Skip to main content
Top
Published in: Heart Failure Reviews 5/2014

01-09-2014

Novel approaches to the post-myocardial infarction/heart failure neural remodeling

Authors: Emilia D’Elia, Alessia Pascale, Nicoletta Marchesi, Paolo Ferrero, Michele Senni, Stefano Govoni, Edoardo Gronda, Emilio Vanoli

Published in: Heart Failure Reviews | Issue 5/2014

Login to get access

Abstract

The review aims to discuss the role of nerve growth factor (NGF) as a potential novel biomarker in post-myocardial infarction (MI) and in heart failure (HF), with a specific focus on neural remodeling and sprouting processes occurring after tissue damage. Many experimental data show that MI induces nerve sprouting, leading to increased sympathetic outflow and higher risk of ventricular arrhythmias and sudden cardiac death. In this framework, cardiac and circulating NGF might be an indicator of the innervation process and neural remodeling: it dramatically increases after MI, while it declines along with advanced HF and ventricular dysfunction. The bimodal behavior of NGF in acute and chronic settings leads to the speculation that NGF modulation may be a pharmacological target for intervention in different stages of the ischemic heart disease. Specifically, a fascinating possibility is to support or to inhibit NGF receptors, in order to prevent negative cardiac remodeling after MI and consequent ventricular dysfunction.
Literature
1.
go back to reference Harris AS (1950) Delayed development of ventricular ectopic rhythms following experimental coronary occlusion. Circulation 1:1318–1328PubMedCrossRef Harris AS (1950) Delayed development of ventricular ectopic rhythms following experimental coronary occlusion. Circulation 1:1318–1328PubMedCrossRef
2.
go back to reference Schwartz PJ, La Rovere MT, Vanoli E (1992) Autonomic nervous system and sudden cardiac death. Experimental basis and clinical observations for post-myocardial infarction risk stratification. Circulation 85(1 Suppl):I77–I91PubMed Schwartz PJ, La Rovere MT, Vanoli E (1992) Autonomic nervous system and sudden cardiac death. Experimental basis and clinical observations for post-myocardial infarction risk stratification. Circulation 85(1 Suppl):I77–I91PubMed
3.
go back to reference Waagstein F, Hjalmarson A, Varnauskas E, Wallentin I (1975) Effect of chronic beta-adrenergic receptor blockade in congestive cardiomyopathy. Br Heart J 37:1022–1036PubMedCentralPubMedCrossRef Waagstein F, Hjalmarson A, Varnauskas E, Wallentin I (1975) Effect of chronic beta-adrenergic receptor blockade in congestive cardiomyopathy. Br Heart J 37:1022–1036PubMedCentralPubMedCrossRef
4.
go back to reference Vanoli E, Dei Cas L, Willenheimer R (2006) Sudden death prevention in heart failure: the case of CIBIS III. Heart Int 2(2):73 Vanoli E, Dei Cas L, Willenheimer R (2006) Sudden death prevention in heart failure: the case of CIBIS III. Heart Int 2(2):73
5.
go back to reference Krum H, van Veldhuisen DJ, Funck-Brentano C et al (2011) Effect on mode of death of heart failure treatment started with bisoprolol followed by enalapril, compared to the opposite order: results of the Randomized CIBIS III Trial. Cardiovasc Ther 29:89–98PubMedCrossRef Krum H, van Veldhuisen DJ, Funck-Brentano C et al (2011) Effect on mode of death of heart failure treatment started with bisoprolol followed by enalapril, compared to the opposite order: results of the Randomized CIBIS III Trial. Cardiovasc Ther 29:89–98PubMedCrossRef
6.
go back to reference Maggioni AP, Anker SD, Dahlström U et al (2013) Are hospitalized or ambulatory patients with heart failure treated in accordance with European Society of Cardiology guidelines? Evidence from 12 440 patients of the ESC Heart Failure Long-Term Registry. Eur J Heart Fail 15:1173–1184PubMedCrossRef Maggioni AP, Anker SD, Dahlström U et al (2013) Are hospitalized or ambulatory patients with heart failure treated in accordance with European Society of Cardiology guidelines? Evidence from 12 440 patients of the ESC Heart Failure Long-Term Registry. Eur J Heart Fail 15:1173–1184PubMedCrossRef
7.
go back to reference Wiesmann C, de Vos AM (2001) Nerve growth factor: structure and function. Cell Mol Life Sci 58:748–759PubMedCrossRef Wiesmann C, de Vos AM (2001) Nerve growth factor: structure and function. Cell Mol Life Sci 58:748–759PubMedCrossRef
8.
go back to reference McDonald NQ, Lapatto R, Murray-Rust J et al (1991) New protein fold revealed by a 2.3—a resolution crystal structure of nerve growth factor. Nature 354:411–414PubMedCrossRef McDonald NQ, Lapatto R, Murray-Rust J et al (1991) New protein fold revealed by a 2.3—a resolution crystal structure of nerve growth factor. Nature 354:411–414PubMedCrossRef
9.
go back to reference Schwartz PJ, De Ferrari GM (2011) Sympathetic-parasympathetic interaction in health and disease: abnormalities and relevance in heart failure. Heart Fail Rev 16:101–107PubMedCrossRef Schwartz PJ, De Ferrari GM (2011) Sympathetic-parasympathetic interaction in health and disease: abnormalities and relevance in heart failure. Heart Fail Rev 16:101–107PubMedCrossRef
10.
go back to reference Berg T, Jensen J (2011) Simultaneous parasympathetic and sympathetic activation reveals altered autonomic control of heart rate, vascular tension, and epinephrine release in anesthetized hypertensive rats. Front Neurol 2:71PubMedCentralPubMedCrossRef Berg T, Jensen J (2011) Simultaneous parasympathetic and sympathetic activation reveals altered autonomic control of heart rate, vascular tension, and epinephrine release in anesthetized hypertensive rats. Front Neurol 2:71PubMedCentralPubMedCrossRef
11.
go back to reference Oh YS, Jong AY, Kim DT et al (2006) Spatial distribution of nerve sprouting after myocardial infarction in mice. Heart Rhythm 3:728–736PubMedCrossRef Oh YS, Jong AY, Kim DT et al (2006) Spatial distribution of nerve sprouting after myocardial infarction in mice. Heart Rhythm 3:728–736PubMedCrossRef
12.
go back to reference Cao JM, Fishbein MC, Han JB et al (2000) Relationship between regional and cardiac hyperinnervation and ventricular arrhythmia. Circulation 101:1960–1969PubMedCrossRef Cao JM, Fishbein MC, Han JB et al (2000) Relationship between regional and cardiac hyperinnervation and ventricular arrhythmia. Circulation 101:1960–1969PubMedCrossRef
13.
go back to reference Schwartz PJ, Vanoli E, Zaza A et al (1985) The effect of antiarrhythmic drugs on life-threatening arrhythmias induced by the interaction between acute myocardial ischemia and sympathetic hyperactivity. Am Heart J 109:937–948PubMedCrossRef Schwartz PJ, Vanoli E, Zaza A et al (1985) The effect of antiarrhythmic drugs on life-threatening arrhythmias induced by the interaction between acute myocardial ischemia and sympathetic hyperactivity. Am Heart J 109:937–948PubMedCrossRef
14.
go back to reference Heusch G, Deussen A, Thämer V (1985) Cardiac sympathetic nerve activity and progressive vasoconstriction distal to coronary stenoses: feed-back aggravation of myocardial ischemia. J Auton Nerv Syst 13(4):311–326PubMedCrossRef Heusch G, Deussen A, Thämer V (1985) Cardiac sympathetic nerve activity and progressive vasoconstriction distal to coronary stenoses: feed-back aggravation of myocardial ischemia. J Auton Nerv Syst 13(4):311–326PubMedCrossRef
15.
go back to reference Vanoli E, De Ferrari GM, Stramba-Badiale M, Hull SS Jr, Foreman RD, Schwartz PJ (1991) Vagal stimulation and prevention of sudden death in conscious dogs with a healed myocardial infarction. Circ Res 68(5):1471–1481PubMedCrossRef Vanoli E, De Ferrari GM, Stramba-Badiale M, Hull SS Jr, Foreman RD, Schwartz PJ (1991) Vagal stimulation and prevention of sudden death in conscious dogs with a healed myocardial infarction. Circ Res 68(5):1471–1481PubMedCrossRef
16.
go back to reference Zhou S, Chen LS, Miyauchi Y et al (2004) Mechanism of cardiac nerve sprouting after myocardial infarction in dogs. Circ Res 95:76–83PubMedCrossRef Zhou S, Chen LS, Miyauchi Y et al (2004) Mechanism of cardiac nerve sprouting after myocardial infarction in dogs. Circ Res 95:76–83PubMedCrossRef
17.
go back to reference Barber MJ, Mueller TM, Henry DP, Felten SY, Zipes DP (1983) Transmural myocardial infarction in the dog produces sympathectomy in noninfarcted myocardium. Circulation 67(4):787–796PubMedCrossRef Barber MJ, Mueller TM, Henry DP, Felten SY, Zipes DP (1983) Transmural myocardial infarction in the dog produces sympathectomy in noninfarcted myocardium. Circulation 67(4):787–796PubMedCrossRef
18.
go back to reference Chen PS, Chen LS, Cao JM et al (2001) Sympathetic nerve sprouting, electrical remodeling and the mechanisms of sudden cardiac death. Cardiovasc Res 50:409–416PubMedCrossRef Chen PS, Chen LS, Cao JM et al (2001) Sympathetic nerve sprouting, electrical remodeling and the mechanisms of sudden cardiac death. Cardiovasc Res 50:409–416PubMedCrossRef
19.
go back to reference Voroshilovsky O, Qu Z, Lee MH (2000) Mechanisms of ventricular fibrillation induction by 60 Hz alternating current in isolated swine right ventricle. Circulation 102:1569–1745PubMedCrossRef Voroshilovsky O, Qu Z, Lee MH (2000) Mechanisms of ventricular fibrillation induction by 60 Hz alternating current in isolated swine right ventricle. Circulation 102:1569–1745PubMedCrossRef
21.
go back to reference Chen LS, Zhou S, Fishbein MC et al (2007) New perspectives on the role of autonomic nervous system in the genesis of arrhythmias. J Cardiovasc Electrophysiol 18:123–127PubMedCrossRef Chen LS, Zhou S, Fishbein MC et al (2007) New perspectives on the role of autonomic nervous system in the genesis of arrhythmias. J Cardiovasc Electrophysiol 18:123–127PubMedCrossRef
22.
go back to reference Zhou S, Paz O, Cao JM et al (2005) Differential β-adrenoceptor expression induced by nerve growth factor infusion into the canine right and left stellate ganglia. Heart Rhythm 2:1347–1355PubMedCrossRef Zhou S, Paz O, Cao JM et al (2005) Differential β-adrenoceptor expression induced by nerve growth factor infusion into the canine right and left stellate ganglia. Heart Rhythm 2:1347–1355PubMedCrossRef
23.
go back to reference Bosch RF, Schneck AC, Kiehn J et al (2002) β3-Adrenergic regulation of an ion channel in the heart-inhibition of the slow delayed rectifier potassium current I(Ks) in guinea pig ventricular myocytes. Cardiovasc Res 56:393–403PubMedCrossRef Bosch RF, Schneck AC, Kiehn J et al (2002) β3-Adrenergic regulation of an ion channel in the heart-inhibition of the slow delayed rectifier potassium current I(Ks) in guinea pig ventricular myocytes. Cardiovasc Res 56:393–403PubMedCrossRef
24.
go back to reference Cheng HJ, Zhang ZS, Onishi K et al (2001) Upregulation of functional β (3)-adrenergic receptor in the failing canine myocardium. Circ Res 89:599–606PubMedCrossRef Cheng HJ, Zhang ZS, Onishi K et al (2001) Upregulation of functional β (3)-adrenergic receptor in the failing canine myocardium. Circ Res 89:599–606PubMedCrossRef
25.
go back to reference Han S, Kobayashi K, Joung B et al (2012) Electroanatomic remodeling of the left stellate ganglion after myocardial infarction. JACC 10:954–961CrossRef Han S, Kobayashi K, Joung B et al (2012) Electroanatomic remodeling of the left stellate ganglion after myocardial infarction. JACC 10:954–961CrossRef
27.
go back to reference Zhang H, Yuan X, Jin PF, Hou JF, Wang W, Wei YJ, Hu S (2010) Alteration of parasympathetic/sympathetic ratio in the infarcted myocardium after Schwann cell transplantation modified electrophysiological function of heart: a novel antiarrhythmic therapy. Circulation 122(11 Suppl):S193–S200PubMedCrossRef Zhang H, Yuan X, Jin PF, Hou JF, Wang W, Wei YJ, Hu S (2010) Alteration of parasympathetic/sympathetic ratio in the infarcted myocardium after Schwann cell transplantation modified electrophysiological function of heart: a novel antiarrhythmic therapy. Circulation 122(11 Suppl):S193–S200PubMedCrossRef
28.
go back to reference Nicol GD, Vasko MR (2007) Unraveling the story of NGF-mediated sensitization of nociceptive sensory neurons: ON or OFF the Trks? Mol Interv 7:26–41PubMedCrossRef Nicol GD, Vasko MR (2007) Unraveling the story of NGF-mediated sensitization of nociceptive sensory neurons: ON or OFF the Trks? Mol Interv 7:26–41PubMedCrossRef
29.
go back to reference Adams DO, Hamilton TA (1984) The cell biology of macrophage activation. Annu Rev Immunol 2:283–318PubMedCrossRef Adams DO, Hamilton TA (1984) The cell biology of macrophage activation. Annu Rev Immunol 2:283–318PubMedCrossRef
30.
go back to reference Caroleo MC, Costa N, Bracci-Laudiero L, Aloe L (2001) Human monocyte/macrophages activate by exposure to LPS overexpress NGF and NGF receptors. J Neuroimmunol 113:193–201PubMedCrossRef Caroleo MC, Costa N, Bracci-Laudiero L, Aloe L (2001) Human monocyte/macrophages activate by exposure to LPS overexpress NGF and NGF receptors. J Neuroimmunol 113:193–201PubMedCrossRef
31.
go back to reference Wernli G, Hasan W, Bhattacherjee A, van Rooijen N, Smith PG (2009) Macrophage depletion suppresses sympathetic hyperinnervation following myocardial infarction. Basic Res Cardiol 104:681–693PubMedCentralPubMedCrossRef Wernli G, Hasan W, Bhattacherjee A, van Rooijen N, Smith PG (2009) Macrophage depletion suppresses sympathetic hyperinnervation following myocardial infarction. Basic Res Cardiol 104:681–693PubMedCentralPubMedCrossRef
32.
go back to reference Bonvini R, Hendiri T, Camenzid E (2005) Inflammatory response post-myocardial infarction and reperfusion: a new therapeutic target? Eur Heart J Suppl 7:I27–I36CrossRef Bonvini R, Hendiri T, Camenzid E (2005) Inflammatory response post-myocardial infarction and reperfusion: a new therapeutic target? Eur Heart J Suppl 7:I27–I36CrossRef
33.
go back to reference Kou HS, Tsai MJ, Huang MC (2011) Acid fibroblast growth factor and peripheral nerve grafts regulate Th2 cytokine expression, macrophage activation, polyamine synthesis, and neurotrophin expression in transected rat spinal cords. J Neurosci 31:4137–4147CrossRef Kou HS, Tsai MJ, Huang MC (2011) Acid fibroblast growth factor and peripheral nerve grafts regulate Th2 cytokine expression, macrophage activation, polyamine synthesis, and neurotrophin expression in transected rat spinal cords. J Neurosci 31:4137–4147CrossRef
34.
go back to reference Hasan W, Jama A, Donohue T (2006) Sympathetic hyperinnervation and inflammatory cell NGF synthesis following myocardial infarction in rats. Brain Res 1124:142–154PubMedCentralPubMedCrossRef Hasan W, Jama A, Donohue T (2006) Sympathetic hyperinnervation and inflammatory cell NGF synthesis following myocardial infarction in rats. Brain Res 1124:142–154PubMedCentralPubMedCrossRef
35.
go back to reference Gee AP, Boyle MD, Munger KL (1983) Nerve growth factor: stimulation of polymorphonuclear leukocyte chemotaxis in vitro. Proc Natl Acad Sci USA 80:7215–7218PubMedCentralPubMedCrossRef Gee AP, Boyle MD, Munger KL (1983) Nerve growth factor: stimulation of polymorphonuclear leukocyte chemotaxis in vitro. Proc Natl Acad Sci USA 80:7215–7218PubMedCentralPubMedCrossRef
36.
go back to reference Cantarella G, Lampereur L, Presta M et al (2002) Nerve growth factor-endothelial cell interaction leads to angiogenesis in vitro and in vivo. FASEB J 16:1307–1309PubMed Cantarella G, Lampereur L, Presta M et al (2002) Nerve growth factor-endothelial cell interaction leads to angiogenesis in vitro and in vivo. FASEB J 16:1307–1309PubMed
37.
go back to reference Caporali A, Sala GB, Meloni M et al (2008) Identification of the prosurvival activity of nerve growth factors on cardiac myocytes. Cell Death Differ 15:299–311PubMedCentralPubMedCrossRef Caporali A, Sala GB, Meloni M et al (2008) Identification of the prosurvival activity of nerve growth factors on cardiac myocytes. Cell Death Differ 15:299–311PubMedCentralPubMedCrossRef
38.
go back to reference Glebova NO, Ginty DD (2004) Heterogeneous requirement of NGF for sympathetic target innervation in vivo. J Neurosci 24:743–751PubMedCrossRef Glebova NO, Ginty DD (2004) Heterogeneous requirement of NGF for sympathetic target innervation in vivo. J Neurosci 24:743–751PubMedCrossRef
39.
go back to reference Ajijola OA, Shivkumar K (2012) Neural remodeling and myocardial infarction. JACC 10:962–964CrossRef Ajijola OA, Shivkumar K (2012) Neural remodeling and myocardial infarction. JACC 10:962–964CrossRef
40.
go back to reference Korsching S, Thoenen H (1983) Nerve growth factor in sympathetic ganglia and corresponding target organs of the rat: correlation with density of sympathetic innervation. Proc Natl Acad Sci USA 80:212–220CrossRef Korsching S, Thoenen H (1983) Nerve growth factor in sympathetic ganglia and corresponding target organs of the rat: correlation with density of sympathetic innervation. Proc Natl Acad Sci USA 80:212–220CrossRef
41.
go back to reference Yang SS, Han W, Cao Y et al (2011) Effects of high thoracic epidural anesthesia on atrial electrophysiological characteristics and sympathetic nerve sprouting in a canine model of atrial fibrillation. Basic Res Cardiol 106:495–605PubMedCrossRef Yang SS, Han W, Cao Y et al (2011) Effects of high thoracic epidural anesthesia on atrial electrophysiological characteristics and sympathetic nerve sprouting in a canine model of atrial fibrillation. Basic Res Cardiol 106:495–605PubMedCrossRef
42.
go back to reference Lindsay RM, Thoenen H, Barde YA (1985) Placode and neural crest-derived sensory neurons are responsive at early developmental stages to brain-derived neurotrophic factor. Dev Biol 112:319–328PubMedCrossRef Lindsay RM, Thoenen H, Barde YA (1985) Placode and neural crest-derived sensory neurons are responsive at early developmental stages to brain-derived neurotrophic factor. Dev Biol 112:319–328PubMedCrossRef
43.
go back to reference Emanuele E, Politi P, Bianchi M et al (2006) Raised plasma nerve growth factor levels associated with early-stage romantic love. Psychoneuroendocrinology 31:288–294PubMedCrossRef Emanuele E, Politi P, Bianchi M et al (2006) Raised plasma nerve growth factor levels associated with early-stage romantic love. Psychoneuroendocrinology 31:288–294PubMedCrossRef
44.
go back to reference Ieda M, Fukuda K (2009) New aspects for the treatment of cardiac diseases based on the diversity of functional controls on cardiac muscles: the regulatory mechanisms of cardiac innervation and their critical roles in cardiac performance. J Pharmacol Sci 109:348–353PubMedCrossRef Ieda M, Fukuda K (2009) New aspects for the treatment of cardiac diseases based on the diversity of functional controls on cardiac muscles: the regulatory mechanisms of cardiac innervation and their critical roles in cardiac performance. J Pharmacol Sci 109:348–353PubMedCrossRef
45.
go back to reference Manni L, Antonelli A, Costa N, Aloe L (2005) Stress alters vascular-endothelial growth factor expression in rat arteries: role of nerve growth factor. Basic Res Cardiol 100:121–130PubMedCrossRef Manni L, Antonelli A, Costa N, Aloe L (2005) Stress alters vascular-endothelial growth factor expression in rat arteries: role of nerve growth factor. Basic Res Cardiol 100:121–130PubMedCrossRef
46.
go back to reference Kaye DM, Vaddadi G, Gruskin SL et al (2000) Reduced myocardial nerve growth factor expression in human and experimental heart failure. Circ Res 86:80–84CrossRef Kaye DM, Vaddadi G, Gruskin SL et al (2000) Reduced myocardial nerve growth factor expression in human and experimental heart failure. Circ Res 86:80–84CrossRef
47.
go back to reference Chen GP, Caldwell JH (2009) Evaluating presynaptic and postsynaptic innervation in heart failure. Curr Cardiol Rep 11:141–147PubMedCrossRef Chen GP, Caldwell JH (2009) Evaluating presynaptic and postsynaptic innervation in heart failure. Curr Cardiol Rep 11:141–147PubMedCrossRef
48.
go back to reference Qin F, Vulapalli RS, Stevens SY et al (2002) Loss of cardiac sympathetic neurotransmitters in heart failure and NE infusion is associated with reduced NGF. Am J Physiol Heart Circ Physiol 282:363–371 Qin F, Vulapalli RS, Stevens SY et al (2002) Loss of cardiac sympathetic neurotransmitters in heart failure and NE infusion is associated with reduced NGF. Am J Physiol Heart Circ Physiol 282:363–371
49.
go back to reference Kimura K, Kanazawa H, Ieda M et al (2010) Norepinephrine-induced nerve growth factor depletion causes cardiac sympathetic denervation in severe heart failure. Auton Neurosci 156:27–35PubMedCrossRef Kimura K, Kanazawa H, Ieda M et al (2010) Norepinephrine-induced nerve growth factor depletion causes cardiac sympathetic denervation in severe heart failure. Auton Neurosci 156:27–35PubMedCrossRef
50.
go back to reference Haider N, Bailiga RR, Chandrashekhar Y et al (2010) Adrenergic excess, hNET1 down-regulation, and compromised mIBG uptake in heart failure poverty in the presence of plenty. JACC 3:71–75PubMedCrossRef Haider N, Bailiga RR, Chandrashekhar Y et al (2010) Adrenergic excess, hNET1 down-regulation, and compromised mIBG uptake in heart failure poverty in the presence of plenty. JACC 3:71–75PubMedCrossRef
51.
go back to reference Yoshida M, Fukumoto Y, Kuroda Y (1997) Sympathetic denervation of myocardium demonstrated by 123I-MIBG scintigraphy in pure progressive autonomic failure. Eur Neurol 38:291–296PubMedCrossRef Yoshida M, Fukumoto Y, Kuroda Y (1997) Sympathetic denervation of myocardium demonstrated by 123I-MIBG scintigraphy in pure progressive autonomic failure. Eur Neurol 38:291–296PubMedCrossRef
52.
go back to reference Jacobson HF, Senior R, Cerquiera MD et al (2010) Myocardial iodine-123 meta-iodobenzylguanidine imaging and cardiac events in heart failure. Results of the prospective ADMIRE-HF (AdreView Myocardial Imaging for Risk Evaluation in Heart Failure) study. J Am Coll Cardiol 55:2212–2221PubMedCrossRef Jacobson HF, Senior R, Cerquiera MD et al (2010) Myocardial iodine-123 meta-iodobenzylguanidine imaging and cardiac events in heart failure. Results of the prospective ADMIRE-HF (AdreView Myocardial Imaging for Risk Evaluation in Heart Failure) study. J Am Coll Cardiol 55:2212–2221PubMedCrossRef
53.
go back to reference Dal Toso R, De Bernardi MA, Brooker G et al (1998) Beta adrenergic and prostaglandin receptor activation increases nerve growth factor mRNA content in C6-2B rat astrocytoma cells. J Pharmacol Exp Ther 246:1190–1193 Dal Toso R, De Bernardi MA, Brooker G et al (1998) Beta adrenergic and prostaglandin receptor activation increases nerve growth factor mRNA content in C6-2B rat astrocytoma cells. J Pharmacol Exp Ther 246:1190–1193
54.
go back to reference Creedon D, Tuttle JB (1991) Nerve growth factor synthesis in vascular smooth muscle. Hypertension 18:730–741PubMedCrossRef Creedon D, Tuttle JB (1991) Nerve growth factor synthesis in vascular smooth muscle. Hypertension 18:730–741PubMedCrossRef
55.
go back to reference Nisoli E, Tonello C, Benarese M et al (1996) Expression of nerve growth factor in brown adipose tissue: implications for thermogenesis and obesity. Endocrinology 137:495–503PubMed Nisoli E, Tonello C, Benarese M et al (1996) Expression of nerve growth factor in brown adipose tissue: implications for thermogenesis and obesity. Endocrinology 137:495–503PubMed
56.
go back to reference Hellweg R, Bandtlow CE, Heumann R et al (1988) Nerve growth factor synthesis in cultured rat iris: modulation by endogenous transmitter substances. Exp Cell Res 179:18–30PubMedCrossRef Hellweg R, Bandtlow CE, Heumann R et al (1988) Nerve growth factor synthesis in cultured rat iris: modulation by endogenous transmitter substances. Exp Cell Res 179:18–30PubMedCrossRef
57.
go back to reference Gong YT, Li WM, Li Y et al (2009) Probucol attenuates atrial autonomic remodeling in a canine model of atrial fibrillation produced by prolonged atrial pacing. Chin Med J (Engl) 122:74–82 Gong YT, Li WM, Li Y et al (2009) Probucol attenuates atrial autonomic remodeling in a canine model of atrial fibrillation produced by prolonged atrial pacing. Chin Med J (Engl) 122:74–82
58.
59.
go back to reference Serrano T, Lorigados LC, Armenteros S (1996) Nerve growth factor levels in normal human sera. NeuroReport 8:179–181PubMedCrossRef Serrano T, Lorigados LC, Armenteros S (1996) Nerve growth factor levels in normal human sera. NeuroReport 8:179–181PubMedCrossRef
60.
go back to reference Shelton DL, Reichardt LF (1984) Expression of the beta-nerve growth factor gene correlates with the density of sympathetic innervation in effector organs. Proc Natl Acad Sci USA 81:7951–7955PubMedCentralPubMedCrossRef Shelton DL, Reichardt LF (1984) Expression of the beta-nerve growth factor gene correlates with the density of sympathetic innervation in effector organs. Proc Natl Acad Sci USA 81:7951–7955PubMedCentralPubMedCrossRef
62.
go back to reference Miera A, Lambiase A, Aloe L et al (2004) Nerve growth factor involvement in the visual system: implications in allergic and neurodegenerative diseases. Cytokine Growth Factor Rev 15:411–417CrossRef Miera A, Lambiase A, Aloe L et al (2004) Nerve growth factor involvement in the visual system: implications in allergic and neurodegenerative diseases. Cytokine Growth Factor Rev 15:411–417CrossRef
63.
go back to reference Hiltunen JO, Arumäe U, Moshnyakov M et al (1996) Expression of mRNAs for neurotrophins and their receptors in developing rat heart. Circ Res 79:930–939PubMedCrossRef Hiltunen JO, Arumäe U, Moshnyakov M et al (1996) Expression of mRNAs for neurotrophins and their receptors in developing rat heart. Circ Res 79:930–939PubMedCrossRef
64.
go back to reference Lambiase A, Micera A, Sgrulletta R et al (2004) Nerve growth factor and the immune system: old and new concepts in the cross-talk between immune and resident cells during pathophysiological conditions. Curr Opin Allergy Clin Immunol 4:425–430PubMedCrossRef Lambiase A, Micera A, Sgrulletta R et al (2004) Nerve growth factor and the immune system: old and new concepts in the cross-talk between immune and resident cells during pathophysiological conditions. Curr Opin Allergy Clin Immunol 4:425–430PubMedCrossRef
65.
go back to reference Govoni S, Pascale A, Amadio ML et al (2011) NGF and heart: is there a role in heart disease? Pharmacol Res 4:266–277CrossRef Govoni S, Pascale A, Amadio ML et al (2011) NGF and heart: is there a role in heart disease? Pharmacol Res 4:266–277CrossRef
Metadata
Title
Novel approaches to the post-myocardial infarction/heart failure neural remodeling
Authors
Emilia D’Elia
Alessia Pascale
Nicoletta Marchesi
Paolo Ferrero
Michele Senni
Stefano Govoni
Edoardo Gronda
Emilio Vanoli
Publication date
01-09-2014
Publisher
Springer US
Published in
Heart Failure Reviews / Issue 5/2014
Print ISSN: 1382-4147
Electronic ISSN: 1573-7322
DOI
https://doi.org/10.1007/s10741-013-9415-6

Other articles of this Issue 5/2014

Heart Failure Reviews 5/2014 Go to the issue