Renal cyst formation in Fh1-deficient mice is independent of the Hif/Phd pathway: roles for fumarate in KEAP1 succination and Nrf2 signaling.

PubWeight™: 3.00‹?› | Rank: Top 1%

🔗 View Article (PMC 3202623)

Published in Cancer Cell on October 18, 2011

Authors

Julie Adam1, Emine Hatipoglu, Linda O'Flaherty, Nicola Ternette, Natasha Sahgal, Helen Lockstone, Dilair Baban, Emma Nye, Gordon W Stamp, Kathryn Wolhuter, Marcus Stevens, Roman Fischer, Peter Carmeliet, Patrick H Maxwell, Chris W Pugh, Norma Frizzell, Tomoyoshi Soga, Benedikt M Kessler, Mona El-Bahrawy, Peter J Ratcliffe, Patrick J Pollard

Author Affiliations

1: Nuffield Department of Medicine, Henry Wellcome Building for Molecular Physiology, University of Oxford, Oxford OX3 7BN, UK.

Articles citing this

(truncated to the top 100)

Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell (2012) 9.88

Mitochondria and cancer. Nat Rev Cancer (2012) 4.81

Modulation of oxidative stress as an anticancer strategy. Nat Rev Drug Discov (2013) 4.72

Integrated molecular analysis of clear-cell renal cell carcinoma. Nat Genet (2013) 4.61

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

Fueling immunity: insights into metabolism and lymphocyte function. Science (2013) 3.62

The emerging role of the Nrf2-Keap1 signaling pathway in cancer. Genes Dev (2013) 3.40

NRF2 and cancer: the good, the bad and the importance of context. Nat Rev Cancer (2012) 3.04

Cellular metabolism and disease: what do metabolic outliers teach us? Cell (2012) 2.90

Inhibition of α-KG-dependent histone and DNA demethylases by fumarate and succinate that are accumulated in mutations of FH and SDH tumor suppressors. Genes Dev (2012) 2.70

Influence of metabolism on epigenetics and disease. Cell (2013) 2.64

Metabolic targets for cancer therapy. Nat Rev Drug Discov (2013) 2.32

The Keap1-Nrf2 pathway: Mechanisms of activation and dysregulation in cancer. Redox Biol (2013) 1.94

Functions of autophagy in normal and diseased liver. Autophagy (2013) 1.81

Oncometabolites: linking altered metabolism with cancer. J Clin Invest (2013) 1.78

Metabolism of kidney cancer: from the lab to clinical practice. Eur Urol (2012) 1.75

The Keap1-Nrf2 system in cancers: stress response and anabolic metabolism. Front Oncol (2012) 1.64

State of the science: an update on renal cell carcinoma. Mol Cancer Res (2012) 1.58

Mitochondrial dysfunction in cancer. Front Oncol (2013) 1.57

Hypoxia, Hypoxia-inducible Transcription Factors, and Renal Cancer. Eur Urol (2015) 1.56

Targeting ABL1-mediated oxidative stress adaptation in fumarate hydratase-deficient cancer. Cancer Cell (2014) 1.54

The proto-oncometabolite fumarate binds glutathione to amplify ROS-dependent signaling. Mol Cell (2013) 1.54

Protein lysine acylation and cysteine succination by intermediates of energy metabolism. ACS Chem Biol (2012) 1.49

Oxygen sensing and hypoxia signalling pathways in animals: the implications of physiology for cancer. J Physiol (2013) 1.35

Fumarate is cardioprotective via activation of the Nrf2 antioxidant pathway. Cell Metab (2012) 1.35

Molecular pathways: Fumarate hydratase-deficient kidney cancer--targeting the Warburg effect in cancer. Clin Cancer Res (2013) 1.34

Defects in mitochondrial metabolism and cancer. Cancer Metab (2014) 1.24

Mitochondrial reactive oxygen species and cancer. Cancer Metab (2014) 1.20

Alterations of metabolic genes and metabolites in cancer. Semin Cell Dev Biol (2012) 1.18

Mechanisms of activation of the transcription factor Nrf2 by redox stressors, nutrient cues, and energy status and the pathways through which it attenuates degenerative disease. Free Radic Biol Med (2015) 1.17

TCA Cycle Defects and Cancer: When Metabolism Tunes Redox State. Int J Cell Biol (2012) 1.17

SQSTM1 is a pathogenic target of 5q copy number gains in kidney cancer. Cancer Cell (2013) 1.15

Metabolic reprogramming for producing energy and reducing power in fumarate hydratase null cells from hereditary leiomyomatosis renal cell carcinoma. PLoS One (2013) 1.12

Succination of Keap1 and activation of Nrf2-dependent antioxidant pathways in FH-deficient papillary renal cell carcinoma type 2. Cancer Cell (2011) 1.12

Mitochondria and Cancer. Mol Cell (2016) 1.11

Genetically-defined metabolic reprogramming in cancer. Trends Endocrinol Metab (2012) 1.09

Fundamentals of cancer metabolism. Sci Adv (2016) 1.09

Inhibition of mitochondrial aconitase by succination in fumarate hydratase deficiency. Cell Rep (2013) 1.08

The emerging role of fumarate as an oncometabolite. Front Oncol (2012) 1.08

Identification of novel microRNAs in post-transcriptional control of Nrf2 expression and redox homeostasis in neuronal, SH-SY5Y cells. PLoS One (2012) 1.06

Recurrent chromosomal gains and heterogeneous driver mutations characterise papillary renal cancer evolution. Nat Commun (2015) 1.05

Fumarate induces redox-dependent senescence by modifying glutathione metabolism. Nat Commun (2015) 1.04

Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: an evolutionarily conserved mechanism. Cell Mol Life Sci (2016) 1.04

Mitochondria and Cancer. Cell (2016) 1.02

Cytoprotection "gone astray": Nrf2 and its role in cancer. Onco Targets Ther (2014) 1.00

Reversed argininosuccinate lyase activity in fumarate hydratase-deficient cancer cells. Cancer Metab (2013) 1.00

Changing appetites: the adaptive advantages of fuel choice. Trends Cell Biol (2013) 1.00

Hereditary leiomyomatosis and renal cell carcinoma. Int J Nephrol Renovasc Dis (2014) 0.99

A role for cytosolic fumarate hydratase in urea cycle metabolism and renal neoplasia. Cell Rep (2013) 0.99

Hypoxia-inducible factor signaling in pheochromocytoma: turning the rudder in the right direction. J Natl Cancer Inst (2013) 0.98

New strategies in renal cell carcinoma: targeting the genetic and metabolic basis of disease. Clin Cancer Res (2015) 0.98

Dual roles of NRF2 in tumor prevention and progression: possible implications in cancer treatment. Free Radic Biol Med (2014) 0.98

Nrf2 activation as target to implement therapeutic treatments. Front Chem (2015) 0.96

Mesenchymal stroma: primary determinant and therapeutic target for epithelial cancer. Trends Cell Biol (2013) 0.94

The role of angiogenic factors in fibroid pathogenesis: potential implications for future therapy. Hum Reprod Update (2013) 0.93

Metabolic mechanisms of epigenetic regulation. ACS Chem Biol (2013) 0.92

The complexity of the Nrf2 pathway: beyond the antioxidant response. J Nutr Biochem (2015) 0.91

Monitoring Keap1-Nrf2 interactions in single live cells. Biotechnol Adv (2014) 0.91

KEAP1 is a redox sensitive target that arbitrates the opposing radiosensitive effects of parthenolide in normal and cancer cells. Cancer Res (2013) 0.90

The succinated proteome. Mass Spectrom Rev (2013) 0.89

Aerobic glycolysis: a novel target in kidney cancer. Expert Rev Anticancer Ther (2013) 0.89

Hypoxia-inducible factor-1α causes renal cyst expansion through calcium-activated chloride secretion. J Am Soc Nephrol (2013) 0.87

Frequent alteration of the protein synthesis of enzymes for glucose metabolism in hepatocellular carcinomas. J Gastroenterol (2013) 0.86

Fatty Acid Oxidation is Impaired in An Orthologous Mouse Model of Autosomal Dominant Polycystic Kidney Disease. EBioMedicine (2016) 0.86

Regulation of ventilatory sensitivity and carotid body proliferation in hypoxia by the PHD2/HIF-2 pathway. J Physiol (2015) 0.85

Fumarate hydratase inactivation in renal tumors: HIF1α, NRF2, and "cryptic targets" of transcription factors. Chin J Cancer (2012) 0.84

p62/Sqstm1 promotes malignancy of HCV-positive hepatocellular carcinoma through Nrf2-dependent metabolic reprogramming. Nat Commun (2016) 0.84

Dimethyl fumarate and the oleanane triterpenoids, CDDO-imidazolide and CDDO-methyl ester, both activate the Nrf2 pathway but have opposite effects in the A/J model of lung carcinogenesis. Carcinogenesis (2015) 0.84

Metabolic, autophagic, and mitophagic activities in cancer initiation and progression. Biomed J (2016) 0.83

Cells lacking the fumarase tumor suppressor are protected from apoptosis through a hypoxia-inducible factor-independent, AMPK-dependent mechanism. Mol Cell Biol (2012) 0.83

Oxygen availability and metabolic adaptations. Nat Rev Cancer (2016) 0.83

Modulation of nuclear factor E2-related factor-2 (Nrf2) activation by the stress response gene immediate early response-3 (IER3) in colonic epithelial cells: a novel mechanism of cellular adaption to inflammatory stress. J Biol Chem (2013) 0.82

Advances in mechanisms of anti-oxidation. Discov Med (2014) 0.82

Hereditary kidney cancer syndromes. Adv Chronic Kidney Dis (2014) 0.82

Protein profiling of blood samples from patients with hereditary leiomyomatosis and renal cell cancer by surface-enhanced laser desorption/ionization time-of-flight mass spectrometry. Int J Mol Sci (2012) 0.81

Adipocyte pseudohypoxia suppresses lipolysis and facilitates benign adipose tissue expansion. Diabetes (2014) 0.81

Decade in review-kidney cancer: discoveries, therapies and opportunities. Nat Rev Urol (2014) 0.81

Altered metabolite levels in cancer: implications for tumour biology and cancer therapy. Nat Rev Cancer (2016) 0.80

Mitochondria, cholesterol and cancer cell metabolism. Clin Transl Med (2016) 0.80

The SWI/SNF Protein PBRM1 Restrains VHL-Loss-Driven Clear Cell Renal Cell Carcinoma. Cell Rep (2017) 0.79

Mitochondrial metabolism in TCA cycle mutant cancer cells. Cell Cycle (2013) 0.79

Succination is Increased on Select Proteins in the Brainstem of the NADH dehydrogenase (ubiquinone) Fe-S protein 4 (Ndufs4) Knockout Mouse, a Model of Leigh Syndrome. Mol Cell Proteomics (2015) 0.79

Acetoacetate Accelerates Muscle Regeneration and Ameliorates Muscular Dystrophy in Mice. J Biol Chem (2015) 0.79

Glutaminolysis as a target for cancer therapy. Oncogene (2015) 0.78

Insights into the Genetic Basis of the Renal Cell Carcinomas from The Cancer Genome Atlas. Mol Cancer Res (2016) 0.78

Friedreich's ataxia, frataxin, PIP5K1B: echo of a distant fracas. Oxid Med Cell Longev (2013) 0.78

Genetically modeled mice with mutations in mitochondrial metabolic enzymes for the study of cancer. Front Oncol (2014) 0.78

The Succinated Proteome of FH-Mutant Tumours. Metabolites (2014) 0.78

Integrated data analysis reveals uterine leiomyoma subtypes with distinct driver pathways and biomarkers. Proc Natl Acad Sci U S A (2016) 0.78

Oncometabolites: Unconventional triggers of oncogenic signalling cascades. Free Radic Biol Med (2016) 0.78

Autophagy in the liver: functions in health and disease. Nat Rev Gastroenterol Hepatol (2017) 0.77

Cullin 3 Ubiquitin Ligases in Cancer Biology: Functions and Therapeutic Implications. Front Oncol (2016) 0.77

Role of mitochondrial dysfunction in cancer progression. Exp Biol Med (Maywood) (2016) 0.77

Perspectives of the Nrf-2 signaling pathway in cancer progression and therapy. Toxicol Rep (2017) 0.77

Structural basis for oxygen degradation domain selectivity of the HIF prolyl hydroxylases. Nat Commun (2016) 0.76

Novel insights into FH-associated disease are KEAPing the lid on oncogenic HIF signalling. Oncotarget (2011) 0.76

Changing perspective on oncometabolites: from metabolic signature of cancer to tumorigenic and immunosuppressive agents. Oncotarget (2016) 0.76

Mitochondrial metabolic remodeling in response to genetic and environmental perturbations. Wiley Interdiscip Rev Syst Biol Med (2016) 0.76

Keap1 expression has independent prognostic value in pancreatic adenocarcinomas. Diagn Pathol (2015) 0.76

Mitochondrial health, the epigenome and healthspan. Clin Sci (Lond) (2016) 0.76

Articles cited by this

Hypoxia--a key regulatory factor in tumour growth. Nat Rev Cancer (2002) 20.51

C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell (2001) 19.75

Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature (2010) 14.50

Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell (2008) 13.49

Oncogene-induced Nrf2 transcription promotes ROS detoxification and tumorigenesis. Nature (2011) 9.70

HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell (2003) 9.12

Germline mutations in FH predispose to dominantly inherited uterine fibroids, skin leiomyomata and papillary renal cell cancer. Nat Genet (2002) 8.19

Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell (2011) 7.33

Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol Cell Biol (2005) 6.44

Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu Rev Pharmacol Toxicol (2002) 6.22

HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell (2007) 6.16

Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell (2009) 5.91

The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem (2009) 5.80

HIF overexpression correlates with biallelic loss of fumarate hydratase in renal cancer: novel role of fumarate in regulation of HIF stability. Cancer Cell (2005) 5.47

Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab Rev (2006) 4.71

NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer. Trends Biochem Sci (2009) 4.50

The von Hippel-Lindau tumour suppressor protein: O2 sensing and cancer. Nat Rev Cancer (2008) 4.42

Accumulation of Krebs cycle intermediates and over-expression of HIF1alpha in tumours which result from germline FH and SDH mutations. Hum Mol Genet (2005) 4.12

Deficiency or inhibition of oxygen sensor Phd1 induces hypoxia tolerance by reprogramming basal metabolism. Nat Genet (2008) 3.94

Molecular mechanisms of the Keap1–Nrf2 pathway in stress response and cancer evolution. Genes Cells (2011) 3.76

Acute postnatal ablation of Hif-2alpha results in anemia. Proc Natl Acad Sci U S A (2007) 3.51

Genetic and functional studies implicate HIF1α as a 14q kidney cancer suppressor gene. Cancer Discov (2011) 3.45

Fumaric acid esters exert neuroprotective effects in neuroinflammation via activation of the Nrf2 antioxidant pathway. Brain (2011) 3.38

Cell-permeating alpha-ketoglutarate derivatives alleviate pseudohypoxia in succinate dehydrogenase-deficient cells. Mol Cell Biol (2007) 3.33

Epithelial-specific Cre/lox recombination in the developing kidney and genitourinary tract. J Am Soc Nephrol (2002) 3.28

Mammalian zinc transport, trafficking, and signals. J Biol Chem (2006) 3.05

Renal cyst development in mice with conditional inactivation of the von Hippel-Lindau tumor suppressor. Cancer Res (2006) 3.04

Mutations in the fumarate hydratase gene cause hereditary leiomyomatosis and renal cell cancer in families in North America. Am J Hum Genet (2003) 2.88

Inhibition of hypoxia-inducible factor (HIF) hydroxylases by citric acid cycle intermediates: possible links between cell metabolism and stabilization of HIF. J Biol Chem (2006) 2.86

Targeted inactivation of fh1 causes proliferative renal cyst development and activation of the hypoxia pathway. Cancer Cell (2007) 2.69

Placental but not heart defects are associated with elevated hypoxia-inducible factor alpha levels in mice lacking prolyl hydroxylase domain protein 2. Mol Cell Biol (2006) 2.58

Cancer chemoprevention mechanisms mediated through the Keap1-Nrf2 pathway. Antioxid Redox Signal (2010) 2.45

Aberrant succination of proteins in fumarate hydratase-deficient mice and HLRCC patients is a robust biomarker of mutation status. J Pathol (2011) 2.45

Role of hypoxia-inducible factor (HIF)-1alpha versus HIF-2alpha in the regulation of HIF target genes in response to hypoxia, insulin-like growth factor-I, or loss of von Hippel-Lindau function: implications for targeting the HIF pathway. Cancer Res (2006) 2.43

Regulation of adult erythropoiesis by prolyl hydroxylase domain proteins. Blood (2007) 2.40

The von Hippel-Lindau tumor suppressor protein and clear cell renal carcinoma. Clin Cancer Res (2007) 2.19

Hypoxic induction of Ctgf is directly mediated by Hif-1. Am J Physiol Renal Physiol (2004) 2.19

Physiological significance of reactive cysteine residues of Keap1 in determining Nrf2 activity. Mol Cell Biol (2008) 2.15

UOK 262 cell line, fumarate hydratase deficient (FH-/FH-) hereditary leiomyomatosis renal cell carcinoma: in vitro and in vivo model of an aberrant energy metabolic pathway in human cancer. Cancer Genet Cytogenet (2010) 2.06

Inborn and acquired metabolic defects in cancer. J Mol Med (Berl) (2011) 2.06

Role and regulation of prolyl hydroxylase domain proteins. Cell Death Differ (2008) 2.03

Structural and mechanistic studies on the inhibition of the hypoxia-inducible transcription factor hydroxylases by tricarboxylic acid cycle intermediates. J Biol Chem (2006) 1.75

Keap1 perceives stress via three sensors for the endogenous signaling molecules nitric oxide, zinc, and alkenals. Proc Natl Acad Sci U S A (2010) 1.72

Oxygen-regulated beta(2)-adrenergic receptor hydroxylation by EGLN3 and ubiquitylation by pVHL. Sci Signal (2009) 1.66

Increased risk of cancer in patients with fumarate hydratase germline mutation. J Med Genet (2005) 1.61

Role of Nrf1 in antioxidant response element-mediated gene expression and beyond. Toxicol Appl Pharmacol (2009) 1.49

S-(2-Succinyl)cysteine: a novel chemical modification of tissue proteins by a Krebs cycle intermediate. Arch Biochem Biophys (2006) 1.46

Familial cutaneous leiomyomatosis is a two-hit condition associated with renal cell cancer of characteristic histopathology. Am J Pathol (2001) 1.46

Succination of protein thiols during adipocyte maturation: a biomarker of mitochondrial stress. J Biol Chem (2007) 1.38

Dysregulation of hypoxia pathways in fumarate hydratase-deficient cells is independent of defective mitochondrial metabolism. Hum Mol Genet (2010) 1.33

Mutation analysis of hypoxia-inducible factors HIF1A and HIF2A in renal cell carcinoma. Anticancer Res (2009) 1.24

The Nrf2-Keap1-ARE signaling pathway: The regulation and dual function of Nrf2 in cancer. Antioxid Redox Signal (2010) 1.23

Inactivation of glyceraldehyde-3-phosphate dehydrogenase by fumarate in diabetes: formation of S-(2-succinyl)cysteine, a novel chemical modification of protein and possible biomarker of mitochondrial stress. Diabetes (2007) 1.17

Cancer. Puzzling patterns of predisposition. Science (2009) 1.09

HIF prolyl hydroxylase-3 mediates alpha-ketoglutarate-induced apoptosis and tumor suppression. J Mol Med (Berl) (2010) 1.06

Expression profiling in progressive stages of fumarate-hydratase deficiency: the contribution of metabolic changes to tumorigenesis. Cancer Res (2010) 1.05

Succination of proteins by fumarate: mechanism of inactivation of glyceraldehyde-3-phosphate dehydrogenase in diabetes. Ann N Y Acad Sci (2008) 0.99

Succination of proteins in diabetes. Free Radic Res (2010) 0.96

Fumarate hydratase deficiency and cancer: activation of hypoxia signaling? Cancer Cell (2007) 0.93

Articles by these authors

Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell (2008) 13.49

Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol (2004) 9.05

Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med (2003) 8.54

Hypoxia and inflammation. N Engl J Med (2011) 7.71

Gene prioritization through genomic data fusion. Nat Biotechnol (2006) 7.48

Contrasting properties of hypoxia-inducible factor 1 (HIF-1) and HIF-2 in von Hippel-Lindau-associated renal cell carcinoma. Mol Cell Biol (2005) 6.44

Binding of ras to phosphoinositide 3-kinase p110alpha is required for ras-driven tumorigenesis in mice. Cell (2007) 6.44

Basic and therapeutic aspects of angiogenesis. Cell (2011) 6.40

uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol (2002) 6.24

MassBank: a public repository for sharing mass spectral data for life sciences. J Mass Spectrom (2010) 6.16

Multiple high-throughput analyses monitor the response of E. coli to perturbations. Science (2007) 5.87

Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med (2002) 5.50

HIF overexpression correlates with biallelic loss of fumarate hydratase in renal cancer: novel role of fumarate in regulation of HIF stability. Cancer Cell (2005) 5.47

IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat Immunol (2011) 5.11

Loss of HIF-2alpha and inhibition of VEGF impair fetal lung maturation, whereas treatment with VEGF prevents fatal respiratory distress in premature mice. Nat Med (2002) 5.10

Anti-PlGF inhibits growth of VEGF(R)-inhibitor-resistant tumors without affecting healthy vessels. Cell (2007) 5.09

Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J Biol Chem (2004) 5.05

The oncometabolite 2-hydroxyglutarate inhibits histone lysine demethylases. EMBO Rep (2011) 4.89

HIF activation identifies early lesions in VHL kidneys: evidence for site-specific tumor suppressor function in the nephron. Cancer Cell (2002) 4.82

Plasma hepcidin levels are elevated but responsive to erythropoietin therapy in renal disease. Kidney Int (2009) 4.61

Haem oxygenase is synthetically lethal with the tumour suppressor fumarate hydratase. Nature (2011) 4.32

VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death. Nat Genet (2003) 4.19

Disruption of oxygen homeostasis underlies congenital Chuvash polycythemia. Nat Genet (2002) 4.06

Modification of kidney barrier function by the urokinase receptor. Nat Med (2007) 4.01

Deficiency or inhibition of oxygen sensor Phd1 induces hypoxia tolerance by reprogramming basal metabolism. Nat Genet (2008) 3.94

Hypoxia-inducible factor (HIF) asparagine hydroxylase is identical to factor inhibiting HIF (FIH) and is related to the cupin structural family. J Biol Chem (2002) 3.91

HRG inhibits tumor growth and metastasis by inducing macrophage polarization and vessel normalization through downregulation of PlGF. Cancer Cell (2011) 3.89

Characterization of human DNGR-1+ BDCA3+ leukocytes as putative equivalents of mouse CD8alpha+ dendritic cells. J Exp Med (2010) 3.84

The European dimension for the mouse genome mutagenesis program. Nat Genet (2004) 3.84

Widespread hypoxia-inducible expression of HIF-2alpha in distinct cell populations of different organs. FASEB J (2002) 3.81

Structural basis for the recognition of hydroxyproline in HIF-1 alpha by pVHL. Nature (2002) 3.78

The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature (2004) 3.77

Genetic loci influencing kidney function and chronic kidney disease. Nat Genet (2010) 3.75

Identification of a mutation in complement factor H-related protein 5 in patients of Cypriot origin with glomerulonephritis. Lancet (2010) 3.74

Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis. Mol Cell (2004) 3.73

Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J Clin Invest (2002) 3.70

Quantitative metabolome profiling of colon and stomach cancer microenvironment by capillary electrophoresis time-of-flight mass spectrometry. Cancer Res (2009) 3.50

A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc Natl Acad Sci U S A (2004) 3.48

FLT1 and its ligands VEGFB and PlGF: drug targets for anti-angiogenic therapy? Nat Rev Cancer (2008) 3.46

Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J Biol Chem (2006) 3.43

Chemistry-based functional proteomics reveals novel members of the deubiquitinating enzyme family. Chem Biol (2002) 3.43

VE-Cadherin-Cre-recombinase transgenic mouse: a tool for lineage analysis and gene deletion in endothelial cells. Dev Dyn (2006) 3.38

Expression of hypoxia-inducible factor-1alpha and -2alpha in hypoxic and ischemic rat kidneys. J Am Soc Nephrol (2002) 3.34

Treatment of motoneuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat Neurosci (2004) 3.31

Silencing or fueling metastasis with VEGF inhibitors: antiangiogenesis revisited. Cancer Cell (2009) 3.27

A vascular niche and a VEGF-Nrp1 loop regulate the initiation and stemness of skin tumours. Nature (2011) 3.25

Genome-wide association of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha DNA binding with expression profiling of hypoxia-inducible transcripts. J Biol Chem (2009) 3.23

Role of PlGF in the intra- and intermolecular cross talk between the VEGF receptors Flt1 and Flk1. Nat Med (2003) 3.17

Molecular mechanisms of lymphangiogenesis in health and disease. Cancer Cell (2002) 3.11

The GATA2 transcriptional network is requisite for RAS oncogene-driven non-small cell lung cancer. Cell (2012) 3.10

VEGF delivery with retrogradely transported lentivector prolongs survival in a mouse ALS model. Nature (2004) 3.08

Dynamic regulatory network controlling TH17 cell differentiation. Nature (2013) 3.07

An immunohistochemical procedure to detect patients with paraganglioma and phaeochromocytoma with germline SDHB, SDHC, or SDHD gene mutations: a retrospective and prospective analysis. Lancet Oncol (2009) 3.05

Role of PFKFB3-driven glycolysis in vessel sprouting. Cell (2013) 3.04

High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood (2011) 3.00

Predominant role of hypoxia-inducible transcription factor (Hif)-1alpha versus Hif-2alpha in regulation of the transcriptional response to hypoxia. Cancer Res (2003) 2.93

VEGF pathway genetic variants as biomarkers of treatment outcome with bevacizumab: an analysis of data from the AViTA and AVOREN randomised trials. Lancet Oncol (2012) 2.92

Progranulin functions as a neurotrophic factor to regulate neurite outgrowth and enhance neuronal survival. J Cell Biol (2008) 2.91

A family with erythrocytosis establishes a role for prolyl hydroxylase domain protein 2 in oxygen homeostasis. Proc Natl Acad Sci U S A (2006) 2.90

VEGF: once regarded as a specific angiogenic factor, now implicated in neuroprotection. Bioessays (2004) 2.83

Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney. EMBO J (2006) 2.80

Vascular endothelial growth factor is an important determinant of sepsis morbidity and mortality. J Exp Med (2006) 2.75

Conditional switching of VEGF provides new insights into adult neovascularization and pro-angiogenic therapy. EMBO J (2002) 2.74

Targeted inactivation of fh1 causes proliferative renal cyst development and activation of the hypoxia pathway. Cancer Cell (2007) 2.69

Targeting placental growth factor/neuropilin 1 pathway inhibits growth and spread of medulloblastoma. Cell (2013) 2.64

Regulation of glycolysis by Pdk functions as a metabolic checkpoint for cell cycle quiescence in hematopoietic stem cells. Cell Stem Cell (2013) 2.58

Signalling hypoxia by HIF hydroxylases. Biochem Biophys Res Commun (2005) 2.50

Aberrant succination of proteins in fumarate hydratase-deficient mice and HLRCC patients is a robust biomarker of mutation status. J Pathol (2011) 2.45

A deubiquitinating enzyme encoded by HSV-1 belongs to a family of cysteine proteases that is conserved across the family Herpesviridae. Mol Cell (2005) 2.43

Activation of the lectin DC-SIGN induces an immature dendritic cell phenotype triggering Rho-GTPase activity required for HIV-1 replication. Nat Immunol (2007) 2.43

Impaired angiogenesis and endochondral bone formation in mice lacking the vascular endothelial growth factor isoforms VEGF164 and VEGF188. Mech Dev (2002) 2.39

CXCL12 and vascular endothelial growth factor synergistically induce neoangiogenesis in human ovarian cancers. Cancer Res (2005) 2.38

VEGF receptor 2 endocytic trafficking regulates arterial morphogenesis. Dev Cell (2010) 2.37

First United Kingdom Heart and Renal Protection (UK-HARP-I) study: biochemical efficacy and safety of simvastatin and safety of low-dose aspirin in chronic kidney disease. Am J Kidney Dis (2005) 2.36

Protective role of reactive astrocytes in brain ischemia. J Cereb Blood Flow Metab (2007) 2.35

Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum. Genome Res (2006) 2.32

Expression of hypoxia-inducible factors in human renal cancer: relationship to angiogenesis and to the von Hippel-Lindau gene mutation. Cancer Res (2002) 2.31

Structure of factor-inhibiting hypoxia-inducible factor (HIF) reveals mechanism of oxidative modification of HIF-1 alpha. J Biol Chem (2002) 2.29

Further pharmacological and genetic evidence for the efficacy of PlGF inhibition in cancer and eye disease. Cell (2010) 2.26

Substantial histone reduction modulates genomewide nucleosomal occupancy and global transcriptional output. PLoS Biol (2011) 2.26

Common genetic variants at the 11q13.3 renal cancer susceptibility locus influence binding of HIF to an enhancer of cyclin D1 expression. Nat Genet (2012) 2.25

Regulation of E-cadherin expression by VHL and hypoxia-inducible factor. Cancer Res (2006) 2.24

Fbw7 controls neural stem cell differentiation and progenitor apoptosis via Notch and c-Jun. Nat Neurosci (2010) 2.23