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Disrupted propionate metabolism evokes transcriptional changes in the heart by increasing histone acetylation and propionylation

Abstract:
Propiogenic substrates and gut bacteria produce propionate, a post-translational protein modifier. In this study, we used a mouse model of propionic acidaemia (PA) to study how disturbances to propionate metabolism result in histone modifications and changes to gene expression that affect cardiac function. Plasma propionate surrogates were raised in PA mice, but female hearts manifested more profound changes in acyl-CoAs, histone propionylation and acetylation, and transcription. These resulted in moderate diastolic dysfunction with raised diastolic Ca2+, expanded end-systolic ventricular volume and reduced stroke volume. Propionate was traced to histone H3 propionylation and caused increased acetylation genome-wide, including at promoters of Pde9a and Mme, genes related to contractile dysfunction through downscaled cGMP signaling. The less severe phenotype in male hearts correlated with β-alanine buildup. Raising β-alanine in cultured myocytes treated with propionate reduced propionyl-CoA levels, indicating a mechanistic relationship. Thus, we linked perturbed propionate metabolism to epigenetic changes that impact cardiac function.
Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.1038/s44161-023-00365-0

Authors

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Institution:
University of Oxford
Division:
MSD
Department:
Physiology Anatomy & Genetics
Role:
Author
ORCID:
0000-0001-7203-0127
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
RDM
Sub department:
Weatherall Insti. of Molecular Medicine
Role:
Author
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
Physiology Anatomy & Genetics
Role:
Author


More from this funder
Funding agency for:
Swietach, P
Grant:
723997
More from this funder
Grant:
RG/15/9/31534
FS/16/59/32735
Funding agency for:
Park, KC
More from this funder
Funding agency for:
Choeng, YJ
Trefely, S
Grant:
P013406/1
More from this funder
Funding agency for:
Crump, NT
Milne, TA
Grant:
MC_UU_00016/6


Publisher:
Springer Nature
Journal:
Nature Cardiovascular Research More from this journal
Volume:
2
Issue:
12
Pages:
1221-1245
Publication date:
2023-11-23
Acceptance date:
2023-10-15
DOI:
EISSN:
2731-0590


Language:
English
Pubs id:
1544841
Local pid:
pubs:1544841
Deposit date:
2023-10-16
ARK identifier:

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