Aminolevulinic acid (ala) as a prodrug in photodynamic therapy of cancer

Molecules

Volumn 16, Issue 5, 2011, Pages 4140-4164

  Wachowska, Malgorzata ^a   Muchowicz, Angelika ^a   Firczuk, Malgorzata ^a   Gabrysiak, Magdalena ^a   Winiarska, Magdalena ^a   Wańczyk, Malgorzata ^a   Bojarczuk, Kamil ^a   Golab, Jakub ^a,b  

^a MEDICAL UNIVERSITY OF WARSAW   (Poland)

^b INSTITUTE OF PHYSICAL CHEMISTRY   (Poland)

Author keywords

5 Aminolevulinic acid; Cancer; Laser; Photodynamic therapy; Singlet oxygen

Indexed keywords

EID: 79957610304     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules16054140     Document Type: Review

References (149)

1. Castano, A.P.; Mroz, P.; Wu, M.X.; Hamblin, M.R. Photodynamic therapy plus low-dose cyclophosphamide generates antitumor immunity in a mouse model.Proc. Natl. Acad. Sci. USA 2008, 105, 5495-5500. (Pubitemid 351753891)
2. Dougherty, T.J.; Gomer, C.J.; Henderson, B.W.; Jori, G.; Kessel, D.; Korbelik, M.; Moan, J.; Peng, Q. Photodynamic therapy. J. Natl. Cancer Inst. 1998, 90, 889-905. (Pubitemid 28304157)
3. Firczuk, M.; Winiarska, M.; Szokalska, A.; Jodlowska, M.; Swiech, M.; Bojarczuk, K.; Salwa, P.; Nowis, D. Approaches to improve photodynamic therapy of cancer. Front Biosci. 2011, 16, 208-224.
4. Garg, A.D.; Nowis, D.; Golab, J.; Agostinis, P. Photodynamic therapy: Illuminating the road from cell death towards anti-tumour immunity. Apoptosis 2010, 15, 1050-1071.
5. Nowis, D.; Makowski, M.; Stoklosa, T.; Legat, M.; Issat, T.; Golab, J. Direct tumor damage mechanisms of photodynamic therapy. Acta Biochim. Pol. 2005, 52, 339-352. (Pubitemid 41133769)
6. Peng, Q.; Berg, K.; Moan, J.; Kongshaug, M.; Nesland, J.M. 5-Aminolevulinic acid-based photodynamic therapy: Principles and experimental research. Photochem. Photobiol. 1997, 65, 235-251. (Pubitemid 27158805)
7. Collaud, S.; Juzeniene, A.; Moan, J.; Lange, N. On the selectivity of 5-aminolevulinic acidinduced protoporphyrin IX formation. Curr. Med. Chem. Anticancer Agents 2004, 4, 301-316. (Pubitemid 38647588)
8. Kennedy, J.C.; Pottier, R.H.; Pross, D.C. Photodynamic therapy with endogenous protoporphyrin IX: Basic principles and present clinical experience.J. Photochem. Photobiol. B 1990, 6, 143-148.
9. Ajioka, R.S.; Phillips, J.D.; Kushner, J.P. Biosynthesis of heme in mammals. Biochim. Biophys. Acta 2006, 1763, 723-736. (Pubitemid 44189548)
10. Fukuda, H.; Casas, A.; Batlle, A. Aminolevulinic acid: From its unique biological function to its star role in photodynamic therapy. Int. J. Biochem. Cell. Biol. 2005, 37, 272-276. (Pubitemid 39330188)
11. Ishizuka, M.; Abe, F.; Sano, Y.; Takahashi, K.; Inoue, K.; Nakajima, M.; Kohda, T.; Komatsu, N.; Ogura, S.I.; Tanaka, T. Novel development of 5-aminolevurinic acid (ALA) in cancer diagnoses and therapy. Int. Immunopharmacol. 2011, 11, 358-365.
12. Riddle, R.D.; Yamamoto, M.; Engel, J.D. Expression of delta-aminolevulinate synthase in avian cells: Separate genes encode erythroid-specific and nonspecific isozymes. Proc. Natl. Acad. Sci. USA 1989, 86, 792-796. (Pubitemid 19056242)
13. Anderson, P.M.; Desnick, R.J. Purification and properties of delta-aminolevulinate dehydrase from human erythrocytes. J. Biol. Chem. 1979, 254, 6924-6930. (Pubitemid 9243546)
14. Jarret, C.; Stauffer, F.; Henz, M.E.; Marty, M.; Luond, R.M.; Bobalova, J.; Schurmann, P.; Neier, R. Inhibition of Escherichia coli porphobilinogen synthase using analogs of postulated intermediates. Chem. Biol. 2000, 7, 185-196. (Pubitemid 30147203)
15. Shoolingin-Jordan, P.M.; Al-Dbass, A.; McNeill, L.A.; Sarwar, M.; Butler, D. Human porphobilinogen deaminase mutations in the investigation of the mechanism of dipyrromethane cofactor assembly and tetrapyrrole formation. Biochem. Soc. Trans. 2003, 31, 731-735. (Pubitemid 36750768)
16. Jordan, P.M.; Seehra, J.S. The biosynthesis of uroporphyrinogen III: Order of assembly of the four porphobilinogen molecules in the formation of the tetrapyrrole ring. FEBS Lett. 1979, 104, 364-366. (Pubitemid 9243482)
17. Straka, J.G.; Kushner, J.P. Purification and characterization of bovine hepatic uroporphyrinogen decarboxylase. Biochemistry 1983, 22, 4664-4672. (Pubitemid 13016990)
18. Taketani, S.; Kohno, H.; Furukawa, T.; Tokunaga, R. Involvement of peripheral-type benzodiazepine receptors in the intracellular transport of heme and porphyrins. J. Biochem. 1995, 117, 875-880.
19. Taketani, S.; Kohno, H.; Okuda, M.; Furukawa, T.; Tokunaga, R. Induction of peripheral-type benzodiazepine receptors during differentiation of mouse erythroleukemia cells. A possible involvement of these receptors in heme biosynthesis. J. Biol. Chem. 1994, 269, 7527-7531.
20. Yoshinaga, T.; Sano, S. Coproporphyrinogen oxidase. II. Reaction mechanism and role of tyrosine residues on the activity. J. Biol. Chem. 1980, 255, 4727-4731.
21. Dailey, H.A. Terminal steps of haem biosynthesis. Biochem. Soc. Trans.2002, 30, 590-595. (Pubitemid 35001605)
22. Delfau-Larue, M.H.; Martasek, P.; Grandchamp, B. Coproporphyrinogen oxidase: Gene organization and description of a mutation leading to exon 6 skipping. Hum.Mol. Genet. 1994, 3, 1325-1330. (Pubitemid 24255466)
23. Grandchamp, B.; Phung, N.; Nordmann, Y. The mitochondrial localizationof coproporphyrinogen III oxidase. Biochem. J. 1978, 176, 97-102. (Pubitemid 9060515)
24. Dailey, T.A.; Dailey, H.A. Identification of an FAD superfamily containing protoporphyrinogen oxidases, monoamine oxidases, and phytoene desaturase. Expression and characterization of phytoene desaturase of Myxococcus xanthus. J. Biol. Chem. 1998, 273, 13658-13662. (Pubitemid 28268411)
25. Koch, M.; Breithaupt, C.; Kiefersauer, R.; Freigang, J.; Huber, R.; Messerschmidt, A. Crystal structure of protoporphyrinogen IX oxidase: A key enzyme in haem and chlorophyll biosynthesis. EMBO J. 2004, 23, 1720-1728. (Pubitemid 38649635)
26. Wu, C.K.; Dailey, H.A.; Rose, J.P.; Burden, A.; Sellers, V.M.; Wang, B.C. The 2.0 A structure of human ferrochelatase, the terminal enzyme of heme biosynthesis. Nat. Struct. Biol. 2001, 8, 156-160. (Pubitemid 32116069)
27. Maines, M.D. Heme oxygenase: Function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 1988, 2, 2557-2568.
28. Was, H.; Dulak, J.; Jozkowicz, A. Heme oxygenase-1 in tumor biology and therapy. Curr. Drug Targets 2010, 11, 1551-1570.
29. Docherty, J.C.; Firneisz, G.D.; Schacter, B.A. Methene bridge carbon atom elimination in oxidative heme degradation catalyzed by heme oxygenase and NADPH-cytochrome P-450 reductase. Arch. Biochem. Biophys. 1984, 235, 657-664.
30. Kutty, R.K.; Daniel, R.F.; Ryan, D.E.; Levin, W.; Maines, M.D. Rat liver cytochrome P-450b, P-420b, and P-420c are degraded to biliverdin by hemeoxygenase. Arch. Biochem. Biophys. 1988, 260, 638-644. (Pubitemid 18058312)
31. Yoshida, T.; Kikuchi, G. Features of the reaction of heme degradation catalyzed by the reconstituted microsomal heme oxygenase system. J. Biol. Chem. 1978, 253, 4230-4236. (Pubitemid 8380645)
32. Migita, C.T.; Matera, K.M.; Ikeda-Saito, M.; Olson, J.S.; Fujii, H.; Yoshimura, T.; Zhou, H.; Yoshida, T. The oxygen and carbon monoxide reactions of heme oxygenase. J. Biol. Chem. 1998, 273, 945-949. (Pubitemid 28049189)
33. Yoshida, T.; Kikuchi, G. Sequence of the reaction of heme catabolism catalyzed by the microsomal heme oxygenase system. FEBS Lett. 1974, 48, 256-261.
34. Tenhunen, R.; Ross, M.E.; Marver, H.S.; Schmid, R. Reduced nicotinamide-adenine dinucleotide phosphate dependent biliverdin reductase: Partial purification and characterization. Biochemistry 1970, 9, 298-303.
35. Munakata, H.; Sun, J.Y.; Yoshida, K.; Nakatani, T.; Honda, E.; Hayakawa, S.; Furuyama, K.; Hayashi, N. Role of the heme regulatory motif in the heme-mediated inhibition of mitochondrial import of 5-aminolevulinate synthase. J. Biochem. 2004, 136, 233-238. (Pubitemid 39264977)
36. Srivastava, G.; Borthwick, I.A.; Maguire, D.J.; Elferink, C.J.; Bawden, M.J.; Mercer, J.F.; May, B.K. Regulation of 5-aminolevulinate synthase mRNA in different rat tissues. J. Biol. Chem. 1988, 263, 5202-5209.
37. Surinya, K.H.; Cox, T.C.; May, B.K. Transcriptional regulation of the human erythroid 5-aminolevulinate synthase gene. Identification of promoterelements and role of regulatory proteins. J. Biol. Chem. 1997, 272, 26585-26594. (Pubitemid 27458881)
38. Hinnen, P.; de. Rooij, F.W.; van Velthuysen, M.L.; Edixhoven, A.; van Hillegersberg, R.; Tilanus, H.W.; Wilson, J.H.; Siersema, P.D. Biochemical basis of 5-aminolaevulinic acid-induced protoporphyrin IX accumulation: A study in patients with (pre)malignant lesions of the oesophagus. Br. J. Cancer 1998, 78, 679-682. (Pubitemid 28375603)
39. Krieg, R.C.; Fickweiler, S.; Wolfbeis, O.S.; Knuechel, R. Cell-type specific protoporphyrin IX metabolism in human bladder cancer in vitro. Photochem. Photobiol. 2000, 72, 226-233.
40. Hefti, M.; Holenstein, F.; Albert, I.; Looser, H.; Luginbuehl, V. Susceptibility to 5-aminolevulinic acid based photodynamic therapy in WHO I meningioma cells corresponds to ferrochelatase activity. Photochem. Photobiol. 2011, 87, 235-241.
41. Ohgari, Y.; Nakayasu, Y.; Kitajima, S.; Sawamoto, M.; Mori, H.; Shimokawa, O.; Matsui, H.; Taketani, S. Mechanisms involved in delta-aminolevulinic acid (ALA)-induced photosensitivity of tumor cells: Relation of ferrochelatase and uptake of ALA to the accumulation of protoporphyrin. Biochem. Pharmacol. 2005, 71, 42-49. (Pubitemid 41713525)
42. Stout, D.L.; Becker, F.F. Heme synthesis in normal mouse liver and mouse liver tumors. Cancer Res. 1990, 50, 2337-2340. (Pubitemid 20134491)
43. Navone, N.M.; Polo, C.F.; Frisardi, A.L.; Andrade, N.E.; Battle, A.M. Heme biosynthesis in human breast cancer-mimetic "in vitro" studies and some heme enzymic activity levels. Int. J. Biochem. 1990, 22, 1407-1411. (Pubitemid 20370322)
44. Kondo, M.; Hirota, N.; Takaoka, T.; Kajiwara, M. Heme-biosynthetic enzyme activities and porphyrin accumulation in normal liver and hepatoma celllines of rat. Cell. Biol. Toxicol. 1993, 9, 95-105. (Pubitemid 23135641)
45. Feuerstein, T.; Schauder, A.; Malik, Z. Silencing of ALA dehydratase affects ALA-photodynamic therapy efficacy in K562 erythroleukemic cells. Photochem. Photobiol. Sci. 2009, 8, 1461-1466.
46. Grinblat, B.; Pour, N.; Malik, Z. Regulation of porphyrin synthesis and photodynamic therapy in heavy metal intoxication. J. Environ. Pathol. Toxicol. Oncol. 2006, 25, 145-158. (Pubitemid 43341237)
47. Sinha, A.K.; Anand, S.; Ortel, B.J.; Chang, Y.; Mai, Z.; Hasan, T.; Maytin, E.V. Methotrexate used in combination with aminolaevulinic acid for photodynamic killing of prostate cancer cells. Br. J. Cancer 2006, 95, 485-495. (Pubitemid 44232558)
48. Fingar, V.H.; Wieman, T.J.; McMahon, K.S.; Haydon, P.S.; Halling, B.P.; Yuhas, D.A.; Winkelman, J.W. Photodynamic therapy using a protoporphyrinogen oxidase inhibitor. Cancer Res. 1997, 57, 4551-4556. (Pubitemid 27441060)
49. Miyake, M.; Ishii, M.; Kawashima, K.; Kodama, T.; Sugano, K.; Fujimoto, K.; Hirao, Y. siRNAmediated knockdown of the heme synthesis and degradation pathways: Modulation of treatment effect of 5-aminolevulinic acid-based photodynamic therapy in urothelial cancer cell lines. Photochem. Photobiol. 2009, 85, 1020-1027.
50. Amo, T.; Kawanishi, N.; Uchida, M.; Fujita, H.; Oyanagi, E.; Utsumi, T.; Ogino, T.; Inoue, K.; Shuin, T.; Utsumi, K.; Sasaki, J. Mechanism of cell death by 5-aminolevulinic acid-based photodynamic action and its enhancement by ferrochelatase inhibitors in human histiocytic lymphoma cell line U937. Cell Biochem. Funct. 2009, 27, 503-515.
51. Tan, W.C.; Krasner, N.; O'Toole, P.; Lombard, M. Enhancement of photodynamic therapy in gastric cancer cells by removal of iron. Gut 1997, 41, 14-18. (Pubitemid 27351633)
52. Blake, E.; Curnow, A. The hydroxypyridinone iron chelator CP94 can enhance PpIX-induced PDT of cultured human glioma cells. Photochem. Photobiol. 2010, 86, 1154-1160.
53. Loh, C.S.; MacRobert, A.J.; Bedwell, J.; Regula, J.; Krasner, N.; Bown, S.G. Oral versus intravenous administration of 5-aminolaevulinic acid for photodynamic therapy. Br. J. Cancer 1993, 68, 41-51. (Pubitemid 23178549)
54. Dalton, J.T.; Yates, C.R.; Yin, D.; Straughn, A.; Marcus, S.L.; Golub,A.L.; Meyer, M.C. Clinical pharmacokinetics of 5-aminolevulinic acid in healthy volunteers and patients at high risk for recurrent bladder cancer. J. Pharmacol. Exp. Ther. 2002, 301, 507-512. (Pubitemid 34429961)
55. Ackroyd, R.; Brown, N.; Vernon, D.; Roberts, D.; Stephenson, T.; Marcus, S.; Stoddard, C.; Reed, M. 5-Aminolevulinic acid photosensitization of dysplastic Barrett's esophagus: A pharmacokinetic study. Photochem. Photobiol. 1999, 70, 656-662. (Pubitemid 129555838)
56. Szeimies, R.M.; Sassy, T.; Landthaler, M. Penetration potency of topical applied deltaaminolevulinic acid for photodynamic therapy of basal cell carcinoma. Photochem. Photobiol. 1994, 59, 73-76. (Pubitemid 2043025)
57. Wennberg, A.M.; Larko, O.; Lonnroth, P.; Larson, G.; Krogstad, A.L. Delta-aminolevulinic acid in superficial basal cell carcinomas and normal skin-a microdialysis and perfusion study. Clin. Exp. Dermatol. 2000, 25, 317-322. (Pubitemid 30670591)
58. Ahmadi, S.; McCarron, P.A.; Donnelly, R.F.; Woolfson, A.D.; McKenna, K. Evaluation of the penetration of 5-aminolevulinic acid through basal cell carcinoma: A pilot study. Exp. Dermatol. 2004, 13, 445-451. (Pubitemid 39077312)
59. Rick, K.; Sroka, R.; Stepp, H.; Kriegmair, M.; Huber, R.M.; Jacob, K.;Baumgartner, R. Pharmacokinetics of 5-aminolevulinic acid-induced protoporphyrin IX in skin and blood. J. Photochem. Photobiol. B 1997, 40, 313-319. (Pubitemid 27478319)
60. Gerritsen, M.J.; Smits, T.; Kleinpenning, M.M.; van de Kerkhof, P.C.; van Erp, P.E. Pretreatment to enhance protoporphyrin IX accumulation in photodynamic therapy. Dermatology 2009, 218, 193-202.
61. Juzeniene, A.; Juzenas, P.; Kaalhus, O.; Iani, V.; Moan, J. Temperature effect on accumulation of protoporphyrin IX after topical application of 5-aminolevulinic acid and its methylester and hexylester derivatives in normal mouse skin. Photochem. Photobiol. 2002, 76, 452-456.
62. Juzeniene, A.; Juzenas, P.; Bronshtein, I.; Vorobey, A.; Moan, J. The influence of temperature on photodynamic cell killing in vitro with 5-aminolevulinic acid. J. Photochem. Photobiol. B 2006, 84, 161-166.
63. Wyld, L.; Reed, M.W.; Brown, N.J. The influence of hypoxia and pH on aminolaevulinic acidinduced photodynamic therapy in bladder cancer cells in vitro. Br. J. Cancer 1998, 77, 1621-1627. (Pubitemid 28230462)
64. Piot, B.; Rousset, N.; Lenz, P.; Eleouet, S.; Carre, J.; Vonarx, V.; Bourre, L.; Patrice, T. Enhancement of delta aminolevulinic acid-photodynamic therapy in vivo by decreasing tumor pH with glucose and amiloride. Laryngoscope 2001, 111, 2205-2213. (Pubitemid 33117227)
65. Bech, O.; Berg, K.; Moan, J. The pH dependency of protoporphyrin IX formation in cells incubated with 5-aminolevulinic acid. Cancer Lett. 1997, 113, 25-29. (Pubitemid 27113224)
66. Foster, T.H.; Murant, R.S.; Bryant, R.G.; Knox, R.S.; Gibson, S.L.; Hilf, R. Oxygen consumption and diffusion effects in photodynamic therapy. Radiat. Res. 1991, 126, 296-303.
67. Forster, B.; Klein, A.; Szeimies, R.M.; Maisch, T. Penetration enhancement of two topical 5-aminolaevulinic acid formulations for photodynamic therapy by erbium:YAG laser ablation of the stratum corneum: Continuous versus fractional ablation. Exp. Dermatol. 2010, 19, 806-812.
68. Fotinos, N.; Campo, M.A.; Popowycz, F.; Gurny, R.; Lange, N. 5-Aminolevulinic acid derivatives in photomedicine: Characteristics, application andperspectives. Photochem. Photobiol. 2006, 82, 994-1015. (Pubitemid 44450185)
69. Rodriguez, L.; de Bruijn, H.S.; Di Venosa, G.; Mamone, L.; Robinson, D.J.; Juarranz, A.; Batlle, A.; Casas, A. Porphyrin synthesis from aminolevulinic acid esters in endothelial cells and its role in photodynamic therapy. J. Photochem. Photobiol. B 2009, 96, 249-254.
70. Lee, J.B.; Choi, J.Y.; Chun, J.S.; Yun, S.J.; Lee, S.C.; Oh, J.; Park, H.R. Relationship of protoporphyrin IX synthesis to photodynamic effects by 5-aminolaevulinic acid and its esters on various cell lines derived from the skin. Br. J. Dermatol. 2008, 159, 61-67. (Pubitemid 351874495)
71. Pudroma, X.; Moan, J.; Ma, L.W.; Iani, V.; Juzeniene, A. A comparison of 5-aminolaevulinic acid- and its heptyl ester: Dark cytotoxicity and protoporphyrin IX synthesis in human adenocarcinoma WiDr cells and in athymic nude mice healthy skin. Exp. Dermatol. 2009, 18, 985-987.
72. Di Venosa, G.; Hermida, L.; Fukuda, H.; Defain, M.V.; Rodriguez, L.; Mamone, L.; MacRobert, A.; Casas, A.; Batlle, A. Comparation of liposomal formulations of ALA Undecanoyl ester for its use in photodynamic therapy. J. Photochem. Photobiol. B 2009, 96, 152-158.
73. Tunstall, R.G.; Barnett, A.A.; Schofield, J.; Griffiths, J.; Vernon, D.I.; Brown, S.B.; Roberts, D.J. Porphyrin accumulation induced by 5-aminolaevulinic acid esters in tumour cells growing in vitro and in vivo. Br. J. Cancer 2002, 87, 246-250.
74. Wakui, M.; Yokoyama, Y.; Wang, H.; Shigeto, T.; Futagami, M.; Mizunuma, H. Efficacy of amethyl ester of 5-aminolevulinic acid in photodynamic therapy for ovarian cancers. J. Cancer Res. Clin. Oncol. 2010, 136, 1143-1150.
75. Casas, A.; Perotti, C.; Saccoliti, M.; Sacca, P.; Fukuda, H.; Batlle, A.M. ALA and ALA hexyl ester in free and liposomal formulations for the photosensitisation of tumour organ cultures. Br. J. Cancer 2002, 86, 837-842. (Pubitemid 34250830)
76. Merclin, N.; Bender, J.; Sparr, E.; Guy, R.H.; Ehrsson, H.; Engstrom, S. Transdermal delivery from a lipid sponge phase-iontophoretic and passive transport in vitro of 5-aminolevulinic acid and its methyl ester. J. Control. Release 2004, 100, 191-198. (Pubitemid 39491271)
77. De Rosa, F.S.; Marchetti, J.M.; Thomazini, J.A.; Tedesco, A.C.; Bentley, M.V. A vehicle for photodynamic therapy of skin cancer: Influence of dimethylsulphoxide on 5-aminolevulinic acid in vitro cutaneous permeation and in vivo protoporphyrin IX accumulation determined by confocal microscopy. J. Control. Release 2000, 65, 359-366. (Pubitemid 30122938)
78. Oo, M.K.; Yang, X.; Du, H.; Wang, H. 5-aminolevulinic acid-conjugated gold nanoparticles for photodynamic therapy of cancer. Nanomedicine (Lond) 2008, 3, 777-786.
79. Yang, S.J.; Shieh, M.J.; Lin, F.H.; Lou, P.J.; Peng, C.L.; Wei, M.F.; Yao, C.J.; Lai, P.S.; Young, T.H. Colorectal cancer cell detection by 5-aminolaevulinic acid-loaded chitosan nano-particles. Cancer Lett. 2009, 273, 210-220.
80. Donnelly, R.F.; Ma, L.W.; Juzenas, P.; Iani, V.; McCarron, P.A.; Woolfson, A.D.; Moan, J. Topical bioadhesive patch systems enhance selectivity of protoporphyrin IX accumulation. Photochem. Photobiol. 2006, 82, 670-675. (Pubitemid 44032785)
81. Boyle, R.W.; Dolphin, D. Structure and biodistribution relationships of photodynamic sensitizers. Photochem. Photobiol. 1996, 64, 469-485. (Pubitemid 27039801)
82. Kessel, D.; Luo, Y.; Deng, Y.; Chang, C.K. The role of subcellular localization in initiation of apoptosis by photodynamic therapy. Photochem. Photobiol. 1997, 65, 422-426. (Pubitemid 27158974)
83. Warren, C.B.; Karai, L.J.; Vidimos, A.; Maytin, E.V. Pain associated with aminolevulinic acidphotodynamic therapy of skin disease. J. Am. Acad. Dermatol. 2009, 61, 1033-1043.
84. O'Connor, A.E.; Gallagher, W.M.; Byrne, A.T. Porphyrin and nonporphyrin photosensitizers in oncology: Preclinical and clinical advances in photodynamic therapy. Photochem. Photobiol. 2009, 85, 1053-1074.
85. Profio, A.E.; Doiron, D.R. Dosimetry considerations in phototherapy. Med. Phys. 1981, 8, 190-196. (Pubitemid 11156333)
86. Peng, Q.; Warloe, T.; Berg, K.; Moan, J.; Kongshaug, M.; Giercksky, K.E.; Nesland, J.M. 5-Aminolevulinic acid-based photodynamic therapy. Clinical research and future challenges. Cancer 1997, 79, 2282-2308.
87. Berlin, N.I.; Neuberger, A.; Scott, J.J. The metabolism of delta -aminolaevulic acid. 1. Normal pathways, studied with the aid of 15N. Biochem. J. 1956, 64, 80-90.
88. Malik, Z.; Djaldetti, M. 5-Aminolevulinic acid stimulation of porphyrin and hemoglobin synthesis by uninduced Friend erythroleukemic cells. Cell Differ. 1979, 8, 223-233. (Pubitemid 9217621)
89. Malik, Z.; Lugaci, H. Destruction of erythroleukaemic cells by photoactivation of endogenous porphyrins. Br. J. Cancer 1987, 56, 589-595. (Pubitemid 17165652)
90. Qian, P.; Evensen, J.F.; Rimington, C.; Moan, J. A comparison of different photosensitizing dyes with respect to uptake C3H-tumors and tissues of mice. Cancer Lett. 1987, 36, 1-10. (Pubitemid 17091064)
91. Kennedy, J.C.; Pottier, R.H. Endogenous protoporphyrin IX, a clinically useful photosensitizer for photodynamic therapy. J. Photochem. Photobiol. B 1992, 14, 275-292.
92. Van Hillegersberg, R.; Van den Berg, J.W.; Kort, W.J.; Terpstra, O.T.;Wilson, J.H. Selective accumulation of endogenously produced porphyrins ina liver metastasis model in rats. Gastroenterology 1992, 103, 647-651.
93. Bedwell, J.; MacRobert, A.J.; Phillips, D.; Bown, S.G. Fluorescence distribution and photodynamic effect of ALA-induced PP IX in the DMH rat colonic tumour model. Br. J. Cancer 1992, 65, 818-824.
94. Uekusa, M.; Omura, K.; Nakajima, Y.; Hasegawa, S.; Harada, H.; Morita,K.I.; Tsuda, H. Uptake and kinetics of 5-aminolevulinic acid in oral squamous cell carcinoma. Int. J. Oral. Maxillofac. Surg. 2010, 39, 802-805.
95. Inoue, K.; Karashima, T.; Kamada, M.; Shuin, T.; Kurabayashi, A.; Furihata, M.; Fujita, H.; Utsumi, K.; Sasaki, J. Regulation of 5-aminolevulinicacid-mediated protoporphyrin IX accumulation in human urothelial carcinomas. Pathobiology 2009, 76, 303-314.
96. Bergmann, F.; Stepp, H.; Metzger, R.; Rolle, U.; Johansson, A.; Till, H. In vitro and in vivo evaluation of photodynamic techniques for the experimental treatment of human hepatoblastoma and neuroblastoma: Preliminary results. Pediatr. Surg. Int. 2008, 24, 1331-1333.
97. Kruijt, B.; de Bruijn, H.S.; van der Ploeg-van den Heuvel, A.; de Bruin, R.W.; Sterenborg, H.J.; Amelink, A.; Robinson, D.J. Monitoring ALA-induced PpIX photodynamic therapy in the rat esophagus using fluorescence and reflectance spectroscopy. Photochem. Photobiol. 2008, 84, 1515-1527.
98. Boere, I.A.; Robinson, D.J.; de Bruijn, H.S.; Kluin, J.; Tilanus, H.W.; Sterenborg, H.J.; de Bruin, R.W. Protoporphyrin IX fluorescence photobleaching and the response of rat Barrett's esophagus following 5-aminolevulinic acid photodynamic therapy. Photochem. Photobiol. 2006, 82, 1638-1644. (Pubitemid 46158857)
99. Sheng, C.; Hoopes, P.J.; Hasan, T.; Pogue, B.W. Photobleaching-based dosimetry predicts deposited dose in ALA-PpIX PDT of rodent esophagus. Photochem. Photobiol. 2007, 83, 738-748. (Pubitemid 46854943)
100. Abels, C.; Heil, P.; Dellian, M.; Kuhnle, G.E.; Baumgartner, R.; Goetz, A.E. In vivo kinetics and spectra of 5-aminolaevulinic acid-induced fluorescence in an amelanotic melanoma of the hamster. Br. J. Cancer 1994, 70, 826-833. (Pubitemid 24331072)
101. Iinuma, S.; Bachor, R.; Flotte, T.; Hasan, T. Biodistribution and phototoxicity of 5-aminolevulinic acid-induced PpIX in an orthotopic rat bladder tumor model. J. Urol. 1995, 153, 802-806.
102. Yow, C.M.; Wong, C.K.; Huang, Z.; Ho, R.J. Study of the efficacy and mechanism of ALAmediated photodynamic therapy on human hepatocellular carcinoma cell. Liver Int. 2007, 27, 201-208. (Pubitemid 46680723)
103. Manivasager, V.; Heng, P.W.; Hao, J.; Zheng, W.; Soo, K.C.; Olivo, M. Macro-microscopic fluorescence imaging of human NPC xenografts in a murine model using topical vs intravenous administration of 5-aminolevulinic acid. Int. J. Oncol. 2002, 21, 1003-1007.
104. Murayama, Y.; Harada, Y.; Imaizumi, K.; Dai, P.; Nakano, K.; Okamoto, K.; Otsuji, E.; Takamatsu, T. Precise detection of lymph node metastases in mouse rectal cancer by using 5-aminolevulinic acid. Int. J. Cancer 2009, 125, 2256-2263.
105. Gronlund-Pakkanen, S.; Wahlfors, J.; Talja, M.; Kosma, V.M.; Pakkanen, T.M.; Ala-Opas, M.; Alhava, E.; Moore, R.B. The effect of photodynamic therapy on rat urinary bladder with orthotopic urothelial carcinoma. BJU Int. 2003, 92, 125-130. (Pubitemid 36843042)
106. Angell-Petersen, E.; Spetalen, S.; Madsen, S.J.; Sun, C.H.; Peng, Q.; Carper, S.W.; Sioud, M.;vHirschberg, H. Influence of light fluence rate on the effects of photodynamic therapy in an orthotopic rat glioma model. J. Neurosurg. 2006, 104, 109-117.
107. Grebenova, D.; Halada, P.; Stulik, J.; Havlicek, V.; Hrkal, Z. Protein changes in HL60 leukemia vcells associated with 5-aminolevulinic acid-based photodynamic therapy. Early effects on endoplasmic reticulum chaperones. Photochem. Photobiol. 2000, 72, 16-22.
108. Inoue, H.; Kajimoto, Y.; Shibata, M.A.; Miyoshi, N.; Ogawa, N.; Miyatake, S.; Otsuki, Y.; Kuroiwa, T. Massive apoptotic cell death of human glioma cells via a mitochondrial pathway following 5-aminolevulinic acid-mediated photodynamic therapy. J. Neurooncol. 2007, 83, 223-231. (Pubitemid 46952232)
109. Kuzelova, K.; Grebenova, D.; Pluskalova, M.; Marinov, I.; Hrkal, Z. Early apoptotic features of K562 cell death induced by 5-aminolaevulinic acid-based photodynamic therapy. J. Photochem. Photobiol. B 2004, 73, 67-78. (Pubitemid 38145769)
110. Ji, H.T.; Chien, L.T.; Lin, Y.H.; Chien, H.F.; Chen, C.T. 5-ALA mediated photodynamic therapy induces autophagic cell death via AMP-activated protein kinase. Mol. Cancer 2010, 9, 91.
111. Christensen, E.; Skogvoll, E.; Viset, T.; Warloe, T.; Sundstrom, S. Photodynamic therapy with 5-aminolaevulinic acid, dimethylsulfoxide and curettage in basal cell carcinoma: A 6-year clinical and histological follow-up. J. Eur. Acad. Dermatol. Venereol. 2009, 23, 58-66.
112. Kotimaki, J. Photodynamic therapy of eyelid basal cell carcinoma. J. Eur. Acad. Dermatol. Venereol. 2009, 23, 1083-1087.
113. Apalla, Z.; Sotiriou, E.; Chovarda, E.; Lefaki, I.; Devliotou- Panagiotidou, D.; Ioannides, D. Skin cancer: Preventive photodynamic therapy in patients with face and scalp cancerization. A randomized placebo-controlled study. Br. J. Dermatol. 2010, 162, 171-175.
114. Souza, C.S.; Felicio, L.B.; Ferreira, J.; Kurachi, C.; Bentley, M.V.; Tedesco, A.C.; Bagnato, V.S. Long-term follow-up of topical 5-aminolaevulinic acid photodynamic therapy diode laser single session for non-melanoma skin cancer. Photodiagnosis Photodyn. Ther. 2009, 6, 207-213.
115. Coors, E.A.; von den Driesch, P. Topical photodynamic therapy for patients with therapyresistant lesions of cutaneous T-cell lymphoma. J. Am. Acad. Dermatol. 2004, 50, 363-367. (Pubitemid 38316128)
116. Morton, C.A.; Whitehurst, C.; Moseley, H.; McColl, J.H.; Moore, J.V.;Mackie, R.M. Comparison of photodynamic therapy with cryotherapy in the treatment of Bowen's disease. Br. J. Dermatol. 1996, 135, 766-771. (Pubitemid 26375895)
117. Piacquadio, D.J.; Chen, D.M.; Farber, H.F.; Fowler, J.F., Jr.; Glazer, S.D.; Goodman, J.J.; Hruza, L.L.; Jeffes, E.W.; Ling, M.R.; Phillips, T.J.; Rallis, T.M.; Scher, R.K.; Taylor, C.R.; Weinstein, G.D. Photodynamic therapy with aminolevulinic acid topical solution and vi ible blue light in the treatment of multiple actinic keratoses of the face and scalp: Investigator-blinded, phase 3, multicenter trials. Arch. Dermatol. 2004, 140, 41-46. (Pubitemid 38090269)
118. Tschen, E.H.; Wong, D.S.; Pariser, D.M.; Dunlap, F.E.; Houlihan, A.; Ferdon, M.B. Photodynamic therapy using aminolaevulinic acid for patients with nonhyperkeratotic actinic keratoses of the face and scalp: Phase IV multicentre clinical trial with 12-month follow up. Br. J. Dermatol. 2006, 155, 1262-1269. (Pubitemid 44730005)
119. Grant, W.E.; Hopper, C.; MacRobert, A.J.; Speight, P.M.; Bown, S.G. Photodynamic therapy of oral cancer: Photosensitisation with systemic aminolaevulinic acid. Lancet 1993, 342, 147-148. (Pubitemid 23200442)
120. Fan, K.F.; Hopper, C.; Speight, P.M.; Buonaccorsi, G.; MacRobert, A.J.; Bown, S.G. Photodynamic therapy using 5-aminolevulinic acid for premalignant and malignant lesions of the oral cavity. Cancer 1996, 78, 1374-1383. (Pubitemid 26317856)
121. Chen, H.M.; Chen, C.T.; Yang, H.; Kuo, M.Y.; Kuo, Y.S.; Lan, W.H.; Wang, Y.P.; Tsai, T.; Chiang, C.P. Successful treatment of oral verrucous hyperplasia with topical 5-aminolevulinic acid-mediated photodynamic therapy. Oral Oncol. 2004, 40, 630-637. (Pubitemid 38452683)
122. Sieron, A.; Namyslowski, G.; Misiolek, M.; Adamek, M.; Kawczyk-Krupka, A. Photodynamic therapy of premalignant lesions and local recurrence of laryngeal and hypopharyngeal cancers. Eur. Arch. Otorhinolaryngol. 2001, 258, 349-352.
123. Barr, H.; Dix, A.J.; Kendall, C.; Stone, N. Review article: The potential role for photodynamic therapy in the management of upper gastrointestinal disease. Aliment. Pharmacol. Ther. 2001, 15, 311-321. (Pubitemid 32187553)
124. Tan, W.C.; Fulljames, C.; Stone, N.; Dix, A.J.; Shepherd, N.; Roberts, D.J.; Brown, S.B.; Krasner, N.; Barr, H. Photodynamic therapy using 5-aminolaevulinic acid for oesophageal adenocarcinoma associated with Barrett's metaplasia. J. Photochem. Photobiol. B 1999, 53, 75-80. (Pubitemid 30047589)
125. Peters, F.P.; Kara, M.A.; Rosmolen, W.D.; Aalders, M.C.; Ten Kate, F.J.; Bultje, B.C.; Krishnadath, K.K.; Fockens, P.; van Lanschot, J.J.; van Deventer, S.J.; Bergman, J.J. Endoscopic treatment of high-grade dysplasia and early stage cancer in Barrett's esophagus. Gastrointest. Endosc. 2005, 61, 506-514 (Pubitemid 40462188)
126. Fritsch, C.; Homey, B.; Stahl, W.; Lehmann, P.; Ruzicka, T.; Sies, H. Preferential relative porphyrin enrichment in solar keratoses upon topical application of delta-aminolevulinic acid methylester. Photochem. Photobiol. 1998, 68, 218-221. (Pubitemid 128472013)
127. Moloney, F.J.; Collins, P. Randomized, double-blind, prospective study to compare topical 5-aminolaevulinic acid methylester with topical 5-aminolaevulinic acid photodynamic therapy for extensive scalp actinic keratosis. Br. J. Dermatol. 2007, 157, 87-91. (Pubitemid 46934264)
128. Valentine, R.M.; Ibbotson, S.H.; Brown, C.T.; Wood, K.; Moseley, H. A quantitative comparison of 5-aminolaevulinic acid- and methyl aminolevulinate-induced fluorescence, photobleaching and pain during photodynamic therapy. Photochem. Photobiol. 2011, 87, 242-249.
129. Tarstedt, M.; Rosdahl, I.; Berne, B.; Svanberg, K.; Wennberg, A.M. A randomized multicenter study to compare two treatment regimens of topical methyl aminolevulinate (Metvix)-PDT in actinic keratosis of the face and scalp. Acta Derm. Venereol. 2005, 85, 424-428. (Pubitemid 41345617)
130. Freeman, M.; Vinciullo, C.; Francis, D.; Spelman, L.; Nguyen, R.; Fergin, P.; Thai, K.E.; Murrell, D.; Weightman, W.; Anderson, C.; Reid, C.; Watson, A.; Foley, P. A comparison of photodynamic therapy using topical methyl aminolevulinate (Metvix) with single cycle cryotherapy in patients with actinic keratosis: A prospective, randomized study. J. Dermatolog Treat. 2003, 14, 99-106. (Pubitemid 36648700)
131. Morton, C.; Campbell, S.; Gupta, G.; Keohane, S.; Lear, J.; Zaki, I.; Walton, S.; Kerrouche, N.; Thomas, G.; Soto, P. Intraindividual, right-left comparison of topical methyl aminolaevulinatephotodynamic therapy and cryotherapy in subjects with actinic keratoses: A multicentre, randomized controlled study. Br. J. Dermatol. 2006, 155, 1029-1036. (Pubitemid 44564515)
132. Fantini, F.; Greco, A.; Del Giovane, C.; Cesinaro, A.; Venturini, M.; Zane, C.; Surrenti, T.; Peris, K.; Calzavara-Pinton, P. Photodynamic therapy for basal cell carcinoma: Clinical and pathological determinants of response. J. Eur. Acad. Dermatol. Venereol. 2010, in press.
133. Foley, P.; Freeman, M.; Menter, A.; Siller, G.; El-Azhary, R.A.; Gebauer, K.; Lowe, N.J.; Jarratt, M.T.; Murrell, D.F.; Rich, P.; Pariser, D.M.; Oseroff, A.R.; Barnetson, R.; Anderson, C.; Kossard, S.; Gibson, L.E.; Tope, W.D. Photodynamic therapy with methyl aminolevulinate for primary nodular basal cell carcinoma: Results of two randomized studies. Int. J. Dermatol. 2009, 48, 1236-1245.
134. Vinciullo, C.; Elliott, T.; Francis, D.; Gebauer, K.; Spelman, L.; Nguyen, R.; Weightman, W.; Sheridan, A.; Reid, C.; Czarnecki, D.; Murrell, D. Photodynamic therapy with topical methyl aminolaevulinate for 'difficult-to-treat' basal cell carcinoma. Br. J. Dermatol. 2005, 152, 765-772. (Pubitemid 40571312)
135. Zane, C.; Venturini, M.; Sala, R.; Calzavara-Pinton, P. Photodynamic therapy with methylaminolevulinate as a valuable treatment option for unilesional cutaneous T-cell lymphoma. Photodermatol. Photoimmunol. Photomed. 2006, 22, 254-258. (Pubitemid 44317159)
136. Dognitz, N.; Salomon, D.; Zellweger, M.; Ballini, J.P.; Gabrecht, T.; Lange, N.; van den Bergh, H.; Wagnieres, G. Comparison of ALA- and ALA hexyl-ester-induced PpIX depth distribution in human skin carcinoma. J. Photochem. Photobiol. B 2008, 93, 140-148.
137. Christensen, E.; Warloe, T.; Kroon, S.; Funk, J.; Helsing, P.; Soler,
138. Makowski, M.; Grzela, T.; Niderla, J.; M, L.A.; Mroz, P.; Kopee, M.; Legat, M.; Strusinska, K.; Koziak, K.; Nowis, D.; Mrowka, P.; Wasik, M.; Jakobisiak, M.; Golab, J. Inhibition of cyclooxygenase-2 indirectly potentiates antitumor effects of photodynamic therapy in mice. Clin. Cancer Res. 2003, 9, 5417-5422. (Pubitemid 37413598)
139. Hsieh, Y.J.; Wu, C.C.; Chang, C.J.; Yu, J.S. Subcellular localization of Photofrin determines the death phenotype of human epidermoid carcinoma A431 cells triggered by photodynamic therapy: When plasma membranes are the main targets. J. Cell. Physiol. 2003, 194, 363-375.
140. Korbelik, M.; Dougherty, G.J. Photodynamic therapy-mediated immune response against subcutaneous mouse tumors. Cancer Res. 1999, 59, 1941-1946. (Pubitemid 29186169)
141. Ji, Z.; Yang, G.; Vasovic, V.; Cunderlikova, B.; Suo, Z.; Nesland, J.M.; Peng, Q. Subcellular localization pattern of protoporphyrin IX is an important determinant for its photodynamic efficiency of human carcinoma and normal cell lines. J. Photochem. Photobiol. B 2006, 84, 213-220. (Pubitemid 44184915)
142. Obwegeser, A.; Jakober, R.; Kostron, H. Uptake and kinetics of 14C-labelled metatetrahydroxyphenylchlorin and 5-aminolaevulinic acid in the C6 rat glioma model. Br. J. Cancer 1998, 78, 733-738. (Pubitemid 28418304)
143. Woodburn, K.W.; Fan, Q.; Miles, D.R.; Kessel, D.; Luo, Y.; Young, S.W. Localization and efficacy analysis of the phototherapeutic lutetium texaphyrin (PCI-0123) in the murine EMT6 sarcoma model. Photochem. Photobiol. 1997, 65, 410-415. (Pubitemid 27158972)
144. Stockert, J.C.; Canete, M.; Juarranz, A.; Villanueva, A.; Horobin, R.W.; Borrell, J.I.; Teixido, J.; Nonell, S. Porphycenes: Facts and prospects in photodynamic therapy of cancer. Curr. Med. Chem. 2007, 14, 997-1026. (Pubitemid 46672636)
145. Kaplan, M.J.; Somers, R.G.; Greenberg, R.H.; Ackler, J. Photodynamic therapy in the management of metastatic cutaneous adenocarcinomas: Case reports from phase 1/2 studies using tin ethyl etiopurpurin (SnET2). J. Surg. Oncol. 1998, 67, 121-125. (Pubitemid 28109978)
146. Mang, T.S.; Allison, R.; Hewson, G.; Snider, W.; Moskowitz, R. A phase II/III clinical study of tin ethyl etiopurpurin (Purlytin)-induced photodynamic therapy for the treatment of recurrent cutaneous metastatic breast cancer. Cancer. J. Sci. Am. 1998, 4, 378-384.
147. Taber, S.W.; Fingar, V.H.; Coots, C.T.; Wieman, T.J. Photodynamic therapy using mono-Laspartyl chlorin e6 (Npe6) for the treatment of cutaneous disease: A Phase I clinical study. Clin. Cancer Res. 1998, 4, 2741-2746. (Pubitemid 28523500)
148. Lee, T.K.; Baron, E.D.; Foster, T.H. Monitoring Pc 4 photodynamic therapy in clinical trials of cutaneous T-cell lymphoma using noninvasive spectroscopy. J. Biomed. Opt. 2008, 13, 030507.
149. Borodoker, N.; Spaide, R.F.; Maranan, L.; Murray, J.; Freund, K.B.; Slakter, J.S.; Sorenson, J.A.; Yannuzzi, L.A.; Guyer, D.R.; Fisher, Y.L. Verteporfin infusion-associated pain. Am. J. Ophthalmol. 2002, 133, 211-214. (Pubitemid 34072049)