Diabetic neuropathy and heart failure: role of neuropeptides

Asma Ejaz; Frank W. LoGerfo; Leena Pradhan

doi:10.1017/S1462399411001979

Diabetic neuropathy and heart failure: role of neuropeptides

Published online by Cambridge University Press: 10 August 2011

Asma Ejaz ,

Frank W. LoGerfo and

Leena Pradhan

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Asma Ejaz: Affiliation:
Department of Surgery, Division of Vascular and Endovascular Surgery, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, USA
Frank W. LoGerfo: Affiliation:
Department of Surgery, Division of Vascular and Endovascular Surgery, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, USA
Leena Pradhan*: Affiliation:
Department of Surgery, Division of Vascular and Endovascular Surgery, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, USA
*: *Corresponding author: Leena Pradhan, Beth Israel Deaconess Medical Center, 330 Brookline Avenue, Dana-805, Boston, MA, USA. E-mail: [email protected]

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Abstract

Cardiovascular autonomic neuropathy (CAN), in which patients present with damage of autonomic nerve fibres, is one of the most common complications of diabetes. CAN leads to abnormalities in heart rate and vascular dynamics, which are features of diabetic heart failure. Dysregulated neurohormonal activation, an outcome of diabetic neuropathy, has a significant pathophysiological role in diabetes-associated cardiovascular disease. Key players in neurohormonal activation include cardioprotective neuropeptides and their receptors, such as substance P (SP), neuropeptide Y (NPY), calcitonin-gene-related peptide (CGRP), atrial natriuretic peptide (ANP), brain natriuretic peptide (BNP) and C-type natriuretic peptide (CNP). These neuropeptides are released from the peripheral or autonomic nervous system and have vasoactive properties. They are further implicated in cardiomyocyte hypertrophy, calcium homeostasis, ischaemia-induced angiogenesis, protein kinase C signalling and the renin–angiotensin–aldosterone system. Therefore, dysregulation of the expression of neuropeptides or activation of the neuropeptide signalling pathways can negatively affect cardiac homeostasis. Targeting neuropeptides and their signalling pathways might thus serve as new therapeutic interventions in the treatment of heart failure associated with diabetes. This review discusses how neuropeptide dysregulation in diabetes might affect cardiac functions that contribute to the development of heart failure.

Type: Review Article
Information: Expert Reviews in Molecular Medicine , Volume 13 , March 2011 , e26

DOI: https://doi.org/10.1017/S1462399411001979 [Opens in a new window]
Copyright: Copyright © Cambridge University Press 2011

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References

1Resnick, H.E. et al. (2001) Prevalence and clinical implications of American Diabetes Association-defined diabetes and other categories of glucose dysregulation in older adults: the health, aging and body composition study. Journal of Clinical Epidemiology 54, 869-876CrossRef Google Scholar PubMed

2Cohen-Solal, A., Beauvais, F. and Logeart, D. (2008) Heart failure and diabetes mellitus: epidemiology and management of an alarming association. Journal of Cardiac Failure 14, 615-625Google Scholar

3Giles, T.D. and Sander, G.E. (2004) Diabetes mellitus and heart failure: basic mechanisms, clinical features, and therapeutic considerations. Cardiology Clinics 22, 553-568CrossRef Google Scholar PubMed

4Stratton, I.M. et al. (2000) Association of glycaemia with macrovascular and microvascular complications of type 2 diabetes (UKPDS 35): prospective observational study. BMJ 321, 405-412CrossRef Google Scholar PubMed

5Tesfaye, S. et al. (2010) Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care 33, 2285-2293CrossRef Google Scholar PubMed

6Rudy, A. (1945) Diabetic neuropathy. New England Journal of Medicine 233, 684-689Google Scholar

7Levy, D.M. et al. (1992) Immunohistochemical measurements of nerves and neuropeptides in diabetic skin: relationship to tests of neurological function. Diabetologia 35, 889-897Google Scholar

8Bolinder, J. et al. (2002) Autonomic neuropathy is associated with impaired pancreatic polypeptide and neuropeptide Y responses to insulin-induced hypoglycaemia in Type I diabetic patients. Diabetologia 45, 1043-1044Google Scholar

9Kunt, T. et al. (2000) Serum levels of substance P are decreased in patients with type 1 diabetes. Experimental and Clinical Endocrinology and Diabetes 108, 164-167CrossRef Google Scholar PubMed

10Ponery, E.A.a.A. (2003) Pancreatic peptides, neuropeptides and neurotransmitters in diabetes mellitus: a review. International Journal of Diabetes and Metabolism 11, 1-6Google Scholar

11McKenna, K. et al. (2000) Acute hyperglycaemia causes elevation in plasma atrial natriuretic peptide concentrations in Type 1 diabetes mellitus. Diabetic Medicine 17, 512-517CrossRef Google Scholar PubMed

12Ziegler, D. (1994) Diabetic cardiovascular autonomic neuropathy: prognosis, diagnosis and treatment. Diabetes/Metabolism Reviews 10, 339-383CrossRef Google Scholar PubMed

13Veves, A. et al. (1998) Endothelial dysfunction and the expression of endothelial nitric oxide synthetase in diabetic neuropathy, vascular disease, and foot ulceration. Diabetes 47, 457-463CrossRef Google Scholar PubMed

14Aronson, D. (2008) Hyperglycemia and the pathobiology of diabetic complications. Advances in Cardiology 45, 1-16CrossRef Google Scholar PubMed

15Monahan, T.S. et al. (2005) Preoperative cardiac evaluation does not improve or predict perioperative or late survival in asymptomatic diabetic patients undergoing elective infrainguinal arterial reconstruction. Journal of Vascular Surgery 41, 38-45; discussion 45Google Scholar

16Bauters, C. et al. (2003) Influence of diabetes mellitus on heart failure risk and outcome. Cardiovascular Diabetology 2, 1CrossRef Google Scholar PubMed

17Gheorghiade, M. and Bonow, R.O. (1998) Chronic heart failure in the United States: a manifestation of coronary artery disease. Circulation 97, 282-289CrossRef Google Scholar PubMed

18Orasanu, G. et al. (2008) The peroxisome proliferator-activated receptor-gamma agonist pioglitazone represses inflammation in a peroxisome proliferator-activated receptor-alpha-dependent manner in vitro and in vivo in mice. Journal of the American College of Cardiology 52, 869-881Google Scholar

19Morel, O. et al. (2010) Diabetes and the platelet: toward new therapeutic paradigms for diabetic atherothrombosis. Atherosclerosis 212, 367-376CrossRef Google Scholar PubMed

20Rask-Madsen, C. and King, G.L. (2007) Mechanisms of disease: endothelial dysfunction in insulin resistance and diabetes. Nature Clinical Practice. Endocrinology and Metabolism 3, 46-56CrossRef Google Scholar PubMed

21Hayat, S.A. et al. (2004) Diabetic cardiomyopathy: mechanisms, diagnosis and treatment. Clinical Science (London) 107, 539-557Google Scholar

22Falcao-Pires, I. and Leite-Moreira, A.F. (2011) Diabetic cardiomyopathy: understanding the molecular and cellular basis to progress in diagnosis and treatment. Heart Failure Reviews [epub]Google Scholar

23Pittenger, G. and Vinik, A. (2003) Nerve growth factor and diabetic neuropathy. Experimental Diabesity Research 4, 271-285Google Scholar

24Obrosova, I.G. (2009) Diabetic painful and insensate neuropathy: pathogenesis and potential treatments. Neurotherapeutics 6, 638-647CrossRef Google Scholar PubMed

25Valensi, P. et al. (1997) Diabetic peripheral neuropathy: effects of age, duration of diabetes, glycemic control, and vascular factors. Journal of Diabetes and its Complications 11, 27-34CrossRef Google Scholar PubMed

26Dinh, T. et al. (2009) Foot muscle energy reserves in diabetic patients without and with clinical peripheral neuropathy. Diabetes Care 32, 1521-1524Google Scholar

27NINDS, F.S. Peripheral Neuropathy. NIH http://www.ninds.nih.gov/disorders/peripheralneuropathy/detail_peripheralneuropathy.htm Google Scholar

28Krendel, D.A. (1998) Vascular inflammation in proximal diabetic neuropathy. Journal of Neurology 245, 748Google Scholar

29Said, G. (2007) Diabetic neuropathy – a review. Nature Clinical Practice. Neurology 3, 331-340CrossRef Google Scholar PubMed

30Pittenger, G.L. et al. (1999) Specific fiber deficits in sensorimotor diabetic polyneuropathy correspond to cytotoxicity against neuroblastoma cells of sera from patients with diabetes. Diabetes Care 22, 1839-1844CrossRef Google Scholar PubMed

31Veves, A. and King, G.L. (2001) Can VEGF reverse diabetic neuropathy in human subjects? Journal of Clinical Investigation 107, 1215-1218CrossRef Google Scholar PubMed

32Cameron, N.E. and Cotter, M.A. (1997) Metabolic and vascular factors in the pathogenesis of diabetic neuropathy. Diabetes 46 (Suppl 2), S31-S37Google Scholar

33Hoeldtke, R.D. et al. (2002) Nitrosative stress, uric Acid, and peripheral nerve function in early type 1 diabetes. Diabetes 51, 2817-2825Google Scholar

34Winkler, G. and Kempler, P. (2010) Pathomechanism of diabetic neuropathy: background of the pathogenesis-oriented therapy. Orvosi Hetilap 151, 971-981CrossRef Google Scholar PubMed

35Vinik, A.I. and Erbas, T. (2001) Recognizing and treating diabetic autonomic neuropathy. Cleveland Clinic Journal of Medicine 68, 928-930, 932, 934-944Google Scholar

36Vinik, A.I. et al. (2003) Diabetic autonomic neuropathy. Diabetes Care 26, 1553-1579CrossRef Google Scholar PubMed

37Schumer, MP, Joyner, S.A., Pfeifer, MA (1998) Cardiovascular autonomic neuropathy testing in patients with diabetes. Diabetes Spectrum 11, 227-231Google Scholar

38Ziegler, D. (1999) Cardiovascular autonomic neuropathy: clinical manifestations and measurement. Diabetes Reviews 7, 300-315Google Scholar

39Vinik, A.I. and Erbas, T. (2006) Cardiovascular autonomic neuropathy: diagnosis and management. Current Diabetes Reports 6, 424-430CrossRef Google Scholar PubMed

40Maser, R.E. and Lenhard, M.J. (2005) Cardiovascular autonomic neuropathy due to diabetes mellitus: clinical manifestations, consequences, and treatment. Journal of Clinical Endocrinology and Metabolism 90, 5896-5903CrossRef Google Scholar

41Weimer, L.H. (2010) Autonomic testing: common techniques and clinical applications. Neurologist 16, 215-222CrossRef Google Scholar PubMed

42Pop-Busui, R. et al. (2010) Effects of cardiac autonomic dysfunction on mortality risk in the Action to Control Cardiovascular Risk in Diabetes (ACCORD) trial. Diabetes Care 33, 1578-1584CrossRef Google Scholar PubMed

43Debono, M. and Cachia, E. (2007) The impact of cardiovascular autonomic neuropathy in diabetes: is it associated with left ventricular dysfunction? Autonomic Neuroscience 132, 1-7CrossRef Google Scholar PubMed

44Uusitupa, M.I., Mustonen, J.N. and Airaksinen, K.E. (1990) Diabetic heart muscle disease. Annals of Medicine 22, 377-386CrossRef Google Scholar PubMed

45Taskiran, M. et al. (2004) Left ventricular dysfunction in normotensive Type 1 diabetic patients: the impact of autonomic neuropathy. Diabetic Medicine 21, 524-530Google Scholar

46Rapacciuolo, A. et al. (2001) Important role of endogenous norepinephrine and epinephrine in the development of in vivo pressure-overload cardiac hypertrophy. Journal of the American College of Cardiology 38, 876-882CrossRef Google Scholar PubMed

47King, B.D. et al. (1987) Absence of hypertension despite chronic marked elevations in plasma norepinephrine in conscious dogs. Hypertension 9, 582-590CrossRef Google Scholar PubMed

48Pop-Busui, R. (2010) Cardiac autonomic neuropathy in diabetes: a clinical perspective. Diabetes Care 33, 434-441CrossRef Google Scholar PubMed

49Sundkvist, G. et al. (1992) Plasma neuropeptide Y (NPY) and galanin before and during exercise in type 1 diabetic patients with autonomic dysfunction. Diabetes Research and Clinical Practice 15, 219-226CrossRef Google Scholar PubMed

50El-Sayed, Z.A. et al. (2009) Cardiovascular autonomic function assessed by autonomic function tests and serum autonomic neuropeptides in Egyptian children and adolescents with rheumatic diseases. Rheumatology (Oxford) 48, 843-848Google Scholar

51Ralevic, V., Aberdeen, J.A. and Burnstock, G. (1991) Acrylamide-induced autonomic neuropathy of rat mesenteric vessels: histological and pharmacological studies. Journal of the Autonomic Nervous System 34, 77-87CrossRef Google Scholar PubMed

52Meit Björndahl, R.C., Luxun, X. and Yihai, C. (2006) NPY-induced Angiogenesis in Retinopathy and Wound Healing, Birkhäuser Basel, StockholmGoogle Scholar

53Chen, M. et al. (2005) Neuropeptide Y induces cardiomyocyte hypertrophy via calcineurin signaling in rats. Regulatory Peptides 125, 9-15Google Scholar

54Ekstrand, A.J. et al. (2003) Deletion of neuropeptide Y (NPY) 2 receptor in mice results in blockage of NPY-induced angiogenesis and delayed wound healing. Proceedings of the National Academy of Sciences of the United States of America 100, 6033-6038CrossRef Google Scholar PubMed

55Zukowska-Grojec, Z. et al. (1998) Neuropeptide Y: a novel angiogenic factor from the sympathetic nerves and endothelium. Circulation Research 83, 187-195Google Scholar

56Pradhan, L. et al. (2009) Inflammation and neuropeptides: the connection in diabetic wound healing. Expert Reviews in Molecular Medicine 11, e2CrossRef Google Scholar PubMed

57Jain, M. et al. (2011) Effect of hyperglycemia and neuropeptides on interleukin-8 expression and angiogenesis in dermal microvascular endothelial cells. Journal of Vascular Surgery 53, 1654-1660CrossRef Google Scholar PubMed

58Kim, S.Z., Cho, K.W. and Kim, S.H. (1999) Modulation of endocardial natriuretic peptide receptors in right ventricular hypertrophy. American Journal of Physiology 277, H2280-H2289Google Scholar PubMed

59Woo, N.D. and Ganguly, P.K. (1995) Neuropeptide Y prevents agonist-stimulated increases in contractility. Hypertension 26, 480-484CrossRef Google Scholar PubMed

60Sieburth, D., Madison, J.M. and Kaplan, J.M. (2007) PKC-1 regulates secretion of neuropeptides. Nature Neuroscience 10, 49-57CrossRef Google Scholar PubMed

61Hackenthal, E. et al. (1987) Neuropeptide Y inhibits renin release by a pertussis toxin-sensitive mechanism. American Journal of Physiology 252, F543-F550Google Scholar

62Blomqvist, A.G. and Herzog, H. (1997) Y-receptor subtypes – how many more? Trends in Neurosciences 20, 294-298CrossRef Google Scholar PubMed

63Adrian, T.E. et al. (1983) Neuropeptide Y distribution in human brain. Nature 306, 584-586Google Scholar

64Kaye, W.H. et al. (1990) Altered cerebrospinal fluid neuropeptide Y and peptide YY immunoreactivity in anorexia and bulimia nervosa. Archives of General Psychiatry 47, 548-556Google Scholar

65Zukowska, Z. et al. (2003) Neuropeptide Y: a new mediator linking sympathetic nerves, blood vessels and immune system? Canadian Journal of Physiology and Pharmacology 81, 89-94Google Scholar

66Brothers, S.P. and Wahlestedt, C. (2010) Therapeutic potential of neuropeptide Y (NPY) receptor ligands. EMBO Molecular Medicine 2, 429-439CrossRef Google Scholar PubMed

67Pedrazzini, T., Pralong, F. and Grouzmann, E. (2003) Neuropeptide Y: the universal soldier. Cellular and Molecular Life Sciences 60, 350-377CrossRef Google Scholar PubMed

68Kohno, D. et al. (2003) Ghrelin directly interacts with neuropeptide-Y-containing neurons in the rat arcuate nucleus: Ca2+ signaling via protein kinase A and N-type channel-dependent mechanisms and cross-talk with leptin and orexin. Diabetes 52, 948-956Google Scholar

69Pons, J. et al. (2008) Interactions of multiple signaling pathways in neuropeptide Y-mediated bimodal vascular smooth muscle cell growth. Canadian Journal of Physiology and Pharmacology 86, 438-448CrossRef Google Scholar PubMed

70Kuncova, J. et al. (2005) Heterogenous changes in neuropeptide Y, norepinephrine and epinephrine concentrations in the hearts of diabetic rats. Autonomic Neuroscience 121, 7-15CrossRef Google Scholar PubMed

71Watanabe, M. et al. (2008) Direct and indirect modulation of neuropeptide Y gene expression in response to hypoglycemia in rat arcuate nucleus. FEBS Letters 582, 3632-3638Google Scholar

72Andersson, D. et al. (1992) Diminished contractile responses to neuropeptide Y of arteries from diabetic rabbits. Journal of the Autonomic Nervous System 37, 215-222CrossRef Google Scholar PubMed

73Lind, H. et al. (1995) Selective attenuation of neuropeptide-Y-mediated contractile responses in blood vessels from patients with diabetes mellitus. Clinical Autonomic Research 5, 191-197CrossRef Google Scholar PubMed

74Zhang, X.M., Han, S. and Zhou, L. (2004) The investigation of Syn and NPY expression in brain tissues of diabetic model rat induced by streptozotocin. Shi Yan Sheng Wu Xue Bao 37, 449-455Google Scholar

75Matyal, R. et al. Chronic type II diabetes mellitus leads to changes in neuropeptide Y receptor expression and distribution in human myocardial tissue. European Journal of Pharmacology 665, 19-28CrossRef Google Scholar

76Olcese, J. (1991) Neuropeptide Y: an endogenous inhibitor of norepinephrine-stimulated melatonin secretion in the rat pineal gland. Journal of Neurochemistry 57, 943-947CrossRef Google Scholar PubMed

77Allen, A.R. et al. (2006) Modulation of contractile function through neuropeptide Y receptors during development of cardiomyocyte hypertrophy. Journal of Pharmacology and Experimental Therapeutics 319, 1286-1296CrossRef Google Scholar PubMed

78Wier, W.G. et al. (2009) Sympathetic neurogenic Ca2+ signalling in rat arteries: ATP, noradrenaline and neuropeptide Y. Experimental Physiology 94, 31-37CrossRef Google Scholar PubMed

79Prieto, D. et al. (2000) Neuropeptide Y regulates intracellular calcium through different signalling pathways linked to a Y(1)-receptor in rat mesenteric small arteries. British Journal of Pharmacology 129, 1689-1699Google Scholar

80Chottova Dvorakova, M. et al. (2008) Expression of neuropeptide Y and its receptors Y1 and Y2 in the rat heart and its supplying autonomic and spinal sensory ganglia in experimentally induced diabetes. Neuroscience 151, 1016-1028Google Scholar

81Woo, N.D. et al. (1994) Adrenoreceptor-mediated effect of neuropeptide Y decreases cardiac inotropic responses. Biochimica et Biophysica Acta 1222, 457-463Google Scholar

82Goldberg, Y. et al. (1998) Intracellular signaling leads to the hypertrophic effect of neuropeptide Y. American Journal of Physiology 275, C1207-C1215CrossRef Google Scholar

83Pellieux, C. et al. (2000) Neuropeptide Y (NPY) potentiates phenylephrine-induced mitogen-activated protein kinase activation in primary cardiomyocytes via NPY Y5 receptors. Proceedings of the National Academy of Sciences of the United States of America 97, 1595-1600Google Scholar

84Robich, M.P. et al. (2010) Effects of neuropeptide Y on collateral development in a swine model of chronic myocardial ischemia. Journal of Molecular and Cellular Cardiology 49, 1022-1030Google Scholar

85Waeber, B. et al. (1990) Role of atrial natriuretic peptides and neuropeptide Y in blood pressure regulation. Hormone Research 34, 161-165Google Scholar

86Winaver, J. and Abassi, Z. (2006) Role of neuropeptide Y in the regulation of kidney function. EXS 95, 123-132Google Scholar

87Piao, F.L. et al. (2008) Different regulation of atrial ANP release through neuropeptide Y2 and Y4 receptors. Journal of Korean Medical Science 23, 1027-1032Google Scholar

88Zelis, R. et al. (1994) Neuropeptide Y infusion decreases plasma renin activity in postmyocardial infarction rats. Journal of Cardiovascular Pharmacology 24, 896-899CrossRef Google Scholar PubMed

89Ohtori, S. et al. (2002) Up-regulation of substance P and NMDA receptor mRNA in dorsal horn and preganglionic sympathetic neurons during adjuvant-induced noxious stimulation in rats. Annals of Anatomy 184, 71-76Google Scholar

90Hokfelt, T. et al. (1975) Experimental immunohistochemical studies on the localization and distribution of substance P in cat primary sensory neurons. Brain Research 100, 235-252CrossRef Google Scholar PubMed

91Roth, K.A. and Gordon, J.I. (1990) Spatial differentiation of the intestinal epithelium: analysis of enteroendocrine cells containing immunoreactive serotonin, secretin, and substance P in normal and transgenic mice. Proceedings of the National Academy of Sciences of the United States of America 87, 6408-6412Google Scholar

92Nieber, K. and Oehme, P. (1982) [Substance P – a neuropeptide transmitter]. Zeitschift für die gesamte innere Medizin und ihre Grenzgebiete 37, 577-582Google Scholar PubMed

93Khawaja, A.M. and Rogers, D.F. (1996) Tachykinins: receptor to effector. International Journal of Biochemistry and Cell Biology 28, 721-738CrossRef Google Scholar PubMed

94Trippodo, N.C. et al. (1993) Combined inhibition of neutral endopeptidase and angiotensin converting enzyme in cardiomyopathic hamsters with compensated heart failure. Journal of Pharmacology and Experimental Therapeutics 267, 108-116Google Scholar PubMed

95Tsui, H. et al. (2007) ‘Sensing’ autoimmunity in type 1 diabetes. Trends in Molecular Medicine 13, 405-413Google Scholar

96Lindberger, M. et al. (1989) Nerve fibre studies in skin biopsies in peripheral neuropathies. I. Immunohistochemical analysis of neuropeptides in diabetes mellitus. Journal of Neurological Sciences 93, 289-296Google Scholar

97Iwasaki, H. et al. (2006) A deficiency of gastric interstitial cells of Cajal accompanied by decreased expression of neuronal nitric oxide synthase and substance P in patients with type 2 diabetes mellitus. Journal of Gastroenterology 41, 1076-1087Google Scholar

98Boer, P.A. et al. (2011) Early potential impairment of renal sensory nerves in streptozotocin-induced diabetic rats: role of neurokinin receptors. Nephrology, Dialysis, Transplantation 26, 823-832CrossRef Google Scholar PubMed

99Paulus, W.J. (2001) The role of nitric oxide in the failing heart. Heart Failure Reviews 6, 105-118CrossRef Google Scholar PubMed

100Tingberg, E. et al. (2006) Neurohumoral changes in patients with left ventricular dysfunction following acute myocardial infarction and the effect of nitrate therapy: a randomized, double-blind, placebo-controlled long-term study. Journal of Cardiovascular Pharmacology 48, 166-172CrossRef Google Scholar PubMed

101Pradhan, L. et al. (2011) Gene expression of pro-inflammatory cytokines and neuropeptides in diabetic wound healing. Journal of Surgical Research 167, 336-342Google Scholar

102Calderone, A. et al. (1998) Nitric oxide, atrial natriuretic peptide, and cyclic GMP inhibit the growth-promoting effects of norepinephrine in cardiac myocytes and fibroblasts. Journal of Clinical Investigation 101, 812-818CrossRef Google Scholar PubMed

103Yu, Y. et al. (2011) Parasympathetic and substance P-immunoreactive nerve denervation in atrial fibrillation models. Cardiovascular Pathology [epub]Google Scholar

104Wang, L. and Wang, D.H. (2005) TRPV1 gene knockout impairs postischemic recovery in isolated perfused heart in mice. Circulation 112, 3617-3623CrossRef Google Scholar PubMed

105Wharton, J. et al. (1986) Capsaicin induces a depletion of calcitonin gene-related peptide (CGRP)-immunoreactive nerves in the cardiovascular system of the guinea pig and rat. Journal of the Autonomic Nervous System 16, 289-309CrossRef Google Scholar

106Ren, J.Y. et al. Cardioprotection by ischemic postconditioning is lost in isolated perfused heart from diabetic rats: involvement of transient receptor potential vanilloid 1, calcitonin gene-related peptide and substance P. Regulatory Peptides 169, 49-57CrossRef Google Scholar

107Yan, C., Gao, M. and Deng, Z. (1998) Study on changes of plasma substance P in essential hypertension with left ventricular hypertrophy patients and the effect of promoting blood circulation and eliminating phlegm. Zhongguo Zhong Xi Yi Jie He Za Zhi 18, 336-338Google Scholar

108Valdemarsson, S. et al. (1991) Increased plasma level of substance P in patients with severe congestive heart failure treated with ACE inhibitors. Journal of Internal Medicine 230, 325-331Google Scholar

109Dzurik, M.V. et al. (2007) Endogenous substance P modulates human cardiovascular regulation at rest and during orthostatic load. Journal of Applied Physiology 102, 2092-2097Google Scholar

110Wang, L.L. et al. (2011) Implication of Substance P in myocardial contractile function during ischemia in rats. Regulatory Peptides 167, 185-191Google Scholar

111D'Souza, M. et al. (2007) Substance P is associated with heart enlargement and apoptosis in murine dilated cardiomyopathy induced by Taenia crassiceps infection. Journal of Parasitology 93, 1121-1127Google Scholar

112Edvinsson, L. et al. (1990) Congestive heart failure: involvement of perivascular peptides reflecting activity in sympathetic, parasympathetic and afferent fibres. European Journal of Clinical Investigation 20, 85-89CrossRef Google Scholar PubMed

113Bergdahl, A. et al. (1999) Dilatory responses to acetylcholine, calcitonin gene-related peptide and substance P in the congestive heart failure rat. Acta Physiologica Scandinavica 165, 15-23CrossRef Google Scholar PubMed

114Quirion, R. et al. (1992) Characterization of CGRP1 and CGRP2 receptor subtypes. Annals of the New York Academy of Sciences 657, 88-105CrossRef Google Scholar PubMed

115Juaneda, C., Dumont, Y. and Quirion, R. (2000) The molecular pharmacology of CGRP and related peptide receptor subtypes. Trends in Pharmacological Sciences 21, 432-438Google Scholar

116McLatchie, L.M. et al. (1998) RAMPs regulate the transport and ligand specificity of the calcitonin-receptor-like receptor. Nature 393, 333-339CrossRef Google Scholar PubMed

117Adeghate, E. (1999) Distribution of calcitonin-gene-related peptide, neuropeptide-Y, vasoactive intestinal polypeptide, cholecystokinin-8, substance P and islet peptides in the pancreas of normal and diabetic rats. Neuropeptides 33, 227-235Google Scholar

118Saffir, A.J. (1976) Letter: clinical evaluation of a newly designed contoured toothbrush. Journal of Periodontology 47, 487CrossRef Google Scholar PubMed

119Parlapiano, C. et al. (1995) Calcitonin gene-related peptide in diabetes mellitus type 2: a possible etiopathogenetic role. European review for medical and pharmacological studies 17, 35-39Google Scholar PubMed

120Sun, W. et al. (2003) Intramuscular transfer of naked calcitonin gene-related peptide gene prevents autoimmune diabetes induced by multiple low-dose streptozotocin in C57BL mice. European Journal of Immunology 33, 233-242CrossRef Google Scholar PubMed

121Morrison, J.F., Dhanasekaran, S. and Howarth, F.C. (2008) Neuropeptide Y and CGRP concentrations in the rat tail artery: effects of age and two types of diabetes. Peptides 30, 710-714CrossRef Google Scholar PubMed

122Creager, M.A. et al. (2003) Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: Part I. Circulation 108, 1527-1532CrossRef Google Scholar PubMed

123Clementi, G. et al. (1995) Anti-inflammatory activity of amylin and CGRP in different experimental models of inflammation. Life Sciences 57, PL193-PL197CrossRef Google Scholar PubMed

124Wu, D. et al. (2000) Characterisation of calcitonin gene-related peptide receptors in rat atrium and vas deferens: evidence for a [Cys(Et)(2, 7)]hCGRP-preferring receptor. European Journal of Pharmacology 400, 313-319CrossRef Google Scholar

125Li, J. et al. (2009) Nitroglycerin protects small intestine from ischemia-reperfusion injury via NO-cGMP pathway and upregulation of alpha-CGRP. Journal of Gastrointestinal Surgery 13, 478-485Google Scholar

126Liu, N. et al. (2011) Differential effects of the calcitonin gene-related peptide on cardiac performance in acute myocardial ischemia and reperfusion in isolated rat hearts. Minerva Anestesiologica 77, 789-796Google Scholar

127Covino, E. and Spadaccio, C. (2011) Calcitonin gene related peptide: a new ally in cardiac ischemic disease. Minerva Anestesiologica 77, 763-765Google Scholar

128Mishima, T. et al. (2011) Calcitonin gene-related peptide facilitates revascularization during hindlimb ischemia in mice. American Journal of Physiology. Heart and Circulatory Physiology 300, H431-H439Google Scholar PubMed

129Levin, E.R., Gardner, D.G. and Samson, W.K. (1998) Natriuretic peptides. New England Journal of Medicine 339, 321-328Google Scholar PubMed

130Hirose, S., Hagiwara, H. and Takei, Y. (2001) Comparative molecular biology of natriuretic peptide receptors. Canadian Journal of Physiology and Pharmacology 79, 665-672CrossRef Google Scholar PubMed

131Barr, C.S., Rhodes, P. and Struthers, A.D. (1996) C-type natriuretic peptide. Peptides 17, 1243-1251CrossRef Google Scholar PubMed

132Garg, R. and Pandey, K.N. (2005) Regulation of guanylyl cyclase/natriuretic peptide receptor-A gene expression. Peptides 26, 1009-1023Google Scholar

133Nakayama, T. (2005) The genetic contribution of the natriuretic peptide system to cardiovascular diseases. Endocrine Journal 52, 11-21CrossRef Google Scholar PubMed

134Potter, L.R. et al. (2009) Natriuretic peptides: their structures, receptors, physiologic functions and therapeutic applications. Handbook of Experimental Pharmacology, 191, 341-366Google Scholar

135Struthers, A.D. (1994) Ten years of natriuretic peptide research: a new dawn for their diagnostic and therapeutic use? BMJ 308, 1615-1619Google Scholar

136Nonoguchi, H., Sands, J.M. and Knepper, M.A. (1988) Atrial natriuretic factor inhibits vasopressin-stimulated osmotic water permeability in rat inner medullary collecting duct. Journal of Clinical Investigation 82, 1383-1390CrossRef Google Scholar PubMed

137Woodman, O.L. et al. (2008) Atrial natriuretic peptide prevents diabetes-induced endothelial dysfunction. Life Sciences 82, 847-854Google Scholar

138Chattington, P.D. et al. (1998) Atrial natriuretic peptide in type 2 diabetes mellitus: response to a physiological mixed meal and relationship to renal function. Diabetic Medicine 15, 375-3793.0.CO;2-N>CrossRef Google Scholar PubMed

139Sechi, L.A. et al. (1995) Receptors for atrial natriuretic peptide are decreased in the kidney of rats with streptozotocin-induced diabetes mellitus. Journal of Clinical Investigation 95, 2451-2457Google Scholar

140Walther, T., Schuitheiss, H.P. and Tschope, C. (2001) Impaired angiotensin II regulation of renal C-type natriuretic peptide mRNA expression in experimental diabetes mellitus. Cardiovascular Research 51, 562-566Google Scholar

141Ganguly, P.K. (1991) Role of atrial natriuretic peptide in congestive heart failure due to chronic diabetes. Canadian Journal of Cardiology 7, 275-280Google Scholar

142Bhalla, M.A. et al. (2004) Prognostic role of B-type natriuretic peptide levels in patients with type 2 diabetes mellitus. Journal of the American College of Cardiology 44, 1047-1052Google Scholar

143van der Horst, I.C. et al. (2010) Neurohormonal profile of patients with heart failure and diabetes. Netherlands Heart Journal 18, 190-196Google Scholar

144Saulnier, P.J. et al. (2011) Impact of Natriuretic Peptide Clearance Receptor (NPR3) Gene Variants on Blood Pressure in Type 2 Diabetes. Diabetes Care 34, 1199-1204CrossRef Google Scholar PubMed

145Lainchbury, J.G. et al. (2000) Effects of natriuretic peptides on load and myocardial function in normal and heart failure dogs. American Journal of Physiology. Heart and Circulatory Physiology 278, H33-H40CrossRef Google Scholar PubMed

146Morishita, R. et al. (1994) Autocrine and paracrine effects of atrial natriuretic peptide gene transfer on vascular smooth muscle and endothelial cellular growth. Journal of Clinical Investigation 94, 824-829CrossRef Google Scholar PubMed

147Thomas, C.J., Head, G.A. and Woods, R.L. (1998) ANP and bradycardic reflexes in hypertensive rats: influence of cardiac hypertrophy. Hypertension 32, 548-555Google Scholar

148Oliver, P.M. et al. (1997) Hypertension, cardiac hypertrophy, and sudden death in mice lacking natriuretic peptide receptor A. Proceedings of the National Academy of Sciences of the United States of America 94, 14730-14735Google Scholar

149Kasama, S. et al. (2008) Effect of atrial natriuretic peptide on left ventricular remodelling in patients with acute myocardial infarction. European Heart Journal 29, 1485-1494Google Scholar

150Backlund, T. et al. (2001) Dual inhibition of angiotensin converting enzyme and neutral endopeptidase by omapatrilat in rat in vivo. Pharmacological Research 44, 411-418CrossRef Google Scholar PubMed

151Stevens, T.L. et al. (1995) A functional role for endogenous atrial natriuretic peptide in a canine model of early left ventricular dysfunction. Journal of Clinical Investigation 95, 1101-1108CrossRef Google Scholar

152Lohmeier, T.E. et al. (1996) Atrial natriuretic peptide and sodium homeostasis in compensated heart failure. American Journal of Physiology 271, R1353-R1363Google Scholar PubMed

153Barrios, V. et al. (2011) Clinical applicability of B-type natriuretic peptide in patients with suspected heart failure in primary care in Spain: the PANAMA study. Expert Review of Cardiovascular Therapy 9, 579-585Google Scholar

154Nadir, M.A. et al. (2011) Meta-analysis of B-type natriuretic peptide's ability to identify stress induced myocardial ischemia. American Journal of Cardiology 107, 662-667Google Scholar

155Atisha, D. et al. (2004) A prospective study in search of an optimal B-natriuretic peptide level to screen patients for cardiac dysfunction. American Heart Journal 148, 518-523Google Scholar

156Chen, H.H. et al. (2000) Subcutaneous administration of brain natriuretic peptide in experimental heart failure. Journal of the American College of Cardiology 36, 1706-1712CrossRef Google Scholar PubMed

157Baliga, V. and Sapsford, R. (2009) Review article: diabetes mellitus and heart failure–an overview of epidemiology and management. Diabetes and Vascular Disease Research 6, 164-171CrossRef Google Scholar

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Diabetic neuropathy and heart failure: role of neuropeptides

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Diabetic neuropathy and heart failure: role of neuropeptides

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