Advertisement

Analytical and Bioanalytical Chemistry

, Volume 410, Issue 29, pp 7575–7589 | Cite as

Versatile nano-platform for tailored immuno-magnetic carriers

  • Emanuela Bonaiuto
  • Massimiliano Magro
  • Luca Fasolato
  • Enrico Novelli
  • Saeed Shams
  • Alessandra Piccirillo
  • Bita Bakhshi
  • Tahereh Tohidi Moghadam
  • Davide Baratella
  • Fabio VianelloEmail author
Paper in Forefront

Abstract

Custom immuno-magnetic devices are desirable tools for biomedical and biotechnological applications. Herein, surface active maghemite nanoparticles (SAMNs) are proposed as a versatile platform for developing tailored immuno-magnetic nano-carriers by simple wet reactions. Two examples for conjugating native and biotinylated antibodies were presented along with their successful applications in the recognition of specific foodborne pathogens. Nanoparticles were functionalized with rhodamine B isothiocyanate (RITC), leading to a fluorescent nano-conjugate, and used for binding anti-Campylobacter fetus antibodies (SAMN@RITC@Anti-Cf). The microorganism was selectively captured in the presence of two other Campylobacter species (C. jejuni and C. coli), as verified by PCR. Alternatively, SAMNs were modified with avidin, forming a biotin-specific magnetic nano-carrier and used for the immobilization of biotinylated anti-Listeria monocytogenes antibodies (SAMN@avidin@Anti-Lm). This immuno-magnetic carrier was integrated in piezoelectric quartz crystal microbalance (QCM) sensor for the detection of L. monocytogenes in milk, showing a detection limit of 3 bacterial cells. The present work presents a new category of customized immuno-magnetic nano-carriers as a competitive option for suiting specific applications.

Graphical abstract

Keywords

Immuno-magnetic separation Magnetic nano-carrier Antibody conjugation Campylobacter fetus Listeria monocytogenes Pathogen recognition 

Abbreviations

ALOA

Agar Listeria Ottavani and Agosti medium

aPEMC

Anchored piezoelectric-excited millimeter-sized cantilever

CE

Capture efficiency

Cf

Campylobacter fetus

CFU

Colony-forming units

CMC

N-Cyclohexyl-N′-(2-morpholinoethyl) carbodiimide metho-p-toluenesulfonate

DMF

N,N-Dimethylformamide

ELISA

Enzyme-linked immunosorbent assay

FTIR

Fourier transform infrared spectroscopy

Lm

Listeria monocytogenes

LOD

Limit of detection

NHS

N-Hydroxysuccinimide

OD

Optical density

PBS

Phosphate-buffered saline

PCA

Plate count agar

PCR

Polymerase chain reaction

QCM

Quartz crystal microbalance

RITC

Rhodamine B isothiocyanate

SAMNs

Surface active maghemite nanoparticles

TEM

Transmission electron microscope

TMAOH

Tetramethylammonium perchlorate

TSA

Tryptone soya agar

TSB

Tryptone soya broth

XRPD

X-ray powder diffraction

Notes

Acknowledgements

The authors thank the electron microscopy facility of the Biology Department of Padua University and the CARIPARO Foundation for the support.

Funding information

The present experimental work was partially funded by AIPOL Reg. CE n. 867/08 S.M.I, project “Miglioramento delle condizioni di magazzinaggio e di valorizzazione dei residui della produzione di olio di oliva e delle olive da tavola” approved by the Italian Ministry for Agricolture and Forest Politics and AGEA.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Eivazzadeh-Keihan R, Pashazadeh-Panahi P, Baradaran B, Maleki A, Hejazi M, Mokhtarzadeh A, et al. Recent advances on nanomaterial based electrochemical and optical aptasensors for detection of cancer biomarkers. Trends Anal Chem. 2018;100:103–15.CrossRefGoogle Scholar
  2. 2.
    Park H, Hwang MP, Lee KH. Immunomagnetic nanoparticle-based assays for detection of biomarkers. Int J Nanomedicine. 2013;8:4543–52.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Su XL, Li YB. Quantum dot biolabeling coupled with immunomagnetic separation for detection of Escherichia coli O157:H7. Anal Chem. 2004;76:4806–10.CrossRefGoogle Scholar
  4. 4.
    Martin J, Nguyen QN. Highly multiplexed particle based assays. United States Patent US 20120202293 May 5, 2012.Google Scholar
  5. 5.
    Liu F, Zhang Y, Ge LJ, Yu J, Song X, Liu S. Magnetic graphene nanosheets based electrochemiluminescence immunoassay of cancer biomarker using CdTe quantum dots coated silica nanospheres as labels. Talanta. 2012;99:512–9.CrossRefGoogle Scholar
  6. 6.
    Xiao L, Li J, Brougham DF, Fox EK, Feliu N, Bushmelev A, et al. Water-soluble superparamagnetic magnetite nanoparticles with biocompatible coating for enhanced magnetic resonance imaging. ACS Nano. 2011;5:6315–24.CrossRefGoogle Scholar
  7. 7.
    Gupta AK, Gupta M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials. 2005;26:3995–4021.CrossRefGoogle Scholar
  8. 8.
    Wu W, He QG, Jiang CZ. Magnetic iron oxide nanoparticles: synthesis and surface functionalization strategies. Nanoscale Res Lett. 2008;3:397–415.CrossRefGoogle Scholar
  9. 9.
    Reddy LH, Arias JL, Nicolas J, Couvreur P. Magnetic nanoparticles: design and characterization, toxicity and biocompatibility, pharmaceutical and biomedical applications. Chem Rev. 2012;112:5818–78.CrossRefGoogle Scholar
  10. 10.
    Arias JL, Clares B, Morales ME, Gallardo V, Ruiz MA. Lipid based drug delivery systems for cancer treatment. Curr Drug Targets. 2011;12:1151–65.CrossRefGoogle Scholar
  11. 11.
    Portet D, Denizot B, Rump E, Lejeune JJ, Jallet P. Nonpolymeric coatings of iron oxide colloids for biological use as magnetic resonance imaging contrast agents. J Colloid Interface Sci. 2001;238:37–42.CrossRefGoogle Scholar
  12. 12.
    Kreller DI, Gibson G, Novak W, van Loon GW, Horton JH. Competitive adsorption of phosphate and carboxylate with natural organic matter on hydrous iron oxides as investigated by chemical force microscopy. Colloids Surf A Physicochem Eng Asp. 2003;212:249–64.CrossRefGoogle Scholar
  13. 13.
    Soenen SJH, Himmelreich U, Nuytten N, Pisanic TR II, Ferrari A, De Cuyper M. Intracellular nanoparticle coating stability determines nanoparticle diagnostics efficacy and cell functionality. Small. 2010;6:2136–45.CrossRefGoogle Scholar
  14. 14.
    Wu W, Wu Z, Yu T, Jiang C, Kim W-S. Recent progress on magnetic iron oxide nanoparticles: synthesis, surface functional strategies and biomedical applications. Sci Technol Adv Mater. 2015;16:023501.CrossRefGoogle Scholar
  15. 15.
    Kolhatkar AG, Jamison AC, Litvinov D, Willson RC, Lee TR. Tuning the magnetic properties of nanoparticles. Int J Mol Sci. 2013;14:15977–6009.CrossRefGoogle Scholar
  16. 16.
    Mackay ME, Tuteja A, Duxbury PM, Hawker CJ, Van Horn B, Guan Z, et al. General strategies for nanoparticle dispersion. Science. 2006;311:1740–3.CrossRefGoogle Scholar
  17. 17.
    Horak D, Babic M, Mackova H, Benes MJ. Preparation and properties of magnetic nano- and microsized particles for biological and environmental separations. J Sep Sci. 2007;30:1751–72.CrossRefGoogle Scholar
  18. 18.
    Anderson CJ, Bulte JW, Chen K, Chen X, Khaw BA, Shokeen M, et al. Design of targeted cardiovascular molecular imaging probes. J Nucl Med. 2010;51:3S–17S.CrossRefGoogle Scholar
  19. 19.
    Algar WR, Prasuhn DE, Stewart MH, Jennings TL, Blanco-Canosa JB, Dawson PE, et al. The controlled display of biomolecules on nanoparticles: a challenge suited to bioorthogonal chemistry. Bioconjug Chem. 2011;22:825–58.CrossRefGoogle Scholar
  20. 20.
    Lin P-C, Chen S-H, Wang K-Y, Chen M-L, Adak AK, Hwu J-RR, et al. Fabrication of oriented antibody-conjugated magnetic nanoprobes and their immunoaffinity application. Anal Chem. 2009;81:8774–82.CrossRefGoogle Scholar
  21. 21.
    Joshi PP, Yoon SJ, Hardin WG, Emelianov S, Sokolov KV. Conjugation of antibodies to gold nanorods through Fc portion: synthesis and molecular specific imaging. Bioconjug Chem. 2013;24:878–88.CrossRefGoogle Scholar
  22. 22.
    Song HY, Zhou X, Hobley J, Su X. Comparative study of random and oriented antibody immobilization as measured by dual polarization interferometry and surface plasmon resonance spectroscopy. Langmuir. 2012;28:997–1004.CrossRefGoogle Scholar
  23. 23.
    Sapsford KE, Algar WR, Berti L, Gemmill KB, Casey BJ, Oh E, et al. Functionalizing nanoparticles with biological molecules: developing chemistries that facilitate nanotechnology. Chem Rev. 2013;113:1904–2074.CrossRefGoogle Scholar
  24. 24.
    Redeker ES, Ta DT, Cortens D, Billen B, Guedens W, Adriaensens P. Protein engineering for directed immobilization. Bioconjug Chem. 2013;24:1761–77.CrossRefGoogle Scholar
  25. 25.
    Polo E, Puertas S, Moros M, Batalla P, Guisán JM, de la Fuente JM, et al. Tips for the functionalization of nanoparticles with antibodies. Methods Mol Biol. 2013;1051:149–63.CrossRefGoogle Scholar
  26. 26.
    Makaraviciute A, Ramanaviciene A. Site-directed antibody immobilization techniques for immunosensors. Biosens Bioelectron. 2013;50:460–71.CrossRefGoogle Scholar
  27. 27.
    Magro M, Martinello T, Bonaiuto E, Gomiero C, Baratella D, Zoppellaro G, et al. Covalently bound DNA on naked iron oxide nanoparticles: intelligent colloidal nano-vector for cell transfection. BBA Gen Sub. 2017;1861:2802–10.CrossRefGoogle Scholar
  28. 28.
    Baratella D, Magro M, Jakubec P, Bonaiuto E, de Almeida Roger J, Gerotto E, et al. Electrostatically stabilized hybrids of carbon and maghemite nanoparticles: electrochemical study and application. Phys Chem Chem Phys. 2017;19:11668–77.CrossRefGoogle Scholar
  29. 29.
    Magro M, Bonaiuto E, Baratella D, de Almeida Roger J, Jakubec P, Corraducci V, et al. Electrocatalytic nanostructured ferric tannates: characterization and application of a polyphenol nanosensor. Chem Phys Chem. 2016;17:3196–203.CrossRefGoogle Scholar
  30. 30.
    Miotto G, Magro M, Terzo M, Zaccarin M, Da Dalt L, Bonaiuto E, et al. Protein corona as a proteome fingerprint: the example of hidden biomarkers for cow mastitis. Colloids Surf B Biointerfaces. 2016;140:40–9.CrossRefGoogle Scholar
  31. 31.
    Magro M, Zaccarin M, Miotto G, Da Dalt L, Baratella D, Fariselli P, et al. Analysis of hard protein corona composition on selective iron oxide nanoparticles by MALDI-TOF mass spectrometry: identification and amplification of a hidden mastitis biomarker in milk proteome. Anal Bioanal Chem. 2018;410:2949–59.CrossRefGoogle Scholar
  32. 32.
    Sinigaglia G, Magro M, Miotto G, Cardillo S, Agostinelli E, Zboril R, et al. Catalytically active bovine serum amine oxidase bound to fluorescent and magnetically drivable nanoparticles. Int J Nanomedicine. 2012;7:2249–59.PubMedPubMedCentralGoogle Scholar
  33. 33.
    Venerando R, Miotto G, Magro M, Dallan M, Baratella D, Bonaiuto E, et al. Magnetic nanoparticles with covalently bound self-assembled protein corona for advanced biomedical applications. J Phys Chem C. 2013;117:20320–31.CrossRefGoogle Scholar
  34. 34.
    Cmiel V, Skopalik J, Polakova K, Solar J, Havrdova M, Milde D, et al. Rhodamine bound maghemite as a long-term dual imaging nanoprobe of adipose tissue-derived mesenchymal stromal cells. Eur Biophys J. 2017;46:433–44.CrossRefGoogle Scholar
  35. 35.
    Magro M, Faralli A, Baratella D, Bertipaglia I, Giannetti S, Salviulo G, et al. Avidin functionalized maghemite nanoparticles and their application for recombinant human biotinyl-SERCA purification. Langmuir. 2012;28:15392–401.CrossRefGoogle Scholar
  36. 36.
    Magro M, Russo U, Nodari L, Valle G, Vianello F. Maghemite nanoparticles and method for preparing thereof. United States Patent US 8,980,218 B2 Mar. 17, 2015.Google Scholar
  37. 37.
    Xiong QR, Cui X, Saini J, Liu DF, Shan S, Jin Y. Development of an immunomagnetic separation method for efficient enrichment of Escherichia coli O157:H7. Food Control. 2014;37:41–5.CrossRefGoogle Scholar
  38. 38.
    Jasson V, Uyttendaele M, Rajkovic A, Debevere J. Establishment of procedures provoking sub-lethal injury of Listeria monocytogenes, Campylobacter jejuni and Escherichia coli O157 to serve method performance testing. Int J Food Microbiol. 2007;118:241–9.CrossRefGoogle Scholar
  39. 39.
    Yamazaki-Matsune W, Taguchi M, Seto K, Kawahara R, Kawatsu K, Kumeda Y, et al. Development of a multiplex PCR assay for identification of Campylobacter coli, Campylobacter fetus, Campylobacter hyointestinalis subsp. hyointestinalis, Campylobacter jejuni, Campylobacter lari and Campylobacter upsaliensis. J Med Microbiol. 2007;56:1467–73.CrossRefGoogle Scholar
  40. 40.
    Ferreira MI, Magro M, Ming LC, da Silva MB, Ormond Sobreira Rodrigues LF, Zanoni do Prado D, et al. Sustainable production of high purity curcuminoids from Curcuma longa by magnetic nanoparticles: a case study in Brazil. J Clean Prod. 2017;154:233–41.CrossRefGoogle Scholar
  41. 41.
    de Almeida Roger J, Magro M, Spagnolo S, Bonaiuto E, Baratella D, Fasolato L, et al. Antimicrobial and magnetically removable tannic acid nanocarrier: a processing aid for Listeria monocytogenes treatment for food industry applications. Food Chem. 2018;267:430–6.CrossRefGoogle Scholar
  42. 42.
    Magro M, Fasolato L, Bonaiuto E, Andreani NA, Baratella D, Corraducci V, et al. Enlightening mineral iron sensing in Pseudomonas fluorescens by surface active maghemite nanoparticles: involvement of the OprF porin. Biochim Biophys Acta Gen Subj. 2016;1860:2202–10.CrossRefGoogle Scholar
  43. 43.
    Magro M, Moritz DE, Bonaiuto E, Baratella D, Terzo M, Jakubec P, et al. Citrinin mycotoxin recognition and removal by naked magnetic nanoparticles. Food Chem. 2016;203:505–12.CrossRefGoogle Scholar
  44. 44.
    Bonaiuto E, Magro M, Baratella D, Jakubec P, Sconcerle E, Terzo M, et al. Ternary hybrid γ-Fe2O3/CrVI/amine oxidase nanostructure for electrochemical sensing: application for polyamine detection in tumor tissue. Chem Eur J. 2016;22:6846–52.CrossRefGoogle Scholar
  45. 45.
    Magro M, Domeneghetti S, Baratella D, Jakubec P, Salviulo G, Bonaiuto E, et al. Colloidal surface active maghemite nanoparticles for biologically safe CrVI remediation: from core-shell nanostructures to pilot plant development. Chem Eur J. 2016;22:14219–26.CrossRefGoogle Scholar
  46. 46.
    Chemello G, Piccinetti C, Randazzo B, Carnevali O, Maradonna F, Magro M, et al. Oxytetracycline delivery in adult female zebrafish by iron oxide nanoparticles. Zebrafish. 2016;13:495–503.CrossRefGoogle Scholar
  47. 47.
    Magro M, Baratella D, Jakubec P, Zoppellaro G, Tucek J, Aparicio C, et al. Triggering mechanism for DNA electrical conductivity: reversible electron transfer between DNA and iron oxide nanoparticles. Adv Funct Mater. 2015;25:1822–31.CrossRefGoogle Scholar
  48. 48.
    Magro M, Campos R, Baratella D, Ferreira MI, Bonaiuto E, Corraducci V, et al. Magnetic purification of curcumin from Curcuma longa rhizome by novel naked maghemite nanoparticles. J Agric Food Chem. 2015;63:912–20.CrossRefGoogle Scholar
  49. 49.
    Skopalik J, Polakova K, Havrdova M, Justan I, Magro M, Milde D, et al. Mesenchymal stromal cell labeling by new uncoated superparamagnetic maghemite nanoparticles in comparison with commercial Resovist - an initial in vitro study. Int J Nanomedicine. 2014;9:5355–72.CrossRefGoogle Scholar
  50. 50.
    Gu C, Karthikeyan KG. Interaction of tetracycline with aluminum and iron hydrous oxides. Environ Sci Technol. 2005;39:2660–7.CrossRefGoogle Scholar
  51. 51.
    Rea BA, Davis JA, Waychunas GA. Studies of the reactivity of the ferrihydrite surface by iron isotopic exchange and Mössbauer spectroscopy. Clay Clay Miner. 1994;42:23–43.CrossRefGoogle Scholar
  52. 52.
    Graaf-van Bloois L, Miller WG, Yee E, Gorkiewicz G, Forbes KJ, Zomer AL, et al. Campylobacter fetus subspecies contain conserved type IV secretion systems on multiple genomic islands and plasmids. PLoS One. 2016;11:e0152832.CrossRefGoogle Scholar
  53. 53.
    Devenish J, Brooks B, Perry K, Milnes D, Burke T, McCabe D, et al. Validation of a monoclonal antibody-based capture enzyme-linked immunosorbent assay for detection of Campylobacter fetus. Clin Diagn Lab Immunol. 2005;12:1261–8.PubMedPubMedCentralGoogle Scholar
  54. 54.
    Patrick ME, Gilbert MJ, Blaser MJ, Tauxe RV, Wagenaar JA, Fitzgerald C. Human infections with new subspecies of Campylobacter fetus. Emerg Infect Dis. 2013;19:1678–80.CrossRefGoogle Scholar
  55. 55.
    Wagenaar JA, van Bergen MA, Blaser MJ, Tauxe RV, Newell DG, van Putten JP. Campylobacter fetus infections in humans: exposure and disease. Clin Infect Dis. 2014;58:1579–86.CrossRefGoogle Scholar
  56. 56.
    Yamazaki W, Taguchi M, Ishibashi M, Nukina M, Misawa N, Inoue K. Development of a loop-mediated isothermal amplification assay for sensitive and rapid detection of Campylobacter fetus. Vet Microbiol. 2009;136:393–6.CrossRefGoogle Scholar
  57. 57.
    Kaakoush NO, Castano-Rodriguez N, Mitchell HM, Man SM. Global epidemiology of Campylobacter infection. Clin Microbiol Rev. 2015;28:687–720.CrossRefGoogle Scholar
  58. 58.
    Zhao H, Liu H, Du Y, Liu S, Ni H, Wang Y, et al. Development and evaluation of an indirect enzyme-linked immunosorbent assay for the detection of antibodies against Campylobacter fetus in cattle. Res Vet Sci. 2010;88:446–51.CrossRefGoogle Scholar
  59. 59.
    Groff ACM, Kirinus JK, Sa e Silva M, Machado G, Costa MM, Vargas APC. Polymerase chain reaction for the diagnosis of bovine genital campylobacteriosis. Pesqui Vet Bras. 2010;30:1031–5.CrossRefGoogle Scholar
  60. 60.
    Varshney M, Yang L, Su X-L, Li Y. Magnetic nanoparticle-antibody conjugates for the separation of Escherichia coli O157:H7 in ground beef. J Food Prot. 2005;68:1804–11.CrossRefGoogle Scholar
  61. 61.
    Amagliani G, Brandi G, Omiccioli E, Casiere A, Bruce IJ, Magnani M. Direct detection of Listeria monocytogenes from milk by magnetic based DNA isolation and PCR. Food Microbiol. 2004;21:597–603.CrossRefGoogle Scholar
  62. 62.
    Zhou H, Gao Z, Luo G, Han L, Sun S, Wang H. Determination of Listeria monocytogenes in milk samples by signal amplification quartz crystal microbalance sensor. Anal Lett. 2010;43:312–22.CrossRefGoogle Scholar
  63. 63.
    Donnelly CW. Detection and isolation of Listeria monocytogenes from food samples: implications of sublethal injury. J AOAC Int. 2002;85:495–500.PubMedGoogle Scholar
  64. 64.
    Griffiths MW. Listeria monocytogenes: its importance in the dairy industry. J Sci Food Agric. 1989;47:133–58.CrossRefGoogle Scholar
  65. 65.
    Doyle MP, Beuchat LR. Food microbiology: fundamentals and frontiers. 3rd ed. Washington: ASM Press; 2007.Google Scholar
  66. 66.
    Germini A, Masola A, Carnevali P, Marchelli R. Simultaneous detection of Escherichia coli O175:H7, Salmonella spp., and Listeria monocytogenes by multiplex PCR. Food Control. 2009;20:733–8.CrossRefGoogle Scholar
  67. 67.
    Kim H-S, Cho I-H, Seo S-M, Jeon J-W, Paek S-H. In situ immuno-magnetic concentration-based biosensor systems for the rapid detection of Listeria monocytogenes. Mater Sci Eng C. 2012;32:160–6.CrossRefGoogle Scholar
  68. 68.
    Ryser ET, Marth EH. Listeria, listeriosis and food safety. 3rd ed. Boca Raton: CRC Press; 2007. p. 2007.Google Scholar
  69. 69.
    Vytrasova J, Zachova I, Cervenka L, Stepankova J, Pejchalova M. Non-specific reactions during immunomagnetic separation of Listeria. Food Technol Biotechnol. 2005;43:397–401.Google Scholar
  70. 70.
    Murakami T, Sumaoka J, Komiyama M. Sensitive isothermal detection of nucleic-acid sequence by primer generation–rolling circle amplification. Nucleic Acids Res. 2009;37:e19.CrossRefGoogle Scholar
  71. 71.
    Valimaa A-L, Tilsala-Timisjarvi A, Virtanen E. Rapid detection and identification methods for Listeria monocytogenes in the food chain – a review. Food Control. 2015;55:103–14.CrossRefGoogle Scholar
  72. 72.
    Amagliani G, Giammarini C, Omiccioli E, Brandi G, Magnai M. Detection of Listeria monocytogenes using a commercial PCR kit and different DNA extraction methods. Food Control. 2007;18:1137–42.CrossRefGoogle Scholar
  73. 73.
    Arora P, Sindhu A, Dilbaghi N, Chaudhury A. Biosensors as innovative tools for the detection of food borne pathogens. Biosens Bioelectron. 2011;28:1–12.CrossRefGoogle Scholar
  74. 74.
    Jiang X, Wang R, Wang Y, Su X, Ying Y, Wang J, et al. Evaluation of different micro/nanobeads used as amplifiers in QCM immunosensor for more sensitive detection of E. coli O157:H7. Biosens Bioelectron. 2011;29:23–8.CrossRefGoogle Scholar
  75. 75.
    Salmain M, Ghasemi M, Boujday S, Pradier C-M. Elaboration of a reusable immunosensor for the detection of staphylococcal enterotoxin A (SEA) in milk with a quartz crystal microbalance. Sensors Actuators B Chem. 2012;173:148–56.CrossRefGoogle Scholar
  76. 76.
    Hitchins AD, Jinneman K, Chen Y. Detection and enumeration of Listeria monocytogenes in foods and environmental samples, and enumeration of Listeria monocytogenes in foods. In: Bacteriological Analytical Manual, https://www.fda.gov/Food/FoodScienceResearch/LaboratoryMethods/ucm071400.htm; 2017.
  77. 77.
    Chen Q, Lin J, Gan C, Wang Y, Wang D, Xiong Y, et al. A sensitive impedance biosensor based on immunomagnetic separation and urease catalysis for rapid detection of Listeria monocytogenes using an immobilization-free interdigitated array microelectrode. Biosens Bioelectron. 2015;74:504–51.CrossRefGoogle Scholar
  78. 78.
    Minunni M, Mascini M, Carter RM, Jacobs MB, Lubrano GJ, Guillbault GG. A quartz crystal microbalance displacement assay for Listeria monocytogenes. Anal Chim Acta. 1996;325:169–74.CrossRefGoogle Scholar
  79. 79.
    Vaughan RD, O’Sullivan CK, Guilbault GG. Development of a quartz crystal microbalance (QCM) immunosensor for the detection of Listeria monocytogenes. Enzym Microb Technol. 2001;29:635–8.CrossRefGoogle Scholar
  80. 80.
    Nanduri V, Kim G, Morgan MT, Ess D, Hahm B-K, Kothapalli A, et al. Antibody immobilization on waveguides using a flow–through system shows improved Listeria monocytogenes detection in an automated fiber optic biosensor: RAPTOR™. Sensors. 2006;6:808–22.CrossRefGoogle Scholar
  81. 81.
    Ohk SH, Koo OK, Sen T, Yamamoto CM, Bhunia AK. Antibody–aptamer functionalized fibre-optic biosensor for specific detection of Listeria monocytogenes from food. J Appl Microbiol. 2010;109:808–17.CrossRefGoogle Scholar
  82. 82.
    Zhang L, Huang R, Liu W, Liu H, Zhou X, Xing D. Rapid and visual detection of Listeria monocytogenes based on nanoparticle cluster catalyzed signal amplification. Biosens Bioelectron. 2016;86:1–7.CrossRefGoogle Scholar
  83. 83.
    Sharma H, Mutharasan R. Rapid and sensitive immunodetection of Listeria monocytogenes in milk using a novel piezoelectric cantilever sensor. Sens Actuators B Chem. 2013;153:64–70.CrossRefGoogle Scholar
  84. 84.
    Mendonҫa M, Conrad NL, Conceição FR, Moreira AN, da Silva WP, Aleixo JAG, et al. Highly specific fiber optic immunosensor coupled with immunomagnetic separation for detection of low levels of Listeria monocytogenes and L. ivanovii. BMC Microbiol. 2012;12:275.Google Scholar
  85. 85.
    Soni DK, Ahmad R, Dubey SK. Biosensor for the detection of Listeria monocytogenes: emerging trends. Crit Rev Microbiol. 2018;44:590–608.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Emanuela Bonaiuto
    • 1
  • Massimiliano Magro
    • 1
    • 2
  • Luca Fasolato
    • 1
  • Enrico Novelli
    • 1
  • Saeed Shams
    • 1
    • 3
  • Alessandra Piccirillo
    • 1
  • Bita Bakhshi
    • 4
  • Tahereh Tohidi Moghadam
    • 5
  • Davide Baratella
    • 1
  • Fabio Vianello
    • 1
    Email author
  1. 1.Department of Comparative Biomedicine and Food ScienceUniversity of PaduaLegnaroItaly
  2. 2.Regional Centre of Advanced Technologies and MaterialsPalacký UniversityOlomoucCzech Republic
  3. 3.Cellular and Molecular Research CenterQom University of Medical SciencesQomIran
  4. 4.Department of Medical Bacteriology, Faculty of Medical SciencesTarbiat Modares UniversityTehranIran
  5. 5.Department of Nanobiotechnology, Faculty of Biological SciencesTarbiat Modares UniversityTehranIran

Personalised recommendations