Cardioprotective effects of α-cardiac actin on oxidative stress in a dilated cardiomyopathy mouse model.
cardiac remodeling
dilated cardiomyopathy
oxidative stress
α-cardiac actin
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
19
09
2019
revised:
12
12
2019
accepted:
15
12
2019
pubmed:
8
1
2020
medline:
30
9
2020
entrez:
8
1
2020
Statut:
ppublish
Résumé
The expression of α-cardiac actin, a major constituent of the cytoskeleton of cardiomyocytes, is dramatically decreased in a mouse model of dilated cardiomyopathy triggered by inducible cardiac-specific serum response factor (Srf) gene disruption that could mimic some forms of human dilated cardiomyopathy. To investigate the consequences of the maintenance of α-cardiac actin expression in this model, we developed a new transgenic mouse based on Cre/LoxP strategy, allowing together the induction of SRF loss and a compensatory expression of α-cardiac actin. Here, we report that maintenance of α-cardiac actin within cardiomyocytes temporally preserved cytoarchitecture from adverse cardiac remodeling through a positive impact on both structural and transcriptional levels. These protective effects were accompanied in vivo by the decrease of ROS generation and protein carbonylation and the downregulation of NADPH oxidases NOX2 and NOX4. We also show that ectopic expression of α-cardiac actin protects HEK293 cells against oxidative stress induced by H
Identifiants
pubmed: 31908029
doi: 10.1096/fj.201902389R
doi:
Substances chimiques
Actins
0
Hydrogen Peroxide
BBX060AN9V
Cybb protein, mouse
EC 1.6.3.-
NADPH Oxidase 2
EC 1.6.3.-
NADPH Oxidase 4
EC 1.6.3.-
Nox4 protein, mouse
EC 1.6.3.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2987-3005Informations de copyright
© 2019 Federation of American Societies for Experimental Biology.
Références
McNally EM, Mestroni L. Dilated cardiomyopathy: genetic determinants and mechanisms. Circ Res. 2017;121:731-748.
Weintraub RG, Semsarian C, Macdonald P. Dilated cardiomyopathy. Lancet. 2017;390:400-414.
Codd MB, Sugrue DD, Gersh BJ, Melton LJ 3rd. Epidemiology of idiopathic dilated and hypertrophic cardiomyopathy. A population-based study in Olmsted County, Minnesota, 1975-1984. Circulation. 1989;80:564-572.
Parlakian A, Charvet C, Escoubet B, et al. Temporally controlled onset of dilated cardiomyopathy through disruption of the SRF gene in adult heart. Circulation. 2005;112:2930-2939.
Bui AL, Horwich TB, Fonarow GC. Epidemiology and risk profile of heart failure. Nat Rev Cardiol. 2011;8:30-41.
Xu Q, Dewey S, Nguyen S, Gomes AV. Malignant and benign mutations in familial cardiomyopathies: insights into mutations linked to complex cardiovascular phenotypes. J Mol Cell Cardiol. 2010;48:899-909.
Daehmlow S, Erdmann J, Knueppel T, et al. Novel mutations in sarcomeric protein genes in dilated cardiomyopathy. Biochem Biophys Res Commun. 2002;298:116-120.
Mundia MM, Demers RW, Chow ML, Perieteanu AA, Dawson JF. Subdomain location of mutations in cardiac actin correlate with type of functional change. PLoS ONE. 2012;7:e36821.
Olson TM, Michels VV, Thibodeau SN, Tai YS, Keating MT. Actin mutations in dilated cardiomyopathy, a heritable form of heart failure. Science. 1998;280:750-752.
Sassoon DA, Garner I, Buckingham M. Transcripts of alpha-cardiac and alpha-skeletal actins are early markers for myogenesis in the mouse embryo. Development. 1988;104:155-164.
Suurmeijer AJ, Clement S, Francesconi A, et al. Alpha-actin isoform distribution in normal and failing human heart: a morphological, morphometric, and biochemical study. J Pathol. 2003;199:387-397.
Vandekerckhove J, Bugaisky G, Buckingham M. Simultaneous expression of skeletal muscle and heart actin proteins in various striated muscle tissues and cells. A quantitative determination of the two actin isoforms. J Biol Chem. 1986;261:1838-1843.
Kumar A, Crawford K, Close L, et al. Rescue of cardiac alpha-actin-deficient mice by enteric smooth muscle gamma-actin. Proc Natl Acad Sci U S A. 1997;94:4406-4411.
Touvron M, Escoubet B, Mericskay M, et al. Locally expressed IGF1 propeptide improves mouse heart function in induced dilated cardiomyopathy by blocking myocardial fibrosis and SRF-dependent CTGF induction. Dis Model Mech. 2012;5:481-491.
Sun Q, Chen G, Streb JW, et al. Defining the mammalian CArGome. Genome Res. 2006;16:197-207.
Minty A, Kedes L. Upstream regions of the human cardiac actin gene that modulate its transcription in muscle cells: presence of an evolutionarily conserved repeated motif. Mol Cell Biol. 1986;6:2125-2136.
Diguet N, Mallat Y, Ladouce R, et al. Muscle creatine kinase deficiency triggers both actin depolymerization and desmin disorganization by advanced glycation end products in dilated cardiomyopathy. J Biol Chem. 2011;286:35007-35019.
Diguet N, Trammell SAJ, Tannous C, et al. Nicotinamide riboside preserves cardiac function in a mouse model of dilated cardiomyopathy. Circulation. 2018;137:2256-2273.
Agbulut O, Li Z, Perie S, et al. Lack of desmin results in abortive muscle regeneration and modifications in synaptic structure. Cell Motil Cytoskeleton. 2001;49:51-66.
Guillet-Deniau I, Mieulet V, Le Lay S, et al. Sterol regulatory element binding protein-1c expression and action in rat muscles: insulin-like effects on the control of glycolytic and lipogenic enzymes and UCP3 gene expression. Diabetes. 2002;51:1722-1728.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248-254.
Parlakian A, Tuil D, Hamard G, et al. Targeted inactivation of serum response factor in the developing heart results in myocardial defects and embryonic lethality. Mol. Cell. Biol. 2004;24:5281-5289.
Agbulut O, Li Z, Mouly V, Butler-Browne GS. Analysis of skeletal and cardiac muscle from desmin knock-out and normal mice by high resolution separation of myosin heavy-chain isoforms. Biol Cell. 1996;88:131-135.
Blum H, Beier H, Gross HJ. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis. 1987;8:93-99.
Angelini A, Li Z, Mericskay M, Decaux JF. Regulation of connective tissue growth factor and cardiac fibrosis by an SRF/MicroRNA-133a Axis. PLoS ONE. 2015;10:e0139858.
Gary-Bobo G, Parlakian A, Escoubet B, et al. Mosaic inactivation of the serum response factor gene in the myocardium induces focal lesions and heart failure. Eur J Heart Fail. 2008;10:635-645.
Tritsch E, Mallat Y, Lefebvre F, et al. An SRF/miR-1 axis regulates NCX1 and annexin A5 protein levels in the normal and failing heart. Cardiovasc Res. 2013;98:372-380.
Wu YT, Lee HC, Liao CC, Wei YH. Regulation of mitochondrial F(o)F(1)ATPase activity by Sirt3-catalyzed deacetylation and its deficiency in human cells harboring 4977bp deletion of mitochondrial DNA. Biochim Biophys Acta. 4977bp;1832:216-227.
Dieterich S, Bieligk U, Beulich K, Hasenfuss G, Prestle J. Gene expression of antioxidative enzymes in the human heart: increased expression of catalase in the end-stage failing heart. Circulation. 2000;101:33-39.
Ide T, Tsutsui H, Kinugawa S, et al. Direct evidence for increased hydroxyl radicals originating from superoxide in the failing myocardium. Circ Res. 2000;86:152-157.
Lynch TL, Sivaguru M, Velayutham M, et al. Oxidative stress in dilated cardiomyopathy caused by MYBPC3 mutation. Oxid Med Cell Longev. 2015;2015:424751.
Dalle-Donne I, Giustarini D, Colombo R, Rossi R, Milzani A. Protein carbonylation in human diseases. Trends Mol Med. 2003;9:169-176.
Dalle-Donne I, Rossi R, Giustarini D, Milzani A, Colombo R. Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta. 2003;329:23-38.
Schratt G, Philippar U, Berger J, Schwarz H, Heidenreich O, Nordheim A. Serum response factor is crucial for actin cytoskeletal organization and focal adhesion assembly in embryonic stem cells. J Cell Biol. 2002;156:737-750.
Asakura M, Kitakaze M. Global gene expression profiling in the failing myocardium. Circ J. 2009;73:1568-1576.
Harvey PA, Leinwand LA. The cell biology of disease: cellular mechanisms of cardiomyopathy. J Cell Biol. 2011;194:355-365.
Hofmann WA, Stojiljkovic L, Fuchsova B, et al. Actin is part of pre-initiation complexes and is necessary for transcription by RNA polymerase II. Nat Cell Biol. 2004;6:1094-1101.
Hu P, Wu S, Hernandez N. A role for beta-actin in RNA polymerase III transcription. Genes Dev. 2004;18:3010-3015.
Philimonenko VV, Zhao J, Iben S, et al. Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat Cell Biol. 2004;6:1165-1172.
Percipalle P, Jonsson A, Nashchekin D, et al. Nuclear actin is associated with a specific subset of hnRNP A/B-type proteins. Nucleic Acids Res. 2002;30:1725-1734.
Sjolinder M, Bjork P, Soderberg E, Sabri N, Farrants AK, Visa N. The growing pre-mRNA recruits actin and chromatin-modifying factors to transcriptionally active genes. Genes Dev. 2005;19:1871-1884.
Kuwahara K, Teg Pipes GC, McAnally J, et al. Modulation of adverse cardiac remodeling by STARS, a mediator of MEF2 signaling and SRF activity. J Clin Invest. 2007;117:1324-1334.
Miano JM, Ramanan N, Georger MA, et al. Restricted inactivation of serum response factor to the cardiovascular system. Proc Natl Acad Sci U S A. 2004;101:17132-17137.
Zhang X, Azhar G, Chai J, et al. Cardiomyopathy in transgenic mice with cardiac-specific overexpression of serum response factor. Am J Physiol Heart Circ Physiol. 2001;280:H1782-H1792.
Garner I, Minty AJ, Alonso S, Barton PJ, Buckingham ME. A 5' duplication of the alpha-cardiac actin gene in BALB/c mice is associated with abnormal levels of alpha-cardiac and alpha-skeletal actin mRNAs in adult cardiac tissue. EMBO J. 1986;5:2559-2567.
Hewett TE, Grupp IL, Grupp G, Robbins J. Alpha-skeletal actin is associated with increased contractility in the mouse heart. Circ Res. 1994;74:740-746.
Lamon S, Wallace MA, Russell AP. The STARS signaling pathway: a key regulator of skeletal muscle function. Pflug Arch Eur J Phy. 2014;466:1659-1671.
de Tombe PP. Cardiac myofilaments: mechanics and regulation. J Biomech. 2003;36:721-730.
Suzuki M, Fujita H, Ishiwata S. A new muscle contractile system composed of a thick filament lattice and a single actin filament. Biophys J. 2005;89:321-328.
Halliwell B, Cross CE. Oxygen-derived species: their relation to human disease and environmental stress. Environ Health Perspect. 1994;102(Suppl 10):5-12.
Shao D, Oka S, Brady CD, Haendeler J, Eaton P, Sadoshima J. Redox modification of cell signaling in the cardiovascular system. J Mol Cell Cardiol. 2012;52:550-558.
Victorino VJ, Mencalha AL, Panis C. Post-translational modifications disclose a dual role for redox stress in cardiovascular pathophysiology. Life Sci. 2015;129:42-47.
Farah ME, Amberg DC. Conserved actin cysteine residues are oxidative stress sensors that can regulate cell death in yeast. Mol Biol Cell. 2007;18:1359-1365.
Farah ME, Sirotkin V, Haarer B, Kakhniashvili D, Amberg DC. Diverse protective roles of the actin cytoskeleton during oxidative stress. Cytoskeleton. 2011;68:340-354.
Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87:245-313.
Ichihara S, Suzuki Y, Chang J, et al. Involvement of oxidative modification of proteins related to ATP synthesis in the left ventricles of hamsters with cardiomyopathy. Sci Rep. 2017;7:1-11.
Nabeebaccus A, Zhang M, Shah AM. NADPH oxidases and cardiac remodelling. Heart Fail Rev. 2011;16:5-12.
Paravicini TM, Touyz RM. NADPH oxidases, reactive oxygen species, and hypertension: clinical implications and therapeutic possibilities. Diabetes Care. 2008;31(Suppl 2):S170-S180.
Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ. Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem. 2003;278:36027-36031.
Han D, Antunes F, Canali R, Rettori D, Cadenas E. Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J Biol Chem. 2003;278:5557-5563.
St-Pierre J, Buckingham JA, Roebuck SJ, Brand MD. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem. 2002;277:44784-44790.
Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol. 2003;552:335-344.
Shoshan-Barmatz V, De Pinto V, Zweckstetter M, Raviv Z, Keinan N, Arbel N. VDAC, a multi-functional mitochondrial protein regulating cell life and death. Mol Aspects Med. 2010;31:227-285.
Gourlay CW, Ayscough KR. Identification of an upstream regulatory pathway controlling actin-mediated apoptosis in yeast. J Cell Sci. 2005;118:2119-2132.
Nauseef WM. Biological roles for the NOX family NADPH oxidases. J Biol Chem. 2008;283:16961-16965.
Vignais PV. The superoxide-generating NADPH oxidase: structural aspects and activation mechanism. Cell Mol Life Sci. 2002;59:1428-1459.
Paclet MH, Berthier S, Kuhn L, Garin J, Morel F. Regulation of phagocyte NADPH oxidase activity: identification of two cytochrome b558 activation states. FASEB J. 2007;21:1244-1255.
Rasmussen I, Pedersen LH, Byg L, Suzuki K, Sumimoto H, Vilhardt F. Effects of F/G-actin ratio and actin turn-over rate on NADPH oxidase activity in microglia. BMC Immunol. 2010;11:1-15.
Cave A, Grieve D, Johar S, Zhang M, Shah AM. NADPH oxidase-derived reactive oxygen species in cardiac pathophysiology. Philos Trans R Soc Lond B Biol Sci. 2005;360:2327-2334.
Tsutsui H, Kinugawa S, Matsushima S. Oxidative stress and heart failure. Am J Physiol Heart Circ Physiol. 2011;301:H2181-H2190.
Debold EP, Saber W, Cheema Y, et al. Human actin mutations associated with hypertrophic and dilated cardiomyopathies demonstrate distinct thin filament regulatory properties in vitro. J Mol Cell Cardiol. 2010;48:286-292.
Muller M, Mazur AJ, Behrmann E, et al. Functional characterization of the human alpha-cardiac actin mutations Y166C and M305L involved in hypertrophic cardiomyopathy. Cell Mol Life Sci. 2012;69:3457-3479.