Cited by 313Erythropoietin and Anemia TreatmentCancer, Hypoxia, and MetabolismAcute Kidney Injury Research

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Mechanisms of hypoxia signalling: new implications for nephrology

Schödel, Johannes, Ratcliffe, Peter J.·2019·Nature Reviews Nephrology

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Abstract

Studies of the regulation of erythropoietin (EPO) production by the liver and kidneys, one of the classical physiological responses to hypoxia, led to the discovery of human oxygen-sensing mechanisms, which are now being targeted therapeutically. The oxygen-sensitive signal is generated by 2-oxoglutarate-dependent dioxygenases that deploy molecular oxygen as a co-substrate to catalyse the post-translational hydroxylation of specific prolyl and asparaginyl residues in hypoxia-inducible factor (HIF), a key transcription factor that regulates transcriptional responses to hypoxia. Hydroxylation of HIF at different sites promotes both its degradation and inactivation. Under hypoxic conditions, these processes are suppressed, enabling HIF to escape destruction and form active transcriptional complexes at thousands of loci across the human genome. Accordingly, HIF prolyl hydroxylase inhibitors stabilize HIF and stimulate expression of HIF target genes, including the EPO gene. These molecules activate endogenous EPO gene expression in diseased kidneys and are being developed, or are already in clinical use, for the treatment of renal anaemia. In this Review, we summarize information on the molecular circuitry of hypoxia signalling pathways underlying these new treatments and highlight some of the outstanding questions relevant to their clinical use.

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The Endothelial Landscape and Its Role in Von Hippel–Lindau Disease
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“HIF’s binding to promoters and enhancers of target genes regulates the hypoxic survival response [11].”
Background
Disturbance of Hypoxia Response and Its Implications in Kidney Diseases
Li, Z., Wang, B., Wen, Y., Wu, Q., Lv, L., & Liu, B. (2022) · Antioxidants and Redox Signaling · doi:10.1089/ars.2021.0271 · Cited by 11
The interplay between H19 and HIF-1α in mitochondrial dysfunction in myocardial infarction
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Postoperative pulmonary complications in patients undergoing aortic surgery: A single-center retrospective study
Yan, Y. Y., Zhang, X., Yao, Y.-T., & The Evidence in Cardiovascular Anesthesia (EICA) Group (2023) · Medicine · doi:10.1097/md.0000000000034668 · Cited by 10
“[20] In addition, diabetes mellitus was also reported as an independent risk factor for PPCs after cardiac surgery in some studies.”
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The Mechanism of Acupuncture Regulating Autophagy: Progress and Prospect
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“Under hypoxic conditions, mitochondrial adenosine triphosphate (ATP) production is reduced in aerobic organisms, which cannot perform everyday life activities through cellular respiration [12].”
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Li, Z., Shen, L., Tu, Y., Lü, S., & Liu, B.-C. (2025) · Chinese Medical Journal · doi:10.1097/cm9.0000000000003470 · Cited by 10
“[10,11] The HIF-PHI could stabilize HIF expression by inhibiting PHD and preventing N-terminal hydroxylation of HIF-α and subsequent HIF degradation.”
Integrated analysis reveals effects of bioactive ingredients from Limonium Sinense (Girard) Kuntze on hypoxia-inducible factor (HIF) activation
Zhao, H., Wang, S., Zhou, Y., Ertay, A., Williamson, P. T. F., Ewing, R. M., Tang, X., Wang, J., & Wang, Y. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.994036 · Cited by 10
“Studies have shown that regulating HIF levels provide novel therapeutic strategies for a broad variety of diseases, including anemia (De Bels et al., 2011; Semenza, 2012; Schodel and Ratcliffe, 2019).”
Background
HIF-PHD inhibitor regulates the function of group2 innate lymphoid cells and polarization of M2 macrophages
Nagashima, R., Ishikawa, H., Kuno, Y., Kohda, C., & Iyoda, M. (2023) · Scientific Reports · doi:10.1038/s41598-023-29161-3 · Cited by 12
Hypoxia signaling in bone physiology and energy metabolism
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Cardiovascular safety and efficacy of vadadustat for the treatment of anemia in non-dialysis-dependent CKD: Design and baseline characteristics
Chertow, G. M., Pérgola, P. E., Agarwal, R., Block, G. A., Farag, Y. M. K., Jardine, A. G., Koury, M. J., Luo, W. F., Khawaja, Z., Lewis, E. F., et al. (2020) · American Heart Journal · doi:10.1016/j.ahj.2020.10.068 · Cited by 10
The Association between Serum Hemoglobin and Renal Prognosis of IgA Nephropathy
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“CKD and anemia are known to be related through various mechanisms, and recent studies show that anemia might lead to hypoxic injury in end-organs, including the kidneys, through the hypoxia-inducible factor (HIF) signaling pathway [14,15].”
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RETSAT Mutation Selected for Hypoxia Adaptation Inhibits Tumor Growth
Jiang, X., He, Y., Shen, Q., Duan, L., Yuan, Y., Tang, L., Shi, Y., Liu, B., Zhai, H., Shi, P., et al. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.744992 · Cited by 9
“These factors include hypoxia-inducible factors (HIFs), the von Hippel–Lindau (VHL) and prolyl hydroxylases (PHD1/2/3 or so-called EglN1/2/3, respectively) of the 2-oxoglutarate (or α-ketoglutarate) dioxygenase super-family (Schödel and Ratcliffe, 2019), which provide valuable therapeutic targets for various types of…”
Background
EPO Enhances Adaptation to Hypoxic Environment in the Freshwater Teleost ( Micropterus salmoides ) through the PI3K/AKT Pathway
Yan, H., Zhao, L., He, K., Liu, H., Zhang, C., Liu, Q., Song, K., Yang, H., Xu, T., & Yang, S. Y. (2025) · Environmental Science & Technology · doi:10.1021/acs.est.5c00093 · Cited by 9
Hypertension Induced by Hypoxia‐Inducible Factor Prolyl Hydroxylase Inhibitors in Treating Anemia in Patients With Chronic Kidney Disease: A Mini‐Review
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Effect of hypoxia on the mucus system and intragastric microecology in the gastrointestinal tract
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Acidosis attenuates the hypoxic stabilization of HIF-1α by activating lysosomal degradation
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Phosphate sensing in health and disease
Zechner, C., & Rhee, E. P. (2024) · Current Opinion in Nephrology & Hypertension · doi:10.1097/mnh.0000000000000984 · Cited by 8
Kapasitas Vital Paru Berkorelasi Positif dengan Kemampuan Tahan Nafas pada Laki-Laki Usia 19-25 Tahun
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Defining the functionally sufficient regulatory region and liver-specific roles of the erythropoietin gene by transgene complementation
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From Proteomic Mapping to Invasion-Metastasis-Cascade Systemic Biomarkering and Targeted Drugging of Mutant BRAF-Dependent Human Cutaneous Melanomagenesis
Giannopoulou, A. F., Velentzas, A. D., Anagnostopoulos, A. K., Agalou, A., Papandreou, N. C., Katarachia, S. A., Koumoundourou, D. G., Konstantakou, E. G., Pantazopoulou, V. I., Delis, A. D., et al. (2021) · Cancers · doi:10.3390/cancers13092024 · Cited by 8
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Efficacy and safety of vadadustat compared to darbepoetin alfa on anemia in patients with chronic kidney disease: a meta-analysis
Huang, Q., Liao, Z., Liu, X., Xia, Y., & Wang, J. (2022) · International Urology and Nephrology · doi:10.1007/s11255-022-03316-z · Cited by 8
“The corresponding inhibitors (HIF-PHIs) are a new class of drugs that activate HIF transcription factors and have broad therapeutic potential in clinical medicine [10].”
Background
Safety and Efficacy of Hypoxia-Inducible Factor-Prolyl Hydroxylase Inhibitors vs. Erythropoietin-Stimulating Agents in Treating Anemia in Renal Patients (With or Without Dialysis): A Meta-Analysis and Systematic Review
Damarlapally, N., Thimmappa, V., Irfan, H., Sikandari, M. H., MADHU, K., Desai, A., Pavani, P., Zakir, S. J., Gupta, M., Khosa, M. M., et al. (2023) · Cureus · doi:10.7759/cureus.47430 · Cited by 11
Oxygen sensing in the kidney
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Comparative effectiveness and acceptability of HIF prolyl-hydroxylase inhibitors versus for anemia patients with chronic kidney disease undergoing dialysis: a systematic review and network meta-analysis
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“HIF-PHIs are a new class of drugs that can activate HIF transcription factors and may have broad therapeutic potential in clinical practice (Schödel and Ratcliffe, 2019).”
Background
Mitochondrial iron regulation as an emerging target in ischemia/reperfusion injury during kidney transplantation
Qi, Y., Hu, M., Wang, Z., & Shang, W. (2023) · Biochemical Pharmacology · doi:10.1016/j.bcp.2023.115725 · Cited by 7
Progesterone receptor membrane component 2 is critical for human placental extravillous trophoblast invasion
Yokouchi-Konishi, T., Liu, Y., & Feng, L. (2023) · Biology of Reproduction · doi:10.1093/biolre/ioad109 · Cited by 7
“Under non-hypoxic conditions, HIF1 α subunits have a very short half-life, only a few minutes [36], through ubiquitin–proteasome pathway-mediated protein degradation [37– 40].”
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Comparative Analysis of Real-World Efficacy and Safety of Hypoxia-Inducible Factor Prolyl-Hydroxylase Inhibitors in Kidney Transplant Recipients Versus Nontransplant Individuals: A Single-Center Study
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Can Erythropoietin Reduce Hypoxemic Neurological Damages in Neonates With Congenital Heart Defects?
Ottolenghi, S., Milano, G., Dei, M., Findley, T. O., Paroni, R. C., & Corno, A. F. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.770590 · Cited by 7
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Background
Signal transduction mechanisms in heme-based globin-coupled oxygen sensors with a focus on a histidine kinase (AfGcHK) and a diguanylate cyclase (YddV or EcDosC)
Vávra, J., Sergunin, A., Jeřábek, P., Shimizu, T., & Martínková, M. (2022) · Biological Chemistry · doi:10.1515/hsz-2022-0185 · Cited by 7
Jian-Pi-Yi-Shen formula ameliorates renal fibrosis-induced anemia in rats with chronic kidney disease
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Intestine epithelial–specific hypoxia-inducible factor-1α overexpression ameliorates western diet–induced MASLD
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Hypoxia-inducible factor-prolyl hydroxylase inhibitor Roxadustat (FG-4592) reduces renal fibrosis in Dahl salt-sensitive rats
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“8,9 Nevertheless, the intricate molecular mechanisms driving hypoxia-induced HCC progression remain predominantly unclear, warranting further studies for a comprehensive understanding.”
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A pilot study to evaluate the changes in venous blood gas parameters and hypoxia biomarkers in health care workers using different kinds of masks
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“[10] Among the various studied molecular mechanisms involved in the response to hypoxia at the cellular level, hypoxia-inducible factor-α (HIF-α) and erythropoietin (EPO) are used as key markers to detect hypoxia.[11] Therefore, measuring venous blood gas parameters along with measurement of oxygenation saturation (us…”
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“HIF⁃1α and HIF⁃2α all mediate the transcriptional response in hypoxia, but their distribution, transcriptional target and oxygen dependence are different (Schödel and Ratcliffe, 2019).”
Background
The effect of physical exercise on vital lung capacity in Tapak Suci athletes
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Targeting hypoxia-related metabolism molecules: How to improve tumour immune and clinical treatment?
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Authors: Schödel, J., & Ratcliffe, P. J.
Affiliations: Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
The Francis Crick Institute (GB)
Corresponding author: Ratcliffe, Peter J.
ORCID: Schödel, Johannes
Ratcliffe, Peter J.
Venue: Nature Reviews Nephrology
Publisher: Springer Science and Business Media LLC
Published: 2019-09-05
Volume: 15
Issue: 10
Pages: 641-659
ISSN: 1745-8323 (ISSN-L)
1759-5061
1759-507X
DOI: 10.1038/s41581-019-0182-z
OpenAlex: W2971880737
Cited by: 309
References: 255
Citations by year: 2026: 22 · 2025: 36 · 2024: 48 · 2023: 64 · 2022: 53 · 2021: 54 · 2020: 31 · 2019: 1
FWCI: 5.53
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Reviews Nephrology (publishedVersion)
PubMed (publishedVersion)
Funders: Wellcome Trust (FC001501)
Cancer Research UK (FC001501)
British Heart Foundation (RG/11/1/28684)
Topics: Health Sciences › Medicine › Hematology › Erythropoietin and Anemia Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
Health Sciences › Medicine › Nephrology › Acute Kidney Injury Research
Keywords: hypoxia signaling, hypoxia-inducible factor, prolyl hydroxylase inhibitors, erythropoietin, anemia of chronic kidney disease, 2-oxoglutarate-dependent dioxygenase, oxygen sensing, kidney disease, HIF target genes
MeSH terms: Animals, Hypoxia, Humans, Kidney, Kidney Diseases, Hypoxia-Inducible Factor 1

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Mechanisms of hypoxia signalling: new implications for nephrology

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