Photodynamic therapy with fullerenes

H. W. Kroto, J. R. Heath, S. C. O’Brien, R. F. Curl and R. E. Smalley, C60: Buckminsterfullerene, Nature, 1985, 318, 162–163.

S. Bosi, T. Da Ros, G. Spalluto and M. Prato, Fullerene derivatives: an attractive tool for biological applications, Eur. J. Med. Chem., 2003, 38, 913–923.

A. W. Jensen, S. R. Wilson and D. I. Schuster, Biological applications of fullerenes, Bioorg. Med. Chem., 1996, 4, 767–779.

N. Tagmatarchis and H. Shinohara, Fullerenes in medicinal chemistry and their biological applications, Mini Rev. Med. Chem., 2001, 1, 339–348.

N. Levi, R. R. Hantgan, M. O. Lively, D. L. Carroll and G. L. Prasad, C60-Fullerenes: detection of intracellular photoluminescence and lack of cytotoxic effects, J. Nanobiotechnol., 2006, 4, 14.

B. Belgorodsky, L. Fadeev, J. Kolsenik and M. Gozin, Formation of a soluble stable complex between pristine C60-fullerene and a native blood protein, ChemBioChem, 2006, 7, 1783–1789.

N. Gharbi, M. Pressac, M. Hadchouel, H. Szwarc, S. R. Wilson and F. Moussa, [60]fullerene is a powerful antioxidant in vivo with no acute or subacute toxicity, Nano Lett., 2005, 5, 2578–2585.

C. M. Sayes, A. M. Gobin, K. D. Ausman, J. Mendez, J. L. West and V. L. Colvin, Nano-C60 cytotoxicity is due to lipid peroxidation, Biomaterials, 2005, 26, 7587–7595.

E. Nakamura and H. Isobe, Functionalized fullerenes in water. The first 10 years of their chemistry, biology, and nanoscience, Acc. Chem. Res., 2003, 36, 807–815.

D. Pantarotto, N. Tagmatarchis, A. Bianco and M. Prato, Synthesis and biological properties of fullerene-containing amino acids and peptides, Mini Rev. Med. Chem., 2004, 4, 805–814.

A. Bagno, S. Claeson, M. Maggini, M. L. Martini, M. Prato and G. Scorrano, 60]Fullerene as a substituent, Chemistry (Weinheim an der Bergstrasse, Germany), 2002, 8, 1015–1023.

N. Martin, M. Maggini and D. M. Guldi, Fullerenes 2000 - Volume 9: Functionalized Fullerenes, Proceedings of the International Symposium, 2000.

D. E. Dolmans, D. Fukumura and R. K. Jain, Photodynamic therapy for cancer, 2003, 3, 380–387.

A. P. Castano, T. N. Demidova and M. R. Hamblin, Mechanisms in photodynamic therapy: part one-photosensitizers, photochemistry and cellular localization, Photodiagn. Photodyn. Ther., 2004, 1, 279–293.

A. P. Castano, T. N. Demidova and M. R. Hamblin, Mechanisms in photodynamic therapy: part two-cellular signalling, cell metabolism and modes of cell death, Photodiagn. Photodyn. Ther. 2, 2005.

A. P. Castano, T. N. Demidova and M. R. Hamblin, Mechanisms in photodynamic therapy: part three-photosensitizer pharmacokinetics, biodistribution, tumor localization and modes of tumor destruction, Photodiagn. Photodyn. Ther., 2005, 2, 91–106.

A. P. Castano, T. N. Demidova and M. R. Hamblin, Mechanisms in photodynamic therapy: part one-photosensitizers, photochemistry and cellular localization, Photodiagn. Photodyn. Ther., 2004, 1, 279–293.

P. Agostinis, E. Buytaert, H. Breyssens and N. Hendrickx, Regulatory pathways in photodynamic therapy induced apoptosis, Photochem. Photobiol. Sci., 2004, 3, 721–729.

J. Moan and Q. Peng, An outline of the hundred-year history of PDT, Anticancer Res., 2003, 23, 3591–3600.

A. Jesionek and H. von Tappenier, Zur behandlung der hautcarcinomit mit fluorescierenden stoffen, Muench. Med. Wochneshr., 2042, 47, 1903.

T. J. Dougherty, A brief history of clinical photodynamic therapy development at Roswell Park Cancer Institute, J. Clin. Laser Med. Surg., 1996, 14, 219–221.

T. J. Dougherty, C. J. Gomer, B. W. Henderson, G. Jori, D. Kessel, M. Korbelik, J. Moan and Q. Peng, Photodynamic therapy, J. Natl. Cancer Inst., 1998, 90, 889–905.

P. Baas, I. van Mansom, H. van Tinteren, F. A. Stewart and N. van Zandwijk, Effect of N-acetylcysteine on Photofrin-induced skin photosensitivity in patients, Lasers Surg. Med., 1995, 16, 359–367.

A. Orenstein, G. Kostenich, L. Roitman, Y. Shechtman, Y. Kopolovic, B. Ehrenberg and Z. Malik, A comparative study of tissue distribution and photodynamic therapy selectivity of chlorin e6, Photofrin II and ALA-induced protoporphyrin IX in a colon carcinoma model, Br. J. Cancer, 1996, 73, 937–944.

J. D. Spikes, Chlorins as photosensitizers in biology and medicine, J. Photochem. Photobiol., B, 1990, 6, 259–274.

D. Kessel and P. Thompson, Purification and analysis of hematoporphyrin and hematoporphyrin derivative by gel exclusion and reverse-phase chromatography, Photochem. Photobiol., 1987, 46, 1023–1025.

R. W. Boyle and D. Dolphin, Structure and biodistribution relationships of photodynamic sensitizers, Photochem. Photobiol., 1996, 64, 469–485.

C. J. Gomer, Preclinical examination of first and second generation photosensitizers used in photodynamic therapy, Photochem. Photobiol., 1991, 54, 1093–1107.

E. S. Nyman and P. H. Hynninen, Research advances in the use of tetrapyrrolic photosensitizers for photodynamic therapy, J. Photochem. Photobiol., B, 2004, 73, 1–28.

M. R. Detty, S. L. Gibson and S. J. Wagner, Current clinical and preclinical photosensitizers for use in photodynamic therapy, J. Med. Chem., 2004, 47, 3897–3915.

P. Agostinis, A. Vantieghem, W. Merlevede and P. A. de Witte, Hypericin in cancer treatment: more light on the way, Int. J. Biochem. Cell Biol., 2002, 34, 221–241.

C. S. Foote, Photophysical and photochemical properties of fullerenes, Top. Curr. Chem., 1994, 169, 347–363.

A. Greer, Christopher Foote’s discovery of the role of singlet oxygen [1O2 (1Δg)] in photosensitized oxidation reactions, Acc. Chem. Res., 2006, 39, 797–804.

R. Schmidt, Photosensitized generation of singlet oxygen, Photochem. Photobiol., 2006, 82, 1161–1177.

J. W. Arbogast, A. P. Darmanyan, C. S. Foote, Y. Rubin, F. N. Diederich, M. M. Alvarez, S. J. Anz and R. L. Whetten, Photophysical properties of C60, J. Phys. Chem. A, 1991, 95, 11–12.

Y. Yamakoshi, N. Umezawa, A. Ryu, K. Arakane, N. Miyata, Y. Goda, T. Masumizu and T. Nagano, Active oxygen species generated from photoexcited fullerene (C60) as potential medicines: O2−˙ versus1O2, J. Am. Chem. Soc., 2003, 125, 12803–12809.

C. S. Foote, Definition of Type-I and Type-II photosensitized oxidation, Photochem. Photobiol., 1991, 54, 659–659.

M. Ochsner, Photophysical and photobiological processes in the photodynamic therapy of tumours, J. Photochem. Photobiol., B, 1997, 39, 1–18.

R. Koeppe and N. S. Sariciftci, Photoinduced charge and energy transfer involving fullerene derivatives, Photochem. Photobiol. Sci., 2006, 5, 1122–1131.

D. M. Guldi and M. Prato, Excited-state properties of C(60) fullerene derivatives, Acc. Chem. Res., 2000, 33, 695–703.

J. W. Arbogast, C. S. Foote and M. Kao, Electron-transfer to triplet C-60, J. Am. Chem. Soc., 1992, 114, 2277–2279.

N. Miyata, Y. Yamakoshi and I. Nakanishi, Reactive species responsible for biological actions of photoexcited fullerenes, J. Pharm. Soc. Jpn., 2000, 120, 1007–1016.

C. Yu, T. Canteenwala, M. E. El-Khouly, Y. Araki, K. Pritzker, O. Ito, B. C. Wilson and L. Y. Chiang, Efficiency of singlet oxygen production from self-assembled nanospheres of molecular micelle-like photosensitizers FC4S, J. Mater. Chem., 2005, 15, 1857–1864.

P. Mroz, A. Pawlak, M. Satti, H. Lee, T. Wharton, H. Gali, T. Sarna and M. R. Hamblin, Functionalized fullerenes mediate photodynamic killing of cancer cells: Type I versus Type II photochemical mechanism, Free Radical Biol. Med., 2007, 43, 711–719.

G. P. Tegos, T. N. Demidova, D. Arcila-Lopez, H. Lee, T. Wharton, H. Gali and M. R. Hamblin, Cationic fullerenes are effective and selective antimicrobial photosensitizers, Chem. Biol., 2005, 12, 1127–1135.

H. Tokuyama, S. Yamago and E. Nakamura, Photoinduced biochemical activity of fullerene carboxylic acid, J. Am. Chem. Soc., 1993, 115, 7918–7919.

Y. Z. An, C. B. Chen, J. L. Anderson, D. S. Sigman, C. S. Foote and Y. Rubin, Sequence-specific modification of guanosine in DNA by a C60-linked deoxyoligonucleotide: evidence for a non-singlet oxygen mechanism, Tetrahedron, 1996, 52, 5179–5189.

A. S. Boutorine, H. Tokuyama, M., T., H., I., E., N., C. Helene, Fullerene-oligonucleotide conjugates: photo-induced sequence-specific DNA cleavage, Angew. Chem., Int. Ed. Engl., 1994, 33, 2462–2465.

I. Nakanishi, S. Fukuzumi, T. Konishi, K. Ohkubo, M. Fujitsuka, O. Ito and N. Miyata, DNA cleavage via electron transfer from NADH to molecular oxygen photosensitized by γ-cyclodextrin-bicapped C60, in Fullerenes for the New Millennium, ed. P. V. Kamat, D. M. Guldi and D. M. Kadish, The Electrochemical Society, Pennigton, NJ, 2001, vol. 11, pp. 138–151.

Y. Yamakoshi, S. Sueyoshi and N. Miyata, Biological activity of photoexcited fullerene, Kokuritsu Iyakuhin Shokuhin Eisei Kenkyujo hokoku = Bulletin of National Institute of Health Sciences, 1999, 117, 50–60.

Y. N. Yamakoshi, T. Yagami, S. Sueyoshi and N. Miyata, Acridine Adduct of [60]Fullerene with Enhanced DNA-Cleaving Activity, J. Org. Chem., 1996, 61, 7236–7237.

Y. Liu, Y. L. Zhao, Y. Chen, P. Liang and L. Li, A water-soluble beta cyclodextrin derivative possessing a fullerene tether as an efficient photodriven DNA-cleavage reagent, Tetrahedron Lett., 2005, 46, 2507–2511.

A. Ikeda, Y. Doi, M. Hashizume, J. Kikuchi and T. Konishi, An extremely effective DNA photocleavage utilizing functionalized liposomes with a fullerene-enriched lipid bilayer, J. Am. Chem. Soc., 2007, 129, 4140–4141.

N. Sera, H. Tokiwa and N. Miyata, Mutagenicity of the fullerene C60-generated singlet oxygen dependent formation of lipid peroxides, Carcinogenesis, 1996, 17, 2163–2169.

J. P. Kamat, T. P. Devasagayam, K. I. Priyadarsini, H. Mohan and J. P. Mittal, Oxidative damage induced by the fullerene C60 on photosensitization in rat liver microsomes, Chem.-Biol. Interact., 1998, 114, 145–159.

J. P. Kamat, T. P. Devasagayam, K. I. Priyadarsini and H. Mohan, Reactive oxygen species mediated membrane damage induced by fullerene derivatives and its possible biological implications, Toxicology, 2000, 155, 55–61.

X. L. Yang, C. Huang, X. G. Qiao, L. Yao, D. X. Zhao and X. Tan, Photo-induced lipid peroxidation of erythrocyte membranes by a bis-methanophosphonate fullerene, Toxicol. In Vitro, 2007.

F. Kasermann and C. Kempf, Photodynamic inactivation of enveloped viruses by buckminsterfullerene, Antiviral Res., 1997, 34, 65–70.

F. Kasermann and C. Kempf, Buckminsterfullerene and photodynamic inactivation of viruses, Rev. Med. Virol., 1998, 8, 143–151.

J. Hirayama, H. Abe, N. Kamo, T. Shinbo, Y. Ohnishi-Yamada, S. Kurosawa, K. Ikebuchi and S. Sekiguchi, Photoinactivation of vesicular stomatitis virus with fullerene conjugated with methoxy polyethylene glycol amine, Biol. Pharm. Bull., 1999, 22, 1106–1109.

Y. L. Lin, H. Y. Lei, Y. Y. Wen, T. Y. Luh, C. K. Chou and H. S. Liu, Light-independent inactivation of dengue-2 virus by carboxyfullerene C3 isomer, Virology, 2000, 275, 258–262.

A. Minnock, D. I. Vernon, J. Schofield, J. Griffiths, J. H. Parish and S. B. Brown, Photoinactivation of bacteria. Use of a cationic water-soluble zinc phthalocyanine to photoinactivate both gram-negative and gram-positive bacteria, J. Photochem. Photobiol., B, 1996, 32, 159–164.

M. Merchat, G. Bertolini, P. Giacomini, A. Villanueva and G. Jori, Meso-substituted cationic porphyrins as efficient photosensitizers of gram-positive and gram-negative bacteria, J. Photochem. Photobiol., B, 1996, 32, 153–157.

M. R. Hamblin and T. Hasan, Photodynamic therapy: a new antimicrobial approach to infectious disease?, Photochem. Photobiol. Sci., 2004, 3, 436–450.

T. N. Demidova and M. R. Hamblin, Photodynamic therapy targeted to pathogens, Int. J. Immunopathol. Pharmacol., 2004, 17, 245–254.

T. N. Demidova and M. R. Hamblin, Effect of cell-photosensitizer binding and cell density on microbial photoinactivation, Antimicrob. Agents Chemother., 2005, 49, 2329–2335.

S. A. Lambrechts, M. C. Aalders, D. H. Langeveld-Klerks, Y. Khayali and J. W. Lagerberg, Effect of monovalent and divalent cations on the photoinactivation of bacteria with meso-substituted cationic porphyrins, Photochem. Photobiol., 2004, 79, 297–302.

R. E. Hancock and A. Bell, Antibiotic uptake into gram-negative bacteria, Eur. J. Clin. Microbiol. Infect. Dis., 1988, 7, 713–720.

M. B. Spesia, M. E. Milanesio and E. N. Durantini, Synthesis, properties and photodynamic inactivation of Escherichia coli by novel cationic fullerene C(60) derivatives, Eur. J. Med. Chem., 2007.

W. A. Scrivens, J. M. Tour, K. E. Creek and L. Pirisi, Synthesis of C-14-labeled C-60, its suspension in water, and its uptake by human keratinocytes, J. Am. Chem. Soc., 1994, 116, 4517–4518.

S. Foley, C. Crowley, M. Smaihi, C. Bonfils, B. F. Erlanger, P. Seta and C. Larroque, Cellular localisation of a water-soluble fullerene derivative, Biochem. Biophys. Res. Commun., 2002, 294, 116–119.

A. E. Porter, M. Gass, K. Muller, J. N. Skepper, P. Midgley and M. Welland, Visualizing the uptake of C60 to the cytoplasm and nucleus of human monocyte-derived macrophage cells using energy-filtered transmission electron microscopy and electron tomography, Environ. Sci. Technol., 2007, 41, 3012–3017.

K. Irie, Y. Nakamura, H. Ohigashi, H. Tokuyama, S. Yamago and E. Nakamura, Photocytotoxicity of water-soluble fullerene derivatives, Biosci., Biotechnol., Biochem., 1996, 60, 1359–1361.

A. P. Burlaka, Y. P. Sidorik, S. V. Prylutska, O. P. Matyshevska, O. A. Golub, Y. I. Prylutskyy and P. Scharff, Catalytic system of the reactive oxygen species on the C60 fullerene basis, Exp. Oncol., 2004, 26, 326–327.

F. Rancan, S. Rosan, F. Boehm, A. Cantrell, M. Brellreich, H. Schoenberger, A. Hirsch and F. Moussa, Cytotoxicity and photocytotoxicity of a dendritic C(60) mono-adduct and a malonic acid C(60) tris-adduct on Jurkat cells, J. Photochem. Photobiol., B, 2002, 67, 157–162.

X. L. Yang, C. H. Fan and H. S. Zhu, Photo-induced cytotoxicity of malonic acid [C(60)]fullerene derivatives and its mechanism, Toxicol. In Vitro, 2002, 16, 41–46.

F. Rancan, M. Helmreich, A. Molich, N. Jux, A. Hirsch, B. Roder, C. Witt and F. Bohm, Fullerene-pyropheophorbide a complexes as sensitizer for photodynamic therapy: uptake and photo-induced cytotoxicity on Jurkat cells, J. Photochem. Photobiol., B, 2005, 80, 1–7.

M. E. Milanesio, M. G. Alvarez, V. Rivarola, J. J. Silber and E. N. Durantini, Porphyrin-fullerene C60 dyads with high ability to form photoinduced charge-separated state as novel sensitizers for photodynamic therapy, Photochem. Photobiol., 2005, 81, 891–897.

M. G. Alvarez, C. Prucca, M. E. Milanesio, E. N. Durantini and V. Rivarola, Photodynamic activity of a new sensitizer derived from porphyrin-C60 dyad and its biological consequences in a human carcinoma cell line, Int. J. Biochem. Cell Biol., 2006, 38, 2092–2101.

A. Ikeda, Y. Doi, K. Nishiguchi, K. Kitamura, M. Hashizume, J. Kikuchi, K. Yogo, T. Ogawa and T. Takeya, Induction of cell death by photodynamic therapy with water-soluble lipid-membrane-incorporated [60]fullerene, Org. Biomol. Chem., 2007, 5, 1158–1160.

C. J. Liang-Takasaki, P. H. Makela and L. Leive, Phagocytosis of bacteria by macrophages: changing the carbohydrate of lipopolysaccharide alters interaction with complement and macrophages, J. Immunol., 1982, 128, 1229–1235.

R. Li, D. J. Bounds, D. Granville, S. H. Ip, H. Jiang, P. Margaron and D. W. Hunt, Rapid induction of apoptosis in human keratinocytes with the photosensitizer QLT0074 via a direct mitochondrial action, Apoptosis, 2003, 8, 269–275.

D. J. Granville, C. M. Carthy, H. Jiang, G. C. Shore, B. M. McManus and D. W. Hunt, Rapid cytochrome c release, activation of caspases 3, 6, 7 and 8 followed by Bap31 cleavage in HeLa cells treated with photodynamic therapy, FEBS Lett., 1998, 437, 5–10.

S. Gupta, N. Ahmad and H. Mukhtar, Involvement of nitric oxide during phthalocyanine (Pc4) photodynamic therapy-mediated apoptosis, Cancer Res., 1998, 58, 1785–1788.

D. Kessel, Y. Luo, P. Mathieu and J. J., Jr. Reiners, Determinants of the apoptotic response to lysosomal photodamage, Photochem. Photobiol., 2000, 71, 196–200.

M. G. Alvarez, F. Principe, M. E. Milanesio, E. N. Durantini and V. Rivarola, Photodynamic damages induced by a monocationic porphyrin derivative in a human carcinoma cell line, Int. J. Biochem. Cell Biol., 2005, 37, 2504–2512.

M. F. Ross, T. Da Ros, F. H. Blaikie, T. A. Prime, C. M. Porteous Severina, II, V. P. Skulachev, H. G. Kjaergaard, R. A. Smith and M. P. Murphy, Accumulation of lipophilic dications by mitochondria and cells, Biochem. J., 2006, 400, 199–208.

H. Rottenberg, Membrane potential and surface potential in mitochondria: uptake and binding of lipophilic cations, J. Membr. Biol., 1984, 81, 127–138.

M. P. Murphy and R. A. Smith, Targeting antioxidants to mitochondria by conjugation to lipophilic cations, Annu. Rev. Pharmacol. Toxicol., 2007, 47, 629–656.

S. M. Hahn, M. E. Putt, J. Metz, D. B. Shin, E. Rickter, C. Menon, D. Smith, E. Glatstein, D. L. Fraker and T. M. Busch, Photofrin uptake in the tumor and normal tissues of patients receiving intraperitoneal photodynamic therapy, Clin. Cancer Res., 2006, 12, 5464–5470.

Y. Tabata, Y. Murakami and Y. Ikada, Photodynamic effect of polyethylene glycol-modified fullerene on tumor, Jpn. J. Cancer Res., 1997, 88, 1108–1116.

J. Liu, S. Ohta, A. Sonoda, M. Yamada, M. Yamamoto, N. Nitta, K. Murata and Y. Tabata, Preparation of PEG-conjugated fullerene containing Gd(3+) ions for photodynamic therapy, J. Controlled Release, 2007, 117, 104–110.

C. Yu, T. Canteenwala, H. H. Chen, B. J. Chen, M. Canteenwala and L. Y. Chiang, Hexa(sulfobutyl)fullerene-induced photodynamic effect on tumors in vivo and toxicity study in rats, Proc. Electrochem. Soc., 1999, 99, 234–249.