Dissociation of mitochondrial depolarization from cytochrome c release during apoptosis induced by photodynamic therapy

British Journal of Cancer

Volumn 84, Issue 8, 2001, Pages 1099-1106

  Chlu, S M ^a   Olelnick, N L ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Cytochrome c; Membrane potential; Mitochondria; Photodynamic therapy; Phthalocyanine Pc 4

Indexed keywords

CASPASE 3; CYTOCHROME C; PHTHALOCYANINE DERIVATIVE;

ANIMAL CELL; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CORRELATION FUNCTION; ENZYME ACTIVITY; ENZYME RELEASE; IMMUNOHISTOCHEMISTRY; IRRADIATION; LIGHT DAMAGE; LYMPHOMA; MITOCHONDRION; MOUSE; NONHUMAN; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; CYTOCHROME C GROUP; DOSE-RESPONSE RELATIONSHIP, DRUG; INDOLES; LYMPHOMA; MEMBRANE POTENTIALS; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; PHOTOCHEMOTHERAPY; PHOTOSENSITIZING AGENTS; TIME FACTORS; TUMOR CELLS, CULTURED;

EID: 0035917568     PISSN: 00070920     EISSN: None     Source Type: Journal    
DOI: 10.1054/bjoc.2000.1714     Document Type: Article

References (47)

1. Agarwal ML, Clay ME, Harvey EJ, Evans HH, Antunez AR and Oleinick NL (1991) Photodynamic therapy induces rapid cell death by apoptosis in L5178Y mouse lymphoma cells. Cancer Res 51: 5993-5996
2. Ankarcrona M, Dypbukt JM, Orrenius S and Nicotera P (1996) Calcineurin and mitochondrial function in glutamate-induced neuronal cell death. FEBS Lett 394: 321-324
3. Bossy-Wetzel E, Newmeyer DD and Green DR (1998) Mitochondrial cytochrome crelease in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J 17:37-49
4. Carthy CM, Granville DJ, Jiang H, Levy J, Rudin CM, Thompson CB, McManus BM and Hunt DWC (1999) 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 79: 953-965.
5. Chaloupka R, Petit PX, Israel N and Sureau F (1999) Overexpression 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: 295-301
6. Chiu SM, Evans HH, Lam M, Nieminen AL and Oleinick NL (2001) Phthalocyanine 4 photodynamic therapy-induced apoptosis of mouse L51787 - R cells results from a delayed but extensive release of cytochrome C from mitochondria. Cancer Le H (in press)
7. Cortese JD, and Hackenbrock CR (1993) Motional dynamics of functional cytochrome c delivered by low pH fusion into the intermembrane space of intact mitochondria. Biochim Biophys Acta 1142: 194-202
8. Cossarizza A, Baccarani Contri M, Kalashnikova G and Fransceschi C (1993) A new method for the cytofluororimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5, 5′, 6,6′-tetrachloro-1, 1′, 3,3′ -tetraethylbenzimidazolylcarbocyanine iodide (JC-1). Biochem Biophys Res Commun 197: 40-45
9. Dougherty TJ (1993) Photodynamic therapy. Photochem Photobiol 58: 895-900
10. Dougherty TJ, Gomer CJ, Henderson BW, Jori G, Kessel D, Korbelik M, Moan J and Peng Q (1998) Photodynamic Therapy: Review, J Natl Cancer Inst 90: 889-902
11. Emaus RK, Grunwald R and Lemasters JJ (1986) Rhodamine 123 as a probe of transmembrane potential in isolated rat-liver mitochondria: special and metabolic properties. Biochim Biophys Acta 850: 436-448
12. Enari M, Sahahira H, Yokoyama H, Okawa K, Iwamatsu A and Nagata S (1998) A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391: 43-50
13. 2+ ions. J Cell Biol 143: 216-224
14. Finucane DM, Bossy-Wetzel E, Waterhouse NJ, Cotter TG and Green DR (1999a) Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibited by Bcl-xL. J Biol Chem 274: 2225-2233
15. Finucane DM, Waterhouse NJ, Amarante-Mendes GP, Cotter TG and Green DR (1999b) Collapse of the inner mitochondrial transmembrane potential is not required for apoptosis of HL60 cells. Exp Cell Res 251: 166-174
16. Goldstein JC, Waterhouse NJ, Julin P, Evan GI and Green DR (2000) The coordinate release of cytochrome c during apoptosis is rapid, complete and kinetically invariant. Nature Cell Biol 2: 156-162
17. Granville DJ, Carthy CM, Jiang H, Shore GC, McManus BM and Hunt DW (1998) Rapid cytochrome c release, activation of caspases 3, 6, 7 and 8 followed by Bap31 cleavage in HeLa cells treated wilh photodynamic therapy. FEBS Lett 437: 5-10
18. Granville DJ, Jiang H, An MT, Levy JG, McManus BM and Hunt DWC (1999) Bcl-2 overexpression blocks caspase activation and downstream apoptotic events instigated by photodynamic therapy. Br J Cancer 79: 95-100
19. Green DR and Reed JC (1998) Mitochondria and apoptosis. Science 281: 1309-1312
20. Gross A, McDonnell JM and Korsmeyer SJ (1999) Bcl-2 family members and the mitochondria in apoptosis. Genes & Develop 13: 1899-1911
21. He XY, Sikes RA, Thomsen S, Chung LWK and Jacques SL (1994) Photodynamic therapy with Photofrin II induces programmed cell death in carcinoma cell lines. Photochem Photobiol 59: 468-473
22. He J, Whitacre CM, Xue L-y, Berger NA and Oleinick NL (1998) Protease activation and cleavage of Poly (ADP-ribose) polymerase: An integral part of apoptosis in response to photodynamic treatment. Cancer Res 58: 940-946
23. Heiskanen KM, Bhat MB, Wang H-W, Ma J, and Nieminen A-L (1999) Mitochondrial depolarization accompanies cytochrome c release during apoptosis in PC6 cells. J Biol Chem 274: 5654-5658
24. Johnson LV, Walsh ML, Bockus BJ and Chen LB (1981) Monitoring of relative mitochondrial membrane potential in living cells by fluorescence microscopy. J Cell Biol 88: 526-535
25. Kessel D and Luo Y (1998) Mitochondrial photodamage and PDT-induced apoptosis. J Photochem Photobiol B Biol 42: 89-95
26. Kessel D and Luo Y (1999) Photodynamic therapy: a mitochondrial inducer of apoptosis. Cell Death Differ 6: 28-35
27. Kluck RM, Bossy-Wetzel E, Green DR and Newmeyer DD (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136
28. Kroemer G, Zamzami N and Susin SA (1997) Mitochondrial control of apoptosis. Immunol Today 18: 44-51
29. Lemasters JJ, Nieminen A-L, Qian T, Trost LC, Elmore SP, Nishimura Y, Crowe RA, Cascio WE, Bradham CA, Brenner DA and Herman B (1998) The mitochondrial permeability transition in cell death: a common mechanism in necrosis, apoptosis and autophagy. Biochim Biophys Acta 1366: 177-196
30. Liu X, Kim CN, Yang J, Jemmerson R and Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147-157
31. Liu X, Zou H, Slaughter C and Wang X (1997) DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89: 175-184
32. Luo Y and Kessel D (1997) Initiation of apoptosis versus necrosis by photodynamic therapy with chloroaluminum phthalocyanine. Photochem Photobiol 66:479-483
33. Luo Y, Chang CK and Kessel D (1996) Rapid initiation of apoptosis by photodynamic therapy. Photochem Photobiol 63: 528-534
34. Martinou J-C, Desagher S and Antonsson B (2000) Cytochrome c release from mitochondria: all or nothing. Nature Cell Biol 2: E41-E43
35. Moan J and Berg K (1992) Photochemotherapy of cancer: experimental research. Photochem Photobiol 55: 931-948
36. Oleinick NL and Evans HH (1998) The photobiology of photodynamic therapy: Cellular targets and mechanisms. Radiat Res 150: S146-S156
37. Pastorino JG, Tafani M, Rothman RJ, Marcineviciute A, Hoek JB and Farber JL (1999) Functional consequences of the sustained or transient activation by Bax of the mitochondrial permeability transition pore. J Biol Chem 274: 31734-31739
38. Reed JC, Jurgensmeier JM and Matsuyama S (1998) Bcl-2 family proteins and mitochondria. Biochim Biophys Acta 1366: 127-137
39. Rosse T, Olivier R, Monney L, Rager M, Conus S, Fellay I, Jansen B and Borner C (1998) Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature 391: 496-499
40. Srinivasan A, Li F, Wong A, Kodandapani L, Smidt R Jr, Krebs JF, Fritz LC, Wu JC and Tomaselli KJ (1998) Bcl-xl functions downstream of caspase-8 to inhibit Fas-and tumor necrosis factor receptor 1-induced apoptosis of MCF7 breast carcinoma cells. J Biol Chem 273: 4523-4529
41. Susin SA, Zamzami N and Kroemer G (1998) Mitochondria as regulators of apoptosis: doubt no more. Biochim Biophys Acta 1366: 151-165
42. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM and Kroemer G (1999) Molecular characterization of mitochondrial apoptosis- inducing factor. Nature 397: 441-446
43. Vander Heiden MG, Chandel NS, Williamson EK, Schumacker PT and Thompson CB (1997) Bcl-xl regulates the membrane potential and volume homeostasis of mitochondria. Cell 91: 627-637
44. Varnes ME, Chiu SM, Xue LY and Oleinick NL (1999) 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: 673-679
45. Weishaupt KR, Gomer CJ and Doughetty TJ (1976) Identification of singlet oxygen as the cytotoxic agent in photoinactivation of a murine tumor. Cancer Res 36: 2326-2329
46. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP and Wang X (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275: 1129-1132
47. Zoratti M and Szabo L (1995)The mitochondrial permeability transition. Biochim Biophys Acta 1241: 139-176