Role of phosphoinositide 3-kinase α, protein kinase C, and L-type Ca2+ channels in mediating the complex actions of angiotensin II on mouse cardiac contractility

Hypertension

Volumn 56, Issue 3, 2010, Pages 422-429

  Liang, Wenbin ^a,b   Oudit, Gavin Y ^c   Patel, Mikin M ^a,b   Shah, Ajay M ^d   Woodgett, James R ^e   Tsushima, Robert G ^f   Ward, Michael E ^a,g   Backx, Peter H ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c UNIVERSITY OF ALBERTA   (Canada)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e MOUNT SINAI HOSPITAL   (Canada)

^f YORK UNIVERSITY   (Canada)

^g ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

cardiac contraction; glycogen synthase kinase 3 ; Langendorff heart; NADPH oxidase; patch clamp

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; ANGIOTENSIN II; CALCIUM CHANNEL L TYPE; GLYCOGEN SYNTHASE KINASE 3BETA; IRBESARTAN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2;

ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CHANNEL GATING; CONTROLLED STUDY; ENZYME ACTIVITY; HEART LEFT VENTRICLE DP-DT; HEART MUSCLE CONTRACTILE FORCE; HEART MUSCLE CONTRACTILITY; INOTROPISM; ISOLATED HEART; MALE; MOUSE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANALYSIS OF VARIANCE; ANGIOTENSIN II; ANIMALS; CALCIUM; CALCIUM CHANNELS, L-TYPE; GLYCOGEN SYNTHASE KINASE 3; MICE; MICE, KNOCKOUT; MYOCARDIAL CONTRACTION; MYOCARDIUM; PROTEIN KINASE C; SIGNAL TRANSDUCTION; VASOCONSTRICTOR AGENTS;

EID: 77955979222     PISSN: 0194911X     EISSN: None     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.109.149344     Document Type: Article

References (56)

1. Sadoshima J, Xu Y, Slayter HS, Izumo S. Autocrine release of angioten-sin II mediates stretch-induced hypertrophy of cardiac myocytes in vitro. Cell. 1993;75:977-984.
2. Serneri GGN, Boddi M, Cecioni I, Vanni S, Coppo M, Papa ML, Bandinelli B, Bertolozzi I, Polidori G, Toscano T, Maccherini M, Modesti PA. Cardiac angiotensin II formation in the clinical course of heart failure and its relationship with left ventricular function. Circ Res. 2001;88: 961-968.
3. 1 receptor subtype. Circ Res. 1993;73: 413-423.
4. Gusev K, Domenighetti AA, Delbridge LMD, Pedrazzini T, Niggli E, Egger M. Angiotensin II-mediated adaptive and maladaptive remodeling of cardiomyocyte excitation-contraction coupling. Circ Res. 2009;105: 42-50.
5. Moravec C, Schluchter M, Paranandi L, Czerska B, Stewart R, Rosenkranz E, Bond M. Inotropic effects of angiotensin II on human cardiac muscle in vitro. Circulation. 1990;82:1973-1984.
6. Petroff MGV, Aiello EA, Palomeque J, Salas MA, Mattiazzi A. Sub-cellular mechanisms of the positive inotropic effect of angiotensin II in cat myocardium. J Physiol. 2000;529:189-203.
7. Cingolani HE, Villa-Abrille MC, Cornelli M, Nolly A, Ennis IL, Gar-ciarena C, Suburo AM, Torbidoni V, Correa MV, Camilionde Hurtado MC, Aiello EA. The positive inotropic effect of angiotensin II: role of endothelin-1 and reactive oxygen species. Hypertension. 2006;47: 727-734.
8. Rajagopal K, Whalen EJ, Violin JD, Stiber JA, Rosenberg PB, Premont RT, Coffman TM, Rockman HA, Lefkowitz RJ./3-Arrestin2-mediated inotropic effects of the angiotensin II type 1A receptor in isolated cardiac myocytes. Proc Natl Acad Sci USA. 2006;103:16284-16289.
9. Palomeque J, Sapia L, Hajjar RJ, Mattiazzi A, Vila Petroff M. Angiotensin II-induced negative inotropy in rat ventricular myocytes: role of reactive oxygen species and p38 MAPK. Am J Physiol Heart Circ Physiol. 2006;290:H96-H106.
10. Lefroy DC, Crake T, Del Monte F, Vescovo G, Dalla Libera L, Harding S, Poole-Wilson PA. Angiotensin II and contraction of isolated myocytes from human, guinea pig, and infarcted rat hearts. Am J Physiol Heart Circ Physiol. 1996;270:H2060-H2069.
11. Mercure C, Yogi A, Callera GE, Aranha AB, Bader M, Ferreira AJ, Santos RAS, Walther T, Touyz RM, Reudelhuber TL. Angiotensin(1-7) blunts hypertensive cardiac remodeling by a direct effect on the heart. Circ Res. 2008;103:1319-1326.
12. Sakurai K, Norota I, Tanaka H, Kubota I, Tomoike H, Endo M. Negative inotropic effects of angiotensin II, endothelin-1 and phenylephrine in indo-1 loaded adult mouse ventricular myocytes. Life Sci. 2002;70: 1173-1184.
13. Wenzel S, Abdallah Y, Helmig S, Schafer C, Piper HM, Schluter K-D. Contribution of PI3-kinase isoforms to angiotensin II-and a-adrenoceptor- mediated signalling pathways in cardiomyocytes. Cardiovasc Res. 2006;71: 352-362.
14. Rabkin SW, Goutsouliak V, Kong JY. Angiotensin II induces activation of phosphatidylinositol 3-kinase in cardiomyocytes. J Hypertens. 1997; 15:891-899.
15. Quignard JF, Mironneau J, Carricaburu V, Fournier B, Babich A, Nurnberg B, Mironneau C, Macrez N. Phosphoinositide 3-kinase y mediates angiotensin II-induced stimulation of L-type calcium channels in vascular myocytes. J Biol Chem. 2001;276:32545-32551.
16. Yano N, Tseng A, Zhao TC, Robbins J, Padbury JF, Tseng YT. Temporally controlled overexpression of cardiac-specific PI3Ka induces enhanced myocardial contractility\a new transgenic model. Am J Physiol Heart Circ Physiol. 2008;295:H1690-H1694.
17. 2+ currents via increased PI3Ka/PKB signaling. Circ Res. 2006;98:1390-1397.
18. Lu Z, Jiang YP, Wang W, Xu XH, Mathias RT, Entcheva E, Ballou LM, Cohen IS, Lin RZ. Loss of cardiac phosphoinositide 3-kinase p110a results in contractile dysfunction. Circulation. 2009;120:318-325.
19. Kerfant B, Rose R, Sun H, Backx P. Phosphoinositide 3-kinase y regulates cardiac contractility by locally controlling cyclic adenosine monophosphate levels. Trends Cardiovasc Med. 2006;16:250-256.
20. Kerfant BG, Zhao D, Lorenzen-Schmidt I, Wilson LS, Cai S, Chen SRW, Maurice DH, Backx PH. PI3Ky is required for PDE4, not PDE3, activity in subcellular microdomains containing the sarcoplasmic reticular calcium ATPase in cardiomyocytes. Circ Res. 2007;101:400-408.
21. Nienaber JJ, Tachibana H, Naga Prasad SV, Esposito G, Wu D, Mao L, Rockman HA. Inhibition of receptor-localized PI3K preserves cardiac/3-adrenergic receptor function and ameliorates pressure overload heart failure. J Clin Invest. 2003;112:1067-1079.
22. Shioi T, Kang P, Douglas P, Hampe J, Yballe C, Lawitts J, Cantley L, Izumo S. The conserved phosphoinositide 3-kinase pathway determines heart size in mice. EMBO J. 2000;19:2537-2548.
23. Sasaki T, Irie-Sasaki J, Horie Y, Bachmaier K, Fata J, Li M, Suzuki A, Bouchard D, Ho A, Redston M, Gallinger S, Khokha R, Mak T, Hawkins P, Stephens L, Scherer S, Tsao M, Penninger J. Colorectal carcinomas in mice lacking the catalytic subunit of PI(3)Ky. Nature. 2000;406:897-902.
24. Tkalcevic J, Novelli M, Phylactides M, Iredale JP, Segal AW, Roes J. Impaired immunity and enhanced resistance to endotoxin in the absence of neutrophil elastase and cathepsin G. Immunity. 2000;12:201-210.
25. Patel S, Doble BW, MacAulay K, Sinclair EM, Drucker DJ, Woodgett JR. Tissue-specific role of glycogen synthase kinase 3/3 in glucose homeostasis and insulin action. Mol Cell Biol. 2008;28:6314-6328.
26. Sohal DS, Nghiem M, Crackower MA, Witt SA, Kimball TR, Tymitz KM, Penninger JM, Molkentin JD. Temporally regulated and tissue-specific gene manipulations in the adult and embryonic heart using a tamoxifen-inducible Cre protein. Circ Res. 2001;89:20-25.
27. kslow currents. Cardiovasc Res. 2004; 62:509-520.
28. Gregg DE. Effect of coronary perfusion pressure or coronary flow on oxygen usage of the myocardium. Circ Res. 1963;13:497-500.
29. ATP channels in ischemic cardioprotection. Circulation. 2000;101: 2418-2423.
30. Sargent CA, Sleph PG, Dzwonczyk S, Normandin D, Antonaccio MJ, Grover GJ. Cardioprotective effects of the cyanoguanidine potassium channel opener P-1075. J Cardiovasc Pharmacol. 1993;22:564-570.
31. ATP channel openers, P-1075, pinacidil, and diazoxide, on energetics and contractile function in isolated rat hearts. J Mol Cell Cardiol. 2002;34:427-440.
32. + channels in guinea pig ventricular cells. J Pharmacol Exp Ther. 1993; 266:978-984.
33. 2+ current in gramicidin D-perforated adult rabbit ventricular myocytes: comparison with conventional patch-clamp method. Pflugers Arch. 2002; 444:107-116.
34. 2+-and protein kinase C-dependent mechanism. Am J Physiol Heart Circ Physiol. 2001;280:H1528-H1536.
35. Oudit GY, Kassiri Z, Patel MP, Chappell M, Butany J, Backx PH, Tsushima RG, Scholey JW, Khokha R, Penninger JM. Angiotensin II-mediated oxidative stress and inflammation mediate the age-dependent cardiomyopathy in ACE2 null mice. Cardiovasc Res. 2007;75:29-39.
36. Brock C, Schaefer M, Reusch HP, Czupalla C, Michalke M, Spicher K, Schultz G, Nurnberg B. Roles of G/3y in membrane recruitment and activation of p110y/p101 phosphoinositide 3-kinase y. J Cell Biol. 2003; 160:89-99.
37. Crackower M, Oudit G, Kozieradzki I, Sarao R, Sun H, Sasaki T, Hirsch E, Suzuki A, Shioi T, Irie-Sasaki J, Sah R, Cheng H, Rybin V, Lembo G, Fratta L, Oliveira-dos-Santos A, Benovic J, Kahn C, Izumo S, Steinberg S, Wymann M, Backx P, Penninger J. Regulation of myocardial contractility and cell size by distinct PI3K-PTEN signaling pathways. Cell. 2002;110:737-749.
38. Kerfant BG, Gidrewicz D, Sun H, Oudit GY, Penninger JM, Backx PH. Cardiac sarcoplasmic reticulum calcium release and load are enhanced by subcellular cAMP elevations in PI3Ky-deficient mice. Circ Res. 2005; 96:1079-1086.
39. Ballou LM, Lin HY, Fan G, Jiang YP, Lin RZ. Activated Gaq inhibits p110a phosphatidylinositol 3-kinase and Akt. J Biol Chem. 2003;278: 23472-23479.
40. Rigor DL, Bodyak N, Bae S, Choi JH, Zhang L, Ter-Ovanesyan D, He Z, McMullen JR, Shioi T, Izumo S, King GL, Kang PM. Phosphoinositide 3-kinase Akt signaling pathway interacts with protein kinase C/32 in the regulation of physiologic developmental hypertrophy and heart function. Am J Physiol Heart Circ Physiol. 2009;296:H566-H572.
41. Fang X, Yu S, Tanyi JL, Lu Y, Woodgett JR, Mills GB. Convergence of multiple signaling cascades at glycogen synthase kinase-3: Edg receptor-mediated phosphorylation and inactivation by lysophosphatidic acid through a protein kinase C-dependent intracellular pathway. Mol Cell Biol. 2002;22:2099-2110.
42. Tong H, Imahashi K, Steenbergen C, Murphy E. Phosphorylation of glycogen synthase kinase-3/3 during preconditioning through a phosphatidylinositol-3- kinase-dependent pathway is cardioprotective. Circ Res. 2002;90:377-379.
43. Braz JC, Gill RM, Corbly AK, Jones BD, Jin N, Vlahos CJ, Wu Q, Shen W. Selective activation of PI3Ka/Akt/GSK-3/3 signalling and cardiac compensatory hypertrophy during recovery from heart failure. Eur J Heart Fail. 2009;11:739-748.
44. Michael A, Haq S, Chen X, Hsich E, Cui L, Walters B, Shao Z, Bhat-tacharya K, Kilter H, Huggins G, Andreucci M, Periasamy M, Solomon RN, Liao R, Patten R, Molkentin JD, Force T. Glycogen synthase kinase-3/3 regulates growth, calcium homeostasis, and diastolic function in the heart. J Biol Chem. 2004;279:21383-21393.
45. 2+-and phospholipid- independent activation of protein kinase C by selective oxidative modification of the regulatory domain. Proc Natl Acad Sci USA. 1989;86:6758-6762.
46. Bendall JK, Cave AC, Heymes C, Gall N, Shah AM. Pivotal role of a gp91phox-containing NADPH oxidase in angiotensin II-induced cardiac hypertrophy in mice. Circulation. 2002;105:293-296.
47. phox by controlling cPKC/PKC 8 but not Akt. Biochem Biophys Res Commun. 2004;316:720-730.
48. Salas M, Vila-Petroff M, Palomeque J, Aiello E, Mattiazzi A. Positive inotropic and negative lusitropic effect of angiotensin II: intracellular mechanisms and second messengers. J Mol Cell Cardiol. 2001;33: 1957-1971.
49. 2+ handling in normal and hypertrophied rat myocardium. J Mol Cell Cardiol. 1998;30:2507-2518.
50. Schumann H, Starke K, Werner U. Interactions of inhibitors of noradrenaline uptake and angiotensin on the sympathetic nerves of the isolated rabbit heart. Br J Pharmacol. 1970;39:390-397.
51. 2+ channels through phosphatidylinositol 3-kinase. J Biol Chem. 2005;280:40347-40354.
52. McHugh D, Sharp EM, Scheuer T, Catterall WA. Inhibition of cardiac L-type calcium channels by protein kinase C phosphorylation of two sites in the N-terminal domain. Proc Natl Acad Sci USA. 2000;97:12334-12338.
53. Pi Y, Sreekumar R, Huang X, Walker JW. Positive inotropy mediated by diacylglycerol in rat ventricular myocytes. Circ Res. 1997;81:92-100.
54. Yuan SH, Sunahara FA, Sen AK. Tumor-promoting phorbol esters inhibit cardiac functions and induce redistribution of protein kinase C in perfused beating rat heart. Circ Res. 1987;61:372-378.
55. Liu Q, Chen X, MacDonnell SM, Kranias EG, Lorenz JN, Leitges M, Houser SR, Molkentin JD. Protein kinase Ca, but not PKC/3 or PKCy, regulates contractility and heart failure susceptibility: implications for ruboxistaurin as a novel therapeutic approach. Circ Res. 2009;105:194-200.
56. 2 receptors. Circ Res. 1999;85:919-930.