Sirt1 counteracts decrease in membrane phospholipid unsaturation and diastolic dysfunction during saturated fatty acid overload.


Journal

Journal of molecular and cellular cardiology
ISSN: 1095-8584
Titre abrégé: J Mol Cell Cardiol
Pays: England
ID NLM: 0262322

Informations de publication

Date de publication:
08 2019
Historique:
received: 18 04 2019
revised: 21 05 2019
accepted: 25 05 2019
pubmed: 31 5 2019
medline: 26 6 2020
entrez: 31 5 2019
Statut: ppublish

Résumé

The fatty acid (FA) composition of membrane phospholipid reflects at least in part dietary fat composition. Saturated FA (SFA) suppress Sirt1 activity, while monounsaturated FA (MUFA) counteract this effect. We explored a role of Sirt1 in homeostatic control of the fatty acid composition of membrane phospholipid in the presence of SFA overload. Sirt1 deficiency in cardiomyocytes decreased the expression levels of liver X receptor (LXR)-target genes, particularly stearoyl-CoA desaturase-1 (Scd1), a rate-limiting enzyme in the cellular synthesis of MUFA from SFA, increased membrane SFA/MUFA ratio, and worsened left ventricular (LV) diastolic function in mice fed an SFA-rich high fat diet. In cultured cardiomyocytes, Sirt1 knockdown (KD) exacerbated the palmitate overload-induced increase in membrane SFA/MUFA ratio, which was associated with decrease in the expression of LXR-target genes, including Scd1. Forced overexpression of Scd1 in palmitate-overloaded Sirt1KD cardiomyocytes lowered the SFA/MUFA ratio. Nicotinamide mononucleotide (NMN) increased Sirt1 activity and Scd1 expression, thereby lowering membrane SFA/MUFA ratio in palmitate-overloaded cardiomyocytes. These effects of NMN were not observed for Scd1KD cardiomyocytes. LXRα/βKD exacerbated palmitate overload-induced increase in membrane SFA/MUFA ratio, while LXR agonist T0901317 alleviated it. NMN failed to rescue Scd1 protein expression and membrane SFA/MUFA ratio in palmitate-overloaded LXRα/βKD cardiomyocytes. The administration of NMN or T0901317 showed a dramatic reversal in membrane SFA/MUFA ratio and LV diastolic function in SFA-rich HFD-fed mice. Cardiac Sirt1 counteracted SFA overload-induced decrease in membrane phospholipid unsaturation and diastolic dysfunction via regulating LXR-mediated transcription of the Scd1 gene.

Sections du résumé

BACKGROUND
The fatty acid (FA) composition of membrane phospholipid reflects at least in part dietary fat composition. Saturated FA (SFA) suppress Sirt1 activity, while monounsaturated FA (MUFA) counteract this effect.
OBJECTIVE
We explored a role of Sirt1 in homeostatic control of the fatty acid composition of membrane phospholipid in the presence of SFA overload.
METHODS AND RESULTS
Sirt1 deficiency in cardiomyocytes decreased the expression levels of liver X receptor (LXR)-target genes, particularly stearoyl-CoA desaturase-1 (Scd1), a rate-limiting enzyme in the cellular synthesis of MUFA from SFA, increased membrane SFA/MUFA ratio, and worsened left ventricular (LV) diastolic function in mice fed an SFA-rich high fat diet. In cultured cardiomyocytes, Sirt1 knockdown (KD) exacerbated the palmitate overload-induced increase in membrane SFA/MUFA ratio, which was associated with decrease in the expression of LXR-target genes, including Scd1. Forced overexpression of Scd1 in palmitate-overloaded Sirt1KD cardiomyocytes lowered the SFA/MUFA ratio. Nicotinamide mononucleotide (NMN) increased Sirt1 activity and Scd1 expression, thereby lowering membrane SFA/MUFA ratio in palmitate-overloaded cardiomyocytes. These effects of NMN were not observed for Scd1KD cardiomyocytes. LXRα/βKD exacerbated palmitate overload-induced increase in membrane SFA/MUFA ratio, while LXR agonist T0901317 alleviated it. NMN failed to rescue Scd1 protein expression and membrane SFA/MUFA ratio in palmitate-overloaded LXRα/βKD cardiomyocytes. The administration of NMN or T0901317 showed a dramatic reversal in membrane SFA/MUFA ratio and LV diastolic function in SFA-rich HFD-fed mice.
CONCLUSION
Cardiac Sirt1 counteracted SFA overload-induced decrease in membrane phospholipid unsaturation and diastolic dysfunction via regulating LXR-mediated transcription of the Scd1 gene.

Identifiants

pubmed: 31145942
pii: S0022-2828(19)30110-5
doi: 10.1016/j.yjmcc.2019.05.019
pii:
doi:

Substances chimiques

Fatty Acids 0
Fatty Acids, Monounsaturated 0
Liver X Receptors 0
Membrane Lipids 0
Phospholipids 0
Sirtuin 1 EC 3.5.1.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1-11

Informations de copyright

Copyright © 2019 Elsevier Ltd. All rights reserved.

Auteurs

Tsunehisa Yamamoto (T)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan.

Jin Endo (J)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan; Japan Science and Technology Agency, Tokyo, Japan.

Masaharu Kataoka (M)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan.

Tomohiro Matsuhashi (T)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan.

Yoshinori Katsumata (Y)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan.

Kohsuke Shirakawa (K)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan.

Naohiro Yoshida (N)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan; Department of Endocrinology and Hypertension, Tokyo Women's Medical University, Tokyo, Japan.

Sarasa Isobe (S)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan.

Hidenori Moriyama (H)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan.

Shinichi Goto (S)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan.

Kaoru Yamashita (K)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan; Department of Endocrinology and Hypertension, Tokyo Women's Medical University, Tokyo, Japan.

Takayo Ohto-Nakanishi (T)

Lipidome Lab Co., Ltd., Akita, Japan.

Hiroki Nakanishi (H)

Lipidome Lab Co., Ltd., Akita, Japan; Research Center for Biosignal, Akita University, Akita, Japan.

Yuta Shimanaka (Y)

Graduate School of Pharmaceutical Sciences, Tokyo University, Tokyo, Japan.

Nozomu Kono (N)

Graduate School of Pharmaceutical Sciences, Tokyo University, Tokyo, Japan.

Ken Shinmura (K)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan; Department of General Medicine, Hyogo College of Medicine, Hyogo, Japan.

Hiroyuki Arai (H)

Graduate School of Pharmaceutical Sciences, Tokyo University, Tokyo, Japan.

Keiichi Fukuda (K)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan.

Motoaki Sano (M)

Department of Cardiology, Keio University School of Medicine, Tokyo, Japan; Japan Science and Technology Agency, Tokyo, Japan. Electronic address: msano@a8.keio.jp.

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Classifications MeSH