Gβγ-independent recruitment of G-protein coupled receptor kinase 2 drives tumor necrosis factor α-induced cardiac β-adrenergic receptor dysfunction

Circulation

Volumn 128, Issue 4, 2013, Pages 377-387

  Vasudevan, Neelakantan T ^a   Mohan, Maradumane L ^a   Gupta, Manveen K ^a   Martelli, Elizabeth E ^a   Hussain, Afshan K ^a   Qin, Yilu ^a   Chandrasekharan, Unni M ^a   Young, David ^a   Feldman, Arthur M ^b   Sen, Subha ^a   Dorn, Gerald W ^c   Dicorleto, Paul E ^a   Prasad, Sathyamangla V Naga ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WASHINGTON UNIVERSITY   (United States)

Author keywords

adrenergic receptor; G protein coupled receptor kinase 2; heart failure; inflammation; phosphoinositide 3 kinase; tumor necrosis factor ; tumor necrosis factor receptor 2

Indexed keywords

ADENYLATE CYCLASE; BETA 2 ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR; CATECHOLAMINE; G PROTEIN COUPLED RECEPTOR KINASE 2; INTERLEUKIN 13; INTERLEUKIN 6; PHOSPHATIDYLINOSITOL 3 KINASE; RECOMBINANT SOMATOMEDIN C; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CATECHOLAMINE BLOOD LEVEL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ECHOCARDIOGRAPHY; ENDOSOME; ENZYME ACTIVITY; HEART DISEASE; HEART MUSCLE CELL; HEART MUSCLE CONTRACTILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; M MODE ECHOCARDIOGRAPHY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RECEPTOR DOWN REGULATION; UPREGULATION;

Β-ADRENERGIC RECEPTOR; G-PROTEIN COUPLED RECEPTOR KINASE 2; HEART FAILURE; INFLAMMATION; PHOSPHOINOSITIDE 3-KINASE; TUMOR NECROSIS FACTOR-Α; TUMOR NECROSIS FACTOR-Α RECEPTOR 2;

ADRENERGIC BETA-ANTAGONISTS; ANIMALS; DISEASE MODELS, ANIMAL; G-PROTEIN-COUPLED RECEPTOR KINASE 2; HEART FAILURE; HEK293 CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, TRANSGENIC; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROPRANOLOL; RECEPTORS, ADRENERGIC, BETA; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; SYMPATHETIC NERVOUS SYSTEM; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84880731037     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.113.003183     Document Type: Article

References (39)

1. Prabhu SD. Cytokine-induced modulation of cardiac function. Circ Res. 2004;95:1140-1153. (Pubitemid 39648205)
2. Amadou A, Nawrocki A, Best-Belpomme M, Pavoine C, Pecker F. Arachidonic acid mediates dual effect of TNF-alpha on Ca2+ transients and contraction of adult rat cardiomyocytes. Am J Physiol Cell Physiol. 2002;282:C1339-C1347. (Pubitemid 34663083)
3. Grandel U, Fink L, Blum A, Heep M, Buerke M, Kraemer HJ, Mayer K, Bohle RM, Seeger W, Grimminger F, Sibelius U. Endotoxin-induced myocardial tumor necrosis factor-alpha synthesis depresses contractility of isolated rat hearts: evidence for a role of sphingosine and cyclooxygenase-2-derived thromboxane production. Circulation. 2000;102:2758-2764.
4. Stein B, Frank P, Schmitz W, Scholz H, Thoenes M. Endotoxin and cytokines induce direct cardiodepressive effects in mammalian cardiomyocytes via induction of nitric oxide synthase. J Mol Cell Cardiol. 1996;28:1631-1639. (Pubitemid 26300563)
5. Rockman HA, Koch WJ, Lefkowitz RJ. Seven-transmembrane-spanning receptors and heart function. Nature. 2002;415:206-212. (Pubitemid 34059526)
6. Iaccarino G, Barbato E, Cipolletta E, De Amicis V, Margulies KB, Leosco D, Trimarco B, Koch WJ. Elevated myocardial and lymphocyte GRK2 expression and activity in human heart failure. Eur Heart J. 2005;26:1752-1758. (Pubitemid 41219848)
7. Vinge LE, Raake PW, Koch WJ. Gene therapy in heart failure. Circ Res. 2008;102:1458-1470.
8. Matkovich SJ, Diwan A, Klanke JL, Hammer DJ, Marreez Y, Odley AM, Brunskill EW, Koch WJ, Schwartz RJ, Dorn GW 2nd. Cardiac-specific ablation of G-protein receptor kinase 2 redefines its roles in heart development and beta-adrenergic signaling. Circ Res. 2006;99:996-1003. (Pubitemid 44657803)
9. Naga Prasad SV, Barak LS, Rapacciuolo A, Caron MG, Rockman HA. Agonist-dependent recruitment of phosphoinositide 3-kinase to the membrane by beta-adrenergic receptor kinase 1. A role in receptor sequestration. J Biol Chem. 2001;276:18953-18959.
10. Nienaber JJ, Tachibana H, Naga Prasad SV, Esposito G, Wu D, Mao L, Rockman HA. Inhibition of receptor-localized PI3K preserves cardiac beta-adrenergic receptor function and ameliorates pressure overload heart failure. J Clin Invest. 2003;112:1067-1079. (Pubitemid 38056322)
11. Perrino C, Schroder JN, Lima B, Villamizar N, Nienaber JJ, Milano CA, Naga Prasad SV. Dynamic regulation of phosphoinositide 3-kinasegamma activity and beta-adrenergic receptor trafficking in end-stage human heart failure. Circulation. 2007;116:2571-2579.
12. Sarkar S, Leaman DW, Gupta S, Sil P, Young D, Morehead A, Mukherjee D, Ratliff N, Sun Y, Rayborn M, Hollyfield J, Sen S. Cardiac overexpression of myotrophin triggers myocardial hypertrophy and heart failure in transgenic mice. J Biol Chem. 2004;279:20422-20434. (Pubitemid 38623489)
13. Kubota T, McTiernan CF, Frye CS, Slawson SE, Lemster BH, Koretsky AP, Demetris AJ, Feldman AM. Dilated cardiomyopathy in transgenic mice with cardiac-specific overexpression of tumor necrosis factor-alpha. Circ Res. 1997;81:627-635. (Pubitemid 27432751)
14. Rockman HA, Chien KR, Choi DJ, Iaccarino G, Hunter JJ, Ross J Jr, Lefkowitz RJ, Koch WJ. Expression of a beta-adrenergic receptor kinase 1 inhibitor prevents the development of myocardial failure in gene-targeted mice. Proc Natl Acad Sci USA. 1998;95:7000-7005. (Pubitemid 28278096)
15. Chandrasekharan UM, Siemionow M, Unsal M, Yang L, Poptic E, Bohn J, Ozer K, Zhou Z, Howe PH, Penn M, DiCorleto PE. Tumor necrosis factor alpha (TNF-alpha) receptor-II is required for TNFalpha-induced leukocyte-endothelial interaction in vivo. Blood. 2007;109:1938-1944. (Pubitemid 46348190)
16. Vasudevan NT, Mohan ML, Gupta MK, Hussain AK, Naga Prasad SV. Inhibition of protein phosphatase 2a activity by pi3kgamma regulates beta-adrenergic receptor function. Mol Cell. 2011;41:636-648.
17. Cavadini G, Petrzilka S, Kohler P, Jud C, Tobler I, Birchler T, Fontana A. TNF-alpha suppresses the expression of clock genes by interfering with E-box-mediated transcription. Proc Natl Acad Sci USA. 2007;104:12843-12848. (Pubitemid 47255242)
18. Perrino C, Naga Prasad SV, Mao L, Noma T, Yan Z, Kim HS, Smithies O, Rockman HA. Intermittent pressure overload triggers hypertrophyindependent cardiac dysfunction and vascular rarefaction. J Clin Invest. 2006;116:1547-1560.
19. Rengo G, Lymperopoulos A, Leosco D, Koch WJ. GRK2 as a novel gene therapy target in heart failure. J Mol Cell Cardiol. 2011;50:785-792.
20. Petrofski JA, Hoopes CW, Bashore TM, Russell SD, Milano CA. Mechanical ventricular support lowers pulmonary vascular resistance in a patient with congential heart disease. Ann Thorac Surg. 2003;75:1005-1007. (Pubitemid 36298387)
21. Tran TM, Friedman J, Qunaibi E, Baameur F, Moore RH, Clark RB. Characterization of agonist stimulation of cAMP-dependent protein kinase and G protein-coupled receptor kinase phosphorylation of the beta2-adrenergic receptor using phosphoserine-specific antibodies. Mol Pharmacol. 2004;65:196-206. (Pubitemid 38113900)
22. DebBurman SK, Ptasienski J, Benovic JL, Hosey MM. G protein-coupled receptor kinase GRK2 is a phospholipid-dependent enzyme that can be conditionally activated by G protein betagamma subunits. J Biol Chem. 1996;271:22552-22562. (Pubitemid 26304694)
23. DebBurman SK, Ptasienski J, Boetticher E, Lomasney JW, Benovic JL, Hosey MM. Lipid-mediated regulation of G protein-coupled receptor kinases 2 and 3. J Biol Chem. 1995;270:5742-5747.
24. Defer N, Azroyan A, Pecker F, Pavoine C. TNFR1 and TNFR2 signaling interplay in cardiac myocytes. J Biol Chem. 2007;282:35564-35573. (Pubitemid 350277148)
25. Graf K, Gräfe M, Dümmler U, O'Connor A, Regitz-Zagrosek V, Kunkel G, Auch-Schwelk W, Fleck E. Regulation of beta-adrenergic receptors on endothelial cells in culture. Eur Heart J. 1993;14(suppl I):173-176. (Pubitemid 23362613)
26. Birks EJ, Latif N, Owen V, Bowles C, Felkin LE, Mullen AJ, Khaghani A, Barton PJ, Polak JM, Pepper JR, Banner NR, Yacoub MH. Quantitative myocardial cytokine expression and activation of the apoptotic pathway in patients who require left ventricular assist devices. Circulation. 2001;104(12 suppl 1):I233-I240. (Pubitemid 32884809)
27. Ohtsuka T, Hamada M, Hiasa G, Sasaki O, Suzuki M, Hara Y, Shigematsu Y, Hiwada K. Effect of beta-blockers on circulating levels of inflammatory and anti-inflammatory cytokines in patients with dilated cardiomyopathy. J Am Coll Cardiol. 2001;37:412-417.
28. Gulick T, Chung MK, Pieper SJ, Lange LG, Schreiner GF. Interleukin 1 and tumor necrosis factor inhibit cardiac myocyte beta-adrenergic responsiveness. Proc Natl Acad Sci USA. 1989;86:6753-6757. (Pubitemid 19236340)
29. Chung MK, Gulick TS, Rotondo RE, Schreiner GF, Lange LG. Mechanism of cytokine inhibition of beta-adrenergic agonist stimulation of cyclic AMP in rat cardiac myocytes. Impairment of signal transduction. Circ Res. 1990;67:753-763. (Pubitemid 20315002)
30. Gulick T, Chung MK, Pieper SJ, Schreiner GF, Lange LG. Immune cytokine inhibition of beta-adrenergic agonist stimulated cyclic AMP generation in cardiac myocytes. Biochem Biophys Res Commun. 1988;150:1-9. (Pubitemid 18036197)
31. Shore SA, Moore PE. Regulation of beta-adrenergic responses in airway smooth muscle. Respir Physiol Neurobiol. 2003;137:179-195. (Pubitemid 37158008)
32. Bozkurt B, Kribbs SB, Clubb FJ Jr, Michael LH, Didenko VV, Hornsby PJ, Seta Y, Oral H, Spinale FG, Mann DL. Pathophysiologically relevant concentrations of tumor necrosis factor-alpha promote progressive left ventricular dysfunction and remodeling in rats. Circulation. 1998;97:1382-1391. (Pubitemid 28182677)
33. Carman CV, Barak LS, Chen C, Liu-Chen LY, Onorato JJ, Kennedy SP, Caron MG, Benovic JL. Mutational analysis of Gbetagamma and phospholipid interaction with G protein-coupled receptor kinase 2. J Biol Chem. 2000;275:10443-10452. (Pubitemid 30202105)
34. Garlie JB, Hamid T, Gu Y, Ismahil MA, Chandrasekar B, Prabhu SD. Tumor necrosis factor receptor 2 signaling limits-adrenergic receptor-mediated cardiac hypertrophy in vivo. Basic Res Cardiol. 2011;106:1193-1205.
35. Park EJ, Lee JH, Yu GY, He G, Ali SR, Holzer RG, Osterreicher CH, Takahashi H, Karin M. Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell. 2010;140:197-208.
36. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest. 2005;115:1111-1119. (Pubitemid 40629025)
37. Hotamisligil GS. Mechanisms of TNF-alpha-induced insulin resistance. Exp Clin Endocrinol Diabetes. 1999;107:119-125.
38. Vroon A, Heijnen CJ, Kavelaars A. GRKs and arrestins: regulators of migration and inflammation. J Leukoc Biol. 2006;80:1214-1221. (Pubitemid 44904958)
39. Mann DL. Inflammatory mediators and the failing heart: past, present, and the foreseeable future. Circ Res. 2002;91:988-998. (Pubitemid 35416635)