Apoptosis, pyroptosis, and necrosis: Mechanistic description of dead and dying eukaryotic cells

Infection and Immunity

Volumn 73, Issue 4, 2005, Pages 1907-1916

  Fink, Susan L ^a   Cookson, Brad T ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN DEPOLYMERIZING FACTOR; CALCIUM; CASPASE; CASPASE 10; CASPASE 11; CASPASE 12; CASPASE 13; CASPASE 14; CASPASE 2; CASPASE 3; CASPASE 4; CASPASE 5; CASPASE 6; CASPASE 7; CASPASE 8; CASPASE 9; CYTOKINE; CYTOSKELETON PROTEIN; DNA; DNA FRAGMENT; GELSOLIN; INTERLEUKIN 18; INTERLEUKIN 1BETA; LAMIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PHOSPHATIDYLSERINE; PHOSPHOLIPASE A2; UNCLASSIFIED DRUG;

APOPTOSIS; AUTOPHAGY; CAENORHABDITIS ELEGANS; CELL DEATH; CELL MEMBRANE; CELL NUCLEUS; CHLAMYDIA TRACHOMATIS; CYTOLYSIS; DNA DAMAGE; EMBRYO DEVELOPMENT; ESCHERICHIA COLI; EUKARYOTIC CELL; HOST CELL; HUMAN; IMMUNE RESPONSE; INFECTION; INFLAMMATION; LISTERIA MONOCYTOGENES; MYCOBACTERIUM TUBERCULOSIS; NICK END LABELING; NONHUMAN; ONCOSIS; PATHOGENESIS; PHAGOCYTOSIS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PYROPTOSIS; SALMONELLA; SHIGELLA FLEXNERI; SHORT SURVEY; YERSINIA PSEUDOTUBERCULOSIS; CYTOLOGY; NECROSIS; REVIEW;

APOPTOSIS; AUTOPHAGY; EUKARYOTIC CELLS; NECROSIS;

EID: 16244362671     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.4.1907-1916.2005     Document Type: Short Survey

References (148)

1. Albert, M. L. 2004. Death-defying immunity: do apoptotic cells influence antigen processing and presentation? Nat. Rev. Immunol. 4:223-231.
2. Alnemri, E. S., D. J. Livingston, D. W. Nicholson, G. Salvesen, N. A. Thornberry, W. W. Wong, and J. Yuan. 1996. Human ICE/CED-3 protease nomenclature. Cell 87:171.
3. Ankarcrona, M., J. M. Dypbukt, E. Bonfoco, B. Zhivotovsky, S. Orrenius, S. A. Lipton, and P. Nicotera. 1995. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15:961-973.
4. Berger, N. A. 1985. Poly(ADP-ribose) in the cellular response to DNA damage. Radiat. Res. 101:4-15.
5. Blagosklonny, M. V. 2000. Cell death beyond apoptosis. Leukemia 14:1502-1508.
6. Boatright, K. M., and G. S. Salvesen. 2003. Mechanisms of caspase activation. Curr. Opin. Cell Biol. 15:725-731.
7. Boise, L. H., and C. M. Collins. 2001. Salmonella-induced cell death: apoptosis, necrosis or programmed cell death? Trends Microbiol. 9:64-67.
8. Bonfoco, E., D. Krainc, M. Ankarcrona, P. Nicotera, and S. A. Lipton. 1995. Apoptosis and necrosis: two distinct events induced, respectively, by mild and incense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA 92:7162-7166.
9. Brennan, M. A., and B. T. Cookson. 2000. Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol. Microbiol. 38:31-40.
10. Buendia, B., A. Santa-Maria, and J. C. Courvalin. 1999. Caspase-dependent proteolysis of integral and peripheral proteins of nuclear membranes and nuclear pore complex proteins during apoptosis. J. Cell Sci. 112:1743-1753.
11. Bursch, W. 2001. The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ. 8:569-581.
12. Bursch, W., A. Ellinger, C. Gerner, U. Frohwein, and R. Schulte-Hermann. 2000. Programmed cell death (PCD). Apoptosis, autophagic PCD, or others? Ann. N. Y. Acad. Sci. 926:1-12.
13. Castedo, M., T. Hirsch, S. A. Susin, N. Zamzami, P. Marchetti, A. Macho, and G. Kroemer. 1996. Sequential acquisition of mitochondrial and plasma membrane alterations during early lymphocyte apoptosis. J. Immunol. 157; 512-521.
14. Castro-Obregon, S., R. V. Rao, G. del Rio, S. F. Chen, K. S. Poksay, S. Rabizadeh, S. Vesce, X. K. Zhang, R. A. Swanson, and D. E. Bredesen. 2004. Alternative, nonapoptotic programmed cell death: mediation by arrestin 2, ERK2, and Nur77. J. Biol. Chem. 279:17543-17553.
15. Chen, Y., M. R. Smith, K. Thirumalai, and A. Zychlinsky. 1996. A bacterial invasin induces macrophage apoptosis by binding directly to ICE. EMBO J. 15:3853-3860.
16. Clarke, P. G. 1990. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berlin) 181:195-213.
17. Collins, R. J., B. V. Harmon, G. C. Gobe, and J. F. Kerr. 1992. Internucleosomal DNA cleavage should not be the sole criterion for identifying apoptosis. Int. J. Radiat. Biol. 61:451-453.
18. Columbano, A. 1995. Cell death: current difficulties in discriminating apoptosis from necrosis in the context of pathological processes in vivo. J. Cell Biochem. 58:181-190.
19. Cookson, B. T., and M. A. Brennan. 2001. Pro-inflammatory programmed cell death. Trends Microbiol. 9:113-114.
20. Creagh, E. M., H. Conroy, and S. J. Martin. 2003. Caspase-activation pathways in apoptosis and immunity. Immunol Rev. 193:10-21.
21. Cryns, V. L., L. Bergeron, H. Zhu, H. Li, and J. Yuan. 1996. Specific cleavage of α-fodrin during Fas- and tumor necrosis factor-induced apoptosis is mediated by an interleukin-1β-converting enzyme/Ced-3 protease distinct from the poly(ADP-ribose) polymerase protease. J. Biol. Chem. 271:31277-31282.
22. 2S in cell injury and death. J. Pharmacol. Exp. Ther. 294:793-799.
23. Dacheux, D., B. Toussaint, M. Richard, G. Brochier, J. Croize, and I. Attree. 2000. Pseudomonas aeruginosa cystic fibrosis isolates induce rapid, type III secretion-dependent, but ExoU-independent, oncosis of macrophages and polymorphonuclear neutrophils. Infect. Immun. 68:2916-2924.
24. de Torres, C., F. Munell, I. Ferrer, J. Reventes, and A. Macaya. 1997. Identification of necrotic cell death by the TUNEL assay in the hypoxic-ischemic neonatal rat brain. Neurosci. Lett. 230:1-4.
25. Dimmeler, S., J. Haendeler, M. Nehls, and A. M. Zeiher. 1997. Suppression of apoptosis by nitric oxide via inhibition of interleukin-1β-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32-like proteases. J. Exp. Med. 185:601-607.
26. Dong, Z., P. Saikumar, J. M. Weinberg, and M. A. Venkatachalam. 1997. Internucleosomal DNA cleavage triggered by plasma membrane damage during necrotic cell death. Involvement of serine but not cysteine proteases. Am. J. Pathol. 151:1205-1213.
27. Dypbukt, J. M., M. Ankarcrona, M. Burkitt, A. Sjoholm, K. Strom, S. Orrenius, and P. Nicotera. 1994. Different prooxidant levels stimulate growth, trigger apoptosis, or produce necrosis of insulin-secreting RINm5F cells. The role of intracellular polyamines. J. Biol. Chem. 269:30553-30560.
28. Ekert, P. G., J. Silke, and D. L. Vaux. 1999. Caspase inhibitors. Cell Death Differ. 6:1081-1086.
29. Enari, M., H. Sakahira, H. Yokoyama, K. Okawa, A. Iwamatsu, and S. Nagata. 1998. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391:43-50.
30. Essmann, F., H. Bantel, G. Totzke, I. H. Engels, B. Sinha, K. Schulze-Osthoff, and R. U. Janicke. 2003. Staphylococcus aureus alpha-toxin-induced cell death: predominant necrosis despite apoptotic caspase activation. Cell Death Differ. 10:1260-1272.
31. Fadok, V. A., D. L. Bratton, A. Konowal, P. W. Freed, J. Y. Westcott, and P. M. Henson. 1998. Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta, PGE2, and PAF. J. Clin. Investig. 101: 890-898.
32. Fadok, V. A., D. R. Voelker, P. A. Campbell, J. J. Cohen, D. L. Bratton, and P. M. Henson. 1992. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148:2207-2216.
33. Fantuzzi, G., and C. A. Dinarello. 1999. Interleukin-18 and interleukin-1β: two cytokine substrates for ICE (caspase-1). J. Clin. Immunol. 19:1-11.
34. Farber, E. 1994. Programmed cell death: necrosis versus apoptosis. Mod. Pathol. 7:605-609.
35. Fischer, S., A. A. Maclean, M. Liu, J. A. Cardella, A. S. Slutsky, M. Suga, J. F. Moreira, and S. Keshavjee. 2000. Dynamic changes in apoptotic and necrotic cell death correlate with severity of ischemia-reperfusion injury in lung transplantation. Am. J. Respir. Crit. Care Med. 162:1932-1939.
36. Frantz, S., A. Ducharme, D. Sawyer, L. E. Ronde, L. Kobzik, R. Fukazawa, D. Tracey, H. Allen, R. T. Lee, and R. A. Kelly. 2003. Targeted deletion of caspase-i reduces early mortality and left ventricular dilatation following myocardial infarction. J. Mol. Cell Cardiol. 35:685-694.
37. Gao, L., and Y. Abu Kwaik. 2000. Hijacking of apoptotic pathways by bacterial pathogens. Microbes Infect. 2:1705-1719.
38. Garcia-Calvo, M., E. P. Peterson, B. Leiting, R. Ruel, D. W. Nicholson, and N. A. Thornberry. 1998. Inhibition of human caspases by peptide-based and macromolecular inhibitors. J. Biol. Chem. 273:32608-32613.
39. Gavrilescu, L. C., and E. Y. Denkers. 2003. Apoptosis and the balance of homeostatic and pathologic responses to protozoan infection. Infect. Immun. 71:6109-6115.
40. Gozuacik, D., and A. Kimchi. 2004. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23:2891-2906.
41. Grasl-Kraupp, B., B. Ruttkay-Nedecky, H. Koudelka, K. Bukowska, W. Bursch, and R. Schulte-Hermann. 1995. In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology 21:1465-1468.
42. Hay, S., and G. Kannourakis. 2002. A time to kill: viral manipulation of the cell death program. J. Gen. Virol. 83:1547-1564.
43. Hedgecock, E. M., J. E. Sulston, and J. N. Thomson. 1983. Mutations affecting programmed cell deaths in the nematode Caenorhabditis elegans. Science 220:1277-1279.
44. Herceg, Z., and Z. Q. Wang. 2001. Functions of poly(ADP-ribose) polymerase (PARP) in DNA repair, genomic integrity and cell death. Mutat. Res. 477:97-110.
45. Hernandez, L. D., M. Pypaert, R. A. Flavell, and J. E. Galan. 2003. A Salmonella protein causes macrophage cell death by inducing autophagy. J. Cell Biol. 163:1123-1131.
46. Hersh, D., D. M. Monack, M. R. Smith, N. Ghori, S. Falkow, and A. Zychlinsky. 1999. The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc. Natl. Acad. Sci. USA 96:2396-2401.
47. Hilbi, H., Y. Chen, K. Thirumalai, and A. Zychlinsky. 1997. The interleukin 1β-converting enzyme, caspase 1, is activated during Shigella flexneri-induced apoptosis in human monocyte-derived macrophages. Infect. Immun. 65:5165-5170.
48. Hilbi, H., J. E. Moss, D. Hersh, Y. Chen, J. Arondel, S. Banerjee, R. A. Flavell, J. Yuan, P. J. Sansonetti, and A. Zychlinsky. 1998. Shigella-induced apoptosis is dependent on caspase-1 which binds to IpaB. J. Biol. Chem. 273:32895-32900.
49. Hirano, T., and B. H. Ruebner. 1966. Studies on the mechanism of destruction of lymphoid tissue in murine hepatitis virus (MHV3) infection. I. Selective prevention of lymphoid necrosis by cortisone and puromycin. Lab. Investig. 15:270-282.
50. Hirsch, T., P. Marchetti, S. A. Susin, B. Dallaporta, N. Zamzami, I. Marzo, M. Geuskens, and G. Kroemer. 1997. The apoptosis-necrosis paradox. Apoptogenic proteases activated after mitochondrial permeability transition determine the mode of cell death. Oncogene 15:1573-1581.
51. Hockenbery, D. 1995. Defining apoptosis. Am. J. Pathol. 146:16-19.
52. Hueffer, K., and J. E. Galan. 2004. Salmonella-induced macrophage death: multiple mechanisms, different outcomes. Cell Microbiol. 6:1019-1025.
53. Huppertz, B., H. G. Frank, and P. Kaufmann. 1999. The apoptosis cascade-morphological and immunohistochemical methods for its visualization. Anat. Embryol. (Berlin) 200:1-18.
54. Jaattela, M. 2002. Programmed cell death: many ways for cells to die decently. Ann. Med. 34:480-488.
55. James, E. R., and D. R. Green. 2004. Manipulation of apoptosis in the host-parasite interaction. Trends Parasitol. 20:280-287.
56. Kanduc, D., A. Mittelman, R. Serpico, E. Sinigaglia, A. A. Sinha, C. Natale, R. Santacroce, M. G. Di Corcia, A. Lucchese, L. Dini, P. Pani, S. Santacroce, S. Simone, R. Bucci, and E. Farber. 2002. Cell death: apoptosis versus necrosis (review). Int. J. Oncol. 21:165-170.
57. Kerr, J. F., A. H. Wyllie, and A. R. Currie. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer. 26:239-257.
58. Kim, Y. M., R. V. Talanian, and T. R. Billiar. 1997. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J. Biol. Chem. 272:31138-31148.
59. Klionsky, D. J., and S. D. Emr. 2000. Autophagy as a regulated pathway of cellular degradation. Science 290:1717-1721.
60. Kolodgie, F. D., J. Narula, A. P. Burke, N. Haider, A. Farb, Y. Hui-Liang, J. Smialek, and R. Virmani. 2000. Localization of apoptotic macrophages at the site of plaque rupture in sudden coronary death. Am. J. Pathol. 157: 1259-1268.
61. Kostin, S., L. Pool, A. Elsasser, S. Hein, H. C. Drexler, E. Arnon, Y. Hayakawa, R. Zimmermann, E. Bauer, W. P. Klovekorn, and J. Schaper. 2003. Myocytes die by multiple mechanisms in failing human hearts. Circ. Res. 92:715-724.
62. Kothakota, S., T. Azuma, C. Reinhard, A. Klippel, J. Tang, K. Chu, T. J. McGarry, M. W. Kirschner, K. Koths, D. J. Kwiatkowski, and L. T. Williams. 1997. Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 278:294-298.
63. Lauber, K., E. Bohn, S. M. Krober, Y. J. Xiao, S. G. Blumenthal, R. K. Lindemann, P. Marini, C. Wiedig, A. Zobywalski, S. Baksh, Y. Xu, I. B. Autenrieth, K. Schulze-Osthoff, C. Belka, G. Stuhler, and S. Wesselborg. 2003. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113:717-730.
64. Lazebnik, Y. A., A. Takahashi, R. D. Moir, R. D. Goldman, G. G. Poirier, S. H. Kaufmann, and W. C. Earnshaw. 1995. Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc. Natl. Acad. Sci. USA 92:9042-9046.
65. Lecoeur, H., M. C. Prevost, and M. L. Gougeon. 2001. Oncosis is associated with exposure of phosphatidylserine residues on the outside layer of the plasma membrane: a reconsideration of the specificity of the annexin V/propidium iodide assay. Cytometry 44:65-72.
66. Leist, M., and M. Jaattela. 2001. Four deaths and a funeral: from caspases to alternative mechanisms. Nat. Rev. Mol. Cell Biol. 2:589-598.
67. Leist, M., B. Single, A. F. Castoldi, S. Kuhnle, and P. Nicotera. 1997. Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J. Exp. Med. 185:1481-1486.
68. Levin, S. 1998. Apoptosis, necrosis, or oncosis: what is your diagnosis? A report from the Cell Death Nomenclature Committee of the Society of Toxicologic Pathologists. Toxicol. Sci. 41:155-156.
69. Levin, S., T. J. Bucci, S. M. Cohen, A. S. Fix, J. F. Hardisty, E. K. LeGrand, R. R. Maronpot, and B. F. Trump. 1999. The nomenclature of cell death: recommendations of an ad hoc committee of the Society of Toxicologic Pathologists. Toxicol. Pathol. 27:484-490.
70. Levine, B., and D. J. Klionsky. 2004. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Dev. Cell 6:463-477.
71. Li, P., H. Allen, S. Banerjee, S. Franklin, L. Herzog, C. Johnston, J. McDowell, M. Paskind, L. Rodman, J. Salfeld, et al. 1995. Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell 80:401-411.
72. Liu, X., and R. G. Schnellmann. 2003. Calpain mediates progressive plasma membrane permeability and proteolysis of cytoskeleton-associated paxillin, talin, and vinculin during renal cell death. J. Pharmacol. Exp. Ther. 304: 63-70.
73. Liu, X., T. Van Vleet, and R. G. Schnellmann. 2004. The role of calpain in oncotic cell death. Annu. Rev. Pharmacol. Toxicol. 44:349-370.
74. Liu, X., H. Zou, C. Slaughter, and X. Wang. 1997. DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89:175-184.
75. Liu, X. H., D. Kwon, G. P. Schielke, G. Y. Yang, F. S. Silverstein, and J. D. Barks. 1999. Mice deficient in interleukin-1 converting enzyme are resistant to neonatal hypoxic-ischemic brain damage. J. Cereb. Blood Flow Metab. 19:1099-1108.
76. Lockshin, R. A., and C. M. Williams. 1965. Programmed cell death. I. Cytology of degeneration in the intersegmental muscles of the pernyi silk-moth. J. Insect Physiol. 11:123-133.
77. Lockshin, R. A., and Z. Zakeri. 2004. Apoptosis, autophagy, and more. Int. J. Biochem. Cell Biol. 36:2405-2419.
78. Lockshin, R. A., and Z. Zakeri. 2001. Programmed cell death and apoptosis: origins of the theory. Nat. Rev. Mol. Cell Biol. 2:545-550.
79. Los, M., S. Wesselborg, and K. Schulze-Osthoff. 1999. The role of caspases in development, immunity, and apoptotic signal transduction: lessons from knockout mice. Immunity 10:629-639.
80. Ma, F., C. Zhang, K. V. Prasad, G. J. Freeman, and S. F. Schlossman. 2001. Molecular cloning of porimin, a novel cell surface receptor mediating oncotic cell death. Proc. Natl. Acad. Sci. USA 98:9778-9783.
81. Majno, G., and I. Joris. 1995. Apoptosis, oncosis, and necrosis. An overview of cell death. Am. J. Pathol. 146:3-15.
82. Mariathasan, S., K. Newton, D. M. Monack, D. Vucic, D. M. French, W. P. Lee, M. Roose-Girma, S. Erickson, and V. M. Dixit. 2004. Differential activation of the inflammasome by caspase-1 adaptors ASC and Ipaf. Nature 430:213-218.
83. Martin, S. J., D. M. Finucane, G. P. Amarante-Mendes, G. A. O'Brien, and D. R. Green. 1996. Phosphatidylserine externalization during CD95-induced apoptosis of cells and cytoplasts requires ICE/CED-3 protease activity. J. Biol. Chem. 271:28753-28756.
84. Matsuda, T., H. Saito, T. Inoue, K. Fukatsu, M. T. Lin, I. Han, S. Furakawa, S. Ikeda, and T. Muto. 1999. Ratio of bacteria to polymorphonuclear neutrophils (PMNs) determines PMN fate. Shock 12:365-372.
85. McCarthy, N. J., and G. I. Evan. 1998. Methods for detecting and quantifying apoptosis. Curr. Top. Dev. Biol. 36:259-278.
86. Melino, G., F. Bernassola, R. A. Knight, M. T. Corasaniti, G. Nistico, and A. Finazzi-Agro. 1997. S-nitrosylation regulates apoptosis. Nature 388:432-433.
87. Mills, E. M., D. Xu, M. M. Fergusson, C. A. Combs, Y. Xu, and T. Finkel. 2002. Regulation of cellular oncosis by uncoupling protein 2. J. Biol. Chem. 277:27385-27392.
88. Monack, D. M., C. S. Detweiler, and S. Falkow. 2001. Salmonella pathogenicity island 2-dependent macrophage death is mediated in part by the host cysteine protease caspase-1. Cell Microbiol. 3:825-837.
89. Monack, D. M., D. Hersh, N. Ghori, D. Bouley, A. Zychlinsky, and S. Falkow. 2000. Salmonella exploits caspase-1 to colonize Peyer's patches in a murine typhoid model. J. Exp. Med. 192:249-258.
90. Monack, D. M., J. Mecsas, D. Bouley, and S. Falkow. 1998. Yersinia-induced apoptosis in vivo aids in the establishment of a systemic infection of mice. J. Exp. Med. 188:2127-2137.
91. Moreira, M. E., and M. A. Barcinski. 2004. Apoptotic cell and phagocyte interplay: recognition and consequences in different cell systems. An. Acad. Bras. Cienc. 76:93-115.
92. Moss, J. E., A. O. Aliprantis, and A. Zychlinsky. 1999. The regulation of apoptosis by microbial pathogens. Int. Rev. Cytol. 187:203-259.
93. Nonaka, T., A. Kuwae, C. Sasakawa, and S. Imajoh-Ohmi. 1999. Shigella flexneri YSH6000 induces two types of cell death, apoptosis and oncosis, in the differentiated human monoblastic cell line U937. FEMS Microbiol. Lett. 174:89-95.
94. Obregon, C., D. Dreher, M. Kok, L. Cochand, G. S. Kiama, and L. P. Nicod. 2003. Human alveolar macrophages infected by virulent bacteria expressing SipB are a major source of active interleukin-18. Infect. Immun. 71:4382-4388.
95. Ogier-Denis, E., J. J. Houri, C. Bauvy, and P. Codogno. 1996. Guanine nucleotide exchange on heterotrimeric Gi3 protein controls autophagic sequestration in HT-29 cells. J. Biol. Chem. 271:28593-28600.
96. Ohno, M., G. Takemura, A. Ohno, J. Misao, Y. Hayakawa, S. Minatoguchi, T. Fujiwara, and H. Fujiwara. 1998. "Apoptotic" myocytes in infarct area in rabbit hearts may be oncotic myocytes with DNA fragmentation: analysis by immunogold electron microscopy combined with in situ nick end-labeling. Circulation 98:1422-1430.
97. Ohsumi, Y. 2001. Molecular dissection of autophagy: two ubiquitin-like systems. Nat. Rev. Mol. Cell. Biol. 2:211-216.
98. Otsuki, Y., Z. Li, and M. A. Shibata. 2003. Apoptotic detection methods-from morphology to gene. Prog. Histochem. Cytochem. 38:275-339.
99. + concentration. Virology 252:17-27.
100. Petiot, A., E. Ogier-Denis, E. F. Blommaart, A. J. Meijer, and P. Codogno. 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.
101. Petit, F., D. Arnoult, J. D. Lelievre, L. Moutouh-de Parseval, A. J. Hance, P. Schneider, J. Corbeil, J. C. Ameisen, and J. Estaquier. 2002. Productive HIV-1 infection of primary CD4+ T cells induces mitochondrial membrane permeabilization leading to a caspase-independent cell death. J. Biol. Chem. 277:1477-1487.
102. Pieper, A. A., A. Verma, J. Zhang, and S. H. Snyder. 1999. Poly (ADP-ribose) polymerase, nitric oxide and cell death. Trends Pharmacol. Sci. 20:171-181.
103. Rao, L., D. Perez, and E. White. 1996. Lamin proteolysis facilitates nuclear events during apoptosis. J. Cell Biol. 135:1441-1455.
104. Rogers, H. W., M. P. Callery, B. Deck, and E. R. Unanue. 1996. Listeria monocytogenes induces apoptosis of infected hepatocytes. J. Immunol. 156: 679-684.
105. Rudel, T., and G. M. Bokoch. 1997. Membrane and morphological changes in apoptotic cells regulated by caspase-mediated activation of PAK2. Science 276:1571-1574.
106. Sakahira, H., M. Enari, and S. Nagata. 1998. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature 391:96-99.
107. Samali, A., B. Zhivotovsky, D. Jones, S. Nagata, and S. Orrenius. 1999. Apoptosis: cell death defined by caspase activation. Cell Death Differ. 6:495-496.
108. Sansonetti, P. J., A. Phalipon, J. Arondel, K. Thirumalai, S. Banerjee, S. Akira, K. Takeda, and A. Zychlinsky. 2000. Caspase-1 activation of IL-1β and IL-18 are essential for Shigella flexneri-induced inflammation. Immunity 12:581-590.
109. Sapirstein, A., R. A. Spech, R. Witzgall, and J. V. Bonventre. 1996. Cytosolic phospholipase A2 (PLA2), but not secretory PLA2, potentiates hydrogen peroxide cytotoxicity in kidney epithelial cells. J. Biol. Chem. 271: 21505-21513.
110. Sarin, A., M. S. Williams, M. A. Alexander-Miller, J. A. Berzofsky, C. M. Zacharchuk, and P. A. Henkart. 1997. Target cell lysis by CTL granule exocytosis is independent of ICE/Ced-3 family proteases. Immunity 6:209-215.
111. Savill, J., I. Dransfield, C. Gregory, and C. Haslett. 2002. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2:965-975.
112. Savill, J., and V. Fadok. 2000. Corpse clearance defines the meaning of cell death. Nature 407:784-788.
113. Scaffidi, P., T. Misteli, and M. E. Bianchi. 2002. Release of chromatin protein HMGBl by necrotic cells triggers inflammation. Nature 418:191-195.
114. Schaub, F. J., D. K. Ban, W. C. Liles, L. D. Adams, S. A. Coats, R. K. Ramachandran, R. A. Seifert, S. M. Schwartz, and D. F. Bowen-Pope. 2000. Fas/FADD-mediated activation of a specific program of inflammatory gene expression in vascular smooth muscle cells. Nat. Med. 6:790-796.
115. Schwartz, S. M., and M. R. Bennett. 1995. Death by any other name. Am. J. Pathol. 147:229-234.
116. Schweichel, J. U., and H. J. Merker. 1973. The morphology of various types of cell death in prenatal tissues. Teratology 7:253-266.
117. Shi, L., G. Chen, G. MacDonald, L. Bergeron, H. Li, M. Miura, R. J. Rotello, D. K. Miller, P. Li, T. Seshadri, J. Yuan, and A. H. Greenberg. 1996. Activation of an interleukin 1 converting enzyme-dependent apoptosis pathway by granzyme B. Proc. Natl. Acad. Sci. USA 93:11002-11007.
118. Shi, Y., J. E. Evans, and K. L. Rock. 2003. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425:516-521.
119. Shimizu, S., Y. Eguchi, W. Kamiike, Y. Itoh, J. Hasegawa, K. Yamabe, Y. Otsuki, H. Matsuda, and Y. Tsujimoto. 1996. Induction of apoptosis as well as necrosis by hyposia and predominant prevention of apoptosis by Bcl-2 and Bcl-XL. Cancer Res. 56:2161-2166.
120. Slee, E. A., M. T. Harte, R. M. Kluck, B. B. Wolf, C. A. Casiano, D. D. Newmeyer, H. G. Wang, J. C. Reed, D. W. Nicholson, E. S. Alnemri, D. R. Green, and S. J. Martin. 1999. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J. Cell Biol. 144:281-292.
121. Sperandio, S., I. de Belle, and D. E. Bredesen. 2000. An alternative, non-apoptotic form of programmed cell death. Proc. Natl. Acad. Sci. USA 97:14376-14381.
122. Sperandio, S., K. Poksay, I. De Belle, M. J. Lafuente, B. Liu, J. Nasir, and D. E. Bredesen. 2004. Paraptosis: mediation by MAP kinases and inhibition by AIP-1/Alix. Cell Death Differ.
123. Stenner-Liewen, F., H. Liewen, J. M. Zapata, K. Pawlowski, A. Godzik, and J. C. Reed. 2002. CADD, a Chlamydia protein that interacts with death receptors. J. Biol. Chem. 277:9633-9636.
124. Stennicke, H. R., C. A. Ryan, and G. S. Salvesen. 2002. Reprieval from execution: the molecular basis of caspase inhibition. Trends Biochem. Sci. 27:94-101.
125. Stockbauer, K. E., A. K. Foreman-Wykert, and J. F. Miller. 2003. Bordetella type III secretion induces caspase 1-independent necrosis. Cell Microbiol. 5:123-132.
126. Thornberry, N. A., T. A. Rano, E. P. Peterson, D. M. Rasper, T. Timkey, M. Garcia-Calvo, V. M. Houtzager, P. A. Nordstrom, S. Roy, J. P. Vaillancourt, K. T. Chapman, and D. W. Nicholson. 1997. 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. 272:17907-17911.
127. Trump, B. F., and I. K. Berezesky. 1996. The role of altered [Ca2+]i regulation in apoptosis, oncosis, and necrosis. Biochim. Biophys. Acta 1313: 173-178.
128. Trump, B. F., I. K. Berezesky, S. H. Chang, and P. C. Phelps. 1997. The pathways of cell death: oncosis, apoptosis, and necrosis. Toxicol. Pathol. 25:82-88.
129. van Engeland, M., L. J. Nieland, F. C. Ramaekers, B. Schutte, and C. P. Reutelingsperger. 1998. Annexin V-affinity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31:1-9.
130. Vaux, D. L. 1999. Caspases and apoptosis: biology and terminology. Cell Death Differ. 6:493-494.
131. Verhoven, B., R. A. Schlegel, and P. Williamson. 1995. Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal, on apoptotic T lymphocytes. J. Exp. Med. 182:1597-1601.
132. Vermes, I., C. Haanen, and C. Reutelingsperger. 2000. Flow cytometry of apoptotic cell death. J. Immunol. Methods 243:167-190.
133. Villa, P., S. H. Kaufmann, and W. C. Earnshaw. 1997. Caspases and caspase inhibitors. Trends Biochem. Sci. 22:388-393.
134. Walisser, J. A., and R. L. Thies. 1999. Poly(ADP-ribose) polymerase inhibition in oxidant-stressed endothelial cells prevents oncosis and permits caspase activation and apoptosis. Exp. Cell Res. 251:401-413.
135. Walker, N. P., R. V. Talanian, K. D. Brady, L. C. Dang, N. J. Bump, C. R. Ferenz, S. Franklin, T. Ghayur, M. C. Hackett, L. D. Hammill, et al. 1994. Crystal structure of the cysteine protease interleukin-1 beta-converting enzyme: a (p20/p10)2 homodimer. Cell 78:343-352.
136. Watson, P. R., A. V. Gautier, S. M. Paulin, A. P. Bland, P. W. Jones, and T. S. Wallis. 2000. Salmonella enterica serovars Typhimurium and Dublin can lyse macrophages by a mechanism distinct from apoptosis. Infect. Immun. 68:3744-3747.
137. Watson, V. E., L. L. Hill, L. B. Owen-Schaub, D. W. Davis, D. J. McConkey, C. Jagannath, R. L. Hunter, Jr., and J. K. Actor. 2000. Apoptosis in Mycobactenum tuberculosis infection in mice exhibiting varied immunopathology. J Pathol. 190:211-220.
138. Weinrauch, Y., and A. Zychlinsky. 1999. The induction of apoptosis by bacterial pathogens. Annu. Rev. Microbiol. 53:155-187.
139. Wen, L. P., J. A. Fahrni, S. Troie, J. L. Guan, K. Orth, and G. D. Rosen. 1997. Cleavage of focal adhesion kinase by caspases during apoptosis. J. Biol. Chem. 272:26056-26061.
140. Wilson, K. P., J. A. Black, J. A. Thomson, E. E. Kim, J. P. Griffith, M. A. Navia, M. A. Murcko, S. P. Chambers, R. A. Aldape, S. A. Raybuck, et al. 1994. Structure and mechanism of interleukin-1β converting enzyme. Nature 370:270-275.
141. Wyllie, A. H. 1980. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555-556.
142. Xiang, J., D. T. Chao, and S. J. Korsmeyer. 1996. BAX-induced cell death may not require interleukin 1β-converting enzyme-like proteases. Proc. Natl. Acad. Sci. USA 93:14559-14563.
143. Yu, L., A. Alva, H. Su, P. Dutt, E. Freundt, S. Welsh, E. H. Baehrecke, and M. J. Lenardo. 2004. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 304:1500-1502.
144. Yuan, J., S. Shaham, S. Ledoux, H. M. Ellis, and H. R. Horvitz. 1993. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 75:641-652.
145. Zhang, W. H., X. Wang, M. Narayanan, Y. Zhang, C. Huo, J. C. Reed, and R. M. Friedlander. 2003. Fundamental role of the Rip2/caspase-1 pathway in hypoxia and ischemia-induced neuronal cell death. Proc. Natl. Acad. Sci. USA 100:16012-16017.
146. Zychlinsky, A., C. Fitting, J. M. Cavaillon, and P. J. Sansonetti. 1994. Interleukin 1 is released by murine macrophages during apoptosis induced by Shigella flexneri. J. Clin. Investig. 94:1328-1332.
147. Zychlinsky, A., and P. Sansonetti. 1997. Perspectives series: host/pathogen interactions. Apoptosis in bacterial pathogenesis. J. Clin. Investig. 100:493-495.
148. Zysk, G., L. Bejo, B. K. Schneider-Wald, R. Nau, and H. Heinz. 2000. Induction of necrosis and apoptosis of neutrophil granulocytes by Streptococcus pneumoniae. Clin. Exp. Immunol. 122:61-66.