Leukemia Research
Volume 33, Issue 12 , Pages 1684-1695 , December 2009

Prednisolone exerts late mitogenic and biphasic effects on resistant acute lymphoblastic leukemia cells: Relation to early gene expression

  • George I. Lambrou

      Affiliations

    • Hematology/Oncology Unit, First Department of Pediatrics, University of Athens Medical School, “Aghia Sophia” Children's Hospital, Thivon & Levadias, 11527, Goudi, Athens, Greece
    • ,
  • Spiros Vlahopoulos

      Affiliations

    • Hematology/Oncology Unit, First Department of Pediatrics, University of Athens Medical School, “Aghia Sophia” Children's Hospital, Thivon & Levadias, 11527, Goudi, Athens, Greece
    • ,
  • Chrisanthi Papathanasiou

      Affiliations

    • Hematology/Oncology Unit, First Department of Pediatrics, University of Athens Medical School, “Aghia Sophia” Children's Hospital, Thivon & Levadias, 11527, Goudi, Athens, Greece
    • ,
  • Maria Papanikolaou

      Affiliations

    • Hematology/Oncology Unit, First Department of Pediatrics, University of Athens Medical School, “Aghia Sophia” Children's Hospital, Thivon & Levadias, 11527, Goudi, Athens, Greece
    • ,
  • Michael Karpusas

      Affiliations

    • University Research Institute for the Study and Treatment of Childhood Genetic and Malignant Diseases, Greece
    • ,
  • Emmanouil Zoumakis

      Affiliations

    • Choremeio Research Laboratory, First Department of Pediatrics, University of Athens Medical School, “Aghia Sophia” Children's Hospital, Athens, Greece
    • ,
  • Fotini Tzortzatou-Stathopoulou

      Affiliations

    • Hematology/Oncology Unit, First Department of Pediatrics, University of Athens Medical School, “Aghia Sophia” Children's Hospital, Thivon & Levadias, 11527, Goudi, Athens, Greece
    • Corresponding Author InformationCorresponding author. Tel.: +30 210 746 7481; fax: +30 210 779 5538.

Received 23 January 2009 ,Revised 13 March 2009 ,Accepted 11 April 2009.

References 

  1. Tissing WJ, Meijerink JP, den Boer ML, Brinkhof B, van Rossum EF, van Wering ER, et al. Genetic variations in the glucocorticoid receptor gene are not related to glucocorticoid resistance in childhood acute lymphoblastic leukemia. Clin Cancer Res. 2005;11:6050–6056
  2. Den Boer ML, Harms DO, Pieters R, Kazemier KM, Gobel U, Korholz D, et al. Patient stratification based on prednisolone–vincristine–asparaginase resistance profiles in children with acute lymphoblastic leukemia. J Clin Oncol. 2003;21:3262–3268
  3. Russcher H, Smit P, van den Akker EL, van Rossum EF, Brinkmann AO, de Jong FH, et al. Two polymorphisms in the glucocorticoid receptor gene directly affect glucocorticoid-regulated gene expression. J Clin Endocrinol Metabol. 2005;90:5804–5810
  4. Kofler R, Schmidt S, Kofler A, Ausserlechner MJ. Resistance to glucocorticoid-induced apoptosis in lymphoblastic leukemia. J Endocrinol. 2003;178:19–27
  5. Takada Y, Kobayashi Y, Aggarwal BB. Evodiamine abolishes constitutive and inducible NF-kappaB activation by inhibiting IkappaBalpha kinase activation, thereby suppressing NF-kappaB-regulated antiapoptotic and metastatic gene expression, up-regulating apoptosis, and inhibiting invasion. J Biol Chem. 2005;280:17203–17212
  6. Medh RD, Webb MS, Miller AL, Johnson BH, Fofanov Y, Li T, et al. Gene expression profile of human lymphoid CEM cells sensitive and resistant to glucocorticoid-evoked apoptosis. Genomics. 2003;81:543–555
  7. Ausserlechner MJ, Obexer P, Wiegers GJ, Hartmann BL, Geley S, Kofler R. The cell cycle inhibitor p16(INK4A) sensitizes lymphoblastic leukemia cells to apoptosis by physiologic glucocorticoid levels. J Biol Chem. 2001;276:10984–10989
  8. Thompson EB, Johnson BH. Regulation of a distinctive set of genes in glucocorticoid-evoked apoptosis in CEM human lymphoid cells. Recent Prog Horm Res. 2003;58:175–197
  9. Kofler R. The molecular basis of glucocorticoid-induced apoptosis of lymphoblastic leukemia cells. Histochem Cell Biol. 2000;114:1–7
  10. Wissink S, van Heerde EC, Schmitz ML, Kalkhoven E, van der Burg B, Baeuerle PA, et al. Distinct domains of the RelA NF-kappaB subunit are required for negative cross-talk and direct interaction with the glucocorticoid receptor. J Biol Chem. 1997;272:22278–22284
  11. Palmer LA, Harmon JM. Biochemical evidence that glucocorticoid-sensitive cell lines derived from the human leukemic cell line CCRF-CEM express a normal and a mutant glucocorticoid receptor gene. Cancer Res. 1991;51:5224–5231
  12. Powers JH, Hillmann AG, Tang DC, Harmon JM. Cloning and expression of mutant glucocorticoid receptors from glucocorticoid-sensitive and -resistant human leukemic cells. Cancer Res. 1993;53:4059–4065
  13. Norman MR, Thompson EB. Characterization of a glucocorticoid-sensitive human lymphoid cell line. Cancer Res. 1977;37:3785–3791
  14. Schmidt S, Rainer J, Riml S, Ploner C, Jesacher S, Achmuller C, et al. Identification of glucocorticoid-response genes in children with acute lymphoblastic leukemia. Blood. 2006;107:2061–2069
  15. Tudhope SJ, Catley MC, Fenwick PS, Russell RE, Rumsey WL, Newton R, et al. The role of IkappaB kinase 2, but not activation of NF-kappaB, in the release of CXCR3 ligands from IFN-gamma-stimulated human bronchial epithelial cells. J Immunol. 2007;179:6237–6245
  16. Miyazato A, Ueno S, Ohmine K, Ueda M, Yoshida K, Yamashita Y, et al. Identification of myelodysplastic syndrome-specific genes by DNA microarray analysis with purified hematopoietic stem cell fraction. Blood. 2001;98:422–427
  17. Yang YH, Speed T. Design issues for cDNA microarray experiments. Nat Rev. 2002;3:579–588
  18. Tindall EA, Speight G, Petersen DC, Padilla EJ, Hayes VM. Novel Plexor SNP genotyping technology: comparisons with TaqMan and homogenous MassEXTEND MALDI-TOF mass spectrometry. Hum Mut. 2007;28:922–927
  19. Watson JV, Chambers SH, Smith PJ. A pragmatic approach to the analysis of DNA histograms with a definable G1 peak. Cytometry. 1987;8:1–8
  20. Ormerod MG, Payne AW, Watson JV. Improved program for the analysis of DNA histograms. Cytometry. 1987;8:637–641
  21. Wu W, Xing EP, Myers C, Mian IS, Bissell MJ. Evaluation of normalization methods for cDNA microarray data by k-NN classification. BMC Bioinformatics. 2005;6:191
  22. Storey JD, Tibshirani R. Statistical methods for identifying differentially expressed genes in DNA microarrays. Methods Mol Biol. 2003;224:149–157
  23. Reyal F, Stransky N, Bernard-Pierrot I, Vincent-Salomon A, de Rycke Y, Elvin P, et al. Visualizing chromosomes as transcriptome correlation maps: evidence of chromosomal domains containing co-expressed genes—a study of 130 invasive ductal breast carcinomas. Cancer Res. 2005;65:1376–1383
  24. Sturn A, Quackenbush J, Trajanoski Z. Genesis: cluster analysis of microarray data. Bioinformatics. 2002;18:207–208
  25. Quackenbush J. Computational analysis of microarray data. Nat Rev. 2001;2:418–427
  26. Cole SW, Yan W, Galic Z, Arevalo J, Zack JA. Expression-based monitoring of transcription factor activity: the TELiS database. Bioinformatics. 2005;21:803–810
  27. Maximo V, Lima J, Soares P, Silva A, Bento I, Sobrinho-Simoes M. GRIM-19 in health and disease. Adv Anat Pathol. 2008;15:46–53
  28. Pruett SB, Fan R, Zheng Q. Characterization of glucocorticoid receptor translocation, cytoplasmic IkappaB, nuclear NFkappaB, and activation of NFkappaB in T lymphocytes exposed to stress-inducible concentrations of corticosterone in vivo. Int Immunopharmacol. 2003;3:1–16
  29. Sterzer P, Wiegers GJ, Reul JM. Long-term in vivo administration of glucocorticoid hormones attenuates their capacity to accelerate in vitro proliferation of rat splenic T cells. Endocrinology. 2004;145:3630–3638
  30. Zhang Q, Fong CC, Zhang Y, Tzang CH, Fong WF, Yang M. cDNA microarray analysis of the differentially expressed genes involved in murine pre-osteoclast RAW264.7 cells proliferation stimulated by dexamethasone. Life Sci. 2008;82:135–148
  31. Neuberger TJ, Kalimi O, Regelson W, Kalimi M, De Vries GH. Glucocorticoids enhance the potency of Schwann cell mitogens. J Neurosci Res. 1994;38:300–313
  32. Brion N, Pibarot ML, Atienza P, Robin P, Carbon C. Comparative serum pharmacokinetics of prednisone and prednisolone methylsulfobenzoate after oral administration. Presse Med. 1988;17:569–571
  33. Petersen KB, Jusko WJ, Rasmussen M, Schmiegelow K. Population pharmacokinetics of prednisolone in children with acute lymphoblastic leukemia. Cancer Chemother Pharmacol. 2003;51:465–473
  34. Nykanen P, Raivio T, Heinonen K, Janne OA, Voutilainen R. Circulating glucocorticoid bioactivity and serum cortisol concentrations in premature infants: the influence of exogenous glucocorticoids and clinical factors. Eur J Endocrinol. 2007;156:577–583
  35. Laane E, Panaretakis T, Pokrovskaja K, Buentke E, Corcoran M, Soderhall S, et al. Dexamethasone-induced apoptosis in acute lymphoblastic leukemia involves differential regulation of Bcl-2 family members. Haematologica. 2007;92:1460–1469
  36. Medh RD, Saeed MF, Johnson BH, Thompson EB. Resistance of human leukemic CEM-C1 cells is overcome by synergism between glucocorticoid and protein kinase A pathways: correlation with c-Myc suppression. Cancer Res. 1998;58:3684–3693
  37. Morita K, Ishimura K, Tsuruo Y, Wong DL. Dexamethasone enhances serum deprivation-induced necrotic death of rat C6 glioma cells through activation of glucocorticoid receptors. Brain Res. 1999;816:309–316
  38. Lee JM, Yan P, Xiao Q, Chen S, Lee KY, Hsu CY, et al. Methylprednisolone protects oligodendrocytes but not neurons after spinal cord injury. J Neurosci. 2008;28:3141–3149
  39. Fong CC, Zhang Y, Zhang Q, Tzang CH, Fong WF, Wu RS, et al. Dexamethasone protects RAW264.7 macrophages from growth arrest and apoptosis induced by H2O2 through alteration of gene expression patterns and inhibition of nuclear factor-kappa B (NF-kappaB) activity. Toxicology. 2007;236:16–28
  40. Wuerzberger-Davis SM, Chang PY, Berchtold C, Miyamoto S. Enhanced G2-M arrest by nuclear factor-{kappa}B-dependent p21waf1/cip1 induction. Mol Cancer Res. 2005;3:345–353
  41. Tonko M, Ausserlechner MJ, Bernhard D, Helmberg A, Kofler R. Gene expression profiles of proliferating vs. G1/G0 arrested human leukemia cells suggest a mechanism for glucocorticoid-induced apoptosis. FASEB J. 2001;15:693–699
  42. Tissing WJ, den Boer ML, Meijerink JP, Menezes RX, Swagemakers S, van der Spek PJ, et al. Genomewide identification of prednisolone-responsive genes in acute lymphoblastic leukemia cells. Blood. 2007;109:3929–3935
  43. Kolla V, Litwack G. Upregulation of mineralocorticoid- and glucocorticoid-receptor gene expression by Sp-I. Mol Cell Biol Res Commun. 1999;1:44–47
  44. Pirity MK, Wang WL, Wolf LV, Tamm ER, Schreiber-Agus N, Cvekl A. Rybp, a polycomb complex-associated protein, is required for mouse eye development. BMC Dev Biol. 2007;7:39
  45. Lim G, Wang S, Zeng Q, Sung B, Yang L, Mao J. Expression of spinal NMDA receptor and PKCgamma after chronic morphine is regulated by spinal glucocorticoid receptor. J Neurosci. 2005;25:11145–11154
  46. Fahnenstich J, Nandy A, Milde-Langosch K, Schneider-Merck T, Walther N, Gellersen B. Promyelocytic leukaemia zinc finger protein (PLZF) is a glucocorticoid- and progesterone-induced transcription factor in human endometrial stromal cells and myometrial smooth muscle cells. Mol Hum Reprod. 2003;9:611–623
  47. Bailey S, Hall AG, Pearson AD, Redfern CP. The role of AP-1 in glucocorticoid resistance in leukaemia. Leukemia. 2001;15:391–397
  48. Li LB, Leung DY, Strand MJ, Goleva E. ATF2 impairs glucocorticoid receptor-mediated transactivation in human CD8+ T cells. Blood. 2007;110:1570–1577
  49. Geng CD, Schwartz JR, Vedeckis WV. A conserved molecular mechanism is responsible for the auto-upregulation of glucocorticoid receptor gene promoters. Mol Endocrinol. 2008;22:2624–2642
  50. Geng CD, Vedeckis WV. c-Myb and members of the c-Ets family of transcription factors act as molecular switches to mediate opposite steroid regulation of the human glucocorticoid receptor 1A promoter. J Biol Chem. 2005;280:43264–43271
  51. Rulten SL, Ripley TL, Hunt CL, Stephens DN, Mayne LV. Sp1 and NFkappaB pathways are regulated in brain in response to acute and chronic ethanol. Genes Brain Behav. 2006;5:257–273
  52. Nicot C, Mahieux R, Pise-Masison C, Brady J, Gessain A, Yamaoka S, et al. Human T-cell lymphotropic virus type 1 Tax represses c-Myb-dependent transcription through activation of the NF-kappaB pathway and modulation of coactivator usage. Mol Cell Biol. 2001;21:7391–7402
  53. Geisler F, Algul H, Paxian S, Schmid RM. Genetic inactivation of RelA/p65 sensitizes adult mouse hepatocytes to TNF-induced apoptosis in vivo and in vitro. Gastroenterology. 2007;132:2489–2503
  54. de Pablos RM, Villaran RF, Arguelles S, Herrera AJ, Venero JL, Ayala A, et al. Stress increases vulnerability to inflammation in the rat prefrontal cortex. J Neurosci. 2006;26:5709–5719
  55. Castro-Caldas M, Mendes AF, Duarte CB, Lopes MC. Dexamethasone-induced and estradiol-induced CREB activation and annexin 1 expression in CCRF-CEM lymphoblastic cells: evidence for the involvement of cAMP and p38 MAPK. Mediators Inflamm. 2003;12:329–337
  56. Caelles C, Gonzalez-Sancho JM, Munoz A. Nuclear hormone receptor antagonism with AP-1 by inhibition of the JNK pathway. Genes Dev. 1997;11:3351–3364

PII: S0145-2126(09)00188-X

doi: 10.1016/j.leukres.2009.04.018

Leukemia Research
Volume 33, Issue 12 , Pages 1684-1695 , December 2009

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