E2fl1 is a meiosis-specific transcription factor in the protist Tetrahymena thermophila

References

• Lathangue NB. Drtf1/E2f: an expanding family of heterodimeric transcription factors implicated in cell cycle control. Trends Biochem Sci 1994; 19:108-14; PMID:8203017; http://dx.doi.org/10.1016/0968-0004(94)90202-X
   PubMed Web of Science ®Google Scholar
• Weinberg RA. The retinoblastoma protein and cell cycle control. Cell 1995; 81:323-30; PMID:7736585; http://dx.doi.org/10.1016/0092-8674(95)90385-2
   PubMed Web of Science ®Google Scholar
• van den Heuvel S, Dyson NJ. Conserved functions of the pRB and E2F families. Nat Rev Mol Cell Bio 2008; 9:713-24; http://dx.doi.org/10.1038/nrm2469
   PubMed Web of Science ®Google Scholar
• Mariconti L, Pellegrini B, Cantoni R, Stevens R, Bergounioux C, Cella R, Albani D. The E2F family of transcription factors from Arabidopsis thaliana: novel and conserved components of the retinoblastoma/E2F pathway in plants. J Biol Chem 2002; 277:9911-9; PMID:11786543; http://dx.doi.org/10.1074/jbc.M110616200
   PubMed Web of Science ®Google Scholar
• Bracken AP, Ciro M, Cocito A, Helin K. E2F target genes: unraveling the biology. Trends Biochem Sci 2004; 29:409-17; PMID:15362224; http://dx.doi.org/10.1016/j.tibs.2004.06.006
   PubMed Web of Science ®Google Scholar
• Dynlacht BD, Brook A, Dembski M, Yenush L, Dyson N. DNA-binding and transactivation properties of Drosophila E2f and Dp proteins. P Natl Acad Sci USA 1994; 91:6359-63; http://dx.doi.org/10.1073/pnas.91.14.6359
   PubMed Web of Science ®Google Scholar
• Blais A, Dynlacht BD. Hitting their targets: an emerging picture of E2F and cell cycle control. Curr Opin Genet Dev 2004; 14:527-32; PMID:15380244; http://dx.doi.org/10.1016/j.gde.2004.07.003
   PubMed Web of Science ®Google Scholar
• Lindeman GJ, Gaubatz S, Livingston DM, Ginsberg D. The subcellular localization of E2f-4 is cell-cycle dependent. P Natl Acad Sci USA 1997; 94:5095-100; http://dx.doi.org/10.1073/pnas.94.10.5095
   PubMed Web of Science ®Google Scholar
• 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; PMID:9271426; http://dx.doi.org/10.1128/MCB.17.9.5508
   PubMed Web of Science ®Google Scholar
• DeGregori J, Leone G, Miron A, Jakoi L, Nevins JR. Distinct roles for E2F proteins in cell growth control and apoptosis. P Natl Acad Sci USA 1997; 94:7245-50; http://dx.doi.org/10.1073/pnas.94.14.7245
   PubMed Web of Science ®Google Scholar
• Cobrinik D. Regulatory interactions among E2Fs and cell cycle control proteins. Curr Top Microbiol Immunol 1996; 208:31-61; PMID:8575212
   PubMed Web of Science ®Google Scholar
• Dyson N. The regulation of E2F by pRB-family proteins. Gene Dev 1998; 12:2245-62; PMID:9694791; http://dx.doi.org/10.1101/gad.12.15.2245
   PubMed Web of Science ®Google Scholar
• Vandepoele K, Vlieghe K, Florquin K, Hennig L, Beemster GTS, Gruissem W, Van De Peer Y, Inze D, De Veylder L. Genome-wide identification of potential plant E2F target genes. Plant Physiol 2005; 139:316-28; PMID:16126853; http://dx.doi.org/10.1104/pp.105.066290
   PubMed Web of Science ®Google Scholar
• Ren B, Cam H, Takahashi Y, Volkert T, Terragni J, Young RA, Dynlacht BD. E2F integrates cell cycle progression with DNA repair, replication, and G2/M checkpoints. Gene Dev 2002; 16:245-56; PMID:11799067; http://dx.doi.org/10.1101/gad.949802
   PubMed Web of Science ®Google Scholar
• Rabinovich A, Jin VX, Rabinovich R, Xu XQ, Farnham PJ. E2F in vivo binding specificity: comparison of consensus versus nonconsensus binding sites. Genome Res 2008; 18:1763-77; PMID:18836037; http://dx.doi.org/10.1101/gr.080622.108
   PubMed Web of Science ®Google Scholar
• Cao LH, Peng B, Yao L, Zhang XM, Sun KA, Yang XM, Yu L. The ancient function of RB-E2F pathway: insights from its evolutionary history. Biol Direct 2010; 5:55; PMID:20849664; http://dx.doi.org/10.1186/1745-6150-5-55
   PubMed Web of Science ®Google Scholar
• Orias E, Cervantes MD, Hamilton EP. Tetrahymena thermophila, a unicellular eukaryote with separate germline and somatic genomes. Res Microbiol 2011; 162:578-86; PMID:21624459; http://dx.doi.org/10.1016/j.resmic.2011.05.001
   PubMed Web of Science ®Google Scholar
• Mochizuki K, Novatchkova M, Loidl J. DNA double-strand breaks, but not crossovers, are required for the reorganization of meiotic nuclei in Tetrahymena. J Cell Sci 2008; 121:2148-58; PMID:18522989; http://dx.doi.org/10.1242/jcs.031799
   PubMed Web of Science ®Google Scholar
• Loidl J, Lukaszewicz A, Howard-Till RA, Koestler T. The Tetrahymena meiotic chromosome bouquet is organized by centromeres and promotes interhomolog recombination. J Cell Sci 2012; 125:5873-80; PMID:22976299; http://dx.doi.org/10.1242/jcs.112664
   PubMed Web of Science ®Google Scholar
• Song XY, Gjoneska E, Ren QH, Taverna SD, Allis CD, Gorovsky MA. Phosphorylation of the SQ H2A.X motif is required for proper meiosis and mitosis in Tetrahymena thermophila. Mol Cell Biol 2007; 27:2648-60.
   PubMed Web of Science ®Google Scholar
• Howard-Till RA, Lukaszewicz A, Loidl J. The recombinases Rad51 and Dmc1 play distinct roles in DNA break repair and recombination partner choice in the meiosis of Tetrahymena. Plos Genet 2011; 7:e1001359; PMID:21483758; http://dx.doi.org/10.1371/journal.pgen.1001359
   PubMed Web of Science ®Google Scholar
• Loidl J, Scherthan H. Organization and pairing of meiotic chromosomes in the ciliate Tetrahymena thermophila. J Cell Sci 2004; 117:5791-801; PMID:15522890; http://dx.doi.org/10.1242/jcs.01504
   PubMed Web of Science ®Google Scholar
• Shodhan A, Lukaszewicz A, Novatchkova M, Loidl J. Msh4 and Msh5 function in SC-independent chiasma formation during the streamlined meiosis of Tetrahymena. Genetics 2014; 198:983-93; PMID:25217051; http://dx.doi.org/10.1534/genetics.114.169698
   PubMed Web of Science ®Google Scholar
• Howard-Till RA, Lukaszewicz A, Novatchkova M, Loidl J. A single cohesin complex performs mitotic and meiotic functions in the protist Tetrahymena. Plos Genet 2013; 9:e1003418; PMID:23555314; http://dx.doi.org/10.1371/journal.pgen.1003418
   PubMedGoogle Scholar
• Miao W, Xiong J, Bowen J, Wang W, Liu YF, Braguinets O, Grigull J, Pearlman RE, Orias E, Gorovsky MA. Microarray analyses of gene expression during the Tetrahymena thermophila life cycle. Plos One 2009; 4:e4429; PMID:19204800; http://dx.doi.org/10.1371/journal.pone.0004429
   PubMed Web of Science ®Google Scholar
• Sugai T, Hiwatashi K. Cytologic and autoradiographic studies of the micronucleus at meiotic prophase in Tetrahymena pyriformis. J Protozool 1974; 21:542-8; PMID:4214068; http://dx.doi.org/10.1111/j.1550-7408.1974.tb03695.x
   PubMedGoogle Scholar
• Morgan DO. The cell cycle: principles of control. London: New Science Press Ltd 2007.
   Google Scholar
• Polager S, Kalma Y, Berkovich E, Ginsberg D. E2Fs up-regulate expression of genes involved in DNA replication, DNA repair and mitosis. Oncogene 2002; 21:437-46; PMID:11821956; http://dx.doi.org/10.1038/sj.onc.1205102
   PubMed Web of Science ®Google Scholar
• Loidl J, Lorenz A. DNA double-strand break formation and repair in Tetrahymena meiosis. Semin Cell Dev Biol 2016; 54:126-34; PMID:26899715; http://dx.doi.org/10.1016/j.semcdb.2016.02.021
   PubMed Web of Science ®Google Scholar
• Drissi R, Dubois ML, Douziech M, Boisvert FM. Quantitative proteomics reveals dynamic interactions of the minichromosome maintenance complex (MCM) in the cellular response to etoposide induced DNA damage. Mol Cell Proteomics 2015; 14:2002-13; PMID:25963833; http://dx.doi.org/10.1074/mcp.M115.048991
   PubMed Web of Science ®Google Scholar
• Shang YH, Li B, Gorovsky MA. Tetrahymena thermophila contains a conventional γ-tubulin that is differentially required for the maintenance of different microtubule-organizing centers. J Cell Biol 2002; 158:1195-206; PMID:12356864; http://dx.doi.org/10.1083/jcb.200205101
   PubMed Web of Science ®Google Scholar
• Kushida Y, Takaine M, Nakano K, Sugai T, Numata O. Dynamic change of cellular localization of microtubule-organizing center during conjugation of ciliate Tetrahymena thermophila. Zool Sci 2015; 32:25-32; PMID:25660693; http://dx.doi.org/10.2108/zs140149
   PubMed Web of Science ®Google Scholar
• Lesca C, Germanier M, Raynaud-Messina B, Pichereaux C, Etievant C, Emond S, Burlet-Schiltz O, Monsarrat B, Wright M, Defais M. DNA damage induce γ-tubulin-Rad51 nuclear complexes in mammalian cells. Oncogene 2005; 24:5165-72; PMID:15897881; http://dx.doi.org/10.1038/sj.onc.1208723
   PubMed Web of Science ®Google Scholar
• Hoog G, Zarrizi R, von Stedingk K, Jonsson K, Alvarado-Kristensson M. Nuclear localization of γ-tubulin affects E2F transcriptional activity and S-phase progression. Faseb J 2011; 25:3815-27; PMID:21788450; http://dx.doi.org/10.1096/fj.11-187484
   PubMed Web of Science ®Google Scholar
• Narbonne-Reveau K, Senger S, Pal M, Herr A, Richardson HE, Asano M, Deak P, Lilly MA. APC/CFzr/Cdh1 promotes cell cycle progression during the Drosophila endocycle. Development 2008; 135:1451-61; PMID:18321983; http://dx.doi.org/10.1242/dev.016295
   PubMed Web of Science ®Google Scholar
• Lammens T, Boudolf V, Kheibarshekan L, Zalmas LP, Gaamouche T, Maes S, Vanstraelen M, Kondorosi E, La Thangue NB, Govaerts W, et al. Atypical E2F activity restrains APC/CCCS52A2 function obligatory for endocycle onset. P Natl Acad Sci USA 2008; 105:14721-6; http://dx.doi.org/10.1073/pnas.0806510105
   PubMed Web of Science ®Google Scholar
• Watrin E, Peters JM. Cohesin and DNA damage repair. Exp Cell Res 2006; 312:2687-93; PMID:16876157; http://dx.doi.org/10.1016/j.yexcr.2006.06.024
   PubMed Web of Science ®Google Scholar
• Sozzani R, Maggio C, Varotto S, Canova S, Bergounioux C, Albani D, Cella R. Interplay between Arabidopsis activating factors E2fb and E2fa in cell cycle progression and development. Plant Physiol 2006; 140:1355-66; PMID:16514015; http://dx.doi.org/10.1104/pp.106.077990
   PubMed Web of Science ®Google Scholar
• DeGregori J. The genetics of the E2F family of transcription factors: shared functions and unique roles. Bba-Rev Cancer 2002; 1602:131-50.
   PubMed Web of Science ®Google Scholar
• Royzman I, Whittaker AJ, OrrWeaver TL. Mutations in Drosophila DP and E2F distinguish G1-S progression from an associated transcriptional program. Gene Dev 1997; 11:1999-2011; PMID:9271122; http://dx.doi.org/10.1101/gad.11.15.1999
   PubMed Web of Science ®Google Scholar
• del Pozo JC, Diaz-Trivino S, Cisneros N, Gutierrez C. The balance between cell division and endoreplication depends on E2Fc-DPb, transcription factors regulated by the ubiquitin-SCFSKP2A pathway in Arabidopsis. Plant Cell 2006; 18:2224-35; PMID:16920782; http://dx.doi.org/10.1105/tpc.105.039651
   PubMed Web of Science ®Google Scholar
• Frolov MV, Huen DS, Stevaux O, Dimova D, Balczarek-Strang K, Elsdon M, Dyson NJ. Functional antagonism between E2F family members. Gene Dev 2001; 15:2146-60; PMID:11511545; http://dx.doi.org/10.1101/gad.903901
   PubMed Web of Science ®Google Scholar
• Rempel RE, Saenz-Robles MT, Storms R, Morham S, Ishida S, Engel A, Jakoi L, Melhem MF, Pipas JM, Smith C, et al. Loss of E2F4 activity leads to abnormal development of multiple cellular lineages. Mol Cell 2000; 6:293-306; PMID:10983977; http://dx.doi.org/10.1016/S1097-2765(00)00030-7
   PubMed Web of Science ®Google Scholar
• Lammens T, Li J, Leone G, De Veylder L. Atypical E2Fs: new players in the E2F transcription factor family. Trends Cell Biol 2009; 19:111-8; PMID:19201609; http://dx.doi.org/10.1016/j.tcb.2009.01.002
   PubMed Web of Science ®Google Scholar
• Orias E, Hamilton EP, Orias JD. Tetrahymena as a laboratory organism: useful strains, cell culture, and cell line maintenance. Method Cell Biol 2000; 62:189-211; http://dx.doi.org/10.1016/S0091-679X(08)61530-7
   PubMed Web of Science ®Google Scholar
• Mochizuki K. High efficiency transformation of Tetrahymena using a codon-optimized neomycin resistance gene. Gene 2008; 425:79-83; PMID:18775482; http://dx.doi.org/10.1016/j.gene.2008.08.007
   PubMed Web of Science ®Google Scholar
• CassidyHanley D, Bowen J, Lee JH, Cole E, VerPlank LA, Gaertig J, Gorovsky MA, Bruns PJ. Germline and somatic transformation of mating Tetrahymena thermophila by particle bombardment. Genetics 1997; 146:135-47; PMID:9136007
   PubMed Web of Science ®Google Scholar
• Lukaszewicz A, Howard-Till RA, Novatchkova M, Mochizuki K, Loidl J. Mre11 and Com1/Sae2 are required for double-strand break repair and efficient chromosome pairing during meiosis of the protist Tetrahymena. Chromosoma 2010; 119:505-18; PMID:20422424; http://dx.doi.org/10.1007/s00412-010-0274-9
   PubMed Web of Science ®Google Scholar
• Howard-Till RA, Lukaszewicz A, Loidl J. The recombinases Rad51 and Dmc1 play distinct roles in DNA break repair and recombination partner choice in the meiosis of Tetrahymena. Plos Genet 2011; 7:e1001359; PMID:21483758; http://dx.doi.org/10.1371/journal.pgen.1001359
   PubMed Web of Science ®Google Scholar
• Loidl J, Mochizuki K. Tetrahymena meiotic nuclear reorganization is induced by a checkpoint kinase-dependent response to DNA damage. Mol Biol Cell 2009; 20:2428-37; PMID:19297526; http://dx.doi.org/10.1091/mbc.E08-10-1058
   PubMed Web of Science ®Google Scholar
• Gao S, Xiong J, Zhang CC, Berquist BR, Yang RD, Zhao M, Molascon AJ, Kwiatkowski SY, Yuan DX, Qin ZH, et al. Impaired replication elongation in Tetrahymena mutants deficient in histone H3 Lys 27 monomethylation. Gene Dev 2013; 27:1662-79; PMID:23884606; http://dx.doi.org/10.1101/gad.218966.113
   PubMed Web of Science ®Google Scholar
• Xiong J, Lu XY, Lu YM, Zeng HH, Yuan DX, Feng LF, Chang Y, Bowen J, Gorovsky M, Fu CJ, et al. Tetrahymena Gene Expression Database (TGED): a resource of microarray data and co-expression analyses for Tetrahymena. Sci China Life Sci 2011; 54:65-7; PMID:21253873; http://dx.doi.org/10.1007/s11427-010-4114-1
   PubMed Web of Science ®Google Scholar
• Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389-402; PMID:9254694; http://dx.doi.org/10.1093/nar/25.17.3389
   PubMed Web of Science ®Google Scholar
• Ramirez-Parra E, Frundt C, Gutierrez C. A genome-wide identification of E2F-regulated genes in Arabidopsis. Plant J 2003; 33:801-11; PMID:12609051; http://dx.doi.org/10.1046/j.1365-313X.2003.01662.x
   PubMed Web of Science ®Google Scholar
• Kirienko NV, Fay DS. Transcriptome profiling of the C. elegans Rb ortholog reveals diverse developmental roles. Dev Biol 2007; 305:674-84; PMID:17368442; http://dx.doi.org/10.1016/j.ydbio.2007.02.021
   PubMed Web of Science ®Google Scholar
• Kehoe SM, Oka M, Hankowski KE, Reichert N, Garcia S, McCarrey JR, Gaubatz S, Terada N. A conserved E2F6-binding element in murine meiosis-specific gene promoters. Biol Reprod 2008; 79:921-30; PMID:18667754; http://dx.doi.org/10.1095/biolreprod.108.067645
   PubMed Web of Science ®Google Scholar
• Lincker F, Messmer M, Houlne G, Devic M, Chaboute ME. E2F factors rate controls the dual role of CDE/E2F composite element: a model of E2F-regulated gene expression in plant development. Febs Lett 2006; 580:5167-71; PMID:16962586; http://dx.doi.org/10.1016/j.febslet.2006.08.067
   PubMed Web of Science ®Google Scholar
• Korenjak M, Anderssen E, Ramaswamy S, Whetstine JR, Dyson NJ. RBF binding to both canonical E2F targets and noncanonical targets depends on functional dE2F/dDP complexes. Mol Cell Biol 2012; 32:4375-87; PMID:22927638; http://dx.doi.org/10.1128/MCB.00536-12
   PubMed Web of Science ®Google Scholar
• Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, et al. Clustal W and clustal X version 2.0. Bioinformatics 2007; 23:2947-8; PMID:17846036; http://dx.doi.org/10.1093/bioinformatics/btm404
   PubMed Web of Science ®Google Scholar
• Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725-9; PMID:24132122; http://dx.doi.org/10.1093/molbev/mst197
   PubMed Web of Science ®Google Scholar
• Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu SN, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, et al. CDD: NCBI's conserved domain database. Nucleic Acids Res 2015; 43:D222-6; PMID:25414356; http://dx.doi.org/10.1093/nar/gku1221
   PubMed Web of Science ®Google Scholar
• Mar JC, Wells CA, Quackenbush J. Defining an informativeness metric for clustering gene expression data. Bioinformatics 2011; 27:1094-100; PMID:21330289; http://dx.doi.org/10.1093/bioinformatics/btr074
   PubMed Web of Science ®Google Scholar
• Xiong J, Lu XY, Zhou ZM, Chang Y, Yuan DX, Tian M, Zhou ZG, Wang L, Fu CJ, Orias E, et al. Transcriptome analysis of the model protozoan, Tetrahymena thermophila, using deep RNA sequencing. Plos One 2012; 7:e30630; PMID:22347391; http://dx.doi.org/10.1371/journal.pone.0030630
   PubMed Web of Science ®Google Scholar
• Wu ZP, Wang X, Zhang XG. Using non-uniform read distribution models to improve isoform expression inference in RNA-Seq. Bioinformatics 2011; 27:502-8; PMID:21169371; http://dx.doi.org/10.1093/bioinformatics/btq696
   PubMed Web of Science ®Google Scholar
• Kim D, Salzberg SL. TopHat-Fusion: an algorithm for discovery of novel fusion transcripts. Genome Biol 2011; 12:R72; PMID:21835007; http://dx.doi.org/10.1186/gb-2011-12-8-r72
   PubMed Web of Science ®Google Scholar
• Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012; 7:562-78; PMID:22383036; http://dx.doi.org/10.1038/nprot.2012.016
   PubMed Web of Science ®Google Scholar
• Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. Gene Ontology: tool for the unification of biology. Nat Genet 2000; 25:25-9; PMID:10802651; http://dx.doi.org/10.1038/75556
   PubMed Web of Science ®Google Scholar
• Maere S, Heymans K, Kuiper M. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 2005; 21:3448-9; PMID:15972284; http://dx.doi.org/10.1093/bioinformatics/bti551
   PubMed Web of Science ®Google Scholar