Relationship between apoptosis and alteration of the energetic metabolism pathways of hypertrophic cardiomyocytes induced by hypoxia-reoxygenation
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1 636 Acta Physiologica Sinica, October 25, 2005, 57 (5): * µmol/l 1 µmol/l 95% N 2 5% CO 2 5 mmhg 8 h (pyruvate dehydrogenase, PDH) -1(carnitine palmitoyltransferase 1, CPT-1) (1) 8 h (PDHa) CPT-1 PDHa (P>0.05) CPT-1 (2) [ (16 ± 0.9)% (48 ± 1.1)%] (3) (4) (5) (6) Q463; Q256; R363 Relationship between apoptosis and alteration of the energetic metabolism pathways of hypertrophic cardiomyocytes induced by hypoxia-reoxygenation FENG Bing *, LIU Wei, XU Jing, HE Zuo-Yun, YANG Hui-Biao Department of Kidney Disease, Xinqiao Hospital, the Third Military Medical University, Chongqing , China Abstract: The apoptosis of cardiomyocytes plays a pivotal role in the pathogenesis of cardiac failure transformed from cardiac hypertrophy, so that suppression of cardiomyocytes apoptosis is an effective pharmacotherapeutic target to prevent cardiac failure. This study focused on the relationship between apoptosis and alteration of the energetic metabolism pathways of hypertrophic cardiomyocytes induced by hypoxia-reoxygenation. Cardiomyocyte hypertrophy was induced by angiotensin (0.1 µmol/l ) and norepinephrine (1 µmol/l), and the cells were cultured under the condition of hypoxia ( 95% N 2 and 5% CO 2, the O 2 partial pressure was regulated at least lower than 5 mmhg ) for 8 h, then were recovered to normal culture environment. Apoptosis was detected with TUNEL. The activity of pyruvate dehydrogenase (PDH) and carnitine palmitoyltransferase 1 (CPT-1), the rate of glycose oxidation and glycolysis, and fatty acid metabolism were detected by liquid scintillation counting. The results are as follows: (1) The activity of active PDH (PDHa) was slightly higher in hypertrophic cardiomyocytes than that in normal cardiomyocytes, but the activity of CPT- 1 was significantly lower in hypertrophic cardiomyoctes than that in normal cardiomyocytes.compared with the hypertrophic cardiomyocytes cultured with normal oxygen concentration, the activities of PDHa and CPT-1 were decreased significantly after hypoxia for 8 h, and the activity of PDHa were decreased further after reoxygenation for 4 h, but the activity of CPT-1 recovered Received Accepted This work was supported by the National Natural Science Foundation of China (No ). * Corresponding author. Tel: ; fxb12@yahoo.com.cn
2 : 637 quickly after reoxygenation. (2) The rate of glucose oxidation in hypertrophic cardiomyocytes increased slightly when cultured under normal O 2 partial pressure than that in normal cardiac cells. The rate of glucose oxidation reduced (16 ± 0.9)% and (48 ± 1.1)% in normal and hypertrophic cardiomyocytes, respectively, after hypoxia. It reduced further in hypertrophic cardiac cells at 4 h of reoxygenation, then recovered gradually. In normal cardiocytes, it recovered quickly after reoxygenation. (3) The rate of glycolysis of hypertrophic cardiocytes increased slightly than that of the normal cardiocytes when cultured in the general O 2 environment. Compared with the normal cardiomyocytes, the rate of glycolysis of hypertrophic cardiac cells was the same during hypoxia-reoxygenation culture, i.e., the rate of glycolysis decreased slightly after hypoxia for 8 h, but increased rapidly and significantly after reoxygenation. (4) The rate of fatty acid oxidation was slightly lower in hypertrophic cardiocytes than that in normal cardiomyocytes. After hypoxia for 8 h, the rate of fatty acid oxidation decreased significantly in normal and hypertrophic cardiomyocytes, there was no difference between normal and hypertrophic cardiomyocytes. But the alterations of fatty acid oxidation after reoxygenation were different between normal and hypertrophic cardiac cells, namely, the fatty acid oxidation of normal cardiomyocytes were activated slowly and slightly, while the rate of fatty acid oxidation of hypertrophic cardiomyocytes increased markedly at the early stage of reoxygenation, and increased further at 8 h of reoxygenation. (5) The rate of apoptosis in hypertrophic cardiocytes increased obviously after hypoxia for 8 h, and increased further and markedly at the early stage of reoxygenation, then gradually decreased to normal level. (6) Dicholoroacetate could inhibit apoptosis of hypertrophic cardiocytes through increasing glucose oxidation and inhibiting the activation of glycolysis and fatty acid oxidation of hypertrophic cardiomyocytes induced by hypoxia-reoxygenation. These data demonstrate that apoptosis in hypertrophic cardiomyocytes after hypoxia-reoxygenation is mainly due to the inhibition of glucose oxidation and the activation of glucolysis and fatty acid oxidation. Furthermore, increasing glucose oxidation may be a new pharmacotherapeutic target to inhibit apoptosis of hypertrophic cardiac cells. Key words: cardiac hypertrophy; apoptosis; hypoxia-reoxygenation; energy metabolism [1] 70% [2] [3] (dicholoroacetate, DCA) [4-6] [7] [8] 48 h 0.1 µmol/l (Ang ) 1 µmol/l (norepinephrine, NE) 12 h Chen [9] 95% N 2 5% CO 2 5 mmhg 8 h (20% O 2 5% CO 2 ) 1.2 (TUNEL) PBS 3 2 4% 30 min PBS TUNEL DAB 5 (400 ) [10] (active pyruvate dehydrogenase, PDHa)
3 638 Acta Physiologica Sinica, October 25, 2005, 57(5): PBS Lowry [(mmol/l): 200 KCl 50 MgCl 2 5 EGTA 5 Tris-HCl 50 NaF 50 dichloroacetate 5, 0.1% Triton X-100 (ph 7.8)] 200 µl 2~3 min 280 µl (37 ) [ (mmol/l): Tris-HCl 100 Na 2 EDTA 0.5 MgCl 2 1 CoASH 0.5 1, ph 7.8] 20 µl (26 mmol/l) 1 mmol/l 10 min 210 µl 40 µl 0.5 mol/l HClO 4 5 min 10 µl 2.2 mol/l KHCO g 3 min 20 µl 4 CoA (PDHt) PBS [(mmol/l): 200 KCl 50 MgCl 2 5 EGTA 5 10 hexokinase 2 U, Tris-HCl 50 (ph 7.8)] 20 µl 10 µl [(mmol/l): 200 KCl 50 MgCl 2 5 EGTA 5 Tris- HCl 50 (ph 7.8) 10 CaCl MgCl DCA 25 hexokinase 2 U] min 280 µl 0.1% Triton X µl 26 mmol/l PDHa CoA CoA 14 C- 14 C CoA 1.4-1(carnitine palmitoyltransferase 1, CPT-1) PBS 2, (mmol/l 250 EDTA 5 ph ) (600 g)10 min g 15 min 2 4 0~4 Lowry CPT-1 [11] 0.5 ml (-)- [methyl- 3 H] carnitine 0.2 mmol/l CoA 50 µmol/l HEPES buffer (ph 7.0) 20 mmol/l 1% BSA KCl 40~75 mmol/l 7.5 mmol/l 22.5 mmol/l KCN 2 mmol/l 50 ml 30 4 min 2 ml 6% HClO r/min 10 min 2 ml 6% HClO ml 1 ml n-butanol 0.4 ml 6% HClO ml n-butanol 0.5 ml n-butanol 10 ml (ppo 0.5%, popup 0.02%, 7 3 ) LS6500 (Multipurpose Scintillation Counter) CPM (efficience)( 92%) DPM dpm/nmol CPT 1.5 [4] 37 PBS 0.5 ml Krebs Henseleit bicarbonate buffer (mmol/l: NaHCO NaCl 118 KCl 4.7 MgSO 4 7H 2 O 1.2 NaH 2 PO 4 2H 2 O 1.2 CaCl NaHCO 3 CaCl 2 ph 7.4) 1% BSA, 2.5 mmol/l [U- 14 C]-D- (14.8 GBq/mol) ph min O 2 /CO 2 (19:1) 2~3 min r/min 0.1 ml 1.0 mol/l 14 CO ml 4 mol/l HClO 4 2 h ( ppo 0.5%, popup 0.02% ) 3 h LS6500 Lowery () 37 PBS 0.5 ml Krebs Henseleit bicarbonate buffer ( 1% BSA 2.5 mmol/l [5-3 H]-D-, 14.8 GBq/mol), min O 2 /CO 2 (19:1) 2~3 min r/ min Dowex 1-X4 3 H 2 O [5-3 H]-D- 3 h LS [12] 37 PBS 0.5 ml Krebs Henseleit bicarbonate buffer BSA 40 mg/ml 0.5 mmol/l Na[1-14 C] (74 GBq/µmol), ph min
4 : mean±sd t P< CPT-1 ( 1) PDHt ( pmol/g protein min -1 ) PDHt ( pmol/g protein min -1 ) 8 h PDHa CPT-1 (P<0.05) PDHa (P<0.05) CPT-1 (P<0.05) 8 h PDHa CPT-1 (P<0.05) PDHa (P>0.05) CPT-1 CPT DCA [(16±0.9)% (48±1.1)%, P<0.05] ( P<0.05) DCA (P<0.01) ( 2) 2.3 DCA (P>0.05) ( 8 h, P<0.05) ( 12 h) DCA ( 3) 2.4 DCA (P<0.05) 1. PDHa CPT-1 Fig. 1. Changes of the activity of PDHa and CPT-1 of the hypertrophic cardiomyocytes after hypoxia-reoxygenation. * P<0.05 compared with normal cardiocytes, + P<0.05 compared with each normal oxygen pressure culture group, # P<0.05 compared with each corresponding hypoxia group. 2. DCA Fig. 2. Changes of glucose oxidation rate of hypertrophic cardiocytes after hypoxia-reoxygenation and the DCA effect. * P<0.05 compared with each normal cardiocytes, + P<0.05 compared with normal oxygen pressure culture of each group, # P<0.05 compared with hypoxia group, $ P<0.05 compared with hypertrophic cardiomyocytes in the corresponding time group.
5 640 Acta Physiologica Sinica, October 25, 2005, 57(5): DCA Fig. 3. Alteration of glucoglysis rate of hypertrophy cardiocytes and the effect of DCA interference. + P<0.05 compared with hypoxia 8 h of each group, # P<0.05 compared with hypertrophic cardiocytes in the corresponding time group. 4. DCA Fig. 4. Changes of fatty acid oxidation rate of hypertrophy cardiocytes after hypoxia-reoxygenation and the effect of DCA interference. + P<0.05 compared with hypoxia 8 h of each group, # P<0.05 compared with hypertrophic cardiocytes in the corresponding time group. 1. DCA Table 1. Changes of hypertrophic cardiomyocyte apoptosis stimulated by hypoxia-reoxygenation and the effect of DCA treatment Normal Hypoxia for Reoxygenation Reoxygenation Reoxygenation culture 8 h for 4 h for 8 h for 12 h Normal cardiocyte (NC) * * Hypertrophic cardiocytes (HC) * *# * * DCA treatment + NC DCA treatment + HC * P<0.05 compared with each corresponding normal oxygen culture group, # P<0.05 compared with each corresponding hypoxia culture for 8 h group, P<0.05 compared with each respective normal cardiomyocytes group, P<0.05 compared with each respective NC and HC. ( 4, 8, 12 h, P<0.05) DCA ( 4) 2.5 DCA 8 h ( 4 h) 12 h DCA ( 1) 3 [1]
6 : 641 [12,13] [3] DCA [7] PDHa CPT-1 [14] 8 h PDHa CPT-1 PDHa CPT-1 PDHa CPT-1 8 h PDHa CPT-1 (, P<0.05) [4,13,14] [15] Malhotra Brosius [16] Bialik [17] DCA DCA [18] DCA Salvi [19] α 1 Bcl-2 1 Giffiths EJ. Mitochondria-potential role in cell life and death. Cardiovasc Res 2000; 46(1): Hein S, Arnon E, Kostin S, Schonburg M, Elsasser A, Polyakova V, Bauer EP, Klovekorn WP, Schaper J. Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: structural deterioration and compensatory mechanisms. Circulation 2003; 107(7): Kantor PF, Lucien A, Kozak R, Lopaschuk GD. The antianginal drug trimetazidine shifts cardiac energy metabolism from fatty acid oxidation to glucose oxidation by inhibiting mitochondrial long-chain 3-ketoacyl coenzyme A thiolase. Circ Res 2000; 86(5):
7 642 Acta Physiologica Sinica, October 25, 2005, 57(5): Lopaschuk GD, Wambolt RB, Barr RL. An imbalance between glycolysis and glucose oxidation is a possible explanation for the detrimental effects of high levels of fatty acids during aerobic reperfusion of ischemic hearts. J Pharmacol Exp Ther 1993; 264(1): Pauly DF, Pepine CJ. Ischemic heart disease: metabolic approaches to management. Clin Cardiol 2004; 27(8): Schofield RS, Hill JA. Role of metabolically active drugs in the management of ischemic heart disease. Am J Cardiovasc Drugs 2001; 1(1): Bersin RM, Stacpoole PW. Dichloroacetate as metabolic therapy for myocardial ischemia and failure. Am Heart J 1997; 134 (5 Pt 1): Yang SL( ), He ZY, Feng B, Wang HC, Xiao YB, Zhang H. The establishment of the model for hypoxia-reoxygenation induced apoptosis of culturing human adult hypertrophic cardiomyocytes. Chongqing Med J 2004; 33(1): 4-6 (Chinese, English abstract). 9 Chen H, Li D, Roberts GJ, Saldeen T, Mehta JL. Eicosapentanoic acid inhibits hypoxia-reoxygenation-induced injury by attenuating upregulation of MMP-1 in adult rat myocytes. Cardiovas Res 2003; 59 (1): Collins-Nakai RL, Noseworthy D, Lopaschuk GD. Epinephrine increases ATP production in hearts by preferentially increasing glucose metabolism. Am J Physiol 1994; 267 (5 Pt 2): H1862-H Bremer J, Woldegiorgis G, Schalinske K, Shrago E. Carnitine palmitoyltransferase: activation by palmitoyl-coa and inactivation by malonyl-coa. Biochim Biophys Acta 1985; 833 (1): Sambandam N, Lopaschuk GD, Brownsey RW, Allard MF. Energy metabolism in the hypertrophied heart. Heart Fail Rev 2002; 7(2): Temsah RM, Netticadan T, Kawabata K, Dhalla NS. Lack of both oxygen and glucose contributes to I/R-induced changes in cardiac SR function. Am J Physiol Cell Physiol 2002; 283 (4): C1306-C SchÖnekess BO, Allard MF, Lopaschuk GD. Recovery of glycolysis and oxidative metabolism during postischemic reperfusion of hypertrophied rat hearts. Am J physiol 1996; 271(2 Pt 2): H798-H Huss JM, Levy FH, Kelly DP. Hypoxia inhibits the peroxisome proliferator-activated receptor α/pretinoid X receptor gene regulatory pathway in cardiac myocytes. J Biol Chem 2001; 276(29): Malhotra R, Brosius FC 3rd. Glucose uptake and glycosis reduce hypoxia-induced apoptosis in cultured neonatal rat myocytes. J Biol Chem 1999; 274(18): Bialik S, Cryns VL, Drincic A, Miyata S, Wollowick AL, Srinivasan A, Kitsis RN. The mitochondrial apoptotic pathway is activated by serum and glucose deprivation in cardiac myocytes. Circ Res 1999; 85(5): Liu Q, Docherty JC, Rendell JC, Clanachan AS, Lopaschuk GD. High levels of fatty acids delay the recovery of intracellular ph and cardiac efficiency in post-ischemic hearts by inhibiting glucose oxidation. J Am Coll Cardiol 2002; 39(4): Salvi S. Protecting the myocardium from ischemic injury: a critical role for alpha(1)-adrenoreceptor? Chest 2001; 119 (4):
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