ArticleCirculation2014
Early remodeling of perinuclear Ca2+ stores and nucleoplasmic Ca2+ signaling during the development of hypertrophy and heart failure.
Open access · bronzeAbstract readComparative Study
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Article in Circulation, 2014. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 51 papers.
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51citing papers in PubMed
3.1field-weighted citation impact, top 8% of its field
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Who cites it
51 citing papers in PubMed, 85 citations in OpenAlex.
- Local calcium dynamics and signalling in cardiomyocytes.Nature reviews. Cardiology · 2026Review
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- A transmission electron microscopy platform for assessing mitochondrial and nuclear architecture in cardiomyocytes.Cell reports methods · 2025Article
- Mechano-energetic uncoupling in heart failure.Nature reviews. Cardiology · 2025Review
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- Improving effect of physical exercise on heart failure: Reducing oxidative stress-induced inflammation by restoring CaMolecular and cellular biochemistry · 2025Review
- Increased Risk for Atrial Alternans in Rabbit Heart Failure: The Role of CaBiomolecules · 2023Article
- Altering Calcium Sensitivity in Heart Failure: A Crossroads of Disease Etiology and Therapeutic Innovation.International journal of molecular sciences · 2023Review
- MicroRNAs in Small Extracellular Vesicles from Amniotic Fluid and Maternal Plasma Associated with Fetal Palate Development in Mice.International journal of molecular sciences · 2023Article
- Store-Operated Calcium Entry Increases Nuclear Calcium in Adult Rat Atrial and Ventricular Cardiomyocytes.Cells · 2023Article
- Cx43 can form functional channels at the nuclear envelope and modulate gene expression in cardiac cells.Open biology · 2023Article
- Nuclear Calcium in Cardiac (Patho)Physiology: Small Compartment, Big Impact.Biomedicines · 2023Review
- Functional remodelling of perinuclear mitochondria alters nucleoplasmic CaPhilosophical transactions of the Royal Society of London. Series B, Biological sciences · 2022Article
- Inositol 1,4,5-trisphosphate receptors in cardiomyocyte physiology and disease.Philosophical transactions of the Royal Society of London. Series B, Biological sciences · 2022Review
- CaJournal of translational medicine · 2022Article
- Loss of Nuclear Envelope Integrity and Increased Oxidant Production Cause DNA Damage in Adult Hearts Deficient in PKP2: A Molecular Substrate of ARVC.Circulation · 2022Article
- β-Adrenergic Receptor Stimulation Maintains NCX-CaMKII Axis and Prevents Overactivation ofBiomedicines · 2022Article
- Loss of autophagy protein ATG5 impairs cardiac capacity in mice and humans through diminishing mitochondrial abundance and disrupting Ca2+ cycling.Cardiovascular research · 2022Article
- Inositol 1,4,5-trisphosphate receptor - reactive oxygen signaling domain regulates excitation-contraction coupling in atrial myocytes.Journal of molecular and cellular cardiology · 2022Article
- Histone deacetylase 4 and 5 translocation elicited by microsecond pulsed electric field exposure is mediated by kinase activity.Frontiers in bioengineering and biotechnology · 2022Article
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Authors and funding
20 authors at 5 institutions in 3 countries.
Senka LjubojevicFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Snjezana RadulovicFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Gerd LeitingerFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Simon SedejFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Michael SachererFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Michael HolzerFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Claudia WinklerFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Elisabeth PritzFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Tobias MittlerFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Albrecht SchmidtFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Michael SereiniggFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Paulina WakulaFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Spyros ZissimopoulosFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Egbert BispingFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Heiner PostFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Gunther MarscheFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Julie BossuytFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Donald M BersFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Jens KockskämperFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.).
Burkert PieskeFrom the Department of Cardiology (S.L., S.R., S.S., M. Sacherer, C.W., T.M., A.S., P.W., E.B., H.P., B.P.), Institute of Cell Biology, Histology and Embryology (G.L., E.P.), Institute of Experimental and Clinical Pharmacology (M.H., G.M.), and Division of Transplantation Surgery (M. Sereinigg), Medical University of Graz, Graz, Austria; Ludwig Boltzmann Institute for Translational Heart Failure Research, Graz, Austria (S.L., S.S., P.W., E.B., B.P.); Department of Pharmacology, University of California, Davis, CA (S.L., J.B., D.M.B.); Wales Heart Research Institute, Cardiff University School of Medicine, Cardiff, United Kingdom (S.Z.); and Institute of Pharmacology and Clinical Pharmacy, Philipps University of Marburg, Marburg, Germany (J.K.). burkert.pieske@medunigraz.at jens.kockskaemper@staff.uni-marburg.de.
Cardiff University · GBLudwig Boltzmann Institute for Translational Heart Failure Research · ATLudwig Boltzmann Institute for Lung Vascular Research · ATUniversity of California, Davis · USCardiff Metropolitan University · GB
Funding
Program AdministrationP01HL080101 · NHLBI · UNIVERSITY OF CALIFORNIA AT DAVIS · PI BERS, DONALD M · 2006 to 2015
$23.4MBIOLOGY OF INFECTIOUS DISEASES TRAINING PROGRAMT32AI007641 · NIAID · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI MATTHEW G DORSEY · 2000 to 2026
$6.9MIONIC CONTROL OF CARDIAC MUSCLE CONTRACTION: EC COUPLINGR01HL030077 · NHLBI · UNIVERSITY OF CALIFORNIA RIVERSIDE · PI BERS, DONALD M · 1986 to 2018
$3.8MMulti-scale Systems Model of Murine Heart FailureR01HL105242 · NHLBI · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI BERS, DONALD M, MCCULLOCH, ANDREW D. · 2012 to 2016
$3.5MThe regulation and role of PKD in the heartR01HL103933 · NHLBI · UNIVERSITY OF CALIFORNIA AT DAVIS · PI BOSSUYT, JULIE B · 2010 to 2014
$1.9MAustrian Science Fund FWF T 607British Heart Foundation FS/08/063/25812NHLBI NIH HHS HL080101NHLBI NIH HHS P01 HL080101NHLBI NIH HHS R01 HL030077NHLBI NIH HHS R01 HL103933NHLBI NIH HHS R01-HL103933NHLBI NIH HHS R01 HL105242NIAID NIH HHS T32 AI007641
Abstract
backgroundA hallmark of heart failure is impaired cytoplasmic Ca(2+) handling of cardiomyocytes. It remains unknown whether specific alterations in nuclear Ca(2+) handling via altered excitation-transcription coupling contribute to the development and progression of heart failure. METHODS AND
resultsUsing tissue and isolated cardiomyocytes from nonfailing and failing human hearts, as well as mouse and rabbit models of hypertrophy and heart failure, we provide compelling evidence for structural and functional changes of the nuclear envelope and nuclear Ca(2+) handling in cardiomyocytes as remodeling progresses. Increased nuclear size and less frequent intrusions of the nuclear envelope into the nuclear lumen indicated altered nuclear structure that could have functional consequences. In the (peri)nuclear compartment, there was also reduced expression of Ca(2+) pumps and ryanodine receptors, increased expression of inositol-1,4,5-trisphosphate receptors, and differential orientation among these Ca(2+) transporters. These changes were associated with altered nucleoplasmic Ca(2+) handling in cardiomyocytes from hypertrophied and failing hearts, reflected as increased diastolic Ca(2+) levels with diminished and prolonged nuclear Ca(2+) transients and slowed intranuclear Ca(2+) diffusion. Altered nucleoplasmic Ca(2+) levels were translated to higher activation of nuclear Ca(2+)/calmodulin-dependent protein kinase II and nuclear export of histone deacetylases. Importantly, the nuclear Ca(2+) alterations occurred early during hypertrophy and preceded the cytoplasmic Ca(2+) changes that are typical of heart failure.
conclusionsDuring cardiac remodeling, early changes of cardiomyocyte nuclei cause altered nuclear Ca(2+) signaling implicated in hypertrophic gene program activation. Normalization of nuclear Ca(2+) regulation may therefore be a novel therapeutic approach to prevent adverse cardiac remodeling.
Indexed as
AnimalsCalciumCalcium-Calmodulin-Dependent Protein Kinase Type 2Calcium SignalingCardiomegalyCell NucleusDisease Models, AnimalElectric StimulationFemaleHeart FailureHistone DeacetylasesHumansInositol 1,4,5-Trisphosphate ReceptorsMaleMiceMice, Inbred C57BLCalciumCalcium-Calmodulin-Dependent Protein Kinase Type 2Histone DeacetylasesInositol 1,4,5-Trisphosphate Receptorscalcium signalingheart failurenuclear enveloperemodeling
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