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Interdigitated impedimetric-based Maackia amurensis lectin biosensor for prostate cancer biomarker

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Abstract

Highly specific detection of tumor-associated biomarkers remains a challenge in the diagnosis of prostate cancer. In this research, Maackia amurensis (MAA) was used as a recognition element in the functionalization of an electrochemical impedance-spectroscopy biosensor without a label to identify cancer-associated aberrant glycosylation prostate-specific antigen (PSA). The lectin was immobilized on gold-interdigitated microelectrodes. Furthermore, the biosensor’s impedance response was used to assess the establishment of a complex binding between MAA and PSA-containing glycans. With a small sample volume, the functionalized interdigitated impedimetric-based (IIB) biosensor exhibited high sensitivity, rapid response, and repeatability. PSA glycoprotein detection was performed by measuring electron transfer resistance values within a concentration range 0.01–100 ng/mL, with a detection limit of 3.574 pg/mL. In this study, the ability of MAA to preferentially recognize α2,3-linked sialic acid in serum PSA was proven, suggesting a potential platform for the development of lectin-based, miniaturized, and cost effective IIB biosensors for future disease detection.

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The authors declare that the data generated or analysed during this study are included in this published article.

References

  1. Díaz-Fernández A, Lorenzo-Gómez R, Miranda-Castro R et al (2020) Electrochemical aptasensors for cancer diagnosis in biological fluids – A review. Anal Chim Acta 1124:1–19. https://doi.org/10.1016/j.aca.2020.04.022

    Article  CAS  PubMed  Google Scholar 

  2. Kirwan A, Utratna M, O’Dwyer ME et al (2015) Glycosylation-based serum biomarkers for cancer diagnostics and prognostics. Biomed Res Int 2015. https://doi.org/10.1155/2015/490531

  3. Rawla P (2019) Epidemiology of Prostate Cancer. World J Oncol 10:63–89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Drake RR, Jones EE, Powers TW, Nyalwidhe JO (2015) Altered glycosylation in prostate cancer, 1st ed. Elsevier Inc.

    Google Scholar 

  5. Lilja H, Ulmert D, Vickers AJ (2008) Prostate-specific antigen and prostate cancer: prediction, detection and monitoring. Nat Rev Cancer 8:268–278

    Article  CAS  PubMed  Google Scholar 

  6. Gilgunn S, Conroy PJ, Saldova R et al (2013) Aberrant PSA glycosylation - a sweet predictor of prostate cancer. Nat Rev Urol 10:99–107

    Article  CAS  PubMed  Google Scholar 

  7. Belick S, Katrl J (2016) Glycan and lectin biosensors ˇ. Essays Biochem 60:37–47. https://doi.org/10.1042/EBC20150005

    Article  Google Scholar 

  8. Belický Š, Tkac J (2014) Can glycoprofiling be helpful in detecting prostate cancer? Chem Pap 69:90–111. https://doi.org/10.1515/chempap-2015-0052.Can

    Article  Google Scholar 

  9. Scott E, Munkley J (2019) Glycans as biomarkers in prostate cancer. Int J Mol Sci 20:1389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Pearce OMT, Läubli H (2015) Sialic acids in cancer biology and immunity. Glycobiology 26:111–128. https://doi.org/10.1093/glycob/cwv097

    Article  CAS  PubMed  Google Scholar 

  11. Hernández-Arteaga AC, de Jesús Z-NJ, Martínez-Martínez MU et al (2019) Determination of salivary sialic acid through nanotechnology: a useful biomarker for the screening of breast cancer. Arch Med Res 50:105–110. https://doi.org/10.1016/j.arcmed.2019.05.013

    Article  CAS  PubMed  Google Scholar 

  12. Berghuis AY, Pijnenborg JFA, Boltje TJ, Pijnenborg JMA (2022) Sialic acids in gynecological cancer development and progression: Impact on diagnosis and treatment. Int J Cancer 150:678–687. https://doi.org/10.1002/ijc.33866

    Article  CAS  PubMed  Google Scholar 

  13. Elgohary MM, Helmy MW, Abdelfattah EZA et al (2018) Targeting sialic acid residues on lung cancer cells by inhalable boronic acid-decorated albumin nanocomposites for combined chemo/herbal therapy. J Control Release 285:230–243. https://doi.org/10.1016/j.jconrel.2018.07.014

    Article  CAS  PubMed  Google Scholar 

  14. Pihikova D, Pakanova Z, Nemcovic M et al (2016) Sweet characterisation of prostate specific antigen using electrochemical lectin-based immunosensor assay and MALDI TOF/TOF analysis: Focus on sialic acid. Proteomics 16:3085–3095. https://doi.org/10.1002/pmic.201500463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Büll C, Stoel MA, Den Brok MH, Adema GJ (2014) Sialic acids sweeten a tumor’s life. Cancer Res 74:3199–3204. https://doi.org/10.1158/0008-5472.CAN-14-0728

    Article  CAS  PubMed  Google Scholar 

  16. Kałuża A, Szczykutowicz J, Ferens-Sieczkowska M (2021) Glycosylation: rising potential for prostate cancer evaluation. Cancers (Basel) 13. https://doi.org/10.3390/cancers13153726

  17. Belicky S, Černocká H, Bertok T et al (2017) Label-free chronopotentiometric glycoprofiling of prostate specific antigen using sialic acid recognizing lectins. Bioelectrochemistry 117:89–94. https://doi.org/10.1016/j.bioelechem.2017.06.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ohyama C, Hosono M, Nitta K et al (2004) Carbohydrate structure and differential binding of prostate specific antigen to Maackia amurensis lectin between prostate cancer and benign prostate hypertrophy. Glycobiology 14:671–679

    Article  CAS  PubMed  Google Scholar 

  19. Silva PMS, Lima ALR, Silva BVM et al (2016) Cratylia mollis lectin nanoelectrode for differential diagnostic of prostate cancer and benign prostatic hyperplasia based on label-free detection. Biosens Bioelectron 85:171–177. https://doi.org/10.1016/j.bios.2016.05.004

    Article  CAS  PubMed  Google Scholar 

  20. Vermassen T, Speeckaert MM, Lumen N et al (2012) Glycosylation of prostate specific antigen and its potential diagnostic applications. Clin Chim Acta 413:1500–1505. https://doi.org/10.1016/j.cca.2012.06.007

    Article  CAS  PubMed  Google Scholar 

  21. Alley WR, Mann BF, Novotny MV (2013) High-sensitivity analytical approaches for the structural characterization of glycoproteins. Chem Rev 113:2668–2732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Hirabayashi J, Yamada M, Kuno A, Tateno H (2013) Lectin microarrays: Concept, principle and applications. Chem Soc Rev 42:4443–4458. https://doi.org/10.1039/c3cs35419a

    Article  CAS  PubMed  Google Scholar 

  23. Shimomura M, Nakayama K, Azuma K et al (2015) Establishment of a novel lectin-antibody ELISA system to determine core-fucosylated haptoglobin. Clin Chim Acta 446:30–36. https://doi.org/10.1016/j.cca.2015.03.037

    Article  CAS  PubMed  Google Scholar 

  24. Lam SK, Ng TB (2011) Lectins: Production and practical applications. Appl Microbiol Biotechnol 89:45–55

    Article  CAS  PubMed  Google Scholar 

  25. Rahman SFA, Md Arshad MK, Gopinath SCB et al (2021) Glycosylated biomarker sensors: advancements in prostate cancer diagnosis. Chem Commun 57:9640–9655. https://doi.org/10.1039/d1cc03080a

    Article  CAS  Google Scholar 

  26. Pihikova D, Kasak P, Kubanikova P et al (2016) Aberrant sialylation of a prostate-specific antigen: electrochemical label-free glycoprofiling in prostate cancer serum samples. Anal Chim Acta 934:72–79. https://doi.org/10.1016/j.aca.2016.06.043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Sánchez-tirado E, González-cortés A, Yáñez-sedeño P, Pingarrón JM (2018) Magnetic multiwalled carbon nanotubes as nanocarrier tags for sensitive determination of fetuin in saliva. Biosens Bioelectron 113:88–94. https://doi.org/10.1016/j.bios.2018.04.056

    Article  CAS  PubMed  Google Scholar 

  28. Dalila RN, Arshad MKM, Gopinath SCB et al (2022) Faradaic electrochemical impedimetric analysis on MoS2/Au-NPs decorated surface for C-reactive protein detection. J Taiwan Inst Chem Eng 138. https://doi.org/10.1016/j.jtice.2022.104450

  29. Tang X, Flandre D, Raskin JP et al (2011) A new interdigitated array microelectrode-oxide-silicon sensor with label-free, high sensitivity and specificity for fast bacteria detection. Sensors Actuators B Chem 156:578–587. https://doi.org/10.1016/j.snb.2011.02.002

    Article  CAS  Google Scholar 

  30. Kuphal M, Mills CA, Korri-Youssoufi H, Samitier J (2012) Polymer-based technology platform for robust electrochemical sensing using gold microelectrodes. Sensors Actuators B Chem 161:279–284. https://doi.org/10.1016/j.snb.2011.10.032

    Article  CAS  Google Scholar 

  31. Sharma PK, Kim ES, Mishra S et al (2022) Ultrasensitive probeless capacitive biosensor for amyloid beta (Aβ1-42) detection in human plasma using interdigitated electrodes. Biosens Bioelectron 212:114365. https://doi.org/10.1016/j.bios.2022.114365

    Article  CAS  PubMed  Google Scholar 

  32. Supraja P, Tripathy S, Singh R et al (2021) Towards point-of-care diagnosis of Alzheimer’s disease: Multi-analyte based portable chemiresistive platform for simultaneous detection of β-amyloid (1–40) and (1–42) in plasma. Biosens Bioelectron 186:113294. https://doi.org/10.1016/j.bios.2021.113294

    Article  CAS  PubMed  Google Scholar 

  33. Ibau C, Arshad MKM, Gopinath SCB et al (2020) Immunosensing prostate-specific antigen: Faradaic vs non-Faradaic electrochemical impedance spectroscopy analysis on interdigitated microelectrode device. Int J Biol Macromol 162:1924–1936. https://doi.org/10.1016/j.ijbiomac.2020.08.125

    Article  CAS  PubMed  Google Scholar 

  34. West A (2018) Chapter 3 - Experimental methods to investigate self-assembly at interfaces. In: Ball V (ed) Interface Science and Technology. Elsevier B.V., pp 131–241

    Google Scholar 

  35. Ubuo EE, Udoetok IA, Tyowua AT et al (2021) The direct cause of amplified wettability : roughness or surface chemistry? J Compos Sci 5:1–9

    Article  Google Scholar 

  36. Swain PS, Lipowsky R (1998) Contact angles on heterogeneous surfaces: a new look at Cassie’s and Wenzel’s Laws. Langmuir 14:6772–6780

    Article  CAS  Google Scholar 

  37. Yan Q, Zheng H-N, Jiang C et al (2015) EDC/NHS activation mechanism of polymethacrylic acid: anhydride versus NHS-ester. RSC Adv 5:69939–69947

    Article  ADS  CAS  Google Scholar 

  38. Lim CY, Owens NA, Wampler RD et al (2014) Succinimidyl ester surface chemistry: implications of the competition between aminolysis and hydrolysis on covalent protein immobilization. Langmuir 30:12868–12878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Nam K, Kimura T, Kishida A (2008) Controlling coupling reaction of EDC and NHS for preparation of collagen gels using ethanol/water co-solvents. Macromol Biosci 8:32–37

    Article  CAS  PubMed  Google Scholar 

  40. Zeng Q (2018) Size matching effect on Wenzel wetting on fractal surfaces. Results Phys 10:588–593

    Article  ADS  Google Scholar 

  41. Ko YG, Ma PX (2009) Surface-grafting of phosphates onto a polymer for potential biomimetic functionalization of biomaterials. J Colloid Interface Sci 330:77–83

    Article  ADS  CAS  PubMed  Google Scholar 

  42. Mendoza SM, Arfaoui I, Zanarini S et al (2007) Improvements in the characterization of the crystalline structure of acid-terminated alkanethiol self-assembled monolayers on Au(111). Langmuir 23:582–588

    Article  CAS  PubMed  Google Scholar 

  43. Delamarche E, Sundarababu G, Biebuyck H et al (1996) Immobilization of antibodies on a photoactive self-assembled monolayer on gold. Langmuir 12:1997–2006

    Article  CAS  Google Scholar 

  44. Böcking T, Wong ELS, James M et al (2006) Immobilization of dendrimers on Si–C linked carboxylic acid-terminated monolayers on silicon(111). Thin Solid Films 515:1857–1863

    Article  ADS  Google Scholar 

  45. Niedermaier I, Kolbeck C, Taccardi N et al (2012) Organic reactions in ionic liquids studied by in situ XPS. ChemPhysChem 13:1725–1735

    Article  CAS  PubMed  Google Scholar 

  46. Castner DG, Hinds K, Grainger DW (1996) X-ray photoelectron spectroscopy sulfur 2p study of organic thiol and disulfide binding interactions with gold surfaces. Langmuir 12:5083–5086

    Article  CAS  Google Scholar 

  47. Azmi UZM, Yusof NA, Kusnin N et al (2018) Sandwich electrochemical immunosensor for early detection of tuberculosis based on graphene/polyaniline-modified screen-printed gold electrode. Sensors (Switzerland) 18:1–14

    Google Scholar 

  48. Jolly P, Damborsky P, Madaboosi N et al (2016) DNA aptamer-based sandwich microfluidic assays for dual quantification and multi-glycan profiling of cancer biomarkers. Biosens Bioelectron 79:313–319

    Article  CAS  PubMed  Google Scholar 

  49. Kavosi B, Salimi A, Hallaj R, Moradi F (2015) Ultrasensitive electrochemical immunosensor for PSA biomarker detection in prostate cancer cells using gold nanoparticles/PAMAM dendrimer loaded with enzyme linked aptamer as integrated triple signal amplification strategy. Biosens Bioelectron 74:915–923

    Article  CAS  PubMed  Google Scholar 

  50. Argoubi W, Sánchez A, Parrado C et al (2018) Label-free electrochemical aptasensing platform based on mesoporous silica thin film for the detection of prostate specific antigen. Sensors Actuators B Chem 255:309–315

    Article  CAS  Google Scholar 

  51. Zapatero-Rodríguez J, Liébana S, Sharma S et al (2018) Detection of free prostate-specific antigen using a novel single-chain antibody (scAb)-based magneto-immunosensor. Bionanoscience 8:680–689

    Article  Google Scholar 

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Funding

This work was supported by the Ministry of Education Malaysia through the (MyPAIR) Hubert Curien Partnership – Hibiscus Grant, grant number MyPAIR/1/2020/STG05/UniMAP/1.

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S.F.A. Rahman: Methodology, Investigation, Writing – Original Draft. M.K. Md Arshad: Conceptualization, Supervision, Project Administration, Funding acquisition. Subash C. B. Gopinath: Supervision, Writing – Review & Editing. M. F. M. Fathil: Supervision, Writing – Review & Editing. Frédéric Sarry: Funding Acquisition. Conlathan Ibau: Resources, Data Curation, Validation. Omar Elmazria: Conceptualization. Sami Hage-Ali: Conceptualization.

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Correspondence to Mohd Khairuddin Md Arshad.

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Rahman, S.F.A., Arshad, M.K.M., Gopinath, S.C.B. et al. Interdigitated impedimetric-based Maackia amurensis lectin biosensor for prostate cancer biomarker. Microchim Acta 191, 118 (2024). https://doi.org/10.1007/s00604-024-06189-4

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