Lessons from phase III clinical trials on anti-VEGF therapy for cancer (original) (raw)

• Folkman J (1971) Tumor angiogenesis: therapeutic implications. N Engl J Med 285: 1182–1186
  Article CAS PubMed Google Scholar
• Carmeliet P and Jain RK (2000) Angiogenesis in cancer and other diseases. Nature 407: 249–257
  Article CAS PubMed Google Scholar
• Dvorak HF (2002) 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
  Article CAS PubMed Google Scholar
• Kerbel R and Folkman J (2002) Clinical translation of angiogenesis inhibitors. Nat Rev Cancer 2: 727–739
  Article CAS PubMed Google Scholar
• Ferrara N et al. (2004) Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat Rev Drug Discov 3: 391–400
  Article CAS PubMed Google Scholar
• Carmeliet P (2005) Angiogenesis in life, disease and medicine. Nature 438: 932–936
  Article CAS PubMed Google Scholar
• Jain RK (2005) Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307: 58–62
  Article CAS PubMed Google Scholar
• Bevacizumab (Avastin™) for Treatment of Solid Tumors: NCI Fact Sheet [http://www.cancer.gov/cancertopics/factsheet/AvastinFactSheet] (accessed in 24 November 2005)
• Hurwitz H et al. (2004) Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med 350: 2335–2342
  Article CAS PubMed Google Scholar
• Miller KD et al. (2005) Randomized phase III trial of capecitabine compared with bevacizumab plus capecitabine in patients with previously treated metastatic breast cancer. J Clin Oncol 23: 792–799
  Article CAS PubMed Google Scholar
• [No authors listed] News in Brief (2005) Nat Rev Drug Discov 4: 448–449
• Rini BI et al. (2005) Therapy targeted at vascular endothelial growth factor in metastatic renal cell carcinoma: biology, clinical results and future development. BJU Int 96: 286–290
  Article CAS PubMed Google Scholar
• Branca MA (2005) Multi-kinase inhibitors create buzz at ASCO. Nat Biotechnol 23: 639
  Article CAS PubMed Google Scholar
• Fukumura D et al. (1998) Tumor induction of VEGF promoter activity in stromal cells. Cell 94: 715–725
  Article CAS PubMed Google Scholar
• Rafii S et al. (2002) Vascular and haematopoietic stem cells: novel targets for anti-angiogenesis therapy? Nat Rev Cancer 2: 826–835
  Article CAS PubMed Google Scholar
• Ferrara N et al. (2003) The biology of VEGF and its receptors. Nat Med 9: 669–676
  Article CAS PubMed Google Scholar
• Gorski DH et al. (1999) Blockage of the vascular endothelial growth factor stress response increases the antitumor effects of ionizing radiation. Cancer Res 59: 3374–3378
  CAS PubMed Google Scholar
• Bocci G et al. (2004) Increased plasma vascular endothelial growth factor (VEGF) as a surrogate marker for optimal therapeutic dosing of VEGF receptor-2 monoclonal antibodies. Cancer Res 64: 6616–6625
  Article CAS PubMed Google Scholar
• Willett CG et al. (2005) 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
  Article PubMed Google Scholar
• Willett CG et al. (2004) Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med 10: 145–147
  Article CAS PubMed PubMed Central Google Scholar
• Sandler AB (2005) Clinical trials comparing carboplatin/paclitaxel with or without bevacizumab in patients with metastatic NSCLC. Lung Cancer Update 2: 6–10
  Google Scholar
• Tuma RS (2005) Success of bevacizumab trials raises questions for future studies. J Natl Cancer Inst 97: 950–951
  Article PubMed Google Scholar
• Chen HX (2004) Expanding the clinical development of bevacizumab. Oncologist 9 (Suppl 1): S27–S35
  Article Google Scholar
• Rosen LS (2005) VEGF-targeted therapy: therapeutic potential and recent advances. Oncologist 10: 382–391
  Article CAS PubMed Google Scholar
• Eskens FA (2004) Angiogenesis inhibitors in clinical development; where are we now and where are we going? Br J Cancer 90: 1–7
  Article CAS PubMed PubMed Central Google Scholar
• Mross K et al. (2005) Phase I clinical and pharmacokinetic study of PTK/ZK, a multiple VEGF receptor inhibitor, in patients with liver metastases from solid tumours. Eur J Cancer 41: 1291–1299
  Article CAS PubMed Google Scholar
• Hecht JR et al. (2005) A randomized, double-blind, placebo-controlled, phase III study in patients with metastatic adenocarcinoma of the colon or rectum receiving first-line chemotherapy with oxaliplatin/5-fluorouracil/leucovorin and PTK787/ZK222584 or placebo [abstract]. J Clin Oncol 23: LBA3
  Article Google Scholar
• Wilhelm SM et al. (2004) BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res 64: 7099–7109
  Article CAS PubMed Google Scholar
• Marx J (2005) Cancer. Encouraging results for second-generation antiangiogenesis drugs. Science 308: 1248–1249
  Article CAS PubMed Google Scholar
• Beaumont J et al. (2005) Patient reported outcomes in a phase 2 trial of SU11248 for metastatic renal cell carcinoma [abstract #8167]. Proc Am Soc Clin Oncol
• Slamon DJ et al. (2001) Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med 344: 783–792
  Article CAS PubMed Google Scholar
• Piccart-Gebhart MJ et al. (2005) Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med 353: 1659–1672
  Article CAS PubMed Google Scholar
• Romond EH et al. (2005) Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N Engl J Med 353: 1673–1684
  Article CAS PubMed Google Scholar
• Clark JW et al. (2005) Safety and pharmacokinetics of the dual action raf kinase and vascular endothelial growth factor receptor inhibitor, BAY 43-9006, in patients with advanced, refractory solid tumors. Clin Cancer Res 11: 5472–5480
  Article CAS PubMed Google Scholar
• Midgley R and Kerr D (2005) Bevacizumab—current status and future directions. Ann Oncol 16: 999–1004
  Article PubMed Google Scholar
• Moore M et al. (2005) Phase I study to determine the safety and pharmacokinetics of the novel Raf kinase and VEGFR inhibitor BAY 43-9006, administered for 28 days on/7 days off in patients with advanced, refractory solid tumors. Ann Oncol 16: 1688–1694
  Article CAS PubMed Google Scholar
• Motzer RJ et al. (2005) Phase 2 trials of SU11248 show antitumor activity in second-line therapy for patients with metastatic renal cell carcinoma (RCC) [abstract #4508]. Proc Am Soc Clin Oncol
• Thomas AL et al. (2005) Phase I study of the safety, tolerability, pharmacokinetics, and pharmacodynamics of PTK787/ZK 222584 administered twice daily in patients with advanced cancer. J Clin Oncol 23: 4162–4171
  Article CAS PubMed Google Scholar
• Teicher BA (1996) A systems approach to cancer therapy. (Antioncogenics + standard cytotoxics—>mechanism(s) of interaction). Cancer Metastasis Rev 15: 247–272
  Article CAS PubMed Google Scholar
• Jain RK (2005) Antiangiogenic therapy for cancer: current and emerging concepts. Oncology (Williston Park) 19 (Suppl): S7–S16
  Google Scholar
• Jain RK (2001) Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat Med 7: 987–989
  Article CAS PubMed Google Scholar
• Winkler F et al. (2004) 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
  CAS PubMed Google Scholar
• Ansiaux R et al. (2005) Thalidomide radiosensitizes tumors through early changes in the tumor microenvironment. Clin Cancer Res 11: 743–750
  CAS PubMed Google Scholar
• Huber PE et al. (2005) Trimodal cancer treatment: beneficial effects of combined antiangiogenesis, radiation, and chemotherapy. Cancer Res 65: 3643–3655
  Article CAS PubMed Google Scholar
• Salnikov AV et al. (2005) Inhibition of TGF-beta modulates macrophages and vessel maturation in parallel to a lowering of interstitial fluid pressure in experimental carcinoma. Lab Invest 85: 512–521
  Article CAS PubMed Google Scholar
• Tong RT et al. (2004) 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
  Article CAS PubMed Google Scholar
• Vosseler S et al. (2005) Angiogenesis inhibition by vascular endothelial growth factor receptor-2 blockade reduces stromal matrix metalloproteinase expression, normalizes stromal tissue, and reverts epithelial tumor phenotype in surface heterotransplants. Cancer Res 65: 1294–1305
  Article CAS PubMed Google Scholar
• Wildiers H et al. (2003) Effect of antivascular endothelial growth factor treatment on the intratumoral uptake of CPT-11. Br J Cancer 88: 1979–1986
  Article CAS PubMed PubMed Central Google Scholar
• Segers J et al.: Potentiation of cyclophosphamide chemotherapy using the antiangiogenic drug thalidomide: importance of optimal scheduling to exploit the normalization window of the tumor vasculature. Cancer Lett, in press
• Morgan B et al. (2003) Dynamic contrast-enhanced magnetic resonance imaging as a biomarker for the pharmacological response of PTK787/ZK 222584, an inhibitor of the vascular endothelial growth factor receptor tyrosine kinases, in patients with advanced colorectal cancer and liver metastases: results from two phase I studies. J Clin Oncol 21: 3955–3964
  Article CAS PubMed Google Scholar
• Jain RK (2003) Molecular regulation of vessel maturation. Nat Med 9: 685–693
  Article CAS PubMed Google Scholar
• Izumi Y et al. (2002) Tumour biology: herceptin acts as an anti-angiogenic cocktail. Nature 416: 279–280
  Article CAS PubMed Google Scholar
• Saltz LB et al. (2005) Randomized Phase II trial of Cetuximab/Bevacizumab/Irinotecan (CBI) versus Cetuximab/Bevacizumab (CB) in Irinotecan-refractory colorectal cancer [abstract #3508]. Proc Am Soc Clin Oncol
• Herbst RS et al. (2005) Phase I/II trial evaluating the anti-vascular endothelial growth factor monoclonal antibody bevacizumab in combination with the HER-1/epidermal growth factor receptor tyrosine kinase inhibitor erlotinib for patients with recurrent non-small-cell lung cancer. J Clin Oncol 23: 2544–2555
  Article CAS PubMed Google Scholar
• Hudis CA (2005) Clinical implications of antiangiogenic therapies. Oncology (Williston Park) 19 (Suppl): 26–31
  Google Scholar
• Kim JJ and Tannock IF (2005) Repopulation of cancer cells during therapy: an important cause of treatment failure. Nat Rev Cancer 5: 516–525
  Article CAS PubMed Google Scholar
• Browder T et al. (2000) Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. Cancer Res 60: 1878–1886
  CAS PubMed Google Scholar
• Kerbel RS and Kamen BA (2004) The anti-angiogenic basis of metronomic chemotherapy. Nat Rev Cancer 4: 423–436
  Article CAS PubMed Google Scholar
• Garcia-Barros M et al. (2003) Tumor response to radiotherapy regulated by endothelial cell apoptosis. Science 300: 1155–1159
  Article CAS PubMed Google Scholar
• Ch'ang HJ et al. (2005) ATM regulates target switching to escalating doses of radiation in the intestines. Nat Med 11: 484–490
  Article CAS PubMed Google Scholar
• Wey JS et al. (2005) Vascular endothelial growth factor receptor-1 promotes migration and invasion in pancreatic carcinoma cell lines. Cancer 104: 427–438
  Article CAS PubMed Google Scholar
• Fan F et al. (2005) Expression and function of vascular endothelial growth factor receptor-1 on human colorectal cancer cells. Oncogene 24: 2647–2653
  Article CAS PubMed Google Scholar
• Akagi M et al. (2003) Induction of neuropilin-1 and vascular endothelial growth factor by epidermal growth factor in human gastric cancer cells. Br J Cancer 88: 796–802
  Article CAS PubMed PubMed Central Google Scholar
• Bachelder RE et al. (2001) Vascular endothelial growth factor is an autocrine survival factor for neuropilin-expressing breast carcinoma cells. Cancer Res 61: 5736–5740
  CAS PubMed Google Scholar
• Klagsbrun, M et al. (2002) The role of neuropilin in vascular and tumor biology. Adv Exp Med Biol 515: 33–48
  Article CAS PubMed Google Scholar
• Kabbinavar F et al. (2003) Phase II, randomized trial comparing bevacizumab plus fluorouracil (FU)/leucovorin (LV) with FU/LV alone in patients with metastatic colorectal cancer. J Clin Oncol 21: 60–65
  Article CAS PubMed Google Scholar
• Ince WL et al. (2005) Association of k-ras, b-raf, and p53 status with the treatment effect of bevacizumab. J Natl Cancer Inst 97: 981–989
  Article CAS PubMed Google Scholar
• Jubb AM et al. Impact of vascular endothelial growth factor-A expression, thrombospondin 2 expression, and microvessel density on the treatment effect of bevacizumab in metastatic colorectal cancer. J Clin Oncol, in press
• Park JW et al. (2004) Rationale for biomarkers and surrogate end points in mechanism-driven oncology drug development. Clin Cancer Res 10: 3885–3896
  Article CAS PubMed Google Scholar
• Boucher Y et al. (1991) Interstitial hypertension in superficial metastatic melanomas in humans. Cancer Res 51: 6691–6694
  CAS PubMed Google Scholar
• Boucher Y et al. (1997) Interstitial fluid pressure in intracranial tumours in patients and in rodents. Br J Cancer 75: 829–836
  Article CAS PubMed PubMed Central Google Scholar
• Gutmann R et al. (1992) Interstitial hypertension in head and neck tumors in patients: correlation with tumor size. Cancer Res 52: 1993–1995
  CAS PubMed Google Scholar
• Less JR et al. (1992) Interstitial hypertension in human breast and colorectal tumors. Cancer Res 52: 6371–6374
  CAS PubMed Google Scholar
• Milosevic M et al. (2001) Interstitial fluid pressure predicts survival in patients with cervix cancer independent of clinical prognostic factors and tumor oxygen measurements. Cancer Res 61: 6400–6405
  CAS PubMed Google Scholar
• Nathanson SD and Nelson L (1994) Interstitial fluid pressure in breast cancer, benign breast conditions, and breast parenchyma. Ann Surg Oncol 1: 333–338
  Article CAS PubMed Google Scholar
• Padera T et al. (2002) Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 296: 1883–1886
  Article CAS PubMed Google Scholar
• Roh HD et al. (1991) Interstitial hypertension in carcinoma of uterine cervix in patients: possible correlation with tumor oxygenation and radiation response. Cancer Res 51: 6695–6698
  CAS PubMed Google Scholar
• Dunst J et al. (1998) A 2-week pretreatment with 13-cis-retinoic acid + interferon-alpha-2a prior to definitive radiation improves tumor tissue oxygenation in cervical cancers. Strahlenther Onkol 174: 571–574
  Article CAS PubMed Google Scholar
• Verheul HM and Pinedo HM (1998) Tumor growth: a putative role for platelets? Oncologist 3: 2
  Google Scholar
• Beaudry P et al. (2005) 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 11: 3514–3522
  Article CAS PubMed Google Scholar
• Bertolini F et al. (2003) Maximum tolerable dose and low-dose metronomic chemotherapy have opposite effects on the mobilization and viability of circulating endothelial progenitor cells. Cancer Res 63: 4342–4346
  CAS PubMed Google Scholar
• Shaked Y et al. (2005) Genetic heterogeneity of the vasculogenic phenotype parallels angiogenesis; Implications for cellular surrogate marker analysis of antiangiogenesis. Cancer Cell 7: 101–111
  CAS PubMed Google Scholar
• Collins JM (2005) Imaging and other biomarkers in early clinical studies: one step at a time or re-engineering drug development? J Clin Oncol 23: 5417–5419
  Article PubMed Google Scholar
• Jennens RR et al. (2004) Complete radiological and metabolic response of metastatic renal cell carcinoma to SU5416 (semaxanib) in a patient with probable von Hippel-Lindau syndrome. Urol Oncol 22: 193–196
  Article PubMed Google Scholar
• Liu G et al. (2005) Dynamic contrast-enhanced magnetic resonance imaging as a pharmacodynamic measure of response after acute dosing of AG-013736, an oral angiogenesis inhibitor, in patients with advanced solid tumors: results from a phase I study. J Clin Oncol 23: 5464–5473
  Article CAS PubMed Google Scholar
• Miller JC et al. (2005) Imaging angiogenesis: applications and potential for drug development. J Natl Cancer Inst 97: 172–187
  Article CAS PubMed Google Scholar
• Chan LW et al. (2004) Urinary VEGF and MMP levels as predictive markers of 1-year progression-free survival in cancer patients treated with radiation therapy: a longitudinal study of protein kinetics throughout tumor progression and therapy. J Clin Oncol 22: 499–506
  Article CAS PubMed Google Scholar
• Moses MA et al. (1998) Increased incidence of matrix metalloproteinases in urine of cancer patients. Cancer Res 58: 1395–1399
  CAS PubMed Google Scholar
• Roy R et al. (2004) ADAM 12 cleaves extracellular matrix proteins and correlates with cancer status and stage. J Biol Chem 279: 51323–51330
  Article CAS PubMed Google Scholar
• Rugo HS et al. (2005) Phase I trial of the oral antiangiogenesis agent AG-013736 in patients with advanced solid tumors: pharmacokinetic and clinical results. J Clin Oncol 23: 5474–5483
  Article CAS PubMed Google Scholar
• McShane LM et al. (2005) Identification of clinically useful cancer prognostic factors: what are we missing? J Natl Cancer Inst 97: 1023–1025
  Article PubMed Google Scholar
• Mundhenke C et al. (2001) Tissue examination to monitor antiangiogenic therapy: a phase I clinical trial with endostatin. Clin Cancer Res 7: 3366–3374
  CAS PubMed Google Scholar
• Blann AD et al. (2005) Circulating endothelial cells. Biomarker of vascular disease. Thromb Haemost 93: 228–235
  Article CAS PubMed Google Scholar
• Kraft A et al. (1999) Vascular endothelial growth factor in the sera and effusions of patients with malignant and nonmalignant disease. Cancer 85: 178–187
  Article CAS PubMed Google Scholar
• Sack U et al. (2005) Vascular endothelial growth factor in pleural effusions of different origin. Eur Respir J 25: 600–604
  Article CAS PubMed Google Scholar