Microtubule-interacting drugs induce moderate and reversible damage to human bone marrow mesenchymal stem cells

Cell Proliferation

Volumn 42, Issue 4, 2009, Pages 434-447

  Polioudaki, H ^a   Kastrinaki, M C ^a   Papadaki, H A ^a   Theodoropoulos, P A ^a  

^a UNIVERSITY OF CRETE   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; NOCODAZOLE; PACLITAXEL; PROTEIN P53; TUBULIN;

ARTICLE; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL DEATH; CELL NUCLEUS MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; DRUG CYTOTOXICITY; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; MESENCHYMAL STEM CELL; MICROTUBULE; NORMAL HUMAN; PROTEIN SYNTHESIS;

BONE MARROW CELLS; CELL CYCLE; CELL DEATH; CELL NUCLEUS; CELL PROLIFERATION; CELLS, CULTURED; GENE EXPRESSION; HUMANS; MESENCHYMAL STEM CELLS; MICROTUBULES; NOCODAZOLE; NUCLEAR ENVELOPE; PACLITAXEL; TUBULIN; TUBULIN MODULATORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 67649881371     PISSN: 09607722     EISSN: 13652184     Source Type: Journal    
DOI: 10.1111/j.1365-2184.2009.00607.x     Document Type: Article

References (46)

1. Arnal I, Wade RH (1995) How does taxol stabilize microtubules? Curr. Biol. 5, 900-908.
2. Mickey B, Howard J (1995) Rigidity of microtubules is increased by stabilizing agents. J. Cell Biol. 130, 909-917.
3. Rowinsky EK, Donehower RC (1995) Paclitaxel (taxol). N. Engl. J. Med. 332, 1004-1014.
4. 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.
5. Theodoropoulos PA, Polioudaki H, Kostaki O, Derdas SP, Georgoulias V, Dargemont C et al. (1999) Taxol affects nuclear lamina and pore complex organization and inhibits import of karyophilic proteins into the cell nucleus. Cancer Res. 59, 46254633.
6. Danesi R, Figg WD, Reed E, Myers CE (1995) Paclitaxel (taxol) inhibits protein isoprenylation and induces apoptosis in PC-3 human prostate cancer cells. Mol. Pharmacol. 47, 1106-1111.
7. Michalakis J, Georgatos SD, Romanos J, Koutala H, Georgoulias V, Tsiftsis D et al. (2005) Micromolar taxol, with or without hyperthermia, induces mitotic catastrophe and cell necrosis in HeLa cells. Cancer Chemother. Pharmacol. 56, 615-622.
8. Schiff PB, Horwitz SB (1980) Taxol stabilizes microtubules in mouse fibroblast cells. Proc. Natl. Acad. Sci. USA 77, 1561-1565.
9. Bogdan C, Ding A (1992) Taxol, a microtubule-stabilizing antineoplastic agent, induces expression of tumor necrosis factor alpha and interleukin-1 in macrophages. J. Leukoc Biol. 52, 119-121.
10. Ding AH, Porteu F, Sanchez E, Nathan CF (1990) Shared actions of endotoxin and taxol on TNF receptors and TNF release. Science 248, 370-372.
11. Lee LF, Schuerer-Maly CC, Lofquist AK, van Haaften-Day C, Ting JP, White CM et al. (1996) Taxol-dependent transcriptional activation of IL-8 expression in a subset of human ovarian cancer. Cancer Res. 56, 1303-1308.
12. Moos PJ, Fitzpatrick FA (1998) Taxane-mediated gene induction is independent of microtubule stabilization: induction of transcription regulators and enzymes that modulate inflammation and apoptosis. Proc. Natl. Acad. Sci. USA 95, 3896-3901.
13. Abal M, Souto AA, Amat-Guerri F, Acuna AU, Andreu JM, Barasoain I (2001) Centrosome and spindle pole microtubules are main targets of a fluorescent taxoid inducing cell death. Cell Motil. Cytoskeleton. 49, 1-15.
14. Pushkarev VM, Starenki DV, Saenko VA, Namba H, Kurebayashi J, Tronko MD et al. (2004) Molecular mechanisms of the effects of low concentrations of taxol in anaplastic thyroid cancer cells. Endocrinology 145,3143-3152.
15. Devine SM, Hoffman R (2000) Role of mesenchymal stem cells in hematopoietic stem cell transplantation. Curr. Opin. Hematol. 7, 358-363.
16. Majumdar MK, Thiede MA, Haynesworth SE, Bruder SP, Gerson SL (2000) Human marrow-derived mesenchymal stem cells (MSCs) express hematopoietic cytokines and support long-term hematopoiesis when differentiated toward stromal and osteogenic lineages. J. Hematother. Stem Cell Res. 9, 841-848.
17. Majumdar MK, Thiede MA, Mosca JD, Moorman M, Gerson SL (1998) Phenotypic and functional comparison of cultures of marrowderived mesenchymal stem cells (MSCs) and stromal cells. J. Cell. Physiol. 176, 57-66.
18. Bianco P, Riminucci M, Gronthos S, Robey PG (2001) Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19, 180-192.
19. Gronthos S, Graves SE, Simmons PJ (1998). Isolation, purification and in vitro manipulation of human bone marrow stromal precursor cells. In: Beresford JN, Owen ME, eds. Marrow Stromal Cell Culture, pp. 26-42. Cambridge, UK: Cambridge University Press.
20. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD et al. (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284, 143-147.
21. Colter DC, Class R, DiGirolamo CM, Prockop DJ (2000) Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow. Proc. Natl. Acad. Sci. USA 97, 3213-3218.
22. Domenech J, Gihana E, Dayan A, Truglio D, Linassier C, Desbois I et al. (1994) Haemopoiesis of transplanted patients with autologous marrows assessed by long-term marrow culture. Br. J. Haematol. 88,488-496.
23. Domenech J, Roingeard F, Herault O, Truglio D, Desbois I, Colombat P et al. (1998) Changes in the functional capacity of marrow stromal cells after autologous bone marrow transplantation. Leuk Lymphoma. 29, 533-546.
24. Galotto M, Berisso G, Delfino L, Podesta M, Ottaggio L, Dallorso S et al. (1999) Stromal damage as consequence of high-dose chemo/radiotherapy in bone marrow transplant recipients. Exp. Hematol. 27, 1460-1466.
25. Li J, Law HK, Lau YL, Chan GC (2004) Differential damage and recovery of human mesenchymal stem cells after exposure to chemotherapeutic agents. Br. J. Haematol. 127, 326-334.
26. Mueller LP, Luetzkendorf J, Mueller T, Reichelt K, Simon H, Schmoll HJ (2006) Presence of mesenchymal stem cells in human bone marrow after exposure to chemotherapy: evidence of resistance to apoptosis induction. Stem Cells 24, 2753-2765.
27. Kastrinaki MC, Sidiropoulos P, Roche S, Ringe J, Lehmann S, Kritikos H et al. (2008) Functional, molecular and proteomic characterisation of bone marrow mesenchymal stem cells in rheumatoid arthritis. Ann. Rheum. Dis. 67, 741-749.
28. Kourmouli N, Theodoropoulos PA, Dialynas G, Bakou A, Politou AS, Cowell IG et al. (2000) Dynamic associations of heterochromatin protein 1 with the nuclear envelope. EMBO J. 19, 6558-6568.
29. Bertani N, Malatesta P, Volpi G, Sonego P, Perris R (2005) Neurogenic potential of human mesenchymal stem cells revisited: analysis by immunostaining, time-lapse video and microarray. J. Cell Sci. 118, 3925-3936.
30. Kavallaris M, Kuo DY, Burkhart CA, Regl DL, Norris MD, Haber M et al. (1997) Taxol-resistant epithelial ovarian tumors are associated with altered expression of specific β-tubulin isotypes. J. Clin. Invest. 100, 1282-1293.
31. Jamis-Dow CA, Klecker RW, Sarosy G, Reed E, Collins JM (1993) Steady-state plasma concentrations and effects of taxol for a 250 mg/m2 dose in combination with granulocyte-colony stimulating factor in patients with ovarian cancer. Cancer Chemother. Pharmacol. 33, 48-52.
32. Kobayashi M, Oba K, Sakamoto J, Kondo K, Nagata N, Okabayashi T et al. (2007) Pharmacokinetic study of weekly administration dose of paclitaxel in patients with advanced or recurrent gastric cancer in Japan. Gastric Cancer 10, 52-57.
33. Papas S, Akoumianaki T, Kalogiros C, Hadjiarapoglou L, Theodoropoulos PA, Tsikaris V (2007) Synthesis and antitumor activity of peptide-paclitaxel conjugates. J. Pept. Sci. 13, 662-671.
34. Teraishi F, Wu S, Sasaki J, Zhang L, Zhu HB, Davis JJ et al. (2005) P-glycoprotein-independent apoptosis induction by a novel synthetic compound, MMPT [5-[(4-Methylphenyl) methylene]-2-(phenylamino)-4 (5H)-thiazolone]. J. Pharmacol. Exp. Ther. 314, 355-362.
35. Michalakis J, Georgatos SD, de Bree E, Polioudaki H, Romanos J, Georgoulias V et al. (2007) Short-term exposure of cancer cells to micromolar doses of paclitaxel, with or without hyperthermia, induces long-term inhibition of cell proliferation and cell death in vitro. Ann. Surg. Oncol. 14, 1220-1228.
36. Giannakakou P, Robey R, Fojo T, Blagosklonny MV (2001) Low concentrations of paclitaxel induce cell type-dependent p53, 21 and G1/G2 arrest instead of mitotic arrest: molecular determinants of paclitaxel-induced cytotoxicity. Oncogene 20, 3806-3813.
37. Carvajal D, Tovar C, Yang H, Vu BT, Heimbrook DC, Vassilev LT (2005) Activation of p53 by MDM2 antagonists can protect proliferating cells from mitotic inhibitors. Cancer Res. 65, 1918-1924.
38. Park JS, Kim HY, Kim HW, Chae GN, Oh HT, Park JY et al. (2005) Increased caveolin-1, a cause for the declined adipogenic potential of senescent human mesenchymal stem cells. Meck Ageing. Dev. 126, 551-559.
39. Ciciarello M, Mangiacasale R, Casenghi M, Zaira Limongi M, D'Angelo M, Soddu S et al. (2001) p53 displacement from centrosomes and p53-mediated Gl arrest following transient inhibition of the mitotic spindle. J. Biol. Chem. 276, 19205-19213.
40. Moro F, Ottaggio L, Bonatti S, Simili M, Miele M, Bozzo S et al. (1995) p53 expression in normal versus transformed mammalian cells. Carcinogenesis 16, 2435-2440.
41. O'Brate A, Giannakakou P (2003) The importance of p53 location: nuclear or cytoplasmic zip code? Drug Resist. Updat. 6, 313-322.
42. Ben-Ze'ev A, Farmer SR, Penman S (1979) Mechanisms of regulating tubulin synthesis in cultured mammalian cells. Cell 17, 319-325.
43. Cleveland DW, Lopata MA, Sherline P, Kirschner MW (1981) Unpolymerized tubulin modulates the level of tubulin mRNAs. Cell 25, 537-546.
44. Gong ZY, Brandhorst B (1988) Autogenous regulation of tubulin synthesis via RNA stability during sea urchin embryogenesis. Development 102, 31-43.
45. Stargell LA, Heruth DP, Gaertig J, Gorovsky MA (1992) Drugs affecting microtubule dynamics increase α -tubulin mRNA accumulation via transcription in Tetrahymena thermophila. Mol. Cell. Biol. 12, 1443-1450.
46. Burkhart CA, Kavallaris M, Band Horwitz S (2001) The role of β-tubulin isotypes in resistance to antimitotic drugs. Biochim. Biophys. Acta 1471, 01-09.