Skip to main content
SpringerLink
Log in

Photoinduced charge separation in pyrenedicarboxamide-linked DNA hairpins

  • Paper
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

The synthesis and photophysical properties of the dihydroxypropylamide derivative of pyrene-1,6-dicaboxamide, its aniline dyad, and DNA conjugates are reported. The dicarboxamide serves as a hairpin linker for bis(oligonucleotide) conjugates having short base pair stems. The dihydroxypropyl derivative has a large fluorescence quantum yield and long singlet decay time, as determined by fluorescence and time-resolved broad band pump-probespectroscopy. The aniline dyad undergoes exergonic charge separation with formation of a radical ion pair which decays via charge recombination. The highly characteristic transient absorption spectrum of the pyrene anion radical is used to monitor the dynamics of its formation and decay. The dicarboxamide-linked hairpin conjugates undergo charge separation with adjacent guanine and adenine bases. Charge separation with guanine is accompanied by efficient pyrene fluorescence quenching. In contrast, reversible charge separation with adenine results in multiple exponential fluorescence decay. The energetics and dynamics of charge separation are compared with those of other arenedicarboxamide DNA hairpin linkers.

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. E. T. Kool, Replacing the nucleobases in DNA with designer molecules, Acc. Chem. Res., 2002, 35, 936–943.

    Article  CAS  PubMed  Google Scholar 

  2. N. Venkatesan, Y. J. Seo and B. H. Kim, Quencher-free molecular beacons: a new strategy in fluorescence based nucleic acid analysis, Chem. Soc. Rev., 2008, 37, 648–663.

    Article  CAS  PubMed  Google Scholar 

  3. N. E. Geacintov, K. Solntsev, L. W. Johnson, J. X. Chen, A. D. Kolbanovskiy, T. M. Liu and V. Y. Shafirovich, Photoinduced electron transfer and strand cleavage in pyrenyl-DNA complexes and adducts, J. Phys. Org. Chem., 1998, 11, 561–565.

    Article  CAS  Google Scholar 

  4. N. Amann, E. Pandurski, T. Fiebig, H.-A. Wagenknecht, A model nucleoside for electron injection into DNA: 5-pyrenyl-2-deoxyribose, Angew. Chem. Int. Ed., 2002, 41, 2978–2980.

    Article  CAS  Google Scholar 

  5. T. L. Netzel, M. Zhao, K. Nafisi, J. Headrick, M. S. Sigman and B. E. Eaton, Photophysics of 2’-deoxyuridine (dU) nucleosides covalently substituted with either 1-pyrenyl or 1-pyrenoyl: Observation of pyrene-to-nucleoside charge-transfer emission in 5-(1-pyrenyl)-dU, J. Am. Chem. Soc, 1995, 117, 9119–9128.

    Article  CAS  Google Scholar 

  6. P. Kaden, E. Mayer-Enthart, A. Trifonov, T. Fiebig, H.-A. Wagenknecht, Real-time spectroscopic and chemical probing of reductive electron transfer in DNA, Angew. Chem. Int. Ed., 2005, 44, 1636–1639.

    Article  CAS  Google Scholar 

  7. R. X. F. Ren, N. C. Chaudhuri, P. L. Paris, S. Rumney and E. T. Kool, Naphthalene, phenanthrene, and pyrene as DNA base analogues: Synthesis, structure, and fluorescence in DNA, J. Am. Chem. Soc., 1996, 118, 7671–7678.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. H. Zhu and F. D. Lewis, Pyrene excimer fluorescence as a probe for parallel G-quadruplex formation, Bioconjugate Chem., 2007, 18, 1213–1217.

    Article  CAS  Google Scholar 

  9. S. M. Langenegger, R. Häner, Excimer formation by interstrand stacked pyrenes, Chem. Commun., 2004, 2792–2793.

    Google Scholar 

  10. I. Trkulja, R. Häner, Triplehelix mediated excimer and exciplex formation, Bioconjugate Chem., 2007, 18, 289–292.

    Article  CAS  Google Scholar 

  11. S. T. Gaballah, J. D. Vaught, B. E. Eaton and T. L. Netzel, Charge-transfer excited state dynamics in DNA hairpins substituted with an ethylenylpyrenyl-dU electron source and halo-dU traps, J. Phys. Chem. B., 2005, 109, 5927–5934.

    Article  CAS  PubMed  Google Scholar 

  12. B. H. Yun, Y. A. Lee, S. K. Kim, V. Kuzmin, A. Kolbanovskiy, P. C. Dedon, N. E. Geacintov and V. Shafirovich, Photosensitized oxidative DNA damage: From hole injection to chemical product formation and strand cleavage, J. Am. Chem. Soc., 2007, 129, 9321–9332.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. F. D. Lewis, T. Wu, X. Liu, R. L. Letsinger, S. R. Greenfield, S. E. Miller and M. R. Wasielewski, Dynamics of photoinduced charge separation and charge recombination in synthetic DNA hairpins with stilbenedicarboxamide linkers, J. Am. Chem. Soc., 2000, 122, 2889–2902.

    Article  CAS  Google Scholar 

  14. F. D. Lewis, T. Wu, Y. Zhang, R. L. Letsinger, S. R. Greenfield and M. R. Wasielewski, Distance-dependent electron transfer in DNA hairpins, Science, 1997, 277, 673–676.

    Article  CAS  PubMed  Google Scholar 

  15. F. D. Lewis, X. Liu, S. E. Miller, R. T. Hayes and M. R. Wasielewski, Formation and decay of localized contact radical ion pairs in DNA hairpins, J. Am. Chem. Soc., 2002, 124, 14020–14026.

    Article  CAS  PubMed  Google Scholar 

  16. F. D. Lewis, Y. Zhang, X. Liu, N. Xu and R. L. Letsinger, Naphthalenedicarboxamides as fluorescent probes of inter- and intramolecular electron transfer in single strand, hairpin, and duplex DNA, J. Phys. Chem. B, 1999, 103, 2570–2578.

    Article  CAS  Google Scholar 

  17. F. D. Lewis, J. Liu, W. Weigel, W. Rettig, I. V. Kurnikov and D. N. Beratan, Donor-bridge-acceptor energetics determine the distance dependence of electron transfer in DNA, Proc. Natl. Acad. Sci. USA, 2002, 99, 12536–12541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. F. D. Lewis, L. Zhang, R. F. Kelley, D. McCamant and M. R. Wasielewski, A perylenedicarboxamide linker for DNA hairpins, Tetrahedron, 2007, 63, 3457–3464.

    Article  CAS  Google Scholar 

  19. R. L. Letsinger and T. Wu, Use of a stilbenedicarboxamide bridge in stabilizing, monitoring, and photochemically altering folded conformations of oligonucleotides, J. Am. Chem. Soc., 1995, 117, 7323–7328.

    Article  CAS  Google Scholar 

  20. S. Bevers, T. P. O’Dea and L. W. McLaughlin, Perylene- and naphthalene-based linkers for duplex and triplex stabilization, J. Am. Chem. Soc., 1998, 120, 11004–11005.

    Article  CAS  Google Scholar 

  21. T. Takada, K. Kawai, X. Cai, A. Sugimoto, M. Fujitsuka and T. Majima, Charge separation in DNA via consecutive adenine hopping, J. Am. Chem. Soc., 2004, 126, 1125–1129.

    Article  CAS  PubMed  Google Scholar 

  22. T. Takada, K. Kawai, M. Fujitsuka and T. Majima, High-yield generation of a long-lived charge-separated state in diphenylacetylene-modified DNA, Angew. Chem. Int. Ed., 2006, 45, 120–122.

    Article  CAS  Google Scholar 

  23. F. D. Lewis, X. Liu, J. Liu, R. T. Hayes and M. R. Wasielewski, Dynamics and equilibria for oxidation of G, GG, and GGG sequences in DNA Hairpins, J. Am. Chem. Soc., 2000, 122, 12037–12038.

    Article  CAS  Google Scholar 

  24. I. B. Berlman, Handbook of Fluorescence Spectra of Aromatic Molecules, Academic Press, New York, 1971.

    Google Scholar 

  25. F. D. Lewis, H. Zhu, P. Daublain, T. Fiebig, M. Raytchev, Q. Wang and V. Shafirovich, Crossover from superexchange to hopping as the mechanism for photoinduced charge transfer in DNA hairpin conjugates, J. Am. Chem. Soc., 2006, 128, 791–800.

    Article  CAS  PubMed  Google Scholar 

  26. F. D. Lewis, P. Daublain, L. Zhang, B. Cohen, J. Vura-Weis, M. R. Wasielewski, V. Shafirovich, Q. Wang, M. Raytchev and T. Fiebig, Reversible bridge-mediated excited state symmetry breaking in stilbene-linked DNA dumbbells, J. Phys. Chem. B, 2008, 112, 3838–3843.

    Article  CAS  PubMed  Google Scholar 

  27. H. Vollmann, H. Becker, M. Corell and H. Streeck, Beiträge zu kenntnis des pyrens und seiner derivate, Justus Liebigs Ann. Chem., 1937, 531, 1–159.

    Article  CAS  Google Scholar 

  28. S. Teramoto, M. Tanaka, H. Shimizu, T. Fujioka, F. Tabusa, T. Imaizumi, K. Yoshida, H. Fujiki, T. Mori, T. Sumida and M. Tominaga, Novel selective hindlimb vasodilators: Synthesis and biological activity of 1-acyl-4-aminopiperidine derivatives, J. Med. Chem., 2003, 46, 3033–3044.

    Article  CAS  PubMed  Google Scholar 

  29. Provided as electronic supplementary information.

  30. L. Zhang, H. Zhu, M. C. Sajimon, J. A. R. Stütz, K. Siegmund, C. Richert, V. Shafirovich and F. D. Lewis, Stabilization of DNA hairpins by stilbene capping of the terminal base pair, J. Chinese Chem. Soc. (Taipei), 2006, 53, 1501–1507.

    Article  CAS  Google Scholar 

  31. F. Mohamadi, N. G. J. Richard, W. C. Guida, L. R. M. Lipton, C. Caufield, G. Chang, T. Hendrickson and W. C. Still, MacroModel - an integrated software system for modeling organic and bioorganic molecules using molecular mechanics, J. Comput. Chem., 1990, 440–467.

    Google Scholar 

  32. F. D. Lewis, X. Liu, Y. Wu, S. E. Miller, M. R. Wasielewski, R. L. Letsinger, R. Sanishvili, A. Joachimiak, V. Tereshko and M. Egli, Structure and photoinduced electron transfer in exceptionally stable synthetic DNA hairpins with stilbenediether linkers, J. Am. Chem. Soc., 1999, 121, 9905–9906.

    Article  CAS  Google Scholar 

  33. D. B. Arter and P. G. Schmidt, Ring current shielding effects in nucleic acid double helices, Nucleic Acids Res., 1976, 3, 1437–1447.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. F. D. Lewis, L. Zhang, X. Liu, X. Zuo, D. M. Tiede, H. Long and G. S. Schatz, DNA as helical ruler: Exciton-coupled circular dichroism in DNA conjugates, J. Am. Chem. Soc., 2005, 127, 14445–14453.

    Article  CAS  PubMed  Google Scholar 

  35. M. Raytchev, E. Mayer, N. Amann, H. A. Wagenknecht and T. Fiebig, Ultrafast proton-coupled electron-transfer dynamics in pyrene-modified pyrimidine nucleosides: Model studies towards an understanding of reductive electron transport in DNA, Chem. Phys. Chem., 2004, 5, 706–712.

    Article  CAS  PubMed  Google Scholar 

  36. T. Okada, M. Migita, N. Mataga, Y. Sakata and S. Misumi, Picosecond laser spectroscopy of intramolecular heteroexcimer systems. Time-resolved absorption studies of p-(CH3)2NC6H4(CH2)n-1-pyrenyl and 9-anthryl systems, J. Am. Chem. Soc., 1981, 103, 4715–4720.

    Article  CAS  Google Scholar 

  37. T. A. Zeidan, Q. Wang, T. Fiebig and F. D. Lewis, Molecular wire behavior in π-stacked donor-brigde-acceptor tertiary arylureas, J. Am. Chem. Soc., 2007, 129, 9848–9849.

    Article  CAS  PubMed  Google Scholar 

  38. C. A. M. Seidel, A. Schulz, M. H. M. Sauer, Nucleobase-specific quenching of fluorescent dyes. 1. Nucleobase one-electron redox potentials and their correlation with static and dynamic quenching efficiencies, J. Phys. Chem., 1996, 100, 5541–5553.

    Article  CAS  Google Scholar 

  39. A. Weller, Photoinduced electron transfer in solution: exciplex and radical ion pair formation free enthalpies and their solvent dependence, Zeit. Phys. Chem., 1982, 133, 93–98.

    Article  CAS  Google Scholar 

  40. J. B. Birks, Photophysics of Aromatic Molecules, Wiley-Interscience, London, 1970.

    Google Scholar 

  41. M. Raytchev, E. Pandurski, I. Buchvarov, C. Modrakowski and T. Fiebig, Bichromophoric interactions and time-dependent excited state mixing in pyrene derivatives. A femtosecond broad-band pump-probe study, J. Phys. Chem. A, 2003, 107, 4592–4600.

    Article  CAS  Google Scholar 

  42. F. D. Lewis, P. Daublain, G. Delos Santos, W. Liu, A. M. Asatryan, S. A. Markarian, T. Fiebig, M. Raytchev and Q. Wang, Dynamics and mechanism of bridge-dependent charge separation in pyreneurea-nitrobenzene π-stacked protophanes, J. Am. Chem. Soc, 2006, 128, 791–800.

    Article  CAS  PubMed  Google Scholar 

  43. F. D. Lewis and T. L. Kurth, Intramolecular excimer fluorescence from floded ground state rotamers of N,N-diemethly-N,N′-dipyrenylurea protophanes, Can. J. Chem., 2003, 81, 770–776.

    Article  CAS  Google Scholar 

  44. D. O’Conner, V. Y. Shafirovich and N. E. Geacintov, Influence of adduct stereochemistry and hydrogen-bonding solvents on photoinduced charge transfer in a covalent benzo[a]pyrene diol epoxide-nucleoside adduct on picosecond time scales, J. Phys. Chem., 1994, 98, 9831–9839.

    Article  Google Scholar 

  45. F. D. Lewis and E. L. Burch, Conformation-dependent intramolecular electron transfer in N-(aminoalkyl)-9-phenanthrenecarboxamides, J. Phys. Chem., 1996, 100, 4055–4063.

    Article  CAS  Google Scholar 

  46. T. Kawai, M. Ikegamie and T. Arai, Exciplex formation between pyrene and guanine in highly polar solvents, Chem. Commun., 2004, 824–825.

    Google Scholar 

  47. R. A. Marcus, Theory of electron-transfer reactions. VI. Unified, treatment for homogeneous and electrode reactions, J. Phys. Chem., 1965, 43, 679–701.

    Article  CAS  Google Scholar 

  48. M. Van der Auweraer, L. Viaene, P. Van Haver, F. C. De Schryver, Influence of solvent polarity on the radiationless decay of the intramolecular exciplexes of ω-phenyl-α-N,N-dimethylaminoalkanes, J. Phys. Chem., 1993, 97, 7178–7184.

    Article  Google Scholar 

  49. F. D. Lewis, H. Zhu, P. Daublain, K. Siegmund, T. Fiebig, M. Raytchev, Q. Wang and V. Shafirovich, Getting to guanine: Mechanism and dynamics of charge separation and charge recombination in DNA revisited, Photochem. Photobiol. Sci., 2008, 7, 534–539.

    Article  CAS  PubMed  Google Scholar 

  50. Y. A. Berlin, A. L. Burin, L. D. A. Siebbeles and M. A. Ratner, Conformationally gated rate processes in biological molecules, J. Phys. Chem. A, 2001, 105, 5666–5678.

    Article  CAS  Google Scholar 

  51. F. C. Grozema, S. Tonzani, Y. A. Berlin, G. C. Schatz, L. D. A. Siebbeles and M. A. Ratner, Effect of structural dynamics on charge transfer in DNA hairpins, J. Am. Chem. Soc., 2008, 130, 5157–5166.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departments of Chemistry, Northwestern University, Evanston, IL, 60208-3113, USA

    Pierre Daublain, Karsten Siegmund, Mahesh Hariharan, Josh Vura-Weis, Michael R. Wasielewski & Frederick D. Lewis

  2. Boston College, Chestnut Hill, MA, 02467, USA

    Vladimir Shafirovich

  3. New York University, New York, NY, 10003, USA

    Qiang Wang, Milen Raytchev & Torsten Fiebig

Authors
  1. Pierre Daublain
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karsten Siegmund
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mahesh Hariharan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Josh Vura-Weis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael R. Wasielewski
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Frederick D. Lewis
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Vladimir Shafirovich
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Qiang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Milen Raytchev
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Torsten Fiebig
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Frederick D. Lewis, Vladimir Shafirovich or Torsten Fiebig.

Additional information

This paper was published as part of the themed issue in honour of Nicholas Turro.

Electronic supplementary information (ESI) available: MALDI-TOFMS data for pyrene conjugates (Table S1), 1H NMR spectrum of Pyd-4G (Figure S1) and transient absorption spectra for Pyd-2G (Figure S2) and Pyd-3G (Figure S3). See DOI: 10.1039/b813995d

Rights and permissions

Reprints and permissions

About this article

Cite this article

Daublain, P., Siegmund, K., Hariharan, M. et al. Photoinduced charge separation in pyrenedicarboxamide-linked DNA hairpins. Photochem Photobiol Sci 7, 1501–1508 (2008). https://doi.org/10.1039/b813995d

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/b813995d

Search

Navigation