Nuclear events of apoptosis in vitro in cell-free mitotic extracts: A model system for analysis of the active phase of apoptosis

Journal of Cell Biology

Volumn 123, Issue 1, 1993, Pages 7-22

  Lazebnik, Yuri A ^a   Cole, Susan ^a   Cooke, Carol A ^a   Nelson, William G ^a   Earnshaw, William C ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GALLUS GALLUS;

APHIDICOLIN; CALCIUM; CELL NUCLEUS DNA; MANGANESE; NOCODAZOLE; NUCLEASE; ZINC;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL NUCLEUS; CELL ULTRASTRUCTURE; CELL VIABILITY; CHICKEN; CHROMATIN; CONTROLLED STUDY; DIAGNOSIS; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MITOSIS; MODEL; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL;

ANIMAL; APHIDICOLIN; APOPTOSIS; CELL FRACTIONATION; CELL NUCLEUS; CELL-FREE SYSTEM; CHICKENS; CHROMOSOMES; COMPARATIVE STUDY; DNA DAMAGE; HELA CELLS; HUMAN; MICE; MITOSIS; NUCLEAR ENVELOPE; NUCLEOSOMES; PROTAMINE KINASE; S PHASE; SUPPORT, NON-U.S. GOV'T; TUMOR CELLS, CULTURED; ZINC;

EID: 0027437541     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.123.1.7     Document Type: Article

References (65)

1. Allan, D, J., B. V. Harmon, and S. A. Roberts. 1992. Spermatogonial apoptosis has three morphologically recognizable phases and shows no circadian rhythm during normal spermatogenesis in the rat. Cell Prolif. 25:241-250.
2. Allen, T. D. 1987. Ultrastructural aspects of cell death. In Perspectives on Mammalian Cell Death (C. S. Potten, editor. Oxford University Press, Oxford. 39-65.
3. Alnemri, E. S., T. F. Fernandes, S. Haldar, C. M. Croce, and G. Litwack. 1992. Involvement of BCL-2 in glucocorticoid-induced apoptosis of human pre-B-leukemias. Cancer Res. 52:491-495.
4. Arenas, M. J., R. G. Morris, and A. H. Wyllie. 1990. Apoptosis: the role of the endonuclease. Am. J. Pathol. 136:593-608.
5. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1991. Current Protocols in Molecular Biology. John Wiley & Sons Inc., New York. Unit 2.1.
6. Barry, M. A., and A. Eastman. 1993. Identification of deoxyribonuclease II as an endonuclease involved in apoptosis. Arch. Biochem. Biophys. 300: 440-450.
7. Cohen, G. M., X.-M. Sun, R. T. Snowden, D. Dinsdale, and D. N. Skilleter. 1992. Key morphological features of apoptosis may occur in the absence of internucleosomal DNA fragmentation. Biochem. J. 286:331-334.
8. Cohen, J. J., and R. C. Duke. 1984. Glucocorticoid activation of a calcium-dependent endonuclease in thymocyte nuclei leads to cell death. J. Immunol. 132:38-42.
9. Cotter, T. G., S. V. Lennon, J. M. Glynn, and D. R. Green. 1992. Microfilament-disrupting agents prevent the formation of apoptotic bodies in tumor cells undergoing apoptosis. Cancer Res. 52:997-1005.
10. Cowan, W. M., J. W. Fawcett, D. D. M. O'Leary, and B. B. Stanfield. 1984. Regressive events in neurogenesis. Science (Wash. DC). 225:1258-1265.
11. Davis, F. M., T. Y. Tsao, S. K. Fowler, and P. N. Rao. 1983. Monoclonal antibodies to mitotic cells. Proc. Natl. Acad. Sci. USA. 80:2926-2930.
12. Duke, R. C., R. Chervenak, and J. J. Cohen. 1983. Endogenous endonuclease-induced DNA fragmentation: an early event in cell mediated cytolysis. Proc. Natl. Acad. Sci. USA. 80:6361-6365.
13. Dwyer, N., and G. Blobel. 1976. A modified procedure for the isolation of a pore complex-lamina fraction from rat liver nuclei. J. Cell Biol. 70:581-591.
14. ++ inhibits both tumor necrosis factor-mediated DNA fragmentation and cytolysis. Int. J. Cancer. 44:315-319.
15. Gerace, L., and G. Blobel. 1980. The nuclear envelope lamina is reversibly depolymerized during mitosis. Cell. 19:277-287.
16. Gerace, L., and B. Burke. 1988. Functional organization of the nuclear envelope. Ann. Rev. Cell. Biol. 4:335-374.
17. Glucksmann, A. 1951. Cell deaths in normal vertebrate ontogeny. Biol. Rev. 26:289-300.
18. Gottlieb, J., and N. Muzczka. 1990. Purification and characterization of HeLa endonuclease R: a G-specific mammalian endonuclease. J. Biol. Chem. 265:10836-10841.
19. Gregory, C., C. Dive, S. Henderson, C. A. Smith, G. T. Williams, J. Gordon, and A. Rickinson. 1991. Activation of Epstein-Barr virus latent genes protects human B cells from death by apoptosis. Nature (Lond.). 349:612-614.
20. Henderson, S., M. Rowe, C. Gregory, D. Croom-Carter, F. Wang, R. Longnecker, E. Kieff, and A. Rickinson. 1991. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell. 65:1107-1115.
21. Hockenbery, D., G. Nunez, C. Milliman, P. D. Schreiber, and S. J Korsmeyer. 1990. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature (Lond.) 348:334-336.
22. Högner, D., K. Lepper, G. Seibold, and E. Jost. 1988. Lamin disassembly kinetics: a cell-free system with extracts from mitotic HeLa cells. Exp. Cell Res. 176:281-296.
23. Junowicz, E., and J. H. Spencer. 1973. Studies on bovine pancreatic deoxyribonuclease A II. The effect of different bivalent metals on the specificity of degradation of DNA. Biochem. Biophys. Acta. 312:85-102.
24. Kaufmann, S. H. 1989. Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, camptothecin, and other cytotoxic anticancer drugs: a cautionary note. Cancer Res. 49:5870-5878.
25. Kerr, J. F. R. 1971. Shrinkage necrosis: a distinct mode of cellular death. J. Pathol. 105:13-20.
26. Kerr, J. F. R., B. Harmon, and J. Searle. 1974. An electron microscope study of cell deletion in the anuran tadpole tail during spontaneous metamorphosis with special reference to apoptosis of striated muscle fibres. J. Cell Sci. 14:571-585.
27. Kerr, J. F. R., J. Searle, B. V. Harmon, and C. J. Bishop. 1987. Apoptosis. In Perspectives on Mammalian Cell Death. C. S. Potten, editor. Oxford University Press, Oxford, pg 93.
28. Kruman, I. I., N. P. Matylevich, I. P. Beletsky. V. N. Afanasyev, and S. R. Umansky. 1991. Apoptosis of murine BW 5147 thymoma cells induced by dexamethasone and γ-irradiation. J. Cell Physiol 148:267-273.
29. Kung, A. L., A. Zetterberg, S. W. Sherwood, and R. T. Schimke. 1990. Cytotoxic effects of cell cycle phase specific agents: Result of cell cycle perturbation. Cancer Res. 50:7307-7317.
30. Kyprianou, N., H. F. English, J. T. Issacs. 1988. Activation of a Ca2 +-Mg2 + -dependent endonuclease as an early event in castration-induced prostatic cell death. Prostate. 13:103-117.
31. Kyprianou, N., and J. T. Issacs. 1988. Activation of programmed cell death in the rat ventral prostate after castration. Endocrinology. 122:552-562.
32. Langlois, A. J., K. Lapis, R. Ishizaki, J. W. Beard, and D. P. Bolognesi. 1974. Isolation of a transplantable cell line induced by the MC29 avian leukosis virus. Cancer Res. 34:1457-1464.
33. Lebkowski, J. S., and U. K. Laemmli. 1982. Non-histone proteins and longrange organization of HeLa interphase DNA. J. Mol. Biol. 156:325-344.
34. Lehner, C. F., V. Kurer, H. M. Eppenberger, and E. A. Nigg. 1986. The nuclear lamin protein family in higher vertebrates: identification of quantitatively minor lamin proteins by monoclonal antibodies. J. Biol Chem. 261:13293-13301.
35. Levine, B., Q. Huang, J. T. Isaacs, J. C. Reed, D. E. Griffin, and J. M. Hardwick. 1993. Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene. Nature (Lond.). 361:739-742.
36. Lohka, M., and J. Maller. 1985. Induction of nuclear envelope breakdown, chromosome condensation, and spindle formation in cell-free extracts. J. Cell Biol. 101:518-523.
37. 1. Cell. 70:949-959.
38. MacDonald, H. R., and R. K. Lees. 1990. Programmed death of autoreactive thymocytes. Nature (Lond.). 343:642-644.
39. Martin, D. P., R. E. Schmidt, P. S. DoStefano, O. H. Lowry, J. G. Carter, and E. M. Johnson, Jr. 1988. Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J. Cell Biol. 106:829-844.
40. McConkey, D. J., P. Hartzell, P. Nicotera, and S. Orrenius. 1989. Calciumactivated DNA fragmentation kills immature thymocytes. FASEB (Fed. Am. Soc. Exp. Biol) J. 3:1843-1849.
41. McNeil, P. L., R. F. Murphy, F. Lanni, and D. L. Taylor. 1984. A method for incorporating macromolecules into adherent cells. J. Cell Biol. 98: 1556-1564.
42. Miake-Lye, R., and M. Kirschner. 1985. Induction of early mitotic events in a cell-free system. Cell. 41:165-175.
43. Molè-Bajer, J. 1958. Cine-micrographic analysis of C-mitosis in endosperm. Chromosoma (Berl.). 9:332-358.
44. Nakagawa, J., G. T. Kitten, and E. A. Nigg. 1989. A somatic cell-derived system for studying both early and late mitotic events in vitro. J. Cell Sci. 94:449-462.
45. Newport, J., and T. Spann. 1987. Disassembly of the nucleus in mitotic extracts: membrane vesicularization. lamin disassembly, and chromosome condensation are independent processes. Cell. 48:219-230.
46. Nurse, P. 1990. Universal control mechanism regulating onset of M-phase. Nature (Lond.). 344:503-508.
47. Oberhammer, F., G. Fritsch, M. Schmied, M. Pavelka, D. Ptintz, A. F. Purchio, H. Lassmann, and R. Schulte-Hermann. 1993. Condensation of the chromatin at the membrane of an apoptotic nucleus is not associated with activation of an endonuclease. J. Cell Sci. 104:317-326.
48. Peitsch, M. C., B. Polzar, H. Stephan, T. Crompton, H. R. MacDonald, H. G. Mannherz, and J. Tschopp. 1993. Characterization of the endogenous deoxyribonuclease involved in nuclear DNA degradation during apoptosis (programmed cell death). EMBO (Eur. Mol. Biol. Organ.) J. 12:371-377.
49. Peter, M., J. Nakagawa, M. Dorée, J. C. Labbé, and E. A. Nigg. 1990. In 2itro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell. 61:591-602.
50. Saunders, J. W., Jr. 1966. Death in embryonic systems. Science (Wash. DC). 154:604-612.
51. Sen, S., and M. D'Ilncalci. 1992. Apoptosis. Biochemical events and relevance to cancer chemotherapy. FEBS (Fed. Eur. Biochem. Soc.) Lett. 307: 122-127.
52. Sheridan, J. W., C. J. Bishop, and R. J. Simmons. 1981. Biophysical and morphological correlates of kinetic change and death in a starved human melanoma cell line. J. Cell Sci. 49:119-137.
53. Shi, Y., B. M. Sahai, and D. R. Green. 1989. Cyclosporin A inhibits activationinduced cell death in T cell hybridomas and in thymocytes. Nature (Lond.). 339:625-627.
54. Smith, C. A., G. T. Williams, R. Kingston, E. J. Jenkinson, and J. J. T. Owen. 1989. Antibodies to CD3/T-cell receptor complex induce death by apoptosis in immature T cells in thymic cultures. Nature (Lond.). 237:181-184.
55. Suprynowicz, F. A., and L. Gerace. 1986. A fractionated cell-free system for analysis of prophase nuclear disassembly. J. Cell Biol. 103:2073-2081.
56. Tsujimoto, Y., E. Jaffe, J. Cossman, and C. M. Croce. 1985. Involvement of the be 1-2 gene in human follicular lymphoma. Science (Wash. DC). 228: 1440-1443.
57. Ucker, D. S. 1987. Cytotoxic T-lymphocytes and glucocorticoids activate an endogenous suicide process in target cells. Nature (Lond.). 327:62-64.
58. Ucker, D. S. 1991. Death by suicide: one way logo in mammalian cellular development. New Biologist. 3:103-109.
59. Ucker, D. S., P. S. Obermiller, W. Eckhart, J. P. Apgar, N. A. Berger, and J. Meyers. 1992. Genome digestion is a dispensable consequence of physiological cell death mediated by cytotoxic T lymphocytes. Mol. Cell Biol. 12:3060-3069.
60. Warters, R. L. 1992. Radiation-induced apoptosis in a murine T-cell hybridoma. Cancer Res. 53:883-890.
61. Williams, G. T., C. A. Smith, E. Spooncer, T. M. Dexter, and D. R. Taylor. 1990. Haematopoietic colony stimulating factors promote cell survival by suppressing apoptosis. Nature. 343:76-79.
62. Wood, E. R., and W. C. Eamshaw. 1990. Mitotic chromatin condensation in vitro using somatic cell extracts and nuclei with variable levels of endogenous topoisomerase II. J. Cell Biol. 111:2839-2850.
63. Wyllie, A.M. 1980. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature (Lond.). 284:555-556.
64. Wyllie, A. H., J. F. R. Kerr, and A. R. Currie. 1980. Cell death: The significance of apoptosis. Int. Rev. Cytol. 68:251-305.
65. Yuan, J. Y., and H. R. Horvitz. 1990. The Caenorhabditis elegans genes ced-3 and ced-4 act cell autonomously to cause programmed cell death. Dev. Biol. 138:33-41.