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Graphene oxide as a photocatalytic nuclease mimicking nanozyme for DNA cleavage

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Abstract

Developing nanomaterial-based enzyme mimics for DNA cleavage is an interesting challenge and it has many potential applications. Single-layered graphene oxide (GO) is an excellent platform for DNA adsorption. In addition, GO has been employed for photosensitized generation of reactive oxygen species (ROS). Herein, we demonstrate that GO sheets could cleave DNA as a nuclease mimicking nanozyme in the presence of UV or blue light. For various DNA sequences and lengths, well-defined product bands were observed along with photobleaching of the fluorophore label on the DNA. Different from previously reported GO cleavage of DNA, our method did not require metal ions such as Cu2+. Fluorescence spectroscopy suggested a high adsorption affinity between GO and DNA. For comparison, although zero-dimensional fluorescent carbon dots (C-dots) had higher photosensitivity in terms of producing ROS, their cleavage activity was much lower and only smeared cleavage products were observed, indicating that the ROS acted on the DNA in solution. Based on the results, GO behaved like a classic heterogeneous catalyst following substrate adsorption, reaction, and product desorption steps. This simple strategy may help in the design of new nanozymes by introducing light.

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References

  1. Loenen, W. A. M.; Dryden, D. T. F.; Raleigh, E. A.; Wilson, G. G.; Murray, N. E. Highlights of the DNA cutters: A short history of the restriction enzymes. Nucleic Acids Res.2013, 42, 3–19.

    Google Scholar 

  2. Lin, Y. H.; Xu, C.; Ren, J. S.; Qu, X. G. Using thermally regenerable cerium oxide nanoparticles in biocomputing to perform label-free, resettable, and colorimetric logic operations. Angew. Chem., Int. Ed.2012, 51, 12579–12583.

    CAS  Google Scholar 

  3. Cong, L.; Ran, F. A.; Cox, D.; Lin, S. L.; Barretto, R.; Habib, N.; Hsu, P. D.; Wu, X. B.; Jiang, W. Y.; Marraffini, L. A. et al. Multiplex genome engineering using CRISPR/Cas systems. Science2013, 339, 819–823.

    CAS  Google Scholar 

  4. Kameshima, W.; Ishizuka, T.; Minoshima, M.; Yamamoto, M.; Sugiyama, H.; Xu, Y.; Komiyama, M. Conjugation of peptide nucleic acid with a pyrrole/imidazole polyamide to specifically recognize and cleave DNA. Angew. Chem., Int. Ed.2013, 52, 13681–13684.

    CAS  Google Scholar 

  5. Moser, H. E.; Dervan, P. B. Sequence-specific cleavage of double helical DNA by triple helix formation. Science1987, 238, 645–650.

    CAS  Google Scholar 

  6. Chen, C. H.; Sigman, D. S. Nuclease activity of 1,10-phenanthrolinecopper: Sequence-specific targeting. Proc. Natl. Acad. Sci. USA1986, 83, 7147–7151.

    CAS  Google Scholar 

  7. François, J. C.; Saison-Behmoaras, T.; Barbier, C.; Chassignol, M.; Thuong, N. T.; Hélène, C. Sequence-specific recognition and cleavage of duplex DNA via triple-helix formation by oligonucleotides covalently linked to a phenanthroline-copper chelate. Proc. Natl. Acad. Sci. USA1989, 86, 9702–9706.

    Google Scholar 

  8. Carmi, N.; Balkhi, S. R.; Breaker, R. R. Cleaving DNA with DNA. Proc. Natl. Acad. Sci. USA1998, 95, 2233–2237.

    CAS  Google Scholar 

  9. Aiba, Y.; Sumaoka, J.; Komiyama, M. Artificial DNA cutters for DNA manipulation and genome engineering. Chem. Soc. Rev.2011, 40, 5657–5668.

    CAS  Google Scholar 

  10. Kitamura, Y.; Komiyama, M. Preferential hydrolysis of gap and bulge sites in DNA by Ce(IV)/EDTA complex. Nucleic Acids Res.2002, 30, e102.

    Google Scholar 

  11. Chen, W.; Kitamura, Y.; Zhou, J. M.; Sumaoka, J.; Komiyama, M. Site-selective DNA hydrolysis by combining Ce(IV)/EDTA with monophosphate-bearing oligonucleotides and enzymatic ligation of the scission fragments. J. Am. Chem. Soc.2004, 126, 10285–10291.

    CAS  Google Scholar 

  12. Gu, H. Z.; Furukawa, K.; Weinberg, Z.; Berenson, D. F.; Breaker, R. R. Small, highly active DNAs that hydrolyze DNA. J. Am. Chem. Soc.2013, 135, 9121–9129.

    CAS  Google Scholar 

  13. Kim, Y. G.; Cha, J.; Chandrasegaran, S. Hybrid restriction enzymes: Zinc finger fusions to Fok I cleavage domain. Proc. Natl. Acad. Sci. USA1996, 93, 1156–1160.

    CAS  Google Scholar 

  14. Urnov, F. D.; Rebar, E. J.; Holmes, M. C.; Zhang, H. S.; Gregory, P. D. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet.2010, 11, 636–646.

    CAS  Google Scholar 

  15. Porteus, M. H.; Carroll, D. Gene targeting using zinc finger nucleases. Nat. Biotechnol.2005, 23, 967–973.

    CAS  Google Scholar 

  16. Cassandri, M.; Smirnov, A.; Novelli, F.; Pitolli, C.; Agostini, M.; Malewicz, M.; Melino, G.; Raschellà, G. Zinc-finger proteins in health and disease. Cell Death Discov.2017, 3, 17071.

    Google Scholar 

  17. Wei, H.; Wang, E. K. Nanomaterials with enzyme-like characteristics (nanozymes): Next-generation artificial enzymes. Chem. Soc. Rev.2013, 42, 6060–6093.

    CAS  Google Scholar 

  18. Wu, J. J. X.; Wang, X. Y.; Wang, Q.; Lou, Z. P.; Li, S. R.; Zhu, Y. Y.; Qin, L.; Wei, H. Nanomaterials with enzyme-like characteristics (nanozymes): Next-generation artificial enzymes (II). Chem. Soc. Rev.2019, 48, 1004–1076.

    CAS  Google Scholar 

  19. Huang, Y. Y.; Ren, J. S.; Qu, X. G. Nanozymes: Classification, catalytic mechanisms, activity regulation, and applications. Chem. Rev.2019, 119, 4357–4412.

    CAS  Google Scholar 

  20. Sun, M. Z.; Xu, L. G.; Qu, A. H.; Zhao, P.; Hao, T. T.; Ma, W.; Hao, C. L.; Wen, X. D.; Colombari, F. M.; de Moura, A. F. et al. Site-selective photoinduced cleavage and profiling of DNA by chiral semiconductor nanoparticles. Nat. Chem.2018, 10, 821–830.

    CAS  Google Scholar 

  21. Xu, F.; Lu, Q. W.; Huang, P. J. J.; Liu, J. W. Nanoceria as a DNase I mimicking nanozyme. Chem. Commun.2019, 55, 13215–13218.

    CAS  Google Scholar 

  22. Lu, C. H.; Yang, H. H.; Zhu, C. L.; Chen, X.; Chen, G. N. A graphene platform for sensing biomolecules. Angew. Chem., Int. Ed.2009, 48, 4785–4787.

    CAS  Google Scholar 

  23. He, S. J.; Song, B.; Li, D.; Zhu, C. F.; Qi, W. P.; Wen, Y. Q.; Wang, L. H.; Song, S. P.; Fang, H. P.; Fan, C. H. A graphene nanoprobe for rapid, sensitive, and multicolor fluorescent DNA analysis. Adv. Funct. Mater.2010, 20, 453–459.

    CAS  Google Scholar 

  24. Guo, Y. J.; Deng, L.; Li, J.; Guo, S. J.; Wang, E. K.; Dong, S. J. Hemin–graphene hybrid nanosheets with intrinsic peroxidase-like activity for label-free colorimetric detection of single-nucleotide polymorphism. ACS Nano2011, 5, 1282–1290.

    CAS  Google Scholar 

  25. Liu, B. W.; Sun, Z. Y.; Zhang, X.; Liu, J. W. Mechanisms of DNA sensing on graphene oxide. Anal. Chem.2013, 85, 7987–7993.

    CAS  Google Scholar 

  26. Ren, H. L.; Wang, C.; Zhang, J. L.; Zhou, X. J.; Xu, D. F.; Zheng, J.; Guo, S. W.; Zhang, J. Y. DNA cleavage system of nanosized graphene oxide sheets and copper ions. ACS Nano2010, 4, 7169–7174.

    CAS  Google Scholar 

  27. Kalluru, P.; Vankayala, R.; Chiang, C. S.; Hwang, K. C. Nano-graphene oxide-mediated in vivo fluorescence imaging and bimodal photodynamic and photothermal destruction of tumors. Biomaterials2016, 95, 1–10.

    CAS  Google Scholar 

  28. Xie, X. Z.; Mao, C. Y.; Liu, X. M.; Zhang, Y. Z.; Cui, Z. D.; Yang, X. J.; Yeung, K. W. K.; Pan, H. B.; Chu, P. K.; Wu, S. L. Synergistic bacteria killing through photodynamic and physical actions of graphene oxide/Ag/collagen coating. ACS Appl. Mater. Interfaces2017, 9, 26417–26428.

    CAS  Google Scholar 

  29. Li, C. B.; Xu, Q.; Xu, S. X.; Zhang, X. F.; Hou, X. D.; Wu, P. Synergy of adsorption and photosensitization of graphene oxide for improved removal of organic pollutants. RSC Adv.2017, 7, 16204–16209.

    CAS  Google Scholar 

  30. Jones, M. R.; Seeman, N. C.; Mirkin, C. A. Programmable materials and the nature of the DNA bond. Science2015, 347, 1260901.

    Google Scholar 

  31. Tan, L. H.; Xing, H.; Lu, Y. DNA as a powerful tool for morphology control, spatial positioning, and dynamic assembly of nanoparticles. Acc. Chem. Res.2014, 47, 1881–1890.

    CAS  Google Scholar 

  32. Hu, Q. Q.; Li, H.; Wang, L. H.; Gu, H. Z.; Fan, C. H. DNA nanotechnology-enabled drug delivery systems. Chem. Rev.2019, 119, 6459–6506.

    CAS  Google Scholar 

  33. Li, J.; Mo, L. T.; Lu, C. H.; Fu, T.; Yang, H. H.; Tan, W. H. Functional nucleic acid-based hydrogels for bioanalytical and biomedical applications. Chem. Soc. Rev.2016, 45, 1410–1431.

    CAS  Google Scholar 

  34. Liu, B. W.; Liu, J. W. Interface-driven hybrid materials based on DNA-functionalized gold nanoparticles. Matter2019, 1, 825–847.

    Google Scholar 

  35. Zhu, S. J.; Meng, Q. N.; Wang, L.; Zhang, J. H.; Song, Y. B.; Jin, H.; Zhang, K.; Sun, H. C.; Wang, H. Y.; Yang, B. Highly photoluminescent carbon dots for multicolor patterning, sensors, and bioimaging. Angew. Chem., Int. Ed.2013, 52, 3953–3957.

    CAS  Google Scholar 

  36. Zhang, J. Y.; Lu, X. M.; Tang, D. D.; Wu, S. H.; Hou, X. D.; Liu, J. W.; Wu, P. Phosphorescent carbon dots for highly efficient oxygen photosensitization and as photo-oxidative nanozymes. ACS Appl. Mater. Interfaces2018, 10, 40808–40814.

    CAS  Google Scholar 

  37. Boyce, R. P.; Howard-Flanders, P. Release of ultraviolet light-induced thymine dimers from DNA in E. coli K-12. Proc. Natl. Acad. Sci. USA1964, 51, 293–300.

    CAS  Google Scholar 

  38. Bilski, P.; Reszka, K.; Bilska, M.; Chignell, C. F. Oxidation of the spin trap 5,5-dimethyl-1-pyrroline N-oxide by singlet oxygen in aqueous solution. J. Am. Chem. Soc.1996, 118, 1330–1338.

    CAS  Google Scholar 

  39. Long, R.; Huang, H.; Li, Y. P.; Song, L.; Xiong, Y. J. Palladium-based nanomaterials: A platform to produce reactive oxygen species for catalyzing oxidation reactions. Adv. Mater.2015, 27, 7025–7042.

    CAS  Google Scholar 

  40. Wang, H.; Jiang, S. L.; Chen, S. C.; Li, D. D.; Zhang, X. D.; Shao, W.; Sun, X. S.; Xie, J. F.; Zhao, Z.; Zhang, Q. et al. Enhanced singlet oxygen generation in oxidized graphitic carbon nitride for organic synthesis. Adv. Mater.2016, 28, 6940–6945.

    CAS  Google Scholar 

  41. Zheng, Y.; Yu, Z. H.; Ou, H. H.; Asiri, A. M.; Chen, Y. L.; Wang, X. C. Black phosphorus and polymeric carbon nitride heterostructure for photoinduced molecular oxygen activation. Adv. Funct. Mater.2018, 28, 1705407.

    Google Scholar 

  42. Zhang, J. Y.; Wu, S. H.; Lu, X. M.; Wu, P.; Liu, J. W. Lanthanideboosted singlet oxygen from diverse photosensitizers along with potent photocatalytic oxidation. ACS Nano2019, 13, 14152–14161.

    CAS  Google Scholar 

  43. Loh, K. P.; Bao, Q. L.; Eda, G.; Chhowalla, M. Graphene oxide as a chemically tunable platform for optical applications. Nat. Chem.2010, 2, 1015–1024.

    CAS  Google Scholar 

  44. Li, X.; Peng, Y. H.; Ren, J. S.; Qu, X. G. Carboxyl-modified singlewalled carbon nanotubes selectively induce human telomeric i-motif formation. Proc. Natl. Acad. Sci. USA2006, 103, 19658–19663.

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  46. Chen, X.; Zhou, X. J.; Han, T.; Wu, J. Y.; Zhang, J. Y.; Guo, S. W. Stabilization and induction of oligonucleotide i-motif structure via graphene quantum dots. ACS Nano2013, 7, 531–537.

    CAS  Google Scholar 

  47. Liu, B. W.; Salgado, S.; Maheshwari, V.; Liu, J. W. DNA adsorbed on graphene and graphene oxide: Fundamental interactions, desorption and applications. Curr. Opin. Colloid Interface Sci.2016, 26, 41–49.

    CAS  Google Scholar 

  48. Huang, P. J. J.; Kempaiah, R.; Liu, J. W. Synergistic pH effect for reversible shuttling aptamer-based biosensors between graphene oxide and target molecules. J. Mater. Chem.2011, 21, 8991–8993.

    CAS  Google Scholar 

  49. Lu, C.; Liu, Y. B.; Ying, Y. B.; Liu, J. W. Comparison of MoS2, WS2, and graphene oxide for DNA adsorption and sensing. Langmuir2017, 33, 630–637.

    Google Scholar 

  50. Zhang, J. Y.; Wu, S. H.; Lu, X. M.; Wu, P.; Liu, J. W. Manganese as a catalytic mediator for photo-oxidation and breaking the pH limitation of nanozymes. Nano Lett.2019, 19, 3214–3220.

    CAS  Google Scholar 

  51. Ge, J. C.; Lan, M. H.; Zhou, B. J.; Liu, W. M.; Guo, L.; Wang, H.; Jia, Q. Y.; Niu, G. L.; Huang, X.; Zhou, H. Y. et al. A graphene quantum dot photodynamic therapy agent with high singlet oxygen generation. Nat. Commun.2014, 5, 4596.

    CAS  Google Scholar 

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Acknowledgements

Funding for this work was from the Natural Sciences and Engineering Research Council of Canada (NSERC), and the National Natural Science Foundation of China (No. U19A2005).

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Correspondence to Peng Wu or Juewen Liu.

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Zhang, J., Wu, S., Ma, L. et al. Graphene oxide as a photocatalytic nuclease mimicking nanozyme for DNA cleavage. Nano Res. 13, 455–460 (2020). https://doi.org/10.1007/s12274-020-2629-8

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