Ca2+ influx-induced sarcoplasmic reticulum Ca2+ overload causes mitochondrial-dependent apoptosis in ventricular myocytes

Circulation Research

Volumn 97, Issue 10, 2005, Pages 1009-1017

  Chen, Xiongwen ^a   Zhang, Xiaoying ^a   Kubo, Hajime ^a   Harris, David M ^a   Mills, Geoffrey D ^a   Moyer, Jed ^a   Berretta, Remus ^a   Potts, Sabine Telemaque ^b   Marsh, James D ^b   Houser, Steven R ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

2a subunit; Apoptosis; L type calcium channel; Primary culture; Ventricular myocyte

Indexed keywords

CALCIUM CHANNEL L TYPE; CALCIUM ION; CALPAIN; CASPASE 3; CASPASE 9; CASPASE INHIBITOR; CYTOCHROME C; GREEN FLUORESCENT PROTEIN; PROTEIN BCL 2; PROTEIN X; CALCIUM; CALMODULIN DEPENDENT PROTEIN KINASE II; CALMODULIN-DEPENDENT PROTEIN KINASE II; CASP8 PROTEIN, RAT; CASPASE; CASPASE 8; L TYPE CALCIUM CHANNEL ALPHA(1C); L-TYPE CALCIUM CHANNEL ALPHA(1C); PROTEIN BAK; PROTEIN BAX; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN SUBUNIT;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM CURRENT; CALCIUM TRANSPORT; CONTROLLED STUDY; ENZYME RELEASE; HEART MUSCLE CONTRACTILITY; HEART VENTRICLE WALL; MUSCLE CELL; MUSCLE FIBER CULTURE; NONHUMAN; PRIORITY JOURNAL; SARCOPLASMIC RETICULUM; ANIMAL; CAT; CELL CULTURE; HEART CONTRACTION; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART VENTRICLE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; RAT;

ANIMALS; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BCL-2-ASSOCIATED X PROTEIN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CALCIUM CHANNELS, L-TYPE; CASPASE 8; CASPASES; CATS; CELLS, CULTURED; HEART VENTRICLES; MITOCHONDRIA, HEART; MYOCARDIAL CONTRACTION; MYOCYTES, CARDIAC; PHOSPHORYLATION; PROTEIN SUBUNITS; RATS; SARCOPLASMIC RETICULUM;

EID: 27944487173     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000189270.72915.D1     Document Type: Article

References (35)

1. Shorofsky SR, Aggarwal R, Corretti M, Baffa JM, Strum JM, Al-Seikhan BA, Kobayashi YM, Jones LR, Wier WG, Balke CW. Cellular mechanisms of altered contractility in the hypertrophied heart: big hearts, big sparks. Circ Res. 1999;84:424-434.
2. Bristow MR, Kantrowitz NE, Ginsburg R, Fowler MB. Beta-adrenergic function in heart muscle disease and heart failure. J Mol Cell Cardiol. 1985;17(suppl 2):41-52.
3. Frey N, Olson EN. Cardiac hypertrophy: the good, the bad, and the ugly. Annu Rev Physiol. 2003;65:45-79.
4. Gill C, Mestril R, Samali A. Losing heart: the role of apoptosis in heart disease: a novel therapeutic target? FASEB J. 2002;16:135-146.
5. Communal C, Singh K, Pimentel DR, Colucci WS. Norepinephrine stimulates apoptosis in adult rat ventricular myocytes by activation of the beta-adrenergic pathway. Circulation. 1998;98:1329-1334.
6. Saito S, Hiroi Y, Zou Y, Aikawa R, Toko H, Shibasaki F, Yazaki Y, Nagai R, Komuro I. Beta-adrenergic pathway induces apoptosis through calcineurin activation in cardiac myocytes. J Biol Chem. 2000;275:34528-34533.
7. Zhu WZ, Wang SQ, Chakir K, Yang D, Zhang T, Brown JH, Devic E, Kobilka BK, Cheng H, Xiao RP. Linkage of beta1-adrenergic stimulation to apoptotic heart cell death through protein kinase A-independent activation of Ca2+/calmodulin kinase II. J Clin Invest. 2003;111:617-625.
8. Goldenberg I, Grossman E, Jacobson KA, Shneyvays V, Shainberg A. Angiotensin II-induced apoptosis in rat cardiomyocyte culture: a possible role of AT1 and AT2 receptors. J Hypertens. 2001;19:1681-1689.
9. Gao F, Gong B, Christopher TA, Lopez BL, Karasawa A, Ma XL. Anti-apoptotic effect of benidipine, a long-lasting vasodilating calcium antagonist, in ischaemic/reperfused myocardial cells. Br J Pharmacol. 2001;132:869-878.
10. Henaff M, Antoine S, Mercadier JJ, Coulombe A, Hatem SN. The voltage-independent B-type Ca2+ channel modulates apoptosis of cardiac myocytes. FASEB J. 2002;16:99-101.
11. Tanaka T, Nangaku M, Miyata T, Inagi R, Ohse T, Ingelfinger JR, Fujita T. Blockade of calcium influx through L-type calcium channels attenuates mitochondrial injury and apoptosis in hypoxic renal tubular cells. J Am Soc Nephrol. 2004;15:2320-2333.
12. Cano-Abad MF, Villarroya M, Garcia AG, Gabilan NH, Lopez MG. Calcium entry through L-type calcium channels causes mitochondrial disruption and chromaffin cell death. J Biol Chem. 2001;276:39695-39704.
13. Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol. 2003;4:552-565.
14. Canzoniero LM, Babcock DJ, Gottron FJ, Grabb MC, Manzerra P, Snider BJ, Choi DW. Raising intracellular calcium attenuates neuronal apoptosis triggered by staurosporine or oxygen-glucose deprivation in the presence of glutamate receptor blockade. Neurobiol Dis. 2004;15:520-528.
15. Crow MT, Mani K, Nam YJ, Kitsis RN. The mitochondrial death pathway and cardiac myocyte apoptosis. Circ Res. 2004;95:957-970.
16. Balaban RS. Cardiac energy metabolism homeostasis: role of cytosolic calcium. J Mol Cell Cardiol. 2002;34:1259-1271.
17. Nitahara JA, Cheng W, Liu Y, Li B, Leri A, Li P, Mogul D, Gambert SR, Kajstura J, Anversa P. Intracellular calcium, DNase activity and myocyte apoptosis in aging Fischer 344 rats. J Mol Cell Cardiol. 1998;30:519-535.
18. Bers DM. Cardiac Na/Ca exchange function in rabbit, mouse and man: what's the difference? J Mol Cell Cardiol. 2002;34:369-373.
19. Bailey BA, Houser SR. Sarcoplasmic reticulum-related changes in cytosolic calcium in pressure-overload-induced feline LV hypertrophy. Am J Physiol. 1993;265:H2009-H2016.
20. Colecraft HM, Alseikhan B, Takahashi SX, Chaudhuri D, Mittman S, Yegnasubramanian V, Alvania RS, Johns DC, Marban E, Yue DT. Novel functional properties of Ca(2+) channel beta subunits revealed by their expression in adult rat heart cells. J Physiol. 2002;541:435-452.
21. Stern MD, Capogrossi MC, Lakatta EG. Spontaneous calcium release from the sarcoplasmic reticulum in myocardial cells: mechanisms and consequences. Cell Calcium. 1988;9:247-256.
22. Chen X, Piacentino V 3rd, Furukawa S, Goldman B, Margulies KB, Houser SR. L-type Ca2+ channel density and regulation are altered in failing human ventricular myocytes and recover after support with mechanical assist devices. Circ Res. 2002;91:517-524.
23. Szabadkai G, Rizzuto R. Participation of endoplasmic reticulum and mitochondrial calcium handling in apoptosis: more than just neighborhood? FEBS Lett. 2004;567:111-115.
24. Davis BA, Schwartz A, Samaha FJ, Kranias EG. Regulation of cardiac sarcoplasmic reticulum calcium transport by calcium-calmodulin-dependent phosphorylation. J Biol Chem. 1983;258:13587-13591.
25. Ledoux J, Chartier D, Leblanc N. Inhibitors of calmodulin-dependent protein kinase are nonspecific blockers of voltage-dependent K+ channels in vascular myocytes. J Pharmacol Exp Ther. 1999;290:1165-1174.
26. Xiao RP, Cheng H, Lederer WJ, Suzuki T, Lakatta EG. Dual regulation of Ca2+/calmodulin-dependent kinase II activity by membrane voltage and by calcium influx. Proc Natl Acad Sci U S A. 1994;91:9659-9663.
27. De Windt LJ, Lim HW, Taigen T, Wencker D, Condorelli G, Dorn GW 2nd, Kitsis RN, Molkentin JD. Calcineurin-mediated hypertrophy protects cardiomyocytes from apoptosis in vitro and in vivo: an apoptosis-independent model of dilated heart failure. Circ Res. 2000;86:255-263.
28. Fabiato A. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol. 1983;245:C1-C14.
29. Satoh H, Katoh H, Velez P, Fill M, Bers DM. Bay K 8644 increases resting Ca2+ spark frequency in ferret ventricular myocytes independent of Ca influx: contrast with caffeine and ryanodine effects. Circ Res. 1998;83:1192-1204.
30. Muth JN, Bodi I, Lewis W, Varadi G, Schwartz A. A Ca(2+)-dependent transgenic model of cardiac hypertrophy: a role for protein kinase Calpha. Circulation. 2001;103:140-147.
31. Ma TS, Mann DL, Lee JH, Gallinghouse GJ. SR compartment calcium and cell apoptosis in SERCA overexpression. Cell Calcium. 1999;26:25-36.
32. Tantral L, Malathi K, Kohyama S, Silane M, Berenstein A, Jayaraman T. Intracellular calcium release is required for caspase-3 and -9 activation. Cell Biochem Funct. 2004;22:35-40.
33. Pollack PS, Carson NL, Nuss HB, Marino TA, Houser SR. Mechanical properties of adult feline ventricular myocytes in culture. Am J Physiol. 1991;260:H234-H241.
34. Mitcheson JS, Hancox JC, Levi AJ. Cultured adult cardiac myocytes: future applications, culture methods, morphological and electrophysiological properties. Cardiovasc Res. 1998;39:280-300.
35. Torella D, Rota M, Nurzynska D, Musso E, Monsen A, Shiraishi I, Zias E, Walsh K, Rosenzweig A, Sussman MA, Urbanek K, Nadal-Ginard B, Kajstura J, Anversa P, Leri A. Cardiac stem cell and myocyte aging, heart failure, and insulin-like growth factor-1 overexpression. Circ Res. 2004;94:514-524.