Arsenic trioxide and paclitaxel induce apoptosis by different mechanisms

Cell Cycle

Volumn 3, Issue 3, 2004, Pages 324-334

  Akay, Cagla ^a   Thomas III, Charles ^a   Gazitt, Yair ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

AIF; Apoptosis; Arsenic trioxide; Cell cycle; Myeloma; Taxol

Indexed keywords

ARSENIC TRIOXIDE; CASPASE 8; CASPASE 9; CYTOCHROME C; MUTANT PROTEIN; PACLITAXEL; PROTEIN BCL 2; PROTEIN P53; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; APOPTOSIS INDUCING FACTOR; APOPTOSIS REGULATORY PROTEIN; BID PROTEIN, HUMAN; CARRIER PROTEIN; CASPASE; FLAVOPROTEIN; MEMBRANE PROTEIN; ORGANOARSENIC DERIVATIVE; OXIDE; PDCD8 PROTEIN, HUMAN; PHOSPHOSERINE; PROTEIN BID; TNFSF10 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTICLE; CHROMATIN; CHROMATIN CONDENSATION; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE; MYELOMA CELL; PROTEIN EXPRESSION; PROTEIN SECRETION; CELL LINE; CELL NUCLEUS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENETICS; INTRACELLULAR MEMBRANE; METABOLISM; MITOCHONDRION; PROTEIN TRANSPORT; TIME;

APOPTOSIS; APOPTOSIS INDUCING FACTOR; APOPTOSIS REGULATORY PROTEINS; ARSENICALS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CARRIER PROTEINS; CASPASES; CELL LINE; CELL NUCLEUS; CHROMATIN; CYTOCHROMES C; ENZYME ACTIVATION; FLAVOPROTEINS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR MEMBRANES; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MITOCHONDRIA; OXIDES; PACLITAXEL; PHOSPHOSERINE; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-BCL-2; TIME FACTORS; TNF-RELATED APOPTOSIS-INDUCING LIGAND; TUMOR NECROSIS FACTOR-ALPHA;

EID: 13244260526     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: None     Document Type: Article

References (83)

1. Gregory W, Richards M, Malpas J. Combination chemotherapy versus melphalan and prednisone in the treatment of multiple myeloma: An overview of published trials. J Clin Oncol 1992; 10:336-42.
2. Alexanian R, Dimopoulos MA, Delasalle K, Barlogie B. Primary dexamethasone treatment for multiple myeloma. Blood 1992; 80:887-92.
3. Attal M, Harousseau JL, Stoppa AM, Sotto JJ, Fuzibet JG, Rossi JF, et al. Prospective randomized trial of autologous transplantation and chemotherapy in multiple myeloma. N Eng J Med 1996; 335:91-7.
4. Hu J, Shen ZX, Sun GL, Chen SJ, Wang ZY, Chen Z. Long-term survival and prognostic study in acute promyelocytic leukemia treated with ATRA, chemotherapy, and As2O3: An experience of 120 patients. Int J Hematol 1999; 70:248-60.
5. Soignet SL, Maslak P, Wang ZG, Jhanwar S, Calleja E, Dardashti LJ, et al. Complete remission after treatment of acute promyelocytic leukemia with arsenic trioxide. N Eng J Med 1998; 339:1341-8.
6. Gianni M. de The H. In acute promyelocytic leukemia NB4 cells, the synthetic retinoid CD437 induces contemporaneously apoptosis, a caspase-3-mediated degradation of PML/RARalpha protein and the PML retargeting on PML-nuclear bodies. Leukemia 1999; 13:739-49.
7. Kinjo K, Kizaki M, Muto A, Fukuchi Y, Umezawa A, Yamato K, et al. Arsenic trioxide (As2O3)-induced apoptosis and differentiation in retinoic acid-resistant acute promyelocytic leukemia model in hGM-CSF-producing transgenic SCID mice. Leukemia 2000; 14:431-8.
8. Rego EM, He LZ, Warrell Jr RP, Wang ZG, Pandolfi PP. Retinoic acid (RA) and As2O3 treatment in transgenic models of acute promyelocytic leukemia (APL) unravel the distinct nature of the leukemogenic process induced by the PML-RARalpha and PLZF-RARalpha oncoproteins. Proc Natl Acad Sci (USA) 2000; 97:10173-8.
9. Cai X, Shen YL, Zhu Q, Jia PM, Yu Y, Zhou L, et al. Arsenic trioxide-induced apoptosis and differentiation are associated respectively with mitochondrial transmembrane potential collapse and retinoic acid signaling pathways in acute promyelocytic leukemia. Leukemia 2000; 14:262-70.
10. Perkins C, Kim CN, Fang G, Bhalla KN. Arsenic induces apoptosis of multidrug-resistant human myeloid leukemia cells that express Bcr-Abl or overexpress MDR, MRP, Bcl-2, or Bcl-xL. Blood 2000; 95:1014-22.
11. Larochette N, Decaudin D, Jacotot E, Brenner C, Marzo I, Susin SA, et al. Arsenite induces apoptosis via a direct effect on the mitochondrial permeability transition pore. Expt Cell Res 1999; 249:413-21.
12. Warrell Jr RP. Arsenicals and inhibitors of histone deacetylase as anticancer therapy. Haematologica 1999; 84:75-7.
13. Zhang TC, Cao EH, Li JF, Ma W, Qin JF. Induction of apoptosis and inhibition of human gastric cancer MGC-803 cell growth by arsenic trioxide. Euro J Cancer 1999; 35:1258-63.
14. Akao Y, Nakagawa Y, Akiyama K. Arsenic trioxide induces apoptosis in neuroblastoma cell lines through the activation of caspase 3 in vitro. FEBS Letters 1999; 455:59-62.
15. Ora I, Bondesson L, Jonsson C, Ljungberg J, Porn-Ares I, Garwicz S, et al. Arsenic trioxide inhibits neuroblastoma growth in vivo and promotes apoptotic cell death in vitro. Biochem Biophys Res Comm 2000; 277:179-85.
16. Jiang X, Wong B, Yuen S, SH Jiang, CH Cho, KC Lai, et al. Arsenic trioxide induces apoptosis in human gastric cancer cells through up-regulation of p53 and activation of caspase-3. Int J Cancer 2001; 93:916-920.
17. Kitamura K, Minami Y, Yamamoto K, Akao Y, Kiyoi H, Saito H, et al. Involvement of CD95-independent caspase 8 activation in arsenic trioxide-induced apoptosis. Leukemia 2000; 14:1743-50.
18. Park WH, Seol JG, Kim ES, Hyun JM, Jung CW, Lee CC, et al. Arsenic trioxide-mediated growth inhibition in MC/CAR myeloma cells via cell cycle arrest and induction of cyclin-dependent kinase inhibitor, p21, and apoptosis. Cancer Res 2000; 60:3065-3071.
19. Shen ZY, Shen J, Cai Wf, Hong C, Zheng MH. Multiple mechanisms are involved in differentiation induced by arsenic trioxide in acute promyelocytic leukemia. Blood 2000; 96:310a.
20. Seol JG, Park WH, Kim ES, Jung CW, Hyun JM, Lee YY, et al. Potential role of caspase-3 and -9 in arsenic trioxide-mediated apoptosis in PCI-1 head and neck cancer cells. Int J Oncol 2001; 18:249-455.
21. 2/M growth arrest and apoptosis after caspase-3 activation and bcl-2 phosphorylation in promonocytic U937 cells. Biochem Biophys Res Comm 2001; 6:726-34.
22. Shen ZY, Shen J, Cai WJ, Hong C, Zheng MH. The alteration of mitochondria is an early event of arsenic trioxide induced apoptosis in esophageal carcinoma cells. Int J Mol Med 2000; 5:155-8.
23. Dai J, Weinberg RS, Waxman S, Jing Y. Malignant cells can be sensitized to undergo growth inhibition and apoptosis by arsenic trioxide through modulation of the glutathione redox system. Blood 1999; 93:268-77.
24. Iwama K, Nakajo S, Aiuchi T, Nakaya K. Apoptosis induced by arsenic trioxide in leukemia U937 cells is dependent on activation of p38, inactivation of ERK and the Ca2+-dependent production of superoxide. International Journal of Cancer 2001; 92:518-26.
25. Baj G, Arnulfo A, Deaglio S, Mallone R, Vigone A, De Cesaris MG, et al. Arsenic trioxide and breast cancer: Analysis of the apoptotic, differentiative and immunomodulatory effects. Breast Cancer Research & Treatment 2002; 73:61-73.
26. Hayashi T, Hideshima T, Akiyama M, Richardson P, Schlossman RL, Chauhan D, et al. Arsenic trioxide inhibits growth of human multiple myeloma cells in the bone marrow microenvironment. Molecular Cancer Therapeutics 2002; 1:851-60.
27. Blagosklonny MV, Fojo T. Molecular effects of paclitaxolel: myths and reality (a critical review). Intl J Cancer 1999; 83:151-6.
28. Halder SJ, Chintapapplli, Croce C. Taxol-induced bcl-2 phosphorylation and death of prostate cancer cells. Cancer Res 1996; 56:1253-5.
29. Srivastava RK, Srivastava AR, Korsmeyer SJ, Nesterova M, Cho-Chung YS, Longo DL. Involvement of microtubules in the regulation of Bcl2 phosphorylation and apoptosis through cyclic AMP-dependent protein kinase. Mol Cell Biol 1998; 18:3509-17.
30. Blagosklonny MV, Chuman Y, Bergan RC, Fojo T. Mitogen-activated protein kinase pathway is dispensable for microtubule-active drug-induced Raf-1/Bcl-2 phosphorylation and apoptosis in leukemia cells. Leukemia Jul 1999; 13:1028-36.
31. Nagane M, Pan G, Weddle JJ, Dixit VM, Cavenee WK, Huang HJ. Increased death receptor 5 expression by chemotherapeutic agents in human gliomas causes synergistic cytotoxicity with tumor necrosis factor related apoptosis inducing ligand in vitro and in vivo. Cancer Res 2000; 60:847-53.
32. Lacour S, Hammann A, Wotawa A, Corcos L, Solary E, Dimanche-Boitrel MT. Anticancer agents sensitize tumor cells to tumor necrosis factor-related apoptosis-inducing ligand-mediated caspase-8 activation and apoptosis. Cancer Res 2001; 61:1645-51.
33. Nimmanapalli R, Perkins CL, Orlando M, O'Bryan E, Nguyen D, Bhalla KN. Pretreatment with paclitaxolel enhances apo-2 ligand/tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis of prostate cancer cells by inducing death receptors 4 and 5 protein levels. Cancer Res 2001; 61:759-63.
34. Pan J, Xu G, Yeung SC. Cytochrome c release is upstream to activation of caspase-9, caspase-8, and caspase-3 in the enhanced apoptosis of anaplastic thyroid cancer cells induced by manumycin and paclitaxolel. J Clin Endocrinology & Metabolism 2001; 86:4731-40.
35. Ofir R, Seidman R, Rabinski T, Krup M, Yavelsky V, Weinstein Y, et al. Taxolol-induced apoptosis in human SKOV3 ovarian and MCF7 breast carcinoma cells is caspase-3 and caspase-9 independent. Cell Death & Differentiation 2002; 9:636-42.
36. Yuan SY, Hsu SL, Tsai KJ, Yang CR. Involvement of mitochondrial pathway in Taxolol-induced apoptosis of human T24 bladder cancer cells. Urological Research 2002; 30:282-8.
37. Gazitt Y, Rothenberg ML, Hilsenbeck S, Fey V, Thomas C, Montegomrey W. Bcl-2 overexpression is associated with resistance to paclitaxolel but not gemcitabine in multiple myeloma cell lines. Int J Oncol 1998; 13:839-48.
38. Kroemer G, Reed J C. Mitochondrial control of cell death. Nat Med 2000; 6:513-9.
39. Green D R, Kroemer G. The central executioner of apoptosis: Mitochondria or caspases? Trends Cell Biol 1998; 8:267-71.
40. Budihardjo I, Oliver H, Lutter M, Luo X, Wang X. Biochemical pathways of caspase activation during apoptosis. Ann Rev Cell Dev Biol 1999; 15:269-90.
41. Cande C, Cecconi F, Dessen P, Kroemer G. Apoptosis-inducing factor (AIF): Key to the conserved caspase-independent pathways of cell death? J Cell Sci 2002; 115:4727-34.
42. Lipton SA, Bossy-Wetzel E. Dueling activities of AIF in cell death versus survival: DNA binding and redox activity. Cell 2002; 111:147-50.
43. Adams JM, Cory S. The bcl-2 protein family: Arbiters of cell survival. Science 1998; 281:1322-6.
44. Wang K, Yin XM, Copeland NG, Gilbert DJ, Jenkins NA, Keck CL, et al. BID, a proapoptotic BCL-2 family member, is localized to mouse chromosome 6 and human chromosome 22q11. Genomics 1998; 53:235-8.
45. 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; 274:1156-63.
46. 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 & Differentiation 2000; 7:1166-73.
47. Zha J, Weiler S, Oh KJ, Wei MC, Korsmeyer SJ. Posttranslational N-myristoylation of BID as a molecular switch for targeting mitochondria and apoptosis. Science 2000; 290:1761-5.
48. Wei MC, Lindsten T, Mootha VK, Weiler S, Gross A, Ashiya M, et al. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Gen Dev 2000; 14:2060-71.
49. 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; 292:727-30.
50. Roth W, Reed JC. Apoptosis and cancer: When BAX is TRAILing away. Nature Medicine 2002; 8:216-8.
51. Wiley SR, Schooley K, Smolak PJ, Din WS, Huang CP, Nicholl JK, et al. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 1995; 3:673-82.
52. Marsters SA, Sheridan JP, Donahue J, Pitti RM, Gray CL, Goddard AD, et al. Apo-3, a new member of the tumor necrosis factor receptor family, contains a death domain and activates apoptosis and NF-kB. Current Biol 1996; 6:1669-76.
53. Pitti RM, Marsters SA, Ruppert S, Donahue CJ, Moore A, Ashkenazi A. Induction of apoptosis by APO-2 ligand, a new member of the tumor necrosis factor cytokine family. J Biol Chem 1996; 271:12687-90.
54. Pan G, Ni J, Wei YF, Yu G, Gentz R, Dixit VM. An antagonistic decoy receptor and a death domain containing receptor for APO2/TRAIL. Science 1997; 815-8.
55. Ashkenazi A, Dixit VM. Death receptors: Signaling and modulation. Science 1998; 281:1305-8.
56. Griffith TS, Chin WA, Jackson GC, Lynch DH, Kubin MZ. Intracellular regulation of APO2/TRAIL-induced apoptosis in human melanoma. J Immunol 1998; 161:2833-40.
57. Sheikh MS, Huang Y, Fernandez-Salas EA, El-Deiry WS, Friess H, Amundson S, et al. The antiapoptotic decoy receptor TRID/APO2/TRAIL-R3 is a p53 regulated DNA damage inducible gene that is overexpressed in primary tumors of the gastrointestinal tract. Oncogene 1999; 18:4153-9.
58. Sheridan JP, Marsters SA, Pitti RM, Gurney A, Skubatch M, Baldwin D, et al. Control of APO2/TRAIL-induced apoptosis by a family of signaling and decoy receptors. Science 1997; 277:818-21.
59. Kim K, Fisher MJ, Xu SQ, El-Deiry WS. Molecular determinants of response to APO2/TRAIL in killing of normal and cancer cells. Clin Cancer Res 2000; 6:335-46.
60. Kischkel FC, Lawrence DA, Chuntharapai A, Schow P, Kim KJ, Ashkenazi A. APO2/TRAIL dependent recruitment of endogenous FADD and caspase-8 to death receptors 4 and 5. Immunity 2000; 12:611-20.
61. Sprick MR, Weigand MA, Rieser E, Rauch CT, Juo P, Blenis J, et al. FADD/MORT1 and caspase-8 are recruited to APO2/TRAIL receptors 1 and 2 and are essential for apoptosis mediated by APO2/TRAIL receptor 2. Immunity 2000; 12:599-609.
62. Ozoren N, El-Deiry WS. Defining characteristics of types I and II apoptotic cells in response to TRAIL. Neoplasia 2002; 4:551-7.
63. 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 Jun 1 2000; 60:3051-7.
64. Lamothe B, Aggarwal BB. Ectopic expression of Bcl-2 and Bcl-xL inhibits apoptosis induced by TNF-related apoptosis-inducing ligand (TRAIL) through suppression of caspases-8, 7, and 3 and BID cleavage in human acute myelogenous leukemia cell line HL-60. J Interferon Cytokine Res 2002; 22:269-79.
65. Gazitt Y. APO2/TRAIL is a potent inducer of apoptosis in myeloma cells derived from multiple myeloma patients and is not cytotoxic to hematopoietic stem cells. LEUKEMIA 1999; 13:1817-24.
66. Tian E, Gazitt Y. The role of P53, bcl-2 and bax in dexamethasone induced apoptosis in myeloma cell lines. Int J Oncol 1996; 8:719-26.
67. Tian E, Hu W-X, Gazitt Y. Bcl-2 plays a critical role in growth and in spontaneous or induced apoptosis in myeloma cell lines: A study with inducible bcl-2 transfection constructs. Int J Oncol 1996; 9:165-9.
68. Liu Q, Gazitt Y. Adenovirus-mediated delivery of p53 results in a substantial apoptosis to myeloma cells and is not cytotoxic to flow-sorted CD34+ hematopoietic progenitor cells and normal lymphocytes. Expt Hematol 2000; 28:1354-62.
69. Liu Q, Gazitt Y. Potentiation of dexamethasone, taxolol and Ad-p53-induced apoptosis by Bcl-2 anti-sense oligodeoxynucleotides in drug-resistant multiple myeloma cells. Blood 2003; 101:4105-14. 1st ed prepublished online 2003.
70. 2/M cell cycle arrest, activation of caspase 8 or caspase 9 and synergy with APO2/TRAIL. Blood 2003; 101:4078-87. 1st ed prepublished online 2003.
71. Akay C, Gazitt Y. Arsenic trioxide selectively induces early and extensive apoptosis via the APO2/Caspase-8 pathway engaging the mitochondrial pathway in myeloma cells with mutant p53. Cell Cycle 2003; 2:358-68.
72. Li YM, Broome JD. Arsenic targets tubulins to induce apoptosis in myeloid leukemia cells. Cancer Res 15 Feb 1999; 59:776-80.
73. Ling Y-H, Jian-Dong Jiang, James F. Holland, and Roman Perez-Soler. Arsenic trioxide produces polymerization of microtubules and mitotic arrest before apoptosis in human tumor cell lines. Mol Pharmacol 2002; 62:529-38.
74. Cai X, Yu Y, Huang Y, Zhang L, Jia PM, Zhao Q, et al. Arsenic trioxide-induced mitotic arrest and apoptosis in acute promyelocytic leukemia cells. Leukemia 2003; 17:1333-7.
75. Halicka HD, Smolewski P, Darzynkiewicz Z, Dai W, Traganos F. Arsenic trioxide arrests cells early in mitosis leading to apoptosis. Cell Cycle 2002; 1:201-9.
76. Chen GQ, J Zhu, XG Shi, JH Ni, HJ Zhong, GY Si, et al. In vitro studies on cellular and molecular mechanisms of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia: As2O3 induces NB4 cell apoptosis with downregulation of Bcl-2 expression and modulation of PML-RAR alpha/PML proteins. Blood 1996; 88:1052-61.
77. Mahieux R, Pise-Masison C, Gessain A, Brady JN, Olivier R, Perret E, et al. Arsenic trioxide induces apoptosis in human T-cell leukemia virus type 1- and type 2-infected cells by a caspase-3-dependent mechanism involving Bcl-2 cleavage. Blood 2001; 98:3762-9.
78. Scatena CD, Stewart ZA, Mays D, Tang LJ, Keefer CJ, Leach SD, et al. Mitotic phosphorylation of Bcl-2 during normal cell cycle progression and Taxolol-induced growth arrest. J Biol Chem 1998; 273:30777-84.
79. Park WH, Yeon Hee Cho, Chul Won Jung, Joon Oh Park, Kihyun Kim, Young Hyuck Im, et al. Arsenic trioxide inhibits the growth of A498 renal cell carcinoma cells via cell cycle arrest or apoptosis. Bioch Biophy Res Comm 2003; 300:230-5.
80. Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 1999; 397:441-6.
81. Susin SA, Daugas E, Ravagnan L, Samejima K, Zamzami N, Loeffler M, et al. Two distinct pathways leading to nuclear apoptosis. J Expt Med 2000; 192:571-80.
82. Ye H, Cande C, Stephanou NC, Jiang S, Gurbuxani S, Larochette N, et al. DNA binding is required for the apoptogenic action of apoptosis inducing factor. Nature Structural Biology 2002; 9:680-4.
83. Ravagnan I, Gurbuxani S, Susin SA, Maisse C, Daugas E, Zamzami N, et al. Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nature Cell Biol 2001; 3:839-43.