α1-Adrenergic receptors prevent a maladaptive cardiac response to pressure overload

Journal of Clinical Investigation

Volumn 116, Issue 4, 2006, Pages 1005-1015

  O'Connell, Timothy D ^a,b,d   Swigart, Philip M ^a   Rodrigo, M C ^a,b   Ishizaka, Shinji ^b,f   Joho, Shuji ^b   Turnbull, Lynne ^a,b,e   Tecott, Laurence H ^b   Baker, Anthony J ^a,b   Foster, Elyse ^b   Grossman, William ^b   Simpson, Paul C ^a,b,c  

^a SAN FRANCISCO VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d UNIVERSITY OF SOUTH DAKOTA   (United States)

^e MONASH UNIVERSITY   (Australia)

^f UNIVERSITY OF TOYAMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; ADRENERGIC RECEPTOR ALPHA(1A); ADRENERGIC RECEPTOR ALPHA(1B);

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; APOPTOSIS; ARTICLE; CARDIOMYOPATHY; CELL ISOLATION; CELL SIZE; CONTROLLED STUDY; DRUG MECHANISM; FIBROSING ALVEOLITIS; HEART VENTRICLE ENDDIASTOLIC PRESSURE; HEART VENTRICLE PRESSURE; HEART WEIGHT; LOCOMOTION; MALE; MOUSE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; SURVIVAL RATE; ANIMAL; BLOOD PRESSURE; C57BL MOUSE; CELL CULTURE; CONGESTIVE CARDIOMYOPATHY; FIBROSIS; GENE EXPRESSION REGULATION; HEART MUSCLE; HEART MUSCLE CELL; HYPERTENSION; METABOLISM; MOUSE MUTANT; MOUSE STRAIN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BLOOD PRESSURE; CARDIOMYOPATHY, DILATED; CELLS, CULTURED; FIBROSIS; GENE EXPRESSION REGULATION; HYPERTENSION; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; MICE, KNOCKOUT; MYOCARDIUM; MYOCYTES, CARDIAC; RECEPTORS, ADRENERGIC, ALPHA-1; SIGNAL TRANSDUCTION;

EID: 33645529873     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI22811     Document Type: Article

References (86)

1. O'Connell, T.D., et al. 2003. The α(1a/c)- and α(1b)- adrenergic receptors are required for physiological cardiac hypertrophy in the double-knockout mouse. J. Clin. Invest. 111:1783-1791. doi:10.1172/JCI200316100.
2. McCloskey, D.T., et al. 2003. Abnormal myocardial contraction in alpha(1a)- and alpha(1b)-adrenoceptor double-knockout mice. J. Mol. Cell. Cardiol. 35:1207-1216.
3. Mani, K., Ashton, A.W., and Kitsis, R.N. 2002. Taking the bad out of adrenergic stimulation. J. Mol. Cell. Cardiol. 34:709-712.
4. Salvi, S. 2001. Protecting the myocardium from ischemic injury: a critical role for alpha(1)-adrenoreceptors? Chest. 119:1242-1249.
5. ALLHAT Collaborative Research Group. 2000. Major cardiovascular events in hypertensive patients randomized to doxazosin vs chlorthalidone: the antihypertensive and lipid-lowering treatment to prevent heart attack trial (ALLHAT). JAMA. 283:1967-1975.
6. Davis, B.R., et al. 2002. Relationship of antihypertensive treatment regimens and change in blood pressure to risk for heart failure in hypertensive patients randomly assigned to doxazosin or chlorthalidone: further analyses from the antihypertensive and lipid-lowering treatment to prevent heart attack trial. Ann. Intern. Med. 137:313-320.
7. Piller, L.B., et al. 2002. Validation of heart failure events in the Antihypertensive and Lipid Lowering Treatment to Prevent Heart Attack Trial (ALLHAT) participants assigned to doxazosin and chlorthalidone. Curr. Control. Trials Cardiovasc. Med. 3:10.
8. ALLHAT Collaborative Research Group. 2003. Diuretic versus alpha-blocker as first-step antihypertensive therapy: final results from the Antihypertensive and Lipid-Lowering Treatment to Prevent Heart Attack Trial (ALLHAT). Hypertension. 42:239-246.
9. Cohn, J.N. 1993. The Vasodilator-Heart Failure Trials (V-HeFT). Mechanistic data from the VA Cooperative Studies. Introduction. Circulation. 87:VI1-VI4.
10. Anglin, I.E., Glassman, D.T., and Kyprianou, N. 2002. Induction of prostate apoptosis by alpha1-adrenoceptor antagonists: mechanistic significance of the quinazoline component. Prostate Cancer Prostatic Dis. 5:88-95.
11. Gonzalez-Juanatey, J.R., Iglesias, M.J., Alcaide, C., Pineiro, R., and Lago, F. 2003. Doxazosin induces apoptosis in cardiomyocytes cultured in vitro by a mechanism that is independent of alpha1-adrenergic blockade. Circulation. 107:127-131.
12. Weinshank, R.L., et al. 1990. Cloning, expression, and pharmacological characterization of a human alpha 2b-adrenergic receptor. Mol. Pharmacol. 38:681-688.
13. Bylund, D.B., et al. 1992. Pharmacological characteristics of alpha 2-adrenergic receptors: comparison of pharmacologically defined subtypes with subtypes identified by molecular cloning. Mol. Pharmacol. 42:1-5.
14. Vaughan, E.D., Jr. 2003. Medical management of benign prostatic hyperplasia: are two drugs better than one? N. Engl. J. Med. 349:2449-2451.
15. Cohn, J.N. 2002. Sympathetic nervous system in heart failure. Circulation. 106:2417-2418.
16. Bristow, M. 2003. Antiadrenergic therapy of chronic heart failure: surprises and new opportunities. Circulation. 107:1100-1102.
17. Gottlieb, S.S. 2003. The neurohormonal paradigm: have we gone too far? J. Am. Coll. Cardiol. 41:1458-1459.
18. Mehra, M.R., Uber, P.A., and Francis, G.S. 2003. Heart failure therapy at a crossroad: are there limits to the neurohormonal model? J. Am. Coll. Cardiol. 41:1606-1610.
19. Nakamura, A., et al. 2001. LV systolic performance improves with development of hypertrophy after transverse aortic constriction in mice. Am. J. Physiol. Heart Circ. Physiol. 281:H1104-H1112.
20. The SOLVD Investigators. 1991. Effect of enalapril on survival in patients with reduced left ventricular ejection fractions and congestive heart failure. N. Engl. J. Med. 325:293-302.
21. The SOLVD Investigators. 1992. Effect of enalapril on mortality and the development of heart failure in asymptomatic patients with reduced left ventricular ejection fractions. N. Engl. J. Med. 327:685-691.
22. Wong, M., et al. 2004. Severity of left ventricular remodeling defines outcomes and response to therapy in heart failure: Valsartan heart failure trial (Val-HeFT) echocardiographic data. J. Am. Coll. Cardiol. 43:2022-2027.
23. Koide, M., et al. 1997. Premorbid determinants of left ventricular dysfunction in a novel model of gradually induced pressure overload in the adult canine. Circulation. 95:1601-1610.
24. Badorff, C., et al. 2002. Fas receptor signaling inhibits glycogen synthase kinase 3 β and induces cardiac hypertrophy following pressure overload. J. Clin. Invest. 109:373-381. doi:10.1172/JCI200213779.
25. Gunther, S., and Grossman, W. 1979. Determinants of ventricular function in pressure-overload hypertrophy in man. Circulation. 59:679-688.
26. Weber, K.T., and Brilla, C.G. 1991. Pathological hypertrophy and cardiac interstitium. Fibrosis and renin-angiotensin-aldosterone system. Circulation. 83:1849-1865.
27. Lindsey, M.L., et al. 2003. Effect of a cleavage-resistant collagen mutation on left ventricular remodeling. Circ. Res. 93:238-245.
28. Simpson, P.C., Long, C.S., Waspe, L.E., Henrich, C.J., and Ordahl, C.P. 1989. Transcription of early developmental isogenes in cardiac myocyte hypertrophy. J. Mol. Cell. Cardiol. 21(Suppl. 5):79-89.
29. Kang, P.M., and Izumo, S. 2003. Apoptosis in heart: basic mechanisms and implications in cardiovascular diseases. Trends Mol. Med. 9:177-182.
30. Wencker, D., et al. 2003. A mechanistic role for cardiac myocyte apoptosis in heart failure. J. Clin. Invest. 111:1497-1504. doi:10.1172/ JCI200317664.
31. Kubota, T., et al. 2001. Overexpression of tumor necrosis factor-alpha activates both anti- and proapoptotic pathways in the myocardium. J. Mol. Cell. Cardiol. 33:1331-1344.
32. Bayer, A.L., et al. 2003. Alterations in protein kinase C isoenzyme expression and autophosphorylation during the progression of pressure overload-induced left ventricular hypertrophy. Mol. Cell. Biochem. 242:145-152.
33. Narula, J., et al. 1999. Apoptosis in heart failure: release of cytochrome c from mitochondria and activation of caspase-3 in human cardiomyopathy. Proc. Natl. Acad. Sci. U. S. A. 96:8144-8149.
34. Byrne, J.A., et al. 2003. Contrasting roles of NADPH oxidase isoforms in pressure-overload versus angiotensin II-induced cardiac hypertrophy. Circ. Res. 93:802-805.
35. Ide, T., et al. 2000. Direct evidence for increased hydroxyl radicals originating from superoxide in the failing myocardium. Circ. Res. 86:152-157.
36. Cohn, J.N., et al. 1984. Plasma norepinephrine as a guide to prognosis in patients with chronic congestive heart failure. N. Engl. J. Med. 311:819-823.
37. Ostman-Smith, I. 1981. Cardiac sympathetic nerves as the final common pathway in the induction of adaptive cardiac hypertrophy. Clin. Sci. (Lond.) 61:265-272.
38. Hagemann, D., and Xiao, R.P. 2002. Dual site phospholamban phosphorylation and its physiological relevance in the heart. Trends Cardiovasc. Med. 12:51-56.
39. Zambrowicz, B.P., and Sands, A.T. 2003. Knockouts model the 100 best-selling drugs: will they model the next 100? Nat. Rev. Drug Discov. 2:38-51.
40. Swedberg, K., et al. 2002. Effects of sustained-release moxonidine, an imidazoline agonist, on plasma norepinephrine in patients with chronic heart failure. Circulation. 105:1797-1803.
41. Coats, A.J. 1999. Heart failure 99: the MOXCON story. Int. J. Cardiol. 71:109-111.
42. Bristow, M.R., et al. 2004. Effect of baseline or changes in adrenergic activity on clinical outcomes in the beta-blocker evaluation of survival trial. Circulation. 110:1437-1442.
43. Schwarz, F., et al. 1981. Reduced volume fraction of myofibrils in myocardium of patients with decompensated pressure overload. Circulation. 63:1299-1304.
44. Zimmer, G., et al. 1992. Decreased concentration of myofibrils and myofiber hypertrophy are structural determinants of impaired left ventricular function in patients with chronic heart diseases: a multiple logistic regression analysis. J. Am. Coll. Cardiol. 20:1135-1142.
45. Kostin, S., et al. 2003. Myocytes die by multiple mechanisms in failing human hearts. Circ. Res. 92:715-724.
46. Razeghi, P., et al. 2001. Metabolic gene expression in fetal and failing human heart. Circulation. 104:2923-2931.
47. Rodrigue-Way, A., et al. 2005. Sarcomeric genes involved in reverse remodeling of the heart during left ventricular assist device support. J. Heart Lung Transplant. 24:73-80.
48. Long, C.S., Ordahl, C.P., and Simpson, P.C. 1989. α 1-Adrenergic receptor stimulation of sarcomeric actin isogene transcription in hypertrophy of cultured rat heart muscle cells. J. Clin. Invest. 83:1078-1082.
49. Bishopric, N.H., Simpson, P.C., and Ordahl, C.P. 1987. Induction of the skeletal α-actin gene in α 1-adrenoceptor-mediated hypertrophy of rat cardiac myocytes. J. Clin. Invest. 80:1194-1199.
50. Waspe, L.E., Ordahl, C.P., and Simpson, P.C. 1990. The cardiac beta-myosin heavy chain isogene is induced selectively in α 1-adrenergic receptor-stimulated hypertrophy of cultured rat heart myocytes. J. Clin. Invest. 85:1206-1214.
51. Iwai-Kanai, E., et al. 1999. Alpha- and beta-adrenergic pathways differentially regulate cell type-specific apoptosis in rat cardiac myocytes. Circulation. 100:305-311.
52. Valks, D.M., et al. 2002. Phenylephrine promotes phosphorylation of Bad in cardiac myocytes through the extracellular signal-regulated kinases 1/2 and protein kinase A. J. Mol. Cell. Cardiol. 34:749-763.
53. Zhu, H., McElwee-Witmer, S., Perrone, M., Clark, K.L., and Zilberstein, A. 2000. Phenylephrine protects neonatal rat cardiomyocytes from hypoxia and serum deprivation-induced apoptosis. Cell Death Differ. 7:773-784.
54. De Windt, L.J., et al. 2000. Calcineurin-mediated hypertrophy protects cardiomyocytes from apoptosis in vitro and in vivo: an apoptosis-independent model of dilated heart failure. Circ. Res. 86:255-263.
55. Amin, J.K., et al. 2001. Reactive oxygen species mediate alpha-adrenergic receptor-stimulated hypertrophy in adult rat ventricular myocytes. J. Mol. Cell. Cardiol. 33:131-139.
56. Tejero-Taldo, M.I., Gursoy, E., Zhao, T.C., and Kukreja, R.C. 2002. Alpha-adrenergic receptor stimulation produces late preconditioning through inducible nitric oxide synthase in mouse heart. J. Mol. Cell. Cardiol. 34:185-195.
57. Stewart, A.F., et al. 1994. Cloning of the rat alpha 1c-adrenergic receptor from cardiac myocytes. Alpha 1c, alpha 1b, and alpha 1d mRNAs are present in cardiac myocytes but not in cardiac fibroblasts. Circ. Res. 75:796-802.
58. Hanford, D.S., Thuerauf, D.J., Murray, S.F., and Glembotski, C.C. 1994. Brain natriuretic peptide is induced by alpha 1-adrenergic agonists as a primary response gene in cultured rat cardiac myocytes. J. Biol. Chem. 269:26227-26233.
59. Cao, L., and Gardner, D.G. 1995. Natriuretic peptides inhibit DNA synthesis in cardiac fibroblasts. Hypertension. 25:227-234.
60. Redondo, J., Bishop, J.E., and Wilkins, M.R. 1998. Effect of atrial natriuretic peptide and cyclic GMP phosphodiesterase inhibition on collagen synthesis by adult cardiac fibroblasts. Br. J. Pharmacol. 124:1455-1462.
61. Calderone, A., Thaik, C.M., Takahashi, N., Chang, D.L., and Colucci, W.S. 1998. Nitric oxide, atrial natriuretic peptide, and cyclic GMP inhibit the growth-promoting effects of norepinephrine in cardiac myocytes and fibroblasts. J. Clin. Invest. 101:812-818.
62. Tamura, N., et al. 2000. Cardiac fibrosis in mice lacking brain natriuretic peptide. Proc. Natl. Acad. Sci. U. S. A. 97:4239-4244.
63. Kuwano, K., Hagimoto, N., and Nakanishi, Y. 2004. The role of apoptosis in pulmonary fibrosis. Histol. Histopathol. 19:867-881.
64. Canbay, A., Friedman, S., and Gores, G.J. 2004. Apoptosis: the nexus of liver injury and fibrosis. Hepatology. 39:273-278.
65. Lohse, M.J., Engelhardt, S., and Eschenhagen, T. 2003. What is the role of beta-adrenergic signaling in heart failure? Circ. Res. 93:896-906.
66. Perrino, C., et al. 2005. Restoration of beta-adrenergic receptor signaling and contractile function in heart failure by disruption of the betaark1/ phosphoinositide 3-kinase complex. Circulation. 111:2579-2587.
67. Rokosh, D.G., and Simpson, P.C. 2002. Knockout of the alpha 1a/c-adrenergic receptor subtype: the alpha 1a/c is expressed in resistance arteries and is required to maintain arterial blood pressure. Proc. Natl. Acad. Sci. U. S. A. 99:9474-9479.
68. Hakuno, D., et al. 2002. Bone marrow-derived regenerated cardiomyocytes (CMG cells) express functional adrenergic and muscarinic receptors. Circulation. 105:380-386.
69. Shioi, T., et al. 2000. The conserved phosphoinositide 3-kinase pathway determines heart size in mice. EMBO J. 19:2537-2548.
70. Belke, D.D., et al. 2002. Insulin signaling coordinately regulates cardiac size, metabolism, and contractile protein isoform expression. J. Clin. Invest. 109:629-639. doi:10.1172/JCI200213946.
71. Crackower, M.A., et al. 2002. Regulation of myocardial contractility and cell size by distinct PI3K-PTEN signaling pathways. Cell. 110:737-749.
72. McMullen, J.R., et al. 2003. Phosphoinositide 3-kinase(p110alpha) plays a critical role for the induction of physiological, but not pathological, cardiac hypertrophy. Proc. Natl. Acad. Sci. U. S. A. 100:12355-12360.
73. Hu, P., et al. 2003. Minimally invasive aortic banding in mice: effects of altered cardiomyocyte insulin signaling during pressure overload. Am. J. Physiol. Heart Circ. Physiol. 285:H1261-H1269.
74. Aries, A., Paradis, P., Lefebvre, C., Schwartz, R.J., and Nemer, M. 2004. Essential role of gata-4 in cell survival and drug-induced cardiotoxicity. Proc. Natl. Acad. Sci. U. S. A. 101:6975-6980.
75. Bernstein, D., et al. 2005. Differential cardioprotective/ cardiotoxic effects mediated by beta-adrenergic receptor subtypes. Am. J. Physiol. Heart Circ. Physiol. 289:H2441-H2449.
76. Ishizaka, S., et al. 2004. New technique for measurement of left ventricular pressure in conscious mice. Am. J. Physiol. Heart Circ. Physiol. 286:H1208-H1215.
77. Deng, X.F., Rokosh, D.G., and Simpson, P.C. 2000. Autonomous and growth factor-induced hypertrophy in cultured neonatal mouse cardiac myocytes. Comparison with rat. Circ. Res. 87:781-788.
78. O'Connell, T.D., Rodrigo, M.C., and Simpson, P.C. 2006. Isolation and culture of adult mouse cardiac myocytes. In Cardiovascular proteomics: methods and protocols. F. Vivanco, editor. Humana Press. Totowa, New Jersey, USA. In press.
79. Rokosh, D.G., et al. 1996. Alpha1-adrenergic receptor subtype mRNAs are differentially regulated by alpha1-adrenergic and other hypertrophic stimuli in cardiac myocytes in culture and in vivo. Repression of alpha1b and alpha1d but induction of alpha1c. J. Biol. Chem. 271:5839-5843.
80. Rohrer, D.K., et al. 1996. Targeted disruption of the mouse beta1-adrenergic receptor gene: developmental and cardiovascular effects. Proc. Natl. Acad. Sci. U. S. A. 93:7375-7380.
81. Rybin, V.O., Xu, X., Lisanti, M.P., and Steinberg, S.F. 2000. Differential targeting of beta-adrenergic receptor subtypes and adenylyl cyclase to cardiomyocyte caveolae. A mechanism to functionally regulate the camp signaling pathway. J. Biol. Chem. 275:41447-41457.
82. Oudit, G.Y., et al. 2003. Phosphoinositide 3-kinase gamma-deficient mice are protected from isoproterenol-induced heart failure. Circulation. 108:2147-2152.
83. Turnbull, L., McCloskey, D.T., O'Connell, T.D., Simpson, P.C., and Baker, A.J. 2003. Alpha 1-adrenergic receptor responses in alpha 1AB-AR knockout mouse hearts suggest the presence of alpha 1D-AR. Am. J. Physiol. Heart Circ. Physiol. 284:H1104-H1109.
84. Rocha, B.A., et al. 2002. Enhanced locomotor, reinforcing, and neurochemical effects of cocaine in serotonin 5-hydroxytryptamine 2c receptor mutant mice. J. Neurosci. 22:10039-10045.
85. Youn, H.J., et al. 1999. Two-dimensional echocardiography with a 15-MHz transducer is a promising alternative for in vivo measurement of left ventricular mass in mice. J. Am. Soc. Echocardiogr. 12:70-75.
86. Liao, Y., et al. 2002. Echocardiographic assessment of LV hypertrophy and function in aortic-banded mice: necropsy validation. Am. J. Physiol. Heart Circ. Physiol. 282:H1703-H1708.