Requirement of a functional spindle checkpoint for arsenite-induced apoptosis

Journal of Cellular Biochemistry

Volumn 105, Issue 3, 2008, Pages 678-687

  Wu, Yi Chen ^a   Yen, Wen Yen ^a   Yih, Ling Huei ^a  

^a INSTITUTE OF CELLULAR AND ORGANISMIC BIOLOGY   (Taiwan)

Author keywords

Apoptosis; Arsenic trioxide; Mitotic arrest; Spindle checkpoint; Taxol

Indexed keywords

ARSENIC TRIOXIDE; BROXURIDINE; BUB1 RELATED PROTEIN; CAMPTOTHECIN; PACLITAXEL; PROTEIN MAD2; PROTEIN P53;

APOPTOSIS; ARTICLE; CANCER CELL; CELL CYCLE PROGRESSION; CELL DIVISION; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; MITOSIS INHIBITION; MITOSIS SPINDLE; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANTINEOPLASTIC AGENTS; APOPTOSIS; ARSENICALS; CELL LINE, TUMOR; FIBROBLASTS; HELA CELLS; HUMANS; MITOSIS; MITOTIC SPINDLE APPARATUS; OXIDES; PACLITAXEL; TUMOR SUPPRESSOR PROTEIN P53;

EID: 54849423905     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.21861     Document Type: Article

References (61)

1. Akao Y, Mizoguchi H, Kojima S, Naoe T, Ohishi N, Yagi K. 1998. Arsenic induces apoptosis in B-cell leukaemic cell lines in vitro: Activation of caspases and down-regulation of Bcl-2 protein. Br J Haematol 102:1055-1060.
2. Bhonde MR, Hanski ML, Budczies J, Cao M, Gillissen B, Moorthy D, Simonetta F, Scherubl H, Truss M, Hagemeier C, Mewes HW, Daniel PT, Zeitz M, Hanski C. 2006. DNA damage-induced expression of p53 suppresses mitotic checkpoint kinase hMps1: The lack of this suppression in p53MUT cells contributes to apoptosis. J Biol Chem 281:8675-8685.
3. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
4. Cahill DP, Lengauer C, Yu J, Riggins GJ, Willson JK, Markowitz SD, Kinzler KW, Vogelstein B. 1998. Mutations of mitotic checkpoint genes in human cancers. Nature 392:300-303.
5. Cai X, Yu Y, Huang Y, Zhang L, Jia PM, Zhao Q, Chen Z, Tong JH, Dai W, Chen GQ. 2003. Arsenic trioxide-induced mitotic arrest and apoptosis in acute promyelocytic leukemia cells. Leukemia 17:1333-1337.
6. Casenghi M, Mangiacasale R, Tuynder M, Caillet-Fauquet P, Elhajouji A, Lavia P, Mousset S, Kirsch-Volders M, Cundari E. 1999. p53-independent apoptosis and p53-dependent block of DNA rereplication following mitotic spindle inhibition in human cells. Exp Cell Res 250:339-350.
7. Chen JG, Horwitz SB. 2002. Differential mitotic responses to microtubule-stabilizing and -destabilizing drugs. Cancer Res 62:1935-1938.
8. Chen GQ, Zhu J, Shi XG, Ni JH, Zhong HJ, Si GY, Jin XL, Tang W, Li XS, Xong SM, Shen ZX, Sun GL, Ma J, Zhang P, Zhang TD, Gazin C, Naoe T, Chen SJ, Wang ZY, Chen Z. 1996. 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 88:1052-1061.
9. 3 exerts dose-dependent dual effects on APL cells. Blood 89:3345-3353.
10. Chen JG, Yang CP, Cammer M, Horwitz SB. 2003. Gene expression and mitotic exit induced by microtubule-stabilizing drugs. Cancer Res 63:7891-7899.
11. Doherty SC, McKeown SR, McKelvey-Martin V, Downes CS, Atala A, Yoo JJ, Simpson DA, Kaufmann WK. 2003. Cell cycle checkpoint function in bladder cancer. J Natl Cancer Inst 95:1859-1868.
12. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. 2001. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498.
13. Filippova M, Duerksen-Hughes PJ. 2003. Inorganic and dimethylated arsenic species induce cellular p53. Chem Res Toxicol 16:423-431.
14. Huang SC, Lee TC. 1998. Arsenite inhibits mitotic division and perturbs spindle dynamics in HeLa S3 cells. Carcinogenesis 19:889-896.
15. Huang SC, Huang CYF, Lee TC. 2000. Induction of mitosis-mediated apoptosis by sodium arsenite in HeLa S3 cells. Biochem Pharmacol 60:771-780.
16. Hut HM, Lemstra W, Blaauw EH, Van Cappellen GW, Kampinga HH, Sibon OC. 2003. Centrosomes split in the presence of impaired DNA integrity during mitosis. Mol Biol Cell 14:1993-2004.
17. Hyun ParkW, Hee Cho Y, Won Jung C, Oh Park J, Kim K, Hyuck Im Y, Lee MH, Ki Kang W, Park K. 2003. Arsenic trioxide inhibits the growth of A498 renal cell carcinoma cells via cell cycle arrest or apoptosis. Biochem Biophys Res Commun 300:230-235.
18. Jordan MA, Wilson L. 2004. Microtubules as a target for anticancer drugs. Nat Rev Cancer 4:253-265.
19. Kajiguchi T, Yamamoto K, Hossain K, Akhand AA, Nakashima I, Naoe T, Saito H, Emi N. 2003. Sustained activation of c-jun-terminal kinase (JNK) is closely related to arsenic trioxide-induced apoptosis in an acute myeloid leukemia (M2)-derived cell line, NKM-1. Leukemia 17:2189-2195.
20. Kasai T, Iwanaga Y, Iha H, Jeang KT. 2002. Prevalent loss of mitotic spindle checkpoint in adult T-cell leukemia confers resistance to microtubule inhibitors. J Biol Chem 277:5187-5193.
21. Kops GJ, Weaver BA, Cleveland DW. 2005. On the road to cancer: Aneuploidy and the mitotic checkpoint. Nat Rev Cancer 5:773-785.
22. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
23. Li YM, Broome JD. 1999. Arsenic targets tubulins to induce apoptosis in myeloid leukemia cells. Cancer Res 59:776-780.
24. Ling YH, Jiang JD, Holland JF, Perez-Soler R. 2002. Arsenic trioxide produces polymerization of microtubules and mitotic arrest before apoptosis in human tumor cell lines. Mol Pharmacol 62:529-538.
25. Liu Q, Hilsenbeck S, Gazitt Y. 2003. Arsenic trioxide-induced apoptosis in myeloma cells: p53-dependent G1 or G2/M cell cycle arrest, activatio o caspase-8 or caspase-9, and synergy with APO2/TRAIL. Blood 101:4078-4087.
26. Masuda A, Maeno K, Nakagawa T, Saito H, Takahashi T. 2003. Association between mitotic spindle checkpoint impairment and susceptibility to the induction of apoptosis by anti-microtubule agents in human lung cancers. Am J Pathol 163:1109-1116.
27. Mathas S, Lietz A, Janz M, Hinz M, Jundt F, Scheidereit C, Bommert K, Dorken B. 2003. Inhibition of NF-kappaB essentially contributes to arsenic-induced apoptosis. Blood 102:1028-1034.
28. Morrison C, Rieder CL. 2004. Chromosome damage and progression into and through mitosis in vertebrates. DNA Repair (Amst) 3:1133-1139.
29. Niida H, Tsuge S, Katsuno Y, Konishi A, Takeda N, Nakanishi M. 2005. Depletion of Chk1 leads to premature activation of Cdc2-cyclin B and mitotic catastrophe. J Biol Chem 280:39246-39252.
30. Ora I, Bondesson L, Jonsson C, Ljungberg J, Porn-Ares I, Garwicz S, Pahlman S. 2000. Arsenic trioxide inhibits neuroblastoma growth in vivo and promotes apoptotic cell death in vitro. Biochem Biophys Res Commun 277:179-185.
31. Rieder CL, Cole RW, Khodjakov A, Sluder G. 1995: The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitor signal produced by unattached kinetochores. J Cell Biol 130:941-948.
32. Salazar AM, Ostrosky Wegman P, Menendez D, Miranda E, Garcia Carranca A, Rojas E. 1997. Induction of p53 protein expression by sodium arsenite. Mutat Res 381:259-265.
33. Soignet SL, Maslak P, Wang ZG, Jhanwar S, Calleja E, Dardashti LJ, Corso D, DeBlasio A, Gabrilove J, Scheinberg DA, Pandolfi PP, Warrell RP, Jr. 1998. Complete remission after treatment of acute promyelocytic leukemia with arsenic trioxide. N Engl J Med 339:1341-1348.
34. Stanbridge EJ, Flandermeyer RR, Daniels DW, Nelson-Rees WA. 1981. Specific chromosome loss associated with the expression of tumorigenicity in human cell hybrids. Somatic Cell Genet 7:699-712.
35. States JC, Reiners JJ, Jr., Pounds JG, Kaplan DJ, Beauerle BD, McNeely SC, Mathieu P, McCabe MJ, Jr. 2002. Arsenite disrupts mitosis and induces apoptosis in SV40-transformed human skin fibroblasts. Toxicol Appl Pharmacol 180:83-91.
36. Sudo T, Nitta M, Saya H, Ueno NT. 2004. Dependence of paclitaxel sensitivity on a functional spindle assembly checkpoint. Cancer Res 64:2502-2508.
37. Sze KM, Ching YP, Jin DY, Ng IO. 2004. Association of MAD2 expression with mitotic checkpoint competence in hepatoma cells. J Biomed Sci 11:920-927.
38. Takada S, Kelkar A, Theurkauf WE. 2003. Drosophila checkpoint kinase 2 couples centrosome function and spindle assembly to genomic integrity. Cell 113:87-99.
39. Takahashi T, Haruki N, Nomoto S, Masuda A, Saji S, Osada H, Takahashi T. 1999. Identification of frequent impairment of the mitotic checkpoint and molecular analysis of the mitotic checkpoint genes, hsMAD2 and p55CDC, in human lung cancers. Oncogene 18:4295-4300.
40. Tao W, South VJ, Zhang Y, Davide JP, Farrell L, Kohl NE, Sepp-Lorenzino L, Lobell RB. 2005. Induction of apoptosis by an inhibitor of the mitotic kinesin KSP requires both activation of the spindle assembly checkpoint and mitotic slippage. Cancer Cell 8:49-59.
41. Taylor SS, McKeon F. 1997. Kinetochore localization of murine Bub1 is required for normal mitotic timing and checkpoint response to spindle damage. Cell 89:727-735.
42. Taylor BF, McNeely SC, Miller HL, Lehmann GM, McCabe MJ, Jr., States JC. 2006. P53 suppression of arsenite-induced mitotic catastrophe is mediated by p21CIP1/WAF1. J Pharmacol Exp Ther.
43. Tighe A, Johnson VL, Albertella M, Taylor SS. 2001. Aneuploid colon cancer cells have a robust spindle checkpoint. EMBO Rep 2:609-614.
44. Torres K, Horwitz SB. 1998. Mechanisms of Taxol-induced cell death are concentration dependent. Cancer Res 58:3620-3626.
45. Tzeng CC, Liu HS, Li C, Jin YT, Chen RM, Yang WH, Lin JS. 1996. Characterization of two urothelium cancer cell lines derived from a blackfoot disease endemic area in Taiwan. Anticancer Res 16:1797-1804.
46. Vogel C, Kienitz A, Hofmann I, Muller R, Bastians H. 2004. Crosstalk of the mitotic spindle assembly checkpoint with p53 to prevent polyploidy. Oncogene 23:6845-6853.
47. Vogel C, Kienitz A, Muller R, Bastians H. 2005. The mitotic spindle checkpoint is a critical determinant for topoisomerase-based chemotherapy. J Biol Chem 280:4025-4028.
48. Wang TS, Kuo CF, Jan KY, Huang H. 1996. Arsenite induces apoptosis in Chinese hamster ovary cells by generation of reactive oxygen species. J Cell Physiol 169:256-268.
49. Wang ZG, Rivi R, Delva L, Konig A, Scheinberg DA, Gambacorti-Passerini C, Gabrilove JL, Warrell RP, Jr., Pandolfi PP. 1998. Arsenic trioxide and melarsoprol induce programmed cell death in myeloid leukemia cell lines and function in a PML and PML-RARalpha independent manner. Blood 92:1497-1504.
50. Wang X, Jin DY, Wong YC, Cheung AL, Chun AC, Lo AK, Liu Y, Tsao SW. 2000. Correlation of defective mitotic checkpoint with aberrantly reduced expression of MAD2 protein in nasopharyngeal carcinoma cells. Carcinogenesis 21:2293-2297.
51. Wang X, Jin DY, Ng RW, Feng H, Wong YC, Cheung AL, Tsao SW. 2002. Significance of MAD2 expression to mitotic checkpoint control in ovarian cancer cells. Cancer Res 62:1662-1668.
52. Yang Z, Guo J, Chen Q, Ding C, Du J, Zhu X. 2005. Silencing mitosin induces misaligned chromosomes, premature chromosome decondensation before anaphase onset, and mitotic cell death. Mol Cell Biol 25:4062-4074.
53. Yih LH, Lee TC. 2000. Arsenite induces p53 accumulation through an ATM-dependent pathway in human fibroblasts. Cancer Res 60:6346-6352.
54. Yih LH, Lee TC. 2003. Induction of C-anaphase and diplochromosome through dysregulation of spindle assembly checkpoint by sodium arsenite in human fibroblasts. Cancer Res 63:6680-6688.
55. Yih LH, Ho IC, Lee TC. 1997. Sodium arsenite disturbs mitosis and induces chromosome loss in human fibroblasts. Cancer Res 57:5051-5059.
56. Yih LH, Hsueh SW, Luu WS, Chiu TH, Lee TC. 2005. Arsenite induces prominent mitotic arrest via inhibition of G2 checkpoint activation in CGL-2 cells. Carcinogenesis 26:53-63.
57. Yih LH, Tseng YY, Wu YC, Lee TC. 2006. Induction of centrosome amplification during arsenite-induced mitotic arrest in CGL-2 cells. Cancer Res 66:2098-2106.
58. Yu HJ, Tsai TC, Hsieh TS, Chiu TY. 1992. Characterization of a newly established human bladder carcinoma cell line, NTUB1. J Formos Med Assoc 91:608-613.
59. Zhang TC, Cao EH, Li JF, Ma W, Qin JF. 1999. Induction of apoptosis and inhibition of human gastric cancer MGC-803 cell growth by arsenic trioxide. Eur J Cancer 35:1258-1263.
60. Zheng Y, Shi Y, Tian C, Jiang C, Jin H, Chen J, Almasan A, Tang H, Chen Q. 2003. Essential role of the voltage-dependent anion channel (VDAC) in mitochondrial permeability transition pore opening and cytochrome c release induced by arsenic trioxide. Oncogene 1:1.
61. Zhu XH, Shen YL, Jing YK, Cai X, Jia PM, Huang Y, Tang W, Shi GY, Sun YP, Dai J, Wang ZY, Chen SJ, Zhang TD, Waxman S, Chen Z, Chen GQ. 1999. Apoptosis and growth inhibition in malignant lymphocytes after treatment with arsenic trioxide at clinically achievable concentrations. J Natl Cancer Inst 91:772-778.