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Fullerenes as Photosensitizers in Photodynamic Therapy

  • Pawel Mroz
  • George P. Tegos
  • Hariprasad Gali
  • Timothy Wharton
  • Tadeusz Sarna
  • Michael R. Hamblin
Part of the Carbon Materials: Chemistry and Physics book series (CMCP, volume 1)

Abstract

Fullerenes are a class of closed-cage nanomaterials made exclusively from carbon atoms. A great deal of attention has been focused on developing medical uses of these unique molecules especially when they are derivatized with functional groups to make them soluble and therefore able to interact with biological systems. Due to their extended π-conjugation they absorb visible light, have a high triplet yield and can generate reactive oxygen species (ROS) upon illumination, suggesting a possible role of fullerenes in photodynamic therapy (PDT). Depending on the functional groups introduced into the molecule, fullerenes can effectively photoinactivate either or both pathogenic microbial cells and malignant cancer cells. The mechanism appears to involve Superoxide anion as well as singlet oxygen, and under the right conditions fullerenes may have advantages over clinically applied photosensitizers (PSs) for mediating photodynamic therapy of certain diseases.

Keywords

Photodynamic therapy Photosensitizer Photochemistry Reactive oxygen species Cancer Microorganism Infection 

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References

  1. Agostinis P, Vantieghem A, Merlevede W, de Witte PA (2002) Hypericin in cancer treatment: more light on the way. Int J Biochem Cell Biol 34:221-41. Google Scholar
  2. Agostinis P, Buytaert E, Breyssens H, Hendrickx N (2004) Regulatory pathways in photodynamic therapy induced apoptosis. Photochem Photobiol Sci 3:721-729. Google Scholar
  3. Alvarez MG, Prucca C, Milanesio ME, Durantini EN, Rivarola V (2006) 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 38:2092-2101. Google Scholar
  4. An YZ, Chen CB, Anderson JL, Sigman DS, Foote CS, Rubin Y (1996) Sequence-specific modi-fication of guanosine in DNA by a C60-linked deoxyoligonucleotide: evidence for a non-singlet oxygen mechanism. Tetrahedron 52:5179-5189. Google Scholar
  5. Arbogast JW, Darmanyan AP, Foote CS, Rubin Y, Diederich FN, Alvarez MM, Anz SJ, Whetten RL (1991a) Photophysical properties of C60. J Phys Chem A 95:11-12. Google Scholar
  6. Arbogast JW, Darmanyan AP, Foote CS, Rubin Y, Diederich FN, Alvarez MM, Anz SJ, Whetten RL (1991b) Photophysical properties of C60. J Phys Chem A Mol Spectrosc Kinet Environ Gen Theory 95:11-12. Google Scholar
  7. Arbogast JW, Foote CS, Kao M (1992) Electron-transfer to triplet C-60. J Am Chem Soc 114:2277-2279. Google Scholar
  8. Bachowski GJ, Pintar TJ, Girotti AW (1991) Photosensitized lipid peroxidation and enzyme inactivation by membrane-bound merocyanine 540: reaction mechanisms in the absence and presence of ascorbate. Photochem Photobiol 53:481-491. Google Scholar
  9. Bachowski GJ, Korytowski W, Girotti AW (1994) Characterization of lipid hydroperoxides generated by photodynamic treatment of leukemia cells. Lipids 29:449-459. Google Scholar
  10. Bagno A, Claeson S, Maggini M, Martini ML, Prato M, Scorrano G (2002) [60]Fullerene as a substituent. Chemistry 8:1015-1023. Google Scholar
  11. Belgorodsky B, Fadeev L, Kolsenik J, Gozin M (2006) Formation of a soluble stable complex between pristine C60-fullerene and a native blood protein. Chembiochem 7:1783-1789.Google Scholar
  12. Belousova IM, Mironova NG, Yur’ev MS (2005) A mathematical model of the photodynamic fullerene-oxygen action on biological tissues. Optic Spectrosc 98:349-356.Google Scholar
  13. Bilski P, Motten AG, Bilska M, Chignell CF (1993) The photooxidation of diethylhydroxylamine by rose bengal in micellar and nonmicellar aqueous solutions. Photochem Photobiol 58:11-18.Google Scholar
  14. Bosi S, Da Ros T, Spalluto G, Prato M (2003) Fullerene derivatives: an attractive tool for biological applications. Eur J Med Chem 38:913-923. Google Scholar
  15. Bottiroli G, Croce AC, Balzarini P, Locatelli D, Baglioni P, Lo Nostro P, Monici M, Pratesi R (1997) Enzyme-assisted cell photosensitization: a proposal for an efficient approach to tumor therapy and diagnosis. The rose bengal fluorogenic substrate. Photochem Photobiol 66:374-383.Google Scholar
  16. Boutorine AS, Tokuyama H, Takasugi M, Isobe H, Nkamura E, Helene C (1994) Fullerene-oligonucleotide conjugates: photo-induced sequence-specific DNA cleavage. Angew Chem Int Ed Engl 33:2462-2465. Google Scholar
  17. Buchko GW, Cadet J, Ravanat JL, Labataille P (1993) Isolation and characterization of a new product produced by ionizing irradiation and type I photosensitization of 2′-deoxyguanosine in oxygen-saturated aqueous solution: (2S)-2,5′-ANHYDRO-1-(2′-deoxy-beta-D-erythro-pentofuranosyl)-5-guanidin ylidene-2-hydroxy-4-oxoimidazolidine. Int J Radiat Biol 63:669-76. Google Scholar
  18. Buchko GW, Wagner JR, Cadet J, Raoul S, Weinfeld M (1995) Methylene blue-mediated photo-oxidation of 7,8-dihydro-8-oxo-2′-deoxyguanosine. Biochim Biophys Acta 1263:17-24.Google Scholar
  19. Burlaka AP, Sidorik YP, Prylutska SV, Matyshevska OP, Golub OA, Prylutskyy YI, Scharff P (2004) Catalytic system of the reactive oxygen species on the C60 fullerene basis. Exp Oncol 26:326-327. Google Scholar
  20. Castano AP, Demidova TN, Hamblin MR (2004) Mechanisms in photodynamic therapy: part one - photosensitizers, photochemistry and cellular localization. Photodiagn Photodyn Ther 1:279-293. Google Scholar
  21. Castano AP, Demidova TN, Hamblin MR (2005) Mechanisms in photodynamic therapy: part two - cellular signalling, cell metabolism and modes of cell death. Photodiagn Photodyn Ther 2:1-23. Google Scholar
  22. Davydenko MO, Radchenko EO, Yashchuk VM, Dmitruk IM, Prylutskyy YI, Matishevska OP, Golub AA (2006) Sensibilization of fullerene C60 immobilized at silica nanoparticles for can-cer photodynamic therapy. J Molec Liq 127:145-147. Google Scholar
  23. Demidova TN, Hamblin MR (2004) Photodynamic therapy targeted to pathogens. Int J Immunopathol Pharmacol 17:245-254. Google Scholar
  24. Demidova TN, Hamblin MR (2005) Effect of cell-photosensitizer binding and cell density on microbial photoinactivation. Antimicrob Agents Chemother 49:2329-2335.Google Scholar
  25. Detty MR, Gibson SL, Wagner SJ (2004) Current clinical and preclinical photosensitizers for use in photodynamic therapy. J Med Chem 47:3897-3915. Google Scholar
  26. Dolmans DE, Fukumura D, Jain RK (2003) Photodynamic therapy for cancer. Nat Rev Cancer 3:380-387. Google Scholar
  27. Fingar VH, Wieman TJ, Karavolos PS, Doak KW, Ouellet R, van Lier JE (1993) The effects of photodynamic therapy using differently substituted zinc phthalocyanines on vessel constric-tion, vessel leakage and tumor response. Photochem Photobiol 58:251-258.Google Scholar
  28. Foley S, Crowley C, Smaihi M, Bonfils C, Erlanger BF, Seta P, Larroque C (2002) Cellular locali-sation of a water-soluble fullerene derivative. Biochem Biophys Res Commun 294:116-119.Google Scholar
  29. Foote CS (1991) Definition of Type-I and Type-II photosensitized oxidation. Photochem Photobiol 54:659-659. Google Scholar
  30. Foote CS (1994) Photophysical and photochemical properties of fullerenes. Top Curr Chem 169:347-363. Google Scholar
  31. Gharbi N, Pressac M, Hadchouel M, Szwarc H, Wilson SR, Moussa F (2005) [60]fullerene is a powerful antioxidant in vivo with no acute or subacute toxicity. Nano Lett 5:2578-2585.Google Scholar
  32. Girotti AW (1983) Mechanisms of photosensitization. Photochem Photobiol 38:745-51.Google Scholar
  33. Girotti AW (1985) Mechanisms of lipid peroxidation. J Free Radic Biol Med 1:87-95.Google Scholar
  34. Granville DJ, Carthy CM, Jiang H, Shore GC, McManus BM, Hunt DW (1998) 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 437:5-10.Google Scholar
  35. Greer A (2006) Christopher Foote’s discovery of the role of singlet oxygen [1O2 (1Delta g)] in photosensitized oxidation reactions. Acc Chem Res 39:797-804. Google Scholar
  36. Grune T, Klotz LO, Gieche J, Rudeck M, Sies H (2001) Protein oxidation and proteolysis by the nonradical oxidants singlet oxygen or peroxynitrite. Free Radic Biol Med 30:1243-1253.Google Scholar
  37. Guldi DM, Prato M (2000) Excited-state properties of C(60) fullerene derivatives. Acc Chem Res 33:695-703. Google Scholar
  38. Gupta S, Ahmad N, Mukhtar H (1998) Involvement of nitric oxide during phthalocyanine (Pc4) photodynamic therapy-mediated apoptosis. Cancer Res 58:1785-1788. Google Scholar
  39. Hahn SM, Putt ME, Metz J, Shin DB, Rickter E, Menon C, Smith D, Glatstein E, Fraker DL, Busch TM (2006) Photofrin uptake in the tumor and normal tissues of patients receiving intra-peritoneal photodynamic therapy. Clin Cancer Res 12:5464-5470. Google Scholar
  40. Hamblin MR, Hasan T (2004) Photodynamic therapy: a new antimicrobial approach to infectious disease? 3:436-450.Google Scholar
  41. Hancock RE, Bell A (1988) Antibiotic uptake into gram-negative bacteria. Eur J Clin Microbiol Infect Dis 7:713-720. Google Scholar
  42. Hirayama J, Abe H, Kamo N, Shinbo T, Ohnishi-Yamada Y, Kurosawa S, Ikebuchi K, Sekiguchi S (1999) Photoinactivation of vesicular stomatitis virus with fullerene conjugated with methoxy polyethylene glycol amine. Biol Pharm Bull 22:1106-1109. Google Scholar
  43. Ikeda A, Doi Y, Hashizume M, Kikuchi J, Konishi T (2007a) An extremely effective DNA photo-cleavage utilizing functionalized liposomes with a fullerene-enriched lipid bilayer. J Am Chem Soc 129:4140-4141. Google Scholar
  44. Ikeda A, Doi Y, Nishiguchi K, Kitamura K, Hashizume M, Kikuchi J, Yogo K, Ogawa T, Takeya T (2007b) Induction of cell death by photodynamic therapy with water-soluble lipid-membrane-incorporated [60]fullerene. Org Biomol Chem 5:1158-1160. Google Scholar
  45. Irie K, Nakamura Y, Ohigashi H, Tokuyama H, Yamago S, Nakamura E (1996) Photocytotoxicity of water-soluble fullerene derivatives. Biosci Biotechnol Biochem 60:1359-1361.Google Scholar
  46. Isobe H, Nakanishi W, Tomita N, Jinno S, Okayama H, Nakamura E (2006) Nonviral gene delivery by tetraamino fullerene. Mol Pharm 3:124-34. Google Scholar
  47. Jensen AW, Wilson SR, Schuster DI (1996) Biological applications of fullerenes. Bioorg Med Chem 4:767-779. Google Scholar
  48. Kamat JP, Devasagayam TP, Priyadarsini KI, Mohan H, Mittal JP (1998) Oxidative damage induced by the fullerene C60 on photosensitization in rat liver microsomes. Chem Biol Interact 114:145-159. Google Scholar
  49. Kamat JP, Devasagayam TP, Priyadarsini KI, Mohan H (2000) Reactive oxygen species mediated membrane damage induced by fullerene derivatives and its possible biological implications. Toxicol 155:55-61. Google Scholar
  50. Kasermann F, Kempf C (1997) Photodynamic inactivation of enveloped viruses by buckminster-fullerene. Antiviral Res 34:65-70. Google Scholar
  51. Kasermann F, Kempf C (1998) Buckminsterfullerene and photodynamic inactivation of viruses. Rev Med Virol 8:143-151. Google Scholar
  52. Kessel D (1982) Components of hematoporphyrin derivatives and their tumor-localizing capacity. Cancer Res 42:1703-1706. Google Scholar
  53. Kessel D (1986) Photosensitization with derivatives of haematoporphyrin. [Review]. Int J Radiat Biol Relat Stud Phys Chem Med 49:901-907. Google Scholar
  54. Kessel D (1989a) On the purity and definition of oligomeric HPD formulations. J Photochem Photobiol B 3:637-638. Google Scholar
  55. Kessel D (1989b) Probing the structure of HPD by fluorescence spectroscopy. Photochem Photobiol 50:345-350. Google Scholar
  56. Kessel D, Thompson P (1987) Purification and analysis of hematoporphyrin and hematoporphyrin derivative by gel exclusion and reverse-phase chromatography. Photochem Photobiol 46:1023-1025. Google Scholar
  57. Kessel D, Thompson P, Musselman B, Chang CK (1987a) Chemistry of hematoporphyrin-derived photosensitizers. Photochem Photobiol 46:563-568.Google Scholar
  58. Kessel D, Thompson P, Musselman B, Chang CK (1987b) Probing the structure and stability of the tumor-localizing derivative of hematoporphyrin by reductive cleavage with LiAlH4. Cancer Res 47:4642-4645. Google Scholar
  59. Kessel D, Luo Y, Mathieu P, Reiners JJ (2000) Determinants of the apoptotic response to lyso-somal photodamage. Photochem Photobiol 71:196-200. Google Scholar
  60. Koeppe R, Sariciftci NS (2006) Photoinduced charge and energy transfer involving fullerene derivatives. Photochem Photobiol Sci 5:1122-1131. Google Scholar
  61. Kral V, Davis J, Andrievsky A, Kralova J, Synytsya A, Pouckova P, Sessler JL (2002) Synthesis and biolocalization of water-soluble sapphyrins. J Med Chem 45:1073-1078.Google Scholar
  62. Krätschmer W, Lamb LD, Fostiropoulos K, Huffman DR (1990) Solid C60: a new form of carbon. Nature 347:354-356. Google Scholar
  63. Kroto HW, Heath JR, O’Brien SC, Curl RF, Smalley RE (1985) C60: Buckminsterfullerene. Nature 318:162-163. Google Scholar
  64. Lambrechts SA, Aalders MC, Langeveld-Klerks DH, Khayali Y, Lagerberg JW (2004) Effect of monovalent and divalent cations on the photoinactivation of bacteria with meso-substituted cationic porphyrins. Photochem Photobiol 79:297-302. Google Scholar
  65. Levi N, Hantgan RR, Lively MO, Carroll DL, Prasad GL (2006) C60-Fullerenes: detection of intracellular photoluminescence and lack of cytotoxic effects. J Nanobiotechnology 4:14.Google Scholar
  66. Li R, Bounds DJ, Granville D, Ip SH, Jiang H, Margaron P, Hunt DW (2003) Rapid induction of apoptosis in human keratinocytes with the photosensitizer QLT0074 via a direct mitochondrial action. Apoptosis 8:269-275. Google Scholar
  67. Liang-Takasaki CJ, Makela PH, Leive L (1982) Phagocytosis of bacteria by macrophages: changing the carbohydrate of lipopolysaccharide alters interaction with complement and macrophages. J Immunol 128:1229-35. Google Scholar
  68. Lin YL, Lei HY, Wen YY, Luh TY, Chou CK, Liu HS (2000) Light-independent inactivation of dengue-2 virus by carboxyfullerene C3 isomer. Virology 275:258-262. Google Scholar
  69. Liu J, Ohta S, Sonoda A, Yamada M, Yamamoto M, Nitta N, Murata K, Tabata Y (2007) Preparation of PEG-conjugated fullerene containing Gd(3+) ions for photodynamic therapy. J Control Rel 117:104-10. Google Scholar
  70. Liu Y, Zhao YL, Chen Y, Liang P, Li L (2005) A water-soluble beta cyclodextrin derivative possessing a fullerene tether as an efficient photodriven DNA-cleavage reagent. Tetrahedron Lett 46:2507 -2511.Google Scholar
  71. Ma J, Jiang L (2001) Photogeneration of singlet oxygen (1O2) and free radicals (Sen*-, O2*-) by tetra-brominated hypocrellin B derivative. Free Radic Res 35:767-777. Google Scholar
  72. Martin N, Maggini M, Guldi DM (2000) Functionalized Fullerenes. Proceedings of theGoogle Scholar
  73. International Symposium, Vol. 9, The Electrochemical Society, Toronto, Canada.Google Scholar
  74. Merchat M, Bertolini G, Giacomini P, Villanueva A, Jori G (1996) Meso-substituted cationic por-phyrins as efficient photosensitizers of gram-positive and gram-negative bacteria. J Photochem Photobiol B 32:153-157. Google Scholar
  75. Midden WR, Dahl TA (1992) Biological inactivation by singlet oxygen: distinguishing O2(1 delta g) and O2(1 sigma g+). Biochim Biophys Acta 1117:216-222. Google Scholar
  76. Milanesio ME, Alvarez MG, Rivarola V, Silber JJ, Durantini EN (2005) Porphyrin-fullerene C60 dyads with high ability to form photoinduced charge-separated state as novel sensitizers for photodynamic therapy. Photochem Photobiol 81:891-897. Google Scholar
  77. Minnock A, Vernon DI, Schofield J, Griffiths J, Parish JH, Brown SB (1996) Photoinactivation of bacteria. Use of a cationic water-soluble zinc phthalocyanine to photoinactivate both gram-negative and gram-positive bacteria. J. Photochem. Photobiol. B 32:159-164.Google Scholar
  78. Miyata N, Yamakoshi Y, Nakanishi I (2000) Reactive species responsible for biological actions of photoexcited fullerenes. J Pharm Soc Jpn 120:1007-1016. Google Scholar
  79. Moan J, Berg K (1991) The photodegradation of porphyrins in cells can be used to estimate the lifetime of singlet oxygen. Photochem Photobiol 53:549-553. Google Scholar
  80. Mroz P, Pawlak A, Satti M, Lee H, Wharton T, Gali H, Sarna T, Hamblin MR (2007a) Functionalized fullerenes mediate photodynamic killing of cancer cells: Type I versus Type II photochemical mechanism. Free Radic Biol Med 43:711-9. Google Scholar
  81. Mroz P, Pawlak A, Satti M, Lee H, Wharton T, Gali H, Sarna T, Hamblin MR (2007b) Functionalized fullerenes mediate photodynamic killing of cancer cells: Type I versus Type II photochemical mechanism. Free Radical Biol Med 43:711-719. Google Scholar
  82. Mroz P, Tegos GP, Gali H, Wharton T, Sarna T, Hamblin MR (2007c) Photodynamic therapy with fullerenes. Photochem Photobiol Sci 6:1139-1149. Google Scholar
  83. Nakamura E, Isobe H (2003) Functionalized fullerenes in water. The first 10 years of their chemistry, biology, and nanoscience. Acc Chem Res 36:807-815. Google Scholar
  84. Nakanishi I, Fukuzumi S, Konishi T, Ohkubo K, Fujitsuka M, Ito O, Miyata N (2001) In: Kamat PV, Guldi DM, and Kadish DM (eds.) Fullerenes for the new millennium, The Electrochemical Society, Pennigton, NJ, X1, Toronto, Canada, pp. 138-151.Google Scholar
  85. Ochsner M (1997) Photophysical and photobiological processes in the photodynamic therapy of tumours. J Photochem Photobiol B 39:1-18. Google Scholar
  86. Pantarotto D, Tagmatarchis N, Bianco A, Prato M (2004) Synthesis and biological properties of fullerene-containing amino acids and peptides. Mini Rev Med Chem 4:805-814.Google Scholar
  87. Peng Q, Moan J, Nesland JM, Rimington C (1990) Aluminum phthalocyanines with asymmetrical lower sulfonation and with symmetrical higher sulfonation: a comparison of localizing and photosensitizing mechanism in human tumor LOX xenografts. Int J Cancer 46:719-26.Google Scholar
  88. Porter AE, Gass M, Muller K, Skepper JN, Midgley P, Welland M (2007) 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 41:3012-7. Google Scholar
  89. Rancan F, Rosan S, Boehm F, Cantrell A, Brellreich M, Schoenberger H, Hirsch A, Moussa F (2002) 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 67:157-162.Google Scholar
  90. Rancan F, Helmreich M, Molich A, Jux N, Hirsch A, Roder B, Witt C, Bohm F (2005) Fullerene-pyropheophorbide a complexes as sensitizer for photodynamic therapy: uptake and photo-induced cytotoxicity on Jurkat cells. J Photochem Photobiol B 80:1-7. Google Scholar
  91. Ravanat JL, Cadet J (1995) Reaction of singlet oxygen with 2′-deoxyguanosine and DNA. Isolation and characterization of the main oxidation products. Chem Res Toxicol 8:379-388.Google Scholar
  92. Rosenthal I, Murali Krishna C, Riesz P, Ben-Hur E (1986) The role of molecular oxygen in the photodynamic effect of phthalocyanines. Radiat Res 107:136-142. Google Scholar
  93. Sayes CM, Gobin AM, Ausman KD, Mendez J, West JL, Colvin VL (2005) Nano-C60 cytotoxicity is due to lipid peroxidation. Biomaterials 26:7587-7595. Google Scholar
  94. Schmidt R (2006) Photosensitized generation of singlet oxygen. Photochem Photobiol 82:1161-1177 Google Scholar
  95. Scrivens WA, Tour JM, Creek KE, Pirisi L (1994) Synthesis of C-14-labeled C-60, its suspension in water, and its uptake by human keratinocytes. J Am Chem Soc 116:4517-4518.Google Scholar
  96. Sera N, Tokiwa H, Miyata N (1996) Mutagenicity of the fullerene C60-generated singlet oxygen dependent formation of lipid peroxides. Carcinogenesis 17:2163-2169. Google Scholar
  97. Spesia MB, Milanesio ME, Durantini EN (2008) Synthesis, properties and photodynamic inacti-vation of Escherichia coli by novel cationic fullerene C(60) derivatives. Eur J Med Chem 43 (4):853-861. Google Scholar
  98. Stockert JC, Juarranz A, Villanueva A, Canete M (1996) Photodynamic damage to HeLa cell microtubules induced by thiazine dyes. Cancer Chemother Pharmacol 39:167-169.Google Scholar
  99. Szeimies RM, Karrer S, Abels C, Steinbach P, Fickweiler S, Messmann H, Baumler W, Landthaler M (1996) 9-Acetoxy-2,7,12,17-tetrakis-(beta-methoxyethyl)-porphycene (ATMPn), a novel pho-tosensitizer for photodynamic therapy: uptake kinetics and intracellular localization. J Photochem Photobiol B 34:67-72. Google Scholar
  100. Tabata Y, Murakami Y, Ikada Y (1997) Photodynamic effect of polyethylene glycol-modified fullerene on tumor. Jpn J Cancer Res 88:1108-1116. Google Scholar
  101. Tagmatarchis N, Shinohara H (2001) Fullerenes in medicinal chemistry and their biological appli-cations. Mini Rev Med Chem 1:339-348. Google Scholar
  102. Tegos GP, Demidova TN, Arcila-Lopez D, Lee H, Wharton T, Gali H, Hamblin MR (2005) Cationic fullerenes are effective and selective antimicrobial photosensitizers. Chem Biol 12:1127-1135. Google Scholar
  103. Tokuyama H, Yamago S, Nakamura E (1993) Photoinduced biochemical activity of fullerene carboxylic acid. J Am Chem Soc 115:7918-7919. Google Scholar
  104. Yamakoshi Y, Sueyoshi S, Miyata N (1999) Biological activity of photoexcited fullerene. Bull Natl Inst Health Sci 117:50-60. Google Scholar
  105. Yamakoshi Y, Umezawa N, Ryu A, Arakane K, Miyata N, Goda Y, Masumizu T, Nagano T (2003) Active oxygen species generated from photoexcited fullerene (C60) as potential medicines: O2-* versus 1O2. J Am Chem Soc 125:12803-12809. Google Scholar
  106. Yamakoshi YN, Yagami T, Sueyoshi S, Miyata N (1996) Acridine Adduct of [60]Fullerene with Enhanced DNA-Cleaving Activity. J Org Chem 61:7236-7237. Google Scholar
  107. Yang XL, Fan CH, Zhu HS (2002) Photo-induced cytotoxicity of malonic acid [C(60)]fullerene derivatives and its mechanism. Toxicol In Vitro 16:41-46. Google Scholar
  108. Yang XL, Huang C, Qiao XG, Yao L, Zhao DX, Tan X (2007) Photo-induced lipid peroxidation of erythrocyte membranes by a bis-methanophosphonate fullerene. Toxicol In Vitro 21(8):1493-1498. Google Scholar
  109. Yu C, Canteenwala T, Chen HH, Chen BJ, Canteenwala M, Chiang LY (1999) Hexa(sulfobutyl) fullerene-induced photodynamic effect on tumors in vivo and toxicity study in rats. Proc Electrochem Soc 99:234-249. Google Scholar
  110. Yu C, Canteenwala T, Chiang LY, Wilson BC, Pritzker K (2005a) Photodynamic effect of hydrophilic C60-derived nanostructures for catalytic antitumoral antibacterial applications. Synth Metals 153:37-40. Google Scholar
  111. Yu C, Canteenwala T, El-Khouly ME, Araki Y, Pritzker K, Ito O, Wilson BC, Chiang LY (2005b) Efficiency of singlet oxygen production from self-assembled nanospheres of molecular micelle-like photosensitizers FC4S. J Mater Chem 15:857-1864. Google Scholar
  112. Zakharian TY, Seryshev A, Sitharaman B, Gilbert BE, Knight V, Wilson LJ (2005) A fullerene-paclitaxel chemotherapeutic: synthesis, characterization, and study of biological activity in tissue culture. J Am Chem Soc 127:12508-12509.Google Scholar

Copyright information

© Springer Science + Business Media B.V 2008

Authors and Affiliations

  • Pawel Mroz
    • 1
    • 2
  • George P. Tegos
    • 1
    • 2
  • Hariprasad Gali
    • 3
  • Timothy Wharton
    • 3
  • Tadeusz Sarna
    • 4
  • Michael R. Hamblin
    • 1
    • 2
    • 5
  1. 1.Wellman Center for PhotomedicineMassachusetts General HospitalBostonUSA
  2. 2.Department of DermatologyHarvard Medical SchoolBostonUSA
  3. 3.Lynntech Inc.College StationUSA
  4. 4.Department of BiophysicsJagiellonian UniversityKrakowPoland
  5. 5.Harvard-MIT Division of Health Sciences and TechnologyCambridgeUSA

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