Leukemia Research
Volume 25, Issue 12 , Pages 1099-1105 , December 2001

p53 and redox state in etoposide-induced acute myeloblastic leukemia cell death

  • Pirjo Koistinen

      Affiliations

    • Department of Internal Medicine, University of Oulu, Kajaanintie 50, FIN-90220 Oulu, Finland
    • Corresponding Author InformationCorresponding author. Tel.: +358-8-3152011; fax: +358-8-3154139
    • ,
  • Timo Siitonen

      Affiliations

    • Department of Internal Medicine, University of Oulu, Kajaanintie 50, FIN-90220 Oulu, Finland
    • ,
  • Pentti Mäntymaa

      Affiliations

    • Department of Clinical Chemistry, Tampere University Hospital, Tampere, Finland
    • ,
  • Eeva-Riitta Savolainen

      Affiliations

    • Department of Clinical Chemistry, University of Oulu, Kajaanintie 50, FIN-90220 Oulu, Finland

Received 11 September 2000 ,Accepted 10 March 2001.

References 

  1. Shimizu T, Kubota M, Tanizawa A, Sano H, Kasai Y, Hashimoto H, et al. Inhibition of both etoposide-induced DNA fragmentation and activation of poly(ADPribose) synthesis by zinc ion. Biochem. Biophys. Res. Commmun. 1990;169:1172–1177
  2. Walker PR, Smith C, Youdale T, Leblanc J, Whitfield JF, Sikorska M. Topoisomerase II-reactive chemotherapeutic drugs induce apoptosis in thymocytes. Cancer Res. 1991;51:1078–1085
  3. Lowe SW, Ruley HE, Jacks T, Housman DE. p53-dependent apoptosis modulates the cytotoxicity of anticancer agents. Cell. 1993;74:957–967
  4. Kastan MB, Onyekwere O, Sidransky D, Vogelstein B, Craig RW. Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 1991;51:6304–6311
  5. Fritsche M, Haessler C, Brandner G. Induction of nuclear accumulation of the tumor-suppressor protein p53 by DNA-damaging agents. Oncogene. 1993;8:307–318
  6. Greenblatt MS, Bennet WP, Hollstein M, Harris CC. Mutations in the p53 tumor suppressor gene: clues to cancer etiology and molecular pathogenesis. Cancer Res. 1994;54:4855–4878
  7. Hollstein M, Rice K, Greenblatt MS, Soussi T, Fuchs R, Sorlie T, et al. Database of p53 gene somatic mutations in human tumors and cell lines. Nucleic Acid Res. 1994;22:3551–3555
  8. Fan S, el-Deiry WS, Bae I, Freeman J, Jondle D, Bhatia K, et al. p53 gene mutations are associated with decreased sensitivity of human lymphoma cells to DNA damaging agents. Cancer Res. 1994;54:5824–5830
  9. Chresta CM, Masters JRW, Hickman JA. Hypersensitivity of human testicular tumors to etoposide induced apoptosis is associated with functional p53 and high bax:bcl-2 ratio. Cancer Res. 1996;56:1834–1841
  10. Skladanowski A, Larsen AK. Expression of wild-type p53 increases etoposide cytotoxicity in M1 myeloid leukemia cells by facilitated G2 to M transition: implications for gene therapy. Cancer Res. 1997;57:818–823
  11. Blagosklonny MV, El-Deiry WS. Acute overexpression of wt p53 facilitates anticancer drug-induced death of cancer and normal cells. In. J. Cancer. 1998;75:933–940
  12. Tishler RB, Calderwood SK, Coleman N, Price BD. Increases in sequence specific DNA binding by p53 following treatment with chemotherapeutic and DNA damaging agents. Cancer Res. 1993;53:2212–2216
  13. Hainaut P. The tumor suppressor protein p53: a receptor to genotoxic stress that controls cell growth and survival. Curr. Op. Oncol. 1995;7:76–82
  14. Steegenga WT, van der Eb AJ, Jochemsen AG. How phosphorylation regulates the activity of p63. J. Mol. Biol. 1996;263:103–113
  15. Lennon SV, Martin SJ, Cotter TG. Dose-dependent induction of apoptosis in human tumour cell lines by widely diverging stimuli. Cell. Prolif. 1991;24:203–214
  16. Hockenberry DM, Oltvai ZN, Yin X-M, Millman CL, Korsmeyer SJ. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 1993;75:241–251
  17. Sheng-Tanner X, Bump EA, Hedley DW. An oxidative stress-mediated death pathway in irridiated human leukemia cells mapped using multilaser flow cytometry. Radiat. Res. 1998;150:636–647
  18. Sandström PA, Buttke TM. Autocrine production of extracellular catalase prevents apoptosis of the human CEM T-cell line in serum-free medium. Proc. Natl. Acad. Sci. USA. 1993;90:4708–4712
  19. Tew KD. Glutathione-associated enzymes in anticancer drug resistance. Cancer Res. 1994;54:4313–4320
  20. O'Dwyer PJ, Hamilton TC, Yao K-S, Tew KD, Ozols RF. Modulation of glutathione and related enzymes in reversal of resistance to anticancer drugs. Drug Resistance. Hematology/Oncology Clinics of North America 1995, vol. 9. p. 383–396.
  21. Wong GHW. Protective roles of cytokines against radiation: induction of mitochondrial MnSOD. Biochim. Biophys. Acta. 1995;1271:205–209
  22. Mehlen P, Kretz-Remy C, Preville X, Arrigo AP. Human hsp27, Drosophila hsp27 and human alphaB-crystallin expression-mediated increase in glutathione is essential for the protective activity of these proteins against TNF-alpha-induced cell death. EMBO J. 1996;15:2695–2706
  23. Look MP, Musch E. Lipid peroxides in the olychemotherapy of cancer patients. Chemotherapy. 1994;40:8–15
  24. Wolfe JT, Ross D, Cohen GM. A role for metals and free radicals in the induction of apoptosis in thymocytes. FEBS Lett. 1994;352:58–62
  25. Stoyanovsky D, Yalowich J, Gantchev T, Kagan V. Tyrosinase-induced phenoxyl radicals of etoposide (VP-16): interaction with reductants in model systems, K562 leukemic cell and nuclear homogenates. Free Radic. Res. Commun. 1993;19:371–386
  26. Kagan VE, Yalowich JC, Day BW, Goldman R, Gantchev TG, Stoyanovsky DA. Ascorbate is the primary reductant of the phenoxyl radical of etoposide in the presence of thiols both in cell homogenates and in model systems. Biochemistry. 1994;33:9651–9660
  27. Lizard G, Gueldry S, Sordet O, Monier S, Athias A, Miguet C, et al. Glutathione is implied in the control of 7-ketocholesterol-induced apoptosis, which is associated with radical oxygen species production. FASEB J. 1998;12:1651–1663
  28. Siitonen T, Alaruikka P, Mäntymaa P, Savolainen E-R, Kavanagh TJ, Krejsa CM, et al. Protection of acute myeloblastic leukemia cells against apoptotic cell death by high glutathione and gamma-glutamylcysteine synthetase levels during etoposide-induced oxidative stress. Ann. Oncol. 1999;10:1361–1367
  29. Mäntymaa P, Siitonen T, Guttorm T, Säily M, Kinnula V, Savolainen E-R, et al. Induction of mitochondrial manganese superoxide dismutase confers resistance to apoptosis in acute myeloblastic leukaemia cells exposed to etoposide. Br. J. Haematol. 2000;108:574–581
  30. Wang C, Curtis JE, Minden MD, McCulloch EA. Expression of a retinoic acid receptor gene in myeloid leukemia cells. Leukemia. 1999;3:264–269
  31. Zheng A, Mäntymaa P, Säily M, Siitonen T, Savolainen E-R, Koistinen P. An association between mitochondrial function and all-trans retinoic acid-induced apoptosis in acute myeloblastic leukemia cells. Br. J. Haematol. 1999;105:215–224
  32. Zheng A, Castren K, Säily M, Savolainen E-R, Koistinen P, Vähäkangas K. p53 status of newly established acute myeloid leukaemia cell lines. Br. J. Cancer. 1999;79:407–415
  33. Zhu Y-M, Bradbury D, Russell N. Expression of different conformations of p53 in the blast cells of acute myeloblastic leukaemia is related to in vitro growth characteristics. Br. J. Cancer. 1993;68:851–855
  34. Tyurina YY, Tyurin VA, Yalowich JC, Quinn PJ, Claycamp HG, Schor NF, et al. Phenoxyl radicals of etoposide (VP-16) can directly oxidize intracellular thiols: protective versus damaging effects of phenolic antioxidants. Toxicol. Appl. Pharmacol. 1995;131:277–288
  35. Ritov VB, Goldman R, Stoyanovsky DA, Menshikova EV, Kagan VE. Antioxidant paradoxes of phenolic compounds: peroxyl redical scavenger and lipid antioxidant, etoposide (VP-16), inhibits sarcoplasmic reticulum Ca(2+)-ATPase via thiol oxidation by its phenoxyl radical. Arch. Biochem. Biophys. 1995;321:140–152
  36. Gorman A, McGowan A, Cotter TG. Role of peroxide and superoxide anion during tumour cell apoptosis. FEBS Lett. 1997;404:27–33
  37. Garcia-Bermejo L, Perez C, Vilaboa NE, Blas E, Aller P. cAMP increasing agents attenuate the generation of apoptosis by etoposide in promonocytic leukemia cells. J. Cell. Sci. 1998;111:637–644
  38. Mans DR, Schuurhuis GJ, Treskes M, Lafleur MV, Retel J, Pinedo HM, et al. Modulation by d,l-buthionine-S,R-sulfoximine of etoposide cytotoxicity on human non-small cell lung, ovarian and breast carcinoma cell lines. Eur. J. Cancer. 1992;28A:1447–1452
  39. Schneider E, Yamazaki H, Sinha BK, Cowan KH. Buthionine sulfoximine-mediated sensitation of etoposide-resistant human breast cancer MCF7 cells overexpressing the multidrug resistance-associated protein involves increased drug accumulation. Br. J. Cancer. 1995;71:738–743
  40. Lu X, Lane DP. Differential induction of transcriptionally active p53 following UV or ionizing irradiation: defects in chromosome instability syndromes?. Cell. 1993;75:765–778
  41. Lutzker S, Levine AJ. A functionally inactive p53 protein in embryonal carcinoma cells is activated by DNA damage or cellular differentiation. Nature Med. 1996;2:804–810
  42. Zhang W, Hu G, Estey E, Hester J, Deisseroth A. Altered conformation of the p53 protein in myeloid leukemia cells and mitogen-stimulated normal blood cells. Oncogene. 1992;7:1645–1647
  43. Milner J. Forms and functions of p53. Semin. Cancer Biol. 1994;5:211–219
  44. Levine AJ. P53, the cellular gatekeeper for growth and division. Cell. 1997;88:323–331
  45. Fenaux P, Preudhomme C, Quiquandron I, Jonveaux P, Lai JL, Vanrumbeke M, et al. Mutations of the p53 gene in acute myeloid leukemia. Br. J. Haematol. 1992;80:178–183
  46. Schottelius A, Brennscheidt U, Ludwig W-D, Mertelsmann RH, Herrmann F, Lubbert M. Mechanisms of p53 alteration in acute leukemias. Leukemia. 1994;8:1673–1681
  47. Zhu Y-M, Bradbury D, Russell N. Wild-type p53 is required for apoptosis induced by growth factor deprivation in factor-dependent leukaemic cells. Br. J. Cancer. 1994;69:468–474
  48. Zheng A, Mäntymaa P, Säily M, Savolainen E-R, Vähäkangas K, Koistinen P. p53 pathway in apoptosis induced by all-trans retinoic acid in acute myeloblastic leukaemia cells. Acta Haematol 2000; in press.
  49. Funk WD, Pak DT, Karas RH, Wright WE, Shay JW. A transcriptionally active DNA-binding site for human p53 protein complexes. Mol. Cell. Biol. 1992;12:2866–2871
  50. Moll OM, Ostermeyer AG, Halady R, Winkfield B, Frazier M, Zambetti G. Cytoplasmic sequestration of wild-type p53 protein impairs the G1 checkpoint after DNA damage. Mol. Cell. Biol. 1996;16:1126–1137
  51. Clarke AR, Purdie CA, Harrsion DJ, Morris RG, Bird CC, Hooper ML, et al. Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature. 1993;362:849–852
  52. Malcomson RD, Oren M, Wyllie AH, Harrsion DJ. p53-independent death and p53-induced protection against apoptosis in fibroblasts treated with chemotherapeutic drugs. Br. J. Cancer. 1995;72:952–957
  53. Macfarlane M, Jones NA, Dive C, Cohen GM. DNA-damaging agents induce both p53-dependent and p53-independent apoptosis in immature thymocytes. Mol. Pharmacol. 1996;50:900–911

PII: S0145-2126(01)00076-5

Leukemia Research
Volume 25, Issue 12 , Pages 1099-1105 , December 2001

Article Tools

* Image Usage & Resolution