"How Do Cardiomyocytes Die?" Apoptosis and Autophagic Cell Death in Cardiac Myocytes

Journal of Cardiac Failure

Volumn 12, Issue 5, 2006, Pages 381-391

  Kunapuli, Sanjay ^a   Rosanio, Salvatore ^a   Schwarz, Ernst R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEINASE; UBIQUITIN;

APOPTOSIS; ATROPHY; AUTOPHAGY; CARDIOVASCULAR DISEASE; CARDIOVASCULAR SYSTEM; CELL DEATH; CELL LOSS; DEGENERATION; HEART DISEASE; HEART FAILURE; HEART MUSCLE CELL; HUMAN; HYPERTENSION; ISCHEMIC HEART DISEASE; NECROSIS; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

APOPTOSIS; CARDIOVASCULAR DISEASES; CELL DEATH; HUMANS; MYOCYTES, CARDIAC; PHAGOCYTOSIS;

EID: 33744525885     PISSN: 10719164     EISSN: 15328414     Source Type: Journal    
DOI: 10.1016/j.cardfail.2006.02.002     Document Type: Review

References (143)

1. MacLellan W.R., and Schneider M.D. Death by design: programmed cell death in cardiovascular biology and disease. Circ Res 81 (1997) 137-144
2. Hetts S.W. To die or not to die: an overview of apoptosis and its role in disease. JAMA 279 (1998) 300-307
3. Kerr J.F.R., Wyllie A.H., and Currie A.R. Apoptosis: a basic biological phenomenon with wide ranging implications in tissue kinetics. Br J Cancer 26 (1972) 239-257
4. Wyllie A.H., Kerr J.F., and Currie A.R. Cell death: the significance of apoptosis. Int Rev Cytol 68 (1980) 251-306
5. Searle J., Kerr J.F.R., and Bishop C.J. Necrosis and apoptosis: distinct modes of cell death with fundamentally different significance. Pathol Annu 17 (1982) 229-259
6. Ucker D.S. Death by suicide: one way to go in mammalian cellular development?. New Biol 3 (1991) 103-109
7. Arends M.J., and Wyllie A.H. Apoptosis: mechanisms and roles in pathology. Int Rev Exp Pathol 32 (1991) 223-254
8. Buja L.M., Eigenbrodt M.L., and Eigenbrodt E.H. Apoptosis and necrosis: basic types and mechanisms of cell death. Arch Pathol Lab Med 117 (1993) 1208-1214
9. Majno G., and Joris I. Apoptosis, oncosis, and necrosis: an overview of cell death. Am J Pathol 146 (1995) 3-15
10. Buja L.M., and Entman M.L. Modes of myocardial cell injury and cell death in ischemic heart disease. Circulation 98 (1998) 1355-1357
11. Collins R.J., Harmon B.V., Gobé G.C., and Kerr J.F.R. Internucleosomal DNA cleavage should not be the sole criterion for identifying apoptosis. Int J Radiat Biol 61 (1992) 451-453
12. Arends M.J., Morris R.G., and Wyllie A.H. Apoptosis. The role of the endonuclease. Am J Pathol 136 (1990) 593-608
13. Bursch W., Kline L., and Tenniswood M. The biochemistry of cell death by apoptosis. Biochem Cell Biol 68 (1990) 1071-1074
14. Gold R., Schmied M., Giegerich G., Breitschopf H., Hartung H.P., Tokya K.V., et al. Differentiation between cellular apoptosis and necrosis by the combined use of in situ tailing and nick translation. Lab Invest 71 (1994) 219-225
15. Jacobson M.D., Weil M., and Raff M.C. Programmed cell death in animal development. Cell 88 (1997) 347-354
16. Nagata S. Apoptosis by death factor. Cell 88 (1997) 355-365
17. Wyllie A.H. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284 (1980) 555-556
18. Cohen J.J. Programmed cell death in the immune system. Adv Immunol 50 (1991) 55-85
19. Raff M.C., Barres B.A., Burne J.F., Coles H.S., Ishizaki Y., and Jacobson M.D. Programmed cell death and the control of cell survival, lessons from the nervous system. Science 262 (1996) 695-700
20. Martinou J.C., Dubois-Dauphin M., Staple J.K., Rodriguez I., Frankowsky H., Missotten M., et al. Over expression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13 (1994) 1017-1030
21. Banda N.K., Bernier J., Kurahara D.K., Kurrie R., Haigwood N., Sekaly R.P., et al. Cross-linking CD4 by human immunodeficiency virus gp120 primes T cells for activation-induced apoptosis. J Exp Med 176 (1992) 1099-1106
22. Bessis M.C. Death of a cell, 16-mm film (1958), Swift Motion Picture Laboratories, New York
23. Hall D.H., Gu G., Garcia-Anoveros J., Gong L., Chalfie M., and Driscoll M. Neuropathology of degenerative cell death in Caenorhabditis elegans. J Neurosci 17 (1997) 1033-1035
24. Xu K., Tavernarakis N., and Driscoll M. Necrotic cell death in C. elegans requires the function of calreticulin and regulators of Ca(2+) release from the endoplasmic reticulum. Neuron 31 (2001) 957-971
25. Syntichaki P., Xu K., Driscoll M., and Tavernarakis N. Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans. Nature 419 (2002) 939-944
26. Proskuryakov S.Y., Konoplyannikov A.G., and Gabai V.L. Necrosis: a specific form of programmed cell death?. Exp Cell Res 283 (2003) 1-16
27. Dunn Jr. W.A. Studies on the mechanisms of autophagy; formation of the autophagic vacuole. J Cell Biol 110 (1990) 1923-1933
28. Danial N.N., and Korsmeyer S.J. Cell death: critical control points. Cell 116 (2004) 205-219
29. Thornberry N.A., and Lazebnik Y. Caspases: enemies within. Science 281 (1998) 1312-1316
30. Budihardjo I., Oliver H., Lutter M., Luo X., and Wang X. Biochemical pathways of caspase activation during apoptosis. Annu Rev Cell Dev Biol 15 (1999) 269-290
31. Cikala M., Wilm B., Hobmayer E., Bottger A., and David C.N. Identification of caspases and apoptosis in the simple metazoan Hydra. Curr Biol 9 (1999) 959-962
32. Earnshaw W.C., Martins L.M., and Kauffman S.A. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 68 (1999) 383-424
33. Thornberry N.A., Rano T.A., Peterson E.P., Rasper T.M., Timkey T., Garcia-calvo M., et al. A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J Biol Chem 272 (1997) 17907-17911
34. Grütter M.G. Caspases: key players in programmed cell death. Curr Opin Struct Biol 10 (2000) 649-655
35. Wolf B.B., and Green D.R. Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem 274 (1999) 20049-5
36. Green D.R. Apoptotic pathways: paper wraps stone blunt scissors. Cell 102 (2001) 1-4
37. Goyal L. Cell death inhibition: keeping caspases in check. Cell 104 (2001) 805-808
38. Srinivasula S.M., Hegde R., Saleh A., Datta P., Shiozaki E., Chai J., et al. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature 410 (2001) 112-116
39. Zheng L., Fisher G., Miller R.E., Peschon J., Lynch P.H., and Lenardo M.J. Induction of apoptosis in mature T cells by tumor necrosis factor. Nature 377 (1995) 348-351
40. Suda T., Takahashi T., Golstein P., and Nagata S. Molecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family. Cell 75 (1993) 1169-1178
41. Pitti R.M., Marsters S.A., Ruppert S., Donahue C.J., Moore A., and Ashkenazi A. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J Biol Chem 271 (1996) 12687-12690
42. Marsters S.A., Sheridan J.P., Pitti R.M., Brush J., Goddard A., and Ashkenazi A. Identification of a ligand for the death-domain-containing receptor Apo3. Curr Biol 8 (1998) 525-528
43. Itoh N., Yonehara S., Ishii A., Yonehara M., Mizushima S., Sameshima M., et al. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 66 (1991) 233-243
44. Loetscher H., Pan Y.C., Lahm H.W., Gentz R., Brockhaus M., Tabuchi H., et al. Molecular cloning and expression of the human 55 kd tumor necrosis factor receptor. Cell 61 (1990) 351-359
45. Chinnaiyan A.M., O'Rourke K., Yu G.L., Lyons R.H., Garg M., Duan D.R., et al. Signal transduction by DR3, a death domain-containing receptor related to TNFR-1 and CD95. Science 274 (1996) 990-992
46. Kitson J., Raven T., Jiang Y.P., Goeddel D.V., Giles K.M., Pun K.T., et al. A death-domain-containing receptor that mediates apoptosis. Nature 384 (1996) 372-375
47. Pan G., O'Rourke K., Chinnaiyan A.M., Gentz R., Ebner R., Ni J., et al. The receptor for the cytotoxic ligand TRAIL. Science 276 (1997) 111-113
48. Walczak H., Degli-Esposti M.A., Johnson R.S., Smolak P.J., Waugh J.Y., Boiani N., et al. TRAIL-R2: a novel apoptosis-mediating receptor for TRAIL. EMBO J 16 (1997) 5386-5397
49. Kischkel F.C., Hellbardt S., Behrmann I., Germer M., Pawlita M., Krammer P.H., et al. Cytotoxicity-dependent APO-1 (Fas/CD95)-associated proteins form a death-inducing signaling complex (DISC) with the receptor. EMBO J 14 (1995) 5579-5588
50. Boldin M.P., Varfolomeev E.E., Pancer Z., Mett I.L., Camonis J.H., and Wallach D. A novel protein that interacts with the death domain of Fas/APO1 contains a sequence motif related to the death domain. J Biol Chem 270 (1995) 7795-7798
51. Muzio M. Signaling by proteolysis: death receptors induce apoptosis. Int J Clin Lab Res 28 (1998) 141-147
52. Ashkenazi A., and Dixit V.M. Apoptosis control by death and decoy receptors. Curr Opin Cell Biol 11 (1999) 255-260
53. Boatright K.M., Renatus M., Scott F.L., Sperandio S., Shin H., Pederson I.M., et al. A unified model for apical caspase activation. Mol Cell 11 (2003) 529-541
54. Luo X., Budihardjo I., Zou H., Slaughter C., and Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94 (1998) 481-490
55. Li H., Zhu H., Xu C.J., and Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94 (1998) 491-501
56. Gross A., Yin X.M., Wang K., Wei M.L., Jockel J., Millman C., et al. 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 (1999) 1156-1163
57. Bennett M.R. Apoptosis in the cardiovascular system. Heart 87 (2002) 480-487
58. Shimizu S., Narita M., and Tsujimoto Y. Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399 (1999) 483-487 Erratum in: Nature 2000;407:767
59. Gavrieli Y., Sherman Y., and Ben-sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119 (1992) 493-501
60. Ohno M., Takemura G., Ohno H., Misao J., Hayakawa Y., Minatoguchi S., et al. "Apoptotic" myocytes in the infarct area in rabbit hearts may be oncotic myocytes with DNA fragmentation: analysis by immunogold electron microscopy combined with in situ neck labeling. Circulation 98 (1998) 1422-1430
61. Kanoh M., Takemura G., Misao J., Hayakawa Y., Aoyama T., Nishigaki K., et al. Significance of myocytes with positive DNA end-labeling (TUNEL) in hearts with dilated cardiomyopathy. Circulation 99 (1999) 2757-2764
62. Gonzalez A., Fortuno M.A., Querejeta R., Ravassa S., Lopez B., Lopez N., et al. Cardiomyocyte apoptosis in hypertensive cardiomyopathy. Cardiovasc Res 59 (2003) 549-562
63. Didenko V.V., and Hornsby P.J. Presence of double-strand breaks with single-base 3′ overhangs in cells undergoing apoptosis but not necrosis. J Cell Biol 135 (1996) 1369-1376
64. Didenko V.V., Tunstead J.R., and Hornsby P.J. Biotin-labeled hairpin oligonucleotides: probes to detect double-strand breaks in DNA in apoptotic cells. Am J Pathol 152 (1998) 897-902
65. Guerra S., Leri A., Wang X., Finato N., Di Loreto C., Beltrami C.A., et al. Myocyte death in the failing human heart is gender dependent. Circ Res 85 (1999) 856-866
66. Petrovic D., Zorc-Pleskovic R., and Zorc M. Apoptosis and proliferation of cardiomyocytes in heart failure of different etiologies. Cardiovasc Pathol 9 (2000) 149-152
67. Fadok V.A., Voelker D.R., Campbell P.A., Cohen J.J., Bratton D.L., and Henson P.M. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J Immunol 148 (1992) 2207-2216
68. Verhoven B., Schlegel R.A., and Williamson P. Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal, on apoptotic T lymphocytes. J Exp Med 182 (1995) 1597-1601
69. 2+-bridging mechanism and phospholipid head group recognition in the membrane-binding protein annexin V. Nat Struct Biol 2 (1995) 968-974
70. Vermes I., Haanen C., and Reutelingsperger C. Flow cytometry of apoptotic cell death. J Immunol Methods 243 (2000) 167-190
71. Gottlieb R.A., and Kitsis R.N. Seeing death in the living. Nat Med 17 (2001) 1277-1278
72. Rodriguez M., and Schaper J. Apoptosis: measurement and technical issues. J Mol Cell Cardiol 38 (2005) 15-20
73. Thompson C.B. Apoptosis in the pathogenesis and treatment of disease. Science 267 (1995) 1456-1462
74. Narula J., Haider N., Virmani R., DiSalvo T.G., Kolodgie F.D., Hajjar R.J., et al. Apoptosis in myocytes in end-stage heart failure. N Eng J Med 335 (1996) 1182-1189
75. Quiaini F., Cigola E., Lagraste C., Saccani G., Quaini E., Rossi C., et al. End-stage cardiac failure in humans is coupled with the induction of proliferating cell nuclear antigen and nuclear mitotic division in ventricular myocytes. Circ Res 75 (1994) 1050-1063
76. Isner J.M., Kearney M., Bortman S., and Paseri J. Apoptosis in human atherosclerosis and restenosis. Circulation 91 (1995) 2703-2711
77. Braunwald E. Pathophysiology of Heart Failure. In: Braunwald E. (Ed). Heart disease: a textbook of cardiovascular medicine. 4th ed. (1992), W.B. Saunders, Philadelphia 393-418
78. Katz A.M. The cardiomyopathy of overload: an unnatural growth response in the hypertrophied heart. Ann Intern Med 121 (1994) 363-371
79. Chien K.R., Zhu H., Knowlton K.U., Miller-Hance W., van-Bilsten M., O'Brien T.X., et al. Transcriptional regulation during cardiac growth and development. Annu Rev Physiol 55 (1993) 77-95
80. Izumo S., Nadal-Ginard B., and Madhavi V. Protooncogene induction and reprogramming of the cardiac gene expression produced by pressure overload. Proc Natl Acad Sci 85 (1998) 339-343
81. Olivetti G., Abbi R., Quaini F., Kajstura J., Cheng W., Nitahara J.A., et al. Apoptosis in the failing human heart. N Eng J Med 336 (1997) 1131-1141
82. Tanaka M., Hiroshi I., Adachi S., Akimoto H., Nishikawa T., Kasajima T., et al. Hypoxia induces apoptosis with enhanced expression of Fas antigen messenger RNA in cultured neonatal rat cardiomyocytes. Circ Res 75 (1994) 426-433
83. Kajstura J., Cheng W., Reiss K., Clark W.A., Sonnenblick E.H., Krajewski S., et al. Apoptotic and necrotic myocyte cell deaths are independent contributing variables of infarct size in rats. Lab Invest 74 (1996) 86-107
84. Sharov V.G., Sabbah H.N., Shimoyama H., Goussev A.V., Lesch M., and Goldstein S. Evidence of cardiomyocyte apoptosis in myocardium of dogs with chronic heart failure. Am J Pathol 148 (1996) 141-149
85. Gottlieb R.A., Burleson K.A., Kloner R.A., Babior B.M., and Engler R.L. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J Clin Invest 94 (1994) 1621-1628
86. Hamet P., Richard L., Dam T.V., Teiger E., Orlov S.N., Gaboury L., et al. Apoptosis in target organs of hypertension. Hypertension 26 (1995) 642-648
87. Lui Y., Cigola E., Cheng W., Kajstura J., Olivetti G., Hintze T.H., et al. Myocyte nuclear mitotic division and programmed myocyte cell death characterize the cardiac myopathy induced by rapid ventricular pacing in dogs. Lab Invest 73 (1995) 771-787
88. Cheng W., Li B.S., Kajstura J., Li P., Wolin M.S., Sonnenblick E.H., et al. Stretch-induced programmed myocyte cell death. J Clin Invest 96 (1995) 2247-2259
89. American Heart Association. Heart and stroke statistical update (2002), American Heart Association, Dallas, TX p.11-4
90. Garg S., Narula J., and Chandrashekhar Y. Apoptosis and heart failure: clinical relevance and therapeutic target. J Moll Cell Cardiol 38 (2005) 73-79
91. Fliss H., and Gattinger D. Apoptosis in ischemic and reperfused rat myocardium. Circ Res 79 (1996) 949-956
92. Saraste A., Pulkki K., Kallajoki M., Henriksen K., Parvinen M., and Voipio-Pulkki M. Apoptosis in human acute myocardial infarction. Circulation 95 (1997) 320-323
93. Entman M., Michael L., Rosen R.D., Dreyer W.J., Anderson D.C., Taylor A.A., et al. Inflammation in the course of early myocardial ischemia. FASEB J 5 (1991) 2529-2553
94. Matturri L., Milei J., Grana D.R., and Lavezzi A.M. Characterization of myocardial hypertrophy by DNA content, PCNA expression and apoptotic index. Int J Cardiol 82 (2002) 33-39
95. Li Z., Bing O.H., Long X., Robinson K.G., and Lakatta E.G. Increased cardiomyocyte apoptosis during the transition to heart failure in the spontaneously hypertensive rat. Am J Physiol 272 (1997) H2313-H2319
96. Condorelli G., Morisco C., Stassi G., et al. Increased cardiomyocyte apoptosis and changes in proapoptotic and antiapoptotic genes bax and Bcl-2 during left ventricular adaptations to chronic pressure overload in the rat. Circulation 99 (1999) 3071-3078
97. Baldi A., Abbate A., Bussani R., Patti G., Melfi R., Angelini A., et al. Apoptosis and post-infarction left ventricular remodeling. J Mol Cell Cardiol 34 (2002) 165-174
98. Palojoki E., Saraste A., Eriksson A., Pulkki K., Kallajoki M., Voipio-Pulkki L.M., et al. Cardiomyocyte apoptosis and ventricular remodeling after myocardial infarction in rats. Am J Physiol 280 (2001) H2726-H2730
99. Sam F., Sawyer D.B., Chang D.L., Eberli F.R., Ngoy S., Jain M., et al. Progressive left ventricular remodeling and apoptosis late after myocardial infarction in mouse heart. Am J Physiol 279 (2000) H422-H428
100. Abbate A., Bionde-Zoccai G.G., Bussani R., Dobrina A., Camilot D., Feroce F., Rossielo R., et al. Increased myocardial apoptosis in patients with unfavorable left ventricular remodeling and early symptomatic post-infarction heart failure. J Am Coll Cardiol 41 (2003) 753-760
101. Cohn J.N., Ferrari R., and Sharpe N. Cardiac remodeling-concepts and clinical implications: a consensus paper from international forum on cardiac remodeling. J Am Coll Cardiol 35 (2000) 569-582
102. Cigola E., Kajstura J., Li B., Meggs L.G., and Anversa P. Angiotensin II activates programmed myocyte cell death in vitro. Exp Cell Res 231 (1997) 363-371
103. 2 adrenergic receptors on cardiac myocyte apoptosis: role of pertussis-toxin sensitive G protein. Circulation 100 (1999) 2210-2212
104. Díez J., Panizo A., Hernández M., Vega F., Sola I., Fortuno M.A., et al. Cardiomyocyte apoptosis and cardiac angiotensin-converting enzyme in spontaneously hypertensive rats. Hypertension 30 (1997) 1029-1034
105. Liu J.J., Peng L., Bradley C.J., Zulli A., Shen J., and Braxton B.F. Increased apoptosis in the heart of genetic hypertension, associated with increased fibroblasts. Cardiovasc Res 45 (2000) 729-735
106. Li P., Zhang X., Capasso J.M., Meggs L.G., Sonnenblick E.H., and Anversa P. Myocyte loss and left ventricular failure characterise the long term effects of coronary artery narrowing or renal hypertension in rats. Cardiovasc Res 27 (1993) 1066-1075
107. Diep Q.N., El Mabrouk M., Yue P., and Schiffrin E.L. Effect of AT(1) receptor blockade on cardiac apoptosis in angiotensin II-induced hypertension. Am J Physiol Heart Circ Physiol 282 (2002) H1635-H1641
108. Ikeda S., Hamada M., Qu P., Hiasa G., Hashida H., and Shigematsu Y. Relationship between cardiomyocyte cell death and cardiac function during hypertensive cardiac remodeling in Dahl rats. Clin Sci (Lond) 102 (2002) 329-335
109. Mirsky I., Pfeffer J.M., Pfeffer M.A., and Braunwald E. The contractile state as a major determinant in the evolution of left ventricular dysfunction in the spontaneously hypertensive rat. Circ Res 53 (1983) 767-778
110. Pfeffer J.M., Pfeffer M.A., Fishbein M.C., and Frolich E.D. Cardiac hypertensive rat. Am J Physiol 237 (1979) H461-H468
111. Conrad C.H., Brooks W.W., Hayes J.A., Sen S., Robinson K.G., and Bing O.H. Myocardial fibrosis and stiffness with hypertrophy and heart failure in the spontaneously hypertensive rat. Circulation 91 (1995) 161-170
112. González A., López B., Ravassa S., Querejeta R., Larman M., and Diez J. Stimulation of cardiac apoptosis in essential hypertension: potential role of angiotensin II. Hypertension 39 (2002) 75-80
113. Yamamoto S., Sawada K., Shimomura H., Kawamura K., et al. On the nature of cell death during remodeling of hypertrophied human myocardium. J Mol Cell Cardiol 32 (2000) 161-175
114. González A, Ravassa S, López B. Apoptosis in the failing hypertensive human heart. Unpublished data.
115. Olivetti G., Melissari M., Balbi T., Quaini F., Cigola E., Sonnenblick E.H., et al. Myocyte cellular hypertrophy is responsible for ventricular remodeling in the hypertrophied heart of middle-aged individuals in the absence of cardiac failure. Cardiovasc Res 28 (1994) 1199-1208
116. Olivetti G., Melissari M., Balbi T., Quaini F., Sonnenblick E.H., and Anversa P. Myocyte nuclear and possible cellular hyperplasia contribute to ventricular remodeling in the hypertrophic senescent heart in humans. J Am Coll Cardiol 24 (1994) 140-149
117. Klionsky D.J., and Emr S.D. Autophagy as a regulated pathway of cellular degradation. Science 290 (2000) 1717-1720
118. Thomas G., and Hall M.N. TOR signaling and control of cell growth. Curr Opin Cell Biol 9 (1997) 782
119. Brown E.J., Beal P.A., Keith C.T., Chen J., Shin T.B., and Schreiber S.L. Control of p70 s6 kinase by kinase activity of FRAP in vivo. Nature 377 (1995) 441-446
120. Petiot A., Ogier-Denis E., Blommaart E.F., Meijer A.J., and Codogno P. Distinct classes of phosphatidylinositol 3'-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem 275 (2000) 992-998 Erratum in J Biol Chem 2000;275:12360
121. Scott S.V., Nice III D.C., Nau J.J., Weisman L.S., Kamada Y., Keizer-Gunnink I., et al. Apg13p and Vac8p are part of a complex of phosphoproteins that are required for cytoplasm to vacuole targeting. J Biol Chem 275 (2000) 25840-25849
122. Takeshige K., Baba M., Tsuboi S., Noda T., and Ohsumi Y. Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J Cell Biol 119 (1992) 301-311
123. Matsuura A., Tsukada M., Wada Y., and Ohsumi Y. Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 192 (1997) 245-250
124. Teter S.A., and Klionsky D.J. Transport of proteins to the yeast vacuole: autophagy, cytoplasm-to-vacuole targeting, and role of the vacuole in degradation. Semin Cell Dev Biol 11 (2000) 173-179
125. Mitch W.E., and Goldberg A.L. Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N Engl J Med 335 (1996) 1897-1905
126. Ciechanover A., Orian A., and Schwartz A.L. The ubiquitin-mediated proteolytic pathway: mode of action and clinical implications. J Cell Biochem 77 (2000) 40-51
127. Pickart C.M. Mechanisms of ubiquitination. Annu Rev Biochem 70 (2001) 503-533
128. Glickman M.H., and Ciechanover A. The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. Physiol Rev 82 (2002) 373-428
129. Hicke L., and Dunn R. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19 (2003) 141-172
130. Schwartz D.C., and Hochstrasser M.A. Superfamily of protein tags: ubiquitin, SUMO and related modifiers. Trends Biochem Sci 28 (2003) 321-328
131. Huang D.T., Walden H., Duda D., and Schulman B.A. Ubiquitin-like protein activation. Oncogene 23 (2004) 1958-1971
132. Zwickl P., Seemüller E., Kapelari B., and Baumeister W. The proteasome: a supramolecular assembly designed for controlled proteolysis. Adv Protein Chem 59 (2001) 187-222
133. Gröll M., and Huber R. Substrate access and processing by the 20S proteasome core particle. Int J Biochem Cell Biol 35 (2003) 606-616
134. Adams J. The proteasome: structure, function, and role in the cell. Cancer Treat Rev 29 (2003) 3-9
135. Glickman M.H., and Adir N. The proteasome and the delicate balance between destruction and rescue. Plos Biol 2 (2004) E13
136. Anglade P., Vyas S., Javoy-Agid F., Herrero M.T., Michel P.P., Marquez J., et al. Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol Histopathol 12 (1997) 25-31
137. Stadelmann C., Deckwerth T.L., Srinivasan A., Bancher C., Bruck W., Jellinger K., et al. Activation of caspase-3 in single neurons and autophagic granules of granulovacuolar degeneration in Alzheimer's disease. Evidence for apoptotic cell death. Am J Pathol 155 (1999) 1459-1466
138. Hein S., Arnon E., Kostin S., Schonburg M., Elsasser A., Polyakova V., et al. Progression from compensated hypertrophy to failure in the pressure-overloaded human heart. Structural deterioration and compensatory mechanisms. Circulation 107 (2003) 984-991
139. Knaapen M.W., Davies M.J., De Brie M., Haven A.J., Martinet W., and Kockx M.M. Apoptotic versus autophagic cell death in heart failure. Cardiovascular Res 51 (2001) 304-312
140. Kostin S., Pool L., Elsasser A., Hein S., Drexler H.C., Arnon E., et al. Myocytes die by multiple mechanisms in failing human hearts. Circulation Res 92 (2003) 715-724
141. Elsasser A., Vogt A.M., Nef H., Kostin S., Mollmann H., Skwara W., et al. Human hibernating myocardium is jeopardized by apoptotic and autophagic cell death. J Am Coll Cardiol 43 (2004) 2191-2199
142. Blommaart E.F., Luiken J.J., and Meijer A.J. Autophagic proteolysis: control and specificity. Histochem J 29 (1997) 365-385
143. Stefanis L., Larsen K.E., Rideout H.J., Sulzer D., and Greene L.A. Expression of A53T mutant but not wild-type alpha-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. J Neurosci 15 (2001) 9549-9560