The Complex Containing Drosophila Myb and RB/E2F2 Regulates Cytokinesis in a Histone H2Av-Dependent Manner

REFERENCES

• Thorner AR, Hoadley KA, Parker JS, Winkel S, Millikan RC, Perou CM. 2009. In vitro and in vivo analysis of B-Myb in basal-like breast cancer. Oncogene 28:742–751.
   PubMed Web of Science ®Google Scholar
• Amatschek S, Koenig U, Auer H, Steinlein P, Pacher M, Gruenfelder A, Dekan G, Vogl S, Kubista E, Heider KH, Stratowa C, Schreiber M, Sommergruber W. 2004. Tissue-wide expression profiling using cDNA subtraction and microarrays to identify tumor-specific genes. Cancer Res. 64:844–856.
   PubMedGoogle Scholar
• Ramsay RG, Gonda TJ. 2008. MYB function in normal and cancer cells. Nat. Rev. Cancer 8:523–534.
   PubMed Web of Science ®Google Scholar
• Nomura N, Takahashi M, Matsui M, Ishii S, Date T, Sasamoto S, Ishizaki R. 1988. Isolation of human cDNA clones of myb-related genes, A-myb and B-myb. Nucleic Acids Res. 16:11075–11089.
   PubMed Web of Science ®Google Scholar
• Katzen AL, Kornberg TB, Bishop JM. 1985. Isolation of the proto-oncogene c-myb from D. melanogaster. Cell 41:449–456.
   PubMedGoogle Scholar
• Davidson CJ, Tirouvanziam R, Herzenberg LA, Lipsick JS. 2005. Functional evolution of the vertebrate Myb gene family: B-Myb, but neither A-Myb nor c-Myb, complements Drosophila Myb in hemocytes. Genetics 169:215–229.
   PubMedGoogle Scholar
• Korenjak M, Taylor-Harding B, Binne UK, Satterlee JS, Stevaux O, Aasland R, White-Cooper H, Dyson N, Brehm A. 2004. Native E2F/RBF complexes contain Myb-interacting proteins and repress transcription of developmentally controlled E2F target genes. Cell 119:181–193.
   PubMed Web of Science ®Google Scholar
• Lewis PW, Beall EL, Fleischer TC, Georlette D, Link AJ, Botchan MR. 2004. Identification of a Drosophila Myb-E2F2/RBF transcriptional repressor complex. Genes Dev. 18:2929–2940.
   PubMed Web of Science ®Google Scholar
• Schmit F, Korenjak M, Mannefeld M, Schmitt K, Franke C, von Eyss B, Gagrica S, Hanel F, Brehm A, Gaubatz S. 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
• Beall EL, Manak JR, Zhou S, Bell M, Lipsick JS, Botchan MR. 2002. Role for a Drosophila Myb-containing protein complex in site-specific DNA replication. Nature 420:833–837.
   PubMedGoogle Scholar
• Litovchick L, Sadasivam S, Florens L, Zhu X, Swanson SK, Velmurugan S, Chen R, Washburn MP, Liu XS, DeCaprio JA. 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
• Pilkinton M, Sandoval R, Colamonici OR. 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 26:7535–7543.
   PubMed Web of Science ®Google Scholar
• Georlette D, Ahn S, MacAlpine DM, Cheung E, Lewis PW, Beall EL, Bell SP, Speed T, Manak JR, Botchan MR. 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
• Lipsick JS. 2004. synMuv verité—Myb comes into focus. Genes Dev. 18:2837–2844.
   PubMedGoogle Scholar
• Beall EL, Bell M, Georlette D, Botchan MR. 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
• Beall EL, Lewis PW, Bell M, Rocha M, Jones DL, Botchan MR. 2007. Discovery of tMAC: a Drosophila testis-specific meiotic arrest complex paralogous to Myb-Muv B. Genes Dev. 21:904–919.
   PubMed Web of Science ®Google Scholar
• Katzen AL, Jackson J, Harmon BP, Fung SM, Ramsay G, Bishop JM. 1998. Drosophila myb is required for the G2/M transition and maintenance of diploidy. Genes Dev. 12:831–843.
   PubMedGoogle Scholar
• Fung SM, Ramsay G, Katzen AL. 2002. Mutations in Drosophila myb lead to centrosome amplification and genomic instability. Development 129:347–359.
   PubMed Web of Science ®Google Scholar
• Manak JR, Wen H, Van T, Andrejka L, Lipsick JS. 2007. Loss of Drosophila Myb interrupts the progression of chromosome condensation. Nat. Cell Biol. 9:581–587.
   PubMed Web of Science ®Google Scholar
• Manak JR, Mitiku N, Lipsick JS. 2002. Mutation of the Drosophila homologue of the Myb protooncogene causes genomic instability. Proc. Natl. Acad. Sci. U. S. A. 99:7438–7443.
   PubMed Web of Science ®Google Scholar
• Wen H, Andrejka L, Ashton J, Karess R, Lipsick JS. 2008. Epigenetic regulation of gene expression by Drosophila Myb and E2F2-RBF via the Myb-MuvB/dREAM complex. Genes Dev. 22:601–614.
   PubMed Web of Science ®Google Scholar
• Okada M, Akimaru H, Hou DX, Takahashi T, Ishii S. 2002. Myb controls G(2)/M progression by inducing cyclin B expression in the Drosophila eye imaginal disc. EMBO J. 21:675–684.
   PubMedGoogle Scholar
• Cayirlioglu P, Bonnette PC, Dickson MR, Duronio RJ. 2001. Drosophila E2f2 promotes the conversion from genomic DNA replication to gene amplification in ovarian follicle cells. Development 128:5085–5098.
   PubMedGoogle Scholar
• Anderson AE, Karandikar UC, Pepple KL, Chen Z, Bergmann A, Mardon G. 2011. The enhancer of trithorax and polycomb gene Caf1/p55 is essential for cell survival and patterning in Drosophila development. Development 138:1957–1966.
   PubMedGoogle Scholar
• Lewis P, Sahoo D, Geng C, Bell M, Lipsick JS, Botchan MR. 2012. Drosophila Lin-52 Acts in opposition to repressive components of the Myb-MuvB/dREAM complex. Mol. Cell. Biol. 32:3218–3227.
   PubMedGoogle Scholar
• Li D, Morley G, Whitaker M, Huang JY. 2010. Recruitment of Cdc20 to the kinetochore requires BubR1 but not Mad2 in Drosophila melanogaster. Mol. Cell. Biol. 30:3384–3395.
   PubMedGoogle Scholar
• Andrejka L, Wen H, Ashton J, Grant M, Iori K, Wang A, Manak JR, Lipsick JS. 2011. Animal-specific C-terminal domain links myeloblastosis oncoprotein (Myb) to an ancient repressor complex. Proc. Natl. Acad. Sci. U. S. A. 108:17438–17443.
   PubMedGoogle Scholar
• Schuh M, Lehner CF, Heidmann S. 2007. Incorporation of Drosophila CID/CENP-A and CENP-C into centromeres during early embryonic anaphase. Curr. Biol. 17:237–243.
   PubMedGoogle Scholar
• Gepner J, Li M, Ludmann S, Kortas C, Boylan K, Iyadurai SJ, McGrail M, Hays TS. 1996. Cytoplasmic dynein function is essential in Drosophila melanogaster. Genetics 142:865–878.
   PubMed Web of Science ®Google Scholar
• Yohn CB, Pusateri L, Barbosa V, Lehmann R. 2003. l(3)malignant brain tumor and three novel genes are required for Drosophila germ-cell formation. Genetics 165:1889–1900.
   PubMedGoogle Scholar
• Fyodorov DV, Blower MD, Karpen GH, Kadonaga JT. 2004. Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin in vivo. Genes Dev. 18:170–183.
   PubMedGoogle Scholar
• McClure KD, Schubiger G. 2005. Developmental analysis and squamous morphogenesis of the peripodial epithelium in Drosophila imaginal discs. Development 132:5033–5042.
   PubMedGoogle Scholar
• Schmittgen TD, Livak KJ. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3:1101–1108.
   PubMed Web of Science ®Google Scholar
• Spradling AC. 1993. Developmental genetics of oogenesis, p 1–70. InMartinez-Arias B (ed),The development of Drosophila melanogaster, vol I. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Katzen AL, Bishop JM. 1996. myb provides an essential function during Drosophila development. Proc. Natl. Acad. Sci. U. S. A. 93:13955–13960.
   PubMedGoogle Scholar
• Bosco G, Du W, Orr-Weaver TL. 2001. DNA replication control through interaction of E2F-RB and the origin recognition complex. Nat. Cell Biol. 3:289–295.
   PubMed Web of Science ®Google Scholar
• Margolis J, Spradling A. 1995. Identification and behavior of epithelial stem cells in the Drosophila ovary. Development 121:3797–3807.
   PubMedGoogle Scholar
• de Cuevas M, Spradling AC. 1998. Morphogenesis of the Drosophila fusome and its implications for oocyte specification. Development 125:2781–2789.
   PubMed Web of Science ®Google Scholar
• Ruchaud S, Carmena M, Earnshaw WC. 2007. Chromosomal passengers: conducting cell division. Nat. Rev. Mol. Cell Biol. 8:798–812.
   PubMed Web of Science ®Google Scholar
• Petronczki M, Lenart P, Peters JM. 2008. Polo on the rise—from mitotic entry to cytokinesis with Plk1. Dev. Cell 14:646–659.
   PubMed Web of Science ®Google Scholar
• Ridgway P, Almouzni G. 2000. CAF-1 and the inheritance of chromatin states: at the crossroads of DNA replication and repair. J. Cell Sci. 113(Pt 15):2647–2658.
   PubMedGoogle Scholar
• Schotta G, Ebert A, Dorn R, Reuter G. 2003. Position-effect variegation and the genetic dissection of chromatin regulation in Drosophila. Semin. Cell Dev. Biol. 14:67–75.
   PubMed Web of Science ®Google Scholar
• Lewis EB. 1978. A gene complex controlling segmentation in Drosophila. Nature 276:565–570.
   PubMed Web of Science ®Google Scholar
• Wen P, Quan Z, Xi R. 2012. The biological function of the WD40 repeat-containing protein p55/Caf1 in Drosophila. Dev. Dyn. 241:455–464.
   PubMedGoogle Scholar
• Lee H, Ohno K, Voskoboynik Y, Ragusano L, Martinez A, Dimova DK. 2010. Drosophila RB proteins repress differentiation-specific genes via two different mechanisms. Mol. Cell. Biol. 30:2563–2577.
   PubMedGoogle Scholar
• Frolov MV, Dyson NJ. 2004. Molecular mechanisms of E2F-dependent activation and pRB-mediated repression. J. Cell Sci. 117:2173–2181.
   PubMed Web of Science ®Google Scholar
• Talluri S, Dick FA. 2012. Regulation of transcription and chromatin structure by pRB: here, there and everywhere. Cell Cycle 11:3189–3198.
   PubMed Web of Science ®Google Scholar
• Field CM, Coughlin M, Doberstein S, Marty T, Sullivan W. 2005. Characterization of anillin mutants reveals essential roles in septin localization and plasma membrane integrity. Development 132:2849–2860.
   PubMed Web of Science ®Google Scholar
• Adams RR, Tavares AA, Salzberg A, Bellen HJ, Glover DM. 1998. Pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis. Genes Dev. 12:1483–1494.
   PubMed Web of Science ®Google Scholar
• Echard A, Hickson GR, Foley E, O'Farrell PH. 2004. Terminal cytokinesis events uncovered after an RNAi screen. Curr. Biol. 14:1685–1693.
   PubMed Web of Science ®Google Scholar
• Eggert US, Kiger AA, Richter C, Perlman ZE, Perrimon N, Mitchison TJ, Field CM. 2004. Parallel chemical genetic and genome-wide RNAi screens identify cytokinesis inhibitors and targets. PLoS Biol. 2:e379. doi:10.1371/journal.pbio.0020379.
   PubMed Web of Science ®Google Scholar
• Yamauchi T, Ishidao T, Nomura T, Shinagawa T, Tanaka Y, Yonemura S, Ishii S. 2008. A B-Myb complex containing clathrin and filamin is required for mitotic spindle function. EMBO J. 27:1852–1862.
   PubMedGoogle Scholar
• Shepard JL, Amatruda JF, Stern HM, Subramanian A, Finkelstein D, Ziai J, Finley KR, Pfaff KL, Hersey C, Zhou Y, Barut B, Freedman M, Lee C, Spitsbergen J, Neuberg D, Weber G, Golub TR, Glickman JN, Kutok JL, Aster JC, Zon LI. 2005. A zebrafish bmyb mutation causes genome instability and increased cancer susceptibility. Proc. Natl. Acad. Sci. U. S. A. 102:13194–13199.
   PubMed Web of Science ®Google Scholar
• Haga N, Kato K, Murase M, Araki S, Kubo M, Demura T, Suzuki K, Muller I, Voss U, Jurgens G, Ito M. 2007. R1R2R3-Myb proteins positively regulate cytokinesis through activation of KNOLLE transcription in Arabidopsis thaliana. Development 134:1101–1110.
   PubMedGoogle Scholar
• Frolov MV, Huen DS, Stevaux O, Dimova D, Balczarek-Strang K, Elsdon M, Dyson NJ. 2001. Functional antagonism between E2F family members. Genes Dev. 15:2146–2160.
   PubMedGoogle Scholar
• Dimova DK, Stevaux O, Frolov MV, Dyson NJ. 2003. Cell cycle-dependent and cell cycle-independent control of transcription by the Drosophila E2F/RB pathway. Genes Dev. 17:2308–2320.
   PubMedGoogle Scholar
• Taylor-Harding B, Binne UK, Korenjak M, Brehm A, Dyson NJ. 2004. p55, the Drosophila ortholog of RbAp46/RbAp48, is required for the repression of dE2F2/RBF-regulated genes. Mol. Cell. Biol. 24:9124–9136.
   PubMed Web of Science ®Google Scholar
• Müller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, Wild B, Miller EL, O'Connor MB, Kingston RE, Simon JA. 2002. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111:197–208.
   PubMed Web of Science ®Google Scholar
• Jin J, Cai Y, Li B, Conaway RC, Workman JL, Conaway JW, Kusch T. 2005. In and out: histone variant exchange in chromatin. Trends Biochem. Sci. 30:680–687.
   PubMedGoogle Scholar
• Leach TJ, Mazzeo M, Chotkowski HL, Madigan JP, Wotring MG, Glaser RL. 2000. Histone H2A. Z is widely but nonrandomly distributed in chromosomes of Drosophila melanogaster. J. Biol. Chem. 275:23267–23272.
   PubMed Web of Science ®Google Scholar
• Mavrich TN, Jiang C, Ioshikhes IP, Li X, Venters BJ, Zanton SJ, Tomsho LP, Qi J, Glaser RL, Schuster SC, Gilmour DS, Albert I, Pugh BF. 2008. Nucleosome organization in the Drosophila genome. Nature 453:358–362.
   PubMed Web of Science ®Google Scholar
• Weber CM, Henikoff JG, Henikoff S. 2010. H2A.Z nucleosomes enriched over active genes are homotypic. Nat. Struct. Mol. Biol. 17:1500–1507.
   PubMedGoogle Scholar
• Swaminathan J, Baxter EM, Corces VG. 2005. The role of histone H2Av variant replacement and histone H4 acetylation in the establishment of Drosophila heterochromatin. Genes Dev. 19:65–76.
   PubMedGoogle Scholar
• Billon P, Cote J. 2012. Precise deposition of histone H2A.Z in chromatin for genome expression and maintenance. Biochim. Biophys. Acta 1819:290–302.
   Web of Science ®Google Scholar
• Kusch T, Florens L, Macdonald WH, Swanson SK, Glaser RL, Yates JR3rd, Abmayr SM, Washburn MP, Workman JL. 2004. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306:2084–2087.
   PubMed Web of Science ®Google Scholar
• Qi D, Jin H, Lilja T, Mannervik M. 2006. Drosophila Reptin and other TIP60 complex components promote generation of silent chromatin. Genetics 174:241–251.
   PubMedGoogle Scholar
• Ruhf ML, Braun A, Papoulas O, Tamkun JW, Randsholt N, Meister M. 2001. The domino gene of Drosophila encodes novel members of the SWI2/SNF2 family of DNA-dependent ATPases, which contribute to the silencing of homeotic genes. Development 128:1429–1441.
   PubMedGoogle Scholar
• Sinclair DA, Clegg NJ, Antonchuk J, Milne TA, Stankunas K, Ruse C, Grigliatti TA, Kassis JA, Brock HW. 1998. Enhancer of Polycomb is a suppressor of position-effect variegation in Drosophila melanogaster. Genetics 148:211–220.
   PubMedGoogle Scholar
• Fay DS, Yochem J. 2007. The SynMuv genes of Caenorhabditis elegans in vulval development and beyond. Dev. Biol. 306:1–9.
   PubMed Web of Science ®Google Scholar
• Andersen EC, Saffer AM, Horvitz HR. 2008. Multiple levels of redundant processes inhibit Caenorhabditis elegans vulval cell fates. Genetics 179:2001–2012.
   PubMedGoogle Scholar
• Cui M, Kim EB, Han M. 2006. Diverse chromatin remodeling genes antagonize the Rb-involved SynMuv pathways in C. elegans. PLoS Genet. 2:e74. doi:10.1371/journal.pgen.0020074.
   PubMedGoogle Scholar
• Lu J, Ruhf ML, Perrimon N, Leder P. 2007. A genome-wide RNA interference screen identifies putative chromatin regulators essential for E2F repression. Proc. Natl. Acad. Sci. U. S. A. 104:9381–9386.
   PubMedGoogle Scholar
• Swaminathan A, Gajan A, Pile LA. 2012. Epigenetic regulation of transcription in Drosophila. Front. Biosci. 17:909–937.
   Google Scholar