Skip to main content
SpringerLink
Log in

Luminescent pyrenyl-GNA nucleosides: synthesis, photophysics and confocal microscopy studies in cancer HeLa cells

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

Abstract

Glycol nucleic acids (GNA) are synthetic genetic-like polymers with an acyclic three-carbon propylene glycol phosphodiester backbone. Here, synthesis, luminescence properties, circular dichroism (CD) spectra, and confocal microscopy speciation studies of (R,S) and (S,R) pyrenyl-GNA (pyr-GNA) nucleosides are reported in HeLa cells. Enantiomerically pure nucleosides were obtained by a Sharpless asymmetric dihydroxylation reaction followed by semi-preparative high-performance liquid chromatography (HPLC) separation using Amylose-2 as the chiral stationary phase. The enantiomeric relationship between stereoisomers was confirmed by CD spectra, and the absolute configurations were assigned based on experimental and theoretical CD spectra comparisons. The pyr-GNA nucleosides were not cytotoxic against human cervical (HeLa) cancer cells and thus were utilized as luminescent probes in the imaging of these cells with confocal microscopy. Cellular staining patterns were identical for both enantiomers in HeLa cells. Compounds showed no photocytotoxic effect and were localized in the lipid membranes of the mitochondria, in cellular vesicles and in other lipid cellular compartments. The overall distribution of the pyrene and pyrenyl-GNA nucleosides inside the living HeLa cells differed, since the former compound gives a more granular staining pattern and the latter a more diffuse one.

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. P. Perlíková and M. Hocek, Pyrrolo[2,3-d]pyrimidine (7-deazapurine) as a privileged scaffold in design of antitumor and antiviral nucleosides, Med. Res. Rev., 2017, 37, 1429–1460.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. J. Shelton, X. Lu, J. A. Hollenbaugh, J. H. Cho, F. Amblard and R. Schinazi, Metabolism, Biochemical Actions, and Chemical Synthesis of Anticancer Nucleosides, Nucleotides, and Base Analogs, Chem. Rev., 2016, 116, 14379–14455.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. J.-L. H. A. Duprey and J. H. R. Tucker, Metal–Carbon Bonds in Biopolymer Conjugates: Bioorganometallic Nucleic Acid Chemistry, Chem. Lett., 2014, 43, 157–163.

    Article  CAS  Google Scholar 

  4. C. Holzhauser and H.-A. Wagenknecht, DNA and RNA “Traffic Lights”: Synthetic Wavelength-Shifting Fluorescent Probes Based on Nucleic Acid Base Substitutes for Molecular Imaging, J. Org. Chem., 2013, 78, 7373–7379.

    Article  CAS  PubMed  Google Scholar 

  5. A. W. Feldman and F. E. Romesberg, Expansion of the Genetic Alphabet: A Chemist’s Approach to Synthetic Biology, Acc. Chem. Res., 2018, 51, 394–403.

    Article  CAS  PubMed  Google Scholar 

  6. S. Hoshika, N. A. Leal, M.-J. Kim, M.-S. Kim, N. B. Karalkar, H.-J. Kim, A. M. Bates, N. E. Watkins Jr., H. A. SantaLucia, A. J. Meyer, S. DasGupta, J. A. Piccirilli, A. D. Ellington, J. SantaLucia Jr., M. M. Georgiadis and S. A. Benner, Hachimoji DNA and RNA: A genetic system with eight building blocks, Science, 2019, 363, 884–887.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. T. Carell, C. Brandmayr, A. Hienzsch, M. Müller, D. Pearson, V. Reiter, I. Thoma, P. Thumbs and M. Wagner, Structure and function of noncanonical nucleobases, Angew. Chem., Int. Ed., 2012, 51, 7110–7131.

    Article  CAS  Google Scholar 

  8. T. Carell, M. Q. Kurz, M. Müller, M. Rossa and F. Spada, Non-canonical Bases in the Genome: The Regulatory Information Layer in DNA, Angew. Chem., Int. Ed., 2018, 57, 4296–4312.

    Article  CAS  Google Scholar 

  9. Ch. Schneider, S. Becker, H. Okamura, A. Crisp, T. Amatov, M. Stadlmeier and T. Carell, Noncanonical RNA Nucleosides as Molecular Fossils of an Early Earth—Generation by Prebiotic Methylations and Carbamoylations, Angew. Chem., Int. Ed., 2018, 57, 5943–5946.

    Article  CAS  Google Scholar 

  10. P. Herdewijn and P. Marlière, Toward safe genetically modified organisms through the chemical diversification of nucleic acids, Chem. Biodivers., 2009, 6, 791–808.

    Article  CAS  PubMed  Google Scholar 

  11. V. B. Pinheiro and P. Hollinger, The XNA world: progress towards replication and evolution of synthetic genetic polymers, Curr. Opin. Chem. Biol., 2012, 16, 245–252.

    Article  CAS  PubMed  Google Scholar 

  12. V. B. Pinheiro, A. I. Taylor, C. Cozens, M. Abramov, M. Renders, S. Zhang, J. C. Chaput, J. Wengel, S.-Y. Peak- Chew, S. H. McLaughlin, P. Herdewijn and P. Hollinger, Synthetic genetic polymers capable of heredity and evolution, Science, 2012, 336, 341–344.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. A. Taylor and P. Hollinger, Directed evolution of artificial enzymes (XNAzymes) from diverse repertoires of synthetic genetic polymers, Nat. Protoc., 2015, 10, 1625–1642.

    Article  CAS  PubMed  Google Scholar 

  14. L. Zhang, A. Peritz and E. Meggers, A Simple Glycol Nucleic Acid, J. Am. Chem. Soc., 2005, 127, 4174–4175.

    Article  CAS  PubMed  Google Scholar 

  15. M. K. Schlegel, A. E. Peritz, K. Kittigowittana, L. Zhang and E. Meggers, Duplex Formation of the Simplified Nucleic Acid GNA, ChemBioChem, 2007, 8, 927–932.

    Article  CAS  PubMed  Google Scholar 

  16. M. K. Schlegel, L.-O. Essen and E. Meggers, Duplex Structure of a Minimal Nucleic Acid, J. Am. Chem. Soc., 2008, 130, 8158–8159.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. E. Meggers and L. Zhang, Synthesis and Properties of the Simplified Nucleic Acid Glycol Nucleic Acid, Acc. Chem. Res., 2010, 43, 1092–1102.

    Article  CAS  PubMed  Google Scholar 

  18. G. F. Joyce, A. W. Schwartz, S. L. Miller and L. E. Orgel, The case for an ancestral genetic system involving simple analogues of the nucleotides, Proc. Natl. Acad. Sci. U. S. A., 1987, 84, 4398–4402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. B. D. Heuberger and C. Switzer, A Pre-RNA Candidate Revisited: Both Enantiomers of Flexible Nucleoside Triphosphates are DNA Polymerase Substrates, J. Am. Chem. Soc., 2008, 130, 412–413.

    Article  CAS  PubMed  Google Scholar 

  20. A. M. Noronha, C. J. Wilds, C.-N. Lok, K. Viazovkina, D. Arion, M. A. Parniak and M. J. Damha, Synthesis and Biophysical Properties of Arabinonucleic Acids (ANA): Circular Dichroic Spectra, Melting Temperatures, and Ribonuclease H Susceptibility of ANA·RNA Hybrid Duplexes, Biochemistry, 2000, 39, 7050–7062.

    Article  CAS  PubMed  Google Scholar 

  21. C. J. Wilds and M. J. Damha, 2′-Deoxy-2′-fluoro-β-D-arabinonucleosides and oligonucleotides (2′F-ANA): synthesis and physicochemical studies, Nucleic Acids Res., 2000, 28, 3625–3635.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. K.-U. Schöning, P. Scholz, S. Guntha, X. Wu, R. Krishnamurthy and A. Eschenmoser, Chemical Etiology of Nucleic Acid Structure: The α-Threofuranosyl-(3′→2′) Oligonucleotide System, Science, 2000, 290, 1347–1351.

    Article  PubMed  Google Scholar 

  23. D. Zhou, I. M. Lagoja, J. Rozenski, R. Busson, A. Van Aerschot and P. Herdewijn, Synthesis and Properties of Aminopropyl Nucleic Acids, ChemBioChem, 2005, 6, 2298–2304.

    Article  CAS  PubMed  Google Scholar 

  24. H. Kashida, K. Murayama, T. Toda and H. Asanuma, Control of the Chirality and Helicity of Oligomers of Serinol Nucleic Acid (SNA) by Sequence Design, Angew. Chem., Int. Ed., 2011, 50, 1285–1288.

    Article  CAS  Google Scholar 

  25. K. Toti, M. Renders, E. Groaz, P. Herdewijn and S. Van Calenbergh, Nucleosides with Transposed Base or 4′- Hydroxymethyl Moieties and Their Corresponding Oligonucleotides, Chem. Rev., 2015, 115, 13484–13525.

    Article  CAS  PubMed  Google Scholar 

  26. H. Asanuma, T. Toda, K. Murayama, X. Liang and H. Kashida, Unexpectedly Stable Artificial Duplex from Flexible Acyclic Threoninol, J. Am. Chem. Soc., 2010, 132, 14702–14703.

    Article  CAS  PubMed  Google Scholar 

  27. M. Egli, P. S. Pallan, R. Pattanayek, C. J. Wilds, P. Lubini, G. Minasov, M. Dobler, C. J. Leumann and A. Eschenmoser, Crystal Structure of Homo-DNA and Nature’s Choice of Pentose over Hexose in the Genetic System, J. Am. Chem. Soc., 2006, 128, 10847–10856.

    Article  CAS  PubMed  Google Scholar 

  28. R. Declerq, A. Van Aerschot, R. J. Read, P. Herdewijn and L. Van Meervelt, Crystal Structure of Double Helical Hexitol Nucleic Acids, J. Am. Chem. Soc., 2002, 124, 928–933.

    Article  CAS  Google Scholar 

  29. J. Wang, B. Verbeure, I. Luyten, E. Lescrinier, M. Froeyen, C. Hendrix, H. Rosemeyer, F. Seela, A. Van Aerschot and P. Herdewijn, Cyclohexene Nucleic Acids (CeNA): Serum Stable Oligonucleotides that Activate RNase H and Increase Duplex Stability with Complementary RNA, J. Am. Chem. Soc., 2000, 122, 8595–8602.

    Article  CAS  Google Scholar 

  30. S. Paul and M. H. Caruthers, Synthesis of Phosphorodiamidate Morpholino Oligonucleotides and Their Chimeras Using Phosphoramidite Chemistry, J. Am. Chem. Soc., 2016, 138, 15663–15672.

    Article  CAS  PubMed  Google Scholar 

  31. S. M. Daly, C. R. Sturge, K. R. Marshall-Batty, C. F. Felder- Scott, R. Jain, B. L. Geller and D. Greenberg, ACS Infect. Dis., 2018, 4, 806–814.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. P. Perlíková, K. K. Karlsen, E. B. Pedersen and J. Wengel, Unlocked Nucleic Acids with a Pyrene-Modified Uracil: Synthesis, Hybridization Studies, Fluorescent Properties and i-Motif Stability, ChemBioChem, 2014, 15, 146–156.

    Article  PubMed  CAS  Google Scholar 

  33. M. A. Campbell and J. Wengel, Locked vs. unlocked nucleic acids (LNA vs.UNA): contrasting structures work towards common therapeutic goals, Chem. Soc. Rev., 2011, 40, 5680–5689.

    CAS  PubMed  Google Scholar 

  34. I. Anisimov, S. Saloman, A. Hildebrandt, H. Lang, D. Trzybiński, K. Woźniak, D. Šakić, V. Vrček and K. Kowalski, 1,1′-Bis(thymine)ferrocene Nucleoside: Synthesis and. Study of Its Stereoselective Formation, ChemPlusChem, 2017, 82, 859–866.

    Article  CAS  PubMed  Google Scholar 

  35. J. Skiba, Q. Yuan, A. Hildebrandt, H. Lang, D. Trzybiński, K. Woźniak, R. K. Balogh, B. Gyurcsik, V. Vrček and K. Kowalski, Ferrocenyl GNA Nucleosides: A Bridge between Organic and Organometallic Xeno-nucleic Acids, ChemPlusChem, 2018, 83, 77–86.

    Article  CAS  PubMed  Google Scholar 

  36. H. V. Nguyen, A. Sallustrau, J. Balzarini, M. R. Bedford, J. C. Eden, N. Georgousi, N. J. Hodges, J. Kedge, Y. Mehellou, C. Tselepis and J. H. R. Tucker, Organometallic Nucleoside Analogues with Ferrocenyl Linker Groups: Synthesis and Cancer Cell Line Studies, J. Med. Chem., 2014, 57, 5817–5822.

    Article  CAS  PubMed  Google Scholar 

  37. K. Kowalski, J. Skiba, L. Oehninger, I. Ott, J. Solecka, A. Rajnisz and B. Therrien, Metallocene-Modified Uracils: Synthesis, Structure, and Biological Activity, Organometallics, 2013, 32, 5766–5773.

    Article  CAS  Google Scholar 

  38. H. V. Nguyen, Z. Zhao, A. Sallustrau, S. L. Horswell, L. Male, A. Mulas and J. H. R. Tucker, A ferrocene nucleic acid oligomer as an organometallic structural mimic of DNA, Chem. Commun., 2012, 48, 12165–12167.

    Article  CAS  Google Scholar 

  39. P. E. Nielsen, M. Egholm, R. H. Berg and O. Buchardt, Sequence-selective recognition of DNA by strand displacement with a thymine-substituted polyamide, Science, 1991, 254, 1497–1500.

    Article  CAS  PubMed  Google Scholar 

  40. M. K. Schlegel and E. Meggers, Improved Phosphoramidite Building Blocks for the Synthesis of the Simplified Nucleic Acid GNA, J. Org. Chem., 2009, 74, 4615–4618.

    Article  CAS  PubMed  Google Scholar 

  41. J. Skiba, R. Karpowicz, I. Szabó, B. Therrien and K. Kowalski, Synthesis and anticancer activity studies of ferrocenyl-thymine-3,6-dihydro-2H-thiopyranes - A new class of metallocene-nucleobase derivatives, J. Organomet. Chem., 2015, 794, 216–222.

    Article  CAS  Google Scholar 

  42. K. Kowalski, Ferrocenyl-nucleobase complexes: Synthesis, chemistry and applications, Coord. Chem. Rev., 2016, 317, 132–156.

    Article  CAS  Google Scholar 

  43. J. Skiba, C. Schmidt, P. Lippmann, P. Ensslen, H.-A. Wagenknecht, R. Czerwieniec, F. Brandl, I. Ott, T. Bernaś, B. Krawczyk, D. Szczukocki and K. Kowalski, Substitution of Metallocenes with [2.2]Paracyclophane to Enable Confocal Microscopy Imaging in Living Cells, Eur. J. Inorg. Chem., 2017, 297–305.

  44. K. Kowalski, A. Koceva-Chyła, A. Pieniążek, J. Bernasińska, J. Skiba, A. J. Rybarczyk-Pirek and Z. Jóźwiak, The synthesis, structure, electrochemistry and in vitro anticancer activity studies of ferrocenyl-thymine conjugates, J. Organomet. Chem., 2012, 700, 58–68.

    CAS  Google Scholar 

  45. J. Skiba, K. Kowalski, A. Prochnicka, I. Ott, J. Solecka, A. Rajnisz and B. Therrien, Metallocene-uracil conjugates: Synthesis and biological evaluation of novel mono-, di- and tri-nuclear systems, J. Organomet. Chem., 2015, 782, 52–61.

    Article  CAS  Google Scholar 

  46. P. Ensslen, Y. Fritz and H.-A. Wagenknecht, Mixed noncovalent assemblies of ethynyl nile red and ethynyl pyrene along oligonucleotide templates, Org. Biomol. Chem., 2015, 13, 487–492.

    Article  CAS  PubMed  Google Scholar 

  47. Y. N. Teo and E. T. Kool, DNA-Multichromophore Systems, Chem. Rev., 2012, 112, 4221–4245.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. F. Wojciechowski, J. Lietard and C. J. Leumann, 2-Pyrenyl- DNA: Synthesis, Pairing, and Fluorescence Properties, Org. Lett., 2012, 14, 5176–5179.

    Article  CAS  PubMed  Google Scholar 

  49. S. P. Sau and P. J. Hrdlicka, C2′-Pyrene-Functionalized Triazole-Linked DNA: Universal DNA/RNA Hybridization Probes, J. Org. Chem., 2012, 77, 5–16.

    Article  CAS  PubMed  Google Scholar 

  50. P. Ensslen and H.-A. Wagenknecht, One-Dimensional Multichromophor Arrays Based on DNA: From Self- Assembly to Light-Harvesting, Acc. Chem. Res., 2015, 48, 2724–2733.

    Article  CAS  PubMed  Google Scholar 

  51. S. Edwards, T. Ono, S. Wang, W. Jiang, R. Franzini, J. Jung, K. Chan and E. Kool, In Vitro Fluorogenic Real-Time Assay of the Repair of Oxidative DNA Damage, ChemBioChem, 2015, 16, 1637–1646.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. A. Jabłoński, Y. Fritz, H.-A. Wagenknecht, R. Czerwieniec, T. Bernaś, D. Trzybiński and K. Kowalski, Pyrene–nucleobase conjugates: synthesis, oligonucleotide binding and confocal bioimaging studies, Beilstein J. Org. Chem., 2017, 13, 2521–2534.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. H. C. Kolb, M. S. Van Nieuwenhze and K. B. Sharpless, Catalytic Asymmetric Dihydroxylation, Chem. Rev., 1994, 94, 2483–2547.

    Article  CAS  Google Scholar 

  54. N. J. Turro, V. Ramamurthy and J. C. Scaiano, Modern Molecular Photochemistry of Organic Molecules, University Science Books, Sausalito, California, USA, 2010, p. 217.

  55. A. G. Crawford, A. D. Dwyer, Z. Liu, A. Steffen, A. Beeby, L.-O. Pålsson, D. J. Tozer and T. B. Marder, Experimental and Theoretical Studies of the Photophysical Properties of 2- and 2,7-Functionalized Pyrene Derivatives, J. Am. Chem. Soc., 2011, 133, 13349–13362.

    Article  CAS  PubMed  Google Scholar 

  56. A. Mohr, P. Talbiersky, H.-G. Korth, R. Sustmann, R. Boese, D. Bläser and H. Rehage, A New Pyrene-Based Fluorescent Probe for the Determination of Critical Micelle Concentrations, J. Phys. Chem. B, 2007, 111, 12985–12992.

    Article  CAS  PubMed  Google Scholar 

  57. N. J. Turro and P.-L. Kuo, Pyrene excimer formations in micelles of nonionic detergents and of water-soluble polymers, Langmuir, 1986, 2, 438–442.

    Article  CAS  Google Scholar 

  58. N. Berova, P. L. Polavarapu, K. Nakanishi and R. W. Woody, Comprehensive Chiroptical Spectroscopy, Applications in Stereochemical Analysis of Synthetic Compounds, Natural Products and Biomolecules, Wiley, New York, 2012.

  59. E. L. Eliel, S. H. Wilen and L. N. Mander, Stereochemistry of Organic Compounds, Wiley, New York, 1994.

  60. PCMODEL, version 10.0, Serena Software, Box 3076, Bloomington, IN 47402.

  61. J. J. Gajewski, K. E. Gillbert and J. McKelvey, in Advances in Molecular Modeling, ed. D. Liotta, JAI Press, Inc., London, 1990, vol. 2, pp. 65–92.

    CAS  Google Scholar 

  62. M. J. Frisch, G. W. Trucks, H. B. Schlegel, G. E. Scuseria, M. A. Robb, J. R. Cheeseman, G. Scalmani, V. Barone, G. A. Petersson and H. Nakatsuji, X. Li, M. Caricato, A. V. Marenich, J. Bloino, B. G. Janesko, R. Gomperts, B. Mennucci, H. P. Hratchian, J. V. Ortiz, A. F. Izmaylov, J. L. Sonnenberg, D. Williams-Young, F. Ding and F. Lipparini, F. Egidi, J. Goings, B. Peng, A. Petrone, T. Henderson, D. Ranasinghe, V. G. Zakrzewski, J. Gao, N. Rega, G. Zheng, W. Liang, M. Hada, M. Ehara, K. Toyota, R. Fukuda, J. Hasegawa, M. Ishida, T. Nakajima, Y. Honda, O. Kitao and H. Nakai, T. Vreven, K. Throssell, J. A. Montgomery, Jr., J. E. Peralta, F. Ogliaro, M. J. Bearpark, J. J. Heyd, E. N. Brothers, K. N. Kudin, V. N. Staroverov, T. A. Keith, R. Kobayashi and J. Normand, K. Raghavachari, A. P. Rendell, J. C. Burant, S. S. Iyengar, J. Tomasi, M. Cossi, J. M. Millam, M. Klene, C. Adamo, R. Cammi, J. W. Ochterski, R. L. Martin, K. Morokuma and O. Farkas, J. B. Foresman and D. J. Fox, Gaussian 16, Revision A.03, Gaussian, Inc., Wallingford CT, 2016.

  63. W. K. Dunn, M. M. Kamocka and H. J. McDonald, A practical guide to evaluating colocalization in biological microscopy, Am. J. Physiol.: Cell Physiol., 2011, 300, C723–C742.

    Article  CAS  Google Scholar 

  64. CrysAlis CCD and CrysAlis RED, Oxford Diffraction, Oxford diffraction Ltd, Yarnton, UK, 2008.

  65. G. M. Sheldrick, A short history of SHELX, Acta Crystallogr., Sect. A: Found. Crystallogr., 2008, 64, 112–122.

    Article  CAS  Google Scholar 

  66. A. L. Spek, Structure validation in chemical crystallography, Acta Crystallogr., Sect. D: Biol. Crystallogr., 2009, 65, 148–155.

    Article  CAS  Google Scholar 

  67. O. V. Dolomanov, L. J. Bourhis, R. J. Gildea, J. A. K. Howard and H. Puschmann, OLEX2: a complete structure solution, refinement and analysis program, J. Appl. Crystallogr., 2009, 42, 339–341.

    Article  CAS  Google Scholar 

  68. C. F. Macrae, I. J. Bruno, J. A. Chisholm, P. R. Edgington, P. McCabe, E. Pidcock, L. Rodriguez-Monge, R. Taylor, J. van de Streek and P. A. Wood, Mercury CSD 2.0 –new features for the visualization and investigation of crystal structures, J. Appl. Crystallogr., 2008, 41, 466–470.

    Article  CAS  Google Scholar 

  69. A. Jabłoński, A. Kowalczyk, M. A. Fik, D. Trzybiński, K. Woźniak, K. Vinogradova, S. Glińska, V. Vrček, R. Czerwieniec and K. Kowalski, Anthracene-thymine luminophores: Synthesis, photophysical properties, and imaging in living HeLa cells, Dyes Pigm., 2019, 170, 107554–107565.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Organic Chemistry, Faculty of Chemistry, University of Łódź, Tamka 12, 91-403, Łódź, Poland

    Joanna Skiba & Konrad Kowalski

  2. Department of Microbial Genetics, Faculty of Biology and Environmental Protection, University of Łódź, Banacha 12/16, 90-237, Łódź, Poland

    Aleksandra Kowalczyk

  3. Department of Bioinorganic Chemistry, Faculty of Chemistry, Adam Mickiewicz University, Poznań, Poland

    Marta A. Fik

  4. Laboratory of Microscopic Imaging and Specialized Biological Techniques, Faculty of Biology and Environmental Protection, University of Łódź, Banacha 12/16, 90-237, Łódź, Poland

    Magdalena Gapiñska

  5. Biological and Chemical Research Centre, Department of Chemistry, University of Warsaw, Żwirki i Wigury 101, 02-089, Warszawa, Poland

    Damian Trzybiñski & Krzysztof Woźniak

  6. Faculty of Pharmacy and Biochemistry, University of Zagreb, Ante Kovačića 1, 10000, Zagreb, Croatia

    Valerije Vrček

  7. Institut für Physikalische und Theoretische Chemie, Universität Regensburg, Universitätsstraße 31, D-93040, Regensburg, Germany

    Rafai Czerwieniec

Authors
  1. Joanna Skiba
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aleksandra Kowalczyk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marta A. Fik
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Magdalena Gapiñska
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Damian Trzybiñski
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Krzysztof Woźniak
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Valerije Vrček
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rafai Czerwieniec
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Konrad Kowalski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joanna Skiba.

Additional information

Electronic supplementary information (ESI) available. CCDC 1902423. For ESI and crystallographic data in CIF or other electronic format see DOI: 10.1039/ c9pp00271e

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Skiba, J., Kowalczyk, A., Fik, M.A. et al. Luminescent pyrenyl-GNA nucleosides: synthesis, photophysics and confocal microscopy studies in cancer HeLa cells. Photochem Photobiol Sci 18, 2449–2460 (2019). https://doi.org/10.1039/c9pp00271e

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1039/c9pp00271e

Search

Navigation