Hypoxia biology · Interactive figure

The same chemistry

Oxygen is not only a signal. It is a substrate for the enzymes that sense it, that make and break chromatin marks, and that decide which genes a cell can switch on. Move the oxygen dial and watch both pathways respond together.

21%O₂

Sea level · normoxia

PHD 100% · FIH 100% · TET 100% · KDM 100%

Nonlinear scale, expanding the low-oxygen range. Arrow keys adjust; Home and End jump to the extremes.

With oxygen present, the cell actively destroys its own hypoxia signal.

Without enough oxygen, the destruction machinery stalls and HIF survives.

PHD enzymes and FIH are Fe(II)- and 2-oxoglutarate-dependent dioxygenases that use molecular oxygen directly. When oxygen falls, their chemistry slows.

PHD enzymes, TET enzymes and JmjC histone demethylases all belong to the Fe(II)- and 2-oxoglutarate-dependent dioxygenase family. They use molecular oxygen as part of their reactions. When oxygen falls, these enzyme systems are affected in parallel, linking oxygen sensing directly to changes in gene regulation and chromatin.

Transcriptional

Stability, dimerisation and DNA binding

HIF-1 alpha stability and nuclear translocationIn normoxia, hydroxylated HIF-1 alpha is recognised by VHL, ubiquitinated and destroyed by the proteasome. As oxygen falls, HIF-1 alpha accumulates, moves into the nucleus, dimerises with ARNT, binds an HRE and drives transcription.cytoplasmnucleusVHLUb26SHIF-1α destroyedARNTHIF-1α5′-RCGTG-3′genesHIF-1α stabilised
Normoxia: HIF-1α is hydroxylated, recognised by VHL and destroyed. Hypoxia: it accumulates, enters the nucleus, dimerises with ARNT and binds HREs.

Normoxia — destructionactivestalled

Hypoxia — survival and outputoffactive

Isoform switch and modulation

Epigenomic

DNA and histone marks under the same oxygen dependence

DNA methylation and TET activityCpG sites along a DNA strand carry 5-methylcytosine and 5-hydroxymethylcytosine. As oxygen falls, TET activity decreases, 5hmC declines and methylation patterns shift.TET1/2/3● 5mC◌ 5hmC↓ O₂ → ↓ TET activity → less 5hmC
Histone methylation and JmjC demethylase activity Histone tails carry methylation marks. JmjC demethylases remove them using oxygen. When their activity falls in hypoxia, methylation can accumulate.H3 / H4H3K4me3H3K27me3JmjC KDMs↓ O₂ → ↓ KDM activity

Oxygen-sensitive and HIF-regulated KDMs

Different chemistry

Not every demethylase is an oxygen-dependent dioxygenase.

Context-dependentPseudohypoxia — changes without low oxygen

Mutations in IDH1/2, SDH or FH cause metabolite accumulation that inhibits 2-OG-dependent dioxygenases. Epigenetic changes can therefore occur without hypoxia at all.

Succinate and 2-hydroxyglutarate compete with 2-oxoglutarate, inhibiting TET and JmjC enzymes. This pseudohypoxic state demonstrates the shared chemistry underlying both pathways.

Genes: IDH1, IDH2, SDH, FH

Emerging mechanisms

Labelled Emerging: active areas where causality is still being established.

Both layers are hidden. Enable the transcriptional or epigenomic layer above to view the pathway.

Full text and referencesEvery node in this figure, with evidence status and sources
EstablishedContext-dependentEmergingEvidence status, not a ranking.

O₂

Established

Molecular oxygen is a co-substrate, not only a signal

Oxygen is consumed directly by Fe(II)- and 2-oxoglutarate-dependent dioxygenases. Its availability therefore sets the rate of the reactions these enzymes perform.

Related

Kaelin WG 2008Semenza GL 2014

PHD1/2/3

Established

Gene EGLN1/2/3

Prolyl hydroxylases gate HIF stability

PHD enzymes hydroxylate proline residues in HIF-1α and HIF-2α. This modification is required for VHL recognition and rapid degradation.

Deeper explanation

PHD2 (EGLN1) is the principal regulator of HIF-1α in most cell types. PHD activity depends on oxygen, Fe(II), ascorbate and 2-oxoglutarate. The relative oxygen sensitivities of PHD1, PHD2 and PHD3 differ between tissues.

Related

Kaelin WG 2008Semenza GL 2014

FIH

Established

Gene HIF1AN

Asparaginyl hydroxylation tunes HIF activity

FIH hydroxylates asparagine 803 in HIF-1α, blocking recruitment of the p300/CBP co-activators.

Deeper explanation

Because FIH restrains HIF activity rather than its stability, loss of FIH activity in hypoxia affects which targets are switched on, not simply whether HIF is present.

Related

Kaelin WG 2008Lando D 2002

VHL

Established

Gene VHL

VHL reads the hydroxyl mark

The von Hippel–Lindau E3 ubiquitin ligase complex recognises hydroxylated HIF-1α and targets it for ubiquitination.

Related

Kaelin WG 2008Ivan M 2001Jaakkola P 2001

Proteasome

Established

Rapid destruction keeps HIF low

When oxygen and PHD activity are sufficient, HIF-1α is destroyed within minutes, so transcriptional output stays low.

Semenza GL 2014Kaelin WG 2008

HIF-1α

Established

Gene HIF1A

HIF-1α accumulates when hydroxylation fails

As oxygen falls, PHD activity drops. HIF-1α is no longer marked for degradation, so it accumulates in the cytoplasm, translocates to the nucleus and dimerises with ARNT.

Related

Semenza GL 2014Kaelin WG 2008

HIF-1β / ARNT

Established

Gene ARNT

The constitutive partner

ARNT is expressed independently of oxygen. The HIF-1α–ARNT heterodimer is the active transcription factor.

Semenza GL 2014

HRE

Established

A short DNA motif recruits the dimer

The hypoxia response element contains the core sequence 5′-RCGTG-3′. HIF dimers bind HREs in the enhancers and promoters of target genes.

Semenza GL 2014

p300 / CBP

Established

Genes EP300, CREBBP

Co-activators set transcriptional output

Once bound to DNA, HIF recruits the p300/CBP acetyltransferases, which acetylate chromatin and help assemble the transcriptional machinery.

Related

Semenza GL 2014

Transcription

Established

Aerobic metabolism is re-tuned

HIF drives glycolytic enzymes, angiogenic factors such as VEGF and many other targets, changing how cells use oxygen and nutrients.

Semenza GL 2014

HIF-2α

Established

Gene EPAS1

The chronic partner

HIF-2α shares the PHD–VHL control system but drives a partly distinct programme, including erythropoietin in the kidney. It often dominates the later phase of the response.

Semenza GL 2014

HIF-3α

Context-dependent

Gene HIF3A

Predominantly regulatory

HIF-3α is expressed as multiple splice variants and is best understood as a negative or modulatory regulator of the response rather than a classic activator.

Semenza GL 2014

TET1/2/3

Established

Genes TET1, TET2, TET3

Oxygen is a substrate for DNA demethylation

TET enzymes are Fe(II)- and 2-oxoglutarate-dependent dioxygenases that oxidise 5-methylcytosine towards 5-hydroxymethylcytosine and further products as part of active DNA demethylation. In hypoxia, reduced TET activity is associated with altered DNA methylation.

Deeper explanation

The DNA methylation response is region-specific. Some loci gain methylation while others lose it, so hypoxic changes should not be described as a uniform global shift.

Related

Thienpont B 2016Kaelin WG 2008

5mC / 5hmC

Context-dependent

Methylation balance shifts

When TET activity falls, 5-methylcytosine is less efficiently oxidised, so 5hmC can decline and methylation patterns can shift. The effect differs between genomic regions rather than being uniform.

Related

Thienpont B 2016

JmjC KDMs

Established

Genes KDM6A, KDM5A, KDM4A

Histone demethylases are also oxygen-dependent

JmjC-domain histone demethylases use the same Fe(II)/2-OG chemistry as PHD and TET enzymes. Hypoxia causes rapid changes in histone methylation that can in turn influence HIF signalling.

Deeper explanation

Batie and colleagues reported rapid hypoxia-induced changes to histone methylation, while Chakraborty and colleagues showed that KDM6A can sense oxygen directly to control chromatin and cell fate.

Related

Batie M 2019Chakraborty AA 2019

H3K4me3 / H3K27me3

Context-dependent

Repressive and active marks accumulate

Reduced demethylase activity can cause histone methylation to accumulate. These marks can influence chromatin accessibility and gene expression.

Related

Batie M 2019Chakraborty AA 2019

KDM6A / UTX

Context-dependent

Gene KDM6A

A demethylase that directly senses oxygen

KDM6A can behave as a direct oxygen sensor controlling chromatin state and cell fate, linking oxygen availability to developmental decisions.

Chakraborty AA 2019

KDM5A

Context-dependent

Gene KDM5A

Sensitive oxygen-dependent regulator

Some JmjC enzymes are proposed to act as unusually sensitive oxygen-dependent regulators of chromatin, adding to the complexity of the response.

Chakraborty AA 2019Batie M 2019

LSD1 / KDM1A

Established

Gene KDM1A

A demethylase with different chemistry

LSD1/KDM1A is not a JmjC demethylase. It is a FAD-dependent amine oxidase that uses a distinct catalytic mechanism and is not directly oxygen-dependent in the same way.

Related

Batie M 2019

KDM3A / KDM4A

Context-dependent

Genes KDM3A, KDM4A

Feedback from HIF to chromatin

Some KDMs, including KDM3A/JMJD1A and KDM4 family members, are themselves HIF target genes. The epigenomic and transcriptional responses therefore feed into one another.

Related

Batie M 2019Semenza GL 2014

Pseudohypoxia

Context-dependent

Genes IDH1, IDH2, SDH, FH

The relationship is chemical, not only transcriptional

Mutations in IDH1/2, SDH or FH cause metabolite accumulation that inhibits 2-OG-dependent dioxygenases. Epigenetic changes can therefore occur without hypoxia at all.

Deeper explanation

Succinate and 2-hydroxyglutarate compete with 2-oxoglutarate, inhibiting TET and JmjC enzymes. This pseudohypoxic state demonstrates the shared chemistry underlying both pathways.

Kaelin WG 2008Thienpont B 2016

miR-210

Established

Gene MIR210

The canonical hypoxamiR

miR-210 is a hypoxia-induced microRNA that fine-tunes mitochondrial metabolism by targeting transcripts including ISCU, COX10 and GPD1L.

Chan SY 2010Semenza GL 2014

lncRNAs

Context-dependent

Genes NEAT1, MALAT1, HIF1A-AS2

Long non-coding RNA layer

Several long non-coding RNAs are hypoxia-responsive and contribute to chromatin organisation, splicing and the stability of HIF transcripts.

Semenza GL 2014

m6A / ALKBH5

Context-dependent

Gene ALKBH5

Oxygen-sensitive RNA modification

ALKBH5 is a Fe(II)- and 2-OG-dependent dioxygenase that removes the m6A mark from RNA, giving another link between oxygen and gene regulation beyond chromatin.

Zheng G 2013Semenza GL 2014

Histone lactylation

Emerging

Metabolite-derived chromatin marks

Lactate produced by increased glycolysis can be deposited as lactyl groups on histones, offering a metabolic route to chromatin regulation in hypoxia.

Zhang D 2019

Acetyl-CoA / acetylation

Emerging

Metabolite availability shapes acetylation

Histone acetylation depends on acetyl-CoA availability, which is altered by hypoxic metabolic rewiring. This is an area of active investigation.

Zhang D 2019

Intermittent vs sustained hypoxia

Emerging

Pattern matters

Repeated cycles of hypoxia and reoxygenation can produce different transcriptional and epigenomic outcomes from sustained hypoxia, and are used experimentally in therapeutic protocols.

Semenza GL 2014

Hypoxic memory

Emerging

Persistent programming

Developmental or repeated hypoxic exposure may leave lasting chromatin and methylation changes that alter later responses, sometimes described as hypoxic memory or developmental programming.

Thienpont B 2016Semenza GL 2014

Carotid body

Established

The first alarm, within seconds

Glomus cells in the carotid body detect falling oxygen and rapidly increase respiratory drive through ion-channel and mitochondrial mechanisms, triggering the ventilatory response.

Semenza GL 2014

Lungs

Established

The only vascular bed that constricts

Hypoxic pulmonary vasoconstriction narrows pulmonary arterioles to divert blood towards better-ventilated regions. It is unique among vascular beds, which otherwise dilate when oxygen falls.

Related

Sylvester JT 2012

HAPE

Established

When the response turns pathological

Exaggerated and uneven pulmonary vasoconstriction raises capillary pressure and contributes to high-altitude pulmonary oedema, a life-threatening condition.

Bärtsch P 2013Sylvester JT 2012

Brain

Established

Swelling and sickness

Cerebral vasodilation, altered vascular permeability and impaired autoregulation contribute to acute mountain sickness and, in severe cases, high-altitude cerebral oedema.

Bärtsch P 2013

Kidney

Established

The oxygen meter of the blood

Renal interstitial cells sense reduced oxygen and increase erythropoietin production, largely under HIF-2α control, linking oxygen sensing to red cell mass.

Related

Semenza GL 2014

Liver / gut

Context-dependent

Freeing up iron

Hepcidin suppression during hypoxia increases dietary iron absorption and its release from stores, supporting increased erythropoiesis.

Semenza GL 2014

Bone marrow

Established

Building the oxygen carriers

Rising erythropoietin drives erythroid progenitor expansion and reticulocytosis, gradually raising haemoglobin concentration and oxygen-carrying capacity.

Semenza GL 2014

Heart / skeletal muscle

Established

Rewiring metabolism

HIF targets increase glucose uptake and glycolysis and induce PDK1, which restrains mitochondrial oxygen consumption. Longer-term adaptation includes changes in mitochondrial content and mitophagy.

Semenza GL 2014

Immune cells

Context-dependent

Inflammation gets louder

Hypoxia interacts with inflammatory signalling, including HIF/NF-κB relationships, while extracellular adenosine provides a regulatory counterweight.

Semenza GL 2014

Population adaptation

Established

Genes EPAS1, EGLN1

Evolution, not acclimatisation

Tibetans carry variants near EPAS1 (HIF-2α) and EGLN1 (PHD2) associated with altered haemoglobin and ventilatory responses; the EPAS1 haplotype shows evidence of Denisovan-like introgression. Andean and Ethiopian highlanders show partly distinct signals.

Deeper explanation

These are population-genetic adaptations that arose over many generations. They are not the next step of an individual's physiological acclimatisation and should be read as a separate axis of the story.

Huerta-Sánchez E 2014Semenza GL 2014

References

  1. Semenza GL. Oxygen sensing, hypoxia-inducible factors, and disease pathophysiology. Annual Review of Pathology. 2014.
  2. Kaelin WG, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Molecular Cell. 2008.
  3. Thienpont B, et al.. Tumour hypoxia causes DNA hypermethylation by reducing TET activity. Nature. 2016.
  4. Batie M, et al.. Hypoxia induces rapid changes to histone methylation and reprograms chromatin. Science. 2019.
  5. Chakraborty AA, et al.. Histone demethylase KDM6A directly senses oxygen to control chromatin and cell fate. Science. 2019.
  6. Huerta-Sánchez E, et al.. Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA. Nature. 2014.
  7. Bärtsch P, Swenson ER. Acute high-altitude illnesses. New England Journal of Medicine. 2013.
  8. Sylvester JT, et al.. Hypoxic pulmonary vasoconstriction. Physiological Reviews. 2012.
  9. Zhang D, et al.. Metabolic regulation of gene expression by histone lactylation. Nature. 2019.
  10. Jaakkola P, et al.. Targeting of HIF-α to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science. 2001.
  11. Ivan M, et al.. HIFα targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science. 2001.
  12. Lando D, et al.. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes & Development. 2002.
  13. Chan SY, Loscalzo J. MicroRNA-210: a unique and pleiotropic hypoxamir. Cell Cycle. 2010.
  14. Zheng G, et al.. ALKBH5 is a mammalian RNA demethylase that impacts RNA metabolism and mouse fertility. Molecular Cell. 2013.