Metformin intervention prevents cardiac dysfunction in a murine model of adult congenital heart disease

Alshawabkeh, 2016, Burden of heart failure in adults with congenital heart disease, Current Heart Failure Reports, 13, 247, 10.1007/s11897-016-0301-0 Marelli, 2014, Lifetime prevalence of congenital heart disease in the general population from 2000 to 2010, Circulation, 130, 749, 10.1161/CIRCULATIONAHA.113.008396 Lui, 2017, Diagnosis and management of noncardiac complications in adults with congenital heart disease: a scientific statement from the American Heart Association, Circulation, 136, e348, 10.1161/CIR.0000000000000535 Ogden, 2014, Prevalence of childhood and adult obesity in the United States, 2011–2012, Journal of the American Medical Association, 311, 806, 10.1001/jama.2014.732 Writing Group, 2016, Executive summary: heart disease and stroke statistics--2016 update: a report from the American Heart Association, Circulation, 133, 447, 10.1161/CIR.0000000000000366 Roche, 2013, Hypertension, obesity, and coronary artery disease in the survivors of congenital heart disease, Canadian Journal of Cardiology, 29, 841, 10.1016/j.cjca.2013.03.021 Islam, 2016, Hospital readmission of patients with congenital heart disease in Canada, Canadian Journal of Cardiology, 32, 10.1016/j.cjca.2015.12.018 Costa, 2013, Functional characterization of a novel mutation in NKX2-5 associated with congenital heart disease and adult-onset cardiomyopathy, Circulation: Cardiovascular Genetics, 6, 238 Furtado, 2017, Point mutations in murine Nkx2-5 phenocopy human congenital heart disease and induce pathogenic Wnt signaling, JCI Insight, 2, 10.1172/jci.insight.88271 Heiberg, 2010, Design and validation of segment – freely available software for cardiovascular image analysis, BMC Medical Imaging, 10, 1, 10.1186/1471-2342-10-1 Gnaiger, 2000, Mitochondria in the cold, 431 Schopf, 2016, Oxidative phosphorylation and mitochondrial function differ between human prostate tissue and cultured cells, FEBS Journal, 283, 2181, 10.1111/febs.13733 Xia, 2016, Using MetaboAnalyst 3.0 for comprehensive metabolomics data analysis, Current Protocols in Bioinformatics, 55, 14.10.1, 10.1002/cpbi.11 Hackstadt, 2009, Filtering for increased power for microarray data analysis, BMC Bioinformatics, 10, 11, 10.1186/1471-2105-10-11 Dieterle, 2006, Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures. Application in 1H NMR metabonomics, Analytical Chemistry, 78, 4281, 10.1021/ac051632c van den Boogaard, 2012, Genetic variation in T-box binding element functionally affects SCN5A/SCN10A enhancer, Journal of Clinical Investigation, 122, 2519, 10.1172/JCI62613 McLean, 2010, GREAT improves functional interpretation of cis-regulatory regions, Nature Biotechnology, 28, 495, 10.1038/nbt.1630 Martin, 2011, Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet.journal, 17, 10, 10.14806/ej.17.1.200 Dobin, 2013, STAR: ultrafast universal RNA-seq aligner, Bioinformatics, 29, 15, 10.1093/bioinformatics/bts635 Anders, 2015, HTSeq – a Python framework to work with high-throughput sequencing data, Bioinformatics, 31, 166, 10.1093/bioinformatics/btu638 Law, 2014, voom: precision weights unlock linear model analysis tools for RNA-seq read counts, Genome Biology, 15, R29, 10.1186/gb-2014-15-2-r29 Ferrari, 2015, Heart failure with preserved ejection fraction: uncertainties and dilemmas, European Journal of Heart Failure, 17, 665, 10.1002/ejhf.304 Graham, 2016, Chronic consumption of a western diet induces robust glial activation in aging mice and in a mouse model of Alzheimer's disease, Scientific Reports, 6, 21568, 10.1038/srep21568 Dai, 2002, The transcription factors GATA4 and dHAND physically interact to synergistically activate cardiac gene expression through a p300-dependent mechanism, Journal of Biological Chemistry, 277, 24390, 10.1074/jbc.M202490200 Dirkx, 2013, Nfat and miR-25 cooperate to reactivate the transcription factor Hand2 in heart failure, Nature Cell Biology, 15, 1282, 10.1038/ncb2866 Hartmann, 2015, The function of Rho-associated kinases ROCK1 and ROCK2 in the pathogenesis of cardiovascular disease, Frontiers in Pharmacology, 6, 276, 10.3389/fphar.2015.00276 Heineke, 2006, Regulation of cardiac hypertrophy by intracellular signalling pathways, Nature Reviews Molecular Cell Biology, 7, 589, 10.1038/nrm1983 Yanazume, 2003, Cardiac p300 is involved in myocyte growth with decompensated heart failure, Molecular and Cellular Biology, 23, 3593, 10.1128/MCB.23.10.3593-3606.2003 Djouadi, 1998, A gender-related defect in lipid metabolism and glucose homeostasis in peroxisome proliferator- activated receptor alpha- deficient mice, Journal of Clinical Investigation, 102, 1083, 10.1172/JCI3949 Luptak, 2005, Decreased contractile and metabolic reserve in peroxisome proliferator-activated receptor-alpha-null hearts can be rescued by increasing glucose transport and utilization, Circulation, 112, 2339, 10.1161/CIRCULATIONAHA.105.534594 Lopaschuk, 2010, Myocardial fatty acid metabolism in health and disease, Physiological Reviews, 90, 207, 10.1152/physrev.00015.2009 Aubert, 2016, The failing heart relies on ketone bodies as a fuel, Circulation, 133, 698, 10.1161/CIRCULATIONAHA.115.017355 Ventura-Clapier, 2004, Energy metabolism in heart failure, The Journal of Physiology, 555, 1, 10.1113/jphysiol.2003.055095 Doenst, 2013, Cardiac metabolism in heart failure: implications beyond ATP production, Circulation Research, 113, 709, 10.1161/CIRCRESAHA.113.300376 Chowdhury, 2015, A mouse model of human congenital heart disease: progressive atrioventricular block induced by a heterozygous Nkx2-5 homeodomain missense mutation, Circulation Arrhythmia and Electrophysiology, 8, 1255, 10.1161/CIRCEP.115.002720 Gutierrez-Roelens, 2002, Progressive AV-block and anomalous venous return among cardiac anomalies associated with two novel missense mutations in the CSX/NKX2-5 gene, Human Mutation, 20, 75, 10.1002/humu.9041 Jay, 2004, Nkx2-5 mutation causes anatomic hypoplasia of the cardiac conduction system, Journal of Clinical Investigation, 113, 1130, 10.1172/JCI19846 Pashmforoush, 2004, Nkx2-5 pathways and congenital heart disease; loss of ventricular myocyte lineage specification leads to progressive cardiomyopathy and complete heart block, Cell, 117, 373, 10.1016/S0092-8674(04)00405-2 Ritterhoff, 2017, Metabolism in cardiomyopathy: every substrate matters, Cardiovascular Research, 113, 411, 10.1093/cvr/cvx017 Taegtmeyer, 2016, Assessing cardiac metabolism: a scientific statement from the American Heart Association, Circulation Research, 118, 1659, 10.1161/RES.0000000000000097 Rena, 2017, The mechanisms of action of metformin, Diabetologia, 60, 1577, 10.1007/s00125-017-4342-z Wende, 2017, Metabolic origins of heart failure, JACC: Basic to Translational Science, 2, 297 Huss, 2005, Mitochondrial energy metabolism in heart failure: a question of balance, Journal of Clinical Investigation, 115, 547, 10.1172/JCI24405 Kundu, 2015, Remodeling of glucose metabolism precedes pressure overload-induced left ventricular hypertrophy: review of a hypothesis, Cardiology, 130, 211, 10.1159/000369782 Diez-Roux, 2011, A high-resolution anatomical atlas of the transcriptome in the mouse embryo, PLoS Biology, 9, e1000582, 10.1371/journal.pbio.1000582 Komuro, 1993, Csx: a murine homeobox-containing gene specifically expressed in the developing heart, Proceedings of the National Academy of Sciences of the United States of America, 90, 8145, 10.1073/pnas.90.17.8145 Stanley, 2002, Efficient Cre-mediated deletion in cardiac progenitor cells conferred by a 3'UTR-ires-Cre allele of the homeobox gene Nkx2-5, International Journal of Developmental Biology, 46, 431 Cardoso-Weide, 2015, DuOx2 promoter regulation by hormones, transcriptional factors and the coactivator TAZ, European Thyroid Journal, 4, 6, 10.1159/000379749 Dentice, 2006, Missense mutation in the transcription factor NKX2-5: a novel molecular event in the pathogenesis of thyroid dysgenesis, The Journal of Clinical Endocrinology and Metabolism, 91, 1428, 10.1210/jc.2005-1350 Dritsoula, 2018, Molecular basis for dysregulated activation of NKX2-5 in the vascular remodeling of systemic sclerosis, Arthritis & Rheumatology, 70, 920, 10.1002/art.40419 Du, 2016, Nkx2-5 is expressed in atherosclerotic plaques and attenuates development of atherosclerosis in apolipoprotein E-deficient mice, Journal of the American Heart Association, 5, 10.1161/JAHA.116.004440 Eppinga, 2017, Effect of metformin on metabolites and relation with myocardial infarct size and left ventricular ejection fraction after myocardial infarction, Circulation. Cardiovascular Genetics, 10, 10.1161/CIRCGENETICS.116.001564 Lexis, 2014, Effect of metformin on left ventricular function after acute myocardial infarction in patients without diabetes: the GIPS-III randomized clinical trial, Journal of the American Medical Association, 311, 1526, 10.1001/jama.2014.3315 Pernicova, 2014, Metformin – mode of action and clinical implications for diabetes and cancer, Nature Reviews Endocrinology, 10, 143, 10.1038/nrendo.2013.256 Kim, 2016, Metformin prevents fatty liver and improves balance of white/brown adipose in an obesity mouse model by inducing FGF21, Mediators of Inflammation, 2016, 5813030, 10.1155/2016/5813030 Riera-Borrull, 2017, Metformin potentiates the benefits of dietary restraint: a metabolomic study, International Journal of Molecular Sciences, 18, 10.3390/ijms18112263 Tajima, 2013, Metformin prevents liver tumorigenesis induced by high-fat diet in C57Bl/6 mice, American Journal of Physiology. Endocrinology and Metabolism, 305, E987, 10.1152/ajpendo.00133.2013 Martin-Montalvo, 2013, Metformin improves healthspan and lifespan in mice, Nature Communications, 4, 2192, 10.1038/ncomms3192 Valencia, 2017, Metformin and ageing: improving ageing outcomes beyond glycaemic control, Diabetologia, 60, 1630, 10.1007/s00125-017-4349-5 Heckman-Stoddard, 2017, Repurposing metformin for the prevention of cancer and cancer recurrence, Diabetologia, 60, 1639, 10.1007/s00125-017-4372-6 Griffin, 2017, Impact of metformin on cardiovascular disease: a meta-analysis of randomised trials among people with type 2 diabetes, Diabetologia, 60, 1620, 10.1007/s00125-017-4337-9 Kobashigawa, 2014, Metformin protects cardiomyocyte from doxorubicin induced cytotoxicity through an AMP-activated protein kinase dependent signaling pathway: an in vitro study, PLoS One, 9, e104888, 10.1371/journal.pone.0104888 Sun, 2017, Metformin improves cardiac function in mice with heart failure after myocardial infarction by regulating mitochondrial energy metabolism, Biochemical and Biophysical Research Communications, 486, 329, 10.1016/j.bbrc.2017.03.036 Tzanavari, 2016, Metformin protects against infection-induced myocardial dysfunction, Metabolism, 65, 1447, 10.1016/j.metabol.2016.06.012 Lozano, 2018, Genetic heterogeneity of SLC22 family of transporters in drug disposition, Journal of Personalized Medicine, 8, 10.3390/jpm8020014 Gilboa, 2016, Congenital heart defects in the United States: estimating the magnitude of the affected population in 2010, Circulation, 134, 101, 10.1161/CIRCULATIONAHA.115.019307 Deen, 2016, Metabolic syndrome in adults with congenital heart disease, Journal of the American Heart Association, 5, e001132, 10.1161/JAHA.114.001132 Goodpaster, 2017, Metabolic flexibility in health and disease, Cell Metabolism, 25, 1027, 10.1016/j.cmet.2017.04.015 Neglia, 2007, Impaired myocardial metabolic reserve and substrate selection flexibility during stress in patients with idiopathic dilated cardiomyopathy, American Journal of Physiology: Heart and Circulatory Physiology, 293, H3270 Brown, 2017, Expert consensus document: mitochondrial function as a therapeutic target in heart failure, Nature Reviews Cardiology, 14, 238, 10.1038/nrcardio.2016.203