
[58]
Kim, C.-H.; Lyun-Pyo, L.; Jeong-Ran, M.; Myung-Woon, L.; Sang-Hee, J. An indirect competitive assay-based aptasensor for detection of oxytetracycline in milk. Biosens. Bioelectron. 2014, 51, 426–430.
[59]
Dapra, J.; Lauridsen, L.H.; Nielsen, A.T.; Rozlosnik, N. Comparative study on aptamers as recognition elements for antibiotics in a label-free all-polymer biosensor. Biosens. Bioelectron. 2013, 43, 315–320.
[60]
Yildirim, N.; Long, F.; Gao, C.; He, M.; Shi, H.C.; Gu, A.Z. Aptamer-based optical biosensor for rapid and sensitive detection of 17 beta-estradiol in water samples. Environ. Sci. Technol. 2012, 46, 3288–3294.
[61]
Kantiani, L.; Llorca, M.; Sanchis, J.; Farre, M.; Barcelo, D. Emerging food contaminants: A review. Anal. Bioanal. Chem. 2010, 398, 2413–2427.
[62]
Stead, S.; Ashwin, H.; Johnston, B.; Dallas, A.; Kazakov, S.; Tarbin, J.; Sharman, M.; Kay, J.; Keely, B. 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.
[63]
Fan, L.; Zhao, G.; Shi, H.; Liu, M.; Li, Z. A highly selective electrochemical impedance spectroscopy-based aptasensor for sensitive detection of acetamiprid. Biosens. Bioelectron. 2013, 43, 12–18.
[64]
Jiang, Z.; Zhou, L.; Liang, A. Resonance scattering detection of trace melamine using aptamer-modified nanosilver probe as catalyst without separation of its aggregations. Chem. Commun. 2011, 47, 3162–3164.
[65]
Liang, A.H.; Zhou, L.P.; Qin, H.M.; Zhang, Y.; Ouyang, H.X.; Jiang, Z.L. A highly sensitive aptamer-nanogold catalytic resonance scattering spectral assay for melamine. J. Fluoresc. 2011, 21, 1907–1912.
[66]
Lee, J.; Jo, M.; Kim, T.H.; Ahn, J.-Y.; Lee, D.-k.; Kim, S.; Hong, S. Aptamer sandwich-based carbon nanotube sensors for single-carbon-atomic-resolution detection of non-polar small molecular species. Lab Chip 2011, 11, 52–56.
[67]
Kim, Y.S.; Niazi, J.H.; Chae, Y.J.; Ko, U.R.; Gu, M.B. Aptamers-in-liposomes for selective and multiplexed capture of small organic compounds. Macromol. Rapid Commun. 2011, 32, 1169–1173.
[68]
Dwivedi, H.P.; Smiley, R.D.; Jaykus, L.A. Selection of DNA aptamers for capture and detection of salmonella typhimurium using a whole-cell SELEX approach in conjunction with cell sorting. Appl. Microbiol. Biotechnol. 2013, 97, 3677–3686.
[69]
Joshi, R.; Janagama, H.; Dwivedi, H.P.; Kumar, T.M.A.S.; Jaykus, L.A.; Schefers, J.; Sreevatsan, S. Selection, characterization, and application of DNA aptamers for the capture and detection of Salmonella enterica serovars. Mol. Cell. Probes. 2009, 23, 20–28.
[70]
Suh, S.H.; Jaykus, L.A. Nucleic acid aptamers for capture and detection of Listeria spp. J. Biotechnol. 2013, 167, 454–461.
Wu, X.M.; Hu, J.; Zhu, B.H.; Lu, L.; Huang, X.D.; Pang, D.W. Aptamer-targeted magnetic nanospheres as a solid-phase extraction sorbent for determination of ochratoxin A in food samples. J. Chromatogr. A 2011, 1218, 7341–7346.
[74]
Huy, G.D.; Jin, N.; Yin, B.C.; Ye, B.C. A novel separation and enrichment method of 17 beta-estradiol using aptamer-anchored microbeads. Bioprocess Biosyst. Eng. 2011, 34, 189–195.
[75]
Cruz-Aguado, J.A.; Penner, G. Determination of ochratoxin A with a DNA aptamer. J. Agric. Food Chem. 2008, 56, 10456–10461.
[76]
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.
[77]
Rhouati, A.; Paniel, N.; Meraihi, Z.; Marty, J.L. Development of an oligosorbent for detection of ochratoxin A. Food Control 2011, 22, 1790–1796.
