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Fatty acids prevent Hypoxia-Inducible Factor 1α signalling through decreased succinate in diabetes

Abstract:

Hypoxia-inducible factor 1α (HIF1α) is activated following myocardial infarction (MI), and is critical for cardiomyocyte survival in hypoxia. Patients with type 2 diabetes have poorer prognosis post-MI, which is associated with abnormal cardiac fatty acid (FA) metabolism. We questioned whether increased FA metabolism prevented HIF1α activation during myocardial ischemia and downstream adaptation in diabetes.

Type 2 diabetic rat hearts had decreased HIF1α protein accumulation following ischemia, with ischemic HIF1α levels correlating negatively with plasma FAs. HIF1α accumulation and downstream metabolic adaptation to hypoxia were suppressed in insulin-resistant cardiomyocytes. This blunted adaptation to hypoxia was due to increased FAs, as long chain FAs palmitate and oleate prevented HIF1α accumulation in hypoxia in a concentration-dependent manner, which could be reversed by blocking FA uptake. FA exerted their effects by decreasing intracellular succinate, an inhibitor of the regulatory HIF hydroxylases. HIF1α stabilisation by succinate was derived from malate-aspartate shuttle activity coupled to glycolysis, and facilitated by reverse succinate dehydrogenase activity, as decreasing flux through these pathways during hypoxia decreased HIF1α levels. In contrast, supplementing succinate in insulin resistant cells increased HIF1α accumulation. Pharmacologic inhibition of the HIF hydroxylases using dimethyloxalylglycine (DMOG) promoted HIF1α accumulation in insulin resistance, and in vivo treatment with DMOG improved post-ischemic recovery of cardiac function in diabetes.

In conclusion, elevated FAs prevent cardiac HIF1α activation by decreasing succinate concentrations, resulting in impaired adaptation to ischemia and hypoxia in diabetes. Pharmacologically overriding this HIF1α inhibition improves recovery of the diabetic heart following an ischemic insult.

Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.1016/j.jacbts.2018.04.005

Authors

More by this author
Institution:
University of Oxford
Division:
Medical Sciences Division
Department:
Physiology Anatomy and Genetics
Role:
Author
More by this author
Institution:
University of Oxford
Division:
Medical Sciences Division
Department:
Physiology Anatomy and Genetics
Role:
Author
More by this author
Institution:
University of Oxford
Division:
Medical Sciences Division
Department:
Physiology Anatomy and Genetics
Role:
Author
More by this author
Institution:
University of Oxford
Division:
Medical Sciences Division
Department:
Physiology Anatomy and Genetics
Role:
Author
More by this author
Institution:
University of Oxford
Division:
Medical Sciences Division
Department:
Physiology Anatomy and Genetics
Role:
Author


Publisher:
Elsevier
Journal:
JACC: Basic to Translational Science More from this journal
Volume:
3
Issue:
4
Pages:
485-498
Publication date:
2018-08-27
Acceptance date:
2018-05-10
DOI:
EISSN:
2452-302X
ISSN:
2452-302X


Pubs id:
pubs:853037
UUID:
uuid:62bfdb0b-593f-4600-86fa-6276ca37e8c3
Local pid:
pubs:853037
Deposit date:
2018-05-21
ARK identifier:

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