Metabolic and hypoxic adaptation to anti-angiogenic therapy: a target for induced essentiality.

PubWeight™: 1.07‹?› | Rank: Top 10%

🔗 View Article (PMC 4403040)

Published in EMBO Mol Med on February 19, 2015

Authors

Alan McIntyre1, Adrian L Harris2

Author Affiliations

1: Hypoxia and angiogenesis Group, Department of Oncology Weatherall Institute of Molecular Medicine University of Oxford, Oxford, UK.
2: Hypoxia and angiogenesis Group, Department of Oncology Weatherall Institute of Molecular Medicine University of Oxford, Oxford, UK aharris.lab@imm.ox.ac.uk.

Associated clinical trials:

A Phase I Trial of AZD3965 in Patients With Advanced Cancer | NCT01791595

Study of Hydroxychloroquine Before Surgery in Patients With Primary Renal Cell Carcinoma | NCT01144169

Study of the Glutaminase Inhibitor CB-839 in Solid Tumors | NCT02071862

A Phase II, Single-Arm Study of RAD001 (Everolimus), Letrozole, and Metformin in Patients With Advanced or Recurrent Endometrial Carcinoma | NCT01797523

Metformin Plus Modified FOLFOX 6 in Metastatic Pancreatic Cancer | NCT01666730

Everolimus and Bortezomib in Treating Patients With Relapsed or Refractory Lymphoma | NCT00671112

Phase 1 Safety Study of ACT-PFK-158, 2HCl in Patients With Advanced Solid Malignancies | NCT02044861

TORC1/2 Inhibitor MLN0128 and Bevacizumab in Treating Patients With Recurrent Glioblastoma or Advanced Solid Tumors | NCT02142803

Metformin Hydrochloride, Carboplatin, and Paclitaxel in Treating Patients With Recurrent Ovarian, Fallopian Tube, or Primary Peritoneal Cancer | NCT02050009

Metformin Hydrochloride and Combination Chemotherapy in Treating Patients With Stage III-IV Ovarian, Fallopian Tube, or Primary Peritoneal Cancer | NCT02122185

Metformin Hydrochloride in Treating Patients With Pancreatic Cancer That Can be Removed by Surgery | NCT01954732

A Randomized Phase II Study of Metformin Plus Paclitaxel/Carboplatin/Bevacizumab in Patients With Adenocarcinoma. (NA_00052073) | NCT01578551

Tivantinib and Bevacizumab in Treating Patients With Solid Tumors That Are Metastatic or Cannot Be Removed by Surgery | NCT01749384

Trial to Determine Optimal Phase II Dose of the Oral Dual CAIX Inhibitor/ Radiosensitizer | NCT02216669

Topotecan, Cisplatin and Bevacizumab for Recurrent/Persistent Cervical Cancer | NCT00548418

Dose Escalation Study of Pazopanib Plus TH-302 (PATH) | NCT01485042

Safety and Efficacy Study of TH-302 CNS Penetration in Recurrent High Grade Astrocytoma Following Bevacizumab | NCT01403610

Study of Safety and Effects of cG250 and Sunitinib in Patients With Advanced Renal Cell Carcinoma | NCT00520533

Sorafenib Tosylate and Hypoxia-Activated Prodrug TH-302 in Treating Patients With Advanced Kidney Cancer or Liver Cancer That Cannot Be Removed By Surgery | NCT01497444

HYPONCO - Hypoxia in Brain Tumors (HYPONCO) | NCT01200134

NCT00052053

Dose-Escalation Study of TH-302 in Combination With Sunitinib to Treat Patients With Advanced Renal Cell Carcinoma,Gastrointestinal Stromal Tumors and Pancreatic Neuroendocrine Tumors (TH-CR-410) | NCT01381822

NCT10749384

FMISO PET Study of Glioblastoma | NCT02076152

Articles citing this

Metabolic Symbiosis Enables Adaptive Resistance to Anti-angiogenic Therapy that Is Dependent on mTOR Signaling. Cell Rep (2016) 1.03

Overcoming Hypoxia-Mediated Tumor Progression: Combinatorial Approaches Targeting pH Regulation, Angiogenesis and Immune Dysfunction. Front Cell Dev Biol (2016) 0.84

Antiangiogenic cancer treatment: The great discovery and greater complexity (Review). Int J Oncol (2016) 0.83

The BET inhibitor JQ1 selectively impairs tumour response to hypoxia and downregulates CA9 and angiogenesis in triple negative breast cancer. Oncogene (2016) 0.81

Lack of R-Ras Leads to Increased Vascular Permeability in Ischemic Retinopathy. Invest Ophthalmol Vis Sci (2016) 0.80

Identification of functional metabolic biomarkers from lung cancer patient serum using PEP technology. Biomark Res (2016) 0.78

Glycolysis gene expression analysis and selective metabolic advantage in the clinical progression of colorectal cancer. Pharmacogenomics J (2016) 0.78

Targeting carbonic anhydrase IX improves the anti-cancer efficacy of mTOR inhibitors. Oncotarget (2016) 0.78

EphrinB2 repression through ZEB2 mediates tumour invasion and anti-angiogenic resistance. Nat Commun (2016) 0.77

Microenvironmental Targets in Sarcoma. Front Oncol (2015) 0.76

Genomic alterations underlie a pan-cancer metabolic shift associated with tumour hypoxia. Genome Biol (2016) 0.76

Biomarkers of evasive resistance predict disease progression in cancer patients treated with antiangiogenic therapies. Oncotarget (2016) 0.76

The EGLN-HIF O2-Sensing System: Multiple Inputs and Feedbacks. Mol Cell (2017) 0.75

Arg-Leu-Tyr-Glu tetrapeptide inhibits tumor progression by suppressing angiogenesis and vascular permeability via VEGF receptor-2 antagonism. Oncotarget (2016) 0.75

Epidermal growth factor, latrophilin, and seven transmembrane domain-containing protein 1 marker, a novel angiogenesis marker. Onco Targets Ther (2015) 0.75

Association of Angiopoietin-2 and Ki-67 Expression with Vascular Density and Sunitinib Response in Metastatic Renal Cell Carcinoma. PLoS One (2016) 0.75

Self-renewal molecular mechanisms of colorectal cancer stem cells. Int J Mol Med (2016) 0.75

HIGD1A-mediated dormancy and tumor survival. Mol Cell Oncol (2015) 0.75

Hypoxia and antitumor CD8(+) T cells: An incompatible alliance? Oncoimmunology (2016) 0.75

Commentary: A Metabolic Immune Checkpoint: Adenosine in Tumor Microenvironment. Front Immunol (2016) 0.75

Fine-Tuning Tumor Endothelial Cells to Selectively Kill Cancer. Int J Mol Sci (2017) 0.75

Gold nanoparticles attenuate metastasis by tumor vasculature normalization and epithelial-mesenchymal transition inhibition. Int J Nanomedicine (2017) 0.75

Non-invasive monitoring of the therapeutic response in sorafenib-treated hepatocellular carcinoma based on photoacoustic imaging. Eur Radiol (2017) 0.75

A ketogenic diet supplemented with medium-chain triglycerides enhances the anti-tumor and anti-angiogenic efficacy of chemotherapy on neuroblastoma xenografts in a CD1-nu mouse model. Oncotarget (2017) 0.75

Articles cited by this

Hallmarks of cancer: the next generation. Cell (2011) 140.01

The hallmarks of cancer. Cell (2000) 113.05

Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N Engl J Med (2004) 49.02

Tumor angiogenesis: therapeutic implications. N Engl J Med (1971) 35.36

Modes of resistance to anti-angiogenic therapy. Nat Rev Cancer (2008) 15.20

Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell (2008) 11.18

Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med (2004) 9.80

Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol (2009) 5.55

How cancer metabolism is tuned for proliferation and vulnerable to disruption. Nature (2012) 3.77

Anti-VEGF treatment reduces blood supply and increases tumor cell invasion in glioblastoma. Proc Natl Acad Sci U S A (2011) 3.48

Making new contacts: the mTOR network in metabolism and signalling crosstalk. Nat Rev Mol Cell Biol (2014) 3.36

Targeting GLUT1 and the Warburg effect in renal cell carcinoma by chemical synthetic lethality. Sci Transl Med (2011) 2.97

Rapid decrease in delivery of chemotherapy to tumors after anti-VEGF therapy: implications for scheduling of anti-angiogenic drugs. Cancer Cell (2012) 2.76

Hypoxic and Ras-transformed cells support growth by scavenging unsaturated fatty acids from lysophospholipids. Proc Natl Acad Sci U S A (2013) 2.57

Genetic interactions in cancer progression and treatment. Cell (2011) 2.54

Oxygen sensing, hypoxia-inducible factors, and disease pathophysiology. Annu Rev Pathol (2013) 2.44

Glucose utilization via glycogen phosphorylase sustains proliferation and prevents premature senescence in cancer cells. Cell Metab (2012) 2.43

Increased survival of glioblastoma patients who respond to antiangiogenic therapy with elevated blood perfusion. Cancer Res (2011) 2.40

Improved tumor oxygenation and survival in glioblastoma patients who show increased blood perfusion after cediranib and chemoradiation. Proc Natl Acad Sci U S A (2013) 2.14

Recent molecular discoveries in angiogenesis and antiangiogenic therapies in cancer. J Clin Invest (2013) 2.03

Anti-VEGF/VEGFR therapy for cancer: reassessing the target. Cancer Res (2012) 2.01

Hypoxia and the extracellular matrix: drivers of tumour metastasis. Nat Rev Cancer (2014) 2.00

Disrupting proton dynamics and energy metabolism for cancer therapy. Nat Rev Cancer (2013) 1.93

The VHL/HIF axis in clear cell renal carcinoma. Semin Cancer Biol (2012) 1.90

Blocking lipid synthesis overcomes tumor regrowth and metastasis after antiangiogenic therapy withdrawal. Cell Metab (2014) 1.84

AMPK: a contextual oncogene or tumor suppressor? Cancer Res (2013) 1.82

DLL4-Notch signaling mediates tumor resistance to anti-VEGF therapy in vivo. Cancer Res (2011) 1.78

Antiangiogenic therapy, hypoxia, and metastasis: risky liaisons, or not? Nat Rev Clin Oncol (2011) 1.72

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) 1.70

Hypoxia and energetic tumour metabolism. Curr Opin Genet Dev (2010) 1.61

The pentose phosphate pathway: an antioxidant defense and a crossroad in tumor cell fate. Free Radic Biol Med (2012) 1.53

Molecular aspects of cancer cell resistance to chemotherapy. Biochem Pharmacol (2013) 1.50

Heterogeneity of the tumor vasculature. Semin Thromb Hemost (2010) 1.48

Phase I trial of combretastatin A4 phosphate (CA4P) in combination with bevacizumab in patients with advanced cancer. Clin Cancer Res (2012) 1.42

VEGF and Notch in tip and stalk cell selection. Cold Spring Harb Perspect Med (2013) 1.38

Vessel co-option in primary human tumors and metastases: an obstacle to effective anti-angiogenic treatment? Cancer Med (2013) 1.36

Gene expression profile identifies tyrosine kinase c-Met as a targetable mediator of antiangiogenic therapy resistance. Clin Cancer Res (2013) 1.35

Microarray analysis verifies two distinct phenotypes of glioblastomas resistant to antiangiogenic therapy. Clin Cancer Res (2012) 1.35

Oxygen-independent regulation of HIF-1: novel involvement of PI3K/AKT/mTOR pathway in cancer. Curr Cancer Drug Targets (2013) 1.33

Carbonic anhydrase IX promotes tumor growth and necrosis in vivo and inhibition enhances anti-VEGF therapy. Clin Cancer Res (2012) 1.30

3D cell culture systems modeling tumor growth determinants in cancer target discovery. Adv Drug Deliv Rev (2014) 1.30

Fatty acid uptake and lipid storage induced by HIF-1α contribute to cell growth and survival after hypoxia-reoxygenation. Cell Rep (2014) 1.25

Phase II study of the safety and antitumor activity of the hypoxia-activated prodrug TH-302 in combination with doxorubicin in patients with advanced soft tissue sarcoma. J Clin Oncol (2014) 1.17

Bevacizumab and micrometastases: revisiting the preclinical and clinical rollercoaster. Pharmacol Ther (2013) 1.16

Hypoxic regulation of glutamine metabolism through HIF1 and SIAH2 supports lipid synthesis that is necessary for tumor growth. Cell Metab (2014) 1.15

Antitumor effect of the angiogenesis inhibitor bevacizumab is dependent on susceptibility of tumors to hypoxia-induced apoptosis. Biochem Pharmacol (2007) 1.14

Extensive regulation of the non-coding transcriptome by hypoxia: role of HIF in releasing paused RNApol2. EMBO Rep (2013) 1.14

Value of DCE-MRI and FDG-PET/CT in the prediction of response to preoperative chemotherapy with bevacizumab for colorectal liver metastases. Br J Cancer (2012) 1.13

Bortezomib represses HIF-1α protein expression and nuclear accumulation by inhibiting both PI3K/Akt/TOR and MAPK pathways in prostate cancer cells. J Mol Med (Berl) (2011) 1.13

Serial magnetic resonance spectroscopy reveals a direct metabolic effect of cediranib in glioblastoma. Cancer Res (2011) 1.13

Use of macrophages to target therapeutic adenovirus to human prostate tumors. Cancer Res (2011) 1.12

Balancing glycolytic flux: the role of 6-phosphofructo-2-kinase/fructose 2,6-bisphosphatases in cancer metabolism. Cancer Metab (2013) 1.12

Assessing early therapeutic response to bevacizumab in primary breast cancer using magnetic resonance imaging and gene expression profiles. J Natl Cancer Inst Monogr (2011) 1.12

Activating oxidative phosphorylation by a pyruvate dehydrogenase kinase inhibitor overcomes sorafenib resistance of hepatocellular carcinoma. Br J Cancer (2012) 1.11

Angiogenesis and the tumor microenvironment: vascular endothelial growth factor and beyond. Semin Oncol (2014) 1.11

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) 1.10

Regulation of mTORC1 signaling by pH. PLoS One (2011) 1.04

Principles of targeting endothelial cell metabolism to treat angiogenesis and endothelial cell dysfunction in disease. EMBO Mol Med (2014) 1.04

Bevacizumab impairs oxidative energy metabolism and shows antitumoral effects in recurrent glioblastomas: a 31P/1H MRSI and quantitative magnetic resonance imaging study. Neuro Oncol (2011) 1.02

Gene expression and hypoxia in breast cancer. Genome Med (2011) 1.02

The angiogenic process as a therapeutic target in cancer. Biochem Pharmacol (2011) 1.01

A novel approach to cancer therapy using PX-478 as a HIF-1α inhibitor. Arch Pharm Res (2011) 0.99

Carbonic anhydrase IX is a clinically significant tissue and serum biomarker associated with renal cell carcinoma. Oncol Lett (2012) 0.95

Dichloroacetate reverses the hypoxic adaptation to bevacizumab and enhances its antitumor effects in mouse xenografts. J Mol Med (Berl) (2013) 0.95

The chemistry, physiology and pathology of pH in cancer. Philos Trans R Soc Lond B Biol Sci (2014) 0.94

Predictive biomarkers for bevacizumab: are we there yet? Clin Cancer Res (2013) 0.94

Inhibition of autophagy enhances anticancer effects of bevacizumab in hepatocarcinoma. J Mol Med (Berl) (2012) 0.94

PERK/eIF2α signaling protects therapy resistant hypoxic cells through induction of glutathione synthesis and protection against ROS. Proc Natl Acad Sci U S A (2013) 0.92

A cyclic peptide inhibitor of HIF-1 heterodimerization that inhibits hypoxia signaling in cancer cells. J Am Chem Soc (2013) 0.92

Hypoxia and metabolism in cancer. Adv Exp Med Biol (2014) 0.91

Pilot trial of EZN-2968, an antisense oligonucleotide inhibitor of hypoxia-inducible factor-1 alpha (HIF-1α), in patients with refractory solid tumors. Cancer Chemother Pharmacol (2013) 0.90

Optical imaging of tumor microenvironment. Am J Nucl Med Mol Imaging (2013) 0.90

Proton NMR-based metabolite analyses of archived serial paired serum and urine samples from myeloma patients at different stages of disease activity identifies acetylcarnitine as a novel marker of active disease. PLoS One (2013) 0.89

ImmunoPET imaging of renal cell carcinoma with (124)I- and (89)Zr-labeled anti-CAIX monoclonal antibody cG250 in mice. Cancer Biother Radiopharm (2013) 0.85

HIF-1α activation mediates resistance to anti-angiogenic therapy in neuroblastoma xenografts. J Pediatr Surg (2013) 0.85

Critical role of aberrant angiogenesis in the development of tumor hypoxia and associated radioresistance. Cancers (Basel) (2014) 0.83

Chemotherapy counteracts metastatic dissemination induced by antiangiogenic treatment in mice. Mol Cancer Ther (2013) 0.83

Inhibition of monocarboxylate transporter-1 (MCT1) by AZD3965 enhances radiosensitivity by reducing lactate transport. Mol Cancer Ther (2014) 0.82

Angiogenesis revisited - role and therapeutic potential of targeting endothelial metabolism. J Cell Sci (2014) 0.82

Gene Expression Analysis Reveals Distinct Pathways of Resistance to Bevacizumab in Xenograft Models of Human ER-Positive Breast Cancer. J Cancer (2014) 0.82

Metabolic asymmetry in cancer: a "balancing act" that promotes tumor growth. Cancer Cell (2014) 0.81

ATF4 orchestrates a program of BH3-only protein expression in severe hypoxia. Mol Biol Rep (2012) 0.79

Weekly EZN-2208 (PEGylated SN-38) in combination with bevacizumab in patients with refractory solid tumors. Invest New Drugs (2013) 0.79

Mixed-effects modeling of clinical DCE-MRI data: application to colorectal liver metastases treated with bevacizumab. J Magn Reson Imaging (2014) 0.78

Ensemble analyses improve signatures of tumour hypoxia and reveal inter-platform differences. BMC Bioinformatics (2014) 0.77

Monitoring tumour response during chemo-radiotherapy: a parametric method using FDG-PET/CT images in patients with oesophageal cancer. EJNMMI Res (2014) 0.77

Hypoxic regulation of RIOK3 is a major mechanism for cancer cell invasion and metastasis. Oncogene (2014) 0.77

When cancer co-opts the vasculature. N Engl J Med (2014) 0.76