Increased efferent cardiac sympathetic nerve activity and defective intrinsic heart rate regulation in type 2 diabetes

Diabetes

Volumn 64, Issue 8, 2015, Pages 2944-2956

  Thaung, H P Aye ^a   Baldi, J Chris ^b   Wang, Heng Yu ^a   Hughes, Gillian ^a   Cook, Rosalind F ^a   Bussey, Carol T ^a   Sheard, Phil W ^a   Bahn, Andrew ^a   Jones, Peter P ^a   Schwenke, Daryl O ^a   Lamberts, Regis R ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

BETA ADRENERGIC RECEPTOR; DOBUTAMINE; GLUCOSE; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; INSULIN; STIMULATORY GUANINE NUCLEOTIDE BINDING PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY MASS; CONTROLLED STUDY; EFFERENT NERVE; EX VIVO STUDY; GLUCOSE BLOOD LEVEL; HEART CONTRACTION; HEART DENERVATION; HEART NERVE; HEART RHYTHM; INOTROPISM; INSULIN BLOOD LEVEL; ISOLATED HEART; LEFT VENTRICULAR DIASTOLIC DYSFUNCTION; MALE; NERVE CONDUCTION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RAT MODEL; STELLATE GANGLION; SYMPATHETIC NERVE; SYMPATHETIC NERVE ACTIVITY; ZUCKER DIABETIC FATTY RAT;

EID: 84969517706     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0955     Document Type: Article

References (62)

1. Galderisi M, Anderson KM, Wilson PW, Levy D. Echocardiographic evidence for the existence of a distinct diabetic cardiomyopathy (the Framingham Heart Study). Am J Cardiol 1991;68:85-89
2. Palmieri V, Bella JN, Arnett DK, et al. Effect of type 2 diabetes mellitus on left ventricular geometry and systolic function in hypertensive subjects: Hypertension Genetic Epidemiology Network (HyperGEN) study. Circulation 2001;103: 102-107
3. Berry C, Brett M, Stevenson K, McMurray JJ, Norrie J. Nature and prognostic importance of abnormal glucose tolerance and diabetes in acute heart failure. Heart 2008;94:296-304
4. Vinik AI, Ziegler D. Diabetic cardiovascular autonomic neuropathy. Circulation 2007;115:387-397
5. Lloyd-Mostyn RH, Watkins PJ Defective innervation of heart in diabetic autonomic neuropathy. BMJ 1975;3:15-17
6. Scognamiglio R, Avogaro A, Casara D, et al. Myocardial dysfunction and adrenergic cardiac innervation in patients with insulin-dependent diabetes mellitus. J Am Coll Cardiol 1998;31:404-412
7. Langer A, Freeman MR, Josse RG, Armstrong PW Metaiodobenzylguanidine imaging in diabetes mellitus: assessment of cardiac sympathetic denervation and its relation to autonomic dysfunction and silent myocardial ischemia. J Am Coll Cardiol 1995;25:610-618
8. Lefkowitz RJ, Caron MG, Stiles GL Mechanisms of membrane-receptor regulation. Biochemical, physiological, and clinical insights derived from studies of the adrenergic receptors. N Engl J Med 1984;310:1570-1579
9. Bristow MR. Changes in myocardial and vascular receptors in heart failure. J Am Coll Cardiol 1993;22(Suppl. A):61A-71A
10. Vadlamudi RV, McNeill JH Effect of experimental diabetes on isolated rat heart responsiveness to isoproterenol. Can J Physiol Pharmacol 1984;62:124-131
11. Atkins FL, Dowell RT, Love S. beta-Adrenergic receptors, adenylate cyclase activity, and cardiac dysfunction in the diabetic rat. J Cardiovasc Pharmacol 1985;7:66-70
12. Yu Z, McNeill JH Altered inotropic responses in diabetic cardiomyopathy and hypertensive-diabetic cardiomyopathy. J Pharmacol Exp Ther 1991;257:64-71
13. Amour J, David JS, Vivien B, Coriat P, Riou B. Interaction of halogenated anesthetics with alpha- and beta-adrenoceptor stimulations in diabetic rat myocardium. Anesthesiology 2004;101:1145-1152
14. Latifpour J, McNeill JH Cardiac autonomic receptors: effect of long-term experimental diabetes. J Pharmacol Exp Ther 1984;230:242-249
15. Gando S, Hattori Y, Akaishi Y, Nishihira J, Kanno M. Impaired contractile response to beta adrenoceptor stimulation in diabetic rat hearts: alterations in beta adrenoceptors-G protein-adenylate cyclase system and phospholamban phosphorylation. J Pharmacol Exp Ther 1997;282:475-484
16. Dinçer UD, Bidasee KR, Güner S, Tay A, Ozçelikay AT, Altan VM The effect of diabetes on expression of beta1-, beta2-, and beta3-adrenoreceptors in rat hearts. Diabetes 2001;50:455-461
17. Ganguly PK, Dhalla KS, Innes IR, Beamish RE, Dhalla NS Altered norepinephrine turnover and metabolism in diabetic cardiomyopathy. Circ Res 1986;59:684-693
18. Ganguly PK, Beamish RE, Dhalla KS, Innes IR, Dhalla NS Norepinephrine storage, distribution, and release in diabetic cardiomyopathy. Am J Physiol 1987; 252:E734-E739
19. Hoffman RP, Sinkey CA, Anderson EA Muscle sympathetic nerve activity is higher in intensively versus conventionally treated IDDM subjects. Diabetes Care 1995;18:287-291
20. Huggett RJ, Scott EM, Gilbey SG, Stoker JB, Mackintosh AF, Mary DA Impact of type 2 diabetes mellitus on sympathetic neural mechanisms in hypertension. Circulation 2003;108:3097-3101
21. Morrison SF. Differential control of sympathetic outflow. Am J Physiol Regul Integr Comp Physiol 2001;281:R683-R698
22. May CN, Frithiof R, Hood SG, McAllen RM, McKinley MJ, Ramchandra R. Specific control of sympathetic nerve activity to the mammalian heart and kidney. Exp Physiol 2010;95:34-40
23. Malpas SC. Sympathetic nervous system overactivity and its role in the development of cardiovascular disease. Physiol Rev 2010;90:513-557
24. Vaz M, Jennings G, Turner A, Cox H, Lambert G, Esler M. Regional sympathetic nervous activity and oxygen consumption in obese normotensive human subjects. Circulation 1997;96:3423-3429
25. Haas SJ, Vos T, Gilbert RE, Krum H. Are beta-blockers as efficacious in patients with diabetes mellitus as in patients without diabetes mellitus who have chronic heart failure? A meta-analysis of large-scale clinical trials. Am Heart J 2003;146:848-853
26. Rengo G, Lymperopoulos A, Leosco D, Koch WJ GRK2 as a novel gene therapy target in heart failure. J Mol Cell Cardiol 2011;50:785-792
27. Owens B. Cell physiology: the changing colour of fat. Nature 2014;508: S52-S53
28. Schlaich MP, Sobotka PA, Krum H, Lambert E, Esler MD Renal sympatheticnerve ablation for uncontrolled hypertension. N Engl J Med 2009;361:932-934
29. Schwenke DO, Tokudome T, Kishimoto I, et al. One dose of ghrelin prevents the acute and sustained increase in cardiac sympathetic tone after myocardial infarction. Endocrinology 2012;153:2436-2443
30. Pacher P, Nagayama T, Mukhopadhyay P, Bátkai S, Kass DA Measurement of cardiac function using pressure-volume conductance catheter technique in mice and rats. Nat Protoc 2008;3:1422-1434
31. Woolley AG, Sheard PW, Duxson MJ Neurotrophin-3 null mutant mice display a postnatal motor neuropathy. Eur J Neurosci 2005;21:2100-2110
32. Lamberts RR, Onderwater G, Hamdani N, et al. Reactive oxygen species induced stimulation of 5'AMP-activated protein kinase mediates sevoflurane-induced cardioprotection. Circulation 2009;120(Suppl.):S10-S15
33. Schouten VJ, Allaart CP, Westerhof N. Effect of perfusion pressure on force of contraction in thin papillary muscles and trabeculae from rat heart. J Physiol 1992;451:585-604
34. Lamberts RR, Lingam SJ, Wang HY, et al. Impaired relaxation despite up regulated calcium-handling protein atrial myocardium from type 2 diabetic patients with preserved ejection fraction. Cardiovasc Diabetol 2014;13:72
35. Gando S, Hattori Y, Kanno M. Altered cardiac adrenergic neurotransmission in streptozotocin-induced diabetic rats. Br J Pharmacol 1993;109:1276-1281
36. Bradley T, Hjemdahl P. Further studies on renal nerve stimulation induced release of noradrenaline and dopamine from the canine kidney in situ. Acta Physiol Scand 1984;122:369-379
37. Esler M, Jennings G, Lambert G, Meredith I, Horne M, Eisenhofer G. Overflow of catecholamine neurotransmitters to the circulation: source, fate, and functions. Physiol Rev 1990;70:963-985
38. Spallone V, Bernardi L, Ricordi L, et al. Relationship between the circadian rhythms of blood pressure and sympathovagal balance in diabetic autonomic neuropathy. Diabetes 1993;42:1745-1752
39. Jokkel G, Bonyhay I, Kollai M. Heart rate variability after complete autonomic blockade in man. J Auton Nerv Syst 1995;51:85-89
40. Elstad M, Walløe L, Chon KH, Toska K. Low-frequency fluctuations in heart rate, cardiac output and mean arterial pressure in humans: what are the physiological relationships? J Hypertens 2011;29:1327-1336
41. Chidsey CA, Braunwald E. Sympathetic activity and neurotransmitter depletion in congestive heart failure. Pharmacol Rev 1966;18:685-700
42. Levin BE, Triscari J, Sullivan AC Studies of origins of abnormal sympathetic function in obese Zucker rats. Am J Physiol 1983;245:E87-E93
43. Aasum E, Hafstad AD, Severson DL, Larsen TS Age-dependent changes in metabolism, contractile function, and ischemic sensitivity in hearts from db/db mice. Diabetes 2003;52:434-441
44. Wang P, Chatham JC Onset of diabetes in Zucker diabetic fatty (ZDF) rats leads to improved recovery of function after ischemia in the isolated perfused heart. Am J Physiol Endocrinol Metab 2004;286:E725-E736
45. D'Souza A, Bucchi A, Johnsen AB, et al. Exercise training reduces resting heart rate via downregulation of the funny channel HCN4. Nat Commun 2014;5:3775
46. Malone MA, Schocken DD, Hanna SK, Liang X, Malone JI Diabetes-induced bradycardia is an intrinsic metabolic defect reversed by carnitine. Metabolism 2007;56:1118-1123
47. Brubaker PH, Kitzman DW Chronotropic incompetence: causes, consequences, and management. Circulation 2011;123:1010-1020
48. Soltysinska E, Thiele S, Olesen SP, Osadchii OE Chronic sympathetic activation promotes downregulation of β-adrenoceptor-mediated effects in the guinea pig heart independently of structural remodeling and systolic dysfunction. Pflugers Arch 2011;462:529-543
49. Saito K, Torda T, Potter WZ, Saavedra JM Characterization of beta 1- and beta 2-adrenoceptor subtypes in the rat sinoatrial node and stellate ganglia by quantitative autoradiography. Neurosci Lett 1989;96:35-41
50. Barbuti A, Terragni B, Brioschi C, DiFrancesco D. Localization of f-channels to caveolae mediates specific beta2-adrenergic receptor modulation of rate in sinoatrial myocytes. J Mol Cell Cardiol 2007;42:71-78
51. Nikolaev VO, Moshkov A, Lyon AR, et al. Beta2-adrenergic receptor redistribution in heart failure changes cAMP compartmentation. Science 2010;327: 1653-1657
52. Li J, Yan B, Huo Z, et al. beta2- but not beta1-adrenoceptor activation modulates intracellular oxygen availability. J Physiol 2010;588:2987-2998
53. Pérez-Schindler J, Philp A, Baar K, Hernández-Cascales J. Regulation of contractility and metabolic signaling by the β2-adrenergic receptor in rat ventricular muscle. Life Sci 2011;88:892-897
54. Hardie DG. AMPK: a target for drugs and natural products with effects on both diabetes and cancer. Diabetes 2013;62:2164-2172
55. Jardine DL, Charles CJ, Melton IC, et al. Continual recordings of cardiac sympathetic nerve activity in conscious sheep. Am J Physiol Heart Circ Physiol 2002;282:H93-H99
56. Maggi CA, Meli A. Suitability of urethane anesthesia for physiopharmaco logical investigations in various systems. Part 1: General considerations. Experientia 1986;42:109-114
57. Jardine DL, Charles CJ, Frampton CM, Richards AM Cardiac sympathetic nerve activity and ventricular fibrillation during acute myocardial infarction in a conscious sheep model. Am J Physiol Heart Circ Physiol 2007;293:H433-H439
58. Watson AM, Hood SG, Ramchandra R, McAllen RM, May CN Increased cardiac sympathetic nerve activity in heart failure is not due to desensitization of the arterial baroreflex. Am J Physiol Heart Circ Physiol 2007;293:H798-H804
59. Ramchandra R, Hood SG, Frithiof R, May CN Discharge properties of cardiac and renal sympathetic nerves and their impaired responses to changes in blood volume in heart failure. Am J Physiol Regul Integr Comp Physiol 2009;297: R665-R674
60. Hopkins PN, Hunt SC, Wu LL, Williams GH, Williams RR Hypertension, dyslipidemia, and insulin resistance: links in a chain or spokes on a wheel? Curr Opin Lipidol 1996;7:241-253
61. Dunbar JC, Hu Y, Lu H. Intracerebroventricular leptin increases lumbar and renal sympathetic nerve activity and blood pressure in normal rats. Diabetes 1997;46:2040-2043
62. Shek EW, Brands MW, Hall JE Chronic leptin infusion increases arterial pressure. Hypertension 1998;31:409-414