Literature DB >> 31166588

Low cardiac lipolysis reduces mitochondrial fission and prevents lipotoxic heart dysfunction in Perilipin 5 mutant mice.

Stephanie Kolleritsch1, Benedikt Kien1, Gabriele Schoiswohl1, Clemens Diwoky1, Renate Schreiber1, Christoph Heier1, Lisa Katharina Maresch1, Martina Schweiger1, Thomas O Eichmann1,2, Sarah Stryeck3,4, Petra Krenn4,5, Tamara Tomin4,5, Matthias Schittmayer4,5, Dagmar Kolb6, Thomas Rülicke7, Gerald Hoefler8, Heimo Wolinski1, Tobias Madl3,4, Ruth Birner-Gruenberger4,5, Guenter Haemmerle1.   

Abstract

AIMS: Lipotoxic cardiomyopathy in diabetic and obese patients typically encompasses increased cardiac fatty acid (FA) uptake eventually surpassing the mitochondrial oxidative capacity. Lowering FA utilization via inhibition of lipolysis represents a strategy to counteract the development of lipotoxic heart dysfunction. However, defective cardiac triacylglycerol (TAG) catabolism and FA oxidation in humans (and mice) carrying mutated ATGL alleles provokes lipotoxic heart dysfunction questioning a therapeutic approach to decrease cardiac lipolysis. Interestingly, decreased lipolysis via cardiac overexpression of Perilipin 5 (Plin5), a binding partner of ATGL, is compatible with normal heart function and lifespan despite massive cardiac lipid accumulation. Herein, we decipher mechanisms that protect Plin5 transgenic mice from the development of heart dysfunction. METHODS AND
RESULTS: We generated mice with cardiac-specific overexpression of Plin5 encoding a serine-155 to alanine exchange (Plin5-S155A) of the protein kinase A phosphorylation site, which has been suggested as a prerequisite to stimulate lipolysis and may play a crucial role in the preservation of heart function. Plin5-S155A mice showed a substantial increase in cardiac TAG and ceramide levels, which was comparable to mice overexpressing non-mutated Plin5. Lipid accumulation was compatible with normal heart function even under mild stress. Plin5-S155A mice showed reduced cardiac FA oxidation but normal ATP production and changes in the Plin5-S155A phosphoproteome compared to Plin5 transgenic mice. Interestingly, mitochondrial recruitment of dynamin-related protein 1 (Drp1) was markedly reduced in cardiac muscle of Plin5-S155A and Plin5 transgenic mice accompanied by decreased phosphorylation of mitochondrial fission factor, a mitochondrial receptor of Drp1.
CONCLUSIONS: This study suggests that low cardiac lipolysis is associated with reduced mitochondrial fission and may represent a strategy to combat the development of lipotoxic heart dysfunction.
© The Author(s) 2019. Published by Oxford University Press on behalf of the European Society of Cardiology.

Entities:  

Keywords:  Cardiac lipolysis; Heart dysfunction; Lipotoxicity; Mitochondrial dynamics; Perilipin 5

Mesh:

Substances:

Year:  2020        PMID: 31166588      PMCID: PMC7338219          DOI: 10.1093/cvr/cvz119

Source DB:  PubMed          Journal:  Cardiovasc Res        ISSN: 0008-6363            Impact factor:   10.787


  31 in total

1.  Fatty acid trafficking in starved cells: regulation by lipid droplet lipolysis, autophagy, and mitochondrial fusion dynamics.

Authors:  Angelika S Rambold; Sarah Cohen; Jennifer Lippincott-Schwartz
Journal:  Dev Cell       Date:  2015-03-05       Impact factor: 12.270

2.  Triglyceride accumulation protects against fatty acid-induced lipotoxicity.

Authors:  Laura L Listenberger; Xianlin Han; Sarah E Lewis; Sylvaine Cases; Robert V Farese; Daniel S Ory; Jean E Schaffer
Journal:  Proc Natl Acad Sci U S A       Date:  2003-03-10       Impact factor: 11.205

3.  Lipid metabolism and toxicity in the heart.

Authors:  Ira J Goldberg; Chad M Trent; P Christian Schulze
Journal:  Cell Metab       Date:  2012-06-06       Impact factor: 27.287

4.  Unique regulation of adipose triglyceride lipase (ATGL) by perilipin 5, a lipid droplet-associated protein.

Authors:  Hong Wang; Ming Bell; Urmila Sreenivasan; Urmilla Sreenevasan; Hong Hu; Jun Liu; Knut Dalen; Constantine Londos; Tomohiro Yamaguchi; Mark A Rizzo; Rosalind Coleman; Dawei Gong; Dawn Brasaemle; Carole Sztalryd
Journal:  J Biol Chem       Date:  2011-03-09       Impact factor: 5.157

5.  Metabolism. AMP-activated protein kinase mediates mitochondrial fission in response to energy stress.

Authors:  Erin Quan Toyama; Sébastien Herzig; Julien Courchet; Tommy L Lewis; Oliver C Losón; Kristina Hellberg; Nathan P Young; Hsiuchen Chen; Franck Polleux; David C Chan; Reuben J Shaw
Journal:  Science       Date:  2016-01-15       Impact factor: 47.728

6.  Mitochondrial fission and fusion factors reciprocally orchestrate mitophagic culling in mouse hearts and cultured fibroblasts.

Authors:  Moshi Song; Katsuyoshi Mihara; Yun Chen; Luca Scorrano; Gerald W Dorn
Journal:  Cell Metab       Date:  2015-01-15       Impact factor: 27.287

7.  Functional cardiac lipolysis in mice critically depends on comparative gene identification-58.

Authors:  Kathrin A Zierler; Doris Jaeger; Nina M Pollak; Sandra Eder; Gerald N Rechberger; Franz P W Radner; Gerald Woelkart; Dagmar Kolb; Albrecht Schmidt; Manju Kumari; Karina Preiss-Landl; Burkert Pieske; Bernd Mayer; Robert Zimmermann; Achim Lass; Rudolf Zechner; Guenter Haemmerle
Journal:  J Biol Chem       Date:  2013-02-14       Impact factor: 5.486

8.  Nuclear Perilipin 5 integrates lipid droplet lipolysis with PGC-1α/SIRT1-dependent transcriptional regulation of mitochondrial function.

Authors:  Violeta I Gallardo-Montejano; Geetu Saxena; Christine M Kusminski; Chaofeng Yang; John L McAfee; Lisa Hahner; Kathleen Hoch; William Dubinsky; Vihang A Narkar; Perry E Bickel
Journal:  Nat Commun       Date:  2016-08-24       Impact factor: 14.919

9.  Development of small-molecule inhibitors targeting adipose triglyceride lipase.

Authors:  Nicole Mayer; Martina Schweiger; Matthias Romauch; Gernot F Grabner; Thomas O Eichmann; Elisabeth Fuchs; Jakov Ivkovic; Christoph Heier; Irina Mrak; Achim Lass; Gerald Höfler; Christian Fledelius; Rudolf Zechner; Robert Zimmermann; Rolf Breinbauer
Journal:  Nat Chem Biol       Date:  2013-10-06       Impact factor: 15.040

10.  Cardiac-specific overexpression of perilipin 5 provokes severe cardiac steatosis via the formation of a lipolytic barrier.

Authors:  Nina M Pollak; Martina Schweiger; Doris Jaeger; Dagmar Kolb; Manju Kumari; Renate Schreiber; Stephanie Kolleritsch; Philipp Markolin; Gernot F Grabner; Christoph Heier; Kathrin A Zierler; Thomas Rülicke; Robert Zimmermann; Achim Lass; Rudolf Zechner; Guenter Haemmerle
Journal:  J Lipid Res       Date:  2013-01-23       Impact factor: 6.676

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  15 in total

Review 1.  The biology of lipid droplet-bound mitochondria.

Authors:  Michaela Veliova; Anton Petcherski; Marc Liesa; Orian S Shirihai
Journal:  Semin Cell Dev Biol       Date:  2020-05-20       Impact factor: 7.727

Review 2.  Lipid Droplet-a New Target in Ischemic Heart Disease.

Authors:  Xiaoying Guo; Qi Shi; Wanqin Zhang; Zhongwen Qi; Hao Lv; Fujing Man; Yingyu Xie; Yaping Zhu; Junping Zhang
Journal:  J Cardiovasc Transl Res       Date:  2022-01-04       Impact factor: 4.132

Review 3.  Lipolysis: cellular mechanisms for lipid mobilization from fat stores.

Authors:  Gernot F Grabner; Hao Xie; Martina Schweiger; Rudolf Zechner
Journal:  Nat Metab       Date:  2021-11-19

Review 4.  The Role of Adipose Triglyceride Lipase and Cytosolic Lipolysis in Cardiac Function and Heart Failure.

Authors:  Ulrich Kintscher; Anna Foryst-Ludwig; Guenter Haemmerle; Rudolf Zechner
Journal:  Cell Rep Med       Date:  2020-03-25

5.  Mitochondrial shaping proteins as novel treatment targets for cardiomyopathies.

Authors:  Siavash Beikoghli Kalkhoran; Sauri Hernandez-Resendiz; Sang-Ging Ong; Chrishan J A Ramachandra; Derek J Hausenloy
Journal:  Cond Med       Date:  2020-08

Review 6.  The Lipolysome-A Highly Complex and Dynamic Protein Network Orchestrating Cytoplasmic Triacylglycerol Degradation.

Authors:  Peter Hofer; Ulrike Taschler; Renate Schreiber; Petra Kotzbeck; Gabriele Schoiswohl
Journal:  Metabolites       Date:  2020-04-10

Review 7.  Lipotoxicity and Diabetic Nephropathy: Novel Mechanistic Insights and Therapeutic Opportunities.

Authors:  Lucas Opazo-Ríos; Sebastián Mas; Gema Marín-Royo; Sergio Mezzano; Carmen Gómez-Guerrero; Juan Antonio Moreno; Jesús Egido
Journal:  Int J Mol Sci       Date:  2020-04-10       Impact factor: 5.923

8.  The Gene and Protein Expression of the Main Components of the Lipolytic System in Human Myocardium and Heart Perivascular Adipose Tissue. Effect of Coronary Atherosclerosis.

Authors:  Małgorzata Knapp; Jan Górski; Janina Lewkowicz; Anna Lisowska; Monika Gil; Beata Wójcik; Tomasz Hirnle; Adrian Chabowski; Agnieszka Mikłosz
Journal:  Int J Mol Sci       Date:  2020-01-22       Impact factor: 5.923

Review 9.  Understanding the Role of Perilipin 5 in Non-Alcoholic Fatty Liver Disease and Its Role in Hepatocellular Carcinoma: A Review of Novel Insights.

Authors:  Paola Berenice Mass Sanchez; Marinela Krizanac; Ralf Weiskirchen; Anastasia Asimakopoulos
Journal:  Int J Mol Sci       Date:  2021-05-17       Impact factor: 5.923

Review 10.  Mitochondrial Mechanisms in Diabetic Cardiomyopathy.

Authors:  Johannes Gollmer; Andreas Zirlik; Heiko Bugger
Journal:  Diabetes Metab J       Date:  2020-02       Impact factor: 5.376

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