Presence of double-strand breaks with single-base 3′ overhangs in cells undergoing apoptosis but not necrosis

Journal of Cell Biology

Volumn 135, Issue 5, 1996, Pages 1369-1376

  Didenko, Vladimir V ^a   Hornsby, Peter J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I; DNA NUCLEOTIDYLEXOTRANSFERASE; DOUBLE STRANDED DNA; ENDONUCLEASE;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CONCENTRATION RESPONSE; CONTROLLED STUDY; DIAGNOSIS; DNA DAMAGE; DNA STRAND BREAKAGE; ENZYME ANALYSIS; NONHUMAN; PREDICTION; PRIORITY JOURNAL; RAT;

ADRENAL GLANDS; ANIMALS; APOPTOSIS; AUTOLYSIS; CATTLE; CHILD, PRESCHOOL; DNA; DNA DAMAGE; DNA FRAGMENTATION; HEAT; HUMANS; MALE; NECROSIS; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; THYMUS GLAND; WILMS TUMOR;

EID: 0030458564     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.5.1369     Document Type: Article

References (39)

1. +-requiring mechanism(s). J. Biol. Chem. 265:17323-17333.
2. Arends, M.J., R.G. Morris, and A.H. Wyllie. 1990. Apoplosis. The role of the endonuclease. Am. J. Pathol. 136:593-608.
3. Ausubel, F.M., R. Brent, R.E. Kingston, D.D. Moore, J.G. Seidman, J.A. Smith, and K. Struhl. 1992. Short Protocols in Molecular Biology. Greene Publishing Associates, New York. pp. A3-6-A3-7.
4. Beletsky, I.P., J. Matyasova, L.V. Nikonova, M. Skalka, and S.R. Umansky 1989. On the role of Ca, Mg-dcpendent nuclease in the postirradiation degradation of chromatin in lymphoid tissues. Gen. Physiol. Biophys. 8:381-398.
5. Campagne, M.V., P.J. Lucassen, J.P. Vermeulen, and R. Balazs. 1995. NMDA and kainate induce internucleosomal DNA cleavage associated with both apoptotic and necrotic cell death in the neonatal rat brain. Eur. J. Neurosci. 7:1627-1640.
6. Clark, J.M. 1988. Novel non-templated nucleotide addition reactions catalyzed by procaryotic and eucaryotic DNA polymerases. Nucleic Acids Res. 16:9677-9686.
7. Cusick, M.E., P.M. Wassarman, and M.L. DePamphilis. 1989. Application of nucleases to visualizing chromatin organization at replication forks. Methods Enzymol. 170:290-316.
8. Didenko, V.V., and P.J. Hornsby. 1996. A quantitative luminescence assay for nonradioactive nucleic acid probes. J. Histochem. Cytochem. 44:657-660.
9. WAF1/CIP1/SDII and p53 apopiotic cells in the adrenal cortex and induction by ischemia/reperfusion injury. J. Clin. Invest. 97:1723-1731.
10. Gates, G.F., J.H. Miller, and P. Stanley. 1980. Necrosis of Wilms tumors. J. Urol. 123:916-920.
11. Gavrieli, Y., Y. Sherman, and S.A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:493-501.
12. Gottlieb, R.A., H.A. Giesing, R.L. Engler, and B.M. Babior. 1995. The acid deoxyribonuclease of neutrophils: a possible participant in apoptosis-associated genome destruction. Blood. 86:2414-2418.
13. Grosse, F., and A. Manns. 1993. Terminal deoxyribonucleotidyl transferase (EC 2.7.7.31). In Methods in Molecular Biology. Vol. 16. Enzymes of Molecular Biology. M.M. Burrell. editor. Humana Press, Totowa, NJ. 95-105.
14. Holtzman, E. 1989. Lysosomcs. Plenum Press, New York. p.2.
15. Hu, G. 1993. DNA polymerase-catalyzed addition of nontemplated extra nucleolides to the 3′ end of a DNA fragment. DNA Cell Biol. 12:763-770.
16. Imlay, J.A., and S. Linn. 1988. DNA damage and oxygen radical toxicity. Science (Wash. DC) 240:1302-1309.
17. 2+ -dependent endonuclease associated with apoptosis. J Immunol. 156:922-931.
18. Lindahl, T. 1993. Instability and decay of the primary structure of DNA. Nature (Lond.). 362:709-715.
19. Lutter, L.C. 1979. Precise location of DNase 1 cutting sites in the nucleosome core determined by high resolution gel electrophoresis. Nucleic Acids Res. 6:41-56.
20. Majno, G., and I. Joris. 1995. Apoptosis, oncosts, and necrosis. An overview of cell death. Am. J. Pathol. 146:3-15.
21. Mannherz, H.G., M.C. Peitsch, S. Zanotti, R. Paddenberg, and B. Polzar. 1995. A new function for an old enzyme: the role of DNase I in apoptosis. Curr. Top. Microbiol. Immunol. 198:161-174.
22. Maunders, M.J. 1993. DNA and RNA ligases (EC 6.6.1.1 EC 6.5.1.2, and EC 6.5.1.3). In Methods in Molecular Biology. Vol. 16. Enzymes of Molecular Biology. M.M. Burrell, editor. Humana Press, Totowa, NJ. 213-230.
23. Metcalf, D. 1964. The thymus and lymphopoiesis. In The Thymus in Immunobiology. Structure, Function, and Role in Disease. R.A. Good and A.E. Gabrielson, editors. Harper and Row, New York. 150-182.
24. Montague, J.W., M.L. Gaido, C. Frye, and J.A. Cidlowski. 1994. A calcium-dependent nuclease from apoptotic rat thymocytes is homologous with cyclophilin. Recombinant cyclophilins A. B, and C have nuclease activity. J. Biol. Chem. 269:18877-18880.
25. Nikonova, L.V., P.A. Nelipovich, and S.R. Umansky. 1982. The involvement of nuclear nucleases in rat thymocyte DNA degradation after γ-irradiation. Biochim. Biophys. Acta. 699:281-289.
26. Peitsch, M.C., C. Muller, and J. Tschopp. 1993. DNA fragmentation during apoptosis is caused by frequent single-strand cuts. Nucleic Acids Res. 21:4206-4209.
27. Polzar, B., M.C. Peitsch, R. Loos, J. Tschopp, and H.G. Mannherz. 1993. Overexpression of deoxyribonuclease I (DNase I) transfected inlo COS-cells: its distribution during apoptotic cell death. Eur. J. Cell Biol. 62:397-405.
28. Polzar, B., S. Zanotti, H. Stephan, F. Rauch, M.C. Peitsch, M. Irmler, J. Tschopp, and H.G. Mannherz. 1994. Distribution of deoxyribonuciease I in rat tissues and its correlation to cellular turnover and apoptosis (programmed cell death). Eur. J. Cell Biol. 64:200-210.
29. Rink, A., K.M. Fung, J.Q. Trojanowski, V.M.Y. Lee, E. Neugehauer, and T.K. Mcintosh. 1995. Evidence of apoplotic cell death after experimental traumatic brain injury in the rat. Am. J. Pathol. 147:1575-1583.
30. Shiokawa, D., H. Ohyama, T. Yamada, K. Takahashi, and S. Tanuma. 1994. Identification of an endonuclease responsible for apoptosis in rat thymocytes. Eur. J. Biochem. 226:23-30.
31. Sollner-Webb, B., W. Melchior, Jr., and G. Felsenfeld. 1978. DNAase I. DNAase II and staphylococcal nuclease cut at different, yet symmetrically located, sites in the nucleosome core. Cell. 14:611-627.
32. Van Dyck, J.M., and R. Wattiaux. 1968. Distribution intracellulaire de l'exonuclease acide dans le foie de rat. Eur. J. Biochem. 7:13-20.
33. van Haelst, U. 1967. Light and electron microscopic study of the normal and pathological thymus of the rat. 1. The normal thymus. Z. Zellforsch. Mikrosk. Anat. 77:534-553.
34. van Haelst, U. 1967. Light and electron microscopic study of the normal and pathological thymus of the rat. II. The acute thymic involution. Z. Zellforsch. Mikrosk. Anat. 80:153-182.
35. Wolffe, A.P. 1992. Chromatin: Structure and Function. Academic Press, New York. pp. 33-38.
36. Wyllie, A.H. 1980. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature (Lond.). 284:555-556.
37. Sdil in adrenocortical cells when they are placed in culture. Exp. Cell Res. 221:126-131.
38. Zanotti, S., B. Polzar, H. Stephan, U. Doll, J. Niessing, and H.G. Mannherz. 1995. Localization of deoxyribonuclease I gene transcripts and protein in rat tissues and its correlation with apoptotic cell elimination. Histochem. Cell Biol. 103:369-377.
39. Zhang, C, M.J. Robertson, and S.F. Schlossman. 1995. A triplet of nuclease proteins (NP42-50) is activated in human Jurkat cells undergoing apoptosis. Cell. Immunol. 165:161-167.