Autophagy in cell death: An innocent convict?

Journal of Clinical Investigation

Volumn 115, Issue 10, 2005, Pages 2679-2688

  Levine, Beth ^a,c   Yuan, Junying ^b  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLADENINE; ADENOSINE TRIPHOSPHATE; ALPHA SYNUCLEIN; CASPASE; CELL PROTEIN; CERAMIDE; DNA; DNA FRAGMENT; ECDYSONE; FIBROBLAST GROWTH FACTOR; GROWTH FACTOR; INITIATION FACTOR 2ALPHA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR GCN4; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UBIQUITIN;

APOPTOSIS; AUTOPHAGY; BIOENERGY; CANCER; CELL DEATH; CELL SURVIVAL; CELL ULTRASTRUCTURE; CELL VIABILITY; DEGENERATIVE DISEASE; DICTYOSTELIUM DISCOIDEUM; DNA CLEAVAGE; DROSOPHILA; HUMAN; INFECTION; LYSOSOME; MITOCHONDRION; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; RNA INTERFERENCE;

ANIMALS; APOPTOSIS; AUTOPHAGY; CELL SURVIVAL; HUMANS; SIGNAL TRANSDUCTION;

EID: 25144506835     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI26390     Document Type: Review

References (124)

1. Klionsky, D.J., and Emr, S.D. 2000. Autophagy as a regulated pathway of cellular degradation. Science. 290:1717-1721.
2. Levine, B., and Klionsky, D.J. 2004. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell. 6:463-477.
3. Lum, J.J., DeBarardinis, R.J., and Thompson, C.B. 2005. Autophagy in metazoans: cell survival in the land of plenty [review]. Nat. Rev. Mol. Cell Biol. 6:439-448.
4. Talloczy, Z., et al. 2002. Regulation of starvation- and virus-induced autophagy by the eIF2α kinase signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 99:190-195.
5. Klionsky, D.J., et al. 2003. A unified nomenclature for yeast autophagy-related genes. Dev. Cell. 5:539-545.
6. Schweichel, J.-U., and Merker, H.-J. 1973. The morphology of various types of cell death in prenatal tissues. Teratology. 7:253-266.
7. Bursch, W. 2001. The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ. 8:569-581.
8. Clarke, P.G. 1990. Developmental cell death: morphological diversity and multiple mechanisms [review]. Anat. Embryol (Berl.) 181:195-213.
9. Lockshin, R.A., and Zakeri, Z. 2004. Apoptosis, autophagy, and more. Int. J. Biochem. Cell Biol. 36:2405-2419.
10. Lee, C.Y., and Baehrecke, E.H. 2001. Steroid regulation of autophagic programmed cell death during development. Development. 128:1443-1455.
11. Kosta, A., et al. 2004. Autophagy gene disruption reveals a non-vacuolar cell death pathway in dictyostelium. J. Biol. Chem. 279:48404-48409.
12. Seglen, P.O., and Gordon, P.B. 1982. 3-Methyladenine: specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl. Acad. Sci. U. S. A. 79:1889-1892.
13. Blommaart, E.F., Krause, U., Schellens, J.P, Vreeling-Sindelarova, H., and Meijer, A.J. 1997. The phosphatidylinositol 3-kinase inhibitors wortmannin and LY294002 inhibit autophagy in isolated rat hepatocytes. Eur. J. Biochem. 243:240-246.
14. Periot, A., Ogier-Denis, E., Blommaart, E.F., Meijer, A.J., and Codogno, P. 2000. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275:992-998.
15. Schwarze, P.E., and Seglen, P.O. 1985. Reduced autophagic activity, improved protein balance and enhanced in vitro survival of hepatocytes isolated from carcinogen-treated rats. Exp. Cell Res. 157:15-28.
16. Bursch, W., et al. 1996. Active cell death induced by the anti-estrogens tamoxifen and ICI 164 384 in human mammary carcinoma cells (MCF-7) in culture: the role of autophagy. Carcinogenesis. 17:1595-1607.
17. Kaidi, A.U., et al. 2001. Chloroquine-induced neuronal cell death is p53 and Bcl-2 family-dependent but caspase-independent. J. Neuropathol. Exp. Neurol. 60:937-945.
18. Xue, L., Fletcher, G.C., and Tolkovsky, A.M. 1999. Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution. Mol. Cell. Neurosci. 14:180-198.
19. Canu, N., et al. 2005. Role of the autophagic-lysosomal system on low potassium-induced apoptosis in cultured cerebellar granule cells. J. Neurochem. 92:1228-1242.
20. Uchiyama, Y. 2001. Autophagic cell death and its execution by lysosomal cathepsins. Arch. Histol. Cytol. 64:233-246,
21. Jia, L., et al. 1997. Inhibition of autophagy abrogates tumour necrosis factor alpha induced apoptosis in human T-lymphoblastic leukaemic cells. Br. J. Haematol. 98:673-685.
22. Xue, L., Borutaite, V., and Tolkovsky, A.M. 2002. Inhibition of mitochondrial permeability transition and release of cytochrome c by anti-apoptotic nucleoside analogues. Biochem. Pharmacol. 64:441-449.
23. Yu, L., et al. 2004. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase 8. Science. 304:1500-1502.
24. Shimizu, S., et al. 2004. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat. Cell Biol. 6:1221-1228.
25. Lum, J.J., et al. 2005. Growth factor regulation of autophagy and cell survival in the absence of autophagy. Cell. 120:237-248.
26. Hourdry, J. 1977. Cytological and cytochemical changes in the intestinal epithelium during anuran metamorphosis. Int. Rev. Cytol. Suppl. 5:337-385.
27. Tsukada, M., and Ohsumi, Y. 1993. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett. 333:169-174.
28. Otto, G.P., Wu, M.Y., Kazgan, N., Anderson, O.R., and Kessin, R.H. 2003. Macroautophagy is required for multicellular development of the social amoeba Dictyostelium dixoideum. J. Biol. Chem. 278:17636-17645.
29. Otto, G.P., Wu, M.Y., Kazgan, N., Anderson, O.R., and Kessin, R.H. 2004. Dictyostelium macroautophagy mutants vary in the severity of their developmental defects. J. Biol. Chem. 279:15621-15629.
30. Doelling, J.H., Walker, J.M., Friedman, E.M., Thompson, A.R., and Vierstra, R.D. 2002. The APG8/12-activating enzyme APG7 is required for proper nutrient recycling and senescence in Arabidopsis thaliana. J. Biol. Chem. 277:33105-33114.
31. Hanaoka, H., et al. 2002. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 129:1181-1193.
32. Liu, Y., et al. 2005. Autophagy genes are essential for limiting the spread of programmed cell death associated with plant innate immunity. Cell. 121:567-577.
33. Kuma, A., et al. 2004. The role of autophagy during the early neonatal starvation period. Nature. 432:1032-1036.
34. Melendez, A., et al. 2003. Autophagy genes are essential for dauer development and lifespan extension in C. elegans. Science. 301:1387-1391.
35. Edinger, A.L., Cinnalli, R.M., and Thompson, C.B. 2003. Rab7 prevents growth factor-independent survival by inhibiting cell-autonomous nutrient transport expression. Dev. Cell. 5:571-582.
36. Boya, P., et al. 2005. Inhibition of macroautophagy triggers apoptosis. Mol. Cell. Biol. 25:1025-1040.
37. Mills, K.R., Reginato, M., Debnath, J., Queenan, B., and Brugge, J.S. 2004. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) is required for induction of autophagy during lumen formation in vitro. Proc. Natl. Acad. Sci. U. S. A. 101:3438-3443.
38. Thorburn, J., et al. 2005. Selective inactivation of FADD-dependent apoptosis and autophagy pathway in immortal epithelial cells. Mol. Biol. Cell. 16:1189-1199.
39. Prins, J., et al. 1998. Tumour necrosis factor induced autophagy and mitochondrial morphological abnormalities are mediated by TNFR-1 and/or TNFR-II and do not invariably lead to cell death. Biochem. Soc. Trans. 26:S314.
40. Pyo, J.-O., et al. 2005. Essential roles of Atg5 and FADD in autophagic cell death: dissection of autophagic cell death into vacuole formation and cell death. J. Biol. Chem. 280:20722-20729.
41. Inbal, B., Bialik, S., Sabanay, I., Shani, G., and Kimchi, A. 2002. DAP kinase and DRP-1 mediate membrane blebbing and the formation of autophagic vesicles during programmed cell death. J. Cell Biol. 157:455-468.
42. Scarlatti, F., et al. 2004. Ceramide-mediated macroautophagy involves inhibition of protein kinase B and upregulation of Beclin 1. J. Biol. Chem. 279:18384-18391.
43. Daido, S., et al. 2004. Pivotal role of the cell death factor BNIP3 in ceramide-induced autophagic cell death in malignant glioma cells. Cancer Res. 64:4286-4293.
44. Meijer, A.J., and Codogno, P. 2004. Regulation and role of autophagy in mammalian cells. Int. J. Biochem. Cell Biol. 36:2445-2462.
45. Lee, C.-Y., et al. 2003. Genome-wide analyses of steroid- and radiation-triggered programmed cell death in Drosophila. Curr. Biol. 13:350-357.
46. Gorski, S.M., et al. 2003. A SAGE approach to discovery of genes involved in autophagic cell death. Curr. Biol. 13:358-363.
47. Kissova, I., Deffieu, M., Manon, S., and Camougrand, N. 2004. Uth1p is involved in the autophagic degradation of mitochondria. J. Biol. Chem. 279:39068-39074.
48. Camougrand, N., et al. 2003. The product of the UTH1 gene, required for Bax-induced cell death in yeast, is involved in the response to rapamycin. Mol. Microbiol. 47:495-506.
49. Saeki, K., et al. 2000. Bcl-2 down-regulation causes autophagy in caspase-independent manner in human leukemic HL60 cells. Cell Death Differ. 7:1263-1269.
50. Cardenas-Aguayo, M.D.C., Santa-Olalla, J., Baizabal, J.M., Salgado, L.M., and Covatrubias, L. 2003. Growth factor deprivation induces an alternative non-apoptotic death mechanism that is inhibited by Bcl2 in cells derived from neural precursor cells. J. Hematother. Stem Cell Res. 12:735-748.
51. Pattingre, S., et al. 2005. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. In press.
52. Velde, C.V., et al. 2000. BNIP3 and genetic control of necrosis-like cell death through the mitochondrial permeability transition pore. Mol. Cell. 20:5454-5468.
53. Yanagisawa, H., Miyashita, T., Nakano, Y., and Yamamoto, D. 2003. HSpin1, a transmembrane protein interacting with Bc-2/Bcl-xL, induces a caspase-independenf autophagic cell death. Cell Death Differ. 10:798-807.
54. Nakano, Y., et al. 2001. Mutations in the novel membrane protein spinster interfere with programmed cell death and cause neural degeneration in Drosophila melanogaster. Mol. Cell. Biol. 21:3775-3788.
55. Elmore, S.P., Qian, T., Grissom, S.F., and Lemasters, J.J. 2001. The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J. 15:2286-2287.
56. Jacotot, E., et al. 1999. Mitochondrial membrane permeabilization during the apoptotic process. Ann. N. Y. Acad. Sci. 887:18-30.
57. Marzo, I., et al. 1998. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science. 281:2027-2031.
58. 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.
59. Tolkovsky, A.M., Xue, L., Fletcher, G.C., and Borutaite, V. 2002. Mitochondrial disappearance from cells: a clue to the role of autophagy in programmed cell death and disease [review]? Biochimie. 84:233-240.
60. Xue, L., Fletcher, G.C., and Tolkovsky, A.M. 2001. Mitochondria are selectively eliminated from eukaryotic cells after blockade of caspases during apoptosis. Curr. Biol. 11:361-365.
61. Grune, T., Jung, T., Merker, K., and Davies, K.J. 2004. Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and "aggresomes" during oxidative stress, aging, and disease. Int. J. Biochem. Cell Biol. 36:2519-2530.
62. Qin, Z.H., et al. 2003. Autophagy regulates the processing of amino terminal huntingtin fragments. Hum. Mol. Genet. 12:3231-3244.
63. Anglade, P., et al. 1997. Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol. Histopathol. 12:25-31.
64. Yu, W.H., et al. 2004. Autophagic vacuoles are enriched in amyloid precursor protein-secretase activities: implications for beta-amyloid peptide over-production and localization in Alzheimer's disease. Int. J. Biochem. Cell Biol. 36:2531-2540.
65. Liberski, P.P., Sikorska, B., Bratosiewicz-Wasik, J., Gajdusek, D.C., and Brown, P. 2004. Neuronal cell death in transmissible spongiform encephalopathies (prion diseases) revisited: from apoptosis to autophagy. Int. J. Biochem. Cell Biol. 36:2473-2490.
66. Shintani, T., and Klionsky, D.J. 2004. Autophagy in health and disease: a double-edged sword. Science. 306:990-995.
67. Yue, Z., et al. 2002. A novel protein complex linking the δ2 glutamate receptor and autophagy: implications for neurodegeneration in lurcher mice. Neuron. 35:921-933.
68. Maries, E., Dass, B., Collier, T.J., Kordower, J.H., and Steece-Collier, K. 2003. The role of alpha-synuclein in Parkinson's diseases: insights from animal models. Nat. Rev. Neurosci. 4:727-738.
69. Webb, J.L., Ravikumar, B., Atkins, J., Stepper, J.N., and Rubinsztein, D.C. 2003. Alpha-synuclein is degraded by both autophagy and the proteasome. J. Biol. Chem. 278:25009-25013.
70. Cuervo, A.M., Stefanis, L., Fredenburg, R., Lansbury, P.T., and Sulzer, D. 2004. Impaired degradation of mutant α-synuclein by chaperone-mediated autophagy. Science. 305:1292-1295.
71. Polymeropoulos, M.H., et al. 1997. Mutation in the α-synuclein gene identified in families with Parkinson's disease. Science. 276:2045-2047.
72. Kruger, R., et al. 1998. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat. Genet. 18:106-108.
73. DiFiglia, M., et al. 1997. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science. 277:1990-1993.
74. Venkatraman, P., Wetzel, R., Tanaka, M., Nukina, N., and Goldberg, A.L. 2004. Eukaryotic proteasomes cannot digest polyglutamine sequences and release them during degradation of polyglutamine-containing proteins. Mol. Cell. 14:95-104.
75. Ravikumar, B., Duden, R., and Rubinsztein, D.C. 2002. Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum. Mol. Genet. 11:1107-1117.
76. Ravikumar, B., et al. 2004. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 36:585-595.
77. Kirkegaard, K., Taylor, M.P., and Jackson, W.T. 2004. Cellular autophagy: surrender, avoidance and subversion by microorganisms [review]. Nat. Rev. Microbiol. 2:301-314.
78. Seay, M., Dinesh-Kumar, S., and Levine, B. 2005. Digesting oneself and digesting microbes: autophagy as a host response to viral infection. In Modulation of host gene expression and innate immunity by viruses. P. Palese, editor. Springer. Dordrecht, The Netherlands. 245-279.
79. Liang, X.H., et al. 1998. Protection against fatal Sindbis virus encephalitis by Beclin, a novel Bcl-2-interacting protein. J. Virol. 72:8586-8596.
80. Ogawa, M., et al. 2005. Escape of intracellular Shigella from autophagy. Science. 307:727-731.
81. Gutierrez, M.G., et al. 2004. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell. 119:753-766.
82. Nakagawa, I., et al. 2004. Autophagy defends cells against invading group A Streptococcus. Science. 306:1037-1040.
83. Hernandez, L.D., Pypaert, M., Flavell, R.A., and Galan, J.E. 2003. A Salmonella protein causes macrophage cell death by inducing autophagy. J. Cell Biol. 163:1123-1131.
84. Rusten, T.E., et al. 2004. Programmed autophagy in the Drosophila fat body is induced by ecdysone through regulation of the PI3K pathway. Dev. Cell. 7:179-192.
85. Scott, R.C., Schuldiner, O., and Neufeld, T.P. 2004. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell. 7:167-178.
86. Liang, X.H., et al. 1999. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 402:672-676.
87. Aita, V.M., et al. 1999. Cloning and genomic organization of beclin 1, a candidate tumor suppressor gene on chromosome 17q21. Genomics. 59:59-65.
88. Qu, X., et al. 2003. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 gene. J. Clin. Invest. 112:1809-1820. doi:10.1172/JCI200320039.
89. Yue, Z., Jin, S., Yang, C., Levine, A.J., and Heintz, N. 2003. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc. Natl. Acad. Sci. U. S. A. 100:15077-15082.
90. Furuya, N., Liang, X.H., and Levine, B. 2004. Autophagy and cancer. In Autophagy. D.J. Klionsky, editor. Landes Bioscience. Georgetown, Texas, USA. 244-253.
91. Ogier-Denis, E., and Codogno, P. 2003. Autophagy: a barrier or an adaptive response to cancer? Biochim. Biophys. Acta. 1603:113-128.
92. Edinger, A.L., and Thompson, C.B. 2004. Death by design: apoptosis, necrosis and autophagy. Curr. Opin. Cell Biol. 16:663-669.
93. Gozuacik, D., and Kimchi, A. 2004. Autophagy as a cell death and tumor suppressor mechanism. Oncogene. 23:2891-2906.
94. Nelson, D.A., and White, E. 2004. Exploiting different ways to die. Genes Dev. 18:1223-1226.
95. Kanzawa, T., Kondo, Y., Ito, H., Kondo, S., and Germane, I. 2003. Induction of autophagic cell death in malignant glioma cells by arsenic trioxide. Cancer Res. 63:2103-2108.
96. Huang, S., and Houghton, P.J. 2003. Targeting mTOR signaling for cancer therapy. Curr. Opin. Pharmacol. 3:371-377.
97. Codogno, P., and Meijer, A.J. 2004. Signaling pathways in mammalian autophagy. In Autophagy. D.J. Klionsky, editor. Landes Bioscience. Georgetown, Texas, USA. 26-47.
98. Degterev, A., et al. 2001. Identification of small-molecule inhibitors of interaction between the BH3 domain and BclxL. Nat. Cell Biol. 3:173-182.
99. Kinch, G., Hoffman, K.L., Rodrigues, E.M., Zee, M.C., and Weeks, J.C. 2003. Steroid-triggered programmed cell death of a motoneuron is autophagic and involves structural changes in mitochondria. J. Comp. Neurol. 457:384-403.
100. Muller, F., Adori, C., and Sass, M. 2004. Autophagic and apoptotic features during programmed cell death in the fat body of the tobacco hornworm (Manduca sexta). Eur. J. Cell Biol. 83:67-78.
101. Romer, F., and Martau, T. 1998. Degeneration of moulting glands in male crickets. J. Insect Physiol. 44:981-989.
102. Bowen, I.D., Mullarkey, K., and Morgan, S.M. 1996. Programmed cell death during metamorphosis in the blow-fly Calliphora vomitoria. Microsc. Res. Tech. 34:202-217.
103. Jones, H.E., and Bown, I.D. 1993. Acid phosphatase activity in the larval salivary glands of developing Drosophila melanogaster. Cell Biol. Int. 17:305-315.
104. Lee, C.-Y., Cooksey, B.A.K., and Baehrecke, E.H. 2002. Steroid regulation of midgut cell death during Drosophila development. Dev. Biol. 250:101-111.
105. Butterworth, F.M., and LaTendresse, B.L. 1973. Quantitative studies of cytochemical and cytological changes during cell death in the larval fat body of Drosophila melanogaster. J. Insect. Physiol. 19:1487-1500.
106. Debnath, J., et al. 2002. The role of apoptosis in creating and maintaining luminal space within normal and oncogene-expressing mammary acini. Cell. 111:29-40.
107. Kegel, K.B., et al. 2000. Huntingtin expression stimulates endolysosomal-activity, endosome tubulation, and autophagy. J. Neurosci. 20:7268-7278.
108. Stefanis, L., Larsen, K.E., Rideout, H.J., Sulzer, D., and Greene, L.A. 2001. Expression of A53T mutant but not wild-type α-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation, loss of dopamine release, and autophagic cell death. J. Neurosci. 21:9549-9560.
109. Nitatori, T., et al. 1995. Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J. Neurosci. 2:1001-1011.
110. Kostin, S. 2004. Types and mechanisms of myocyte cell death in diseased human heart. Cardiovasc. J. S. Afr. 15(4Suppl. 1):S1.
111. 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.
112. Bera, A., Singh, S., Nagaraj, R., and Vaidya, T. 2003. Induction of autophagic cell death in Leishmania donovani by antimicrobial peptides. Mol. Biochem. Parasitol. 127:23-35.
113. Christensen, S.T., et al. 1998. Staurosporine-induced cell death in Tetrahymena thermophila has mixed characteristics of both apoptotic and autophagic degeneration. Cell Biol. Int. 22:591-598.
114. Cornillon, S., et al. 1994. Programmed cell death in Dictyostelium. J. Cell Sci. 107:2691-2704.
115. Akazawa, H., et al. 2004. Diphtheria toxin-induced autophagic cardiomyocyte death plays a pathogenic role in mouse model of heart failure. J. Biol. Chem. 279:41095-41103.
116. Guimaraes, C.A., Benchimo, M., Amarante-Mendes, G.P., and Linden, R. 2003. Alternative programs of cell death in developing retinal tissue. J. Biol. Chem. 278:41938-41946.
117. Borsello, T., Croquelois, K., Hornung, J.P., and Clarke, P.G.H. 2003. N-methyl-D-aspartate triggered neuronal death in organotypic hippocampal cultures is endocytic, autophagic and mediated by the c-Jun N-terminal kinase pathway. Eur. J. Neurosci. 18:473-485.
118. Ohsawa, Y., et al. 1998. An ultrastructural and immunohistochemical study of PC12 cells during apoptosis induced by serum deprivation with special reference to autophagy and lysosomal cathepsins. Arch. Histol. Cytol. 61:395-403.
119. von Bultzingslowen, I., Jontell, M., Hurst, P., Nannmark, U., and Kardos, T. 2001. 5-Fluorouracil induces autophagic degeneration in rat oral keratinocytes. Oral Oncol. 37:537-544.
120. Opipari, A.W., Jr., et al. 2004. Resveratrol-induced autophagocytosis in ovarian cancer cells. Cancer Res. 64:696-703.
121. Bursch, W., et al. 2000. Autophagic and apoptotic types of programmed cell death exhibit different fates of cytoskeletal filaments. J. Cell Sci. 113:1189-1198.
122. Kanzawa, T., et al. 2005. Arsenic trioxide induces autophagic cell death in malignant glioma cells by upregulation of mitochondrial cell death protein BNIP3. Oncogene. 24:980-991.
123. Chau, Y.-P., Lin, S.-Y., Chen, J.H.-C., and Tai, M.-H. 2003. Endostatin induced autophagic cell death in EAhy926 human endothelial cells. Histol. Histopathol. 18:715-726.
124. Juhasz, G., Csikos, G., Sinka, R., Erdelyi, M., and Sass, M. 2003. The Drosophila homolog of Aut1 is essential for autophagy and development. FEBS Lett. 543:154-158.