Intracellular signaling mechanisms in photodynamic therapy

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1704, Issue 2, 2004, Pages 59-86

  Almeida, Ramiro D ^a   Manadas, Bruno J ^a   Carvalho, Arsélio P ^a   Duarte, Carlos B ^a  

^a UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

5 aminolevulinate; AIF; ALA; AlPc; AlPcS 4; AlPcS2; Apoptosis; apoptosis inducing factor; bisulfonated aluminum phthalocyanine; Calcium; chloroaluminum phthalocyanine; Necrosis; Phosphorylation; Photodynamic therapy

Indexed keywords

ARACHIDONIC ACID; CALCIUM ION; CERAMIDE; CLUSTERIN; CYCLIC AMP; CYCLIC GMP; CYCLIN DEPENDENT KINASE; CYTOKINE; GLUCOSE REGULATED PROTEIN; HEAT SHOCK PROTEIN; HEME OXYGENASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPID; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXYGEN; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE PHOSPHODIESTERASE; PHOSPHOLIPASE; PHOSPHOLIPASE A2; PHOTOFRIN; PHOTOSENSITIZING AGENT; PROTEIN P53; PROTEIN TYROSINE KINASE; RETINOBLASTOMA PROTEIN; TEMOPORFIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR E2F; UNINDEXED DRUG;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; CELL DEATH; CONCENTRATION (PARAMETERS); CYTOSOL; DRUG EFFICACY; ENZYME ACTIVATION; GENE EXPRESSION; GENOTYPE; HOMEOSTASIS; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIGHT; LIPID METABOLISM; METABOLISM; METABOLITE; MITOCHONDRION; MOLECULE; NONHUMAN; PHOTODYNAMIC THERAPY; PHOTOSENSITIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RADIATION DOSE; REVIEW; SIGNAL TRANSDUCTION; STIMULATION; TUMOR CELL;

APOPTOSIS; CALCIUM; CYCLIC AMP; HOMEOSTASIS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NECROSIS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PHOTOCHEMOTHERAPY; PROTEINS; SIGNAL TRANSDUCTION;

EID: 4444265338     PISSN: 0304419X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbcan.2004.05.003     Document Type: Review

References (295)

1. Takahashi H., Itoh Y., Miyauchi Y., Nakajima S., Sakata I., Ishida-Yamamoto A., Iizuka H. Activation of two caspase cascades, caspase 8/3/6 and caspase 9/3/6, during photodynamic therapy using a novel photosensitizer, ATX-S10(Na), in normal human keratinocytes. Arch. Dermatol. Res. 295:2003;242-248
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. 90:1998;889-905
3. Ackroyd R., Kelty C., Brown N., Reed M. The history of photodetection and photodynamic therapy. Photochem. Photobiol. 74:2001;656-669
4. Dougherty T.J. An update on photodynamic therapy applications. J. Clin. Laser Med. Surg. 20:2002;3-7
5. Gomer C.J. Preclinical examination of first and second generation photosensitizers used in photodynamic therapy. Photochem. Photobiol. 54:1991;1093-1107
6. Jori G. Tumour photosensitizers: approaches to enhance the selectivity and efficiency of photodynamic therapy. J. Photochem. Photobiol., B. 36:1996;87-93
7. MacDonald I.J., Dougherty T.J. Basic principles of photodynamic therapy. J. Porphyr. Phthalocyanines. 5:2001;105-129
8. Reynolds T. Photodynamic therapy expands its horizons. J. Natl. Cancer Inst. 89:1997;112-114
9. Hunt D.W., Chan A.H. Influence of photodynamic therapy on immunological aspects of disease - an update. Expert Opin. Investig. Drugs. 9:2000;807-817
10. Rosenthal I., Ben-Hur E. Role of oxygen in the phototoxicity of phthalocyanines. Int. J. Radiat. Biol. 67:1995;85-91
11. Moan J., Berg K. The photodegradation of porphyrins in cells can be used to estimate the lifetime of singlet oxygen. Photochem. Photobiol. 53:1991;549-553
12. Peng Q., Moan J., Nesland J.M. Correlation of subcellular and intratumoral photosensitizer localization with ultrastructural features after photodynamic therapy. Ultrastruct. Pathol. 20:1996;109-129
13. Luo Y., Chang C.K., Kessel D. Rapid initiation of apoptosis by photodynamic therapy. Photochem. Photobiol. 63:1996;528-534
14. Noodt B.B., Berg K., Stokke T., Peng Q., Nesland J.M. Different apoptotic pathways are induced from various intracellular sites by tetraphenylporphyrins and light. Br. J. Cancer. 79:1999;72-81
15. 6 conjugates. Photochem. Photobiol. 77:2003;645-652
16. Kessel D., Luguya R., Vicente M.G. Localization and photodynamic efficacy of two cationic porphyrins varying in charge distribution. Photochem. Photobiol. 78:2003;431-435
17. Feofanov A., Sharonov G., Grichine A., Karmakova T., Pljutinskaya A., Lebedeva V., Ruziyev R., Yakubovskaya R., Mironov A., Refregier M., Maurizot J.C., Vigny P. Comparative study of photodynamic properties of 13,15-N-cycloimide derivatives of chlorin p6. Photochem. Photobiol. 79:2004;172-188
18. Luo Y., Kessel D. Initiation of apoptosis versus necrosis by photodynamic therapy with chloroaluminum phthalocyanine. Photochem. Photobiol. 66:1997;479-483
19. Ben-Hur E., Oetjen J., Horowitz B. Silicon phthalocyanine Pc 4 and red light causes apoptosis in HIV-infected cells. Photochem. Photobiol. 65:1997;456-460
20. Vantieghem A., Assefa Z., Vandenabeele P., Declercq W., Courtois S., Vandenheede J.R., Merlevede W., de Witte P., Agostinis P. Hypericin-induced photosensitization of HeLa cells leads to apoptosis or necrosis. Involvement of cytochrome c and procaspase-3 activation in the mechanism of apoptosis. FEBS Lett. 440:1998;19-24
21. Zhuang S., Lynch M.C., Kochevar I.E. Caspase-8 mediates caspase-3 activation and cytochrome c release during singlet oxygen-induced apoptosis of HL-60 cells. Exp. Cell Res. 250:1999;203-212
22. Hajri A., Coffy S., Vallat F., Evrard S., Marescaux J., Aprahamian M. Human pancreatic carcinoma cells are sensitive to photodynamic therapy in vitro and in vivo. Br. J. Surg. 86:1999;899-906
23. Kamuhabwa A.R., Agostinis P.M., D'Hallewin M.A., Baert L., de Witte P.A. Cellular photodestruction induced by hypericin in AY-27 rat bladder carcinoma cells. Photochem. Photobiol. 74:2001;126-132
24. Wyld L., Reed M.W., Brown N.J. Differential cell death response to photodynamic therapy is dependent on dose and cell type. Br. J. Cancer. 84:2001;1384-1386
25. Ali S.M., Olivo M. Bio-distribution and subcellular localization of Hypericin and its role in PDT induced apoptosis in cancer cells. Int. J. Oncol. 21:2002;531-540
26. Jiang H., Granville D.J., North J.R., Richter A.M., Hunt D.W. Selective action of the photosensitizer QLT0074 on activated human T lymphocytes. Photochem. Photobiol. 76:2002;224-231
27. 4-PDT. Photochem. Photobiol. Sci. 1:2002;172-177
28. Tsai T., Hong R.L., Tsai J.C., Lou P.J., Ling I.F., Chen C.T. Effect of 5-aminolevulinic acid-mediated photodynamic therapy on MCF-7 and MCF-7/ADR cells. Lasers Surg. Med. 34:2004;62-72
29. Leist M., Nicotera P. The shape of cell death. Biochem. Biophys. Res. Commun. 236:1997;1-9
30. Hengartner M.O. The biochemistry of apoptosis. Nature. 407:2000;770-776
31. Green D.R., Evan G.I. A matter of life and death. Cancer Cell. 1:2002;19-30
32. Lawen A. Apoptosis - an introduction. Bioessays. 25:2003;888-896
33. Wallach D., Varfolomeev E.E., Malinin N.L., Goltsev Y.V., Kovalenko A.V., Boldin M.P. Tumor necrosis factor receptor and Fas signaling mechanisms. Annu. Rev. Immunol. 17:1999;331-367
34. Liu X., Kim C.N., Yang J., Jemmerson R., Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 86:1996;147-157
35. Zou H., Li Y., Liu X., Wang X. An APAF-1·cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 274:1999;11549-11556
36. Lauber K., Appel H.A., Schlosser S.F., Gregor M., Schulze-Osthoff K., Wesselborg S. The adapter protein apoptotic protease-activating factor-1 (Apaf-1) is proteolytically processed during apoptosis. J. Biol. Chem. 276:2001;29772-29781
37. Adams J.M., Cory S. Apoptosomes: engines for caspase activation. Curr. Opin. Cell Biol. 14:2002;715-720
38. Krieser R.J., White K. Engulfment mechanism of apoptotic cells. Curr. Opin. Cell Biol. 14:2002;734-738
39. Ahmad N., Gupta S., Feyes D.K., Mukhtar H. Involvement of Fas (APO-1/CD-95) during photodynamic-therapy-mediated apoptosis in human epidermoid carcinoma A431cells. J. Invest. Dermatol. 115:2000;1041-1046
40. Ali S.M., Chee S.K., Yuen G.Y., Olivo M. Photodynamic therapy induced Fas-mediated apoptosis in human carcinoma cells. Int. J. Mol. Med. 9:2002;257-270
41. Yokota T., Ikeda H., Inokuchi T., Sano K., Koji T. Enhanced cell death in NR-S1 tumor by photodynamic therapy: possible involvement of Fas and Fas ligand system. Lasers Surg. Med. 26:2000;449-460
42. Dahle J., Kaalhus O., Moan J., Steen H.B. Cooperative effects of photodynamic treatment of cells in microcolonies. Proc. Natl. Acad. Sci. U. S. A. 94:1997;1773-1778
43. Tan K.H., Hunziker W. Compartmentalization of Fas and Fas ligand may prevent auto-or paracrine apoptosis in epithelial cells. Exp. Cell Res. 284:2003;283-290
44. Zhuang S., Demirs J.T., Kochevar I.E. p38 Mitogen-activated protein kinase mediates Bid cleavage, mitochondrial dysfunction, and caspase-3 activation during apoptosis induced by singlet oxygen but not by hydrogen peroxide. J. Biol. Chem. 275:2000;25939-25948
45. Antonsson B., Martinou J.C. The Bcl-2 protein family. Exp. Cell Res. 256:2000;50-57
46. Harris M.H., Thompson C.B. The role of the Bcl-2 family in the regulation of outer mitochondrial membrane permeability. Cell Death Differ. 7:2000;1182-1191
47. Cory S., Adams J.M. The Bcl2 family: regulators of the cellular life-or-death switch. Nat. Rev. Cancer. 2:2002;647-656
48. Zhuang S., Kochevar I.E. Ultraviolet A radiation induces rapid apoptosis of human leukemia cells by Fas ligand-independent activation of the Fas death pathways. Photochem. Photobiol. 78:2003;61-67
49. Nagy B., Yeh W.C., Mak T.W., Chiu S.M., Separovic D. FADD null mouse embryonic fibroblasts undergo apoptosis after photosensitization with the silicon phthalocyanine Pc 4. Arch. Biochem. Biophys. 385:2001;194-202
50. Murant R.S., Gibson S.L., Hilf R. Photosensitizing effects of Photofrin II on the site selected mitochondrial enzymes adenylate kinase and monoamine oxidase. Cancer Res. 47:1987;4323-4328
51. Woodburn K.W., Vardaxis N.J., Hill J.S., Kaye A.H., Phillips D.R. Subcellular localization of porphyrins using confocal laser scanning microscopy. Photochem. Photobiol. 54:1991;725-732
52. Ricchelli F., Gobbo S., Jori G., Salet C., Moreno G. Temperature-induced changes in fluorescence properties as a probe of porphyrin microenvironment in lipid membranes: 2. The partition of hematoporphyrin and protoporphyrin in mitochondria. Eur. J. Biochem. 233:1995;165-170
53. Szeimies R.M., Karrer S., Abels C., Steinbach P., Fickweiler S., Messmann H., Baumler W., Landthaler M. 9-Acetoxy-2,7,12,17-tetrakis-(beta-methoxyethyl)- porphycene (ATMPn), a novel photosensitizer for photodynamic therapy: uptake kinetics and intracellular localization. J. Photochem. Photobiol., B. 34:1996;67-72
54. Lam M., Oleinick N.L., Nieminen A.L. Photodynamic therapy-induced apoptosis in epidermoid carcinoma cells. Reactive oxygen species and mitochondrial inner membrane permeabilization. J. Biol. Chem. 276:2001;47379-47386
55. Usuda J., Chiu S.M., Murphy E.S., Lam M., Nieminen A.L., Oleinick N.L. Domain dependent photodamage to Bcl-2. A membrane anchorage region is needed to form the target of phthalocyanine photosensitization. J. Biol. Chem. 278:2003;2021-2029
56. Graham A., Li G., Chen Y., Morgan J., Oseroff A., Dougherty T.J., Pandey R.K. Structure-activity relationship of new octaethylporphyrin-based benzochlorins as photosensitizers for photodynamic therapy. Photochem. Photobiol. 77:2003;561-566
57. Newmeyer D.D., Ferguson-Miller S. Mitochondria: releasing power for life and unleashing the machineries of death. Cell. 112:2003;481-490
58. Kessel D., Luo Y., Deng Y., Chang C.K. The role of subcellular localization in initiation of apoptosis by photodynamic therapy. Photochem. Photobiol. 65:1997;422-426
59. Kessel D., Castelli M. Evidence that bcl-2 is the target of three photosensitizers that induce a rapid apoptotic response. Photochem. Photobiol. 74:2001;318-322
60. Reiners J.J. Jr., Caruso J.A., Mathieu P., Chelladurai B., Yin X.M., Kessel D. Release of cytochrome c and activation of pro-caspase-9 following lysosomal photo damage involves Bid cleavage. Cell Death Differ. 9:2002;934-944
61. Teiten M.H., Marchal S., D'Hallewin M.A., Guillemin F., Bezdetnaya L. Primary photodamage sites and mitochondrial events after Foscan photosensitization of MCF-7 human breast cancer cells. Photochem. Photobiol. 78:2003;9-14
62. Teiten M.H., Bezdetnaya L., Morliere P., Santus R., Guillemin F. Endoplasmic reticulum and Golgi apparatus are the preferential sites of Foscan localisation in cultured tumour cells. Br. J. Cancer. 88:2003;146-152
63. Inanami O., Yoshito A., Takahashi K., Hiraoka W., Kuwabara M. Effects of BAPTA-AM and forskolin on apoptosis and cytochrome c release in photosensitized Chinese hamster V79 cells. Photochem. Photobiol. 70:1999;650-655
64. Varnes M.E., Chiu S.M., Xue L.Y., Oleinick N.L. Photodynamic therapy-induced apoptosis in lymphoma cells: translocation of cytochrome c causes inhibition of respiration as well as caspase activation. Biochem. Biophys. Res. Commun. 255:1999;673-679
65. Carre V., Jayat C., Granet R., Krausz P., Guilloton M. Chronology of the apoptotic events induced in the K562 cell line by photodynamic treatment with hematoporphyrin and monoglucosylporphyrin. Photochem. Photobiol. 69:1999;55-60
66. Oberdanner C.B., Kiesslich T., Krammer B., Plaetzer K. Glucose is required to maintain high ATP-levels for the energy-utilizing steps during PDT-induced apoptosis. Photochem. Photobiol. 76:2002;695-703
67. Kessel D., Luo Y. Photodynamic therapy: a mitochondrial inducer of apoptosis. Cell Death Differ. 6:1999;28-35
68. Vantieghem A., Xu Y., Declercq W., Vandenabeele P., Denecker G., Vandenheede J.R., Merlevede W., de Witte P.A., Agostinis P. Different pathways mediate cytochrome c release after photodynamic therapy with hypericin. Photochem. Photobiol. 74:2001;133-142
69. Chaloupka R., Petit P.X., Israel N., Sureau F. Over-expression of Bcl-2 does not protect cells from hypericin photo-induced mitochondrial membrane depolarization, but delays subsequent events in the apoptotic pathway. FEBS Lett. 462:1999;295-301
70. Chiu S., Evans H.H., Lam M., Nieminen A., Oleinick N.L. Phthalocyanine 4 photodynamic therapy-induced apoptosis of mouse L5178Y-R cells results from a delayed but extensive release of cytochrome c from mitochondria. Cancer Lett. 165:2001;51-58
71. Granville D.J., Carthy C.M., Jiang H., Shore G.C., McManus B.M., Hunt D.W. 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. 437:1998;5-10
72. Granville D.J., Shaw J.R., Leong S., Carthy C.M., Margaron P., Hunt D.W., McManus B.M. Release of cytochrome c, Bax migration, Bid cleavage, and activation of caspases 2, 3, 6, 7, 8, and 9 during endothelial cell apoptosis. Am. J. Pathol. 155:1999;1021-1025
73. L overexpression do not prevent early mitochondrial events but still depress caspase activity. Lab. Invest. 79:1999;953-965
74. Slee E.A., Keogh S.A., Martin S.J. Cleavage of BID during cytotoxic drug and UV radiation-induced apoptosis occurs downstream of the point of Bcl-2 action and is catalysed by caspase-3: a potential feedback loop for amplification of apoptosis-associated mitochondrial cytochrome c release. Cell Death Differ. 7:2000;556-565
75. Granville D.J., Levy J.G., Hunt D.W. Photodynamic therapy induces caspase-3 activation in HL-60 cells. Cell Death Differ. 4:1997;623-628
76. Granville D.J., Jiang H., An M.T., Levy J.G., McManus B.M., Hunt D.W. Overexpression of Bcl-X(L) prevents caspase-3-mediated activation of DNA fragmentation factor (DFF) produced by treatment with the photochemotherapeutic agent BPD-MA. FEBS Lett. 422:1998;151-154
77. Granville D.J., Jiang H., An M.T., Levy J.G., McManus B.M., Hunt D.W. Bcl-2 overexpression blocks caspase activation and downstream apoptotic events instigated by photodynamic therapy. Br. J. Cancer. 79:1999;95-100
78. Grebenova D., Kuzelova K., Smetana K., Pluskalova M., Cajthamlova H., Marinov I., Fuchs O., Soucek J., Jarolim P., Hrkal Z. Mitochondrial and endoplasmic reticulum stress-induced apoptotic pathways are activated by 5-aminolevulinic acid-based photodynamic therapy in HL60 leukemia cells. J. Photochem. Photobiol., B. 69:2003;71-85
79. Granville D.J., Carthy C.M., Jiang H., Levy J.G., McManus B.M., Matroule J.Y., Piette J., Hunt D.W. Nuclear factor-kappaB activation by the photochemotherapeutic agent verteporfin. Blood. 95:2000;256-262
80. Assefa Z., Vantieghem A., Declercq W., Vandenabeele P., Vandenheede J.R., Merlevede W., de Witte P., Agostinis P. The activation of the c-Jun N-terminal kinase and p38 mitogen-activated protein kinase signaling pathways protects HeLa cells from apoptosis following photodynamic therapy with hypericin. J. Biol. Chem. 274:1999;8788-8796
81. 2/M phase arrested cells following photodynamic therapy with hypericin involves a CDK1-mediated signal and delays the onset of apoptosis. J. Biol. Chem. 2002;M204348200
82. Ahmad N., Kalka K., Mukhtar H. In vitro and in vivo inhibition of epidermal growth factor receptor-tyrosine kinase pathway by photodynamic therapy. Oncogene. 20:2001;2314-2317
83. He J., Whitacre C.M., Xue L.Y., Berger N.A., Oleinick N.L. Protease activation and cleavage of poly(ADP-ribose) polymerase: an integral part of apoptosis in response to photodynamic treatment. Cancer Res. 58:1998;940-946
84. Xue L.Y., Qiu Y., He J., Kung H.J., Oleinick N.L. Etk/Bmx, a PH-domain containing tyrosine kinase, protects prostate cancer cells from apoptosis induced by photodynamic therapy or thapsigargin. Oncogene. 18:1999;3391-3398
85. Wispriyono B., Schmelz E., Pelayo H., Hanada K., Separovic D. A role for the de novo sphingolipids in apoptosis of photosensitized cells. Exp. Cell Res. 279:2002;153-165
86. Counis M.F., Torriglia A. DNases and apoptosis. Biochem. Cell. Biol. 78:2000;405-414
87. 2+-dependent and caspase-3-independent apoptosis caused by damage in Golgi apparatus due to 2,4,5,7-tetrabromorhodamine 123 bromide-induced photodynamic effects. Photochem. Photobiol. 78:2003;241-247
88. Xue L.Y., Chiu S.M., Oleinick N.L. Photodynamic therapy-induced death of MCF-7 human breast cancer cells: a role for caspase-3 in the late steps of apoptosis but not for the critical lethal event. Exp. Cell Res. 263:2001;145-155
89. Whitacre C.M., Satoh T.H., Xue L., Gordon N.H., Oleinick N.L. Photodynamic therapy of human breast cancer xenografts lacking caspase-3. Cancer Lett. 179:2002;43-49
90. L inhibit CD95-mediated apoptosis by preventing mitochondrial release of Smac/DIABLO and subsequent inactivation of X-linked inhibitor-of-apoptosis protein. J. Biol. Chem. 277:2002;11345-11351
91. He J., Agarwal M.L., Larkin H.E., Friedman L.R., Xue L.Y., Oleinick N.L. The induction of partial resistance to photodynamic therapy by the protooncogene BCL-2. Photochem. Photobiol. 64:1996;845-852
92. Zhang W.G., Ma L.P., Wang S.W., Zhang Z.Y., Cao G.D. Antisense bcl-2 retrovirus vector increases the sensitivity of a human gastric adenocarcinoma cell line to photodynamic therapy. Photochem. Photobiol. 69:1999;582-586
93. Srivastava M., Ahmad N., Gupta S., Mukhtar H. Involvement of Bcl-2 and Bax in photodynamic therapy-mediated apoptosis. Antisense Bcl-2 oligonucleotide sensitizes RIF1 cells to photodynamic therapy apoptosis. J. Biol. Chem. 276:2001;15481-15488
94. Kim H.R., Luo Y., Li G., Kessel D. Enhanced apoptotic response to photodynamic therapy after bcl-2 transfection. Cancer Res. 59:1999;3429-3432
95. L isoforms by photodynamic therapy with the phthalocyanine photosensitizer Pc 4. Oncogene. 22:2003;9197-9204
96. Kessel D., Castelli M., Reiners J.J. Jr. Apoptotic response to photodynamic therapy versus the Bcl-2 antagonist HA14-1. Photochem. Photobiol. 76:2002;314-319
97. Xue L.Y., Chiu S.M., Oleinick N.L. Photochemical destruction of the Bcl-2 oncoprotein during photodynamic therapy with the phthalocyanine photosensitizer Pc 4. Oncogene. 20:2001;3420-3427
98. Usuda J., Azizuddin K., Chiu S.M., Oleinick N.L. Association between the photodynamic loss of Bcl-2 and the sensitivity to apoptosis caused by phthalocyanine photodynamic therapy. Photochem. Photobiol. 78:2003;1-8
99. Usuda J., Chiu S.M., Azizuddin K., Xue L.Y., Lam M., Nieminen A.L., Oleinick N.L. Promotion of photodynamic therapy-induced apoptosis by the mitochondrial protein Smac/DIABLO: dependence on Bax. Photochem. Photobiol. 76:2002;217-223
100. Chiu S.M., Xue L.Y., Usuda J., Azizuddin K., Oleinick N.L. Bax is essential for mitochondrion-mediated apoptosis but not for cell death caused by photodynamic therapy. Br. J. Cancer. 89:2003;1590-1597
101. Du C., Fang M., Li Y., Li L., Wang X. Smac, a mitochondrial protein that promotescytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 102:2000;33-42
102. Verhagen A.M., Ekert P.G., Pakusch M., Silke J., Connolly L.M., Reid G.E., Moritz R.L., Simpson R.J., Vaux D.L. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell. 102:2000;43-53
103. 2+ concentrations related to PDT-induced apoptosis in photosensitized human cancer cells. Cancer Lett. 128:1998;205-210
104. Hubmer A., Hermann A., Uberriegler K., Krammer B. Role of calcium in photodynamically induced cell damage of human fibroblasts. Photochem. Photobiol. 64:1996;211-215
105. Gederaas O.A., Thorstensen K., Romslo I. The effect of brief illumination on intracellular free calcium concentration in cells with 5-aminolevulinic acid-induced protoporphyrin IX synthesis. Scand. J. Clin. Lab. Invest. 56:1996;583-589
106. Cui Z.J., Habara Y., Wang D.Y., Kanno T. A novel aspect of photodynamic action: induction of recurrent spikes in cytosolic calcium concentration. Photochem. Photobiol. 65:1997;382-386
107. Cui Z.J., Kanno T. Photodynamic triggering of calcium oscillation in the isolated rat pancreatic acini. J. Physiol. 504:1997;47-55
108. Penning L.C., Rasch M.H., Ben-Hur E., Dubbelman T.M., Havelaar A.C., Van der Zee J., Van Steveninck J. A role for the transient increase of cytoplasmic free calcium in cell rescue after photodynamic treatment. Biochim. Biophys. Acta. 1107:1992;255-260
109. Penning L.C., Lagerberg J.W., VanDierendonck J.H., Cornelisse C.J., Dubbelman T.M., VanSteveninck J. The role of DNA damage and inhibition of poly(ADP-ribosyl)ation in loss of clonogenicity of murine L929 fibroblasts, caused by photodynamically induced oxidative stress. Cancer Res. 54:1994;5561-5567
110. Ben-Hur E., Dubbelman T.M., Van Steveninck J. Phthalocyanine-induced photodynamic changes of cytoplasmic free calcium in Chinese hamster cells. Photochem. Photobiol. 54:1991;163-166
111. Specht K.G., Rodgers M.A. Plasma membrane depolarization and calcium influx during cell injury by photodynamic action. Biochim. Biophys. Acta. 1070:1991;60-68
112. 2+ stores during photodynamic therapy-induced apoptosis. Cell Calcium. 30:2001;343-350
113. 4-photosensitized rat bladder RR 1022 epithelial cells. Photochem. Photobiol. 72:2000;210-216
114. Ben-Her E., Dubbelman T.M. Cytoplasmic free calcium changes as a trigger mechanism in the response of cells to photosensitization. Photochem. Photobiol. 58:1993;890-894
115. Yonuschot G. Early increase in intracellular calcium during photodynamic permeabilization. Free Radic. Biol. Med. 11:1991;307-317
116. 2+ influx induced by photodynamic action in human cerebral glioma (U-87 MG) cells: possible involvement of a calcium channel. Photochem. Photobiol. 60:1994;244-248
117. An Y.P., Xiao R., Cui H., Cui Z.J. Selective activation by photodynamic action of cholecystokinin receptor in the freshly isolated rat pancreatic acini. Br. J. Pharmacol. 139:2003;872-880
118. Marks D.I., Fox R.M. Mechanisms of photochemotherapy-induced apoptotic cell death in lymphoid cells. Biochem. Cell. Biol. 69:1991;754-760
119. 2 induction reduces haematoporphyrin-derivative-induced cytotoxicity of T24 human bladder transitional carcinoma cells in vitro. Biochem. J. 292:1993;237-240
120. Agarwal M.L., Larkin H.E., Zaidi S.I., Mukhtar H., Oleinick N.L. Phospholipase activation triggers apoptosis in photosensitized mouse lymphoma cells. Cancer Res. 53:1993;5897-5902
121. 2+ influx in endoplasmic reticulum: a comparison with mitochondria. Biochem. J. 338:1999;221-227
122. Pozzan T., Rizzuto R., Volpe P., Meldolesi J. Molecular and cellular physiology of intracellular calcium stores. Physiol. Rev. 74:1994;595-636
123. 2+ sequestration. FEBS Lett. 224:1987;331-336
124. 2+-ATPase. Proc. Natl. Acad. Sci. U. S. A. 87:1990;2466-2470
125. i regulation by glutamate receptor agonists in cultured chick retina cells. Vis. Res. 36:1996;1091-1102
126. Nakagawa T., Zhu H., Morishima N., Li E., Xu J., Yankner B.A., Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature. 403:2000;98-103
127. Rao R.V., Castro-Obregon S., Frankowski H., Schuler M., Stoka V., del Rio G., Bredesen D.E., Ellerby H.M. Coupling endoplasmic reticulum stress to the cell death program. An Apaf-1-independent intrinsic pathway. J. Biol. Chem. 277:2002;21836-21842
128. Nakagawa T., Yuan J. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 150:2000;887-894
129. Rao R.V., Hermel E., Castro-Obregon S., del Rio G., Ellerby L.M., Ellerby H.M., Bredesen D.E. Coupling endoplasmic reticulum stress to the cell death program. Mechanism of caspase activation. J. Biol. Chem. 276:2001;33869-33874
130. Schwab B.L., Guerini D., Didszun C., Bano D., Ferrando-May E., Fava E., Tam J., Xu D., Xanthoudakis S., Nicholson D.W., Carafoli E., Nicotera P. Cleavage of plasma membrane calcium pumps by caspases: a link between apoptosis and necrosis. Cell Death Differ. 9:2002;818-831
131. 2+ activates phospholipase C. Trends Neurosci. 11:1988;517-520
132. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature. 361:1993;315-325
133. Bokoch G.M. Caspase-mediated activation of PAK2 during apoptosis: proteolytic kinase activation as a general mechanism of apoptotic signal transduction? Cell Death Differ. 5:1998;637-645
134. Cross T.G., Scheel-Toellner D., Henriquez N.V., Deacon E., Salmon M., Lord J.M. Serine/threonine protein kinases and apoptosis. Exp. Cell Res. 256:2000;34-41
135. Rasch M.H., Tijssen K., Lagerberg J.W., Corver W.E., VanSteveninck J., Dubbelman T.M. The role of protein kinase C activity in the killing of Chinese hamster ovary cells by ionizing radiation and photodynamic treatment. Photochem. Photobiol. 66:1997;209-213
136. 2 from cells by photodynamic treatment in vitro. Cancer Res. 49:1989;6896-6900
137. Henderson B.W., Owczarczak B., Sweeney J., Gessner T. Effects of photodynamic treatment of platelets or endothelial cells in vitro on platelet aggregation. Photochem. Photobiol. 56:1992;513-521
138. al-Laith M., Matthews E.K., Cui Z.J. Photodynamic drug action on isolated rat pancreatic acini. Mobilization of arachidonic acid and prostaglandin production. Biochem. Pharmacol. 46:1993;567-573
139. Fingar V.H., Wieman T.J., Karavolos P.S., Doak K.W., Ouellet R., van Lier J.E. The effects of photodynamic therapy using differently substituted zinc phthalocyanines on vessel constriction, vessel leakage and tumor response. Photochem. Photobiol. 58:1993;251-258
140. Duarte C.B., Santos P.F., Sanchez-Prieto J., Carvalho A.P. Glutamate release evoked by glutamate receptor agonists in cultured chick retina cells: modulation by arachidonic acid. J. Neurosci. Res. 44:1996;363-373
141. 2. Annu. Rev. Pharmacol. Toxicol. 39:1999;175-189
142. Dixon J.F., Hokin L.E. Secretogogue-stimulated phosphatidylinositol breakdown in the exocrine pancreas liberates arachidonic acid, stearic acid, and glycerol by sequential actions of phospholipase C and diglyceride lipase. J. Biol. Chem. 259:1984;14418-14425
143. Foultier M.T., Patrice T., Yactayo S., Lajat Y., Resche F. Photodynamic treatment of normal endothelial cells or glioma cells in vitro. Surg. Neurol. 37:1992;83-88
144. Ferrario A., Von Tiehl K., Wong S., Luna M., Gomer C.J. Cyclooxygenase-2 inhibitor treatment enhances photodynamic therapy-mediated tumor response. Cancer Res. 62:2002;3956-3961
145. Hendrickx N., Volanti C., Moens U., Seternes O.M., De Witte P., Vandenheede J.R., Piette J., Agostinis P. Up-regulation of cyclooxygenase-2 and apoptosis resistance by p38 MAPK in hypericin-mediated photodynamic therapy of human cancer cells. J. Biol. Chem. 278:2003;52231-52239
146. Morrow J.D., Harris T.M., Roberts L.J. 2nd Noncyclooxygenase oxidative formation of a series of novel prostaglandins: analytical ramifications for measurement of eicosanoids. Anal. Biochem. 184:1990;1-10
147. Fingar V.H., Wieman T.J., Doak K.W. Role of thromboxane and prostacyclin release on photodynamic therapy-induced tumor destruction. Cancer Res. 50:1990;2599-2603
148. Fingar V.H., Wieman T.J., Doak K.W. Mechanistic studies of PDT-induced vascular damage: evidence that eicosanoids mediate this process. Int. J. Radiat. Biol. 60:1991;303-309
149. Fingar V.H., Wieman T.J., Wiehle S.A., Cerrito P.B. The role of microvascular damage in photodynamic therapy: the effect of treatment on vessel constriction, permeability, and leukocyte adhesion. Cancer Res. 52:1992;4914-4921
150. Fingar V.H., Siegel K.A., Wieman T.J., Doak K.W. The effects of thromboxane inhibitors on the microvascular and tumor response to photodynamic therapy. Photochem. Photobiol. 58:1993;393-399
151. Mathias S., Pena L.A., Kolesnick R.N. Signal transduction of stress via ceramide. Biochem. J. 335:1998;465-480
152. Andrieu-Abadie N., Gouaze V., Salvayre R., Levade T. Ceramide in apoptosis signaling: relationship with oxidative stress. Free Radic. Biol. Med. 31:2001;717-728
153. Hannun Y.A., Luberto C., Argraves K.M. Enzymes of sphingolipid metabolism: from modular to integrative signaling. Biochemistry. 40:2001;4893-4903
154. Separovic D., He J., Oleinick N.L. Ceramide generation in response to photodynamic treatment of L5178Y mouse lymphoma cells. Cancer Res. 57:1997;1717-1721
155. Separovic D., Mann K.J., Oleinick N.L. Association of ceramide accumulation with photodynamic treatment-induced cell death. Photochem. Photobiol. 68:1998;101-109
156. Separovic D., Pink J.J., Oleinick N.A., Kester M., Boothman D.A., McLoughlin M., Pena L.A., Haimovitz-Friedman A. Niemann-Pick human lymphoblasts are resistant to phthalocyanine 4-photodynamic therapy-induced apoptosis. Biochem. Biophys. Res. Commun. 258:1999;506-512
157. Chiu S.M., Davis T.W., Meyers M., Ahmad N., Mukhtar H., Separovic D. Phthalocyanine 4-photodynamic therapy induces ceramide generation and apoptosis in acid sphingomyelinase-deficient mouse embryonic fibroblasts. Int. J. Oncol. 16:2000;423-427
158. Nagy B., Chiu S.M., Separovic D. Fumonisin B1 does not prevent apoptosis in A431 human epidermoid carcinoma cells after photosensitization with a silicon phthalocyanine. J. Photochem. Photobiol., B. 57:2000;132-141
159. Dolgachev V., Farooqui M.S., Kulaeva O.I., Tainsky M.A., Nagy B., Hanada K., Separovic D. De novo ceramide accumulation due to inhibition of its conversion to complex sphingolipids in apoptotic photosensitized cells. J. Biol. Chem. 279:2004;23238-23249
160. Matroule J.Y., Bonizzi G., Morliere P., Paillous N., Santus R., Bours V., Piette J. Pyropheophorbide-a methyl ester-mediated photosensitization activates transcription factor NF-kappaB through the interleukin-1 receptor-dependent signaling pathway. J. Biol. Chem. 274:1999;2988-3000
161. Dolgachev V., Nagy B., Taffe B., Hanada K., Separovic D. Reactive oxygen species generation is independent of de novo sphingolipids in apoptotic photosensitized cells. Exp. Cell Res. 288:2003;425-436
162. Coroneos E., Wang Y., Panuska J.R., Templeton D.J., Kester M. Sphingolipid metabolites differentially regulate extracellular signal-regulated
163. Verheij M., Bose R., Lin X.H., Yao B., Jarvis W.D., Grant S., Birrer M.J., Szabo E., Zon L.I., Kyriakis J.M., Haimovitz-Friedman A., Fuks Z., Kolesnick R.N. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature. 380:1996;75-79
164. Penning L.C., VanSteveninck J., Dubbelman T.M. HPD-induced photodynamic changes in intracellular cyclic AMP levels in human bladder transitional carcinoma cells, clone T24. Biochem. Biophys. Res. Commun. 194:1993;1084-1089
165. Jadeski L.C., Hum K.O., Chakraborty C., Lala P.K. Nitric oxide promotes murine mammary tumour growth and metastasis by stimulating tumour cell migration, invasiveness and angiogenesis. Int. J. Cancer. 86:2000;30-39
166. Tozer G.M., Prise V.E., Chaplin D.J. Inhibition of nitric oxide synthase induces a selective reduction in tumor blood flow that is reversible with L-arginine. Cancer Res. 57:1997;948-955
167. Coutier S., Bezdetnaya L., Marchal S., Melnikova V., Belitchenko I., Merlin J.L., Guillemin F. Foscan (mTHPC) photosensitized macrophage activation: enhancement of phagocytosis, nitric oxide release and tumour necrosis factor-alpha-mediated cytolytic activity. Br. J. Cancer. 81:1999;37-42
168. Ali S.M., Olivo M. Nitric oxide mediated photo-induced cell death in human malignant cells. Int. J. Oncol. 22:2003;751-756
169. Dalbasti T., Cagli S., Kilinc E., Oktar N., Ozsoz M. Online electrochemical monitoring of nitric oxide during photodynamic therapy. Nitric Oxide. 7:2002;301-305
170. Förstermann U. Regulation of nitric oxide synthase expression and activity. Mayer B. Handbook of Experimental Pharmacology. 2000;71-91 Springer-Verlag, Berlin
171. Star W.M., Marijnissen H.P., van den Berg-Blok A.E., Versteeg J.A., Franken K.A., Reinhold H.S. Destruction of rat mammary tumor and normal tissue microcirculation by hematoporphyrin derivative photoradiation observed in vivo in sandwich observation chambers. Cancer Res. 46:1986;2532-2540
172. Reed M.W., Miller F.N., Wieman T.J., Tseng M.T., Pietsch C.G. The effect of photodynamic therapy on the microcirculation. J. Surg. Res. 45:1988;452-459
173. Krosl G., Korbelik M., Dougherty G.J. Induction of immune cell infiltration into murine SCCVII tumour by photofrin-based photodynamic therapy. Br. J. Cancer. 71:1995;549-555
174. Gollnick S.O., Liu X., Owczarczak B., Musser D.A., Henderson B.W. Altered expression of interleukin 6 and interleukin 10 as a result of photodynamic therapy in vivo. Cancer Res. 57:1997;3904-3909
175. Moilanen E., Vuorinen P., Kankaanranta H., Metsa-Ketela T., Vapaatalo H. Inhibition by nitric oxide-donors of human polymorphonuclear leucocyte functions. Br. J. Pharmacol. 109:1993;852-858
176. Schmidt H.H., Walter U. NO at work. Cell. 78:1994;919-925
177. Hirst D.G., Flitney F.W. Bicknell R., Lewis C.E., Ferrara N. Tumor Angiogenesis. 1997;153-167 Oxford Univ. Press, Oxford
178. Henderson B.W., Sitnik-Busch T.M., Vaughan L.A. Potentiation of photodynamic therapy antitumor activity in mice by nitric oxide synthase inhibition is fluence rate-dependent. Photochem. Photobiol. 70:1999;64-71
179. Korbelik M., Parkins C.S., Shibuya H., Cecic I., Stratford M.R., Chaplin D.J. Nitric oxide production by tumour tissue: impact on the response to photodynamic therapy. Br. J. Cancer. 82:2000;1835-1843
180. Liu L., Stamler J.S. NO: an inhibitor of cell death. Cell Death Differ. 6:1999;937-942
181. Gomes E.R., Cruz T., Lopes C.F., Carvalho A.P., Duarte C.B. Photosensitization of lymphoblastoid cells with phthalocyanines at different saturating incubation times. Cell Biol. Toxicol. 15:1999;249-260
182. Niziolek M., Korytowski W., Girotti A.W. Chain-breaking antioxidant and cytoprotective action of nitric oxide on photodynamically stressed tumor cells. Photochem. Photobiol. 78:2003;262-270
183. Gomes E.R., Almeida R.D., Carvalho A.P., Duarte C.B. Nitric oxide modulates tumor cell death induced by photodynamic therapy through a cGMP-dependent mechanism. Photochem. Photobiol. 76:2002;423-430
184. Kim Y.M., de Vera M.E., Watkins S.C., Billiar T.R. Nitric oxide protects cultured rat hepatocytes from tumor necrosis factor-alpha-induced apoptosis by inducing heat shock protein 70 expression. J. Biol. Chem. 272:1997;1402-1411
185. Foresti R., Motterlini R. The heme oxygenase pathway and its interaction with nitric oxide in the control of cellular homeostasis. Free Radic. Res. 31:1999;459-475
186. Suschek C.V., Krischel V., Bruch-Gerharz D., Berendji D., Krutmann J., Kroncke K.D., Kolb-Bachofen V. Nitric oxide fully protects against UVA-induced apoptosis in tight correlation with Bcl-2 up-regulation. J. Biol. Chem. 274:1999;6130-6137
187. Niziolek M., Korytowski W., Girotti A.W. Nitric oxide inhibition of free radical-mediated lipid peroxidation in photodynamically treated membranes and cells. Free Radic. Biol. Med. 34:2003;997-1005
188. Chang L., Karin M. Mammalian MAP kinase signalling cascades. Nature. 410:2001;37-40
189. Matos T.J., Duarte C.B., Carvalho A.P., Lopes M.C. Heilmeyer L., Friedrich P. Protein Modules in Cellular Signalling. 2001;12-28 IOS Press, Amsterdam
190. Tao J., Sanghera J.S., Pelech S.L., Wong G., Levy J.G. Stimulation of stress-activated protein kinase and p38 HOG1 kinase in murine keratinocytes following photodynamic therapy with benzoporphyrin derivative. J. Biol. Chem. 271:1996;27107-27115
191. Klotz L.O., Fritsch C., Briviba K., Tsacmacidis N., Schliess F., Sies H. Activation of JNK and p38 but not ERK MAP kinases in human skin cells by 5-aminolevulinate photodynamic therapy. Cancer Res. 58:1998;4297-4300
192. Wong T.W., Tracy E., Oseroff A.R., Baumann H. Photodynamic therapy mediates immediate loss of cellular responsiveness to cytokines and growth factors. Cancer Res. 63:2003;3812-3818
193. Xue L., He J., Oleinick N.L. Promotion of photodynamic therapy-induced apoptosis by stress kinases. Cell Death Differ. 6:1999;855-864
194. Zhuang S., Kochevar I.E. Singlet oxygen-induced activation of Akt/protein kinase B is independent of growth factor receptors. Photochem. Photobiol. 78:2003;361-371
195. Tong Z., Singh G., Rainbow A.J. Sustained activation of the extracellular signal regulated kinase pathway protects cells from photofrin-mediated photodynamic therapy. Cancer Res. 62:2002;5528-5535
196. Tong Z., Singh G., Valerie K., Rainbow A.J. Activation of the stress-activated JNK and p38 MAPK kinases in human cells by Photofrin-mediated photodynamic therapy. J. Photochem. Photobiol., B. 71:2003;77-85
197. Xue L.Y., He J., Oleinick N.L. Rapid tyrosine phosphorylation of HS1 in the response of mouse lymphoma L5178Y-R cells to photodynamic treatment sensitized by the phthalocyanine Pc 4. Photochem. Photobiol. 66:1997;105-113
198. Granville D.J., Levy J.G., Hunt D.W. Photodynamic treatment with benzoporphyrin derivative monoacid ring A produces protein tyrosine phosphorylation events and DNA fragmentation in murine P815 cells. Photochem. Photobiol. 67:1998;358-362
199. 2+ influx and glutamate release from hippocampal synaptosomes: putative non-specific effects. Neurochem. Int. 42:2003;179-188
200. Kitamura D., Kaneko H., Miyagoe Y., Ariyasu T., Watanabe T. Isolation and characterization of a novel human gene expressed specifically in the cells of hematopoietic lineage. Nucleic Acids Res. 17:1989;9367-9379
201. Fukuda T., Kitamura D., Taniuchi I., Maekawa Y., Benhamou L.E., Sarthou P., Watanabe T. Restoration of surface IgM-mediated apoptosis in an anti-IgM-resistant variant of WEHI-231 lymphoma cells by HS1, a protein-tyrosine kinase substrate. Proc. Natl. Acad. Sci. U. S. A. 92:1995;7302-7306
202. Taniuchi I., Kitamura D., Maekawa Y., Fukuda T., Kishi H., Watanabe T. Antigen receptor-induced clonal expansion and deletion of lymphocytes are impaired in mice lacking HS1 protein, a substrate of the antigen-receptor- coupled tyrosine kinases. EMBO J. 14:1995;3664-3678
203. Agostinis P., Vandenbogaerde A., Donella-Deana A., Pinna L.A., Lee K.T., Goris J., Merlevede W., Vandenheede J.R., De Witte P. Photosensitized inhibition of growth factor regulated protein kinases by hypericin. Biochem. Pharmacol. 49:1995;1615-1622
204. Spaulding D.C., Spaulding B.O. Epidermal growth factor receptor expression and measurement in solid tumors. Semin. Oncol. 29:2002;45-54
205. Nunez G., del Peso L. Linking extracellular survival signals and the apoptotic machinery. Curr. Opin. Neurobiol. 8:1998;613-618
206. Downward J. Mechanisms and consequences of activation of protein kinase B/Akt. Curr. Opin. Cell Biol. 10:1998;262-267
207. Kandel E.S., Hay N. The regulation and activities of the multifunctional serine/threonine kinase Akt/PKB. Exp. Cell Res. 253:1999;210-229
208. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell. 103:2000;211-225
209. Fukada T., Yoshida Y., Nishida K., Ohtani T., Shirogane T., Hibi M., Hirano T. Signaling through Gp130: toward a general scenario of cytokine action. Growth Factors. 17:1999;81-91
210. Hirano T., Ishihara K., Hibi M. Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors. Oncogene. 19:2000;2548-2556
211. Ishibashi T., Kimura H., Uchida T., Kariyone S., Friese P., Burstein S.A. Human interleukin 6 is a direct promoter of maturation of megakaryocytes in vitro. Proc. Natl. Acad. Sci. U. S. A. 86:1989;5953-5957
212. Grant S.L., Begley C.G. The oncostatin M signalling pathway: reversing the neoplastic phenotype? Mol. Med. Today. 5:1999;406-412
213. Klausen P., Pedersen L., Jurlander J., Baumann H. Oncostatin M and interleukin 6 inhibit cell cycle progression by prevention of p27kip1 degradation in HepG2 cells. Oncogene. 19:2000;3675-3683
214. Shaulian E., Karin M. AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4:2002;E131-E136
215. Ameyar M., Wisniewska M., Weitzman J.B. A role for AP-1 in apoptosis: the case for and against. Biochimie. 85:2003;747-752
216. Luna M.C., Wong S., Gomer C.J. Photodynamic therapy mediated induction of early response genes. Cancer Res. 54:1994;1374-1380
217. Kick G., Messer G., Plewig G., Kind P., Goetz A.E. Strong and prolonged induction of c-jun and c-fos proto-oncogenes by photodynamic therapy. Br. J. Cancer. 74:1996;30-36
218. Kick G., Messer G., Goetz A., Plewig G., Kind P. Photodynamic therapy induces expression of interleukin 6 by activation of AP-1 but not NF-kappa B DNA binding. Cancer Res. 55:1995;2373-2379
219. Ryter S.W., Gomer C.J. Nuclear factor kappa B binding activity in mouse L1210 cells following photofrin II-mediated photosensitization. Photochem. Photobiol. 58:1993;753-756
220. Ghosh S., May M.J., Kopp E.B. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16:1998;225-260
221. Pahl H.L. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene. 18:1999;6853-6866
222. Barkett M., Gilmore T.D. Control of apoptosis by Rel/NF-kappaB transcription factors. Oncogene. 18:1999;6910-6924
223. Kaltschmidt B., Kaltschmidt C., Hofmann T.G., Hehner S.P., Droge W., Schmitz M.L. The pro- or anti-apoptotic function of NF-kappaB is determined by the nature of the apoptotic stimulus. Eur. J. Biochem. 267:2000;3828-3835
224. Kucharczak J., Simmons M.J., Fan Y., Gelinas C. To be, or not to be: NF-kappaB is the answer-role of Rel/NF-kappaB in the regulation of apoptosis. Oncogene. 22:2003;8961-8982
225. Piret B., Legrand-Poels S., Sappey C., Piette J. NF-kappa B transcription factor and human immunodeficiency virus type 1 (HIV-1) activation by methylene blue photosensitization. Eur. J. Biochem. 228:1995;447-455
226. Legrand-Poels S., Bours V., Piret B., Pflaum M., Epe B., Rentier B., Piette J. Transcription factor NF-kappa B is activated by photosensitization generating oxidative DNA damages. J. Biol. Chem. 270:1995;6925-6934
227. Volanti C., Matroule J.Y., Piette J. Involvement of oxidative stress in NF-kappaB activation in endothelial cells treated by photodynamic therapy. Photochem. Photobiol. 75:2002;36-45
228. Matroule J.Y., Hellin A.C., Morliere P., Fabiano A.S., Santus R., Merville M.P., Piette J. Role of nuclear factor-kappa B in colon cancer cell apoptosis mediated by aminopyropheophorbide photosensitization. Photochem. Photobiol. 70:1999;540-548
229. Ahmad N., Feyes D.K., Agarwal R., Mukhtar H. Photodynamic therapy results in induction of WAF1/CIP1/P21 leading to cell cycle arrest and apoptosis. Proc. Natl. Acad. Sci. U. S. A. 95:1998;6977-6982
230. Colussi V.C., Feyes D.K., Mulvihill J.W., Li Y.S., Kenney M.E., Elmets C.A., Oleinick N.L., Mukhtar H. Phthalocyanine 4 (Pc 4) photodynamic therapy of human OVCAR-3 tumor xenografts. Photochem. Photobiol. 69:1999;236-241
231. Whitacre C.M., Feyes D.K., Satoh T., Grossmann J., Mulvihill J.W., Mukhtar H., Oleinick N.L. Photodynamic therapy with the phthalocyanine photosensitizer Pc 4 of SW480 human colon cancer xenografts in athymic mice. Clin. Cancer Res. 6:2000;2021-2027
232. Trimarchi J.M., Lees J.A. Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell Biol. 3:2002;11-20
233. Ahmad N., Gupta S., Mukhtar H. Involvement of retinoblastoma (Rb) and E2F transcription factors during photodynamic therapy of human epidermoid carcinoma cells A431. Oncogene. 18:1999;1891-1896
234. Bowen C., Spiegel S., Gelmann E.P. Radiation-induced apoptosis mediated by retinoblastoma protein. Cancer Res. 58:1998;3275-3281
235. Lam E.W., Watson R.J. An E2F-binding site mediates cell-cycle regulated repression of mouse B-myb transcription. EMBO J. 12:1993;2705-2713
236. Weintraub S.J., Chow K.N., Luo R.X., Zhang S.H., He S., Dean D.C. Mechanism of active transcriptional repression by the retinoblastoma protein. Nature. 375:1995;812-815
237. Harbour J.W., Dean D.C. Rb function in cell-cycle regulation and apoptosis. Nat. Cell Biol. 2:2000;E65-E67
238. Gomer C.J., Luna M., Ferrario A., Rucker N. Increased transcription and translation of heme oxygenase in Chinese hamster fibroblasts following photodynamic stress or Photofrin II incubation. Photochem. Photobiol. 53:1991;275-279
239. Maines M.D. Heme oxygenase: function, multiplicity, regulatory mechanisms, and clinical applications. FASEB J. 2:1988;2557-2568
240. Schacter B.A. Heme catabolism by heme oxygenase: physiology, regulation, and mechanism of action. Semin. Hematol. 25:1988;349-369
241. Stocker R., Yamamoto Y., McDonagh A.F., Glazer A.N., Ames B.N. Bilirubin is an antioxidant of possible physiological importance. Science. 235:1987;1043-1046
242. Elbirt K.K., Bonkovsky H.L. Heme oxygenase: recent advances in understanding its regulation and role. Proc. Assoc. Am. Physicians. 111:1999;438-447
243. Alam J., Den Z. Distal AP-1 binding sites mediate basal level enhancement and TPA induction of the mouse heme oxygenase-1 gene. J. Biol. Chem. 267:1992;21894-21900
244. Gomer C.J., Ferrario A., Rucker N., Wong S., Lee A.S. Glucose regulated protein induction and cellular resistance to oxidative stress mediated by porphyrin photosensitization. Cancer Res. 51:1991;6574-6579
245. Gomer C.J., Ryter S.W., Ferrario A., Rucker N., Wong S., Fisher A.M. Photodynamic therapy-mediated oxidative stress can induce expression of heat shock proteins. Cancer Res. 56:1996;2355-2360
246. Curry P.M., Levy J.G. Stress protein expression in murine tumor cells following photodynamic therapy with benzoporphyrin derivative. Photochem. Photobiol. 58:1993;374-379
247. Morimoto R.I. Cells in stress: transcriptional activation of heat shock genes. Science. 259:1993;1409-1410
248. Luna M.C., Ferrario A., Wong S., Fisher A.M., Gomer C.J. Photodynamic therapy mediated oxidative stress as a molecular switch for the temporal expression of genes ligated to the human heat shock promoter. Cancer Res. 60:2000;1637-1644
249. Mitra S., Goren E.M., Frelinger J.G., Foster T.H. Activation of heat shock protein 70 promoter with mTHPC-photodynamic therapy reported by green fluorescent protein in vitro and in vivo. Photochem. Photobiol. 78:2003;615-622
250. Nonaka M., Ikeda H., Inokuchi T. Inhibitory effect of heat shock protein 70 on apoptosis induced by photodynamic therapy in vitro. Photochem. Photobiol. 79:2004;94-98
251. Saleh A., Srinivasula S.M., Balkir L., Robbins P.D., Alnemri E.S. Negative regulation of the Apaf-1 apoptosome by Hsp70. Nat. Cell Biol. 2:2000;476-483
252. Beere H.M., Wolf B.B., Cain K., Mosser D.D., Mahboubi A., Kuwana T., Tailor P., Morimoto R.I., Cohen G.M., Green D.R. Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat. Cell Biol. 2:2000;469-475
253. Pandey P., Nakazawa A., Ito Y., Datta R., Kharbanda S., Kufe D. Requirement for caspase activation in monocytic differentiation of myeloid leukemia cells. Oncogene. 19:2000;3941-3947
254. Golab J., Nowis D., Skrzycki M., Czeczot H., Baranczyk-Kuzma A., Wilczynski G.M., Makowski M., Mroz P., Kozar K., Kaminski R., Jalili A., Kopec M., Grzela T., Jakobisiak M. Antitumor effects of photodynamic therapy are potentiated by 2-methoxyestradiol. A superoxide dismutase inhibitor. J. Biol. Chem. 278:2003;407-414
255. Das H., Koizumi T., Sugimoto T., Yamaguchi S., Hasegawa K., Tenjin Y., Nishimura R. Induction of apoptosis and manganese superoxide dismutase gene by photodynamic therapy in cervical carcinoma cell lines. Int. J. Clin. Oncol. 5:2000;97-103
256. Miccoli L., Beurdeley-Thomas A., De Pinieux G., Sureau F., Oudard S., Dutrillaux B., Poupon M.F. Light-induced photoactivation of hypericin affects the energy metabolism of human glioma cells by inhibiting hexokinase bound to mitochondria. Cancer Res. 58:1998;5777-5786
257. Grebenova D., Halada P., Stulik J., Havlicek V., Hrkal Z. Protein changes in HL60 leukemia cells associated with 5-aminolevulinic acid-based photodynamic therapy. Early effects on endoplasmic reticulum chaperones. Photochem. Photobiol. 72:2000;16-22
258. Anderson C., Hrabovsky S., McKinley Y., Tubesing K., Tang H.P., Dunbar R., Mukhtar H., Elmets C.A. Phthalocyanine photodynamic therapy: disparate effects of pharmacologic inhibitors on cutaneous photosensitivity and on tumor regression. Photochem. Photobiol. 65:1997;895-901
259. Evans S., Matthews W., Perry R., Fraker D., Norton J., Pass H.I. Effect of photodynamic therapy on tumor necrosis factor production by murine macrophages. J. Natl. Cancer Inst. 82:1990;34-39
260. Jones S.E., Jomary C. Clusterin. Int. J. Biochem. Cell Biol. 34:2002;427-431
261. Kalka K., Ahmad N., Criswell T., Boothman D., Mukhtar H. Up-regulation of clusterin during phthalocyanine 4 photodynamic therapy-mediated apoptosis of tumor cells and ablation of mouse skin tumors. Cancer Res. 60:2000;5984-5987
262. Oren M. Decision making by p53: life, death and cancer. Cell Death Differ. 10:2003;431-442
263. Fisher A.M., Ferrario A., Rucker N., Zhang S., Gomer C.J. Photodynamic therapy sensitivity is not altered in human tumor cells after abrogation of p53 function. Cancer Res. 59:1999;331-335
264. Tong Z., Singh G., Rainbow A.J. The role of the p53 tumor suppressor in the response of human cells to photofrin-mediated photodynamic therapy. Photochem. Photobiol. 71:2000;201-210
265. Hajri A., Wack S., Meyer C., Smith M.K., Leberquier C., Kedinger M., Aprahamian M. In vitro and in vivo efficacy of photofrin and pheophorbide a, a bacteriochlorin, in photodynamic therapy of colonic cancer cells. Photochem. Photobiol. 75:2002;140-148
266. Gollnick S.O., Evans S.S., Baumann H., Owczarczak B., Maier P., Vaughan L., Wang W.C., Unger E., Henderson B.W. Role of cytokines in photodynamic therapy-induced local and systemic inflammation. Br. J. Cancer. 88:2003;1772-1779
267. Sun J., Cecic I., Parkins C.S., Korbelik M. Neutrophils as inflammatory and immune effectors in photodynamic therapy-treated mouse SCCVII tumours. Photochem. Photobiol. Sci. 1:2002;690-695
268. Korbelik M., Krosl G., Krosl J., Dougherty G.J. The role of host lymphoid populations in the response of mouse EMT6 tumor to photodynamic therapy. Cancer Res. 56:1996;5647-5652
269. Di Carlo E., Forni G., Lollini P., Colombo M.P., Modesti A., Musiani P. The intriguing role of polymorphonuclear neutrophils in antitumor reactions. Blood. 97:2001;339-345
270. Cecic I., Korbelik M. Mediators of peripheral blood neutrophilia induced by photodynamic therapy of solid tumors. Cancer Lett. 183:2002;43-51
271. Ferrario A., von Tiehl K.F., Rucker N., Schwarz M.A., Gill P.S., Gomer C.J. Antiangiogenic treatment enhances photodynamic therapy responsiveness in a mouse mammary carcinoma. Cancer Res. 60:2000;4066-4069
272. Forsythe J.A., Jiang B.H., Iyer N.V., Agani F., Leung S.W., Koos R.D., Semenza G.L. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell Biol. 16:1996;4604-4613
273. Schofield C.J., Ratcliffe P.J. Oxygen sensing by HIF hydroxylases. Nat. Rev. Mol. Cell Biol. 5:2004;343-354
274. Shweiki D., Itin A., Soffer D., Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature. 359:1992;843-845
275. Ferrario A., Chantrain C.F., von Tiehl K., Buckley S., Rucker N., Shalinsky D.R., Shimada H., DeClerck Y.A., Gomer C.J. The matrix metalloproteinase inhibitor prinomastat enhances photodynamic therapy responsiveness in a mouse tumor model. Cancer Res. 64:2004;2328-2332
276. Guo H., Zucker S., Gordon M.K., Toole B.P., Biswas C. Stimulation of matrix metalloproteinase production by recombinant extracellular matrix metalloproteinase inducer from transfected Chinese hamster ovary cells. J. Biol. Chem. 272:1997;24-27
277. Wojtowicz-Praga S. Clinical potential of matrix metalloprotease inhibitors. Drugs R&D. 1:1999;117-129
278. Kessel D., Luo Y., Mathieu P., Reiners J.J. Jr. Determinants of the apoptotic response to lysosomal photodamage. Photochem. Photobiol. 71:2000;196-200
279. Xiang W., Weingandt H., Liessmann F., Klein S., Stepp H., Baumgartner R., Hillemanns P. Photodynamic effects induced by aminolevulinic acid esters on human cervical carcinoma cells in culture. Photochem. Photobiol. 74:2001;617-623
280. Subbarayan M., Hafeli U.O., Feyes D.K., Unnithan J., Emancipator S.N., Mukhtar H. A simplified method for preparation of 99mTc-annexin V and its biologic evaluation for in vivo imaging of apoptosis after photodynamic therapy. J. Nucl. Med. 44:2003;650-656
281. Noodt B.B., Berg K., Stokke T., Peng Q., Nesland J.M. Apoptosis and necrosis induced with light and 5-aminolaevulinic acid-derived protoporphyrin IX. Br. J. Cancer. 74:1996;22-29
282. Webber J., Luo Y., Crilly R., Fromm D., Kessel D. An apoptotic response to photodynamic therapy with endogenous protoporphyrin in vivo. J. Photochem. Photobiol., B. 35:1996;209-211
283. Lilge L., Portnoy M., Wilson B.C. Apoptosis induced in vivo by photodynamic therapy in normal brain and intracranial tumour tissue. Br. J. Cancer. 83:2000;1110-1117
284. Agarwal M.L., Clay M.E., Harvey E.J., Evans H.H., Antunez A.R., Oleinick N.L. Photodynamic therapy induces rapid cell death by apoptosis in L5178Y mouse lymphoma cells. Cancer Res. 51:1991;5993-5996
285. Zaidi S.I., Oleinick N.L., Zaim M.T., Mukhtar H. Apoptosis during photodynamic therapy-induced ablation of RIF-1 tumors in C3H mice: electron microscopic, histopathologic and biochemical evidence. Photochem. Photobiol. 58:1993;771-776
286. Ball D.J., Luo Y., Kessel D., Griffiths J., Brown S.B., Vernon D.I. The induction of apoptosis by a positively charged methylene blue derivative. J. Photochem. Photobiol., B. 42:1998;159-163
287. Laukka M.A., Wang K.K., Bonner J.A. Apoptosis occurs in lymphoma cells but not in hepatoma cells following ionizing radiation and photodynamic therapy. Dig. Dis. Sci. 39:1994;2467-2475
288. 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. 65:1997;410-415
289. Chen J.Y., Mak N.K., Wen J.M., Leung W.N., Chen S.C., Fung M.C., Cheung N.H. A comparison of the photodynamic effects of temoporfin (mTHPC) and MC540 on leukemia cells: efficacy and apoptosis. Photochem. Photobiol. 68:1998;545-554
290. Agarwal R., Korman N.J., Mohan R.R., Feyes D.K., Jawed S., Zaim M.T., Mukhtar H. Apoptosis is an early event during phthalocyanine photodynamic therapy-induced ablation of chemically induced squamous papillomas in mouse skin. Photochem. Photobiol. 63:1996;547-552
291. Fisher A.M., Danenberg K., Banerjee D., Bertino J.R., Danenberg P., Gomer C.J. Increased photosensitivity in HL60 cells expressing wild-type p53. Photochem. Photobiol. 66:1997;265-270
292. Tajiri H., Shinomiya N., Hayakawa A., Matsumoto Y., Yoshida S. Photodynamic therapy-induced rapid cell death by apoptosis in human pancreatic carcinoma transplanted-into nude mice. J. Clin. Biochem. Nutr. 21:1996;29-37
293. He X.Y., Sikes R.A., Thomsen S., Chung L.W., Jacques S.L. Photodynamic therapy with photofrin II induces programmed cell death in carcinoma cell lines. Photochem. Photobiol. 59:1994;468-473
294. Kochevar I.E., Lynch M.C., Zhuang S., Lambert C.R. Singlet oxygen, but not oxidizing radicals, induces apoptosis in HL-60 cells. Photochem. Photobiol. 72:2000;548-553
295. Tremblay J.F., Dussault S., Viau G., Gad F., Boushira M., Bissonnette R. Photodynamic therapy with toluidine blue in Jurkat cells: cytotoxicity, subcellular localization and apoptosis induction. Photochem. Photobiol. Sci. 1:2002;852-856