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We report lanthanide-based micelles integrating hypericin (Hyp) for X-ray-triggered photodynamic therapy (PDT). The lanthanide luminescence induced by X-ray irradiation excites the photosensitizer, which leads to the generation of singlet oxygen. This versatile approach can be extended to other photosensitizers or other types of liponanoparticles and can allow for magnetic resonance imaging (MRI) guidance.


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X-ray-induced radiophotodynamic therapy (RPDT) using lanthanide micelles: Beyond depth limitations

Show Author's information Slávka Kaščáková1,2Alexandre Giuliani1,3Sara Lacerda4Agnès Pallier4Pascal Mercère1Éva Tóth4Matthieu Réfrégiers1( )
Synchrotron SOLEILL'Orme des Merisiers91190Gif-sur-Yvette, France
UMR-S1193Université Paris-Sud XI94800Villejuif, France
INRACaractérisation et Élaboration des Produits Issus de l'Agriculture44316Nantes, France
Centre de Biophysique MoléculaireCNRSRue Charles Sadron45071Orléans Cedex 2, France

Abstract

We report lanthanide-based micelles integrating hypericin (Hyp) for X-ray-triggered photodynamic therapy (PDT). The lanthanide luminescence induced by X-ray irradiation excites the photosensitizer, which leads to the generation of singlet oxygen. This versatile approach can be extended to other photosensitizers or other types of liponanoparticles and can allow for magnetic resonance imaging (MRI) guidance.

Keywords: photodynamic therapy, liponanoparticles, X-ray, deep tumour, photosensitizer

References(38)

1

Setua, S.; Menon, D.; Asok, A.; Nair S.; Koyakutty, M. Folate receptor targeted, rare-earth oxide nanocrystals for bi-modal fluorescence and magnetic imaging of cancer cells. Biomaterials 2010, 31, 714–729.

2

Bünzli, J. C. G.; Piguet, C. Taking advantage of luminescent lanthanide ions. Chem. Soc. Rev. 2005, 34, 1048–1077.

3

Bruchez, M.; Moronne, M.; Gin, P.; Weiss, S.; Alivisatos, A. P. Semiconductor nanocrystals as fluorescent biological labels. Science 1998, 281, 2013–2016.

4

Chan, W. C. W.; Nie, S. M. Quantum dot bioconjugates for ultrasensitive nonisotopic detection. Science 1998, 281, 2016–2018.

5

Delehanty, J. B.; Bradburne, C. E.; Susumu, K.; Boeneman, K.; Mei, B. C.; Farrell, D.; Blanco-Canosa, J. B.; Dawson, P. E.; Mattoussi, H.; Medintz, I. L. Spatiotemporal multicolor labeling of individual cells using peptide-functionalized quantum dots and mixed delivery techniques. J. Am. Chem. Soc. 2011, 133, 10482–10489.

6

Pinaud, F.; Clarke, S.; Sittner, A.; Dahan, M. Probing cellular events, one quantum dot at a time. Nat. Methods 2010, 7, 275–285.

7

Faulkner, S.; Pope, S. J. A.; Burton-Pye, B. P. Lanthanide complexes for luminescence imaging applications. Appl. Spectrosc. Rev. 2005, 40, 1–31.

8

LaVan, D. A.; McGuire, T.; Langer, R. Small-scale systems for in vivo drug delivery. Nat. Biotechnol. 2003, 21, 1184– 1191.

9

Brigger, I.; Dubernet, C.; Couvreur, P. Nanoparticles in cancer therapy and diagnosis. Adv. Drug Delivery Rev. 2002, 54, 631–651.

10

Xie, J.; Lee, S.; Chen, X. Y. Nanoparticle-based theranostic agents. Adv. Drug Delivery Rev. 2010, 62, 1064–1079.

11

Caravan, P.; Ellison, J. J.; McMurry, T. J.; Lauffer, R. B. Gadolinium (Ⅲ) chelates as MRI contrast agents: Structure, dynamics, and applications. Chem. Rev. 1999, 99, 2293– 2352.

12

Zhou, Z. X.; Lu, Z. R. Gadolinium-based contrast agents for magnetic resonance cancer imaging. Wiley Interdiscip. Rev. : Nanomed. Nanobiotechnol. 2013, 5, 1–18.

13

Merbach, A. S.; Helm, L. Toth, E. The Chemistry of Contrast Agents in Medical Magnetic Resonance Imaging; John Wiley & Sons, Ltd: Chichester, West Sussex, UK, 2013.

DOI
14

Maguire, J. A.; Zhu, Y. Boron and Gadolinium Neutron Capture Therapy for Cancer Treatment; World Scientific Pub. Co. : Hackensack, NJ, 2012.

15

Eliseeva, S. V.; Bünzli, J. C. G. Lanthanide luminescence for functional materials and bio-sciences. Chem. Soc. Rev. 2010, 39, 189–227.

16

Werts, M. H. V. Making sense of lanthanide luminescence. Sci. Prog. 2005, 88, 101–131.

17

Urbain, G. La phosphorescence cathodique des terres rares. Ann. Chim. Phys. 1909, 8, 222–375.

18

Kaščáková, S.; Giuliani, A.; Jamme, F.; Refregiers, M. Photodynamic Therapy. In Radiation Damage in Biomolecular Systems; Springer: Dordrecht, Heidelberg, London, New York, 2012; pp 445–460.

19

Roelants, M.; Lackner, B.; Waser, M.; Falk, H.; Agostinis, P.; Van Poppel, H.; de Witte, P. A. M. In vitro study of the phototoxicity of bathochromically-shifted hypericin derivatives. Photochem. Photobiol. Sci. 2009, 8, 822–829.

20

Carpenter, S.; Fehr, M. J.; Kraus, G. A.; Petrich, J. W. Chemiluminescent activation of the antiviral activity of hypericin: A molecular flashlight. Proc. Natl. Acad. Sci. USA 1994, 91, 12273–12277.

21

Wen, J.; Chowdhury, P.; Wills, N. J.; Wannemuehler, Y.; Park, J.; Kesavan, S.; Carpenter, S.; Kraus, G. A.; Petrich, J. W. Toward the molecular flashlight: Preparation, properties and photophysics of a hypericin-luciferin tethered molecule. Photochem. Photobiol. 2002, 76, 153–157.

DOI
22

Theodossiou, T.; Hothersall, J. S.; Woods, E. A.; Okkenhaug, K.; Jacobson, J.; MacRobert, A. J. Firefly luciferin-activated rose bengal: In vitro photodynamic therapy by intracellular chemiluminescence in transgenic NIH 3T3 cells. Cancer Res. 2003, 63, 1818–1821.

23

Wang, F.; Zhang, Y.; Fan, X. P.; Wang, M. Q. Facile synthesis of water-soluble LaF3: Ln3+ nanocrystals. J. Mater. Chem. 2006, 16, 1031–1034.

24

Liu, Y. F.; Chen, W.; Wang, S. P.; Joly, A. G.; Westcott, S.; Woo, B. K. X-ray luminescence of LaF3: Tb3+ and LaF3: Ce3+, Tb3+ water-soluble nanoparticles. J. Appl. Phys. 2008, 103, 063105.

25

Liu, Y. F.; Chen, W.; Wang, S. P.; Joly, A. G. Investigation of water-soluble X-ray luminescence nanoparticles for photodynamic activation. Appl. Phys. Lett. 2008, 92, 043901.

26

Bulin, A. L.; Truillet, C.; Chouikrat, R.; Lux, F.; Frochot, C.; Amans, D.; Ledoux, G.; Tillement, O.; Perriat, P.; Barberi- Heyob, M. et. al. X-ray-induced singlet oxygen activation with nanoscintillator-coupled porphyins. J. Phys. Chem. C 2013, 117, 21583–21589.

27

Ma, L.; Zou, X.; Chen, W. A new X-ray activated nanoparticle photosensitizer for cancer treatment. J. Biomed. Nanotechnol. 2014, 10, 1501–1508.

28

Ma, L.; Zou, X. J.; Bui, B.; Chen, W.; Song, K. H.; Solberg, T. X-ray excited ZnS: Cu, Co afterglow nanoparticles for photodynamic activation. Appl. Phys. Lett. 2014, 105, 013702.

29

Bonnet, C. S.; Pellegatti, L.; Buron, F.; Shade, C. M.; Villette, S.; Kubíček, V.; Guillaumet, G.; Suzenet, F.; Petoud, S.; Tóth, É. Hydrophobic chromophore cargo in micellar structures: A different strategy to sensitize lanthanide cations. Chem. Commun. 2010, 46, 124–126.

30

Bonnet, C. S.; Buron, F.; Caillé, F., Shade, C. M.; Drahoš, B.; Pellegatti, L.; Zhang, J.; Villette, S.; Helm, L.; Pichon, C. et. al. Pyridine-based lanthanide complexes combining MRI and NIR luminescence activities. Chem. —Eur. J. 2012, 18, 1419–1431.

31

Chrysochoos, J. Fluorescence enhancement of Eu3+ by Tb3+ in dimethylsulfoxide (DMSO). J. Lumin. 1974, 9, 79–93.

32

Jiao, H.; Zhang, N.; Jing, X. P.; Jiao, D. M. Influence of rare earth elements (Sc, La Gd and Lu) on the luminescent properties of green phosphor Y2SiO5: Ce, Tb. Opt. Mater. (Amst). 2007, 29, 1023–1028.

33

Armelao, L.; Heigl, F.; Jürgensen, A.; Blyth, R. I. R.; Regier, T.; Zhou, X. T.; Sham, T. K. X-ray excited optical luminescence studies of ZnO and Eu-doped ZnO nanostructures. J. Phys. Chem. C 2007, 111, 10194–10200.

34
Trans-1-(2'-methoxyvinyl)pyrene. http://products.invitrogen.com/ivgn/product/M7913 (accessed Dec 24, 2014).
35

Kascakova, S.; Refregiers, M.; Jancura, D.; Sureau, F.; Maurizot, J. C.; Miskovsky, P. High level of low-density lipoprotein receptors enhance hypericin uptake by U-87 MG cells in the presence of LDL. Photochem. Photobiol. 2005, 81, 1395–1403.

36

Giuliani, A.; Jamme, F.; Rouam, V.; Wien, F.; Giorgetta, J. L.; Lagarde, B.; Chubar, O.; Bac, S.; Yao, I.; Rey, S. et al. DISCO: A low-energy multipurpose beamline at synchrotron SOLEIL. J. Synchrotron Radiat. 2009, 16, 835–841.

37

Jamme, F.; Villette, S.; Giuliani, A.; Rouam, V.; Wien, F.; Lagarde, B.; Réfrégiers, M. Synchrotron UV fluorescence microscopy uncovers new probes in cells and tissues. Microsc. Microanal. 2010, 16, 507–514.

38

Edelstein, A.; Amodaj, N.; Hoover, K.; Vale, R.; Stuurman, N. Computer control of microscopes using micromanager. Curr. Protoc. Mol. Biol. 2010, 92, 14.20.1–14.20.17.

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Publication history
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Acknowledgements

Publication history

Received: 24 December 2014
Revised: 03 February 2015
Accepted: 10 February 2015
Published: 20 May 2015
Issue date: July 2015

Copyright

© Tsinghua University Press and Springer-Verlag Berlin Heidelberg 2015

Acknowledgements

Acknowledgements

Data collection was performed on the METROLOGY and DISCO beamline (using the Biology support lab) at Synchrotron SOLEIL, France. We thank Dr. Célia Bonnet for her help in the preparation of the micelles, and Dr Frédéric Jamme, Valérie Rouam and Paulo Da Silva for their help and technical support. We are grateful to the SOLEIL synchrotron for general facilities placed at our disposure. This research was supported by SOLEIL (No. 20100575) and the Regional Council of the Région Centre (convention SOLEIL/Région Centre 201100070573 - DEEP-PDT).

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