Paclitaxel induced apoptosis in breast cancer cells requires cell cycle transit but not Cdc2 activity

Cancer Chemotherapy and Pharmacology

Volumn 59, Issue 2, 2007, Pages 235-249

  Henley, D ^a   Isbill, M ^a   Fernando, R ^a   Foster, J S ^a   Wimalasena, J ^a,b  

^a UNIVERSITY OF TENNESSEE   (United States)

^b UNIVERSITY OF TENNESSEE GRADUATE SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Cdc2; Cell cycle; Microtubules; Paclitaxel

Indexed keywords

CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; DIMETHYL SULFOXIDE; DNA FRAGMENT; FULVESTRANT; HYDROXYUREA; PACLITAXEL; PROTEIN BAD; PROTEIN KINASE B; PROTEIN P27; ROSCOVITINE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; THYMIDINE;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CELL CYCLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL NUCLEUS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INDUCTION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MICROSCOPY; MICROTUBULE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; APOPTOSIS; BCL-ASSOCIATED DEATH PROTEIN; BLOTTING, WESTERN; BREAST NEOPLASMS; CDC2 PROTEIN KINASE; CELL CYCLE; CELL LINE, TUMOR; CELL NUCLEUS; CELL SURVIVAL; DNA FRAGMENTATION; ESTRADIOL; FLOW CYTOMETRY; HUMANS; HYDROXYUREA; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MITOTIC SPINDLE APPARATUS; NEOPLASM PROTEINS; PACLITAXEL; PURINES; RNA, SMALL INTERFERING; THYMIDINE; TRANSFECTION;

EID: 33845360031     PISSN: 03445704     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00280-006-0262-1     Document Type: Article

References (90)

1. Gilewski TA, Dang C, Surbone A, Norton L (2000) Principles of chemotherapy: cytokinetics. In: Holland JF, Frei E (eds) Cancer medicine, 5th edn. B.C. Decker, Canada, pp 511-538
2. Yarden Y, Sliwkowski MX (2001) Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2:127-137
3. Mollinedo F, Gajate C (2003) Microtubules, microtubule-interfering agents and apoptosis. Apoptosis 8:413-450
4. Beck WT, Cass CE, Houghton PJ (2000) Microtublue-targetting anticancer drugs derived from plants and microbes. In: Holland JF, Frei E (eds) Cancer medicine, 5th edn. B.C. Decker Inc, Canada, pp 680-698
5. Jordan MA, Wilson L (2004) Microtubules as a target for anticancer drugs. Nat Rev Cancer 4:253-265
6. DeAngelis LMPJB (2005) Neurologic complications. In: Blast RC Jr, et al (eds) B.C Decker inc, Canada
7. Jordan MA, Wendell K, Gardiner S, Derry WB, Copp H, Wilson L (1996) Mitotic block induced in HeLa cells by low concentrations of paclitaxel (Taxol) results in abnormal mitotic exit and apoptotic cell death. Cancer Res 56:816-825
8. Mamay CL, Mingo-Sion AM, Wolf DM, Molina MD, Van Den Berg CL (2003) An inhibitory function for JNK in the regulation of IGF-I signaling in breast cancer. Oncogene 22:602-614
9. Razandi M, Pedram A, Levin ER (2000) Plasma membrane estrogen receptors signal to antiapoptosis in breast cancer [In Process Citation]. Mol Endocrinol 14(9):1434-1447
10. Lin MT, Chang CC, Chen ST, Chang HL, Su JL, Chau YP, Kuo ML (2004) Cyr61 expression confers resistance to apoptosis in breast cancer MCF-7 cells by a mechanism of NF-kappaB-dependent XIAP up-regulation. J Biol Chem 279:24015-24023
11. Chadderton A, Villeneuve DJ, Gluck S, Kirwan-Rhude AF, Gannon BR, Blais DE, Parissenti AM (2000) Role of specific apoptotic pathways in the restoration of paclitaxel-induced apoptosis by valspodar in doxorubicin-resistant MCF-7 breast cancer cells. Breast Cancer Res Treat 59:231-244
12. Ling X, Bernacki RJ, Brattain MG, Li F (2004) Induction of survivin expression by taxol (paclitaxel) is an early event, which is independent of taxol-mediated G2/M arrest. J Biol Chem 279:15196-15203
13. Wang TH, Wang HS, Ichijo H, Giannakakou P, Foster JS, Fojo T, Wimalasena J (1998) Microtubule-interfering agents activate c-Jun N-terminal kinase/stress-activated protein kinase through both Ras and apoptosis signal- regulating kinase pathways. J Biol Chem 273:4928-4936
14. Lee LF, Li G, Templeton DJ, Ting JP (1998) Paclitaxel (Taxol)-induced gene expression and cell death are both mediated by the activation of c-Jun NH2-terminal kinase (JNK/SAPK). J Biol Chem 273:28253-28260
15. Amato SF, Swart JM, Berg M, Wanebo HJ, Mehta SR, Chiles TC (1998) Transient stimulation of the c-Jun-NH2-terminal kinase/activator protein 1 pathway and inhibition of extracellular signal-regulated kinase are early effects in paclitaxel-mediated apoptosis in human B lymphoblasts. Cancer Res 58:241-247
16. Wang TH, Popp DM, Wang HS, Saitoh M, Mural JG, Henley DC, Ichijo H, Wimalasena J (1999) Microtubule dysfunction induced by paclitaxel initiates apoptosis through both c-Jun N-terminal kinase (JNK)-dependent and -independent pathways in ovarian cancer cells. J Biol Chem 274:8208-8216
17. Harborth J, Elbashir SM, Bechert K, Tuschl T, Weber K (2001) Identification of essential genes in cultured mammalian cells using small interfering RNAs. J Cell Sci 114:4557-4565
18. McConnell BB, Gregory FJ, Stott FJ, Hara E, Peters G (1999) Induced expression of p16(INK4a) inhibits both CDK4- and CDK2-associated kinase activity by reassortment of cyclin-CDK-inhibitor complexes. Mol Cell Biol 19:1981-1989
19. Carrano AC, Eytan E, Hershko A, Pagano M (1999) SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat Cell Biol 1:193-199
20. Tsai LH, Lees E, Faha B, Harlow E, Riabowol K (1993) The cdk2 kinase is required for the G1-to-S transition in mammalian cells. Oncogene 8:1593-1602
21. Craig C, Kim M, Ohri E, Wersto R, Katayose D, Li Z, Choi YH, Mudahar B, Srivastava S, Seth P, et al (1998) Effects of adenovirus-mediated p16INK4A expression on cell cycle arrest are determined by endogenous p16 and Rb status in human cancer cells. Oncogene 16:265-272
22. Leone G, DeGregori J, Sears R, Jakoi L, Nevins JR (1997) Myc and Ras collaborate in inducing accumulation of active cyclin E/Cdk2 and E2F [published erratum appears in Nature 387(6636):932]. Nature 387:422-426
23. Craig C, Wersto R, Kim M, Ohri E, Li Z, Katayose D, Lee SJ, Trepel J, Cowan K, Seth P (1997) A recombinant adenovirus expressing p27Kip1 induces cell cycle arrest and loss of cyclin-Cdk activity in human breast cancer cells. Oncogene 14:2283-2289
24. Sears R, Leone G, DeGregori J, Nevins JR (1999) Ras enhances Myc protein stability. Mol Cell 3:169-179
25. Stein GS, Stein JL, Lian JB, Last TJ, McCabe L (1998) Synchronization of normal diploid and transformed mammalian cells. In: Julio E. Celis (ed) Cell biology, vol 1, 2nd edn. pp253-260
26. Foster JS, Henley DC, Bukovsky A, Seth P, Wimalasena J (2001) Multifaceted regulation of cell cycle progression by estrogen: regulation of Cdk inhibitors and Cdc25A independent of cyclin D1-Cdk4 function. Mol Cell Biol 21:794-810
27. Foster JS, Wimalasena J (1996) Estrogen regulates activity of cyclin-dependent kinases and retinoblastoma protein phosphorylation in breast cancer cells. Mol Endocrinol 10:488-498
28. Ahamed S, Foster JS, Bukovsky A, Wimalasena J (2001) Signal transduction through the ras/Erk pathway is essential for the mycoestrogen zearalenone-induced cell-cycle progression in MCF-7 cells. Mol Carcinog 30:88-98
29. Foster JS, Henley DC, Ahamed S, Wimalasena J (2001) Estrogens and cell-cycle regulation in breast cancer. Trends Endocrinol Metab 12:320-327
30. Foster JS, Fernando RI, Ishida N, Nakayama KI, Wimalasena J (2003) Estrogens down-regulate p27Kip1 in breast cancer cells through SKP2,and through nuclear export mediated by the extracellular signal-regulatedkinase (Erk) pathway. J Biol Chem 278:41355-41366
31. Ahamed S, Foster JS, Bukovsky A, Diehl JA, Wimalasena J (2002) Removal of Cdk inhibitors through both sequestration and downregulation in zearalenone-treated MCF-7 breast cancer cells. Mol Carcinog 34:45-58
32. Fernando RI, Wimalasena J (2004) Estradiol abrogates apoptosis in breast cancer cells through inactivation of BAD: ras-dependent nongenomic pathways requiring signaling through ERK and Akt. Mol Biol Cell 15:3266-3284
33. Resnitzky D, Reed SI (1995) Different roles for cyclins D1 and E in regulation of the G1-to-S transition. Mol Cell Biol 15:3463-3469
34. Jazirehi AR, Gan XH, De Vos S, Emmanouilides C, Bonavida B (2003) Rituximab (anti-CD20) selectively modifies Bcl-xL and apoptosis protease activating factor-1 (Apaf-1) expression and sensitizes human non-Hodgkin's lymphoma B cell lines to paclitaxel-induced apoptosis. Mol Cancer Ther 2:1183-1193
35. Strobel T, Tai YT, Korsmeyer S, Cannistra SA (1998) BAD partly reverses paclitaxel resistance in human ovarian cancer cells. Oncogene 17:2419-2427
36. Page C, Lin HJ, Jin Y, Castle VP, Nunez G, Huang M, Lin J (2000) Overexpression of Akt/AKT can modulate chemotherapy-induced apoptosis. Anticancer Res 20:407-416
37. Blajeski AL, Phan VA, Kottke TJ, Kaufmann SH (2002) G(1) and G(2) cell-cycle arrest following microtubule depolymerization in human breast cancer cells. J Clin Invest 110:91-99
38. Torres K, Horwitz SB (1998) Mechanisms of Taxol-induced cell death are concentration dependent. Cancer Res 58:3620-3626
39. Jordan MA (2002) Mechanism of action of antitumor drugs that interact with microtubules and tubulin. Curr Med Chem Anti-Canc Agents 2:1-17
40. Wahl AF, Donaldson KL, Fairchild C, Lee FY, Foster SA, Demers GW, Galloway DA (1996) Loss of normal p53 function confers sensitization to Taxol by increasing G2/M arrest and apoptosis [see comments]. Nat Med 2:72-79
41. Blajeski AL, Kottke TJ, Kaufmann SH (2001) A multistep model for paclitaxel-induced apoptosis in human breast cancer cell lines. Exp Cell Res 270:277-288
42. Johnson KR, Young KK, Fan W (1999) Antagonistic interplay between antimitotic and G1-S arresting agents observed in experimental combination therapy. Clin Cancer Res 5:2559-2565
43. Castedo M, Perfettini JL, Roumier T, Kroemer G (2002) Cyclin-dependent kinase-1: linking apoptosis to cell cycle and mitotic catastrophe. Cell Death Differ 9:1287-1293
44. Harvey KJ, Lukovic D, Ucker DS (2000) Caspase-dependent Cdk activity is a requisite effector of apoptotic death events. J Cell Biol 148:59-72
45. Chadebech P, Truchet I, Brichese L, Valette A (2000) Upregulation of cdc2 protein during paclitaxel-induced apoptosis. Int J Cancer 87:779-786
46. Motwani M, Delohery TM, Schwartz GK (1999) Sequential dependent enhancement of caspase activation and apoptosis by flavopiridol on paclitaxel-treated human gastric and breast cancer cells. Clin Cancer Res 5:1876-1883
47. Ling YH, Consoli U, Tornos C, Andreeff M, Perez-Soler R (1998) 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 75:925-932
48. Harvey KJ, Blomquist JF, Ucker DS (1998) Commitment and effector phases of the physiological cell death pathway elucidated with respect to Bcl-2 caspase, and cyclin-dependent kinase activities. Mol Cell Biol 18:2912-2922
49. Shen SC, Huang TS, Jee SH, Kuo ML (1998) Taxol-induced p34cdc2 kinase activation and apoptosis inhibited by 12-O-tetradecanoylphorbol-13-acetate in human breast MCF-7 carcinoma cells. Cell Growth Differ 9:23-29
50. Vantieghem A, Xu Y, Assefa Z, Piette J, Vandenheede JR, Merlevede W, De Witte PA, Agostinis P (2002) Phosphorylation of Bcl-2 in G2/M phase-arrested cells following photodynamic therapy with hypericin involves a CDK1-mediated signal and delays the onset of apoptosis. J Biol Chem 277:37718-37731
51. Tan X, Wang JY (1998) The caspase-RB connection in cell death. Trends Cell Biol 8:116-120
52. Meikrantz W (1996) Suppression of apoptosis by dominant negative mutants of cyclin-dependent protein kinases. J Biol Chem 271:10205-10209
53. Ye K, Zhou J, Landen JW, Bradbury EM, Joshi HC (2001) Sustained activation of p34(cdc2) is required for noscapine-induced apoptosis. J Biol Chem 276:46697-46700
54. Konishi Y, Lehtinen M, Donovan N, Bonni A (2002) Cdc2 phosphorylation of BAD links the cell cycle to the cell death machinery. Mol Cell 9:1005-1016
55. Yao SL (1996) Requirement of p34cdc2 kinase for apoptosis mediated by the Fas/APO-1 receptor and interleukin 1beta-converting enzyme-related proteases. Cancer Res 56:4551-4555
56. Yu C, Rahmani M, Dai Y, Conrad D, Krystal G, Dent P, Grant S (2003) The lethal effects of pharmacological cyclin-dependent kinase inhibitors in human leukemia cells proceed through a phosphatidylinositol 3-kinase/Akt-dependent process. Cancer Res 63:1822-1833
57. Ham YM, Choi KJ, Song SY, Jin YH, Chun MW, Lee SK (2003) Xylocydine, a novel inhibitor of cyclin-dependent kinases, prevents the TRAIL-induced apoptotic cell death of SK-HEP-1 cells. J Pharmacol Exp Ther
58. Shu CH, Yang WK, Shih YL, Kuo ML, Huang TS (1997) Cell cycle G2/M arrest and activation of cyclin-dependent kinases associated with low-dose paclitaxel-induced sub-G1 apoptosis. Apoptosis 2:463-470
59. Shi L, Nishioka WK, Th'ng J, Bradbury EM, Litchfield DW, Greenberg AH (1994) Premature p34cdc2 activation required for apoptosis. Science 263:1143-1145
60. Hiromura K, Pippin JW, Blonski MJ, Roberts JM, Shankland SJ (2002) The subcellular localization of cyclin dependent kinase 2 determines the fate of mesangial cells: role in apoptosis and proliferation. Oncogene 21:1750-1758
61. Ongkeko W, Ferguson DJ, Harris AL, Norbury C (1995) Inactivation of Cdc2 increases the level of apoptosis induced by DNA damage. J Cell Sci 108(Pt 8):2897-2904
62. Itzhaki JE, Gilbert CS, Porter AC (1997) Construction by gene targeting in human cells of a "conditional" CDC2 mutant that rereplicates its DNA. Nat Genet 15:258-265
63. Patel V, Senderowicz AM, Pinto DJ, Igishi T, Raffeld M, Quintanilla-Martinez L, Ensley JF, Sausville EA, Gutkind JS (1998) Flavopiridol, a novel cyclin-dependent kinase inhibitor, suppresses the growth of head and neck squamous cell carcinomas by inducing apoptosis. J Clin Invest 102:1674-1681
64. Zhai S, Senderowicz AM, Sausville EA, Figg WD (2002) Flavopiridol, a novel cyclin-dependent kinase inhibitor, in clinical development. Ann Pharmacother 36:905-911
65. Tamm I, Schumacher A, Karawajew L, Ruppert V, Arnold W, Nussler AK, Neuhaus P, Dorken B, Wolff G (2002) Adenovirus-mediated gene transfer of P16INK4/CDKN2 into bax-negative colon cancer cells induces apoptosis and tumor regression in vivo. Cancer Gene Ther 9:641-650
66. Samuelsson MK, Pazirandeh A, Okret S (2002) A pro-apoptotic effect of the CDK inhibitor p57(Kip2) on staurosporine-induced apoptosis in HeLa cells. Biochem Biophys Res Commun 296:702-709
67. Basile JR, Eichten A, Zacny V, Munger K (2003) NF-kappaB-mediated induction of p21(Cip1/Waf1) by tumor necrosis factor alpha induces growth arrest and cytoprotection in normal human keratinocytes. Mol Cancer Res 1:262-270
68. Carvalho A, Carmena M, Sambade C, Earnshaw WC, Wheatley SP (2003) Survivin is required for stable checkpoint activation in taxol-treated HeLa cells. J Cell Sci 116:2987-2998
69. O'Connor DS, Wall NR, Porter AC, Altieri DC (2002) A p34(cdc2) survival checkpoint in cancer. Cancer Cell 2:43-54
70. Mesri M, Wall NR, Li J, Kim RW, Altieri DC (2001) Cancer gene therapy using a survivin mutant adenovirus. J Clin Invest 108:981-990
71. Giodini A, Kallio MJ, Wall NR, Gorbsky GJ, Tognin S, Marchisio PC, Symons M, Altieri DC (2002) Regulation of microtubule stability and mitotic progression by survivin. Cancer Res 62:2462-2467
72. Tanaka K, Iwamoto S, Gon G, Nohara T, Iwamoto M, Tanigawa N (2000) Expression of survivin and its relationship to loss of apoptosis in breast carcinomas. Clin Cancer Res 6:127-134
73. Song Z, Yao X, Wu M (2003) Direct Interaction between Survivin and Smac/DIABLO is essential for the anti-apoptotic activity of Survivin during Taxol-induced apoptosis. J Biol Chem 278:23130-23140
74. O'Connor DS, Grossman D, Plescia J, Li F, Zhang H, Villa A, Tognin S, Marchisio PC, Altieri DC (2000) Regulation of apoptosis at cell division by p34cdc2 phosphorylation of survivin. Proc Natl Acad Sci USA 97:13103-13107
75. Boldt S, Weidle UH, Kolch W (2002) The role of MAPK pathways in the action of chemotherapeutic drugs. Carcinogenesis 23:1831-1838
76. Shtil AA, Mandlekar S, Yu R, Walter RJ, Hagen K, Tan TH, Roninson IB, Kong AN (1999) Differential regulation of mitogen-activated protein kinases by microtubule-binding agents in human breast cancer cells. Oncogene 18:377-384
77. McDaid HM, Horwitz SB (2001) Selective potentiation of paclitaxel (taxol)-induced cell death by mitogen-activated protein kinase kinase inhibition in human cancer cell lines. Mol Pharmacol 60:290-301
78. Stadheim TA, Xiao H, Eastman A (2001) Inhibition of extracellular signal-regulated kinase (ERK) mediates cell cycle phase independent apoptosis in vinblastine-treated ML-1 cells. Cancer Res 61:1533-1540
79. Kolfschoten GM, Hulscher TM, Duyndam MC, Pinedo HM, Boven E (2002) Variation in the kinetics of caspase-3 activation, Bcl-2 phosphorylation and apoptotic morphology in unselected human ovarian cancer cell lines as a response to docetaxel. Biochem Pharmacol 63:733-743
80. Zhang H, Shi X, Zhang QJ, Hampong M, Paddon H, Wahyuningsih D, Pelech S (2002) Nocodazole-induced p53-dependent c-Jun N-terminal kinase activation reduces apoptosis in human colon carcinoma HCT116 cells. J Biol Chem 277:43648-43658
81. Denicourt C, Dowdy SF (2004) Cip/Kip proteins: more than just CDKs inhibitors. Genes Dev 18:851-855
82. Besson A, Gurian-West M, Schmidt A, Hall A, Roberts JM (2004) p27Kip1 modulates cell migration through the regulation of RhoA activation. Genes Dev 18:862-876
83. Kim GY, Mercer SE, Ewton DZ, Yan Z, Jin K, Friedman E (2002) The stress-activated protein kinases p38 alpha and JNK1 stabilize p21(Cip1) by phosphorylation. J Biol Chem 277:29792-29802
84. Heliez C, Baricault L, Barboule N, Valette A (2003) Paclitaxel increases p21 synthesis and accumulation of its AKT-phosphorylated form in the cytoplasm of cancer cells. Oncogene 22:3260-3268
85. MacKeigan JP, Taxman DJ, Hunter D, Earp HS III, Graves LM, Ting JP (2002) Inactivation of the antiapoptotic phosphatidylinositol 3-kinase-akt pathway by the combined treatment of taxol and mitogen-activated protein kinase kinase inhibition. Clin Cancer Res 8:2091-2099
86. Hu L, Hofmann J, Lu Y, Mills GB, Jaffe RB (2002) Inhibition of phosphatidylinositol 3′-kinase increases efficacy of paclitaxel in in vitro and in vivo ovarian cancer models. Cancer Res 62:1087-1092
87. Mitsuuchi Y, Johnson SW, Selvakumaran M, Williams SJ, Hamilton TC, Testa JR (2000) The phosphatidylinositol 3-kinase/AKT signal transduction pathway plays a critical role in the expression of p21WAF1/CIP1/SDI1 induced by cisplatin and paclitaxel. Cancer Res 60:5390-5394
88. Lin HL, Lui WY, Liu TY, Chi CW (2003) Reversal of Taxol resistance in hepatoma by cyclosporin a: involvement of the PI-3 kinase-AKT 1 pathway. Br J Cancer 88:973-980
89. Boudny V, Nakano S (2003) Src tyrosine kinase but not activated Ras augments sensitivity to taxanes through apoptosis in human adenocarcinoma cells. Anticancer Res 23:7-12
90. Beck WT, Cass CE, Houghton P (2000) In: Holland JF, Frei E (eds) Cancer medicine, 5th edn. B.C. Decker, Canada, pp 680-695