Cell death via mitochondrial apoptotic pathway due to activation of Bax by lysosomal photodamage

Free Radical Biology and Medicine

Volumn 51, Issue 1, 2011, Pages 53-68

  Liu, Lei ^a   Zhang, Zhenzhen ^a   Xing, Da ^a,b  

^a SOUTH CHINA NORMAL UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

Apoptosis; Bax; Free radicals; Lysosomal photodamage; Mitochondrial pathway; NPe6 PDT

Indexed keywords

ACETYLCYSTEINE; ASCORBIC ACID; CASPASE 3; CASPASE 9; CATHEPSIN; CYTOCHROME C; N ASPARTYL CHLORIN E6; PHOTOSENSITIZING AGENT; PROTEIN BAX; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CARCINOMA CELL; CELL ASSAY; CELL DEATH; CELL PROTECTION; CONTROLLED STUDY; DRUG CYTOTOXICITY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LUNG ADENOCARCINOMA; LYSOSOME; PHOTODYNAMIC THERAPY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ADENOCARCINOMA; APOPTOSIS; ASCORBIC ACID; BCL-2-ASSOCIATED X PROTEIN; CASPASE 3; CASPASE 9; CATHEPSINS; CELL LINE, TUMOR; CYTOCHROMES C; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; LUNG NEOPLASMS; LYSOSOMES; MICROSCOPY, CONFOCAL; MITOCHONDRIA; PHOTOSENSITIZING AGENTS; PORPHYRINS; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; RNA, SMALL INTERFERING;

EID: 79957969020     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.03.042     Document Type: Article

References (45)

1. R.D. Almeida, B.J. Manadas, A.P. Carvalho, and C.B. Duarte Intracellular signaling mechanisms in photodynamic therapy Biochim. Biophys. Acta 1704 2004 59 86 (Pubitemid 39195350)
2. E. Buytaert, M. Dewaele, and P. Agostinis Molecular effectors of multiple cell death pathways initiated by photodynamic therapy Biochim. Biophys. Acta 1776 2007 86 107 (Pubitemid 47332075)
3. J.P. Celli, B.Q. Spring, I. Rizvi, C.L. Evans, K.S. Samkoe, S. Verma, B.W. Pogue, and T. Hasan Imaging and photodynamic therapy: mechanisms, monitoring, and optimization Chem. Rev. 110 2010 2795 2838
4. M.H. Teiten, L. Bezdetnaya, P. Morliere, R. Santus, and F. Guillemin Endoplasmic reticulum and Golgi apparatus are the preferential sites of Foscan localisation in cultured tumour cells Br. J. Cancer 88 2003 146 152 (Pubitemid 36241232)
5. R.L. Morris, K. Azizuddin, M. Lam, J. Berlin, A.L. Nieminen, M.E. Kenney, A.C. Samia, C. Burda, and N.L. Oleinick Fluorescence resonance energy transfer reveals a binding site of a photosensitizer for photodynamic therapy Cancer Res. 63 2003 5194 5197 (Pubitemid 37139826)
6. J. Usuda, S.M. Chiu, E.S. Murphy, M. Lam, A.L. Nieminen, and N.L. Oleinick 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 (Pubitemid 36801445)
7. D. Kessel, Y. Luo, Y. Deng, and C.K. Chang The role of subcellular localization in initiation of apoptosis by photodynamic therapy Photochem. Photobiol. 65 1997 422 426 (Pubitemid 27158974)
8. B.B. Noodt, K. Berg, T. Stokke, Q. Peng, and J.M. Nesland Different apoptotic pathways are induced from various intracellular sites by tetraphenylporphyrins and light Br. J. Cancer 79 1999 72 81 (Pubitemid 28566929)
9. D. Kessel, R. Luguya, and M.G. Vicente Localization and photodynamic efficacy of two cationic porphyrins varying in charge distributions Photochem. Photobiol. 78 2003 431 435
10. N.L. Oleinick, R.L. Morris, and I. Belichenko The role of apoptosis in response to photodynamic therapy: what, where, why, and how Photochem. Photobiol. Sci. 1 2002 1 21 (Pubitemid 37069701)
11. J. Moan, and K. Berg The photodegradation of porphyrins in cells can be used to estimate the lifetime of singlet oxygen Photochem. Photobiol. 53 1991 549 553
12. D. Kessel, Y. Luo, P. Mathieu, and J.J. Reiners Jr. Determinants of the apoptotic response to lysosomal photodamage Photochem. Photobiol. 71 2000 196 200
13. J.J. Reiners Jr., J.A. Caruso, P. Mathieu, B. Chelladurai, X.M. Yin, and D. Kessel Release of cytochrome c and activation of pro-caspase-9 following lysosomal photodamage involves Bid cleavage Cell Death Differ. 9 2002 934 944 (Pubitemid 35033432)
14. J.A. Caruso, P.A. Mathieu, A. Joiakim, B. Leeson, D. Kessel, B.F. Sloane, and J.J. Reiners Jr. Differential susceptibilities of murine hepatoma 1c1c7 and Tao cells to the lysosomal photosensitizer NPe6: influence of aryl hydrocarbon receptor on lysosomal fragility and protease contents Mol. Pharmacol. 65 2004 1016 1028 (Pubitemid 38420508)
15. J.A. Caruso, P.A. Mathieu, and J.J. Reiners Jr. Sphingomyelins suppress the targeted disruption of lysosomes/endosomes by the photosensitizer NPe6 during photodynamic therapy Biochem. J. 392 2005 325 334 (Pubitemid 41796521)
16. Q. Wan, L. Liu, D. Xing, and Q. Chen Bid is required in NPe6-PDT-induced apoptosis Photochem. Photobiol. 84 2008 250 257 (Pubitemid 350265108)
17. D.R. Green, and G. Kroemer The pathophysiology of mitochondrial cell death Science 305 2004 626 629 (Pubitemid 39006738)
18. A. Antignani, and R.J. Youle How do Bax and Bak lead to permeabilization of the outer mitochondrial membrane? Curr. Opin. Cell Biol. 18 2006 685 689 (Pubitemid 44692478)
19. J.M. Adams, and S. Cory Bcl-2-regulated apoptosis: mechanism and therapeutic potential Curr. Opin. Immunol. 19 2007 488 496 (Pubitemid 47487452)
20. E. Buytaert, G. Callewaert, N. Hendrickx, L. Scorrano, D. Hartmann, L. Missiaen, J.R. Vandenheede, I. Heirman, J. Grooten, and P. Agostinis Role of endoplasmic reticulum depletion and multidomain proapoptotic BAX and BAK proteins in shaping cell death after hypericin-mediated photodynamic therapy FASEB J. 20 2006 756 758 (Pubitemid 46671205)
21. D.J. Granville, J.R. Shaw, S. Leong, C.M. Carthy, P. Margaron, D.W. Hunt, and B.M. McManus 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 (Pubitemid 29488907)
22. R. Bhowmick, and A.W. Girotti Signaling events in apoptotic photokilling of 5-aminolevulinic acid-treated tumor cells: inhibitory effects of nitric oxide Free Radic. Biol. Med. 47 2009 731 740
23. S.M. Chiu, L.Y. Xue, J. Usuda, K. Azizuddin, and N.L. Oleinick Bax is essential for mitochondrion-mediated apoptosis but not for cell death caused by photodynamic therapy Br. J. Cancer 89 2003 1590 1597 (Pubitemid 37386619)
24. J.M. Adams Ways of dying: multiple pathways to apoptosis Genes Dev. 17 2003 2481 2495 (Pubitemid 37271417)
25. Y. Shi Mechanisms of caspase activation and inhibition during apoptosis Mol. Cell 9 2002 459 470 (Pubitemid 34273778)
26. Y. Zhang, D. Xing, and L. Liu PUMA promotes Bax translocation by both directly interacting with Bax and by competitive binding to Bcl-X L during UV-induced apoptosis Mol. Biol. Cell 20 2009 3077 3087
27. L. Liu, D. Xing, W.R. Chen, T. Chen, Y. Pei, and X. Gao Calpain-mediated pathway dominates cisplatin-induced apoptosis in human lung adenocarcinoma cells as determined by real-time single cell analysis Int. J. Cancer 122 2008 2210 2222 (Pubitemid 351542323)
28. L. Liu, D. Xing, and W.R. Chen Micro-calpain regulates caspase-dependent and apoptosis inducing factor-mediated caspase-independent apoptotic pathways in cisplatin-induced apoptosis Int. J. Cancer 125 2009 2757 2766
29. L.Y. Xue, S.M. Chiu, and N.L. Oleinick Photochemical destruction of the Bcl-2 oncoprotein during photodynamic therapy with the phthalocyanine photosensitizer Pc 4 Oncogene 20 2001 3420 3427 (Pubitemid 32588990)
30. R. Ishisaka, T. Utsumi, T. Kanno, K. Arita, N. Katunuma, J. Akiyama, and K. Utsumi Participation of a cathepsin L-type protease in the activation of caspase-3 Cell Struct. Funct. 24 1999 465 470 (Pubitemid 30128954)
31. 2+: a control point for apoptosis Science 300 2003 135 139 (Pubitemid 36423046)
32. W.X. Zong, C. Li, G. Hatzivassiliou, T. Lindsten, Q.C. Yu, J. Yuan, and C.B. Thompson Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis J. Cell Biol. 162 2003 59 69 (Pubitemid 36859535)
33. K. Kagedal, A.C. Johansson, U. Johansson, G. Heimlich, K. Roberg, N.S. Wang, J.M. Jurgensmeier, and K. Ollinger Lysosomal membrane permeabilization during apoptosis-involvement of Bax? Int. J. Exp. Pathol. 86 2005 309 321 (Pubitemid 41413626)
34. A.E. Feldstein, N.W. Werneburg, Z. Li, S.F. Bronk, and G.J. Gores Bax inhibition protects against free fatty acid-induced lysosomal permeabilization Am. J. Physiol. 290 2006 G1339 G1346
35. L.D. Walensky, K. Pitter, J. Morash, K.J. Oh, S. Barbuto, J. Fisher, E. Smith, G.L. Verdine, and S.J. Korsmeyer A stapled BID BH3 helix directly binds and activates BAX Mol. Cell 24 2006 199 210 (Pubitemid 44557124)
36. S.N. Willis, J.I. Fletcher, T. Kaufmann, M.F. van Delft, L. Chen, P.E. Czabotar, H. Ierino, E.F. Lee, W.D. Fairlie, P. Bouillet, A. Strasser, R.M. Kluck, J.M. Adams, and D.C. Huang Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak Science 315 2007 856 859
37. R.T. Uren, G. Dewson, L. Chen, S.C. Coyne, D.C. Huang, J.M. Adams, and R.M. Kluck Mitochondrial permeabilization relies on BH3 ligands engaging multiple prosurvival Bcl-2 relatives, not Bak J. Cell Biol. 177 2007 277 287 (Pubitemid 46658639)
38. N. Bidere, H.K. Lorenzo, S. Carmona, M. Laforge, F. Harper, C. Dumont, and A. Senik Cathepsin D triggers Bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis J. Biol. Chem. 278 2003 31401 31411 (Pubitemid 36994661)
39. R. Castino, N. Bellio, G. Nicotra, C. Follo, N.F. Trincheri, and C. Isidoro Cathepsin D-Bax death pathway in oxidative stressed neuroblastoma cells Free Radic. Biol. Med. 42 2007 1305 1316 (Pubitemid 46467267)
40. J.E. Chipuk, T. Kuwana, L. Bouchier-Hayes, N.M. Droin, D.D. Newmeyer, M. Schuler, and D.R. Green Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis Science 303 2004 1010 1014 (Pubitemid 38209704)
41. J.E. Chipuk, L. Bouchier-Hayes, T. Kuwana, D.D. Newmeyer, and D.R. Green PUMA couples the nuclear and cytoplasmic proapoptotic function of p53 Science 309 2005 1732 1735 (Pubitemid 41285944)
42. G. Gao, and Q.P. Dou N-terminal cleavage of bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes bcl-2-independent cytochrome C release and apoptotic cell death J. Cell. Biochem. 80 2000 53 72
43. P.F. Cartron, L. Oliver, P. Juin, K. Meflah, and F.M. Vallette The p18 truncated form of Bax behaves like a Bcl-2 homology domain 3-only protein J. Biol. Chem. 279 2004 11503 11512 (Pubitemid 38401650)
44. D.E. Dolmans, D. Fukumura, and R.K. Jain Photodynamic therapy for cancer Nat. Rev. Cancer 3 2003 380 387 (Pubitemid 37328858)
45. A.P. Castano, P. Mroz, and M.R. Hamblin Photodynamic therapy and anti-tumour immunity Nat. Rev. Cancer 6 2006 535 545 (Pubitemid 43980542)