Review
You have free access to this content
Anti-angiogenesis and metastasis: a tumour and stromal cell alliance
Article first published online: 19 JAN 2013
DOI: 10.1111/joim.12018
© 2012 The Association for the Publication of the Journal of Internal Medicine
Additional Information
How to Cite
, Catalan Institute of Oncology – IDIBELL, Spain. Anti-angiogenesis and metastasis: a tumour and stromal cell alliance (Review). J Intern Med 2013; 273: 128–137.
Publication History
- Issue published online: 19 JAN 2013
- Article first published online: 19 JAN 2013
- Accepted manuscript online: 30 NOV 2012 07:47AM EST
Funded by
- European Union-Framework Programme 7. Grant Numbers: EU-FP7, ERC-StG-281830
- MinEco-Spain. Grant Numbers: SAF2009-08375, RTICC-RD2006-0092
- AGAUR-Generalitat. Grant Number: SGR681
References
- 1. VEGF as a key mediator of angiogenesis in cancer. Oncology 2005; 69(Suppl 3): 4–10.
- 2, . Antiangiogenic therapy: impact on invasion, disease progression, and metastasis. Nat Rev Clin Onco 2011; 8: 210–21.
- 3, . Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer 2008; 8: 592–603.
- 4, , , , , . Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis. Cancer Cell 2009; 15: 232–9.
- 5, , et al. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis. Cancer Cell 2009; 15: 220–31.
- 6, , et al. Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors. Cancer Discov 2012; 2: 270–87.
- 7, . Hallmarks of cancer: the next generation. Cell 2011; 144: 646–74.
- 8, . The hallmarks of cancer. Cell 2000; 100: 57–70.
- 9, . Pericytes: gatekeepers in tumour cell metastasis? J Mol Med (Berl) 2008; 86: 135–44.
- 10, , et al. Pericytes limit tumor cell metastasis. J Clin Invest 2006; 116: 642–51.
- 11. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005; 307: 58–62.
- 12, , et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature 2005; 438: 820–7.
- 13, . VEGF-targeted therapy: mechanisms of anti-tumour activity. Nat Rev Cancer 2008; 8: 579–91.
- 14, , . Mechanisms of resistance to antiangiogenesis therapy. Eur J Cancer 2010; 46: 1323–32.
- 15
- 16, . Role of the hypoxic tumor microenvironment in the resistance to anti-angiogenic therapies. Drug Resist Updat 2009; 12: 74–80.
- 17, , . Angiogenesis as a strategic target for ovarian cancer therapy. Nat Clin Pract Oncol 2008; 5: 194–204.
- 18, . Anticancer strategies involving the vasculature. Nat Rev Clin Oncol 2009; 6: 395–404.
- 19. Hypoxia and cancer. Cancer Metastasis Rev 2007; 26: 223–4.
- 20, . Hypoxia and hypoxia-inducible factors: master regulators of metastasis. Clin Cancer Res 2010; 16: 5928–35.
- 21, , . Antiangiogenic therapy, hypoxia, and metastasis: risky liaisons, or not? Nat Rev Clin Oncol 2011; 8: 393–404.
- 22, , , . Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors. Cancer Cell 2005; 8: 299–309.
- 23, , et al. Hypoxia generates a more invasive phenotype of tumour cells: an in vivo experimental setup based on the chorioallantoic membrane. Pathol Oncol Res 2009; 15: 417–22.
- 24, , , , , . Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene. Cancer Cell 2003; 3: 347–61.
- 25, . MET receptor tyrosine kinase as a therapeutic anticancer target. Cancer Lett 2009; 280: 1–14.
- 26, , et al. VEGF inhibits tumor cell invasion and Mesenchymal transition through a MET/VEGFR2 Complex. Cancer Cell 2012; 22: 21–35.
- 27, , , , . HGF/c-Met pathway is one of the mediators of sunitinib-induced tumor cell type-dependent metastasis. Cancer Lett 2012; 320: 48–55.
- 28, , et al. Tumor-stromal cell interaction under hypoxia increases the invasiveness of pancreatic cancer cells through the hepatocyte growth factor/c-Met pathway. Int J Cancer 2006; 119: 2750–9.
- 29, . Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 2003; 3: 362–74.
- 30, , . Integrin-mediated adhesion regulates cell polarity and membrane protrusion through the Rho family of GTPases. Mol Biol Cell 2001; 12: 265–77.
- 31, . Mechanisms of collective cell migration at a glance. J Cell Sci 2009; 122: 3203–8.
- 32, . Cancer invasion and the microenvironment: plasticity and reciprocity. Cell 2011; 147: 992–1009.
- 33, . Cancer dissemination–lessons from leukocytes. Dev Cell 2010; 19: 13–26.
- 34
- 35, . Microenvironmental regulation of metastasis. Nat Rev Cancer 2009; 9: 239–52.
- 36, , , , . Inflammation-mediated promotion of invasion and metastasis. Cancer Metastasis Rev 2010; 29: 243–8.
- 37, , et al. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 2007; 11: 83–95.
- 38. Endothelial cells form a phalanx to block tumor metastasis. Cell 2009; 136: 810–2.
- 39, , et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 2009; 136: 839–51.
- 40, , et al. Semaphorin 3A overcomes cancer hypoxia and metastatic dissemination induced by antiangiogenic treatment in mice. J Clin Invest 2012; 122: 1832–48.
- 41, , et al. Semaphorin 3A is an endogenous angiogenesis inhibitor that blocks tumor growth and normalizes tumor vasculature in transgenic mouse models. J Clin Invest 2009; 119: 3356–72.
- 42, . Graded hypoxia modulates the invasive potential of HT1080 fibrosarcoma and MDA MB231 carcinoma cells. Clin Exp Metastasis 2008; 25: 253–64.
- 43, , et al. The hypoxic response of tumors is dependent on their microenvironment. Cancer Cell 2003; 4: 133–46.
- 44, , et al. Tumour growth inhibition and anti-metastatic activity of a mutated furin-resistant Semaphorin 3E isoform. EMBO Mol Med 2012; 4: 234–50.
- 45, . Exploiting pleiotropic activities of semaphorins as multi-target therapies for cancer. EMBO Mol Med 2012; 4: 168–70.
- 46, , et al. Differential drug-class specific metastatic effects following treatment with a panel of angiogenesis inhibitors. J Pathol 2012; 227: 404–16.
- 47, , et al. Anti-VEGF antibody therapy does not promote metastasis in genetically engineered mouse tumor models. J Pathol 2012; 227: 417–30.
- 48, , , , . Benefits of targeting both pericytes and endothelial cells in the tumor vasculature with kinase inhibitors. J Clin Invest 2003; 111: 1287–95.
- 49
- 50, . Double target for tumor mass destruction. J Clin Invest 2003; 111: 1277–80.
- 51, . Targeted therapies: Sunitinib versus interferon-alpha in metastatic RCC. Nat Rev Clin Oncol 2009; 7: 7–8.
- 52, , et al. Progression-free survival as a clinical trial endpoint in advanced renal cell carcinoma. Curr Oncol 2011; 18(Suppl 2): S11–9.
- 53, , , . Molecular basis for sunitinib efficacy and future clinical development. Nat Rev Drug Discov 2007; 6: 734–45.
- 54, , , . The clinical implications of the genetics of renal cell carcinoma. Urol Oncol 2009; 27: 131–6.
- 55, , , , . Fas/Fas ligand interaction in human colorectal hepatic metastases: A mechanism of hepatocyte destruction to facilitate local tumor invasion. Am J Pathol 1999; 154: 693–703.
- 56, , . Genetic modulation of hypoxia induced gene expression and angiogenesis: relevance to brain tumors. Front Biosci 2003; 8: d100–16.
- 57, , . Antiangiogenic therapies for high-grade glioma. Nat Rev Neurol 2009; 5: 610–20.
- 58, , et al. Efficacy, safety and patterns of response and recurrence in patients with recurrent high-grade gliomas treated with bevacizumab plus irinotecan. J Neurooncol 2009; 91: 329–36.
- 59, , et al. Bevacizumab plus interferon alfa-2a for treatment of metastatic renal cell carcinoma: a randomised, double-blind phase III trial. Lancet 2007; 370: 2103–11.
- 60, , et al. Sunitinib versus interferon alfa in metastatic renal-cell carcinoma. N Engl J Med 2007; 356: 115–24.
- 61, , et al. Phase III randomized trial of conventional-dose chemotherapy with or without high-dose chemotherapy and autologous hematopoietic stem-cell rescue as first-line treatment for patients with poor-prognosis metastatic germ cell tumors. J Clin Oncol 2007; 25: 247–56.
- 62, , et al. Bevacizumab plus interferon alfa compared with interferon alfa monotherapy in patients with metastatic renal cell carcinoma: CALGB 90206. J Clin Oncol 2008; 26: 5422–8.
- 63, , , , . Patterns of disease progression in metastatic renal cell carcinoma patients treated with antivascular agents and interferon: impact of therapy on recurrence patterns and outcome measures. Cancer 2009; 115: 1859–66.
- 64, , et al. Disease course patterns after discontinuation of bevacizumab: pooled analysis of randomized phase III trials. J Clin Oncol 2011; 29: 83–8.
- 65. Is the postprogression survival time really not shortened in the bevacizumab-containing arms of phase III clinical trials? J Clin Oncol 2011; 29: e384–5; author reply e6.
- 66, , et al. Understanding the “lethal” drivers of tumor-stroma co-evolution: emerging role(s) for hypoxia, oxidative stress and autophagy/mitophagy in the tumor micro-environment. Cancer Biol Ther 2010; 10: 537–42.
- 67, , et al. Cancer cells metabolically “fertilize” the tumor microenvironment with hydrogen peroxide, driving the Warburg effect: implications for PET imaging of human tumors. Cell Cycle 2011; 10: 2504–20.

1365-2796/asset/olbannerleft.gif?v=1&s=2c0da92fd7dd29d6387a79c865c2e722951f9b9b)
1365-2796/asset/olbannercenter.gif?v=1&s=e1b4b2f8709bbf2cd315f2b365ae538cedfe9fdf)
1365-2796/asset/olbannerright.gif?v=1&s=99fa1da70758a077581e13cbfc3cd514826924d8)
