Death begets failure in the heart

Journal of Clinical Investigation

Volumn 115, Issue 3, 2005, Pages 565-571

  Foo, Roger S Y ^a   Mani, Kartik ^a   Kitsis, Richard N ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS INDUCING FACTOR; APOPTOSIS INHIBITOR; CASPASE 8; CASPASE INHIBITOR; CYTOCHROME C; FAS ANTIGEN; FAS LIGAND; PROTEIN BCL 2; PROTEIN KINASE B; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; AUTOPHAGY; CELL DEATH; CELL SURVIVAL; CONGESTIVE CARDIOMYOPATHY; GENE EXPRESSION; HEART FAILURE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HUMAN; IN VIVO STUDY; NECROSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TRANSGENE;

EID: 14644413468     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI24569     Document Type: Review

References (125)

1. Mann, D.L. 1999. Mechanisms and models in heart failure: a combinatorial approach. Circulation. 100:999-1008.
2. Lower, R. 1669. Tractatus de corde. Item de motu et colore sanguinis et chyli in eum transitu. Jo. Redmayne for Jacob Allestry. London, United Kingdom.
3. Lefkowicz, R.J, Rockman, H.A., and Koch, W.J. 2000. Catecholamines, cardiac beta-adrenergic receptors, and heart failure. Circulation. 101:1634-1637.
4. Marks, A.R. 2002. Ryanodine receptors, FKBP12, and heart failure. Front. Biosci. 7:d970-d977.
5. Luo, W., et al. 1994. Targeted ablation of the phospholamban gene is associated with markedly enhanced myocardial contractility and loss of beta-agonist stimulation. Circ. Res. 75:401-409.
6. Chien, K.R. 1999. Stress pathways and heart failure. Cell. 98:555-558.
7. Nakao, K., Minobe, W., Roden, R., Bristow, M.R., and Leinwand, L.A. 1997. Myosin heavy chain gene expression in human heart failure. J. Clin. Invest. 100:2362-2370.
8. Taegtmeyer, H. 2002. Switching metabolic genes to build a better heart. Circulation. 106:2043-2045.
9. Kelly, D.P., and Strauss, A.W. 1994. Inherited cardiomyopathies. N. Engl. J. Med. 330:913-919.
10. Danial, N.N., and Korsmeyer, S.J. 2004. Cell death: critical control points. Cell. 116:205-219.
11. Yuan, J., Lipinski, M., and Degterev, A. 2003. Diversity in the mechanisms of neuronal cell death. Neuron. 40:401-413.
12. Zong, W.X., Ditsworth, D., Bauer, D.E., Wang, Z.Q., and Thompson, C.B. 2004. Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev. 18:1272-1282.
13. Klionsky, D.J., and Emr, S.D. 2000. Autophagy as a regulated pathway of cellular degradation. Science. 290:1717-1721.
14. Shintani, T., and Klionsky, D.J. 2004. Autophagy in health and disease: a double-edged sword. Science. 306:990-995.
15. Ashkenazi, A., and Dixit, V.M. 1998. Death receptors: signaling and modulation. Science. 281:1305-1308.
16. Kischkel, F.C., et al. 1995. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J. 14:5579-5588.
17. Boldin, M.P., Goncharov, T.M., Goltsev, Y.V., and Wallach, D. 1996. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell. 85:803-815.
18. Muzio, M., et al. 1996. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell. 85:817-827.
19. Boatright, K.M., et al. 2003. A unified model for apical caspase activation. Mol. Cell. 11:529-541.
20. Crow, M.T., Mani, K., Nam, Y.J., and Kitsis, R.N. 2004. The mitochondrial death pathway and cardiac myocyte apoptosis. Circ. Res. 95:957-970.
21. Liu, X., Kim, C.N., Yang, J., Jemmerson, R., and Wang, X. 1996. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 86:147-157.
22. Kluck, R.M., Bossy-Wetzel, E., Green, D.R., and Newmeyer, D.D. 1997. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 275:1132-1136.
23. Du, C., Fang, M., Li, Y., Li, L., and Wang, X. 2000. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 102:33-42.
24. Verhagen, A.M., et al. 2000. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell. 102:43-53.
25. Suzuki, Y., et al. 2001. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol. Cell. 8:613-621.
26. Susin, S.A., et al. 1999. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature. 397:441-446.
27. Li, L.Y., Luo, X., and Wang, X. 2001. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature. 412:95-99.
28. Zou, H., Henzel, W.J., Liu, X., Lutschg, A., and Wang, X. 1997 Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell. 90:405-413.
29. Li, P., et al. 1997 Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 91:479-489.
30. Srinivasula, S.M., Ahmad, M., Fernandes-Alnemri, T., and Alnemri, E.S. 1998. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol. Cell. 1:949-957.
31. Hu, Y., Ding, L., Spencer, D.M., and Nunez, G. 1998. WD-40 repeat region regulates Apaf-1 self-association and procaspase-9 activation. J. Biol. Chem. 273:33489-33494.
32. Saleh, A., Srinivasula, S.M., Acharya, S., Fishel, R., and Alnemri, E.S. 1999. Cytochrome c and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation. J. Biol. Chem. 274:17941-17945.
33. Zou, H., Li, Y., Liu, X., and Wang, X. 1999. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 274:11549-11556.
34. Qin, H., et al. 1999. Structural basis of procaspase-9 recruitment by the apoptotic protease-activating factor 1. Nature. 399:549-557.
35. Vaughn, D.E., Rodriguez, J., Lazebnik, Y., and Joshua-Tor, L. 1999. Crystal structure of Apaf-1 caspase recruitment domain: an alpha-helical Greek key fold for apoptotic signaling. J. Mol. Biol. 293:439-447.
36. Zhou, P., Chou, J., Olea, R.S., Yuan, J., and Wagner, G. 1999. Solution structure of Apaf-1 CARD and its interaction with caspase-9 CARD: a structural basis for specific adaptor/caspase interaction. Proc. Natl. Acad. Sci. U. S. A. 96:11265-11270.
37. Day, C.L., Dupont, C., Lackmann, M., Vaux, D.L., and Hinds, M.G. 1999. Solution structure and mutagenesis of the caspase recruitment domain (CARD) from Apaf-1. Cell Death Differ. 6:1125-1132.
38. Jiang, X., and Wang, X. 2000. Cytochrome c promotes caspase-9 activation by inducing nucleotide binding to Apaf-1. J. Biol. Chem. 275:31199-31203.
39. Acehan, D., et al. 2002. Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol. Cell. 9:423-432.
40. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. 1998. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 94:481-490.
41. Li, H., Zhu, H., Xu, C.J., and Yuan, J. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94:491-501.
42. Gross, A., et al. 1999. Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J. Biol. Chem. 274:1156-1163.
43. Peter, M.E. 2004. The flip side of FLIP. Biochem. J. 382:e1-e3.
44. Sawada, M., et al. 2003. Ku70 suppresses the apoptotic translocation of Bax to mitochondria. Nat. Cell Biol. 5:320-329.
45. Guo, B., et al. 2003. Humanin peptide suppresses apoptosis by interfering with Bax activation. Nature. 423:456-461.
46. Sun, C., et al. 2000. NMR structure and mutagenesis of the third Bir domain of the inhibitor of apoptosis protein XIAP. J. Biol. Chem. 275:33777-33781.
47. Chai, J., et al. 2001. Structural basis of caspase-7 inhibition by XIAP. Cell. 104:769-780.
48. Huang, Y., et al. 2001. Structural basis of caspase inhibition by XIAP: differential roles of the linker versus the BIR domain. Cell. 104:781-790.
49. Riedl, S.J., et al. 2001. Structural basis for the inhibition of caspase-3 by XIAP. Cell. 104:791-800.
50. Shiozaki, E.N., et al. 2003. Mechanism of XIAP-mediated inhibition of caspase-9. Mol. Cell. 11:519-527.
51. Nam, Y.J., et al. 2004. Inhibition of both the extrinsic and intrinsic death pathways through nonhomotypic death-fold interactions. Mol. Cell. 15:901-912.
52. Koseki, T., Inohara, N., Chen, S., and Nunez, G. 1998. ARC, an inhibitor of apoptosis expressed in skeletal muscle and heart that interacts selectively with caspases. Proc. Natl. Acad. Sci. U. S. A. 95:5156-5160.
53. Gustafsson, A.B., Tsai, J.G., Logue, S.E., Crow, M.T., and Gottlieb, R.A. 2004. Apoptosis repressor with caspase recruitment domain protects against cell death by interfering with Bax activation. J. Biol. Chem. 279:21233-21238.
54. Potts, P.R., Singh, S., Knezek, M., Thompson, C.B., and Deshmukh, M. 2003. Critical function of endogenous XIAP in regulating caspase activation during sympathetic neuronal apoptosis. J. Cell Biol. 163:789-799.
55. Yang, Q.H., Church-Hajduk, R., Ren, J., Newton, M.L., and Du, C. 2003. Omi/HtrA2 catalytic cleavage of inhibitor of apoptosis (IAP) irreversibly inactivates IAPs and facilitates caspase activity in apoptosis. Genes Dev. 17:1487-1496.
56. Scorrano, L., et al. 2003. BAX and BAK regulation of endoplasmic reticulum Ca2+: acontrol point for apoptosis. Science. 300:135-139.
57. Morishima, N., Nakanishi, K., Tsuchiya, K., Shibata, T., and Seiwa, E. 2004. Translocation of Bim to the endoplasmic reticulum (ER) mediates ER stress signaling for activation of caspase-12 during ER stress-induced apoptosis. J. Biol. Chem. 279:50375-50381.
58. Oakes, S.A., et al. 2005. Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc. Natl. Acad. Sci. U. S. A. 102:105-110.
59. Halestrap, A.P., McStay, G.P., and Clarke, S.J. 2002. The permeability transition pore complex: another view. Biochimie. 84:153-166.
60. Scorrano, L., et al. 2002. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev. Cell. 2:55-67.
61. Nakagawa, T., et al. 2000. Caspase-12 mediates endoplasmic-reticulum- specific apoptosis and cytotoxicity by amyloid-beta. Nature. 403:98-103.
62. Szegezdi, E., Fitzgerald, U., and Samali, A. 2003. Caspase-12 and ER-stress-mediated apoptosis: the story so far. Ann. N. Y. Acad. Sci. 1010:186-194.
63. Nakagawa, T., and Yuan, J. 2000. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell Biol. 150:887-894.
64. Morishima, N., Nakanishi, K., Takenouchi, H., Shibata, T., and Yasuhiko, Y. 2002. An endoplasmic reticulum stress-specific caspase cascade in apoptosis. Cytochrome c-independent activation of caspase-9 by caspase-12. J. Biol. Chem. 277:34287-34294.
65. Saleh, M., et al. 2004. Differential modulation of endotoxin responsiveness by human caspase-12 polymorphisms. Nature. 429:75-79.
66. Gottlieb, R.A., Burleson, K.O., Kloner, R.A., Babior, B.M., and Engler, R.L. 1994. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J. Clin. Invest. 94:1621-1628.
67. Fliss, H., and Gattinger, D. 1996. Apoptosis in ischemic and reperfused rat myocardium. Circ. Res. 79:949-956.
68. Lee, P., et al. 2003. Fas pathway is a critical mediator of cardiac myocyte death and MI during ischemia-reperfusion in vivo. Am. J. Physiol. Heart Circ. Physiol. 284:H456-H463.
69. Jeremias, I., et al. 2000. Involvement of CD95/Apo1/Fas in cell death after myocardial ischemia. Circulation. 102:915-920.
70. Peng, C.-F., et al. 2001. Multiple independent mutations in apoptotic signaling pathways markedly decrease infarct size due to myocardial ischemia-reperfusion [abstract]. Circulation. 104(Suppl. II):II-187.
71. Brocheriou, V., et al. 2000. Cardiac functional improvement by a human Bcl-2 transgene in a mouse model of ischemia/reperfusion injury. J. Gene Med. 2:326-333.
72. Chen, Z., Chua, C.C., Ho, Y.S., Hamdy, R.C., and Chua, B.H. 2001. Overexpression of Bcl-2 attenuates apoptosis and protects against myocardial I/R injury in transgenic mice. Am. J. Physiol. Heart Circ. Physiol. 280:H2313-H2320.
73. Guerra, S., et al. 1999. Myocyte death in the failing human heart is gender dependent. Circ. Res. 85:856-866.
74. Hein, S., et al. 2003. Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: structural deterioration and compensatory mechanisms. Circulation. 107:984-991.
75. Olivetti, G., et al. 1997. Apoptosis in the failing human heart. N. Engl. J. Med. 336:1131-1141.
76. Saraste, A., et al. 1999. Cardiomyocyte apoptosis and progression of heart failure to transplantation. Eur. J. Clin. Invest. 29:380-386.
77. Wencker, D., et al. 2003. A mechanistic role for cardiac myocyte apoptosis in heart failure. Cell. 111:1497-1504.
78. Dorn, G.W., 2nd, and Brown, J.H. 1999. Gq signaling in cardiac adaptation and maladaptation. Trends Cardiovasc. Med. 9:26-34.
79. D'Angelo, D.D., et al. 1997. Transgenic Galphaq overexpression induces cardiac contractile failure in mice. Proc. Natl. Acad. Sci. U. S. A. 94:8121-8126.
80. Adams, J.W., et al. 1998. Enhanced Galphaq signaling: a common pathway mediates cardiac hypertrophy and apoptotic heart failure. Proc. Natl. Acad. Sci. U. S. A. 95:10140-10145.
81. Sakata, Y., Hoit, B.D., Liggett, S.B., Walsh, R.A., and Dorn, G.W., 2nd. 1998. Decompensation of pressure-overload hypertrophy in G alpha q-overexpressing mice. Circulation. 97:1488-1495.
82. Yussman, M.G., et al. 2002. Mitochondrial death protein Nix is induced in cardiac hypertrophy and triggers apoptotic cardiomyopathy. Nat. Med. 8:725-730.
83. Hayakawa, Y., et al. 2003. Inhibition of cardiac myocyte apoptosis improves cardiac function and abolishes mortality in the peripartum cardiomyopathy of Galpha(q) transgenic mice. Circulation. 108:3036-3041.
84. Chatterjee, S., et al. 2002. Viral gene transfer of the antiapoptotic factor Bcl-2 protects against chronic postischemic heart failure. Circulation. 106:I212-I217.
85. Chatterjee, S., et al. 2003. Blocking the development of postischemic cardiomyopathy with viral gene transfer of the apoptosis repressor with caspase recruitment domain. J. Thorac. Cardiovasc. Surg. 125:1461-1469.
86. Hirota, H., et al. 1999. Loss of a gp130 cardiac muscle cell survival pathway is a critical event in the onset of heart failure during biomechanical stress. Cell. 97:189-198.
87. Fujio, Y., Kunisada, K., Hirota, H., Yamauchi-Takihara, K., and Kishimoto, T. 1997. Signals through gp130 upregulate bcl-x gene expression via STAT1-binding cis-element in cardiac myocytes. Cell. 99:2898-2905.
88. Xing, H., Zhang, S., Weinheimer, C., Kovacs, A., and Muslin, A.J. 2000. 14-3-3 proteins block apoptosis and differentially regulate MAPK cascades. EMBO J. 19:349-358.
89. Zhang, D., et al. 2000. TAK1 is activated in the myocardium after pressure overload and is sufficient to provoke heart failure in transgenic mice. Nat. Med. 6:556-563.
90. Cheng, W., et al. 1995. Stretch-induced programmed myocyte cell death. Cell. 96:2247-2259.
91. Ide, T., et al. 2000. Direct evidence for increased hydroxyl radicals originating from superoxide in the failing myocardium. Circ. Res. 86:152-157.
92. Communal, C., Singh, K., Pimentel, D.R., and Colucci, W.S. 1998. Norepinephrine stimulates apoptosis in adult rat ventricular myocytes by activation of the beta-adrenergic pathway. Circulation. 98:1329-1334.
93. Shizukuda, Y., et al. 1998. beta-adrenergic stimulation causes cardiocyte apoptosis: influence of tachycardia and hypertrophy. Am J. Physiol. 275:H961-H968.
94. Cigola, E., Kajstura, J., Li, B., Meggs, L.G., and Anversa, P. 1997. Angiotensin II activates programmed myocyte cell death in vitro. Exp. Cell Res. 231:363-371.
95. Mann, D.L. 1999. Inflammatory mediators in heart failure: homogeneity through heterogeneity. Lancet. 353:1812-1813.
96. Nikolova, V., et al. 2004. Defects in nuclear structure and function promote dilated cardiomyopathy in lamin A/C-deficient mice. Cell. 113:357-369.
97. Wang, L., Ma, W., Markovich, R., Chen, J.W., and Wang, P.H. 1998. Regulation of cardiomyocyte apoptotic signaling by insulin-like growth factor I. Circ. Res. 83:516-522.
98. Oh, H., et al. 2001. Telomerase reverse transcriptase promotes cardiac muscle cell proliferation, hypertrophy, and survival. Proc. Natl. Acad. Sci. U. S. A. 98:10308-10313.
99. Leri, A., et al. 2003. Ablation of telomerase and telomere loss leads to cardiac dilatation and heart failure associated with p53 upregulation. EMBO J. 22:131-139.
100. Oh, H., et al. 2003. Telomere attrition and Chk2 activation in human heart failure. Proc. Natl. Acad. Sci. U. S. A. 100:5378-5383.
101. Okada, K., et al. 2004. Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation. 110:705-712.
102. Chesley, A., et al. 2000. The beta(2)-adrenergic receptor delivers an antiapoptotic signal to cardiac myocytes through G(i)-dependent coupling to phosphatidylinositol 3′-kinase. Circ. Res. 87:1172-1179.
103. Xiao, R.P. 2001. Beta-adrenergic signaling in the heart: dual coupling of the beta2- adrenergic receptor to G(s) and G(i) proteins. Sci. STKE. 2001:RE15.
104. Datta, S.R., et al. 1997. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell. 91:231-241.
105. Mehrhof, F.B., et al. 2001. In cardiomyocyte hypoxia, insulin-like growth factor-I-induced antiapoptotic signaling requires phosphatidylinositlol-3-OH- kinase-dependent and mitogen-activated protein kinase-dependent activation of the transcription factor cAMP response element-binding protein. Circulation. 104:2088-2094.
106. Romashkova, J.A., and Makarov, S.S. 1999. NF-kappaB is a target of AKT in anti-apoptotic PDGF signalling. Nature. 401:86-90.
107. Brunet, A., et al. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 96:857-868.
108. Cardone, M.H., et al. 1998. Regulation of cell death protease caspase-9 by phosphorylation. Science. 282:1318-1321.
109. Fujita, E., et al. 1999. Akt phosphorylation site found in human caspase-9 is absent in mouse caspase-9. Biochem. Biophys. Res. Commun. 264:550-555.
110. Matsui, T., et al. 1999. Adenoviral gene transfer of activated phosphatidylinositol 3′-kinase and Akt inhibits apoptosis of hypoxic cardiomyocytes in vitro. Circulation. 100:2373-2379.
111. Fujio, Y., Nguyen, T., Wencker, D., Kitsis, R.N., and Walsh, K. 2000. Akt promotes survival of cardiomyocytes in vitro and protects against ischemiareperfusion injury in mouse heart. Circulation. 101:660-667.
112. Bock-Matquette, I., Saxena, A., White, M.D., Dimaio, J.M., and Srivastava, D. 2004. Thymosin beta4 activates integrin-linked kinase and promotes cardiac cell migration, survival and cardiac repair. Nature. 432:466-472.
113. Buerke, M., et al. 1995. Cardioprotective effect of insulin-like growth factor I in myocardial ischemia followed by reperfusion. Proc. Natl. Acad. Sci. U. S. A. 92:8031-8035.
114. Li, Q., et al. 1997. Overexpression of insulin-like growth factor-1 in mice protects from myocyte death after infarction, attenuating ventricular dilation, wall stress, and cardiac hypertrophy. Cell. 100:1991-1999.
115. Miao, W., Luo, Z., Kitsis, R.N., and Walsh, K. 2000. Intracoronary, adenovirus-mediated Akt gene transfer in heart limits infarct size following ischemia-reperfusion injury in vivo. J. Mol. Cell. Cardiol. 32:2397-2402.
116. Matsui, T., et al. 2001. Akt activation preserves cardiac function and prevents injury after transient cardiac ischemia in vivo. Circulation. 104:330-335.
117. Chao, W., et al. 2003. Strategic advantages of insulin-like growth factor-I expression for cardioprotection. J. Gene Med. 5:277-286.
118. Welch, S., et al. 2002. Cardiac-specific IGF-1 expression attenuates dilated cardiomyopathy in tropomodulin-overexpressing transgenic mice. Circ. Res. 90:641-648.
119. Reiss, K., et al. 1996. Overexpression of insulin-like growth factor-1 in the heart is coupled with myocyte proliferation in transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 93:8630-8635.
120. Fazio, S., et al. 1996. A preliminary study of growth hormone in the treatment of dilated cardiomyopathy. N. Engl. J. Med. 334:809-814.
121. Matsui, T., et al. 2002. Phenotypic spectrum caused by transgenic overexpression of activated Akt in the heart. J. Biol. Chem. 277:22896-22901.
122. Pennica, D., Wood, W.I., and Chien, K.R. 1996. Cardiotrophin-1: a multifunctional cytokine that signals via LIF receptor-gp 130 dependent pathways. Cytokine Growth Factor Rev. 7:81-91.
123. Yaoita, H., Ogawa, K., Maehara, K., and Maruyama, Y. 1998. Attenuation of ischemia/reperfusion injury in rats by a caspase inhibitor. Circulation. 97:276-281.
124. Holly, T.A., et al. 1999. Caspase inhibition reduces myocyte cell death induced by myocardial ischemia and reperfusion in vivo. J. Mol. Cell. Cardiol. 31:1709-1715.
125. Huang, J.Q., Radinovic, S., Rezaiefar, P., and Black, S.C. 2000. In vivo myocardial infarct size reduction by a caspase inhibitor administered after the onset of ischemia. Eur. J. Pharmacol. 402:139-142.