The cyclin-dependent kinase inhibitor flavopiridol disrupts sodium butyrate-induced p21WAF1/CIP1 expression and maturation while reciprocally potentiating apoptosis in human leukemia cells

Molecular Cancer Therapeutics

Volumn 1, Issue 4, 2002, Pages 253-266

  Rosato, Roberto R ^a   Almenara, Jorge A ^a   Cartee, Leanne ^a   Betts, Vicki ^b   Chellappan, Srikumar P ^b   Grant, Steven ^a  

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

^b Columbia University College of Physicians and Surgeons ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRIC ACID DERIVATIVE; CASPASE; CDKN1A PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; CYCLINE; CYTOCHROME C; ENZYME INHIBITOR; FLAVONOID; FLAVOPIRIDOL; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PIPERIDINE DERIVATIVE;

APOPTOSIS; ARTICLE; BIOSYNTHESIS; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENETICS; HUMAN; LEUKEMIA; METABOLISM; PATHOLOGY; PHYSIOLOGY; WESTERN BLOTTING;

APOPTOSIS; BLOTTING, WESTERN; BUTYRATES; CASPASES; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLIN-DEPENDENT KINASES; CYCLINS; CYTOCHROME C GROUP; ENZYME INHIBITORS; FLAVONOIDS; HUMANS; LEUKEMIA; PIPERIDINES; POLY(ADP-RIBOSE) POLYMERASES; TUMOR CELLS, CULTURED;

EID: 0036463521     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: None     Document Type: Article

References (71)

1. Trock, B., Lanza, E., and Greenwald, P. Dietary fiber, vegetables, and colon cancer: critical review and meta-analyses of the epidemiologic evidence. J. Natl. Cancer Inst., 82: 650-661, 1990. (Pubitemid 20154271)
2. McIntyre, A., Gibson, P. R., and Young, G. P. Butyrate production from dietary fiber and protection against large bowel cancer in a rat model. Gut, 34: 386-391, 1993. (Pubitemid 23080267)
3. 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. (Pubitemid 28262111)
4. 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.
5. Hodin, R. A., Meng, S., Archer, S., and Tang, R. Cellular growth state differentially regulates enterocyte gene expression in butyrate-treated HT-29 cells. Cell Growth Differ., 7: 647-653, 1996. (Pubitemid 26360763)
6. Vaziri, C., Stice, L., and Faller, D. V. Butyrate-induced G1 arrest results from p21-independent disruption of retinoblastoma protein-mediated signals. Cell Growth Differ., 9: 465-474, 1998. (Pubitemid 28345871)
7. Freemerman, A. J., Vrana, J. A., Tombes, R. M., Jiang, H., Chellappan, S. P., Fisher, P. B., and Grant, S. Effects of antisense p21 (WAF1/CIP1/MDA6) expression on the induction of differentiation and drug-mediated apoptosis in human myeloid leukemia cells (HL-60). Leukemia (Baltimore), 11: 504-513, 1997. (Pubitemid 27173937)
8. WAF1/CIP1/MDA6 in the reciprocal regulation of PKC activator-induced apoptosis and differentation in human myelomonocytic leukemia cells. Exp. Cell Res., 244: 105-116, 1998.
9. WAF1/CIP1/MDA6 increases the susceptibility of human leukemia cells (U937) to 1-β-D-arabinofuranosylcytosine-mediated mitochondrial dysfunction and apoptosis. Cancer Res., 15: 1259-1267, 1999.
10. Asada, M., Yamada, T., Fukumuro, K., and Mizutani, S. p21Cip1/WAF1 is important for differentiation and survival of U937 cells. Leukemia (Baltimore), 12: 1944-1950, 1998. (Pubitemid 28554467)
11. Sherr, C. J., and Roberts, J. M. Inhibitors of mammalian G1. Genes Dev., 9: 1149-1163, 1995.
12. El-Deiry, W. S., Tokino, T., Velculescu, V. E., Levy, D. B., Parsons, R., Trent, J. M., Lin, D., Mercer, W. E., Kinzler, K. W., and Vogelstein, B. WAF1, a potential mediator of p53 tumor suppression. Cell, 75: 817-825, 1993. (Pubitemid 23346378)
13. Chen, J., Jackson, P. K., Kirschner, M. W., and Dutta, A. Separate domains of p21 involved in the inhibition of cdk kinase and PCNA. Nature (Lond.), 374: 386-388, 1995.
14. Zhang, W., Grasso, L., McClain, C. D., Gambel, A. M., Cha, Y., Travali, S., Deisseroth, A. B., and Mercer, W. E. p53-independent induction of WAF1/CIP1 in human leukemia cells is correlated with growth arrest accompanying monocyte/macrophage differentiation. Cancer Res., 55: 668-674, 1995.
15. Afshari, C. A., Nichols, M. A., Xiong, Y., and Mudryj, M. A role for a p21-E2F interaction during senescence arrest of normal human fibroblasts. Cell Growth Differ., 7: 979-998, 1996.
16. Harper, J. W. Cyclin dependent kinase inhibitors. Cancer Surv., 29: 91-107, 1997.
17. El-Deiry, W. S., Tokino, T., Waldman, T., Oliner, J. D., Velculescu, V. E., Burrell, M., Hill, D. E., Healy, E., Rees, J. L., and Hamilton, S. R. Topological control of p21WAF1/CIP1 expression in normal and neoplastic tissues. Cancer Res., 55: 2910-2919, 1995.
18. Waldman, T., Kinzler, K. W., and Vogelstein, B. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res., 55: 5187-5190, 1995.
19. Macleod, K. F., Sherry, N., Hannon, G., Beach, D., Tokino, T., Kinzler, K., Vogelstein, B., and Jacks, T. p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev., 9: 935-944, 1995.
20. Jiang, H., Lin, J., Su, Z. Z., Collart, F. R., Huberman, E., and Fisher, P. B. Induction of differentiation in human promyelocytic HL-60 leukemia cells activates p21, WAF1/CIP1, expression in the absence of p53. Oncogene, 9: 3397-3406, 1994. (Pubitemid 24338472)
21. Senderowicz, A. M. Small molecule modulators of cyclin-dependent kinases for cancer therapy. Oncogene, 19: 6600-6606, 2000. (Pubitemid 32197698)
22. Senderowicz, A. M. Flavopiridol: the first cyclin-dependent kinase inhibitor in human clinical trials. Investig. New Drugs, 17: 313-320, 1999. (Pubitemid 30037961)
23. Carlson, B., Lahusen T., Singh, S., Loaiza-Perez, A., Worland, P. J., Pestell, R., Albanese, C., Sausville, E. A., and Senderowicz, A. M. Downregulation of cyclin D1 by transcriptional repression in MCF-7 human breast carcinoma cells induced by flavopiridol. Cancer Res., 59: 4634-4641, 1999. (Pubitemid 29428969)
24. Parker, B. W., Kaur, G., Nieves-Neira, W., Taim, i M., Kohlhagen, G., Shimizu, T., Losiewicz, M. D., Pommier, Y., Sausville, E. A., and Senderowicz, A. M. Early induction of apoptosis in hematopoietic cell lines after exposure to flavopiridol. Blood, 91: 458-465, 1998.
25. Bible, K. C., and Kaufmann, S. H. Cytotoxic synergy between flavopiridol (NSC 649890, L86-8275) and various antineoplastic agents: the importance of sequence of administration. Cancer Res., 57: 3375-3380, 1997. (Pubitemid 27355478)
26. Meikrantz, W., and Schlegel, R. Apoptosis and the cell cycle. J. Cell Biochem., 58: 160-174, 1995.
27. Lee, H. R., Chang, T. H., Tebalt, M. J., III, Senderowicz, A. M., and Szabo E. Induction of differentiation accompanies inhibition of Cdk2 in a non-small cell lung cancer cell line. Int. J. Oncol., 15: 161-166, 1999.
28. Freytag, S. O. Enforced expression of the c-myc oncogene inhibits cell differentiation by precluding entry into a distinct predifferentiation state in G0/G1. Mol. Cell. Biol., 8: 1614-1624, 1988.
29. Cartee, L., Wang, Z., Decker, R. H., Chellappan, S. P., Fusaro, G., Hirsch, K. G., Sankala, H. M., Dent, P., and Grant, S. The cyclin-dependent kinase inhibitor (CDKI) flavopiridol disrupts phorbol 12-myristate13-acetate- induced differentiation and CDKI expression while enhancing apoptosis in human myeloid leukemia cells. Cancer Res., 61: 2583-2591, 2001. (Pubitemid 32685843)
30. Burgess, A. J., Pavey, S., Warrener, R., Hunter, L. J., Piva, T. J., Musgrove, E. A., Saunders, N., Parsons, P. G., and Gabrielli, B. G. Up-Regulation of p21(WAF1/CIP1) by histone deacetylase inhibitors reduces their cytotoxicity. Mol. Pharmacol., 60: 828-837, 2001. (Pubitemid 32900266)
31. Chellappan, S. P., Hiebert, S., Mudryj, M., Horowitz, J. M., and Nevins, J. R. The E2F transcription factor is a cellular target for the RB protein. Cell, 65: 1053-1061, 1991. (Pubitemid 121001693)
32. Marchetti, P., Castedo, M., Susin, S. A., Zamzami, N., Hirsch, T., Macho, A., Haeffner, A., Hirsch, F., Geuskens, M., and Kroemer, G. Mitochondrial permeability transition is a central coordinating event of apoptosis. J. Exp. Med., 184: 1155-1160, 1996. (Pubitemid 26313572)
33. Decker, R. H., Dai, Y., and Grant, S. The cyclin-dependent kinase inhibitor flavopiridol induces apoptosis in human leukemia cells (U937) through the mitochondrial rather than the receptor-mediated pathway. Cell Death Differ., 8: 715-724, 2001. (Pubitemid 32685169)
34. Sedlacek, H. H. Mechanisms of action of flavopiridol. Crit. Rev. Oncol.-Hematol. 38: 139-170, 2001. (Pubitemid 32328317)
35. Shapiro, G. I., Koestner, D. A., Matranga, C. B., and Rollins, B. J. Flavopiridol induces cell cycle arrest and p53-independent apoptosis in non-small cell lung cancer cell lines. Clin. Cancer Res., 5: 2925-2938, 1999. (Pubitemid 29493972)
36. Lallemand, F., Courilleau, D., Buquet-Fagot, C., Atfi, A., Montagne. M. N., and Mester, J. Sodium butyrate induces G2 arrest in the human breast cancer cells MDA-MB-231 and renders them competent for DNA rereplication. Exp. Cell Res., 247: 432-440, 1999. (Pubitemid 29394781)
37. Delgado, M. D., Vaque, J. P., Arozarena, I., Lopez-Ilasaca, M. A., Martinez, C., Crespo, P., and Leon J. H-, K-, and N-Ras inhibit myeloid leukemia cell proliferation by a p21WAF1-dependent mechanism. Oncogene, 19: 783-790, 2000. (Pubitemid 30107709)
38. Kouzarides, T. Histone acetylases and deacetylases in cell proliferation. Curr. Opin. Genet. Dev., 9: 40-48, 1999. (Pubitemid 29080385)
39. Marks, P. A., Richon, V. M., and Rifkind, R. A. Histone deacetylase inhibitors: inducers of differentiation or apoptosis of transformed cells. J. Natl. Cancer Inst., 92: 1210-1216, 2000. (Pubitemid 30627729)
40. Janson, W., Brandner, G., and Siegel, J. Butyrate modulates DNA-damage-induced p53 response by induction of p53-independent differentiation and apoptosis. Oncogene, 15: 1395-1406, 1997. (Pubitemid 27437829)
41. Adams, J, M., and Cory, S. The Bcl-2 protein family: arbiters of cell survival. Science (Wash. DC), 281: 1322-1326, 1998. (Pubitemid 28406819)
42. 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. (Pubitemid 28013242)
43. 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. (Pubitemid 30463354)
44. Carlson, B. A., Dubay, M. M., Sausville, E. A., Brizuela, L., and Worland, P. J. Flavopiridol induces G1 arrest with inhibition of cyclin-dependent kinase (CDK) 2 and CDK4 in human breast carcinoma cells. Cancer Res., 56: 2973-2978, 1996. (Pubitemid 26200251)
45. Johnson, D. G., and Walker, C. L. Cyclins and cell cycle checkpoints. Annu. Rev. Pharmacol. Toxicol., 39: 295-312, 1999. (Pubitemid 29222561)
46. 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. (Pubitemid 27013725)
47. Ito, N., Sawa, H., Nagane, M., Noguchi, A., Hara, M., and Saito, I. Inhibitory effects of sodium butyrate on proliferation and invasiveness of human glioma cells. Neurosurgery (Baltimore), 49: 430-436, 2001.
48. Selvakumaran, M., Reed, J. C., Liebermann, D., and Hoffman, B. Progression of the myeloid differentiation program is dominant to transforming growth factor-β 1-induced apoptosis in M1 myeloid leukemic cells. Blood, 84: 1036-1042, 1994. (Pubitemid 24245866)
49. Adams, J. M., and Cory, S. Life-or-death decisions by the Bcl-2 protein family. Trends Biochem. Sci., 26: 61-66, 2001. (Pubitemid 32124712)
50. Mandal, M., and Kumar, R. Bcl-2 expression regulates sodium butyrate-induced apoptosis in human MCF-7 breast cancer cells. Cell Growth Differ., 7: 311-318, 1996. (Pubitemid 26360770)
51. Hague, A., Diaz, G. D., Hicks, D. J., Krajewski, S., Reed, J. C., and Paraskeva, C. Bcl-2 and Bak may play a pivotal role in sodium butyrate-induced apoptosis in colonic epithelial cells; however overexpression of bcl-2 does not protect against bak-mediated apoptosis. Int. J. Cancer, 72: 898-905, 1997.
52. 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. (Pubitemid 28412628)
53. Kirsch, D. G., Doseff, A., Chau, B. N., Lim, D. S., de 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.
54. Li, H., Zhu, H., Xu, C. J., and Yuan, J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell, 94: 491-501, 1998. (Pubitemid 28391865)
55. Bible, K. C., Bible, R. H., Jr., Kottke, T. J., Svingen, P. A., Xu, K., Pang, Y. P., Hajdu, E., and Kaufmann S. H. Flavopiridol binds to duplex DNA. Cancer Res., 60: 2419-2428, 2000. (Pubitemid 30262432)
56. Lam, L. T., Pickeral, O. K., Peng, A. C., Rosenwald, A., Hurt, E. M., Giltnane, J. M., Averett, L. M., Zhao, H., Davis, R. E., Sathyamoorthy, M., Wahl, L. M., Harris, E. D., Mikovits, J. A., Monks, A. P., Hollingshead, M. G., Sausville, E. A., and Staudt, L. M. Genomic-scale measurement of mRNA turnover and the mechanisms of action of the anti-cancer drug flavopiridol. Genome Biol. 2: Research 0041.1-Research 0041.11, 2001.
57. Chao, S. H., and Price, D. H. Flavopiridol inactivates P-TEFb and blocks most RNA polymerase II transcription in vivo. J. Biol. Chem., 276: 31793-31799, 2001.
58. Meinhardt, G., Roth, J., and Hass, R. Activation of protein kinase C relays distinct signaling pathways in the same cell type: differentiation and caspase-mediated apoptosis. Cell Death Differ., 7: 795-803, 2000.
59. St Croix, B., and Kerbel, R. S. Cell adhesion and drug resistance in cancer. Curr. Opin. Oncol., 9: 549-556, 1997. (Pubitemid 27480858)
60. Levkau, B., Koyama, H., Raines, E. W., Clurman, B. E., Herren, B., Orth, K., Roberts, J. M., and Ross, R. Cleavage of p21Cip1/Waf1 and p27Kip1 mediates apoptosis in endothelial cells through activation of Cdk2: role of a caspase cascade. Mol. Cell, 1: 553-563, 1998. (Pubitemid 128374691)
61. Harbour, J. W., and Dean, D. C. The Rb/E2F pathway: expanding roles and emerging paradigms. Genes Dev., 14: 2393-2409, 2000.
62. Lipinski, M. M., and Jacks, T. The retinoblastoma gene family in differentiation and development. Oncogene, 18: 7873-7882, 1999. (Pubitemid 30066233)
63. Helin, K. Regulation of cell proliferation by the E2F transcription factors. Curr. Opin. Genet. Dev., 8: 28-35, 1998. (Pubitemid 28122137)
64. Muller, H., Bracken, A. P., Vernell, R, Moroni, M. C., Christians, F., Grassilli, E., Prosperini, E., Vigo, E., Oliner, J. D., and Helin, K. E2Fs regulate the expression of genes involved in differentiation, development, proliferation, and apoptosis. Genes Dev., 15: 267-285, 2001. (Pubitemid 32155143)
65. Geng, Y., Eaton, E. N., Picon, M., Roberts, J. M., Lundberg, A. S., Gifford, A., Sardet, C., and Weinberg, R. A. Regulation of cyclin E transcription by E2Fs and retinoblastoma protein. Oncogene, 12: 1173-1180, 1996. (Pubitemid 26127247)
66. Schulze, A., Zerfass, K., Spitkovsky, D., Middendorp, S., Berges, J., Helin, K., Jansen-Durr, P., and Henglein B. Cell cycle regulation of the cyclin A gene promoter is mediated by a variant E2F site. Proc. Natl. Acad. Sci. USA, 92: 11264-11268, 1995.
67. Girard, F., Strausfeld, U., Fernandez, A., and Lamb, N. J. Cyclin A is required for the onset of DNA replication in mammalian fibroblasts. Cell, 67: 1169-1179, 1991. (Pubitemid 121001529)
68. Giuliano, M., Lauricella, M., Calvaruso, G., Carabillo, M., Emanuele, S., Vento, R., and Tesoriere, G. The apoptotic effects and synergistic interaction of sodium butyrate and MG132 in human retinoblastoma Y79 cells. Cancer Res., 59: 5586-5595, 1999. (Pubitemid 29526478)
69. Cheng, E. H., Wei, M. C., Weiler, S., Flavell, R. A., Mak, T. W., Lindsten, T., and Korsmeyer, S. J. Bcl-2, bcl-x(l) sequester bh3 domain-only molecules preventing bax- and bak-mediated mitochondrial apoptosis. Mol. Cell, 3: 705-711, 2001. (Pubitemid 32946946)
70. Feldman, E. J., Seiter, K., Chiao, J. W., Halicka, H. D., Traganos, F., Fatora, S. R., McMichael, J., Baskind, P., Goff, H., Beer, M., Ahmed, T., and Darzynkiewicz Z. In vitro effects and clinical evaluation of a human chorionic gonadotrophin preparation in acute leukemia. Leukemia (Baltimore), 12: 1749-1755, 1998. (Pubitemid 28502494)
71. Gilbert, J., Baker, S. D., Bowling, M. K., Grochow, L., Figg, W. D., Zabelina, Y., Donehower, R. C., and Carducci, M. A. A phase I dose escalation and bioavailability study of oral sodium phenylbutyrate in patients with refractory solid tumor malignancies. Clin. Cancer Res., 7: 2292-3000, 2001.