Issue
Nerve growth factor as an important possible component of novel therapy for cancer, diabetes and cardiovascular diseases
Corresponding Author(s) : Ewelina Barcińska
Cellular and Molecular Biology,
Vol. 64 No. 9: Issue 9
Abstract
Nerve growth factor (NGF) is protein discovered by Rita Levi Montalcini in the 1950s. It plays a crucial role in the development of nervous system. NGF may be produced by a variety of cells even beyond nervous system. NGF modulate cell metabolism by binding to p75NTR and TrkA receptors. NGF is involved in psychological processes and may be the possible therapeutical agent for diabetes, cancer and cardiovascular diseases, which will be described in the article.
Keywords
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- Levi"Montalcini R, Hamburger V. Selective growth stimulating effects of mouse sarcoma on the sensory and sympathetic nervous system of the chick embryo. J Exp Zool 1951;116:321–361.
- Aloe L, Tirassa P, Lambiase A. The topical application of nerve growth factor as a pharmacological tool for human corneal and skin ulcers. Pharmacol Res 2008;57:253–258.
- Wang W, Chen J, Guo X. The role of nerve growth factor and its receptors in tumorigenesis and cancer pain. Biosci Trends 2014;8:68–74.
- Lee R, Kermani P, Teng KK, Hempstead BL. Regulation of cell survival by secreted proneurotrophins. Science 2001;294:1945–1948.
- Allen SJ, Watson JJ, Shoemark DK, Barua NU, Patel NK. GDNF, NGF and BDNF as therapeutic options for neurodegeneration. Pharmacol Ther 2013;138:155–175.
- Mufson EJ, Kroin JS, Sendera TJ, Sobreviela T. Distribution and retrograde transport of trophic factors in the central nervous system: Functional implications for the treatment of neurodegenerative diseases. Prog Neurobiol 1999;57:451–484.
- Aloe L, Rocco ML. NGF and therapeutic prospective: what have we learned from the NGF transgenic models? Ann Ist Super Sanití 2015;51:5–10.
- Missale C, Boroni F, Sigala S, Buriani A, Fabris M, Leon A et al. Nerve growth factor in the anterior pituitary: localization in mammotroph cells and cosecretion with prolactin by a dopamine-regulated mechanism. Proc Natl Acad Sci U S A 1996;93:4240–4245.
- Nam JW, Chung JW, Kho HS, Chung SC, Kim YK. Nerve growth factor concentration in human saliva. Oral Dis 2007;13:187–192.
- Galve-Roperh I, Haro A, Díaz-Laviada I. Induction of nerve growth factor synthesis by sphingomyelinase and ceramide in primary astrocyte cultures. Mol Brain Res 1997;52:90–97.
- Leon Α, Buriani A, Dal Toso R, Fabris M, Romanello S, Aloe L et al. Mast cells synthesize, store, and release nerve growth factor. Proc Natl Acad Sci U S A 1994;91:3739–3743.
- Lambiase A, Bracci-Laudiero L, Bonini S, Bonini S, Starace G, D'Elios MM et al. Human CD4+ T cell clones produce and release nerve growth factor and express high-affinity nerve growth factor receptors. J Allergy Clin Immunol 1997;100:408–414.
- Taniuchi M, Clark HB, Schweitzer JB, Johnson EM. Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: ultrastructural location, suppression by axonal contact, and binding properties. J Neurosci 1988;8:664–681.
- Heumann R, Lindholm D, Bandtlow C, Meyer M, Radeke MJ, Misko TP et al. Differential regulation of mRNA encoding nerve growth factor and its receptor in rat sciatic nerve during development, degeneration, and regeneration: role of macrophages. Proc Natl Acad Sci U S A 1987;84:8735–8739.
- Kawamoto K, Aoki J, Tanaka A, Itakura A, Hosono H, Arai H et al. Nerve growth factor activates mast cells through the collaborative interaction with lysophosphatidylserine expressed on the membrane surface of activated platelets. J Immunol 2002;168:6412–6419.
- Freund V, Pons F, Joly V, Mathieu E, Martinet N, Frossard N. Upregulation of nerve growth factor expression by human airway smooth muscle cells in inflammatory conditions. Eur Respir J 2002;20:458–463.
- Lukoyanov N V., Pereira PA, Paula-Barbosa MM, Cadete-Leite A. Nerve growth factor improves spatial learning and restores hippocampal cholinergic fibers in rats withdrawn from chronic treatment with ethanol. Exp Brain Res 2003;148:88–94.
- Sathishkumar M, Pavagadhi S, Mahadevan A, Balasubramanian R. Biosynthesis of gold nanoparticles and related cytotoxicity evaluation using A549 cells. Ecotoxicol Environ Saf 2015;114:232–240.
- Tuszynski MH, Yang JH, Barba D, U H-S, Bakay R a. E, Pay MM et al. Nerve Growth Factor Gene Therapy. JAMA Neurol 2015;626:1–9.
- Parikh V, Evans DR, Khan MM, Mahadik SP. Nerve growth factor in never-medicated first-episode psychotic and medicated chronic schizophrenic patients: Possible implications for treatment outcome. Schizophr Res 2003;60:117–123.
- Stanzel RDP, Lourenssen S, Blennerhassett MG. Inflammation causes expression of NGF in epithelial cells of the rat colon. Exp Neurol 2008;211:203–213.
- Emanuele E, Politi P, Bianchi M, Minoretti P, Bertona M, Geroldi D. Raised plasma nerve growth factor levels associated with early-stage romantic love. Psychoneuroendocrinology 2006;31:288–294.
- Alleva E, Branchi I. NGF: A social molecule. Psychoneuroendocrinology 2006;31:295–296.
- Govoni S, Pascale A, Amadio M, Calvillo L, D'Elia E, Cereda C et al. NGF and heart: Is there a role in heart disease? Pharmacol Res 2011;63:266–277.
- Nakagawara A. Trk receptor tyrosine kinases: A bridge between cancer and neural development. Cancer Lett 2001;169:107–114.
- Caporali A, Emanueli E. Cardiovascular Actions of Neurotrophins. Physiol Rev 2011;89:279–308.
- Garcia TB, Hollborn M, Bringmann A. Expression and signaling of NGF in the healthy and injured retina. Cytokine Growth Factor Rev 2017;34:43–57.
- Marlin MC, Li G. Biogenesis and Function of the NGF/TrkA Signaling Endosome. Elsevier Ltd 2015 doi:10.1016/bs.ircmb.2014.10.002
- Bradshaw RA, Pundavela J, Biarc J, Chalkley RJ, Burlingame AL, Hondermarck H. NGF and ProNGF: Regulation of neuronal and neoplastic responses through receptor signaling. Adv Biol Regul 2015;58:16–27.
- Lee NH, Malek RL. Nerve growth factor regulation of m4 muscarinic receptor mRNA stability but not gene transcription requires mitogen-activated protein kinase activity. J Biol Chem 1998;273:22317–22325.
- Nico B, Mangieri D, Benagiano V, Crivellato E, Ribatti D. Nerve growth factor as an angiogenic factor. Microvasc Res 2008;75:135–141.
- Chamary VL, Robson T, Loizidou M, Boulos PB, Burnstock G. Progressive loss of perivascular nerves adjacent to colorectal cancer. Eur J Surg Oncol 2000;26:588–593.
- Goda M, Atagi S, Amitani K, Hobara N, Kitamura Y, Kawasaki H. Nerve growth factor suppresses prostate tumor growth. J Pharmacol Sci 2010;112:463–466.
- Campos X, Muñoz Y, Selman A, Yazigi R, Moyano L, Weinstein-Oppenheimer C et al. Nerve growth factor and its high-affinity receptor trkA participate in the control of vascular endothelial growth factor expression in epithelial ovarian cancer. Gynecol Oncol 2007;104:168–175.
- Davidson B, Reich R, Lazarovici P, Nesland JM, Skrede M, Risberg B et al. Expression and activation of the nerve growth factor receptor TrkA in serous ovarian carcinoma. Clin Cancer Res 2003;9:2248–2259.
- Lu Q-L, Liu J, Zhu X-L, Xu W-J. Expression of nerve growth factor and hypoxia inducible factor-1α and its correlation with angiogenesis in non-small cell lung cancer. J Huazhong Univ Sci Technolog Med Sci 2014;34:359–362.
- Romon R, Adriaenssens E, Lagadec C, Germain E, Hondermarck H, Le Bourhis X. Nerve growth factor promotes breast cancer angiogenesis by activating multiple pathways. Mol Cancer 2010;9:157.
- Siegel RL, Miller KD, Jemal A. Cancer statistics. CA Cancer J Clin 2016;66:7–30.
- Shibayama E, Koizumi H. Cellular localization of the Trk neurotrophin receptor family in human non-neuronal tissues. Am J Pathol 1996;148:1807–1818.
- World Health Organization. Global Report on Diabetes. 2016 doi:ISBN 978 92 4 156525 7
- Diabetes Federation. Annual Report 2015 - International Diabetes Federation. 2015http://www.idf.org/sites/default/files/IDF_AnnualReport_2015_WEB.pdf
- Gezginci-Oktayoglu S, Bolkent S. Ras signaling in NGF reduction and TNF-?β-related pancreatic ?? cell apoptosis in hyperglycemic rats. Apoptosis 2012;17:14–24.
- Sposato V, Manni L, Chaldakov GN, Aloe L. Streptozotocin-induced diabetes is associated with changes in NGF levels in pancreas and brain. Arch Ital Biol 2007;145:87–97.
- Rosenbaum T, Vidaltamayo R, Sánchez-Soto MC, Zentella A, Hiriart M. Pancreatic beta cells synthesize and secrete nerve growth factor. Proc Natl Acad Sci U S A 1998;95:7784–7788.
- Pierucci D, Cicconi S, Bonini P, Ferrelli F, Pastore D, Matteucci C et al. NGF-withdrawal induces apoptosis in pancreatic beta cells in vitro. Diabetologia 2001;44:1281–1295.
- Navarro-Tableros V, Sánchez-Soto MC, García S, Hiriart M. Autocrine regulation of single pancreatic ?β-cell survival. Diabetes 2004;53:2018–2023.
- Lee PG, Hohman TC, Cai F, Regalia J, Helke CJ. Streptozotocin-induced diabetes causes metabolic changes and alterations in neurotrophin content and retrograde transport in the cervical vagus nerve. Exp Neurol 2001;170:149–161.
- Schwartz S, Adornato BT, Freeman R, Biton V, Rendell M, Vinik A et al. Efficacy and Safety of Recombinant Human. 2000;284:2215–2221.
- Goss JR, Goins WF, Lacomis D, Mata M, Glorioso JC, Fink DJ. Herpes Simplex – Mediated Gene Transfer of Nerve Growth Factor Protects Against Peripheral Neuropathy in Streptozotocin-Induced Diabetes in the Mouse. Diabetes 2002;51:2227–2232.
- Li Y, Shi B, Wang D, Wang P, Laudon V, Zhang J et al. Nerve growth factor and substance P: Expression in a rat model of diabetic bladder. Int Urol Nephrol 2011;43:109–116.
- Sasaki K, Chancellor MB, Phelan MW, Yokoyama T, Fraser MO, Seki S et al. Diabetic cystopathy correlates with a long-term decrease in nerve growth factor levels in the bladder and lumbosacral dorsal root Ganglia. J Urol 2002;168:1259–1264.
- Poduslo JF, Curran GL. Permeability at the blood-brain and blood-nerve barriers of the neurotrophic factors: NGF, CNTF, NT-3, BDNF. Mol Brain Res 1996;36:280–286.
- Manni L, Nikolova V, Vyagova D, Chaldakov GN, Aloe L. Reduced plasma levels of NGF and BDNF in patients with acute coronary syndromes. Int J Cardiol 2005;102:169–171.
- Kaye DM, Krum H. Drug discovery for heart failure: a new era or the end of the pipeline? Nat Rev Drug Discov 2007;6:127–139.
- Hasan W, Smith PG. Decreased adrenoceptor stimulation in heart failure rats reduces NGF expression by cardiac parasympathetic neurons. Auton Neurosci Basic Clin 2014;181:13–20.
- Wang Z, Li H, Huang Y, Li R, Wang X, Yu L et al. Nerve growth factor-induced Akt/mTOR activation protects the ischemic heart via restoring autophagic flux and attenuating ubiquitinated protein accumulation. Oncotarget 2017;8:5400–5413.
- Abe T, Morgan DA, Gutterman DD. Protective role of nerve growth factor against postischemic dysfunction of sympathetic coronary innervation. Circulation 1997;95:213–220.
- Hiltunen J, Arumäe U, Moshnyakov M, Saarma M. Expression of mRNAs for neurotrophins and their receptors in developing rat heart. Circ Res 1996;79:930–939.
- Caporali A, Sala-Newby GB, Meloni M, Graiani G, Pani E, Cristofaro B et al. Identification of the prosurvival activity of nerve growth factor on cardiac myocytes. Cell Death Differ 2008;15:299–311.
- Saygili E, Kluttig R, Rana OR, Saygili E, Gemein C, Zink MD et al. Age-related regional differences in cardiac nerve growth factor expression. Age (Dordr) 2012;34:659–667.
- Furukawa Y, Tomioka N, Sato W, Satoyoshi E, Hayashi K, Furukawa S. Catecholamines increase nerve growth factor mRNA content in both mouse astroglial cells and fibroblast cells. FEBS Lett 1989;247:463–467.
- Creedon D, Tuttle JB. Nerve growth factor synthesis in vascular smooth muscle. Hypertension 1991;18:730–741.
- Qin F, Vulapalli RS, Stevens SY, Liang C. Loss of cardiac sympathetic neurotransmitters in heart failure and NE infusion is associated with reduced NGF Loss of cardiac sympathetic neurotransmitters in heart failure and NE infusion is associated with reduced NGF. 2013;14642:363–371.
- Kimura K, Kanazawa H, Ieda M, Kawaguchi-Manabe H, Miyake Y, Yagi T et al. Norepinephrine-induced nerve growth factor depletion causes cardiac sympathetic denervation in severe heart failure. Auton Neurosci 2010;156:27–35.
- Kaye DM, Vaddadi G, Gruskin SL, Du X-JJ, Esler MD. Reduced myocardial nerve growth factor expression in human and experimental heart failure. Circ Res 2000;86:E80-4.
- Hasan W, Smith PG. Modulation of rat parasympathetic cardiac ganglion phenotype and NGF synthesis by adrenergic nerves. Auton Neurosci Basic Clin 2009;145:17–26.
- Bibevski S, Dunlap ME. Evidence for impaired vagus nerve activity in heart failure. Heart Fail Rev 2011;16:129–135.
- Kaye DM, Lefkovits J, Jennings GL, Bergin P, Broughton A, Esler MD. Adverse consequences of high sympathetic nervous activity in the failing human heart. J Am Coll Cardiol 1995;26:1257–1263.
- Lam NT, Currie PD, Lieschke GJ, Rosenthal NA, Kaye DM. Nerve Growth Factor Stimulates Cardiac Regeneration via Cardiomyocyte Proliferation in Experimental Heart Failure. PLoS One 2012;7. doi:10.1371/journal.pone.0053210
References
Levi"Montalcini R, Hamburger V. Selective growth stimulating effects of mouse sarcoma on the sensory and sympathetic nervous system of the chick embryo. J Exp Zool 1951;116:321–361.
Aloe L, Tirassa P, Lambiase A. The topical application of nerve growth factor as a pharmacological tool for human corneal and skin ulcers. Pharmacol Res 2008;57:253–258.
Wang W, Chen J, Guo X. The role of nerve growth factor and its receptors in tumorigenesis and cancer pain. Biosci Trends 2014;8:68–74.
Lee R, Kermani P, Teng KK, Hempstead BL. Regulation of cell survival by secreted proneurotrophins. Science 2001;294:1945–1948.
Allen SJ, Watson JJ, Shoemark DK, Barua NU, Patel NK. GDNF, NGF and BDNF as therapeutic options for neurodegeneration. Pharmacol Ther 2013;138:155–175.
Mufson EJ, Kroin JS, Sendera TJ, Sobreviela T. Distribution and retrograde transport of trophic factors in the central nervous system: Functional implications for the treatment of neurodegenerative diseases. Prog Neurobiol 1999;57:451–484.
Aloe L, Rocco ML. NGF and therapeutic prospective: what have we learned from the NGF transgenic models? Ann Ist Super Sanití 2015;51:5–10.
Missale C, Boroni F, Sigala S, Buriani A, Fabris M, Leon A et al. Nerve growth factor in the anterior pituitary: localization in mammotroph cells and cosecretion with prolactin by a dopamine-regulated mechanism. Proc Natl Acad Sci U S A 1996;93:4240–4245.
Nam JW, Chung JW, Kho HS, Chung SC, Kim YK. Nerve growth factor concentration in human saliva. Oral Dis 2007;13:187–192.
Galve-Roperh I, Haro A, Díaz-Laviada I. Induction of nerve growth factor synthesis by sphingomyelinase and ceramide in primary astrocyte cultures. Mol Brain Res 1997;52:90–97.
Leon Α, Buriani A, Dal Toso R, Fabris M, Romanello S, Aloe L et al. Mast cells synthesize, store, and release nerve growth factor. Proc Natl Acad Sci U S A 1994;91:3739–3743.
Lambiase A, Bracci-Laudiero L, Bonini S, Bonini S, Starace G, D'Elios MM et al. Human CD4+ T cell clones produce and release nerve growth factor and express high-affinity nerve growth factor receptors. J Allergy Clin Immunol 1997;100:408–414.
Taniuchi M, Clark HB, Schweitzer JB, Johnson EM. Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: ultrastructural location, suppression by axonal contact, and binding properties. J Neurosci 1988;8:664–681.
Heumann R, Lindholm D, Bandtlow C, Meyer M, Radeke MJ, Misko TP et al. Differential regulation of mRNA encoding nerve growth factor and its receptor in rat sciatic nerve during development, degeneration, and regeneration: role of macrophages. Proc Natl Acad Sci U S A 1987;84:8735–8739.
Kawamoto K, Aoki J, Tanaka A, Itakura A, Hosono H, Arai H et al. Nerve growth factor activates mast cells through the collaborative interaction with lysophosphatidylserine expressed on the membrane surface of activated platelets. J Immunol 2002;168:6412–6419.
Freund V, Pons F, Joly V, Mathieu E, Martinet N, Frossard N. Upregulation of nerve growth factor expression by human airway smooth muscle cells in inflammatory conditions. Eur Respir J 2002;20:458–463.
Lukoyanov N V., Pereira PA, Paula-Barbosa MM, Cadete-Leite A. Nerve growth factor improves spatial learning and restores hippocampal cholinergic fibers in rats withdrawn from chronic treatment with ethanol. Exp Brain Res 2003;148:88–94.
Sathishkumar M, Pavagadhi S, Mahadevan A, Balasubramanian R. Biosynthesis of gold nanoparticles and related cytotoxicity evaluation using A549 cells. Ecotoxicol Environ Saf 2015;114:232–240.
Tuszynski MH, Yang JH, Barba D, U H-S, Bakay R a. E, Pay MM et al. Nerve Growth Factor Gene Therapy. JAMA Neurol 2015;626:1–9.
Parikh V, Evans DR, Khan MM, Mahadik SP. Nerve growth factor in never-medicated first-episode psychotic and medicated chronic schizophrenic patients: Possible implications for treatment outcome. Schizophr Res 2003;60:117–123.
Stanzel RDP, Lourenssen S, Blennerhassett MG. Inflammation causes expression of NGF in epithelial cells of the rat colon. Exp Neurol 2008;211:203–213.
Emanuele E, Politi P, Bianchi M, Minoretti P, Bertona M, Geroldi D. Raised plasma nerve growth factor levels associated with early-stage romantic love. Psychoneuroendocrinology 2006;31:288–294.
Alleva E, Branchi I. NGF: A social molecule. Psychoneuroendocrinology 2006;31:295–296.
Govoni S, Pascale A, Amadio M, Calvillo L, D'Elia E, Cereda C et al. NGF and heart: Is there a role in heart disease? Pharmacol Res 2011;63:266–277.
Nakagawara A. Trk receptor tyrosine kinases: A bridge between cancer and neural development. Cancer Lett 2001;169:107–114.
Caporali A, Emanueli E. Cardiovascular Actions of Neurotrophins. Physiol Rev 2011;89:279–308.
Garcia TB, Hollborn M, Bringmann A. Expression and signaling of NGF in the healthy and injured retina. Cytokine Growth Factor Rev 2017;34:43–57.
Marlin MC, Li G. Biogenesis and Function of the NGF/TrkA Signaling Endosome. Elsevier Ltd 2015 doi:10.1016/bs.ircmb.2014.10.002
Bradshaw RA, Pundavela J, Biarc J, Chalkley RJ, Burlingame AL, Hondermarck H. NGF and ProNGF: Regulation of neuronal and neoplastic responses through receptor signaling. Adv Biol Regul 2015;58:16–27.
Lee NH, Malek RL. Nerve growth factor regulation of m4 muscarinic receptor mRNA stability but not gene transcription requires mitogen-activated protein kinase activity. J Biol Chem 1998;273:22317–22325.
Nico B, Mangieri D, Benagiano V, Crivellato E, Ribatti D. Nerve growth factor as an angiogenic factor. Microvasc Res 2008;75:135–141.
Chamary VL, Robson T, Loizidou M, Boulos PB, Burnstock G. Progressive loss of perivascular nerves adjacent to colorectal cancer. Eur J Surg Oncol 2000;26:588–593.
Goda M, Atagi S, Amitani K, Hobara N, Kitamura Y, Kawasaki H. Nerve growth factor suppresses prostate tumor growth. J Pharmacol Sci 2010;112:463–466.
Campos X, Muñoz Y, Selman A, Yazigi R, Moyano L, Weinstein-Oppenheimer C et al. Nerve growth factor and its high-affinity receptor trkA participate in the control of vascular endothelial growth factor expression in epithelial ovarian cancer. Gynecol Oncol 2007;104:168–175.
Davidson B, Reich R, Lazarovici P, Nesland JM, Skrede M, Risberg B et al. Expression and activation of the nerve growth factor receptor TrkA in serous ovarian carcinoma. Clin Cancer Res 2003;9:2248–2259.
Lu Q-L, Liu J, Zhu X-L, Xu W-J. Expression of nerve growth factor and hypoxia inducible factor-1α and its correlation with angiogenesis in non-small cell lung cancer. J Huazhong Univ Sci Technolog Med Sci 2014;34:359–362.
Romon R, Adriaenssens E, Lagadec C, Germain E, Hondermarck H, Le Bourhis X. Nerve growth factor promotes breast cancer angiogenesis by activating multiple pathways. Mol Cancer 2010;9:157.
Siegel RL, Miller KD, Jemal A. Cancer statistics. CA Cancer J Clin 2016;66:7–30.
Shibayama E, Koizumi H. Cellular localization of the Trk neurotrophin receptor family in human non-neuronal tissues. Am J Pathol 1996;148:1807–1818.
World Health Organization. Global Report on Diabetes. 2016 doi:ISBN 978 92 4 156525 7
Diabetes Federation. Annual Report 2015 - International Diabetes Federation. 2015http://www.idf.org/sites/default/files/IDF_AnnualReport_2015_WEB.pdf
Gezginci-Oktayoglu S, Bolkent S. Ras signaling in NGF reduction and TNF-?β-related pancreatic ?? cell apoptosis in hyperglycemic rats. Apoptosis 2012;17:14–24.
Sposato V, Manni L, Chaldakov GN, Aloe L. Streptozotocin-induced diabetes is associated with changes in NGF levels in pancreas and brain. Arch Ital Biol 2007;145:87–97.
Rosenbaum T, Vidaltamayo R, Sánchez-Soto MC, Zentella A, Hiriart M. Pancreatic beta cells synthesize and secrete nerve growth factor. Proc Natl Acad Sci U S A 1998;95:7784–7788.
Pierucci D, Cicconi S, Bonini P, Ferrelli F, Pastore D, Matteucci C et al. NGF-withdrawal induces apoptosis in pancreatic beta cells in vitro. Diabetologia 2001;44:1281–1295.
Navarro-Tableros V, Sánchez-Soto MC, García S, Hiriart M. Autocrine regulation of single pancreatic ?β-cell survival. Diabetes 2004;53:2018–2023.
Lee PG, Hohman TC, Cai F, Regalia J, Helke CJ. Streptozotocin-induced diabetes causes metabolic changes and alterations in neurotrophin content and retrograde transport in the cervical vagus nerve. Exp Neurol 2001;170:149–161.
Schwartz S, Adornato BT, Freeman R, Biton V, Rendell M, Vinik A et al. Efficacy and Safety of Recombinant Human. 2000;284:2215–2221.
Goss JR, Goins WF, Lacomis D, Mata M, Glorioso JC, Fink DJ. Herpes Simplex – Mediated Gene Transfer of Nerve Growth Factor Protects Against Peripheral Neuropathy in Streptozotocin-Induced Diabetes in the Mouse. Diabetes 2002;51:2227–2232.
Li Y, Shi B, Wang D, Wang P, Laudon V, Zhang J et al. Nerve growth factor and substance P: Expression in a rat model of diabetic bladder. Int Urol Nephrol 2011;43:109–116.
Sasaki K, Chancellor MB, Phelan MW, Yokoyama T, Fraser MO, Seki S et al. Diabetic cystopathy correlates with a long-term decrease in nerve growth factor levels in the bladder and lumbosacral dorsal root Ganglia. J Urol 2002;168:1259–1264.
Poduslo JF, Curran GL. Permeability at the blood-brain and blood-nerve barriers of the neurotrophic factors: NGF, CNTF, NT-3, BDNF. Mol Brain Res 1996;36:280–286.
Manni L, Nikolova V, Vyagova D, Chaldakov GN, Aloe L. Reduced plasma levels of NGF and BDNF in patients with acute coronary syndromes. Int J Cardiol 2005;102:169–171.
Kaye DM, Krum H. Drug discovery for heart failure: a new era or the end of the pipeline? Nat Rev Drug Discov 2007;6:127–139.
Hasan W, Smith PG. Decreased adrenoceptor stimulation in heart failure rats reduces NGF expression by cardiac parasympathetic neurons. Auton Neurosci Basic Clin 2014;181:13–20.
Wang Z, Li H, Huang Y, Li R, Wang X, Yu L et al. Nerve growth factor-induced Akt/mTOR activation protects the ischemic heart via restoring autophagic flux and attenuating ubiquitinated protein accumulation. Oncotarget 2017;8:5400–5413.
Abe T, Morgan DA, Gutterman DD. Protective role of nerve growth factor against postischemic dysfunction of sympathetic coronary innervation. Circulation 1997;95:213–220.
Hiltunen J, Arumäe U, Moshnyakov M, Saarma M. Expression of mRNAs for neurotrophins and their receptors in developing rat heart. Circ Res 1996;79:930–939.
Caporali A, Sala-Newby GB, Meloni M, Graiani G, Pani E, Cristofaro B et al. Identification of the prosurvival activity of nerve growth factor on cardiac myocytes. Cell Death Differ 2008;15:299–311.
Saygili E, Kluttig R, Rana OR, Saygili E, Gemein C, Zink MD et al. Age-related regional differences in cardiac nerve growth factor expression. Age (Dordr) 2012;34:659–667.
Furukawa Y, Tomioka N, Sato W, Satoyoshi E, Hayashi K, Furukawa S. Catecholamines increase nerve growth factor mRNA content in both mouse astroglial cells and fibroblast cells. FEBS Lett 1989;247:463–467.
Creedon D, Tuttle JB. Nerve growth factor synthesis in vascular smooth muscle. Hypertension 1991;18:730–741.
Qin F, Vulapalli RS, Stevens SY, Liang C. Loss of cardiac sympathetic neurotransmitters in heart failure and NE infusion is associated with reduced NGF Loss of cardiac sympathetic neurotransmitters in heart failure and NE infusion is associated with reduced NGF. 2013;14642:363–371.
Kimura K, Kanazawa H, Ieda M, Kawaguchi-Manabe H, Miyake Y, Yagi T et al. Norepinephrine-induced nerve growth factor depletion causes cardiac sympathetic denervation in severe heart failure. Auton Neurosci 2010;156:27–35.
Kaye DM, Vaddadi G, Gruskin SL, Du X-JJ, Esler MD. Reduced myocardial nerve growth factor expression in human and experimental heart failure. Circ Res 2000;86:E80-4.
Hasan W, Smith PG. Modulation of rat parasympathetic cardiac ganglion phenotype and NGF synthesis by adrenergic nerves. Auton Neurosci Basic Clin 2009;145:17–26.
Bibevski S, Dunlap ME. Evidence for impaired vagus nerve activity in heart failure. Heart Fail Rev 2011;16:129–135.
Kaye DM, Lefkovits J, Jennings GL, Bergin P, Broughton A, Esler MD. Adverse consequences of high sympathetic nervous activity in the failing human heart. J Am Coll Cardiol 1995;26:1257–1263.
Lam NT, Currie PD, Lieschke GJ, Rosenthal NA, Kaye DM. Nerve Growth Factor Stimulates Cardiac Regeneration via Cardiomyocyte Proliferation in Experimental Heart Failure. PLoS One 2012;7. doi:10.1371/journal.pone.0053210