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Antibody-based magneto-elastic biosensors: potential devices for detection of pathogens and associated toxins

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Abstract

This work describes the design and development process of an immunosensor. The creation of such devices goes through various steps, which complement each other, and choosing an efficient immobilization method that binds to a specific target is essential to achieve satisfactory diagnostic results. In this perspective, the emphasis here is on developing biosensors based on binding antigens/antibodies on particular surfaces of magneto-elastic sensors. Different aspects leading to the improvement of these sensors, such as the antibody structure, the chemical functionalization of the surface, and cross-linking antibody reticulation were summarized and discussed. This paper deals with the progress of magneto-elastic immunosensors to detect bacterial pathogens and associated toxins. Biologically modified surface characterization methods are further considered. Thus, research opportunities and trends of future development in these areas are finally discussed.

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References

  • Ahmed A, Rushworth JV, Wright JD, Millner PA (2013) Novel impedimetric immunosensor for detection of pathogenic bacteria Streptococcus pyogenes in human saliva. Anal Chem 85(24):12118–12125. doi:10.1021/ac403253j

    Article  CAS  PubMed  Google Scholar 

  • Allara DL, Nuzzo RG (1985) Spontaneously organized molecular assemblies. 1. Formation, dynamics, and physical properties of n-alkanoic acids adsorbed from solution on an oxidized aluminum surface. Langmuir 1(1):45–52. doi:10.1021/la00061a007

    Article  CAS  Google Scholar 

  • Amit AG, Mariuzza RA, Phillips SE, Poljak RJ (1986) Three-dimensional structure of an antigen-antibody complex at 2.8 A resolution. Science 233(4765):747–753. doi:10.1126/science.2426778

    Article  CAS  PubMed  Google Scholar 

  • Arkan E, Saber R, Karimi Z, Shamsipur M (2015) A novel antibody-antigen based impedimetric immunosensor for low level detection of HER2 in serum samples of breast cancer patients via modification of a gold nanoparticles decorated multiwall carbon nanotube-ionic liquid electrode. Anal Chim Acta 874:66–74. doi:10.1016/j.aca.2015.03.022

    Article  CAS  PubMed  Google Scholar 

  • Arlett JL, Myers EB, Roukes ML (2011) Comparative advantages of mechanical biosensors. Nat Nanotechnol 6(4):203–215. doi:10.1038/nnano.2011.44

    Article  CAS  PubMed  Google Scholar 

  • Awsiuk K, Budkowski A, Petrou P, Bernasik A, Marzec MM, Kakabakos S, Rysz J, Raptis I (2013) Model immunoassay on silicon surfaces: vertical and lateral nanostructure vs. protein coverage. Colloids Surf B: Biointerfaces 103:253–260. doi:10.1016/j.colsurfb.2012.10.047

    Article  CAS  PubMed  Google Scholar 

  • Ayyad AH, Stettner J, Magnussen OM (2005) Electrocompression of the Au(111) surface layer during Au electrodeposition. Phys Rev Lett 94(6):066106. doi:10.1103/PhysRevLett.94.066106

    Article  CAS  PubMed  Google Scholar 

  • Barton AC, Collyer SD, Davis F, Garifallou GZ, Tsekenis G, Tully E, O’Kennedy R, Gibson T, Millner PA, Higson SP (2009) Labeless AC impedimetric antibody-based sensors with pgml(−1) sensitivities for point-of-care biomedical applications. Biosens Bioelectron 24(5):1090–1095. doi:10.1016/j.bios.2008.06.001

    Article  CAS  PubMed  Google Scholar 

  • Baselt DR, Lee GU, Natesan M, Metzger SW, Sheehan PE, Colton RJ (1998) A biosensor based on magnetoresistence technology. Biosens Bioelectron 13:721–729. doi:10.1016/S0956-5663(98)00037-2

    Google Scholar 

  • Basu J, Datta S, RoyChaudhuri C (2015) A graphene field effect capacitive immunosensor for sub-femtomolar food toxin detection. Biosens Bioelectron 68:544–549. doi:10.1016/j.bios.2015.01.046

    Article  CAS  PubMed  Google Scholar 

  • Berkenpas E, Millard P, Pereira da Cunha M (2006) Detection of Escherichia coli O157:H7 with langasite pure shear horizontal surface acoustic wave sensors. Biosens Bioelectron 21(12):2255–2262. doi:10.1016/j.bios.2005.11.005

    Article  CAS  PubMed  Google Scholar 

  • Bhadra P, Shajahan MS, Bhattacharya E, Chadha A (2015) Studies on varying n-alkanethiol chain lengths on a gold coated surface and their effect on antibody-antigen binding efficiency. RSC Adv 5(98):80480–80487. doi:10.1039/C5RA11725A

    Article  CAS  Google Scholar 

  • Bigelow WC, Glass E, Zisman WA (1947) Oleophobic monolayers; temperature effects and energy of adsorption. J Colloid Sci 2(6):563–591. doi:10.1016/0095-8522(47)90058-5

    Article  CAS  PubMed  Google Scholar 

  • Bjorck L, Kronvall G (1984) Purification and some properties of streptococcal protein G, a novel IgG-binding reagent. J Immunol 133(2):969–974

    CAS  PubMed  Google Scholar 

  • Blodgett KB (1935) Films built by depositing successive monomolecular layers on a solid surface. J Am Chem Soc 57(6):1007–1022. doi:10.1021/ja01309a011

    Article  CAS  Google Scholar 

  • Bordeaux J, Welsh A, Agarwal S, Killiam E, Baquero M, Hanna J, Anagnostou V, Rimm D (2010) Antibody validation. Biotechniques 48(3):197–209. doi:10.2144/000113382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Braden BC, Goldman ER, Mariuzza RA, Poljak RJ (1998) Anatomy of an antibody molecule: structure, kinetics, thermodynamics and mutational studies of the antilysozyme antibody D1.3. Immunol Rev 163:45–57. doi:10.1111/j.1600-065X.1998.tb01187.x

    Article  CAS  PubMed  Google Scholar 

  • Burshtain D, Mandler D (2006) The effect of surface attachment on ligand binding: studying the association of Mg2+, Ca2+ and Sr2+ by 1-thioglycerol and 1,4-dithiothreitol monolayers. Phys Chem Chem Phys 8(1):158–164. doi:10.1039/b511285k

    Article  CAS  PubMed  Google Scholar 

  • Butler JE, Ni L, Nessler R, Joshi KS, Suter M, Rosenberg B, Chang J, Brown WR, Cantarero LA (1992) The physical and functional behavior of capture antibodies adsorbed on polystyrene. J Immunol Methods 150(1–2):77–90. doi:10.1016/0022-1759(92)90066-3

    Article  CAS  PubMed  Google Scholar 

  • Byrne B, Gilmartin N, Lakshmanan RS, O’Kennedy R (2015) 3 - antibodies, enzymes, and nucleic acid sensors for high throughput screening of microbes and toxins in food. In: Bhunia AK, Kim MS, Taitt CR (eds) High throughput screening for food safety assessment. Woodhead Publishing, Cambridge, pp. 25–80

    Google Scholar 

  • Carrigan SD, Scott G, Tabrizian M (2005) Real-time QCM-D immunoassay through oriented antibody immobilization using cross-linked hydrogel biointerfaces. Langmuir 21(13):5966–5973. doi:10.1021/la0503294

    Article  CAS  PubMed  Google Scholar 

  • Cerrutti BM, Moraes ML, Pulcinelli SH, Santilli CV (2015) Lignin as immobilization matrix for HIV p17 peptide used in immunosensing. Biosens Bioelectron 71:420–426. doi:10.1016/j.bios.2015.04.054

    Article  CAS  PubMed  Google Scholar 

  • Chai Y, Li S, Horikawa S, Park M-K, Vodyanoy V, Chin BA (2012) Rapid and sensitive detection of Salmonella typhimurium on eggshells by using wireless biosensors. J Food Prot 75(4):631–636. doi:10.4315/0362-028X.JFP-11-339

    Article  PubMed  Google Scholar 

  • Chen L, Li J, ThanhThuy TT, Zhou L, Huang C, Yuan L, Cai Q (2014) A wireless and sensitive detection of octachlorostyrene using modified AuNPs as signal-amplifying tags. Biosens Bioelectron 52:427–432. doi:10.1016/j.bios.2013.08.026

    Article  CAS  PubMed  Google Scholar 

  • Chiang PL, Chou TC, Wu TH, Li CC, Liao CD, Lin JY, Tsai MH, Tsai CC, Sun CJ, Wang CH, Fang JM, Chen YT (2012) Nanowire transistor-based ultrasensitive virus detection with reversible surface functionalization. Chem Asian J 7(9):2073–2079. doi:10.1002/asia.201200222

    Article  CAS  PubMed  Google Scholar 

  • Chin BA, Cheng Z, Li S, Park MK, Horikawa S, Chai Y, Weerakoon K, Best SR, Baltazar-Lopez ME, Wikle HC (2014) In-situ pathogen detection using magnetoelastic sensors. Google Patents

  • Chinwangso P, Jamison AC, Lee TR (2011) Multidentate adsorbates for self-assembled monolayer films. Acc Chem Res 44(7):511–519. doi:10.1021/ar200020s

    Article  CAS  PubMed  Google Scholar 

  • Cohn C, Leung SL, Zha Z, Crosby J, Teng W, Wu X (2015) Comparative study of antibody immobilization mediated by lipid and polymer fibers. Colloids Surf B: Biointerfaces 134:1–7. doi:10.1016/j.colsurfb.2015.06.021

    Article  CAS  PubMed  Google Scholar 

  • Conroy PJ, Hearty S, Leonard P, O’Kennedy RJ (2009) Antibody production, design and use for biosensor-based applications. Semin Cell Dev Biol 20(1):10–26. doi:10.1016/j.semcdb.2009.01.010

    Article  CAS  PubMed  Google Scholar 

  • Crudden CM, Horton JH, Ebralidze II, Zenkina OV, McLean AB, Drevniok B, She Z, Kraatz H-B, Mosey NJ, Seki T, Keske EC, Leake JD, Rousina-Webb A, Wu G (2014) Ultra stable self-assembled monolayers of N-heterocyclic carbenes on gold. Nat Chem 6(5):409–414. doi:10.1038/nchem.1891

    Article  CAS  PubMed  Google Scholar 

  • Culp L, Sukenik C (1994) Glass and metal surfaces derivatized with self-assembled monolayers: cell type-specific modulation of fibronectin adhesion functions. J Tissue Cult Methods 16(3–4):161–172. doi:10.1007/BF01540644

    Article  Google Scholar 

  • Davis F, Higson SPJ (2005) Structured thin films as functional components within biosensors. Biosens Bioelectron 21(1):1–20. doi:10.1016/j.bios.2004.10.001

    Article  CAS  PubMed  Google Scholar 

  • Duangkaew P, Tapaneeyakorn S, Apiwat C, Dharakul T, Laiwejpithaya S, Kanatharana P, Laocharoensuk R (2015) Ultrasensitive electrochemical immunosensor based on dual signal amplification process for p16(INK4a) cervical cancer detection in clinical samples. Biosens Bioelectron 74:673–679. doi:10.1016/j.bios.2015.07.004

    Article  CAS  PubMed  Google Scholar 

  • Dugas V, Chevalier Y (2003) Surface hydroxylation and silane grafting on fumed and thermal silica. J Colloid Interface Sci 264(2):354–361. doi:10.1016/S0021-9797(03)00552-6

    Article  CAS  PubMed  Google Scholar 

  • Eggers PK, Da Silva P, Darwish NA, Zhang Y, Tong Y, Ye S, Paddon-Row MN, Gooding JJ (2010) Self-assembled monolayers formed using zero net curvature norbornylogous bridges: the influence of potential on molecular orientation. Langmuir 26(19):15665–15670. doi:10.1021/la101590b

    Article  CAS  PubMed  Google Scholar 

  • Escamilla-Gómez V, Campuzano S, Pedrero M, Pingarrón JM (2008) Electrochemical immunosensor designs for the determination of Staphylococcus aureus using 3,3-dithiodipropionic acid di(N-succinimidyl ester)-modified gold electrodes. Talanta 77(2):876–881. doi:10.1016/j.talanta.2008.07.045

    Article  CAS  Google Scholar 

  • Fuentes M, Mateo C, Guisan JM, Fernandez-Lafuente R (2005) Preparation of inert magnetic nano-particles for the directed immobilization of antibodies. Biosens Bioelectron 20(7):1380–1387. doi:10.1016/j.bios.2004.06.004

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Zhang Y, Wu Q, Chen H, Chen Z, Lin X (2011) One step electrochemically deposited nanocomposite film of chitosan-carbon nanotubes-gold nanoparticles for carcinoembryonic antigen immunosensor application. Talanta 85(4):1980–1985. doi:10.1016/j.talanta.2011.07.012

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Zhen R, Zhang Y, Grimes CA (2009) Detecting penicillin in milk with a wireless magnetoelastic biosensor. Sens Lett 7(1):6–10. doi:10.1166/sl.2009.1002

    Article  CAS  Google Scholar 

  • Garcia-Arribas A, Gutierrez J, Kurlyandskaya GV, Barandiaran JM, Svalov A, Fernandez E, Lasheras A, de Cos D, Bravo-Imaz I (2014) Sensor applications of soft magnetic materials based on magneto-impedance, magneto-elastic resonance and magneto-electricity. Sensors (Basel) 14(5):7602–7624. doi:10.3390/s140507602

    Article  CAS  Google Scholar 

  • Gates BD, Xu Q, Stewart M, Ryan D, Willson CG, Whitesides GM (2005) New approaches to nanofabrication: molding, printing, and other techniques. Chem Rev 105(4):1171–1196. doi:10.1021/cr030076o

    Article  CAS  PubMed  Google Scholar 

  • Gikunoo E, Abera A, Woldesenbet E (2014) A novel carbon nanofibers grown on glass microballoons immunosensor: a tool for early diagnosis of malaria. Sensors (Basel) 14(8):14686–14699. doi:10.3390/s140814686

    Article  CAS  Google Scholar 

  • Graille M, Stura EA, Corper AL, Sutton BJ, Taussig MJ, Charbonnier JB, Silverman GJ (2000) Crystal structure of a Staphylococcus aureus protein a domain complexed with the fab fragment of a human IgM antibody: structural basis for recognition of B-cell receptors and superantigen activity. Proc Natl Acad Sci U S A 97(10):5399–5404. doi:10.1073/pnas.97.10.5399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grimes C, Mungle C, Zeng K, Jain M, Dreschel W, Paulose M, Ong K (2002) Wireless magnetoelastic resonance sensors: a critical review. Sensors (Basel) 2(7):294. doi:10.3390/s20700294

    Article  CAS  Google Scholar 

  • Grimes CA, Roy SC, Rani S, Cai Q (2011) Theory, instrumentation and applications of magnetoelastic resonance sensors: a review. Sensors (Basel) 11(3):2809–2844. doi:10.3390/s110302809

    Article  Google Scholar 

  • Gronenborn AM, Clore GM (1993) Identification of the contact surface of a streptococcal protein G domain complexed with a human Fc fragment. J Mol Biol 233(3):331–335. doi:10.1006/jmbi.1993.1514

    Article  CAS  PubMed  Google Scholar 

  • Guntupalli R, Hu J, Lakshmanan RS, Huang TS, Barbaree JM, Chin BA (2007a) A magnetoelastic resonance biosensor immobilized with polyclonal antibody for the detection of Salmonella typhimurium. Biosens Bioelectron 22(7):1474–1479. doi:10.1016/j.bios.2006.06.037

    Article  CAS  PubMed  Google Scholar 

  • Guntupalli R, Lakshmanan RS, Hu J, Huang TS, Barbaree JM, Vodyanoy V, Chin BA (2007b) Rapid and sensitive magnetoelastic biosensors for the detection of Salmonella typhimurium in a mixed microbial population. J Microbiol Methods 70(1):112–118. doi:10.1016/j.mimet.2007.04.001

    Article  CAS  PubMed  Google Scholar 

  • Guo Y, Wang Y, Liu S, Yu J, Wang H, Cui M, Huang J (2015) Electrochemical immunosensor assay (EIA) for sensitive detection of E. coli O157:H7 with signal amplification on a SG-PEDOT-AuNPs electrode interface. Analyst 140(2):551–559. doi:10.1039/c4an01463d

    Article  CAS  PubMed  Google Scholar 

  • Hanly WC, Artwohl JE, Bennett BT (1995) Review of polyclonal antibody production procedures in mammals and poultry. ILAR J 37:93–118. doi:10.1093/ilar.37.3.93

    Article  PubMed  Google Scholar 

  • Hasan A, Pandey LM (2015) Review: polymers, surface-modified polymers, and self assembled monolayers as surface-modifying agents for biomaterials. Polym-Plast Technol Eng 54(13):1358–1378. doi:10.1080/03602559.2015.1021488

    Article  CAS  Google Scholar 

  • Hermanson GT (2008) Bioconjugate techniques, vol, 2nd edn. Salt Lake, Academic

    Google Scholar 

  • Holliger P, Hudson PJ (2005) Engineered antibody fragments and the rise of single domains. Nat Biotechnol 23(9):1126–1136. doi:10.1038/nbt1142

    Article  CAS  PubMed  Google Scholar 

  • Hu X, Spada S, White S, Hudson S, Magner E, Wall JG (2006) Adsorption and activity of a domoic acid binding antibody fragment on mesoporous silicates. J Phys Chem B 110(37):18703–18709. doi:10.1021/jp062423e

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Ge S, He L, Cai Q, Grimes CA (2008a) A remote-query sensor for predictive indication of milk spoilage. Biosens Bioelectron 23(11):1745–1748. doi:10.1016/j.bios.2008.01.036

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Hu J, Wan J, Johnson ML, Shu H, Chin BA (2008b) The effect of annealing and gold deposition on the performance of magnetoelastic biosensors. Mater Sci Eng C Mater Biol Appl 28(3):380–386. doi:10.1016/j.msec.2007.04.006

    Article  CAS  Google Scholar 

  • Jahanshahi P, Zalnezhad E, Sekaran SD, Adikan FR (2014) Rapid immunoglobulin M-based dengue diagnostic test using surface plasmon resonance biosensor. Sci Rep 4:3851. doi:10.1038/srep03851

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kastern W, Sjobring U, Bjorck L (1992) Structure of peptostreptococcal protein L and identification of a repeated immunoglobulin light chain-binding domain. J Biol Chem 267(18):12820–12825

    CAS  PubMed  Google Scholar 

  • Kato K, Lian L-Y, Barsukov IL, Derrick JP, Kim H, Tanaka R, Yoshino A, Shiraishi M, Shimada I, Arata Y, Roberts GCK (1995) Model for the complex between protein G and an antibody Fc fragment in solution. Structure 3(1):79–85. doi:10.1016/S0969-2126(01)00136-8

    Article  CAS  PubMed  Google Scholar 

  • Kausaite-Minkstimiene A, Ramanaviciene A, Kirlyte J, Ramanavicius A (2010) Comparative study of random and oriented antibody immobilization techniques on the binding capacity of immunosensor. Anal Chem 82(15):6401–6408. doi:10.1021/ac100468k

    Article  CAS  PubMed  Google Scholar 

  • Kengne-Momo RP, Daniel P, Lagarde F, Jeyachandran YL, Pilard JF, Durand-Thouand MJ, Thouand G (2012a) Protein interactions investigated by the raman spectroscopy for biosensor applications. Int J Spectrosc 2012:1–7. doi:10.1155/2012/462901

    Article  CAS  Google Scholar 

  • Konigsberg W (1972) [13] reduction of disulfide bonds in proteins with dithiothreitol methods enzymol. Method Enzymol 25:185–188. doi:10.1016/S0076-6879(72)25015-7

  • Kosobrodova E, Jones RT, Kondyurin A, Chrzanowski W, Pigram PJ, McKenzie DR, Bilek MMM (2015) Orientation and conformation of anti-CD34 antibody immobilised on untreated and plasma treated polycarbonate. Acta Biomater 19:128–137. doi:10.1016/j.actbio.2015.02.027

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Khan I, Sinha S (2015) Nature of immobilization surface affects antibody specificity to placental alkaline phosphatase. J Immunoass Immunochem 36(4):405–413. doi:10.1080/15321819.2014.973117

    Article  CAS  Google Scholar 

  • Kunert R, Reinhart D (2016) Advances in recombinant antibody manufacturing. Appl Microbiol Biotechnol 100:3451–3461. doi:10.1007/s00253-016-7388-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurlyandskaya GV, Miyar VF (2007) Surface modified amorphous ribbon based magnetoimpedance biosensor. Biosens Bioelectron 22:2341–2345. doi:10.1016/j.bios.2006.07.011

    Article  CAS  PubMed  Google Scholar 

  • Kurlyandskaya GV, de Cos D, Volchkov SO (2009) Magnetosensitive transducers for nondestructive testing operating on the basis of the giant magnetoimpedance effect: a review. Russ J Nondestruct Test 45:377–398. doi:10.1134/S1061830909060023

    Article  Google Scholar 

  • Kurlyandskaya GV, Fernández E, Safronov AP, Svalov AV, Beketov I, Burgoa Beitia A, Garcia-Arribas A, Blyahkman FA (2015) Giant magnetoimpedance biosensor for ferrogel detection: model system to evaluate properties of natural tissue. Appl Phys Lett 196:193702. doi:10.1063/1.4921224

    Article  CAS  Google Scholar 

  • Dubois LH, Nuzzo RG (1992) Synthesis, structure, and properties of model organic surfaces. Annu Rev Biophys Biophys Chem 43(1):437–463. doi:10.1146/annurev.pc.43.100192.002253

    CAS  Google Scholar 

  • Langmuir I (1917) The constitution and fundamental properties of solids and liquids. II. Liquids.1. J Am Chem Soc 39(9):1848–1906. doi:10.1021/ja02254a006

    Article  CAS  Google Scholar 

  • Lee J, Seo J, Kim C, Kwon Y, Ha J, Choi S, Cha H (2013) A comparative study on antibody immobilization strategies onto solid surface. Korean J Chem Eng 30(10):1934–1938. doi:10.1007/s11814-013-0117-5

    Article  CAS  Google Scholar 

  • Lee M-T, Hsueh C-C, Freund MS, Ferguson GS (1998) Air oxidation of self-assembled monolayers on polycrystalline gold: the role of the gold substrate. Langmuir 14(22):6419–6423. doi:10.1021/la980724c

    Article  CAS  Google Scholar 

  • Li N, Wang Y, Cao W, Zhang Y, Yan T, Du B, Wei Q (2015) An ultrasensitive electrochemical immunosensor for CEA using MWCNT-NH2 supported PdPt nanocages as labels for signal amplification. J Mater Chem B Mater Biol Med 3(9):2006–2011. doi:10.1039/C4TB01695E

    Article  CAS  Google Scholar 

  • Li S, Horikawa S, M-k P, Chai Y, Vodyanoy VJ, Chin BA (2012) Amorphous metallic glass biosensors. Intermetallics 30:80–85. doi:10.1016/j.intermet.2012.03.030

    Article  CAS  Google Scholar 

  • Li S, Li Y, Chen H, Horikawa S, Shen W, Simonian A, Chin BA (2010) Direct detection of Salmonella typhimurium on fresh produce using phage-based magnetoelastic biosensors. Biosens Bioelectron 26(4):1313–1319. doi:10.1016/j.bios.2010.07.029

    Article  CAS  PubMed  Google Scholar 

  • Liang C, Morshed S, Prorok BC (2007) Correction for longitudinal mode vibration in thin slender beams. Appl Phys Lett 90(22):221912. doi:10.1063/1.2745262

    Article  CAS  Google Scholar 

  • Liu F, Dubey M, Takahashi H, Castner DG, Grainger DW (2010a) Immobilized antibody orientation analysis using secondary ion mass spectrometry and fluorescence imaging of affinity-generated patterns. Anal Chem 82(7):2947–2958. doi:10.1021/ac902964q

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu P, O’Mara BW, Warrack BM, Wu W, Huang Y, Zhang Y, Zhao R, Lin M, Ackerman MS, Hocknell PK, Chen G, Tao L, Rieble S, Wang J, Wang-Iverson DB, Tymiak AA, Grace MJ, Russell RJ (2010b) A tris (2-carboxyethyl) phosphine (TCEP) related cleavage on cysteine-containing proteins. J Am Soc Mass Spectrom 21(5):837–844. doi:10.1016/j.jasms.2010.01.016

    Article  CAS  PubMed  Google Scholar 

  • Liu T, Sin ML, Pyne JD, Gau V, Liao JC, Wong PK (2014) Electrokinetic stringency control in self-assembled monolayer-based biosensors for multiplex urinary tract infection diagnosis. Nanomedicine 10(1):159–166. doi:10.1016/j.nano.2013.07.006

    CAS  PubMed  Google Scholar 

  • Love JC, Estroff LA, Kriebel JK, Nuzzo RG, Whitesides GM (2005) Self-assembled monolayers of thiolates on metals as a form of nanotechnology. Chem Rev 105(4):1103–1169. doi:10.1021/cr0300789

    Article  CAS  PubMed  Google Scholar 

  • Love JC, Wolfe DB, Haasch R, Chabinyc ML, Paul KE, Whitesides GM, Nuzzo RG (2003) Formation and structure of self-assembled monolayers of alkanethiolates on palladium. J Am Chem Soc 125(9):2597–2609. doi:10.1021/ja028692+

    Article  CAS  PubMed  Google Scholar 

  • Lu J, Liu S, Ge S, Yan M, Yu J, Hu X (2012) Ultrasensitive electrochemical immunosensor based on Au nanoparticles dotted carbon nanotube-graphene composite and functionalized mesoporous materials. Biosens Bioelectron 33(1):29–35. doi:10.1016/j.bios.2011.11.054

    Article  PubMed  CAS  Google Scholar 

  • Mahara A, Chen H, Ishihara K, Yamaoka T (2014) Phospholipid polymer-based antibody immobilization for cell rolling surfaces in stem cell purification system. J Biomater Sci Polym Ed 25(14–15):1590–1601. doi:10.1080/09205063.2014.936926

    Article  CAS  PubMed  Google Scholar 

  • Makaraviciute A, Ramanaviciene A (2013) Site-directed antibody immobilization techniques for immunosensors. Biosens Bioelectron 50:460–471. doi:10.1016/j.bios.2013.06.060

    Article  CAS  PubMed  Google Scholar 

  • Mandler D, Turyan I (1996) Applications of self-assembled monolayers in electroanalytical chemistry. Electroanalysis 8(3):207–213. doi:10.1002/elan.1140080302

    Article  CAS  Google Scholar 

  • Mendonca M, Conrad NL, Conceicao FR, Moreira AN, da Silva WP, Aleixo JA, Bhunia AK (2012) Highly specific fiber optic immunosensor coupled with immunomagnetic separation for detection of low levels of Listeria monocytogenes and L. ivanovii. BMC Microbiol 12:275. doi:10.1186/1471-2180-12-275

    Article  PubMed  PubMed Central  Google Scholar 

  • Menti C, Beltrami M, Possan AL, Martins ST, Henriques JAP, Santos AD, Missell FP, Roesch-Ely M (2016) Biocompatibility and degradation of gold-covered magneto-elastic biosensors exposed to cell culture. Colloids Surf B. doi:10.1016/j.colsurfb.2016.03.034

    Google Scholar 

  • Meyerson JR, Rao P, Kumar J, Chittori S, Banerjee S, Pierson J, Mayer ML, Subramaniam S (2014) Self-assembled monolayers improve protein distribution on holey carbon cryo-EM supports. Sci Rep 4:7084. doi:10.1038/srep07084

    Article  PubMed  PubMed Central  Google Scholar 

  • Miyajima K, Itabashi G, Koshida T, Tamari K, Takahashi D, Arakawa T, Kudo H, Saito H, Yano K, Shiba K, Mitsubayashi K (2011) Fluorescence immunoassay using an optical fiber for determination of Dermatophagoides farinae (der f1). Environ Monit Assess 182(1–4):233–241. doi:10.1007/s10661-011-1872-6

    Article  CAS  PubMed  Google Scholar 

  • Mustafaoglu N, Alves NJ, Bilgicer B (2015) Oriented immobilization of fab fragments by site-specific biotinylation at the conserved nucleotide binding site for enhanced antigen detection. Langmuir 31(35):9728–9736. doi:10.1021/acs.langmuir.5b01734

    Article  CAS  PubMed  Google Scholar 

  • Newton L, Slater T, Clark N, Vijayaraghavan A (2013) Self assembled monolayers (SAMs) on metallic surfaces (gold and graphene) for electronic applications. J Mater Chem C Mater Opt Electron Devices 1(3):376–393. doi:10.1039/C2TC00146B

    CAS  Google Scholar 

  • Nilson BH, Solomon A, Bjorck L, Akerstrom B (1992) Protein L from Peptostreptococcus magnus binds to the kappa light chain variable domain. J Biol Chem 267(4):2234–2239

    CAS  PubMed  Google Scholar 

  • Niu LM, Liu F, Wang W, Lian KQ, Ma L, Shi HM, Kang WJ (2015) Electrochemical behavior of paraquat on a highly ordered biosensor based on an unmodified DNA-3D gold nanoparticle composite and its application. Electrochim Acta 153:190–199. doi:10.1016/j.electacta.2014.11.191

    Article  CAS  Google Scholar 

  • Noh J, Kato HS, Kawai M, Hara M (2006) Surface structure and interface dynamics of alkanethiol self-assembled monolayers on Au(111). J Phys Chem B 110(6):2793–2797. doi:10.1021/jp055538b

    Article  CAS  PubMed  Google Scholar 

  • Nuzzo RG, Allara DL (1983) Adsorption of bifunctional organic disulfides on gold surfaces. J Am Chem Soc 105(13):4481–4483. doi:10.1021/ja00351a063

    Article  CAS  Google Scholar 

  • O’Shannessy DJ, Dobersen MJ, Quarles RH (1984) A novel procedure for labeling immunoglobulins by conjugation to oligosaccharide moieties. Immunol Lett 8(5):273–277

    Article  PubMed  Google Scholar 

  • Park M-K, Li S, Chin B (2013) Detection of Salmonella typhimurium grown directly on tomato surface using phage-based magnetoelastic biosensors. Food Bioprocess Technol 6(3):682–689. doi:10.1007/s11947-011-0708-2

    Article  CAS  Google Scholar 

  • Pauling L, Corey RB, Branson HR (1951) The structure of proteins; two hydrogen-bonded helical configurations of the polypeptide chain. Proc Natl Acad Sci U S A 37(4):205–211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pennacchio A, Varriale A, Esposito MG, Scala A, Marzullo VM, Staiano M, D’Auria S (2015) A rapid and sensitive assay for the detection of benzylpenicillin (PenG) in milk. PLoS One 10(7):e0132396. doi:10.1371/journal.pone.0132396

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Poltronieri P, Mezzolla V, Primiceri E, Maruccio G (2014) Biosensors for the detection of food pathogens. Foods 3(3):511. doi:10.3390/foods3030511

    Article  CAS  Google Scholar 

  • Possan AL, Menti C, Beltrami M, Santos AD, Roesch-Ely M, Missell FP (2016) Effect of surface roughness on performance of magnetoelastic biosensors for the detection of Escherichia coli. Mater Sci Eng C Mater Biol Appl 58:541–547. doi:10.1016/j.msec.2015.08.029

    Article  CAS  PubMed  Google Scholar 

  • Ramanaviciene A, German N, Kausaite-Minkstimiene A, Voronovic J, Kirlyte J, Ramanavicius A (2012) Comparative study of surface plasmon resonance, electrochemical and electroassisted chemiluminescence methods based immunosensor for the determination of antibodies against human growth hormone. Biosens Bioelectron 36(1):48–55. doi:10.1016/j.bios.2012.03.036

    Article  CAS  PubMed  Google Scholar 

  • Ripka P, Zaveta K (2009) Magnetic sensors: principles and applications. In: Buschow KHJ (ed) Handbook of magnetic materials vol. 18. Elsevier, Amsterdam, pp. 347–420

    Chapter  Google Scholar 

  • Rocha MC, Grady JP, Grünewald A, Vincent A, Dobson PF, Taylor RW, Turnbull DM, Rygiel KA (2015) A novel immunofluorescent assay to investigate oxidative phosphorylation deficiency in mitochondrial myopathy: understanding mechanisms and improving diagnosis. Sci Rep 5:15037. doi:10.1038/srep15037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruan C, Zeng K, Varghese OK, Grimes CA (2003) Magnetoelastic immunosensors: amplified mass immunosorbent assay for detection of Escherichia coli O157:H7. Anal Chem 75(23):6494–6498. doi:10.1021/ac034562n

    Article  CAS  PubMed  Google Scholar 

  • Ruan C, Zeng K, Varghese OK, Grimes CA (2004) A staphylococcal enterotoxin B magnetoelastic immunosensor. Biosens Bioelectron 20(3):585–591. doi:10.1016/j.bios.2004.03.003

    Article  CAS  PubMed  Google Scholar 

  • Ruan Y, Foo TC, Warren-Smith S, Hoffmann P, Moore RC, Ebendorff-Heidepriem H, Monro TM (2008) Antibody immobilization within glass microstructured fibers: a route to sensitive and selective biosensors. Opt Express 16(22):18514–18523. doi:10.1364/OE.16.018514

    Article  CAS  PubMed  Google Scholar 

  • Sagiv J (1980) Organized monolayers by adsorption. 1. Formation and structure of oleophobic mixed monolayers on solid surfaces. J Am Chem Soc 102(1):92–98. doi:10.1021/ja00521a016

    Article  CAS  Google Scholar 

  • Samanta D, Sarkar A (2011) Immobilization of bio-macromolecules on self-assembled monolayers: methods and sensor applications. Chem Soc Rev 40(5):2567–2592. doi:10.1039/c0cs00056f

    Article  PubMed  CAS  Google Scholar 

  • Schlenoff JB, Li M, Ly H (1995) Stability and self-exchange in alkanethiol monolayers. J Am Chem Soc 117(50):12528–12536. doi:10.1021/ja00155a016

    Article  CAS  Google Scholar 

  • Schroeder HW, Cavacini L (2010) Structure and function of immunoglobulins. J Allergy Clin Immunol 125(2 0 2):S41–S52. doi:10.1016/j.jaci.2009.09.046

    Article  PubMed  PubMed Central  Google Scholar 

  • Schwartz DK (2001) Mechanisms and kinetics of self-assembled monolayer formation. Annu Rev Phys Chem 52(1):107–137. doi:10.1146/annurev.physchem.52.1.107

    Article  CAS  PubMed  Google Scholar 

  • See WP, Heng LY, Nathan S (2015) Highly sensitive aluminium(III) ion sensor based on a self-assembled monolayer on a gold nanoparticles modified screen-printed carbon electrode. Anal Sci 31(10):997–1003. doi:10.2116/analsci.31.997

    Article  CAS  PubMed  Google Scholar 

  • Sek S (2007) Two metal−molecule binding modes for peptide molecular junctions. J Phys Chem C Nanomater Interfaces 111(34):12860–12865. doi:10.1021/jp073960h

    Article  CAS  Google Scholar 

  • Shen W, Lakshmanan RS, Mathison LC, Petrenko VA, Chin BA (2009) Phage coated magnetoelastic micro-biosensors for real-time detection of Bacillus anthracis spores. Sensors Actuators B Chem 137(2):501–506. doi:10.1016/j.snb.2009.01.027

    Article  CAS  Google Scholar 

  • Sohn Y-S, Lee YK (2014) Site-directed immobilization of antibody using EDC-NHS-activated protein a on a bimetallic-based surface plasmon resonance chip. J Biomed Opt 19(5):051209–051209. doi:10.1117/1.JBO.19.5.051209

    Article  PubMed  CAS  Google Scholar 

  • Srisombat L, Jamison AC, Lee TR (2011) Stability: a key issue for self-assembled monolayers on gold as thin-film coatings and nanoparticle protectants. Colloids Surf A Physicochem Eng Asp 390(1–3):1–19. doi:10.1016/j.colsurfa.2011.09.020

    Article  CAS  Google Scholar 

  • Stavis C, Clare TL, Butler JE, Radadia AD, Carr R, Zeng H, King WP, Carlisle JA, Aksimentiev A, Bashir R, Hamers RJ (2011) Surface functionalization of thin-film diamond for highly stable and selective biological interfaces. Proc Natl Acad Sci U S A 108(3):983–988. doi:10.1073/pnas.1006660107

    Article  CAS  PubMed  Google Scholar 

  • Subramanian A, Irudayaraj J, Ryan T (2006) A mixed self-assembled monolayer-based surface plasmon immunosensor for detection of E. coli O157:H7. Biosens Bioelectron 21(7):998–1006. doi:10.1016/j.bios.2005.03.007

    Article  CAS  PubMed  Google Scholar 

  • Sun H, Qi C, Niu Y, Kang T, Wei Y, Jin G, Dong X, Wang C, Zhu W (2015) Detection of cytomegalovirus antibodies using a biosensor based on imaging ellipsometry. PLoS One 10(8):e0136253. doi:10.1371/journal.pone.0136253

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sun H, Wu GM, Chen YY, Tian Y, Yue YH, Zhang GL (2014) Expression, production, and renaturation of a functional single-chain variable antibody fragment (scFv) against human ICAM-1. Braz J Med Biol Res 47(7):540–547. doi:10.1590/1414-431X20143276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tack L, Schickle K, Boke F, Fischer H (2015) Immobilization of specific proteins to titanium surface using self-assembled monolayer technique. Dent Mater 31(10):1169–1179. doi:10.1016/j.dental.2015.06.019

    Article  CAS  PubMed  Google Scholar 

  • Tam-Chang S-W, Biebuyck HA, Whitesides GM, Jeon N, Nuzzo RG (1995) Self-assembled monolayers on gold generated from alkanethiols with the structure RNHCOCH2SH. Langmuir 11(11):4371–4382. doi:10.1021/la00011a033

    Article  CAS  Google Scholar 

  • Tan YH, Schallom JR, Ganesh NV, Fujikawa K, Demchenko AV, Stine KJ (2011) Characterization of protein immobilization on nanoporous gold using atomic force microscopy and scanning electron microscopy. Nanoscale 3(8):3395–3407. doi:10.1039/c1nr10427f

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tegl G, Schiffer D, Sigl E, Heinzle A, Guebitz GM (2015) Biomarkers for infection: enzymes, microbes, and metabolites. Appl Microbiol Biotechnol 99(11):4595–4614. doi:10.1007/s00253-015-6637-7

    Article  CAS  PubMed  Google Scholar 

  • Toworfe GK, Bhattacharyya S, Composto RJ, Adams CS, Shapiro IM, Ducheyne P (2009) Effect of functional end groups of silane self-assembled monolayer surfaces on apatite formation, fibronectin adsorption and osteoblast cell function. J Tissue Eng Regen Med 3(1):26–36. doi:10.1002/term.131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tran QH, Nguyen THH, Mai AT, Nguyen TT, Vu QK, Phan TN (2012) Development of electrochemical immunosensors based on different serum antibody immobilization methods for detection of Japanese encephalitis virus. Adv Nat Sci: Nanosci Nanotechnol 3(1):015012. doi:10.1088/2043-6262/3/1/015012

    Google Scholar 

  • Tully E, Higson SP, O’Kennedy R (2008) The development of a 'labeless' immunosensor for the detection of Listeria monocytogenes cell surface protein, Internalin B. Biosens Bioelectron 23(6):906–912. doi:10.1016/j.bios.2007.09.011

    Article  CAS  PubMed  Google Scholar 

  • Turner APF (2000) Biosensors sense and sensitivity. Science 290:1315–1317. doi:10.1039/C3CS35528D

    Article  CAS  PubMed  Google Scholar 

  • Vashist SK (2012) Comparison of 1-ethyl-3-(3-dimethylaminopropyl) carbodiimide based strategies to crosslink antibodies on amine-functionalized platforms for immunodiagnostic applications. Diagnostics 2(3):23. doi:10.3390/diagnostics2030023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vashist SK, Dixit CK, MacCraith BD, O’Kennedy R (2011) Effect of antibody immobilization strategies on the analytical performance of a surface plasmon resonance-based immunoassay. Analyst 136(21):4431–4436. doi:10.1039/c1an15325k

    Article  CAS  PubMed  Google Scholar 

  • Vashist SK, Lam E, Hrapovic S, Male KB, Luong JH (2014a) Immobilization of antibodies and enzymes on 3-aminopropyltriethoxysilane-functionalized bioanalytical platforms for biosensors and diagnostics. Chem Rev 114(21):11083–11130. doi:10.1021/cr5000943

    Article  CAS  PubMed  Google Scholar 

  • Vashist SK, Marion Schneider E, Lam E, Hrapovic S, Luong JH (2014b) One-step antibody immobilization-based rapid and highly-sensitive sandwich ELISA procedure for potential in vitro diagnostics. Sci Rep 4:4407. doi:10.1038/srep04407

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vashist SK, Schneider EM, Luong JH (2015) Rapid sandwich ELISA-based in vitro diagnostic procedure for the highly-sensitive detection of human fetuin a. Biosens Bioelectron 67:73–78. doi:10.1016/j.bios.2014.06.058

    Article  CAS  PubMed  Google Scholar 

  • Vericat C, Benitez GA, Grumelli DE, Vela ME, Salvarezza RC (2008) Thiol-capped gold: from planar to irregular surfaces. J Phys Condens Matter 20(18):184004. doi:10.1088/0953-8984/20/18/184004

    Article  CAS  Google Scholar 

  • Vericat C, Vela ME, Benitez G, Carro P, Salvarezza RC (2010) Self-assembled monolayers of thiols and dithiols on gold: new challenges for a well-known system. Chem Soc Rev 39(5):1805–1834. doi:10.1039/b907301a

    Article  CAS  PubMed  Google Scholar 

  • Vericat C, Vela ME, Corthey G, Pensa E, Cortes E, Fonticelli MH, Ibanez F, Benitez GE, Carro P, Salvarezza RC (2014) Self-assembled monolayers of thiolates on metals: a review article on sulfur-metal chemistry and surface structures. RSC Adv 4(53):27730–27754. doi:10.1039/C4RA04659E

    Article  CAS  Google Scholar 

  • Vericat C, Vela ME, Salvarezza RC (2005) Self-assembled monolayers of alkanethiols on Au(111): surface structures, defects and dynamics. Phys Chem Chem Phys 7(18):3258–3268. doi:10.1039/b505903h

    Article  CAS  PubMed  Google Scholar 

  • Vuillaume D, Fontaine P, Collet J, Deresmes D, Garet M, Rondelez F (1993) Alkyl-trichlorosilane monolayer as ultra-thin insulating film for silicon MIS devices. Microelectron Eng 22(1–4):101–104. doi:10.1016/0167-9317(93)90140-Z

    Article  CAS  Google Scholar 

  • Wang C, Yan Q, Liu H-B, Zhou X-H, Xiao S-J (2011) Different EDC/NHS activation mechanisms between PAA and PMAA brushes and the following amidation reactions. Langmuir 27(19):12058–12068. doi:10.1021/la202267p

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Tu Y, Liu S (2008) Electrochemical immunoassay for α-fetoprotein through a phenylboronic acid monolayer on gold. Talanta 77(2):815–821. doi:10.1016/j.talanta.2008.07.039

    Article  CAS  Google Scholar 

  • Wong SS (1991) Conjugation of protein to solid matrices. In Chemistry of protein conjugation and cross-linking, 1 edn, Florida

  • Yan D, Evans DG (2014) Molecular crystalline materials with tunable luminescent properties: from polymorphs to multi-component solids. Mater Horiz 1(1):46–57. doi:10.1039/C3MH00023K

    Article  CAS  Google Scholar 

  • Yang G, Amro NA, Starkewolfe ZB, G-y L (2004) Molecular-level approach to inhibit degradations of alkanethiol self-assembled monolayers in aqueous media. Langmuir 20(10):3995–4003. doi:10.1021/la0499160

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Biswas ME, Chen P (2003) Study of binding between protein A and immunoglobulin G using a surface tension probe. Biophys J 84(1):509–522. doi:10.1016/S0006-3495(03)74870-X

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Lin R, Ge L, Hou L, Bernhardt P, Rufford TE, Wang S, Rudolph V, Wang Y, Zhu Z (2015) Synthesis and characterization of three amino-functionalized metal-organic frameworks based on the 2-aminoterephthalic ligand. Dalton Trans 44(17):8190–8197. doi:10.1039/c4dt03927k

    Article  CAS  PubMed  Google Scholar 

  • Zaitsev VN, Colomiets LI, Elskaya AV, Skopenko VV, Evans J (1991) Covalent immobilization of immunoglobulin on a wafer surface for immunosensor bioselective matrix construction. Anal Chim Acta 252(1–2):1–6. doi:10.1016/0003-2670(91)87188-D

    Article  CAS  Google Scholar 

  • Zourob M, Ong KG, Zeng K, Mouffouk F, Grimes CA (2007) A wireless magnetoelastic biosensor for the direct detection of organophosphorus pesticides. Analyst 132(4):338–343. doi:10.1039/b616035b

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Instituto de Biotecnologia, Universidade de Caxias do Sul, Rua Francisco Getúlio Vargas 1130, Caxias do Sul, RS, 95070-560, Brazil

    C. Menti, J. A. P. Henriques & M. Roesch-Ely

  2. Centro de Ciências Exatas e Tecnologia, Universidade de Caxias do Sul, Caxias do Sul, Brazil

    F. P. Missell

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  1. C. Menti
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  2. J. A. P. Henriques
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  3. F. P. Missell
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  4. M. Roesch-Ely
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Correspondence to M. Roesch-Ely.

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Funding

This work is supported by Project 098,412–7 from Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS), Project 403–2500/12–5 from Secretaria de Desenvolvimento Econômico, Ciência e Tecnologia do Estado do Rio Grande do sul (SDECT/RS) and Project 44,777/2014–9 from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). CM was supported by fellowships from FAPERGS-CAPES, and FPM received partial support from CNPq. We acknowledge support from FINEP (contract 01.13.0359.00).

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Menti, C., Henriques, J.A.P., Missell, F.P. et al. Antibody-based magneto-elastic biosensors: potential devices for detection of pathogens and associated toxins. Appl Microbiol Biotechnol 100, 6149–6163 (2016). https://doi.org/10.1007/s00253-016-7624-3

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