Reconstitution of human MCF-7 breast cancer cells with caspase-3 does not sensitize them to action of CDK inhibitors

Journal of Cellular Biochemistry

Volumn 112, Issue 1, 2011, Pages 273-288

  Wȩsierska Ga̧dek, Józefa ^a   Hackl, Stefan ^a   Zulehner, Nora ^a   Maurer, Margarita ^a   Komina, Oxana ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

CDK inhibitors; Cell cycle arrest; G2 arrest; P53AIP1

Indexed keywords

CASPASE 3; DNA; OLOMOUCINE; PROTEIN P53; ROSCOVITINE;

APOPTOSIS; ARTICLE; BREAST CANCER; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL FRACTIONATION; CELL PROLIFERATION; CELL STRAIN MCF 7; CONTROLLED STUDY; DNA DAMAGE; DOSE RESPONSE; DRUG EFFECT; DRUG MECHANISM; ENZYME ACTIVITY; ENZYME RECONSTITUTION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY;

ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CASPASE 3; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASES; FEMALE; HUMANS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS;

EID: 78651274005     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22918     Document Type: Article

References (61)

1. Alvi AJ, Austen B, Weston VJ, Fegan C, MacCallum D, Gianella-Borradori A, Lane DP, Hubank M, Powell JE, Wei W, Taylor AM, Moss PA, Stankovic T. 2005. A novel CDK inhibitor, CYC202 (R-roscovitine), overcomes the defect in p53-dependent apoptosis in B-CLL by down-regulation of genes involved in transcription regulation and survival. Blood 105:4484-4491.
2. Blagosklonny MV, Pardee AB. 2001. Exploiting cancer cell cycling for selective protection of normal cells. Cancer Res 61:4301-4305.
3. Bruno S, Ardelt B, Skierski JS, Traganos F, Darzynkiewicz Z. 1992. Different effects of staurosporine, an inhibitor of protein kinases, on the cell cycle and chromatin structure of normal and leukemic lymphocytes. Cancer Res 52: 470-473.
4. Couse JF, Korach KS. 1999. Estrogen receptor null mice: What have we learned and where will they lead uš Endocr Rev 20:358-417.
5. David-Pfeuty T. 1999. Potent inhibitors of cyclin-dependent kinase 2 induce nuclear accumulation of wild-type p53 and nucleolar fragmentation in human untransformed and tumor-derived cells. Oncogene 18:7409-7422.
6. De Azevedo WF, Leclerc S, Meijer L, Havlicek L, Strnad M, Kim SH. 1997. Inhibition of cyclin-dependent kinases by purine analogues: Crystal structure of human cdk2 complexed with roscovitine. Eur J Biochem 243:518-526.
7. Devarajan E, Sahin AA, Chen JS, Krishnamurthy RR, Aggarwal N, Brun AM, Sapino A, Zhang F, Sharma D, Yang XH, Tora AD, Mehta K. 2002. Downregulation of caspase 3 in breast cancer: A possible mechanism for chemoresistance. Oncogene 21:8843-8851.
8. Fan S, Smith ML, Rivet DJ II, Duba D, Zhan Q, Kohn KW, Fornace AJ, Jr., O'Connor PM. 1995. Disruption of p53 function sensitizes breast cancer MCF- 7 cells to cisplatin and pentoxifylline. Cancer Res 55:1649-1654.
9. Fiskum G, Kowaltowksi AJ, Andreyev AY, Kushnareva YE, Starkov AA. 2000. Apoptosis-related activities measured with isolated mitochondria and digitonin- permeabilized cells. Methods Enzymol 322:222-234.
10. Galons H, Oumata N, Meijer L. 2010. Cyclin-dependent kinase inhibitors: A survey of recent patent literature. Expert Opin Ther Pat 20:377-404.
11. Havlicek L, Hanus J, Vesely J, Leclerc S, Meijer L, Shaw G, Strnad M. 1997. Cytokinin-derived cyclin-dependent kinase inhibitors: Synthesis and cdc2 inhibitory activity of olomoucine and related compounds. J Med Chem 40: 408-412.
12. Janicke RU, Ng P, Sprengart ML, Porter AG. 1998a. Caspase-3 is required for alpha-fodrin cleavage but dispensable for cleavage of other death substrates in apoptosis. J Biol Chem 273:15540-15545.
13. Janicke RU, Sprengart ML, Wati MR, Porter AG. 1998b. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 273:9357-9360.
14. Komina O, Wesierska-Gadek J. 2008. Action of resveratrol alone or in combination with roscovitine, a CDK inhibitor, on cell cycle progression in human HL-60 leukemia cells. Biochem Pharmacol 76:1554-1562.
15. Kovar H, Jug G, Printz D, Bartl S, Schmid G, Wesierska-Gadek J. 2000. Characterization of distinct consecutive phases in non-genotoxic p53- induced apoptosis of Ewing tumor cells and the rate-limiting role of caspase 8. Oncogene 19:4096-4107.
16. Lapenna S, Giordano A. 2009. Cell cycle kinases as therapeutic targets for cancer. Nat Rev Drug Discov 8:547-566.
17. Ljungman M, Paulsen MT. 2001. The cyclin-dependent kinase inhibitor roscovitine inhibits RNA synthesis and triggers nuclear accumulation of p53 that is unmodified at Ser15 and Lys382. Mol Pharmacol 60:785-789.
18. Lu W, Chen L, Peng Y, Chen J. 2001. Activation of p53 by roscovitinemediated suppression of MDM2 expression. Oncogene 20:3206-3216.
19. MacCallum DE, Melville J, Frame S, Watt K, Anderson S, Gianella-Borradori A, Lane DP, Green SR. 2005. Seliciclib (CYC202, R-Roscovitine) induces cell death in multiple myeloma cells by inhibition of RNA polymerase IIdependent transcription and down-regulation of Mcl-1. Cancer Res 65: 5399-5407.
20. Maurer M, Komina O, Wesierska-Gadek J. 2009. Roscovitine differentially affects asynchronously growing and synchronized human MCF-7 breast cancer cells. Ann NY Acad Sci 1171:250-256.
21. Meijer L, Borgne A, Mulner O, Chong JP, Blow JJ, Inagaki N, Inagaki M, Delcros JG, Moulinoux JP. 1997. Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur J Biochem 243:527-536.
22. Murphy CG, Fornier M. 2010. HER2-positive breast cancer: Beyond trastuzumab. Oncology (Williston Park) 24:410-415.
23. Nathanson KL, Wooster R, Weber BL. 2001. Breast cancer genetics: What we know and what we need. Nat Med 7:552-556.
24. Negrini S, Gorgoulis VG, Halazonetis TD. 2010. Genomic instability-An evolving hallmark of cancer. Nat Rev Mol Cell Biol 11:220-228.
25. 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.
26. Oda K, Arakawa H, Tanaka T, Matsuda K, Tanikawa C, Mori T, Nishimori H, Tamai K, Tokino T, Nakamura Y, Taya Y. 2000. p53AIP1, a potential mediator of p53-dependent apoptosis, and its regulation by Ser-46-phosphorylated p53. Cell 102:849-862.
27. Paprskarova M, Krystof V, Jorda R, Dzubak P, Hajduch M, Wesierska-Gadek J, Strnad M. 2009. Functional p53 in cells contributes to the anticancer effect of the cyclin-dependent kinase inhibitor roscovitine. J Cell Biochem 107: 428-437.
28. Reers M, Smith TW, Chen LB. 1991. J-Aggregate formation of a carbocyanine as a quantitative fluorescent indicator of membrane potential. Biochemistry 30:4480-4486.
29. Rizzolio F, Tuccinardi T, Caligiuri I, Lucchetti C, Giordano A. 2010. CDK inhibitors: From the bench to clinical trials. Curr Drug Targets 11:279-290.
30. Rogalinska M, Blonski JZ, Komina O, Goralski P, Zolnierczyk JD, Piekarski H, Robak T, Kilianska ZM, Wesierska-Gadek J. 2010. R-roscovitine (Seliciclib) affects CLL cells more strongly than combinations of fludarabine or cladribine with cyclophosphamide: Inhibition of CDK7 sensitizes leukemic cells to caspase-dependent apoptosis. J Cell Biochem 109:217-235.
31. Schmid G, Wojciechowski J, Wesierska-Gadek J. 2005. Advantage of a baculovirus expression system for protein-protein interaction studies. Involvement of posttranslational phosphorylation in the interaction between wt p53 protein and poly(ADP-ribose) polymerase-1. Acta Biochim Pol 52:713-719.
32. Schuuring E, Verhoeven E, Mooi WJ, Michalides RJ. 1992. Identification and cloning of two overexpressed genes, U21B31/PRAD1 and EMS1, within the amplified chromosome 11q13 region in human carcinomas. Oncogene 7: 355-361.
33. Senderowicz AM. 2001. Cyclin-dependent kinase modulators: A novel class of cell cycle regulators for cancer therapy. Cancer Chemother Biol Response Modif 19:165-188.
34. Sherr CJ, Roberts JM. 1999. CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes Dev 13:1501-1512.
35. Silver DP, Richardson AL, Eklund AC, Wang ZC, Szallasi Z, Li Q, Juul N, Leong CO, Calogrias D, Buraimoh A, Fatima A, Gelman RS, Ryan PD, Tung NM, De Nicolo A, Ganesan S, Miron A, Colin C, Sgroi DC, Ellisen LW, Winer EP, Garber JE. 2010. Efficacy of neoadjuvant cisplatin in triple-negative breast cancer. J Clin Oncol 28:1145-1153.
36. Sutherland RL, Musgrove EA. 2004. Cyclins and breast cancer. J Mammary Gland Biol Neoplasia 9:95-104.
37. Sutherland RL, Musgrove EA. 2009. CDK inhibitors as potential breast cancer therapeutics: New evidence for enhanced efficacy in ER+ disease. Breast Cancer Res 11:112.
38. te Poele RH, Okorokov AL, Joel SP. 1999. RNA synthesis block by 5,6-dichloro-1-beta-D-ribofuranosylbenzimidazole (DRB) triggers p53- dependent apoptosis in human colon carcinoma cells. Oncogene 18:5765-5772.
39. Vesely J, Havlicek L, Strnad M, Blow JJ, Donella-Deana A, Pinna L, Letham DS, Kato J, Detivaud L, Leclerc S, Meijer L. 1994. Inhibition of cyclindependent kinases by purine analogues. Eur J Biochem 224:771-786.
40. Vindelov LL, Christensen IJ, Nissen NI. 1983. A detergent-trypsin method for the preparation of nuclei for flow cytometric DNA analysis. Cytometry 3: 323-327.
41. Wesierska-Gadek J, Krystof V. 2009. Selective cyclin-dependent kinase inhibitors discriminating between cell cycle and transcriptional kinases: Future reality or utopia̧ Ann NY Acad Sci 1171:228-241.
42. Wesierska-Gadek J, Schmid G. 2000. Overexpressed poly(ADP-ribose) polymerase delays the release of rat cells from p53-mediated G(1) checkpoint. J Cell Biochem 80:85-103.
43. Wesierska-Gadek J, Schmid G. 2006. Dual action of the inhibitors of cyclindependent kinases: Targeting of the cell-cycle progression and activation of wild-type p53 protein. Expert Opin Investig Drugs 15:23-38.
44. Wesierska-Gadek J, Bohrn E, Herceg Z, Wang ZQ, Wurzer G. 2000. Differential susceptibility of normal and PARP knock-out mouse fibroblasts to proteasome inhibitors. J Cell Biochem 78:681-696.
45. Wesierska-Gadek J, Schloffer D, Kotala V, Horky M. 2002. Escape of p53 protein from E6-mediated degradation in HeLa cells after cisplatin therapy. Int J Cancer 101:128-136.
46. Wesierska-Gadek J, Gueorguieva M, Wojciechowski J, Horky M. 2004a. Cell cycle arrest induced in human breast cancer cells by cyclin-dependent kinase inhibitors: A comparison of the effects exerted by roscovitine and olomoucine. Pol J Pharmacol 56:635-641.
47. Wesierska-Gadek J, Schloffer D, Gueorguieva M, Uhl M, Skladanowski A. 2004b. Increased susceptibility of poly(ADP-ribose) polymerase-1 knockout cells to antitumor triazoloacridone C-1305 is associated with permanent G2 cell cycle arrest. Cancer Res 64:4487-4497.
48. Wesierska-Gadek J, Gueorguieva M, Horky M. 2005a. Roscovitine-induced up-regulation of p53AIP1 protein precedes the onset of apoptosis in human MCF-7 breast cancer cells. Mol Cancer Ther 4:113-124.
49. Wesierska-Gadek J, Gueorguieva M, Ranftler C, Zerza-Schnitzhofer G. 2005b. A new multiplex assay allowing simultaneous detection of the inhibition of cell proliferation and induction of cell death. J Cell Biochem 96:1-7.
50. Wesierska-Gadek J, Schreiner T, Gueorguieva M, Ranftler C. 2006. Phenol red reduces ROSC mediated cell cycle arrest and apoptosis in human MCF-7 cells. J Cell Biochem 98:1367-1379.
51. Wesierska-Gadek J, Schmitz ML, Ranftler C. 2007. Roscovitine-Activated HIP2 kinase induces phosphorylation of wt p53 at Ser-46 in human MCF-7 breast cancer cells. J Cell Biochem 100:865-874.
52. Wesierska-Gadek J, Gueorguieva M, Komina O, Schmid G, Kramer MP. 2008a. Signaling of DNA damage is not sufficient to induce p53 response: (re)activation of wt p53 protein strongly depends on cellular context. J Cell Biochem 103:1607-1620.
53. Wesierska-Gadek J, Hajek SB, Sarg B, Wandl S, Walzi E, Lindner H. 2008b. Pleiotropic effects of selective CDK inhibitors on human normal and cancer cells. Biochem Pharmacol 76:1503-1514.
54. Wesierska-Gadek J, Wandl S, Kramer MP, Pickem C, Krystof V, Hajek SB. 2008c. Roscovitine up-regulates p53 protein and induces apoptosis in human HeLaS(3) cervix carcinoma cells. J Cell Biochem 105:1161-1171.
55. Wȩsierska-Ga̧dek J, Borza A, Komina O, Maurer M. 2009a. Impact of roscovitine, a selective CDK inhibitor, on cancer cells: Bi-functionality increases its therapeutic potential. Acta Biochim Pol 56:495-501.
56. Wȩsierska-Ga̧dek J, Borza A, Walzi E, Krystof V, Maurer M, Komina O, Wandl S. 2009b. Outcome of treatment of human HeLa cervical cancer cells with roscovitine strongly depends on the dosage and cell cycle status prior to the treatment. J Cell Biochem 106:937-955.
57. Wesierska-Gadek J, Maurer M, Zulehner N, Komina O. 2010. Whether to target single or multiple CDKs for therapy? That is the question. J Cell Physiol. DOI: 10.1002/jcp.22426.
58. Wȩsierska-Ga̧dek J, Chamrád I, Kryštof V. 2009c. Novel potent pharmacological cyclin-dependent kinase inhibitors. Future Med Chem 1:1561-1581.
59. Wojciechowski J, Horky M, Gueorguieva M, Wesierska-Gadek J. 2003. Rapid onset of nucleolar disintegration preceding cell cycle arrest in roscovitineinduced apoptosis of human MCF-7 breast cancer cells. Int J Cancer 106: 486-495.
60. Yang XH, Sladek TL, Liu X, Butler BR, Froelich CJ, Thor AD. 2001. Reconstitution of caspase 3 sensitizes MCF-7 breast cancer cells to doxorubicinand etoposide-induced apoptosis. Cancer Res 61:348-354.
61. Yoshida K, Monden M, Nakamura Y, Arakawa H. 2004. Adenovirus-mediated p53AIP1 gene transfer as a new strategy for treatment of p53-resistant tumors. Cancer Sci 95:91-97.