Differential involvement of Bax and Bak in TRAIL-mediated apoptosis of leukemic T cells

Leukemia

Volumn 18, Issue 10, 2004, Pages 1671-1680

  Han, J ^a   Goldstein, L A ^a   Gastman, B R ^a   Rabinovitz, A ^a   Wang, G Q ^a   Fang, B ^b   Rabinowich, H ^a,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

Apoptosis; Bak; Bax; Cytochrome c; Leukemia; Mitochondria; TRAIL

Indexed keywords

ADENOVIRUS VECTOR; ANTINEOPLASTIC AGENT; BENZYLOXYCARBONYLISOLEUCYLGLUTAMYLTHREONYLASPARTYL FLUOROMETHYL KETONE; BENZYLOXYCARBONYLVALYLALANYLASPARTYL FLUOROMETHYL KETONE; BETULIC ACID; CASPASE 3; CASPASE 3 INHIBITOR; CISPLATIN; CYTOTOXIC AGENT; ETOPOSIDE; LONIDAMINE; MITOCHONDRIAL PROTEIN; PACLITAXEL; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN SUBUNIT; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER RESISTANCE; CELL VIABILITY; CELLULAR IMMUNITY; CHEMOSENSITIVITY; CLINICAL OBSERVATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; LEUKEMIA CELL; LEUKEMOGENESIS; NONHUMAN; PRIORITY JOURNAL; T CELL LEUKEMIA; TUMOR IMMUNITY; VIRAL GENE DELIVERY SYSTEM;

EID: 6344253246     PISSN: 08876924     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.leu.2403496     Document Type: Article

References (60)

1. Green DR. Apoptotic pathways: paper wraps stone blunts scissors. Cell 2000; 102: 1-4.
2. Cande C, Cohen I, Daugas E, Ravagnan L, Larochette N, Zamzami N et al. Apoptosis-inducing factor (AIF): a novel caspase-independent death effector released from mitochondria. Biochimie 2002; 84: 215-222.
3. Daugas E, Susin SA, Zamzami N, Ferri KF, Irinopoulou T, Larochette N et al. Mitochondrio-nuclear translocation of AIF in apoptosis and necrosis. FASEB J 2000; 14: 729-739.
4. Hegde R, Srinivasula SM, Zhang Z, Wassell R, Mukattash R, Cilenti L et al. Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J Biol Chem 2002; 277: 432-438.
5. Srinivasula SM, Hegde R, Saleh A, Datta P, Shiozaki E, Chai J et al. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 2001; 410: 112-116.
6. Wu G, Chai J, Suber TL, Wu JW, Du C, Wang X et al. Structural basis of IAP recognition by Smac/DIABLO. Nature 2000; 408: 1008-1012.
7. Li S, Zhao Y, He X, Kim TH, Kuharsky DK, Rabinowich H et al. Relief of extrinsic pathway inhibition by the bid-dependent mitochondrial release of Smac in Fas-mediated hepatocyte apoptosis. J Biol Chem 2002; 277: 26912-26920.
8. 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 1999; 274: 11549-11556.
9. Vucic D, Deshayes K, Ackerly H, Pisabarro MT, Kadkhodayan S, Fairbrother WJ et al. SMAC negatively regulates the anti-apoptotic activity of melanoma inhibitor of apoptosis (ML-IAP). J Biol Chem 2002; 277: 12275-12279.
10. Ashkenazi A, Dixit VM. Death receptors: signaling and modulation. Science 1998; 281: 1305-1308.
11. Kischkel FC, Lawrence DA, Tinel A, LeBlanc H, Virmani A, Schow P et al. Death receptor recruitment of endogenous caspase-10 and apoptosis initiation in the absence of caspase-8. J Biol Chem 2001; 276: 46639-46646.
12. Gastman BR, Yin XM, Johnson DE, Wieckowski E, Wang GQ, Watkins SC et al. Tumor-induced apoptosis of T cells: amplification by a mitochondrial cascade. Cancer Res 2000; 60: 6811-6817.
13. Sun XM, Bratton SB, Butterworth M, MacFarlane M, Cohen GM. Bcl-2 and Bcl-xL inhibit CD95-mediated apoptosis by preventing mitochondrial release of Smac/DIABLO and subsequent inactivation of X- linked inhibitor-of-apoptosis protein. J Biol Chem 2002; 277: 11345-11351.
14. Gross A, Yin XM, Wang K, Wei MC, Jockel J, Milliman C et al. Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J Biol Chem 1999; 274: 1156-1163.
15. Wei MC, Zong WX, Cheng EH, Lindsten T, Panoutsakopoulou V, Ross AJ et al. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 2001; 292: 727-730.
16. Korsmeyer SJ, Wei MC, Saito M, Weiler S, Oh KJ, Schlesinger PH. Pro-apoptotic cascade activates BID, which oligomerizes BAK or BAX into pores that result in the release of cytochrome c. Cell Death Differ 2000; 7: 1166-1173.
17. LeBlanc H, Lawrence D, Varfolomeev E, Totpal K, Morlan J, Schow P et al. Tumor-cell resistance to death receptor-induced apoptosis through mutational inactivation of the proapoptotic Bcl-2 homolog Bax. Nat Med 2002; 8: 274-281.
18. Deng Y, Lin Y, Wu X. TRAIL-induced apoptosis requires Bax-dependent mitochondrial release of Smac/DIABLO. Genes Dev 2002; 16: 33-45.
19. Zhang L, Yu J, Park BH, Kinzler KW, Vogelstein B. Role of BAX in the apoptotic response to anticancer agents. Science 2000; 290: 989-992.
20. Lindsten T, Ross AJ, King A, Zong WX, Rathmell JC, Shiels HA et al. The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol Cell 2000; 6: 1389-1399.
21. Theodorakis P, Lomonosova E, Chinnadurai G. Critical requirement of BAX for manifestation of apoptosis induced by multiple stimuli in human epithelial cancer cells. Cancer Res 2002; 62 3373-3376.
22. Kagawa S, Pearson SA, Ji L, Xu K, McDonnell TJ, Swisher SG et al. A binary adenoviral vector system for expressing high levels of the proapoptotic gene bax. Gene Ther 2000; 7: 75-79.
23. Fang B, Ji L, Bouvet M, Roth JA. Evaluation of GAL4/TATA in vivo. Induction of transgene expression by adenovirally mediated gene codelivery. J Biol Chem 1998; 273: 4972-4975.
24. Wang GQ, Wieckowski E, Goldstein LA, Gastman BR, Rabinovitz A, Gambotto A et al. Resistance to granzyme B-mediated cytochrome c release in Bak-deficient cells. J Exp Med 2001; 194: 1325-1337.
25. Gao G, Dou QP. 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 2000; 80: 53-72.
26. Gao CF, Ren S, Zhang L, Nakajima T, Ichinose S, Hara T et al. Caspase-dependent cytosolic release of cytochrome c and membrane translocation of Bax in p53-induced apoptosis. Exp Cell Res 2001; 265: 145-151.
27. Heibein JA, Goping IS, Barry M, Pinkoski MJ, Shore GC, Green DR et al. Granzyme B-mediated cytochrome c release is regulated by the Bcl-2 family members bid and Bax. J Exp Med 2000; 192: 1391-1402.
28. Li B, Dou QP. Bax degradation by the ubiquitin/proteasome-dependent pathway: involvement in tumor survival and progression. Proc Natl Acad Sci USA 20001; 97: 3850-3855.
29. Brimmell M, Mendiola R, Mangion J, Packham G. BAX frameshift mutations in cell lines derived from human haemopoietic malignancies are associated with resistance to apoptosis and microsatellite instability. Oncogene 1998; 16: 1803-1812.
30. Meijerink JP, Mensink EJ, Wang K, Sedlak TW, Sloetjes AW, de Witte T et al. Hematopoietic malignancies demonstrate loss-of-function mutations of BAX. Blood 1998; 91: 2991-2997.
31. Rampino N, Yamamoto H, Ionov Y, Li Y, Sawai H, Reed JC et al. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science 1997; 275: 967-969.
32. Andre N, Braguer D, Brasseur G, Goncalves A, Lemesle-Meunier D, Guise S et al. Paclitaxel induces release of cytochrome c from mitochondria isolated from human neuroblastoma cells. Cancer Res 2000; 60: 5349-5353.
33. Fulda S, Debatin KM. Betulinic acid induces apoptosis through a direct effect on mitochondria in neuroectodermal tumors. Med Pediatr Oncol 2000; 35: 616-618.
34. Sordet O, Rebe C, Leroy I, Bruey JM, Garrido C, Miguet C et al. Mitochondria-targeting drugs arsenic trioxide and lonidamine bypass the resistance of TPA-differentiated leukemic cells to apoptosis. Blood 2001; 97: 3931-3940.
35. Andre N, Carre M, Brasseur G, Pourroy B, Kovacic H, Briand C et al. Paclitaxel targets mitochondria upstream of caspase activation in intact human neuroblastoma cells. FEBS Lett 2002; 532: 256-260.
36. Wang GQ, Gastman BR, Wieckowski E, Goldstein LA, Gambotto A, Kim TH et al. A role for mitochondrial Bak in apoptotic response to anticancer drugs. J Biol Chem 2001; 276: 34307-34317.
37. Han Z, Hendrickson EA, Bremner TA, Wyche JH. A sequential two-step mechanism for the production of the mature p17:p12 form of caspase-3 in vitro. J Biol Chem 1997; 272: 13432-13436.
38. Boatright KM, Renatus M, Scott FL, Sperandio S, Shin H, Pedersen IM et al. A unified model for apical caspase activation. Mol Cell 2003; 11: 529-541.
39. Donepudi M, Mac Sweeney A, Briand C, Grutter MG. Insights into the regulatory mechanism for caspase-8 activation. Mol Cell 2003; 11: 543-549.
40. Cirman T, Oresic K, Mazovec GD, Turk V, Reed JC, Myers RM e al. Selective disruption of lysosomes in HeLa cells triggers apoptosis mediated by cleavage of Bid by multiple papain-like lysosomal cathepsins. J Biol Chem 2004; 279: 3578-3587.
41. Pataer A, Fang B, Yu R, Kagawa S, Hunt KK, McDonnell TJ et al. Adenoviral Bak overexpression mediates caspase-dependent tumor killing. Cancer Res 2000; 60: 788-792.
42. Ashkenazi A, Pai RC, Fong S, Leung S, Lawrence DA, Marsters SA et al. Safety and antitumor activity of recombinant soluble Apo2 ligand. J Clin Invest 1999; 104: 155-162.
43. Lawrence D, Shahrokh Z, Marsters S, Achilles K, Shih D, Mounho B et al. Differential hepatocyte toxicity of recombinant Apo2L/TRAIL versions. Nat Med 2001; 7: 383-385.
44. Ashkenazi A, Dixit VM. Apoptosis control by death and decoy receptors. Curr Opin Cell Biol 1999; 11: 255-260.
45. Walczak H, Miller RE, Ariail K, Gliniak B, Griffith TS, Kubin M et al. Tumoricidal activity of tumor necrosis factor-related apoptosis-inducing ligand in vivo. Nat Med 1999; 5: 157-163.
46. Roth W, Isenmann S, Naumann U, Kugler S, Bahr M, Dichgans J et al. Locoregional Apo2L/TRAIL eradicates intracranial human malignant glioma xenografts in athymic mice in the absence of neurotoxicity. Biochem Biophys Res Commun 1999; 265: 479-483.
47. Keogh SA, Walczak H, Bouchier-Hayes L, Martin SJ. Failure of Bcl-2 to block cytochrome c redistribution during TRAIL-induced apoptosis. FEBS Lett 2000; 471: 93-98.
48. Walczak H, Bouchon A, Stahl H, Krammer PH. Tumor necrosis factor-related apoptosis-inducing ligand retains its apoptosis-inducing capacity on Bcl-2- or Bcl-xL-overexpressing chemotherapy-resistant tumor cells. Cancer Res 2000; 60: 3051-3057.
49. Fulda S, Meyer E, Debatin KM. Inhibition of TRAIL-induced apoptosis by Bcl-2 overexpression. Oncogene 2002; 21: 2283-2294.
50. Scaffidi C, Schmitz I, Zha J, Korsmeyer SJ, Krammer PH, Peter ME. Differential modulation of apoptosis sensitivity in CD95 type I and type II cells. J Biol Chem 1999; 274: 22532-22538.
51. Salvesen GS, Duckett CS. Apoptosis: IAP proteins: blocking the road to death's door. Nat Rev Mol Cell Biol 2002; 3: 401-410.
52. Verhagen AM, Vaux DL. Cell death regulation by the mammalian IAP antagonist Diablo/Smac. Apoptosis 2002; 7: 163-166.
53. Ke N, Godzik A, Reed JC. Bcl-B, a novel Bcl-2 family member that differentially binds and regulates Bax and Bak. J Biol Chem 2001; 276: 12481-12484.
54. Cheng EH, Sheiko TV, Fisher JK, Craigen WJ, Korsmeyer SJ. VDAC2 inhibits BAK activation and mitochondrial apoptosis. Science 2003; 301: 513-517.
55. Petak I, Vernes R, Szucs KS, Anozie M, Izeradjene K, Douglas L et al. A caspase-8-independent component in TRAIL/Apo-2L-induced cell death in human rhabdomyosarcoma cells. Cell Death Differ 2003; 10: 729-739.
56. Deveraux QL, Leo E, Stennicke HR, Welsh K, Salvesen GS, Reed JC. Cleavage of human inhibitor of apoptosis protein XIAP results in fragments with distinct specificities for caspases. EMBO J 1999; 18: 5242-5251.
57. Li S, Zhao Y, He X, Kim TH, Kuharsky DK, Rabinowich H et al. Relief of extrinsic pathway inhibition by the Bid-dependent mitochondrial release of Smac in Fas-mediated hepatocyte apoptosis. J Biol Chem 2002; 277: 26912-26920.
58. Arnt CR, Chiorean MV, Heldebrant MP, Gores GJ, Kaufmann SH. Synthetic Smac/DIABLO peptides enhance the effects of chemotherapeutic agents by binding XIAP and cIAP1 in situ. J Biol Chem 2002; 277: 44236-44243.
59. Fulda S, Wick W, Weller M, Debatin KM. Smac agonists sensitize for Apo2L/TRAIL- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat Med 2002; 8: 808-815.
60. Wu G, Chai J, Suber TL, Wu JW, Du C, Wang X et al. Structural basis of IAP recognition by Smac/DIABLO. Nature 2000; 408: 1008-1012.