Skip to main content
SpringerLink
Log in

Diaminorhodamine and Light-Activatable NO Donors: Photorelease Quantification and Potential Pitfalls

  • SHORT COMMUNICATION
  • Published:
Journal of Fluorescence Aims and scope Submit manuscript

Abstract

Light-activatable nitric oxide (NO) donors have become of interest in the recent years. They produce NO when illuminated by light, which enables the control of its local concentration and is promising for biomedical applications. Several successful prototypes of photodonors have been published, but further research is needed to improve their properties such as water-solubility, activation wavelength, biocompatibility etc. One of major challenges on this way is to evaluate the efficiency of NO generation. Several methods may be used to track NO, including spin traps, specific electrodes and fluorescence-based probes. We have studied the applicability of well-known fluorescent reporter, diaminorhodamine (DAR-2), for the evaluation of NO production by photodonors. Our results indicate that DAR-2 can be used for the quantification of NO photorelease if this process is not accompanied by the singlet oxygen formation. Otherwise the oxidation of probe results in huge fluorescence increase, which interferes with signal due to reaction with NO. This issue should be taken into account when studying hybrids releasing both NO and 1O2, which are promising for photodynamic therapy.

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

Data Availability

All the data and materials from this manuscript will be made available on request.

References

  1. Tuteja N, Chandra M, Tuteja R, Misra MK (2004) Nitric oxide as a unique bioactive signaling messenger in physiology and pathophysiology. J Biomed Biotechnol 2004(4):227–237. https://doi.org/10.1155/S1110724304402034

    Article  PubMed  PubMed Central  Google Scholar 

  2. Fukuhara K, Kurihara M, Miyata N (2001) Photochemical generation of nitric oxide from 6-Nitrobenzo[a]pyrene. J Am Chem Soc 123(36):8662–8666

    Article  CAS  Google Scholar 

  3. Parisi C, Failla M, Fraix A, Rescifina A, Rolando B, Lazzarato L, Cardile V, Graziano ACE, Fruttero R, Gasco A, Sortino S (2019) A molecular hybrid producing simultaneously singlet oxygen and nitric oxide by single photon excitation with green light. Bioorg Chem 85:18–22. https://doi.org/10.1016/j.bioorg.2018.12.027

    Article  CAS  PubMed  Google Scholar 

  4. Nakagawa H (2016) Photocontrollable NO-releasing compounds and their biological applications. J Clin Biochem Nutr 58(1):2–6. https://doi.org/10.3164/jcbn.15-100

    Article  CAS  PubMed  Google Scholar 

  5. Ieda N, Hishikawa K, Eto K, Kitamura K, Kawaguchi M, Suzuki T, Fukuhara K, Miyata N, Furuta T, Nabekura J, Nakagawa H (2015) A double bond-conjugated Dimethylnitrobenzene-type Photolabile nitric oxide donor with improved two-photon cross section. Bioorg Med Chem Lett 25(16):3172–3175. https://doi.org/10.1016/j.bmcl.2015.05.095

    Article  CAS  PubMed  Google Scholar 

  6. Kitamura K, Ieda N, Hishikawa K, Suzuki T, Miyata N, Fukuhara K, Nakagawa H (2014) Visible light-induced nitric oxide release from a novel nitrobenzene derivative cross-conjugated with a Coumarin fluorophore. Bioorg Med Chem Lett 24(24):5660–5662. https://doi.org/10.1016/j.bmcl.2014.10.075

    Article  CAS  PubMed  Google Scholar 

  7. Okuno H, Ieda N, Hotta Y, Kawaguchi M, Kimura K, Nakagawa H (2017) A yellowish-green-light-controllable nitric oxide donor based on N-Nitrosoaminophenol applicable for Photocontrolled vasodilation. Org Biomol Chem 15(13):2791–2796. https://doi.org/10.1039/C7OB00245A

    Article  CAS  PubMed  Google Scholar 

  8. Zhou EY, Knox HJ, Reinhardt CJ, Partipilo G, Nilges MJ, Chan J (2018) Near-infrared photoactivatable nitric oxide donors with integrated photoacoustic monitoring. J Am Chem Soc 140(37):11686–11697. https://doi.org/10.1021/jacs.8b05514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Hishikawa K, Nakagawa H, Miyata N (2011) Nitric oxide donors activated by two-photon excitation. Yakugaku Zasshi 131(3):317–324

    Article  CAS  Google Scholar 

  10. Maia LB, Moura JJG (2016) Detection of nitric oxide by Electron paramagnetic resonance spectroscopy: spin-trapping with iron-Dithiocarbamates. Methods Mol Biol 1424:81–102. https://doi.org/10.1007/978-1-4939-3600-7_8

    Article  CAS  PubMed  Google Scholar 

  11. Davies IR, Zhang X (2008) Nitric Oxide Selective Electrodes. Methods Enzymol 436:63–95. https://doi.org/10.1016/S0076-6879(08)36005-4

    Article  CAS  PubMed  Google Scholar 

  12. Csonka C, Páli T, Bencsik P, Görbe A, Ferdinandy P, Csont T (2015) Measurement of NO in biological samples. Br J Pharmacol 172(6):1620–1632. https://doi.org/10.1111/bph.12832

    Article  CAS  PubMed  Google Scholar 

  13. Li H, Wan A (2015) Fluorescent probes for real-time measurement of nitric oxide in living cells. Analyst 140(21):7129–7141. https://doi.org/10.1039/C5AN01628B

    Article  CAS  PubMed  Google Scholar 

  14. Dong X, Heo CH, Chen S, Kim HM, Liu Z (2014) Quinoline-based two-photon fluorescent probe for nitric oxide in live cells and tissues. Anal Chem 86(1):308–311. https://doi.org/10.1021/ac403226h

    Article  CAS  PubMed  Google Scholar 

  15. Yao H-W, Zhu X-Y, Guo X-F, Wang H (2016) An amphiphilic fluorescent probe designed for extracellular visualization of nitric oxide released from living cells. Anal Chem 88(18):9014–9021. https://doi.org/10.1021/acs.analchem.6b01532

    Article  CAS  PubMed  Google Scholar 

  16. Kojima H, Hirotani M, Urano Y, Kikuchi K, Higuchi T, Nagano T (2000) Fluorescent indicators for nitric oxide based on rhodamine chromophore. Tetrahedron Lett 41(1):69–72. https://doi.org/10.1016/S0040-4039(99)02002-X

    Article  CAS  Google Scholar 

  17. He H, Ye Z, Xiao Y, Yang W, Qian X, Yang Y (2018) Super-resolution monitoring of mitochondrial dynamics upon time-gated photo-triggered release of nitric oxide. Anal Chem 90(3):2164–2169. https://doi.org/10.1021/acs.analchem.7b04510

    Article  CAS  PubMed  Google Scholar 

  18. Lazzarato L, Gazzano E, Blangetti M, Fraix A, Sodano F, Picone GM, Fruttero R, Gasco A, Riganti C, Sortino S (2019) Combination of PDT and NOPDT with a tailored BODIPY derivative. Antioxidants 8(11):531. https://doi.org/10.3390/antiox8110531

    Article  CAS  PubMed Central  Google Scholar 

  19. Kojima H, Hirotani M, Nakatsubo N, Kikuchi K, Urano Y, Higuchi T, Hirata Y, Nagano T (2001) Bioimaging of nitric oxide with fluorescent indicators based on the rhodamine chromophore. Anal Chem 73(9):1967–1973. https://doi.org/10.1021/ac001136i

    Article  CAS  PubMed  Google Scholar 

  20. Fraix A, Blangetti M, Guglielmo S, Lazzarato L, Marino N, Cardile V, Graziano ACE, Manet I, Fruttero R, Gasco A, Sortino S (2016) Light-tunable generation of singlet oxygen and nitric oxide with a Bichromophoric molecular hybrid: a bimodal approach to killing Cancer cells. ChemMedChem 11(12):1371–1379. https://doi.org/10.1002/cmdc.201500396

    Article  CAS  PubMed  Google Scholar 

  21. Vorob’ev AY, Dranova TY, Moskalensky AE (2018) Visible light-triggered nitric oxide donors for applications in biology and medicine. In: 2018 11th International Multiconference Bioinformatics of Genome Regulation and Structure\Systems Biology (BGRS\SB), pp 114–116. https://doi.org/10.1109/CSGB.2018.8544806

  22. Rosenthal I, Peretz P, Muszkat KA (1979) Thermochromic and hyperchromic effects in rhodamine B solutions. J Phys Chem 83(3):350–353. https://doi.org/10.1021/j100466a010

    Article  CAS  Google Scholar 

  23. Klymchenko AS (2017) Solvatochromic and fluorogenic dyes as environment-sensitive probes: design and biological applications. Acc Chem Res 50(2):366–375. https://doi.org/10.1021/acs.accounts.6b00517

    Article  CAS  PubMed  Google Scholar 

  24. Bonnett R, Martı́nez G (2001) Photobleaching of sensitisers used in photodynamic therapy. Tetrahedron 57(47):9513–9547. https://doi.org/10.1016/S0040-4020(01)00952-8

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The study was supported by Russian Science Foundation (Grant #18-15-00049). The synthesis of NOD550 was done in Novosibirsk Institute of Organic Chemistry SB RAS (affiliation #3), and we acknowledge fruitful discussions of the paper in the Institute of Chemical Kinetics and Combustion SB RAS (affiliation #2).

Funding

The study was supported by the Russian Science Foundation (Grant #18–15-00049).

Author information

Authors and Affiliations

  1. Novosibirsk State University, Pirogova 2, 630090, Novosibirsk, Russia

    Tatyana Yu. Dranova, Aleksey Yu. Vorobev, Eduard V. Pisarev & Alexander E. Moskalensky

  2. Voevodsky Institute of Chemical Kinetics and Combustion SB RAS, Institutskaya str. 3, 630090, Novosibirsk, Russia

    Tatyana Yu. Dranova & Alexander E. Moskalensky

  3. N.N. Vorozhtsov Novosibirsk Institute of Organic Chemistry SB RAS, 9 Lavrentiev Ave., 630090, Novosibirsk, Russia

    Aleksey Yu. Vorobev

Authors
  1. Tatyana Yu. Dranova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aleksey Yu. Vorobev
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eduard V. Pisarev
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexander E. Moskalensky
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

T.D.: experiments and data treatment; A.V.: synthesis of the compounds NOD-550 and NO-TPP; E.P.: some measurements of fluorescence; A.M.: study design and writing of the manuscript.

Corresponding author

Correspondence to Alexander E. Moskalensky.

Ethics declarations

Competing Interests

The authors declare no competing interests.

Ethical Approval

Not applicable.

Additional information

Publisher’s Note

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

Supplementary Information

ESM 1

(PDF 369 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dranova, T.Y., Vorobev, A.Y., Pisarev, E.V. et al. Diaminorhodamine and Light-Activatable NO Donors: Photorelease Quantification and Potential Pitfalls. J Fluoresc 31, 11–16 (2021). https://doi.org/10.1007/s10895-020-02643-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10895-020-02643-7

Keywords

Search

Navigation