Cytostatic activity of paclitaxel in coronary artery smooth muscle cells is mediated through transient mitotic arrest followed by permanent post-mitotic arrest: Comparison with cancer cells

Cell Cycle

Volumn 5, Issue 14, 2006, Pages 1574-1579

  Blagosklonny, Mikhail V ^a,b,c   Demidenko, Zoya N ^c   Giovino, Maria ^d   Szynal, Carmin ^d   Donskoy, Elina ^d   Herrmann, Robert A ^d   Barry, James J ^d   Whalen, Anne M ^d  

^a NEW YORK MEDICAL COLLEGE   (United States)

^b ORDWAY RESEARCH INSTITUTE   (United States)

^c Oncotarget Inc   (United States)

^d BOSTON SCIENTIFIC CORPORATION   (United States)

Author keywords

Cancer cells; Cell cycle; Paclitaxel; Restenosis; Smooth muscle cells; Stent

Indexed keywords

BETA GALACTOSIDASE; CYCLIN B1; CYCLINE; PACLITAXEL;

ARTICLE; CANCER CELL; CELL CYCLE; CELL CYCLE G1 PHASE; CELL STRAIN HL 60; CELL SURVIVAL; CONTROLLED STUDY; CORONARY ARTERY; CYTOSTASIS; DRUG ELUTING STENT; ENZYME ACTIVITY; GROWTH INHIBITION; HUMAN; HUMAN CELL; INFLAMMATION; LEUKEMIA CELL; LUNG CANCER; METABOLIC ACTIVATION; MITOSIS INHIBITION; PHENOTYPE; RESTENOSIS; SMOOTH MUSCLE FIBER; TETRAPLOIDY;

EID: 33746268096     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.5.14.3113     Document Type: Article

References (40)

1. Grube E, Silber S, Hauptmann KE, Mueller R, Buellesfeld L, Gerckens U, Russell ME. TAXUS I: six- and twelve-month results from a randomized, double-blind trial on a slow-release paclitaxel-eluting stent for de novo coronary lesions. Circulation 2003; 107:38-42.
2. Park SJ, Shim WH, Ho DS, Raizner AE, Park SW, Hong MK, Lee CW, Choi D, Jang Y, Lam R, Weissman NJ, Mintz GS. A Paclitaxel-eluting stent for the prevention of coronary restenosis. N Engl J Med 2003; 348:1537-45.
3. Ferguson JE, Patterson C. Break the cycle: The role of cell-cycle modulation in the prevention of vasculoproliferative diseases. Cell Cycle 2003; 2:211-9.
4. Ong AT, Serruys PW. Technology Insight: an overview of research in drug-eluting stents. Nat Clin Pract Cardiovasc Med 2005; 2:647-58.
5. Sollott SJ, Cheng L, Pauly RR, Jenkins GM, Monticone RE, Kuzuya M, Froehlich JP, Crow MT, Lakatta EG, Rowinsky EK, et al. Taxol inhibits neointimal smooth muscle cell accumulation after angioplasty in the rat. J Clin Invest. 1995; 95:1869-76.
6. Herdeg C, Oberhoff M, Baumbach A, Blattner A, Axel DI, Schroder S, Heinle H, Karsch KR. Local paclitaxel delivery for the prevention of restenosis: biological effects and efficacy in vivo. J Am Coll Cardiol 2000; 35:1969-76.
7. Horwitz SB. Mechanism of action of taxol. Trends Pharmacol Sci 1992; 13:134-6.
8. Jordan MA, Toso RJ, Thrower D, Wilson L. Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proc Natl Acad Sci USA 1993; 90:9552-6.
9. Jordan MA, Wendell K, Gardiner S, Derry WB, Copp H, Wilson L. Mitotic block induced in HeLa cells by low concentrations of paclitaxel (taxol) results in abnormal mitotic exit and apoptotic cell death. Cancer Res 1996; 56:816-25.
10. Abal M, Andreu JM, Barasoain I. Taxanes: microtubule and centrosome targets, and cell cycle dependent mechanisms of action. Curr Cancer Drug Targets 2003; 3:193-203.
11. Rieder CL, Maiato H. Stuck in division or passing through: what happens when cells cannot satisfy the spindle assembly checkpoint. Dev Cell 2004; 7:637-51.
12. Donaldson KL, Goolsby GL, Wahl AF. Cytotoxicity of the anticancer agents cisplatin and taxol during cell proliferation and the cell cycle. Int J Cancer 1994; 57:847-55.
13. Woods CM, Zhu J, McQueney PA, Bollag D, Lazarides E. Taxol-induced mitotic block triggers rapid onset of a p53-independent apoptotic pathway. Mol Medicine 1995; 1:506-26.
14. Frankel A, Buckman R, Kerbel RS. Abrogation of taxol-induced G2-M arrest and apoptosis in human ovarian cancer cells grown as multicellular tumor spheroids. Cancer Res 1997; 57:2388-93.
15. Torres K, Horwitz SB. Mechanisms of Taxol-induced cell death are concentration dependent. Cancer Res 1998; 58:3620-6.
16. Perkins CL, Fang G, Kim CN, Bhalla KN. The role of Apaf-1, caspase-9, and bid proteins in etoposide- or paclitaxel-induced mitochondrial events during apoptosis. Cancer Res 2000; 60:1645-53.
17. Bhalla KN. Microtubule-targeted anticancer agents and apoptosis. Oncogene 2003; 22:9075-86.
18. Blagosklonny MV, Darzynkiewicz Z, Halicka HD, Pozarowski P, Demidenko ZN, Barry JJ, Kamath KR, Herrmann RA. Paclitaxel induces primary and postmitotic G(1) arrest in human arterial smooth muscle cells. Cell Cycle 2004; 3:1050-6.
19. Kung AL, Sherwood SW, Schimke RT. Cell line-specific differences in control of cell cycle progression in the absence of mitosis. Proc Natl Acad Sci USA 1990;87:9553-7.
20. Giannakakou P, Robey R, Fojo T, Blagosklonny MV. Low concentrations of paclitaxel induce cell type-dependent p53, p21 and G1/G2 cell cycle arrest instead of mitotic arrest: molecular determinants of paclitaxel-induced cytotoxicity. Oncogene 2001; 20:3806-13.
21. Blagosklonny MV, Robey R, Sheikh MS, Fojo T. Paclitaxel-induced FasL-independent apoptosis and slow (non-apoptotic) cell death. Cancer Biol Ther 2002;1:113-7.
22. Broker LE, Huisman C, Ferreira CG, Rodriguez JA, Kruyt FAE, Giaccone G. Late activation of apoptotic pathways plays a negligible role in mediating the cytotoxic effects of discodermolide and epothilone B in non-small cell lung cancer cells. Cancer Res 2002; 62:4081-8.
23. Bhalla K, Ibrado AM, Tourkina E, Tang C, Maloney ME, Huang Y. Taxol induces internucleosomal DNA fragmentation associated with programmed cell death in human myeloid leukemia cells. Leukemia 1993; 7:563-8.
24. Donaldson KL, Goolsby G, Kiener PA, Wahl AF. Activation of p34cdc coincident with taxol-induced apoptosis. Cell Growth Diff 1994; 5:1041-50.
25. Kolfschoten GM, Hulscher TM, Duyndam MC, Pinedo HM, Boven E. 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 2002; 63:733-43.
26. Long BH, Fairchild CR. Paclitaxel inhibits progression of mitotic cells to G1 phase by interference with spindle formation without affecting other microtubule functions during anaphase and telephase. Cancer Res 1994; 54:4355-61.
27. Barboule N, Chadebech P, Baldin V, Vidal S, Valette A. Involvement of p21 in mitotic exit after paclitaxel treatment in MCF-7 breast adenocarcinoma cell lines. Oncogene 1997; 15:2867-75.
28. Parry TJ, Brosius R, Thyagarajan R, Carter D, Argentieri D, Falotico R, Siekierka J. Drug-eluting stents: sirolimus and paclitaxel differentially affect cultured cells and injured arteries. Eur J Pharmacol 2005; 524:19-29.
29. Axel DI, Kunert W, Goggelmann C, Oberhoff M, Herdeg C, Kuttner A, Wild DH, Brehm BR, Riessen R, Koveker G, Karsch KR. Paclitaxel inhibits arterial smooth muscle cell proliferation and migration in vitro and in vivo using local drug delivery. Circulation 1997; 96:636-45.
30. Wiskirchen J, Schober W, Schart N, Kehlbach R, Wersebe A, Tepe G, Claussen CD, Duda SH. The effects of paclitaxel on the three phases of restenosis: smooth muscle cell proliferation, migration, and matrix formation: an in vitro study. Invest Radiol 2004; 39:565-71.
31. Klein LE, Freeze B.S., Smith AB, Horwitz SB. The microtubule stabilizing agent discodermolide is a potent inducer of accelerated cell senescence. Cell Cycle 2005; 4:501-17.
32. Minamino T, Yoshida T, Tateno K, Miyauchi H, Zou Y, Toko H, Komuro I. Ras induces vascular smooth muscle cell senescence and inflammation in human atherosclerosis. Circulation 2003; 108:2264-9.
33. Demidenko ZN, Blagosklonny MV. Flavopiridol induces p53 via initial inhibition of Mdm2 and p21 and, independently of p53, sensitizes apoptosis-reluctant cells to tumor necrosis factor. Cancer Res 2004; 64:3653-60.
34. Pasquier E, Carre M, Pourroy B, Camoin L, Rebai O, Briand C, Braguer D. Antiangiogenic activity of paclitaxel is associated with its cytostatic effect, mediated by the initiation but not completion of a mitochondrial apoptotic signaling pathway. Mol Cancer Ther 2004; 3:1301-10.
35. Wright KM, Deshmukh M. Restricting apoptosis for postmitotic cell survival and its relevance to cancer. Cell Cycle 2006; In press.
36. Kroemer G, El-Deiry WS, Golstein P, Peter ME, Vaux D, Vandenabeele P, Zhivotovsky B, Blagosklonny MV, Malorni W, Knight RA, Piacentini M, Nagata S, Melino G. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ 2005; 12:S1463-7.
37. Darzynkiewicz Z, Bedner E, Smolewski P. Flow cytometry in analysis of cell cycle and apoptosis. Semin Hematol 2001; 38:179-93.
38. Brehm BR, Bock C, Wesselborg S, Pfeiffer S, Schuler S, Schulze-Osthoff K. Prevention of human smooth muscle cell proliferation without induction of apoptosis by the topoisomerase I inhibitor topotecan. Biochem Pharmacol 2001; 61:119-27.
39. Lanni JS, Jacks T. Characterization of the p53-dependent postmitotic checkpoint following spindle disruption. Mol Cell Biol 1998; 18:1055-64.
40. Panvichian R, Orth K, Day ML, Day KC, Pilat MJ, Pienta KJ. Paclitaxel-associated multimininucleation is permitted by the inhibition of caspase activation: a potential early step in drug resistance. Cancer Res 1998; 58:4667-72.