Glycoprofiling of cancer biomarkers: Label-free
electrochemical lectin-based biosensors

• Authors: Dominika Pihíková , Peter Kasák , Jan Tkac
• Languages of publication: EN

Abstracts

EN

Keywords

EN

glycosylation; lectins; electrochemicalimpedance spectroscopy; cancer biomarkers; biosensors

• Publisher: De Gruyter Open
• Journal: Open Chemistry
• Year: 2015
• Volume: 13
• Issue: 1

Dates

received

23 - 5 - 2014

accepted

26 - 9 - 2014

online

7 - 1 - 2015

Contributors

author

Dominika Pihíková

• Department of Glycobiotechnology,
  Institute of Chemistry, Slovak Academy of Sciences, Dúbravská cesta
  9, SK-845 38 Bratislava, Slovakia

author

Peter Kasák

• Center for Advanced Materials, Qatar University,
  P.O.Box 2713 Doha, Qatar

author

Jan Tkac

• Department of Glycobiotechnology,
  Institute of Chemistry, Slovak Academy of Sciences, Dúbravská cesta
  9, SK-845 38 Bratislava, Slovakia

References

• [1] Ghazarian H., Idoni B., Oppenheimer S.B., A glycobiologyreview: carbohydrates, lectins and implications in cancertherapeutics, Acta Histochem., 2011, 113, 236-247.[Crossref]
• [2] Burton D.R., Poignard P., Stanfield R.L., Wilson I.A., Broadlyneutralizing antibodies present new prospects to counter highlyantigenically diverse viruses, Science, 2012, 337, 183-186.
• [3] Hirabayashi J., Yamada M., Kuno A., Tateno H., Lectinmicroarrays: concept, principle and applications, Chem. Soc.Rev., 2013, 42, 4443-4458.[Crossref]
• [4] Tong L., Baskaran G., Jones M.B., Rhee J.K., Yarema K.J.,Glycosylation changes as markers for the diagnosis andtreatment of human disease, Biotechnol. Gen. Eng. Rev., 2003,20, 199-244.[Crossref]
• [5] Wang B., Boons G.-J. Carbohydrate recognition: Biologicalproblems, methods and applications.: John Wiley & Sons, Inc.;2011.
• [6] Tkac J., Bertok T., Nahalka J., Gemeiner P., Perspectives inglycomics and lectin engineering, Methods in MolecularBiology, 2014, 1200, 421-445.
• [7] Dalziel M., Crispin M., Scanlan C.N., Zitzmann N., DwekR.A., Emerging principles for the therapeutic exploitationof glycosylation, Science, 2014, 343, 37. DOI: 10.1126/science.1235681.[Crossref]
• [8] Choi E., Hill M.M., Targeted high-throughput glycoproteomicsfor glyco-biomarker discovery, Integrative Proteomics. InTech,2012.[Crossref]
• [9] Varki A., Cummings R.D., Esko J.D., Freeze H.H., Stanley P.,Bertozzi C.R., et al. Essential of glycobiology. 2nd ed: ColdSpring Harbor Laboratory Press (NY); 2009.
• [10] Nelson D.L., Cox M.M. Carbohydrates and glycobiology, Chapter7 in Lehninger principles of biochemistry. 4 ed: W.H. Freeman &Company; 2004.
• [11] Sharon N., Lis H., Carbohydrates in cell recognition, Sci. Am.,1993, 268, 82-89.
• [12] Cummings R.D., Pierce J.M., The challenge and promise ofglycomics, Chem. Biol., 2014, 21, 1-15.[Crossref]
• [13] Reuel N.F., Mu B., Zhang J., Hinckley A., Strano M.S.,Nanoengineered glycan sensors enabling native glycoprofilingfor medicinal applications: towards profiling glycoproteinswithout labeling or liberation steps, Chem. Soc. Rev., 2012, 41,5744-5779.[Crossref]
• [14] Alley W.R., Mann B.F., Novotny M.V., High-sensitivity analyticalapproaches for the structural characterization of glycoproteins,Chem. Rev., 2013, 113, 2668-2732.[Crossref]
• [15] Arthur C.M., Cummings R.D., Stowell S.R., Using glycanmicroarrays to understand immunity, Curr. Opin. Chem. Biol.,2014, 18, 55-61.[Crossref]
• [16] Geissner A., Anish C., Seeberger P.H., Glycan arrays as tools forinfectious disease research, Curr. Opin. Chem. Biol., 2014, 18,38-45.[Crossref]
• [17] Gemeiner P., Mislovicova D., Tkac J., Svitel J., Patoprsty V.,Hrabarova E., et al., Lectinomics II. A highway to biomedical/clinical diagnostics, Biotechnol. Adv., 2009, 27, 1-15.[Crossref]
• [18] Katrlik J., Svitel J., Gemeiner P., Kozar T., Tkac J., Glycan andlectin microarrays for glycomics and medicinal applications,Med. Res. Rev., 2010, 30, 394-418.
• [19] Palma A.S., Feizi T., Childs R.A., Chai W., Liu Y., The neoglycolipid(NGL)-based oligosaccharide microarray system poised todecipher the meta-glycome, Curr. Opin. Chem. Biol., 2014, 18,87-94.[Crossref]
• [20] Park S., Gildersleeve J.C., Blixt O., Shin I., Carbohydratemicroarrays, Chem. Soc. Rev., 2013, 42, 4310-4326.[Crossref]
• [21] Sharon N., Lis H., History of lectins: from hemagglutinins tobiological recognition molecules, Glycobiology, 2004, 14, 53R-62R.
• [22] Nilsson C.L. Lectins: Analytical technologies. Oxford: Elsevier;2007.
• [23] Boyd W.C., The protein of the immune reactions, The Proteins,1954, 2, 756-844.
• [24] Lis H., Sharon N., Lectin-carbohydrate interactions, Curr. Opin.Struct. Biol., 1991, 1, 741-749.[Crossref]
• [25] Mody R., Joshi S., Chaney W., Use of lectins as diagnostic andtherapeutic tools for cancer, J. Pharmacol. Toxicol. Methods,1995, 33, 1-10.[Crossref]
• [26] Arnaud J., Audfray A., Imberty A., Binding sugars: from naturallectins to synthetic receptors and engineered neolectins, Chem.Soc. Rev., 2013, 42, 4798-4813.[Crossref]
• [27] Minko T., Drug targeting to the colon with lectins andneoglycoconjugates, Adv. Drug Deliv. Rev., 2004, 56, 491-509.[Crossref]
• [28] Varrot A., Blanchard B., Imberty A. Lectin binding and itsstructural basic. In: Wang B, Boons G-J, editors. CarbohydrateRecognition: Biological Problems, Methods and Applications:Wiley; 2011.
• [29] Goldstein I.J., Poretz R.D. Isolation, physicochemicalcharacterization, and carbohydrate-binding specificity. TheLectins: Properties, Functions, and Applications in Biology andMedicine: Orlando: Academic Press Inc.; 1986. p. 33-243.
• [30] Ieth C., Lütteke T., Frank M. Bioinformatics for glycobioogy andglycomics: an introduction: Wiley-Blackwell; 2009.
• [31] Drake P.M., Cho W., Li B., Prakobphol A., Johansen E., AndersonN.L., et al., Sweetening the pot: adding glycosylation to thebiomarker discovery equation, Clin. Chem., 2010, 56, 223-236.[Crossref]
• [32] Yamazaki N., Kojima S., Bovin N.V., Andre S., Gabius S., GabiusH.J., Endogenous lectins as targets for drug delivery, Adv. DrugDeliv. Rev., 2000, 43, 225-244.[Crossref]
• [33] Hsu K.L., Mahal L.K., A lectin microarray approach for the rapidanalysis of bacterial glycans, Nat. Protocols, 2006, 1, 543-549.[Crossref]
• [34] Hirabayashi J., Glycome ‚fingerprints‘ provide definitive clues toHIV origins, Nat. Chem. Biol., 2009, 5, 198-199.[Crossref]
• [35] Mislovičová D., Gemeiner P., Kozarova A., Kožár T., Lectinomics I.Relevance of exogenous plant lectins in biomedical diagnostics,Biologia, 2009, 64, 1-19.[Crossref]
• [36] Bertók T., Šefčovičová J., Gemeiner P., Tkáč J., Lektinomika:Nástroj pre klinickú diagnostiku, Chem. Listy, 2012, 106, 10-26.
• [37] Bertók T., Katrlík J., Gemeiner P., Tkac J., Electrochemical lectinbased biosensors as a label-free tool in glycomics, Microchim.Acta, 2012, 180, 1-13.
• [38] https://www.vectorlabs.com/, 2012, Vector Laboratories.
• [39] Dube D.H., Bertozzi C.R., Glycans in cancer and inflammation--potential for therapeutics and diagnostics, Nat. Rev. DrugDiscov., 2005, 4, 477-488.[Crossref]
• [40] Svarovsky S.A., Joshi L., Cancer glycan biomarkers and theirdetection – past, present and future, Anal. Methods, 2014, 6,3918-3936.[Crossref]
• [41] Meezan E., Wu H.C., Black P.H., Robbins P.W., Comparativestudies on the carbohydrate-containing membrane componentsof normal and virus-transformed mouse fibroblasts. II.Separation of glycoproteins and glycopeptides by Sephadexchromatography, Biochemistry, 1969, 8, 2518-2524.[Crossref]
• [42] Kim E.H., Misek D.E., Glycoproteomics-based identification ofcancer biomarkers, Int. J. Proteom., 2011, 2011, 601937.
• [43] Kim Y.J., Varki A., Perspectives on the significance of alteredglycosylation of glycoproteins in cancer, Glycoconjugate J.,1997, 14, 569-576.[Crossref]
• [44] Fernandes B., Sagman U., Auger M., Demetrio M., DennisJ.W., Beta 1-6 branched oligosaccharides as a marker of tumorprogression in human breast and colon neoplasia, Cancer Res.,1991, 51, 718-723.
• [45] Seelentag W.K., Li W.P., Schmitz S.F., Metzger U., AeberhardP., Heitz P.U., et al., Prognostic value of beta1,6-branchedoligosaccharides in human colorectal carcinoma, Cancer Res.,1998, 58, 5559-5564.
• [46] Burchell J., Poulsom R., Hanby A., Whitehouse C., Cooper L.,Clausen H., et al., An alpha2,3 sialyltransferase (ST3Gal I) iselevated in primary breast carcinomas, Glycobiology, 1999, 9,1307-1311.
• [47] Peracaula R., Tabares G., Royle L., Harvey D.J., Dwek R.A., RuddP.M., et al., Altered glycosylation pattern allows the distinctionbetween prostate-specific antigen (PSA) from normal and tumororigins, Glycobiology, 2003, 13, 457-470.[Crossref]
• [48] Thompson S., Dargan E., Turner G.A., Increased fucosylation andother carbohydrate changes in haptoglobin in ovarian cancer,Cancer Lett., 1992, 66, 43-48.[Crossref]
• [49] Misonou Y., Shida K., Korekane H., Seki Y., Noura S., Ohue M.,et al., Comprehensive clinico-glycomic study of 16 colorectalcancer specimens: Elucidation of aberrant glycosylation and itsmechanistic causes in colorectal cancer cells, J. Proteome Res.,2009, 8, 2990-3005.[Crossref]
• [50] Aubert M., Panicot L., Crotte C., Gibier P., Lombardo D., SadouletM.O., et al., Restoration of alpha(1,2) fucosyltransferase activitydecreases adhesive and metastatic properties of humanpancreatic cancer cells, Cancer Res., 2000, 60, 1449-1456.
• [51] Nakamori S., Kameyama M., Imaoka S., Furukawa H., IshikawaO., Sasaki Y., et al., Increased expression of sialyl Lewisxantigen correlates with poor survival in patients with colorectalcarcinoma: clinicopathological and immunohistochemicalstudy, Cancer Res., 1993, 53, 3632-3637.
• [52] Atkinson A.J., Colburn W.A., DeGruttola V.G., DeMets D.L.,Downing G.J., Hoth D.F., et al., Biomarkers and surrogateendpoints: preferred definitions and conceptual framework,Clin. Pharm. Therap., 2001, 69, 89-95.
• [53] Majkić-Singh N., What is a biomarker? From its discovery toclinical application, J. Med. Biochem., 2011, 30.
• [54] Li J., Li S., Yang C.F., Electrochemical biosensors for cancerbiomarker detection, Electroanal., 2012, 24, 2213-2229.[Crossref]
• [55] Etzioni R., Urban N., Ramsey S., McIntosh M., Schwartz S., ReidB., et al., The case for early detection, Nat. Rev. Cancer, 2003,3, 243-252.[Crossref]
• [56] Saldova R., Royle L., Radcliffe C.M., Abd Hamid U.M., EvansR., Arnold J.N., et al., Ovarian cancer is associated withchanges in glycosylation in both acute-phase proteins and IgG,Glycobiology, 2007, 17, 1344-1356.[Crossref]
• [57] Turner G.A., Goodarzi M.T., Thompson S., Glycosylation ofalpha-1-proteinase inhibitor and haptoglobin in ovarian cancer:evidence for two different mechanisms, Glycoconjugate J., 1995,12, 211-218.
• [58] Chen K., Gentry-Maharaj A., Burnell M., Steentoft C., Marcos-Silva L., Mandel U., et al., Microarray glycoprofiling of CA125improves differential diagnosis of ovarian cancer, J. ProteomeRes., 2013, 12, 1408-1418.[Crossref]
• [59] Saldova R., Struwe W., Wynne K., Elia G., Duffy M., Rudd P.,Exploring the glycosylation of serum CA125, Int. J. Mol. Sci.,2013, 14, 15636-15654.[Crossref]
• [60] Cazet A., Julien S., Bobowski M., Burchell J., Delannoy P.,Tumour-associated carbohydrate antigens in breast cancer,Breast Cancer Res., 2010, 12, 204.[Crossref]
• [61] Park S.Y., Yoon S.J., Jeong Y.T., Kim J.M., Kim J.Y., Bernert B.,et al., N-glycosylation status of beta-haptoglobin in sera ofpatients with colon cancer, chronic inflammatory diseases andnormal subjects, Int. J. Cancer, 2010, 126, 142-155.[Crossref]
• [62] Vercoutter-Edouart A.S., Slomianny M.C., Dekeyzer-BesemeO., Haeuw J.F., Michalski J.C., Glycoproteomics and glycomicsinvestigation of membrane N-glycosylproteins from humancolon carcinoma cells, Proteomics, 2008, 8, 3236-3256.[Crossref]
• [63] Saeland E., Belo A.I., Mongera S., van Die I., Meijer G.A., vanKooyk Y., Differential glycosylation of MUC1 and CEACAM5between normal mucosa and tumour tissue of colon cancerpatients, Int. J. Cancer, 2012, 131, 117-128.
• [64] Zhao Y.P., Ruan C.P., Wang H., Hu Z.Q., Fang M., Gu X., et al.,Identification and assessment of new biomarkers for colorectalcancer with serum N-glycan profiling, Cancer, 2012, 118, 639-650.[Crossref]
• [65] Qiu Y., Patwa T.H., Xu L., Shedden K., Misek D.E., Tuck M., et al.,Plasma glycoprotein profiling for colorectal cancer biomarkeridentification by lectin glycoarray and lectin blot, J. ProteomeRes., 2008, 7, 1693-1703.[Crossref]
• [66] Li C., Simeone D.M., Brenner D.E., Anderson M.A., SheddenK.A., Ruffin M.T., et al., Pancreatic cancer serum detection usinga lectin/glyco-antibody array method, J. Proteome Res., 2009,8, 483-492.[Crossref]
• [67] Zhao J., Patwa T.H., Qiu W., Shedden K., Hinderer R., Misek D.E.,et al., Glycoprotein microarrays with multi-lectin detection:unique lectin binding patterns as a tool for classifying normal,chronic pancreatitis and pancreatic cancer sera, J. ProteomeRes., 2007, 6, 1864-1874.[Crossref]
• [68] Miyoshi E., Nakano M., Fucosylated haptoglobin is a novel markerfor pancreatic cancer: detailed analyses of oligosaccharidestructures, Proteomics, 2008, 8, 3257-3262.[Crossref]
• [69] Fujimura T., Shinohara Y., Tissot B., Pang P.C., Kurogochi M.,Saito S., et al., Glycosylation status of haptoglobin in sera ofpatients with prostate cancer vs. benign prostate disease ornormal subjects, Int. J. Cancer, 2008, 122, 39-49.[Crossref]
• [70] Ohyama C., Hosono M., Nitta K., Oh-eda M., Yoshikawa K.,Habuchi T., et al., Carbohydrate structure and differentialbinding of prostate specific antigen to Maackia amurensis lectinbetween prostate cancer and benign prostate hypertrophy,Glycobiology, 2004, 14, 671-679.[Crossref]
• [71] Takeya A., Hosomi O., Nishijima H., Ohe Y., Sugahara K., SagiM., et al., Presence of beta-linked GalNAc residues on N-glycansof human thyroglobulin, Life Sci., 2007, 80, 538-545.[Crossref]
• [72] Yamamoto K., Tsuji T., Tarutani O., Osawa T., Structural changesof carbohydrate chains of human thyroglobulin accompanyingmalignant transformations of thyroid glands, Eur. J. Biochem.,1984, 143, 133-144.[Crossref]
• [73] Naitoh A., Aoyagi Y., Asakura H., Highly enhanced fucosylation ofserum glycoproteins in patients with hepatocellular carcinoma,J. Gastroenter. Hepatol., 1999, 14, 436-445.
• [74] Hoagland L.F.t., Campa M.J., Gottlin E.B., Herndon J.E., 2nd,Patz E.F., Jr., Haptoglobin and posttranslational glycan-modifiedderivatives as serum biomarkers for the diagnosis of nonsmallcell lung cancer, Cancer, 2007, 110, 2260-2268.
• [75] Gutman S., Kessler L.G., The US Food and Drug Administrationperspective on cancer biomarker development, Nat. Rev. Cancer,2006, 6, 565-571.[Crossref]
• [76] Badr H.A., Alsadek D.M., Darwish A.A., Elsayed A.I., BekmanovB.O., Khussainova E.M., et al., Lectin approaches forglycoproteomics in FDA-approved cancer biomarkers, ExpertRev. Proteomics, 2014, 11, 227-236.[Crossref]
• [77] Balog C.I., Stavenhagen K., Fung W.L., Koeleman C.A., McDonnellL.A., Verhoeven A., et al., N-glycosylation of colorectal cancertissues: a liquid chromatography and mass spectrometry-basedinvestigation, Mol. Cell. Proteomics, 2012, 11, 571-585.[Crossref]
• [78] Schmidt M.M., Thurber G.M., Wittrup K.D., Kinetics of anticarcinoembryonicantigen antibody internalization: effects ofaffinity, bivalency, and stability, Cancer Immunol. Immunother.,2008, 57, 1879-1890.[Crossref]
• [79] Ahn Y.H., Ji E.S., Shin P.M., Kim K.H., Kim Y.-S., Ko J.H., et al., Amultiplex lectin-channel monitoring method for human serumglycoproteins by quantitative mass spectrometry, Analyst, 2012,137, 691-703.[Crossref]
• [80] Cheng T.M., Lee T.C., Tseng S.H., Chu H.L., Pan J.P., ChangC.C., Human haptoglobin phenotypes and concentrationdetermination by nanogold-enhanced electrochemicalimpedance spectroscopy, Nanotechnology, 2011, 22, 245105.[Crossref]
• [81] Thompson S., Turner G.A., Elevated levels of abnormallyfucosylatedhaptoglobins in cancer sera, Br. J. Cancer, 1987, 56,605-610.[Crossref]
• [82] Zhang B., Cai F.F., Zhong X.Y., An overview of biomarkers for theovarian cancer diagnosis, Eur. J. Obstetrics Gynec. Reprod. Biol.,2011, 158, 119-123.[Crossref]
• [83] World Health Organization I.A.f.R.o.C. Globocan 2012. Availablefrom: http://globocan.iarc.fr/Default.aspx.
• [84] World Health Organization I.A.f.R.o.C. European CancerObservatory 2012. Available from: http://eu-cancer.iarc.fr/.
• [85] Christiansen M.N., Chik J., Lee L., Anugraham M., AbrahamsJ.L., Packer N.H., Cell surface protein glycosylation in cancer,Proteomics, 2014, 14, 525-546.[Crossref]
• [86] Bhoola S., Hoskins W.J., Diagnosis and management of epithelialovarian cancer, Obstetrics Gynecol., 2006, 107, 1399-1410.[Crossref]
• [87] Eltabbakh G.H., Mount S.L., Beatty B., Simmons-Arnold L.,Cooper K., Morgan A., Factors associated with cytoreducibility among women with ovarian carcinoma, Gynecol. Oncol., 2004,95, 377-383.[Crossref]
• [88] Biskup K., Braicu E.I., Sehouli J., Fotopoulou C., Tauber R., BergerM., et al., Serum glycome profiling: A biomarker for diagnosis ofovarian cancer, J. Proteome Res., 2013, 12, 4056-4063.[Crossref]
• [89] Park C.W., Jo Y., Jo E.J., Enhancement of ovarian tumorclassification by improved reproducibility in matrix-assistedlaser desorption/ionization time-of-flight mass spectrometry ofserum glycans, Anal. Biochem., 2013, 443, 58-65.
• [90] Moore R.G., McMeekin D.S., Brown A.K., DiSilvestro P., MillerM.C., Allard W.J., et al., A novel multiple marker bioassayutilizing HE4 and CA125 for the prediction of ovarian cancer inpatients with a pelvic mass, Gynecol. Oncol., 2009, 112, 40-46.[Crossref]
• [91] Ghasemi N., Ghobadzadeh S., Zahraei M., MohammadpourH., Bahrami S., Ganje M.B., et al., HE4 combined with CA125:favorable screening tool for ovarian cancer, Med. Oncol., 2014,31, 808.[Crossref]
• [92] La Belle J.T., Fairchild A., Demirok U.K., Verma A., Method forfabrication and verification of conjugated nanoparticle-antibodytuning elements for multiplexed electrochemical biosensors,Methods, 2013, 61, 39-51.[Crossref]
• [93] Yurkovetsky Z., Skates S., Lomakin A., Nolen B., Pulsipher T.,Modugno F., et al., Development of a multimarker assay for earlydetection of ovarian cancer, J. Clin. Oncol., 2010, 28, 2159-2166.[Crossref]
• [94] Vermassen T., Speeckaert M.M., Lumen N., Rottey S., DelangheJ.R., Glycosylation of prostate specific antigen and its potentialdiagnostic applications, Clin. Chim. Acta, 2012, 413, 1500-1505.
• [95] Cary K.C., Cooperberg M.R., Biomarkers in prostate cancersurveillance and screening: past, present, and future, Ther. Adv.Urol., 2013, 5, 318-329.[Crossref]
• [96] Hori S., Blanchet J.S., McLoughlin J., From prostate-specificantigen (PSA) to precursor PSA (proPSA) isoforms: a review ofthe emerging role of proPSAs in the detection and managementof early prostate cancer, BJU Int., 2013, 112, 717-728.[Crossref]
• [97] Velonas V.M., Woo H.H., Remedios C.G., Assinder S.J., Currentstatus of biomarkers for prostate cancer, Int. J. Mol. Sci., 2013,14, 11034-11060.[Crossref]
• [98] Crawford E.D., Ventii K., Shore N.D., New biomarkers in prostatecancer, Oncology, 2014, 28, 135-142.
• [99] Okada T., Sato Y., Kobayashi N., Sumida K., Satomura S.,Matsuura S., et al., Structural characteristics of the N-glycansof two isoforms of prostate-specific antigens purified fromhuman seminal fluid, Biochim. Biophys. Acta, 2001, 1525, 149-160.
• [100] Gilgunn S., Conroy P.J., Saldova R., Rudd P.M., O‘Kennedy R.J.,Aberrant PSA glycosylation--a sweet predictor of prostatecancer, Nat. Rev. Urol., 2013, 10, 99-107.[Crossref]
• [101] Kuno A., Kato Y., Matsuda A., Kaneko M.K., Ito H., Amano K.,et al., Focused differential glycan analysis with the platformantibody-assisted lectin profiling for glycan-related biomarkerverification, Mol. Cell. Proteomics : MCP, 2009, 8, 99-108.[Crossref]
• [102] Duverger E., Lamerant-Fayel N., Frison N., Monsigny M.,Carbohydrate-lectin interactions assayed by SPR, Methods Mol.Biol., 2010, 627, 157-178.
• [103] Safina G., Duran Iu B., Alasel M., Danielsson B., Surfaceplasmon resonance for real-time study of lectin-carbohydrateinteractions for the differentiation and identification ofglycoproteins, Talanta, 2011, 84, 1284-1290.[Crossref]
• [104] Choi Y.E., Kwak J.W., Park J.W., Nanotechnology for early cancerdetection, Sensors, 2010, 10, 428-455.[Crossref]
• [105] Qian X., Peng X.-H., Ansari D.O., Yin-Goen Q., Chen G.Z.,Shin D.M., et al., In vivo tumor targeting and spectroscopicdetection with surface-enhanced Raman nanoparticle tags, Nat.Biotechnol., 2008, 26, 83-90.
• [106] Liu X., Dai Q., Austin L., Coutts J., Knowles G., Zou J., et al., Aone-step homogeneous immunoassay for cancer biomarkerdetection using gold nanoparticle probes coupled with dynamiclight scattering, J. Am. Chem. Soc., 2008, 130, 2780-2782.[Crossref]
• [107] Gao X., Cui Y., Levenson R.M., Chung L.W.K., Nie S., In vivocancer targeting and imaging with semiconductor quantumdots, Nat. Biotechnol., 2004, 22, 969-976.[Crossref]
• [108] Gao X., Yang L., Petros J.A., Marshall F.F., Simons J.W., Nie S., Invivo molecular and cellular imaging with quantum dots, Curr.Opin. Biotechnol., 2005, 16, 63-72.[Crossref]
• [109] Iijima S., Helical microtubules of graphitic carbon, Nature, 1991,354, 56-58.
• [110] Iijima S., Ichihashi T., Single-shell carbon nanotubes of 1-nmdiameter, Nature, 1993, 363, 603-605.
• [111] Geim A.K., Novoselov K.S., The rise of graphene, Nat. Mater.,2007, 6, 183-191.[Crossref]
• [112] Geim A.K., Graphene: status and prospects, Science, 2009, 324,1530-1534.
• [113] Novoselov K.S., Geim A.K., Morozov S., Jiang D., Zhang Y.,Dubonos S., et al., Electric field effect in atomically thin carbonfilms, Science, 2004, 306, 666-669.
• [114] Dreyer D.R., Park S., Bielawski C.W., Ruoff R.S., The chemistry ofgraphene oxide, Chem. Soc. Rev., 2010, 39, 228-240.[Crossref]
• [115] Reichardt N.C., Martín-Lomas M., Penadés S.,Glyconanotechnology, Chem. Soc. Rev., 2013, 42, 4358-4376.[Crossref]
• [116] Park D.W., Kim Y.H., Kim B.S., So H.M., Won K., Lee J.O., etal., Detection of tumor markers using single-walled carbonnanotube field effect transistors, J. Nanosci. Nanotechnol.,2006, 6, 3499-3502.
• [117] Kerman K., Saito M., Tamiya E., Yamamura S., Takamura Y.,Nanomaterial-based electrochemical biosensors for medicalapplications, Trends Anal. Chem., 2008, 27, 585-592.[Crossref]
• [118] Perumal V., Hashum U., Advances in biosensors: Principle,architecture and applications, J. Appl. Biomed., 2014, 12, 1-15.[Crossref]
• [119] Lee S.Y., Hwang S.Y. Electrical and electrochemicalimmunosensor for cancer study. Biosensors and Cancer:Science Publishers; 2012. p. 125-145.
• [120] Yun Y.-H., Eteshola E., Bhattacharya A., Dong Z., ShimJ.-S., Conforti L., et al., Tiny medicine: Nanomaterial-basedbiosensors, Sensors, 2009, 9, 9275-9299.[Crossref]
• [121] Xu J.J., Zhao W.W., Song S., Fan C., Chen H.Y., Functionalnanoprobes for ultrasensitive detection of biomolecules: anupdate, Chem. Soc. Rev., 2014, 43, 1601-1611.[Crossref]
• [122] Wang Y., Qu K., Tang L., Li Z., Moore E., Zeng X., et al.,Nanomaterials in carbohydrate biosensors, Trends Anal. Chem.,2014, 58, 54-70.[Crossref]
• [123] Mu B., Zhang J., McNicholas T.P., Reuel N.F., Kruss S., StranoM.S., Recent advances in molecular recognition based onnanoengineered platforms, Acc. Chem. Res., 2014, 47, 979-988.[Crossref]
• [124] Kluková Ľ., Bertók T., Kasák P., Tkac J., Nanoscale controlledarchitecture for development of ultrasensitive lectin biosensorsapplicable in glycomics, Anal. Methods, 2014, 6, 4922-4931.[Crossref]
• [125] Katz E., Willner I., Probing biomolecular interactions atconductive and semiconductive surfaces by impedancespectroscopy: Routes to impedimetric immunosensors, DNA sensors, and enzyme biosensors, Electroanal., 2003, 15, 913-947.[Crossref]
• [126] Thévenot D.R., Toth K., Durst R.A., Wilson G.S., Electrochemicalbiosensors: recommended definitions and classification,Biosens. Bioelectron., 2001, 16, 121-131.[Crossref]
• [127] Bertok T., Šefčovičová J., Gemeiner P., Tkac J., Vývoj a súčasnétrendy pri príprave nanoštrukturovaných biosenzorov, Chem.Listy, 2012, 106, 174-181.
• [128] Tkac J., Davis J.J., An optimised electrode pre-treatment for SAMformation on polycrystalline gold, J. Electroanal. Chem., 2008,621, 117-120.
• [129] Cao G., Wang Y. Nanostructures and nanomaterials: Synthesis,properties, and applications. 2 ed: World Scientific Publishing;2011.
• [130] Alvarez T.V. Highly sensitive nanomaterial based electrochemicalbiosensor: Arizona State University; 2009.
• [131] Zhou Y., Xu Z., Wang M., Meng X., Yin H., Electrochemicalimmunoassay platform for high sensitivity detection of indole-3-acetic acid, Electrochim. Acta, 2013, 96, 66-73.[Crossref]
• [132] Sluyters-Rehbach M., Sluyters J.H., On the impedance ofgalvanic cells XXVIII. The frequency-dependence of the electrodeadmittance for systems with first-order homogeneous chemicalreactions and reactant adsorption occurring simultaneously, J.Electroanal. Chem. Interf. Electrochem., 1969, 23, 457-474.[Crossref]
• [133] Ershler B., Investigation of electrode reactions by the methodof charging-curves and with the aid of alternating currents,Discuss. Faraday Soc., 1947, 1, 269-277.[Crossref]
• [134] Hu Y., Zuo P., Ye B.C., Label-free electrochemical impedancespectroscopy biosensor for direct detection of cancer cellsbased on the interaction between carbohydrate and lectin,Biosens. Bioelectron., 2013, 43, 79-83.[Crossref]
• [135] Bertok T., Sediva A., Katrlik J., Gemeiner P., Mikula M., NoskoM., et al., Label-free detection of glycoproteins by the lectinbiosensor down to attomolar level using gold nanoparticles,Talanta, 2013, 108, 11-18.[Crossref]
• [136] Suni I.I., Impedance methods for electrochemical sensors usingnanomaterials, Trends Anal. Chem., 2008, 27, 604-611.[Crossref]
• [137] Scouten W.H., Luong J.H.T., Stephen Brown R., Enzyme orprotein immobilization techniques for applications in biosensordesign, Trends Biotechnol., 1995, 13, 178-185.[Crossref]
• [138] Li S., Singh J., Li H., Banerjee I.A. Biosensor Nanomaterials:Wiley-VCH Verlag GmbH&Co. ; 2011.
• [139] Putzbach W., Ronkainen N., Immobilization techniques in thefabrication of nanomaterial-based electrochemical biosensors:A review, Sensors, 2013, 13, 4811-4840.[Crossref]
• [140] Davis J.J., Tkac J., Humphreys R., Buxton A.T., Lee T.A., KoFerrigno P., Peptide aptamers in label-free protein detection:2. Chemical optimization and detection of distinct proteinisoforms, Anal. Chem., 2009, 81, 3314-3320.[Crossref]
• [141] Davis J.J., Tkac J., Laurenson S., Ferrigno P.K., Peptide aptamersin label-free protein detection: 1. Characterization of theimmobilized scaffold, Anal. Chem., 2007, 79, 1089-1096.[Crossref]
• [142] Ericsson E. Biosensor surface chemistry for oriented proteinimmobilization and biochip patterning: Linköping University;2013.
• [143] Love J.C., Estroff L.A., Kriebel J.K., Nuzzo R.G., Whitesides G.M.,Self-assembled monolayers of thiolates on metals as a form ofnanotechnology, Chem. Rev., 2005, 105, 1103-1170.[Crossref]
• [144] Gooding J.J., Mearns F., Yang W., Liu J., Self-assembledmonolayers into the 21st century: Recent advances andapplications, Electroanal., 2003, 15, 81-96.[Crossref]
• [145] Hushegyi A., Tkac J., Are glycan biosensors an alternative toglycan microarrays?, Anal. Methods, 2014, 6, 6610-6620.[Crossref]
• [146] Ron H., Matlis S., Rubinstein I., Self-assembled monolayerson oxidized metals. 2. gold surface oxidative pretreatment,monolayer properties, and depression formation, Langmuir,1998, 14, 1116-1121.[Crossref]
• [147] Bertok T., Gemeiner P., Mikula M., Gemeiner P., Tkac J.,Ultrasensitive impedimetric lectin based biosensor forglycoproteins containing sialic acid, Microchim. Acta, 2013,180, 151-159.[Crossref]
• [148] Fischer L.M., Tenje M., Heiskanen A.R., Masuda N., Castillo J.,Bentien A., et al., Gold cleaning methods for electrochemicaldetection applications, Microelectronic Eng., 2009, 86, 1282-1285.[Crossref]
• [149] Chen S., LaRoche T., Hamelinck D., Bergsma D., Brenner D.,Simeone D., et al., Multiplexed analysis of glycan variationon native proteins captured by antibody microarrays, Nat.Methods, 2007, 4, 437-444.
• [150] Haab B.B., Antibody-lectin sandwich arrays for biomarker andglycobiology studies, Expert Rev. Proteomics, 2010, 7, 9-11.[Crossref]
• [151] Chen H., Jiang C., Yu C., Zhang S., Liu B., Kong J., Proteinchips and nanomaterials for application in tumor markerimmunoassays, Biosens. Bioelectron., 2009, 24, 3399-3411.[Crossref]
• [152] La Belle J.T., Gerlach J.Q., Svarovsky S., Joshi L., Label-freeimpedimetric detection of glycan−lectin interactions, Anal.Chem., 2007, 79, 6959-6964.[Crossref]
• [153] Yang H., Li Z., Wei X., Huang R., Qi H., Gao Q., et al., Detectionand discrimination of alpha-fetoprotein with a label-freeelectrochemical impedance spectroscopy biosensor arraybased on lectin functionalized carbon nanotubes, Talanta,2013, 111, 62-68.[Crossref]
• [154] Oliveira M.D.L., Correia M.T.S., Diniz F.B., A novel approach toclassify serum glycoproteins from patients infected by dengueusing electrochemical impedance spectroscopy analysis,Synth. Met., 2009, 159, 2162-2164.[Crossref]
• [155] Nagaraj V.J., Aithal S., Eaton S., Bothara M., Wiktor P., PrasadS., NanoMonitor: a miniature electronic biosensor for glycanbiomarker detection, Nanomedicine, 2010, 5, 369-378.[Crossref]
• [156] Bertok T., Klukova L., Sediva A., Kasak P., Semak V., MicusikM., et al., Ultrasensitive impedimetric lectin biosensors withefficient antifouling properties applied in glycoprofiling ofhuman serum samples, Anal. Chem., 2013, 85, 7324-7332.[Crossref]
• [157] Silva M.L.S., Gutiérrez E., Rodríguez J.A., Gomes C., David L.,Construction and validation of a Sambucus nigra biosensor forcancer-associated STn antigen, Biosens. Bioelectron., 2014, 57,254-261.[Crossref]
• [158] Kongsuphol P., Ng H.H., Pursey J.P., Arya S.K., Wong C.C., StulzE., et al., EIS-based biosensor for ultra-sensitive detection ofTNF-α from non-diluted human serum, Biosens. Bioelectron.,2014, 61, 274-279.[Crossref]
• [159] Luo X., Xu Q., James T., Davis J.J., Redox and label-free arraydetection of protein markers in human serum, Anal. Chem.,2014, 86, 5553-5558.[Crossref]
• [160] Xia N., Deng D., Zhang L., Yuan B., Jing M., Du J., et al., Sandwichtypeelectrochemical biosensor for glycoproteins detectionbased on dual-amplification of boronic acid-gold nanoparticles and dopamine-gold nanoparticles, Biosens. Bioelectron., 2013,43, 155-159.[Crossref]
• [161] Cao J.T., Hao X.Y., Zhu Y.D., Sun K., Zhu J.J., Microfluidic platformfor the evaluation of multi-glycan expressions on living cellsusing electrochemical impedance spectroscopy and opticalmicroscope, Anal. Chem., 2012, 84, 6775-6782. [Crossref]

Identifiers

DOI

10.1515/chem-2015-0082