Combination treatment with arsenic trioxide and irradiation enhances apoptotic effects in U937 cells through increased mitotic arrest and ROS generation

Chemico-Biological Interactions

Volumn 179, Issue 2-3, 2009, Pages 304-313

  Ho, Sheng Yow ^a   Chen, Wei Chih ^b   Chiu, Hui Wen ^b   Lai, Ching Shu ^b   Guo, How Ran ^b   Wang, Ying Jan ^b  

^a TAINAN SIN LAU HOSPITAL   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Arsenic trioxide; Irradiation; Leukemia; Mitotic arrest

Indexed keywords

ACETYLCYSTEINE; ARSENIC TRIOXIDE; CASPASE 3; CYCLIN B; CYCLIN DEPENDENT KINASE 2; CYTOCHROME C; HYDROGEN PEROXIDE; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN P53; REACTIVE OXYGEN METABOLITE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL STRAIN U937; CONTROLLED STUDY; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVATION; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; IONIZING RADIATION; LEUKEMIA CELL; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOSIS INHIBITION; PROTEIN EXPRESSION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; ARSENICALS; CASPASES; CELL CYCLE; CELL DIVISION; CYCLIN A; CYCLIN B; CYTOCHROMES C; DRUG SCREENING ASSAYS, ANTITUMOR; G2 PHASE; HUMANS; MITOCHONDRIAL MEMBRANES; MITOSIS; OXIDES; RADIATION, IONIZING; REACTIVE OXYGEN SPECIES; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEIN P53; U937 CELLS;

EID: 62549106143     PISSN: 00092797     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbi.2008.12.015     Document Type: Article

References (65)

1. Antman K.H. Introduction: the history of arsenic trioxide in cancer therapy. Oncologist 6 (2001) 1-2
2. Shen Y., Shen Z.X., Yan H., Chen J., Zeng X.Y., Li J.M., Li X.S., Wu W., Xiong S.M., Zhao W.L., Tang W., Wu F., Liu Y.F., Niu C., Wang Z.Y., Chen S.J., and Chen Z. Studies on the clinical efficacy and pharmacokinetics of low-dose arsenic trioxide in the treatment of relapsed acute promyelocytic leukemia: a comparison with conventional dosage. Leukemia 15 (2001) 735-741
3. Soignet S.L. Clinical experience of arsenic trioxide in relapsed acute promyelocytic leukemia. Oncologist 6 (2001) 11-16
4. Bernstam L., and Nriagu J. Molecular aspects of arsenic stress. J. Toxicol. Environ. Health B Crit. Rev. 3 (2000) 293-322
5. Chen Y.C., Lin-Shiau S.Y., and Lin J.K. Involvement of reactive oxygen species and caspase 3 activation in arsenite-induced apoptosis. J. Cell Physiol. 177 (1998) 324-333
6. Jing Y., Dai J., Chalmers-Redman R.M., Tatton W.G., and Waxman S. Arsenic trioxide selectively induces acute promyelocytic leukemia cell apoptosis via a hydrogen peroxide-dependent pathway. Blood 94 (1999) 2102-2111
7. Jabs T. Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem. Pharmacol. 57 (1999) 231-245
8. Cai X., Yu Y., Huang Y., Zhang L., Jia P.M., Zhao Q., Chen Z., Tong J.H., Dai W., and Chen G.Q. Arsenic trioxide-induced mitotic arrest and apoptosis in acute promyelocytic leukemia cells. Leukemia 17 (2003) 1333-1337
9. Huang S.C., and Lee T.C. Arsenite inhibits mitotic division and perturbs spindle dynamics in HeLa S3 cells. Carcinogenesis 19 (1998) 889-896
10. Pawlik T.M., and Keyomarsi K. Role of cell cycle in mediating sensitivity to radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 59 (2004) 928-942
11. McDonnell T.J., Meyn R.E., and Robertson L.E. Implications of apoptotic cell death regulation in cancer therapy. Semin. Cancer Biol. 6 (1995) 53-60
12. Shackelford R.E., Kaufmann W.K., and Paules R.S. Cell cycle control, checkpoint mechanisms, and genotoxic stress. Environ. Health Perspect. 107 (1999) 5-24
13. Aldridge D.R., and Radford I.R. Explaining differences in sensitivity to killing by ionizing radiation between human lymphoid cell lines. Cancer Res. 58 (1998) 2817-2824
14. Su L.N., and Little J.B. Prolonged cell cycle delay in radioresistant human cell lines transfected with activated ras oncogene and/or simian virus 40 T-antigen. Radiat. Res. 133 (1993) 73-79
15. Huang C., Ma W.Y., Li J., and Dong Z. Arsenic induces apoptosis through a c-Jun NH2-terminal kinase-dependent, p53-independent pathway. Cancer Res. 59 (1999) 3053-3058
16. Giaccia A.J., and Kastan M.B. The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev. 12 (1998) 2973-2983
17. Kinzler K.W., and Vogelstein B. Life (and death) in a malignant tumour. Nature 379 (1996) 19-20
18. Dong Z. The molecular mechanisms of arsenic-induced cell transformation and apoptosis. Environ. Health Perspect. 110 (2002) 757-759
19. 2+-dependent production of superoxide. Int. J. Cancer 92 (2001) 518-526
20. Park J.W., Choi Y.J., Jang M.A., Baek S.H., Lim J.H., Passaniti T., and Kwon T.K. Arsenic trioxide induces G2/M growth arrest and apoptosis after caspase-3 activation and bcl-2 phosphorylation in promonocytic U937 cells. Biochem. Biophys. Res. Commun. 286 (2001) 726-734
21. Shinomiya N., Kuno Y., Yamamoto F., Fukasawa M., Okumura A., Uefuji M., and Rokutanda M. Different mechanisms between premitotic apoptosis and postmitotic apoptosis in X-irradiated U937 cells. Int. J. Radiat. Oncol. Biol. Phys. 47 (2000) 767-777
22. 3). FEBS Lett. 519 (2002) 195-200
23. Ho S.Y., Huang P.C., Guo H.R., Chang W.H., Chen R.J., Wei B.L., Wu W.J., Tai C., and Wang Y.J. Mechanisms of apoptosis induction and cell cycle regulation in irradiated leukemia U937 cells and enhancement by arsenic trioxide. Radiat. Res. 165 (2006) 390-399
24. McCabe Jr. M.J., Singh K.P., Reddy S.A., Chelladurai B., Pounds J.G., Reiners Jr. J.J., and States J.C. Sensitivity of myelomonocytic leukemia cells to arsenite-induced cell cycle disruption, apoptosis, and enhanced differentiation is dependent on the inter-relationship between arsenic concentration, duration of treatment, and cell cycle phase. J. Pharmacol. Exp. Ther. 295 (2000) 724-733
25. Ma D.C., Sun Y.H., Chang K.Z., Ma X.F., Huang S.L., Bai Y.H., Kang J., Liu Y.G., and Chu J.J. Selective induction of apoptosis of NB4 cells from G2 + M phase by sodium arsenite at lower doses. Eur. J. Haematol. 61 (1998) 27-35
26. Doherty S.C., McKeown S.R., McKelvey-Martin V., Downes C.S., Atala A., Yoo J.J., Simpson D.A., and Kaufmann W.K. Cell cycle checkpoint function in bladder cancer. J. Natl. Cancer Inst. 95 (2003) 1859-1868
27. Zegura B., Lah T.T., and Filipic M. The role of reactive oxygen species in microcystin-LR-induced DNA damage. Toxicology 200 (2004) 59-68
28. Morgan D.O. Principles of CDK regulation. Nature 374 (1995) 131-134
29. Sherr C.J., and Roberts J.M. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9 (1995) 1149-1163
30. Antonsson B., Montessuit S., Sanchez B., and Martinou J.C. Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells. J. Biol. Chem. 276 (2001) 11615-11623
31. Narvaez C.J., and Welsh J. Role of mitochondria and caspases in vitamin D-mediated apoptosis of MCF-7 breast cancer cells. J. Biol. Chem. 276 (2001) 9101-9107
32. Koniaras K., Cuddihy A.R., Christopoulos H., Hogg A., and O'Connell M.J. Inhibition of Chk1-dependent G2 DNA damage checkpoint radiosensitizes p53 mutant human cells. Oncogene 20 (2001) 7453-7463
33. Matsui Y., Tsuchida Y., and Keng P.C. Effects of p53 mutations on cellular sensitivity to ionizing radiation. Am. J. Clin. Oncol. 24 (2001) 486-490
34. Hornhardt S., Gomolka M., Walsh L., and Jung T. Comparative investigations of sodium arsenite, arsenic trioxide and cadmium sulfate in combination with gamma-radiation on apoptosis, micronuclei induction and DNA damage in a human lymphoblastoid cell line. Mutat. Res. 600 (2006) 165-176
35. King K.L., and Cidlowski J.A. Cell cycle and apoptosis: common pathways to life and death. J. Cell Biochem. 58 (1995) 175-180
36. Choi K.S., Eom Y.W., Kang Y., Ha M.J., Rhee H., Yoon J.W., and Kim S.J. Cdc2 and Cdk2 kinase activated by transforming growth factor-beta1 trigger apoptosis through the phosphorylation of retinoblastoma protein in FaO hepatoma cells. J. Biol. Chem. 274 (1999) 31775-31783
37. Ling Y.H., Consoli U., Tornos C., Andreeff M., and Perez-Soler R. Accumulation of cyclin B1, activation of cyclin B1-dependent kinase and induction of programmed cell death in human epidermoid carcinoma KB cells treated with taxol. Int. J. Cancer 75 (1998) 925-932
38. Shen S.C., Huang T.S., Jee S.H., and Kuo M.L. Taxol-induced p34cdc2 kinase activation and apoptosis inhibited by 12-O-tetradecanoylphorbol-13-acetate in human breast MCF-7 carcinoma cells. Cell Growth Differ. 9 (1998) 23-29
39. Shimizu T., O'Connor P.M., Kohn K.W., and Pommier Y. Unscheduled activation of cyclin B1/Cdc2 kinase in human promyelocytic leukemia cell line HL60 cells undergoing apoptosis induced by DNA damage. Cancer Res. 55 (1995) 228-231
40. Yao S.L., Akhtar A.J., McKenna K.A., Bedi G.C., Sidransky D., Mabry M., Ravi R., Collector M.I., Jones R.J., Sharkis S.J., Fuchs E.J., and Bedi A. Selective radiosensitization of p53-deficient cells by caffeine-mediated activation of p34cdc2 kinase. Nat. Med. 2 (1996) 1140-1143
41. Muschel R.J., Zhang H.B., Iliakis G., and McKenna W.G. Cyclin B expression in HeLa cells during the G2 block induced by ionizing radiation. Cancer Res. 51 (1991) 5113-5117
42. Smeets M.F., Mooren E.H., and Begg A.C. The effect of radiation on G2 blocks, cyclin B expression and cdc2 expression in human squamous carcinoma cell lines with different radiosensitivities. Radiother. Oncol. 33 (1994) 217-227
43. Yih L.H., Ho I.C., and Lee T.C. Sodium arsenite disturbs mitosis and induces chromosome loss in human fibroblasts. Cancer Res. 57 (1997) 5051-5059
44. Wang S., Hasham M.G., Isordia-Salas I., Tsygankov A.Y., Colman R.W., and Guo Y.L. Upregulation of Cdc2 and cyclin A during apoptosis of endothelial cells induced by cleaved high-molecular-weight kininogen. Am. J. Physiol. Heart Circ. Physiol. 284 (2003) H1917-1923
45. Yi J., Gao F., Shi G., Li H., Wang Z., Shi X., and Tang X. The inherent cellular level of reactive oxygen species: one of the mechanisms determining apoptotic susceptibility of leukemic cells to arsenic trioxide. Apoptosis 7 (2002) 209-215
46. Hendrikse A.S., Hunter A.J., Keraan M., and Blekkenhorst G.H. Effects of low dose irradiation on TK6 and U937 cells: induction of p53 and its role in cell-cycle delay and the adaptive response. Int. J. Radiat. Biol. 76 (2000) 11-21
47. Fan S., el-Deiry W.S., Bae I., Freeman J., Jondle D., Bhatia K., Fornace Jr. A.J., Magrath I., Kohn K.W., and O'Connor P.M. p53 gene mutations are associated with decreased sensitivity of human lymphoma cells to DNA damaging agents. Cancer Res. 54 (1994) 5824-5830
48. el-Deiry W.S. p21/p53, cellular growth control and genomic integrity. Curr. Top. Microbiol. Immunol. 227 (1998) 121-137
49. Cai Z., Lin M., Wuchter C., Ruppert V., Dorken B., Ludwig W.D., and Karawajew L. Apoptotic response to homoharringtonine in human wt p53 leukemic cells is independent of reactive oxygen species generation and implicates Bax translocation, mitochondrial cytochrome c release and caspase activation. Leukemia 15 (2001) 567-574
50. Kuerbitz S.J., Plunkett B.S., Walsh W.V., and Kastan M.B. Wildtype p53 is a cell cycle checkpoint determinant following irradiation. Proc. Natl. Acad. Sci. U.S.A. 89 (1992) 7491-7495
51. Han Z., Chatterjee D., He D.M., Early J., Pantazis P., Wyche J.H., and Hendrickson E.A. Evidence for a G2 checkpoint in p53-independent apoptosis induction by X-irradiation. Mol. Cell. Biol. 15 (1995) 5849-5857
52. Oltvai Z.N., Milliman C.L., and Korsmeyer S.J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74 (1993) 609-619
53. Akao Y., Mizoguchi H., Kojima S., Naoe T., Ohishi N., and Yagi K. Arsenic induces apoptosis in B-cell leukaemic cell lines in vitro: activation of caspases and down-regulation of Bcl-2 protein. Br. J. Haematol. 102 (1998) 1055-1060
54. Brockhaus F., and Brune B. U937 apoptotic cell death by nitric oxide: Bcl-2 downregulation and caspase activation. Exp. Cell Res. 238 (1998) 33-41
55. 3 induces NB4 cell apoptosis with downregulation of Bcl-2 expression and modulation of PML-RAR alpha/PML proteins. Blood 88 (1996) 1052-1061
56. Filomeni G., Rotilio G., and Ciriolo M.R. Glutathione disulfide induces apoptosis in U937 cells by a redox-mediated p38 MAP kinase pathway. FASEB J. 17 (2003) 64-66
57. Gross A., McDonnell J.M., and Korsmeyer S.J. BCL-2 family members and the mitochondria in apoptosis. Genes Dev. 13 (1999) 1899-1911
58. Huang D.C., and Strasser A. BH3-only proteins-essential initiators of apoptotic cell death. Cell 103 (2000) 839-842
59. Kluck R.M., Bossy-Wetzel E., Green D.R., and Newmeyer D.D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275 (1997) 1132-1136
60. Verheij M., and Bartelink H. Radiation-induced apoptosis. Cell Tissue Res. 301 (2000) 133-142
61. Gil J., Almeida S., Oliveira C.R., and Rego A.C. Cytosolic and mitochondrial ROS in staurosporine-induced retinal cell apoptosis. Free Radic. Biol. Med. 35 (2003) 1500-1514
62. Liu X., Kim C.N., Yang J., Jemmerson R., and Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86 (1996) 147-157
63. Zhivotovsky B., Orrenius S., Brustugun O.T., and Doskeland S.O. Injected cytochrome c induces apoptosis. Nature 391 (1998) 449-450
64. Yu L., Orlandi L., Wang P., Orr M.S., Senderowicz A.M., Sausville E.A., Silvestrini R., Watanabe N., Piwnica-Worms H., and O'Connor P.M. UCN-01 abrogates G2 arrest through a Cdc2-dependent pathway that is associated with inactivation of the Wee1Hu kinase and activation of the Cdc25C phosphatase. J. Biol. Chem. 273 (1998) 33455-33464
65. 3) in the treatment of acute promyelocytic leukemia (APL): II. Clinical efficacy and pharmacokinetics in relapsed patients. Blood 89 (1997) 3354-3360