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Sci. STKE, 18 October 2005
Vol. 2005, Issue 306, p. re12
[DOI: 10.1126/stke.3062005re12]


Integration of Oxygen Signaling at the Consensus HRE

Roland H. Wenger*, Daniel P. Stiehl, and Gieri Camenisch

Institute of Physiology and Center for Integrative Human Physiology (CIHP), University of Zürich, CH-8057 Zürich, Switzerland.

Abstract: The hypoxia-inducible factor 1 (HIF-1) was initially identified as a transcription factor that regulated erythropoietin gene expression in response to a decrease in oxygen availability in kidney tissue. Subsequently, a family of oxygen-dependent protein hydroxylases was found to regulate the abundance and activity of three oxygen-sensitive HIFα subunits, which, as part of the HIF heterodimer, regulated the transcription of at least 70 different effector genes. In addition to responding to a decrease in tissue oxygenation, HIF is proactively induced, even under normoxic conditions, in response to stimuli that lead to cell growth, ultimately leading to higher oxygen consumption. The growing cell thus profits from an anticipatory increase in HIF-dependent target gene expression. Growth stimuli–activated signaling pathways that influence the abundance and activity of HIFs include pathways in which kinases are activated and pathways in which reactive oxygen species are liberated. These pathways signal to the HIF protein hydroxylases, as well as to HIF itself, by means of covalent or redox modifications and protein-protein interactions. The final point of integration of all of these pathways is the hypoxia-response element (HRE) of effector genes. Here, we provide comprehensive compilations of the known growth stimuli that promote increases in HIF abundance, of protein-protein interactions involving HIF, and of the known HIF effector genes. The consensus HRE derived from a comparison of the HREs of these HIF effectors will be useful for identification of novel HIF target genes, design of oxygen-regulated gene therapy, and prediction of effects of future drugs targeting the HIF system.

*Corresponding author. Institute of Physiology and Center for Integrative Human Physiology (CIHP), University of Zürich-Irchel, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland. E-Mail: roland.wenger{at}

Citation: R. H. Wenger, D. P. Stiehl, G. Camenisch, Integration of Oxygen Signaling at the Consensus HRE. Sci. STKE 2005, re12 (2005).

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Hypoxia Up-Regulates Hypoxia-Inducible Factor-1{alpha} Transcription by Involving Phosphatidylinositol 3-Kinase and Nuclear Factor {kappa}B in Pulmonary Artery Smooth Muscle Cells.
R. S. BelAiba, S. Bonello, C. Zahringer, S. Schmidt, J. Hess, T. Kietzmann, and A. Gorlach (2007)
Mol. Biol. Cell 18, 4691-4697
   Abstract »    Full Text »    PDF »
Oxygen-dependent ATF-4 stability is mediated by the PHD3 oxygen sensor.
J. Koditz, J. Nesper, M. Wottawa, D. P. Stiehl, G. Camenisch, C. Franke, J. Myllyharju, R. H. Wenger, and D. M. Katschinski (2007)
Blood 110, 3610-3617
   Abstract »    Full Text »    PDF »
From critters to cancers: bridging comparative and clinical research on oxygen sensing, HIF signaling, and adaptations towards hypoxia.
D. Hoogewijs, N. B. Terwilliger, K. A. Webster, J. A. Powell-Coffman, S. Tokishita, H. Yamagata, T. Hankeln, T. Burmester, K. T. Rytkonen, M. Nikinmaa, et al. (2007)
Integr. Comp. Biol. 47, 552-577
   Abstract »    Full Text »    PDF »
Myocardial hypoxia-inducible HIF-1{alpha}, VEGF, and GLUT1 gene expression is associated with microvascular and ICAM-1 heterogeneity during endotoxemia.
R. M. Bateman, C. Tokunaga, T. Kareco, D. R. Dorscheid, and K. R. Walley (2007)
Am J Physiol Heart Circ Physiol 293, H448-H456
   Abstract »    Full Text »    PDF »
Hypoxia-inducible Factor-1 (HIF-1) Is a Transcriptional Activator of the TrkB Neurotrophin Receptor Gene.
L. K. Martens, K. M. Kirschner, C. Warnecke, and H. Scholz (2007)
J. Biol. Chem. 282, 14379-14388
   Abstract »    Full Text »    PDF »
Glycogen Synthase Kinase 3 Phosphorylates Hypoxia-Inducible Factor 1{alpha} and Mediates Its Destabilization in a VHL-Independent Manner.
D. Flugel, A. Gorlach, C. Michiels, and T. Kietzmann (2007)
Mol. Cell. Biol. 27, 3253-3265
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Reactive Oxygen Species Activate the HIF-1{alpha} Promoter Via a Functional NF{kappa}B Site.
S. Bonello, C. Zahringer, R. S. BelAiba, T. Djordjevic, J. Hess, C. Michiels, T. Kietzmann, and A. Gorlach (2007)
Arterioscler Thromb Vasc Biol 27, 755-761
   Abstract »    Full Text »    PDF »
Glucose-Stimulated Insulin Production in Mice Deficient for the PAS Kinase PASKIN.
E. Borter, M. Niessen, R. Zuellig, G. A. Spinas, P. Spielmann, G. Camenisch, and R. H. Wenger (2007)
Diabetes 56, 113-117
   Abstract »    Full Text »    PDF »
Translational Control of Collagen Prolyl 4-Hydroxylase-{alpha}(I) Gene Expression under Hypoxia.
M. Fahling, R. Mrowka, A. Steege, G. Nebrich, A. Perlewitz, P. B. Persson, and B. J. Thiele (2006)
J. Biol. Chem. 281, 26089-26101
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Hypoxia Modifies the Transcriptome of Primary Human Monocytes: Modulation of Novel Immune-Related Genes and Identification Of CC-Chemokine Ligand 20 as a New Hypoxia-Inducible Gene.
M. C. Bosco, M. Puppo, C. Santangelo, L. Anfosso, U. Pfeffer, P. Fardin, F. Battaglia, and L. Varesio (2006)
J. Immunol. 177, 1941-1955
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