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[Cancer Research 57, 229-233, January 15, 1997]
© 1997 American Association for Cancer Research
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Bcl2 Is the Guardian of Microtubule Integrity1

Subrata Haldar2, Aruna Basu and Carlo M. Croce

Kimmel Cancer Center, Jefferson Medical College, Philadelphia, Pennsylvania 19107

We have investigated the ability of several drugs commonly used in the treatment of human cancer to induce bcl2 phosphorylation and cell death in human cell lines derived from acute leukemia, lymphoma, breast cancer, and prostate cancer. The results of this analysis indicate that drugs affecting the integrity of microtubules induce bcl2 phosphorylation, whereas anticancer drugs damaging DNA do not. Comparison of the effects of taxol and its analogue, taxotere, indicates that taxotere is capable of inducing bcl2 phosphorylation and apoptotic cell death at 100-fold lower concentrations than taxol. Induction of cancer cell death through phosphorylation of bcl2 thus provides an opportunity not only for more refined targeting of therapeutic drugs but for understanding of an important pathway leading to apoptosis.

Phosphorylation of bcl2 in drug-treated cancer cells occurs in G2-M, the phase of the cell cycle in which this class of drugs is active. No induction of bcl2 phosphorylation occurs in chronic lymphocytic leukemia cells that overexpress bcl2 but are blocked at G0-G1. Thus, prevention of polymerization or depolymerization of cellular microtubules by this class of cancer therapeutic drugs causes phosphorylation of bcl2, abrogating the normal antiapoptotic function of bcl2 and initiating the apoptotic program in the cycling cancer cells; these results are consistent with a normal physiological role of bcl2 as "guardian of microtubule integrity."

1 Supported by the Council for Tobacco Research Grant 3496A (to S. H.) and National Cancer Institute Grant CA39860 (to C. M. C.).

2 To whom requests for reprints should be addressed, at Kimmel Cancer Center, Bluemle Life Sciences Building, Rm. 1032, 233 South 10th Street, Philadelphia, PA 19107-5799.

Received 12/ 2/96. Accepted 12/23/96.




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[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
B. Kurdoglu, N. Cheong, J. Guan, B. W. Corn, W. J. Curran Jr., and G. Iliakis
Apoptosis as a Predictor of Paclitaxel-induced Radiosensitization in Human Tumor Cell Lines
Clin. Cancer Res., September 1, 1999; 5(9): 2580 - 2587.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
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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 JEMHome page
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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 JCOHome page
R. S. DiPaola, M. M. Rafi, V. Vyas, D. Toppmeyer, E. Rubin, J. Patel, S. Goodin, M. Medina, P. Medina, R. Zamek, et al.
Phase I Clinical and Pharmacologic Study of 13-cis-Retinoic Acid, Interferon Alfa, and Paclitaxel in Patients With Prostate Cancer and Other Advanced Malignancies
J. Clin. Oncol., July 1, 1999; 17(7): 2213 - 2213.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Gibson, C. Widmann, and G. L. Johnson
Differential Involvement of MEK Kinase 1 (MEKK1) in the Induction of Apoptosis in Response to Microtubule-targeted Drugs versus DNA Damaging Agents
J. Biol. Chem., April 16, 1999; 274(16): 10916 - 10922.
[Abstract] [Full Text] [PDF]

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 Neuro Oncol DukeHome page
S. H. Tseng, M. S. Bobola, M. S. Berger, and J. R. Silber
Characterization of paclitaxel (Taxol(R)) sensitivity in human glioma- and medulloblastoma-derived cell lines
Neuro-oncol, April 1, 1999; 1(2): 101 - 108.
[Abstract] [PDF]

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 Mol. Biol. CellHome page
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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 Proc. Natl. Acad. Sci. USAHome page
R. K. Srivastava, Q.-S. Mi, J. M. Hardwick, and D. L. Longo
Deletion of the loop region of Bcl-2 completely blocks paclitaxel-induced apoptosis
PNAS, March 30, 1999; 96(7): 3775 - 3780.
[Abstract] [Full Text] [PDF]

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 JCOHome page
D. P. Petrylak, R. B. Macarthur, J. O'Connor, G. Shelton, T. Judge, J. Balog, C. Pfaff, E. Bagiella, D. Heitjan, R. Fine, et al.
Phase I Trial of Docetaxel With Estramustine in Androgen-Independent Prostate Cancer
J. Clin. Oncol., March 1, 1999; 17(3): 958 - 958.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
S. K. Manna and B. B. Aggarwal
Lipopolysaccharide Inhibits TNF-Induced Apoptosis: Role of Nuclear Factor-{kappa}B Activation and Reactive Oxygen Intermediates
J. Immunol., February 1, 1999; 162(3): 1510 - 1518.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
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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 BloodHome page
Z.-B. Hu, M.D. Minden, and E.A. McCulloch
Phosphorylation of BCL-2 After Exposure of Human Leukemic Cells to Retinoic Acid
Blood, September 1, 1998; 92(5): 1768 - 1775.
[Abstract] [Full Text] [PDF]

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 ScienceHome page
J. M. Adams and S. Cory
The Bcl-2 Protein Family: Arbiters of Cell Survival
Science, August 28, 1998; 281(5381): 1322 - 1326.
[Abstract] [Full Text]

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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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 Physiol. Rev.Home page
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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 Mol. Cell. Biol.Home page
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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 Proc. Natl. Acad. Sci. USAHome page
P. J. Moos and F. A. Fitzpatrick
Taxane-mediated gene induction is independent of microtubule stabilization: Induction of transcription regulators and enzymes that modulate inflammation and apoptosis
PNAS, March 31, 1998; 95(7): 3896 - 3901.
[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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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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 J. Biol. Chem.Home page
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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 J. Biol. Chem.Home page
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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