Molecular and cellular neurocardiology: development, and cellular and molecular adaptations to heart disease

The nervous system and cardiovascular system develop in concert and are functionally interconnected in both health and disease. This white paper focuses on the cellular and molecular mechanisms that underlie neural–cardiac interactions during development, during normal physiological function in the mature system, and during pathological remodelling in cardiovascular disease. The content on each subject was contributed by experts, and we hope that this will provide a useful resource for newcomers to neurocardiology as well as aficionados.

[1]  D. Paterson,et al.  Protection against ventricular fibrillation via cholinergic receptor stimulation and the generation of nitric oxide , 2016, The Journal of physiology.

[2]  C. Ripplinger,et al.  Molecular Mechanisms of Sympathetic Remodeling and Arrhythmias. , 2016, Circulation. Arrhythmia and electrophysiology.

[3]  W. Woodward,et al.  Myocardial Infarction Causes Transient Cholinergic Transdifferentiation of Cardiac Sympathetic Nerves via gp130 , 2016, The Journal of Neuroscience.

[4]  S. Birren,et al.  Innervating sympathetic neurons regulate heart size and the timing of cardiomyocyte cell cycle withdrawal , 2015, The Journal of physiology.

[5]  Pradeep S Rajendran,et al.  Central-peripheral neural network interactions evoked by vagus nerve stimulation: functional consequences on control of cardiac function. , 2015, American journal of physiology. Heart and circulatory physiology.

[6]  M. Lythgoe,et al.  Control of ventricular excitability by neurons of the dorsal motor nucleus of the vagus nerve , 2015, Heart rhythm.

[7]  M. Kay,et al.  Neurotransmission to parasympathetic cardiac vagal neurons in the brain stem is altered with left ventricular hypertrophy-induced heart failure. , 2015, American journal of physiology. Heart and circulatory physiology.

[8]  D. Bers,et al.  S-Nitrosylation Induces Both Autonomous Activation and Inhibition of Calcium/Calmodulin-dependent Protein Kinase II δ* , 2015, The Journal of Biological Chemistry.

[9]  Richard T. Lee,et al.  Nerves Regulate Cardiomyocyte Proliferation and Heart Regeneration. , 2015, Developmental cell.

[10]  D. Bers,et al.  CaMKIIδ mediates β-adrenergic effects on RyR2 phosphorylation and SR Ca(2+) leak and the pathophysiological response to chronic β-adrenergic stimulation. , 2015, Journal of molecular and cellular cardiology.

[11]  Stefan Luther,et al.  Optogenetic determination of the myocardial requirements for extrasystoles by cell type-specific targeting of ChannelRhodopsin-2 , 2015, Proceedings of the National Academy of Sciences.

[12]  Ian A. White,et al.  Sympathetic Reinnervation Is Required for Mammalian Cardiac Regeneration. , 2015, Circulation research.

[13]  M. Zaccolo,et al.  Efficacy of B-Type Natriuretic Peptide Is Coupled to Phosphodiesterase 2A in Cardiac Sympathetic Neurons , 2015, Hypertension.

[14]  Udi Nussinovitch,et al.  Optogenetics for in vivo cardiac pacing and resynchronization therapies , 2015, Nature Biotechnology.

[15]  D. Paterson,et al.  CAPON Modulates Neuronal Calcium Handling and Cardiac Sympathetic Neurotransmission During Dysautonomia in Hypertension , 2015, Hypertension.

[16]  E. Niggli,et al.  Maximal acceleration of Ca2+ release refractoriness by β‐adrenergic stimulation requires dual activation of kinases PKA and CaMKII in mouse ventricular myocytes , 2015, The Journal of physiology.

[17]  Donald M Bers,et al.  Decreased inward rectifying K+ current and increased ryanodine receptor sensitivity synergistically contribute to sustained focal arrhythmia in the intact rabbit heart , 2015, The Journal of physiology.

[18]  D. Kass,et al.  Cardiac resynchronization therapy restores sympathovagal balance in the failing heart by differential remodeling of cholinergic signaling. , 2015, Circulation research.

[19]  W. Woodward,et al.  Targeting protein tyrosine phosphatase σ after myocardial infarction restores cardiac sympathetic innervation and prevents arrhythmias , 2015, Nature Communications.

[20]  M. Kay,et al.  Optogenetic release of norepinephrine from cardiac sympathetic neurons alters mechanical and electrical function. , 2015, Cardiovascular research.

[21]  Richard T. Lee,et al.  A systematic analysis of neonatal mouse heart regeneration after apical resection. , 2015, Journal of molecular and cellular cardiology.

[22]  N. Herring Autonomic control of the heart: going beyond the classical neurotransmitters , 2014, Experimental physiology.

[23]  X. Wehrens,et al.  Oxidative stress and ca(2+) release events in mouse cardiomyocytes. , 2014, Biophysical journal.

[24]  N. Chattipakorn,et al.  Vagus nerve stimulation initiated late during ischemia, but not reperfusion, exerts cardioprotection via amelioration of cardiac mitochondrial dysfunction. , 2014, Heart rhythm.

[25]  Aleksandra Klimas,et al.  Cardiac applications of optogenetics. , 2014, Progress in biophysics and molecular biology.

[26]  P. Schwartz Cardiac sympathetic denervation to prevent life-threatening arrhythmias , 2014, Nature Reviews Cardiology.

[27]  Xin Wang,et al.  Optogenetic Stimulation of Locus Ceruleus Neurons Augments Inhibitory Transmission to Parasympathetic Cardiac Vagal Neurons via Activation of Brainstem α1 and β1 Receptors , 2014, The Journal of Neuroscience.

[28]  Douglas P. Zipes,et al.  Role of the Autonomic Nervous System in Modulating Cardiac Arrhythmias , 2014, Circulation research.

[29]  A. Mahajan,et al.  Cardiac sympathetic denervation in patients with refractory ventricular arrhythmias or electrical storm: intermediate and long-term follow-up. , 2014, Heart rhythm.

[30]  A. Gourine,et al.  Neural Mechanisms of Cardioprotection , 2014, Physiology.

[31]  Kyung-In Jang,et al.  3D multifunctional integumentary membranes for spatiotemporal cardiac measurements and stimulation across the entire epicardium , 2014, Nature Communications.

[32]  D. Bers,et al.  Nitric Oxide-Dependent Activation of CaMKII Increases Diastolic Sarcoplasmic Reticulum Calcium Release in Cardiac Myocytes in Response to Adrenergic Stimulation , 2014, PloS one.

[33]  A. Curtis,et al.  Regional myocardial sympathetic denervation predicts the risk of sudden cardiac arrest in ischemic cardiomyopathy. , 2014, Journal of the American College of Cardiology.

[34]  M. Rubart,et al.  In situ three-dimensional reconstruction of mouse heart sympathetic innervation by two-photon excitation fluorescence imaging , 2014, Journal of Neuroscience Methods.

[35]  G. Haddad,et al.  Calcitonin Gene-Related Peptide Regulates Cardiomyocyte Survival through Regulation of Oxidative Stress by PI3K/Akt and MAPK Signaling Pathways. , 2014, Annals of clinical and experimental hypertension.

[36]  N. Herring,et al.  Peripheral cardiac sympathetic hyperactivity in cardiovascular disease: role of neuropeptides. , 2013, American journal of physiology. Regulatory, integrative and comparative physiology.

[37]  E. Niggli,et al.  NO-dependent CaMKII activation during b -adrenergic stimulation of cardiac muscle , 2013 .

[38]  R. Weiss,et al.  Oxidized Ca2+/Calmodulin-Dependent Protein Kinase II Triggers Atrial Fibrillation , 2013, Circulation.

[39]  Wei Zhou,et al.  Focal myocardial infarction induces global remodeling of cardiac sympathetic innervation: neural remodeling in a spatial context. , 2013, American journal of physiology. Heart and circulatory physiology.

[40]  D. Paterson,et al.  Cardiac sympathetic dysfunction in the prehypertensive spontaneously hypertensive rat. , 2013, American journal of physiology. Heart and circulatory physiology.

[41]  J. Coote Myths and realities of the cardiac vagus , 2013, The Journal of physiology.

[42]  Gerald W. Hart,et al.  Diabetic Hyperglycemia activates CaMKII and Arrhythmias by O linked Glycosylation , 2013, Nature.

[43]  J. S. Janicki,et al.  Alpha-calcitonin gene-related peptide is protective against pressure overload-induced heart failure , 2013, Regulatory Peptides.

[44]  Zheng Guo,et al.  CGRP inhibits norepinephrine induced apoptosis with restoration of Bcl-2/Bax in cultured cardiomyocytes of rat , 2013, Neuroscience Letters.

[45]  F. Atienza,et al.  Nerves projecting from the intrinsic cardiac ganglia of the pulmonary veins modulate sinoatrial node pacemaker function. , 2013, Cardiovascular research.

[46]  J. Walter,et al.  Hypertrophy of Neurons Within Cardiac Ganglia in Human, Canine, and Rat Heart Failure: The Potential Role of Nerve Growth Factor , 2013, Journal of the American Heart Association.

[47]  B. Habecker,et al.  Infarct-Derived Chondroitin Sulfate Proteoglycans Prevent Sympathetic Reinnervation after Cardiac Ischemia-Reperfusion Injury , 2013, The Journal of Neuroscience.

[48]  Wei Zhou,et al.  Functional differences between junctional and extrajunctional adrenergic receptor activation in mammalian ventricle. , 2013, American journal of physiology. Heart and circulatory physiology.

[49]  B. Prendergast,et al.  Relationship of plasma neuropeptide Y with angiographic, electrocardiographic and coronary physiology indices of reperfusion during ST elevation myocardial infarction , 2013, Heart.

[50]  F. Wang,et al.  Cardiotoxic and Cardioprotective Features of Chronic &bgr;-Adrenergic Signaling , 2013, Circulation research.

[51]  Y. Kakinuma,et al.  Heart‐Specific Overexpression of Choline Acetyltransferase Gene Protects Murine Heart Against Ischemia Through Hypoxia‐Inducible Factor‐1α–Related Defense Mechanisms , 2013, Journal of the American Heart Association.

[52]  D. Paterson,et al.  Ganglion-Specific Impairment of the Norepinephrine Transporter in the Hypertensive Rat , 2013, Hypertension.

[53]  D. Paterson,et al.  Targeted Neuronal Nitric Oxide Synthase Transgene Delivery Into Stellate Neurons Reverses Impaired Intracellular Calcium Transients in Prehypertensive Rats , 2013, Hypertension.

[54]  W. Woodward,et al.  Altered atrial neurotransmitter release in transgenic p75−/− and gp130 KO mice , 2012, Neuroscience Letters.

[55]  A. Rokita,et al.  New Therapeutic Targets in Cardiology: Arrhythmias and Ca2+/Calmodulin-Dependent Kinase II (CaMKII) , 2012, Circulation.

[56]  D. Hoover,et al.  Development of cardiac parasympathetic neurons, glial cells, and regional cholinergic innervation of the mouse heart , 2012, Neuroscience.

[57]  Mark E. Anderson,et al.  CaMKII determines mitochondrial stress responses in heart , 2012, Nature.

[58]  K. M. Spyer,et al.  Cardioprotection evoked by remote ischaemic preconditioning is critically dependent on the activity of vagal pre-ganglionic neurones , 2012, Cardiovascular research.

[59]  Mark E. Anderson,et al.  Calmodulin-dependent protein kinase II: linking heart failure and arrhythmias. , 2012, Circulation research.

[60]  Donald M Bers,et al.  Local &bgr;-Adrenergic Stimulation Overcomes Source-Sink Mismatch to Generate Focal Arrhythmia , 2012, Circulation research.

[61]  R. Lux,et al.  Sympathetic stimulation increases dispersion of repolarization in humans with myocardial infarction. , 2012, American journal of physiology. Heart and circulatory physiology.

[62]  Donald M. Bers,et al.  Requirement for Ca 2+/calmodulin-dependent kinase II in the transition from pressure overload-induced cardiac hypertrophy to heart failure in mice (Journal of Clinical Investigation (2009) 119, 5, (1230-1240) doi: 10.1172/JCI38022) , 2012 .

[63]  Jack Waters,et al.  Selective optogenetic stimulation of cholinergic axons in neocortex. , 2012, Journal of neurophysiology.

[64]  Lan Zhou,et al.  Nerve Sprouting Contributes to Increased Severity of Ventricular Tachyarrhythmias by Upregulating iGluRs in Rats with Healed Myocardial Necrotic Injury , 2012, Journal of Molecular Neuroscience.

[65]  D. Paterson,et al.  The cardiac sympathetic co-transmitter galanin reduces acetylcholine release and vagal bradycardia: Implications for neural control of cardiac excitability , 2012, Journal of molecular and cellular cardiology.

[66]  D. Paterson,et al.  Abnormal Intracellular Calcium Homeostasis in Sympathetic Neurons From Young Prehypertensive Rats , 2012, Hypertension.

[67]  M. Kuehl,et al.  Cardiovascular autonomic neuropathies as complications of diabetes mellitus , 2012, Nature Reviews Endocrinology.

[68]  L H Wang,et al.  Serum Levels of Calcitonin Gene-Related Peptide and Substance P are Decreased in Patients with Diabetes Mellitus and Coronary Artery Disease , 2012, The Journal of international medical research.

[69]  K. Kimura,et al.  Development, Maturation, and Transdifferentiation of Cardiac Sympathetic Nerves , 2012, Circulation research.

[70]  S. Werns Effect of Nesiritide in Patients with Acute Decompensated Heart Failure , 2012 .

[71]  J. S. Janicki,et al.  Substance P induces adverse myocardial remodelling via a mechanism involving cardiac mast cells. , 2011, Cardiovascular research.

[72]  Mark E. Anderson,et al.  Oxidation of CaMKII determines the cardiotoxic effects of aldosterone , 2011, Nature Medicine.

[73]  Jay T. Groves,et al.  A Mechanism for Tunable Autoinhibition in the Structure of a Human Ca2+/Calmodulin- Dependent Kinase II Holoenzyme , 2011, Cell.

[74]  J. Coote,et al.  Vagus nerve stimulation protects against ventricular fibrillation independent of muscarinic receptor activation. , 2011, Cardiovascular research.

[75]  Niels Voigt,et al.  Oxidized CaMKII causes cardiac sinus node dysfunction in mice. , 2011, The Journal of clinical investigation.

[76]  L. Deckelbaum,et al.  Effect of nesiritide in patients with acute decompensated heart failure. , 2011, The New England journal of medicine.

[77]  D. Hoover,et al.  Remodeling of cardiac cholinergic innervation and control of heart rate in mice with streptozotocin-induced diabetes , 2011, Autonomic Neuroscience.

[78]  M. Cutler,et al.  Cardiac electrical remodeling in health and disease. , 2011, Trends in pharmacological sciences.

[79]  E. Olson,et al.  Transient Regenerative Potential of the Neonatal Mouse Heart , 2011, Science.

[80]  D. Paterson,et al.  Pravastatin normalises peripheral cardiac sympathetic hyperactivity in the spontaneously hypertensive rat , 2011, Journal of molecular and cellular cardiology.

[81]  Yonggang Huang,et al.  Waterproof AlInGaP optoelectronics on stretchable substrates with applications in biomedicine and robotics. , 2010, Nature materials.

[82]  K. Kimura,et al.  Norepinephrine-induced nerve growth factor depletion causes cardiac sympathetic denervation in severe heart failure , 2010, Autonomic Neuroscience.

[83]  T. Nakata,et al.  Impaired Cardiac Sympathetic Innervation and Myocardial Perfusion Are Related to Lethal Arrhythmia: Quantification of Cardiac Tracers in Patients with ICDs , 2010, The Journal of Nuclear Medicine.

[84]  Jeroen J. Bax,et al.  Cardiac sympathetic denervation assessed with 123-iodine metaiodobenzylguanidine imaging predicts ventricular arrhythmias in implantable cardioverter-defibrillator patients. , 2010, Journal of the American College of Cardiology.

[85]  B. Habecker,et al.  Heterogeneous ventricular sympathetic innervation, altered beta-adrenergic receptor expression, and rhythm instability in mice lacking the p75 neurotrophin receptor. , 2010, American journal of physiology. Heart and circulatory physiology.

[86]  C. Lagrasta,et al.  Nerve Growth Factor Promotes Cardiac Repair following Myocardial Infarction , 2010, Circulation research.

[87]  H. Okano,et al.  Heart failure causes cholinergic transdifferentiation of cardiac sympathetic nerves via gp130-signaling cytokines in rodents. , 2010, The Journal of clinical investigation.

[88]  H. Rohrer,et al.  Infarction‐induced cytokines cause local depletion of tyrosine hydroxylase in cardiac sympathetic nerves , 2010, Experimental physiology.

[89]  J. Paton,et al.  Control of cardiac contractility in the rat working heart–brainstem preparation , 2010, Experimental physiology.

[90]  金澤 英明 Heart failure causes cholinergic transdifferentiation of cardiac sympathetic nerves via gp130-signaling cytokines in rodents , 2010 .

[91]  西里 仁男 Impaired cardiac sympathetic innervation and myocardial perfusion are related to lethal arrhythmia : quantification of cardiac tracers in patients with ICDs , 2010 .

[92]  P. Pagé,et al.  Localization of multiple neurotransmitters in surgically derived specimens of human atrial ganglia , 2009, Neuroscience.

[93]  K. Fukuda,et al.  Cardiac Innervation and Sudden Cardiac Death , 2009, Current cardiology reviews.

[94]  Y. Kakinuma,et al.  Cholinoceptive and cholinergic properties of cardiomyocytes involving an amplification mechanism for vagal efferent effects in sparsely innervated ventricular myocardium , 2009, The FEBS journal.

[95]  J. Coote,et al.  Direct evidence of nitric oxide release from neuronal nitric oxide synthase activation in the left ventricle as a result of cervical vagus nerve stimulation , 2009, The Journal of physiology.

[96]  Tong Zhang,et al.  Requirement for Ca2+/calmodulin-dependent kinase II in the transition from pressure overload-induced cardiac hypertrophy to heart failure in mice. , 2009, The Journal of clinical investigation.

[97]  J. Luther,et al.  p75 and TrkA Signaling Regulates Sympathetic Neuronal Firing Patterns via Differential Modulation of Voltage-Gated Currents , 2009, The Journal of Neuroscience.

[98]  X. Wehrens,et al.  Calmodulin kinase II is required for fight or flight sinoatrial node physiology , 2009, Proceedings of the National Academy of Sciences.

[99]  U. Schotten,et al.  Regulation of nerve growth factor in the heart: the role of the calcineurin-NFAT pathway. , 2009, Journal of molecular and cellular cardiology.

[100]  Geoffrey Burnstock,et al.  Autonomic neurotransmission: 60 years since sir Henry Dale. , 2009, Annual review of pharmacology and toxicology.

[101]  Michael Z. Lin,et al.  Characterization of engineered channelrhodopsin variants with improved properties and kinetics. , 2009, Biophysical journal.

[102]  T. Rea,et al.  Genetic Variations in Nitric Oxide Synthase 1 Adaptor Protein Are Associated With Sudden Cardiac Death in US White Community-Based Populations , 2009, Circulation.

[103]  Hugo A. Katus,et al.  The δ isoform of CaM kinase II is required for pathological cardiac hypertrophy and remodeling after pressure overload , 2009, Proceedings of the National Academy of Sciences.

[104]  T. Südhof,et al.  Membrane Fusion: Grappling with SNARE and SM Proteins , 2009, Science.

[105]  D. Henderson,et al.  Autonomic innervation of the developing heart: Origins and function , 2009, Clinical anatomy.

[106]  M. Barlow,et al.  Repeated Arterial Occlusion, Delta-Opioid Receptor (DOR) Plasticity and Vagal Transmission Within the Sinoatrial Node of the Anesthetized Dog , 2009, Experimental biology and medicine.

[107]  D. Hoover,et al.  Structural and functional cardiac cholinergic deficits in adult neurturin knockout mice , 2008, Cardiovascular research.

[108]  Ji-min Cao,et al.  Chemical sympathetic denervation, suppression of myocardial transient outward potassium current, and ventricular fibrillation in the rat. , 2008, Canadian journal of physiology and pharmacology.

[109]  R. Blakely,et al.  Cholinergic neurons of mouse intrinsic cardiac ganglia contain noradrenergic enzymes, norepinephrine transporters, and the neurotrophin receptors tropomyosin-related kinase A and p75 , 2008, Neuroscience.

[110]  D. Paterson,et al.  Cardiac cholinergic NO-cGMP signaling following acute myocardial infarction and nNOS gene transfer. , 2008, American journal of physiology. Heart and circulatory physiology.

[111]  J. Ardell,et al.  Neurochemical diversity of afferent neurons that transduce sensory signals from dog ventricular myocardium , 2008, Autonomic Neuroscience.

[112]  B. Habecker,et al.  Regulation of cardiac innervation and function via the p75 neurotrophin receptor , 2008, Autonomic Neuroscience.

[113]  Mark E. Anderson,et al.  A Dynamic Pathway for Calcium-Independent Activation of CaMKII by Methionine Oxidation , 2008, Cell.

[114]  J. Moon,et al.  Target-dependent inhibition of sympathetic neuron growth via modulation of a BMP signaling pathway. , 2008, Developmental biology.

[115]  D. Paterson,et al.  Neuropeptide Y reduces acetylcholine release and vagal bradycardia via a Y2 receptor-mediated, protein kinase C-dependent pathway. , 2008, Journal of molecular and cellular cardiology.

[116]  D. Bers Calcium cycling and signaling in cardiac myocytes. , 2008, Annual review of physiology.

[117]  J. A. Armour,et al.  Potential clinical relevance of the ‘little brain’ on the mammalian heart , 2008, Experimental physiology.

[118]  J. Wess,et al.  Deficiency of M2 muscarinic acetylcholine receptors increases susceptibility of ventricular function to chronic adrenergic stress. , 2008, American journal of physiology. Heart and circulatory physiology.

[119]  D. Paterson,et al.  Neuronal nitric oxide synthase gene transfer decreases [Ca2+]i in cardiac sympathetic neurons. , 2007, Journal of molecular and cellular cardiology.

[120]  M. Sugimachi,et al.  Angiotensin II attenuates myocardial interstitial acetylcholine release in response to vagal stimulation. , 2007, American journal of physiology. Heart and circulatory physiology.

[121]  D. Paterson,et al.  Noradrenergic Cell Specific Gene Transfer With Neuronal Nitric Oxide Synthase Reduces Cardiac Sympathetic Neurotransmission in Hypertensive Rats , 2007, Hypertension.

[122]  K. Yoshimi,et al.  Cardiac Sympathetic Rejuvenation: A Link Between Nerve Function and Cardiac Hypertrophy , 2007, Circulation research.

[123]  K. Kimura,et al.  Sema3a maintains normal heart rhythm through sympathetic innervation patterning , 2007, Nature Medicine.

[124]  S. Satoh,et al.  Re-expression of proteins involved in cytokinesis during cardiac hypertrophy. , 2007, Experimental cell research.

[125]  J. Coote,et al.  Autonomic modulation of electrical restitution, alternans and ventricular fibrillation initiation in the isolated heart. , 2007, Cardiovascular research.

[126]  Julian F. Thayer,et al.  The role of vagal function in the risk for cardiovascular disease and mortality , 2007, Biological Psychology.

[127]  D. Paterson,et al.  Gene Transfer of Neuronal Nitric Oxide Synthase into Intracardiac Ganglia Reverses Vagal Impairment in Hypertensive Rats , 2007, Hypertension.

[128]  T. Donohue,et al.  Sympathetic hyperinnervation and inflammatory cell NGF synthesis following myocardial infarction in rats , 2006, Brain Research.

[129]  M. Eren,et al.  Calmodulin kinase II inhibition protects against myocardial cell apoptosis in vivo. , 2006, American journal of physiology. Heart and circulatory physiology.

[130]  K. Kimura,et al.  Nerve Growth Factor Is Critical for Cardiac Sensory Innervation and Rescues Neuropathy in Diabetic Hearts , 2006, Circulation.

[131]  B. Habecker,et al.  The lack of cardiotrophin-1 alters expression of interleukin-6 and leukemia inhibitory factor mRNA but does not impair cardiac injury response. , 2006, Cytokine.

[132]  H. Katus,et al.  Preserved norepinephrine reuptake but reduced sympathetic nerve endings in hypertrophic volume-overloaded rat hearts. , 2006, Journal of cardiac failure.

[133]  J. Luther,et al.  Nerve growth factor decreases potassium currents and alters repetitive firing in rat sympathetic neurons. , 2006, Journal of neurophysiology.

[134]  E. Callaway,et al.  Selective and Quickly Reversible Inactivation of Mammalian Neurons In Vivo Using the Drosophila Allatostatin Receptor , 2006, Neuron.

[135]  Christian Gieger,et al.  A common genetic variant in the NOS1 regulator NOS1AP modulates cardiac repolarization , 2006, Nature Genetics.

[136]  D. Hoover,et al.  Localization of cholinergic innervation and neurturin receptors in adult mouse heart and expression of the neurturin gene , 2006, Cell and Tissue Research.

[137]  S. Vatner,et al.  Down regulation of the L-type Ca2+ channel, GRK2, and phosphorylated phospholamban: protective mechanisms for the denervated failing heart. , 2006, Journal of molecular and cellular cardiology.

[138]  F. Markos,et al.  Vasoactive intestinal polypeptide receptor antagonism enhances the vagally induced increase in cardiac interval of the rat atrium in vitro , 2006, Experimental physiology.

[139]  A. H. Jan Danser,et al.  The role of calcitonin gene-related peptide (CGRP) in ischemic preconditioning in isolated rat hearts. , 2006, European journal of pharmacology.

[140]  K. Deisseroth,et al.  Millisecond-timescale, genetically targeted optical control of neural activity , 2005, Nature Neuroscience.

[141]  D. Ginty,et al.  Growth and survival signals controlling sympathetic nervous system development. , 2005, Annual review of neuroscience.

[142]  Guy Salama,et al.  Calmodulin kinase II inhibition protects against structural heart disease , 2005, Nature Medicine.

[143]  A. Dobson,et al.  How well does B-type natriuretic peptide predict death and cardiac events in patients with heart failure: systematic review , 2005, BMJ : British Medical Journal.

[144]  R. Robinson,et al.  Cardiac ion channel expression and regulation: the role of innervation. , 2004, Journal of molecular and cellular cardiology.

[145]  J. Nerbonne,et al.  Heterogeneous expression of repolarizing, voltage‐gated K+ currents in adult mouse ventricles , 2004, The Journal of physiology.

[146]  M. Fishbein,et al.  Mechanisms of Cardiac Nerve Sprouting After Myocardial Infarction in Dogs , 2004, Circulation research.

[147]  S. Brain,et al.  Vascular actions of calcitonin gene-related peptide and adrenomedullin. , 2004, Physiological reviews.

[148]  B. Habecker,et al.  Infarction alters both the distribution and noradrenergic properties of cardiac sympathetic neurons. , 2004, American journal of physiology. Heart and circulatory physiology.

[149]  H. Katus,et al.  Adrenergic regulation of the rapid component of the cardiac delayed rectifier potassium current, IKr, and the underlying hERG ion channel , 2004, Basic Research in Cardiology.

[150]  R. Blakely,et al.  Localization of cholinergic innervation in guinea pig heart by immunohistochemistry for high-affinity choline transporters. , 2004, Cardiovascular research.

[151]  H. Okano,et al.  Endothelin-1 regulates cardiac sympathetic innervation in the rodent heart by controlling nerve growth factor expression. , 2004, The Journal of clinical investigation.

[152]  J. Coote,et al.  Interaction between direct sympathetic and vagus nerve stimulation on heart rate in the isolated rabbit heart , 2004, Experimental physiology.

[153]  Masaru Sugimachi,et al.  Vagal Nerve Stimulation Markedly Improves Long-Term Survival After Chronic Heart Failure in Rats , 2003, Circulation.

[154]  H. Kato,et al.  Captopril enhances cardiac vagal but not sympathetic neurotransmission in pithed rats. , 2004, Journal of pharmacological sciences.

[155]  L. Rochette,et al.  Calcitonin gene-related peptide partly protects cultured smooth muscle cells from apoptosis induced by an oxidative stress via activation of ERK1/2 MAPK. , 2003, Biochimica et biophysica acta.

[156]  John D. Slonimsky,et al.  BDNF and CNTF regulate cholinergic properties of sympathetic neurons through independent mechanisms , 2003, Molecular and Cellular Neuroscience.

[157]  M. Fishbein,et al.  Sympathetic Nerve Sprouting, Electrical Remodeling, and Increased Vulnerability to Ventricular Fibrillation in Hypercholesterolemic Rabbits , 2003, Circulation research.

[158]  J. Caffrey,et al.  Cardiac enkephalins interrupt vagal bradycardia via δ2-opioid receptors in sinoatrial node , 2003 .

[159]  K. Maehara,et al.  Decreased contractility of the left ventricle is induced by the neurotransmitter acetylcholine, but not by vagal stimulation in rats. , 2003, Japanese heart journal.

[160]  A. Coulombe,et al.  Expression of heart K+ channels in adrenalectomized and catecholamine-depleted reserpine-treated rats. , 2003, Journal of molecular and cellular cardiology.

[161]  L. Biblo,et al.  Identification and Characterization of Atrioventricular Parasympathetic Innervation in Humans , 2002, Journal of cardiovascular electrophysiology.

[162]  T. McDonald,et al.  14‐3‐3 amplifies and prolongs adrenergic stimulation of HERG K+ channel activity , 2002, The EMBO journal.

[163]  Junko Kurokawa,et al.  Requirement of a Macromolecular Signaling Complex for β Adrenergic Receptor Modulation of the KCNQ1-KCNE1 Potassium Channel , 2002, Science.

[164]  D. Bers Cardiac excitation–contraction coupling , 2002, Nature.

[165]  R. Vulapalli,et al.  Loss of cardiac sympathetic neurotransmitters in heart failure and NE infusion is associated with reduced NGF. , 2002, American journal of physiology. Heart and circulatory physiology.

[166]  N. Herring,et al.  NO-cGMP pathway increases the hyperpolarisation-activated current, I(f), and heart rate during adrenergic stimulation. , 2001, Cardiovascular research.

[167]  J. Caffrey,et al.  Delta Opioid Receptors Inhibit Vagal Bradycardia in the Sinoatrial Node , 2001, Journal of cardiovascular pharmacology and therapeutics.

[168]  D. Paterson,et al.  Natriuretic peptides like NO facilitate cardiac vagal neurotransmission and bradycardia via a cGMP pathway. , 2001, American journal of physiology. Heart and circulatory physiology.

[169]  T. A. Harrison,et al.  Distribution of cocaine‐ and amphetamine‐regulated transcript peptide in the guinea pig intrinsic cardiac nervous system and colocalization with neuropeptides or transmitter synthetic enzymes , 2001, The Journal of comparative neurology.

[170]  O. Isacson,et al.  A high-efficiency synthetic promoter that drives transgene expression selectively in noradrenergic neurons. , 2001, Human gene therapy.

[171]  D. Paterson,et al.  Nitric oxide‐cGMP pathway facilitates acetylcholine release and bradycardia during vagal nerve stimulation in the guinea‐pig in vitro , 2001, The Journal of physiology.

[172]  J. Townend,et al.  Vagus nerve stimulation decreases left ventricular contractility in vivo in the human and pig heart , 2001, The Journal of physiology.

[173]  Li Li,et al.  Arrhythmogenesis and Contractile Dysfunction in Heart Failure: Roles of Sodium-Calcium Exchange, Inward Rectifier Potassium Current, and Residual &bgr;-Adrenergic Responsiveness , 2001, Circulation research.

[174]  H. Schultz Cardiac Vagal Chemosensory Afferents , 2001 .

[175]  J. Longhurst,et al.  Cardiac Sympathetic Afferent Activation Provoked by Myocardial Ischemia and Reperfusion , 2001, Annals of the New York Academy of Sciences.

[176]  J. Coote,et al.  Effects of Direct Sympathetic and Vagus Nerve Stimulation on the Physiology of the Whole Heart – A Novel Model of Isolated Langendorff Perfused Rabbit Heart with Intact Dual Autonomic Innervation , 2001, Experimental physiology.

[177]  J. Caffrey,et al.  Local opiate receptors in the sinoatrial node moderate vagal bradycardia , 2001, Autonomic Neuroscience.

[178]  J. Ardell Neurohumoral Control of Cardiac Function , 2001 .

[179]  M. Hansson,et al.  Ingrowth of sympathetic innervation occurs concomitantly with a decrease of ANP in the growing rat cardiac ventricles , 2001, Anatomy and Embryology.

[180]  M. Nash,et al.  Ventricular activation during sympathetic imbalance and its computational reconstruction , 2000 .

[181]  H. Berthoud,et al.  Functional and chemical anatomy of the afferent vagal system , 2000, Autonomic Neuroscience.

[182]  S. Sasayama,et al.  Augmented expression of cardiotrophin-1 and its receptor component, gp130, in both left and right ventricles after myocardial infarction in the rat. , 2000, Journal of molecular and cellular cardiology.

[183]  D. Paterson,et al.  Pre-synaptic NO-cGMP pathway modulates vagal control of heart rate in isolated adult guinea pig atria. , 2000, Journal of molecular and cellular cardiology.

[184]  E. Lakatta,et al.  Cardiac synthesis, processing, and coronary release of enkephalin-related peptides. , 2000, American journal of physiology. Heart and circulatory physiology.

[185]  M. Saarma,et al.  GDNF family receptors in the embryonic and postnatal rat heart and reduced cholinergic innervation in mice hearts lacking Ret or GFRα2 , 2000, Developmental dynamics : an official publication of the American Association of Anatomists.

[186]  D. Pauza,et al.  Morphology, distribution, and variability of the epicardiac neural ganglionated subplexuses in the human heart , 2000, The Anatomical record.

[187]  D. Hopkins,et al.  Pathology of intrinsic cardiac neurons from ischemic human hearts , 2000, The Anatomical record.

[188]  M. Vizzard,et al.  Origin of pituitary adenylate cyclase‐activating polypeptide (PACAP)‐immunoreactive fibers innervating guinea pig parasympathetic cardiac ganglia , 2000, The Journal of comparative neurology.

[189]  D. Burkhoff,et al.  PKA Phosphorylation Dissociates FKBP12.6 from the Calcium Release Channel (Ryanodine Receptor) Defective Regulation in Failing Hearts , 2000, Cell.

[190]  T A Denton,et al.  Relationship between regional cardiac hyperinnervation and ventricular arrhythmia. , 2000, Circulation.

[191]  M. Esler,et al.  Reduced myocardial nerve growth factor expression in human and experimental heart failure. , 2000, Circulation research.

[192]  M. Fishbein,et al.  Nerve sprouting and sudden cardiac death. , 2000, Circulation research.

[193]  R. Lefkowitz,et al.  Catecholamines, Cardiac b-Adrenergic Receptors, and Heart Failure , 2000 .

[194]  J. Mead,et al.  Nerve growth factor collaborates with myocyte-derived factors to promote development of presynaptic sites in cultured sympathetic neurons. , 2000, Journal of neurobiology.

[195]  D M Bers,et al.  Reverse mode of the sarcoplasmic reticulum calcium pump and load-dependent cytosolic calcium decline in voltage-clamped cardiac ventricular myocytes. , 2000, Biophysical journal.

[196]  L. Biblo,et al.  Characterization of Sinoatrial Parasympathetic Innervation in Humans , 1999, Journal of cardiovascular electrophysiology.

[197]  M. Stevens,et al.  Heterogeneous cardiac sympathetic denervation and decreased myocardial nerve growth factor in streptozotocin-induced diabetic rats: implications for cardiac sympathetic dysinnervation complicating diabetes. , 1999, Diabetes.

[198]  K. Kamiya,et al.  β-Adrenergic modulation of L-type Ca2+-channel currents in early-stage embryonic mouse heart. , 1999, American journal of physiology. Heart and circulatory physiology.

[199]  R. Croll,et al.  Regional distribution and extrinsic innervation of intrinsic cardiac neurons in the guinea pig. , 1999, The Journal of comparative neurology.

[200]  C. Liang,et al.  Overexpression of nerve growth factor in the heart alters ion channel activity and β‐adrenergic signalling in an adult transgenic mouse , 1998, The Journal of physiology.

[201]  R. Lefkowitz,et al.  Reciprocal in vivo regulation of myocardial G protein-coupled receptor kinase expression by beta-adrenergic receptor stimulation and blockade. , 1998, Circulation.

[202]  T. Soderling,et al.  Characterization of a calmodulin kinase II inhibitor protein in brain. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[203]  A. Hsu,et al.  Ischemic Preconditioning in the Intact Rat Heart Is Mediated by δ1- But Not μ- or κ-Opioid Receptors , 1998 .

[204]  G G Turrigiano,et al.  Nerve Growth Factor Modulates Synaptic Transmission between Sympathetic Neurons and Cardiac Myocytes , 1997, The Journal of Neuroscience.

[205]  G. Jennings,et al.  Adrenergic nervous system in heart failure. , 1997, The American journal of cardiology.

[206]  A. Gerdes,et al.  Rapid transition of cardiac myocytes from hyperplasia to hypertrophy during postnatal development. , 1996, Journal of molecular and cellular cardiology.

[207]  G. Steinbeck,et al.  Regional differences in current density and rate-dependent properties of the transient outward current in subepicardial and subendocardial myocytes of human left ventricle. , 1996, Circulation.

[208]  R. A. Hunt,et al.  Sympathetic innervation modulates the expression of angiotensin II receptors in embryonic rat heart grafted in oculo. , 1995, Journal of molecular and cellular cardiology.

[209]  U. Förstermann,et al.  Endogenous and exogenous nitric oxide inhibits norepinephrine release from rat heart sympathetic nerves. , 1995, Circulation research.

[210]  E. Botvinick,et al.  Acute and chronic effects of transient myocardial ischemia on sympathetic nerve activity, density, and norepinephrine content. , 1995, Cardiovascular research.

[211]  G. Ellis‐Davies,et al.  Rapid adaptation of cardiac ryanodine receptors: modulation by Mg2+ and phosphorylation. , 1995, Science.

[212]  R. Applegate,et al.  The effect of vagal stimulation on left ventricular systolic and diastolic performance. , 1994, The American journal of physiology.

[213]  J. Choate,et al.  Innervation of the pacemaker in guinea-pig sinoatrial node. , 1994, Journal of the autonomic nervous system.

[214]  J. Lundberg,et al.  Prognostic value of plasma neuropeptide-Y in coronary care unit patients with and without acute myocardial infarction. , 1994, European heart journal.

[215]  W. Edwards,et al.  Natriuretic peptide system in human heart failure. , 1993, Circulation.

[216]  P. Schwartz,et al.  Pharmacologic modulation of the autonomic nervous system in the prevention of sudden cardiac death. A study with propranolol, methacholine and oxotremorine in conscious dogs with a healed myocardial infarction. , 1993, Journal of the American College of Cardiology.

[217]  M. Komajda,et al.  Plasma calcitonin gene-related peptide decreases in chronic congestive heart failure. , 1992, European heart journal.

[218]  P. Schwartz,et al.  Prevention of life-threatening arrhythmias by pharmacologic stimulation of the muscarinic receptors with oxotremorine. , 1992, American heart journal.

[219]  H. Schulman,et al.  Calmodulin Trapping by Calcium-Calmodulin-Dependent Protein Kinase , 1992, Science.

[220]  G. Gintant,et al.  Heterogeneity within the ventricular wall. Electrophysiology and pharmacology of epicardial, endocardial, and M cells. , 1991, Circulation research.

[221]  S. S. Hull,et al.  Vagal stimulation and prevention of sudden death in conscious dogs with a healed myocardial infarction. , 1991, Circulation research.

[222]  P. Schmid,et al.  Innervation patterns of the middle cervical - stellate ganglion complex in the rat , 1990, Neuroscience Letters.

[223]  R. Hellweg,et al.  Endogenous levels of nerve growth factor (NGF) are altered in experimental diabetes mellitus: A possible role for NGF in the pathogenesis of diabetic neuropathy , 1990, Journal of neuroscience research.

[224]  N. Minamino,et al.  C-type natriuretic peptide (CNP): a new member of natriuretic peptide family identified in porcine brain. , 1990, Biochemical and biophysical research communications.

[225]  A. Sollevi,et al.  Plasma neuropeptide Y on admission to a coronary care unit: raised levels in patients with left heart failure. , 1990, Cardiovascular research.

[226]  R. Aebersold,et al.  The cholinergic neuronal differentiation factor from heart cells is identical to leukemia inhibitory factor. , 1989, Science.

[227]  M. Stanton,et al.  Regional sympathetic denervation after myocardial infarction in humans detected noninvasively using I-123-metaiodobenzylguanidine. , 1989, Journal of the American College of Cardiology.

[228]  Y. Yazaki,et al.  Expression of Cellular Oncogenes in the Myocardium During the Developmental Stage and Pressure‐Overloaded Hypertrophy of the Rat Heart , 1988, Circulation research.

[229]  J. S. Gutkind,et al.  Angiotensin II binding sites in the conduction system of rat hearts. , 1987, The American journal of physiology.

[230]  T. Soderling,et al.  Reversible generation of a Ca2+-independent form of Ca2+(calmodulin)-dependent protein kinase II by an autophosphorylation mechanism. , 1986, The Journal of biological chemistry.

[231]  B. Evans,et al.  Innervation of bat heart: cholinergic and adrenergic nerves innervate all chambers. , 1985, The American journal of physiology.

[232]  S. Vatner,et al.  Mechanisms of Supersensitivity to Sympathomimetic Amines in the Chronically Denervated Heart of the Conscious Dog , 1985, Circulation research.

[233]  H. Schulman,et al.  Mechanism of autophosphorylation of the multifunctional Ca2+/calmodulin-dependent protein kinase. , 1985, The Journal of biological chemistry.

[234]  S. Landis,et al.  Evidence for neurotransmitter plasticity in vivo: developmental changes in properties of cholinergic sympathetic neurons. , 1983, Developmental biology.

[235]  D. Zipes,et al.  Transmural Myocardial Infarction in the Dog Produces Sympathectomy in Noninfarcted Myocardium , 1983, Circulation.

[236]  P. Patterson,et al.  Role of nerve growth factor in the development of rat sympathetic neurons in vitro. I. Survival, growth, and differentiation of catecholamine production , 1977, The Journal of cell biology.

[237]  J. Kampine,et al.  Ventral root mapping of cardiac nerves in the canine using evoked potentials. , 1977, The American journal of physiology.

[238]  J. Han,et al.  Effects of vagal stimulation, atropine, and propranolol on fibrillation threshold of normal and ischemic ventricles. , 1977, American heart journal.

[239]  K. Spyer,et al.  The location of cardiac vagal preganglionic motoneurones in the medulla of the cat. , 1976, The Journal of physiology.

[240]  R. Liden Reflexes from the heart. , 1975, Progress in cardiovascular diseases.

[241]  R. Foreman,et al.  Responses of the canine heart to stimulation of the first five ventral thoracic roots. , 1974, The American journal of physiology.

[242]  P. Corr,et al.  Role of the Vagus Nerves in the Cardiovascular Changes Induced by Coronary Occlusion , 1974, Circulation.

[243]  R. Zak Cell proliferation during cardiac growth. , 1973, The American journal of cardiology.

[244]  W. C. Randall,et al.  Localized Myocardial Responses to Stimulation of Cardiac Sympathetic Nerves , 1967, Circulation research.

[245]  M. N. Levy,et al.  Depression of Ventricular Contractility by Stimulation of the Vagus Nerves , 1965, Circulation research.