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Howard Hughes Medical Institute and Cancer Center, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104 [M. V. B., W. S. E-D.], Medicine Branch; NIH National Cancer Institute, Bethesda, Maryland 20892 [P. G., T. F.]; Department of Chemistry, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061 [D. G. I. K., P. I. H.]; and Clinical Pharmacology Branch, NIH, National Cancer Institute, Bethesda, Maryland 20892 [L. N.]
Recent studies have shown that paclitaxel leads to activation of Raf-1 kinase and have suggested that this activation is essential for bcl-2 phosphorylation and apoptosis. In the present study, we demonstrate that, in addition to paclitaxel, other agents that interact with tubulin and microtubules also induce Raf-1/bcl-2 phosphorylation, whereas DNA-damaging drugs, antimetabolites, and alkylating agents do not. Activation of Raf-1 kinase by paclitaxel is linked to tubulin polymerization; the effect is blunted in paclitaxel-resistant cells, the tubulin of which does not polymerize following the addition of paclitaxel. In contrast, vincristine and vinblastine, drugs to which the paclitaxel-resistant cells retain sensitivity were able to bring about Raf-1 phosphorylation. The requirement for disruption of microtubules in this signaling cascade was strengthened further using paclitaxel analogues by demonstrating a correlation between tubulin polymerization, Raf-1/bcl-2 phosphorylation, and cytotoxicity. Inhibition of RNA or protein synthesis prevents Raf-1 activation and bcl-2 phosphorylation, suggesting that an intermediate protein(s) acts upstream of Raf-1 in this microtubule damage-activating pathway. A model is proposed that envisions a pathway of Raf-1 activation and bcl-2 phosphorylation following disruption of microtubular architecture, serving a role similar to p53 induction following DNA damage.
1 To whom requests for reprints should be addressed, at Medicine Branch, NIH, National Cancer Institute, Building 10, Room 12N226, 9000 Rockville Pike, Bethesda, MD 20892.
Received 9/26/96. Accepted 10/30/96.
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Z. A. Stewart, D. Mays, and J. A. Pietenpol Defective G1-S Cell Cycle Checkpoint Function Sensitizes Cells to Microtubule Inhibitor-induced Apoptosis Cancer Res., August 1, 1999; 59(15): 3831 - 3837. [Abstract] [Full Text] [PDF]
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 R. K. Srivastava, C. Y. Sasaki, J. M. Hardwick, and D. L. Longo Bcl-2-Mediated Drug Resistance: Inhibition of Apoptosis by Blocking Nuclear Factor of Activated T Lymphocytes (Nfat)-Induced FAS Ligand Transcription J. Exp. Med., July 19, 1999; 190(2): 253 - 266. [Abstract] [Full Text] [PDF]
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T. J. Kottke, A. L. Blajeski, L. M. Martins, P. W. Mesner Jr., N. E. Davidson, W. C. Earnshaw, D. K. Armstrong, and S. H. Kaufmann Comparison of Paclitaxel-, 5-Fluoro-2'-deoxyuridine-, and Epidermal Growth Factor (EGF)-induced Apoptosis. EVIDENCE FOR EGF-INDUCED ANOIKIS J. Biol. Chem., May 28, 1999; 274(22): 15927 - 15936. [Abstract] [Full Text] [PDF]
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G. Tortora, R. Caputo, G. Pomatico, S. Pepe, A. R. Bianco, S. Agrawal, J. Mendelsohn, and F. Ciardiello Cooperative Inhibitory Effect of Novel Mixed Backbone Oligonucleotide Targeting Protein Kinase A in Combination with Docetaxel and Anti-Epidermal Growth Factor-Receptor Antibody on Human Breast Cancer Cell Growth Clin. Cancer Res., April 1, 1999; 5(4): 875 - 881. [Abstract] [Full Text] [PDF]
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 A.-M. C. Yvon, P. Wadsworth, and M. A. Jordan Taxol Suppresses Dynamics of Individual Microtubules in Living Human Tumor Cells Mol. Biol. Cell, April 1, 1999; 10(4): 947 - 959. [Abstract] [Full Text]
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T.-H. Wang, D. M. Popp, H.-S. Wang, M. Saitoh, J. G. Mural, D. C. Henley, H. Ichijo, and J. Wimalasena 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., March 19, 1999; 274(12): 8208 - 8216. [Abstract] [Full Text] [PDF]
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P. B. Poommipanit, B. Chen, and Z. N. Oltvai Interleukin-3 Induces the Phosphorylation of a Distinct Fraction of Bcl-2 J. Biol. Chem., January 8, 1999; 274(2): 1033 - 1039. [Abstract] [Full Text] [PDF]
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S. Sanders and S. S. Thorgeirsson Phenobarbital promotes liver growth in c-myc/TGF-{alpha} transgenic mice by inducing hypertrophy and inhibiting apoptosis Carcinogenesis, January 1, 1999; 20(1): 41 - 49. [Abstract] [Full Text] [PDF]
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H. M. McDaid and P. G. Johnston Synergistic Interaction between Paclitaxel and 8-Chloro-adenosine 3',5'-Monophosphate in Human Ovarian Carcinoma Cell Lines Clin. Cancer Res., January 1, 1999; 5(1): 215 - 220. [Abstract] [Full Text] [PDF]
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E. L. K. Goh, T. J. Pircher, and P. E. Lobie Growth Hormone Promotion of Tubulin Polymerization Stabilizes the Microtubule Network and Protects Against Colchicine-Induced Apoptosis Endocrinology, October 1, 1998; 139(10): 4364 - 4372. [Abstract] [Full Text] [PDF]
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Y.-H. Ling, C. Tornos, and R. Perez-Soler Phosphorylation of Bcl-2 Is a Marker of M Phase Events and Not a Determinant of Apoptosis J. Biol. Chem., July 24, 1998; 273(30): 18984 - 18991. [Abstract] [Full Text] [PDF]
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 P. A. JANMEY The Cytoskeleton and Cell Signaling: Component Localization and Mechanical Coupling Physiol Rev, July 1, 1998; 78(3): 763 - 781. [Abstract] [Full Text] [PDF]
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R. K. Srivastava, A. R. Srivastava, S. J. Korsmeyer, M. Nesterova, Y. S. Cho-Chung, and D. L. Longo Involvement of Microtubules in the Regulation of Bcl2 Phosphorylation and Apoptosis through Cyclic AMP-Dependent Protein Kinase Mol. Cell. Biol., June 1, 1998; 18(6): 3509 - 3517. [Abstract] [Full Text]
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 G. P. Amarante-Mendes, C. Naekyung Kim, L. Liu, Y. Huang, C. L. Perkins, D. R. Green, and K. Bhalla Bcr-Abl Exerts Its Antiapoptotic Effect Against Diverse Apoptotic Stimuli Through Blockage of Mitochondrial Release of Cytochrome C and Activation of Caspase-3 Blood, March 1, 1998; 91(5): 1700 - 1705. [Abstract] [Full Text] [PDF]
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T.-H. Wang, H.-S. Wang, H. Ichijo, P. Giannakakou, J. S. Foster, T. Fojo, and J. Wimalasena 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., February 27, 1998; 273(9): 4928 - 4936. [Abstract] [Full Text] [PDF]
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S. Wang, J. A. Vrana, T. M. Bartimole, A. J. Freemerman, W. D. Jarvis, L. B. Kramer, G. Krystal, P. Dent, and S. Grant Agents that Down-Regulate or Inhibit Protein Kinase C Circumvent Resistance to 1-beta -D-Arabinofuranosylcytosine-Induced Apoptosis in Human Leukemia Cells that Overexpress Bcl-2 Mol. Pharmacol., December 1, 1997; 52(6): 1000 - 1009. [Abstract] [Full Text]
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J. P. MacKeigan, T. S. Collins, and J. P.-Y. Ting MEK Inhibition Enhances Paclitaxel-induced Tumor Apoptosis J. Biol. Chem., December 8, 2000; 275(50): 38953 - 38956. [Abstract] [Full Text] [PDF]
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A. M. Domina, J. H. Smith, and R. W. Craig Myeloid Cell Leukemia 1 Is Phosphorylated through Two Distinct Pathways, One Associated with Extracellular Signal-regulated Kinase Activation and the Other with G2/M Accumulation or Protein Phosphatase 1/2A Inhibition J. Biol. Chem., July 7, 2000; 275(28): 21688 - 21694. [Abstract] [Full Text] [PDF]
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M. Fan, M. Goodwin, T. Vu, C. Brantley-Finley, W. A. Gaarde, and T. C. Chambers Vinblastine-induced Phosphorylation of Bcl-2 and Bcl-XL Is Mediated by JNK and Occurs in Parallel with Inactivation of the Raf-1/MEK/ERK Cascade J. Biol. Chem., September 22, 2000; 275(39): 29980 - 29985. [Abstract] [Full Text] [PDF]
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Y. Furukawa, S. Iwase, J. Kikuchi, Y. Terui, M. Nakamura, H. Yamada, Y. Kano, and M. Matsuda Phosphorylation of Bcl-2 Protein by CDC2 Kinase during G2/M Phases and Its Role in Cell Cycle Regulation J. Biol. Chem., July 7, 2000; 275(28): 21661 - 21667. [Abstract] [Full Text] [PDF]
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A. J. Butt, S. M. Firth, M. A. King, and R. C. Baxter Insulin-like Growth Factor-binding Protein-3 Modulates Expression of Bax and Bcl-2 and Potentiates p53-independent Radiation-induced Apoptosis in Human Breast Cancer Cells J. Biol. Chem., December 8, 2000; 275(50): 39174 - 39181. [Abstract] [Full Text] [PDF]
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