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PMID: 22525710 Published · epublish English Journal Article Research Support, N.I.H., Extramural Review

Overcoming disappointing results with antiangiogenic therapy by targeting hypoxia.

Nature reviews. Clinical oncology ·Vol. 9 ·No. 7 ·2012-04-24 ·Pages 378-90

Rapisarda A, Melillo G

Abstract

Cancer cells rely on angiogenesis to fulfil their need for oxygen and nutrients; hence, agents targeting angiogenic pathways and mediators have been investigated as potential cancer drugs. Although this strategy has demonstrated delayed tumour progression--leading to progression-free survival and overall survival benefits compared with standard therapy--in some patients, the results are more modest than predicted. A significant number of patients either do not respond to antiangiogenic agents or fairly rapidly develop resistance to them, which raises questions about how resistance develops and how it can be overcome. Furthermore, whether cancers, once they develop resistance, become more invasive or lead to metastatic disease remains unclear. Several mechanisms of resistance have been recently proposed and emerging evidence indicates that, under certain experimental conditions, antiangiogenic agents increase intratumour hypoxia by promoting vessel pruning and inhibiting neoangiogenesis. Indeed, several studies have highlighted the possibility that inhibitors of VEGF (and its receptors) can promote an invasive metastatic switch, in part by creating an increasingly hypoxic tumour microenvironment. As a potential remedy, a number of therapeutic approaches have been investigated that target the hypoxic tumour compartment to improve the clinical outcome of antiangiogenic therapy.

MeSH Terms
Angiogenesis Inhibitors/therapeutic use Animals Drug Resistance, Neoplasm/drug effects Humans Hypoxia/drug therapy Neoplasms/blood supply,drug therapy Neovascularization, Pathologic/drug therapy
Chemicals
Angiogenesis Inhibitors
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Rapisarda Annamaria
SAIC-Frederick Inc., Frederick National Laboratory for Cancer Research, 1050 Boyles Street, Frederick, MD 21702, USA.
Melillo Giovanni
References (149)
149 references, click to expand
  1. Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability.
    Nat Rev Cancer. 2008 Mar;8(3):180-92 PMID: 18273037
  2. Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma.
    Proc Natl Acad Sci U S A. 2011 Mar 1;108(9):3749-54 PMID: 21321221
  3. CXCL12 / CXCR4 / CXCR7 chemokine axis and cancer progression.
    Cancer Metastasis Rev. 2010 Dec;29(4):709-22 PMID: 20839032
  4. Antiangiogenic and radiation therapy: early effects on in vivo computed tomography perfusion parameters in human colon cancer xenografts in mice.
    Invest Radiol. 2012 Jan;47(1):25-32 PMID: 22178893
  5. Regulation of angiogenesis by hypoxia-inducible factor 1.
    Crit Rev Oncol Hematol. 2006 Jul;59(1):15-26 PMID: 16716598
  6. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1.
    Nat Med. 2004 Aug;10(8):858-64 PMID: 15235597
  7. Sorafenib in advanced hepatocellular carcinoma.
    N Engl J Med. 2008 Jul 24;359(4):378-90 PMID: 18650514
  8. Sunitinib malate for the treatment of pancreatic neuroendocrine tumors.
    N Engl J Med. 2011 Feb 10;364(6):501-13 PMID: 21306237
  9. CXCL12 (SDF1alpha)-CXCR4/CXCR7 pathway inhibition: an emerging sensitizer for anticancer therapies?
    Clin Cancer Res. 2011 Apr 15;17(8):2074-80 PMID: 21349998
  10. Accelerated metastasis after short-term treatment with a potent inhibitor of tumor angiogenesis.
    Cancer Cell. 2009 Mar 3;15(3):232-9 PMID: 19249681
  11. Targeting GLUT1 and the Warburg effect in renal cell carcinoma by chemical synthetic lethality.
    Sci Transl Med. 2011 Aug 3;3(94):94ra70 PMID: 21813754
  12. FDA drug approval summary: bevacizumab (Avastin) as treatment of recurrent glioblastoma multiforme.
    Oncologist. 2009 Nov;14(11):1131-8 PMID: 19897538
  13. Human cancers converge at the HIF-2alpha oncogenic axis.
    Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21306-11 PMID: 19955413
  14. Bevacizumab plus irinotecan in recurrent glioblastoma multiforme.
    J Clin Oncol. 2007 Oct 20;25(30):4722-9 PMID: 17947719
  15. Therapy-induced acute recruitment of circulating endothelial progenitor cells to tumors.
    Science. 2006 Sep 22;313(5794):1785-7 PMID: 16990548
  16. Gemcitabine plus bevacizumab compared with gemcitabine plus placebo in patients with advanced pancreatic cancer: phase III trial of the Cancer and Leukemia Group B (CALGB 80303).
    J Clin Oncol. 2010 Aug 1;28(22):3617-22 PMID: 20606091
  17. VEGF-targeted therapy: mechanisms of anti-tumour activity.
    Nat Rev Cancer. 2008 Aug;8(8):579-91 PMID: 18596824
  18. Glucose deprivation-induced metabolic oxidative stress and cancer therapy.
    J Cancer Res Ther. 2009 Sep;5 Suppl 1:S2-6 PMID: 20009288
  19. Principles and mechanisms of vessel normalization for cancer and other angiogenic diseases.
    Nat Rev Drug Discov. 2011 Jun;10(6):417-27 PMID: 21629292
  20. VEGF and c-Met blockade amplify angiogenesis inhibition in pancreatic islet cancer.
    Cancer Res. 2011 Jul 15;71(14):4758-68 PMID: 21613405
  21. Pazopanib in locally advanced or metastatic renal cell carcinoma: results of a randomized phase III trial.
    J Clin Oncol. 2010 Feb 20;28(6):1061-8 PMID: 20100962
  22. Phase III randomized trial of sunitinib versus capecitabine in patients with previously treated HER2-negative advanced breast cancer.
    Breast Cancer Res Treat. 2010 May;121(1):121-31 PMID: 20339913
  23. Potent and sustained inhibition of HIF-1α and downstream genes by a polyethyleneglycol-SN38 conjugate, EZN-2208, results in anti-angiogenic effects.
    Angiogenesis. 2011 Sep;14(3):245-53 PMID: 21452059
  24. Paclitaxel-carboplatin alone or with bevacizumab for non-small-cell lung cancer.
    N Engl J Med. 2006 Dec 14;355(24):2542-50 PMID: 17167137
  25. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer.
    N Engl J Med. 2004 Jun 3;350(23):2335-42 PMID: 15175435
  26. Homologous recombination is the principal pathway for the repair of DNA damage induced by tirapazamine in mammalian cells.
    Cancer Res. 2008 Jan 1;68(1):257-65 PMID: 18172318
  27. Approval summary: sunitinib for the treatment of imatinib refractory or intolerant gastrointestinal stromal tumors and advanced renal cell carcinoma.
    Clin Cancer Res. 2007 Mar 1;13(5):1367-73 PMID: 17332278
  28. XBP1 is essential for survival under hypoxic conditions and is required for tumor growth.
    Cancer Res. 2004 Sep 1;64(17):5943-7 PMID: 15342372
  29. Vandetanib plus docetaxel versus docetaxel as second-line treatment for patients with advanced non-small-cell lung cancer (ZODIAC): a double-blind, randomised, phase 3 trial.
    Lancet Oncol. 2010 Jul;11(7):619-26 PMID: 20570559
  30. Bevacizumab in combination with oxaliplatin, fluorouracil, and leucovorin (FOLFOX4) for previously treated metastatic colorectal cancer: results from the Eastern Cooperative Oncology Group Study E3200.
    J Clin Oncol. 2007 Apr 20;25(12):1539-44 PMID: 17442997
  31. Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases.
    Cancer Cell. 2004 Dec;6(6):553-63 PMID: 15607960
  32. Phase III study of bevacizumab plus docetaxel compared with placebo plus docetaxel for the first-line treatment of human epidermal growth factor receptor 2-negative metastatic breast cancer.
    J Clin Oncol. 2010 Jul 10;28(20):3239-47 PMID: 20498403
  33. Anthracycline chemotherapy inhibits HIF-1 transcriptional activity and tumor-induced mobilization of circulating angiogenic cells.
    Proc Natl Acad Sci U S A. 2009 Feb 17;106(7):2353-8 PMID: 19168635
  34. Dynamic contrast-enhanced MRI in clinical trials of antivascular therapies.
    Nat Rev Clin Oncol. 2012 Feb 14;9(3):167-77 PMID: 22330689
  35. Is angiogenesis an organizing principle in biology and medicine?
    J Pediatr Surg. 2007 Jan;42(1):1-11 PMID: 17208533
  36. Tumor refractoriness to anti-VEGF treatment is mediated by CD11b+Gr1+ myeloid cells.
    Nat Biotechnol. 2007 Aug;25(8):911-20 PMID: 17664940
  37. Phase III trial of bevacizumab plus interferon alfa-2a in patients with metastatic renal cell carcinoma (AVOREN): final analysis of overall survival.
    J Clin Oncol. 2010 May 1;28(13):2144-50 PMID: 20368553
  38. Normalization of the vasculature for treatment of cancer and other diseases.
    Physiol Rev. 2011 Jul;91(3):1071-121 PMID: 21742796
  39. Molecular mechanisms for the activity of PX-478, an antitumor inhibitor of the hypoxia-inducible factor-1alpha.
    Mol Cancer Ther. 2008 Jan;7(1):90-100 PMID: 18202012
  40. Pazopanib.
    Nat Rev Drug Discov. 2010 Jan;9(1):17-8 PMID: 20043026
  41. Antiangiogenic therapy for primary liver cancer: correlation of changes in dynamic contrast-enhanced magnetic resonance imaging with tissue hypoxia markers and clinical response.
    Ann Surg Oncol. 2011 Aug;18(8):2192-9 PMID: 21286939
  42. Targeting MET in cancer: rationale and progress.
    Nat Rev Cancer. 2012 Jan 24;12(2):89-103 PMID: 22270953
  43. Hypoxia-inducible factors in stem cells and cancer.
    J Cell Mol Med. 2009 Nov-Dec;13(11-12):4319-28 PMID: 19900215
  44. FLT1 and its ligands VEGFB and PlGF: drug targets for anti-angiogenic therapy?
    Nat Rev Cancer. 2008 Dec;8(12):942-56 PMID: 19029957
  45. Predicting treatment response of malignant gliomas to bevacizumab and irinotecan by imaging proliferation with [18F] fluorothymidine positron emission tomography: a pilot study.
    J Clin Oncol. 2007 Oct 20;25(30):4714-21 PMID: 17947718
  46. The interplay between MYC and HIF in cancer.
    Nat Rev Cancer. 2008 Jan;8(1):51-6 PMID: 18046334
  47. Potential of CXCR4 antagonists for the treatment of metastatic lung cancer.
    Expert Rev Anticancer Ther. 2011 Apr;11(4):621-30 PMID: 21504328
  48. Inhibiting hypoxia-inducible factor 1 for cancer therapy.
    Mol Cancer Res. 2006 Sep;4(9):601-5 PMID: 16940159
  49. Hypoxia-induced lysyl oxidase is a critical mediator of bone marrow cell recruitment to form the premetastatic niche.
    Cancer Cell. 2009 Jan 6;15(1):35-44 PMID: 19111879
  50. Hypoxia--a key regulatory factor in tumour growth.
    Nat Rev Cancer. 2002 Jan;2(1):38-47 PMID: 11902584
  51. Differential response of primary tumor versus lymphatic metastasis to VEGFR-2 and VEGFR-3 kinase inhibitors cediranib and vandetanib.
    Mol Cancer Ther. 2008 Aug;7(8):2272-9 PMID: 18687659
  52. Vandetanib plus pemetrexed for the second-line treatment of advanced non-small-cell lung cancer: a randomized, double-blind phase III trial.
    J Clin Oncol. 2011 Mar 10;29(8):1067-74 PMID: 21282537
  53. HIF-2alpha enhances beta-catenin/TCF-driven transcription by interacting with beta-catenin.
    Cancer Res. 2010 Dec 15;70(24):10101-11 PMID: 21159632
  54. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients.
    Cancer Cell. 2007 Jan;11(1):83-95 PMID: 17222792
  55. Antiangiogenic therapy, hypoxia, and metastasis: risky liaisons, or not?
    Nat Rev Clin Oncol. 2011 May 31;8(7):393-404 PMID: 21629216
  56. Oxygen sensing and the DNA-damage response.
    Curr Opin Cell Biol. 2007 Dec;19(6):680-4 PMID: 18023567
  57. A randomized phase IIIB trial of chemotherapy, bevacizumab, and panitumumab compared with chemotherapy and bevacizumab alone for metastatic colorectal cancer.
    J Clin Oncol. 2009 Feb 10;27(5):672-80 PMID: 19114685
  58. Modes of resistance to anti-angiogenic therapy.
    Nat Rev Cancer. 2008 Aug;8(8):592-603 PMID: 18650835
  59. Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer.
    N Engl J Med. 2007 Dec 27;357(26):2666-76 PMID: 18160686
  60. Glioblastoma recurrence after cediranib therapy in patients: lack of "rebound" revascularization as mode of escape.
    Cancer Res. 2011 Jan 1;71(1):19-28 PMID: 21199795
  61. VEGF and PlGF promote adult vasculogenesis by enhancing EPC recruitment and vessel formation at the site of tumor neovascularization.
    FASEB J. 2006 Jul;20(9):1495-7 PMID: 16754748
  62. Overall survival with cisplatin-gemcitabine and bevacizumab or placebo as first-line therapy for nonsquamous non-small-cell lung cancer: results from a randomised phase III trial (AVAiL).
    Ann Oncol. 2010 Sep;21(9):1804-1809 PMID: 20150572
  63. Development of a cell-based reporter assay for screening of inhibitors of hypoxia-inducible factor 2-induced gene expression.
    J Biomol Screen. 2006 Sep;11(6):678-87 PMID: 16858007
  64. Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha.
    Mol Cell Biol. 2002 Nov;22(21):7405-16 PMID: 12370288
  65. Topoisomerase I-mediated inhibition of hypoxia-inducible factor 1: mechanism and therapeutic implications.
    Cancer Res. 2004 Feb 15;64(4):1475-82 PMID: 14983893
  66. Antiangiogenic therapy elicits malignant progression of tumors to increased local invasion and distant metastasis.
    Cancer Cell. 2009 Mar 3;15(3):220-31 PMID: 19249680
  67. The multifaceted circulating endothelial cell in cancer: towards marker and target identification.
    Nat Rev Cancer. 2006 Nov;6(11):835-45 PMID: 17036040
  68. The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5.
    J Clin Invest. 2010 Jan;120(1):127-41 PMID: 20038797
  69. Aminoflavone, a ligand of the aryl hydrocarbon receptor, inhibits HIF-1alpha expression in an AhR-independent fashion.
    Cancer Res. 2010 Sep 1;70(17):6837-48 PMID: 20736373
  70. Hypoxia-inducible factor-1 target genes as indicators of tumor vessel response to vascular endothelial growth factor inhibition.
    Cancer Res. 2008 Mar 15;68(6):1872-80 PMID: 18339868
  71. Clinical translation of angiogenesis inhibitors.
    Nat Rev Cancer. 2002 Oct;2(10):727-39 PMID: 12360276
  72. Hypoxia and cancer.
    Cancer Metastasis Rev. 2007 Jun;26(2):223-4 PMID: 17404692
  73. Targeting hypoxic cells through the DNA damage response.
    Clin Cancer Res. 2010 Dec 1;16(23):5624-9 PMID: 20876254
  74. Glycolytic enzyme inhibitors in cancer treatment.
    Expert Opin Investig Drugs. 2008 Oct;17(10):1533-45 PMID: 18808312
  75. Hypoxic tumors and their effect on immune cells and cancer therapy.
    Methods Mol Biol. 2010;651:1-29 PMID: 20686957
  76. Mitochondrial complex III is required for hypoxia-induced ROS production and cellular oxygen sensing.
    Cell Metab. 2005 Jun;1(6):401-8 PMID: 16054089
  77. Preferential cytotoxicity of bortezomib toward hypoxic tumor cells via overactivation of endoplasmic reticulum stress pathways.
    Cancer Res. 2008 Nov 15;68(22):9323-30 PMID: 19010906
  78. Role of the hypoxic tumor microenvironment in the resistance to anti-angiogenic therapies.
    Drug Resist Updat. 2009 Jun;12(3):74-80 PMID: 19394890
  79. HIF-1: upstream and downstream of cancer metabolism.
    Curr Opin Genet Dev. 2010 Feb;20(1):51-6 PMID: 19942427
  80. Hypoxia-inducible factors and the response to hypoxic stress.
    Mol Cell. 2010 Oct 22;40(2):294-309 PMID: 20965423
  81. DNA repair pathways as targets for cancer therapy.
    Nat Rev Cancer. 2008 Mar;8(3):193-204 PMID: 18256616
  82. Metabolic microenvironment of tumor cells: a key factor in malignant progression.
    Exp Oncol. 2010 Sep;32(3):125-7 PMID: 21403604
  83. Antiangiogenic therapy: impact on invasion, disease progression, and metastasis.
    Nat Rev Clin Oncol. 2011 Mar 01;8(4):210-21 PMID: 21364524
  84. Increased antitumor activity of bevacizumab in combination with hypoxia inducible factor-1 inhibition.
    Mol Cancer Ther. 2009 Jul;8(7):1867-77 PMID: 19584228
  85. Pharmacokinetic/pharmacodynamic modeling identifies SN30000 and SN29751 as tirapazamine analogues with improved tissue penetration and hypoxic cell killing in tumors.
    Clin Cancer Res. 2010 Oct 15;16(20):4946-57 PMID: 20732963
  86. Anticancer drugs that target metabolism: Is dichloroacetate the new paradigm?
    Int J Cancer. 2011 Mar 1;128(5):1001-8 PMID: 20957634
  87. Phase III trial assessing bevacizumab in stages II and III carcinoma of the colon: results of NSABP protocol C-08.
    J Clin Oncol. 2011 Jan 1;29(1):11-6 PMID: 20940184
  88. Phase III study of carboplatin and paclitaxel alone or with sorafenib in advanced non-small-cell lung cancer.
    J Clin Oncol. 2010 Apr 10;28(11):1835-42 PMID: 20212250
  89. Hypoxia promotes invasive growth by transcriptional activation of the met protooncogene.
    Cancer Cell. 2003 Apr;3(4):347-61 PMID: 12726861
  90. Antiangiogenic agents and HIF-1 inhibitors meet at the crossroads.
    Cell Cycle. 2009 Dec 15;8(24):4040-3 PMID: 19923892
  91. A RNA antagonist of hypoxia-inducible factor-1alpha, EZN-2968, inhibits tumor cell growth.
    Mol Cancer Ther. 2008 Nov;7(11):3598-608 PMID: 18974394
  92. Regulation of autophagy through multiple independent hypoxic signaling pathways.
    Curr Mol Med. 2009 May;9(4):417-24 PMID: 19519399
  93. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours.
    Nature. 1996 Jan 4;379(6560):88-91 PMID: 8538748
  94. Differential effects of the vascular endothelial growth factor receptor inhibitor PTK787/ZK222584 on tumor angiogenesis and tumor lymphangiogenesis.
    Mol Cancer Ther. 2009 Jan;8(1):55-63 PMID: 19139113
  95. Drug resistance by evasion of antiangiogenic targeting of VEGF signaling in late-stage pancreatic islet tumors.
    Cancer Cell. 2005 Oct;8(4):299-309 PMID: 16226705
  96. Multihistology, target-driven pilot trial of oral topotecan as an inhibitor of hypoxia-inducible factor-1α in advanced solid tumors.
    Clin Cancer Res. 2011 Aug 1;17(15):5123-31 PMID: 21673063
  97. RIBBON-2: a randomized, double-blind, placebo-controlled, phase III trial evaluating the efficacy and safety of bevacizumab in combination with chemotherapy for second-line treatment of human epidermal growth factor receptor 2-negative metastatic breast cancer.
    J Clin Oncol. 2011 Nov 10;29(32):4286-93 PMID: 21990397
  98. CXCL12 (SDF-1)/CXCR4 pathway in cancer.
    Clin Cancer Res. 2010 Jun 1;16(11):2927-31 PMID: 20484021
  99. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1 alpha-degradative pathway.
    J Biol Chem. 2002 Aug 16;277(33):29936-44 PMID: 12052835
  100. Schedule-dependent inhibition of hypoxia-inducible factor-1alpha protein accumulation, angiogenesis, and tumor growth by topotecan in U251-HRE glioblastoma xenografts.
    Cancer Res. 2004 Oct 1;64(19):6845-8 PMID: 15466170
  101. Regulation of metabolism by hypoxia-inducible factor 1.
    Cold Spring Harb Symp Quant Biol. 2011;76:347-53 PMID: 21785006
  102. Biomarkers of angiogenesis and their role in the development of VEGF inhibitors.
    Br J Cancer. 2010 Jan 5;102(1):8-18 PMID: 20010945
  103. Non-invasive monitoring of hypoxia-inducible factor activation by optical imaging during antiangiogenic treatment in a xenograft model of ovarian carcinoma.
    Int J Oncol. 2011 Sep;39(3):543-52 PMID: 21667025
  104. Regulation of autophagy by ATF4 in response to severe hypoxia.
    Oncogene. 2010 Aug 5;29(31):4424-35 PMID: 20514020
  105. Antiangiogenic therapy using bevacizumab in recurrent high-grade glioma: impact on local control and patient survival.
    J Neurosurg. 2009 Jan;110(1):173-80 PMID: 18834263
  106. Tumor angiogenesis.
    N Engl J Med. 2008 May 8;358(19):2039-49 PMID: 18463380
  107. Targeting tumor hypoxia: suppression of breast tumor growth and metastasis by novel carbonic anhydrase IX inhibitors.
    Cancer Res. 2011 May 1;71(9):3364-76 PMID: 21415165
  108. Targeting hypoxia in cancer therapy.
    Nat Rev Cancer. 2011 Jun;11(6):393-410 PMID: 21606941
  109. Inhibition of vasculogenesis, but not angiogenesis, prevents the recurrence of glioblastoma after irradiation in mice.
    J Clin Invest. 2010 Mar;120(3):694-705 PMID: 20179352
  110. Hypoxia signalling through mTOR and the unfolded protein response in cancer.
    Nat Rev Cancer. 2008 Nov;8(11):851-64 PMID: 18846101
  111. Targeting SDF-1/CXCR4 to inhibit tumour vasculature for treatment of glioblastomas.
    Br J Cancer. 2011 Jun 7;104(12):1805-9 PMID: 21587260
  112. Increased cell killing by metronidazole and nitrofurazone of hypoxic compared to aerobic mammalian cells.
    Cancer Res. 1976 Mar;36(3):930-6 PMID: 1253180
  113. Phase III trial of vandetanib compared with erlotinib in patients with previously treated advanced non-small-cell lung cancer.
    J Clin Oncol. 2011 Mar 10;29(8):1059-66 PMID: 21282542
  114. Phase III trial of bevacizumab plus interferon alfa versus interferon alfa monotherapy in patients with metastatic renal cell carcinoma: final results of CALGB 90206.
    J Clin Oncol. 2010 May 1;28(13):2137-43 PMID: 20368558
  115. The unique physiology of solid tumors: opportunities (and problems) for cancer therapy.
    Cancer Res. 1998 Apr 1;58(7):1408-16 PMID: 9537241
  116. Antiangiogenic potential of the Mammalian target of rapamycin inhibitor temsirolimus.
    Cancer Res. 2006 Jun 1;66(11):5549-54 PMID: 16740688
  117. Tumour hypoxia induces a metabolic shift causing acidosis: a common feature in cancer.
    J Cell Mol Med. 2010 Apr;14(4):771-94 PMID: 20015196
  118. CCI-779 inhibits rhabdomyosarcoma xenograft growth by an antiangiogenic mechanism linked to the targeting of mTOR/Hif-1alpha/VEGF signaling.
    Neoplasia. 2006 May;8(5):394-401 PMID: 16790088
  119. Avastin-Tarceva combination fails in lung cancer.
    Nat Biotechnol. 2009 Feb;27(2):108-9 PMID: 19204674
  120. Bevacizumab for recurrent malignant gliomas: efficacy, toxicity, and patterns of recurrence.
    Neurology. 2008 Mar 4;70(10):779-87 PMID: 18316689
  121. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia.
    Cell Metab. 2006 Mar;3(3):177-85 PMID: 16517405
  122. Hypoxia-mediated down-regulation of Bid and Bax in tumors occurs via hypoxia-inducible factor 1-dependent and -independent mechanisms and contributes to drug resistance.
    Mol Cell Biol. 2004 Apr;24(7):2875-89 PMID: 15024076
  123. Molecular imaging of hypoxia with radiolabelled agents.
    Eur J Nucl Med Mol Imaging. 2009 Oct;36(10):1674-86 PMID: 19565239
  124. Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumor growth factor beta-1, platelet-derived endothelial cell growth factor, placenta growth factor, and pleiotrophin in human primary breast cancer and its relation to angiogenesis.
    Cancer Res. 1997 Mar 1;57(5):963-9 PMID: 9041202
  125. Imaging the unfolded protein response in primary tumors reveals microenvironments with metabolic variations that predict tumor growth.
    Cancer Res. 2010 Jan 1;70(1):78-88 PMID: 20028872
  126. Marked activity of irinotecan and rapamycin combination toward colon cancer cells in vivo and in vitro is mediated through cooperative modulation of the mammalian target of rapamycin/hypoxia-inducible factor-1alpha axis.
    Clin Cancer Res. 2009 Feb 15;15(4):1297-307 PMID: 19190131
  127. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics.
    Oncogene. 2010 Feb 4;29(5):625-34 PMID: 19946328
  128. Bevacizumab in combination with chemotherapy as first-line therapy in advanced gastric cancer: a randomized, double-blind, placebo-controlled phase III study.
    J Clin Oncol. 2011 Oct 20;29(30):3968-76 PMID: 21844504
  129. Hypoxia, HIF1 and glucose metabolism in the solid tumour.
    Nat Rev Cancer. 2008 Sep;8(9):705-13 PMID: 19143055
  130. Oxygen-dependent ATF-4 stability is mediated by the PHD3 oxygen sensor.
    Blood. 2007 Nov 15;110(10):3610-7 PMID: 17684156
  131. Vascular normalization: a real benefit?
    Cancer Chemother Pharmacol. 2011 Aug;68(2):275-8 PMID: 21638121
  132. Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels.
    Cell. 2007 Nov 2;131(3):463-75 PMID: 17981115
  133. RIBBON-1: randomized, double-blind, placebo-controlled, phase III trial of chemotherapy with or without bevacizumab for first-line treatment of human epidermal growth factor receptor 2-negative, locally recurrent or metastatic breast cancer.
    J Clin Oncol. 2011 Apr 1;29(10):1252-60 PMID: 21383283
  134. Bevacizumab has differential and dose-dependent effects on glioma blood vessels and tumor cells.
    Clin Cancer Res. 2011 Oct 1;17(19):6192-205 PMID: 21788357
  135. Chemotherapy, bevacizumab, and cetuximab in metastatic colorectal cancer.
    N Engl J Med. 2009 Feb 5;360(6):563-72 PMID: 19196673
  136. Identification of an Ire1alpha endonuclease specific inhibitor with cytotoxic activity against human multiple myeloma.
    Blood. 2011 Jan 27;117(4):1311-4 PMID: 21081713
  137. EMT: a new vision of hypoxia promoting cancer progression.
    Cancer Biol Ther. 2011 Apr 15;11(8):714-23 PMID: 21389772
  138. Sorafenib for treatment of renal cell carcinoma: Final efficacy and safety results of the phase III treatment approaches in renal cancer global evaluation trial.
    J Clin Oncol. 2009 Jul 10;27(20):3312-8 PMID: 19451442
  139. Bevacizumab in combination with oxaliplatin-based chemotherapy as first-line therapy in metastatic colorectal cancer: a randomized phase III study.
    J Clin Oncol. 2008 Apr 20;26(12):2013-9 PMID: 18421054
  140. Monocarboxylate transporter 4 regulates maturation and trafficking of CD147 to the plasma membrane in the metastatic breast cancer cell line MDA-MB-231.
    Cancer Res. 2007 May 1;67(9):4182-9 PMID: 17483329
  141. Antiangiogenic agents increase breast cancer stem cells via the generation of tumor hypoxia.
    Proc Natl Acad Sci U S A. 2012 Feb 21;109(8):2784-9 PMID: 22308314
  142. Inhibition of ATR leads to increased sensitivity to hypoxia/reoxygenation.
    Cancer Res. 2004 Sep 15;64(18):6556-62 PMID: 15374968
  143. Development of HIF-1 inhibitors for cancer therapy.
    J Cell Mol Med. 2009 Sep;13(9A):2780-6 PMID: 19674190
  144. Antiangiogenic therapy for cancer: current and emerging concepts.
    Oncology (Williston Park). 2005 Apr;19(4 Suppl 3):7-16 PMID: 15934498
  145. Molecular imaging of hypoxia.
    J Nucl Med. 2011 Feb;52(2):165-8 PMID: 21233176
  146. Overall survival and updated results for sunitinib compared with interferon alfa in patients with metastatic renal cell carcinoma.
    J Clin Oncol. 2009 Aug 1;27(22):3584-90 PMID: 19487381
  147. Targeted anti-vascular endothelial growth factor receptor-2 therapy leads to short-term and long-term impairment of vascular function and increase in tumor hypoxia.
    Cancer Res. 2006 Apr 1;66(7):3639-48 PMID: 16585189
  148. Hypoxia signalling in cancer and approaches to enforce tumour regression.
    Nature. 2006 May 25;441(7092):437-43 PMID: 16724055
  149. Phase III trial of bevacizumab in combination with gemcitabine and erlotinib in patients with metastatic pancreatic cancer.
    J Clin Oncol. 2009 May 1;27(13):2231-7 PMID: 19307500
Article Info
Journal
Nature reviews. Clinical oncology
Abbr.
Nat Rev Clin Oncol
ISSN
1759-4782
Published
2012-04-24
Epub
2012-00-24
Pages
378-90
Language
English
Region
England
NLM ID
101500077
Subset
IM
Grants
NCI NIH HHS · N01-CO12400 · United States
Analysis Services
Analysis Services

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