Palmitate-Induced Cardiac Lipotoxicity Is Relieved by the Redox-Active Motif of SELENOT through Improving Mitochondrial Function and Regulating Metabolic State.


Journal

Cells
ISSN: 2073-4409
Titre abrégé: Cells
Pays: Switzerland
ID NLM: 101600052

Informations de publication

Date de publication:
29 03 2023
Historique:
received: 24 02 2023
revised: 22 03 2023
accepted: 27 03 2023
medline: 14 4 2023
entrez: 13 4 2023
pubmed: 14 4 2023
Statut: epublish

Résumé

Cardiac lipotoxicity is an important contributor to cardiovascular complications during obesity. Given the fundamental role of the endoplasmic reticulum (ER)-resident Selenoprotein T (SELENOT) for cardiomyocyte differentiation and protection and for the regulation of glucose metabolism, we took advantage of a small peptide (PSELT), derived from the SELENOT redox-active motif, to uncover the mechanisms through which PSELT could protect cardiomyocytes against lipotoxicity. To this aim, we modeled cardiac lipotoxicity by exposing H9c2 cardiomyocytes to palmitate (PA). The results showed that PSELT counteracted PA-induced cell death, lactate dehydrogenase release, and the accumulation of intracellular lipid droplets, while an inert form of the peptide (I-PSELT) lacking selenocysteine was not active against PA-induced cardiomyocyte death. Mechanistically, PSELT counteracted PA-induced cytosolic and mitochondrial oxidative stress and rescued SELENOT expression that was downregulated by PA through FAT/CD36 (cluster of differentiation 36/fatty acid translocase), the main transporter of fatty acids in the heart. Immunofluorescence analysis indicated that PSELT also relieved the PA-dependent increase in CD36 expression, while in SELENOT-deficient cardiomyocytes, PA exacerbated cell death, which was not mitigated by exogenous PSELT. On the other hand, PSELT improved mitochondrial respiration during PA treatment and regulated mitochondrial biogenesis and dynamics, preventing the PA-provoked decrease in PGC1-α and increase in DRP-1 and OPA-1. These findings were corroborated by transmission electron microscopy (TEM), revealing that PSELT improved the cardiomyocyte and mitochondrial ultrastructures and restored the ER network. Spectroscopic characterization indicated that PSELT significantly attenuated infrared spectral-related macromolecular changes (i.e., content of lipids, proteins, nucleic acids, and carbohydrates) and also prevented the decrease in membrane fluidity induced by PA. Our findings further delineate the biological significance of SELENOT in cardiomyocytes and indicate the potential of its mimetic PSELT as a protective agent for counteracting cardiac lipotoxicity.

Identifiants

pubmed: 37048116
pii: cells12071042
doi: 10.3390/cells12071042
pmc: PMC10093731
pii:
doi:

Substances chimiques

Palmitates 0
Fatty Acids 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

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Auteurs

Carmine Rocca (C)

Cellular and Molecular Cardiovascular Pathophysiology Laboratory, Department of Biology, Ecology and Earth Sciences (DiBEST), University of Calabria, 87036 Rende, Italy.

Anna De Bartolo (A)

Cellular and Molecular Cardiovascular Pathophysiology Laboratory, Department of Biology, Ecology and Earth Sciences (DiBEST), University of Calabria, 87036 Rende, Italy.
UNIROUEN, Inserm U1239, Neuroendocrine, Endocrine and Germinal Differentiation and Communication (NorDiC), Rouen Normandie University, 76000 Mont-Saint-Aignan, France.

Rita Guzzi (R)

Department of Physics, Molecular Biophysics Laboratory, University of Calabria, 87036 Rende, Italy.
CNR-NANOTEC, Department of Physics, University of Calabria, 87036 Rende, Italy.

Maria Caterina Crocco (MC)

Department of Physics, Molecular Biophysics Laboratory, University of Calabria, 87036 Rende, Italy.
STAR Research Infrastructure, University of Calabria, Via Tito Flavio, 87036 Rende, Italy.

Vittoria Rago (V)

Department of Pharmacy, Health and Nutritional Sciences, University of Calabria, 87036 Rende, Italy.

Naomi Romeo (N)

Cellular and Molecular Cardiovascular Pathophysiology Laboratory, Department of Biology, Ecology and Earth Sciences (DiBEST), University of Calabria, 87036 Rende, Italy.

Ida Perrotta (I)

Centre for Microscopy and Microanalysis (CM2), Department of Biology, Biology, Ecology and Earth Sciences (DiBEST), University of Calabria, 87036 Rende, Italy.

Ernestina Marianna De Francesco (EM)

Endocrinology, Department of Clinical and Experimental Medicine, University of Catania, Garibaldi-Nesima Hospital, 95124 Catania, Italy.

Maria Grazia Muoio (MG)

Endocrinology, Department of Clinical and Experimental Medicine, University of Catania, Garibaldi-Nesima Hospital, 95124 Catania, Italy.

Maria Concetta Granieri (MC)

Cellular and Molecular Cardiovascular Pathophysiology Laboratory, Department of Biology, Ecology and Earth Sciences (DiBEST), University of Calabria, 87036 Rende, Italy.

Teresa Pasqua (T)

Department of Health Science, University Magna Graecia of Catanzaro, 88100 Catanzaro, Italy.

Rosa Mazza (R)

Cellular and Molecular Cardiovascular Pathophysiology Laboratory, Department of Biology, Ecology and Earth Sciences (DiBEST), University of Calabria, 87036 Rende, Italy.

Loubna Boukhzar (L)

UNIROUEN, Inserm U1239, Neuroendocrine, Endocrine and Germinal Differentiation and Communication (NorDiC), Rouen Normandie University, 76000 Mont-Saint-Aignan, France.

Benjamin Lefranc (B)

UNIROUEN, Inserm U1239, Neuroendocrine, Endocrine and Germinal Differentiation and Communication (NorDiC), Rouen Normandie University, 76000 Mont-Saint-Aignan, France.
UNIROUEN, UMS-UAR HERACLES, PRIMACEN, Cell Imaging Platform of Normandy, Institute for Research and Innovation in Biomedicine (IRIB), 76183 Rouen, France.

Jérôme Leprince (J)

UNIROUEN, Inserm U1239, Neuroendocrine, Endocrine and Germinal Differentiation and Communication (NorDiC), Rouen Normandie University, 76000 Mont-Saint-Aignan, France.
UNIROUEN, UMS-UAR HERACLES, PRIMACEN, Cell Imaging Platform of Normandy, Institute for Research and Innovation in Biomedicine (IRIB), 76183 Rouen, France.

Maria Eugenia Gallo Cantafio (ME)

Department of Experimental and Clinical Medicine, Magna Graecia University, 88100 Catanzaro, Italy.

Teresa Soda (T)

Department of Health Science, University Magna Graecia of Catanzaro, 88100 Catanzaro, Italy.

Nicola Amodio (N)

Department of Experimental and Clinical Medicine, Magna Graecia University, 88100 Catanzaro, Italy.

Youssef Anouar (Y)

UNIROUEN, Inserm U1239, Neuroendocrine, Endocrine and Germinal Differentiation and Communication (NorDiC), Rouen Normandie University, 76000 Mont-Saint-Aignan, France.
UNIROUEN, UMS-UAR HERACLES, PRIMACEN, Cell Imaging Platform of Normandy, Institute for Research and Innovation in Biomedicine (IRIB), 76183 Rouen, France.

Tommaso Angelone (T)

Cellular and Molecular Cardiovascular Pathophysiology Laboratory, Department of Biology, Ecology and Earth Sciences (DiBEST), University of Calabria, 87036 Rende, Italy.
National Institute of Cardiovascular Research (INRC), 40126 Bologna, Italy.

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