Two cytodifferentiation agent-induced pathways, differentiation and apoptosis, are distinguished by the expression of human papillomavirus 16 E7 in human bladder carcinoma cells

Cancer Research

Volumn 57, Issue 13, 1997, Pages 2789-2798

  Richon, Victoria M ^a   Russo, Paul ^a   Venta Perez, Gisela ^a   Cordon Cardo, Carlos ^a   Rifkind, Richard A ^a   Marks, Paul A ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEXAMETHYLENEBISACETAMIDE; REGULATOR PROTEIN;

APOPTOSIS; ARTICLE; BLADDER CARCINOMA; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CELL TRANSFORMATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; VIRUS EXPRESSION;

ACETAMIDES; ACTINS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOMA, TRANSITIONAL CELL; CARRIER PROTEINS; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL DIVISION; CELL SIZE; DNA-BINDING PROTEINS; E2F TRANSCRIPTION FACTORS; G1 PHASE; GROWTH INHIBITORS; HUMANS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; NUCLEAR PROTEINS; ONCOGENE PROTEINS, VIRAL; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEINS; RETINOBLASTOMA PROTEIN; RETINOBLASTOMA-LIKE PROTEIN P107; RETINOBLASTOMA-LIKE PROTEIN P130; TRANSCRIPTION FACTOR DP1; TRANSCRIPTION FACTORS; TRANSFECTION; TUMOR CELLS, CULTURED; URINARY BLADDER NEOPLASMS;

EID: 0030745314     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (87)

1. Marks, P. A., Richon, V. M., and Rifkind, R. A. Cell cycle regulatory proteins are targets for induced differentiation of transformed cells: molecular and clinical studies employing hybrid polar compounds. Int. J. Hematol., 63: 1-17, 1996.
2. Reuben, R. C., Wife, R. L., Breslow, R., Rifkind, R. A., and Marks, P. A. A new group of potent inducers of differentiation in murine erythroleukemia cells. Proc. Natl. Acad. Sci. USA, 73: 862-866, 1976.
3. Friend, S. H., Horowitz, J. M., Gerber, M. R., Wang, X. F., Bogenmann, E., Li, F. P., and Weinberg, R. A. Deletions of a DNA sequence in retinoblastomas and mesenchymal tumors: organization of the sequence and its encoded protein. Proc. Natl. Acad. Sci. USA, 84: 9059-9063, 1987.
4. Lee, W-H., Bookstein, R., Hong, F., Young, L., Shew, J., and Lee, E. Y. H. Human retinoblastoma susceptibility gene: cloning, identification, and sequence. Science (Washington DC), 235: 1394-1399, 1987.
5. Fung, Y. T., Murphree, A. L., T'Ang, A., Qian, J., Hinrichs, S. H., and Benedict, W. F. Structural evidence for the authenticity of the human retinoblastoma gene. Science (Washington DC), 236: 1657-1659, 1987.
6. Ewen, M. E., Xing, Y., Lawrence, J. B., and Livingston, D. M. Molecular cloning, chromosomal mapping and expression of the cDNA for p107, a retinoblastoma gene product-related protein. Cell, 66: 1155-1164, 1991.
7. Cobrinik, D., Whyte, P., Pepper, D. S., Jackson, T., and Weinberg, R. A. Cell cycle-specific association of E2F with the p130 E1A-binding domain. Genes Dev., 7: 2392-2404, 1993.
8. Li, Y., Graham, C., Lacy, S., Dunean, A. M. W., and Whyte, P. The adenovirus E1A-associated 130-kD is encoded by a member of the retinoblastoma gene family and physically interacts with cyclin A and E. Genes Dev., 7: 2366-2377, 1993.
9. Hannon, G. J., Demetrick, D., and Beach, D. Isolation of the Rb-related p130 through its interaction with CDK2 and cyclins. Genes Dev., 7: 2378-2391, 1993.
10. Kaelin, W. G., Jr., Krek, W., Sellers, W. R., DeCaprio, J. A., Ajchenbaum-Cymbalista, F., Fuchs, C. S., Chittenden, T., Li, Y., Farnham, P. J., Blanar, M. A., Livingston, D. M., and Flemington, E. K. Expression cloning of a cDNA encoding a retinoblastoma-binding protein with E2F-like properties. Cell, 70: 351-364, 1992.
11. Helin, K., Lees, J. A., Vidal, M., Dyson, N., Harlow, E., and Fattaey, A. A cDNA encoding a pRB-binding protein with properties of the transcription factor E2F. Cell, 70: 337-350, 1992.
12. Shan, B., Zhu, X., Chen, P-L., Durfee, T., Yang, Y., Sharp, D., and Lee, W-H. Molecular cloning of cellular genes encoding retinoblastoma-associated proteins: identification of a gene with properties of the transcription factor E2F. Mol. Cell. Biol., 12: 5620-5631, 1992.
13. Bandara, L. R., Buck, V. M., Zamanian, M., Johnston, L. H., and La Thangue, N. B. Functional synergy between DP-1 and E2F-1 in the cell cycle-regulating transcription factor DRTF1/E2F. EMBO J., 12: 4317-4324, 1993.
14. Girling, R., Partridge, J. F., Bandara, L. R., Burden, N., Totty, N. F., Hsuan, J. J., and La Thangue, N. B. A new component of the transcription factor DRTF1/E2F. Nature (Lond.), 362: 83-87, 1993.
15. Helin, K., Wu, C., Fattaey, A. R., Lees, J. A., Dynlacht, B. D., Ngwu, C., and Harlow, E. Heterodimerization of the transcription factors E2F-1 and DP-1 leads to cooperative trans-activation. Genes Dev., 7: 1850-1861, 1993.
16. Krek, W., Livingston, D. M., and Shirodkar, S. Binding to DNA, and the retinoblastoma gene product promoted by complex formation of different E2F family members. Science (Washington DC), 262: 1557-1560, 1993.
17. Ivey-Hoyle, M., Conroy, R., Huber, H. E., Goodhart, P. J., Oliff, A., and Heimbrook, D. C. Cloning and characterization of E2F-2, a novel protein with the biochemical properties of transcription factor E2F. Mol. Cell. Biol., 13: 7802-7812, 1993.
18. Lees, J. A., Saito, M., Vidal, M., Valentine, M., Look, T., Harlow, E., Dyson, N., and Helin, K. The retinoblastoma protein binds to a family of E2F transcription factors. Mol. Cell. Biol., 13: 7813-7825, 1993.
19. Ginsberg, D., Vairo, G., Chittenden, T., Xiao, Z., Xu, G., Wydner, K. L., DeCaprio, J. A., Lawrence, J. B., and Livingston, D. M. E2F-4, a new member of the E2F transcription factor family, interacts with p107. Genes Dev., 8: 2665-2679, 1994.
20. Beijersbergen, R. L., Kerkhoven, R. M., Zhu, L., Carlee, L., Voorhoeve, P. M., and Bernards, R. E2F-4, a new member of the E2F gene family, has oncogenic activity and associates with p107 in vivo. Genes Dev., 8: 2680-2690, 1994.
21. Sardet, C., Vidal, M., Cobrinik, D., Geng, Y., Onufryk, C., Chen, A., and Weinberg, R. A. E2F-4 and E2F-5, two members of the E2F family, are expressed in the early phases of the cell cycle. Proc. Natl. Acad. Sci. USA, 92: 2403-2407, 1995.
22. Bandara, L. R., Lam, E. W., Sorensen, M., Zamanian, M., Girling, R., and La Thangue, N. B. DP-1: a cell cycle-regulated and phosphorylated component of transcription factor DRTF1/E2F which is functionally important for recognition by pRB and the adenovirus E4 of 6/7 protein. EMBO J., 13: 3104-3114, 1994.
23. Wu, C., Zukerberg, L. R., Ngwu, C., Harlow, E., and Lees, J. A. In vivo association of E2F and DP family proteins. Mol. Biol. Cell, 15: 2536-2546, 1995.
24. Hamel, P. A., Gill, R. M., Phillips, R. A., and Gallie, B. L. Transcriptional repression of the E2-containing promoters EIIaE, c-myc, and RB1 by the product of the RB1 gene. Mol. Cell. Biol., 12: 3431-3438, 1992.
25. Hiebert, S. W., Chellappan, S. P., Horowitz, J. M., and Nevins, J. R. The interaction of RB with E2F coincides with an inhibition of the transcriptional activity of E2F. Genes Dev., 6: 177-185, 1992.
26. Weintraub, S. J., Prater, C. A., and Dean, D. C. Retinoblastoma protein switches the E2F site from positive to negative element. Nature (Lond.), 358: 259-261, 1992.
27. Zamanian, M., and La Thangue, N. B. Adenovirus E1A prevents the retinoblastoma gene product from repressing the activity of a cellular transcription factor. EMBO J., 11: 2603-2610, 1992.
28. Schwartz, J. K., Devoto, S. H., Smith, E. J., Chellappan, S. P., Jakoi, L., and Nevins, J. R. Interactions of the p107 and Rb proteins with E2F during the cell proliferation response. EMBO J., 12: 1013-1020, 1993.
29. Zamanian, M., and La Thangue, N. B. Transcriptional repression by the Rb-related protein p107. Mol. Biol. Cell, 4: 389-396, 1993.
30. Zhu, L., van den Heuvel, S., Helin, K., Fattaey, A., Ewen, M., Livingston, D. M., Dyson, N., and Harlow, E. Inhibition of cell proliferation by p107, a relative of the retinoblastoma protein. Genes Dev., 7: 1111-1125, 1993.
31. 1-S-regulatory genes. Mol. Cell. Biol., 15: 4215-4224, 1995.
32. Nevins, J. R. E2F: a link between the Rb tumor suppressor protein and viral oncoprotein. Science (Washington DC), 258: 424-429, 1992.
33. Lam, E. W., and Watson, R. J. An E2F-binding site mediates cell-cycle regulated repression of mouse B-myb transcription. EMBO J., 12: 2705-2713, 1994.
34. Hsiao, K-M., McMahon, S. L., and Farnham, P. J. Multiple DNA elements are required for the growth regulation of the mouse E2F1 promoter. Genes Dev., 8: 1526-1537, 1994.
35. Johnson, D. G., Ohtani, K., and Nevins, J. R. Autoregulatory control of E2F1 expression in response to positive and negative regulators of cell cycle progression. Genes Dev., 8: 1514-1525, 1994.
36. Bagchi, S., Weinmann, R., and Raychaudhuri, P. The retinoblastoma protein copurifies with E2F-I, an E1A-regulated inhibitor of the transcription factor E2F. Cell, 65: 1063-1072, 1991.
37. Bandara, L. R., and La Thangue, N. B. Adenovirus E1A prevents the retinoblastoma gene product from complexing with a cellular transcription factor. Nature (Lond.), 351: 494-497, 1991.
38. 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.
39. Chittenden, T., Livingston, D. M., and Kaelin, W. G., Jr. The T/E1 A-binding domain of the retinoblastoma product can interact selectively with a sequence-specific DNA-binding protein. Cell, 65: 1073-1082, 1991.
40. Ewen, M. E., Sluss, H. K., Sherr, C. J., Matsushime, H., Kato, J., and Livingston, D. M. Functional interactions of the retinoblastoma protein with mammalian D-type cyclins. Cell, 73: 487-497, 1993.
41. Hinds, P. W., Mittnacht, S., Dulic, V., Arnold, A., Reed, S. I., and Weinberg, R. A. Regulation of retinoblastoma protein functions by ectopic expression of human cyclins. Cell, 70: 993-1006, 1992.
42. Lees, J. A., Buchkovich, K. J., Marshak, D. R., Anderson, C. W., and Harlow, E. The retinoblastoma protein is phosphorylated on multiple sites by human cdc2. EMBO J., 10: 4279-4290, 1991.
43. Matsushime, H., Quelle, D. E., Shurtleff, S., Sherr, C. J., and Kato, J. D-type cyclin-dependent kinase activity in mammalian cells. Mol. Cell. Biol., 14: 2066-2076, 1994.
44. Meyerson, M., and Harlow, E. Identification of G1 kinase activity for cdk6 a novel cyclin D partner. Mol. Cell. Biol., 14: 2077-2086, 1994.
45. Cao, L., Faha, B., Dembski, M., Tsai, L-H., Harlow, E., and Dyson, N. Independent binding of the retinoblastoma protein and p107 to the transcription factor E2F. Nature (Lond.), 355: 176-179, 1992.
46. Lees, E., Faha, B., Dulic, V., Reed, S. I., and Harlow, E. Cyclin E/cdk2 and cyclin A/cdk2 kinase associate with p107 and E2F in a temporally distinct manner. Genes Dev., 6: 1874-1885, 1992.
47. Shirodkar, S., Ewen, M., DeCaprio, J. A., Morgan, J., Livingston, D. M., and Chittenden, T. The transcription factor E2F interacts with the retinoblastoma product and a p107-cyclin A complex in cell cycle-regulated manner. Cell, 68: 157-166, 1992.
48. Cobrinik, D., Dowdy, S. F., Hinds, P. W., Mittnacht, S., and Weinberg, R. A. The retinoblastoma protein and the regulation of cell cycling. Trends Biochem. Sci., 17: 312-315, 1992.
49. Shin, E. K., Shin, A., Paulding, C., Schaffhausen, B., and Yee, A. S. Multiple changes in E2F function and regulation occur upon muscle differentiation. Mol. Cell. Biol., 15: 2252-2262, 1995.
50. Kiess, M., Gill, R. M., and Hamel, P. A. Expression and activity of the retinoblastoma protein (pRB)-family proteins, p107 and p130, during L6 myoblast differentiation. Cell Growth & Differ., 6: 1287-1298, 1995.
51. Buchkovich, K. J., and Ziff, E. B. Nerve growth factor regulates the expression and activity of p33cdk2 and p34cdc2 kinases in PC12 pheochromocytoma cells. Mol. Biol. Cell, 5: 1225-1241, 1994.
52. Ikeda, M., Jakoi, L., and Nevins, J. R. A unique role for the Rb protein in controlling E2F accumulation during cell growth and differentiation. Proc. Natl. Acad. Sci. USA, 93: 3215-3220, 1996.
53. Schneider, J. W., Gu, W., Zhu, L., Mahdavi, V., and Nadal-Ginard, B. Reversal of terminal differentiation mediated by p107 in Rb-/- muscle cells. Science (Washington DC), 264: 1467-1471, 1994.
54. Dyson, N., Howley, P. M., Munger, K., and Harlow, E. The human papillomavirus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science (Washington DC), 243: 934-937, 1989.
55. Chellappan, S. P., Kraus, V. B., Kroger, B., Munger, K., Howley, P. M., Phelps, W. C., and Nevins, J. R. Adenovirus E1A, simian virus 40 tumor antigen, and human papillomavirus E7 protein share the capacity to disrupt the interaction between transcription factor E2F and the retinoblastoma gene product. Proc. Natl. Acad. Sci. USA, 89: 4549-4553, 1992.
56. Dyson, N., Guida, P., Munger, K., and Harlow, E. Homologous sequences in adenovirus E1A and human papillomavirus E7 proteins mediate interaction with the same set of cellular proteins. J. Virol., 66: 6893-6902, 1992.
57. Wigler, M., Pellicer, A., Silverstein, S., Axel, R., Urlaub, G., and Chasin, L. DNA-mediated transfer of the adenine phosphoribosyltransferase locus into mammalian cells. Proc. Natl. Acad. Sci. USA, 76: 1373-1376, 1979.
58. Cordon-Cardo, C., and Richon, V. M. Expression of the retinoblastoma protein is regulated in normal human tissues. Am. J. Pathol., 144: 500-510, 1994.
59. Gavrieli, Y., Sherman, Y., and Ben-Sasson, S. A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol., 119: 493-501, 1992.
60. Dignam, J. D., Lebovitz, R. M., and Roeder, R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res., 11: 1475-1489, 1983.
61. Dyson, N., Dembski, M., Fattaey, A., Ngwu, C., Ewen, M., and Helin, K. Analysis of p107-associated proteins: p107 associates with a form of E2F that differs from pRB-associated E2F-1. J. Virol., 67: 7641-7647, 1993.
62. Towbin, H., Staehelin, T., and Gordon, J. Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA, 76: 4350-4354, 1979.
63. Burnette, W. N. Western blotting: electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal. Biochem., 112: 195-203, 1981.
64. Melton, D. A., Krief, P. A., Rebagliati, M. R., Maniatis, T., Zinn, K.,. and Green, M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res., 12: 7035-7056, 1984.
65. Rosenblatt, J., Gun, Y., and Morgan, D. O. Human cyclin-dependent kinase 2 is activated during the S and G2 phases of the cell cycle and associates with cyclin A. Proc. Natl. Acad. Sci. USA, 89: 2824-2828, 1992.
66. Kiyokawa, H., Richon, V. M., Rifkind, R. A., and Marks, P. A. Suppression of cyclin-dependent kinase 4 during induced differentiation of erythroleukemia cells. Mol. Cell. Biol., 14: 7195-7203, 1994.
67. Southgate, J., Hutton, K. A. R., Thomas, D. F. M., and Trejdosiewicz, L. K. Normal human urothelial cells in vitro: proliferation and induction of stratification. Lab. Invest., 71: 583-593, 1994.
68. Koss, E. G. Some ultrastructural aspects of experimental and human carcinoma of the bladder. Cancer Res., 37: 2824-2835, 1977.
69. Mayol, X., Garriga, J., and Grana, X. Cell cycle-dependent phosphorylation of the retinoblastoma-related protein p130. Oncogene, 11: 801-808, 1995.
70. Yamasaki, E., Jacks, T., Bronson, R., Goillot, E., Harlow, E., and Dyson, N. Tumor induction and tissue atrophy in mice lacking E2F-1. Cell, 85: 537-548, 1996.
71. Moberg, K., Starz, M. A., and Lees, J. A. E2F-4 switches from p130 to p107 and pRB in response to cell cycle reentry. Mol. Cell. Biol., 16: 1436-1449, 1996.
72. Jacks, T., Fazeli, A., Schmitt, E. M., Bronson, R. T., Goodell, M. A., and Weinberg, R. A. Effects of an Rb mutation in the mouse. Nature (Lond.), 359: 295-300, 1992.
73. Clarke, A. R., Maandag, E. R., van Roon, M., van der Lugt, N. M. T., van der Valk, M., Hooper, M. L., Berns, A., and te Riele, H. Requirement for a functional Rb-1 gene in murine development. Nature (Lond.), 359: 328-330, 1992.
74. Lee, E. Y. H., Chang, C-Y., Hu, N., Wang, Y-C. J., Lai, C-C., Herrup, K., Lee, W-H., and Bradley, A. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature (Lond.), 359: 288-294, 1992.
75. Johnson, D. G., Schwarz, J. K., Cress, W. D., and Nevins, J. R. Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature (Lond.), 365: 349-352, 1993.
76. Qin, X., Livingston, D. M., Kaelin, W. G., Jr., and Adams, P. D. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA, 91: 10918-10922, 1994.
77. Shan, B., and Lee, W-H. Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell. Biol., 14: 8166-8173, 1994.
78. Kowalik, T. F., DeGregori, J., Schwartz, J. K., and Nevins, J. R. E2F1 overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J. Virol., 69: 2491-2500, 1995.
79. Dobrowolski, S. F., Stacey, D. W., Harter, M. L., Stine, J. T., and Hiebert, S. W. An E2F dominant negative mutant blocks E1A induced cell cycle progression. Oncogene, 9: 2605-2612, 1994.
80. Wu, X., and Levine, A. J. p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA, 91: 3602-3606, 1994.
81. Pan, H., and Griep, A. E. Altered cell cycle regulation in the lens of HPV-16 E6 or E7 transgenic mice: implications for tumor suppressor gene function in development. Genes Dev., 8: 1285-1299, 1994.
82. DeGregori, J., Leone, G., Ohtani, K., Miron, A., and Nevins, J. R. E2F-1 accumulation bypasses a G1 arrest resulting from the inhibition of G1 cyclin-dependent kinase activity. Genes Dev., 9: 2873-2887, 1995.
83. Krek, W., Ewen, M. E., Shirodkar, S., Arany, Z., Kaelin, W. G., Jr., and Livingston, D. M. Negative regulation of the growth-promoting transcription factor E2F-1 by a stably bound cyclin A-dependent protein kinase. Cell, 78: 161-172, 1994.
84. Krek, W., Xu, G., and Livingston, D. M. Cyclin A-kinase regulation of E2F-1 DNA binding function underlies suppression of an S phase checkpoint. Cell, 83: 1149-1158, 1995.
85. Dynlacht, B. D., Flores, O., Lees, J. A., and Harlow, E. Differential regulation of E2F trans-activation by cyclin/cdk2 complexes. Genes Dev., 8: 1772-1786, 1994.
86. Xu, M., Sheppard, K. A., Peng, C-Y., Yee, A. S., and Piwnica-Worms, H. Cyclin A/cdk2 binds directly to E2F-1 and inhibits the DNA-binding activity of E2F-1/Dp-1 by phosphorylation. Mol. Cell. Biol., 14: 8420-8431, 1994.
87. Richon, V. M., and Venta-Perez, G. Changes in E2F DNA-binding activity during induced erythroid differentiation. Cell Growth & Differ., 7: 31-42, 1996.