Taiwan cobra cardiotoxins induce apoptotic death of human neuroblastoma SK-N-SH cells mediated by reactive oxygen species generation and mitochondrial depolarization

Toxicon

Volumn 51, Issue 4, 2008, Pages 624-634

  Chen, Ku Chung ^a   Chiou, Yi Ling ^a   Kao, Pei Hsiu ^a   Lin, Shinne Ren ^b   Chang, Long Sen ^a  

^a NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Cardiotoxin; Cytotoxicity; Mitochondrial dysfunction; ROS generation

Indexed keywords

2,3 DIHYDROXYBENZOIC ACID; ANTIOXIDANT; CASPASE 3 INHIBITOR; COBROTOXIN; COBROTOXIN 3; COBROTOXIN 4; CYCLOSPORIN A; CYTOCHROME C; REACTIVE OXYGEN METABOLITE; SNAKE VENOM; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DEATH; CELL MEMBRANE PERMEABILITY; CYTOTOXICITY; DEPOLARIZATION; HUMAN; HUMAN CELL; MITOCHONDRION; NEUROBLASTOMA CELL; PRIORITY JOURNAL;

NAJA ATRA;

EID: 40249118306     PISSN: 00410101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxicon.2007.11.024     Document Type: Article

References (42)

1. A. Bilwes B. Rees D. Moras R. Menez A. Menez X-ray structure at 1.55 Å of toxin γ , a cardiotoxin from Naja nigricollis venom. Crystal packing reveals a model for insertion into membranes J. Mol. Biol. 239 1994 122 136
2. J. Chandra A. Samali S. Orrenius Triggering and modulation of apoptosis by oxidative stress Free Radic. Biol. Med. 29 2000 323 333
3. E. Cadenas K.J.A. Davies Mitochondrial free radical generation, oxidative stress, and aging Free Radic. Biol. Med. 29 2000 222 230
4. K.C. Chen P.H. Kao S.R. Lin L.S. Chang The mechanism of cytotoxicity by Naja naja atra cardiotoxin 3 is physically distant from its membrane-damaging effect Toxicon 50 2007 816 824
5. Y.M. Chung Y.S. Bae S.Y. Lee Molecular ordering of ROS production, mitochondrial changes, and caspase activation during sodium salicylate-induced apoptosis Free Radic. Biol. Med. 34 2003 434 442
6. S. David M.J. Weiss J.R. Wong T.J. Lampidis L.B. Chen Mitochondrial and plasma membrane potentials cause unusual accumulation and retention of rhodamine 123 by human breast adenocarcinma-derived MCF-7 cells J. Biol. Chem. 260 1985 13844 13850
7. M.J. Dufton R.C. Hider The structure and pharmacology of elapid cytotoxins A.L. Harvey Snake Toxins 1991 Pergamon Press New York 259 302
8. A.V. Feofanov G.V. Sharonov M.V. Astapova D.I. Rodionov Y.N. Utkin A.S. Arseniev Cancer cell injury by cytotoxins from cobra venom is mediated through lysosomal damage Biochem. J. 390 2005 11 18
9. T. Finkel N.J. Holbrook Oxidants, oxidative stress and the biology of ageing Nature 408 2000 239 247
10. F. Forouhar W.N. Huang J.H. Liu K.Y. Chien W.G. Wu C.D. Hsiao Structural basis of membrane-induced cardiotoxin A3 oligomerization J. Biol. Chem. 278 2003 21980 21988
11. E. Gatineau F. Toma T. Montenay-Garestier M. Takechi P. Fromageot A. Menez Role of tyrosine and tryptophan residues in the structure–activity relationships of a cardiotoxin from Naja nigricollis venom Biochemistry 26 1987 8046 8055
12. E. Gatineau M. Takechi F. Bouet P. Mansuelle H. Rochat A.L. Harvey T. Montenay-Garestier A. Menez Delineation of the functional site of a snake venom cardiotoxin: preparation, structure, and function of monoacetylated derivatives Biochemistry 29 1990 6480 6489
13. D.R. Green J.C. Reed Mitochondria and apoptosis Science 281 1998 1309 1312
14. M.O. Hengartner The biochemistry of apoptosis Nature 407 2000 770 776
15. G. Jayaraman T.K. Kumar C.C. Tsai S. Srisailam S.H. Chou C.L. Ho C. Yu Elucidation of the solution structure of cardiotoxin analogue V from the Taiwan cobra ( Naja naja atra ), identification of structural features important for the lethal action of snake venom cardiotoxins Protein Sci. 9 2000 637 646
16. G. Kroemer J.C. Reed Mitochondrial control of cell death Nat. Med. 6 2000 513 519
17. G. Kroemer P. Petit N. Zamzami J.L. Vayssiere B. Mignotte The biochemistry of programmed cell death FASEB J. 9 1995 1277 1287
18. G. Kroemer B. Dallaporta M. Resche-Rigon The mitochondrial death/life regulator in apoptosis and necrosis Annu. Rev. Physiol. 60 1998 619 642
19. P. Li D. Nijhawan I. Budihardjo S.M. Srinivasula E.S. Ahmad E.S. Alnemri X. Wang Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade Cell 14 1997 479 489
20. L.Y. Li X. Luo X. Wang Endonuclease G is an apoptotic DNase when released from mitochondria Nature 412 2001 95 99
21. S.R. Lin L.S. Chang K.L. Chang Separation and structure–function studies of Taiwan cobra cardiotoxins J. Protein Chem. 21 2002 81 86
22. D. Ma A. Armugam K. Jeyaseelan Cytotoxic potency of cardiotoxin from Naja sputatrix : development of a new cytolytic assay Biochem. J. 366 2002 35 43
23. I. Matsuzaki S. Chatterjee K. DeBolt Y. Manevich Q. Zhang A.B. Fisher Membrane depolarization and NADPH oxidase activation in aortic endothelium during ischemia reflect altered mechanotransduction Am. J. Physiol. Heart Circ. Physiol. 288 2005 336 343
24. M.P. Mattson Apoptosis in neurodegenerative disorders Nat. Rev. Mol. Cell Biol. 1 2000 120 129
25. D.G. Nicholls Simultaneous monitoring of ionophore- and inhibitor-mediated plasma and mitochondrial membrane potential changes in cultured neurons J. Biol. Chem. 281 2006 14864 14874
26. M. Obrero D.V. Yu D.J. Shapiro Estrogen receptor-dependent and estrogen receptor-independent pathways for tamoxifen and 4-hydroxytamoxifen-induced programmed cell death J. Biol. Chem. 277 2002 45695 45703
27. H.V. Patel A.A. Vyas K.A. Vyas Y.S. Liu C.M. Chiang L.M. Chi W.G. Wu Heparin and heparan sulfate bind to snake cardiotoxin. Sulfated oligosaccharides as a potential target for cardiotoxin action J. Biol. Chem. 272 1997 1484 1492
28. S.J. Reidl Y. Shi Molecular mechanisms of caspase regulation during apoptosis Nat. Rev. Mol. Cell Biol. 5 2004 897 907
29. H.U. Simon A. Haj-Yehia F. Levi-Schaffer Role of reactive oxygen species (ROS) in apoptosis induction Apoptosis 5 2000 415 418
30. E.A. Slee M.T. Harte R.M. Kluck B.B. Wolf C.A. Casiano D.D. Newmeyer H.G. Wang J.C. Reed D.W. Nicholson E.S. Alnemri D.R. Green S.J. Martin Ordering the cytochrome c -initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner J. Cell Biol. 144 1999 281 292
31. R. Stevens-Truss C.L. Hinman Chemical modification of methionines in a cobra venom cytotoxin differentiates between lytic and binding domains Toxicol. Appl. Pharmacol. 139 1996 234 242
32. R. Stevens-Truss C.L. Hinman Activities of cobra venom cytotoxins toward heart and leukemic T-cells depend on localized amino acid differences Toxicon 35 1997 659 669
33. S.H. Su S.J. Su S.R. Lin K.L. Chang Cardiotoxin-III selectively enhances activation-induced apoptosis of human CD8+ T lymphocytes Toxicol. Appl. Pharmacol. 193 2003 97 105
34. S.C. Sue K.Y. Chien W.N. Huang J.K. Abraham K.M. Chen W.G. Wu Heparin binding stabilizes the membrane-bound form of cobra cardiotoxin J. Biol. Chem. 277 2002 2666 2673
35. Y.J. Sun W.G. Wu C.M. Chiang A.Y. Hsin C.D. Hsiao Crystal structure of cardiotoxin V from Taiwan cobra venom: pH-dependent conformational change and a novel membrane-binding motif identified in the three-finger loops of P-type cardiotoxin Biochemistry 36 1997 2403 2413
36. S.C. Tjong P.L. Wu C.M. Wang W.N. Huang N.L. Ho W.G. Wu Role of glycosphingolipid conformational change in membrane pore forming activity of cobra cardiotoxin Biochemistry 46 2007 12111 12123
37. C.H. Wang W.G. Wu Amphiphilic β -sheet cobra cardiotoxin targets mitochondria and disrupts its network FEBS Lett. 579 2005 3169 3174
38. C.H. Wang R. Monette S.C. Lee P. Morley W.G. Wu Cobra cardiotoxin-induced cell death in fetal rat cardiomyocytes and cortical neurons: different pathway but similar cell surface target Toxicon 46 2005 430 440
39. C.H. Wang J.H. Liu S.C. Lee C.D. Hsiao W.G. Wu Glycosphingolipid-facilitated membrane insertion and internalization of cobra cardiotoxin. The sulfatide-cardiotoxin complex structure in a membrane-like environment suggests a lipid-dependent cell-penetrating mechanism for membrane binding polypeptides J. Biol. Chem. 281 2006 656 667
40. S.H. Yang C.M. Chien M.C. Lu Y.H. Lin X.W. Hu S.R. Lin Up-regulation of Bax and endonuclease G, and down-modulation of Bcl-XL involved in cardiotoxin III-induced apoptosis in K562 cells Exp. Mol. Med. 38 2006 435 444
41. ATP channel dependent Am. J. Physiol. Heart Circ. Physiol. 289 2005 954 961
42. K.C. Zimmermann D.R. Green How cells die: apoptosis pathways J. Allergy Clin. Immunol. 108 2001 S99 S103