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Science 7 January 2005:
Vol. 307. no. 5706, pp. 58 - 62
DOI: 10.1126/science.1104819
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Review

Normalization of Tumor Vasculature: An Emerging Concept in Antiangiogenic Therapy

Rakesh K. Jain

Solid tumors require blood vessels for growth, and many new cancer therapies are directed against the tumor vasculature. The widely held view is that these antiangiogenic therapies should destroy the tumor vasculature, thereby depriving the tumor of oxygen and nutrients. Here, I review emerging evidence supporting an alternative hypothesis—that certain antiangiogenic agents can also transiently "normalize" the abnormal structure and function of tumor vasculature to make it more efficient for oxygen and drug delivery. Drugs that induce vascular normalization can alleviate hypoxia and increase the efficacy of conventional therapies if both are carefully scheduled. A better understanding of the molecular and cellular underpinnings of vascular normalization may ultimately lead to more effective therapies not only for cancer but also for diseases with abnormal vasculature, as well as regenerative medicine, in which the goal is to create and maintain a functionally normal vasculature.

E. L. Steele Lab for Tumor Biology, Department of Radiation Oncology, Massachusetts General Hospital, and Harvard Medical School, Cox-7, 100 Blossom Street, Boston, MA 02114, USA. E-mail: jain{at}steele.mgh.harvard.edu

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C. Su, M. Na, J. Chen, X. Wang, Y. Liu, W. Wang, Q. Zhang, L. Li, J. Long, X. Liu, et al. (2008)
Mol. Cancer Res. 6, 568-575
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Targeted Therapies for the Treatment of Breast Cancer in the Post-trastuzumab Era.
F. Petrelli, M. Cabiddu, M. E. Cazzaniga, M. Cremonesi, and S. Barni (2008)
Oncologist 13, 373-381
   Abstract »    Full Text »    PDF »
Tumor cell cycle arrest induced by shear stress: Roles of integrins and Smad.
S.-F. Chang, C. A. Chang, D.-Y. Lee, P.-L. Lee, Y.-M. Yeh, C.-R. Yeh, C.-K. Cheng, S. Chien, and J.-J. Chiu (2008)
PNAS 105, 3927-3932
   Abstract »    Full Text »    PDF »
Impact of Angiogenesis Inhibition by Sunitinib on Tumor Distribution of Temozolomide.
Q. Zhou, P. Guo, and J. M. Gallo (2008)
Clin. Cancer Res. 14, 1540-1549
   Abstract »    Full Text »    PDF »
Rapid xenograft tumor progression in beta-arrestin1 transgenic mice due to enhanced tumor angiogenesis.
L. Zou, R. Yang, J. Chai, and G. Pei (2008)
FASEB J 22, 355-364
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Early Antiangiogenic Activity of Bevacizumab Evaluated by Computed Tomography Perfusion Scan in Patients with Advanced Hepatocellular Carcinoma.
A. X. Zhu, N. S. Holalkere, A. Muzikansky, K. Horgan, and D. V. Sahani (2008)
Oncologist 13, 120-125
   Abstract »    Full Text »    PDF »
Critical Role of the Stress Chaperone GRP78/BiP in Tumor Proliferation, Survival, and Tumor Angiogenesis in Transgene-Induced Mammary Tumor Development.
D. Dong, M. Ni, J. Li, S. Xiong, W. Ye, J. J. Virrey, C. Mao, R. Ye, M. Wang, L. Pen, et al. (2008)
Cancer Res. 68, 498-505
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Differential Involvement of Vascular Endothelial Growth Factor in the Survival of Hypoxic Colon Cancer Cells.
M. Calvani, D. Trisciuoglio, C. Bergamaschi, R. H. Shoemaker, and G. Melillo (2008)
Cancer Res. 68, 285-291
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Phase II study of temozolomide, thalidomide, and celecoxib for newly diagnosed glioblastoma in adults.
S. Kesari, D. Schiff, J. W. Henson, A. Muzikansky, D. C. Gigas, L. Doherty, T. T. Batchelor, J. A. Longtine, K. L. Ligon, S. Weaver, et al. (2008)
Neuro-oncol 10, 300-308
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Modulation of the antitumor activity of metronomic cyclophosphamide by the angiogenesis inhibitor axitinib.
J. Ma and D. J. Waxman (2008)
Mol. Cancer Ther. 7, 79-89
   Abstract »    Full Text »    PDF »
Molecular mechanisms for the activity of PX-478, an antitumor inhibitor of the hypoxia-inducible factor-1{alpha}.
M. Y. Koh, T. Spivak-Kroizman, S. Venturini, S. Welsh, R. R. Williams, D. L. Kirkpatrick, and G. Powis (2008)
Mol. Cancer Ther. 7, 90-100
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Antiangiogenic compounds interfere with chemotherapy of brain tumors due to vessel normalization.
A. Claes, P. Wesseling, J. Jeuken, C. Maass, A. Heerschap, and W. P.J. Leenders (2008)
Mol. Cancer Ther. 7, 71-78
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Effect of Tumor Microenvironment Modulation on the Efficacy of Oncolytic Virus Therapy.
K. Kurozumi, J. Hardcastle, R. Thakur, M. Yang, G. Christoforidis, G. Fulci, F. H. Hochberg, R. Weissleder, W. Carson, E. A. Chiocca, et al. (2007)
J Natl Cancer Inst 99, 1768-1781
   Abstract »    Full Text »    PDF »
Blood Vessel Morphologic Changes Depicted with MR Angiography during Treatment of Brain Metastases: A Feasibility Study.
E. Bullitt, N. U. Lin, J. K. Smith, D. Zeng, E. P. Winer, L. A. Carey, W. Lin, and M. G. Ewend (2007)
Radiology 245, 824-830
   Abstract »    Full Text »    PDF »
Bevacizumab for the Treatment of Epithelial Ovarian Cancer: Will This Be Its Finest Hour?.
S. B. Kaye (2007)
J. Clin. Oncol. 25, 5150-5152
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Inhibition of Protein Kinase C{beta} by Enzastaurin Enhances Radiation Cytotoxicity in Pancreatic Cancer.
A. C. Spalding, R. Watson, M. E. Davis, A. C. Kim, T. S. Lawrence, and E. Ben-Josef (2007)
Clin. Cancer Res. 13, 6827-6833
   Abstract »    Full Text »    PDF »


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