Glycogen synthase kinase-3β inhibition ameliorates cardiac parasympathetic dysfunction in type 1 diabetic akita mice

Diabetes

Volumn 63, Issue 6, 2014, Pages 2097-2113

  Zhang, Yali ^a   Welzig, Charles M ^b,c   Picard, Kristen L ^a   Du, Chuang ^c   Wang, Bo ^a   Pan, Jen Q ^d   Kyriakis, John M ^a   Aronovitz, Mark J ^a   Claycomb, William C ^e   Blanton, Robert M ^a,c   Park, Ho Jin ^a   Galper, Jonas B ^a,c  

^a TUFTS MEDICAL CENTER   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ACETYLCHOLINE ACTIVATED INWARD RECTIFYING CALCIUM CHANNEL; ATROPINE; BETA CATENIN; CARBACHOL; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL 4; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN; INWARDLY RECTIFYING POTASSIUM CHANNEL; KENPAULLONE; LITHIUM; PHOSPHATIDYLINOSITOL 3 KINASE; PROPRANOLOL; PROTEIN KINASE B; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTONOMIC DYSFUNCTION; AUTONOMIC NEUROPATHY; BRADYCARDIA; CONTROLLED STUDY; DIABETIC AUTONOMIC NEUROPATHY; DIABETIC NEUROPATHY; ECHOCARDIOGRAPHY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FLUORESCENCE MICROSCOPY; GENE OVEREXPRESSION; HEART RATE VARIABILITY; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SLOW RELEASE FORMULATION; WESTERN BLOTTING; WILD TYPE;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; DIABETES MELLITUS, TYPE 1; DIABETIC NEUROPATHIES; ELECTROCARDIOGRAPHY; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; GLYCOGEN SYNTHASE KINASE 3; HEART ATRIA; HEART RATE; MICE; MICE, MUTANT STRAINS; MYOCYTES, CARDIAC; PARASYMPATHETIC NERVOUS SYSTEM; PATCH-CLAMP TECHNIQUES; STEROL REGULATORY ELEMENT BINDING PROTEIN 1;

EID: 84901303561     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db12-1459     Document Type: Article

References (53)

1. Aronson D, Rayfield EJ, Chesebro JH. Mechanisms determining course and outcome of diabetic patients who have had acute myocardial infarction. Ann Intern Med 1997;126:296-306
2. Brown DW, Giles WH, Greenlund KJ, Valdez R, Croft JB. Impaired fasting glucose, diabetes mellitus, and cardiovascular disease risk factors are associated with prolonged QTc duration. Results from the Third National Health and Nutrition Examination Survey. J Cardiovasc Risk 2001;8:227-233
3. Allessie MA, Lammers WJ, Bonke IM, Hollen J. Intra-atrial reentry as a mechanism for atrial flutter induced by acetylcholine and rapid pacing in the dog. Circulation 1984;70:123-135
4. Aronson D. Pharmacologic modulation of autonomic tone: implications for the diabetic patient. Diabetologia 1997;40:476-481
5. Valensi P, Paries J, Attali JR; French Group for Research and Study of Diabetic Neuropathy. Cardiac autonomic neuropathy in diabetic patients: influence of diabetes duration, obesity, and microangiopathic complications-the French multicenter study. Metabolism 2003;52:815-820
6. Heller S. Dead in bed. Diabet Med 1999;16:782-785
7. Logothetis DE, Kurachi Y, Galper J, Neer EJ, Clapham DE. The beta gamma subunits of GTP-binding proteins activate the muscarinic K+ channel in heart. Nature 1987;325:321-326
8. Vivaudou M, Chan KW, Sui JL, Jan LY, Reuveny E, Logothetis DE. Probing the G-protein regulation of GIRK1 and GIRK4, the two subunits of the KACh channel, using functional homomeric mutants. J Biol Chem 1997;272:31553- 31560
9. Krapivinsky G, Gordon EA, Wickman K, Velimirovic B, Krapivinsky L, Clapham DE. The G-protein-gated atrial K+ channel IKACh is a heteromultimer of two inwardly rectifying K(+)-channel proteins. Nature 1995;374:135-141
10. Thomas SL, Chmelar RS, Lu C, Halvorsen SW, Nathanson NM. Tissuespecific regulation of G-protein-coupled inwardly rectifying K+ channel expression by muscarinic receptor activation in ovo. J Biol Chem 1997;272: 29958-29962 (Pubitemid 27508099)
11. Pertovaara A, Ostergård M, Ankö ML, et al. RFamide-related peptides signal through the neuropeptide FF receptor and regulate pain-related responses in the rat. Neuroscience 2005;134:1023-1032 (Pubitemid 41133403)
12. Dobrev D, Graf E, Wettwer E, et al. Molecular basis of downregulation of G-protein-coupled inward rectifying K(+) current (I(K,ACh) in chronic human atrial fibrillation: decrease in GIRK4 mRNA correlates with reduced I(K,ACh) and muscarinic receptor-mediated shortening of action potentials. Circulation 2001; 104:2551-2557 (Pubitemid 33104792)
13. Brown MS, Ye J, Rawson RB, Goldstein JL. Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 2000; 100:391-398
14. Matsuda M, Korn BS, Hammer RE, et al. SREBP cleavage-activating protein (SCAP) is required for increased lipid synthesis in liver induced by cholesterol deprivation and insulin elevation. Genes Dev 2001;15:1206-1216 (Pubitemid 32472750)
15. Foretz M, Guichard C, Ferré P, Foufelle F. Sterol regulatory element binding protein-1c is a major mediator of insulin action on the hepatic expression of glucokinase and lipogenesis-related genes. Proc Natl Acad Sci USA 1999;96: 12737-12742 (Pubitemid 29513572)
16. Park HJ, Kong D, Iruela-Arispe L, Begley U, Tang D, Galper JB. 3-hydroxy-3- methylglutaryl coenzyme A reductase inhibitors interfere with angiogenesis by inhibiting the geranylgeranylation of RhoA. Circ Res 2002;91:143-150 (Pubitemid 34827225)
17. Park HJ, Georgescu SP, Du C, et al. Parasympathetic response in chick myocytes and mouse heart is controlled by SREBP. J Clin Invest 2008;118:259- 271
18. Kayo T, Koizumi A. Mapping of murine diabetogenic gene mody on chromosome 7 at D7Mit258 and its involvement in pancreatic islet and beta cell development during the perinatal period. J Clin Invest 1998;101:2112-2118 (Pubitemid 28244095)
19. Mathews CE, Langley SH, Leiter EH. New mouse model to study islet transplantation in insulin-dependent diabetes mellitus. Transplantation 2002;73: 1333-1336 (Pubitemid 34454284)
20. Park HJ, Zhang Y, Du C, et al. Role of SREBP-1 in the development of parasympathetic dysfunction in the hearts of type 1 diabetic Akita mice. Circ Res 2009;105:287-294
21. Rylatt DB, Aitken A, Bilham T, Condon GD, Embi N, Cohen P. Glycogen synthase from rabbit skeletal muscle. Amino acid sequence at the sites phosphorylated by glycogen synthase kinase-3, and extension of the N-terminal sequence containing the site phosphorylated by phosphorylase kinase. Eur J Biochem 1980;107:529-537
22. Lee J, Kim MS. The role of GSK3 in glucose homeostasis and the development of insulin resistance. Diabetes Res Clin Pract 2007;77(Suppl. 1):S49-S57 (Pubitemid 47212553)
23. Wagman AS, Nuss JM. Current therapies and emerging targets for the treatment of diabetes. Curr Pharm Des 2001;7:417-450 (Pubitemid 32409729)
24. De Sarno P, Axtell RC, Raman C, Roth KA, Alessi DR, Jope RS. Lithium prevents and ameliorates experimental autoimmune encephalomyelitis. J Immunol 2008;181:338-345
25. Gehrmann J, Hammer PE, Maguire CT, Wakimoto H, Triedman JK, Berul CI. Phenotypic screening for heart rate variability in the mouse. Am J Physiol Heart Circ Physiol 2000;279:H733-H740
26. Thireau J, Zhang BL, Poisson D, Babuty D. Heart rate variability in mice: a theoretical and practical guide. Exp Physiol 2008;93:83-94 (Pubitemid 350293971)
27. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation 1996;93: 1043-1065
28. DeHaan RL. Development of form in the embryonic heart. An experimental approach. Circulation 1967;35:821-833
29. Barnett JV, Haigh LS, Marsh JD, Galper JB. Effects of low density lipoproteins and mevinolin on sympathetic responsiveness in cultured chick atrial cells. Regulation of beta-adrenergic receptors and as. J Biol Chem 1989;264: 10779-10786 (Pubitemid 19161651)
30. Park HJ, Begley U, Kong D, et al. Role of sterol regulatory element binding proteins in the regulation of Galpha(i2) expression in cultured atrial cells. Circ Res 2002;91:32-37
31. Bain J, McLauchlan H, Elliott M, Cohen P. The specificities of protein kinase inhibitors: an update. Biochem J 2003;371:199-204 (Pubitemid 36458094)
32. Doble BW, Woodgett Jr. Role of glycogen synthase kinase-3 in cell fate and epithelial-mesenchymal transitions. Cells Tissues Organs 2007;185:73-84 (Pubitemid 46956846)
33. Claycomb WC, Lanson NA Jr, Stallworth BS, et al. HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc Natl Acad Sci USA 1998;95:2979-2984 (Pubitemid 28135840)
34. O'Brien WT, Klein PS. Validating GSK3 as an in vivo target of lithium action. Biochem Soc Trans 2009;37:1133-1138
35. Darbar D, Yang T, Churchwell K, Wilde AA, Roden DM. Unmasking of brugada syndrome by lithium. Circulation 2005;112:1527-1531 (Pubitemid 41324512)
36. Hunter DR, Haworth RA, Berkoff HA. Cellular lithium uptake as a probe of sodium channels in the rat heart: modulation of lithium uptake by tetrodotoxin, verapamil, anthopleurin-A, isoproterenol and external stimulation. J Mol Cell Cardiol 1984;16:1083-1090 (Pubitemid 15013883)
37. Bain J, Plater L, Elliott M, et al. The selectivity of protein kinase inhibitors: a further update. Biochem J 2007;408:297-315
38. McDowell TS, Hajduczok G, Abboud FM, Chapleau MW. Baroreflex dysfunction in diabetes mellitus. II. Site of baroreflex impairment in diabetic rabbits. Am J Physiol 1994;266:H244-H249
39. Fazan R Jr, Ballejo G, Salgado MC, Moraes MF, Salgado HC. Heart rate variability and baroreceptor function in chronic diabetic rats. Hypertension 1997; 30:632-635 (Pubitemid 27444244)
40. De Angelis K, Schaan BD, Maeda CY, Dall'Ago P, Wichi RB, Irigoyen MC. Cardiovascular control in experimental diabetes. Braz J Med Biol Res 2002;35: 1091-1100 (Pubitemid 35476808)
41. Van Buren T, Schiereck P, De Ruiter GJ, Gispen WH, De Wildt DJ. Vagal efferent control of electrical properties of the heart in experimental diabetes. Acta Diabetol 1998;35:19-25 (Pubitemid 28306250)
42. Lu Z, Jiang YP, Xu XH, Ballou LM, Cohen IS, Lin RZ. Decreased L-type Ca2+ current in cardiac myocytes of type 1 diabetic Akita mice due to reduced phosphatidylinositol 3-kinase signaling. Diabetes 2007;56:2780-2789 (Pubitemid 350044922)
43. Russell JW, Feldman EL. Insulin-like growth factor-I prevents apoptosis in sympathetic neurons exposed to high glucose. Horm Metab Res 1999;31:90-96 (Pubitemid 29169481)
44. Russell JW, Sullivan KA, Windebank AJ, Herrmann DN, Feldman EL. Neurons undergo apoptosis in animal and cell culture models of diabetes. Neurobiol Dis 1999;6:347-363 (Pubitemid 29496214)
45. Yang B, Chon KH. Assessment of diabetic cardiac autonomic neuropathy in type I diabetic mice. Conf Proc IEEE Eng Med Biol Soc 2011:6560-6563
46. Liberman Z, Plotkin B, Tennenbaum T, Eldar-Finkelman H. Coordinated phosphorylation of insulin receptor substrate-1 by glycogen synthase kinase-3 and protein kinase C betaII in the diabetic fat tissue. Am J Physiol Endocrinol Metab 2008;294:E1169-E1177
47. Mussmann R, Geese M, Harder F, et al. Inhibition of GSK3 promotes replication and survival of pancreatic beta cells. J Biol Chem 2007;282:12030-12037 (Pubitemid 47100714)
48. Sundqvist A, Bengoechea-Alonso MT, Ye X, et al. Control of lipid metabolism by phosphorylation-dependent degradation of the SREBP family of transcription factors by SCF(Fbw7). Cell Metab 2005;1:379-391 (Pubitemid 43960622)
49. Schwartz PJ, Billman GE, Stone HL. Autonomic mechanisms in ventricular fibrillation induced by myocardial ischemia during exercise in dogs with healed myocardial infarction. An experimental preparation for sudden cardiac death. Circulation 1984;69:790-800 (Pubitemid 14125661)
50. Kataoka M, Ito C, Sasaki H, Yamane K, Kohno N. Low heart rate variability is a risk factor for sudden cardiac death in type 2 diabetes. Diabetes Res Clin Pract 2004;64:51-58 (Pubitemid 38249457)
51. Jouven X, Empana JP, Schwartz PJ, Desnos M, Courbon D, Ducimetière P. Heart-rate profile during exercise as a predictor of sudden death. N Engl J Med 2005;352:1951-1958 (Pubitemid 40638365)
52. Burger AJ, Charlamb M, Sherman HB. Circadian patterns of heart rate variability in normals, chronic stable angina and diabetes mellitus. Int J Cardiol 1999;71:41-48 (Pubitemid 29457779)
53. Valensi PE, Johnson NB, Maison-Blanche P, Extramania F, Motte G, Coumel P. Influence of cardiac autonomic neuropathy on heart rate dependence of ventricular repolarization in diabetic patients. Diabetes Care 2002;25:918-923 (Pubitemid 41094293)