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Electrochemically and DNA-triggered cell release from ferrocene/β-cyclodextrin and aptamer modified dualfunctionalized graphene substrate

Abstract

Here we report a dual-functionalized electrochemical substrate to trigger cancer cells release based on the supramolecular interaction between β-cyclodextrin (β-CD) and Fc on clinical trial II aptamer AS1411 functionalized graphene platform. On one hand, the host-guest interaction can be reversible electrochemically controlled to realize cancer cells capture/release, and 1-adamantylamine binding can further amplify this surface change by competing interaction with β-CD. On the other hand, the AS1411 aptamer and its complementary DNA (cDNA) also can be used as a switchable anchor for cell adhesion. Our work gives an example for label-free, multi-functionalized triggered cell release based on aptamer and β-CD/graphene-modified surface and this multi-ways for cell catch-and-release on graphene modified surface also provides their potential biomedical application.

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References

  1. [1]

    Mendes, P. M. Stimuli-responsive surfaces for bio-applications. Chem. Soc. Rev. 2008, 37, 2512–2529.

    Article  Google Scholar 

  2. [2]

    Guillaume-Gentil, O.; Akiyama, Y.; Schuler, M.; Tang, C.; Textor, M.; Yamato, M.; Okano, T.; Voeroes, J. Polyelectrolyte coatings with a potential for electronic control and cell sheet engineering. Adv. Mater. 2008, 20, 560–565.

    Article  Google Scholar 

  3. [3]

    Richert, L.; Lavalle, P.; Vautier, D.; Senger, B.; Stoltz, J. F.; Schaaf, P.; Voegel, J. C.; Picart. C. Cell interactions with polyelectrolyte multilayer films. Biomacromolecules, 2002, 3, 1170–1178.

    Article  Google Scholar 

  4. [4]

    Zhao, C.; Song, Y.; Ren, J.; Qu, X. A DNA nanomachine induced by single-walled carbonnanotubes on gold surface. Biomaterials, 2009, 30, 1739–1745.

    Article  Google Scholar 

  5. [5]

    Guillaume-Gentil, O.; Semenov, O.; Roca, A.; Groth, T.; Zahn, R.; Vörös, J.; Zenobi-Wong, M. Engineering the extracellular environment: Strategies for building 2D and 3D cellular structures. Adv. Mater. 2010, 22, 5443–5462.

    Article  Google Scholar 

  6. [6]

    Luo, W.; Yousaf, M. N. Tissue morphing control on dynamic gradient surfaces. J. Am. Chem. Soc. 2011, 133, 10780–10783.

    Article  Google Scholar 

  7. [7]

    Inaba, R.; Khademhosseini, A.; Suzuki, H.; Fukuda, J. Electrochemical desorption of self-assembled monolayers for engineering cellular tissues. Biomaterials, 2009, 30, 3573–3579.

    Article  Google Scholar 

  8. [8]

    Chan, E. W. L.; Park, S.; Yousaf, M. N. An electroactive catalytic dynamic substrate that immobilizes and releases patterned ligands, proteins, and cells. Angew. Chem. Int. Ed. 2008, 47, 6267–6271.

    Article  Google Scholar 

  9. [9]

    Okano, T.; Yamaka, N.; Okuhara, M.; Sakai, H.; Sakurai, Y. Mechanism of cell detachment from temperature-modulated, hydrophilic-hydrophobic polymer surfaces. Biomaterials. 1995, 16, 297–303.

    Article  Google Scholar 

  10. [10]

    Shimizu, T.; Yamato, M.; Kikuchi, A.; Okano, T. Cell sheet engineering for myocardial tissue reconstruction. Biomaterials, 2003, 24, 2309–2316.

    Article  Google Scholar 

  11. [11]

    Kuralay, F.; Sattayasamitsathit, S.; Gao, W.; Uygun, A.; Katzenberg, A.; Wang, J. Self-propelled carbohydrate-sensitive microtransporters with built-in boronic acid recognition for isolating sugars and cells. J. Am. Chem. Soc. 2012, 134, 15217–15220.

    Article  Google Scholar 

  12. [12]

    Nakanishi, J.; Kikuchi, Y.; Takarada, T.; Nakayama, H.; Yamaguchi, K.; Maeda, M. Photoactivation of a substrate for cell adhesion under standard fluorescence microscopes. J. Am. Chem. Soc. 2004, 126, 16314–16315.

    Article  Google Scholar 

  13. [13]

    Wirkner, M.; Alonso, J. M.; Maus, V.; Salierno, M.; Lee, T. T.; García, A. J.; Campo, A. D. Triggered cell release from materials using bioadhesive photocleavable linkers. Adv. Mater. 2011, 23, 3907–3910.

    Article  Google Scholar 

  14. [14]

    Liu, D.; Xie, Y.; Shao, H.; Jiang, X. Using azobenzene-embedded self-assembled monolayers to photochemically control cell adhesion reversibly. Angew. Chem. Int. Ed. 2009, 48, 4406–4408.

    Article  Google Scholar 

  15. [15]

    Ng, C. C. A.; Magenau, A.; Ngalim, S. H.; Ciampi, S.; Chockalingham, M.; Harper, J. B.; Gaus, K.; Gooding, J. J. Using an electrical potential to reversibly switch surfaces between two states for dynamically controlling cell adhesion. Angew. Chem. Int. Ed. 2012, 51, 7706–7710.

    Article  Google Scholar 

  16. [16]

    Chen, L.; Liu, X.; Su, B.; Li, J.; Jiang, L.; Han, D.; Wang, S. Aptamer-mediated efficient capture and release of T lymphocytes on nanostructured surfaces. Adv. Mater. 2011, 23, 4376–4380.

    Article  Google Scholar 

  17. [17]

    Li, W.; Wang, J.; Ren, J.; Qu, X. Near-infrared- and pH-responsive system for reversible cell adhesion using graphene/gold nanorods functionalized with i-motif DNA. Angew. Chem. Int. Ed. 2013, 52, 6726–6730.

    Article  Google Scholar 

  18. [18]

    Liu, H.; Li, Y.; Sun, K.; Fan, J.; Zhang, P.; Meng, J.; Wang, S.; Jiang, L. Dual-responsive surfaces modified with phenylboronic acid-containing polymer brush to reversibly capture and release cancer cells. J. Am. Chem. Soc. 2013, 135, 7603–7609.

    Article  Google Scholar 

  19. [19]

    Yousaf, M. N.; Houseman, B. T.; Mrksich, M. Using electroactive substrates to pattern the attachment of two different cell populations. Proc Natl Acad Sci U.S.A. 2001, 98, 5992–5996.

    Article  Google Scholar 

  20. [20]

    Yousaf, M.; Houseman, B.; Mrksich, M. Turning on cell migration with electroactive substrates. Angew. Chem. Int. Ed. 2001, 40, 1093–1096.

    Article  Google Scholar 

  21. [21]

    Yoon, S-H.; Mofrad, M. R. K. Cell adhesion and detachment on gold surfaces modified with a thiol-functionalized RGD peptide. Biomaterials, 2011, 32, 7286–7296.

    Article  Google Scholar 

  22. [22]

    Seto, Y.; Inaba, R.; Okuyama, T.; Sassa, F.; Suzuki, H.; Fukuda, J. Engineering of capillary-like structures in tissue constructs by electrochemical detachment of cells. Biomaterials 2010, 31, 2209–2215.

    Article  Google Scholar 

  23. [23]

    Jiang, X. Y.; Ferrigno, R.; Mrksich, M.; Whitesides, G. M. Electrochemical desorption of self-assembled monolayers noninvasively releases patterned cells from geometrical confinements. J. Am. Chem. Soc. 2003, 125, 2366–2367.

    Article  Google Scholar 

  24. [24]

    Zhang, P.; Chen, L.; Xu, T.; Liu, H.; Liu, X.; Meng, J.; Yang, G.; Jiang, L.; Wang, S. Programmable fractal nanostructured interfaces for specific recognition and electrochemical release of cancer cells. Adv. Mater. 2013, 25, 3566–3570.

    Article  Google Scholar 

  25. [25]

    Chen, G. S.; Jiang, M. Cyclodextrin-based inclusion complexation bridging supramolecular chemistry and macromolecular self-assembly. Chem. Soc. Rev. 2011, 40, 2254–2266.

    Article  Google Scholar 

  26. [26]

    Rica, R.; Fratila, R. M.; Szarpak, A.; Huskens, J.; Velders, A. H. Multivalent nanoparticle networks as ultrasensitive enzyme sensors. Angew. Chem. Int. Ed. 2011, 50, 5703–5706.

    Google Scholar 

  27. [27]

    Dubacheva, G. V.; Galibert, M.; Coche-Guerente, L.; Dumy, P.; Boturyn, D.; Labbe’, P. Redox strategy for reversible attachment of biomolecules using bifunctional linkers. Chem. Commun. 2011, 47, 3565–3567.

    Article  Google Scholar 

  28. [28]

    Ihara, T.; Wasano, T.; Nakatake, R.; Arslan, P.; Futamura, A.; Jyo, A. Electrochemical signal modulation in homogeneous solutions using the formation of an inclusion complex between ferrocene and b-cyclodextrin on a DNA scaffold. Chem. Commun. 2011, 47, 12388–12390.

    Article  Google Scholar 

  29. [29]

    An, Q.; Brinkmann, J.; Huskens, J.; Krabbenborg, S.; Boer, J.; Jonkheijm, P. A Supramolecular system for the electrochemically controlled release of cells. Angew. Chem. Int. Ed. 2012, 51, 233–237.

    Google Scholar 

  30. [30]

    Péter, M.; Kooij, S.; Jenkins, T.; Roser, S.; Knoll, W.; Vancso, G. J. Electrochemically induced morphology and volume changes in surface-grafted poly(ferrocenyldimethylsilane). Langmuir 2004, 20, 891–897.

    Article  Google Scholar 

  31. [31]

    Dubacheva, G. V.; Heyden, A.; Dumy, P.; Kaftan, O.; Auzely-Velty, R.; Coche-Guerente, L.; Labbé, P. Electrochemically controlled adsorption of Fc-functionalized polymers on β-CD-modified self-assembled monolayers. Langmuir 2010, 26, 13976–13986.

    Article  Google Scholar 

  32. [32]

    Nijhuis, C. A.; Yu, F.; Knoll, W.; Huskens, J.; Reinhoudt, D. N. Multivalent dendrimers at molecular printboards: Influence of dendrimer structure on binding strength and stoichiometry and their electrochemically induced desorption. Langmuir 2005, 21, 7866–7876.

    Article  Google Scholar 

  33. [33]

    Chen, Y. F.; Banerjee, I.; Yu, L.; Djalali, R.; Matsui, H. Attachment of ferrocene nanotubes on β-cyclodextrin self-Assembled monolayers with molecular recognitions. Langmuir 2004, 20, 8409–8413.

    Article  Google Scholar 

  34. [34]

    Allen, M. J.; Tung, V. C.; Kaner, R. B. Honeycomb carbon: A review of graphene. Chem. Rev. 2010, 110, 132–145.

    Article  Google Scholar 

  35. [35]

    Mohanty, N.; Berry, V. Graphene-based single-bacterium resolution biodevice and DNA transistor: interfacing graphene derivatives with nanoscale and microscale biocomponents. Nano. Lett. 2008, 8, 4469–4476.

    Article  Google Scholar 

  36. [36]

    Ruiz, O. N.; Fernando, K. A. S.; Wang, B.; Brown, N. A.; Luo, P. G.; McNamara, N. D.; Vangsness, M.; Sun, Y. P.; Bunker. C. E. Graphene oxide: A nonspecific enhancer of cellular growth. ACS Nano, 2011, 5, 8100–8107.

    Article  Google Scholar 

  37. [37]

    Hess, L. H.; Jansen, M.; Maybeck, V.; Hauf, M. V.; Seifert, M.; Stutzmann, M.; Sharp, I. D.; Offenhäusser, A.; Garrido. J. A. Graphene transistor arrays for recording action potentials from electrogenic cells. Adv. Mater. 2011, 23, 5045–5049.

    Article  Google Scholar 

  38. [38]

    Park, S. Y.; Park, J.; Sim, S. H.; Sung, M. G.; Kim, K. S.; Hong, B. H.; Hong, S. Enhanced differentiation of human neural stem cells into neurons on graphene. Adv. Mater. 2011, 23, H263–H267

    Article  Google Scholar 

  39. [39]

    Chen, G. Y.; Pand, D. W.; Hwang, S. M.; Tuan, H. Y.; Hu, Y. C. A graphene-based platform for induced pluripotent stem cells culture and differentiation. Biomaterials, 2012, 33, 418–427.

    Article  Google Scholar 

  40. [40]

    Li, Y.; Liu, Y.; Fu, Y.; Wei, T.; Le Guyader, L.; Gao, G.; Liu, R. S.; Chang, Y. Z.; Chen, C. The triggering of apoptosis in macrophages by pristine graphene through the MAPK and TGF-beta signaling pathways. Biomaterials, 2012, 33, 402–411

    Article  Google Scholar 

  41. [41]

    Feng, L.; Chen, Y.; Ren, J.; Qu, X. A graphene functionalized electrochemical aptasensor for selective label-free detection of cancer cells. Biomaterials, 2011, 32, 2930–2937.

    Article  Google Scholar 

  42. [42]

    Hsiao, S. C.; Crow, A. K.; Lam, W. A.; Bertozzi, C. R.; Fletcher, D. A.; Francis, M. B. DNA-coating AFM cantilevers for the investigation of cell adhesion and the patterning of live cells. Angew. Chem. Int. Ed. 2008, 47, 8473–8477.

    Article  Google Scholar 

  43. [43]

    Bailey, R. C.; Kwong, G. A.; Radu, C. G.; Witte, O. N.; Heath, J. R. DNA-encoded antibody libraries: A unified platform for multiplexed cell sorting and detection of genes and proteins. J. Am. Chem. Soc. 2007, 129, 1959–1967

    Article  Google Scholar 

  44. [44]

    Kwong, G. A.; Radu, C. G.; Hwang, K.; Shu, C. J.; Ma, C.; Koya, R. C.; Comin-Auduix, B.; Hadrup, S. R.; Bailey, R. C.; Witte, O. N.; et al. Modular nucleic acid assembled p/MHC microarrays for multiplexed sorting of antigen-specific T cells. J. Am. Chem. Soc. 2009, 131, 9695–9703.

    Article  Google Scholar 

  45. [45]

    Twite, A. A.; Hsiao, S. C.; Onoe, H.; Mathies, R. A.; Francis, M. B. Direct attachment of microbial organism to material surfaces through sequence-specific DNA hybridization. Adv. Mater. 2012, 24, 2380–2385.

    Article  Google Scholar 

  46. [46]

    Shangguan, D.; Li, Y.; Tang, Z.; Cao, Z. C.; Chen, H. W.; Mallikaratchy, P.; Sefah, K.; Yang, C. J.; Tan, W. Aptamer evolved from live cells as effective molecular probes for cancer study. PNAS 2006, 103, 11838–11843.

    Article  Google Scholar 

  47. [47]

    Chen, L.; Liu, X.; Su, B.; Li, J.; Jiang, L.; Han, D.; Wang, S. Aptamer-mediated efficient capture and release of T lymphocytes on nanostructured surfaces. Adv. Mater. 2011, 23, 4 4376–4380.

    Google Scholar 

  48. [48]

    Shen, Q.; Xu, L.; Zhao, L.; Wu, D.; Fan, Y.; Zhou, Y.; Ouyang, W.; Xu, X.; Zhang, Z.; Song, M.; et al. Specific capture and release of circulating tumor cells using aptamermodified nanosubstrates. Adv. Mater. 2013, 25, 2368–2373.

    Article  Google Scholar 

  49. [49]

    Bates, P. J.; Kahlon, J. B.; Thomas, S. D.; Trent, J. O.; Miller, D. M. Antiproliferative activity of G-rich oligonucleotides correlates with protein binding. J. Biol. Chem. 1999, 274, 26369–26377.

    Article  Google Scholar 

  50. [50]

    Müller, V.; Abdomerović, V.; Marrington, R.; Peberdy, J.; Rodger, A.; Trent, J. O.; Bates, P. Biophysical and biological properties of quadruplex oligodeoxyribonucleotides. Nucleic. Acids. Res. 2003, 31, 2097–2107.

    Article  Google Scholar 

  51. [51]

    Soundararajan, S.; Wang, L.; Sridharan, V.; Chen, W.; Courtenay-Luck, N.; Jones, D.; Spicer, E.; Fernandes, D. J. Plasma membrane nucleolin is a receptor for the anticancer aptamer AS1411 in MV4-11 leukemia cells. Mol. Pharmacol. 2009, 76, 984–991.

    Article  Google Scholar 

  52. [52]

    Cao, Z.; Tong, R.; Mishra, A.; Xu, W.; Wong, G. C. L.; Cheng, J.; Lu, Y. Reversible cell-specific drug delivery with aptamer-functionalized liposomes. Angew. Chem. Int. Ed. 2009, 48, 6494–6498.

    Article  Google Scholar 

  53. [53]

    Dubacheva, G. V.; Galibert, M.; Coche-Guerente, L.; Dumy, P.; Boturyn, D.; Labbe’, P. Redox strategy for reversible attachment of biomolecules using bifunctional linkers. Chem. Commun. 2011, 47, 3565–3567.

    Article  Google Scholar 

  54. [54]

    Peng, Y.; Wang, X.; Xiao, Y.; Feng, L.; Zhao, C.; Ren, J.; Qu, X. i-Motif quadruplex DNA-based biosensor for distinguishing single- and multiwalled carbon nanotubes. J. Am. Chem. Soc. 2009, 131, 13813–13818.

    Article  Google Scholar 

  55. [55]

    Feng, L.; Li, X.; Peng, Y.; Geng, J.; Ren, J.; Qu, X. Spectral and electrochemical detection of protonated triplex formation by a small-molecule anticancer agent. Chem. Phys. Lett. 2009, 480, 309–312.

    Article  Google Scholar 

  56. [56]

    Feng, L. Y.; Wu, L.; Wang, J. S.; Ren, J. S.; Miyoshi, D.; Sugimoto, N.; Qu, X. G. Detection of a prognostic indicator in early-stage cancer using functionalized graphene-based peptide sensor. Adv. Mater. 2012, 24, 125–131.

    Article  Google Scholar 

  57. [57]

    Guo, Y.; Guo, S.; Ren, J.; Zhai, Y.; Dong, S.; Wang, E. Cyclodextrin functionalized graphene nanosheets with high supramolecular recognition capability: Synthesis and host-guest inclusion for enhanced electrochemical performance. ACS Nano 2010, 4, 4001–4010.

    Article  Google Scholar 

  58. [58]

    Li, D.; Dapić, M. B.; Gilje, S.; Kaner, R. B.; Wallace, G. G. Processable aqueous dispersions of graphene nanosheets. Nat. Nanotech. 2008, 3, 101–105.

    Article  Google Scholar 

  59. [59]

    Feng, L.; Wu, L.; Qu, X. New horizons for diagnostics and therapeutic applications of graphene and graphene oxide. Adv. Mater. 2013, 25, 168–186

    Article  Google Scholar 

  60. [60]

    Wang, J.; Musameh, M.; Lin, Y. H. Solubilization of carbon nanotubes by nafion toward the preparation of amperometric biosensors. J. Am. Chem. Soc. 2003, 125, 2408–2409.

    Article  Google Scholar 

  61. [61]

    Morra, S.; Valetti, F.; Sadeghi, S. J.; King, P. W.; Meyerc, T.; Gilardi, G Direct electrochemistry of an [FeFe]-hydrogenase on a TiO2 Electrode. Chem. Commun. 2011, 47, 10566–10568.

    Article  Google Scholar 

  62. [62]

    Radi, A. E.; Sanchez, J. L. A.; Baldrich, E.; O’sullivan, C. K. Reagentless, reusable, ultrasensitive electrochemical molecular beacon aptasensor. J. Am. Chem. Soc. 2006, 128, 117–124.

    Article  Google Scholar 

  63. [63]

    Park, I. K.; Recum, H. A.; Jiang, S.; Pun, S, H. Supramolecular assembly of cyclodextrin-based nanoparticles on solid surfaces for gene delivery. Langmuir, 2006, 22, 8478–8484.

    Article  Google Scholar 

  64. [64]

    Li, Y. F.; Breaker, R. R. Deoxyribozymes: New players in the ancient game biocatalysis. Curr. Opin. Chem. Biol. 1999, 9, 315–323.

    Google Scholar 

  65. [65]

    Song, Y.; Zhao, C.; Ren, J.; Qu, X. Rapid and ultra-sensitive detection of AMP using a fluorescent and magnetic nano-silica sandwich complex. Chem. Commun. 2009, 45, 1975–1977.

    Article  Google Scholar 

  66. [66]

    K’Owino, I. O.; Sadik, O. A. Impedance spectroscopy: A powerful tool for rapid biomolecular screening and cell culture monitoring. Electroanalysis 2005, 17, 2101–2113.

    Article  Google Scholar 

  67. [67]

    Kurkina, T.; Vlandas, A.; Ahmand, A.; Kern, K.; Balasubramanian, K. Label-free detection of few copies of DNA with carbon nanotube impedance biosensors. Angew. Chem. Int. Ed. 2011, 50, 3710–3714.

    Article  Google Scholar 

  68. [68]

    Bagnaninchi, P. O.; Drummond, N. Real-time label-free monitoring of adipose-derived stem cell differentiation with electric cell-substrate impedance sensing. Proc Natl Acad Sci U.S.A. 2011, 108, 6462–6467.

    Article  Google Scholar 

  69. [69]

    Hummers, W. S.; Offeman, R. E. Preparation of graphitic oxide. J. Am. Chem. Soc. 1958, 80, 1339–1339.

    Article  Google Scholar 

  70. [70]

    Zhang, Y. L.; Huang, Y.; Jiang, J. H.; Shen, G. L.; Yu, R. Q. Electrochemical aptasensor based on proximity-dependent surface hybridization assay for single-step, reusable, sensitive protein detection. J. Am. Chem. Soc. 2007, 129, 15448–15449.

    Article  Google Scholar 

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Feng, L., Li, W., Ren, J. et al. Electrochemically and DNA-triggered cell release from ferrocene/β-cyclodextrin and aptamer modified dualfunctionalized graphene substrate. Nano Res. 8, 887–899 (2015). https://doi.org/10.1007/s12274-014-0570-4

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Keywords

  • cell release
  • ferrocene/β-cyclodextrin
  • AS1411
  • graphene