RB family tumor suppressor activity may not relate to active silencing of E2F target genes

Cancer Research

Volumn 74, Issue 18, 2014, Pages 5266-5276

  Vormer, Tinke L ^a   Wojciechowicz, Kamila ^a   Dekker, Marleen ^a   De Vries, Sandra ^a   Van Der Wal, Anja ^a   Delzenne Goette, Elly ^a   Naik, Sjalin H ^a   Song, Ji Ying ^a   Dannenberg, Jan Hermen ^a   Hansen, Jacob B ^a,b   Te Riele, Hein ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR E2F;

ANIMAL; CELL GROWTH; GENE SILENCING; GENETIC TRANSFECTION; GENETICS; HUMAN; METABOLISM; MOUSE;

ANIMALS; CELL GROWTH PROCESSES; E2F TRANSCRIPTION FACTORS; GENE SILENCING; HUMANS; MICE; RETINOBLASTOMA PROTEIN; TRANSFECTION;

EID: 84907495493     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-3706     Document Type: Article

References (53)

1. DeGregori J, Johnson DG. Distinct and overlapping roles for E2F family members in transcription, proliferation and apoptosis. Curr Mol Med 2006;6:739-48.
2. Dimova DK, Dyson NJ. The E2F transcriptional network: old acquaintances with new faces. Oncogene 2005;24:2810-26.
3. Frolov MV, Dyson NJ. Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. J Cell Sci 2004;117:2173-8.
4. Dick FA. Structure-function analysis of the retinoblastoma tumor suppressor protein - is the whole a sum of its parts? Cell Div 2007;2:26.
5. Nielsen SJ, Schneider R, Bauer UM, Bannister AJ, Morrison A, O'Carroll D, et al. Rb targets histone H3 methylation and HP1 to promoters. Nature 2001;412:561-5.
6. Vandel L, Nicolas E, Vaute O, Ferreira R, it-Si-Ali S, Trouche D. Transcriptional repression by the retinoblastoma protein through the recruitment of a histone methyltransferase. Mol Cell Biol 2001;21:6484-94.
7. Magnaghi-Jaulin L, Groisman R, Naguibneva I, Robin P, Lorain S, Le Villain JP, et al. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature 1998;391:601-5.
8. Dannenberg JH, Schuijff L, Dekker M, van der Valk M, te Riele H. Tissue-specific tumor suppressor activity of retinoblastoma gene homologs p107 and p130. Genes Dev 2004;18:2952-62.
9. Harrison DJ, Hooper ML, Armstrong JF, Clarke AR. Effects of heterozygosity for the Rb-1t19neo allele in the mouse. Oncogene 1995;10:1615-20.
10. Maandag EC, van der Valk M, Vlaar M, Feltkamp C, O'Brien J, van Roon M, et al. Developmental rescue of an embryonic-lethal mutation in the retinoblastoma gene in chimeric mice. EMBO J 1994;13:4260-8.
11. Cam H, Dynlacht BD. Emerging roles for E2F: beyond the G1/S transition and DNA replication. Cancer Cell 2003;3:311-6.
12. Rayman JB, Takahashi Y, Indjeian VB, Dannenberg JH, Catchpole S, Watson RJ, et al. E2F mediates cell cycle-dependent transcriptional repression in vivo by recruitment of an HDAC1/mSin3B corepressor complex. Genes Dev 2002;16:933-47.
13. Takahashi Y, Rayman JB, Dynlacht BD. Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression. Genes Dev 2000;14:804-16.
14. Isaac CE, Francis SM, Martens AL, Julian LM, Seifried LA, Erdmann N, et al. The retinoblastoma protein regulates pericentric heterochromatin. Mol Cell Biol 2006;26:3659-71.
15. Morrison AJ, Sardet C, Herrera RE. Retinoblastoma protein transcriptional repression through histone deacetylation of a single nucleosome. Mol Cell Biol 2002;22:856-65.
16. Narita M, Nunez S, Heard E, Narita M, Lin AW, Hearn SA, et al. Rbmediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003;113:703-16.
17. Dahiya A, Wong S, Gonzalo S, Gavin M, Dean DC. Linking the Rb and polycomb pathways. Mol Cell 2001;8:557-69.
18. Nicolas E, Roumillac C, Trouche D. Balance between acetylation and methylation of histone H3 lysine 9 on the E2F-responsive dihydrofolate reductase promoter. Mol Cell Biol 2003;23:1614-22.
19. Ferreira R, Magnaghi-Jaulin L, Robin P, Harel-Bellan A, Trouche D. The three members of the pocket proteins family share the ability to repress E2F activity through recruitment of a histone deacetylase. Proc Natl Acad Sci U S A 1998;95:10493-8.
20. Vormer TL, Foijer F, Wielders CL, te Riele H. Anchorage-independent growth of pocket protein-deficient murine fibroblasts requires bypass of G2 arrest and can be accomplished by expression of TBX2. Mol Cell Biol 2008;28:7263-73.
21. Aarts M, Dekker M, de VS, van der Wal A, te Riele H. Generation of a mouse mutant by oligonucleotide-mediated gene modification in ES cells. Nucleic Acids Res 2006;34:e147.
22. Dannenberg JH, van Rossum A, Schuijff L, te Riele H. Ablation of the retinoblastoma gene family deregulates G (1) control causing immortalization and increased cell turnover under growth-restricting conditions. Genes Dev 2000;14:3051-64.
23. Lee JO, Russo AA, Pavletich NP. Structure of the retinoblastoma tumour-suppressor pocket domain bound to a peptide from HPV E7. Nature 1998;391:859-65.
24. Chen TT, Wang JY. Establishment of irreversible growth arrest in myogenic differentiation requires the RB LXCXE-binding function. Mol Cell Biol 2000;20:5571-80.
25. Dahiya A, Gavin MR, Luo RX, Dean DC. Role of the LXCXE binding site in Rb function. Mol Cell Biol 2000;20:6799-805.
26. Otterson GA, Chen W, Coxon AB, Khleif SN, Kaye FJ. Incomplete penetrance of familial retinoblastoma linked to germ-line mutations that result in partial loss of RB function. Proc Natl Acad Sci U S A 1997;94:12036-40.
27. Kaye FJ, Kratzke RA, Gerster JL, Horowitz JM. A single amino acid substitution results in a retinoblastoma protein defective in phosphorylation and oncoprotein binding. Proc Natl Acad Sci U S A 1990;87:6922-6.
28. Sellers WR, Rodgers JW, Kaelin WG Jr. A potent transrepression domain in the retinoblastoma protein induces a cell cycle arrest when bound to E2F sites. Proc Natl Acad Sci U S A 1995;92:11544-8.
29. Kratzke RA, Otterson GA, Hogg A, Coxon AB, Geradts J, Cowell JK, et al. Partial inactivation of the RB product in a family with incomplete penetrance of familial retinoblastoma and benign retinal tumors. Oncogene 1994;9:1321-6.
30. Sellers WR, Novitch BG, Miyake S, Heith A, Otterson GA, Kaye FJ, et al. Stable binding to E2F is not required for the retinoblastoma protein to activate transcription, promote differentiation, and suppress tumor cell growth. Genes Dev 1998;12:95-106.
31. Muller H, Moroni MC, Vigo E, Petersen BO, Bartek J, Helin K. Induction of S-phase entry by E2F transcription factors depends on their nuclear localization. Mol Cell Biol 1997;17:5508-20.
32. Brugarolas J, Moberg K, Boyd SD, Taya Y, Jacks T, Lees JA. Inhibition of cyclin-dependent kinase 2 by p21 is necessary for retinoblastoma protein-mediated G1 arrest after gamma-irradiation. Proc Natl Acad Sci U S A 1999;96:1002-7.
33. Bourgo RJ, Thangavel C, Ertel A, Bergseid J, McClendon AK, Wilkens L, et al. RB restricts DNA damage-initiated tumorigenesis through an LXCXE-dependent mechanism of transcriptional control. Mol Cell 2011;43:663-72.
34. Peeper DS, Dannenberg JH, Douma S, te Riele H, Bernards R. Escape from premature senescence is not sufficient for oncogenic transformation by Ras. Nat Cell Biol 2001;3:198-203.
35. Ciemerych MA, Sicinski P. Cell cycle in mouse development. Oncogene 2005;24:2877-98.
36. Robanus-Maandag E, Dekker M, van der Valk M, Carrozza ML, Jeanny JC, Dannenberg JH, et al. p107 is a suppressor of retinoblastoma development in pRb-deficient mice. Genes Dev 1998;12:1599-609.
37. Viatour P, Somervaille TC, Venkatasubrahmanyam S, Kogan S, McLaughlin ME, Weissman IL, et al. Hematopoietic stem cell quiescence is maintained by compound contributions of the retinoblastoma gene family. Cell Stem Cell 2008;3:416-28.
38. Walkley CR, Shea JM, Sims NA, Purton LE, Orkin SH. Rb regulates interactions between hematopoietic stem cells and their bone marrow microenvironment. Cell 2007;129:1081-95.
39. Pennaneach V, Salles-Passador I, Munshi A, Brickner H, Regazzoni K, Dick F, et al. The large subunit of replication factor C promotes cell survival after DNA damage in an LxCxE motif- and Rb-dependent manner. Mol Cell 2001;7:715-27.
40. Hertel L, Rolle S, DeAndrea M, Azzimonti B, Osello R, Gribaudo G, et al. The retinoblastoma protein is an essential mediator that links the interferon-inducible 204 gene to cell-cycle regulation. Oncogene 2000;19:3598-608.
41. Binne UK, Classon MK, Dick FA, Wei W, Rape M, Kaelin WG Jr., et al. Retinoblastoma protein and anaphase-promoting complex physically interact and functionally cooperate during cell-cycle exit. Nat Cell Biol 2007;9:225-32.
42. Rowland BD, Denissov SG, Douma S, Stunnenberg HG, Bernards R, Peeper DS. E2Ftranscriptional repressor complexes are critical downstream targets of p19 (ARF)/p53-induced proliferative arrest. Cancer Cell 2002;2:55-65.
43. Francis SM, Chakrabarti S, Dick FA. A context-specific role for retinoblastoma protein-dependent negative growth control in suppressing mammary tumorigenesis. PLoS ONE 2011;6:e16434.
44. Talluri S, Francis SM, Dick FA. Mutation of the LXCXE binding cleft of pRb facilitates transformation by ras in vitro but does not promote tumorigenesis in vivo. PLoS ONE 2013;8:e72236.
45. Gaubatz S, Lindeman GJ, Ishida S, Jakoi L, Nevins JR, Livingston DM, et al. E2F4 and E2F5 play an essential role in pocket protein-mediated G1 control. Mol Cell 2000;6:729-35.
46. Cobrinik D, Lee MH, Hannon G, Mulligan G, Bronson RT, Dyson N, et al. Shared role of the pRB-related p130 and p107 proteins in limb development. Genes Dev 1996;10:1633-44.
47. Scime A, Grenier G, Huh MS, Gillespie MA, Bevilacqua L, Harper ME, et al. Rb and p107 regulate preadipocyte differentiation into white versus brown fat through repression of PGC-1alpha. Cell Metab 2005;2:283-95.
48. Hansen JB, Jorgensen C, Petersen RK, Hallenborg P, De MR, Boye HA, et al. Retinoblastoma protein functions as a molecular switch determining white versus brown adipocyte differentiation. Proc Natl Acad Sci U S A 2004;101:4112-7.
49. Coschi CH, Martens AL, Ritchie K, Francis SM, Chakrabarti S, Berube NG, et al. Mitotic chromosome condensation mediated by the retinoblastoma protein is tumor-suppressive. Genes Dev 2010;24:1351-63.
50. Manning AL, Longworth MS, Dyson NJ. Loss of pRB causes centromere dysfunction and chromosomal instability. Genes Dev 2010;24:1364-76.
51. Chong J-L, Wenzel PL, Sáenz-Robles MT, Nair V, Ferrey A, Hagan JP, et al. E2F1-3 switch from activators in progenitor cells to repressors in differentiating cells. Nature 2009;462:930-4.
52. Chen D, Pacal M, Wenzel P, Knoepfler PS, Leone G, Bremner R. Division and apoptosis in the E2f-deficient retina. Nature 2009;462:925-9.
53. Wenzel PL, Chong JL, Sáenz-Robles MT, Ferrey A, Hagan JP, Gomez YM, et al. Proliferation in the absence of E2F1-3. Dev Biol 2011;351:35-45.