β-adrenergic receptor responsiveness in aging heart and clinical implications

Frontiers in Physiology

Volumn 4 JAN, Issue , 2014, Pages

  Ferrara, Nicola ^a,b   Komici, Klara ^a   Corbi, Graziamaria ^c   Pagano, Gennaro ^a   Furgi, Giuseppe ^b   Rengo, Carlo ^a,b   Femminella, Grazia D ^a   Leosco, Dario ^a   Bonaduce, Domenico ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b IRCCS   (Italy)

^c UNIVERSITY OF MOLISE   (Italy)

Author keywords

adrenergic receptors; adrenoceptor desensitization; adrenoceptor down regulation; Aging heart; Exercise; Failing heart; G protein coupled receptor kinase

Indexed keywords

EID: 84893597436     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2013.00396     Document Type: Review

References (91)

1. Abrass, I. B., and Scapace, P. J. (1981). Human lymphocytes β-adrenergic receptors are unaltered with age. J. Gerontol. 36, 298-301. doi: 10.1093/geronj/36.3.298.
2. Alquist, R. F. (1948). A study of the adrenotropic receptors. Am. J. Physiol. 153, 586-600.
3. 2-adrenergic stimulation. Circulation 92, 1612-1618. doi: 10.1161/01.CIR.92.6.1612.
4. iα-proteins in rat heart. Res. Pharmacol. 48, 479-486. doi: 10.1016/0006-2952(94)90277-1.
5. Benovic, J. L., Onorato, J. J., Arriza, J. L., Stone, W. C., Lohse, M., Jenkins, N. A., et al. (1991). Cloning, expression and chromosomal localization of β-adrenergic receptor kinase 2. J. Biol. Chem. 266, 14939-14946.
6. Bogoyevitch, M. A., Andersson, M. B., Gillespie-Brown, J., Clerck, A., Glennon, P. E., Fuller, S. J., et al. (1996). Adrenergic receptor stimulation of the mitogen-activated protein kinase cascade and cardiac hypertrophy. Biochem. J. 314, 115-121.
7. Bohm, M., Dorner, H., Htun, P., Lensche, H., Platt, D., and Erdmann, E. (1993). Effects of exercise on myocardial adenylatecyclase and Gi alpha expression in senescence. Am. J. Physiol. 264, H805-H814.
8. 2-adrenoceptors in sheep cardiac ventricular muscle. J. Mol. Cell. Cardiol. 24, 753-763. doi: 10.1016/0022-2828(92)93389-2.
9. Boyle, A. J., Shih, H., Hwang, J., Ye, J., Lee, B., Zhang, Y., et al. (2011). Cardiomyopathy of aging in the mammalian heart is characterized by myocardial hypertrophy, fibrosis and a predisposition towards cardiomyocyte apoptosis and autophagy. Exp. Gerontol. 46, 549-559. doi: 10.1016/j.exger.2011.02.010.
10. Bristow, M. R., Ginsburg, R., Minobe, W., Cubicciotti, R. S., Sageman, W. S., Lurie, K., et al. (1982). Decreased catecholamine sensitivity and β-adrenergic-receptor density in failing human hearts. N. Engl. J. Med. 307, 205-211. doi: 10.1056/NEJM198207223070401.
11. 1-receptor downregulation in heart failure. Circ. Res. 59, 297-309. doi: 10.1161/01.RES.59.3.297.
12. 2-adrenoceptor function related to the degree of heart failure in patients with mitral valve disease. J. Am. Coll. Cardiol. 14, 323-331. doi: 10.1016/0735-1097(89)90181-2.
13. Buxton, L. O., and Bruton, L. L. (1985). Direct analyses of β-adrenergic receptor subtype in intact adult ventricular myocytes of the rats. Circ. Res. 56, 126-132. doi: 10.1161/01.RES.56.1.126.
14. Cacciatore, F., Gallo, C., Ferrara, N., Abete, P., Paolisso, G., Canonico, S., et al. (1998). Morbidity patterns in aged population in southern Italy. A survey sampling. Arch. Gerontol. Geriatr. 26, 201-213. doi: 10.1016/S0167-4943(98)00003-X.
15. Cannavo, A., Rengo, G., Liccardo, D., Pironti, G., Scimia, M. C., Scudiero, L., et al. (2013). Prothymosin alpha protects cardiomyocytes againts ischemia-induced apoptosis via presentation of Act activation. Apoptosis. 18, 1252-1261. doi: 10.1007/s10495-013-0876-9.
16. Cerbai, E., Varani, K., Barbieri, M., Borea, P. A., and Mugelli, A. (1995). β-adrenoreceptor subtypes in young and old rat ventricular myocytes. A combined patch-clamp and binding study. Br. J. Pharmacol. 116, 1835-1842. doi: 10.1111/j.1476-5381.1995.tb16671.x.
17. Cohn, J. N., Levine, T. B., Olivari, M. T., Garberg, V., Lura, D., and Francis, G. S., et al. (1984). Plasma norepinephrine as a guide to prognosis in patients with chronic congestive heart failure. N. Engl. J. Med. 311, 819-823. doi: 10.1056/NEJM198409273111303.
18. Corbi, G., Acanfora, D., Iannuzzi, G. L., Longobardi, G., Cacciatore, F., Furgi, G., et al. (2008). Hypermagnesemia predicts mortality in elderly with congestive heart disease: relationship with laxative and antacid use. Rejuvenat. Res. 11, 129-138. doi: 10.1089/rej.2007.0583.
19. Corbi, G., Conti, V., Russomanno, G., Longobardi, G., Furgi, G., Filippelli, A., et al. (2013a). Adrenergic signaling and oxidative stress: a role of sirtuins? Front. Physiol. 4:324. doi: 10.3389/fphys.2013.00324.
20. Corbi, G., Bianoc, A., Turchiarelli, V., Cellurale, M., Fatica, F., Daniele, A., et al. (2013b). Potential mechanisms linking atherosclerosis and increased cardiovascular risk in COPD: focus on sirtuins. Int. J. Mol. Sci. 14, 12696-12713. doi: 10.3390/ijms140612696.
21. Corbi, G., Conti, V., Russomanno, G., Rengo, G., Vitulli, P., Ciccarelli, A. L., et al. (2012a). Is physical activity able to modify oxidative damage in cardiovascular aging? Oxid. Med. Cell. Longev. 2012, 728547. doi: 10.1155/2012/728547.
22. Corbi, G., Conti, V., Scapagnini, G., Filippelli, A., and Ferrara, N. (2012b). Role of sirtuins, calorie restriction and physical activity in aging. Front. Biosci. (Elite. Ed). 4:417. doi: 10.2741/417.
23. Corbi, G. M., Carbone, S., Ziccardi, P., Giugliano, G., Marfella, R., Nappo, F., et al. (2002). FFAs and QT intervals in obese women with visceral adiposity: effects of sustained weight loss over 1 year. J. Clin. Endocrinol. Metab. 87, 2080-2083. doi: 10.1210/jc.87.5.2080.
24. Davies, C. H., Ferrara, N., and Harding, S. E. (1996). β-Adrenoceptor function changes with age of subject in myocytes from non-failing human ventricle. Cardiovasc. Res. 31, 152-156. doi: 10.1016/0008-6363(95)00187-5.
25. Dobson, J. G., Fenton, R. A., and Romano, F. D. (1990). Increased myocardial adenosine production and reduction of β-adrenergic contractile response in aged hearts. Cir. Res. 66, 1381-1390. doi: 10.1161/01.RES.66.5.1381.
26. Ehsani, A. A. (1987). Cardiovascular adaptations to exercise training in the elderly. Fed. Proc. 46, 1840-1843.
27. Enns, L. C., Morton, J. F., Treuting, P. R., Edmond, M. J., Wolf, N. S., Dai, D. F., et al. (2009). Disruption of protein kinase A in mice enhances healthy aging. PLoS ONE 4:e5963. doi: 10.1371/journal.pone.0005963.
28. Esler, M. D., Turner, A. G., Kaye, A. G., Thompson, J. M., Kingwell, B. A., Morris, M., et al. (1995). Aging effects on human sympathetic neuronal function. Am. J. Physiol. 268(1 Pt), R278-R285.
29. Feldman, A. M., Cates, A. E., Veazey, W. B., Hershberger, R. E., Bristow, M. R., Baughman, K. L., et al. (1988). Increase of the 40,000-mol wt pertussis toxin substrate (G protein) in the failing human heart. J. Clin. Invest. 82, 189-197. doi: 10.1172/JCI113569.
30. Ferrara, N., Abete, P., Corbi, G., Paolisso, G., Longobardi, G., Calabrese, C., et al. (2005). Insulin-induced changes in β-adrenergic response: an experimental study in the isolated rat papillary muscle. Am. J. Hypertens. 18, 348-353. doi: 10.1016/j.amjhyper.2004.10.006.
31. Ferrara, N., Bohm, M., Zolk, O., O'Gara, P., and Harding, S. E. (1997a). The role of Gi-proteins and β-adrenoceptors in the age-related decline of contraction in guinea-pig ventricular myocytes. J. Mol. Cell. Cardiol. 29, 439-448. doi: 10.1006/jmcc.1996.0397.
32. Ferrara, N., Davia, K., Abete, P., Rengo, F., and Harding, S. E. (1997b). Alterations in β-adrenoceptor mechanisms in the aging heart. Relationship with heart failure. Aging (Milano). 9, 391-403.
33. Ferrara, N., Corbi, G., Bosimini, E., Cobelli, F., Furgi, G., Giannuzzi, P., et al. (2006). Cardiac rehabilitation in the elderly: patient selection and outcomes. Am. J. Geriatr. Cardiol. 15, 22-27. doi: 10.1111/j.1076-7460.2006.05289.x.
34. Ferrara, N., O'Gara, P., Wynne, D. G., Brown, L. A., del Monte, F., Poole-Wilson, P. A., et al. (1995). Decreased contractile responses to isoproterenol in isolated cardiac myocytes from aging guinea-pigs. J. Mol. Cell. Cardiol. 27, 1141-1150. doi: 10.1016/0022-2828(95)90050-0.
35. Fleg, J. L., Schulman, S., O'Connor, F., Becker, L. C., Gerstenblith, G., Clulow, J. F., et al. (1994). Effects of acute β-adrenergic receptor blockade on age associated changes in cardiovascular performance during dynamic exercise. Circulation 90, 2333-2341. doi: 10.1161/01.CIR.90.5.2333.
36. Folkow, B., and Svanborg, A. (1993). Physiology of cardiovascular aging. Physiol. Rev. 73, 725-764.
37. 1-adrenergic receptor: involvement of G protein coupled receptor kinase and cAMP dependent protein kinase. J. Biol. Chem. 270, 17953-17961.
38. Froehlich, J. P., Lakatta, E. G., Beard, E., Spurgeon, H. A., Weisfeldt, M. L., and Gerstenbilth, G. (1978). Studies of sarcoplasmic reticulum function and contraction duration in young and aged rat myocardium. J. Mol. Cell. Cardiol. 10, 427-438. doi: 10.1016/0022-2828(78)90364-4.
39. Fu, L. X., Liang, Q. M., Waagstein, F., Hoebeke, J., Sylvén, C., Jansson, E., et al. (1992). Increase in functional activity rather than in amount of Gi-alpha in failing human heart with dilated cardiomyopathy. Cardiovasc. Res. 26, 950-955. doi: 10.1093/cvr/26.10.950.
40. 2+ channels in rat hearts. Am. J. Physiol. 260(1 Pt 2), H66-H72.
41. + exchange. Nature 392, 626-630. doi:10.1038/33458.
42. 1 inhibition prolongs survival and augments β-blocker therapy in a mouse model of severe heart failure. Proc. Natl. Acad. Sci. U.S.A. 98, 5809-5814. doi: 10.1073/pnas.091102398.
43. Hess, P. S., Fleg, J., Lakatta, E. G., and Shapiro, E. P. (2002). Left ventricular remodeling with age in normal men versus women: novel insights using three-dimensional magnetic resonance imaging. Am. J. Cardiol. 90, 1231-1236. doi: 10.1016/S0002-9149(02)02840-0.
44. Ho, K. K., Pinsky, J. L., Kannel, W. B., and Levy, D. (1993). The epidemiology of heart failure: the Framingham study. J. Am. Coll. Cardiol. 22(4 Suppl. A), 6A-13A. doi: 10.1016/0735-1097(93)90455-A.
45. 2 expression and activity in human heart failure. Eur. Heart J. 17, 1752-1758. doi: 10.1093/eurheartj/ehi429.
46. Jiang, M. T., Moffat, M. P., and Narayanan, N. (1993). Age-related alterations in the phosphorylation of sarcoplasmic reticulum and myofibrillar proteins and diminished contractile response to isoproterenol in intact rat ventricle. Circ. Res. 72, 102-111. doi: 10.1161/01.RES.72.1.102.
47. Khouri, M. G., Maurer, M. S., and El-Khoury Rumbarger, L. (2005). Assessment of age-related changes in left ventricular structure by freehand three-dimensional echocardiography. Am. J. Geriatr. Cardiol. 14, 118-125. doi: 10.1111/j.1076-7460.2005.03845.x.
48. 2-Adrenergic cAMP signaling is uncoupled from phosphorylation of cytoplasmic proteins in canine heart. Circulation. 99, 2458-2465. doi: 10.1161/01.CIR.99.18.2458.
49. Lakatta, E. G., and Levy, D. (2003). Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises: part II: the aging heart in health: links to heart disease. Circulation 107, 346-354. doi: 10.1161/01.CIR.0000048893.62841.F7.
50. 2-adrenergic receptors in mononuclear leucocytes: similar density in young and old normal subjects. Life Sci. 29, 1761-1771. doi: 10.1016/0024-3205(81)90186-7.
51. Leineweber, K., Wangemann, T., Giessler, C., Bruck, H., Dhein, S., Kostelka, M., et al. (2002). Age-dependent changes of cardiac neuronal noradrenaline reuptake transporter (uptake1) in human heart. Am. Coll. Cardiol. 40, 1459-1465. doi: 10.1016/S0735-1097(02)02168-X.
52. Leinweber, K., Klapproth, S., Beilfuss, A., Silber, R. E., Heusch, G., Philipp, T., et al. (2003). Unchanged G-protein-coupled receptor kinase activity in the aging human heart. J. Am. Col. Cardiol. 42, 1487-1492. doi: 10.1016/S0735-1097(03)01063-5.
53. 2-adrenoceptor-mediated functions in feline heart: a β-adrenoceptormediated positive inotropic effect possibly unrelated to cyclic AMP. Naunyn Schmiedebergs. Arch. Pharmacol. 344, 56-59.
54. Leosco, D., Iaccarino, G., Cipolletta, E., De Santis, D., Pisani, E., Trimarco, V., et al. (2003). Exercise restores β-adrenergic vasorelaxation in aged rat carotid arteries. Am. J. Physiol. Heart. Circ. Physiol. 285, 369-374. doi: 10.1152/ajpheart.00019.2003.
55. Leosco, D., Rengo, G., Iaccarino, G., Filippelli, A., Lymperopoulos, A., Zincarelli, C., et al. (2007). Exercise training and β-blocker treatment ameliorate age-dependent impairment of β-adrenergic receptor signaling and enhance cardiac responsiveness to adrenergic stimulation. Am. J. Physiol. Heart Circ. 293, H1596-H1603. doi: 10.1152/ajpheart.00308.2007.
56. 4-adrenoceptor pharmacology. Br. J. Pharmacol. 141, 813-824. doi: 10.1038/sj.bjp.0705668.
57. Lin, J., Lopez, E. F., Jin, Y., Van Remmen, H., Bauch, T., Han, H. C., et al. (2008). Age-related cardiac muscle sarcopenia: combining experimental and mathematical modeling to identify mechanisms. Exp. Gerontol. 43, 296-306. doi: 10.1016/j.exger.2007.12.005.
58. Lonardo, G., Cerbai, E., Casini, S., Giunti, G., Bonacchi, M., Battaglia, F., et al. (2005). Pharmacological modulation of the hyperpolarization-activated current (I f) in human atrial myocytes: focus on G protein-coupled receptors. J. Mol. Cell. Cardiol. 38, 453-460. doi: 10.1016/j.yjmcc.2004.12.010.
59. 2 mediates sympathetic overdrive in heart failure. Nat. Med. 13, 315-323. doi: 10.1038/nm1553.
60. Marshall, C. J. (1995). Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179-185. doi: 10.1016/0092-8674(95)90401-8.
61. McConnachie, G., Langeberg, L. K., and Scott, J. D. (2006). AKAP signaling complexes: getting to the heart of the matter. Trends Mol. Med. 12, 317-323. doi: 10.1016/j.molmed.2006.05.008.
62. Morisco, C., Zebrowski, D., Condorelli, G., Tsichlis, P., Vatner, S. F., and Sadoshima, J. (2000). The Akt-glycogen synthase kinase 3β pathway regulates transcription of atrial natriuretic factor induced by β-adrenergic receptor stimulation in cardiac myocytes. J. Biol. Chem. 275, 14466-14475. doi: 10.1074/jbc.275.19.14466.
63. Ng, A. V., Callister, D. G., Johnson, D. G., and Seals, D. R. (1993). Age and gender influence muscle sympathetic nerve activity at rest in healthy humans. Hypertension. 21, 498-503. doi: 10.1161/01.HYP.21.4.498.
64. Olivetti, G., Melissari, M., Capasso, J. M., and Anversa, P. (1991). Cadiomyopathy of aging human heart. Myocyte loss reactive cellular hypertrophy. Circ. Res. 68, 1560-1568. doi: 10.1161/01.RES.68.6.1560.
65. Ping, P., Anzai, T., Gao, M., and Hammond, H. K. (1997). Adenyl cyclase and G protein receptor kinase expression during development of heart failure. Am. J. Physiol. 273(2 Pt 2), H707-H717.
66. 2+/calmodulin-dependent protein kinase regulates atrial natriuretic factor gene expression in ventricular myocytes. J. Biol. Chem. 272, 31203-31208. doi: 10.1074/jbc.272.49.31203.
67. 2) after exercise training predicts survival in patients with heart failure. Eur. J. Prev. Cardiol. 21, 4-11. doi: 10.1177/2047487313491656.
68. Rengo, G., Perrone-Filardi, P., Femminella, G. D., Liccardo, D., Zincarelli, C., de Lucia, C., et al. (2012a). Targeting the β-adrenergic receptor system through G-protein coupled receptor kinase 2: a new paradigm from therapy and prognostic evaluation in heart failure: from bench to bedside. Circ. Heart Fail. 5, 358-391. doi: 10.1161/CIRCHEARTFAILURE.112.966895.
69. 2-mediated adrenal a2-adrenoceptor-catecholamine production axis in heart failure. Br. J. Pharmacol. 166, 2430-2440. doi: 10.1111/j.1476-5381.2012.01972.x.
70. 2-adrenoceptor gene delivery promotes coordinated cardiac adaptive remodelling and angiogenesis in heart failure. Br. J. Pharmacol. 166, 2348-2361. doi: 10.1111/j.1476-5381.2012.01954.x.
71. Rinaldi, B., Corbi, G., Boccuti, S., Filippelli, W., Rengo, G., Leosco, D., et al. (2006). Exercise training affects age-induced changes in SOD and heat shock protein expression in rat heart. Exp. Gerontol. 41, 764-770. doi: 10.1016/j.exger.2006.05.008.
72. Rockman, H. A., Koch, W. J., and Lefkowitz, R. J. (2002). Seven-transmembrane-spanning receptors and heart function. Nature 415, 206-212. doi: 10.1038/415206a.
73. Rockman, H. A., Koch, W. J., Milano C. A., and Lefkowitz, R. J. (1996). Myocardial β-adrenergic receptor signaling "in vivo": insights from transgenic mice. J. Mol. Med. (Berl.) 74, 489-495. doi: 10.1007/BF00204974.
74. Roger, V. L., Go, A. S., Lloyd-Jones, D. M., Benjamin, E. J., Berry, J. D., Borden, W. B., et al. (2011). Executive summary: heart disease and stroke statistics-2011 update: a report from the american heart association. Circulation 123, 459-463. doi: 10.1161/CIR.0b013e3182009701.
75. Scarpace, P. J., Shu, Y., and Tumer, N. (1994). Influence of exercise training on myocardial-adrenergic signal transduction: differential regulation with age. J. Appl. Physiol. 77, 737-741.
76. Scholtz, D. G., Kitzman, D. W., Hagen, P. T., Ilstrup, D. M., and Edwards, W. D. (1988). Age-related changes in normal human hearts during the first 10 decades of life. Part I (Growth): a quantitative anatomic study of 200 specimens from subjects from birth to 19 years old. Mayo Clin. Proc. 63, 126-136. doi: 10.1016/S0025-6196(12)64945-3.
77. Schutzer, W. E., Reed, J. F., Bliziotes, M., and Mader, S. L. (2001). Up-regulation of G protein-linked receptor kinases with advancing age in rat aorta. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280, R897-R903.
78. Shioi, T., and Inuzuka, Y. (2012). Aging as a substrate of heart failure. J. Cardiol. 60, 423-428. doi: 10.1016/j.jjcc.2012.07.015.
79. Spindler, M. J., Burmeister, B. T., Huang, Y., Hsiao, E. C., Salomonis, N., Scott, M. J., et al. (2013). AKAP13 Rho-GEF and PKD-binding domain deficient mice develop normally but have an abnormal response to β-adrenergic-induced cardiac hypertrophy. PLoS ONE 8:e62705. doi: 10.1371/journal.pone.0062705.
80. 1-adrenergic receptor CaM kinase II-dependent pathway mediates cardiac myocyte fetal gene induction. Am. J. Physiol. Heart Circ. Physiol. 291, H1299-H1308. doi:10.1152/ajpheart.00017.2006.
81. 1-adrenergic receptors in failing human heart. Circulation 87, 454-463. doi: 10.1161/01.CIR.87.2.454.
82. Van Biesen, T., Hawes, B. E., Luttrell, D. K., Krueger, K. M., Touhara, K., Porfiri, E., et al. (1995). Receptor-tyrosine-kinase-and G β gamma-mediated MAP kinase activation by a common signaling pathway. Nature. 376, 781-784. doi: 10.1038/376781a0.
83. Vinge, L. E., Øie, E., Andersson, Y., Grøgaard, H. K., Andersen, G., and Attramadal, H. (2001). Myocardial dystribution and regulation of GRK and arrestin isoforms in congestive heart failure in rats. Am. J. Physiol. 281, H2490-H2499.
84. Wang, J., Yang, H., Hu, X., Fu, W., Xie, J., Zhou, X., et al. (2013). Dobutamine-mediated heme oxygenase-1 induction via PI3K and p38 MAPK inhibits high mobility group box 1 protein release and attenuates rat myocardial ischemia/reperfusion injury in vivo. J. Surg. Res. 183, 509-516. doi: 10.1016/j.jss.2013.02.051.
85. White, M., Roden, R., Minobe, W., Khan, M. F., Larrabee, P., Wollmering, M., et al. (1994). Age-related changes in β-adrenergic neuroeffectors system in the human heart. Circulation 90, 1225-1238. doi: 10.1161/01.CIR.90.3.1225.
86. 2-Adrenergic Signal Transduction Circ. Res. 85, 1092-1100. doi: 10.1161/01.RES.85.11.1092.
87. 2+ dynamics, contractility or phospholamban phosphorylation. J. Biol. Chem. 269, 19151-19156.
88. 2-adrenoceptor to a pertussis toxin-sensitive G protein in cardiac myocytes. Mol. Pharmacol. 47, 322-329.
89. 2-adrenergic responses without changes in inhibitory G proteins or receptor kinases. J. Clin. Invest. 101, 1273-1282. doi: 10.1172/JCI1335.
90. Young, J. B., and Landsberg, L. (1998). "Ch. 17. Catecholamines and the adrenal medulla," in Williams Textbook of Endocrinology, 9th Edn., eds J. D. Wilson, D. W. Foster, H. M. Kronenberg, and P. R. Larsen (Philadelphia, PA: W.B. Saunders), 665-728.
91. 2-adrenergic signaling in adult mouse cardiac myocytes. Proc. Natl. Acad. Sci. U.S.A. 98, 1607-1612. doi: 10.1073/pnas.98.4.1607.