Downregulation of G protein-coupled receptor kinase 2 levels enhances cardiac insulin sensitivity and switches on cardioprotective gene expression patterns

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1842, Issue 12, 2014, Pages 2448-2456

  Lucas, Elisa ^a,b   Jurado Pueyo, María ^a,b   Fortuño, María A ^c   Fernández Veledo, Sonia ^d   Vila Bedmar, Rocío ^a,b   Jiménez Borreguero, Luis J ^b,e   Lazcano, Juan J ^e   Gao, Ehre ^f   Gómez Ambrosi, Javier ^g   Frühbeck, Gema ^g   Koch, Walter J ^f   Díez, Javier ^c,h   Mayor, Federico ^a,b   Murga, Cristina ^a,b  

^a CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^b Instituto de Investigación Sanitaria del Hospital Universitario de La Princesa   (Spain)

^c UNIVERSITY OF NAVARRA   (Spain)

^d HOSPITAL UNIVERSITARI JOAN XXIII   (Spain)

^e CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

^f TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF NAVARRA   (Spain)

^h UNIVERSITY CLINIC OF NAVARRA   (Spain)

Author keywords

Cardiac hypertrophy; G protein coupled receptors; GRK2; Heart failure; High fat diet; Insulin resistance

Indexed keywords

G PROTEIN COUPLED RECEPTOR KINASE 2; INSULIN; ADRBK1 PROTEIN, MOUSE; ANTIDIABETIC AGENT; GLUCOSE TRANSPORTER 4; PROTEIN KINASE B; SLC2A4 PROTEIN, MOUSE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMORBIDITY; CONTROLLED STUDY; DIABETES MELLITUS; DOWN REGULATION; GENE DOSAGE; GENE EXPRESSION; GENE REPRESSION; HEART FUNCTION; HEART HYPERTROPHY; HEART PROTECTION; INSULIN RESISTANCE; INSULIN RESPONSE; INSULIN SENSITIVITY; LIPID DIET; MALE; MOUSE; NONHUMAN; OBESITY; 129 MOUSE; ADVERSE EFFECTS; ANIMAL; C57BL MOUSE; CARDIOMEGALY; CELL MEMBRANE; DNA MICROARRAY; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENETICS; HEART MUSCLE; KNOCKOUT MOUSE; METABOLISM; MOUSE MUTANT; PHOSPHORYLATION; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CARDIOMEGALY; CELL MEMBRANE; DIET, HIGH-FAT; DOWN-REGULATION; G-PROTEIN-COUPLED RECEPTOR KINASE 2; GENE EXPRESSION PROFILING; GLUCOSE TRANSPORTER TYPE 4; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN RESISTANCE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, OBESE; MYOCARDIUM; OBESITY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TIME FACTORS;

EID: 84910029573     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2014.09.004     Document Type: Article

References (53)

1. Gurevich E.V., Tesmer J.J., Mushegian A., Gurevich V.V. G protein-coupled receptor kinases: more than just kinases and not only for GPCRs. Pharmacol. Ther. 2012, 133:40-69.
2. Garcia-Guerra L., Nieto-Vazquez I., Vila-Bedmar R., Jurado-Pueyo M., Zalba G., Diez J., Murga C., Fernandez-Veledo S., Mayor F., Lorenzo M. G protein-coupled receptor kinase 2 plays a relevant role in insulin resistance and obesity. Diabetes 2010, 59:2407-2417.
3. Vila-Bedmar R., Garcia-Guerra L., Nieto-Vazquez I., Mayor F., Lorenzo M., Murga C., Fernandez-Veledo S. GRK2 contribution to the regulation of energy expenditure and brown fat function. Faseb J. 2012, 26:3503-3514.
4. Avendano M.S., Lucas E., Jurado-Pueyo M., Martinez-Revelles S., Vila-Bedmar R., Mayor F., Salaices M., Briones A.M., Murga C. Increased nitric oxide bioavailability in adult GRK2 hemizygous mice protects against angiotensin II-induced hypertension. Hypertension 2014, 63:369-375.
5. Penela P., Murga C., Ribas C., Tutor A.S., Peregrin S., Mayor F. Mechanisms of regulation of G protein-coupled receptor kinases (GRKs) and cardiovascular disease. Cardiovasc. Res. 2006, 69:46-56.
6. Brinks H., Das A., Koch W.J. A role for GRK2 in myocardial ischemic injury: indicators of a potential future therapy and diagnostic. Futur. Cardiol. 2011, 7:547-556.
7. Dorn G.W. GRK mythology: G-protein receptor kinases in cardiovascular disease. J. Mol. Med. 2009, 87:455-463.
8. Penela P., Murga C., Ribas C., Lafarga V., Mayor F. The complex G protein-coupled receptor kinase 2 (GRK2) interactome unveils new physio-pathological targets. Br. J. Pharmacol. 2010, 160:821-832.
9. Rockman H.A., Choi D.J., Akhter S.A., Jaber M., Giros B., Lefkowitz R.J., Caron M.G., Koch W.J. Control of myocardial contractile function by the level of beta-adrenergic receptor kinase 1 in gene-targeted mice. J. Biol. Chem. 1998, 273:18180-18184.
10. Ribas C., Penela P., Murga C., Salcedo A., Garcia-Hoz C., Jurado-Pueyo M., Aymerich I., Mayor F. The G protein-coupled receptor kinase (GRK) interactome: role of GRKs in GPCR regulation and signaling. Biochim. Biophys. Acta 2007, 1768:913-922.
11. Ciccarelli M., Chuprun J.K., Rengo G., Gao E., Wei Z., Peroutka R.J., Gold J.I., Gumpert A., Chen M., Otis N.J., Dorn G.W., Trimarco B., Iaccarino G., Koch W.J. G protein-coupled receptor kinase 2 activity impairs cardiac glucose uptake and promotes insulin resistance after myocardial ischemia. Circulation 2011, 123:1953-1962.
12. Rett K., Wicklmayr M., Dietze G.J., Haring H.U. Insulin-induced glucose transporter (GLUT1 and GLUT4) translocation in cardiac muscle tissue is mimicked by bradykinin. Diabetes 1996, 45(Suppl. 1):S66-S69.
13. Burks D.J., Wang J., Towery H., Ishibashi O., Lowe D., Riedel H., White M.F. IRS pleckstrin homology domains bind to acidic motifs in proteins. J. Biol. Chem. 1998, 273:31061-31067.
14. Cruz-Adalia A., Jimenez-Borreguero L.J., Ramirez-Huesca M., Chico-Calero I., Barreiro O., Lopez-Conesa E., Fresno M., Sanchez-Madrid F., Martin P. CD69 limits the severity of cardiomyopathy after autoimmune myocarditis. Circulation 2010, 122:1396-1404.
15. Soto-Montenegro M.L., Vaquero J.J., Pascau J., Gispert J.D., Garcia-Barreno P., Desco M. Detection of visual activation in the rat brain using 2-deoxy-2-[(18)F]fluoro-d-glucose and statistical parametric mapping (SPM). Mol. Imaging Biol. 2009, 11:94-99.
16. Bertrand L., Horman S., Beauloye C., Vanoverschelde J.L. Insulin signalling in the heart. Cardiovasc. Res. 2008, 79:238-248.
17. Miquet J.G. Growth hormone modulation of insulin signaling in the heart. Cell Cycle 2012, 11:827-828.
18. Tsybouleva N., Zhang L., Chen S., Patel R., Lutucuta S., Nemoto S., DeFreitas G., Entman M., Carabello B.A., Roberts R., Marian A.J. Aldosterone, through novel signaling proteins, is a fundamental molecular bridge between the genetic defect and the cardiac phenotype of hypertrophic cardiomyopathy. Circulation 2004, 109:1284-1291.
19. Houweling A.C., van Borren M.M., Moorman A.F., Christoffels V.M. Expression and regulation of the atrial natriuretic factor encoding gene Nppa during development and disease. Cardiovasc. Res. 2005, 67:583-593.
20. Sainz N., Rodriguez A., Catalan V., Becerril S., Ramirez B., Gomez-Ambrosi J., Fruhbeck G. Leptin administration downregulates the increased expression levels of genes related to oxidative stress and inflammation in the skeletal muscle of ob/ob mice. Mediat. Inflamm. 2010, 2010:784343.
21. Matkovich S.J., Van Booven D.J., Hindes A., Kang M.Y., Druley T.E., Vallania F.L., Mitra R.D., Reilly M.P., Cappola T.P., Dorn G.W. Cardiac signaling genes exhibit unexpected sequence diversity in sporadic cardiomyopathy, revealing HSPB7 polymorphisms associated with disease. J. Clin. Invest. 2010, 120:280-289.
22. Senbonmatsu T., Saito T., Landon E.J., Watanabe O., Price E., Roberts R.L., Imboden H., Fitzgerald T.G., Gaffney F.A., Inagami T. A novel angiotensin II type 2 receptor signaling pathway: possible role in cardiac hypertrophy. EMBO J. 2003, 22:6471-6482.
23. Albig A.R., Becenti D.J., Roy T.G., Schiemann W.P. Microfibril-associate glycoprotein-2 (MAGP-2) promotes angiogenic cell sprouting by blocking notch signaling in endothelial cells. Microvasc. Res. 2008, 76:7-14.
24. Weir R.A., Clements S., Steedman T., Dargie H.J., McMurray J.J., Squire I.B., Ng L.L. Plasma TIMP-4 predicts left ventricular remodeling after acute myocardial infarction. J. Card. Fail. 2011, 17:465-471.
25. Eguchi Y., Eguchi N., Oda H., Seiki K., Kijima Y., Matsu-ura Y., Urade Y., Hayaishi O. Expression of lipocalin-type prostaglandin D synthase (beta-trace) in human heart and its accumulation in the coronary circulation of angina patients. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:14689-14694.
26. Ragolia L., Palaia T., Hall C.E., Maesaka J.K., Eguchi N., Urade Y. Accelerated glucose intolerance, nephropathy, and atherosclerosis in prostaglandin D2 synthase knock-out mice. J. Biol. Chem. 2005, 280:29946-29955.
27. Lee J., Xu Y., Lu L., Bergman B., Leitner J.W., Greyson C., Draznin B., Schwartz G.G. Multiple abnormalities of myocardial insulin signaling in a porcine model of diet-induced obesity. Am. J. Physiol. Heart Circ. Physiol. 2010, 298:H310-H319.
28. Terauchi Y., Tsuji Y., Satoh S., Minoura H., Murakami K., Okuno A., Inukai K., Asano T., Kaburagi Y., Ueki K., Nakajima H., Hanafusa T., Matsuzawa Y., Sekihara H., Yin Y., Barrett J.C., Oda H., Ishikawa T., Akanuma Y., Komuro I., Suzuki M., Yamamura K., Kodama T., Suzuki H., Koyasu S., Aizawa S., Tobe K., Fukui Y., Yazaki Y., Kadowaki T. Increased insulin sensitivity and hypoglycaemia in mice lacking the p85 alpha subunit of phosphoinositide 3-kinase. Nat. Genet. 1999, 21:230-235.
29. Taniguchi C.M., Aleman J.O., Ueki K., Luo J., Asano T., Kaneto H., Stephanopoulos G., Cantley L.C., Kahn C.R. The p85alpha regulatory subunit of phosphoinositide 3-kinase potentiates c-Jun N-terminal kinase-mediated insulin resistance. Mol. Cell. Biol. 2007, 27:2830-2840.
30. Haemmerle G., Moustafa T., Woelkart G., Buttner S., Schmidt A., van de Weijer T., Hesselink M., Jaeger D., Kienesberger P.C., Zierler K., Schreiber R., Eichmann T., Kolb D., Kotzbeck P., Schweiger M., Kumari M., Eder S., Schoiswohl G., Wongsiriroj N., Pollak N.M., Radner F.P., Preiss-Landl K., Kolbe T., Rulicke T., Pieske B., Trauner M., Lass A., Zimmermann R., Hoefler G., Cinti S., Kershaw E.E., Schrauwen P., Madeo F., Mayer B., Zechner R. ATGL-mediated fat catabolism regulates cardiac mitochondrial function via PPAR-alpha and PGC-1. Nat. Med. 2011, 17:1076-1085.
31. Riehle C., Wende A.R., Zaha V.G., Pires K.M., Wayment B., Olsen C., Bugger H., Buchanan J., Wang X., Moreira A.B., Doenst T., Medina-Gomez G., Litwin S.E., Lelliott C.J., Vidal-Puig A., Abel E.D. PGC-1beta deficiency accelerates the transition to heart failure in pressure overload hypertrophy. Circ. Res. 2011, 109:783-793.
32. Zhang C.L., McKinsey T.A., Chang S., Antos C.L., Hill J.A., Olson E.N. Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell 2002, 110:479-488.
33. Chang L., Zhang J., Tseng Y.H., Xie C.Q., Ilany J., Bruning J.C., Sun Z., Zhu X., Cui T., Youker K.A., Yang Q., Day S.M., Kahn C.R., Chen Y.E. Rad GTPase deficiency leads to cardiac hypertrophy. Circulation 2007, 116:2976-2983.
34. Wang G., Zhu X., Xie W., Han P., Li K., Sun Z., Wang Y., Chen C., Song R., Cao C., Zhang J., Wu C., Liu J., Cheng H. Rad as a novel regulator of excitation-contraction coupling and beta-adrenergic signaling in heart. Circ. Res. 2010, 106:317-327.
35. Abi-Gerges A., Richter W., Lefebvre F., Mateo P., Varin A., Heymes C., Samuel J.L., Lugnier C., Conti M., Fischmeister R., Vandecasteele G. Decreased expression and activity of cAMP phosphodiesterases in cardiac hypertrophy and its impact on beta-adrenergic cAMP signals. Circ. Res. 2009, 105:784-792.
36. Xia Y., Dobaczewski M., Gonzalez-Quesada C., Chen W., Biernacka A., Li N., Lee D.W., Frangogiannis N.G. Endogenous thrombospondin 1 protects the pressure-overloaded myocardium by modulating fibroblast phenotype and matrix metabolism. Hypertension 2011, 58:902-911.
37. Wu W.H., Hu C.P., Chen X.P., Zhang W.F., Li X.W., Xiong X.M., Li Y.J. MicroRNA-130a mediates proliferation of vascular smooth muscle cells in hypertension. Am. J. Hypertens. 2011, 24:1087-1093.
38. Simonsen M.L., Alessio H.M., White P., Newsom D.L., Hagerman A.E. Acute physical activity effects on cardiac gene expression. Exp. Physiol. 2010, 95:1071-1080.
39. Bostrom P., Mann N., Wu J., Quintero P.A., Plovie E.R., Panakova D., Gupta R.K., Xiao C., MacRae C.A., Rosenzweig A., Spiegelman B.M. C/EBPbeta controls exercise-induced cardiac growth and protects against pathological cardiac remodeling. Cell 2010, 143:1072-1083.
40. Molkentin J.D. The transcription factor C/EBPbeta serves as a master regulator of physiologic cardiac hypertrophy. Circ. Res. 2011, 108:277-278.
41. Sloan C., Tuinei J., Nemetz K., Frandsen J., Soto J., Wride N., Sempokuya T., Alegria L., Bugger H., Abel E.D. Central leptin signaling is required to normalize myocardial fatty acid oxidation rates in caloric-restricted ob/ob mice. Diabetes 2011, 60:1424-1434.
42. Zhang H., Makarewich C.A., Kubo H., Wang W., Duran J.M., Li Y., Berretta R.M., Koch W.J., Chen X., Gao E., Valdivia H.H., Houser S.R. Hyperphosphorylation of the cardiac ryanodine receptor at serine 2808 is not involved in cardiac dysfunction after myocardial infarction. Circ. Res. 2012, 110:831-840.
43. Bugger H., Abel E.D. Rodent models of diabetic cardiomyopathy. Dis. Model. Mech. 2009, 2:454-466.
44. Boudina S., Bugger H., Sena S., O'Neill B.T., Zaha V.G., Ilkun O., Wright J.J., Mazumder P.K., Palfreyman E., Tidwell T.J., Theobald H., Khalimonchuk O., Wayment B., Sheng X., Rodnick K.J., Centini R., Chen D., Litwin S.E., Weimer B.E., Abel E.D. Contribution of impaired myocardial insulin signaling to mitochondrial dysfunction and oxidative stress in the heart. Circulation 2009, 119:1272-1283.
45. Belke D.D., Betuing S., Tuttle M.J., Graveleau C., Young M.E., Pham M., Zhang D., Cooksey R.C., McClain D.A., Litwin S.E., Taegtmeyer H., Severson D., Kahn C.R., Abel E.D. Insulin signaling coordinately regulates cardiac size, metabolism, and contractile protein isoform expression. J. Clin. Invest. 2002, 109:629-639.
46. 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.
47. Ashrafian H., Frenneaux M.P., Opie L.H. Metabolic mechanisms in heart failure. Circulation 2007, 116:434-448.
48. Shimizu I., Yoshida Y., Katsuno T., Tateno K., Okada S., Moriya J., Yokoyama M., Nojima A., Ito T., Zechner R., Komuro I., Kobayashi Y., Minamino T. p53-Induced adipose tissue inflammation is critically involved in the development of insulin resistance in heart failure. Cell Metab. 2012, 15:51-64.
49. Opie L.H. The metabolic vicious cycle in heart failure. Lancet 2004, 364:1733-1734.
50. von Bibra H., St John Sutton M. Impact of diabetes on postinfarction heart failure and left ventricular remodeling. Curr. Heart Fail. Rep. 2011, 8:242-251.
51. Hata J.A., Williams M.L., Schroder J.N., Lima B., Keys J.R., Blaxall B.C., Petrofski J.A., Jakoi A., Milano C.A., Koch W.J. Lymphocyte levels of GRK2 (betaARK1) mirror changes in the LVAD-supported failing human heart: lower GRK2 associated with improved beta-adrenergic signaling after mechanical unloading. J. Card. Fail. 2006, 12:360-368.
52. Chokshi A., Drosatos K., Cheema F.H., Ji R., Khawaja T., Yu S., Kato T., Khan R., Takayama H., Knoll R., Milting H., Chung C.S., Jorde U., Naka Y., Mancini D.M., Goldberg I.J., Schulze P.C. Ventricular assist device implantation corrects myocardial lipotoxicity, reverses insulin resistance, and normalizes cardiac metabolism in patients with advanced heart failure. Circulation 2012, 125:2844-2853.
53. Rengo G., Galasso G., Femminella G.D., Parisi V., Zincarelli C., Pagano G., De Lucia C., Cannavo A., Liccardo D., Marciano C., Vigorito C., Giallauria F., Ferrara N., Furgi G., Perrone Filardi P., Koch W.J., Leosco D. Reduction of lymphocyte G protein-coupled receptor kinase-2 (GRK2) after exercise training predicts survival in patients with heart failure. Eur. J. Prev. Cardiol. 2014, 21:4-11.