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DREAM complex

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MuvB factors also revealed association of BMYB. Subsequent immunoprecipitation with BMYB yielded all the MuvB core proteins, but not other members of the DREAM complex – p130, p107, E2F4/5 and DP. This indicated that MuvB associated with BMYB to form the BMYB-MuvB complex or with p130/p107, E2F4/5 and DP to form the DREAM complex. The DREAM complex was found prevalent in quiescent or starved cells, and the BMYB-MuvB complex was found in actively dividing cells, hinting at separate functionalities of these two complexes.
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degraded and E2F4 exported from the nucleus. Once the repressive E2Fs are vacated, activating E2Fs bind to the promoter to up-regulate G1/S genes that promote DNA synthesis and transition of the cell cycle. BMYB is also up-regulated during this time, which then binds to genes that peak at G2/M phase. Binding of BMYB to late cell cycle genes is dependent on its association with the MuvB core to form the BMYB-MuvB complex, which is then able to up-regulate genes in the G2/M phase.
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via E2F proteins binding to sequences known as cell cycle-dependent element sites (CDEs). Some cell cycle dependent genes have been found where both CHRs and CDEs are in proximity to one another. Because p130-E2F4 can form stable associations with the MuvB complex, the proximity of CHRs to CDEs suggests that affinity of binding of the DREAM complex to target genes is cooperatively improved by association with both the binding sites.
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Docking of the DREAM complex to promoters is achieved by binding of LIN-54 to regions known as cell cycle genes homology region (CHR). These are specific sequence of nucleotides that are commonly found in the promoters of genes expressed during late S phase or G2/M phase. Docking can also be achieved
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Other components have been shown to be phosphorylated for DREAM complex assembly to occur. Of these, LIN52 phosphorylation on its S28 residue is the most well-understood. Substitution of this serine to alanine led to reduced binding of the MuvB core to p130 and impaired the ability of cells to enter
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The mammalian DREAM complex was identified following immunoprecipitation of p130 with mass-spectrometry analysis. The results showed that p130 was associated with E2F4, E2F5, the dimerization partner DP, and LIN9, LIN54, LIN37, LIN52, and RBBP4 that make up the MuvB complex. Immunoprecipitation of
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Like its counterpart, RB-E2F, the DREAM complex is also affected by similar growth stimuli and subsequent cyclin-CDK activity. Increasing cyclin D-CDK4 and cyclin E-CDK2 activity dissociates the DREAM complex from the promoter by phosphorylation of p130. Hyper-phosphorylated p130 is subsequently
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phase. Abrogation of the DREAM complex on the other hand, led to increased expression of E2F regulated genes normally repressed in the G0 phase. Contrary to mammalian cells, the fly dREAM complex was found at almost one-third of all promoters, which may reflect a broader role for dREAM in gene
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ovarian follicle cells identified a protein complex that bound to repeatedly amplifying chorion genes. The complex included genes that had close homology with the MuvB genes such as Mip130, Mip120 and Mip40. These Mip genes were identified as homologues of the MuvB genes LIN9, LIN54, and LIN37
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Kobayashi, K; Suzuki, T; Iwata, E; Nakamichi, N; Suzuki, T; Chen, P; Ohtani, M; Ishida, T; Hosoya, H; Müller, S; Leviczky, T; Pettkó-Szandtner, A; Darula, Z; Iwamoto, A; Nomoto, M; Tada, Y; Higashiyama, T; Demura, T; Doonan, JH; Hauser, MT; Sugimoto, K; Umeda, M; Magyar, Z; Bögre, L; Ito, M
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Lang, Lucas; Pettkó-Szandtner, Aladár; Tunçay Elbaşı, Hasibe; Takatsuka, Hirotomo; Nomoto, Yuji; Zaki, Ahmad; Dorokhov, Stefan; De Jaeger, Geert; Eeckhout, Dominique; Ito, Masaki; Magyar, Zoltán; Bögre, László; Heese, Maren; Schnittger, Arp (December 2021).
237:. Therefore, unlike RB-E2F, the DREAM complex is unlikely to directly recruit chromatin modifiers to repress gene expression, although some associations have been suggested. DREAM complex may instead down-regulate gene expression by affecting 286:. The loss of this kinase leads to decreased phosphorylation of the S28 residue and association of p130 with MuvB. DYRK1A was also found to degrade cyclin D1, which would increase p21 levels – both of which contribute to cell cycle exit. 1946:
Boichuk, S.; Parry, J. A.; Makielski, K. R.; Litovchick, L.; Baron, J. L.; Zewe, J. P.; Wozniak, A.; Mehalek, K. R.; Korzeniewski, N.; Seneviratne, D. S.; Schoffski, P.; Debiec-Rychter, M.; DeCaprio, J. A.; Duensing, A. (20 June 2013).
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respectively. Further studies in the fly embryo nuclear extracts confirmed the coexistence of these proteins with others such as the RB homologues Rbf1 and Rbf2, and others like E2f and Dp. The protein complex was thus termed as the
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Stiegler, P; De Luca, A; Bagella, L; Giordano, A (1998-11-15). "The COOH-terminal region of pRb2/p130 binds to histone deacetylase 1 (HDAC1), enhancing transcriptional repression of the E2F-dependent cyclin A promoter".
245:. In worms for example, loss of a MuvB complex protein, LIN35, leads to loss of repressive histone associations and high expression of cell cycle dependent genes. However, direct evidence for the link between repressive 282:
quiescence. This indicates that LIN52 S28 phosphorylation is required for proper association and function of the DREAM complex via binding with p130. One known regulator of phosphorylation of the S28 residue is the
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Forristal, C; Henley, SA; MacDonald, JI; Bush, JR; Ort, C; Passos, DT; Talluri, S; Ishak, CA; Thwaites, MJ; Norley, CJ; Litovchick, L; DeCaprio, JA; DiMattia, G; Holdsworth, DW; Beier, F; Dick, FA (June 2014).
138:). Entry into the cell cycle dissociates p130 from the complex and leads to subsequent recruitment of activating E2F proteins. This allows for the expression of E2F regulated late G1 and S phase genes. BMYB ( 72:. When mutated, these genes produced worms with multiple vulva-like organs, hence the name ‘Muv’. Three classes of Muv genes were classified, with class B genes encoding homologues of mammalian RB, 436:
Beitel, GJ; Lambie, EJ; Horvitz, HR (2000-08-22). "The C. elegans gene lin-9, which acts in an Rb-related pathway, is required for gonadal sheath cell development and encodes a novel protein".
24:-dependent gene expression. The complex is evolutionarily conserved, although some of its components vary from species to species. In humans, the key proteins in the complex are 96:, there was also found a testis-specific paralog of the Myb-MuvB/DREAM complex known as tMAC (testis-specific meiotic arrest complex), which is involved in meiotic arrest. 92:
of the components of dREAM complex led to higher expression of E2f regulated genes that are typically silenced, implicating dREAM’s role in gene down-regulation. Later in
1229:"Deletion of the p107/p130-binding domain of Mip130/LIN-9 bypasses the requirement for CDK4 activity for the dissociation of Mip130/LIN-9 from p107/p130-E2F4 complex" 278:. Inhibition of PP2a activity reduced promoter binding of some of the proteins of the DREAM complex in the subsequent G1 phase and de-repression of gene expression. 103:
extract containing DP, RB, and MuvB, and was named as DRM. This complex included mammalian homologues of RB and DP, and other members of the MuvB complex.
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Naetar, N; Soundarapandian, V; Litovchick, L; Goguen, KL; Sablina, AA; Bowman-Colin, C; Sicinski, P; Hahn, WC; DeCaprio, JA; Livingston, DM (2014-06-19).
986:"Genomic profiling and expression studies reveal both positive and negative activities for the Drosophila Myb MuvB/dREAM complex in proliferating cells" 1082:
Müller, GA; Engeland, K (February 2010). "The central role of CDE/CHR promoter elements in the regulation of cell cycle-dependent gene transcription".
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Rashid, NN; Yusof, R; Watson, RJ (November 2014). "A B-myb--DREAM complex is not critical to regulate the G2/M genes in HPV-transformed cell lines".
1035:"The dREAM/Myb–MuvB complex and Grim are key regulators of the programmed death of neural precursor cells at the Drosophila posterior wing margin" 675:"Some C. elegans class B synthetic multivulva proteins encode a conserved LIN-35 Rb-containing complex distinct from a NuRD-like complex" 739:
Litovchick, L; Sadasivam, S; Florens, L; Zhu, X; Swanson, SK; Velmurugan, S; Chen, R; Washburn, MP; Liu, XS; DeCaprio, JA (2007-05-25).
577:"Native E2F/RBF complexes contain Myb-interacting proteins and repress transcription of developmentally controlled E2F target genes" 575:
Korenjak, M; Taylor-Harding, B; Binné, UK; Satterlee, JS; Stevaux, O; Aasland, R; White-Cooper, H; Dyson, N; Brehm, A (2004-10-15).
741:"Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence" 1390:"The pRb-related protein p130 is regulated by phosphorylation-dependent proteolysis via the protein-ubiquitin ligase SCF(Skp2)" 984:
Georlette, D; Ahn, S; MacAlpine, DM; Cheung, E; Lewis, PW; Beall, EL; Bell, SP; Speed, T; Manak, JR; Botchan, MR (2007-11-15).
1537:"Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression" 1584:
Lam, EW; Robinson, C; Watson, RJ (September 1992). "Characterization and cell cycle-regulated expression of mouse B-myb".
210: 29: 25: 1949:"The DREAM Complex Mediates GIST Cell Quiescence and Is a Novel Therapeutic Target to Enhance Imatinib-Induced Apoptosis" 301:
Due to its regulatory role in the cell cycle, targeting the DREAM complex might enhance anticancer treatments such as
524:; Botchan, MR (2002-12-19). "Role for a Drosophila Myb-containing protein complex in site-specific DNA replication". 1809:"Dosage of Dyrk1a shifts cells within a p21-cyclin D1 signaling map to control the decision to enter the cell cycle" 1339:
Latorre, I; Chesney, MA; Garrigues, JM; Stempor, P; Appert, A; Francesconi, M; Strome, S; Ahringer, J (2015-03-01).
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Near the end of mitosis, p130 and p107 are dephosphorylated from their hyperphosphorylated state by the phosphatase
2021: 218: 127: 1711:"PP2A: more than a reset switch to activate pRB proteins during the cell cycle and in response to signaling cues" 473:"New genes that interact with lin-35 Rb to negatively regulate the let-60 ras pathway in Caenorhabditis elegans" 2031: 233:
When DREAM is docked onto the promoter, p130 is bound to LIN52, and this association inhibits LIN52 binding to
193:. Near the end of the cell cycle, the DREAM complex is re-assembled by DYRK1A to repress G1/S and G2/M genes. 1856:
Wolter, P; Schmitt, K; Fackler, M; Kremling, H; Probst, L; Hauser, S; Gruss, OJ; Gaubatz, S (15 May 2012).
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positioning. Compacted DNA at transcription start sites inhibit gene expression by blocking the docking of
33: 1760:"PP2A-mediated regulation of Ras signaling in G2 is essential for stable quiescence and normal G1 length" 76:, and DP1, and others such as LIN-54, LIN-37, LIN-7 and LIN-52, whose functions were not yet understood. 314: 275: 223: 1858:"GAS2L3, a target gene of the DREAM complex, is required for proper cytokinesis and genomic stability" 686: 533: 234: 68:
Genes encoding the MuvB complex were originally identified from loss-of-function mutation studies in
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During quiescence, the DREAM complex represses G1/S and G2/M gene expression. In mammalian systems,
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studies have revealed that DREAM components are found together at promoters of genes that peak in
1899:"The DREAM complex in antitumor activity of imatinib mesylate in gastrointestinal stromal tumors" 1691: 1662:"PP1 and PP2A phosphatases--cooperating partners in modulating retinoblastoma protein activation" 1642: 1468: 1107: 606: 557: 418: 626:"Discovery of tMAC: a Drosophila testis-specific meiotic arrest complex paralogous to Myb-Muv B" 196: 1613:"Mip/LIN-9 regulates the expression of B-Myb and the induction of cyclin A, cyclin B, and CDK1" 1033:
Rovani, Margritte K.; Brachmann, Carrie Baker; Ramsay, Gary; Katzen, Alisa L. (December 2012).
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Beall, E. L.; Lewis, P. W.; Bell, M.; Rocha, M.; Jones, D. L.; Botchan, M. R. (15 April 2007).
2000: 1970: 1928: 1879: 1838: 1789: 1740: 1683: 1634: 1593: 1566: 1517: 1460: 1439:"SKP2 associates with p130 and accelerates p130 ubiquitylation and degradation in human cells" 1419: 1370: 1321: 1286: 1258: 1209: 1157: 1099: 1064: 1015: 966: 914: 862: 812: 762: 714: 655: 598: 549: 502: 453: 410: 369: 1960: 1918: 1910: 1869: 1828: 1820: 1779: 1771: 1730: 1722: 1673: 1624: 1556: 1548: 1507: 1499: 1450: 1409: 1401: 1360: 1352: 1313: 1248: 1240: 1199: 1191: 1147: 1139: 1091: 1054: 1046: 1005: 997: 956: 948: 904: 896: 852: 844: 802: 794: 752: 704: 694: 645: 637: 588: 541: 492: 484: 445: 400: 359: 351: 89: 885:"The MuvB complex sequentially recruits B-Myb and FoxM1 to promote mitotic gene expression" 252: 1178:
Guiley, KZ; Liban, TJ; Felthousen, JG; Ramanan, P; Litovchick, L; Rubin, SM (2015-05-01).
214: 123: 937:"DYRK1A protein kinase promotes quiescence and senescence through DREAM complex assembly" 690: 537: 1923: 1898: 1833: 1808: 1784: 1759: 1735: 1710: 1365: 1340: 1253: 1228: 1204: 1179: 1152: 1127: 1059: 1034: 1010: 985: 961: 936: 909: 884: 857: 832: 807: 782: 709: 674: 650: 625: 497: 472: 364: 339: 242: 1561: 1536: 1414: 1389: 449: 2015: 1678: 1661: 1512: 1487: 1095: 422: 1695: 1646: 1503: 1472: 610: 1437:
Bhattacharya, S; Garriga, J; Calbó, J; Yong, T; Haines, DS; Graña, X (2003-04-24).
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Bai, L; Morozov, AV (November 2010). "Gene regulation by nucleosome positioning".
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Litovchick, L; Florens, LA; Swanson, SK; Washburn, MP; DeCaprio, JA (2011-04-15).
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Proceedings of the National Academy of Sciences of the United States of America
593: 576: 340:"The DREAM complex: master coordinator of cell cycle-dependent gene expression" 1317: 238: 21: 833:"The DREAM complex represses growth in response to DNA damage in Arabidopsis" 798: 699: 2004: 1974: 1932: 1883: 1842: 1793: 1744: 1687: 1638: 1629: 1612: 1611:
Pilkinton, M; Sandoval, R; Song, J; Ness, SA; Colamonici, OR (2007-01-05).
1570: 1521: 1464: 1455: 1438: 1423: 1374: 1356: 1325: 1262: 1213: 1195: 1161: 1128:"Loss of the mammalian DREAM complex deregulates chondrocyte proliferation" 1103: 1068: 1019: 970: 918: 900: 866: 848: 816: 783:"Transcriptional repression by MYB3R proteins regulates plant organ growth" 766: 718: 659: 602: 553: 506: 457: 414: 373: 114:
that include E2F and MYB orthologs combined with LIN9 and LIN54 orthologs.
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RBF, E2f2 and Mip (dREAM) complex. Disruption of the dREAM complex through
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dimerization partner, RB-like, E2F and multi-vulval class B (DREAM) complex
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and DP3, dimerization partners of E2F; and MuvB, which is a complex of
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Gaubatz, S; Lees, JA; Lindeman, GJ; Livingston, DM (February 2001).
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is also able to be expressed at this time, and binds to MuvB during
389:"Cell cycle transcription control: DREAM/MuvB and RB-E2F complexes" 1341:"The DREAM complex promotes gene body H2A.Z for target repression" 190: 178: 170: 166: 139: 99:
A protein complex similar to dREAM was subsequently identified in
57: 49: 45: 1180:"Structural mechanisms of DREAM complex assembly and regulation" 182: 162: 53: 41: 37: 1488:"E2F4 is exported from the nucleus in a CRM1-dependent manner" 73: 471:
Thomas, JH; Ceol, CJ; Schwartz, HT; Horvitz, HR (May 2003).
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Sadasivam, Subhashini; DeCaprio, James A. (11 July 2013).
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Sadasivam, S.; Duan, S.; DeCaprio, J. A. (5 March 2012).
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Harrison, MM; Ceol, CJ; Lu, X; Horvitz, HR (2006-11-07).
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Sandoval, R; Pilkinton, M; Colamonici, OR (2009-10-15).
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is a protein complex responsible for the regulation of
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Critical Reviews in Biochemistry and Molecular Biology
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Takahashi, Y; Rayman, JB; Dynlacht, BD (2000-04-01).
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The main function of the DREAM complex is to repress
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MuvB-like complexes were also recently discovered in
36:(p105) and bind repressive E2F transcription factors 1807:
Chen, JY; Lin, JR; Tsai, FC; Meyer, T (2013-10-10).
142:), which is repressed by the DREAM complex during G 1897:DeCaprio, James A.; Duensing, Anette (July 2014). 930: 928: 878: 876: 734: 732: 730: 728: 189:), while FOXM1 is degraded during mitosis by the 249:and the DREAM complex remains to be elucidated. 1173: 1171: 1388:Tedesco, D; Lukas, J; Reed, SI (2002-11-15). 289:The DREAM complex was also shown to regulate 8: 333: 331: 329: 181:). During late S phase BMYB is degraded via 256:Mammalian DREAM complex disassembly in G1/S 1660:Kolupaeva, V; Janssens, V (January 2013). 200:Mammalian DREAM complex in G0 and early G1 1964: 1922: 1873: 1832: 1783: 1734: 1677: 1628: 1560: 1511: 1454: 1413: 1364: 1252: 1203: 1151: 1058: 1009: 960: 908: 856: 806: 756: 708: 698: 649: 592: 496: 404: 363: 177:to further promote gene expression (e.g. 520:Beall, EL; Manak, JR; Zhou, S; Bell, M; 387:Fischer, M; Müller, GA (December 2017). 251: 195: 325: 32:(p130), both of which are homologs of 7: 211:chromatin-immunoprecipitation (ChIP) 1617:The Journal of Biological Chemistry 14: 150:to promote the expression of key 1679:10.1111/j.1742-4658.2012.08511.x 1096:10.1111/j.1742-4658.2009.07508.x 1709:Kurimchak, A; Graña, X (2015). 1504:10.1128/MCB.21.4.1384-1392.2001 1492:Molecular and Cellular Biology 1132:Molecular and Cellular Biology 1: 1966:10.1158/0008-5472.CAN-13-0579 450:10.1016/s0378-1119(00)00296-1 406:10.1080/10409238.2017.1360836 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173:is then recruited in G 1039:Developmental Biology 837:Life Science Alliance 344:Nature Reviews Cancer 315:Pocket protein family 255: 224:programmed cell death 199: 1553:10.1101/gad.14.7.804 1144:10.1128/MCB.01523-13 222:regulation, such as 161:phase genes such as 1993:Anticancer Research 1868:(Pt 10): 2393–406. 1406:10.1101/gad.1011202 1002:10.1101/gad.1600107 953:10.1101/gad.2034211 691:2006PNAS..10316782H 642:10.1101/gad.1516607 546:10.1038/nature01228 538:2002Natur.420..833B 1875:10.1242/jcs.097253 1306:Trends in Genetics 843:(12): e202101141. 258: 202: 2022:Protein complexes 1959:(16): 5120–5129. 793:(15): 1992–2007. 2039: 2008: 1979: 1978: 1968: 1943: 1937: 1936: 1926: 1894: 1888: 1887: 1877: 1853: 1847: 1846: 1836: 1804: 1798: 1797: 1787: 1755: 1749: 1748: 1738: 1706: 1700: 1699: 1681: 1666:The FEBS Journal 1657: 1651: 1650: 1632: 1608: 1602: 1601: 1581: 1575: 1574: 1564: 1532: 1526: 1525: 1515: 1483: 1477: 1476: 1458: 1434: 1428: 1427: 1417: 1385: 1379: 1378: 1368: 1336: 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Research 1275: 1274: 1270: 1239:(17): 2914–20. 1226: 1225: 1221: 1177: 1176: 1169: 1138:(12): 2221–34. 1124: 1123: 1119: 1081: 1080: 1076: 1032: 1031: 1027: 996:(22): 2880–96. 983: 982: 978: 934: 933: 926: 882: 881: 874: 829: 828: 824: 779: 778: 774: 738: 737: 726: 685:(45): 16782–7. 672: 671: 667: 623: 622: 618: 574: 573: 569: 532:(6917): 833–7. 519: 518: 514: 470: 469: 465: 444:(1–2): 253–63. 435: 434: 430: 386: 385: 381: 356:10.1038/nrc3556 337: 336: 327: 323: 311: 299: 272: 263: 207: 176: 155: 145: 137: 120: 66: 12: 11: 5: 2045: 2043: 2035: 2034: 2029: 2024: 2014: 2013: 2010: 2009: 1986: 1983: 1981: 1980: 1938: 1909:(4): 415–421. 1889: 1848: 1813:Molecular Cell 1799: 1764:Molecular Cell 1750: 1701: 1652: 1603: 1592:(9): 1885–90. 1576: 1527: 1498:(4): 1384–92. 1478: 1429: 1380: 1351:(5): 495–500. 1331: 1312:(11): 476–83. 1296: 1268: 1219: 1167: 1117: 1074: 1025: 976: 924: 895:(5): 474–489. 872: 822: 781:(2015-08-04). 772: 745:Molecular Cell 724: 665: 636:(8): 904–919. 616: 567: 512: 463: 428: 399:(6): 638–662. 379: 350:(8): 585–595. 324: 322: 319: 318: 317: 310: 307: 298: 297:Cancer therapy 295: 271: 268: 262: 259: 243:RNA polymerase 206: 203: 174: 153: 143: 135: 119: 116: 90:RNAi knockdown 65: 62: 56:/37/52/54 and 13: 10: 9: 6: 4: 3: 2: 2044: 2033: 2030: 2028: 2025: 2023: 2020: 2019: 2017: 2006: 2002: 1998: 1994: 1989: 1988: 1984: 1976: 1972: 1967: 1962: 1958: 1954: 1950: 1942: 1939: 1934: 1930: 1925: 1920: 1916: 1912: 1908: 1904: 1900: 1893: 1890: 1885: 1881: 1876: 1871: 1867: 1863: 1859: 1852: 1849: 1844: 1840: 1835: 1830: 1826: 1822: 1819:(1): 87–100. 1818: 1814: 1810: 1803: 1800: 1795: 1791: 1786: 1781: 1777: 1773: 1770:(6): 932–45. 1769: 1765: 1761: 1754: 1751: 1746: 1742: 1737: 1732: 1728: 1724: 1720: 1716: 1712: 1705: 1702: 1697: 1693: 1689: 1685: 1680: 1675: 1672:(2): 627–43. 1671: 1667: 1663: 1656: 1653: 1648: 1644: 1640: 1636: 1631: 1626: 1623:(1): 168–75. 1622: 1618: 1614: 1607: 1604: 1599: 1595: 1591: 1587: 1580: 1577: 1572: 1568: 1563: 1558: 1554: 1550: 1547:(7): 804–16. 1546: 1542: 1538: 1531: 1528: 1523: 1519: 1514: 1509: 1505: 1501: 1497: 1493: 1489: 1482: 1479: 1474: 1470: 1466: 1462: 1457: 1452: 1448: 1444: 1440: 1433: 1430: 1425: 1421: 1416: 1411: 1407: 1403: 1399: 1395: 1391: 1384: 1381: 1376: 1372: 1367: 1362: 1358: 1354: 1350: 1346: 1342: 1335: 1332: 1327: 1323: 1319: 1315: 1311: 1307: 1300: 1297: 1292: 1288: 1284: 1280: 1272: 1269: 1264: 1260: 1255: 1250: 1246: 1242: 1238: 1234: 1230: 1223: 1220: 1215: 1211: 1206: 1201: 1197: 1193: 1190:(9): 961–74. 1189: 1185: 1181: 1174: 1172: 1168: 1163: 1159: 1154: 1149: 1145: 1141: 1137: 1133: 1129: 1121: 1118: 1113: 1109: 1105: 1101: 1097: 1093: 1090:(4): 877–93. 1089: 1085: 1078: 1075: 1070: 1066: 1061: 1056: 1052: 1048: 1045:(1): 88–102. 1044: 1040: 1036: 1029: 1026: 1021: 1017: 1012: 1007: 1003: 999: 995: 991: 987: 980: 977: 972: 968: 963: 958: 954: 950: 947:(8): 801–13. 946: 942: 938: 931: 929: 925: 920: 916: 911: 906: 902: 898: 894: 890: 886: 879: 877: 873: 868: 864: 859: 854: 850: 846: 842: 838: 834: 826: 823: 818: 814: 809: 804: 800: 796: 792: 788: 784: 776: 773: 768: 764: 759: 754: 751:(4): 539–51. 750: 746: 742: 735: 733: 731: 729: 725: 720: 716: 711: 706: 701: 696: 692: 688: 684: 680: 676: 669: 666: 661: 657: 652: 647: 643: 639: 635: 631: 627: 620: 617: 612: 608: 604: 600: 595: 590: 587:(2): 181–93. 586: 582: 578: 571: 568: 563: 559: 555: 551: 547: 543: 539: 535: 531: 527: 523: 516: 513: 508: 504: 499: 494: 490: 486: 483:(1): 135–51. 482: 478: 474: 467: 464: 459: 455: 451: 447: 443: 439: 432: 429: 424: 420: 416: 412: 407: 402: 398: 394: 390: 383: 380: 375: 371: 366: 361: 357: 353: 349: 345: 341: 334: 332: 330: 326: 320: 316: 313: 312: 308: 306: 304: 296: 294: 292: 287: 285: 279: 277: 269: 267: 260: 254: 250: 248: 244: 240: 236: 231: 227: 225: 220: 216: 212: 204: 198: 194: 192: 188: 184: 180: 172: 168: 164: 160: 156: 149: 141: 133: 129: 125: 117: 115: 113: 108: 104: 102: 97: 95: 91: 87: 82: 77: 75: 71: 63: 61: 59: 55: 51: 47: 43: 39: 35: 31: 27: 23: 19: 1996: 1992: 1956: 1952: 1941: 1906: 1902: 1892: 1865: 1861: 1851: 1816: 1812: 1802: 1767: 1763: 1753: 1721:(1): 18–30. 1718: 1714: 1704: 1669: 1665: 1655: 1620: 1616: 1606: 1589: 1585: 1579: 1544: 1540: 1530: 1495: 1491: 1481: 1446: 1442: 1432: 1397: 1393: 1383: 1348: 1344: 1334: 1309: 1305: 1299: 1282: 1278: 1271: 1236: 1232: 1222: 1187: 1183: 1135: 1131: 1120: 1087: 1083: 1077: 1042: 1038: 1028: 993: 989: 979: 944: 940: 892: 888: 840: 836: 825: 790: 786: 775: 748: 744: 682: 678: 668: 633: 629: 619: 584: 580: 570: 529: 525: 515: 480: 476: 466: 441: 437: 431: 396: 392: 382: 347: 343: 300: 288: 280: 273: 270:Late mitosis 264: 232: 228: 208: 121: 112:Arabidoposis 111: 109: 105: 100: 98: 93: 85: 80: 78: 69: 67: 17: 15: 522:Lipsick, JS 291:cytokinesis 187:SCF complex 79:Studies in 28:(p107) and 2027:Cell cycle 2016:Categories 1715:Cell Cycle 321:References 239:nucleosome 132:quiescence 101:C. elegans 86:Drosophila 70:C. elegans 22:cell cycle 423:205695213 64:Discovery 2005:25368258 1975:23786773 1933:24840522 1884:22344256 1843:24119401 1794:24857551 1745:25483052 1696:46705471 1688:22299668 1647:21963932 1639:17098733 1586:Oncogene 1571:10766737 1522:11158323 1473:26125392 1465:12717421 1443:Oncogene 1424:12435635 1375:25737279 1326:20832136 1263:19619530 1214:25917549 1162:24710275 1104:20015071 1069:22960039 1020:17978103 971:21498570 919:22391450 867:34583930 817:26069325 767:17531812 719:17075059 660:17403774 611:17989678 603:15479636 554:12490953 507:12750327 477:Genetics 458:10974557 415:28799433 374:23842645 309:See also 303:imatinib 247:histones 118:Function 1924:4236229 1834:4039290 1785:4118046 1736:4612414 1598:1501895 1366:4358402 1291:9823308 1254:2757496 1205:4421984 1153:4054284 1112:8955433 1060:3621911 1011:2049191 962:3078706 910:3305985 858:8500230 808:4551348 710:1636532 687:Bibcode 651:1847709 562:4425307 534:Bibcode 498:1462563 365:3986830 148:S phase 2003:  1973:  1931:  1921:  1882:  1841:  1831:  1792:  1782:  1743:  1733:  1694:  1686:  1645:  1637:  1596:  1569:  1562:316494 1559:  1520:  1510:  1471:  1463:  1422:  1415:187481 1412:  1373:  1363:  1324:  1289:  1261:  1251:  1212:  1202:  1160:  1150:  1110:  1102:  1067:  1057:  1018:  1008:  969:  959:  917:  907:  865:  855:  815:  805:  765:  717:  707:  658:  648:  609:  601:  560:  552:  526:Nature 505:  495:  456:  421:  413:  372:  362:  284:DYRK1A 1692:S2CID 1643:S2CID 1513:99590 1469:S2CID 1108:S2CID 607:S2CID 558:S2CID 419:S2CID 191:APC/C 179:AURKA 171:FOXM1 167:CCNB1 140:MYBL2 58:RBBP4 2001:PMID 1971:PMID 1929:PMID 1880:PMID 1839:PMID 1790:PMID 1741:PMID 1684:PMID 1635:PMID 1594:PMID 1567:PMID 1518:PMID 1461:PMID 1420:PMID 1371:PMID 1322:PMID 1287:PMID 1259:PMID 1210:PMID 1158:PMID 1100:PMID 1065:PMID 1016:PMID 967:PMID 915:PMID 863:PMID 813:PMID 763:PMID 715:PMID 656:PMID 599:PMID 581:Cell 550:PMID 503:PMID 454:PMID 438:Gene 411:PMID 370:PMID 276:PP2a 261:G1/S 219:G2/M 215:G1/S 183:CUL1 165:and 163:CDK1 128:G2/M 126:and 124:G1/S 54:LIN9 42:E2F5 40:and 38:E2F4 30:RBL2 26:RBL1 16:The 1961:doi 1919:PMC 1911:doi 1870:doi 1866:125 1829:PMC 1821:doi 1780:PMC 1772:doi 1731:PMC 1723:doi 1674:doi 1670:280 1625:doi 1621:282 1557:PMC 1549:doi 1508:PMC 1500:doi 1451:doi 1410:PMC 1402:doi 1361:PMC 1353:doi 1314:doi 1249:PMC 1241:doi 1237:315 1200:PMC 1192:doi 1148:PMC 1140:doi 1092:doi 1088:277 1055:PMC 1047:doi 1043:372 1006:PMC 998:doi 957:PMC 949:doi 905:PMC 897:doi 853:PMC 845:doi 803:PMC 795:doi 753:doi 705:PMC 695:doi 683:103 646:PMC 638:doi 589:doi 585:119 542:doi 530:420 493:PMC 485:doi 481:164 446:doi 442:254 401:doi 360:PMC 352:doi 217:or 74:E2F 50:DP2 46:DP1 2018:: 1997:34 1995:. 1969:. 1957:73 1955:. 1951:. 1927:. 1917:. 1907:26 1905:. 1901:. 1878:. 1864:. 1860:. 1837:. 1827:. 1817:52 1815:. 1811:. 1788:. 1778:. 1768:54 1766:. 1762:. 1739:. 1729:. 1719:14 1717:. 1713:. 1690:. 1682:. 1668:. 1664:. 1641:. 1633:. 1619:. 1615:. 1588:. 1565:. 1555:. 1545:14 1543:. 1539:. 1516:. 1506:. 1496:21 1494:. 1490:. 1467:. 1459:. 1447:22 1445:. 1441:. 1418:. 1408:. 1398:16 1396:. 1392:. 1369:. 1359:. 1349:29 1347:. 1343:. 1320:. 1310:26 1308:. 1283:58 1281:. 1257:. 1247:. 1235:. 1231:. 1208:. 1198:. 1188:29 1186:. 1182:. 1170:^ 1156:. 1146:. 1136:34 1134:. 1130:. 1106:. 1098:. 1086:. 1063:. 1053:. 1041:. 1037:. 1014:. 1004:. 994:21 992:. 988:. 965:. 955:. 945:25 943:. 939:. 927:^ 913:. 903:. 893:26 891:. 887:. 875:^ 861:. 851:. 839:. 835:. 811:. 801:. 791:34 789:. 785:. 761:. 749:26 747:. 743:. 727:^ 713:. 703:. 693:. 681:. 677:. 654:. 644:. 634:21 632:. 628:. 605:. 597:. 583:. 579:. 556:. 548:. 540:. 528:. 501:. 491:. 479:. 475:. 452:. 440:. 417:. 409:. 397:52 395:. 391:. 368:. 358:. 348:13 346:. 342:. 328:^ 305:. 205:G0 169:. 134:(G 60:. 48:, 44:; 34:RB 2007:. 1977:. 1963:: 1935:. 1913:: 1886:. 1872:: 1845:. 1823:: 1796:. 1774:: 1747:. 1725:: 1698:. 1676:: 1649:. 1627:: 1600:. 1590:7 1573:. 1551:: 1524:. 1502:: 1475:. 1453:: 1426:. 1404:: 1377:. 1355:: 1328:. 1316:: 1293:. 1265:. 1243:: 1216:. 1194:: 1164:. 1142:: 1114:. 1094:: 1071:. 1049:: 1022:. 1000:: 973:. 951:: 921:. 899:: 869:. 847:: 841:4 819:. 797:: 769:. 755:: 721:. 697:: 689:: 662:. 640:: 613:. 591:: 564:. 544:: 536:: 509:. 487:: 460:. 448:: 425:. 403:: 376:. 354:: 185:( 175:2 159:M 157:/ 154:2 152:G 144:0 136:0

Index

cell cycle
RBL1
RBL2
RB
E2F4
E2F5
DP1
DP2
LIN9
RBBP4
E2F
RNAi knockdown
G1/S
G2/M
quiescence
MYBL2
S phase
G2
M
CDK1
CCNB1
FOXM1
AURKA
CUL1
SCF complex
APC/C

chromatin-immunoprecipitation (ChIP)
G1/S
G2/M

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