Overexpression of coupling factor 6 attenuates exercise-induced physiological cardiac hypertrophy by inhibiting PI3K/Akt signaling in mice

Journal of Hypertension

Volumn 30, Issue 4, 2012, Pages 778-786

  Sagara, Shigeki ^a   Osanai, Tomohiro ^a   Itoh, Taihei ^a   Izumiyama, Kei ^a   Shibutani, Shuji ^a   Hanada, Kenji ^a   Yokoyama, Hiroaki ^a   Yamamoto, Yuko ^a   Yokota, Takashi ^a   Tomita, Hirofumi ^a   Magota, Koji ^b   Okumura, Ken ^a  

^a HIROSAKI UNIVERSITY   (Japan)

^b DAIICHI SANKYO CO   (Japan)

Author keywords

coupling factor 6; phosphatidylinositol 3 kinase Akt signaling; physiological cardiac hypertrophy; tissue acidosis

Indexed keywords

COUPLING FACTOR 6; PEPTIDES AND PROTEINS; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOINSULIN RECEPTOR SUBSTRATE 1; PHOSPHOPROTEIN; SOMATOMEDIN C; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; COUPLING FACTOR; ENZYME INHIBITION; EXERCISE; GENE EXPRESSION; GENE OVEREXPRESSION; HEART LEFT VENTRICLE WALL; HEART MUSCLE CELL; HEART VENTRICLE HYPERTROPHY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PHYSIOLOGICAL CARDIAC HYPERTROPHY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SWIMMING; TRANSGENIC MOUSE; TRANSTHORACIC ECHOCARDIOGRAPHY;

EID: 84858709388     PISSN: 02636352     EISSN: 14735598     Source Type: Journal    
DOI: 10.1097/HJH.0b013e3283505101     Document Type: Article

References (46)

1. Pina IL, Apstein CS, Balady GJ, Belardinelli R, Chaitman BR, Duscha BD, et al. A statement from the American Heart Association Committee on exercise, rehabilitation, and prevention. Circulation 2003; 107:1210-1225. (Pubitemid 36297217)
2. O'Connor CM, Whellan DJ, Lee KL, Keteyian SJ, Cooper LS, Ellis SJ, et al., HF-ACTION Investigators. Efficacy and safety of exercise training in patients with chronic heart failure: HF-ACTION randomized controlled trial. JAMA 2009; 301:1439-1450.
3. Patwala AY, Woods PR, Sharp L, Goldspink DF, Tan LB, Wright DJ. Maximizing patient benefit fromcardiac resynchronization therapy with the addition of structured exercise training: a randomized controlled study. J Am Coll Cardiol 2009; 53:2332-2339.
4. Wilkins BJ, Dai YS, Bueno OF, Parsons SA, Xu J, Plank DM, , et al. Calcineurin/NFAT coupling participates in pathological, but not physiological, cardiac hypertrophy. Circ Res 2004; 94:110-118. (Pubitemid 38064105)
5. Selvetella G, Hirsch E, Notte A, Tarone G, Lembo G. Adaptive and maladaptive hypertrophic pathways: points of convergence and divergence. Cardiovasc Res 2004; 63:373-380. (Pubitemid 38970181)
6. DeBosch B, Treskov I, Lupu TS, Weinheimer C, Kovacs A, Courtois M, et al. Akt1 is required for physiological cardiac growth. Circulation 2006; 113:2097-2104.
7. Boyer PD. The binding change mechanism for ATP synthase: some probabilities and possibilities. BiochimBiophys Acta 1993; 1140:215-250. (Pubitemid 23015689)
8. Walker JE, Fearnley IM, Gay NJ, Gibson BW, Northrop FD, Powell SJ, et al. Primary structure and subunit stoichiometry of F1-ATPase from bovine mitochondria. J Mol Biol 1985; 184:677-701. (Pubitemid 15024774)
9. Kagawa Y, Racker E. Partial resolution of the enzyme catalyzing oxidative phosphorylation: Correlation of morphology and function in submitochondrial particles. J Biol Chem 1966; 241:2475-2482.
10. Walker JE, Runswick MJ, Poulter L. ATP synthase from bovine mitochondria: characterization and sequence analysis of two membrane associated subunits and of their corresponding c-DNAs. J Mol Biol 1987; 197:89-100.
11. Collinson IR, van Raaij MJ, Runswick MJ, Fearnley IM, Skehel JM, Orriss GL, et al. ATP synthase from bovine heart mitochondria: in vitro assembly of a stalk complex in the presence of F1-ATPase and its absence. J Mol Biol 1994; 242:408-421.
12. Osanai T, Kamada T, Fujiwara N, Katoh T, Takahashi K, Kimura M, et al. A novel inhibitory effect on prostacyclin synthesis of coupling factor 6 extracted from the heart of spontaneous hypertensive rats. J Biol Chem 1998; 273:31778-31783. (Pubitemid 29177110)
13. Osanai T, Tanaka M, Kamada T, Nakano T, Takahashi K, Okada S, et al. Mitochondrial coupling factor 6 as a potent endogenous vasoconstrictor. J Clin Invest 2001; 108:1023-1030. (Pubitemid 32946076)
14. Osanai T, Magota K, Tanaka M, Shimada M, Murakami R, Sasaki S, et al. Intracellular signaling for vasoconstrictor coupling factor 6: Novel function of b-subunit of ATP synthase as receptor. Hypertension 2005; 46:1140-1146. (Pubitemid 41533017)
15. Ashitate T, Osanai T, Tanaka M, Magota K, Echizen T, Izumiyama K, et al. Overexpression of coupling factor 6 causes cardiac dysfunction under high salt diet in mice. J Hypertens 2010; 28:2243-2251.
16. Beauloye C, Bertrand L, Krause U, Marsin AS, Dresselaers T, Vanstapel F, et al. No-flow ischemia inhibits insulin signaling in heart by decreasing intracellular pH. Circ Res 2001; 88:513-519. (Pubitemid 32240915)
17. Ashitate T, Osanai T, Tanaka M, Magota K, Echizen T, Tomita H, et al. Generation and characterization of coupling factor 6-overexpressing transgenic mice. Hirosaki Med J 2009; 60:18-26.
18. Osanai T, Tomita H, Kushibiki M, Yamada M, Tanaka M, Ashitate T, et al. Coupling factor 6 enhances Src-mediated responsiveness to angiotensin II in resistance arterioles and cells. Cardiovasc Res 2009; 81:780-787.
19. Osanai T, Tanaka M, Magota K, Tomita H, Okumura K. Coupling factor 6-induced activation of ecto-F1Fo complex induces insulin resistance, mild glucose intolerance and elevated blood pressure in mice. Diabetologia (in press).
20. Honsho S, Nishikawa S, Amano K, Zen K, Adachi Y, Kishita E, et al. Pressure-mediated hypertrophy and mechanical stretch induces IL-1 release and subsequent IGF-1 generation to maintain compensative hypertrophy by affecting Akt and JNK pathways. Circ Res 2009; 105:1149-1158.
21. McMullen JR, Shioi T, Huang WY, Zhang L, Tarnavski O, Bisping E, et al. The insulin-like growth factor 1 receptor induces physiological heart growth via the phosphoinositide 3-kinase (p110alpha) pathway. J Biol Chem 2004; 279:4782-4793. (Pubitemid 38199073)
22. Miyachi M, Yazawa H, Furukawa M, Tsuboi K, Ohtake M, Nishizawa T, et al. Exercise training alters left ventricular geometry and attenuates heart failure in dahl salt-sensitive hypertensive rats. Hypertension 2009; 53:701-707.
23. Garciarena CD, Pinilla OA, Nolly MB, Laguens RP, Escudero EM, Cingolani HE, et al. Endurance training in the spontaneously hypertensive rat: conversion of pathological into physiological cardiac hypertrophy. Hypertension 2009; 53:708-714.
24. Leosco D, Rengo G, Iaccarino G, Golino L, Marchese M, Fortunato F, et al. Exercise promotes angiogenesis and improves b-adrenergic receptor signalling in the postischaemic failing rat heart. Cardiovasc Res 2008; 78:385-394. (Pubitemid 351556096)
25. Wisloff U, Loennechen JP, Currie S, Smith GL, Ellingsen O. Aerobic exercise reduces cardiomyocyte hypertrophy and increases contractility, Ca2 + sensitivity and SERCA-2 in rat after myocardial infarction. Cardiovasc Res 2002; 54:162-174. (Pubitemid 34327946)
26. Neri Serneri GG, Boddi M, Modesti PA, Cecioni I, Coppo M, Padeletti L, et al. Increased cardiac sympathetic activity and insulin-like growth factor-I formation are associated with physiological hypertrophy in athletes. Circ Res 2001; 89:977-982. (Pubitemid 34640863)
27. Koziris LP, Hickson RC, Chatterton RT Jr, Groseth RT, Christie JM, Goldflies DG, et al. Serum levels of total and free IGF-I and IGFBP-3 are increased and maintained in long-term training. J Appl Physiol 1999; 86:1436-1442. (Pubitemid 29172182)
28. Perrino C, Prasad SV, Mao L, Noma T, Yan Z, Kim HS, et al. Cardiac hypertrophy: stressing out the heart. J Clin Invest 2006; 116:1547-1560.
29. Luo J, McMullen JR, Sobkiw CL, Zhang L, Dorfman AL, Sherwood MC, et al. Class IA phosphoinositide 3-kinase regulates heart size and physiological cardiac hypertrophy. Mol Cell Biol 2005; 25:9491-9502. (Pubitemid 41507849)
30. McMullen JR, Shioi T, Zhang L, Tarnavski O, Sherwood MC, Kang PM, et al. Phosphoinositide 3-kinase (p110alpha) plays a critical role for the induction of physiological, but not pathological, cardiac hypertrophy. Proc Natl Acad Sci USA 2003; 100:12355-12360. (Pubitemid 37271564)
31. Shioi T, Kang PM, Douglas PS, Hampe J, Yballe CM, Lawitts J, et al. The conserved phosphoinositide 3-kinase pathway determines heart size in mice. EMBO 2000; 19:2537-2548. (Pubitemid 30323543)
32. Kim J, Wende AR, Sena S, Theobald HA, Soto J, Sloan C, et al. Insulin-like growth factor I receptor signaling is required for exerciseinduced cardiac hypertrophy. Mol Endocrinol 2008; 22:2531-2543.
33. Scheinowitz M, Kessler-Icekson G, Freimann S, Zimmermann R, Schaper W, Golomb E, et al. Short-and long-term swimming exercise training increases myocardial insulin-like growth factor-I gene expression. Growth Horm IGF Res 2003; 13:19-25. (Pubitemid 36285124)
34. Yeh JK, Aloia JF, Chen M, Ling N, Koo HC, Millard WJ. Effect of growth hormone administration and treadmill exercise on serum and skeletal IGF-I in rats. Am J Physiol 1994; 266:E129-E135.
35. Vaughan-Jones RD, Spitzer KW, Swietach P. Intracellular pH regulation in heart. J Mol Cell Cardiol 2009; 46:318-331.
36. Osanai T, Okada S, Sirato K, Nakano T, Saitoh M, Magota K, et al. Mitochondrial coupling factor 6 is present on the surface of human vascular endothelial cells and released by shear stress. Circulation 2001; 104:3132-3136. (Pubitemid 34014070)
37. Osanai T, Magota K, Okumura K. Coupling factor 6 as a novel vasoactive and proatherogenic peptide in vascular endothelial cells. Naunyn Schmiedebergs Arch Pharmacol 2009; 380:205-214.
38. Tanaka M, Osanai T, Murakami R, Sasaki S, Tomita H, Maeda N, et al. Effect of vasoconstrictor coupling factor 6 on gene expression profile in human vascular endothelial cells: enhanced release of asymmetric dimethylarginine. J Hypertens 2006; 24:489-497. (Pubitemid 43261913)
39. Kumagai A, Osanai T, Katoh C, Tanaka M, Tomita H, Morimoto T, et al. Coupling factor 6 downregulates platelet endothelial cell adhesion molecule-1 via c-Src activation and acts as a proatherogenic molecule. Atherosclerosis 2008; 200:45-50.
40. Goldberg R, Reshef-Bankai E, Coleman R, Green J, Maor G. Chronic acidosis-induced growth retardation is mediated by protoninduced expression ofGs protein. J BoneMinerRes 2006; 21:703-713.
41. Osanai T, Sasaki S, Kamada T, Fujiwara N, Nakano T, Tomita H, et al. Circulating coupling factor 6 in human hypertension: role of reactive oxygen species. J Hypertens 2003; 21:2323-2328. (Pubitemid 38293572)
42. Ding WH, Chu SY, Jiang HF, Cai DY, Pang YZ, Tang CS, et al. Plasma mitochondrial coupling factor 6 in patients with acute myocardial infarction. Hypertens Res 2004; 27:717-722. (Pubitemid 40045510)
43. Osanai T, Nakamura M, Sasaki S, Tomita H, Saitoh M, Osawa H, et al. Plasma concentration of coupling factor 6 and cardiovascular events in patients with end-stage renal disease. Kidney Int 2003; 64:2291-2297. (Pubitemid 37449566)
44. Li XL, Xing QC, Gao YY, Dong B, Pang YZ, Jiang HF, et al. Plasma level of mitochondrial coupling factor 6 increases in patients with type 2 diabetes mellitus. Int J Cardiol 2007; 117:411-412. (Pubitemid 46507638)
45. Osanai T, FujiwaraN, Sasaki S, Metoki N, Saitoh G, Tomita H, et al. Novel pro-atherogenic molecule coupling factor 6 is elevated in patients with stroke: a possible linkage to homocysteine. Ann Med 2010; 42:79-86.
46. Tomita H, Osanai T, Toki T, Sasaki S, Maeda N, Murakami R, et al. Troglitazone and 15-deoxy-deta 12, 14-prostaglandin J2 inhibit shearinduced coupling factor 6 release in endothelial cells. Cardiovasc Res 2005; 67:134-141. (Pubitemid 40798300)