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Effects of canagliflozin on human myocardial redox signalling: clinical implications

Abstract:
Aims Recent clinical trials indicate that sodium-glucose cotransporter 2 (SGLT2) inhibitors improve cardiovascular outcomes in heart failure patients, but the underlying mechanisms remain unknown. We explored the direct effects of canagliflozin, an SGLT2 inhibitor with mild SGLT1 inhibitory effects, on myocardial redox signalling in humans. Methods and results Study 1 included 364 patients undergoing cardiac surgery. Right atrial appendage biopsies were harvested to quantify superoxide (⁠O.−2⁠) sources and the expression of inflammation, fibrosis, and myocardial stretch genes. In Study 2, atrial tissue from 51 patients was used ex vivo to study the direct effects of canagliflozin on NADPH oxidase activity and nitric oxide synthase (NOS) uncoupling. Differentiated H9C2 and primary human cardiomyocytes (hCM) were used to further characterize the underlying mechanisms (Study 3). SGLT1 was abundantly expressed in human atrial tissue and hCM, contrary to SGLT2. Myocardial SGLT1 expression was positively associated with O.−2 production and pro-fibrotic, pro-inflammatory, and wall stretch gene expression. Canagliflozin reduced NADPH oxidase activity via AMP kinase (AMPK)/Rac1signalling and improved NOS coupling via increased tetrahydrobiopterin bioavailability ex vivo and in vitro. These were attenuated by knocking down SGLT1 in hCM. Canagliflozin had striking ex vivo transcriptomic effects on myocardial redox signalling, suppressing apoptotic and inflammatory pathways in hCM. Conclusions We demonstrate for the first time that canagliflozin suppresses myocardial NADPH oxidase activity and improves NOS coupling via SGLT1/AMPK/Rac1 signalling, leading to global anti-inflammatory and anti-apoptotic effects in the human myocardium. These findings reveal a novel mechanism contributing to the beneficial cardiac effects of canagliflozin.
Publication status:
Published
Peer review status:
Peer reviewed

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Publisher copy:
10.1093/eurheartj/ehab420

Authors

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Institution:
University of Oxford
Division:
MSD
Sub department:
HJ SURGICAL SCIENCES; HS RDM Cardiovascular Medicine
Oxford college:
Trinity College
Role:
Author
ORCID:
0000-0002-4674-0210
More by this author
Institution:
University of Oxford
Division:
MSD
Department:
RDM
Sub department:
RDM Cardiovascular Medicine
Role:
Author
ORCID:
0000-0001-7581-2108
More by this author
Role:
Author
ORCID:
0000-0001-6311-7028
More by this author
Role:
Author
ORCID:
0000-0002-1494-8340


Publisher:
Oxford University Press
Journal:
European Heart Journal More from this journal
Volume:
42
Issue:
48
Pages:
4947-4960
Place of publication:
England
Publication date:
2021-07-19
Acceptance date:
2021-06-18
DOI:
EISSN:
1522-9645
ISSN:
0195-668X
Pmid:
34293101


Language:
English
Keywords:
Pubs id:
1187348
Local pid:
pubs:1187348
Deposit date:
2021-08-03
ARK identifier:

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