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[Cancer Research 61, 3071-3076, April 1, 2001]
© 2001 American Association for Cancer Research

Experimental Therapeutics

The Proteasome Inhibitor PS-341 Inhibits Growth, Induces Apoptosis, and Overcomes Drug Resistance in Human Multiple Myeloma Cells1

Teru Hideshima, Paul Richardson, Dharminder Chauhan, Vito J. Palombella, Peter J. Elliott, Julian Adams and Kenneth C. Anderson2

Department of Adult Oncology, Dana-Farber Cancer Institute, and Department of Medicine, Harvard Medical School, Boston, Massachusetts 02115 [T. H., P. R., D. C., K. C. A]; and Millennium Pharmaceuticals, Inc. Cambridge, Massachusetts 02139 [V. J. P., P. J. E., J. A.]

Human multiple myeloma (MM) is a presently incurable hematological malignancy, and novel biologically based therapies are urgently needed. Proteasome inhibitors represent a novel potential anticancer therapy. In this study, we demonstrate that the proteasome inhibitor PS-341 directly inhibits proliferation and induces apoptosis of human MM cell lines and freshly isolated patient MM cells; inhibits mitogen-activated protein kinase growth signaling in MM cells; induces apoptosis despite induction of p21 and p27 in both p53 wild-type and p53 mutant MM cells; overcomes drug resistance; adds to the anti-MM activity of dexamethasone; and overcomes the resistance to apoptosis in MM cells conferred by interleukin-6. PS-341 also inhibits the paracrine growth of human MM cells by decreasing their adherence to bone marrow stromal cells (BMSCs) and related nuclear factor {kappa}B-dependent induction of interleukin-6 secretion in BMSCs, as well as inhibiting proliferation and growth signaling of residual adherent MM cells. These data, therefore, demonstrate that PS-341 both acts directly on MM cells and alters cellular interactions and cytokine secretion in the BM millieu to inhibit tumor cell growth, induce apoptosis, and overcome drug resistance. Given the acceptable animal and human toxicity profile of PS-341, these studies provide the framework for clinical evaluation of PS-341 to improve outcome for patients with this universally fatal hematological malignancy.




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Phase II Pethema Trial of Alternating Bortezomib and Dexamethasone As Induction Regimen Before Autologous Stem-Cell Transplantation in Younger Patients With Multiple Myeloma: Efficacy and Clinical Implications of Tumor Response Kinetics
J. Clin. Oncol., October 1, 2007; 25(28): 4452 - 4458.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
P. Neri, S. Kumar, M. T. Fulciniti, S. Vallet, S. Chhetri, S. Mukherjee, Y. Tai, D. Chauhan, P. Tassone, S. Venuta, et al.
Neutralizing B-Cell Activating Factor Antibody Improves Survival and Inhibits Osteoclastogenesis in a Severe Combined Immunodeficient Human Multiple Myeloma Model
Clin. Cancer Res., October 1, 2007; 13(19): 5903 - 5909.
[Abstract] [Full Text] [PDF]

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 BloodHome page
E. L. Davenport, H. E. Moore, A. S. Dunlop, S. Y. Sharp, P. Workman, G. J. Morgan, and F. E. Davies
Heat shock protein inhibition is associated with activation of the unfolded protein response pathway in myeloma plasma cells
Blood, October 1, 2007; 110(7): 2641 - 2649.
[Abstract] [Full Text] [PDF]

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 J. Virol.Home page
P. Zou, J. Kawada, L. Pesnicak, and J. I. Cohen
Bortezomib Induces Apoptosis of Epstein-Barr Virus (EBV)-Transformed B Cells and Prolongs Survival of Mice Inoculated with EBV-Transformed B Cells
J. Virol., September 15, 2007; 81(18): 10029 - 10036.
[Abstract] [Full Text] [PDF]

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 JCOHome page
R. Z. Orlowski, A. Nagler, P. Sonneveld, J. Blade, R. Hajek, A. Spencer, J. San Miguel, T. Robak, A. Dmoszynska, N. Horvath, et al.
Randomized Phase III Study of Pegylated Liposomal Doxorubicin Plus Bortezomib Compared With Bortezomib Alone in Relapsed or Refractory Multiple Myeloma: Combination Therapy Improves Time to Progression
J. Clin. Oncol., September 1, 2007; 25(25): 3892 - 3901.
[Abstract] [Full Text] [PDF]

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 BloodHome page
Y.-T. Tai, M. Fulciniti, T. Hideshima, W. Song, M. Leiba, X.-F. Li, M. Rumizen, P. Burger, A. Morrison, K. Podar, et al.
Targeting MEK induces myeloma-cell cytotoxicity and inhibits osteoclastogenesis
Blood, September 1, 2007; 110(5): 1656 - 1663.
[Abstract] [Full Text] [PDF]

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 haematolHome page
F. E. Davies, P. Wu, M. Jenner, M. Srikanth, R. Saso, and G. J. Morgan
The combination of cyclophosphamide, velcade and dexamethasone (CVD) induces high response rates with comparable toxicity to velcade alone (V) and velcade plus dexamethasone (VD)
Haematologica, August 1, 2007; 92(8): 1149 - 1150.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
R. Manochakian, K. C. Miller, and A. A. Chanan-Khan
Clinical Impact of Bortezomib in Frontline Regimens for Patients with Multiple Myeloma
Oncologist, August 1, 2007; 12(8): 978 - 990.
[Abstract] [Full Text] [PDF]

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 BloodHome page
T. Kiziltepe, T. Hideshima, K. Ishitsuka, E. M. Ocio, N. Raje, L. Catley, C.-Q. Li, L. J. Trudel, H. Yasui, S. Vallet, et al.
JS-K, a GST-activated nitric oxide generator, induces DNA double-strand breaks, activates DNA damage response pathways, and induces apoptosis in vitro and in vivo in human multiple myeloma cells
Blood, July 15, 2007; 110(2): 709 - 718.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. D. Demo, C. J. Kirk, M. A. Aujay, T. J. Buchholz, M. Dajee, M. N. Ho, J. Jiang, G. J. Laidig, E. R. Lewis, F. Parlati, et al.
Antitumor Activity of PR-171, a Novel Irreversible Inhibitor of the Proteasome
Cancer Res., July 1, 2007; 67(13): 6383 - 6391.
[Abstract] [Full Text] [PDF]

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 BloodHome page
N. Giuliani, F. Morandi, S. Tagliaferri, M. Lazzaretti, S. Bonomini, M. Crugnola, C. Mancini, E. Martella, L. Ferrari, A. Tabilio, et al.
The proteasome inhibitor bortezomib affects osteoblast differentiation in vitro and in vivo in multiple myeloma patients
Blood, July 1, 2007; 110(1): 334 - 338.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
T. Kiziltepe, T. Hideshima, L. Catley, N. Raje, H. Yasui, N. Shiraishi, Y. Okawa, H. Ikeda, S. Vallet, S. Pozzi, et al.
5-Azacytidine, a DNA methyltransferase inhibitor, induces ATR-mediated DNA double-strand break responses, apoptosis, and synergistic cytotoxicity with doxorubicin and bortezomib against multiple myeloma cells
Mol. Cancer Ther., June 1, 2007; 6(6): 1718 - 1727.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
P. G. Richardson, C. Mitsiades, R. Schlossman, N. Munshi, and K. Anderson
New Drugs for Myeloma
Oncologist, June 1, 2007; 12(6): 664 - 689.
[Abstract] [Full Text] [PDF]

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 BloodHome page
R. Spisek, A. Charalambous, A. Mazumder, D. H. Vesole, S. Jagannath, and M. V. Dhodapkar
Bortezomib enhances dendritic cell (DC) mediated induction of immunity to human myeloma via exposure of cell surface heat shock protein 90 on dying tumor cells: therapeutic implications
Blood, June 1, 2007; 109(11): 4839 - 4845.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
K. Sukhdeo, M. Mani, Y. Zhang, J. Dutta, H. Yasui, M. D. Rooney, D. E. Carrasco, M. Zheng, H. He, Y.-T. Tai, et al.
Targeting the beta-catenin/TCF transcriptional complex in the treatment of multiple myeloma
PNAS, May 1, 2007; 104(18): 7516 - 7521.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. J. Strauss, K. Higginbottom, S. Juliger, L. Maharaj, P. Allen, D. Schenkein, T. A. Lister, and S. P. Joel
The Proteasome Inhibitor Bortezomib Acts Independently of p53 and Induces Cell Death via Apoptosis and Mitotic Catastrophe in B-Cell Lymphoma Cell Lines
Cancer Res., March 15, 2007; 67(6): 2783 - 2790.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
J. R. Berenson, J. Matous, R. A. Swift, R. Mapes, B. Morrison, and H. S. Yeh
A Phase I/II Study of Arsenic Trioxide/Bortezomib/Ascorbic Acid Combination Therapy for the Treatment of Relapsed or Refractory Multiple Myeloma
Clin. Cancer Res., March 15, 2007; 13(6): 1762 - 1768.
[Abstract] [Full Text] [PDF]

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 BloodHome page
L. Veschini, D. Belloni, C. Foglieni, M. G. Cangi, M. Ferrarini, F. Caligaris-Cappio, and E. Ferrero
Hypoxia-inducible transcription factor-1 alpha determines sensitivity of endothelial cells to the proteosome inhibitor bortezomib
Blood, March 15, 2007; 109(6): 2565 - 2570.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
J. Voortman, A. Checinska, G. Giaccone, J. A. Rodriguez, and F. A.E. Kruyt
Bortezomib, but not cisplatin, induces mitochondria-dependent apoptosis accompanied by up-regulation of noxa in the non-small cell lung cancer cell line NCI-H460
Mol. Cancer Ther., March 1, 2007; 6(3): 1046 - 1053.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
T. M. Horton, D. Pati, S. E. Plon, P. A. Thompson, L. R. Bomgaars, P. C. Adamson, A. M. Ingle, J. Wright, A. H. Brockman, M. Paton, et al.
A Phase 1 Study of the Proteasome Inhibitor Bortezomib in Pediatric Patients with Refractory Leukemia: a Children's Oncology Group Study
Clin. Cancer Res., March 1, 2007; 13(5): 1516 - 1522.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
J.-P. Armand, A. K. Burnett, J. Drach, J.-L. Harousseau, B. Lowenberg, and J. San Miguel
The Emerging Role of Targeted Therapy for Hematologic Malignancies: Update on Bortezomib and Tipifarnib
Oncologist, March 1, 2007; 12(3): 281 - 290.
[Abstract] [Full Text] [PDF]

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 BloodHome page
C. Jakob, K. Egerer, P. Liebisch, S. Turkmen, I. Zavrski, U. Kuckelkorn, U. Heider, M. Kaiser, C. Fleissner, J. Sterz, et al.
Circulating proteasome levels are an independent prognostic factor for survival in multiple myeloma
Blood, March 1, 2007; 109(5): 2100 - 2105.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. Meister, U. Schubert, K. Neubert, K. Herrmann, R. Burger, M. Gramatzki, S. Hahn, S. Schreiber, S. Wilhelm, M. Herrmann, et al.
Extensive Immunoglobulin Production Sensitizes Myeloma Cells for Proteasome Inhibition
Cancer Res., February 15, 2007; 67(4): 1783 - 1792.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
S. Trudel, A. K. Stewart, Z. Li, Y. Shu, S.-B. Liang, Y. Trieu, D. Reece, J. Paterson, D. Wang, and X.-Y. Wen
The Bcl-2 Family Protein Inhibitor, ABT-737, Has Substantial Antimyeloma Activity and Shows Synergistic Effect with Dexamethasone and Melphalan
Clin. Cancer Res., January 15, 2007; 13(2): 621 - 629.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
J. An and M. B. Rettig
Epidermal growth factor receptor inhibition sensitizes renal cell carcinoma cells to the cytotoxic effects of bortezomib
Mol. Cancer Ther., January 1, 2007; 6(1): 61 - 69.
[Abstract] [Full Text] [PDF]

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 J. Am. Soc. Nephrol.Home page
W.-Z. Ying, H.-G. Zhang, and P. W. Sanders
EGF Receptor Activity Modulates Apoptosis Induced by Inhibition of the Proteasome of Vascular Smooth Muscle Cells
J. Am. Soc. Nephrol., January 1, 2007; 18(1): 131 - 142.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
K. Podar, G. Tonon, M. Sattler, Y.-T. Tai, S. LeGouill, H. Yasui, K. Ishitsuka, S. Kumar, R. Kumar, L. N. Pandite, et al.
The small-molecule VEGF receptor inhibitor pazopanib (GW786034B) targets both tumor and endothelial cells in multiple myeloma
PNAS, December 19, 2006; 103(51): 19478 - 19483.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
M. J. Williamson, J. L. Blank, F. J. Bruzzese, Y. Cao, J. S. Daniels, L. R. Dick, J. Labutti, A. M. Mazzola, A. D. Patil, C. L. Reimer, et al.
Comparison of biochemical and biological effects of ML858 (salinosporamide A) and bortezomib
Mol. Cancer Ther., December 1, 2006; 5(12): 3052 - 3061.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. M. Fribley, B. Evenchik, Q. Zeng, B. K. Park, J. Y. Guan, H. Zhang, T. J. Hale, M. S. Soengas, R. J. Kaufman, and C.-Y. Wang
Proteasome Inhibitor PS-341 Induces Apoptosis in Cisplatin-resistant Squamous Cell Carcinoma Cells by Induction of Noxa
J. Biol. Chem., October 20, 2006; 281(42): 31440 - 31447.
[Abstract] [Full Text] [PDF]

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 Physiol. Rev.Home page
S. J. Marciniak and D. Ron
Endoplasmic reticulum stress signaling in disease.
Physiol Rev, October 1, 2006; 86(4): 1133 - 1149.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
T. Hideshima, P. Neri, P. Tassone, H. Yasui, K. Ishitsuka, N. Raje, D. Chauhan, K. Podar, C. Mitsiades, L. Dang, et al.
MLN120B, a Novel I{kappa}B Kinase {beta} Inhibitor, Blocks Multiple Myeloma Cell Growth In vitro and In vivo.
Clin. Cancer Res., October 1, 2006; 12(19): 5887 - 5894.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
M. Li, S. Cortez, T. Nakamachi, V. Batuman, and A. Arimura
Pituitary Adenylate Cyclase-Activating Polypeptide Is a Potent Inhibitor of the Growth of Light Chain-Secreting Human Multiple Myeloma Cells.
Cancer Res., September 1, 2006; 66(17): 8796 - 8803.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
C. Yu, B. B. Friday, J.-P. Lai, L. Yang, J. Sarkaria, N. E. Kay, C. A. Carter, L. R. Roberts, S. H. Kaufmann, and A. A. Adjei
Cytotoxic synergy between the multikinase inhibitor sorafenib and the proteasome inhibitor bortezomib in vitro: induction of apoptosis through Akt and c-Jun NH2-terminal kinase pathways.
Mol. Cancer Ther., September 1, 2006; 5(9): 2378 - 2387.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
X. Dolcet, D. Llobet, M. Encinas, J. Pallares, A. Cabero, J. A. Schoenenberger, J. X. Comella, and X. Matias-Guiu
Proteasome Inhibitors Induce Death but Activate NF-{kappa}B on Endometrial Carcinoma Cell Lines and Primary Culture Explants
J. Biol. Chem., August 4, 2006; 281(31): 22118 - 22130.
[Abstract] [Full Text] [PDF]

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 J. Leukoc. Biol.Home page
M. Leiba, L. Cahalon, A. Shimoni, O. Lider, A. Zanin-Zhorov, I. Hecht, U. Sela, I. Vlodavsky, and A. Nagler
Halofuginone inhibits NF-{kappa}B and p38 MAPK in activated T cells
J. Leukoc. Biol., August 1, 2006; 80(2): 399 - 406.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
G. Achanta, A. Modzelewska, L. Feng, S. R. Khan, and P. Huang
A Boronic-Chalcone Derivative Exhibits Potent Anticancer Activity through Inhibition of the Proteasome
Mol. Pharmacol., July 1, 2006; 70(1): 426 - 433.
[Abstract] [Full Text] [PDF]

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 BloodHome page
E. A. Obeng, L. M. Carlson, D. M. Gutman, W. J. Harrington Jr, K. P. Lee, and L. H. Boise
Proteasome inhibitors induce a terminal unfolded protein response in multiple myeloma cells
Blood, June 15, 2006; 107(12): 4907 - 4916.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
P. Maiso, X. Carvajal-Vergara, E. M. Ocio, R. Lopez-Perez, G. Mateo, N. Gutierrez, P. Atadja, A. Pandiella, and J. F. San Miguel
The Histone Deacetylase Inhibitor LBH589 Is a Potent Antimyeloma Agent that Overcomes Drug Resistance
Cancer Res., June 1, 2006; 66(11): 5781 - 5789.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
T. Khan, J. K. Stauffer, R. Williams, J. A. Hixon, R. Salcedo, E. Lincoln, T. C. Back, D. Powell, S. Lockett, A. C. Arnold, et al.
Proteasome Inhibition to Maximize the Apoptotic Potential of Cytokine Therapy for Murine Neuroblastoma Tumors
J. Immunol., May 15, 2006; 176(10): 6302 - 6312.
[Abstract] [Full Text] [PDF]

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 BloodHome page
T. Hideshima, L. Catley, H. Yasui, K. Ishitsuka, N. Raje, C. Mitsiades, K. Podar, N. C. Munshi, D. Chauhan, P. G. Richardson, et al.
Perifosine, an oral bioactive novel alkylphospholipid, inhibits Akt and induces in vitro and in vivo cytotoxicity in human multiple myeloma cells
Blood, May 15, 2006; 107(10): 4053 - 4062.
[Abstract] [Full Text] [PDF]


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