Insulin downregulates M2-muscarinic receptors in adult rat atrial cardiomyocytes: A link between obesity and cardiovascular complications

International Journal of Obesity

Volumn 29, Issue 2, 2005, Pages 176-182

  Pathak, A ^a,b   Smih, F ^a   Galinier, M ^a   Verwaerde, P ^a   Rouet, P ^a   Philip Couderc, P ^a   Montastruc, J L ^b   Senard, J M ^a,b  

^a CHU RANGUEIL   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Heart; Insulin; M2 receptor; Parasympathetic system

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; ADENYLATE CYCLASE; CARBACHOL; FORSKOLIN; INSULIN; MESSENGER RNA; MUSCARINIC M2 RECEPTOR; NITRIC OXIDE SYNTHASE; RAPAMYCIN; WORTMANNIN;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CARDIOVASCULAR RISK; CELL CULTURE; CHOLINERGIC SYSTEM; CONTROLLED STUDY; DRUG INHIBITION; DRUG RECEPTOR BINDING; ENDOTHELIUM; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HEART ATRIUM; HEART MUSCLE CELL; MALE; NONHUMAN; OBESITY; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION;

ADENYLATE CYCLASE; ANIMALS; CARDIOVASCULAR DISEASES; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; INSULIN; MALE; MYOCYTES, CARDIAC; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE III; OBESITY; PARASYMPATHETIC NERVOUS SYSTEM; RATS; RATS, WISTAR; RECEPTOR, MUSCARINIC M2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 13244289880     PISSN: 03070565     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.ijo.0802751     Document Type: Article

References (45)

1. Montani JP, Antic V, Yang Z, Dulloo A. Pathways from obesity to hypertension: from the perspective of a vicious triangle. Int J Obes Relat Metab Disord 2002; 26 (Suppl 2): S28-S38.
2. Kenchaiah S, Evans JC, Levy D, Wilson PW, Benjamin EJ, Larson MG, Kannel WB, Vasan RS. Obesity and the risk of heart failure. N Engl J Med 2002; 347: 305-313.
3. Sudden cardiac death in obesity and hypertension. Lancet 1988; 1: 628-629.
4. Rahmouni K, Haynes WG, Mark AL. Cardiovascular and sympathetic effects of leptin. Curr Hypertens Rep 2002; 4: 119-125.
5. Rajapurohitam V, Gan XT, Kirshenbaum LA, Karmazyn M. The obesity-associated peptide leptin induces hypertrophy in neonatal rat ventricular myocytes. Circ Res 2003; 93: 277-279.
6. Balkan B, Strubbe JH, Bruggink JE, Steffens AB. Overfeeding-induced obesity in rats: insulin sensitivity and autonomic regulation of metabolism. Metabolism 1993; 42: 1509-1518.
7. Opie LH, Walfish PG. Plasma free fatty acid concentrations in obesity. N Engl J Med 1963; 268: 757-760.
8. Casavant RH, Xu Z, Dryer SE. Fatty acid-activated K+ channels in autonomic neurons: activation by an endogenous source of free fatty acids. J Neurochem 2000; 74: 1026-1033.
9. Laederach-Hofmann K, Mussgay L, Ruddel H. Autonomic cardiovascular regulation in obesity. J Endocrinol 2000; 164: 59-66.
10. Rossi M, Marti G, Ricordi L, Fornasari G, Finardi G, Fratino P, Bernardi L. Cardiac autonomic dysfunction in obese subjects. Clin Sci (London) 1989; 76: 567-572.
11. Aronne L, Mackintosh R, Rosenbaum M, Leibel R, Hirsh J. Autonomic nervous system activity in weight gain and weight loss. Am J Physiol 1995; 269: R222-R225.
12. La Rovere MT, Bigger J, Marcus F, Mortara A, Schwartz P. Baroreflex sensitivity and heart-rate variability in prediction of total cardiac mortality after myocardial infarction. Lancet 1998; 351: 478-484.
13. Rocchini AP, Moorehead C, Wentz E, Deremer S. Obesity-induced hypertension in the dog. Hypertension 1987; 9 (Suppl III): III64-III68.
14. Rocchini AP. Cardiovascular regulation in obesity-induced hypertension. Hypertension 1992; 19 (Suppl 1): I56-I60.
15. Verwaerde P, Galinier M, Rougé P, Massabuau P, Galitzky J, Berlan M, Montastruc JL. Experimental hypertension induced by hyperlipidic and hypercaloric diet. Arch Mal CoeurVaiss 1996; 89: 1019-1023.
16. Pelat M, Verwaerde P, Merial C, Galitzky J, Berlan M, Montastruc JL, Senard JM. Impaired atrial M(2)-cholinoceptor function in obesity-related hypertension. Hypertension 1999; 34: 1066-1072.
17. Verwaerde P, Senard JM, Galinier M, Rouge P, Massabuau P, Galitzky J, Berlan M, Lafontan M, Montatsruc JL. Changes in short-term variability of blood pressure and heart rate during the development of obesity-associated hypertension in high-fat fed dogs. J Hypertens 1999; 17: 1135-1143.
18. Philip-Couderc P, Smih F, Pelat M, Vidal C, Verwaerde P, Pathak A, Buys S, Galinier M, Senard JM, Rouet P. Cardiac transcriptome analysis in obesity-related hypertension. Hypertension 2003; 41: 414-421.
19. Emdin M, Gastaldelli A, Muscelli E, Macerata A, Natali A, Camastra S, Ferrannini E. Hyperinsulinemia and autonomic nervous system dysfunction in obesity: effects of weight loss. Circulation 2001; 103: 513-519.
20. Polonsky KS, Given BD, Van Cauter E. Twenty-four-hour profiles and pulsatile patterns of insulin secretion in normal and obese subjects. J Clin Invest 1988; 81: 442-448.
21. Mitcheson J, Hancox J, Levi A. Cultured adult myocytes: future application, culture methods, morphological and electrophysiological properties. Cardiovasc Res 1998; 39: 280-300.
22. Arcaro A, Wymann MP. Wortmannin is a potent phosphatidylinositol 3-kinase inhibitor: the role of phosphatidylinositol 3,4,5-trisphosphate in neutrophil responses. Biochem J 1993; 296 (Part 2): 297-301.
23. Brunn GJ, Williams J, Sabers C, Wiederrecht G, Lawrence Jr JC, Abraham RT. Direct inhibition of the signaling functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBO J 1996; 15: 5256-5267.
24. Alessi DR, Cuenda A, Cohen P, Dudley DT, Saltiel AR. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo. J Biol Chem 1995; 270 (46): 27489-27494.
25. Mandawat MK, Wallbridge DR, Pringle SD, Riyami AA, Latif S, Macfarlane PW, Lorimer AR, Cobbe SM. Heart rate variability in left ventricular hypertrophy. Br Heart J 1995; 73: 139-144.
26. Galinier M, Pathak A, Fourcade J, Androdias C, Curnier D, Varnous S, Boveda S, Massabuau P, Fauvel M, Senard JM, Bounhoure JP. Depressed low frequency power of heart rate variability as an independent predictor of sudden death in chronic heart failure. Eur Heart J 2000; 21: 475-482.
27. Valensi P, Phan Thi B, Pariès J, Attali J. Cardiac autonomic function in obese patients. Inter J Obes 1995; 19: 113-118.
28. Stengel PW, Gomeza J, Wess J, Cohen ML. M(2) and M(4) receptor knockout mice: muscarinic receptor function in cardiac and smooth muscle in vitro. J Pharmacol Exp Ther 2000; 292: 877-885.
29. Pelat M, Verwaerde P, Merial C, Galitzky J, Berlan M, Montastruc J, Senard JM. Impaired atrial M2-cholinoceptor function obesity-related hypertension. Hypertension 1999; 34: 1066-1072.
30. Cabrol P, Galinier M, Fourcade J, Verwaerde P, Massabuau P, Tran MA, Montastruc JL, Bounhoure JP, Fauvel JM, Senard JM. Functional decoupling of left ventricular beta-adrenoceptor in a canine model of obesity-hypertension. Arch Mal Coeur Vaiss 1998; 91: 1021-1024.
31. Carroll JF, Kyser CK, Martin MM. Beta-adrenoceptor density and adenylyl cyclase activity in obese rabbit hearts. Int J Obes Relat Metab Disord 2002; 26: 627-632.
32. Haddad E-B, Roussel J. Regulation of the expression and function of the M2 muscarinic receptor. Trends Pharmacol Sci 1998; 19: 322-327.
33. Hotamisligil GS. The role of TNFalpha and TNF receptors in obesity and insulin resistance. J Intern Med 1999; 245: 621-625.
34. Hotamisligil GS. Mechanisms of TNF-alpha-induced insulin resistance. Exp Clin Endocrinol Diabetes 1999; 107: 119-125.
35. Brownsey RW, Boone AN, Allard MF. Actions of insulin on the mammalian heart: metabolism, pathology and biochemical mechanisms. Cardiovasc Res 1997; 34: 3-24.
36. Hirsch J, Macintosh R, Leibel R. Nutritionally-induced changes in parasympathetic function. Brain Res Bull 1991; 27: 541-542.
37. Hirsch J, Leibel R, Mackintosch R, Aguirre A. Heart rate variability as a measure of autonomic function during weight change in humans. Am J Physiol 1991; 261: R1418-R1423.
38. Paolisso G, Manzella D, Rizzo MR, Barbieri M, Varricchio G, Gambardella A, Varricchio M. Effects of insulin on the cardiac autonomic nervous system in insulin- resistant states. Clin Sci (London) 2000; 98: 129-136.
39. Aikawa R, Nawano M, Gu Y, Katagiri H, Asano T, Zhu W, Nagai R, Komuro I. Insulin prevents cardiomyocytes from oxidative stress-induced apoptosis through activation of PI3 kinase/Akt. Circulation 2000; 102: 2873-2879.
40. Jonassen AK, Sack MN, Mjos OD, Yellon DM. Myocardial protection by insulin at reperfusion requires early administration and is mediated via Akt and p70s6 kinase cell-survival signaling. Circ Res 2001; 89: 1191-1198.
41. Haddad E, Roussel J, Barnes P. Long-term carbachol treatment-induced down regulation of muscarinic M2-receptors but not m2 mRNA in a human lung cell line. Br J Pharmacol 1995; 116: 2027-2032.
42. Strassheim D, Houslay MD, Milligan G. Regulation of cardiac adenylate cyclase activity in rodent models of obesity. Biochem J 1992; 283 (Part 1): 203-208.
43. Hohl CM, Hu B, Fertel RH, Russell JC, McCune SA, Altschuld RA. Effects of obesity and hypertension on ventricular myocytes: comparison of cells from adult SHHF/Mcc-cp and JCR:LA-cp rats. Cardiovasc Res 1993; 27: 238-242.
44. Balligand J, Kobzik L, Han X, Kaye D, Belhassen L, O'Hara D, Kelly RA, Smith TW, Michel T. Nitric oxide -dependent parasympathetic signaling is due to activation of constitutive endothelial (TypeIII) nitric oxide synthase in cradiac myocytes. J Biol Chem 1995; 270: 14582-14586.
45. Kelly R, Balligand J, Smith T. Nitric oxide and cardiac function. Circ Res 1996; 79: 363-380.