Phosphorylation of Drosophila Brahma on CDK-phosphorylation sites is important for cell cycle regulation and differentiation

References

• Schnitzler G, Sif S, Kingston RE. Human SWI/SNF interconverts a nucleosome between its base state and a stable remodeled state. Cell. 1998;94:17–27.
   PubMed Web of Science ®Google Scholar
• Imbalzano AN, Kwon H, Green MR, et al. Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature. 1994;370:481–485.
   PubMed Web of Science ®Google Scholar
• Shundrovsky A, Smith CL, Lis JT, et al. Probing SWI/SNF remodeling of the nucleosome by unzipping single DNA molecules. Nat Struct Mol Biol. 2006;13:549–554.
   PubMed Web of Science ®Google Scholar
• Khavari PA, Peterson CL, Tamkun JW, et al. BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature. 1993;366:170–174.
   PubMed Web of Science ®Google Scholar
• Wang W, Cote J, Xue Y, et al. Purification and biochemical heterogeneity of the mammalian SWI-SNF complex. EMBO J. 1996;15:5370–5382.
   PubMed Web of Science ®Google Scholar
• Phelan ML, Sif S, Narlikar GJ, et al. Reconstitution of a core chromatin remodeling complex from SWI/SNF subunits. Mol Cell. 1999;3:247–253.
   PubMed Web of Science ®Google Scholar
• Fry CJ, Peterson CL. Chromatin remodeling enzymes: who’s on first? Curr Biol. 2001;11:R185–97.
   PubMed Web of Science ®Google Scholar
• Roberts CW, Orkin SH. The SWI/SNF complex–chromatin and cancer. Nat Rev Cancer. 2004;4:133–142.
   PubMed Web of Science ®Google Scholar
• Lee K, Shim JH, Kang MJ, et al. Association of BAF53 with mitotic chromosomes. Mol Cells. 2007;24:288–293.
   PubMed Web of Science ®Google Scholar
• Lee K, Kang MJ, Kwon SJ, et al. Expansion of chromosome territories with chromatin decompaction in BAF53-depleted interphase cells. Mol Biol Cell. 2007;18:4013–4023.
   PubMed Web of Science ®Google Scholar
• Zhang L, Chen H, Gong M, et al. The chromatin remodeling protein BRG1 modulates BRCA1 response to UV irradiation by regulating ATR/ATM activation. Front Oncol. 2013;3:7.
   PubMedGoogle Scholar
• Park JH, Park EJ, Lee HS, et al. Mammalian SWI/SNF complexes facilitate DNA double-strand break repair by promoting gamma-H2AX induction. EMBO J. 2006;25:3986–3997.
   PubMed Web of Science ®Google Scholar
• Qi W, Wang R, Chen H, et al. BRG1 promotes the repair of DNA double-strand breaks by facilitating the replacement of RPA with RAD51. J Cell Sci. 2015;128:317–330.
   PubMed Web of Science ®Google Scholar
• Kozmik Z, Machon O, Kralova J, et al. Characterization of mammalian orthologues of the Drosophila osa gene: cDNA cloning, expression, chromosomal localization, and direct physical interaction with Brahma chromatin-remodeling complex. Genomics. 2001;73:140–148.
   PubMed Web of Science ®Google Scholar
• Huang J, Zhao YL, Li Y, et al. Genomic and functional evidence for an ARID1A tumor suppressor role. Genes Chromosomes Cancer. 2007;46:745–750.
   PubMed Web of Science ®Google Scholar
• Decristofaro MF, Betz BL, Rorie CJ, et al. Characterization of SWI/SNF protein expression in human breast cancer cell lines and other malignancies. J Cell Physiol. 2001;186:136–145.
   PubMed Web of Science ®Google Scholar
• Wang X, Nagl NG Jr., Flowers S, et al. Expression of p270 (ARID1A), a component of human SWI/SNF complexes, in human tumors. Int J Cancer. 2004;112:636–642.
   PubMed Web of Science ®Google Scholar
• Versteege I, Sevenet N, Lange J, et al. Truncating mutations of hSNF5/INI1 in aggressive paediatric cancer. Nature. 1998;394:203–206.
   PubMed Web of Science ®Google Scholar
• Kohashi K, Oda Y. Oncogenic roles of SMARCB1/INI1 and its deficient tumors. Cancer Sci. 2017;108:547–552.
   PubMed Web of Science ®Google Scholar
• St Pierre R, Mammalian KC. SWI/SNF complexes in cancer: emerging therapeutic opportunities. Curr Opin Genet Dev. 2017;42:56–67.
   PubMed Web of Science ®Google Scholar
• Kadoch C, Crabtree GR. Mammalian SWI/SNF chromatin remodeling complexes and cancer: mechanistic insights gained from human genomics. Sci Adv. 2015;1:e1500447.
   PubMed Web of Science ®Google Scholar
• Dunaief JL, Strober BE, Guha S, et al. The retinoblastoma protein and BRG1 form a complex and cooperate to induce cell cycle arrest. Cell. 1994;79:119–130.
   PubMed Web of Science ®Google Scholar
• Trouche D, Le Chalony C, Muchardt C, et al. RB and hbrm cooperate to repress the activation functions of E2F1. Proc Natl Acad Sci USA. 1997;94:11268–11273.
   PubMed Web of Science ®Google Scholar
• Staehling-Hampton K, Ciampa PJ, Brook A, et al. A genetic screen for modifiers of E2F in Drosophila melanogaster. Genetics. 1999;153:275–287.
   PubMed Web of Science ®Google Scholar
• Weinberg RA. The retinoblastoma protein and cell cycle control. Cell. 1995;81:323–330.
   PubMed Web of Science ®Google Scholar
• Suryadinata R, Sadowski M, Sarcevic B. Control of cell cycle progression by phosphorylation of cyclin-dependent kinase (CDK) substrates. Biosci Rep. 2010;30:243–255.
   PubMed Web of Science ®Google Scholar
• Shanahan F, Seghezzi W, Parry D, et al. Cyclin E associates with BAF155 and BRG1, components of the mammalian SWI-SNF complex, and alters the ability of BRG1 to induce growth arrest. Mol Cell Biol. 1999;19:1460–1469.
   PubMed Web of Science ®Google Scholar
• Wong AK, Shanahan F, Chen Y, et al. BRG1, a component of the SWI-SNF complex, is mutated in multiple human tumor cell lines. Cancer Res. 2000;60:6171–6177.
   PubMed Web of Science ®Google Scholar
• Brumby AM, Zraly CB, Horsfield JA, et al. Drosophila cyclin E interacts with components of the Brahma complex. EMBO J. 2002;21:3377–3389.
   PubMed Web of Science ®Google Scholar
• Zraly CB, Marenda DR, Dingwall AK. SNR1 (INI1/SNF5) mediates important cell growth functions of the Drosophila Brahma (SWI/SNF) chromatin remodeling complex. Genetics. 2004;168:199–214.
   PubMed Web of Science ®Google Scholar
• Suryadinata R, Sadowski M, Steel R, et al. Cyclin-dependent kinase-mediated phosphorylation of RBP1 and pRb promotes their dissociation to mediate release of the SAP30.mSin3.HDAC transcriptional repressor complex. J Biol Chem. 2011;286:5108–5118.
   PubMed Web of Science ®Google Scholar
• Sarcevic B, Lilischkis R, Sutherland RL. Differential phosphorylation of T-47D human breast cancer cell substrates by D1-, D3-, E-, and A-type cyclin-CDK complexes. J Biol Chem. 1997;272:33327–33337.
   PubMed Web of Science ®Google Scholar
• Herr A, McKenzie L, Suryadinata R, et al. Geminin and Brahma act antagonistically to regulate EGFR-Ras-MAPK signaling in Drosophila. Dev Biol. 2010;344:36–51.
   PubMed Web of Science ®Google Scholar
• Elfring LK, Daniel C, Papoulas O, et al. Genetic analysis of brahma: the Drosophila homolog of the yeast chromatin remodeling factor SWI2/SNF2. Genetics. 1998;148:251–265.
   PubMed Web of Science ®Google Scholar
• Luo RX, Postigo AA, Dean DC. Rb interacts with histone deacetylase to repress transcription. Cell. 1998;92:463–473.
   PubMed Web of Science ®Google Scholar
• Brehm A, Miska EA, McCance DJ, et al. Retinoblastoma protein recruits histone deacetylase to repress transcription. Nature. 1998;391:597–601.
   PubMed Web of Science ®Google Scholar
• Magnaghi-Jaulin L, Groisman R, Naguibneva I, et al. Retinoblastoma protein represses transcription by recruiting a histone deacetylase. Nature. 1998;391:601–605.
   PubMed Web of Science ®Google Scholar
• Duman-Scheel M, Johnston LA, Du W. Repression of dMyc expression by Wingless promotes Rbf-induced G1 arrest in the presumptive Drosophila wing margin. Proc Natl Acad Sci USA. 2004;101:3857–3862.
   PubMed Web of Science ®Google Scholar
• Johnston LA, Edgar BA. Wingless and Notch regulate cell-cycle arrest in the developing Drosophila wing. Nature. 1998;394:82–84.
   PubMed Web of Science ®Google Scholar
• Johnston LA, Prober DA, Edgar BA, et al. Drosophila myc regulates cellular growth during development. Cell. 1999;98:779–790.
   PubMed Web of Science ®Google Scholar
• Prober DA, Edgar BA. Ras1 promotes cellular growth in the Drosophila wing. Cell. 2000;100:435–446.
   PubMed Web of Science ®Google Scholar
• Neufeld TP, de la Cruz AF, Johnston LA, et al. Coordination of growth and cell division in the Drosophila wing. Cell. 1998;93:1183–1193.
   PubMed Web of Science ®Google Scholar
• Coisy-Quivy M, Disson O, Roure V, et al. Role for Brm in cell growth control. Cancer Res. 2006;66:5069–5076.
   PubMed Web of Science ®Google Scholar
• Reis T, Edgar BA. Negative regulation of dE2F1 by cyclin-dependent kinases controls cell cycle timing. Cell. 2004;117:253–264.
   PubMed Web of Science ®Google Scholar
• Hay BA, Wolff T, Rubin GM. Expression of baculovirus P35 prevents cell death in Drosophila. Development. 1994;120:2121–2129.
   PubMed Web of Science ®Google Scholar
• Marenda DR, Zraly CB, Dingwall AK. The Drosophila Brahma (SWI/SNF) chromatin remodeling complex exhibits cell-type specific activation and repression functions. Dev Biol. 2004;267:279–293.
   PubMed Web of Science ®Google Scholar
• Teleman AA, Cohen SM. Dpp gradient formation in the Drosophila wing imaginal disc. Cell. 2000;103:971–980.
   PubMed Web of Science ®Google Scholar
• Restrepo S, Zartman JJ, Basler K. Coordination of patterning and growth by the morphogen DPP. Curr Biol. 2014;24:R245–55.
   PubMed Web of Science ®Google Scholar
• Zhang HS, Gavin M, Dahiya A, et al. Exit from G1 and S phase of the cell cycle is regulated by repressor complexes containing HDAC-Rb-hSWI/SNF and Rb-hSWI/SNF. Cell. 2000;101:79–89.
   PubMed Web of Science ®Google Scholar
• Pagano M, Pepperkok R, Verde F, et al. Cyclin A is required at two points in the human cell cycle. EMBO J. 1992;11:961–971.
   PubMed Web of Science ®Google Scholar
• Schulman BA, Lindstrom DL, Harlow E. Substrate recruitment to cyclin-dependent kinase 2 by a multipurpose docking site on cyclin A. Proc Natl Acad Sci USA. 1998;95:10453–10458.
   PubMed Web of Science ®Google Scholar
• Zarkowska T, Mittnacht S. Differential phosphorylation of the retinoblastoma protein by G1/S cyclin-dependent kinases. J Biol Chem. 1997;272:12738–12746.
   PubMed Web of Science ®Google Scholar
• Amoyel M, Bach EA. Cell competition: how to eliminate your neighbours. Development. 2014;141:988–1000.
   PubMed Web of Science ®Google Scholar
• Moreno E. Is cell competition relevant to cancer? Nat Rev Cancer. 2008;8:141–147.
   PubMed Web of Science ®Google Scholar
• Blair SS. Wing vein patterning in Drosophila and the analysis of intercellular signaling. Annu Rev Cell Dev Biol. 2007;23:293–319.
   PubMed Web of Science ®Google Scholar
• Ondrusova L, Vachtenheim J, Reda J, et al. MITF-independent pro-survival role of BRG1-containing SWI/SNF complex in melanoma cells. PLoS One. 2013;8:e54110.
   PubMed Web of Science ®Google Scholar
• Xi Q, He W, Zhang XH, et al. Genome-wide impact of the BRG1 SWI/SNF chromatin remodeler on the transforming growth factor beta transcriptional program. J Biol Chem. 2008;283:1146–1155.
   PubMed Web of Science ®Google Scholar
• Moreno E, Basler K, Morata G. Cells compete for decapentaplegic survival factor to prevent apoptosis in Drosophila wing development. Nature. 2002;416:755–759.
   PubMed Web of Science ®Google Scholar
• Adachi-Yamada T, Fujimura-Kamada K, Nishida Y, et al. Distortion of proximodistal information causes JNK-dependent apoptosis in Drosophila wing. Nature. 1999;400:166–169.
   PubMed Web of Science ®Google Scholar
• Perez-Garijo A, Martin FA, Struhl G, et al. Dpp signaling and the induction of neoplastic tumors by caspase-inhibited apoptotic cells in Drosophila. Proc Natl Acad Sci USA. 2005;102:17664–17669.
   PubMed Web of Science ®Google Scholar
• Perez-Garijo A, Martin FA, Morata G. Caspase inhibition during apoptosis causes abnormal signalling and developmental aberrations in Drosophila. Development. 2004;131:5591–5598.
   PubMed Web of Science ®Google Scholar
• Perez-Garijo A, Shlevkov E, Morata G. The role of Dpp and Wg in compensatory proliferation and in the formation of hyperplastic overgrowths caused by apoptotic cells in the Drosophila wing disc. Development. 2009;136:1169–1177.
   PubMed Web of Science ®Google Scholar
• Cook O, Biehs B, Bier E. brinker and optomotor-blind act coordinately to initiate development of the L5 wing vein primordium in Drosophila. Development. 2004;131:2113–2124.
   PubMed Web of Science ®Google Scholar
• van Twest S, Murphy VJ, Hodson C, et al. Mechanism of Ubiquitination and Deubiquitination in the Fanconi Anemia Pathway. Mol Cell. 2017;65:247–259.
   PubMed Web of Science ®Google Scholar
• Coulthard R, Deans A, Swuec P, et al. Architecture and DNA recognition elements of the Fanconi anemia FANCM-FAAP24 complex. Structure. 2013;21:1648–1658.
   PubMed Web of Science ®Google Scholar
• Roesley SN, Suryadinata R, Morrish E, et al. Cyclin-dependent kinase-mediated phosphorylation of breast cancer metastasis suppressor 1 (BRMS1) affects cell migration. Cell Cycle. 2016;15:137–151.
   PubMed Web of Science ®Google Scholar
• Dietzl G, Chen D, Schnorrer F, et al. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature. 2007;448:151–156.
   PubMed Web of Science ®Google Scholar