Prolonged leptin treatment increases transient outward K+ current via upregulation of Kv4.2 and Kv4.3 channel subunits in adult rat ventricular myocytes

Pflugers Archiv European Journal of Physiology

Volumn 466, Issue 5, 2014, Pages 903-914

  Gómez Hurtado, Nieves ^a   Fernández Velasco, María ^b   Fernández Alfonso, María Soledad ^c   Boscá, Lisardo ^d   Delgado, Carmen ^a,e  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^b HOSPITAL UNIVERSITARIO LA PAZ IDIPAZ   (Spain)

^c INSTITUTO PLURIDISCIPLINAR   (Spain)

^d INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^e CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Akt signaling; cardiomyocytes; ionic channel remodeling; Kv4.2; Kv4.3; leptin; transient outward potassium current

Indexed keywords

INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; LEPTIN; MESSENGER RNA; POTASSIUM CHANNEL; PROTEIN KINASE B; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL CAV1.2; VOLTAGE GATED CALCIUM CHANNEL CAV3.1; VOLTAGE GATED POTASSIUM CHANNEL KV4.2; VOLTAGE GATED POTASSIUM CHANNEL KV4.3; CACNA1G PROTEIN, RAT; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL T TYPE; KCNIP2 PROTEIN, RAT; KV CHANNEL INTERACTING PROTEIN; L-TYPE CALCIUM CHANNEL ALPHA(1C); POTASSIUM; SHAL POTASSIUM CHANNEL;

ADULT; ALPHA CHAIN; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; ENZYME ACTIVATION; HEART ELECTROPHYSIOLOGY; HEART FUNCTION; HEART MUSCLE CELL; HEART REPOLARIZATION; HEART VENTRICLE; NONHUMAN; PATCH CLAMP TECHNIQUE; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION; WESTERN BLOTTING; ACTION POTENTIAL; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; CALCIUM CHANNELS, L-TYPE; CALCIUM CHANNELS, T-TYPE; CELLS, CULTURED; HEART VENTRICLES; KV CHANNEL-INTERACTING PROTEINS; LEPTIN; MYOCYTES, CARDIAC; POTASSIUM; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RNA, MESSENGER; SHAL POTASSIUM CHANNELS; UP-REGULATION;

EID: 84901915904     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-013-1348-3     Document Type: Article

References (63)

1. Abe Y, Ono K, Kawamura T, Wada H, Kita T, Shimatsu A, Hasegawa K (2007) Leptin induces elongation of cardiac myocytes and causes eccentric left ventricular dilatation with compensation. Am J Physiol Heart Circ Physiol 292:H2387-H2396. doi:10.1152/ajpheart.00579.2006 (Pubitemid 47084621)
2. Abel ED, Litwin SE, Sweeney G (2008) Cardiac remodeling in obesity. Physiol Rev 88:389-419, 10.1152/physrev.00017.2007 (Pubitemid 351520084)
3. Aiba T, Tomaselli GF (2010) Electrical remodeling in the failing heart. Curr Opin Cardiol 25:29-36. doi:10.1097/HCO.0b013e328333d3d6
4. Andjelković M, Jakubowicz T, Cron P, Ming XF, Han JW, Hemmings BA (1996) Activation and phosphorylation of a pleckstrin homology domain containing protein kinase (RAC-PK/PKB) promoted by serum and protein phosphatase inhibitors. Proc Natl Acad Sci U S A 93:5699-5704 (Pubitemid 26190743)
5. Ashrafian H, Athanasiou T, le Roux CW (2011) Heart remodelling and obesity: the complexities and variation of cardiac geometry. Heart 97:171-172. doi:10.1136/hrt.2010.207092
6. 2+ homeostasis in the heart: beyond the action potential. Braz J Med Biol Res 39:393-403
7. Bénitah JP, Gomez AM, Bailly P, Da Ponte JP, Berson G, Delgado C, Lorente P (1993) Heterogeneity of the early outward current in ventricular cells isolated from normal and hypertrophied rat hearts. J Physiol 469:111-138 (Pubitemid 23281572)
8. Bénitah JP, Perrier E, Gómez AM, Vassort G (2001) Effects of aldosterone on transient outward K+current density in rat ventricular myocytes. J Physiol 537:151-160 (Pubitemid 33076962)
9. Berndt N, Yang H, Trinczek B, Betzi S, Zhang Z, Wu B, Lawrence NJ, Pellecchia M, Schönbrunn E, Cheng JQ, Sebti SM (2010) The Akt activation inhibitor TCN-P inhibits Akt phosphorylation by binding to the PH domain of Akt and blocking its recruitment to the plasma membrane. Cell Death Differ 17:1795-1804, 10.1038/cdd.2010.63
10. + currents in isolated human ventricular myocytes from patients with terminal heart failure. Circ Res 73:379-385
11. Brognard J, Sierecki E, Gao T, Newton AC (2007) PHLPP and a second isoform, PHLPP2, differentially attenuate the amplitude of Akt signaling by regulating distinct Akt isoforms. Mol Cell 25:917-931. doi:10.1016/j.molcel. 2007.02.017 (Pubitemid 46436532)
12. Casis O, Gallego M, Iriarte M, Sánchez-Chapula JA (2000) Effects of diabetic cardiomyopathy on regional electrophysiologic characteristics of rat ventricle. Diabetologia 43:101-109. doi:10.1007/s001250050013 (Pubitemid 30129308)
13. de Simone G, Devereux RB, Roman MJ, Alderman MH, Laragh JH (1994) Relation of obesity and gender to left ventricular hypertrophy in normotensive and hypertensive adults. Hypertension 23:600-606 (Pubitemid 24129354)
14. Enriori PJ, Evans AE, Sinnayah P, Cowley MA (2006) Leptin resistance and obesity. Obesity (Silver Spring) 14(Suppl 5):254S-258S. doi:10.1038/oby.2006.319
15. Fernandez-Velasco M, Ruiz-Hurtado G, Hurtado O, Moro MA, Delgado C (2007) TNF-alpha downregulates transient outward potassium current in rat ventricular myocytes through iNOS overexpression and oxidant species generation. Am J Physiol Heart Circ Physiol 293:H238-H245. doi:10.1152/ajpheart.01122.2006 (Pubitemid 47105078)
16. Frame S, Cohen P (2001) GSK3 takes centre stage more than 20 years after its discovery. Biochem J 359:1-16 (Pubitemid 32939202)
17. Friedman JM, Halaas JL (1998) Leptin and the regulation of body weight in mammals. Nature 395:763-770. doi:10.1038/27376 (Pubitemid 28485436)
18. Gómez AM, Benitah JP, Henzel D, Vinet A, Lorente P, Delgado C (1997) Modulation of electrical heterogeneity by compensated hypertrophy in rat left ventricle. Am J Physiol 272:H1078-H1086
19. Gong N, Bodi I, Zobel C, Schwartz A, Molkentin JD, Backx PH (2006) Calcineurin increases cardiac transient outward K+currents via transcriptional up-regulation of Kv4.2 channel subunits. J Biol Chem 281:38498-38506. doi:10.1074/jbc.M607774200 (Pubitemid 46041974)
20. Guzmán-Ruiz R, Somoza B, Gil-Ortega M, Merino B, Cano V, Attané C, Castan-Laurell I, Valet P, Fernández-Alfonso MS, Ruiz-Gayo M (2010) Sensitivity of cardiac carnitine palmitoyltransferase to malonyl-CoA is regulated by leptin: similarities with a model of endogenous hyperleptinemia. Endocrinology 151:1010-1018. doi:10.1210/en.2009-1170
21. 2+ channel gene and current in post-infarction remodeled rat left ventricle. Cardiovasc Res 46:442-449
22. Hughes V (2013) The big fat truth. Nature 497:428-430. doi:10.1038/497428a
23. Kääb S, Dixon J, Duc J, Ashen D, Näbauer M, Beuckelmann DJ, Steinbeck G, McKinnon D, Tomaselli GF (1998) Molecular basis of transient outward potassium current downregulation in human heart failure: a decrease in Kv4.3 mRNA correlates with a reduction in current density. Circulation 98:1383-1393 (Pubitemid 28462798)
24. Kääb S, Nuss HB, Chiamvimonvat N, O'Rourke B, Pak PH, Kass DA, Marban E, Tomaselli GF (1996) Ionic mechanism of action potential prolongation in ventricular myocytes from dogs with pacing-induced heart failure. Circ Res 78:262-273 (Pubitemid 26040856)
25. Kenchaiah S, Evans JC, Levy D, Wilson PW, Benjamin EJ, Larson MG, Kannel WB, Vasan RS (2002) Obesity and the risk of heart failure. N Engl J Med 347:305-313. doi:10.1056/NEJMoa020245 (Pubitemid 34815352)
26. Li GR, Lau CP, Ducharme A, Tardif JC, Nattel S (2002) Transmural action potential and ionic current remodeling in ventricles of failing canine hearts. Am J Physiol Heart Circ Physiol 283:H1031-H1041. doi:10.1152/ajpheart.00105.2002
27. to remodeling in diabetic rat heart. Am J Physiol Heart Circ Physiol 288:H1417-H1424. doi:10.1152/ajpheart.00559.2004
28. Martínez ML, Heredia MP, Delgado C (1999) Expression of T-type Ca(2+) channels in ventricular cells from hypertrophied rat hearts. JMol Cell Cardiol 31:1617-1625. doi:10.1006/jmcc.1999.0998 (Pubitemid 29414582)
29. Matsui T, Li L, Wu JC, Cook SA, Nagoshi T, Picard MH, Liao R, Rosenzweig A (2002) Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart. J Biol Chem 277:22896-22901. doi:10.1074/jbc.M200347200 (Pubitemid 34967272)
30. Matsui T, Rosenzweig A (2005) Convergent signal transduction pathways controlling cardiomyocyte survival and function: the role of PI 3-kinase and Akt. J Mol Cell Cardiol 38:63-71. doi:10.1016/j.yjmcc.2004.11.005 (Pubitemid 40038652)
31. McMullen JR, Amirahmadi F, Woodcock EA, Schinke-Braun M, Bouwman RD, Hewitt KA, Mollica JP, Zhang L, Zhang Y, Shioi T, Buerger A, Izumo S, Jay PY, Jennings GL (2007) Protective effects of exercise and phosphoinositide 3-kinase(p110alpha) signaling in dilated and hypertrophic cardiomyopathy. Proc Natl Acad Sci U S A 104:612-617. doi:10.1073/pnas.0606663104 (Pubitemid 46123073)
32. Mewes T, Ravens U (1994) L-type calcium currents of human myocytes from ventricle of non-failing and failing hearts and from atrium. J Mol Cell Cardiol 26:1307-1320. doi:10.1006/jmcc.1994.1149 (Pubitemid 24335566)
33. Mukherjee R, Hewett KW, Walker JD, Basler CG, Spinale FG (1998) Changes in L-type calcium channel abundance and function during the transition to pacing-induced congestive heart failure. Cardiovasc Res 37:432-444 (Pubitemid 28166003)
34. Nattel S, Maguy A, Le Bouter S, Yeh YH (2007) Arrhythmogenic ion-channel remodeling in the heart: heart failure, myocardial infarction, and atrial fibrillation. Physiol Rev 87:425-456. doi:10.1152/physrev.00014.2006 (Pubitemid 47084677)
35. Nerbonne JM, Kass RS (2005) Molecular physiology of cardiac repolarization. Physiol Rev 85:1205-1253. doi:10.1152/physrev.00002.2005 (Pubitemid 41362269)
36. Oreopoulos A, Padwal R, Kalantar-Zadeh K, Fonarow GC, Norris CM, McAlister FA (2008) Body mass index and mortality in heart failure: a meta-analysis. Am Heart J 156:13-22. doi:10.1016/j.ahj.2008.02.014 (Pubitemid 351862293)
37. Ouadid H, Albat B, Nargeot J (1995) Calcium currents in diseased human cardiac cells. J Cardiovasc Pharmacol 25:282-291
38. Perego L, Pizzocri P, Corradi D, Maisano F, Paganelli M, Fiorina P, Barbieri M, Morabito A, Paolisso G, Folli F, Pontiroli AE (2005) Circulating leptin correlates with left ventricular mass in morbid (grade III) obesity before and after weight loss induced by bariatric surgery: a potential role for leptin in mediating human left ventricular hypertrophy. J Clin Endocrinol Metab 90:4087-4093. doi:10.1210/jc.2004-1963 (Pubitemid 41058177)
39. Philip-Couderc P, Tavares NI, Roatti A, Lerch R, Montessuit C, Baertschi AJ (2008) Forkhead transcription factors coordinate expression of myocardial KATP channel subunits and energy metabolism. Circ Res 102:e20-e35. doi:10.1161/CIRCRESAHA.107.166744 (Pubitemid 351651133)
40. Pitt GS, Dun W, Boyden PA (2006) Remodeled cardiac calcium channels. J Mol Cell Cardiol 41:373-388. doi:10.1016/j.yjmcc.2006.06.071 (Pubitemid 44344291)
41. Purdham DM, Zou MX, Rajapurohitam V, Karmazyn M (2004) Rat heart is a site of leptin production and action. Am J Physiol Heart Circ Physiol 287:H2877-H2884. doi:10.1152/ajpheart.00499.2004 (Pubitemid 39557163)
42. Ren J (2004) Leptin and hyperleptinemia - from friend to foe for cardiovascular function. J Endocrinol 181:1-10
43. Rider OJ, Petersen SE, Francis JM, Ali MK, Hudsmith LE, Robinson MR, Clarke K, Neubauer S (2011) Ventricular hypertrophy and cavity dilatation in relation to body mass index in women with uncomplicated obesity. Heart 97:203-208. doi:10.1136/hrt.2009.185009
44. Romero-Corral A, Montori VM, Somers VK, Korinek J, Thomas RJ, Allison TG, Mookadam F, Lopez-Jimenez F (2006) Association of bodyweight with total mortality and with cardiovascular events in coronary artery disease: a systematic review of cohort studies. Lancet 368:666-678. doi:10.1016/S0140- 6736(06)69251-9 (Pubitemid 44223694)
45. Ruiz-Hurtado G, Gomez-Hurtado N, Fernandez-Velasco M, Calderon E, Smani T, Ordonez A, Cachofeiro V, Bosca L, Diez J, Gomez AM, Delgado C (2012) Cardiotrophin-1 induces sarcoplasmic reticulum Ca-2 leak and arrhythmogenesis in adult rat ventricular myocytes. Cardiovasc Res 96:81-89. doi:10.1093/cvr/cvs234
46. 2+ leak and arrhythmogenesis in adult rat ventricular myocytes. Cardiovasc Res 96:81-89, 10.1093/cvr/cvs234
47. Sah R, Ramirez RJ, Oudit GY, Gidrewicz D, Trivieri MG, Zobel C, Backx PH (2003) Regulation of cardiac excitation-contraction coupling by action potential repolarization: role of the transient outward potassium current (I(to)). J Physiol 546:5-18 (Pubitemid 36104968)
48. Shioi T, Kang PM, Douglas PS, Hampe J, Yballe CM, Lawitts J, Cantley LC, Izumo S (2000) The conserved phosphoinositide 3-kinase pathway determines heart size in mice. EMBO J 19:2537-2548. doi:10.1093/emboj/19.11.2537 (Pubitemid 30323543)
49. Smith CC, Mocanu MM, Davidson SM, Wynne AM, Simpkin JC, Yellon DM (2006) Leptin, the obesity-associated hormone, exhibits direct cardioprotective effects. Br J Pharmacol 149:5-13. doi:10.1038/sj.bjp.0706834 (Pubitemid 44299063)
50. Soliman AT, Omar M, Assem HM, Nasr IS, Rizk MM, El Matary W, El Alaily RK (2002) Serum leptin concentrations in children with type 1 diabetes mellitus: relationship to body mass index, insulin dose, and glycemic control. Metabolism 51:292-296 (Pubitemid 34232628)
51. Stucchi P, Guzmán-Ruiz R, Gil-Ortega M, Merino B, Somoza B, Cano V, de Castro J, Sevillano J, Ramos MP, Fernández-Alfonso MS, Ruiz-Gayo M (2011) Leptin resistance develops spontaneously in mice during adult life in a tissue-specific manner. Consequences for hepatic steatosis. Biochimie 93:1779-1785. doi:10.1016/j.biochi.2011.06.020
52. Sweeney G (2010) Cardiovascular effects of leptin. Nat Rev Cardiol 7:22-29. doi:10.1038/nrcardio.2009.224
53. Van Der Heide LP, Hoekman MF, Smidt MP (2004) The ins and outs of FoxO shuttling: mechanisms of FoxO translocation and transcriptional regulation. Biochem J 380:297-309. doi:10.1042/BJ20040167 (Pubitemid 38788101)
54. Wang Y, Hill JA (2010) Electrophysiological remodeling in heart failure. J Mol Cell Cardiol 48:619-632. doi:10.1016/j.yjmcc.2010.01.009
55. Wannamethee SG, Shaper AG, Whincup PH, Lennon L, Sattar N (2011) Obesity and risk of incident heart failure in oldermen with and without pre-existing coronary heart disease: does leptin have a role? J Am Coll Cardiol 58:1870-1877. doi:10.1016/j.jacc.2011.06.057
56. Yang R, Barouch LA (2007) Leptin signaling and obesity: cardiovascular consequences. Circ Res 101:545 - 559. doi:10.1161/CIRCRESAHA.107.156596
57. Yang KC, Foeger NC, Marionneau C, Jay PY, McMullen JR, Nerbonne JM (2010) Homeostatic regulation of electrical excitability in physiological cardiac hypertrophy. J Physiol 588:5015-5032. doi:10.1113/jphysiol.2010.197418
58. Yang KC, Jay PY, McMullen JR, Nerbonne JM (2012) Enhanced cardiac PI3Kα signalling mitigates arrhythmogenic electrical remodelling in pathological hypertrophy and heart failure. Cardiovasc Res 93:252-262. doi:10.1093/cvr/cvr283
59. Yang KC, Tseng YT, Nerbonne JM (2012) Exercise training and PI3Kα-induced electrical remodeling is independent of cellular hypertrophy and Akt signaling. J Mol Cell Cardiol 53:532-541. doi:10.1016/j.yjmcc.2012.07. 004
60. Yao JJ, Gao XF, Chow CW, Zhan XQ, Hu CL, Mei YA (2012) Neuritin activates insulin receptor pathway to up-regulate Kv4.2-mediated transient outward K+current in rat cerebellar granule neurons. J Biol Chem 287:41534-41545. doi:10.1074/jbc.M112.390260
61. Yao JJ, Sun J, Zhao QR, Wang CY, Mei YA (2013) Neuregulin-1 / ErbB4 signaling regulates Kv4.2-mediated transient outward K+current through the Akt/mTOR pathway. Am J Physiol Cell Physiol 304(12):H1651-H1661. doi:10.1152/ajpcell.00041.2013
62. Zeidan A, Hunter JC, Javadov S, Karmazyn M (2011) mTOR mediates RhoA-dependent leptin-induced cardiomyocyte hypertrophy. Mol Cell Biochem 352:99-108. doi:10.1007/s11010-011-0744-2
63. Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372:425-432. doi:10.1038/372425a0 (Pubitemid 24365442)