The switching role of i 2-adrenergic receptor signalling in cell survival or death decision of cardiomyocytes

Nature Communications

Volumn 5, Issue , 2014, Pages

  Shin, Sung Young ^a   Kim, Taeyong ^b   Lee, Ho Sung ^a   Kang, Jun Hyuk ^a   Lee, Ji Young ^b   Cho, Kwang Hyun ^a   Kim, Do Han ^b  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Gwangju Institute of Science and Technology (GIST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

3 ISOPROPYLAMINO 1 (7 METHYL 4 INDANYLOXY) 2 BUTANOL; BETA ADRENERGIC RECEPTOR; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; ISOPRENALINE; METOPROLOL; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHODIESTERASE III; PHOSPHOLAMBAN; PROTEIN BCL 2; BETA 1 ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR STIMULATING AGENT; CREM PROTEIN, RAT; CYCLIC AMP RESPONSIVE ELEMENT MODULATOR; MITOGEN ACTIVATED PROTEIN KINASE 3;

BIOCHEMISTRY; CARDIOLOGY; CARDIOVASCULAR DISEASE; DISEASE TREATMENT; GENE EXPRESSION; NUMERICAL MODEL;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BETA ADRENERGIC STIMULATION; CELL DEATH; CELL FATE; CELL SURVIVAL; CHEMICAL ANALYSIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FEEDBACK SYSTEM; GENE EXPRESSION; GENE SWITCHING; HEART MUSCLE CELL; MALE; MATHEMATICAL ANALYSIS; NONHUMAN; PROTEIN INTERACTION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SURVIVAL RATE; SYSTEM ANALYSIS; THERAPY EFFECT; ANIMAL; BIOLOGICAL MODEL; COMPUTER SIMULATION; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HEART VENTRICLE; METABOLISM; PRIMARY CELL CULTURE; SPRAGUE DAWLEY RAT;

ADRENERGIC BETA-AGONISTS; ANIMALS; CELL DEATH; CELL SURVIVAL; COMPUTER SIMULATION; CYCLIC AMP RESPONSE ELEMENT MODULATOR; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; HEART VENTRICLES; ISOPROTERENOL; MALE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MODELS, CARDIOVASCULAR; MYOCYTES, CARDIAC; PRIMARY CELL CULTURE; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, BETA-1; RECEPTORS, ADRENERGIC, BETA-2; SIGNAL TRANSDUCTION;

EID: 84922718714     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6777     Document Type: Article

References (68)

1. Sasagawa, S., Ozaki, Y., Fujita, K. & Kuroda, S. Prediction and validation of the distinct dynamics of transient and sustained ERK activation. Nat. Cell Biol. 7, 365-373 (2005).
2. Chen, J. Y., Lin, J. R., Cimprich, K. A. & Meyer, T. A two-dimensional ERK-AKT signaling code for an NGF-triggered cell-fate decision. Mol. Cell 45, 196-209 (2012).
3. von Kriegsheim, A. et al. Cell fate decisions are specified by the dynamic ERK interactome. Nat. Cell Biol. 11, 1458-1464 (2009).
4. Santos, S. D., Verveer, P. J. & Bastiaens, P. I. Growth factor-induced MAPK network topology shapes Erk response determining PC-12 cell fate. Nat. Cell Biol. 9, 324-330 (2007).
5. Nakakuki, T. et al. Ligand-specific c-Fos expression emerges from the spatiotemporal control of ErbB network dynamics. Cell 141, 884-896 (2010).
6. Hasking, G. J. et al. Norepinephrine spillover to plasma in patients with congestive heart failure: evidence of increased overall and cardiorenal sympathetic nervous activity. Circulation 73, 615-621 (1986).
7. Regitz-Zagrosek, V., Hertrampf, R., Steffen, C., Hildebrandt, A. & Fleck, E. Myocardial cyclic AMP and norepinephrine content in human heart failure. Eur. Heart J. 15 (Suppl D), 7-13 (1994).
8. Manolis, A. J. et al. Suppressing sympathetic activation in congestive heart failure. A new therapeutic strategy. Hypertension 26, 719-724 (1995).
9. Venugopalan, P. & Agarwal, A. K. Plasma catecholamine levels parallel severity of heart failure and have prognostic value in children with dilated cardiomyopathy. Eur. J. Heart Fail. 5, 655-658 (2003).
10. Tomita, H. et al. Inducible cAMP early repressor (ICER) is a negative-feedback regulator of cardiac hypertrophy and an important mediator of cardiac myocyte apoptosis in response to beta-adrenergic receptor stimulation. Circ. Res. 93, 12-22 (2003).
11. Nakayama, H. et al. Ca2-and mitochondrial-dependent cardiomyocyte necrosis as a primary mediator of heart failure. J. Clin. Invest. 117, 2431-2444 (2007).
12. Communal, C., Singh, K., Pimentel, D. R. & Colucci, W. S. Norepinephrine stimulates apoptosis in adult rat ventricular myocytes by activation of the betaadrenergic pathway. Circulation 98, 1329-1334 (1998).
13. Communal, C., Singh, K., Sawyer, D. B. & Colucci, W. S. Opposing effects of beta(1)-and beta(2)-adrenergic receptors on cardiac myocyte apoptosis: role of a pertussis toxin-sensitive G protein. Circulation 100, 2210-2212 (1999).
14. Chesley, A. et al. The beta(2)-adrenergic receptor delivers an antiapoptotic signal to cardiac myocytes through G(i)-dependent coupling to phosphatidylinositol 3'-kinase. Circ. Res. 87, 1172-1179 (2000).
15. Zhu, W. Z. et al. Dual modulation of cell survival and cell death by beta(2)-adrenergic signaling in adult mouse cardiac myocytes. Proc. Natl Acad. Sci. USA 98, 1607-1612 (2001).
16. Engelhardt, S., Hein, L., Wiesmann, F. & Lohse, M. J. Progressive hypertrophy and heart failure in beta1-adrenergic receptor transgenic mice. Proc. Natl Acad. Sci. USA 96, 7059-7064 (1999).
17. Homburger, V., Lucas, M., Rosenbaum, E., Vassent, G. & Bockaert, J. Presence of both beta1-and beta2-adrenergic receptors in a single cell type. Mol. Pharmacol. 20, 463-469 (1981).
18. Hall, R. A. Beta-adrenergic receptors and their interacting proteins. Semin. Cell Dev. Biol. 15, 281-288 (2004).
19. Saucerman, J. J., Brunton, L. L., Michailova, A. P. & McCulloch, A. D. Modeling beta-adrenergic control of cardiac myocyte contractility in silico. J. Biol. Chem. 278, 47997-48003 (2003).
20. Himeno, Y., Sarai, N., Matsuoka, S. & Noma, A. Ionic mechanisms underlying the positive chronotropy induced by beta1-adrenergic stimulation in guinea pig sinoatrial node cells: a simulation study. J. Physiol. Sci. 58, 53-65 (2008).
21. Kuzumoto, M. et al. Simulation analysis of intracellular Na and Clhomeostasis during beta 1-adrenergic stimulation of cardiac myocyte. Prog. Biophys. Mol. Biol. 96, 171-186 (2008).
22. Saucerman, J. J. et al. Systems analysis of PKA-mediated phosphorylation gradients in live cardiac myocytes. Proc. Natl Acad. Sci. USA 103, 12923-12928 (2006).
23. Song, H. K., Hong, S. E., Kim, T. & Kim, D. H. Deep RNA sequencing reveals novel cardiac transcriptomic signatures for physiological and pathological hypertrophy. PLoS ONE 7, e35552 (2012).
24. Henaff, M., Hatem, S. N. & Mercadier, J. J. Low catecholamine concentrations protect adult rat ventricular myocytes against apoptosis through cAMPdependent extracellular signal-regulated kinase activation. Mol. Pharmacol. 58, 1546-1553 (2000).
25. De Arcangelis, V., Liu, S., Zhang, D., Soto, D. & Xiang, Y. K. Equilibrium between adenylyl cyclase and phosphodiesterase patterns adrenergic agonist dose-dependent spatiotemporal cAMP/protein kinase A activities in cardiomyocytes. Mol. Pharmacol. 78, 340-349 (2010).
26. Kluck, R. M., Bossy-Wetzel, E., Green, D. R. & Newmeyer, D. D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275, 1132-1136 (1997).
27. Tsujimoto, Y., Shimizu, S., Eguchi, Y., Kamiike, W. & Matsuda, H. Bcl-2 and Bcl-xL block apoptosis as well as necrosis: possible involvement of common mediators in apoptotic and necrotic signal transduction pathways. Leukemia 11 (Suppl 3), 380-382 (1997).
28. Imahashi, K., Schneider, M. D., Steenbergen, C. & Murphy, E. Transgenic expression of Bcl-2 modulates energy metabolism, prevents cytosolic acidification during ischemia, and reduces ischemia/reperfusion injury. Circ. Res. 95, 734-741 (2004).
29. Maulik, N. et al. Ischemic preconditioning reduces apoptosis by upregulating anti-death gene Bcl-2. Circulation 100, II369-II375 (1999).
30. Pattingre, S. et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 122, 927-939 (2005).
31. Kang, P. M., Haunstetter, A., Aoki, H., Usheva, A. & Izumo, S. Morphological and molecular characterization of adult cardiomyocyte apoptosis during hypoxia and reoxygenation. Circ. Res. 87, 118-125 (2000).
32. Chatterjee, S. et al. Viral gene transfer of the antiapoptotic factor Bcl-2 protects against chronic postischemic heart failure. Circulation 106, I212-I217 (2002).
33. Chen, Z., Chua, C. C., Ho, Y. S., Hamdy, R. C. & Chua, B. H. Overexpression of Bcl-2 attenuates apoptosis and protects against myocardial I/R injury in transgenic mice. Am. J. Physiol. Heart Circ. Physiol. 280, H2313-H2320 (2001).
34. Ding, B. et al. Functional role of phosphodiesterase 3 in cardiomyocyte apoptosis: implication in heart failure. Circulation 111, 2469-2476 (2005).
35. Ding, B. et al. A positive feedback loop of phosphodiesterase 3 (PDE3) and inducible cAMP early repressor (ICER) leads to cardiomyocyte apoptosis. Proc. Natl Acad. Sci. USA 102, 14771-14776 (2005).
36. Maruyama, R. et al. Synchronous progression of calcium transient-dependent beating and sarcomere destruction in apoptotic adult cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 290, H1493-H1502 (2006).
37. Oltvai, Z. N., Milliman, C. L. & Korsmeyer, S. J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 74, 609-619 (1993).
38. Baldi, A. et al. Apoptosis and post-infarction left ventricular remodeling. J. Mol. Cell Cardiol. 34, 165-174 (2002).
39. Ma, W., Lai, L., Ouyang, Q. & Tang, C. Robustness and modular design of the Drosophila segment polarity network. Mol. Syst. Biol. 2, 70 (2006).
40. Yao, G., Tan, C., West, M., Nevins, J. R. & You, L. Origin of bistability underlying mammalian cell cycle entry. Mol. Syst. Biol. 7, 485 (2011).
41. Ohtsubo, H. et al. Inducible cAMP early repressor inhibits growth of vascular smooth muscle cell. Arterioscler. Thromb. Vasc. Biol. 27, 1549-1555 (2007).
42. Hjalmarson, A. et al. Effects of controlled-release metoprolol on total mortality, hospitalizations, and well-being in patients with heart failure: the Metoprolol CR/XL Randomized Intervention Trial in congestive heart failure (MERIT-HF). MERIT-HF Study Group. JAMA 283, 1295-1302 (2000).
43. Kawai, K. et al. Importance of antioxidant and antiapoptotic effects of betareceptor blockers in heart failure therapy. Am. J. Physiol. Heart Circ. Physiol. 287, H1003-H1012 (2004).
44. Sabbah, H. N. et al. Chronic therapy with metoprolol attenuates cardiomyocyte apoptosis in dogs with heart failure. J. Am. Coll. Cardiol. 36, 1698-1705 (2000).
45. Chin, B. S. et al. Anti-oxidative properties of beta-blockers and angiotensinconverting enzyme inhibitors in congestive heart failure. Eur. J. Heart Fail. 5, 171-174 (2003).
46. Kukin, M. L. et al. Prospective, randomized comparison of effect of long-term treatment with metoprolol or carvedilol on symptoms, exercise, ejection fraction, and oxidative stress in heart failure. Circulation 99, 2645-2651 (1999).
47. Laser, A. et al. Long-term beta-blocker treatment prevents chronic creatine kinase and lactate dehydrogenase system changes in rat hearts after myocardial infarction. J. Am. Coll. Cardiol. 27, 487-493 (1996).
48. Eichhorn, E. J. & Bristow, M. R. Medical therapy can improve the biological properties of the chronically failing heart. A new era in the treatment of heart failure. Circulation 94, 2285-2296 (1996).
49. George, I., Sabbah, H. N., Xu, K., Wang, N. & Wang, J. beta-adrenergic receptor blockade reduces endoplasmic reticulum stress and normalizes calcium handling in a coronary embolization model of heart failure in canines. Cardiovasc. Res. 91, 447-455 (2011).
50. Kim, D., Kwon, Y. K. & Cho, K. H. The biphasic behavior of incoherent feedforward loops in biomolecular regulatory networks. Bioessays 30, 1204-1211 (2008).
51. Shin, S. Y. et al. Functional roles of multiple feedback loops in extracellular signal-regulated kinase and Wnt signaling pathways that regulate epithelialmesenchymal transition. Cancer. Res. 70, 6715-6724 (2010).
52. Choi, M., Shi, J., Jung, S. H., Chen, X. & Cho, K. H. Attractor landscape analysis reveals feedback loops in the p53 network that control the cellular response to DNA damage. Sci. Signal 5, ra83 (2012).
53. Shizukuda, Y. & Buttrick, P. M. Subtype specific roles of beta-adrenergic receptors in apoptosis of adult rat ventricular myocytes. J. Mol. Cell Cardiol. 34, 823-831 (2002).
54. Zhu, W. Z. et al. Linkage of beta1-adrenergic stimulation to apoptotic heart cell death through protein kinase A-independent activation of Ca2/calmodulin kinase II. J. Clin. Invest. 111, 617-625 (2003).
55. ECC Committee SaTFotAHA. 2005 American Heart Association Guidelines for Cardiopulmonary Resuscitation and Emergency Cardiovascular Care. Circulation 112, IV1-203 (2005).
56. Ahmet, I. et al. Cardioprotective and survival benefits of long-term combined therapy with beta2 adrenoreceptor (AR) agonist and beta1 AR blocker in dilated cardiomyopathy postmyocardial infarction. J. Pharmacol. Exp. Ther. 325, 491-499 (2008).
57. Talan, M. I., Ahmet, I., Xiao, R. P. & Lakatta, E. G. beta(2) AR agonists in treatment of chronic heart failure: long path to translation. J. Mol. Cell. Cardiol. 51, 529-533 (2011).
58. Insel, P. A., Zhang, L., Murray, F., Yokouchi, H. & Zambon, A. C. Cyclic AMP is both a pro-apoptotic and anti-apoptotic second messenger. Acta Physiol. (Oxf) 204, 277-287 (2012).
59. Zhang, L. et al. Gene expression signatures of cAMP/protein kinase A (PKA)-promoted, mitochondrial-dependent apoptosis. Comparative analysis of wild-type and cAMP-deathless S49 lymphoma cells. J. Biol. Chem. 283, 4304-4313 (2008).
60. Shampine, L. F. & Reichelt, M. W. The MATLAB ODE suite. Siam. J. Sci. Comput. 18, 1-22 (1997).
61. Goldberg, D. E. Genetic Algorithms in Search, Optimization, and Machine Learning (Addison-Wesley Pub. Co., 1989).
62. Coleman, T. F., Branch, M. A. & Grace, A. MathWorks Inc. Optimization Toolbox for Use with MATLAB: User's Guide 2 edn. (MathWorks, Inc., 1999).
63. Kholodenko, B. N., Demin, O. V. & Westerhoff, H. V. Control analysis of periodic phenomena in biological systems. J. Phys. Chem. B 101, 2070-2081 (1997).
64. Marino, S., Hogue, I. B., Ray, C. J. & Kirschner, D. E. A methodology for performing global uncertainty and sensitivity analysis in systems biology. J. Theor. Biol. 254, 178-196 (2008).
65. Lebedeva, G. et al. Model-based global sensitivity analysis as applied to identification of anti-cancer drug targets and biomarkers of drug resistance in the ErbB2/3 network. Eur. J. Pharm. Sci. 46, 244-258 (2012).
66. Kwon, S. J. & Kim, D. H. Characterization of junctate-SERCA2a interaction in murine cardiomyocyte. Biochem. Biophys. Res. Commun. 390, 1389-1394 (2009).
67. Zou, Y. et al. Both Gs and Gi proteins are critically involved in isoproterenolinduced cardiomyocyte hypertrophy. J. Biol. Chem. 274, 9760-9770 (1999).
68. Erickson, J. R., Patel, R., Ferguson, A., Bossuyt, J. & Bers, D. M. Fluorescence resonance energy transfer-based sensor Camui provides new insight into mechanisms of calcium/calmodulin-dependent protein kinase II activation in intact cardiomyocytes. Circ. Res. 109, 729-738 (2011).