Angiogenesis in brain tumours

Nature Reviews Neuroscience

Volumn 8, Issue 8, 2007, Pages 610-622

  Jain, Rakesh K ^a   Di Tomaso, Emmanuelle ^a   Duda, Dan G ^a   Loeffler, Jay S ^a   Sorensen, A Gregory ^a   Batchelor, Tracy T ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUORO 2 METHYL 5 INDOLYLOXY) 6 METHOXY 7 [3 (1 PYRROLIDINYL)PROPOXY]QUINAZOLINE; ANGIOGENESIS INHIBITOR; ANTINEOPLASTIC AGENT; BEVACIZUMAB; CILENGITIDE; CORTICOTROPIN RELEASING FACTOR DERIVATIVE; ERLOTINIB; EVEROLIMUS; GEFITINIB; IMATINIB; IRINOTECAN; LAPATINIB; PAZOPANIB; PROTEIN TYROSINE KINASE INHIBITOR; SORAFENIB; STEROID; SUNITINIB; TEMOZOLOMIDE; TEMSIROLIMUS; TIPIFARNIB; VANDETANIB; VASCULOTROPIN; VASCULOTROPIN INHIBITOR; VATALANIB;

ARTERY THROMBOSIS; BLINDNESS; BLOOD VESSEL FUNCTION; BRAIN BLOOD VESSEL; BRAIN EDEMA; BRAIN HEMORRHAGE; BRAIN INFARCTION; BRAIN OXYGEN TENSION; BRAIN TUMOR; CANCER COMBINATION CHEMOTHERAPY; CANCER MORTALITY; CANCER RADIOTHERAPY; CANCER SURGERY; CLINICAL TRIAL; CONFUSION; DRUG EFFICACY; DRUG INDUCED HEADACHE; FATIGUE; GLIOBLASTOMA; HUMAN; LETHARGY; LEUKOENCEPHALOPATHY; MICROENVIRONMENT; MOLECULAR MECHANICS; MORBIDITY; NEUROLOGIC DISEASE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SEIZURE; STEROID THERAPY; THROMBOEMBOLISM; TISSUE PRESSURE; TREATMENT RESPONSE; TUMOR VASCULARIZATION; UNSPECIFIED SIDE EFFECT; VISUAL DISORDER;

ANIMALS; ANTINEOPLASTIC AGENTS; BLOOD VESSELS; BRAIN EDEMA; BRAIN NEOPLASMS; GLIOBLASTOMA; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 34447632643     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn2175     Document Type: Review

References (150)

1. Wong, E. T. et al. Outcomes and prognostic factors in recurrent glioma patients enrolled onto phase II clinical trials. J. Clin. Oncol. 17, 2572-2578 (1999).
2. Stupp, R. et al. Changing paradigms - an update on the multidisciplinary management of malignant glioma. Oncologist 11, 165-180 (2006).
3. van de Beek, D. Brain teasing effect of dexamethasone. Lancet Neurol. 6, 203-204 (2007).
4. Kleihues, P., Burger, P. C. & Scheithauer, B. W. in Histological Typing of Tumours of the Central Nervous System 2nd edn (ed. Sobin, L. H.) 1-105 (Springer, Berlin, 1993).
5. Folkman, J. Tumor angiogenesis: therapeutic implications. N. Engl. J. Med. 285, 1182-1186 (1971).
6. Folkman, J. Angiogenesis: an organizing principle for drug discovery? Nature Rev. Drug Discov. 6, 273-286 (2007). Reference 5 is the seminal paper that led to search for anti-angiogenic therapy for cancer. Reference 6 illustrates how this hypothesis has influenced treatment of cancer and other diseases.
7. Jain, R. K., Duda, D. G., Clark, J. W. & Loeffler, J. S. Lessons from phase III clinical trials on anti-VEGF therapy for cancer. Nature Clin. Pract. Oncol. 3, 24-40 (2006). A critical review of progress and outstanding issues in anti-angiogenic therapy of cancer in patients.
8. Purow, B. & Fine, H. A. Progress report on the potential of angiogenesis inhibitors for neurooncology. Cancer Invest. 22, 577-587 (2004).
9. Pope, W. B., Lai, A., Nghiemphu, P., Mischel, P. & Cloughesy, T. F. MRI in patients with high-grade gliomas treated with bevacizumab and chemotherapy. Neurology 66, 1258-1260 (2006).
10. Jain, R. K. Normalizing tumor vasculature with antiangiogenic therapy: a new paradigm for combination therapy. Nature Med. 7, 987-989 (2001).
11. Jain, R. K. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307, 58-62 (2005). Reference 10 is the seminal paper on the normalization hypothesis and its implications for treatment of cancer and other diseases characterized by abnormal vasculature. Reference 11 provides a critical update on this hypothesis.
12. Winkler, F. et al. Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1 and matrix metalloproteinases. Cancer Cell 6, 553-563 (2004). First pre-clinical evidence of vascular normalization in an orthotopic model of glioma in mice. This paper also provides the molecular mechanisms of vascular normalization and demonstrates that the outcome of radiation therapy is best when given during the window of normalization.
13. Batchelor, T. T. et al. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 11, 83-95 (2007). First clinical evidence of a window of vascular normalization in recurrent glioblastoma induced by an anti-angiogenic agent. Also demonstrates the benefits of normalization in alleviating oedema and identifies potential blood and imaging biomarkers.
14. Vredenburgh, J. J. et al. Phase II trial of bevacizumab and irinotecan in recurrent malignant glioma. Clin. Cancer Res. 13, 1253-1259 (2007).
15. Fidler, I. J., Yano, S., Zhang, R. D., Fujimaki, T. & Bucana, C. D. The seed and soil hypothesis: vascularisation and brain metastases. Lancet Oncol. 3, 53-57 (2002). An excellent review of vascular biology of brain metastases.
16. Neuwelt, E. A. Mechanisms of disease: the blood-brain barrier. Neurosurgery 54, 131-140 (2004).
17. Palmieri, D., Chambers, A. F., Felding-Habermann, B., Huang, S. & Steeg, P. S. The biology of metastasis to a sanctuary site. Clin. Cancer Res. 13, 1656-1662 (2007).
18. Yuan, F. et al. Vascular permeability and microcirculation of gliomas and mammary carcinomas transplanted in rat and mouse cranial windows. Cancer Res. 54, 4564-4568 (1994).
19. Hobbs, S. K. et al. Regulation of transport pathways in tumor vessels: role of tumor type and microenvironment. Proc. Natl Acad. Sci. USA 95, 4607-4612 (1998).
20. Monsky, W. L. et al. Augmentation of transvascular transport of macromolecules and nanoparticles in tumors using vascular endothelial growth factor. Cancer Res. 59, 4129-4135 (1999).
21. Fukumura, D. et al. Hypoxia and acidosis independently up-regulate vascular endothelial growth factor transcription in brain tumors in vivo. Cancer Res. 61, 6020-6024 (2001).
22. Izumi, Y., Xu, L., di Tomaso, E., Fukumura, D. & Jain, R. K. Tumour biology: herceptin acts as an antiangiogenic cocktail. Nature 416, 279-280 (2002). References 18-22 are key papers on the structure and function of tumour vasculature in orthotopic models of primary and metastatic brain tumours in mice.
23. Bullitt, E. et al. Vessel tortuosity and brain tumor malignancy: a blinded study. Acad. Radiol. 12, 1232-1240 (2005).
24. Deeken, J. F. & Loscher, W. The blood-brain barrier and cancer: transporters, treatment, and Trojan horses. Clin. Cancer Res. 13, 1663-1674 (2007).
25. Plate, K. H. & Mennel, H. D. Vascular morphology and angiogenesis in glial tumors. Exp. Toxicol. Pathol. 47, 89-94 (1995).
26. 2 distribution and bioreductive enzymes in human malignant brain tumors. Int. J. Radiat. Oncol. Biol. Phys. 29, 427-431 (1994).
27. Valk, P. E., Mathis, C. A., Prados, M. D., Gilbert, J. C. & Budinger, T. F. Hypoxia in human gliomas: demonstration by PET with fluorine-18- fluoromisonidazole. J. Nucl. Med. 33, 2133-2137 (1992).
28. Guo, P. et al. Platelet-derived growth factor-B enhances glioma angiogenesis by stimulating vascular endothelial growth factor expression in tumor endothelia and by promoting pericyte recruitment. Am. J. Pathol. 162, 1083-1093 (2003).
29. Zagzag, D. et al. In situ expression of angiopoietins in astrocytomas identifies angiopoietin-2 as an early marker of tumor angiogenesis. Exp. Neurol. 159, 391-400 (1999).
30. Kleihues, P. & Cavenee, W. K. Pathology and Genetics of Tumours of the Nervous System (International Agency for Research on Cancer, Lyon, 2000).
31. Jain, R. K. The next frontier of molecular medicine: delivery of therapeutics. Nature Med. 4, 655-657 (1998).
32. Jain, R. K., Munn, L. L. & Fukumura, D. Dissecting tumour pathophysiology using intravital microscopy. Nature Rev. Cancer 2, 266-276 (2002). A comprehensive review of microscopy techniques to measure molecular, cellular, anatomical and physiological parameters of tumour vessels in live animals.
33. Monsky, W. L. et al. Role of host microenvironment in angiogenesis and microvascular functions in human breast cancer xenografts: mammary fat pad versus cranial tumors. Clin. Cancer Res. 8, 1008-1013 (2002).
34. Jain, R. K., Tong, R. T. & Munn, L. L. Effect of vascular normalization by anti-angiogenic therapy on interstitial hypertension, peri-tumor edema and lymphatic metastasis: insights from a mathematical model. Cancer Res. 67, 2729-2735 (2007).
35. Wolf, R. L. et al. Grading of CNS neoplasms using continuous arterial spin labeled perfusion MR imaging at 3 Tesla. J. Magn. Reson. Imaging 22, 475-482 (2005).
36. 2, gradients in solid tumors in vivo: high-resolution measurements reveal a lack of correlation. Nature Med. 3, 177-182 (1997).
37. Carmeliet, P. & Jain, R. K. Angiogenesis in cancer and other diseases. Nature 407, 249-257 (2000). An important and comprehensive review of molecular and cellular mechanisms of blood vessel formation in health and disease.
38. Dvorak, H. F. Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J. Clin. Oncol. 20, 4368-4380 (2002).
39. Ferrara, N. Vascular endothelial growth factor: basic science and clinical progress. Endocr. Rev. 25, 581-611 (2004). References 38 and 39 provide excellent overviews of VEGF biology and its role in angiogenesis.
40. Fukumura, D., Kashiwagi, S. & Jain, R. K. The role of nitric oxide in tumour progression. Nature Rev. Cancer 6, 521-534 (2006).
41. Fukumura, D. et al. Tumor induction of VEGF promoter activity in stromal cells. Cell 94, 715-725 (1998).
42. Boucher, Y., Salehi, H., Witwer, B., Harsh, G. R. & Jain, R. K. Interstitial fluid pressure in intracranial tumours in patients and in rodents. Br. J. Cancer 75, 829-836 (1997).
43. Jain, R. K. Barriers to drug delivery in solid tumors. Sci. Am. 271, 58-65 (1994).
44. 2 in solid tumors. Ann. Biomed. Eng. 28, 543-555 (2000).
45. Fukumura, D. et al. Tumor-necrosis-factor α-induced leukocyte adhesion in normal and tumor vessels: effect of tumor type, transplantation site, and host strain. Cancer Res. 55, 4824-4829 (1995).
46. Melder, R. J. et al. During angiogenesis, vascular endothelial growth factor and basic fibroblast growth factor regulate natural killer cell adhesion to tumor endothelium. Nature Med. 2, 992-997 (1996).
47. Melder, R. J., Salehi, H. A. & Jain, R. K. Interaction of activated natural killer cells with normal and tumor vessels in cranial windows in mice. Microvasc. Res. 50, 35-44 (1995).
48. Holash, J. et al. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science 284, 1994-1998 (1999).
49. Leenders, W. P., Kusters, B. & de Waal, R. M. Vessel co-option: how tumors obtain blood supply in the absence of sprouting angiogenesis. Endothelium 9, 83-87 (2002).
50. Padera, T. P. et al. Pathology: cancer cells compress intratumour vessels. Nature 427, 695 (2004).
51. Carmeliet, P. Angiogenesis in life, disease and medicine. Nature 438, 932-936 (2005). A key review on potential mechanisms of synergy between anti-angiogenic and cytotoxic therapies.
52. Ferrara, N., Hillan, K. J., Gerber, H. P. & Novotny, W. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nature Rev. Drug Discov. 3, 391-400 (2004).
53. Yancopoulos, G. D. et al. Vascular-specific growth factors and blood vessel formation. Nature 407, 242-248 (2000). Another key and comprehensive review of molecular and cellular mechanisms of blood vessel formation in health and disease.
54. Wizigmann-Voos, S. & Plate, K. H. Pathology, genetics and cell biology of hemangioblastomas. Histol. Histopathol. 11, 1049-1061 (1996).
55. Duda, D. G. et al. Evidence for incorporation of bone marrow-derived endothelial cells into perfused blood vessels in tumors. Blood 107, 2774-2776 (2006).
56. + cells in the endothelium of tumor vessels in the mouse brain. Neurosurgery 59, 374-382(2006).
57. Aghi, M., Cohen, K. S., Klein, R. J., Scadden, D. T. & Chiocca, E. A. Tumor stromal-derived factor-1 recruits vascular progenitors to mitotic neovasculature, where microenvironment influences their differentiated phenotypes. Cancer Res. 66, 9054-9064 (2006).
58. Yano, S. et al. Expression of vascular endothelial growth factor is necessary but not sufficient for production and growth of brain metastasis. Cancer Res. 60, 4959-4967 (2000).
59. Patan, S. et al. Vascular morphogenesis and remodeling in a human tumor xenograft: blood vessel formation and growth after ovariectomy and tumor implantation. Circ. Res. 89, 732-739 (2001).
60. Sakariassen, P. O. et al. Angiogenesis-independent tumor growth mediated by stem-like cancer cells. Proc. Natl Acad. Sci. USA 103, 16466-16471 (2006).
61. Leenders, W. P. et al. Antiangiogenic therapy of cerebral melanoma metastases results in sustained tumor progression via vessel co-option. Clin. Cancer Res. 10, 6222-6230 (2004).
62. Plate, K. H., Breier, G., Weich, H. A. & Risau, W. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 359, 845-848 (1992).
63. Shweiki, D., Itin, A., Soffer, D. & Keshet, E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359, 843-845 (1992). References 62 and 63 are seminal papers demonstrating the role of hypoxia in VEGF upregulation in glioblastoma.
64. Millauer, B., Shawver, L., Plate, K. H., Risau, W. & Ullrich, A. Glioblastoma growth inhibited in vivo by a dominant-negative Flk-1 mutant. Nature 367, 576-579 (1994).
65. Fischer, I., Gagner, J. P., Law, M., Newcomb, E. W. & Zagzag, D. Angiogenesis in gliomas: biology and molecular pathophysiology. Brain. Pathol. 15, 297-310 (2005).
66. di Tomaso, E. et al. Correlation between VEGF expression and MVD in sporadic and NF2-related schwanomas. J. Clin. Oncol. 18S (ASCO Proceedings), Abstr. 2083 (2007).
67. Peddinti, R. et al. Prominent microvascular proliferation in clinically aggressive neuroblastoma. Clin. Cancer Res. 13, 3499-3506 (2007).
68. Reiss, Y., Machein, M. R. & Plate, K. H. The role of angiopoietins during angiogenesis in gliomas. Brain Pathol. 15, 311-317 (2005).
69. Machein, M. R. et al. Angiopoietin-1 promotes tumor angiogenesis in a rat glioma model. Am. J. Pathol. 165, 1557-1570 (2004).
70. Hood, J. D. & Cheresh, D. A. Role of integrins in cell invasion and migration. Nature Rev. Cancer 2, 91-100 (2002).
71. Carmeliet, P. et al. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98, 147-157 (1999).
72. Gagnon, M. L. et al. Identification of a natural soluble neuropilin-1 that binds vascular endothelial growth factor: in vivo expression and antitumor activity. Proc. Natl Acad. Sci. USA 97, 2573-2578 (2000).
73. Stan, A. C., Nemati, M. N., Pietsch, T., Walter, G. F. & Dietz, H. In vivo inhibition of angiogenesis and growth of the human U-87 malignant glial tumor by treatment with an antibody against basic fibroblast growth factor. J. Neurosurg. 82, 1044-1052 (1995).
74. Jain, R. K. Molecular regulation of vessel maturation. Nature Med. 9, 685-693 (2003).
75. Sun, L. et al. Neuronal and glioma-derived stem cell factor induces angiogenesis within the brain. Cancer Cell 9, 287-300 (2006).
76. Samoto, K. et al. Expression of vascular endothelial growth factor and its possible relation with neovascularization in human brain tumors. Cancer Res. 55, 1189-1193 (1995).
77. Schmidt, N. O. et al. Levels of vascular endothelial growth factor, hepatocyte growth factor/scatter factor and basic fibroblast growth factor in human gliomas and their relation to angiogenesis. Int. J. Cancer 84, 10-18 (1999).
78. Phung, T. L. et al. Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 10, 159-170 (2006).
79. Dunn, I. F., Heese, O. & Black, P. M. Growth factors in glioma angiogenesis: FGFs, PDGF, EGF and TGFs. J. Neurooncol. 50, 121-137 (2000).
80. Fredriksson, L., Li, H. & Eriksson, U. The PDGF family: four gene products form five dimeric isoforms. Cytokine Growth Factor Rev. 15, 197-204 (2004).
81. Hermansson, M. et al. Endothelial cell hyperplasia in human glioblastoma: coexpression of mRNA for platelet-derived growth factor (PDGF) B chain and PDGF receptor suggests autocrine growth stimulation. Proc. Natl Acad. Sci. USA 85, 7748-7752 (1988).
82. Nystrom, H. C. et al. Platelet-derived growth factor B retention is essential for development of normal structure and function of conduit vessels and capillaries. Cardiovasc. Res. 71, 557-565 (2006).
83. Wen, P. Y. et al. Phase I/II study of imatinib mesylate for recurrent malignant gliomas: North American Brain Tumor Consortium Study 99-08. Clin. Cancer Res. 12, 4899-4907 (2006).
84. Salmaggi, A. et al. Intracavitary VEGF, bFGF, IL-8, IL-12 levels in primary and recurrent malignant glioma. J. Neurooncol. 62, 297-303 (2003).
85. Brat, D. J., Bellail, A. C. & Van Meir, E. G. The role of interleukin-8 and its receptors in gliomagenesis and tumoral angiogenesis. Neuro Oncol. 7, 122-133 (2005).
86. Kim, L. S., Huang, S., Lu, W., Lev, D. C. & Price, J. E. Vascular endothelial growth factor expression promotes the growth of breast cancer brain metastases in nude mice. Clin. Exp. Metastasis 21, 107-118 (2004).
87. Garkavtsev, I. et al. The candidate tumour suppressor protein ING4 regulates brain tumour growth and angiogenesis. Nature 428, 328-332 (2004).
88. Bajetto, A. et al. CXCR4 and SDF1 expression in human meningiomas: a proliferative role in tumoral meningothelial cells in vitro. Neuro Oncol. 9, 3-11 (2007).
89. Bajetto, A. et al. Expression of CXC chemokine receptors 1-5 and their ligands in human glioma tissues: role of CXCR4 and SDF1 in glioma cell proliferation and migration. Neurochem. Int. 49, 423-432 (2006).
90. Florio, T. et al. Chemokine stromal cell-derived factor 1α induces proliferation and growth hormone release in GH4C1 rat pituitary adenoma cell line through multiple intracellular signals. Mol. Pharmacol. 69, 539-546 (2006).
91. Zagzag, D. et al. Hypoxia-inducible factor 1 and VEGF upregulate CXCR4 in glioblastoma: implications for angiogenesis and glioma cell invasion. Lab. Invest. 86, 1221-1232 (2006).
92. Fernandis, A. Z., Prasad, A., Band, H., Klosel, R. & Ganju, R. K. Regulation of CXCR4-mediated chemotaxis and chemoinvasion of breast cancer cells. Oncogene 23, 157-167 (2004).
93. Burger, M. et al. Functional expression of CXCR4 (CD184) on small-cell lung cancer cells mediates migration, integrin activation, and adhesion to stromal cells. Oncogene 22, 8093-8101 (2003).
94. Grunewald, M. et al. VEGF-induced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124, 175-189 (2006).
95. Hattori, K. et al. Plasma elevation of stromal cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells. Blood 97, 3354-3360 (2001).
96. Benedito, R. & Duarte, A. Expression of Dll4 during mouse embryogenesis suggests multiple developmental roles. Gene Expr. Patterns 5, 750-755 (2005).
97. Gridley, T. Vascular biology: vessel guidance. Nature 445, 722-723 (2007).
98. Williams, C. K., Li, J. L., Murga, M., Harris, A. L. & Tosato, G. Up-regulation of the Notch ligand Delta-like 4 inhibits VEGF-induced endothelial cell function. Blood 107, 931-939 (2006).
99. Leslie, J. D. et al. Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development 134, 839-844 (2007).
100. Ridgway, J. et al. Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 444, 1083-1087 (2006).
101. Hellstrom, M. et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445, 776-780 (2007).
102. Sundberg, C. et al. Glomeruloid microvascular proliferation follows adenoviral vascular permeability factor/vascular endothelial growth factor-164 gene delivery. Am. J. Pathol. 158, 1145-1160 (2001).
103. Yuan, F. et al. Time-dependent vascular regression and permeability changes in established human tumor xenografts induced by an anti-vascular endothelial growth factor/vascular permeability factor antibody. Proc. Natl Acad. Sci. USA 93, 14765-14770 (1996).
104. Jain, R. K. et al. Endothelial cell death, angiogenesis, and microvascular function after castration in an androgen-dependent tumor: role of vascular endothelial growth factor. Proc. Natl Acad. Sci. USA 95, 10820-10825 (1998).
105. Tong, R. T. et al. 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. 64, 3731-3736 (2004).
106. Baluk, P., Hashizume, H. & McDonald, D. M. Cellular abnormalities of blood vessels as targets in cancer. Curr. Opin. Genet. Dev. 15, 102-111 (2005).
107. Jain, R. K., Finn, A. V., Kolodgie, F. D., Gold, H. K. & Virmani, R. Antiangiogenic therapy for normalization of atherosclerotic plaque vasculature: a potential strategy for plaque stabilization. Nature Clin. Pract. Cardiovasc. Med. (in the press)
108. Willett, C. G. et al. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nature Med. 10, 145-147 (2004). The first clinical evidence of vascular normalization by bevacizumab in a human tumour.
109. Kerbel, R. S. Antiangiogenic therapy: a universal chemosensitization strategy for cancer? Science 312, 1171-1175 (2006). A key review on potential mechanisms of synergy between anti-angiogenic and cytotoxic therapies.
110. Willet, C. G. et al. Combined vascular endothelial growth factor-targeted therapy and radiotherapy for colorectal cancer: theory and clinical practice. Semin. Oncol. 33, S35-S40 (2006).
111. Gorski, D. H. et al. Blockage of the vascular endothelial growth factor stress response increases the antitumor effects of ionizing radiation. Cancer Res. 59, 3374-3378 (1999).
112. Weichselbaum, R. R. How does antiangiogenic therapy affect brain tumor response to radiation? Nature Clin. Pract. Oncol. 2, 232-233 (2005).
113. Calabrese, C. et al. A perivascular niche for brain tumor stem cells. Cancer cell 11, 69-82 (2007).
114. Gonzalez, J., Kumar, A. J., Conrad, C. A. & Levin, V. A. Effect of bevacizumab on radiation necrosis of the brain. Int. J. Radiat. Oncol. Biol. Phys. 67, 323-326 (2007).
115. Verheul, H. M. & Pinedo, H. M. Possible molecular mechanisms involved in the toxicity of angiogenesis inhibition. Nature Rev. Cancer 7, 475-485 (2007). An important paper that reviews potential mechanisms of toxicity from anti-angiogenic therapy.
116. Gagner, J. P., Law, M., Fischer, I., Newcomb, E. W. & Zagzag, D. Angiogenesis in gliomas: imaging and experimental therapeutics. Brain Pathol. 15, 342-363 (2005).
117. Duda, D. G., Cohen, K. S., Scadden, D. T. & Jain, R. K. A protocol for detection and enumeration of circulating endothelial cells and circulating progenitor cells in human blood. Nature Protoc. 4, 805-810 (2007).
118. Weissman, D. E. Glucocorticoid treatment for brain metastases and epidural spinal cord compression: a review. J. Clin. Oncol. 6, 543-551 (1988).
119. Sorensen, A. G. et al. Comparison of diameter and perimeter methods for tumor volume calculation. J. Clin. Oncol. 19, 551-557 (2001).
120. Sorensen, A. G. & Reimer, P. Cerebral MR Perfusion Imaging: Principles and Current Applications (Thieme Medical Publishers, NY, USA 2001).
121. Sorensen, A. G. Magnetic resonance as a cancer imaging biomarker. J. Clin. Oncol. 24, 3274-3281 (2006).
122. Miller, J. C., Pien, H. H., Sahani, D., Sorensen, A. G. & Thrall, J. H. Imaging angiogenesis: applications and potential for drug development. J. Natl Cancer Inst. 97, 172-187 (2005).
123. Serganova, I., Humm, J., Ling, C. & Blasberg, R. Tumor Hypoxia Imaging. Clin. Cancer Res. 12, 5260-5264 (2006).
124. Akella, N. S. et al. Assessment of brain tumor angiogenesis inhibitors using perfusion magnetic resonance imaging: quality and analysis results of a phase I trial. J. Magn. Reson. Imaging 20, 913-922 (2004).
125. Jackson, A. et al. Reproducibility of quantitative dynamic contrast-enhanced MRI in newly presenting glioma. Br. J. Radiol. 76, 153-162 (2003).
126. Mankoff, D. A. et al. Tumor-specific positron emission tomography imaging in patients: [18F] fluorodeoxyglucose and beyond. Clin. Cancer Res. 13, 3460-3469 (2007).
127. Wester, H. J. Nuclear imaging probes: from bench to bedside. Clin. Cancer Res. 13, 3470-3481 (2007).
128. Vesalius, A. De Humani Corporis Fabrica (The fabric of the human body) (Oporinus, Basel, 1543).
129. Carmeliet, P. & Tessier-Lavigne, M. Common mechanisms of nerve and blood vessel wiring. Nature 436, 193-200 (2005).
130. Klagsbrun, M. & Eichmann, A. A role for axon guidance receptors and ligands in blood vessel development and tumor angiogenesis. Cytokine Growth Factor Rev. 16, 535-548 (2005). References 129 and 130 represent excellent reviews of common mechanisms of axon guidance and angiogenesis.
131. Wilson, B. D. et al. Netrins promote developmental and therapeutic angiogenesis. Science 313, 640-644 (2006).
132. Cirulli, V. & Yebra, M. Netrins: beyond the brain. Nature Rev. Mol. Cell Biol. 8, 296-306 (2007).
133. Egea, J. & Klein, R. Bidirectional Eph-ephrin signaling during axon guidance. Trends Cell Biol. 17, 230-238 (2007).
134. Kuijper, S., Turner, C. J. & Adams, R. H. Regulation of angiogenesis by Eph-ephrin interactions. Trends Cardiovasc. Med. 17, 145-151 (2007).
135. Soker, S., Takashima, S., Miao, H. Q., Neufeld, G. & Klagsbrun, M. Neuropilin-1 is expressed by endothelial and tumor cells as an isoform-specific receptor for vascular endothelial growth factor. Cell 92, 735-745 (1998).
136. Mamluk, R., Klagsbrun, M., Detmar, M. & Bielenberg, D. R. Soluble neuropilin targeted to the skin inhibits vascular permeability. Angiogenesis 8, 217-227 (2005).
137. Bielenberg, D. R. et al. Semaphorin 3F, a chemorepulsant for endothelial cells, induces a poorly vascularized, encapsulated, nonmetastatic tumor phenotype. J. Clin. Invest. 114, 1260-1271 (2004).
138. Pan, Q. et al. Blocking neuropilin-1 function has an additive effect with anti-VEGF to inhibit tumor growth. Cancer Cell 11, 53-67 (2007).
139. + endothelial cells and systemic mobilization of hematopoietic progenitors. J. Clin. Invest. 115, 653-663 (2005).
140. Duda, D. G. & Jain, R. K. Pleiotropy of tissue-specific growth factors: from neurons to vessels via the bone marrow. J. Clin. Invest. 115, 596-598 (2005).
141. Drevs, J. et al. Phase I clinical evaluation of AZD2171, a highly potent VEGF receptor tyrosine kinase inhibitor, in patients with advanced tumors. J. Clin. Oncol. 23, Abstr. 3002 (2005).
142. Drevs, J. et al. Soluble markers for the assessment of biological activity with PTK787/ZK 222584 (PTK/ZK), a vascular endothelial growth factor receptor (VEGFR) tyrosine kinase inhibitor in patients with advanced colorectal cancer from two phase I trials. Ann. Oncol. 16, 558-565 (2005).
143. Motzer, R. J. et al. Activity of SU11248, a multitargeted inhibitor of vascular endothelial growth factor receptor and platelet-derived growth factor receptor, in patients with metastatic renal cell carcinoma. J. Clin. Oncol. 24, 16-24 (2006).
144. Willett, C. G. et al. Surrogate markers for antiangiogenic therapy and dose-limiting toxicities for bevacizumab with radiation and chemotherapy: continued experience of a phase I trial in rectal cancer patients. J. Clin. Oncol. 23, 8136-8139 (2005).
145. Dowlati, A. et al. Prospective correlative assessment of biomarkers in E4599 randomized phase II/III trial of carboplatin and paclitaxel ± bevacizumab in advanced non-small cell lung cancer (NSCLC). J. Clin. Oncol. 24S, 7027 (2006).
146. Sandler, A. et al. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer. N. Engl. J. Med. 355, 2542-2550 (2006).
147. Stratmann, A., Risau, W. & Plate, K. H. Cell type-specific expression of angiopoietin-1 and angiopoietin-2 suggests a role in glioblastoma angiogenesis. Am. J. Pathol. 153, 1459-1466 (1998).
148. Nagy, J. A. et al. VEGF-A induces angiogenesis, arteriogenesis, lymphangiogenesis, and vascular malformations. Cold Spring Harb. Symp. Quant. Biol. 67, 227-237 (2002).
149. Provenzale, J. M. et al. Correlation of relative permeability and relative cerebral blood volume in high-grade cerebral neoplasms. AJR Am. J. Roentgenol. 187, 1036-1042 (2006).
150. Provenzale, J. M., Mukundan, S. & Barboriak, D. P. Diffusion-weighted and perfusion MR imaging for brain tumor characterization and assessment of treatment response. Radiology 239, 632-649 (2006).