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[Cancer Research 60, 1878-1886, April 1, 2000]
© 2000 American Association for Cancer Research

Experimental Therapeutics

Antiangiogenic Scheduling of Chemotherapy Improves Efficacy against Experimental Drug-resistant Cancer1

Timothy Browder, Catherine E. Butterfield, Birgit M. Kräling, Bin Shi, Blair Marshall, Michael S. O’Reilly and Judah Folkman2

Laboratory of Surgical Research [T. B., C. E. B., B. M. K., B. S., B. M., M. S. O., J. F.] and Division of Hematology/Oncology [T. B.], Children’s Hospital; Departments of Surgery and Cell Biology, Harvard Medical School [J. F.]; Department of Pediatric Oncology, Dana-Farber Cancer Institute [T. B.]; and the Joint Center for Radiation Therapy [M. S. O.], Boston, Massachusetts 02115

To reveal the antiangiogenic capability of cancer chemotherapy, we developed an alternative antiangiogenic schedule for administration of cyclophosphamide. We show here that this antiangiogenic schedule avoided drug resistance and eradicated Lewis lung carcinoma and L1210 leukemia, an outcome not possible with the conventional schedule. When Lewis lung carcinoma and EMT-6 breast cancer were made drug resistant before therapy, the antiangiogenic schedule suppressed tumor growth 3-fold more effectively than the conventional schedule. When another angiogenesis inhibitor, TNP-470, was added to the antiangiogenic schedule of cyclophosphamide, drug-resistant Lewis lung carcinomas were eradicated. Each dose of the antiangiogenic schedule of cyclophosphamide induced the apoptosis of endothelial cells within tumors, and endothelial cell apoptosis preceded the apoptosis of drug-resistant tumor cells. This antiangiogenic effect was more pronounced in p53-null mice in which the apoptosis of p53-null endothelial cells induced by cyclophosphamide was so vigorous that drug-resistant tumors comprising 4.5% of body weight were eradicated. Thus, by using a dosing schedule of cyclophosphamide that provided more sustained apoptosis of endothelial cells within the vascular bed of a tumor, we show that a chemotherapeutic agent can more effectively control tumor growth in mice, regardless of whether the tumor cells are drug resistant.




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Y. Shaked, U. Emmenegger, S. Man, D. Cervi, F. Bertolini, Y. Ben-David, and R. S. Kerbel
Optimal biologic dose of metronomic chemotherapy regimens is associated with maximum antiangiogenic activity
Blood, November 1, 2005; 106(9): 3058 - 3061.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
L. Hu, J. Hofmann, J. Holash, G. D. Yancopoulos, A. K. Sood, and R. B. Jaffe
Vascular Endothelial Growth Factor Trap Combined with Paclitaxel Strikingly Inhibits Tumor and Ascites, Prolonging Survival in a Human Ovarian Cancer Model
Clin. Cancer Res., October 1, 2005; 11(19): 6966 - 6971.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
R. Yap, D. Veliceasa, U. Emmenegger, R. S. Kerbel, L. M. McKay, J. Henkin, and O. V. Volpert
Metronomic Low-Dose Chemotherapy Boosts CD95-Dependent Antiangiogenic Effect of the Thrombospondin Peptide ABT-510: A Complementation Antiangiogenic Strategy
Clin. Cancer Res., September 15, 2005; 11(18): 6678 - 6685.
[Abstract] [Full Text] [PDF]

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 Drug Metab. Dispos.Home page
C.-S. Chen, Y. Jounaidi, and D. J. Waxman
ENANTIOSELECTIVE METABOLISM AND CYTOTOXICITY OF R-IFOSFAMIDE AND S-IFOSFAMIDE BY TUMOR CELL-EXPRESSED CYTOCHROMES P450
Drug Metab. Dispos., September 1, 2005; 33(9): 1261 - 1267.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
Y. Shaked, U. Emmenegger, G. Francia, L. Chen, C. R. Lee, S. Man, A. Paraghamian, Y. Ben-David, and R. S. Kerbel
Low-dose Metronomic Combined with Intermittent Bolus-dose Cyclophosphamide Is an Effective Long-term Chemotherapy Treatment Strategy
Cancer Res., August 15, 2005; 65(16): 7045 - 7051.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
C. J. Streck, P. V. Dickson, C. Y.C. Ng, J. Zhou, J. T. Gray, A. C. Nathwani, and A. M. Davidoff
Adeno-Associated Virus Vector-Mediated Systemic Delivery of IFN-{beta} Combined with Low-Dose Cyclophosphamide Affects Tumor Regression in Murine Neuroblastoma Models
Clin. Cancer Res., August 15, 2005; 11(16): 6020 - 6029.
[Abstract] [Full Text] [PDF]

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 Drug Metab. Dispos.Home page
D. S. Riddick, C. Lee, S. Ramji, E. C. Chinje, R. L. Cowen, K. J. Williams, A. V. Patterson, I. J. Stratford, C. S. Morrow, A. J. Townsend, et al.
CANCER CHEMOTHERAPY AND DRUG METABOLISM
Drug Metab. Dispos., August 1, 2005; 33(8): 1083 - 1096.
[Abstract] [Full Text] [PDF]

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 Ann OncolHome page
G. Bocci, M. Tuccori, U. Emmenegger, V. Liguori, A. Falcone, R. S. Kerbel, and M. Del Tacca
Cyclophosphamide-methotrexate 'metronomic' chemotherapy for the palliative treatment of metastatic breast cancer. A comparative pharmacoeconomic evaluation
Ann. Onc., August 1, 2005; 16(8): 1243 - 1252.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
E. di Tomaso, D. Capen, A. Haskell, J. Hart, J. J. Logie, R. K. Jain, D. M. McDonald, R. Jones, and L. L. Munn
Mosaic Tumor Vessels: Cellular Basis and Ultrastructure of Focal Regions Lacking Endothelial Cell Markers
Cancer Res., July 1, 2005; 65(13): 5740 - 5749.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
G. Li, L. Tian, J.-m. Hou, Z.-y. Ding, Q.-m. He, P. Feng, Y.-j. Wen, F. Xiao, B. Yao, R. Zhang, et al.
Improved Therapeutic Effectiveness by Combining Recombinant CXC Chemokine Ligand 10 with Cisplatin in Solid Tumors
Clin. Cancer Res., June 1, 2005; 11(11): 4217 - 4224.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
P. E. Huber, M. Bischof, J. Jenne, S. Heiland, P. Peschke, R. Saffrich, H.-J. Grone, J. Debus, K. E. Lipson, and A. Abdollahi
Trimodal Cancer Treatment: Beneficial Effects of Combined Antiangiogenesis, Radiation, and Chemotherapy
Cancer Res., May 1, 2005; 65(9): 3643 - 3655.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
P. Beaudry, J. Force, G. N. Naumov, A. Wang, C. H. Baker, A. Ryan, S. Soker, B. E. Johnson, J. Folkman, and J. V. Heymach
Differential Effects of Vascular Endothelial Growth Factor Receptor-2 Inhibitor ZD6474 on Circulating Endothelial Progenitors and Mature Circulating Endothelial Cells: Implications for Use as a Surrogate Marker of Antiangiogenic Activity
Clin. Cancer Res., May 1, 2005; 11(9): 3514 - 3522.
[Abstract] [Full Text] [PDF]

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 BloodHome page
R. Okamoto, M. Ueno, Y. Yamada, N. Takahashi, H. Sano, T. Suda, and N. Takakura
Hematopoietic cells regulate the angiogenic switch during tumorigenesis
Blood, April 1, 2005; 105(7): 2757 - 2763.
[Abstract] [Full Text] [PDF]

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 JCOHome page
B. P. Schneider and K. D. Miller
Angiogenesis of Breast Cancer
J. Clin. Oncol., March 10, 2005; 23(8): 1782 - 1790.
[Full Text] [PDF]

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 Integr Cancer TherHome page
R. W. Moss
Patient Perspectives: Tijuana Cancer Clinics in the Post-NAFTA Era
Integr Cancer Ther, March 1, 2005; 4(1): 65 - 86.
[Abstract] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
V. Y. Gorbacheva, R. V. Kondratov, R. Zhang, S. Cherukuri, A. V. Gudkov, J. S. Takahashi, and M. P. Antoch
From The Cover: Circadian sensitivity to the chemotherapeutic agent cyclophosphamide depends on the functional status of the CLOCK/BMAL1 transactivation complex
PNAS, March 1, 2005; 102(9): 3407 - 3412.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
T. E. Sutherland, M. Schuliga, T. Harris, B. L. Eckhardt, R. L. Anderson, L. Quan, and A. G. Stewart
2-Methoxyestradiol Is an Estrogen Receptor Agonist That Supports Tumor Growth in Murine Xenograft Models of Breast Cancer
Clin. Cancer Res., March 1, 2005; 11(5): 1722 - 1732.
[Abstract] [Full Text] [PDF]

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 JCOHome page
G. Gasparini, R. Longo, M. Fanelli, and B. A. Teicher
Combination of Antiangiogenic Therapy With Other Anticancer Therapies: Results, Challenges, and Open Questions
J. Clin. Oncol., February 20, 2005; 23(6): 1295 - 1311.
[Abstract] [Full Text] [PDF]

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 BloodHome page
K. Podar and K. C. Anderson
The pathophysiologic role of VEGF in hematologic malignancies: therapeutic implications
Blood, February 15, 2005; 105(4): 1383 - 1395.
[Abstract] [Full Text] [PDF]

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 JCOHome page
K. Pietras and D. Hanahan
A Multitargeted, Metronomic, and Maximum-Tolerated Dose "Chemo-Switch" Regimen is Antiangiogenic, Producing Objective Responses and Survival Benefit in a Mouse Model of Cancer
J. Clin. Oncol., February 10, 2005; 23(5): 939 - 952.
[Abstract] [Full Text] [PDF]

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 JCOHome page
D. J. Hicklin and L. M. Ellis
Role of the Vascular Endothelial Growth Factor Pathway in Tumor Growth and Angiogenesis
J. Clin. Oncol., February 10, 2005; 23(5): 1011 - 1027.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
H.-P. Gerber and N. Ferrara
Pharmacology and Pharmacodynamics of Bevacizumab as Monotherapy or in Combination with Cytotoxic Therapy in Preclinical Studies
Cancer Res., February 1, 2005; 65(3): 671 - 680.
[Abstract] [Full Text] [PDF]

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 Cold Spring Harb Symp Quant BiolHome page
J. FOLKMAN and S. RYEOM
Is Oncogene Addiction Angiogenesis-dependent?
Cold Spring Harb Symp Quant Biol, January 1, 2005; 70(0): 389 - 397.
[Abstract] [PDF]

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 Arch DermatolHome page
B. Coras, C. Hafner, A. Reichle, U. Hohenleutner, R.-M. Szeimies, M. Landthaler, and T. Vogt
Antiangiogenic Therapy With Pioglitazone, Rofecoxib, and Trofosfamide in a Patient With Endemic Kaposi Sarcoma
Arch Dermatol, December 1, 2004; 140(12): 1504 - 1507.
[Abstract] [Full Text] [PDF]

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 Ann OncolHome page
V. R. Rozados, A. M. Sanchez, S. I. Gervasoni, H. H. Berra, P. Matar, and O. Graciela Scharovsky
Metronomic therapy with cyclophosphamide induces rat lymphoma and sarcoma regression, and is devoid of toxicity
Ann. Onc., October 1, 2004; 15(10): 1543 - 1550.
[Abstract] [Full Text] [PDF]

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 Circ. Res.Home page
E. Khmelewski, A. Becker, T. Meinertz, and W. D. Ito
Tissue Resident Cells Play a Dominant Role in Arteriogenesis and Concomitant Macrophage Accumulation
Circ. Res., September 17, 2004; 95(6): e56 - e64.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
G. Bocci, S. Man, S. K. Green, G. Francia, J. M. L. Ebos, J. M. du Manoir, A. Weinerman, U. Emmenegger, L. Ma, P. Thorpe, et al.
Increased Plasma Vascular Endothelial Growth Factor (VEGF) as a Surrogate Marker for Optimal Therapeutic Dosing of VEGF Receptor-2 Monoclonal Antibodies
Cancer Res., September 15, 2004; 64(18): 6616 - 6625.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
F. Donate, J. C. Juarez, X. Guan, N. V. Shipulina, M. L. Plunkett, Z. Tel-Tsur, D. E. Shaw, W. T. Morgan, and A. P. Mazar
Peptides Derived from the Histidine-Proline Domain of the Histidine-Proline-Rich Glycoprotein Bind to Tropomyosin and Have Antiangiogenic and Antitumor Activities
Cancer Res., August 15, 2004; 64(16): 5812 - 5817.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
G. Kaur, D. Belotti, A. M. Burger, K. Fisher-Nielson, P. Borsotti, E. Riccardi, J. Thillainathan, M. Hollingshead, E. A. Sausville, and R. Giavazzi
Antiangiogenic Properties of 17-(Dimethylaminoethylamino)-17-Demethoxygeldanamycin: An Orally Bioavailable Heat Shock Protein 90 Modulator
Clin. Cancer Res., July 15, 2004; 10(14): 4813 - 4821.
[Abstract] [Full Text] [PDF]

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 Neuro Oncol DukeHome page
J. J. Raizer, M. G. Malkin, M. Kleber, and L. E. Abrey
Phase 1 study of 28-day, low-dose temozolomide and BCNU in the treatment of malignant gliomas after radiation therapy
Neuro-oncol, July 1, 2004; 6(3): 247 - 252.
[Abstract] [PDF]

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 JCOHome page
S. De Placido, G. Scambia, G. Di Vagno, E. Naglieri, A. V. Lombardi, R. Biamonte, M. Marinaccio, G. Carteni, L. Manzione, A. Febbraro, et al.
Topotecan Compared With No Therapy After Response to Surgery and Carboplatin/Paclitaxel in Patients With Ovarian Cancer: Multicenter Italian Trials in Ovarian Cancer (MITO-1) Randomized Study
J. Clin. Oncol., July 1, 2004; 22(13): 2635 - 2642.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
R. T. Tong, Y. Boucher, S. V. Kozin, F. Winkler, D. J. Hicklin, and R. K. Jain
Vascular Normalization by Vascular Endothelial Growth Factor Receptor 2 Blockade Induces a Pressure Gradient Across the Vasculature and Improves Drug Penetration in Tumors
Cancer Res., June 1, 2004; 64(11): 3731 - 3736.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
U. Emmenegger, S. Man, Y. Shaked, G. Francia, J. W. Wong, D. J. Hicklin, and R. S. Kerbel
A Comparative Analysis of Low-Dose Metronomic Cyclophosphamide Reveals Absent or Low-Grade Toxicity on Tissues Highly Sensitive to the Toxic Effects of Maximum Tolerated Dose Regimens
Cancer Res., June 1, 2004; 64(11): 3994 - 4000.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
J. W. Park, R. S. Kerbel, G. J. Kelloff, J. C. Barrett, B. A. Chabner, D. R. Parkinson, J. Peck, R. W. Ruddon, C. C. Sigman, and D. J. Slamon
Rationale for Biomarkers and Surrogate End Points in Mechanism-Driven Oncology Drug Development
Clin. Cancer Res., June 1, 2004; 10(11): 3885 - 3896.
[Full Text] [PDF]

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 The OncologistHome page
E. Bergsland and M. N. Dickler
Maximizing the Potential of Bevacizumab in Cancer Treatment
Oncologist, June 1, 2004; 9(suppl_1): 36 - 42.
[Abstract] [Full Text] [PDF]

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 The OncologistHome page
H. S. Rugo
Bevacizumab in the Treatment of Breast Cancer: Rationale and Current Data
Oncologist, June 1, 2004; 9(suppl_1): 43 - 49.
[Abstract] [Full Text] [PDF]


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