Basal and IGF-I-dependent regulation of potassium channels by MAP kinases and PI3-kinase during eccentric cardiac hypertrophy

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 295, Issue 5, 2008, Pages

  Teos, Leyla Y ^a   Zhao, Aiqiu ^a   Alvin, Zikiar ^a   Laurence, Graham G ^a   Li, Chuanfu ^b   Haddad, Georges E ^a  

^a HOWARD UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b East Tennessee State University   (United States)

Author keywords

Insulin like growth factor I; Mitogen activated protein kinase; Phosphatidylinositol 3 kinase

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; POTASSIUM CHANNEL; PROTEIN KINASE B; SOMATOMEDIN C;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; HEART VENTRICLE HYPERTROPHY; MALE; MUSCLE CELL; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CARDIOMEGALY; DISEASE MODELS, ANIMAL; INSULIN-LIKE GROWTH FACTOR I; MALE; MEMBRANE POTENTIALS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; MYOCYTES, CARDIAC; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; POTASSIUM CHANNELS; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 57049128189     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.321.2008     Document Type: Article

References (60)

1. Adams JP, Anderson AE, Varga AW, Dineley KT, Cook RG, Pfaffinger PJ, Sweatt JD. The A-type potassium channel Kv4.2 is a substrate for the mitogen-activated protein kinase ERK. J Neurochem 75: 2277-2287, 2000.
2. + current ITREK in cardiomyocytes. J Biol Chem 275: 39110-39116, 2000.
3. Barsyte-Lovejoy D, Galanis A, Clancy A, Sharrocks AD. ERK5 is targeted to myocyte enhancer factor 2A (MEF2A) through a MAPK docking motif. Biochem J 381: 693-699, 2004.
4. Barsyte-Lovejoy D, Galanis A, Sharrocks AD. Specificity determinants in MAPK signaling to transcription factors. J Biol Chem 277: 9896-9903, 2002.
5. Brooksby P, Levi AJ, Jones JV. The electrophysiological characteristics of hypertrophied ventricular myocytes from the spontaneously hypertensive rat. J Hypertens 11: 611-622, 1993.
6. Cerbai E, Barbieri M, Li Q, Mugelli A. Ionic basis of action potential prolongation of hypertrophied cardiac myocytes isolated from hypertensive rats of different ages. Cardiovasc Res 28: 1180-1187, 1994.
7. Cobb MH, Ross EM. Principles of cell signaling. In: Cells, edited by Lewin B. Sudbury, MA: Jones and Bartlett publishers, 2007, p. 589-644.
8. DeBosch B, Treskov I, Lupu TS, Weinheimer C, Kovacs A, Courtois M, Muslin AJ. Akt1 is required for physiological cardiac growth. Circulation 113: 2097-2104, 2006.
9. Donohue TJ, Dworkin LD, Lango MN, Fliegner K, Lango RP, Benstein JA, Slater WR, Catanese VM. Induction of myocardial insulin-like growth factor-I gene expression in left ventricular hypertrophy. Circulation 89: 799-809, 1994.
10. Dorn GW, Force T. Protein kinase cascades in the regulation of cardiac hypertrophy. J Clin Invest 115: 527-537, 2005.
11. Eghbali M, Deva R, Alioua A, Minosyan TY, Ruan H, Wang Y, Toro L, Stefani E. Molecular and functional signature of heart hypertrophy during pregnancy. Circ Res 96: 1208-1216, 2005.
12. Foncea R, Andersson M, Ketterman A, Blakesley V, Sapag-Hagar M, Sugden PH, LeRoith D, Lavandero S. Insulin-like growth factor-I rapidly activates multiple signal transduction pathways in cultured rat cardiac myocytes. J Biol Chem 272: 19115-19124, 1997.
13. Furukawa T, Bassett AL, Furukawa N, Kimura S, Myerburg RJ. The ionic mechanism of reperfusion-induced early afterdepolarizations in feline left ventricular hypertrophy. J Clin Invest 91: 1521-1531, 1993.
14. Furukawa T, Myerburg RJ, Furukawa N, Kimura S, Bassett AL. Metabolic inhibition of ICa,L and IK differs in feline left ventricular hypertrophy. Am J Physiol Heart Circ Physiol 266: H1121-H1131, 1994.
15. Gillis AM, Mathison HJ, Kulisz E, Lester WM. Dispersion of ventricular repolarization in left ventricular hypertrophy: influence of afterload and dofetilide. J Cardiovasc Electrophysiol 9: 988-997, 1998.
16. Gomez AM, Benitah JP, Henzel D, Vinet A, Lorente P, Delgado C. Modulation of electrical heterogeneity by compensated hypertrophy in rat left ventricle. Am J Physiol Heart Circ Physiol 272: H1078-H1086, 1997.
17. Grossman W, Jones D, McLaurin LP. Wall stress and patterns of hypertrophy in the human left ventricle. J Clin Invest 56: 56-64, 1975.
18. +-channel expression of cultured neonatal rat ventricular myocytes. Am J Physiol Heart Circ Physiol 272: H2599-H2606, 1997.
19. Ha T, Li Y, Gao X, McMullen JR, Shioi T, Izumo S, Kelley JL, Zhao A, Haddad GE, Williams DL, Browder IW, Kao RL, Li C. Attenuation of cardiac hypertrophy by inhibiting both mTOR and NFkappaB activation in vivo. Free Radic Biol Med 39: 1570-1580, 2005.
20. Haddad GE, Blackwell K, Bikhazi A. Regulation of insulin-like growth factor-1 by the renin-angiotensin system during regression of cardiac eccentric hypertrophy through angiotensin-converting enzyme inhibitor and AT1 antagonist. Can J Physiol Pharmacol 81: 142-149, 2003.
21. Hanson MC, Fath KA, Alexander RW, Delafontaine P. Induction of cardiac insulin-like growth factor I gene expression in pressure overload hypertrophy. Am J Med Sci 306: 69-74, 1993.
22. Haq S, Choukroun G, Lim H, Tymitz KM, del MF, Gwathmey J, Grazette L, Michael A, Hajjar R, Force T, Molkentin JD. Differential activation of signal transduction pathways in human hearts with hypertrophy vs. advanced heart failure. Circulation 103: 670-677, 2001.
23. Heineke J, Molkentin JD. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 7: 589-600, 2006.
24. Hille B. Ionic Channels of Excitable Membranes. Sunderland, MA: Sinauer Associates, 2001.
25. Hu HJ, Glauner KS, Gereau RW. ERK integrates PKA and PKC signaling in superficial dorsal horn neurons. I. Modulation of A-type K+ currents. J Neurophysiol 90: 1671-1679, 2003.
26. Huang CY, Hao LY, Buetow DE. Insulin-like growth factor-II induces hypertrophy of adult cardiomyocytes via two alternative pathways. Cell Biol Int 26: 737-739, 2002.
27. Isgaard J, Wahlander H, Adams MA, Friberg P. Increased expression of growth hormone receptor mRNA and insulin-like growth factor-I mRNA in volume-overloaded hearts. Hypertension 23: 884-888, 1994.
28. Ito H, Hiroe M, Hirata Y, Tsujino M, Adachi S, Shichiri M, Koike A, Nogami A, Marumo F. Insulin-like growth factor-I induces hypertrophy with enhanced expression of muscle specific genes in cultured rat cardiomyocytes. Circulation 87: 1715-1721, 1993.
29. Kleiman RB, Houser SR. Outward currents in normal and hypertrophied feline ventricular myocytes. Am J Physiol Heart Circ Physiol 256: H1450-H1461, 1989.
30. Kleiman RB, Houser SR. Outward currents in hypertrophied feline ventricular myocytes. Prog Clin Biol Res 334: 65-83, 1990.
31. Lang CH, Vary TC, Frost RA. Acute in vivo elevation of insulin-like growth factor (IGF) binding protein-1 decreases plasma free IGF-I and muscle protein synthesis. Endocrinology 144: 3922-3933, 2003.
32. Lavandero S, Foncea R, Perez V, Sapag-Hagar M. Effect of inhibitors of signal transduction on IGF-I-induced protein synthesis associated with hypertrophy in cultured neonatal rat ventricular myocytes. FEBS Lett 422: 193-196, 1998.
33. Lebeche D, Kaprielian R, del MF, Tomaselli G, Gwathmey JK, Schwartz A, Hajjar RJ. In vivo cardiac gene transfer of Kv4.3 abrogates the hypertrophic response in rats after aortic stenosis. Circulation 110: 3435-3443, 2004.
34. Lebeche D, Kaprielian R, Hajjar R. Modulation of action potential duration on myocyte hypertrophic pathways. J Mol Cell Cardiol 40: 725-735, 2006.
35. Matsui T, Li L, Wu JC, Cook SA, Nagoshi T, Picard MH, Liao R, Rosenzweig A. Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart. J Biol Chem 277: 22896-22901, 2002.
36. McIntosh MA, Cobbe SM, Kane KA, Rankin AC. Action potential prolongation and potassium currents in left-ventricular myocytes isolated from hypertrophied rabbit hearts. J Mol Cell Cardiol 30: 43-53, 1998.
37. McIntosh MA, Hicks MN, Kane KA, Rankin AC, Cobbe SM. A characterized model of left ventricular hypertrophy in the rabbit. Cardioscience 5: 95-100, 1994.
38. McMullen JR, Shioi T, Huang WY, Zhang L, Tarnavski O, Bisping E, Schinke M, Kong S, Sherwood MC, Brown J, Riggi L, Kang PM, Izumo S. The insulin-like growth factor 1 receptor induces physiological heart growth via the phosphoinositide 3-kinase(p110alpha) pathway. J Biol Chem 279: 4782-4793, 2004.
39. Modesti PA, Vanni S, Bertolozzi I, Cecioni I, Polidori G, Paniccia R, Bandinelli B, Perna A, Liguori P, Boddi M, Galanti G, Serneri GG. Early sequence of cardiac adaptations and growth factor formation in pressure- and volume-overload hypertrophy. Am J Physiol Heart Circ Physiol 279: H976-H985, 2000.
40. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, Omiya S, Mizote I, Matsumura Y, Asahi M, Nishida K, Hori M, Mizushima N, Otsu K. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med 13: 619-624, 2007.
41. Oudit GY, Sun H, Kerfant BG, Crackower MA, Penninger JM, Backx PH. The role of phosphoinositide-3 kinase and PTEN in cardiovascular physiology and disease. J Mol Cell Cardiol 37: 449-471, 2004.
42. Pramanik R, Qi X, Borowicz S, Choubey D, Schultz RM, Han J, Chen G. p38 isoforms have opposite effects on AP-1-dependent transcription through regulation of c-Jun. The determinant roles of the isoforms in the p38 MAPK signal specificity. J Biol Chem 278: 4831-4839, 2003.
43. Sanna B, Bueno OF, Dai YS, Wilkins BJ, Molkentin JD. Direct and indirect interactions between calcineurin-NFAT and MEK1-extracellular signal-regulated kinase 1/2 signaling pathways regulate cardiac gene expression and cellular growth. Mol Cell Biol 25: 865-878, 2005.
44. Saurin AT, Martin JL, Heads RJ, Foley C, Mockridge JW, Wright MJ, Wang Y, Marber MS. The role of differential activation of p38-mitogen-activated protein kinase in preconditioned ventricular myocytes. FASEB J 14: 2237-2246, 2000.
45. Schrader LA, Birnbaum SG, Nadin BM, Ren Y, Bui D, Anderson AE, Sweatt JD. ERK/MAPK regulates the Kv4.2 potassium channel by direct phosphorylation of the pore-forming subunit. Am J Physiol Cell Physiol 290: C852-C861, 2006.
46. Shioi T, McMullen JR, Kang PM, Douglas PS, Obata T, Franke TF, Cantley LC, Izumo S. Akt/protein kinase B promotes organ growth in transgenic mice. Mol Cell Biol 22: 2799-2809, 2002.
47. Shyu KG, Ko WH, Yang WS, Wang BW, Kuan P. Insulin-like growth factor-1 mediates stretch-induced upregulation of myostatin expression in neonatal rat cardiomyocytes. Cardiovasc Res 68: 405-414, 2005.
48. Sopontammarak S, Aliharoob A, Ocampo C, Arcilla RA, Gupta MP, Gupta M. Mitogen-activated protein kinases (p38 and c-Jun NH2-terminal kinase) are differentially regulated during cardiac volume and pressure overload hypertrophy. Cell Biochem Biophys 43: 61-76, 2005.
49. Stengl M, Ramakers C, Donker DW, Nabar A, Rybin AV, Spatjens RL, van der NT, Wodzig WK, Sipido KR, Antoons G, Moorman AF, Vos MA, Volders PG. Temporal patterns of electrical remodeling in canine ventricular hypertrophy: focus on IKs downregulation and blunted beta-adrenergic activation. Cardiovasc Res 72: 90-100, 2006.
50. Sun H, Oudit GY, Ramirez RJ, Costantini D, Backx PH. The phosphoinositide 3-kinase inhibitor LY294002 enhances cardiac myocyte contractility via a direct inhibition of Ik,slow currents. Cardiovasc Res 62: 509-520, 2004.
51. Tanno M, Bassi R, Gorog DA, Saurin AT, Jiang J, Heads RJ, Martin JL, Davis RJ, Flavell RA, Marber MS. Diverse mechanisms of myocardial p38 mitogen-activated protein kinase activation: evidence for MKK-independent activation by a TAB1-associated mechanism contributing to injury during myocardial ischemia. Circ Res 93: 254 -261, 2003.
52. Tomita F, Bassett AL, Myerburg RJ, Kimura S. Diminished transient outward currents in rat hypertrophied ventricular myocytes. Circ Res 75: 296-303, 1994.
53. + transport by aldosterone: signaling convergence and cross talk between the PI3-K and MAPK1/2 cascades. Am J Physiol Renal Physiol 286: F1232-F1238, 2004.
54. Tourian L Jr, Zhao H, Srikant CB. p38alpha, but not p38beta, inhibits the phosphorylation and presence of c-FLIPS in DISC to potentiate Fas-mediated caspase-8 activation and type I apoptotic signaling. J Cell Sci 117: 6459-6471, 2004.
55. Tsuji Y, Opthof T, Yasui K, Inden Y, Takemura H, Niwa N, Lu Z, Lee JK, Honjo H, Kamiya K, Kodama I. Ionic mechanisms of acquired QT prolongation and torsades de pointes in rabbits with chronic complete atrioventricular block. Circulation 106: 2012-2018, 2002.
56. Volk T, Nguyen TH, Schultz JH, Faulhaber J, Ehmke H. Regional alterations of repolarizing K+ currents among the left ventricular free wall of rats with ascending aortic stenosis. J Physiol 530: 443-455, 2001.
57. Walsh KB, Sweet JK, Parks GE, Long KJ. Modulation of outward potassium currents in aligned cultures of neonatal rat ventricular myocytes during phorbol ester-induced hypertrophy. J Mol Cell Cardiol 33: 1233-1247, 2001.
58. Wiedmann M, Wang X, Tang X, Han M, Li M, Mao Z. PI3K/Aktdependent regulation of the transcription factor myocyte enhancer factor-2 in insulin-like growth factor-1- and membrane depolarization-mediated survival of cerebellar granule neurons. J Neurosci Res 81: 226-234, 2005.
59. Wiedmann M, Wang X, Tang X, Han M, Li M, Mao Z. PI3K/Akt-dependent regulation of the transcription factor myocyte enhancer factor-2 in insulin-like growth factor-1- and membrane depolarization-mediated survival of cerebellar granule neurons. J Neurosci Res 81: 226-234, 2005.
60. Yuan LL, Adams JP, Swank M, Sweatt JD, Johnston D. Protein kinase modulation of dendritic K+ channels in hippocampus involves a mitogen-activated protein kinase pathway. J Neurosci 22: 4860-4868, 2002.