Enhancement of Ca2+‐dependent Endonuclease Activity in L1210 Cells during Apoptosis Induced by 1‐β‐D‐Arabinofuranosylcytosine: Possible Involvement of Activating Factor(s)

Rumiko Takauji; Akira Yoshida; Hiromichi Iwasaki; Kaoru Tohyama; Takanori Ueda; Toru Nakamura

doi:10.1111/j.1349-7006.1995.tb02452.x

. 1995 Jul;86(7):677–684. doi: 10.1111/j.1349-7006.1995.tb02452.x

Enhancement of Ca²⁺‐dependent Endonuclease Activity in L1210 Cells during Apoptosis Induced by 1‐β‐D‐Arabinofuranosylcytosine: Possible Involvement of Activating Factor(s)

Rumiko Takauji ¹, Akira Yoshida ¹, Hiromichi Iwasaki ¹, Kaoru Tohyama ¹, Takanori Ueda ¹, Toru Nakamura ¹

PMCID: PMC5920892 PMID: 7559086

Abstract

Internucleosomal DNA fragmentation and morphological changes in nuclei typical of apoptosis were observed in L1210 cells incubated with 1.0 μg/ml of 1‐β‐D‐arabinofuranosylcytosine (ara‐C). To investigate the mechanisms involved, we examined the activities of endogenous endonucleases in nuclei and cytoplasm. Both fractions of control cells contained Ca²⁺ ‐dependent endonuclease which was capable of mediating internucleosomal DNA fragmentation. The assay system using two kinds of target substrates, i.e., nuclear chromatin of CCRF‐CEM cells and naked DNA purified from the same cells, revealed that the activity of Ca²⁺‐dependent endonuclease was enhanced in the crude nuclear extracts of cells treated with 1.0 μg/ml of ara‐C for 24 h or 48 h. The activity was extracted more easily from ara‐C‐treated cells than control cells without sonication of the nuclear fraction. On the other hand, in the cytoplasmic fraction of the cells, the activity towards naked DNA was unchanged, whereas that towards nuclear chromatin was clearly enhanced. These results suggest that internucleosomal DNA fragmentation induced by ara‐C treatment is associated with enhancement and activation of constitutively expressed Ca²⁺ ‐dependent endonuclease in L1210 cells.

Keywords: Apoptosis, 1‐β‐D‐Arabinofuranosylcytosine, DNA fragmentation, Ca²⁺‐endonuclease

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REFERENCES

1. ) Schrecker , A. W. and Urshel , M. J.Metabolism of 1‐β‐D‐arabinofuranosylcytosine in leukemia L1210: studies with intact cells . Cancer Res. , 28 , 793 – 801 ( 1968. ). [PubMed] [Google Scholar]
2. ) Richel , D. J. , Colly , L. P. , Arentsen‐Honders , M. W. , Starrenburg , C. W. J. and Willemze , R.Deoxycytidine kinase, thymidine kinase and cytidine diaminase and the formation of ara‐CTP in leukemic cells in different phases of the cell cycle . Leuk. Res. , 14 , 363 – 369 ( 1990. ). [DOI] [PubMed] [Google Scholar]
3. ) Major , P. P. , Egan , E. M. , Beardsley , G. P. , Minden , M. D. and Kufe , D. W.Lethality of human myeloblasts correlates with the incorporation of arabinofuranosylcytosine into DNA . Proc. Natl. Acad. Sci. USA , 78 , 3235 – 3239 ( 1981. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
4. ) Takauji , R. , Tohyama , K. , Ueda , T. and Nakamura , T.Enhancement of cytosine arabinoside cytotoxicity by granulocyte/macrophage colony‐stimulating factor and granulocyte colony‐stimulating factor in a human myeloblastic leukemia cell line . Jpn. J. Cancer Res. , 84 , 445 – 450 ( 1993. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
5. ) Kufe , D. W. , Munroe , D. , Herrick , D. , Egan , E. and Spriggs , D.Effects of 1‐β‐D‐arabinofuranosylcytosine incorporation on eukaryotic DNA template function . Mol. Pharmacol. , 26 , 128 – 134 ( 1984. ). [PubMed] [Google Scholar]
6. ) Major , P. P. , Egan , E. M. , Herrick , D. J. and Kufe , D. W.Effect of ara‐C incorporation on deoxyribonucleic acid synthesis in cells . Biochem. Pharmacol. , 31 , 2937 – 2940 ( 1982. ). [DOI] [PubMed] [Google Scholar]
7. ) Ohno , Y. , Spriggs , D. , Matsukage , A. , Ohno , T. and Kufe , D.Effects of l‐β‐D‐arabinofuranosylcytosine incorporation on elongation of specific DNA sequences by DNA polymerase β . Cancer Res. , 48 , 1494 – 1498 ( 1988. ). [PubMed] [Google Scholar]
8. ) Kaufmann , S. H.Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, campothecin, and other cytotoxic anticancer drugs: a cautionary note . Cancer Res. , 49 , 5870 – 5878 ( 1989. ). [PubMed] [Google Scholar]
9. ) Sen , S. and D'Incalci , M.Apoptosis: biochemical events and relevance to cancer chemotherapy . FEBS Lett. , 307 , 122 – 127 ( 1992. ). [DOI] [PubMed] [Google Scholar]
10. ) Yoshida , A. , Ueda , T. , Takauji , R. , Liu , Y.‐P. , Fukushima , T. , Inuzuka , M. and Nakamura , T.Role of calcium ion in induction of apoptosis by etoposide in human leukemia HL‐60 cells . Biochem. Biophys. Res. Commun. , 196 , 927 – 934 ( 1993. ). [DOI] [PubMed] [Google Scholar]
11. ) Gunji , H. , Kharbanda , S. and Kufe , D.Induction of internucleosomal DNA fragmentation in human myeloid leukemia cells by l‐β‐D‐arabinofuranosylcytosine . Cancer Res. , 51 , 741 – 743 ( 1991. ). [PubMed] [Google Scholar]
12. ) Bahlla , K. , Tang , C. , Ibrado , A. M. , Grant , S. , Tourkina , E. , Holladay , C. , Hughes , M. , Mahoney , M. E. and Huang , Y.Granulocyte‐macrophage colony‐stimulating factor/interleukin‐3 fusion protein (pIXY321) enhances high‐dose ara‐C‐induced programmed cell death or apoptosis in human myeloid leukemia cells . Blood , 80 , 2883 – 2890 ( 1992. ). [PubMed] [Google Scholar]
13. ) Miyashita , T. and Reed , J. C.Bcl‐2 oncoprotein blocks chemotherapy‐induced apoptosis in a human leukemia cell line . Blood , 81 , 151 – 157 ( 1993. ). [PubMed] [Google Scholar]
14. ) Wyllie , A. H.Glucocorticoid‐induced thymocyte apoptosis is associated with endogenous endonuclease activation . Nature , 284 , 555 – 556 ( 1980. ). [DOI] [PubMed] [Google Scholar]
15. ) Arends , M. J. , Morris , R. G. and Wyllie , A. H.Apoptosis: the role of the endonuclease . Am. J. Pathol. , 136 , 593 – 608 ( 1990. ). [PMC free article] [PubMed] [Google Scholar]
16. ) Kyprianou , N. , English , H. U. and Issacs , J. T.Activation of a Ca²⁺−Mg²⁺ ‐dependent endonuclease as an early event in castration‐induced prostatic cell death . Prostate , 13 , 103 – 117 ( 1988. ). [DOI] [PubMed] [Google Scholar]
17. ) Peitsch , M. C. , Polzar , B. , Stephan , H. , Crompton , T. , MacDonald , H. R. , Mannherz , H. G. and Tschopp , J.Characterization of the endogenous deoxyribonuclease involved in nuclear DNA degradation during apoptosis (programmed cell death) . EMBO J. , 12 , 371 – 377 ( 1993. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
18. ) Barry , M. A. and Eastman , A.Identification of deoxyribonuclease II as an endonuclease involved in apoptosis . Arch. Biochem. Biophys. , 300 , 440 – 450 ( 1993. ). [DOI] [PubMed] [Google Scholar]
19. ) Alnemri , E. S. and Litwack , G.Activation of internucleosomal DNA cleavage in human CEM lymphocytes by glucocorticoid and novobiocin . J. Biol. Chem. , 265 , 17323 – 17333 ( 1990. ). [PubMed] [Google Scholar]
20. ) Cohen , J. J. and Duke , R. C.Glucocorticoid activation of a calcium‐dependent endonuclease in thymocyte nuclei leads to cell death . J. Immunol. , 132 , 38 – 42 ( 1984. ). [PubMed] [Google Scholar]
21. ) McConkey , D. J. , Hartzell , P. , Nicotera , P. and Orrenius , S.Calcium‐activated DNA fragmentation kills immature thymocytes . FASEB J. , 3 , 1843 – 1849 ( 1989. ). [DOI] [PubMed] [Google Scholar]
22. ) Gaido , M. L. and Cidlowski , J. A.Identification, purification, and characterization of a calcium‐dependent endonuclease (NUC18) from apoptotic rat thymocytes . J. Biol. Chem. , 266 , 18580 – 18585 ( 1991. ). [PubMed] [Google Scholar]
23. ) Caron‐Leslie , L.‐A. M. , Schwartzman , R. A. , Gaido , M. L. , Compton , M. M. and Cidlowski , J. A.Identification and characterization of glucocorticoid‐regulated nuclease(s) in lymphoid cells undergoing apoptosis . J. Steroid Biochem. Mol. Biol. , 40 , 661 – 671 ( 1991. ). [DOI] [PubMed] [Google Scholar]
24. ) Nikonova , L. V. , Beletsky , I. P. and Umansky , S. R.Properties of some nuclear nucleases of rat thymocytes and their changes in radiation‐induced apoptosis . Eur. J. Biochem. , 215 , 893 – 901 ( 1993. ). [DOI] [PubMed] [Google Scholar]
25. ) Tanuma , S. and Shiokawa , D.Multiple forms of nuclear deoxyribonuclease in rat thymocytes . Biochem. Biophys. Res. Commun. , 203 , 789 – 797 ( 1994. ). [DOI] [PubMed] [Google Scholar]
26. ) Takano , Y. S. , Harmon , B. V. and Kerr , J. F. R.Apoptosis induced by mild hyperthermia in human and murine tumour cell lines: a study using electron microscopy and DNA gel electrophoresis . J. Pathol. , 163 , 329 – 336 ( 1991. ). [DOI] [PubMed] [Google Scholar]
27. ) Bertrand , R. , Solary , E. , O'Connor , P. , Kohn , K. W. and Pommier , Y.Induction of a common pathway of apoptosis by staurosporine . Exp. Cell Res. , 211 , 314 – 321 ( 1994. ). [DOI] [PubMed] [Google Scholar]
28. ) Lowry , O. H. , Rosebrough , N. J. , Farr , A. L. and Randall , R. J.Protein measurement with the Folin phenol reagent . J. Biol. Chem. , 193 , 265 ( 1951. ). [PubMed] [Google Scholar]
29. ) Ribeiro , J. M. and Carson , D. A.Ca²⁺/Mg²⁺‐dependent endonuclease from human spleen: purification, properties, and role in apoptosis . Biochemistry , 32 , 9129 – 9136 ( 1993. ). [DOI] [PubMed] [Google Scholar]
30. ) Nakamura , T.Action mechanism of antileukemic agents with special reference to nucleic acid metabolism of leukemic cells . Acta Haematol Jpn. , 45 , 1203 – 1218 ( 1982. ). [PubMed] [Google Scholar]
31. ) Kharbanda , S. , Gunji , H. and Kufe , D.Activation of the c‐jun protooncogene in human myeloid leukemia cells treated with etoposide . Am. Soc. Pharmacol. Exp. Ther. , 39 , 697 – 701 ( 1991. ). [PubMed] [Google Scholar]
32. ) Kharbanda , S. , Rubin , E. , Gunji , H. , Hinz , H. , Giovanella , B. , Pantazis , P. and Kufe , D.Camptothecin and its derivatives induce expression of the c‐jun protooncogene in human myeloid leukemia cells . Cancer Res. , 51 , 6636 – 6642 ( 1991. ). [PubMed] [Google Scholar]
33. ) Lowe , S. W. , Ruley , H. E. , Jacks , T. and Housman , D. E.p53‐dependent apoptosis modulates the cytotoxicity of anticancer agents . Cell , 74 , 957 – 967 ( 1993. ). [DOI] [PubMed] [Google Scholar]
34. ) Kubota , M.Generation of DNA damage by antineoplastic agents . Anti-Cancer Drugs , 2 , 531 – 541 ( 1991. ). [DOI] [PubMed] [Google Scholar]
35. ) Ucker , D. S. , Obermiller , P. S. , Eckhart , W. , Apgar , J. R. , Berger , N. A. and Meyers , J.Genome digestion is a dispensable consequence of physiological cell death mediated by cytotoxic T lymphocytes . Mol. Cell. Biol. , 12 , 3060 – 3069 ( 1992. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
36. ) 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 , 3679 – 3684 ( 1993. ). [DOI] [PMC free article] [PubMed] [Google Scholar]
37. ) Oberhammer , F. , Bursch , W. , Tiefenbacher , R. , Fröschl , G. , Pavelka , M. , Purchio , T. and Schulte‐Hermann , R.Apoptosis is induced by transforming growth factor‐β1 within 5 hours in regressing liver without significant fragmentation of the DNA . Hepatology , 18 , 1238 – 1246 ( 1993. ). [PubMed] [Google Scholar]
38. ) Nakamura , M. , Sakaki , Y. , Watanabe , N. and Takagi , Y.Purification and characterization of the Ca²⁺ plus Mg²⁺‐ dependent endodeoxyribonuclease from calf thymus chromatin . J. Biochem. , 89 , 143 – 152 ( 1981. ). [DOI] [PubMed] [Google Scholar]
39. ) Hashida , T. , Tanaka , Y. , Matsunami , N. , Yoshihara , K. , Kamiya , T. , Tanigawa , Y. and Koide , S. S.Purification and properties of bull seminal plasma Ca²⁺, Mg²⁺‐dependent endonuclease . J. Biol. Chem. , 257 , 13114 – 13119 ( 1982. ). [PubMed] [Google Scholar]
40. ) Okamoto‐Kubo , S. , Nishio , K. , Heike , Y. , Yoshida , M. , Ohmori , T. and Saijo , N.Apoptosis induced by etoposide in small‐cell lung cancer cell lines . Cancer Chemother. Pharmacol. , 33 , 385 – 390 ( 1994. ). [DOI] [PubMed] [Google Scholar]
41. ) Bruno , S. , Bino , G. D. , 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 , 1113 – 1120 ( 1992. ). [PubMed] [Google Scholar]
42. ) Walker , P. R. , Weaver , V. M. , Lach , B. , LeBlanc , J. and Sikorska , M.Endonuclease activities associated with high molecular weight and internucleosomal DNA fragmentation in apoptosis . Exp. Cell Res. , 213 , 100 – 106 ( 1994. ). [DOI] [PubMed] [Google Scholar]

[b1] 1. ) Schrecker , A. W. and Urshel , M. J.Metabolism of 1‐β‐D‐arabinofuranosylcytosine in leukemia L1210: studies with intact cells . Cancer Res. , 28 , 793 – 801 ( 1968. ). [PubMed] [Google Scholar]

[b2] 2. ) Richel , D. J. , Colly , L. P. , Arentsen‐Honders , M. W. , Starrenburg , C. W. J. and Willemze , R.Deoxycytidine kinase, thymidine kinase and cytidine diaminase and the formation of ara‐CTP in leukemic cells in different phases of the cell cycle . Leuk. Res. , 14 , 363 – 369 ( 1990. ). [DOI] [PubMed] [Google Scholar]

[b3] 3. ) Major , P. P. , Egan , E. M. , Beardsley , G. P. , Minden , M. D. and Kufe , D. W.Lethality of human myeloblasts correlates with the incorporation of arabinofuranosylcytosine into DNA . Proc. Natl. Acad. Sci. USA , 78 , 3235 – 3239 ( 1981. ). [DOI] [PMC free article] [PubMed] [Google Scholar]

[b4] 4. ) Takauji , R. , Tohyama , K. , Ueda , T. and Nakamura , T.Enhancement of cytosine arabinoside cytotoxicity by granulocyte/macrophage colony‐stimulating factor and granulocyte colony‐stimulating factor in a human myeloblastic leukemia cell line . Jpn. J. Cancer Res. , 84 , 445 – 450 ( 1993. ). [DOI] [PMC free article] [PubMed] [Google Scholar]

[b5] 5. ) Kufe , D. W. , Munroe , D. , Herrick , D. , Egan , E. and Spriggs , D.Effects of 1‐β‐D‐arabinofuranosylcytosine incorporation on eukaryotic DNA template function . Mol. Pharmacol. , 26 , 128 – 134 ( 1984. ). [PubMed] [Google Scholar]

[b6] 6. ) Major , P. P. , Egan , E. M. , Herrick , D. J. and Kufe , D. W.Effect of ara‐C incorporation on deoxyribonucleic acid synthesis in cells . Biochem. Pharmacol. , 31 , 2937 – 2940 ( 1982. ). [DOI] [PubMed] [Google Scholar]

[b7] 7. ) Ohno , Y. , Spriggs , D. , Matsukage , A. , Ohno , T. and Kufe , D.Effects of l‐β‐D‐arabinofuranosylcytosine incorporation on elongation of specific DNA sequences by DNA polymerase β . Cancer Res. , 48 , 1494 – 1498 ( 1988. ). [PubMed] [Google Scholar]

[b8] 8. ) Kaufmann , S. H.Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, campothecin, and other cytotoxic anticancer drugs: a cautionary note . Cancer Res. , 49 , 5870 – 5878 ( 1989. ). [PubMed] [Google Scholar]

[b9] 9. ) Sen , S. and D'Incalci , M.Apoptosis: biochemical events and relevance to cancer chemotherapy . FEBS Lett. , 307 , 122 – 127 ( 1992. ). [DOI] [PubMed] [Google Scholar]

[b10] 10. ) Yoshida , A. , Ueda , T. , Takauji , R. , Liu , Y.‐P. , Fukushima , T. , Inuzuka , M. and Nakamura , T.Role of calcium ion in induction of apoptosis by etoposide in human leukemia HL‐60 cells . Biochem. Biophys. Res. Commun. , 196 , 927 – 934 ( 1993. ). [DOI] [PubMed] [Google Scholar]

[b11] 11. ) Gunji , H. , Kharbanda , S. and Kufe , D.Induction of internucleosomal DNA fragmentation in human myeloid leukemia cells by l‐β‐D‐arabinofuranosylcytosine . Cancer Res. , 51 , 741 – 743 ( 1991. ). [PubMed] [Google Scholar]

[b12] 12. ) Bahlla , K. , Tang , C. , Ibrado , A. M. , Grant , S. , Tourkina , E. , Holladay , C. , Hughes , M. , Mahoney , M. E. and Huang , Y.Granulocyte‐macrophage colony‐stimulating factor/interleukin‐3 fusion protein (pIXY321) enhances high‐dose ara‐C‐induced programmed cell death or apoptosis in human myeloid leukemia cells . Blood , 80 , 2883 – 2890 ( 1992. ). [PubMed] [Google Scholar]

[b13] 13. ) Miyashita , T. and Reed , J. C.Bcl‐2 oncoprotein blocks chemotherapy‐induced apoptosis in a human leukemia cell line . Blood , 81 , 151 – 157 ( 1993. ). [PubMed] [Google Scholar]

[b14] 14. ) Wyllie , A. H.Glucocorticoid‐induced thymocyte apoptosis is associated with endogenous endonuclease activation . Nature , 284 , 555 – 556 ( 1980. ). [DOI] [PubMed] [Google Scholar]

[b15] 15. ) Arends , M. J. , Morris , R. G. and Wyllie , A. H.Apoptosis: the role of the endonuclease . Am. J. Pathol. , 136 , 593 – 608 ( 1990. ). [PMC free article] [PubMed] [Google Scholar]

[b16] 16. ) Kyprianou , N. , English , H. U. and Issacs , J. T.Activation of a Ca²⁺−Mg²⁺ ‐dependent endonuclease as an early event in castration‐induced prostatic cell death . Prostate , 13 , 103 – 117 ( 1988. ). [DOI] [PubMed] [Google Scholar]

[b17] 17. ) Peitsch , M. C. , Polzar , B. , Stephan , H. , Crompton , T. , MacDonald , H. R. , Mannherz , H. G. and Tschopp , J.Characterization of the endogenous deoxyribonuclease involved in nuclear DNA degradation during apoptosis (programmed cell death) . EMBO J. , 12 , 371 – 377 ( 1993. ). [DOI] [PMC free article] [PubMed] [Google Scholar]

[b18] 18. ) Barry , M. A. and Eastman , A.Identification of deoxyribonuclease II as an endonuclease involved in apoptosis . Arch. Biochem. Biophys. , 300 , 440 – 450 ( 1993. ). [DOI] [PubMed] [Google Scholar]

[b19] 19. ) Alnemri , E. S. and Litwack , G.Activation of internucleosomal DNA cleavage in human CEM lymphocytes by glucocorticoid and novobiocin . J. Biol. Chem. , 265 , 17323 – 17333 ( 1990. ). [PubMed] [Google Scholar]

[b20] 20. ) Cohen , J. J. and Duke , R. C.Glucocorticoid activation of a calcium‐dependent endonuclease in thymocyte nuclei leads to cell death . J. Immunol. , 132 , 38 – 42 ( 1984. ). [PubMed] [Google Scholar]

[b21] 21. ) McConkey , D. J. , Hartzell , P. , Nicotera , P. and Orrenius , S.Calcium‐activated DNA fragmentation kills immature thymocytes . FASEB J. , 3 , 1843 – 1849 ( 1989. ). [DOI] [PubMed] [Google Scholar]

[b22] 22. ) Gaido , M. L. and Cidlowski , J. A.Identification, purification, and characterization of a calcium‐dependent endonuclease (NUC18) from apoptotic rat thymocytes . J. Biol. Chem. , 266 , 18580 – 18585 ( 1991. ). [PubMed] [Google Scholar]

[b23] 23. ) Caron‐Leslie , L.‐A. M. , Schwartzman , R. A. , Gaido , M. L. , Compton , M. M. and Cidlowski , J. A.Identification and characterization of glucocorticoid‐regulated nuclease(s) in lymphoid cells undergoing apoptosis . J. Steroid Biochem. Mol. Biol. , 40 , 661 – 671 ( 1991. ). [DOI] [PubMed] [Google Scholar]

[b24] 24. ) Nikonova , L. V. , Beletsky , I. P. and Umansky , S. R.Properties of some nuclear nucleases of rat thymocytes and their changes in radiation‐induced apoptosis . Eur. J. Biochem. , 215 , 893 – 901 ( 1993. ). [DOI] [PubMed] [Google Scholar]

[b25] 25. ) Tanuma , S. and Shiokawa , D.Multiple forms of nuclear deoxyribonuclease in rat thymocytes . Biochem. Biophys. Res. Commun. , 203 , 789 – 797 ( 1994. ). [DOI] [PubMed] [Google Scholar]

[b26] 26. ) Takano , Y. S. , Harmon , B. V. and Kerr , J. F. R.Apoptosis induced by mild hyperthermia in human and murine tumour cell lines: a study using electron microscopy and DNA gel electrophoresis . J. Pathol. , 163 , 329 – 336 ( 1991. ). [DOI] [PubMed] [Google Scholar]

[b27] 27. ) Bertrand , R. , Solary , E. , O'Connor , P. , Kohn , K. W. and Pommier , Y.Induction of a common pathway of apoptosis by staurosporine . Exp. Cell Res. , 211 , 314 – 321 ( 1994. ). [DOI] [PubMed] [Google Scholar]

[b28] 28. ) Lowry , O. H. , Rosebrough , N. J. , Farr , A. L. and Randall , R. J.Protein measurement with the Folin phenol reagent . J. Biol. Chem. , 193 , 265 ( 1951. ). [PubMed] [Google Scholar]

[b29] 29. ) Ribeiro , J. M. and Carson , D. A.Ca²⁺/Mg²⁺‐dependent endonuclease from human spleen: purification, properties, and role in apoptosis . Biochemistry , 32 , 9129 – 9136 ( 1993. ). [DOI] [PubMed] [Google Scholar]

[b30] 30. ) Nakamura , T.Action mechanism of antileukemic agents with special reference to nucleic acid metabolism of leukemic cells . Acta Haematol Jpn. , 45 , 1203 – 1218 ( 1982. ). [PubMed] [Google Scholar]

[b31] 31. ) Kharbanda , S. , Gunji , H. and Kufe , D.Activation of the c‐jun protooncogene in human myeloid leukemia cells treated with etoposide . Am. Soc. Pharmacol. Exp. Ther. , 39 , 697 – 701 ( 1991. ). [PubMed] [Google Scholar]

[b32] 32. ) Kharbanda , S. , Rubin , E. , Gunji , H. , Hinz , H. , Giovanella , B. , Pantazis , P. and Kufe , D.Camptothecin and its derivatives induce expression of the c‐jun protooncogene in human myeloid leukemia cells . Cancer Res. , 51 , 6636 – 6642 ( 1991. ). [PubMed] [Google Scholar]

[b33] 33. ) Lowe , S. W. , Ruley , H. E. , Jacks , T. and Housman , D. E.p53‐dependent apoptosis modulates the cytotoxicity of anticancer agents . Cell , 74 , 957 – 967 ( 1993. ). [DOI] [PubMed] [Google Scholar]

[b34] 34. ) Kubota , M.Generation of DNA damage by antineoplastic agents . Anti-Cancer Drugs , 2 , 531 – 541 ( 1991. ). [DOI] [PubMed] [Google Scholar]

[b35] 35. ) Ucker , D. S. , Obermiller , P. S. , Eckhart , W. , Apgar , J. R. , Berger , N. A. and Meyers , J.Genome digestion is a dispensable consequence of physiological cell death mediated by cytotoxic T lymphocytes . Mol. Cell. Biol. , 12 , 3060 – 3069 ( 1992. ). [DOI] [PMC free article] [PubMed] [Google Scholar]

[b36] 36. ) 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 , 3679 – 3684 ( 1993. ). [DOI] [PMC free article] [PubMed] [Google Scholar]

[b37] 37. ) Oberhammer , F. , Bursch , W. , Tiefenbacher , R. , Fröschl , G. , Pavelka , M. , Purchio , T. and Schulte‐Hermann , R.Apoptosis is induced by transforming growth factor‐β1 within 5 hours in regressing liver without significant fragmentation of the DNA . Hepatology , 18 , 1238 – 1246 ( 1993. ). [PubMed] [Google Scholar]

[b38] 38. ) Nakamura , M. , Sakaki , Y. , Watanabe , N. and Takagi , Y.Purification and characterization of the Ca²⁺ plus Mg²⁺‐ dependent endodeoxyribonuclease from calf thymus chromatin . J. Biochem. , 89 , 143 – 152 ( 1981. ). [DOI] [PubMed] [Google Scholar]

[b39] 39. ) Hashida , T. , Tanaka , Y. , Matsunami , N. , Yoshihara , K. , Kamiya , T. , Tanigawa , Y. and Koide , S. S.Purification and properties of bull seminal plasma Ca²⁺, Mg²⁺‐dependent endonuclease . J. Biol. Chem. , 257 , 13114 – 13119 ( 1982. ). [PubMed] [Google Scholar]

[b40] 40. ) Okamoto‐Kubo , S. , Nishio , K. , Heike , Y. , Yoshida , M. , Ohmori , T. and Saijo , N.Apoptosis induced by etoposide in small‐cell lung cancer cell lines . Cancer Chemother. Pharmacol. , 33 , 385 – 390 ( 1994. ). [DOI] [PubMed] [Google Scholar]

[b41] 41. ) Bruno , S. , Bino , G. D. , 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 , 1113 – 1120 ( 1992. ). [PubMed] [Google Scholar]

[b42] 42. ) Walker , P. R. , Weaver , V. M. , Lach , B. , LeBlanc , J. and Sikorska , M.Endonuclease activities associated with high molecular weight and internucleosomal DNA fragmentation in apoptosis . Exp. Cell Res. , 213 , 100 – 106 ( 1994. ). [DOI] [PubMed] [Google Scholar]

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Enhancement of Ca²⁺‐dependent Endonuclease Activity in L1210 Cells during Apoptosis Induced by 1‐β‐D‐Arabinofuranosylcytosine: Possible Involvement of Activating Factor(s)

Rumiko Takauji

Akira Yoshida

Hiromichi Iwasaki

Kaoru Tohyama

Takanori Ueda

Toru Nakamura

Abstract

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Enhancement of Ca2+‐dependent Endonuclease Activity in L1210 Cells during Apoptosis Induced by 1‐β‐D‐Arabinofuranosylcytosine: Possible Involvement of Activating Factor(s)

Rumiko Takauji

Akira Yoshida

Hiromichi Iwasaki

Kaoru Tohyama

Takanori Ueda

Toru Nakamura

Abstract

Full Text

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Enhancement of Ca²⁺‐dependent Endonuclease Activity in L1210 Cells during Apoptosis Induced by 1‐β‐D‐Arabinofuranosylcytosine: Possible Involvement of Activating Factor(s)