Regulation of RB transcription in vivo by RB family members

Molecular and Cellular Biology

Volumn 30, Issue 7, 2010, Pages 1729-1745

  Burkhart, Deborah L ^a,c   Ngai, Lynn K ^a   Roake, Caitlin M ^a   Viatour, Patrick ^a   Thangavel, Chellappagounder ^b   Ho, Victoria M ^a,d   Knudsen, Erik S ^b   Sage, Julien ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR E2F; TUMOR SUPPRESSOR PROTEIN;

ADULT; ALLELE; ANIMAL CELL; ARTICLE; AUTOREGULATION; CELL CULTURE; CELL CYCLE PROGRESSION; CONTROLLED STUDY; DEREGULATION; EGFP GENE; FEEDBACK SYSTEM; GENE EXPRESSION; GENE FUNCTION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IN VIVO STUDY; MOUSE; NONHUMAN; P107 GENE; P130 GENE; PRIORITY JOURNAL; RB GENE; TRANSGENE; TUMOR SUPPRESSOR GENE;

ANIMALS; CELL CYCLE; E2F TRANSCRIPTION FACTORS; EMBRYO, MAMMALIAN; GENES, REPORTER; HUMANS; MICE; MICE, TRANSGENIC; NIH 3T3 CELLS; PROMOTER REGIONS, GENETIC; RECOMBINANT FUSION PROTEINS; RETINOBLASTOMA PROTEIN; RETINOBLASTOMA-LIKE PROTEIN P107; RETINOBLASTOMA-LIKE PROTEIN P130; TISSUE DISTRIBUTION; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

BACTERIA (MICROORGANISMS); MAMMALIA; MUS;

EID: 77949408525     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00952-09     Document Type: Article

References (58)

1. Agromayor, M., E. Wloga, B. Naglieri, J. Abrashkin, K. Verma, and L. Yamasaki. 2006. Visualizing dynamic E2F-mediated repression in vivo. Mol. Cell. Biol. 26:4448-4461.
2. Balciunaite, E., A. Spektor, N. H. Lents, H. Cam, H. Te Riele, A. Scime, M. A. Rudnicki, R. Young, and B. D. Dynlacht. 2005. Pocket protein complexes are recruited to distinct targets in quiescent and proliferating cells. Mol. Cell. Biol. 25:8166-8178.
3. Benedict, W. F., S. P. Lerner, J. Zhou, X. Shen, H. Tokunaga, and B. Czerniak. 1999. Level of retinoblastoma protein expression correlates with p16 (MTS-1/INK4A/CDKN2) status in bladder cancer. Oncogene 18:1197-1203.
4. Bookstein, R., P. Rio, S. A. Madreperla, F. Hong, C. Allred, W. E. Grizzle, and W. H. Lee. 1990. Promoter deletion and loss of retinoblastoma gene expression in human prostate carcinoma. Proc. Natl. Acad. Sci. U. S. A. 87:7762-7766.
5. Botos, J., R. Smith III, and D. T. Kochevar. 2002. Retinoblastoma function is a better indicator of cellular phenotype in cultured breast adenocarcinoma cells than retinoblastoma expression. Exp. Biol. Med. (Maywood) 227:354-362.
6. Braden, W. A., A. K. McClendon, and E. S. Knudsen. 2008. Cyclin-dependent kinase 4/6 activity is a critical determinant of pre-replication complex assembly. Oncogene 27:7083-7093.
7. Burkhart, D. L., and J. Sage. 2008. Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat. Rev. Cancer. 8:671-682.
8. Burkhart, D. L., P. Viatour, V. M. Ho, and J. Sage. 2008. GFP reporter mice for the retinoblastoma-related cell cycle regulator p107. Cell Cycle 7:2544-2552.
9. Chen, H. Z., S. Y. Tsai, and G. Leone. 2009. Emerging roles of E2Fs in cancer: an exit from cell cycle control. Nat. Rev. Cancer 9:785-797.
10. Classon, M., and N. Dyson. 2001. p107 and p130: versatile proteins with interesting pockets. Exp. Cell Res. 264:135-147.
11. Cordon-Cardo, C., and V. M. Richon. 1994. Expression of the retinoblastoma protein is regulated in normal human tissues. Am. J. Pathol. 144:500-510.
12. De Falco, G., F. Comes, and C. Simone. 2006. pRb: master of differentiation. Coupling irreversible cell cycle withdrawal with induction of muscle-specific transcription. Oncogene 25:5244-5249.
13. DeGregori, J., T. Kowalik, and J. R. Nevins. 1995. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/S-regulatory genes. Mol. Cell. Biol. 15:4215-4224.
14. Deléhouzée, S., T. Yoshikawa, C. Sawa, J. Sawada, T. Ito, M. Omori, T. Wada, Y. Yamaguchi, Y. Kabe, and H. Handa. 2005. GABP, HCF-1 and YY1 are involved in Rb gene expression during myogenesis. Genes Cells 10:717-731.
15. Di Fiore, B., A. Palena, A. Felsani, F. Palitti, M. Caruso, and P. Lavia. 1999. Cytosine methylation transforms an E2F site in the retinoblastoma gene promoter into a binding site for the general repressor methylcytosine-binding protein 2 (MeCP2). Nucleic Acids Res. 27:2852-2859.
16. Donovan, S. L., B. Schweers, R. Martins, D. Johnson, and M. A. Dyer. 2006. Compensation by tumor suppressor genes during retinal development in mice and humans. BMC Biol. 4:14.
17. Dunn, J. M., R. A. Phillips, X. Zhu, A. Becker, and B. L. Gallie. 1989. Mutations in the RB1 gene and their effects on transcription. Mol. Cell. Biol. 9:4596-4604.
18. Fujita, T., N. Ohtani-Fujita, and T. Sakai. 1996. Identification of an RB-responsive region in the 5′ untranslated region of the RB gene. Cancer Lett. 101:149-157.
19. Gill, R. M., P. A. Hamel, J. Zhe, E. Zacksenhaus, B. L. Gallie, and R. A. Phillips. 1994. Characterization of the human RB1 promoter and of elements involved in transcriptional regulation. Cell Growth Differ. 5:467-474.
20. Gope, M. L., M. Chun, and R. Gope. 1991. Comparative study of the expression of Rb and p53 genes in human colorectal cancers, colon carcinoma cell lines and synchronized human fibroblasts. Mol. Cell. Biochem. 107:55-63.
21. Guo, J., Y. Miao, B. Xiao, R. Huan, Z. Jiang, D. Meng, and Y. Wang. 2009. Differential expression of microRNA species in human gastric cancer versus non-tumorous tissues. J. Gastroenterol. Hepatol. 24:652-657.
22. Hamel, P. A., R. M. Gill, R. A. Phillips, and B. L. Gallie. 1992. 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.
23. Hateboer, G., A. Wobst, B. O. Petersen, L. Le Cam, E. Vigo, C. Sardet, and K. Helin. 1998. Cell cycle-regulated expression of mammalian CDC6 is dependent on E2F. Mol. Cell. Biol. 18:6679-6697.
24. Jiang, Z., Z. Guo, F. A. Saad, J. Ellis, and E. Zacksenhaus. 2001. Retinoblastoma gene promoter directs transgene expression exclusively to the nervous system. J. Biol. Chem. 276:593-600.
25. Jiang, Z., E. Zacksenhaus, B. L. Gallie, and R. A. Phillips. 1997. The retinoblastoma gene family is differentially expressed during embryogenesis. Oncogene 14:1789-1797.
26. Kim, S. J., U. S. Onwuta, Y. I. Lee, R. Li, M. R. Botchan, and P. D. Robbins. 1992. The retinoblastoma gene product regulates Sp1-mediated transcription. Mol. Cell. Biol. 12:2455-2463.
27. Kim, S. J., S. Wagner, F. Liu, M. A. O'Reilly, P. D. Robbins, and M. R. Green. 1992. Retinoblastoma gene product activates expression of the human TGF-beta 2 gene through transcription factor ATF-2. Nature 358:331-334.
28. LeCouter, J. E., B. Kablar, W. R. Hardy, C. Ying, L. A. Megeney, L. L. May, and M. A. Rudnicki. 1998. Strain-dependent myeloid hyperplasia, growth deficiency, and accelerated cell cycle in mice lacking the Rb-related p107 gene. Mol. Cell. Biol. 18:7455-7465.
29. LeCouter, J. E., B. Kablar, P. F. Whyte, C. Ying, and M. A. Rudnicki. 1998. Strain-dependent embryonic lethality in mice lacking the retinoblastoma-related p130 gene. Development 125:4669-4679.
30. Matsumoto, T., N. Ohtani-Fujita, Y. Sowa, F. Bai, T. Nikaido, T. Tamaki, and T. Sakai. 1998. Cell cycle-dependent modulation of promoter activities of RB and WAF1/Cip1 genes. Jpn. J. Cancer Res. 89:626-633.
31. Mercader, J., J. Ribot, I. Murano, S. Feddersen, S. Cinti, L. Madsen, K. Kristiansen, M. L. Bonet, and A. Palou. 2009. Haploinsufficiency of the retinoblastoma protein gene reduces diet-induced obesity, insulin resistance, and hepatosteatosis in mice. Am. J. Physiol. Endocrinol. Metab. 297:E184-E193.
32. Nikitin, A., B. Shan, A. Flesken-Nikitin, K. H. Chang, and W. H. Lee. 2001. The retinoblastoma gene regulates somatic growth during mouse development. Cancer Res. 61:3110-3118.
33. Ohtani-Fujita, N., T. Fujita, R. Takahashi, P. D. Robbins, T. P. Dryja, and T. Sakai. 1994. A silencer element in the retinoblastoma tumor-suppressor gene. Oncogene 9:1703-1711.
34. Osifchin, N. E., D. Jiang, N. Ohtani-Fujita, T. Fujita, M. Carroza, S. J. Kim, T. Sakai, and P. D. Robbins. 1994. Identification of a p53 binding site in the human retinoblastoma susceptibility gene promoter. J. Biol. Chem. 269: 6383-6389.
35. Park, K., J. Choe, N. E. Osifchin, D. J. Templeton, P. D. Robbins, and S. J. Kim. 1994. The human retinoblastoma susceptibility gene promoter is positively autoregulated by its own product. J. Biol. Chem. 269:6083- 6088.
36. Passegué, E., A. J. Wagers, S. Giuriato, W. C. Anderson, and I. L. Weissman. 2005. Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J. Exp. Med. 202:1599-1611.
37. Porrello, A., M. A. Cerone, S. Coen, A. Gurtner, G. Fontemaggi, L. Cimino, G. Piaggio, A. Sacchi, and S. Soddu. 2000. p53 regulates myogenesis by triggering the differentiation activity of pRb. J. Cell Biol. 151:1295-1304.
38. Roesch, A., B. Becker, S. Meyer, C. Hafner, P. J. Wild, M. Landthaler, and T. Vogt. 2005. Overexpression and hyperphosphorylation of retinoblastoma protein in the progression of malignant melanoma. Mod. Pathol. 18:565-572.
39. Sage, J., A. L. Miller, P. A. Perez-Mancera, J. M. Wysocki, and T. Jacks. 2003. Acute mutation of retinoblastoma gene function is sufficient for cell cycle re-entry. Nature 424:223-228.
40. Sage, J., G. J. Mulligan, L. D. Attardi, A. Miller, S. Chen, B. Williams, E. Theodorou, and T. Jacks. 2000. Targeted disruption of the three Rb-related genes leads to loss of G(1) control and immortalization. Genes Dev. 14: 3037-3050.
41. Sakai, T., N. Ohtani, T. L. McGee, P. D. Robbins, and T. P. Dryja. 1991. Oncogenic germ-line mutations in Sp1 and ATF sites in the human retino-blastoma gene. Nature 353:83-86.
42. Sankaran, V. G., S. H. Orkin, and C. R. Walkley. 2008. Rb intrinsically promotes erythropoiesis by coupling cell cycle exit with mitochondrial biogenesis. Genes Dev. 22:463-475.
43. Shan, B., C. Y. Chang, D. Jones, and W. H. Lee. 1994. The transcription factor E2F-1 mediates the autoregulation of RB gene expression. Mol. Cell. Biol. 14:299-309.
44. Sherr, C. J., and F. McCormick. 2002. The RB and p53 pathways in cancer. Cancer Cell 2:103-112.
45. Spencer, C., S. Pajovic, H. Devlin, Q. D. Dinh, T. W. Corson, and B. L. Gallie. 2005. Distinct patterns of expression of the RB gene family in mouse and human retina. Gene Expr. Patterns 5:687-694.
46. Spike, B. T., A. Dirlam, B. C. Dibling, J. Marvin, B. O. Williams, T. Jacks, and K. F. Macleod. 2004. The Rb tumor suppressor is required for stress erythropoiesis. EMBO J. 23:4319-4329.
47. Stengel, K. R., C. Thangavel, D. A. Solomon, S. P. Angus, Y. Zheng, and E. S. Knudsen. 2009. Retinoblastoma/p107/p130 pocket proteins: protein dynamics and interactions with target gene promoters. J. Biol. Chem. 284:19265-19271.
48. Takahashi, Y., J. Rayman, and B. Dynlacht. 2000. Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression. Genes Dev. 14:804-816.
49. Trimarchi, J. M., and J. A. Lees. 2002. Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell Biol. 3:11-20.
50. Vandromme, M., C. Chailleux, F. Escaffit, and D. Trouche. 2008. Binding of the retinoblastoma protein is not the determinant for stable repression of some E2F-regulated promoters in muscle cells. Mol. Cancer Res. 6:418-425.
51. Ventura, A., D. G. Kirsch, M. E. McLaughlin, D. A. Tuveson, J. Grimm, L. Lintault, J. Newman, E. E. Reczek, R. Weissleder, and T. Jacks. 2007. Restoration of p53 function leads to tumour regression in vivo. Nature 445:661-665.
52. Viatour, P., T. C. Somervaille, S. Venkatasubrahmanyam, S. Kogan, M. E. McLaughlin, I. L. Weissman, A. J. Butte, E. Passegue, and J. Sage. 2008. Hematopoietic stem cell quiescence is maintained by compound contributions of the retinoblastoma gene family. Cell Stem Cell 3:416-428.
53. Walkley, C. R., and S. H. Orkin. 2006. Rb is dispensable for self-renewal and multilineage differentiation of adult hematopoietic stem cells. Proc. Natl. Acad. Sci. U. S. A. 103:9057-9062.
54. Walkley, C. R., J. M. Shea, N. A. Sims, L. E. Purton, and S. H. Orkin. 2007. Rb regulates interactions between hematopoietic stem cells and their bone marrow microenvironment. Cell 129:1081-1095.
55. Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
56. Wells, J., and P. J. Farnham. 2002. Characterizing transcription factor binding sites using formaldehyde crosslinking and immunoprecipitation. Methods 26:48-56.
57. Zheng, L., A. Flesken-Nikitin, P. L. Chen, and W. H. Lee. 2002. Deficiency of retinoblastoma gene in mouse embryonic stem cells leads to genetic instability. Cancer Res. 62:2498-2502.
58. Zhu, L., E. Xie, and L. S. Chang. 1995. 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.