The mitochondrial apoptotic pathway is activated by serum and glucose deprivation in cardiac myocytes

Circulation Research

Volumn 85, Issue 5, 1999, Pages 403-414

  Bialik, Shani ^a,d   Cryns, Vincent L ^b   Drincic, Andjela ^b   Miyata, Setsuya ^a   Wollowick, Adam L ^a   Srinivasan, Anu ^c   Kitsis, Richard N ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b NORTHWESTERN UNIVERSITY MEDICAL CENTER   (United States)

^c PFIZER INC   (United States)

^d WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

Apoptosis; Cysteine proteinase; Cytochrome c; Ischemia; Mitochondria

Indexed keywords

CASPASE; CASPASE 3; CYSTEINE PROTEINASE; CYTOCHROME C; GLUCOSE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; DNA CLEAVAGE; ENZYME ACTIVITY; HEART MITOCHONDRION; HEART MUSCLE ISCHEMIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; RAT; SIGNAL TRANSDUCTION;

EID: 0033520463     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.85.5.403     Document Type: Article

References (63)

1. Itoh G, Tamura J, Suzuki M, Suzuki Y, Ikeda H, Koike M, Nomura M, Jie T, Ito K. DNA fragmentation of human infarcted myocardial cells demonstrated by the nick end labeling method and DNA agarose gel electrophoresis. Am J Pathol. 1995;146:1325-1331.
2. Olivetti G, Quaini F, Sala R, Lagrasta C, Corradi D, Bonacina E, Gambert SR, Cigola E, Anversa P. Acute myocardial infarction in humans is associated with activation of programmed myocyte cell death in the surviving portion of the heart. J Mol Cell Cardiol. 1996;28:2005-2016.
3. Misao J, Hayakawa Y, Ohno M, Kato S, Fujiwara T, Fujiwara H. Expression of Bcl-2 protein, an inhibitor of apoptosis, and Bax, an accelerator of apoptosis, in ventricular myocytes of human hearts with myocardial infarction. Circulation. 1996;94:1506-1512.
4. Saraste A, Pulkki K, Kallajoki M, Henriksen K Parvinen M, Voipio-Pulkki LM. Apoptosis in human acute myocardial infarction. Circulation. 1997;95:320-323.
5. Gottlieb RA, Burleson KO, Kloner RA, Babior BM, Engler RL. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest. 1994;94:1621-1628.
6. Kajstura J, Cheng W, Reiss K, Clark WA, Sonnenblick EH, Krajewski S, Reed JC, Olivetti G, Anversa P. Apoptotic and necrotic myocyte cell deaths are independent contributing variables of infarct size in rats. Lab Invest. 1996;74:86-107.
7. Fliss H, Gattinger D. Apoptosis in ischemic and reperfused rat myocardium. Circ Res. 1996;79:949-956.
8. Cheng W, Kajstura J, Nitahara JA, Li B, Reiss K, Liu Y, Clark WA, Krajewski S, Reed JC, Olivetti, G, Anversa P. Programmed myocyte cell death affects the viable myocardium after infarction in rats. Exp Cell Res. 1996;226:316-327.
9. Bialik S, Geenen DL, Sasson IE, Cheng R, Horner JW, Evans SM, Lord EM, Koch CJ, Kitsis RN. Myocyte apoptosis during acute myocardial infarction in the mouse localizes to hypoxic regions but occurs independently of p53. J Clin Invest. 1997;100:1363-1372.
10. Tanaka M, Hioshi I, Susumu A, Hajime A, Toshio N, Takeshi K, Fumiaki M, Michiaki H. Hypoxia induces apoptosis with enhanced expression of Fas antigen messenger RNA in cultured neonatal rat cardiomyocytes. Circ Res. 1994;75:426-433.
11. Long X, Boluyt MO, Hipolito ML, Lundberg MS, Zheng JS, O'Neill L, Cirielli C, Lakaita EG. Crow MT. p53 and the hypoxia-induced apoptosis of cultured neonatal rat cardiac myocytes. J Clin Invest. 1997;99: 2635-2643.
12. Sheng Z, Knowlton K, Chen J, Hoshijima M, Brown JH, Chien KR. Cardiotrophin 1 (CT-1) inhibition of cardiac myocyte apoptosis via a mitogen-activated protein kinase-dependent pathway: divergence from downstream CT-1 signals for myocardial cell hypertrophy. J Biol Chem. 1997;272:5783-5791.
13. Fujio Y, Kunisada K, Hirota H, Yamauchi-Takihara K, T Kishimoto T. Signals through gp130 upregulate bcl-x gene expression via STAT1-binding cis-element in cardiac myocytes. J Clin Invest. 1997;99: 2898-2905.
14. Umansky SR, Cuenco GM, Khutzian SS, Barr PJ, Tomei LD. Postischemic apoptotic death of rat neonatal cardiomyocytes. Cell Death Differ. 1995;2:235-241.
15. Gottlieb RA, Gruol DL, Zhu JY, Engler RL. Preconditioning rabbit cardiomyocytes: role of pH, vacuolar proton ATPase, and apoptosis. J Clin Invest. 1996;97:2391-2398.
16. Chen SJ, Bradley ME, Lee TC. Chemical hypoxia triggers apoptosis of cultured neonatal rat cardiac myocytes: modulation by calcium-regulated proteases and protein kinases. Mol Cell Biochem. 1998;178:141-149.
17. Pierzchalski P, Reiss K, Cheng W, Cirielli C, Kajstura J, Nitahara JA, Rizk M, Capogrossi MC, Anversa P. p53 induces myocyte apoptosis via the activation of the renin-angiotensin system. Exp Cell Res. 1997;234: 57-65.
18. Krown KA, Page MT, Nguyen C, Zechner D, Gutierrez V, Comstock KL, Glembotski CC, Quintana PJ, Sabbadini RA. Tumor necrosis factor alpha-induced apoptosis in cardiac myocytes: involvement of the sphin-golipid signaling cascade in cardiac cell death. J Clin Invest. 1996;98: 2854-2865.
19. Bielawska AE, Shapiro JP, Jiang L, Melkonyan HS, Piot C, Wolfe CL, Tomei LD, Hannun YA, Umansky SR. Ceramide is involved in triggering of cardiomyocyte apoptosis induced by ischemia and reperfusion. Am J Pathol. 1997;151:1257-1263.
20. Cryns V, Yuan J. Proteases to die for. Genes Dev. 1998;12:1551-1570.
21. Bialik S, Geenen DL, Sasson IE, Valentino KL, Fritz LC, Kitsis RN. The caspase family of cysteine proteases mediate cardiac myocyte apoptosis during myocardial infarction. Circulation. 1997;96(suppl I):I-552. Abstract.
22. Black SC, Huang JQ, Rezaiefar P, Radinovic S, Eberhart A, Nicholson DW, Rodger IW. Co-localization of the cysteine protease caspase-3 with apoptotic myocytes after in vivo myocardial ischemia and reperfusion in the rat. J Mol Cell Cardiol. 1998;30:733-742.
23. Yaoita H, Ogawa K, Maehara K, Maruyama Y. Attenuation of ischemia/ reperfusion injury in rats by a caspase inhibitor. Circulation. 1998;97: 276-281.
24. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell. 1997;90:405-413.
25. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/ caspase-9 complex initiates an apoptotic protease cascade. Cell. 1997;91: 479-489.
26. Srinivasula SM, Ahmad M, Fernandes-Alnemri T, Alnemri ES. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol Cell. 1998;1:949-957.
27. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 1996;86:147-157.
28. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 1997;275:1132-1136.
29. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP, Wang X. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science. 1997;275:1129-1132.
30. Vander Heiden MG, Chandel NS, Williamson EK, Schumacker PT, Thompson CB. Bcl-xL regulates the membrane potential and volume homeostasis of mitochondria. Cell. 1997;91:627-637.
31. Jurgensmeier JM, Xie Z, Deveraux Q, Ellerby L, Bredesen D, Reed JC. Bax directly induces release of cytochrome c from isolated mitochondria. Proc Natl Acad Sci U S A. 1998;95:4997-5002.
32. Rosse T, Olivier R, Monney L, Rager M, Conus S, Fellay I, Jansen B, Borner C. Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature. 1998;391:496-499.
33. Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M, Kroemer G. Mitochondrial control of nuclear apoptosis. J Exp Med. 1996;183:1533-1544.
34. Green DR, Reed JC. Mitochondria and apoptosis. Science. 1998;281: 1309-1312.
35. Bossy-Wetzel E, Newmeyer DD, Green DR. Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J. 1998;17:37-49.
36. Kantrow SP, Piantadosi CA. Release of cytochrome c from liver mitochondria during permeability transition. Biochem Biophys Res Commun. 1997;232:669-671.
37. Ferrari R, Pedersini P, Bongrazio M, Gaia G. Bernocchi P, Di Lisa F, Visioli O. Mitochondrial energy production and cation control in myocardial ischemia and reperfusion. Basic Res Cardiol. 1993;88:495-512.
38. Hakem R, Hakem A, Duncan GS, Henderson JT, Woo M, Soengas MS, Elia A, de la Pompa JL, Kagi D, Khoo W, Potter J. Yoshida R. Kaufman SA, Lowe SW, Penninger JM. Mak TW. Differential requirement for caspase-9 in apoptotic pathways in vivo. Cell. 1998;94:339-352.
39. Kuida K, Haydar TF, Kuan C-Y, Gu Y, Taya C, Karasuyama H, Su MS-S, Rakic P, Flavell RA. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell. 1998;94: 325-337.
40. Yoshida H, Kong Y-Y, Yoshida R, Elia AJ, Hakem A, Hakem R, Penninger JM, Mak TW. Apafl is required for mitochondrial pathways of apoptosis and brain development. Cell. 1998;94:739-750.
41. Cecconi F, Alvarez-Bolado G, Meyer BI, Roth KA, Gruss P. Apafl (CED-4 homolog) regulates programmed cell death in mammalian development. Cell. 1998;94:727-737.
42. Kass-Eisler A, Falck-Pedersen E, Alvira M, Rivera J, Buttrick PM, Wittenberg BA, Cipriani L, Leinwand LA. Quantitative determination of adenovirus-mediated gene delivery to rat cardiac myocytes in vitro and in vivo. Proc Natl Acad Sci U S A. 1993;90:11498-11502.
43. Srinivasan A, Roth K, Sayer RO, Shindler KS, Wong AM, Fritz LC, Tomaselli KJ. In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system. Cell Death Differ. 1998;5:1004-1016.
44. Denizot F, Lang R. Rapid colorimetric assay for cell growth and survival: modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. J Immunol Methods. 1986;89:271-277.
45. Reers M, Smiley ST, Mattola-Hartshom C, Chen A, Lin M, Chen LB. Mitochondrial membrane potential monitored by JC-1 dye. Methods Enzymol. 1995;260:406-417.
46. Johnson LV, Walsh ML, Chen LB. Localization of mitochondria in living cells with rhodamine 123. Proc Natl Acad Sci U S A. 1980;77:990-994.
47. Wen LP, Fahrni JA, Troie S, Guan JL, Orth K, Rosen GD. Cleavage of focal adhesion kinase by caspases during apoptosis. J Biol Chem. 1997; 272;26056-26061.
48. Emoto Y, Manome Y, Meinhardt G, Kisaki H, Kharbanda S, Robertson M, Ghayur T, Wong WW, Kamen R, Weichselbaum R, Kufe D. Proteolytic activation of protein kinase C delta by an ICE-like protease in apoptotic cells. EMBO J. 1995;14:6148-6156.
49. Duan H, Orth K, Chinnaiyan AM, Poirier GG, Froelich CJ, He WW, Dixit VM. ICE-LAP6, a novel member of the ICE/Ced-3 gene family, is activated by the cytotoxic T cell protease granzyme B. J Biol Chem. 1996;271:16720-16724.
50. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 1998; 94:491-501.
51. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. Bid. a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 1998;94: 481-490.
52. Medema JP, Scaffidi C, Kischkel FC, Shevchenko A, Mann M, Krammer PH. Peter ME. FLICE is activated by association with the CD95 death-inducing signaling complex (DISC). EMBO J. 1997;16:2794-2804.
53. Mancini M, Nicholson DW, Roy S, Thornberry NA, Peterson EP, Casciola-Rosen LA, Rosen A. The caspase-3 precursor has a cytosolic and mitochondrial distribution: implications for apoptotic signaling. J Cell Biol. 1998;140:1485-1495.
54. Franke TF, Cantley LC. Apoptosis: a Bad kinase makes good. Nature. 1997;390:116-117.
55. Cardone, MH, Roy, N, Stennicke, HR, Salvesen GS, Franke, TF, Stanbridge, E, Frisch, S, Reed, JC. Regulation of cell death protease caspase-9 by phosphorylation. Science. 1998;282:1318-1321.
56. Thakkar NS, Potten CS. Inhibition of doxorubicin-induced apoptosis in vivo by 2-deoxy-D-glucose. Cancer Res. 1993;53:2057-2060.
57. Eguchi Y, Shimizu S, Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 1997;57:1835-1840.
58. Chou CC, Lam CY, Yung BY. Intracellular ATP is required for actinomycin D-induced apoptotic cell death in HeLa cells. Cancer Lett. 1995;96:181-187.
59. Leist M, Single B, Castoldi AF, Kuhnle S, Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med. 1997;185:1481-1486.
60. Halicka HD, Ardelt B, Li X, Melamed MM, Darzynkiewicz Z. 2-Deoxy-D-glucose enhances sensitivity of human histiocytic lymphoma U937 cells to apoptosis induced by tumor necrosis factor. Cancer Res. 1995; 55:444-449.
61. Garland JM, Halestrap A. Energy metabolism during apoptosis: Bcl-2 promotes survival in hematopoietic cells induced to apoptose by growth factor withdrawal by stabilizing a form of metabolic arrest. J Biol Chem. 1997;272:4680-4688.
62. Lee YJ, Galoforo SS, Berns CM, Tong WP, Kim HR, Corry PM. Glucose deprivation-induced cytotoxicity in drug resistant human breast carcinoma MCF-7/ADR cells: role of c-myc and bcl-2 in apoptotic cell death. J Cell Sci. 1997;110:681-686.
63. Malhotra R, Brosius FC III. Glucose uptake and glycolysis reduce hypoxia-induced apoptosis in cultured neonatal rat cardiac myocytes. J Biol Chem. 1999;274:12567-12575.