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Analytical and Bioanalytical Chemistry

, Volume 411, Issue 15, pp 3309–3319 | Cite as

Rapid SERS-based recognition of cell secretome on the folic acid-functionalized gold gratings

  • Olga Guselnikova
  • Barbara Dvorankova
  • Kamila Kakisheva
  • Yevgeniya Kalachyova
  • Pavel Postnikov
  • Vaclav Svorcik
  • Oleksiy LyutakovEmail author
Research Paper

Abstract

Nowadays, functionalization of the plasmon-supported nanostructured surface is considered as a powerful tool for tumour cell recognition. In this study, the SERS on a surface plasmon polariton-supported gold grating functionalized with folic acid was used to demonstrate an unpretentious recognition of melanoma-associated fibroblasts. Using cultivation media conditioned by different cells, we were able to detect reproducible differences in the secretome of melanoma-associated and normal control fibroblasts. The homogeneous distribution of plasmon energy along the grating surface was proved to provide excellent SERS signal reproducibility, while, to increase the affinity of (bio)molecules to SERS substrate, folic acid molecules were covalently grafted to the gold gratings. As proof of concept, fibroblasts were cultured in vitro, and culture media from the normal and tumour-associated lines were collected and analysed with our proposed SERS substrates. Identifying individual peaks of the Raman spectra as well as comparing their relative intensities, we showed that the proposed functional SERS platform can recognise the melanoma-associated cells without the need for further statistical spectral evaluation directly. We also demonstrated that the SERS chip created provided a stable SERS signal over a period of 90 days without loss of sensitivity.

Graphical abstract

Keywords

SERS sensor Surface modification Melanoma Cancer Reproducibility of SERS 

Notes

Funding information

This work was supported by the Ministry of Health of CR under the project 15-33459A, Tomsk Polytechnic University (VIU-RSCABS-68/2019).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

216_2019_1801_MOESM1_ESM.pdf (1.3 mb)
ESM 1 (PDF 1.27 mb)

References

  1. 1.
    Perfézou M, Turner A, Merkoçi A. Cancer detection using nanoparticle-based sensors. Chem Soc Rev. 2012;41(7):2606–22.CrossRefPubMedGoogle Scholar
  2. 2.
    Peto J. Cancer epidemiology in the last century and the next decade. Nature. 2011;411(6835):390–5.CrossRefGoogle Scholar
  3. 3.
    Bernard AM, Moreau D, Lauwerys RR. Latex immunoassay of retinol-binding protein. Clin Chem. 1982;28:1167–71.PubMedGoogle Scholar
  4. 4.
    Song MI, Iwata KM, Yamada YK, Takeuchi T, Tamiya E, Karube I. Multisample analysis using an array of microreactors for an alternating-current field-enhanced latex immunoassay. Anal Chem. 1994;66:778–81.CrossRefPubMedGoogle Scholar
  5. 5.
    Petricoin EF, Ardekani AM, Hitt BA, Levine PJ, Fusaro VA, Steinberg S, et al. Use of proteomic patterns in serum to identify ovarian cancer. Lancet. 2002;359(9306):572–7.CrossRefPubMedGoogle Scholar
  6. 6.
    Luo S, Zhang E, Su Y, Cheng T, Shi C. A review of NIR dyes in cancer targeting and imaging. Biomaterials. 2011;32(29):7127–38.CrossRefPubMedGoogle Scholar
  7. 7.
    González-Solís JL, Martínez-Espinosa JC, Salgado-Román JM, Palomares-Anda P. Monitoring of chemotherapy leukemia treatment using Raman spectroscopy and principal component analysis. Lasers Med Sci. 2014;29:1241–9.CrossRefPubMedGoogle Scholar
  8. 8.
    Rabah R, Weber R, Serhatkulu GK, Cao A, Dai H, Pandya A, et al. Diagnosis of neuroblastoma and ganglioneuroma using Raman spectroscopy. Pediatr Surg. 2008;43:171–6.CrossRefGoogle Scholar
  9. 9.
    Lee M, Kim K, Kim KH, Oh KW, Choo J. SERS-based immunoassay using a gold array-embedded gradient microfluidic chip. Lab Chip. 2012;12:3720–7.CrossRefPubMedGoogle Scholar
  10. 10.
    Que R, Shao M, Zhuo S, Wen C, Wang S, Lee ST. Highly reproducible surface enhanced Raman scattering on a capillarity assisted gold nanoparticle assembly. Adv Funct Mater. 2011;21:3337–43.CrossRefGoogle Scholar
  11. 11.
    Qu L, Wang N, Xu H, Wang W, Liu Y, Kuo L, et al. Gold nanoparticles and gC3N4 intercalated graphene oxide membrane for recyclable surface enhanced Raman scattering. Adv Funct Mater. 2017;27(31):1701714.CrossRefGoogle Scholar
  12. 12.
    Feng S, Chen R, Lin J, Pan J, Wu Y, Li Y, et al. Gastric cancer detection based on blood plasma surface-enhanced Raman spectroscopy excited by polarized laser light. Biosens Bioelectron. 2011;26:3167–74.CrossRefPubMedGoogle Scholar
  13. 13.
    Le Ru EC, Blackie E, Meyer M, Etchegoin PG. Surface enhanced Raman scattering enhancement factors: a comprehensive study. J Phys Chem C. 2007;111(37):13794–803.CrossRefGoogle Scholar
  14. 14.
    De Angelis F, Gentile F, Mecarini F, Das G, Moretti M, Candeloro P, et al. Breaking the diffusion limit with super-hydrophobic delivery of molecules to plasmonic nanofocusing SERS structures. Nat Photonics. 2011;5(11):682–7.CrossRefGoogle Scholar
  15. 15.
    Jia Y, Shmakov SN, Pinkhassik E. General strategy for the synthesis of transition metal phosphide films for electrocatalytic hydrogen and oxygen evolution. ACS Appl Mater Interfaces. 2016;8(30):19755–63.CrossRefPubMedGoogle Scholar
  16. 16.
    Giese B, McNaughton D. Surface-enhanced Raman spectroscopic study of uracil. The influence of the surface substrate, surface potential, and pH. J Phys Chem B. 2002;106(6):1461–70.CrossRefGoogle Scholar
  17. 17.
    Lee M, Lee S, Lee JH, Lim HW, Seong GH, Lee EK, et al. Highly reproducible immunoassay of cancer markers on a gold-patterned microarray chip using surface-enhanced Raman scattering imaging. Biosens Bioelectron. 2011;26(5):2135–41.CrossRefPubMedGoogle Scholar
  18. 18.
    Cialla-May D, Zheng XS, Weber K, Popp J. Recent progress in surface-enhanced Raman spectroscopy for biological and biomedical applications: from cells to clinics. Chem Soc Rev. 2017;46:3945–61.CrossRefPubMedGoogle Scholar
  19. 19.
    Banaei N, Foley A, Houghton JM, Sun Y, Kim B. Multiplex detection of pancreatic cancer biomarkers using a SERS-based immunoassay. Nanotechnology. 2017;28(45):455101–9.CrossRefPubMedGoogle Scholar
  20. 20.
    Lee S, Chon H, Lee J, Ko J, Chung BH, Lim DW, et al. Rapid and sensitive phenotypic marker detection on breast cancer cells using surface-enhanced Raman scattering (SERS) imaging. Biosens Bioelectron. 2014;51:238–43.CrossRefPubMedGoogle Scholar
  21. 21.
    Wu X, Luo L, Yang S, Ma X, Li Y, Dong C, et al. Improved SERS nanoparticles for direct detection of circulating tumor cells in the blood. ACS Appl Mater Interfaces. 2015;7(18):9965–71.CrossRefPubMedGoogle Scholar
  22. 22.
    D’Hollander A, Mathieu E, Jans H, Velde GV, Stakenborg T, Dorpe PV, et al. Development of nanostars as a biocompatible tumor contrast agent: toward in vivo SERS imaging. Int J Nanomed. 2016;11:3703–14.CrossRefGoogle Scholar
  23. 23.
    Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, et al. MicroRNA expression profiles classify human cancers. Nature. 2005;435(7043):834–8.CrossRefPubMedGoogle Scholar
  24. 24.
    Boca S, Farcau C, Baia M, Astilean S. Metanephrine neuroendocrine tumor marker detection by SERS using Au nanoparticle/Au film sandwich architecture. Biomed Microdevices. 2016;18:12–8.CrossRefPubMedGoogle Scholar
  25. 25.
    Yi N, Zhang C, Song Q, Xiao S. A hybrid system with highly enhanced graphene SERS for rapid and tag-free tumor cells detection. Sci Rep. 2016;6:25134.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Zong S, Wang L, Chen Ch LJ, Zhu D, Zhang Y, Wang Z, et al. Facile detection of tumor-derived exosomes using magnetic nanobeads and SERS nanoprobes. Anal Methods. 2016;8:5001–8.CrossRefGoogle Scholar
  27. 27.
    Zhang Y, Yang P, Muhammed MAH, Alsaiari Sh K, Moosa B, Almalik A, et al. Unable and linker free nanogaps in core–shell plasmonic nanorods for selective and quantitative detection of circulating tumor cells by SERS. ACS Appl Mater Interfaces. 2017;9(43):37597–605.CrossRefPubMedGoogle Scholar
  28. 28.
    Yue J, Liu Z, Cai X, Ding X, Shen S, Tao K, et al. Bull serum albumin coated Au@Agnanorods as SERS probes for ultrasensitive osteosarcoma cell detection. Talanta. 2016;150:503–9.CrossRefPubMedGoogle Scholar
  29. 29.
    Kalachyova Y, Mares D, Lyutakov O, Kostejn M, Lapcak L, Švorčík V. Surface plasmon polaritons on silver gratings for optimal SERS response. J Phys Chem C. 2015;119(17):9506–12.CrossRefGoogle Scholar
  30. 30.
    Kalachyova Y, Mares D, Jerabek V, Zaruba K, Ulbrich P, Lapcak L, et al. The effect of silver grating and nanoparticles grafting for LSP-SPP coupling and SERS response intensification. J Phys Chem C. 2016;120(19):10569–77.CrossRefGoogle Scholar
  31. 31.
    Guselnikova O, Postnikov P, Erzina M, Kalachyova Y, Svorcik V, Lyutakov O. Pretreatment-free selective and reproducible SERS-based detection of heavy metal ions on DTPA functionalized plasmonic platform. Sens Actuators B Chem. 2017;253:830–8.CrossRefGoogle Scholar
  32. 32.
    Guselnikova O, Postnikov P, Kalachyova Y, Kolska Z, Libansky M, Zima J, et al. Large-scale, ultrasensitive, highly reproducible and reusable smart SERS platform based on PNIPAm-grafted gold grating. ChemNanoMat. 2017;3(2):135–44.CrossRefGoogle Scholar
  33. 33.
    Guselnikova O, Postnikov P, Elashnikov R, Trusova M, Kalachyova Y, Libansky M, et al. Surface modification of Au and Ag plasmonic thin films via diazonium chemistry: evaluation of structure and properties. Colloids Surf A Physicochem Eng Asp. 2017;516:274–85.CrossRefGoogle Scholar
  34. 34.
    Dvořánková B, Lacina L, Smetana K. Isolation of normal fibroblasts and their cancer associated counterparts (CAFs) for biomedical research. Methods Mol Biol Springer Science. 2018;393–408Google Scholar
  35. 35.
    Filimonov VD, Trusova ME, Postnikov PS, Krasnokutskaya AE, Lee YM, Hwang HY, et al. Unusually stable, versatile, and pure arenediazonium tosylates: their preparation, structures, and synthetic applicability. Org Lett. 2008;18:3961–4.CrossRefGoogle Scholar
  36. 36.
    Geszke M, Murias M, Balan L, Medjahdi G, Korczynski J, Moritz M, et al. Folic acid-conjugated core/shell ZnS:Mn/ZnS quantum dots as targeted probes for two photon fluorescence imaging of cancer cells. Acta Biomater. 2011;7(3):1327–38.CrossRefPubMedGoogle Scholar
  37. 37.
    Mohapatra S, Mallick SK, Maiti TK, Ghosh SK, Pramanik P. Synthesis of highly stable folic acid conjugated magnetite nanoparticles for targeting cancer cells. Nanotechnology. 2007;18(38):385102.CrossRefGoogle Scholar
  38. 38.
    Kim A, Barcelo SJ, Williams RS, Li Z. Melamine sensing in milk products by using surface enhanced Raman scattering. Anal Chem. 2012;84:9303–9.CrossRefPubMedGoogle Scholar
  39. 39.
    Morelli L, Zór K, Jendresen CB, Rindzevicius T, Schmid MS, Nielsen AT, et al. Surface enhanced Raman scattering for quantification of p-coumaric acid produced by Escherichia coli. Anal Chem. 2017;89(7):3981–7.CrossRefPubMedGoogle Scholar
  40. 40.
    Vo-Dinh T, Wang HN, Scaffidi J. Plasmonic nanoprobes for SERS biosensing and bioimaging. J Biophotonics. 2010;3(1–2):89–102.PubMedPubMedCentralGoogle Scholar
  41. 41.
    Wang X, Wang C, Cheng L, Lee ST, Liu Z. Noble metal coated single-walled carbon nanotubes for applications in surface-enhanced Raman scattering imaging and photothermal therapy. J Am Chem Soc. 2012;134(17):7414–22.CrossRefPubMedGoogle Scholar
  42. 42.
    Danhier F, Feron O, Préat V. To exploit the tumor microenvironment: passive and active tumor targeting of nanocarriers for anti-cancer drug delivery. J Control Release. 2010;148(2):135–46.CrossRefPubMedGoogle Scholar
  43. 43.
    Boca-Farcau S, Potara M, Simon T, Juhem A, Baldeck P, Astilean S. Folic acid-conjugated, SERS-labeled silver nanotriangles for multimodal detection and targeted photothermal treatment on human ovarian cancer cells. Mol Pharm. 2013;11(2):391–9.CrossRefPubMedGoogle Scholar
  44. 44.
    Wang Y, Newell BB, Irudayaraj J. Folic acid protected silver nanocarriers for targeted drug delivery. J Biomed Nanotechnol. 2012;8(5):751–9.CrossRefPubMedGoogle Scholar
  45. 45.
    Doppelt P, Hallais G, Pinson J, Podvorica F, Verneyre S. Surface modification of conducting substrates. The existence of azo bonds in the structure of organic layers obtained from diazonium salts. Chem Mater. 2007;19(18):4570–5.CrossRefGoogle Scholar
  46. 46.
    Guselnikova O, Kalachyova Y, Hrobonova K, Trusova M, Barek J, Postnikov P, et al. SERS platform for detection of lipids and disease markers prepared using modification of plasmonic-active gold gratings by lipophilic moieties. Sens Actuator B Chem. 2018;265:182–92.CrossRefGoogle Scholar
  47. 47.
    Hu Z, Li J, Li C, Zhao S, Li N, Wang Y, et al. Folic acid-conjugated graphene–ZnO nanohybrid for targeting photodynamic therapy under visible light irradiation. J Mater Chem B. 2013;1(38):5003–13.CrossRefGoogle Scholar
  48. 48.
    Weitman S, Lark R, Coney L, Fort D, Frasca V, Zurawski V, et al. Distribution of the folate receptor GP38 in normal and malignant cell lines and tissues. Cancer Res. 1992;52:3396–401.PubMedGoogle Scholar
  49. 49.
    Frade V, Chudasama C, Cordeiro S, Caddick S, Gois PMP. Targeting cancer cells with folic acid–iminoboronate fluorescent conjugates. Chem Commun. 2014;50:5261–3.CrossRefGoogle Scholar
  50. 50.
    Zhao J, Lui H, Kalia S, Zeng H. Real-time Raman spectroscopy for automatic in vivo skin cancer detection: an independent validation. Anal Bioanal Chem. 2015;407:8373–9.CrossRefPubMedGoogle Scholar
  51. 51.
    Kanchanapally R, Fan Z, Singh AK, Sinha SS, Ray PC. Multifunctional hybrid graphene oxide for label-free detection of malignant melanoma from infected blood. J Mater Chem B. 2014;2:1934–7.CrossRefGoogle Scholar
  52. 52.
    Lui H, Zhao J, McLean D, Zen H. Real-time Raman spectroscopy for in vivo skin cancer diagnosis. Cancer Res. 2012;72(10):2491–500.CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Olga Guselnikova
    • 1
    • 2
  • Barbara Dvorankova
    • 3
  • Kamila Kakisheva
    • 1
  • Yevgeniya Kalachyova
    • 1
    • 2
  • Pavel Postnikov
    • 2
  • Vaclav Svorcik
    • 1
  • Oleksiy Lyutakov
    • 1
    • 2
    Email author
  1. 1.Department of Solid State EngineeringUniversity of Chemistry and TechnologyPragueCzech Republic
  2. 2.Research School of Chemistry and Applied Biomedical SciencesTomsk Polytechnic UniversityTomskRussian Federation
  3. 3.Institute of Anatomy, 1st Faculty of MedicineCharles UniversityPragueCzech Republic

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