Skip to main content
SpringerLink
Log in

Silver(I)-mediated base pairing in parallel-stranded DNA involving the luminescent cytosine analog 1,3-diaza-2-oxophenoxazine

  • Original Paper
  • Published:
JBIC Journal of Biological Inorganic Chemistry Aims and scope Submit manuscript

Abstract

1,3-Diaza-2-oxophenoxazine (X) has been introduced as a ligand in silver(I)-mediated base pairing in a parallel DNA duplex. This fluorescent cytosine analog is capable of forming stabilizing X–Ag(I)–X and X–Ag(I)–C base pairs in DNA duplexes, as confirmed by temperature-dependent UV spectroscopy and luminescence spectroscopy. DFT calculations of the silver(I)-mediated base pairs suggest the presence of a synergistic hydrogen bond. Molecular dynamics (MD) simulations of entire DNA duplexes nicely underline the geometrical flexibility of these base pairs, with the synergistic hydrogen bond facing either the major or the minor groove. Upon silver(I) binding to the X:X or X:C base pairs, the luminescence emission maximum experiences a red shift from 448 to 460 nm upon excitation at 370 nm. Importantly, the luminescence of the 1,3-diaza-2-oxophenoxazine ligand is not quenched significantly upon binding a silver(I) ion. In fact, the luminescence intensity even increases upon formation of a X–Ag(I)–C base pair, which is expected to be beneficial for the development of biosensors. As a consequence, the silver(I)-mediated phenoxazinone base pairs represent the first strongly fluorescent metal-mediated base pairs.

Graphic abstract

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Müller J (2010) Metallomics 2:318–327

    Article  CAS  PubMed  Google Scholar 

  2. Katz S (1963) Biochim Biophys Acta 68:240–253

    Article  CAS  PubMed  Google Scholar 

  3. Kondo J, Tada Y, Dairaku T, Hattori Y, Saneyoshi H, Ono A, Tanaka Y (2017) Nat Chem 9:956–960

    Article  CAS  PubMed  Google Scholar 

  4. Tanaka Y, Kondo J, Sychrovský V, Šebera J, Dairaku T, Saneyoshi H, Urata H, Torigoe H, Ono A (2015) Chem Commun 51:17343–17360

    Article  CAS  Google Scholar 

  5. Dairaku T, Furuita K, Sato H, Šebera J, Nakashima K, Kondo J, Yamanaka D, Kondo Y, Okamoto I, Ono A, Sychrovský V, Kojima C, Tanaka Y (2016) Chem Eur J 22:13028–13031

    Article  CAS  PubMed  Google Scholar 

  6. Jash B, Müller J (2017) Chem Eur J 23:17166–17178

    Article  CAS  PubMed  Google Scholar 

  7. Takezawa Y, Müller J, Shionoya M (2017) Chem Lett 46:622–633

    Article  CAS  Google Scholar 

  8. Clever GH, Kaul C, Carell T (2007) Angew Chem Int Ed 46:6226–6236

    Article  CAS  Google Scholar 

  9. Mandal S, Müller J (2017) Curr Opin Chem Biol 37:71–79

    Article  CAS  PubMed  Google Scholar 

  10. Kumbhar S, Johannsen S, Sigel RKO, Waller MP, Müller J (2013) J Inorg Biochem 127:203–210

    Article  CAS  PubMed  Google Scholar 

  11. Engelhard DM, Nowack J, Clever GH (2017) Angew Chem Int Ed 56:11640–11644

    Article  CAS  Google Scholar 

  12. Takezawa Y, Yoneda S, Duprey J-LHA, Nakama T, Shionoya M (2016) Chem Sci 7:3006–3010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Müller J (2017) Beilstein J Org Chem 13:2671–2681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Taherpour S, Golubev O, Lönnberg T (2014) J Org Chem 79:8990–8999

    Article  CAS  PubMed  Google Scholar 

  15. Johannsen S, Paulus S, Düpre N, Müller J, Sigel RKO (2008) J Inorg Biochem 102:1141–1151

    Article  CAS  PubMed  Google Scholar 

  16. Schlegel MK, Zhang L, Pagano N, Meggers E (2009) Org Biomol Chem 7:476–482

    Article  CAS  PubMed  Google Scholar 

  17. Seubert K, Fonseca Guerra C, Bickelhaupt FM, Müller J (2011) Chem Commun 47:11041–11043

    Article  CAS  Google Scholar 

  18. de Leon AR, Olatunde AO, Morrow JR, Achim C (2012) Inorg Chem 51:12597–12599

    Article  CAS  PubMed  Google Scholar 

  19. Nakagawa O, Fujii A, Kishimoto Y, Nakatsuji Y, Nozaki N, Obika S (2018) ChemBioChem 19:2372–2379

    Article  CAS  PubMed  Google Scholar 

  20. Ukale DU, Lönnberg T (2018) Angew Chem Int Ed 57:16171–16175

    Article  CAS  Google Scholar 

  21. Ukale D, Shinde VS, Lönnberg T (2016) Chem Eur J 22:7917–7923

    Article  CAS  PubMed  Google Scholar 

  22. Mandal S, Hebenbrock M, Müller J (2016) Angew Chem Int Ed 55:15520–15523

    Article  CAS  Google Scholar 

  23. Jash B, Müller J (2018) Angew Chem Int Ed 57:9524–9527

    Article  CAS  Google Scholar 

  24. Maity SK, Lönnberg T (2018) Chem Eur J 24:1274–1277

    Article  CAS  PubMed  Google Scholar 

  25. Méndez-Arriaga JM, Maldonado CR, Dobado JA, Galindo MA (2018) Chem Eur J 24:4583–4589

    Article  CAS  PubMed  Google Scholar 

  26. Santamaría-Díaz N, Méndez-Arriaga JM, Salas JM, Galindo MA (2016) Angew Chem Int Ed 55:6170–6174

    Article  CAS  Google Scholar 

  27. Guo X, Leonard P, Ingale SA, Liu J, Mei H, Sieg M, Seela F (2018) Chem Eur J 24:8883–8892

    Article  CAS  PubMed  Google Scholar 

  28. Zhao H, Leonard P, Guo X, Yang H, Seela F (2017) Chem Eur J 23:5529–5540

    Article  CAS  PubMed  Google Scholar 

  29. Mandal S, Hepp A, Müller J (2015) Dalton Trans 44:3540–3543

    Article  CAS  PubMed  Google Scholar 

  30. Sinha I, Kösters J, Hepp A, Müller J (2013) Dalton Trans 42:16080–16089

    Article  CAS  PubMed  Google Scholar 

  31. Mei H, Röhl I, Seela F (2013) J Org Chem 78:9457–9463

    Article  CAS  PubMed  Google Scholar 

  32. Jash B, Müller J (2018) Chem Eur J 24:10636–10640

    Article  CAS  PubMed  Google Scholar 

  33. Röthlisberger P, Levi-Acobas F, Sarac I, Marlière P, Herdewijn P, Hollenstein M (2019) J Inorg Biochem 191:154–163

    Article  CAS  PubMed  Google Scholar 

  34. Kobayashi T, Takezawa Y, Sakamoto A, Shionoya M (2016) Chem Commun 52:3762–3765

    Article  CAS  Google Scholar 

  35. Kaul C, Müller M, Wagner M, Schneider S, Carell T (2011) Nat Chem 3:794–800

    Article  CAS  PubMed  Google Scholar 

  36. Funai T, Nakamura J, Miyazaki Y, Kiriu R, Nakagawa O, Wada S-I, Ono A, Urata H (2014) Angew Chem Int Ed 53:6624–6627

    Article  CAS  Google Scholar 

  37. Scharf P, Müller J (2013) ChemPlusChem 78:20–34

    Article  CAS  Google Scholar 

  38. Liu S, Clever GH, Takezawa Y, Kaneko M, Tanaka K, Guo X, Shionoya M (2011) Angew Chem Int Ed 50:8886–8890

    Article  CAS  Google Scholar 

  39. Ehrenschwender T, Schmucker W, Wellner C, Augenstein T, Carl P, Harmer J, Breher F, Wagenknecht H-A (2013) Chem Eur J 19:12547–12552

    Article  CAS  PubMed  Google Scholar 

  40. Hensel S, Eckey K, Scharf P, Megger N, Karst U, Müller J (2017) Chem Eur J 23:10244–10248

    Article  CAS  PubMed  Google Scholar 

  41. Léon JC, She Z, Kamal A, Shamsi MH, Müller J, Kraatz H-B (2017) Angew Chem Int Ed 56:6098–6102

    Article  CAS  Google Scholar 

  42. Taherpour S, Golubev O, Lönnberg T (2016) Inorg Chim Acta 452:43–49

    Article  CAS  Google Scholar 

  43. Guo X, Seela F (2017) Chem Eur J 23:11776–11779

    Article  CAS  PubMed  Google Scholar 

  44. Jash B, Scharf P, Sandmann N, Fonseca Guerra C, Megger DA, Müller J (2017) Chem Sci 8:1337–1343

    Article  CAS  PubMed  Google Scholar 

  45. Léon JC, González-Abradelo G, Strassert CA, Müller J (2018) Chem Eur J 24:8320–8324

    Article  CAS  PubMed  Google Scholar 

  46. Mata G, Schmidt OP, Luedtke NW (2016) Chem Commun 52:4718–4721

    Article  CAS  Google Scholar 

  47. Schmidt OP, Mata G, Luedtke NW (2016) J Am Chem Soc 138:14733–14739

    Article  CAS  PubMed  Google Scholar 

  48. Berry DA, Jung K-Y, Wise DS, Sercel AD, Pearson WH, Mackie H, Randolph JB, Somers RL (2004) Tetrahedron Lett 45:2457–2461

    Article  CAS  Google Scholar 

  49. Park KS, Lee JY, Park HG (2012) Chem Commun 48:4549–4551

    Article  CAS  Google Scholar 

  50. Yang H, Mei H, Seela F (2015) Chem Eur J 21:10207–10219

    Article  CAS  PubMed  Google Scholar 

  51. Lin K-Y, Matteucci MD (1998) J Am Chem Soc 120:8531–8532

    Article  CAS  Google Scholar 

  52. Sandin P, Börjesson K, Li H, Mårtensson J, Brown T, Wilhelmsson LM, Albinsson B (2008) Nucleic Acids Res 36:157–167

    Article  CAS  PubMed  Google Scholar 

  53. Börjesson K, Sandin P, Wilhelmsson LM (2009) Biophys Chem 139:24–28

    Article  CAS  PubMed  Google Scholar 

  54. Ming X, Ding P, Leonard P, Budow S, Seela F (2012) Org Biomol Chem 10:1861–1869

    Article  CAS  PubMed  Google Scholar 

  55. Tsvetkov VB, Zatsepin TS, Belyaev ES, Kostyukevich YI, Shpakovski GV, Podgorsky VV, Pozmogova GE, Varizhuk AM, Aralov AV (2018) Nucleic Acids Res 46:2751–2764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Megger DA, Fonseca Guerra C, Hoffmann J, Brutschy B, Bickelhaupt FM, Müller J (2011) Chem Eur J 17:6533–6544

    Article  CAS  PubMed  Google Scholar 

  57. Kurchavov NA, Stetsenko DA, Skaptsova NV, Potapov VK, Sverdlov ED (1997) Nucleosides Nucleotides Nucleic Acids 16:1837–1846

    Article  CAS  Google Scholar 

  58. Heyd J, Scuseria GE, Ernzerhof M (2003) J Chem Phys 118:8207–8215

    Article  CAS  Google Scholar 

  59. Andrae D, Häußermann U, Dolg M, Stoll H, Preuß H (1990) Theor Chim Acta 77:123–141

    Article  CAS  Google Scholar 

  60. Singh UC, Kollman PA (1984) J Comp Chem 5:129–145

    Article  CAS  Google Scholar 

  61. Bayly CI, Cieplak P, Cornell WD, Kollman PA (1993) J Phys Chem 97:10269–10280

    Article  CAS  Google Scholar 

  62. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Petersson GA, Nakatsuji H, Caricato M, Li X, Hratchian HP, Izmaylov AF, Bloino J, Zheng G, Sonnenberg JL, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Montgomery JA Jr, Peralta JE, Ogliaro F, Bearpark M, Heyd JJ, Brothers E, Kudin KN, Staroverov VN, Kobayashi R, Normand J, Raghavachari K, Rendell A, Burant JC, Iyengar SS, Tomasi J, Cossi M, Rega N, Millam JM, Klene M, Knox JE, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Martin RL, Morokuma K, Zakrzewski VG, Voth GA, Salvador P, Dannenberg JJ, Dapprich S, Daniels AD, Farkas Ö, Foresman JB, Ortiz JV, Cioslowski J, Fox DJ (2009) Gaussian 09, revision A.1. Gaussian, Inc., Wallingford

    Google Scholar 

  63. Case DA, Betz RM, Cerutti DS, Cheatham TE III, Darden TA, Duke RE, Giese TJ, Gohlke H, Goetz AW, Homeyer N, Izadi S, Janowski P, Kaus J, Kovalenko A, Lee TS, LeGrand S, Li P, Lin C, Luchko T, Luo R, Madej B, Mermelstein D, Merz KM, Monard G, Nguyen H, Nguyen HT, Omelyan I, Onufriev A, Roe DR, Roitberg A, Sagui C, Simmerling CL, Botello-Smith WM, Swails J, Walker RC, Wang J, Wolf RM, Wu X, Xiao L, Kollman PA (2016) AMBER 2016. University of California, San Fransisco

    Google Scholar 

  64. Mark P, Nilsson L (2001) J Phys Chem A 105:9954–9960

    Article  CAS  Google Scholar 

  65. Chen X, Karpenko A, Lopez-Acevedo O (2017) ACS Omega 2:7343–7348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Krepl M, Zgarbová M, Stadlbauer P, Otyepka M, Banáš P, Koča J, Cheatham TE III, Jurečka P, Šponer J (2012) J Chem Theory Comput 8:2506–2520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Zgarbová M, Luque FJ, Šponer J, Cheatham TE III, Otyepka M, Jurečka P (2013) J Chem Theory Comput 9:2339–2354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Zgarbová M, Šponer J, Otyepka M, Cheatham TE III, Galindo-Murillo R, Jurečka P (2015) J Chem Theory Comput 11:5723–5736

    Article  CAS  PubMed  Google Scholar 

  69. Ryckaert J-P, Ciccotti G, Berendsen HJC (1977) J Comp Phys 23:327–341

    Article  CAS  Google Scholar 

  70. Darden T, York D, Pedersen L (1993) J Chem Phys 98:10089–10092

    Article  CAS  Google Scholar 

  71. Humphrey W, Dalke A, Schulten K (1996) J Mol Graphics 14:33–38

    Article  CAS  Google Scholar 

  72. Rentzeperis D, Rippe K, Jovin TM, Marky LA (1992) J Am Chem Soc 114:5926–5928

    Article  CAS  Google Scholar 

  73. Megger DA, Fonseca Guerra C, Bickelhaupt FM, Müller J (2011) J Inorg Biochem 105:1398–1404

    Article  CAS  PubMed  Google Scholar 

  74. Fortino M, Marino T, Russo N (2015) J Phys Chem A 119:5153–5157

    Article  CAS  PubMed  Google Scholar 

  75. Ono T, Yoshida K, Saotome Y, Sakabe R, Okamoto I, Ono A (2011) Chem Commun 47:1542–1544

    Article  CAS  Google Scholar 

  76. Swasey SM, Espinosa Leal L, Lopez-Acevedo O, Pavlovich J, Gwinn EG (2015) Sci Rep 5:10163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Richters T, Krug O, Kösters J, Hepp A, Müller J (2014) Chem Eur J 20:7811–7818

    Article  CAS  PubMed  Google Scholar 

  78. Schweizer K, Kösters J, Müller J (2015) J Biol Inorg Chem 20:895–903

    Article  CAS  PubMed  Google Scholar 

  79. Mandal S, Hebenbrock M, Müller J (2017) Chem Eur J 23:5962–5965

    Article  CAS  PubMed  Google Scholar 

  80. Scharf P, Jash B, Kuriappan JA, Waller MP, Müller J (2016) Chem Eur J 22:295–301

    Article  CAS  PubMed  Google Scholar 

  81. Ortega J-A, Blas JR, Orozco M, Grandas A, Pedroso E, Robles J (2007) Org Lett 9:4503–4506

    Article  CAS  PubMed  Google Scholar 

  82. Gu Y, Kar T, Scheiner S (1999) J Am Chem Soc 121:9411–9422

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Funding by the Deutsche Forschungsgemeinschaft (SFB 858) and the Russian Science Foundation (Project no. 18-74-00051—phenoxazine phosphoramidite and modified oligonucleotides synthesis) is gratefully acknowledged. We thank Bart Jan Ravoo for access to the fluorescence spectrometer.

Author information

Author notes

  1. Isabell Schönrath and Vladimir B. Tsvetkov contributed equally to this work.

Authors and Affiliations

  1. Westfälische Wilhelms-Universität Münster, Institut für Anorganische und Analytische Chemie, Corrensstr. 28/30, 48149, Münster, Germany

    Isabell Schönrath & Jens Müller

  2. Computational Oncology Group, I.M. Sechenov First Moscow State Medical University, Trubetskaya Str. 8-2, 119991, Moscow, Russia

    Vladimir B. Tsvetkov

  3. Research and Clinical Center for Physical Chemical Medicine, Malaya Pirogovskaya Str. 1a, 119435, Moscow, Russia

    Vladimir B. Tsvetkov

  4. Shemyakin-Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Miklukho-Maklaya Str. 16/10, 117997, Moscow, Russia

    Vladimir B. Tsvetkov & Andrey V. Aralov

  5. Skolkovo Institute of Science and Technology, Bolshoy Boulevard 30, bld. 1, 121205, Moscow, Russia

    Timofei S. Zatsepin

  6. Department of Chemistry, Lomonosov Moscow State University, Leninskie Gory Str. 1-3, 119992, Moscow, Russia

    Timofei S. Zatsepin

Authors
  1. Isabell Schönrath
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vladimir B. Tsvetkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Timofei S. Zatsepin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrey V. Aralov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jens Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Andrey V. Aralov or Jens Müller.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 3182 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schönrath, I., Tsvetkov, V.B., Zatsepin, T.S. et al. Silver(I)-mediated base pairing in parallel-stranded DNA involving the luminescent cytosine analog 1,3-diaza-2-oxophenoxazine. J Biol Inorg Chem 24, 693–702 (2019). https://doi.org/10.1007/s00775-019-01682-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-019-01682-1

Keywords

Search

Navigation