Methods Utilized in the Study of Apoptosis

Advances in Pharmacology

Volumn 41, Issue C, 1997, Pages 57-87

  Mesner Jr , Peter W ^a   Kaufmann, Scott H ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; ENZYME INHIBITOR;

ANIMAL; APOPTOSIS; FLOW CYTOMETRY; HISTOLOGY; PHYSIOLOGY; REVIEW;

ANIMALS; APOPTOSIS; DNA FRAGMENTATION; ENZYME INHIBITORS; FLOW CYTOMETRY; HISTOLOGICAL TECHNIQUES;

EID: 0030625994     PISSN: 10543589     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1054-3589(08)61054-6     Document Type: Article

References (113)

1. Kerr J.F., Wyllie A.H., and Currie A.R. Apoptosis: A basic biological phenomenon with wide-ranging implications in tissue kinetics. Brit. J. Cancer 26 (1972) 239-257
2. Wyllie A.H., Kerr J.F.R., and Currie A.R. Cell death: The significance of apoptosis. Int. Rev. Cytol. 68 (1980) 251-306
3. Duvall E., and Wyllie A.H. Death and the cell. Immunol. Today 7 (1986) 115-119
4. Searle J., Lawson T.A., Abbott P.J., Harmon B., and Kerr J.F. An electron-microscope study of the mode of cell death induced by cancer-chemotherapeutic agents in populations of proliferating normal and neoplastic cells. J. Pathol. 116 (1995) 129-138
5. Wyllie A.H., and Duvall E. Cell injury and death. In: McGee J.O.D., Isaacson P.G., and Wright N.A. (Eds). In Oxford Textbook of Pathology 1 (1992), Oxford Univ. Press, London 141-179
6. Koss L.G. Diagnostic Cytology and Its Histopathologic Bases. 4th ed. 1 (1992), Lippincott, Philadelphia
7. Martin D.S., Stolfi R.L., Colofiore J.R., Nord L.D., and Sternberg S. Biochemical modulation of tumor cell energy in vivo: II. A lower dose of adriamycin is required and a greater antitumor activity is induced when cellular energy is depressed. Cancer Invest. 12 (1994) 296-307
8. Kornberg R.D. Chromatin structure: A repeating unit of histones and DNA. Science 184 (1974) 868-871
9. Hewish D.R., and Burgoyne L.A. Biochem. Biophys. Res. Commun. 52 (1973) 504
10. Noll M. Subunit structure of chromatin. Nature 251 (1974) 249-251
11. Burgoyne L.A., Hewish D.R., and Mobbs J. Mammalian chromatin substructure studies with the calcium-magnesium endonuclease and two-dimensional polyacrylamide-gel electrophoresis. Biochem. J. 143 (1974) 67-72
12. Wyllie A.H. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284 (1980) 555-556
13. Mesner P.W., Winters T.R., and Green S.H. NGF withdrawal-induced cell death in neuronal PC12 cells resembles that in sympathetic neurons. J. Cell Biol. 119 (1992) 1669-1680
14. Ray S., Ponnathpur V., Huang Y., Tang C., Mahoney M.E., Ibrado A.M., Bullock G., and Bhalla K. 1-Beta-D-arabinofuranosylcytosine-, mitoxantrone-, and paclitaxel-induced apoptosis in HL-60 Cells: Improved method for detection of inter-nucleosomal DNA fragmentation. Cancer Chemother. Pharmacol. 34 (1994) 365-371
15. Tomei L.D., Shapiro J.P., and Cope F.O. Apoptosis in C3H/10T1/2 mouse embryonic cells: Evidence for internucleosomal DNA modification in the absence of double-stranded cleavage. Proc. Natl. Acad. Sci. USA 90 (1993) 853-857
16. Canman C.E., Tang H., Normolle D.P., Lawrence T.S., and Maybaum J. Variations in patterns of DNA damage induced in human colorectal tumor cells by 5-fluorodeoxyuridine-Implications for mechanisms of resistance and cytotoxicity. Proc. Natl. Acad. Sci. USA 89 (1992) 10474-10478
17. Oberhammer F., Wilson J.W., Dive C., Morris I.D., Hickman J.A., Wakeling A.E., Walker P.R., and Sikorska M. Apoptotic death in epithelial cells: Cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation. EMBO. J 12 (1993) 3679-3684
18. Igo-Kemenes T., Greil W., and Zachau H.G. Preparation of soluble chromatin fractions with restriction nucleases. Nucleic Acids Res. 4 (1977) 3387-3400
19. Kyprianou N., and Isaacs J.T. Activation or programmed cell death in the rat ventral prostate after castration. Endocrinology 122 (1988) 552-562
20. Kohn K.W. DNA filter elution: A window on DNA damage in mammalian cells. Bioessays 18 (1996) 505-513
21. Bertrand R., Kohn K.W., Solary E., and Pommier Y. Detection of apoptosis-associated DNA fragmentation using a rapid and quantitative filter elution assay. Drug Dev. Res. 34 (1995) 138-144
22. Solary E., Bertrand R., Jenkins J., and Pommier Y. Radiolabeling of DNA can induce its fragmentation in HL-60 human promyelocytic leukemia cells. Exp. Cell Res. 203 (1992) 495-498
23. Ayusawa D., Arai H., Wataya Y., and Seno T. A specialized form of chromosomal DNA degradation induced by thymidylate stress in mouse FM3A cells. Mutat. Res. 200 (1988) 221-230
24. Dusenbury C.E., Davis M.A., Lawrence T.S., and Maybaum J. Induction of megabase DNA fragments by 5-fluorodeoxyuridine in human colorectal tumor (HT29) cells. Mol. Pharmacol 39 (1991) 285-289
25. Walker P.R., Smith C., Youdale T., Leblanc J., Whitfield J.F., and Sikorska M. Topoisomerase II-reactive chemotherapeutic drugs induce apoptosis in thymocytes. Cancer Res. 51 (1991) 1078-1085
26. Beere H.M., Chresta C.M., and Hickman J.A. Selective inhibition of topoisomerase II by ICRF-193 does not support a role for topoisomerase II activity in the fragmentation of chromatin during apoptosis of human leukemia cells. Mol. Pharmacol. 49 (1996) 842-851
27. Schwartz D.C., Saffran W., Welsh J., Hass R., Goldenberg M., and Cantor C.R. New techniques for purifying large DNAs and studying their properties and packaging. Cold Spring Harbor Symp. Quant. Mol. Biol. 47 (1982) 189-195
28. Carle G.F., Frank M., and Olson M.V. Electrophoretic separations of large DNA molecules by perodic inversion of the electric field. Science 232 (1986) 65-68
29. deGennes P.-B. Reptation of a polymer chain in the presence of fixed obstacles. J. Chem. Phys. 55 (1971) 572-579
30. Bicknell G.R., and Cohen G.M. Cleavage of DNA to large kilobase pair fragments occurs in some forms of necrosis as well as apoptosis. Biochem. Biophys. Res. Commun. 207 (1995) 40-47
31. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd ed. (1989), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
32. 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
33. Gorczyca W., Gong J., and Darzynkiewicz Z. Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res. 53 (1993) 1945-1951
34. Froelich-Ammon S.J., and Osheroff N. Topoisomerase poisons: Harnessing the dark side of enzyme mechanism. J. Biol. Chem. 270 (1995) 21429-21432
35. Gottlieb R.A., Burleson K.O., Kloner R., Babior B.M., and Engler R.L. Reperfusion injury induces apoptosis in rabbit cardiomyocytes. J. Clin. Invest. 94 (1994) 1621-1628
36. Grasl-Kraupp B., Ruttkay-Nedecky B., Koudelka H., Bukowska K., Bursch W., and Schulte-Hermann R. In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: A cautionary note. Hepatology 21 (1995) 1465-1468
37. Charriaut-Marlangue C., and Ben-Ari Y. A cautionary note on the use of the TUNEL stain to determine apoptosis. Neuroreport 7 (1995) 61-64
38. Yasuda M., Umemura S., Osamura R.Y., Kenjo T., and Tsutsumi Y. Apoptotic cells in the human endometrium and placental villi: Pitfalls in applying the TUNEL method. Arch. Histol. Cytol. 58 (1995) 185-190
39. Gong J., Traganos F., and Darzynkiewicz Z. A selective procedure for DNA extraction from apoptotic cells applicable for gel electrophoresis and flow cytometry. Anal. Biochem. 218 (1994) 314-319
40. O'Brien M.C., and Bolton W.E. Comparison of cell viability probes compatible with fixation and permeabilization for combined surface and intracellular staining in flow cytometry. Cytometry 19 (1995) 243-255
41. Vayssiere J.L., Petit P.X., Risler Y., and Mignotte B. Commitment to apoptosis is associated with changes in mitochondrial biogenesis and activity in cell lines conditionally immortalized with Simian Virus 40. Proc. Natl. Acad. Sci. USA 91 (1994) 11752-11756
42. Zamzami N., Marchetti P., Castedo M., Zanin C., Vayssiere J.L., Petit P.X., and Kroemer G. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death. in vivo. J. Exp. Med. 181 (1995) 1661-1672
43. Marchetti P., Susin S.A., Decaudin D., Gamen S., Castedo M., Hirsch T., Zamzami N., Naval J., Senik A., and Kroemer G. Apoptosis-associated derangement of mitochondrial function in cells lacking mitochondrial DNA. Cancer Res. 56 (1996) 2033-2038
44. Krippner A., Matsuno-Yagi A., Gottlieb R.A., and Babior B.M. Loss of function of cytochrome c in Jurkat cells undergoing Fas-mediated apoptosis. J. Biol. Chem. 271 (1996) 21629-21636
45. Liu X., Kim C.N., Yang J., Jemmerson R., and Wang X. Induction of apoptotic program in cell-free extracts: Requirement for dATP and cytochrome c. Cell 86 (1996) 147-157
46. Newmeyer D.D., Farschon D.M., and Reed J.C. Cell-free apoptosis in Xenopus egg extracts: Inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 79 (1994) 353-364
47. Zamzami N., Susin S.A., Marchetti P., Hirsch T., Gomez-Monterrey I., Castedo M., and Guido K. Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183 (1996) 1533-1544
48. Alberts B., Bray D., Lewis J., Raff M., Roberts K., and Watson J.D. Molecular Biology of the Cell. (1989), Garland, New York
49. Azzone G.F., Pietrobon D., and Zoratti M. Curr. Topics Bioenerg. 13 (1984) 1-77
50. Zoratti M., and Szabo I. The mitochondrial permeability transition. Biochim. Biophys. Acta 1241 (1995) 139-176
51. Zamzami N., Marchetti P., Castedo M., Decaudin D., Macho A., Hirsch T., Susin S.A., Petit P.X., Mignotte B., and Kroemer G. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182 (1995) 367-377
52. Cossarizza A., Kalashnikova G., Grassilli E., Chiappelli F., Salvioli S., Capri M., Barbieri D., Troiano L., Monti D., and Franceschi C. Mitochondrial modifications during rat thymocyte apoptosis: A study of the single cell level. Exp. Cell Res. 214 (1994) 323-330
53. Rosser B.G., and Gores G.J. Liver cell necrosis: Cellular mechanisms and clinical implications. Gastroenterology 108 (1995) 252-275
54. van Meer G. Transport and sorting of membrane lipids. Curr. Opin. Cell Biol. 5 (1993) 661-673
55. Koopman G., Reutelingsperger C.P.M., Kuijten G.A.M., Keehnen R.M.J., Pals S.T., and van Oers M.H.J. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84 (1994) 1415-1420
56. Martin S.J., Reutelingsperger C.P., McGahon A.J., Rader J.A., van Schie R.C., LaFace D.M., and Green D.R. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: Inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182 (1995) 1545-1556
57. Kaltenbach J.P., Kaltenbach M.H., and Lyons W.B. Nigrosin as a dye for differentiating live and dead ascites cells. Exp. Cell Res. 15 (1958) 112-117
58. Duke R.C., Chervenak R., and Cohen J.J. Endogenous endonuclease-induced DNA fragmentation: An early event in cell-mediated cytolysis. Proc. Natl. Acad. Sci. USA 80 (1983) 6361-6365
59. Martin D.P., Schmidt R.E., DiStefano P.S., Lowry O.H., Carter J.G., and Johnson E.M. Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J. Cell Biol. 106 (1988) 829-844
60. Fesus L., Thomazy V., and Falus A. Induction and activation of tissue transglutaminase during programmed cell death. FEBS Lett. 224 (1987) 104-108
61. Fesus L., and Thomazy V. Search for the function of tissue transglutaminase: Its possible involvement in the biochemical pathway of programmed cell death. Adv. Exp. Med. Biol. 231 (1988) 119-134
62. English H.F., Kyprianou N., and Isaacs J.T. Relationship between DNA fragmentation and apoptosis in the programmed cell death in the rat prostate following castration. Prostate 15 (1989) 233-250
63. Schwartzman R.A., and Cidlowski J.A. Internucleosomal deoxyribonucleic acid cleavage activity in apoptotic thymocytes: Detection and endocrine regulation. Endocrinology 128 (1991) 1190-1197
64. Lazebnik Y.A., Kaufmann S.H., Desnoyers S., Poirier G.G., and Earnshaw W.C. Cleavage of poly(ADP-ribose)polymerase by a proteinase with properties like ICE. Nature 371 (1994) 346-347
65. Enari M., Talanian R.V., Wong W.W., and Nagata S. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature 380 (1996) 723-726
66. Compton M.M., and Cidlowski J.A. Identification of a glucocorticoid-induced nuclease in thymocytes. A potential "lysis gene" product. J. Biol. Chem. 262 (1987) 8288-8292
67. Alnemri E.S., and Litwack G. Glucocorticoid-induced lymphocytolysis is not mediated by an induced endonuclease. J. Biol. Chem. 264 (1989) 4104-4111
68. Baxter G.D., Smith P.J., and Lavin M.F. Molecular changes associated with induction of cell death in a human T-cell leukaemia line: Putative nucleases identified as histones. Biochem. Biophys. Res. Commun. 162 (1989) 30-37
69. Black R.A., Kronheim S.R., and Sleath P.R. Activation of interleukin-1β by a co-induced protease. FEBS Lett. 247 (1989) 386-390
70. Tata J.R. Requirement for RNA and protein synthesis for induced regression of the tadpole tail in organ culture. Dev. Biol. 13 (1966) 77-94
71. Mosher K.M., Young D.A., and Munck A. Evidence for irreversible, actinomycin D-sensitive, and temperature-sensitive steps following binding of Cortisol to glucocorticoid receptors and preceding effects on glucose metabolism in rat thymus cells. J. Biol. Chem. 246 (1971) 654-659
72. Hallahan C., Young D.A., and Munck A. Time course of early events in the action of glucocorticoids on rat thymus cells in vitro. Synthesis and turnover of a hypothetical cortisol-induced protein inhibition of glucose metabolism and of a presumed ribonucleic acid. J. Biol. Chem. 248 (1973) 2922-2927
73. ++ dependent protein kinase. Biochem. Biophys. Res. Commun. 135 (1986) 397-402
74. Nakano H., Kobayashi E., Takahashi I., Tamaoki T., Kuzuu Y., and Iba H. Staurosporine inhibits tyrosine-specific protein kinase activity of Rous sarcoma virus transforming protein p60. J. Antibiot. 40 (1987) 706-708
75. Fujita-Yamaguchi Y., and Kathuria S. Characterization of receptor tyrosine-specific protein kinases by the use of inhibitors. Staurosporine is a 100-times more potent inhibitor of insulin receptor than IGF-I receptor. Biochem. Biophys. Res. Commun. 157 (1988) 955-962
76. Takahashi I., Saitoh Y., Yoshida M., Sano H., Nakano H., Morimoto M., and Tamaoki T. UCN-01 and UCN-02, new selective inhibitors of protein kinase C. II. Purification, physico-chemical properties, structural determination and biological activities. J. Antibiot. 42 (1989) 571-576
77. Ruegg U.T., and Burgess G.M. Staurosporine, K-252 and UCN-01: Potent but nonspecific inhibitors of protein kinases. Trends Pharmacol. Sci. 10 (1989) 218-220
78. Chow S.C., Peters I., and Orrenius S. Re-evaluation of the role of de novo protein synthesis in rat thymocyte apoptosis. Exp. Cell Res. 216 (1995) 149-159
79. Sheinen R., and Humbert J. Some aspects of eukaryotic DNA replication. Annu. Rev. Biochem. 47 (1978) 277-316
80. Pike L.M., Khym J.X., Jones M.H., Lee W.H., and Volkin E.W. Suppression of cytidylate biosynthesis by protein synthesis antagonists. J. Biol. Chem. 255 (1980) 3340-3347
81. Volkin E., Boling M.E., Jones M.H., Lee W.H., and Pike L.M. Suppression of the biosynthesis of guanosine triphosphate by protein synthesis inhibitors. J. Biol. Chem. 255 (1980) 9105-9109
82. Ennis H.L. Synthesis of ribonucleic acid in L cells during inhibition of protein synthesis by cycloheximide. Mol. Pharmacol. 2 (1966) 543-557
83. Yeh J.Y., Ou B.R., and Forsberg N.E. Amino acid transport system L in muscle cells: Biochemical properties and its relation to protein synthesis. Biochim. Biophys. Acta 1108 (1992) 1-7
84. Low B.C., Ross I.K., and Grigor M.R. Glucose deprivation and acute cycloheximide treatment stimulate system I. amino acid transport in cultured vascular smooth muscle cells. J. Biol. Chem. 269 (1994) 32098-32103
85. Barry M.A., Behnke C.A., and Eastman A. Activation of programmed cell death (apoptosis) by cisplatin, other anticancer drugs, toxins and hyperthermia. Biochem. Pharmacol. 40 (1990) 2353-2362
86. Voris B.P., and Young D.A. Glucocorticoid-induced proteins in rat thymus cells. J. Biol. Chem. 256 (1981) 11319-11329
87. Maytin E.V., and Young D.A. Separate glucocorticoid, heavy metal, and heat shock domains in thymic lymphocytes. J. Biol. Chem. 258 (1983) 12718-12722
88. Hallick R.B., Chelm B.K., Gray P.W., and Orozco E.M. Use of aurintricarboxylic acid as an inhibitor of nucleases during nucleic acid isolation. Nucleic Acids Res. 4 (1977) 3055-3064
89. Stewart M.L., Grollman A.P., and Huang M.T. Aurintricarboxylic acid: inhibitor of initiation of protein synthesis. Proc. Natl. Acad. Sci. USA 68 (1971) 97-101
90. Bina-Stein M., and Tritton T.R. Aurintricarboxylic acid is a nonspecific enzyme inhibitor. Mol. Pharmacol. 21 (1976) 191-193
91. Carias J.R., and Julien R. Inhibition competitive de la PHE: tRNA ligase des embryons de ble par l'acide aurine tricarboxylique. FEBS Lett. 56 (1975) 303-306
92. Givens J.F., and Manly K.F. Inhibition of RNA-directed DNA polymerase by aurintricarboxylic acid. Nucleic Acids Res. 3 (1976) 405-418
93. Akiyama S., Kuwano M., Yamamoto M., and Endo H. The effect of aurintricarboxylic acid on RNA polymerase from rat liver. J. Biol. Chem. 81 (1977) 135-141
94. Lowery C., and Richardson J.P. Characterization of the nucleoside triphosphate phosphohydrolase (ATPase) activity of RNA synthesis termination factor P. I. Enzymatic properties and effects of inhibitors. J. Biol Chem. 252 (1977) 1375-1380
95. Catchpoole D.R., and Stewart B.W. Inhibition of topoisomerase II by aurintricarboxylic acid: Implication for mechanisms of apoptosis. Anticancer Res. 14 (1994) 853-856
96. Benchokroun Y., Couprie J., and Larsen A.K. Aurintricarboxylic acid, a putative inhibitor of apoptosis, is a potent inhibitor of DNA topoisomerase II in vitro and in Chinese hamster fibrosarcoma cells. Biochem. Pharmacol. 49 (1995) 305-313
97. Hough R., Pratt G., and Rechsteiner M. Ubiquitin-lysozyme conjugates. Identification and characterization of an ATP-dependent protease from rabbit reticulocyte lysates. J. Biol. Chem. 261 (1986) 2400-2408
98. Posner A., Raser K.J., Hajimohammadreza I., Yuen P.W., and Wang K.K. Aurintricarboxylic acid is an inhibitor of mu- and m-calpain. Biochem. Mol. Biol. Int. 36 (1995) 291-299
99. Hugunin M., Quintal L.J., Mankovich J.A., and Ghayur T. Protease activity of in vitro transcribed and translated Caenorhabditis elegans cell death gene (ced-3) product. J. Biol. Chem. 271 (1996) 3517-3522
100. Barrett A.J. Human cathcpsin B1: Purification and some properties of the enzyme. Biochem. J. 131 (1973) 809-822
101. Takahashi A., Alnemri E.S., Lazebnik Y.A., Fernandes-Alnemri T., Litwack G., Moir R.D., Goldman R.D., Poirier G.G., Kaufmann S.H., and Earnshaw W.C. Cleavage of Lamin A by Mch2α but not CPP32: Multiple ICE-related proteases with distinct substrate recognition properties are active in apoptosis. Proc. Natl. Acad. Sci. USA 93 (1996) 8395-8400
102. Kaufmann S.H. Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, camptothecin, and other cytotoxic anticancer drugs: A cautionary note. Cancer Res. 49 (1989) 5870-5878
103. Smith G.K., Duch D.S., Dev I.K., and Kaufmann S.H. Metabolic effects and kill of human T-cell leukemia by 5-deazaacyclotetrahydrofolate, a specific inhibitor of glycineamide ribonucleotide transformylase. Cancer Res. 52 (1992) 4895-4903
104. Kaufmann S.H., Desnoyers S., Ottaviano Y., Davidson N.E., and Poirier G.G. Specific proteolytic fragmentation of poly(ADP-ribose)polymerase: An early marker of chemotherapy-induced apoptosis. Cancer Res. 53 (1993) 3976-3985
105. Yuan J., Shaham S., Ledoux S., Ellis H.M., and Horvitz H.R. The C. elegans cell death gene and Ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 75 (1993) 641-652
106. Bruno S., Del Bino G., Lassota P., Giaretti W., and Darzynkiewicz Z. Inhibitors of proteases prevent endonucleolysis accompanying apoptotic death of HL-60 leukemic cells and normal thymocytes. Leukemia 6 (1992) 1113-1120
107. Weaver V.M., Lach B., Walker P.R., and Silorska M. Role of proteolysis in apoptosis: Involvement of serine proteases in internucleosomal DNA fragmentation in immature thymocytes. Biochem. Cell Biol. 71 (1993) 488-500
108. Lazebnik Y.A., Takahaski A., Moir R., Goldman R., Poirier G.G., Kaufmann S.H., and Earnshaw W.C. Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc. Natl. Acad. Sci. USA 92 (1995) 9042-9046
109. Fernandes-Alnemri T., Takahashi A., Armstrong R., Krebs J., Fritz L., Tomaselli K.J., Wang L., Yu Z., Croce C.M., Salveson G., Earnshaw W.C., Litwack G., and Alnemri E.S. Mch3, a novel human apoptotic cystein protease highly related to CPP32. Cancer Res. 55 (1995) 6045-6052
110. Martins L.M., Kottke T.J., Mesner P., Basi G.S., Sinha S., Frigon Jr. N., Tatar E., Tung J.S., Bryant K., Takahashi A., Svingen P.A., Madden B.J., McCormick D.J., Earnshaw W.C., and Kaufmann S.H. Activation of multiple interleukin-1β converting enzyme homologues in cytosol and nuclei of HL-60 cells during etoposide-induced apoptosis. J. Biol. Chem. 272 (1997) 7421-7430
111. Dubrez L., Savoy I., Hamman A., and Solary E. Pivotal role of a DEVD-sensitive step in etoposide-induced and Fas-mediated apoptotic pathways. EMBO J. 15 (1996) 5504-5512
112. Aoyagi T., Miyata S., Nanbo M., Kojima F., Matsuzaki M., Ishizuka M., Takeuchi T., and Umezawa H. Biological activities of leupeptins. J. Antibiot. 22 (1969) 558-568
113. Grimm L.M., Goldberg A.L., Poirier G.G., Schwartz L.M., and Osborne B.A. Proteasomes play an essential role in thymocyte apoptosis. EMBO J. 15 (1996) 3835-3844