The histone deacetylase inhibitor MS-275 promotes differentiation or apoptosis in human leukemia cells through a process regulated by generation of reactive oxygen species and induction of p21CIP1/WAF1

Cancer Research

Volumn 63, Issue 13, 2003, Pages 3637-3645

  Rosato, Roberto R ^a   Almenara, Jorge A ^a   Grant, Steven ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; APICIDIN; CASPASE; CD11B ANTIGEN; CELL CYCLE PROTEIN; CYCLIN D1; CYTOCHROME C; HISTONE DEACETYLASE INHIBITOR; N (2 AMINOPHENYL) 4 (3 PYRIDINYLMETHOXYCARBONYLAMINOMETHYL)BENZAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; PROTEIN MCL 1; PROTEIN P21; PROTEIN P27; REACTIVE OXYGEN METABOLITE; RETINOBLASTOMA PROTEIN; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANTIGEN EXPRESSION; APOPTOSIS; ARTICLE; BLAST CELL; CELL DEATH; CELL STRAIN HL 60; CELL STRAIN K 562; CELL STRAIN U937; CONTROLLED STUDY; CYTOSOL; DOSE RESPONSE; DOWN REGULATION; DRUG ACCUMULATION; DRUG ANTAGONISM; DRUG EFFECT; ENZYME ACTIVATION; GENE CONSTRUCT; HUMAN; HUMAN CELL; LETHALITY; LEUKEMIA CELL; LEUKEMIA CELL LINE; LYMPHOMA CELL; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN INDUCTION; TUMOR DIFFERENTIATION;

APOPTOSIS; BENZAMIDES; CELL CYCLE; CELL DIFFERENTIATION; CELL DIVISION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; HISTONE DEACETYLASES; HL-60 CELLS; HUMANS; INTRACELLULAR MEMBRANES; K562 CELLS; LEUKEMIA; MEMBRANE POTENTIALS; MITOCHONDRIA; PYRIDINES; REACTIVE OXYGEN SPECIES; TUMOR CELLS, CULTURED; U937 CELLS;

EID: 0038079767     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. Vigushin, D. M., and Coombes, R. C. Histone deacetylase inhibitors in cancer treatment. Anticancer Drugs, 13: 1-13, 2002.
2. Marks, P. A., Richon, V. M., Breslow, R., and Rifkind, R. A. Histone deacetylase inhibitors as new cancer drugs. Curr. Opin. Oncol., 13: 477-483, 2001.
3. Rosato, R. R., and Grant, S, Histone deacetylase inhibitors in cancer therapy. Cancer Biol. Ther., 2: 30-37, 2003.
4. Wang, J., Saunthararajah, Y., Redner, R. L., and Liu, J. M. Inhibitors of histone deacetylase relieve ETO-mediated repression and induce differentiation of AML1ETO leukemia cells. Cancer Res., 59: 2766-2769, 1999.
5. Yamamoto, H., Fujimoto, J., Okamoto, E., Furuyama, J., Tamaoki, T., and Hashimoto-Tamaoki, T. Suppression of growth of hepatocellular carcinoma by sodium butyrate in vitro and in vivo. Int. J. Cancer, 76: 897-902, 1998.
6. Ruefli, A. A., Ausserlechner, M. J., Bernhard, D., Sutton, V, R., Tainton, K. M., Kofler, R., Smyth, M. J., and Johnstone, R. W. The histone deacetylase inhibitor and chemotherapeutic agent suberoylanilide hydroxamic acid (SAHA) induces a cell-death pathway characterized by cleavage of Bid and production of reactive oxygen species. Proc. Natl. Acad. Sci. USA, 98: 10833-10838, 2001.
7. Rosato, R. R., Wang, Z., Gopalkrishnan, R. V., Fisher, P. B., and Grant, S. Evidence of a functional role for the cyclin-dependent kinase-inhibitor p21WAF1/CIP1/MDA6 in promoting differentiation and preventing mitochondrial dysfunction and apoptosis induced by sodium butyrate in human myelomonocytic leukemia cells (U937). Int. J. Oncol., 19: 181-191, 2001.
8. Kwon, S. H., Ahn, S. H., Kim, Y. K., Bae, G. U., Yoon, J. W., Hong, S., Lee, H. Y., Lee, Y. W., Lee, H. W., and Han, J. W. Apicidin, a histone deacetylase inhibitor, induces apoptosis and Fas/Fas ligand expression in human acute promyelocytic leukemia cells. J. Biol. Chem., 277: 2073-2080, 2002.
9. Han, J. W., Ahn, S. H., Park, S. H., Wang, S. Y., Bae, G. U., Seo, D. W., Kwon, H. K., Hong, S., Lee, H. Y., Lee, Y. W., and Lee, H. W. Apicidin, a histone deacetylase inhibitor, inhibits proliferation of tumor cells via induction of p21WAFI/Cipl and gelsolin. Cancer Res., 60: 6068-6074, 2000.
10. Herold, C., Ganslmayer, M., Ocker, M., Hermann, M., Geerts, A., Hahn, E. G., and Schuppan, D. The histone-deacetylase inhibitor trichostatin A blocks proliferation and triggers apoptotic programs in hepatoma cells. J. Hepatol., 36: 233-240, 2002.
11. Selvakumaran, M., Reed, J. C., Liebermann, D., and Hoffman, B. Progression of the myeloid differentiation program is dominant to transforming growth factor-β1-induced apoptosis in M1 myeloid leukemic cells. Blood, 84: 1036-1042, 1994.
12. Van Lint, C., Emiliani, S., and Verdin, E. The expression of a small fraction of cellular genes is changed in response to histone hyperacetylation. Gene Expr., 5: 245-253, 1996.
13. Kim, Y. B., Lee, K. H., Sugita, K., Yoshida, M., and Horinouchi, S. Oxamflatin is a novel antitumor compound that inhibits mammalian histone deacetylase. Oncogene, 18: 2461-2470, 1999.
14. WAF1 is required for butyrate-mediated growth inhibition of human colon cancer cells. Proc. Natl. Acad. Sci. USA. 95: 6791-6796, 1998.
15. WAF1 expression and gene-associated histone acetylation. Proc. Natl. Acad. Sci. USA, 97: 10014-10019, 2000.
16. CIP1, but independent of p53. Oncogene, 18: 7016-7025, 1999.
17. Amin, H. M., Saeed, S., and Alkan, S. Histone deacetylase inhibitors induce caspasedependent apoptosis and downregulation of daxx in acute promyelocytic leukaemia with t(15;17). Br. J. Haematol., 115: 287-297, 2001.
18. Gottlicher, M., Minucci, S., Zhu, P., Kramer, O. H., Schimpf, A., Giavara, S., Sleeman, J. P., Lo, C. F., Nervi, C., Pelicci, P. G., and Heinzel, T. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J., 20: 6969-6978, 2001.
19. Almenara, J., Rosato, R., and Grant, S. Synergistic induction of mitochondrial damage and apoptosis in human leukemia cells by flavopiridot and the histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA). Leukemia (Baltimore), 16: 1331-1343, 2002.
20. Suzuki, T., Ando, T., Tsuchiya, K., Fukazawa, N., Saito, A., Mariko, Y., Yamashita, T., and Nakanishi, O. Synthesis and histone deacetylase inhibitory activity of new benzamide derivatives. J. Med. Chem., 42: 3001-3003, 1999.
21. Saito, A., Yamashita, T., Mariko, Y., Nosaka, Y., Tsuchiya, K., Ando, T., Suzuki, T., Tsumo, T., and Nakanishi, O. A synthetic inhibitor of histone deacetylase. MS-27275, with marked in vivo antitumor activity against human tumors. Proc. Natl. Acad. Sci. USA, 96: 4592-4597, 1999.
22. Lee, B. I., Park, S. H., Kim, J. W., Sausville, E. A., Kim, H. T., Nakanishi, O., Trepel, J. B., and Kim, S. J. MS-275, a histone deacetylase inhibitor, selectively induces transforming growth factor β type II receptor expression in human breast cancer cells. Cancer Res., 61: 931-934, 2001.
23. Jaboin, J., Wild, J., Hamidi, H., Khanna, C., Kim, C. J., Robey, R., Bates, S. E., and Thiele, C. J. MS-27-275, an inhibitor of histone deacetylase, has marked in vitro and in vivo antitumor activity against pediatric solid tumors. Cancer Res., 62: 6108-6115, 2002.
24. Wang, S., Vrana, J. A., Bartimole, T. M., Freemerman, A. J., Jarvis, W. D., Kramer, L. B., Krystal, G., Dent, P., and Grant, S. Agents that down-regulate or inhibit protein kinase C circumvent resistance to 1-β-D-arabinofuranosylcytosine-induced apoptosis in human leukemia cells that overexpress Bcl-2. Mol. Pharmacol, 52: 1000-1009, 1997.
25. Wang, S., Wang, Z., Boise, L. H., Dent, P., and Grant, S. Bryostatin I enhances paclitaxel-induced mitochondrial dysfunction and apoptosis in human leukemia cells (U937) ectopically expressing Bcl-xL. Leukemia (Baltimore), 13: 1564-1573, 1999.
26. Rahmani, M., Dai, Y., and Grant, S. The histone deacetylase inhibitor sodium butyrate interacts synergistically with phorbol myristate acetate (PMA) to induce mitochondrial damage and apoptosis in human myeloid leukemia cells through a tumor necrosis factor-α-mediated process. Exp. Cell Res., 277: 31-47, 2002.
27. Jarvis, W. D., Fornari, F. A., Traylor, R. S., Martin, H. A., Kramer, L. B., Erukulla, R. K., Bittman, R., and Grant, S. Induction of apoptosis and potentiation of ceramide-mediated cytotoxicity by sphingoid bases in human myeloid leukemia cells. J. Biol. Chem., 271: 8275-8284, 1996.
28. Tang, L., Boise, L. H., Dent, P., and Grant, S. Potentiation of 1-β-D-arabinofuranosylcytosine-mediated mitochondrial damage and apoptosis in human leukemia cells (U937) overexpressing bcl-2 by the kinase inhibitor 7-hydroxystaurosporine (UCN01). Biochem. Pharmacol., 60: 1445-1456, 2000.
29. Wang, Z., Van Tuyle, G., Conrad, D., Fisher, P. B., Dent, P., and Grant, S. Dysregulation of the cyclin-dependent kinase inhibitor p21WAF1/CIP1/MDA6 increases the susceptibility of human leukemia cells (U937) to 1-β-D-arabinofuranosylcytosine-mediated mitochondrial dysfunction and apoptosis, Cancer Res., 59: 1259-1267, 1999.
30. Xiang, H., Fox, J. A., Totpal, K., Aikawa, M., Dupree, K., Sinicropi, D., Lowe, J., and Escandon, E. Enhanced tumor killing by Apo2L/TRAIL and CPT-11 co-treatment is associated with p21 cleavage and differential regulation of Apo2L/TRAIL ligand and its receptors. Oncogene, 21: 3611-3619, 2002.
31. 1 arrest and apoptosis in myeloid leukemia cells: structure-function analysis. Leukemia (Baltimore), 13: 1243-1253, 1999.
32. Cip1/Waf1 by caspases is an early event during DNA damage-induced apoptosis. J. Biol. Chem., 273: 19207-19212, 1998.
33. Rosato, R. R., Almenara, J. A., Cartee, L., Betts, V., Chellappan, S. P., and Grant, S. The cyclin-dependent kinase inhibitor flavopiridol disrupts sodium butyrate-induced p21WAF1/CIP1 expression and maturation while reciprocally potentiating apoptosis in human leukemia cells. Mol. Cancer Ther., 1: 253-266, 2002.
34. Sherr, C. J. The Pezcoller Lecture: cancer cell cycles revisited. Cancer Res., 60: 3689-3695, 2000.
35. Glick, R. D., Swendeman, S. L., Coffey, D. C., Rifkind, R. A., Marks, P. A., Richon, V. M., and La Quaglia, M. P. Hybrid polar histone deacetylase inhibitor induces apoptosis and CD95/CD95 ligand expression in human neuroblastoma. Cancer Res., 59: 4392-4399, 1999.
36. Aggarwal, B. B., and Natarajan, K. Tumor necrosis factors: developments during the last decade. Eur. Cytokine Netw., 7: 93-124, 1996.
37. Cartee, L., Smith, R., Dai, Y., Rahmani, M., Rosato, R., Almenara, J., Dent. P., and Grant, S. Synergistic induction of apoptosis in human myeloid leukemia cells by phorbol 12-myristate 13-acetate and flavopiridol proceeds via activation of both the intrinsic and tumor necrosis factor-mediated extrinsic cell death pathways. Mol. Pharmacol., 61: 1313-1321, 2002.
38. Zhou, Q., Snipas, S., Orth, K., Muzio, M., Dixit, V. M., and Salvesen, G. S. Target protease specificity of the viral serpin CrmA. Analysis of five caspases. J. Biol. Chem., 272: 7797-7800, 1997.
39. Adams, J. M., and Cory, S. The Bcl-2 protein family: arbiters of cell survival. Science (Wash. DC), 281: 1322-1326, 1998.
40. Cheng, E. H., Kirsch, D. G., Clem, R. J., Ravi, R., Kastan, M. B., Bedi, A., Ueno, K., and Hardwick, J. M. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science (Wash. DC), 278: 1966-1968, 1997.
41. Kannan, K., and Jain, S. K. Oxidative stress and apoptosis. Pathophysiology, 7: 153-163, 2000.
42. Kroemer, G., Dallaporta, B., and Resche-Rigon, M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu. Rev. Physiol., 60: 619-642, 1998.
43. Mignotte, B., and Vayssiere. J. L. Mitochondria and apoptosis. Eur. J. Biochem., 252: 1-15, 1998.
44. Archer, S. Y., Johnson, J. J., Kim. H. J., and Hodin, R. A. p21 gene regulation during enterocyte differentiation. J. Surg. Res., 98: 4-8, 2001.
45. Lallemand. F., Courilleau, D., Sabbah, M., Redeuilh, G., and Mester, J. Direct inhibition of the expression of cyclin D1 gene by sodium butyrate. Biochem. Biophys. Res. Commun., 229: 163-169, 1996.
46. 1 arrest results from p21-independent disruption of retinoblastoma protein-mediated signals. Cell Growth Differ., 9: 465-474, 1998.
47. 1. Mol. Cell. Biol., 8: 1614-1624, 1988.
48. Zamzami, N., Marchetti, P., Castedo. M., Decaudin, D., Macho, A., Hirsch, T., Susin, S. A., Petit, P. X., Mignotte, B., and Kroemer. G. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med., 182: 367-377, 1995.
49. Zamzami, N., Susin, S. A., Marchetti, P., Hirsch, T., Gomez-Monterrey,. I., Castedo, M., and Kroemer, G. Mitochondrial control of nuclear apoptosis. J. Exp. Med., 183: 1533-1544, 1996.
50. Gross, A., McDonnell, J. M., and Korsmeyer, S. J. BCL-2 family members and the mitochondria in apoptosis. Genes Dev., 13: 1899-1911, 1999.
51. Vander Heiden, M. G., and Thompson, C. B. Bcl-2 proteins: regulators of apoptosis or of mitochondrial homeostasis? Nat. Cell Biol., 1: E209-E216, 1999.
52. Hochman, A., Sternin, H., Gorodin, S., Korsmeyer, S., Ziv, I., Melamed, E., and Often, D. Enhanced oxidative stress and altered antioxidants in brains of Bcl-2-deficient mice. J. Neurochem., 71: 741-748. 1998.
53. Hockenbery, D. M., Oltvai, Z. N., Yin, X. M., Milliman, C. L., and Korsmeyer, S. J. Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell. 75: 241-251, 1993.
54. Tyurina. Y. Y., Tyurin, V. A., Carta, G., Quinn, P. J,. Schor. N. F., and Kagan, V. E. Direct evidence for antioxidant effect of Bcl-2 in PC12 rat pheochromocytoma cells. Arch. Biochem. Biophys., 344: 413-423, 1997.
55. Kirsch, D. G., Doseff. A., Chau, B. N,. Lim, D. S., Souza-Pinto, N. C., Hansford. R., Kastan. M. B., Lazebnik, Y. A., and Hardwick, J. M. Caspase-3-dependent cleavage of Bcl-2 promotes release of cytochrome c. J. Biol. Chem., 274:21155-21161, 1999.
56. Fujita, N,. and Tsuruo, T. Involvement of Bcl-2 cleavage in the acceleration of VP-16-induced U937 cell apoptosis. Biochem. Biophys. Res. Commun., 246: 484-488, 1998.
57. Kitada, S., Zapata, J. M., Andreeff. M., and Reed. J. C. Protein kinase inhibitors flavopiridol and 7-hydroxy-staurosporine down-regulate antiapoptosis proteins in B-cell chronic lymphocytic leukemia. Blood. 96: 393-397, 2000.
58. 1 protects cells from apoptosis induced by UV-irradiation or RNA polymerase II blockage. Oncogene. 16: 3461-3469, 1998.
59. WAF1/CIP1 by histone deacetylase inhibitors reduces their cytotoxicity. Mol. Pharmacol., 60: 828-837, 2001.
60. WAF1 in human U266 myeloma cells blocks the lethal signaling induced by oxidative stress but notby Fas. Biochem. Biophys. Res. Commun., 289: 34-38, 2001.
61. Suzuki, A., Tsutomi, Y., Miura, M., and Akahane, K. Caspase 3 inactivation to suppress Fas-mediated apoptosis: identification of binding domain with p21 and ILP and inactivation machinery by p21. Oncogene, 18: 1239-1244. 1999.
62. Jin, Y. H., Yoo, K. J., Lee, Y. H., and Lee. S. K. Caspase 3-mediated cleavage of p21WAF1/CIP1 associated with the cyclin A-cyclin-dependent kinase 2 complex is a prerequisite for apoptosis in SK-HEP-1 cells. J. Biol. Chem., 275: 30256-30263, 2000.
63. Macip, S., lgarashi, M., Fang, L., Chen, A., Pan, Z. Q., Lee, S. W., and Aaronson, S. A. Inhibition of p21-mediated ROS accumulation can rescue p21-induced senescence. EMBO J., 21: 2180-2188, 2002.