Polymeric Encapsulation of Novel Homoleptic Bis(dipyrrinato) Zinc(II) Complexes with Long Lifetimes for Applications as Photodynamic Therapy Photosensitisers
Johannes Karges
Chimie ParisTech, PSL University, CNRS, Institute of Chemistry for Life and Health Sciences, Laboratory for Inorganic Chemical Biology, 75005 Paris, France
Search for more papers by this authorDr. Uttara Basu
Chimie ParisTech, PSL University, CNRS, Institute of Chemistry for Life and Health Sciences, Laboratory for Inorganic Chemical Biology, 75005 Paris, France
Search for more papers by this authorDr. Olivier Blacque
Department of Chemistry, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland
Search for more papers by this authorCorresponding Author
Prof. Hui Chao
MOE Key Laboratory of Bioinorganic and Synthetic Chemistry, School of Chemistry, Sun Yat-sen University, 510275 Guangzhou, P. R. China
Search for more papers by this authorCorresponding Author
Dr. Gilles Gasser
Chimie ParisTech, PSL University, CNRS, Institute of Chemistry for Life and Health Sciences, Laboratory for Inorganic Chemical Biology, 75005 Paris, France
Search for more papers by this authorJohannes Karges
Chimie ParisTech, PSL University, CNRS, Institute of Chemistry for Life and Health Sciences, Laboratory for Inorganic Chemical Biology, 75005 Paris, France
Search for more papers by this authorDr. Uttara Basu
Chimie ParisTech, PSL University, CNRS, Institute of Chemistry for Life and Health Sciences, Laboratory for Inorganic Chemical Biology, 75005 Paris, France
Search for more papers by this authorDr. Olivier Blacque
Department of Chemistry, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland
Search for more papers by this authorCorresponding Author
Prof. Hui Chao
MOE Key Laboratory of Bioinorganic and Synthetic Chemistry, School of Chemistry, Sun Yat-sen University, 510275 Guangzhou, P. R. China
Search for more papers by this authorCorresponding Author
Dr. Gilles Gasser
Chimie ParisTech, PSL University, CNRS, Institute of Chemistry for Life and Health Sciences, Laboratory for Inorganic Chemical Biology, 75005 Paris, France
Search for more papers by this authorAbstract
The use of photodynamic therapy (PDT) to treat cancer has received increasing attention over the last years. However, the clinically used photosensitisers (PSs) have some limitations that include poor aqueous solubility, hepatotoxicity, photobleaching, aggregation, and slow clearance from the body, so the design of new classes of PSs is of great interest. We present the use of bis(dipyrrinato)zinc(II) complexes with exceptionally long lifetimes as efficient PDT PSs. Based on the heavy-atom effect, intersystem crossing of these complexes changes the excited state from singlet to a triplet state, thereby enabling singlet oxygen generation. To overcome the limitation of quenching effects in water and improve water solubility, the lead compound 3 was encapsulated in a polymer matrix. It showed impressive phototoxicity upon irradiation at 500 nm in various monolayer cancer cells as well as 3D multicellular tumour spheroids, without observed dark toxicity.
Conflict of interest
The authors declare no conflict of interest.
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References
- 1
- 1aD. E. Dolmans, D. Fukumura, R. K. Jain, Nat. Rev. Cancer 2003, 3, 380–387;
- 1bA. E. O'Connor, W. M. Gallagher, A. T. Byrne, Photochem. Photobiol. 2009, 85, 1053–1074;
- 1cR. Bonnett, Chem. Soc. Rev. 1995, 24, 19–33;
- 1dS. Bonnet, Dalton Trans. 2018, 47, 10330–10343.
- 2
- 2aK. Plaetzer, B. Krammer, J. Berlanda, F. Berr, T. Kiesslich, Lasers Med. Sci. 2009, 24, 259–268;
- 2bT. J. Dougherty, C. J. Gomer, B. W. Henderson, G. Jori, D. Kessel, M. Korbelik, J. Moan, Q. Peng, JNCI J. Natl. Cancer Inst. 1998, 90, 889–905;
- 2cB. W. Henderson, T. J. Dougherty, Photochem. Photobiol. 1992, 55, 145–157;
- 2dP. Agostinis, K. Berg, K. A. Cengel, T. H. Foster, A. W. Girotti, S. O. Gollnick, S. M. Hahn, M. R. Hamblin, A. Juzeniene, D. Kessel, Ca-Cancer J. Clin. 2011, 61, 250–281;
- 2eS. Callaghan, M. O. Senge, Photochem. Photobiol. Sci. 2018, 17, 1490–1514.
- 3
- 3aF. Heinemann, J. Karges, G. Gasser, Acc. Chem. Res. 2017, 50, 2727–2736;
- 3bM. Jakubaszek, B. Goud, S. Ferrari, G. Gasser, Chem. Commun. 2018, 54, 13040–13059;
- 3cS. Monro, K. L. Colón, H. Yin, J. Roque III, P. Konda, S. Gujar, R. P. Thummel, L. Lilge, C. G. Cameron, S. A. McFarland, Chem. Rev. 2019, 119, 797–828;
- 3dF. E. Poynton, S. A. Bright, S. Blasco, D. C. Williams, J. M. Kelly, T. Gunnlaugsson, Chem. Soc. Rev. 2017, 46, 7706–7756;
- 3eJ. Shum, P. K.-K. Leung, K. K.-W. Lo, Inorg. Chem. 2019, 58, 2231–2247;
- 3fH. Huang, B. Yu, P. Zhang, J. Huang, Y. Chen, G. Gasser, L. Ji, H. Chao, Angew. Chem. Int. Ed. 2015, 54, 14049–14052; Angew. Chem. 2015, 127, 14255–14258;
- 3gC. Mari, V. Pierroz, R. Rubbiani, M. Patra, J. Hess, B. Spingler, L. Oehninger, J. Schur, I. Ott, L. Salassa, Chem. Eur. J. 2014, 20, 14421–14436;
- 3hC. Mari, V. Pierroz, A. Leonidova, S. Ferrari, G. Gasser, Eur. J. Inorg. Chem. 2015, 3879–3891;
- 3iM. Jakubaszek, J. Rossier, J. Karges, J. Delasoie, B. Goud, G. Gasser, F. Zobi, Helv. Chim. Acta 2019, 102, e 1900104;
- 3jJ. Karges, F. Heinemann, F. Maschietto, M. Patra, O. Blacque, I. Ciofini, B. Spingler, G. Gasser, Bioorg. Med. Chem. 2019, 27, 2666–2675;
- 3kR. Lincoln, L. Kohler, S. Monro, H. Yin, M. Stephenson, R. Zong, A. Chouai, C. Dorsey, R. Hennigar, R. P. Thummel, S. A. McFarland, J. Am. Chem. Soc. 2013, 135, 17161–17175;
- 3lK. Qiu, Y. Chen, T. W. Rees, L. Ji, H. Chao, Coord. Chem. Rev. 2019, 378, 66–86;
- 3mE. Wachter, D. K. Heidary, B. S. Howerton, S. Parkin, E. C. Glazer, Chem. Commun. 2012, 48, 9649–9651;
- 3nB. S. Howerton, D. K. Heidary, E. C. Glazer, J. Am. Chem. Soc. 2012, 134, 8324–8327.
- 4
- 4aY. Sun, L. E. Joyce, N. M. Dickson, C. Turro, Chem. Commun. 2010, 46, 6759–6761;
- 4bA. A. Holder, D. F. Zigler, M. T. Tarrago-Trani, B. Storrie, K. J. Brewer, Inorg. Chem. 2007, 46, 4760–4762;
- 4cL. K. McKenzie, H. E. Bryant, J. A. Weinstein, Coord. Chem. Rev. 2019, 379, 2–29.
- 5
- 5aS. Swavey, K. J. Brewer, Inorg. Chem. 2002, 41, 6196–6198;
- 5bW. Su, Z. Luo, S. Dong, X. Chen, J.-a. Xiao, B. Peng, P. Li, Photodiagn. Photodyn. Ther. 2019, 26, 448-454 ;
- 5cJ. D. Knoll, C. Turro, Coord. Chem. Rev. 2015, 282–283, 110–126;
- 5dA. M. Angeles-Boza, P. M. Bradley, P. K. L. Fu, S. E. Wicke, J. Bacsa, K. R. Dunbar, C. Turro, Inorg. Chem. 2004, 43, 8510–8519.
- 6
- 6aA. Zamora, G. Vigueras, V. Rodríguez, M. D. Santana, J. Ruiz, Coord. Chem. Rev. 2018, 360, 34–76;
- 6bL. K. McKenzie, I. V. Sazanovich, E. Baggaley, M. Bonneau, V. Guerchais, J. A. Williams, J. A. Weinstein, H. E. Bryant, Chem. Eur. J. 2017, 23, 234–238;
- 6cH. Huang, S. Banerjee, P. J. Sadler, ChemBioChem 2018, 19, 1574–1589;
- 6dV. Novohradsky, A. Rovira, C. Hally, A. Galindo, G. Vigueras, A. Gandioso, M. Svitelova, R. Bresolí-Obach, H. Kostrhunova, L. Markova, J. Kasparkova, S. Nonell, J. Ruiz, V. Brabec, V. Marchán, Angew. Chem. Int. Ed. 2019, 58, 6311–6315; Angew. Chem. 2019, 131, 6377–6381.
- 7
- 7aA. Loudet, K. Burgess, Chem. Rev. 2007, 107, 4891–4932;
- 7bG. Ulrich, R. Ziessel, A. Harriman, Angew. Chem. Int. Ed. 2008, 47, 1184–1201; Angew. Chem. 2008, 120, 1202–1219;
- 7cN. Boens, V. Leen, W. Dehaen, Chem. Soc. Rev. 2012, 41, 1130–1172;
- 7dJ. Karolin, L. B.-A. Johansson, L. Strandberg, T. Ny, J. Am. Chem. Soc. 1994, 116, 7801–7806.
- 8A. Kamkaew, S. H. Lim, H. B. Lee, L. V. Kiew, L. Y. Chung, K. Burgess, Chem. Soc. Rev. 2013, 42, 77–88.
- 9
- 9aS. O. McDonnell, M. J. Hall, L. T. Allen, A. Byrne, W. M. Gallagher, D. F. O'Shea, J. Am. Chem. Soc. 2005, 127, 16360–16361;
- 9bT. Yogo, Y. Urano, Y. Ishitsuka, F. Maniwa, T. Nagano, J. Am. Chem. Soc. 2005, 127, 12162–12163;
- 9cS. H. Lim, C. Thivierge, P. Nowak-Sliwinska, J. Han, H. van den Bergh, G. Wagnières, K. Burgess, H. B. Lee, J. Med. Chem. 2010, 53, 2865–2874;
- 9dS. Atilgan, Z. Ekmekci, A. L. Dogan, D. Guc, E. U. Akkaya, Chem. Commun. 2006, 4398–4400;
- 9eW. M. Gallagher, L. T. Allen, C. O'Shea, T. Kenna, M. Hall, A. Gorman, J. Killoran, D. F. O'Shea, Br. J. Cancer 2005, 92, 1702–1710;
- 9fY. Cakmak, S. Kolemen, S. Duman, Y. Dede, Y. Dolen, B. Kilic, Z. Kostereli, L. T. Yildirim, A. L. Dogan, D. Guc, E. U. Akkaya, Angew. Chem. Int. Ed. 2011, 50, 11937–11941; Angew. Chem. 2011, 123, 12143–12147;
- 9gL. Huang, X. Yu, W. Wu, J. Zhao, Org. Lett. 2012, 14, 2594–2597;
- 9hM. A. Filatov, S. Karuthedath, P. M. Polestshuk, S. Callaghan, K. J. Flanagan, M. Telitchko, T. Wiesner, F. Laquai, M. O. Senge, Phys. Chem. Chem. Phys. 2018, 20, 8016–8031;
- 9iS. Callaghan, M. A. Filatov, H. Savoie, R. W. Boyle, M. O. Senge, Photochem. Photobiol. Sci. 2019, 18, 495–504.
- 10
- 10aA. M. Potocny, J. J. Teesdale, A. Marangoz, G. P. A. Yap, J. Rosenthal, Inorg. Chem. 2019, 58, 5042–5050;
- 10bT. N. Singh-Rachford, A. Haefele, R. Ziessel, F. N. Castellano, J. Am. Chem. Soc. 2008, 130, 16164–16165;
- 10cM. J. Ortiz, A. R. Agarrabeitia, G. Duran-Sampedro, J. B. Prieto, T. A. Lopez, W. A. Massad, H. A. Montejano, N. A. García, I. L. Arbeloa, Tetrahedron 2012, 68, 1153–1162;
- 10dW. Wu, H. Guo, W. Wu, S. Ji, J. Zhao, J. Org. Chem. 2011, 76, 7056–7064;
- 10eY. Chen, J. Zhao, L. Xie, H. Guo, Q. Li, RSC Adv. 2012, 2, 3942–3953;
- 10fH. He, P.-C. Lo, S.-L. Yeung, W.-P. Fong, D. K. Ng, Chem. Commun. 2011, 47, 4748–4750;
- 10gA. Gorman, J. Killoran, C. O'Shea, T. Kenna, W. M. Gallagher, D. F. O'Shea, J. Am. Chem. Soc. 2004, 126, 10619–10631;
- 10hJ. Killoran, L. Allen, J. F. Gallagher, W. M. Gallagher, F. Donal, Chem. Commun. 2002, 1862–1863.
- 11
- 11aB. C. Wilson, W. P. Jeeves, D. M. Lowe, Photochem. Photobiol. 1985, 42, 153–162;
- 11bK. Ogawa, Y. Kobuke, Anti-Cancer Agents Med. Chem. 2008, 8, 269–279;
- 11cS. Bonnet, Comments Inorg. Chem. 2015, 35, 179–213.
- 12
- 12aH. Huang, S. Banerjee, P. J. Sadler, ChemBioChem 2018, 19, 1574–1589;
- 12bS. Chakrabortty, B. K. Agrawalla, A. Stumper, N. M. Vegi, S. Fischer, C. Reichardt, M. Kögler, B. Dietzek, M. Feuring-Buske, C. Buske, S. Rau, T. Weil, J. Am. Chem. Soc. 2017, 139, 2512–2519;
- 12cR. E. Doherty, I. V. Sazanovich, L. K. McKenzie, A. S. Stasheuski, R. Coyle, E. Baggaley, S. Bottomley, J. A. Weinstein, H. E. Bryant, Sci. Rep. 2016, 6, 22668.
- 13
- 13aR. Sakamoto, T. Iwashima, M. Tsuchiya, R. Toyoda, R. Matsuoka, J. F. Kögel, S. Kusaka, K. Hoshiko, T. Yagi, T. Nagayama, J. Mater. Chem. A 2015, 3, 15357–15371;
- 13bS. A. Baudron, Dalton Trans. 2013, 42, 7498–7509;
- 13cY. Ding, Y. Tang, W. Zhu, Y. Xie, Chem. Soc. Rev. 2015, 44, 1101–1112;
- 13dT. E. Wood, A. Thompson, Chem. Rev. 2007, 107, 1831–1861.
- 14
- 14aI. V. Sazanovich, C. Kirmaier, E. Hindin, L. Yu, D. F. Bocian, J. S. Lindsey, D. Holten, J. Am. Chem. Soc. 2004, 126, 2664–2665;
- 14bS. Lee, C.-H. Seok, Y. Park, A. Lee, D. H. Jung, S.-H. Choi, J. Park, Mol. Cryst. Liq. Cryst. 2010, 531, 365–372;
- 14cC. Trinh, K. Kirlikovali, S. Das, M. E. Ener, H. B. Gray, P. Djurovich, S. E. Bradforth, M. E. Thompson, J. Phys. Chem. C 2014, 118, 21834–21845;
- 14dS. Kusaka, R. Sakamoto, Y. Kitagawa, M. Okumura, H. Nishihara, Chem. Asian J. 2012, 7, 907–910;
- 14eR. Sakamoto, S. Kusaka, Y. Kitagawa, M.-a. Kishida, M. Hayashi, Y. Takara, M. Tsuchiya, J. Kakinuma, T. Takeda, K. Hirata, Dalton Trans. 2012, 41, 14035–14037.
- 15M. C. DeRosa, R. J. Crutchley, Coord. Chem. Rev. 2002, 233–234, 351–371.
- 16
- 16aJ. Karges, P. Goldner, G. Gasser, Inorganics 2019, 7, 4;
- 16bY. Ellahioui, M. Patra, C. Mari, R. Kaabi, J. Karges, G. Gasser, S. Gómez-Ruiz, Dalton Trans. 2019, 48, 5940–5951.
- 17
- 17aM. Patra, T. Joshi, V. Pierroz, K. Ingram, M. Kaiser, S. Ferrari, B. Spingler, J. Keiser, G. Gasser, Chem. Eur. J. 2013, 19, 14768–14772;
- 17bU. Basu, J. Karges, F. Chotard, C. Balan, P. Le Gendre, G. Gasser, E. Bodio, R. Malacea Kabbara, Polyhedron 2019, https://doi.org/10.1016/j.poly.2019.1002.1041;
- 17cA. K. Renfrew, J. Karges, R. Scopelliti, F. D. Bobbink, P. Nowak-Sliwinska, G. Gasser, P. Dyson, ChemBioChem 2019, https://doi.org/10.1002/cbic.201900236.
- 18
- 18aH. Kolarova, J. Macecek, P. Nevrelova, M. Huf, M. Tomecka, R. Bajgar, J. Mosinger, M. Strnad, Toxicol. In Vitro 2005, 19, 971–974;
- 18bJ. M. Dąbrowski, B. Pucelik, M. M. Pereira, L. G. Arnaut, G. Stochel, J. Coord. Chem. 2015, 68, 3116–3134.
- 19C. Pavani, A. F. Uchoa, C. S. Oliveira, Y. Iamamoto, M. S. Baptista, Photochem. Photobiol. Sci. 2009, 8, 233–240.
- 20
- 20aA. Pluen, Y. Boucher, S. Ramanujan, T. D. McKee, T. Gohongi, E. di Tomaso, E. B. Brown, Y. Izumi, R. B. Campbell, D. A. Berk, R. K. Jain, Proc. Natl. Acad. Sci. USA 2001, 98, 4628–4633;
- 20bP. A. Netti, D. A. Berk, M. A. Swartz, A. J. Grodzinsky, R. K. Jain, Cancer Res. 2000, 60, 2497–2503;
- 20cJ. Friedrich, C. Seidel, R. Ebner, L. A. Kunz-Schughart, Nat. Protoc. 2009, 4, 309;
- 20dT. T. Goodman, C. P. Ng, S. H. Pun, Bioconjugate Chem. 2008, 19, 1951–1959.
- 21
- 21aJ. Liu, Y. Chen, G. Li, P. Zhang, C. Jin, L. Zeng, L. Ji, H. Chao, Biomaterials 2015, 56, 140–153;
- 21bR. R. Allison, G. H. Downie, R. Cuenca, X.-H. Hu, C. J. Childs, C. H. Sibata, Photodiagn. Photodyn. Ther. 2004, 1, 27–42.
- 22Q. Zang, J. Yu, W. Yu, J. Qian, R. Hu, B. Z. Tang, Chem. Sci. 2018, 9, 5165–5171.
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