Evidence of a functional role for the cyclin-dependent kinase inhibitor p21(WAF1/CIP1/MDA6) in the reciprocal regulation of PKC activator-induced apoptosis and differentation in human myelomonocytic leukemia cells

Experimental Cell Research

Volumn 244, Issue 1, 1998, Pages 105-116

  Wang, Zhiliang ^a   Su, Zao Zhong ^b   Fisher, Paul B ^b   Wang, Shujie ^a   VanTuyle, Glenn ^a   Grant, Steven ^a  

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

^b The New York Presbyterian Hospital   (United States)

Author keywords

Bryostatin 1; Differentiation; Leukemia; p21; PMA, apoptosis; Protein kinase C

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR; PROTEIN KINASE C ACTIVATOR; PROTEIN P21;

APOPTOSIS; ARTICLE; CELL ADHESION; CELL CYCLE; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME INHIBITION; ENZYME REGULATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; MYELOMONOCYTIC LEUKEMIA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 0032505675     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1998.4191     Document Type: Article

References (73)

1. 1 cyclin-dependent kinases. Genes Dev. 9, 1149-1163.
2. Chellapan, S. P., Giordano, A., and Fisher, P. B. (1977). The role of cyclin-dependent kinases and their inhibitors in cellular differentiation and development. Curr. Topics Microbiol. Immunol. 227, 57-103.
3. 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. (1993). WAF1, a potential mediator of p53 tumor suppression. Cell 75, 817-825.
4. Harper, J. W., Adami, G. R., Wei, N., Keyomarsi, K., and Elledge, S. J. (1993). The p21 cdk-interacting protein cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75, 805-816.
5. Xiong, Y., Hannon, G. J., Zhang, H., Casso, D., Kobayashi, R., and Beach, D. (1993). P21 is a universal inhibitor of cyclin kinases. Nature 366, 701-704.
6. Noda, A., Ning, Y., Venable, S. F., Pereira-Smith, O. M., and Smith, J. R. (1994). Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res. 211, 90-98.
7. Li, R., Waga, S., Hannon, G. J., Beach, D., and Stillman, B. (1994). Differential effects by the p21 CDK inhibitor on PCNA-dependent DNA replication and repair. Nature 371, 534-537.
8. Waga, S., Hannon, G. J., Beach, D., and Stillman, B., (1994). The p21 inhibitor of cyclin-dependent kinases controls DNA replication by interaction with PCNA. Nature 369, 574-578.
9. Chen, J., Jackson, P. K., Kirschner, M. W., and Dutta, A. (1995). Separate domains of p21 involved in the inhibition of cdk kinase and PCNA. Nature 374, 386-388.
10. Agarwal, M. L., Agarwal, A., Taylor, W. R., and Stark, G. R., (1995). p53 controls both the G2/M and the G1 cell cycle checkpoints and mediates reversible growth arrest in human fibroblasts. Proc. Natl. Acad. Sci. USA. 92, 8493-8497.
11. Waldman, T., Kinzler, K. W., and Vogelstein, B. (1995). P21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res. 55, 5187-5190.
12. Zhang, W., Grasso, L., McClain, C. D., Gambel, A. M., Cha, Y., Travali, S., Deisseroth, A. B., and Mercer, W. E. (1995). P53-independent induction of WAF1/CIP1 in human leukemia cells is correlated with growth arrest accompanying monocyte/macrophage differentiation. Cancer Res. 55, 668-674.
13. 1 cyclin-dependent kinase. Genes Dev. 9, 1149-1163.
14. Medrano, E. E., Im, S., Yang, F., and Abdel-Malek, Z. A. (1995). Ultraviolet B light induces G1 arrest in human melanocytes by prolonged inhibition of retinoblastoma protein phosphorylation associated with long-term expression of the p21Waf1/SDI1/ CIP1 protein. Cancer Res. 55, 4047-4052.
15. Afshari, C. A., Nichols, M. A., Xiong, Y., and Mudryj, M. (1996). A role for a p21-E2F interaction during senescence arrest of normal human fibroblasts. Cell Growth Differ. 7, 979-998.
16. Steinman, R., Hoffman, B., Iro, A., Guillouf, C., Liebermann, D., and El-Hoseini, M. (1994). Induction of p21 (WAF1/CIP1) during differentiation. Oncogene 9, 3389-3396.
17. Macleod, K. F., Sherry, N., Hannon, G., Beach, D., Tokino, T., Kinzler, K., Vogelstein, B., and Jacks, T. (1995). p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev. 9, 935-944.
18. Jiang, H., Lin, J., Su, Z. Z., Collart, F. R., Huberman, E., and Fisher, P. B. (1994). Induction of differentiation in human promyelocytic HL-60 leukemia cells activates p21, WAF1/CIP1, expression in the absence of p53. Oncogene 9, 3397-3406.
19. Michieli, P., Chedid, M., Lin, D., Pierce, J. H., Mercer, W. E., and Gigol, D. (1994). Induction of WAF1/CIP1 by a p53-independent pathway. Cancer Res. 54, 3391-3395.
20. Parker, S. B., Eichele, G., Zhang, P., Rawls, A., Sands, A. T., Bradley, A., Olson, E. N., Harper, J. W., and Elledge, S. T. (1995). p53-independent expression of p21Cip1 in muscle and other terminally differentiating cells. Science 267, 1024-1027.
21. Zeng, Y. X., and El-Deiry, W. S. (1996). Regulation of p21WAF1/ CIP1 expression by p53-independent pathways. Oncogens 11, 1557-1163.
22. Kraft, A. S., Smith, J. B., and Berkow, R. L. (1986). Bryostatin, an activator of the calcium phospholipid dependent protein kinase, blocks phorbol ester-induced differentiation of human promyeleocytic leukemia cells HL60. Proc. Natl. Acad. Sci. USA 83, 1334-1338.
23. Stone, R. M., Sariban, E., Pettit, G. R., and Kufe, D. W. (1988). Bryostatin 1 activates protein kinase C and induces monocytic differentiation of HL-60 cells. Blood 72, 208-213.
24. Kraft, A. S., William, F., Pettit, G. R., and Lilly, M. B. (1989). Varied differentiation regulation of human leukemias to bryostatin 1. Cancer Res. 49, 1287-1293.
25. Grant, S., McCrady, C., Boise, L., Westin, E. H., and Pettit, G. R. (1991). Effects of bryostatin 1 on the metabolism and cytotoxicity of 1-β-D arabinofuranosylcytosine in human leukemia cells. Biochem. Pharmacol. 42, 853-867.
26. Asiedu, C., Biggs, J., Lilly, M., and Kraft, A. S. (1995). Inhibition of leukemic cell growth by the protein kinase C activator bryostatin 1 correlates with the dephosphorylation of cyclin-dependent kinase 2. Cancer Res. 55, 3716-3720.
27. Ng, S. B., and Guy, G. R. (1992). Two protein kinase C activators, bryostatin 1 and phorbol-12-myristate-13-acetate, have different effects on haemopoietic cell proliferation and differentiation. Cell. Signal. 4, 405-416.
28. Grant, S., Jarvis, W. D., Swerdlow, P., Turner, A. J., Traylor, R., Wallace, H., Lin, P. S., Pettit, G. R., and Gewirtz, D. A. (1992). Potentiation of the activity of 1-β-D arabinofuranosylcytosine by the macrocyclic lactone PKC activator bryostatin 1 is associated with enhanced fragmentation of mature DNA. Cancer Res. 52, 6270-6278.
29. Grant, S., Turner, A. J., Freemerman, A. J., Wang, Z, Kramer, L., Jarvis, W. D. (1996). Modulation of protein kinase C activity and calcium-sensitive isoform expression in human myeloid leukemia cells by bryostatin 1: Relationship to differentiation and ara-C-induced apoptosis. Exp. Cell Res. 228, 65-75.
30. Jayson, G. C., Crowther, D., Prendville, J., McGowan, A. T., Scheid, C., Stern, P., Young, R., Brenchley, P., Chang, J., Owens, S., Pettit, G. R. (1995). A phase I trial of bryostatin 1 in patients with advanced malignancy using a 24-hour intravenous infusion. Br. J. Cancer 72, 461-468.
31. Freemerman, A. J., Vrana, J. A., Tombes, R. M., Jiang, H., Chellappan, S. P., Fisher, P. B., and Grant, S. (1997). Effects of antisense p21(WAF1/CIP1/MDA6) expression on the induction of differentiation and drug-mediated apoptosis in human myeloid leukemia cells (HL60). Leukemia 11, 504-513.
32. Selvakumaran, M., Reed, J. C., Liebermann, and Hoffman, B. (1994). Progression of myeloid differentiation program is dominant to transforming growth factor-β1-induced apoptosis in M1 myeloid leukemic cells. Blood 84, 1036-1042.
33. Sundstrom, C., and Nilsson, K. (1976). Establishment and characterization of a human histiocytic lymphoma cell line (U937). Int. J. Cancer 17, 565-577.
34. Jarvis, W. D., Povirk, L. F., Turner, A. J., Traylor, R. S., Gewirtz, D. A., Pettit, G. R., and Grant, S. (1994). Effects of bryostatin 1 and other pharmacological activators of protein kinase C on 1-[beta-DD-arabinofuranosyl]cytosine-induced apoptosis in HL-60 human promyelocytic leukemia cells. Biochem. Pharmacol. 47, 839-852.
35. Zamzami, N., Marchetti, P., Castedo, M., Decaudin, D., Macho, A., Hirsch, T., Susin, S. A., Petit, P. X., Mignotte, B., and Kroemer, G. (1995). Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182, 367-377.
36. Yang, J., Liu, X., Bhalla, K., Kim, C. N., Ibrado, A. M., Cai, J., Peng, T-I., Jones, D. P., and Wang, X. (1997). Prevention of apoptosis by Bcl-2; Release of cytochrome c blocked. Science 275, 1129-1132.
37. Vrana, J. A., Saunders, A. M., Chellapan, S. P., and Grant, S. Divergent effects of bryostatin 1 and PMA on cell cycle arrest and maturation in human myelomonocytic leukemia cells (U937). Differentiation, in press.
38. Gu, Y., Rosenblatt, J., and Morgan, D. O. (1992). Cell cycle regulation of cdk2 activity by phosphorylation of Thr160 and Tyr15. EMBO J. 11, 3395-4005.
39. Kato, G. J., and Dang, C. V. (1992). Function of the c-Myc oncoprotein. FASEB J. 6, 3065-3072.
40. Filmus, J., and Buick, R. N. (19850). Relationship of c-myc expression to differentiation and proliferation in HL-60 cells. Cancer Res. 45, 822-825.
41. Kraft, A. S., Baker, V. V., and May, W. S. (1987). Bryostatin 1 induces changes in protein kinase C location and activity without altering c-myc expression in human promyelocytic leukemia cells (HL-60). Oncogene 1, 111-118.
42. Martin, S. J., Bradley, J. G., and Cotter, T. G. (1990). HL-60 cells induced to differentiate towards neutrophils subsequently die via apoptosis. Clin. Exp. Immmunol. 79, 448-453.
43. Bertrand, R., and Pommier, Y. (1994). Apoptosis of human leukemic HL-60 cells induced to differentiate by phorbol ester treatment. Leukemia 8, 792-797.
44. de Vente, J., Kiley, S., Garris, T., Bryant, W., Hooker, J., Posekany, K., Parker, P., Cook, P., Fletcher, D., and Ways, D. K. (1995). Phorbol ester treatment of U937 cells with altered protein kinase C content and distribution induces cell death rather than differentiation. Cell Growth Differ. 6, 371-382.
45. Medina, V., Edmonds, B., Young, G. P., James, R., Appleton, S., and Zalewski, P. D. (1997). Induction of caspase-3 protease activity and apoptosis by butyrate and trichostatin A (Inhibitors of histone deacetylase): Dependence on protein synthesis and synergy with a mitochondrial/cytochrome c-dependent pathway. Cancer Res. 57, 3697-3707.
46. Weinberg, R. A. (1995) The retinoblastoma protein and cell cycle control. Cell 81, 323-330.
47. Morgan, D. O. (1995) Principles of CDK regulation. Nature 374, 131-134.
48. Akiyama, T., Ohuchi T., Sumida S., Matsumoto K., and Toyoshima, K. (1992) Marked alteration in phosphorylation of the RB protein during differentiation of human promyelocytic HL-60 cells. Oncogene 5, 179-183.
49. Zhou, W., Takuwa, N., Kumada, M., and Takuwa, Y. (1993). Protein kinase C-mediated bidirectional regulation of DNA synthesis, RB protein phosphorylation, and cyclin-dependent kinases in human vascular endothelial cells. J. Biol. Chem. 268, 21041-23048.
50. 1. Mol. Cell Biol. 8, 1614-1624.
51. Wang, Q. M., Jones, J. B., and Studzinski, G. P. (1995). Cyclindependent kinase inhibitor p27 as a mediator of the G1-S phase block induced by 1,25-dihydroxyvitamin D3 in HL-60 cells. Cancer Res. 56, 264-267.
52. Steube, K. G., Grunicke, D., and Drexler, H. G. (1994). Different biological effects of the two protein kinase C activators bryostatin-1 and TPA on human carcinoma cell line. Invest. New Drugs 12, 15-23.
53. Carey, J. D., Posekany, K. J., deVente, J. E., Pettit, G. R., and Ways, D. K. (1996). Phorbol ester-stimulated phosphorylation of PU.1: Association with leukemic cell growth inhibition. Blood 87, 4316-4324.
54. Aihira, H., Asaoka, Y., Yoshida, K., and Nishizuka, Y. (1991). Sustained activation of protein kinase C is essential to HL-60 cell differentiation to macrophage. Proc. Natl. Acad. Sci. USA 58, 11062-11066.
55. 1 arrest. J. Clin. Invest. 89, 854-860.
56. Grant, S., Rao, A., Freemerman, A. J., Turner, A. J., Kornstein, M. J., Chelliah, J., and Jarvis, W. D. (1995). Divergent effects of calcium ionophore (A23187) on bryostatin 1-related differentiation and apoptosis in human promyelocytic leukemia cells (HL-60). Mol. Cell Differ. 3, 337-359.
57. Rao A., Freemerman, A. J., Jarvis, W. D., Chelliah, J., Bear, H. D., Mikkelsen, R., and Grant, S. (1996). Effects of AS101 on bryostatin 1-mediated differentiation induction, cell cycle arrest, and modulation of drug-induced apoptosis in human myeloid leukemia cells. Leukemia 10, 1150-1158.
58. Solary, E., Bertrand, R., Kohn, K., and Pommier, Y. (1993). Differential induction of apoptosis in undifferentiated and differentiated HL-60 cells by DNA topoisomerase inhibitors. Blood 81, 1353-1368.
59. Bhatia, U., Traganos, F., and Darzynkiewicz, Z. (1995). Induction of cell differentiation potentiates apoptosis triggered by prior exposure to DNA-damaging drugs. Cell Growth Differ. 6, 937-944.
60. Wang, J., and Walsh, K. (1996). Resistance to apoptosis conferred by cdk inhibitors during myocyte differentiation. Science 273, 359-361.
61. Waldman, T., Lengauer, C., Kinzler, K. W., and Vogelstein, B. (1996). Uncoupling of S phase and mitosis induced by anticancer agents in cells lacking p21. Nature 381, 713-716.
62. Waldman, T., Zhang, Y., Dillehay, L., Kinzler, K., Vogelstein, B., and Williams, J. (1997). Cell cycle arrest versus cell death in cancer therapy. Nat. Med. 3, 1034-1036.
63. Jiang, H., and Fisher, P. B. (1993). Use of a sensitive and efficient subtraction hybridization protocol for the identification of genes differentially regulated during the induction of differentiation in human melanoma cells. Mol. Cell Differ. 1, 285-299.
64. Jiang, H., Lin, J., Su, Z-z., Kerbel, R. S., Herlyn, M., Weissman, R. B., Welch, D., and Fisher, P. B. (1995). The melanoma differentiation associated gene mda-6, which encodes the cyclin-dependent kinase inhibitor p21, is differentially expressed during growth, differentiation, and progression in human melanoma cells. Oncogene 10, 1855-1864.
65. CIP1, Rb, and c-myc signaling in phorbol ester-resistant cancer cells. Cancer Res. 57, 320-325.
66. Marchetti, P. M., Castedo, S. A., Susin, N., Zamzani, T., Hirsch, A., Haeffner, F., Hirsch, M., Geuskens, M., and Kroemer, G. (1996). Mitochondrial permeability transition is a central coordinating event of apoptosis. J. Exp. Med. 184, 1155-1160.
67. Bossy-Wetzel, E., Newmeyer, D. D., and Green, D. R. (1998). Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J. 17, 37-49.
68. Zou, H., Henzel, W. J., Liu, X., Lutschg, A., and Wang, X. (1997) Apaf-1, a human protein homologous to C. Elegans CED-4, participates cytochrome c-dependent activation of caspase-3. Cell 90, 405-413.
69. Fernandes-Alnemri, T., Litwack, G., Alnemri, E. S. (1994). cpp32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein CED-3 and mammalian interleukin-1β-converting enzyme. J. Biol. Chem. 269, 30761-30764.
70. Tang, D. G., Li, L., Zhu, Z., and Joshi, B. (1998). Apoptosis in the absence of cytochrome c accumulation in the cytosol. Biochem. Biophys. Res. Commun. 242, 380-384.
71. Studzinski, G. P., Reddy, K. B., Hill, H. Z., and Bhandal, A. K. (1991). Potentiation of 1-beta-D-arabinsfuranosylcytosine cytotoxicity to HL-60 cells by 1,25-dihydroxyvitamin D3 correlates with reduced rate of maturation of DNA replication intermediates. Cancer Res. 51, 3451-3455.
72. Huang, Y., and Waxman, S. (1994). Enhanced apoptosis in leukemia cells following treatment with combined fluoropyrimidines and differentiation inducers. Mol. Cell Differ. 2, 83-100.
73. Ehinger, M., Bergh, G., Olofsson, T., Baldetorp, B., Olsson, I., and Gullberg, U. (1996). Expression of the p53 tumor suppressor gene induces differentiation and promotes induction of by 1,25-Dihydroxycholecalciferol in leukemic U-937 cells. Blood 87, 1064-1074.