Skip to main content
SpringerLink
Log in

How G-quadruplex topology and loop sequences affect optical properties of DNA-templated silver nanoclusters

  • Research Article
  • Published:
Nano Research Aims and scope Submit manuscript

Abstract

In the study of the fabrication of DNA-templated silver nanoclusters (DNA-Ag NCs), how templates affect the fluorescence of the nanoclusters remains unclear, and it has been a challenge to understand the correlation between the properties of the DNA template and the Ag NCs. In this respect, based on the rational design of a series of structurally defined intramolecular G-quadruplexes, we prepared G-quadruplex-templated Ag NCs with a defined G-tetrad-to-silver ratio of 1:2. We evaluated the effect of G-quadruplex topology and loop sequences on the fluorescence of DNA-Ag NCs using circular dichroism, and extinction and emission spectroscopy. G-quadruplex templates with an anti-parallel topology were found to produce Ag NCs with stronger fluorescence compared with parallel and hybrid configurations. Loop bases adjacent to G-tetrads have a more significant impact on the fluorescence of Ag NCs compared with those in the middle of the loop, with adenine largely exhibiting an enhancement effect and thymine being detrimental. Generally, G-quadruplexes having an anti-parallel topology with adenine in the loop adjacent to the G-tetrad would be good templates for producing highly fluorescent Ag NCs. This is the first study to focus on the correlation between G-quadruplex topology/sequence and the optical properties of Ag NCs. We hope that the results of this study will facilitate a more in-depth understanding of correlation between G-quadruplex templates and Ag NCs, and help to understand and utilize their unique attributes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Zheng, J.; Nicovich, P. R.; Dickson, R. M. Highly fluorescent noble-metal quantum dots. Annu. Rev. Phys. Chem. 2007, 58, 409–431.

    Article  Google Scholar 

  2. Díez, I.; Ras, R. H. A. Fluorescent silver nanoclusters. Nanoscale 2011, 3, 1963–1970.

    Article  Google Scholar 

  3. Shang, L.; Dong, S. J.; Nienhaus, G. U. Ultra-small fluorescent metal nanoclusters: Synthesis and biological applications. Nanotoday 2011, 6, 401–418.

    Article  Google Scholar 

  4. Qian, H. F.; Zhu, M. Z.; Wu, Z. K.; Jin, R. C. Quantum sized gold nanoclusters with atomic precision. Acc. Chem. Res. 2012, 45, 1470–1479.

    Article  Google Scholar 

  5. Obliosca, J. M.; Liu, C.; Yeh, H. C. Fluorescent silver nanoclusters as DNA probes. Nanoscale 2013, 5, 8443–8461.

    Article  Google Scholar 

  6. Vosch, T.; Antoku, Y.; Hsiang, J. C.; Richards, C. I.; Gonzalez, J. I.; Dickson, R. M. Strongly emissive individual DNA-encapsulated Ag nanoclusters as single-molecule fluorophores. Proc. Natl. Acad. Sci. USA 2007, 104, 12616–12621.

    Article  Google Scholar 

  7. Gwinn, E. G.; O’Neill, P.; Guerrero, A. J.; Bouwmeester, D.; Fygenson, D. K. Sequence-dependent fluorescence of DNA-hosted silver nanoclusters. Adv. Mater. 2008, 20, 279–283.

    Article  Google Scholar 

  8. Richards, C. I.; Choi, S.; Hsiang, J.C.; Antoku, Y.; Vosch, T.; Bongiorno, A.; Tzeng, Y. L.; Dickson, R. M. Oligonucleotidestabilized Ag nanocluster fluorophores. J. Am. Chem. Soc. 2008, 130, 5038–5039.

    Article  Google Scholar 

  9. Guo, W. W.; Yuan, J. P.; Dong, Q. Z.; Wang, E. K. Highly sequence-dependent formation of fluorescent silver nanoclusters in hybridized DNA duplexes for single nucleotide mutation identification. J. Am. Chem. Soc. 2010, 132, 932–934.

    Article  Google Scholar 

  10. Lan, G. Y.; Huang, C. C.; Chang, H. T. Silver nanoclusters as fluorescent probes for selective and sensitive detection of copper ions. Chem. Commun. 2010, 46, 1257–1259.

    Article  Google Scholar 

  11. Yeh, H. C.; Sharma, J.; Han, J. J.; Martinez, J. S.; Werner, J. H. A DNA-silver nanocluster probe that fluoresces upon hybridization. Nano Lett. 2010, 10, 3106–3110.

    Article  Google Scholar 

  12. Li, T.; Zhang, L. B.; Ai, J.; Dong, S. J.; Wang, E. K. Iontuned DNA/Ag fluorescent nanoclusters as versatile logic device. Acs Nano 2011, 5, 6334–6338.

    Article  Google Scholar 

  13. Li, J. J.; Zhong, X. Q.; Zhang, H. Q.; Le, X. C.; Zhu, J. J. Binding-induced fluorescence turn-on assay using aptamerfunctionalized silver nanocluster DNA probes. Anal. Chem. 2012, 84, 5170–5174.

    Article  Google Scholar 

  14. Liu, X. Q.; Wang, F.; Aizen, R.; Yehezkeli, O.; Willner, I. Graphene oxide/nucleic-acid-stabilized silver nanoclusters: Functional hybrid materials for optical aptamer sensing and multiplexed analysis of pathogenic DNAs. J. Am. Chem. Soc. 2013, 135, 11832–11839.

    Article  Google Scholar 

  15. Liu, J. W. DNA-stabilized, fluorescent, metal nanoclusters for biosensor development. TrACTrend. Anal. Chem. 2014, 58, 99–111.

    Article  Google Scholar 

  16. Gwinn, E.; Schultz, D.; Copp, S. M.; Swasey, S. DNAprotected silver clusters for nanophotonics. Nanomaterials 2015, 5, 180–207.

    Article  Google Scholar 

  17. Shao, C. Y.; Yuan, B.; Wang, H. Q.; Zhou, Q.; Li, Y. L.; Guan, Y. F.; Deng, Z. X. Eggshell membrane as a multimodal solid state platform for generating fluorescent metal nanoclusters. J. Mater. Chem. 2011, 21, 2863–2866.

    Article  Google Scholar 

  18. Copp, S. M.; Bogdanov, P.; Debord, M.; Singh, A.; Gwinn, E. Base motif recognition and design of DNA templates for fluorescent silver clusters by machine learning. Adv. Mater. 2014, 26, 5839–5845.

    Article  Google Scholar 

  19. Copp, S. M.; Schultz, D.; Swasey, S.; Pavlovich, J.; Debord, M.; Chiu, A.; Olsson, K.; Gwinn, E. Magic numbers in DNA-stabilized fluorescent silver clusters lead to magic colors. J. Phys. Chem. Lett. 2014, 5, 959–963.

    Article  Google Scholar 

  20. Petty, J. T.; Zheng, J.; Hud, N. V.; Dickson, R. M. DNAtemplated Ag nanocluster formation. J. Am. Chem. Soc. 2004, 126, 5207–5212.

    Article  Google Scholar 

  21. Ritchie, C. M.; Johnsen, K. R.; Kiser, J. R.; Antoku, Y.; Dickson, R. M.; Petty, J. T. Ag nanocluster formation using a cytosine oligonucleotide template. J. Phys. Chem. C 2007, 111, 175–181.

    Article  Google Scholar 

  22. Sengupta, B.; Springer, K.; Buckman, J. G.; Story, S. P.; Abe, O. H.; Hasan, Z. W.; Prudowsky, Z. D.; Rudisill, S. E.; Degtyareva, N. N.; Petty, J. T. DNA templates for fluorescent silver clusters and I-motif folding. J. Phys. Chem. C 2009, 113, 19518–19524.

    Article  Google Scholar 

  23. Ai, J.; Guo, W. W.; Li, B. L.; Li, T.; Li, D.; Wang, E. K. DNA G-quadruplex-templated formation of the fluorescent silver nanocluster and its application to bioimaging. Talanta 2012, 88, 450–455.

    Article  Google Scholar 

  24. Neidig, M. L.; Sharma, J.; Yeh, H. C.; Martinez, J. S.; Conradson, S. D.; Shreve, A. P. Ag K-Edge EXAFS analysis of DNA-templated fluorescent silver nanoclusters: Insight into the structural origins of emission tuning by DNA sequence variations. J. Am. Chem. Soc. 2011, 133, 11837–11839.

    Article  Google Scholar 

  25. Petty, J. T.; Sergev, O. O.; Ganguly, M.; Rankine, I. J.; Chevrier, D. M.; Zhang, P. A segregated, partially oxidized, and compact Ag10 cluster within an encapsulating DNA host. J. Am. Chem. Soc. 2016, 138, 3469–3477.

    Article  Google Scholar 

  26. Schultz, D.; Gwinn, E. G. Silver atom and strand numbers in fluorescent and dark Ag:DNAs. Chem. Commun. 2012, 48, 5748–5750.

    Article  Google Scholar 

  27. Schultz, D.; Gardner, K.; Oemrawsingh, S. S. R.; Markešević, N.; Olsson, K.; Debord, M.; Bouwmeester, D.; Gwinn, E. Evidence for rod-shaped DNA-stabilized silver nanocluster emitters. Adv. Mater. 2013, 25, 2797–2803.

    Article  Google Scholar 

  28. O’Neill,P. R.; Velazquez, L. R.; Dunn, D. G.; Gwinn, E. G.; Fygenson, D. K. Hairpins with poly-C loops stabilize four types of fluorescent Agn:DNA. J. Phys. Chem. C 2009, 113, 4229–4233.

    Article  Google Scholar 

  29. Morishita, K.; MacLean, J. L.; Liu, B. W.; Jiang, H.; Liu, J. W. Correlation of photobleaching, oxidation and metal induced fluorescence quenching of DNA-templated silver nanoclusters. Nanoscale 2013, 5, 2840–2849.

    Article  Google Scholar 

  30. Li, J.; Jia, X. F.; Li, D. Y.; Ren, J. T.; Han, Y. C.; Xia, Y.; Wang, E. K. Stem-directed growth of highly fluorescent silver nanoclusters for versatile logic devices. Nanoscale 2013, 5, 6131–6138.

    Article  Google Scholar 

  31. Lan, G. Y.; Chen, W. Y.; Chang, H. T. Control of synthesis and optical properties of DNA templated silver nanoclusters by varying DNA length and sequence. RSC Adv. 2011, 1, 802–807.

    Article  Google Scholar 

  32. Feng, L. Y.; Huang, Z. Z.; Ren, J. S.; Qu, X. G. Toward sitespecific, homogeneous and highly stable fluorescent silver nanoclusters fabrication on triplex DNA scaffolds. Nucleic Acids. Res. 2012, 40, e122.

    Article  Google Scholar 

  33. Weadick, D. S.; Liu, J. W. Phosphorothioate DNA stabilized fluorescent gold and silver nanoclusters. Nanomaterials 2015, 5, 804–813.

    Article  Google Scholar 

  34. Walczak, S.; Morishita, K.; Ahmed, M.; Liu, J. W. Towards understanding of poly-guanine activated fluorescent silver nanoclusters. Nanotechnology 2014, 25, 155501.

    Article  Google Scholar 

  35. Li, T. T.; He, N. Y.; Wang, J. H.; Li, S.; Deng, Y.; Wang, Z. L. Effects of the i-motif DNA loop on the fluorescence of silver nanoclusters. RSC Adv. 2016, 6, 22839–22844.

    Article  Google Scholar 

  36. Burge, S.; Parkinson, G. N.; Hazel, P.; Todd, A. K.; Neidle, S. Quadruplex DNA: Sequence, topology and structure. Nucleic Acids. Res. 2006, 34, 5402–5415.

    Article  Google Scholar 

  37. Ma, D. L.; Che, C. M.; Yan, S. C. Platinum(II) complexes with dipyridophenazine ligands as human telomerase inhibitors and luminescent probes for G-quadruplex DNA. J. Am. Chem. Soc. 2009, 131, 1835–1846.

    Article  Google Scholar 

  38. Lu, L. H.; Chan, D. S.H.; Kwong, D. W. J.; He, H. Z.; Leung, C. H.; Ma, D. L. Detection of nicking endonuclease activity using a G-quadruplex-selective luminescent switch-on probe. Chem. Sci. 2014, 5, 4561–4568.

    Article  Google Scholar 

  39. Wang, M. D.; Mao, Z. F.; Kang, T. S.; Wong, C. Y.; Mergny, J. L.; Leung, C. H.; Ma, D. L. Conjugating a groovebinding motif to an Ir(III) complex for the enhancement of G-quadruplex probe behavior. Chem. Sci. 2016, 7, 2516–2523.

    Article  Google Scholar 

  40. Berti, L.; Burley, G. A. Nucleic acid and nucleotide-mediated synthesis of inorganic nanoparticles. Nat. Nanotechnol. 2008, 3, 81–87.

    Article  Google Scholar 

  41. Swasey, S. M.; Leal, L. E.; Lopez-Acevedo, O.; Pavlovich, J.; Gwinn, E. G. Silver (I) as DNA glue: Ag+-mediated guanine pairing revealed by removing Watson-Crick constraints. Sci. Rep. 2015, 5, 10163.

    Article  Google Scholar 

  42. Fu, Y.; Zhang, J. L.; Chen, X. F.; Huang, T. T.; Duan, X. L.; Li, W.; Wang, J. K. Silver nanomaterials regulated by structural competition of G-/C-rich oligonucleotides. J. Phys. Chem. C 2011, 115, 10370–10379.

    Article  Google Scholar 

  43. Lee, H. M.; Chan, D. S. H.; Yang, F.; Lam, H. Y.; Yan, S. C.; Che, C. M.; Ma, D. L.; Leung, C. H. Identification of natural product Fonsecin B as a stabilizing ligand of c-myc G-quadruplex DNA by high-throughput virtual screening. Chem. Commun. 2010, 46, 4680–4682.

    Article  Google Scholar 

  44. Yang, X.; Gan, L. F.; Han, L.; Wang, E. K.; Wang, J. High-yield synthesis of silver nanoclusters protected by DNA monomers and DFT prediction of their photoluminescence properties. Angew. Chem., Int. Ed. 2013, 52, 2022–2026.

    Article  Google Scholar 

  45. Hazel, P.; Huppert, J.; Balasubramanian, S.; Neidle, S. Loop-length-dependent folding of G-quadruplexes. J. Am. Chem. Soc. 2004, 126, 16405–16415.

    Article  Google Scholar 

  46. Bugaut, A.; Balasubramanian, S. A sequence-independent study of the influence of short loop lengths on the stability and topology of intramolecular DNA G-quadruplexes. Biochemistry 2008, 47, 689–697.

    Article  Google Scholar 

  47. Smargiasso, N.; Rosu, F.; Hsia, W.; Colson, P.; Baker, E. S.; Bowers, M. T.; Pauw, E. D.; Gabelica, V. G-quadruplex DNA assemblies: Loop length, cation identity, and multimer formation. J. Am. Chem. Soc. 2008, 130, 10208–10216.

    Article  Google Scholar 

  48. Guédin, A.; Gros, J.; Alberti, P.; Mergny, J. L. How long is too long? Effects of loop size on G-quadruplex stability. Nucleic Acids. Res. 2010, 38, 7858–7868.

    Article  Google Scholar 

  49. Soto-Verdugo, V.; Metiu, H.; Gwinn, E. The properties of small Ag clusters bound to DNA bases. J. Chem. Phys. 2010, 132, 195102.

    Article  Google Scholar 

  50. Lin, R. Y.; Tao, G. Y.; Chen, Y.; Chen, M. X.; Liu, F.; Li, N. Constructing a robust fluorescent DNA-stabilized silver nanocluster probe module by attaching a duplex moiety. Chem.—Eur. J. 2017, 23, 10893–10900.

    Article  Google Scholar 

  51. Sharma, J.; Rocha, R. C.; Phipps, M. L.; Yeh, H. C.; Balatsky, K. A.; Vu, D. M.; Shreve, A. P.; Werner, J. H.; Martinez, J. S. A DNA-templated fluorescent silver nanocluster with enhanced stability. Nanoscale 2012, 4, 4107–4110.

    Article  Google Scholar 

  52. Zeng, C. J.; Jin, R. C. Gold nanoclusters: Size-controlled synthesis and crystal structures. In Gold Clusters, Colloids and Nanoparticles I. Structure and Bonding. Mingos, D. M. P., Ed.; Springer: Cham, 2014; pp. 87–115.

    Google Scholar 

  53. Ramazanov, R. R.; Sych, T. S.; Reveguk, Z. V.; Maksimov, D. A.; Vdovichev, A. A.; Kononov, A. I. Ag-DNA emitter: Metal nanorod or supramolecular complex? J. Phys. Chem. Lett. 2016, 7, 3560–3566.

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 21535006, 21475004, and 21275011).

Author information

Authors and Affiliations

  1. Beijing National Laboratory for Molecular Sciences (BNLMS), Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education, Institute of Analytical Chemistry, College of Chemistry and Molecular Engineering, Peking University, Beijing, 100871, China

    Guangyu Tao, Yang Chen, Ruoyun Lin, Jiang Zhou, Xiaojing Pei, Feng Liu & Na Li

Authors
  1. Guangyu Tao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ruoyun Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiang Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiaojing Pei
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Feng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Na Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Na Li.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tao, G., Chen, Y., Lin, R. et al. How G-quadruplex topology and loop sequences affect optical properties of DNA-templated silver nanoclusters. Nano Res. 11, 2237–2247 (2018). https://doi.org/10.1007/s12274-017-1844-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12274-017-1844-4

Keywords

Search

Navigation