Toward an understanding of the functional complexity of the E2F and retinoblastoma families

Cell Growth and Differentiation

Volumn 9, Issue 8, 1998, Pages 585-593

  Nevins, Joseph R ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F;

BIOACCUMULATION; CELL CYCLE; CELL GROWTH; DNA REPLICATION; GENE REPRESSION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; REVIEW; TRANSCRIPTION REGULATION;

ANIMALS; CARRIER PROTEINS; CELL CYCLE; CELL CYCLE PROTEINS; CELL DIVISION; DNA-BINDING PROTEINS; E2F TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTORS;

EID: 0031815596     PISSN: 10449523     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (100)

1. 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.
2. Chittenden, T., Livingston, D. M., and Kaelin, W. G., Jr. The T/E1A-binding domain of the retinoblastoma product can interact selectively with a sequence-specific DNA-binding protein. Cell, 65: 1073-1082, 1991.
3. 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.
4. 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.
5. Ewen, M. E., Xing, Y. G., 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.
6. 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.
7. Li, Y., Graham, C., Lacy, S., Duncan, A. M. V., and Whyte, P. The adenovirus E1A-associated 130-kd protein is encoded by a member of the retinoblastoma gene family and physically interacts with cyclins A and E. Genes Dev., 7: 2366-2377, 1993.
8. Mayol, X., Grana, X., Baldi, A., Sang, N., Hu, Q., and Giordano, A. Cloning of a new member of the retinoblastoma gene family (pRb2) which binds to the E1A transforming domain. Oncogene, 8: 2561-2566, 1993.
9. 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.
10. Kaelin, W. G., Krek, W., Sellers, W. R., DeCaprio, J. A., Ajchenbaum, 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., 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. 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.
13. Hijmans, E. M., Voorhoeve, P. M., Beijersbergen, R. L., van'T Veer, L. J., and Bernards, R. E2F-5, a new E2F family member that interacts with p130 in vivo. Mol. Cell. Biol., 15: 3082-3089, 1995.
14. Ginsberg, D., Vairo, G., Chittenden, T., Xiao, Z-X., 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.
15. 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.
16. 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.
17. Zhang, Y., and Chellappan, S. Cloning and characterization of human DP2, a novel dimerization partner of E2F. Oncogene, 10: 2085-2093, 1995.
18. Trimarchi, J. M., Fairchild, B., Verona, R., Moberg, K., Andon, N., and Lees, J. A. E2F-6, a member of the E2F family that can behave as a transcriptional repressor. Proc. Natl. Acad. Sci. USA, 95: 2850-2855, 1998.
19. Morkel, M., Wenkel, J., Bannister, A. J., Kouzarides, T., and Hagemeier, C. An E2F-like repressor of transcription. Nature (Lond.), 390: 567-568, 1997.
20. Friend, S. H., Bernards, R., Rogers, J., Weinberg, R. A., Rapin, A. M. C., Albert, D. M., and Dryja, T. P. A human DNA segment with properties of the gene that predisposes to retinoblastoma and osteosarcoma. Nature (Lond.), 323: 643-646, 1986.
21. 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.
22. Lee, E. Y. H. P., 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.
23. 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: 328-333, 1992.
24. Cobrinik, D., Lee, M-H., Hannon, G., Mulligan, G., Bronson, R. T., Dyson, N., Harlow, E., Beach, D., Weinberg, R. A., and Jacks, T. Shared role of the pRB-related p130 and p107 proteins in limb development. Genes Dev., 10: 1633-1644, 1996.
25. 1 cell state. Mol. Cell. Biol., 16: 6965-6976, 1996.
26. Dong, F., Cress, W. D., Jr., Agrawal, D., and Pledger, W. J. The role of cyclin D3-dependent kinase in the phosphorylation of p130 in mouse BALB/c 3T3 fibroblasts. J. Biol. Chem., 273: 6190-6195, 1998.
27. Smith, E. J., Leone, G., and Nevins, J. Distinct mechanisms control the accumulation of the Rb-related p107 and p130 proteins during cell growth. Cell Growth & Differ., 9: 297-303, 1998.
28. Clurman, B. E., Sheaff, R. J., Thress, K., Groudine, M., and Roberts, J. M. Turnover of cyclin E by the ubiquitin-proteasome pathway is regulated by cdk2 binding and cyclin phosphorylation. Genes Dev., 10: 1979-1990, 1996.
29. 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.
30. 1 cyclin complexes. Genes Dev., 9: 1340-1353, 1995.
31. 1 cyclin-associated kinases. Proc. Natl. Acad. Sci. USA, 93: 4633-4637, 1996.
32. 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.
33. ink4 requires functional retinoblastoma protein. Proc. Natl. Acad. Sci. USA, 92: 6289-6293, 1995.
34. 1 cyclins in the functional inactivation of the retinoblastoma protein. Genes Dev., 8: 1759-1771, 1994.
35. Dowdy, S. F., Hinds, P. W., Louie, K., Reed, S. I., Arnold, A., and Weinberg, R. A. Physical interaction of the retinoblastoma protein with human D cyclins. Cell, 73: 499-511, 1993.
36. 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.
37. 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.
38. Neuman, E., Flemington, E. K., Sellers, W. R., and Kaelin, W. G., Jr. Transcription of the E2F-1 gene is rendered cell cycle dependent by E2F DNA-binding sites within its promoter. Mol. Cell. Biol., 14: 6607-6615, 1994.
39. Zhu, L., Xie, E., and Chang, L-S. Differential roles of two tandem E2F sites in repression of the human p107 promoter by retinoblastoma and p107 proteins. Mol. Cell. Biol., 15: 3552-3562, 1995.
40. Shan, B., Chang, C-Y., Jones, D., and Lee, W-H. The transcription factor E2F-1 mediates the autoregulation of RB gene expression. Mol. Cell. Biol., 14: 299-309, 1994.
41. Buchkovich, K., Duffy, L. A., and Harlow, E. The retinoblastoma protein is phosphorylated during specific phases of the cell cycle. Cell, 58: 1097-1105, 1989.
42. Chen, P-L., Scully, P., Shew, J-Y., Wang, J. Y. J., and Lee, W-H. Phosphorylation of the retinoblastoma gene product is modulated during the cell cycle and cellular differentiation. Cell, 58: 1192-1198, 1989.
43. Furukawa, Y., DeCaprio, J. A., Freedman, A. X., Nakamura, M., Ernst, T. J., Livingston, D. M., and Griffin, J. D. Expression and state of phosphorylation of the retinoblastoma susceptibility gene product in cycling and noncycling human hematopoietic cells. Proc. Natl. Acad. Sci. USA, 87: 2770-2774, 1990.
44. Mihara, K., Cao, X-R., Yen, A., Chandler, S., Driscoll, B., Murphree, A. L., T'Ang, A., and Fung, Y-K. T. Cell cycle-dependent regulation of phosphorylation of the human retinoblastoma gene product. Science (Washington DC), 246: 1300-1303, 1989.
45. Mittnacht, S., Lees, J. A., Desai, D., Harlow, E., Morgan, D. O., and Weinberg, R. A. Distinct sub-populations of the retinoblastoma protein show a distinct pattern of phosphorylation. EMBO J., 13: 118-127, 1994.
46. 1 control in retinoblastoma gene-deficient cells independently of cdk4 activity. Mol. Cell. Biol., 15: 2600-2611, 1995.
47. Lundberg, A. S., and Weinberg, R. A. Functional inactivation of the retinoblastoma protein requires sequential modification by at least two distinct cyclin-cdk complexes. Mol. Cell. Biol., 18: 753-761, 1998.
48. Sears, R., Ohtani, K., and Nevins, J. R. Identification of positively and negatively acting elements regulating expression of the E2F2 gene in response to cell growth signals. Mol. Cell. Biol., 17: 5227-5235, 1997.
49. Dynlacht, B. D., Flores, O., Lees, J. A., and Harlow, E. Differential regulation of E2F trans-activation by cyclin/cdk2 complexes. Genes Dev., 8: 1772-1787, 1994.
50. 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.
51. 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.
52. Dynlacht, B. D., Moberg, K., Lees, J. A., Harlow, E., and Zhu, L. Specific regulation of E2F family members by cyclin-dependent kinases. Mol. Cell. Biol., 17: 3867-3875, 1997.
53. Hateboer, G., Kerkhoven, R. M., Shvarts, A., Bernards, R., and Beijersbergen, R. L. Degradation of E2F by the ubiquitin-proteasome pathway: regulation by retinoblastoma family proteins and adenovirus transforming proteins. Genes Dev., 10: 2960-2970, 1996.
54. Campanero, M. R., and Flemington, E. K. Regulation of E2F through ubiquitin-proteasome-dependent degradation: stabilization by the pRB tumor suppressor protein. Proc. Natl. Acad. Sci. USA, 94: 2221-2226, 1997.
55. Hofmann, F., Martelli, F., Livingston, D. M., and Wang, Z. The retinoblastoma gene product protects E2F-1 from degradation by the ubiquitin-proteasome pathway. Genes Dev., 10: 2949-2959, 1996.
56. Lindeman, G. J., Gaubatz, S., Livingston, D. M., and Ginsberg, D. The subcellular localization of E2F-4 is cell-cycle dependent. Proc. Natl. Acad. Sci. USA, 94: 5095-5100, 1997.
57. Verona, R., Moberg, K., Estes, S., Starz, M., Vernon, J. P., and Lees, J. A. E2F activity is regulated by cell cycle-dependent changes in subcellular localization. Mol. Cell. Biol., 17: 7268-7282, 1997.
58. Vairo, G., Livingston, D. M., and Ginsberg, D. Functional interaction between E2F-4 and p130: evidence for distinct mechanisms underlying growth suppression by different retinoblastoma protein family members. Genes Dev., 9: 869-881, 1995.
59. cdk2 is a component of the E2F-cyclin A complex. Cell, 68: 167-176, 1992.
60. 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 a cell cycle-regulated manner. Cell, 68: 157-166, 1992.
61. 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.
62. Smith, E. J., and Nevins, J. R. The Rb-related p107 protein can suppress E2F function independently of binding to cyclin A/cdk2. Mol. Cell. Biol., 15: 338-344, 1995.
63. Faha, B., Ewen, M. E., Tsai, L. H., Livingston, D. M., and Harlow, E. Interaction between human cyclin A and adenovirus E1A-associated p107 protein. Science (Washington DC), 255: 87-90, 1992.
64. 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.
65. Ikeda, M-A., 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.
66. Cobrinik, D., Whyte, P., Peeper, D. S., Jacks, T., and Weinberg, R. A. Cell cycle specific association of E2F with the p130 E1A-binding protein. Genes Dev., 7: 2392-2404, 1993.
67. Lee, M-H., Williams, B. O., Mulligan, G., Mukai, S., Bronson, R. T., Dyson, N., Harlow, E., and Jacks, T. Targeted disruption of p107: functional overlap between p107 and Rb. Genes Dev., 10: 1621-1632, 1996.
68. 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.
69. 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.
70. Qin, X-Q., Livingston, D. M., Kaelin, W. G., 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.
71. 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.
72. Johnson, D. G., Cress, W. D., Jakoi, L., and Nevins, J. R. Oncogenic capacity of the E2F1 gene. Proc. Natl. Acad. Sci. USA, 91: 12823-12827, 1994.
73. Xu, G., Livingston, D. M., and Krek, W. Multiple members of the E2F transcription factor family are the products of oncogenes. Proc. Natl. Acad. Sci. USA, 92: 1357-1361, 1995.
74. Pierce, A. M., Gimenez-Conti, I. B., Schneider-Broussard, R., Martinez, L. A., Conti, C. J., and Johnson, D. G. Increased E2F1 activity induces skin tumors in mice heterozygous and nullizygous for p53. Proc. Natl. Acad. Sci. USA, in press, 1998.
75. DeGregori, J., Leone, G., Miron, A., Jakoi, L., and Nevins, J. R. Distinct roles for E2F proteins in cell growth control and apoptosis. Proc. Natl. Acad. Sci. USA, 94: 7245-7250, 1997.
76. 1 cyclin-dependent kinase activity. Genes Dev., 9: 2873-2887, 1995.
77. 1-S regulatory genes. Mol. Cell. Biol., 15: 4215-4224, 1995.
78. Wu, X., and Levine, A. J. p53 and E2F-1 cooperate to mediate apoptosis. Proc. Natl. Acad. Sci. USA, 91: 3602-3606, 1994.
79. Kowalik, T. F., DeGregori, J., Schwarz, 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.
80. Kowalik, T. F., DeGregori, J., Leone, G., and Nevins, J. R. E2F1-specific induction of apoptosis and p53 accumulation is modulated by mdm2. Cell Growth Differ., 9: 113-118, 1998.
81. Field, S. J., Tsai, F-Y., Kuo, F., Zubiaga, A. M., Kaelin, W. G., Jr., Livingston, D. M., Orkin, S. H., and Greenberg, M. E. E2F-1 functions in mice to promote apoptosis and suppress proliferation. Cell, 85: 549-561, 1996.
82. Yamasaki, L., Jacks, T., Bronson, R., Goillot, E., Harlow, E., and Dyson, N. J. Tumor induction and tissue atrophy in mice lacking E2F-1. Cell, 85: 537-548, 1996.
83. 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.
84. Weintraub, S. J., Chow, K. N. B., Luo, R. X., Zhang, S. H., He, S., and Dean, D. C. Mechanism of active transcriptional repression by the retinoblastoma protein. Nature (Lond.), 375: 812-815, 1995.
85. Zwicker, J., Liu, N., Engeland, K., Lucibello, F. C., and Muller, R. Cell cycle regulation of E2F site occupation in vivo. Science (Washington DC), 271: 1595-1596, 1996.
86. Hurford, R. K., Jr., Cobrinik, D., Lee, M-H., and Dyson, N. pRB and p107/p130 are required for the regulated expression of different sets of E2F responsive genes. Genes Dev., 11: 1447-1463, 1997.
87. Leone, G., DeGregori, J., Van, Z., Jakoi, L., Ishida, S., Williams, R. S., and Nevins, J. R. E2F3 activity is regulated during the cell cycle and is required for the induction of S phase. Genes Dev., in press, 1998.
88. Hagemeier, C., Cook, A., and Kouzarides, T. The retinoblastoma protein binds E2F residues required for activation in vivo and TBP binding in vitro. Nucleic Acids Res., 21: 4998-5004, 1993.
89. Laherty, C. D., Yang, W-M., Sun, J-M., Davie, J. R., Seto, E., and Eisenman, R. N. Histone deacetylases associated with the mSin3 corepressor mediate mad transcriptional repression. Cell, 89: 349-356, 1997.
90. Nagy, L., Kao, H-Y., Chakravarti, D., Lin, R. J., Hassig, C. A., Ayer, D. E., Schreiber, S. L., and Evans, R. M. Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell, 89: 373-380, 1997.
91. Luo, R. X., Postigo, A. A., and Dean, D. C. Rb interacts with histone deacetylase to repress transcription. Cell, 92: 463-473, 1998.
92. Brehm, A., Miska, E. A., McCance, D. J., Reid, J. L., Bannister, A. J., and Kouzarides, T. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature (Lond.), 391: 597-601, 1998.
93. Magnaghi-Jaulin, L., Groisman, R., Naguibneva, I., Robin, P., Lorain, S., LeVillain, J. P., Troalen, F., Trouche, D., and Harel-Bellan, A. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature (Lond.), 391: 601-605, 1998.
94. Tevosian, S. G., Shih, H. H., Mendelson, K. G., Sheppard, K-A., Paulson, K. E., and Yee, A. S. HBP1: a HMG box transcriptional repressor that is targeted by the retinoblastoma family. Genes Dev., 11: 383-396, 1997.
95. Peeper, D. S., Upton, T. M., Ladha, M. H., Neuman, E., Zalvide, J., Bernards, R., DeCaprio, J. A., and Ewen, M. E. Ras signalling linked to the cell-cycle machinery by the retinoblastoma protein. Nature (Lond.), 386: 177-181, 1997.
96. Leone, G., DeGregori, J., Sears, R., Jakoi, L., and Nevins, J. R. Myc, and Ras collaborate in inducing accumulation of active cyclin E/Cdk2 and E2F. Nature (Lond.), 387: 422-426, 1997.
97. Kubbutat, M. H. G., Jones, S. N., and Vousden, K. H. Regulation of p53 stability by Mdm2. Nature (Lond.), 387: 299-302, 1997.
98. Haupt, Y., Maya, R., Kazaz, A., and Oren, M. Mdm2 promotes the rapid degradation of p53. Nature (Lond.), 387: 296-299, 1997.
99. Jones, S. N., Roe, A. E., Donehower, L. A., and Bradley, A. Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature (Lond.), 378: 206-208, 1995.
100. Montes de Oca Luna, R., Wagner, D. S., and Lozano, G. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature (Lond.), 378: 203-206, 1995.