Porphyrin-mediated photosensitization - Taking the apoptosis fast lane

Current Opinion in Drug Discovery and Development

Volumn 3, Issue 2, 2000, Pages 232-243

  Granville, David J ^a   Hunt, David W C ^b  

^a ÖLT PhotoTherapeutics Ino 887 Great Northern Way ^*  (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Apoptosis; Caspases; Death receptors; Mitochondria; Photodynamic therapy; Photosensitizer; Verteporfin; Visudyne

Indexed keywords

BENZOPORPHYRIN DERIVATIVE; CASPASE; PHOTOFRIN; PHOTOSENSITIZING AGENT; PORPHYRIN; PROTEIN BCL 2;

APOPTOSIS; CELL DEATH; DRUG STRUCTURE; MITOCHONDRION; PHOTOACTIVATION; PHOTODYNAMIC THERAPY; PHOTODYNAMICS; PHOTOSENSITIZATION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TREATMENT INDICATION;

EID: 0033998061     PISSN: 13676733     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (139)

1. Levy JG, Photodynamic therapy. Trends Biotechnol (1995) 13:14-18.
2. Moore JV, West CM, Whitehurst C, The biology of photodynamic therapy. Phys Med Biol (1997) 42:913-935.
3. Dougherty TJ, Corner CJ, Henderson, Jori G, Kessel D, Korbelik M, Moan J, Peng Q, Photodynamic therapy. J Natl Cancer Inst (1998) 90:889-905.
4. Granville DJ, Levy JG, Hunt DW, Photodynamic therapy induces caspase-3 activation in HL-60 cells. Cell Death Differ (1997) 4:623-628.
5. Granville DJ, Jiang H, An MT, Levy JG, McManus BM, Hunt DW, Overexpression of Bcl-X(L) prevents caspase-3mediated activation of DNA fragmentation factor (OFF) produced by treatment with the photochemotherapeutic agent BPD-MA. FEBS Lett (1998) 422:151-154.
6. Granville DJ, Levy JG, Hunt DW, Photodynamic treatment with benzoporphyrin derivative monoacid ring A produces protein tyrosine phosphorylation events and DNA fragmentation in murine P815 cells. Photochem Photobiol (1998)67:358-362.
7. Granville DJ, Jiang H, An MT, Levy JG, McManus BM, Hunt DW, Bcl-2 overexpresslon blocks caspase activation and downstream apoptotic events instigated by photodynamic therapy. Br J Cancer (1998) 79:95-100.
8. Granville DJ, Carthy CM, Jiang H, Shore GC, McManus BM, Hunt DW, Rapid cytochrome c release, activation of caspases 3,6, 7 and 8 followed by Bap31 cleavage in HeLa cells treated with photodynamic therapy. FEBSLett (1998) 437:5-10.
9. Granville DJ, Shaw JR, Leong S, Carthy CM, Margaron P, Hunt DW, McManus BM, 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 (1999)155:1021-1025.
10. Carthy CM, Granville DJ, Jiang H, Levy JG, Rudin CM, Thompson CB, McManus BM, Hunt DW, Early release of mitochondrial cytochrome c and expression of mitochondrial epitope 7A6 with a porphyrin-derived photosensitizer: Bcl-2 and Bcl-XL overexpression do not prevent early mitochondrial events but still depress caspase activity. Lab Invest (1999) 79:953-965.
11. •• This study demonstrated that PDT with verteporfin triggered immediate mitochondrial apoptosis-related events in HeLa cells. These changes were not prevented by overexpression of Bcl-2 or Bcl-XL while these anti-apoptotic factors prevented features associated with UVB light-induced apoptosis. PDT-induced cell death was more rapid than with UVB light. This work was the first to delineate the involvement of caspase-9 in PDT-induced apoptosis.
12. Jiang H, Granville DJ, McManus BM, Levy JG, Hunt DW, Selective depletion of a thymocyte subset in vitro with an immunomodulatory photosensitizer. Clin Immunol (1999) 91:178-187.
13. Kessel D, Luo Y, Photodynamic therapy: A mitochondrial inducer of apoptosis. Cell Death Differ (1999) 6:28-35.
14. Oleinick NL, Evans HH, The photobiology of photodynamic therapy: Cellular targets and mechanisms. Radiât Res (1998)150:8146-8156.
15. Granville DJ, Carthy CM, Hunt DW, McManus BM, Apoptosis: Molecular aspects of cell death and disease. Lab Invest (1998)78:893-913.
16. Ren Y, Savil! J, Apoptosis: The importance of being eaten. Cell Death Differ (1998) 5:563-568.
17. Nicholson DW, Thomberry NA, Caspases: Killer proteases. Trends Bio Sc/(1997) 22:299-306.
18. Salvesen GS, Dixit VM, Caspases: Intracellular signaling by proteolysis. Cell (1997) 91:443-446.
19. Green DR, Reed JC, Mitochondria and apoptosis. Science (1998)281:1309-1312.
20. Zaidi SI, Oleinick NL, Zaim MT, Mukhtar H, Apoptosis during photodynamic therapy-induced ablation of RIF-1 tumors in C3H mice: Electron microscopic, histopathologic and biochemical evidence. Photochem Rfiotob/o/(1993) 58:771-776.
21. Woodbum KW, Fan Q, Miles DR, Kessel D, Lou Y, Young SW, Localization and efficacy analysis of the phototherapeutic lutetium texaphyrin (PCI-0123) in the murine EMT6 sarcoma model. Photochem P/)Otod/o/(1997) 65:410-415.
22. Ratkay LG, Chowdhary RK, lamaroon A, Richter AM, Neyndorff HC, Keystone EC, Waterfield JD, Levy JG, Amelioration of antigen-induced arthritis in rabbits by induction of apoptosis of inflammatory cells with local application of transdermal photodynamic therapy. Arthritis Rheum (1998) 41:525-534.
23. Kennedy JC, Potter RH, Pross DC, Photodynamic therapy with endogenous protoporphyrin IX: Basic principles and present clinical experience. J Photochem Photobiol (1990) 6:143-148.
24. Peng Q, Berg K, Moan J, Kongshaug M, Nesland JM: 5aminolevulinic acid-based photodynamic therapy, Principles and experimental research. Photochem Photobiol (1997)65:235-251.
25. Noodt BB, Berg K, Stokke T, Peng Q, Nesland JM, Apoptosis and necrosis induced with light and 5-aminolaevulinic acid-derived protoporphyrin IX. Br J Cancer (1996) 74:2229.
26. Lui H, Photodynamic therapy in dermatology with porfimer sodium and benzoporphyrin derivative: An update. Semin Oncol (1994) 21:11-14.
27. Calzavara-Pinton PG, Szeimies R-M, Ortel B, Zane C, Photodynamic therapy with systemic administration of photosensitizers in dermatology. J Photochem Photobiol B (1996)35:225-231.
28. Bissonnette R, McLean Dl, Reid G, Kelsall J, Lui H, Photodynamic therapy of psoriasis and psoriatic arthritis with BPD verteporfin. Seventh Biennial Congress of the International Photodynamic Association, Nantes France (1998):AbsRC87.
29. Chowdhary RK, Ratkay LG, Neyndorff HC, Richter A, Obochi M, Waterfield DJ, Levy JG, The use of transcutaneous photodynamic therapy in the prevention of adjuvantenhanced arthritis in MRL/lpr mice. Clin Immunol Immunopathol (1994) 72:255-263.
30. Leong S, Chan AH, Levy JG, Hunt DW, Transcutaneous photodynamic therapy alters the development of an adoptively transferred form of murine experimental autoimmune encephalomyelitis. Photochem Photobiol (1996)64:751-757.
31. Simkin GO, King DE, Chan AH, Hunt DW, Inhibition of contact hypersensitivity with different analogs of benzoporphyrin derivative. Immunopharmacology (1997) 37:221-230.
32. Richter AM, Kelly B, Chow J, Liu DJ, Towers GH, Dolphin D, Levy JG, Preliminary studies on a more effective phototoxic agent than hematoporphyrin. J Natl Cancer Inst (1987)79:1327-1332.
33. Stemberg E, Dolphin D, Pyrrolic photosensitizers. Curr Med Chem (1996) 3:239-272.
34. Runnels JM, Chen N, Kalo D, Hasan T, BPD-MA-mediated photosensitization in vitro and in vivo: Cellular adhesion and , integrin expression in ovarian cancer cells. Br J Cancer (1999) 80:946-953.
35. Kessel D, Luo Y, Mathieu P, Heiners JJ, Determinants of the apoptotic response to lysosomal photodamage. Photochem Photobiol (2000) 71:196-200.
36. King DE, Jiang H, Simkin GO, Obochi MO, Levy JG, Hunt DW, Photodynamic alteration of the surface receptor expression pattern of murine splenic dendritic cells. Scand J Immunol (1999) 49:184-192.
37. Hunt DW, Jiang H, Granville DJ, Chan AH, Leong S, Levy JG, Consequences of the photodynamic treatment of resting and activated peripheral T lymphocytes. Immunopharmacology(1999) 41:31-44.
38. Jamieson C, Hornby A, Richter A, Mitchell D, Levy J, Relative sensitivity of leukemic (CML) and normal progenitor cells to treatment with the photosensitizer benzoporphyrin derivative and light. J Hematother (1993) 2:383-386.
39. Arnold J, Blemenkranz M, Bressler NM, Bressler SB, Deslandes J-Y, Donati G, Fish G, Gragoudas ES, Harvey P, Huber G, Kaiser PK, Kaus L, Koenig F, Koester J, Lewis H, Lobes L, Margherio RR, Miller JW, Mones J, Murphy S, Reaves A, Rosenfeld PJ, Schachat AP, Schmidt-Erfurth U, Sickenberg M, Singerman L, Slakler JS, Strong HA, Stur M, Williams GA, Photodynamic therapy of subfoveal choroidal neovascularization in age-related macular degeneration with verteporfin: One-year results of 2 randomized clinical trials-TAP report. Treatment of agerelated macular degeneration with photodynamic therapy (TAP) study group. Arch Ophthalmol (1999) 117:1329-1345.
40. Green D, Kroemer G: The central executioners of apoptosis: Caspases or mitochondria? Trends Cell Biol (1998)8:267-271.
41. Kroemer G, Zamzami N, Susin SA, Mitochondria! control of apoptosis. Immunol Today (1997) 18:44-51.
42. Kroemer G, Mitochondria! implication in apoptosis. Towards an endosymbiont hypothesis of apoptosis evolution. Cell Death Differ (1997) 4:443-456.
43. Reed JC, Cytochrome c: Can't live with it - can't live Without it. Cell (1997) 91:559-562.
44. Hu Y, Benedict MA, Wu D, Inohara N, Nunez G, Bcl- Interacts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. Proc Natl Acad Sci USA (1998) 95:4386-4391.
45. Pan G, O'Rourke K, Dixit VM, Caspase-9, Bcl-X, and Apaf-1 form a ternary complex. J Biol Chem (1998) 273:5841-5845.
46. Qin H, Srinivasula SM, Wu G, Femandes-Alnemri T, Alnemri ES, Shi Y, Structural basis of procaspase-9 recruitment by the apoptotic protease-activating factor 1. Nature (1999) 399:549-557.
47. Srinivasula SM, Ahmad M, Femandes-Alnemri T, Alnemri ES, Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol Cell (1998) 1:949-957.
48. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X, Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell (1997) 91:479-489.
49. Vames ME, Chiu SM, Xue LY, Oleinick NL, Photodynamic therapy-induced apoptosis in lymphoma cells: Translocation of cytochrome c causes Inhibition of respiration as well as caspase activation. Biochem Biophys Res Commun (1999) 255:673-679.
50. Vantieghem A, Assefa Z, Vandenabeele P, Declercq W, Courtois S, Vandenheede JR, Merievede 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 f.eff (1998) 440:19-24.
51. 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 (1999) 70:650-655.
52. Zhang Z, Ao Z, Seth A, Schlossman SF, A mitochondria! mambrane protein defined by a novel monoclonal antibody Is preferentially detected in apoptotic cells. J Immunol (1996) 157:3980-3987.
53. Thomberry NA, Lazebnik Y, Caspases: Enemies within. Science (1998) 281:1312-1316.
54. Verma A, Nye JS, Snyder SH, Porphyrins are endogenous ligands for the mitochondrial (peripheral-type) benzodiazepine receptor. Proc Natl Acad Sci USA (1987) 84:2256-2260.
55. Verma A, Snyder SH: Characterization of porphyrin interactions with peripheral type benzodiazepine receptors. /Wo/P/7amiaco/(1988) 34:800-805.
56. Verma A, Facchina SL, Hirsch DJ, Song SY, Dillahey LF, Williams JR, Snyder SH: Photodynamic tumor therapy: Mitochondrial benzodiazepine receptors as a therapeutic target Mo/Med(1998) 4:40-45.
57. Anholt RR, Pedersen PL, De Souza EB, Snyder SH, The peripheral-type benzodiazepine receptor. Localization to the mitochondrial outer membrane. J Biol Chem (1986) 261:576-583.
58. Kinnally KW, Zorov DB, Antonenko YN, Snyder SH, McEnery MW, Tedeschi H, Mitochondrial benzodiazepine receptor linked to inner membrane ion channels by nanomolar actions of ligands. Proc Natl Acad Sci USA (1993) 90:13741378.
59. McEnery MW, Snowman AM, Trifiletti RR, Snyder SH, Isolation of the mitochondrial benzodiazepine receptor: Association with the voltage-dependent anion channel and the adenine nucleotide carrier. Proc Natl Acad Sci USA (1992)89:3170-3174.
60. Ricchelli F, Barbato P, Milani M, Gobbo S, Salet C, Moreno G, Photodynamic action of porphyrin on Ca influx in endoplasmic reticulum: A comparison with mitochondria. Biochem J (1999) 338:221-227.
61. Grover AK, Samson SE, Misquitta CM, Sarco(endo)plasm!c reticulum Ca2 pump isoform SERCA3 is more resistant than SERCA2b to peroxide. Am J Physiol (1997) 273:C420C425.
62. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J, Caspase-12 mediates endoplasmlc-reticulumspecific apoptosis and cytotoxicity by amyloid-. Nature (2000)403:98-103.
63. Yuan J, Evolutionary conservation of a genetic pathway of programmed cell death. J Cell Biochem (1996) 60:4-11.
64. Wu D, Wallen HD, Inohara N, Nunez G, Interaction and regulation of the Caenorhabditis elegans death protease CED-3 by CED-4 and CED-9. J Biol Chem (1997) 272:2144921454.
65. Martin SJ, Green 'OR: Protease activation during apoptosis: Death by a thousand cuts? Cell (1995) 82:349-352.
66. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thomberry NA, Wong WW, Yuan J, Human ICE/CED-3 protease nomenclature. Ce//(1996) 87:171.
67. Kennedy NJ, Kataoka T, Tschopp J, Budd RC, Caspase activation is required for T-cell proliferation. J Exp Med (1999)190:1891-1895.
68. Alam A, Cohen LY, Aouad S, Sekaly R-P, Early activation of caspases during T-lymphocyte stimulation results in selective substrate cleavage in nonapoptotic cells. J Exp Wed (1999) 190:1879-1890.
69. Reed JC, Caspases and cytokines: Roles in Inflammation and autoimmunity. Adv Immunol (1999) 73:265-299.
70. Granville DJ, Carthy CM, Jiang H, Levy JG, McManus BM, Matroule JY, Piette J, Hunt DW, Nuclear factor-KB activation by the photochemotherapeutic agent verteporfin. Blood (2000) 95:256-262.
71. Nicholson DW, Ali A, Thomberry NA, Vaillancourt JP, Ding CK, Gallant M, Gareau Y, Griffin PR, Labelle M, Lazebnik YA, Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature (1995) 376:37-43.
72. Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, Beidler DR, Poirier GG, Salvesen GS, Dixit VM, Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADPribose) polymerase. Cell (1995) 81:801-809.
73. Mancini M, Nicholson DW, Roy S, Thomberry NA, Peterson EP, Casciola-Rosen LA, Rosen A, The caspase-3 precursor has a cytosolic and mitochondria! distribution: Implications for apoptotic signaling. J Cell Bid (1998) 140:1485-1495.
74. Wang X, Zelenski NG, Yang J, Sakai J, Brown MS, Goldstein JL, Cleavage of sterol regulatory element binding proteins (SREBPs) by CPP32 during apoptosis. EMBO J (1996) 15:1012-1020.
75. Casciola-Rosen L, Nicholson DW, Chong T, Rowan KR, Thomberry NA, Miller DK, Rosen A, Apopain/CPP32 cleaves proteins that are essential for cellular repair: A fundamental principle of apoptotic death. J Exp Med (1996) 183:1957-1964.
76. Liu X, Zou H, Slaughter C, Wang X, OFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell (1997) 89:175-184.
77. Enari M, Talanian RV, Wong WW, Nagata S, Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature (1996) 380:723-726.
78. Kamada S, Washida M, Hasegawa J, Kusano H, Funahashi Y, Tsujimoto Y, Involvement of caspase-4(-)ike) protease in Fasmediated apoptotic pathway. Oncogene (1997) 15:285-290.
79. Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Litwack G, Alnemri ES, Molecular ordering of the Fas-apoptotic pathway: The Fas/APO-1 protease MchS is a CrmAinhibitable protease that activates multiple Ced-3/lCE-like cysteine proteases. Proc Natl Acad Sci USA (1996) 93:14486-14491.
80. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, Wang HG, Reed JC, Nicholson DW, Alnemri ES, Green DR, Martin SJ, Ordering the cytochrome cinitiated caspase cascade: Hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9- dependent manner. J Ce//B/o/(1999) 144:281-292.
81. Sun XM, MacFarïane M, Zhuang J, Wolf BB, Green DR, Cohen GM, Distinct caspase cascades are initiated in receptormediated and chemical-induced apoptosis. J Biol Chem (1999)274:5053-5060.
82. Pegoraro L, Palumbo A, Erikson J, Falda M, Giovanazzo B, Emanuel BS, Rovera G, Nowell PC, Croce CM, A 14;18 and an 8;14 chromosome translocation in a cell line derived from an acute B-cell leukemia. P roc Nat! Acad Sci USA (1984)81:7166-7170.
83. Tsujimoto Y, Jaffe E, Cossman J, Gorham J, Nowell PC, Croce CM, Clustering of breakpoints on chromosome 11 in human B-cell neoplasms with the t(11;14) chromosome translocation. Nature (1985) 315:340-343.
84. Reed JC, Regulation of apoptosis by bcl-2 family proteins and its role in cancer and chemoresistance. Curr Opin Oncol (1995) 7:541 -546.
85. Schlesinger PH, Gross A, Yin XM, Yamamoto K, Saito M, Waksman G, Korsmeyer SJ, Comparison of the ion channel characteristics of proapoptotic Bax and antiapoptotic Bcl2. Proc Natl Acad Sci USA (1997) 94:11357-11362.
86. Schendel SL, Azimov R, Pawlowski K, Godzik A, Kagan BL, Reed JC, Ion channel activity of the BH3 only Bcl-2 family member, Bid. J Biol Chem (1999) 274:21932-21936.
87. Schendel SL, Xie Z, Montai MO, Matsuyama S, Montai M, Reed JC, Channel formation by antiapoptotic protein Bcl-2. Proc Natl Acad Sci USA (1997) 94:5113-5118.
88. Marzo I, Brenner C, Zamzami N, Susin SA, Beutner G, Brdiczka D, Remy R, Xie ZH, Reed JC, Kroemer G, The permeability transition pore complex: A target for apoptosis regulation by caspases and Bcl-2-related proteins. JExp Med (1998) 187:1261-1271.
89. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X, Apaf-1, a human protein homologous to C elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell (1997) 90:405-413.
90. Oltvai ZN, Milliman CL, Korsmeyer SJ, Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell (1993) 74:609-619.
91. Yang E, Zha J, Jockei J, Boise LH, Thompson CB, Korsmeyer SJ, Bad, a heterodimeric partner for Bcl-XL and Bcl-2, displaces Bax and promotes cell death. Cell (1995) 80:285291.
92. Hsu YT, Youle RJ, Non-ionic detergents induce dimerization among members of the Bcl-2 family. J Biol Chem (1997) 272:3829-13834.
93. Diaz JL, Oltersdorf T, Home W, McConnell M, Wilson G, Weeks S, Garcia T, Fritz LC, A common binding site mediates heterodimerization and homodimerization of Bcl2 family members. J Biol Chem (1997) 272:11350-11355.
94. St Clair EG, Anderson SJ, Oltvai ZN, Bcl-2 counters apoptosis by Bax heterodimerization-dependent and independent mechanisms in the T-cell lineage. J Biol Chem (1997)272:29347-29355.
95. Kelekar A, Chang BS, Marian JE, Fesik SW, Thompson CB: Bad is a BH3 domain-containing protein that forms an Inactivating dimer with Bel-XL Mol Cell Bid (1997) 17:7040-7046.
96. Korsmeyer SJ, Yin XM, Oltvai ZN, Veis-Novack DJ, Linette GP, Reactive oxygen species and the regulation of cell death by the Bcl-2 gene family. Biochim Biophys Acta (1995) 1271:63-66.
97. Jacobson MD, Reactive oxygen species and programmed cell death. Trends Biochem Sci (1996) 21:83-86.
98. Rimpler MM, Rauen U, Schmidt T, Moray T, de Groot H, Protection against hydrogen peroxide cytotoxicity in rat-1 fibroblasts provided by the oncoprotein Bcl-2: Maintenance of calcium homoeostasis is secondary to the effect of Bcl-2 on cellular glutathione. Biochem J (1999) 340:291-297.
99. He J, Agarwal ML, Larkin HE, Friedman LR, Xue LY, Oleinick NL, The induction of partial resistance to photodynamic therapy by the protooncogene Bcl-2. Photochem Photobiol (1996) 64:845-852.
100. Kirn HR, Luo Y, Li G, Kessel D, Enhanced apoptotic response to photodynamic therapy after bc/-2transfection. Cancer Res (1999) 59:3429-3432.
101. Weller M, Trepel M, Grimmel C, Schabet M, Bremen D, Krajewski S, Reed JC, Hypericin-induced apoptosis of human malignant glioma cells is light-dependent, independent of bcl-2 expression, and does not require wild-type p53. NeurolRes (1997) 19:459-470.
102. Li H, Zhu H, Xu CJ, Yuan J, Cleavage of Bid by caspase 8 mediates the mitochondria! damage In the Fas pathway of apoptosis. Ce//(1998) 94:491-501.
103. Reed JC, Bcl-2 family proteins. Oncogene (1998) 17:3225-3236.
104. Reed JC, Dysregulation of apoptosis in cancer. Cancer J Sci Am (1998) 4(Suppl 1):S8-S14.
105. Ashkenazi A, Dixit VM, Death receptors: Signaling and modulation. Science (1998) 281:1305-1308.
106. Ogasawara J, Watanabe-Fukunaga R, Adachi M, Matsuzawa A, Kasugai T, Kitamura Y, Itoh N, Suda T, Nagata S, Lethal effect of the anti-Fas antibody in mice. Nature (1993) 364:806-809.
107. Rodriguez I, Matsuura K, Ody C, Nagata S, Vassalli P, Systemic injection of a tripeptide inhibits the intracellular activation of CPP32-like proteases In vivo and fully protects mice against Fas-mediated fulminant liver destruction and death. J Exp Med (1996) 184:2067-2072.
108. Bonavida B, Ng CP, Jazirehi A, Schiller G, Mizutani Y, Selectivity of TRAIL-mediated apoptosis of cancer cells and synergy with drugs: The trail to non-toxic cancer therapeutics (review). Int JOnco/(1999) 15:793-802.
109. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA, Blackie C, Chang L, McMurtrey AE, Hebert A, DeForge L, Koumenis IL, Lewis D, Harris L, Bussiere J, Koeppen H, Shahrokh Z, Schwall RH, Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest (1999) 104:155-162.
110. Rehemtulla A, Hamilton CA, Chinnaiyan AM, Dixit VM, Ultraviolet radiation-induced apoptosis is mediated by activation of CD-95 (Fas/APO-1). J Biol Chem (1997) 272:25783-25786.
111. Aragane Y, Kulms D, Metze D, Wilkes G, Poppelmann B, Luger TA, Schwarz T, Ultraviolet light induces apoptosis via direct activation of CD95 (Fas/APO-1) independently of its ligand CD95L. J Ce//B/o/(1998) 140:171-182.
112. Bellnier DA, Potentiation of photodynamic therapy In mice with recombinant human tumor necrosis factor-o. J Photochem Photobiol B (1991) 8:203-210.
113. Reiter I, Schwamberger G, Krammer B, Effect of photodynamic pretreatment on the susceptibility of murine tumor cells to macrophage antitumor mechanisms. Photochem Photobiol (1997) 66:384-388.
114. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M, Chin W, Jones J, Woodward A, Le T, Smith C, Smolak P, Goodwin RG, Rauch CT, Schuh JC, Lynch DH, Tumoricidal activity of tumor necrosis factor-related apoptosisinducing ligand In vivo. Nature Med (1999) 5:157-163.
115. Tibbies LA, Woodgett JR, The stress-activated protein kinase pathways. Cell Mol Life Sci (1999) 55:1230-1254.
116. Xue LY, Qiu Y, He J, Kung HJ, Oleinick NL, Etk/Bmx, a PHdomain containing tyrosine kinase, protects prostate cancer cells from apoptosis induced by photodynamic therapy or thapsigargln. Oncogens (1999) 18:3391-3398.
117. Xue L, He J, Oleinick NL, Promotion of photodynamic therapy-induced apoptosis by stress kinases. Cell Death Differ (1999) 6:855-864.
118. Tao J, Sanghera JS, Pelech SL, Wong G, Levy JG, Stimulation of stress-activated protein kinase and p38 HOG1 kinase in murine keratinocytes following photodynamic therapy with benzoporphyrin derivative. J Biol Chem (1996) 271:27107-27115.
119. Assefa Z, Vantieghem A, Declercq W, Vandenabeele P, Vandenheede JR, Mertevede W, de Witte P, Agostinis P, The activation of the c-Jun N-terminal kinase and p38 mitogenactivated protein kinase signaling pathways protects HeLa cells from apoptosis following photodynamic therapy with hypericin. J Biol Chem (1999) 274:8788-8796.
120. Xue LY, He J, Oleinick NL, 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 (1997) 66:1 OS113.
121. Klotz LO, 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 (1998) 58:4297-4300.
122. Lenczowski JM, Dominguez L, Eder AM, King LB, Zacharchuk CM, Ashwell JD, Lack of a role for Jun kinase and AP-1 in Fas-induced apoptosis. Mol Cell Biol (1997) 17:170-181.
123. Legrand-Poels S, Schoonbroodt S, Matroule JY, Piette J, NFxB: An important transcription factor in photobiology. J Photochem Photobiol B (1998) 45:1-8.
124. Ryter SW, Gomer CJ, Nuclear factor kappa B binding activity in mouse L1210 cells following Photofrin IImediated photosensitization. Photochem Photobiol (1993) 58:753-756.
125. 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-KB DNA binding. Cancer Res (1995) 55:2373-2379.
126. Kick G, Messer G, Plewig G, Kind P, Goetz AE, Strong and prolonged induction of c-jun and c-fos proto-oncogenes by photodynamic therapy. BrJ Cancer (1996) 74:30-36.
127. Matroule JY, Bonizzi G, Morliere P, Paillous N, Santus R, Bours V, Piette J, Pyropheophorbide-a methyl estermediated photosensitization activates transcription factor NF-KB through the interleukin-1 receptor-dependent signaling pathway. J Biol Chem (1999) 274:2988-3000.
128. Matroule J-Y, Hellin A-C, Morliere P, Fabiano A-S, Santus R, Merville MP, Piette J, Role of nuclear factor-xB in colon cancer cell apoptosis mediated by aminopyropheophorbide photosensitization. Photochem Photobiol (1999) 70:540-548.
129. Lee HH, Dadgostar H, Cheng Q, Shu J, Cheng G, NF-tcBmediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B-lymphocytes. Proc Natl AcadSci USA (1999) 96:9136-9141.
130. Wang CY, Guttridge DC, Mayo MW, Baldwin AS Jr, NF-x induces expression of the Bcl-2 homologue A1/Bfl-1 to preferentially suppress chemotherapy-induced apoptosis. Mol Cell Biol (1999) 19:5923-5929.
131. Stroka DM, Badrichani AZ, Bach FH, Ferran C, Overexpression of A1, an NF-KB-inducible anti-apoptotic bel gene, inhibits endothelial cell activation. Blood (1999) 93:3803-3810.
132. Zong WX, Edelstein LC, Chen C, Bash J, Gelinas C, The prosurvival Bcl-2 homolog Bf 1-1/A 1 is a direct transcriptional target of NF-KB that blocks TNFa-induced apoptosis. Genes Dei/(1999) 13:382-387.
133. Hu X, Yee E, Hartan JM, Wong F, Karsan A, Lipopolysaccharide induces the antiapoptotic molecules, A1 and A20, in microvascular endothelial cells. Blood (1998)92:2759-2765.
134. Wang CY, Mayo MW, Korneluk RG, Goeddel DV, Baldwin AS Jr, NF-KB antiapoptosis: Induction of TRAF1 and TRAF2 and C-IAP1 and C-IAP2 to suppress caspase-8 activation. Science (1998) 281:1680-1683.
135. Kasibhatla S, Genestier L, Green DR, Regulation of fasligand expression during activation-Induced cell death in T-lymphocytes via nuclear factor xB. J Biol Chem (1999) 274:987-992.
136. Fisher AM, Danenberg K, Banerjee D, Bertino JR, Danenberg P, Gomer CJ, Increased photosensitivity in HL60 cells expressing wild-type p53. Photochem Photobiol (1997) 66:265-270.
137. Fisher AM, Rucker N, Wong S, Gomer CJ, Differential photosensitivity in wild-type and mutant p53 human colon carcinoma cell lines. J Photochem Photobiol B (1998) 42:104-107.
138. Zhang W, Li XW, Ma LB, Wang SW, Yang HY, Zhang ZY, Wild-type p53 protein potentiates phototoxicity of 2-BA-2DMHA in HT29 cells expressing endogenous mutant p53. Cancer Lett (1999) 138:189-195.
139. Fisher AM, Ferrario A, Rucker N, Zhang S, Gomer CJ, Photodynamic therapy sensitivity is not altered in human tumor cells after abrogation of p53 function. Cancer Res (1999)59:331-335.