Lin9, a Subunit of the Mammalian DREAM Complex, Is Essential for Embryonic Development, for Survival of Adult Mice, and for Tumor Suppression

REFERENCES

• Baker, D. J., K. B. Jeganathan, L. Malureanu, C. Perez-Terzic, A. Terzic, and J. M. van Deursen. 2006. Early aging-associated phenotypes in Bub3/Rae1 haploinsufficient mice. J. Cell Biol. 172:529–540.
   PubMed Web of Science ®Google Scholar
• Beall, E. L., M. Bell, D. Georlette, and M. R. Botchan. 2004. Dm-myb mutant lethality in Drosophila is dependent upon mip130: positive and negative regulation of DNA replication. Genes Dev. 18:1667–1680.
   PubMedGoogle Scholar
• Beitel, G. J., E. J. Lambie, and H. R. Horvitz. 2000. 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. Gene 254:253–263.
   PubMedGoogle Scholar
• Bernstein, B. E., M. Kamal, K. Lindblad-Toh, S. Bekiranov, D. K. Bailey, D. J. Huebert, S. McMahon, E. K. Karlsson, E. J. Kulbokas, 3rd, T. R. Gingeras, S. L. Schreiber, and E. S. Lander. 2005. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120:169–181.
   PubMed Web of Science ®Google Scholar
• Cotsiki, M., R. L. Lock, Y. Cheng, G. L. Williams, J. Zhao, D. Perera, R. Freire, A. Entwistle, E. A. Golemis, T. M. Roberts, P. S. Jat, and O. V. Gjoerup. 2004. Simian virus 40 large T antigen targets the spindle assembly checkpoint protein Bub1. Proc. Natl. Acad. Sci. U. S. A. 101:947–952.
   PubMedGoogle Scholar
• Dai, W., Q. Wang, T. Liu, M. Swamy, Y. Fang, S. Xie, R. Mahmood, Y. M. Yang, M. Xu, and C. V. Rao. 2004. Slippage of mitotic arrest and enhanced tumor development in mice with BubR1 haploinsufficiency. Cancer Res. 64:440–445.
   PubMed Web of Science ®Google Scholar
• DeGregori, J., and D. G. Johnson. 2006. Distinct and overlapping roles for E2F family members in transcription, proliferation and apoptosis. Curr. Mol. Med. 6:739–748.
   PubMed Web of Science ®Google Scholar
• Eggert, U. S., T. J. Mitchison, and C. M. Field. 2006. Animal cytokinesis: from parts list to mechanisms. Annu. Rev. Biochem. 75:543–566.
   PubMedGoogle Scholar
• Fay, D. S., and M. Han. 2000. The synthetic multivulval genes of C. elegans: functional redundancy, Ras-antagonism, and cell fate determination. Genesis 26:279–284.
   PubMedGoogle Scholar
• Fu, J., M. Bian, Q. Jiang, and C. Zhang. 2007. Roles of Aurora kinases in mitosis and tumorigenesis. Mol. Cancer Res. 5:1–10.
   PubMed Web of Science ®Google Scholar
• Gagrica, S., S. Hauser, I. Kolfschoten, L. Osterloh, R. Agami, and S. Gaubatz. 2004. Inhibition of oncogenic transformation by mammalian Lin-9, a pRB-associated protein. EMBO J. 23:4627–4638.
   PubMedGoogle Scholar
• Gaubatz, S., G. J. Lindeman, S. Ishida, L. Jakoi, J. R. Nevins, D. M. Livingston, and R. E. Rempel. 2000. E2F4 and E2F5 play an essential role in pocket protein-mediated G1 control. Mol. Cell 6:729–735.
   PubMed Web of Science ®Google Scholar
• Georlette, D., S. Ahn, D. M. MacAlpine, E. Cheung, P. W. Lewis, E. L. Beall, S. P. Bell, T. Speed, J. R. Manak, and M. R. Botchan. 2007. Genomic profiling and expression studies reveal both positive and negative activities for the Drosophila Myb MuvB/dREAM complex in proliferating cells. Genes Dev. 21:2880–2896.
   PubMed Web of Science ®Google Scholar
• Harrison, M. M., C. J. Ceol, X. Lu, and H. R. Horvitz. 2006. Some C. elegans class B synthetic multivulva proteins encode a conserved LIN-35 Rb-containing complex distinct from a NuRD-like complex. Proc. Natl. Acad. Sci. U. S. A. 103:16782–16787.
   PubMed Web of Science ®Google Scholar
• Howman, E. V., K. J. Fowler, A. J. Newson, S. Redward, A. C. MacDonald, P. Kalitsis, and K. H. Choo. 2000. Early disruption of centromeric chromatin organization in centromere protein A (Cenpa) null mice. Proc. Natl. Acad. Sci. U. S. A. 97:1148–1153.
   PubMed Web of Science ®Google Scholar
• Hurford, R. K., Jr., D. Cobrinik, M. H. Lee, and N. Dyson. 1997. pRB and p107/p130 are required for the regulated expression of different sets of E2F responsive genes. Genes Dev. 11:1447–1463.
   PubMed Web of Science ®Google Scholar
• Jat, P. S., and P. A. Sharp. 1986. Large T antigens of simian virus 40 and polyomavirus efficiently establish primary fibroblasts. J. Virol. 59:746–750.
   PubMed Web of Science ®Google Scholar
• Kerkhoff, E., L. M. Fedorov, R. Siefken, A. O. Walter, T. Papadopoulos, and U. R. Rapp. 2000. Lung-targeted expression of the c-Raf-1 kinase in transgenic mice exposes a novel oncogenic character of the wild-type protein. Cell Growth Differ. 11:185–190.
   PubMedGoogle Scholar
• Kleinschmidt, M. A., T. U. Wagner, D. Liedtke, S. Spahr, B. Samans, and S. Gaubatz. 2009. lin9 is required for mitosis and cell survival during early zebrafish development. J. Biol. Chem. 284:13119–13127.
   PubMedGoogle Scholar
• Knight, A. S., M. Notaridou, and R. J. Watson. 2009. A Lin-9 complex is recruited by B-Myb to activate transcription of G(2)/M genes in undifferentiated embryonal carcinoma cells. Oncogene 28:1737–1747.
   PubMed Web of Science ®Google Scholar
• Korenjak, M., and A. Brehm. 2005. E2F-Rb complexes regulating transcription of genes important for differentiation and development. Curr. Opin. Genet. Dev. 15:520–527.
   PubMed Web of Science ®Google Scholar
• Lee, H., D. J. Lee, S. P. Oh, H. D. Park, H. H. Nam, J. M. Kim, and D. S. Lim. 2006. Mouse emi1 has an essential function in mitotic progression during early embryogenesis. Mol. Cell. Biol. 26:5373–5381.
   PubMedGoogle Scholar
• Leimeister, C., N. Schumacher, C. Steidl, and M. Gessler. 2000. Analysis of HeyL expression in wild-type and Notch pathway mutant mouse embryos. Mech. Dev. 98:175–178.
   PubMed Web of Science ®Google Scholar
• Lewis, P. W., E. L. Beall, T. C. Fleischer, D. Georlette, A. J. Link, and M. R. Botchan. 2004. Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex. Genes Dev. 18:2929–2940.
   PubMed Web of Science ®Google Scholar
• Litovchick, L., S. Sadasivam, L. Florens, X. Zhu, S. K. Swanson, S. Velmurugan, R. Chen, M. P. Washburn, X. S. Liu, and J. A. DeCaprio. 2007. Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol. Cell 26:539–551.
   PubMed Web of Science ®Google Scholar
• Lu, L. Y., J. L. Wood, K. Minter-Dykhouse, L. Ye, T. L. Saunders, X. Yu, and J. Chen. 2008. Polo-like kinase 1 is essential for early embryonic development and tumor suppression. Mol. Cell. Biol. 28:6870–6876.
   PubMed Web of Science ®Google Scholar
• Mountford, P., B. Zevnik, A. Duwel, J. Nichols, M. Li, C. Dani, M. Robertson, I. Chambers, and A. Smith. 1994. Dicistronic targeting constructs: reporters and modifiers of mammalian gene expression. Proc. Natl. Acad. Sci. U. S. A. 91:4303–4307.
   PubMedGoogle Scholar
• Nichols, J., B. Zevnik, K. Anastassiadis, H. Niwa, D. Klewe-Nebenius, I. Chambers, H. Schöler, and A. Smith. 1998. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95:379–391.
   PubMed Web of Science ®Google Scholar
• Osterloh, L., B. von Eyss, F. Schmit, L. Rein, D. Hubner, B. Samans, S. Hauser, and S. Gaubatz. 2007. The human synMuv-like protein LIN-9 is required for transcription of G2/M genes and for entry into mitosis. EMBO J. 26:144–157.
   PubMed Web of Science ®Google Scholar
• Petronczki, M., P. Lenart, and J. M. Peters. 2008. Polo on the rise: from mitotic entry to cytokinesis with Plk1. Dev. Cell 14:646–659.
   PubMed Web of Science ®Google Scholar
• Pilkinton, M., R. Sandoval, and O. R. Colamonici. 2007. Mammalian Mip/LIN-9 interacts with either the p107, p130/E2F4 repressor complex or B-Myb in a cell cycle-phase-dependent context distinct from the Drosophila dREAM complex. Oncogene 29:7535–7543.
   Google Scholar
• Pilkinton, M., R. Sandoval, J. Song, S. A. Ness, and O. R. Colamonici. 2007. Mip/LIN-9 regulates the expression of B-Myb and the induction of cyclin A, cyclin B, and CDK1. J. Biol. Chem. 282:168–175.
   PubMedGoogle Scholar
• Poirier, F., C. T. Chan, P. M. Timmons, E. J. Robertson, M. J. Evans, and P. W. Rigby. 1991. The murine H19 gene is activated during embryonic stem cell differentiation in vitro and at the time of implantation in the developing embryo. Development 113:1105–1114.
   PubMed Web of Science ®Google Scholar
• Rapp, U. R., C. Korn, F. Ceteci, C. Karreman, K. Luetkenhaus, V. Serafin, E. Zanucco, I. Castro, and T. Potapenko. 2009. MYC is a metastasis gene for non-small-cell lung cancer. PLoS One 4:e6029.
   PubMed Web of Science ®Google Scholar
• Rodriguez, C. I., F. Buchholz, J. Galloway, R. Sequerra, J. Kasper, R. Ayala, A. F. Stewart, and S. M. Dymecki. 2000. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 25:139–140.
   PubMed Web of Science ®Google Scholar
• Rundell, K., and R. Parakati. 2001. The role of the SV40 ST antigen in cell growth promotion and transformation. Semin. Cancer Biol. 11:5–13.
   PubMed Web of Science ®Google Scholar
• Sandoval, R., J. Xue, X. Tian, K. Barrett, M. Pilkinton, D. S. Ucker, P. Raychaudhuri, R. D. Kineman, R. M. Luque, G. Baida, X. Zou, V. E. Valli, J. L. Cook, H. Kiyokawa, and O. R. Colamonici. 2006. A mutant allele of BARA/LIN-9 rescues the cdk4-/- phenotype by releasing the repression on E2F-regulated genes. Exp. Cell Res. 312:2465–2475.
   PubMedGoogle Scholar
• Sauer, B. 1993. Manipulation of transgenes by site-specific recombination: use of Cre recombinase. Methods Enzymol. 225:890–900.
   PubMedGoogle Scholar
• Schmit, F., S. Cremer, and S. Gaubatz. 2009. LIN54 is an essential core subunit of the DREAM/LINC complex that binds to the cdc2 promoter in a sequence-specific manner. FEBS J. 276:5703–5716.
   PubMed Web of Science ®Google Scholar
• Schmit, F., M. Korenjak, M. Mannefeld, K. Schmitt, C. Franke, B. V. Eyss, S. Gagrica, F. Hanel, A. Brehm, and S. Gaubatz. 2007. LINC, a human complex that is related to pRB-containing complexes in invertebrates regulates the expression of G2/M genes. Cell Cycle 6:1903–1913.
   PubMed Web of Science ®Google Scholar
• Schneider, R., A. J. Bannister, F. A. Myers, A. W. Thorne, C. Crane-Robinson, and T. Kouzarides. 2004. Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat. Cell Biol. 6:73–77.
   PubMed Web of Science ®Google Scholar
• Schwenk, F., U. Baron, and K. Rajewsky. 1995. A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res. 23:5080–5081.
   PubMed Web of Science ®Google Scholar
• Serrano, M. 1997. The tumor suppressor protein p16INK4a. Exp. Cell Res. 237:7–13.
   PubMed Web of Science ®Google Scholar
• Tanaka, Y., N. P. Patestos, T. Maekawa, and S. Ishii. 1999. B-myb is required for inner cell mass formation at an early stage of development. J. Biol. Chem. 274:28067–28070.
   PubMed Web of Science ®Google Scholar
• Tarasov, K. V., Y. S. Tarasova, W. L. Tam, D. R. Riordon, S. T. Elliott, G. Kania, J. Li, S. Yamanaka, D. G. Crider, G. Testa, R. A. Li, B. Lim, C. L. Stewart, Y. Liu, J. E. Van Eyk, R. P. Wersto, A. M. Wobus, and K. R. Boheler. 2008. B-MYB is essential for normal cell cycle progression and chromosomal stability of embryonic stem cells. PLoS One 3:e2478.
   PubMed Web of Science ®Google Scholar
• Vooijs, M., J. Jonkers, and A. Berns. 2001. A highly efficient ligand-regulated Cre recombinase mouse line shows that LoxP recombination is position dependent. EMBO Rep. 2:292–297.
   PubMed Web of Science ®Google Scholar
• Zhu, W., P. H. Giangrande, and J. R. Nevins. 2004. E2Fs link the control of G1/S and G2/M transcription. EMBO J. 23:4615–4626.
   PubMed Web of Science ®Google Scholar