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Specificity factors in cytoplasmic polyadenylation

Amanda Charlesworth, Hedda A. Meijer, Cornelia H. de Moor

WIREs RNA · 2013 · Review

doi:10.1002/wrna.1171

Abstract

Poly(A) tail elongation after export of an messenger RNA ( mRNA ) to the cytoplasm is called cytoplasmic polyadenylation. It was first discovered in oocytes and embryos, where it has roles in meiosis and development. In recent years, however, has been implicated in many other processes, including synaptic plasticity and mitosis. This review aims to introduce cytoplasmic polyadenylation with an emphasis on the factors and elements mediating this process for different mRNAs and in different animal species. We will discuss the RNA sequence elements mediating cytoplasmic polyadenylation in the 3′ untranslated regions of mRNAs , including the CPE , MBE , TCS , eCPE , and C‐ CPE . In addition to describing the role of general polyadenylation factors, we discuss the specific RNA binding protein families associated with cytoplasmic polyadenylation elements, including CPEB ( CPEB1 , CPEB2 , CPEB3 , and CPEB4 ), Pumilio ( PUM2 ), Musashi ( MSI1 , MSI2 ), zygote arrest ( ZAR2 ), ELAV like proteins ( ELAVL1 , HuR ), poly(C) binding proteins ( PCBP2 , αCP2 , hnRNP‐E2 ), and Bicaudal C ( BICC1 ). Some emerging themes in cytoplasmic polyadenylation will be highlighted. To facilitate understanding for those working in different organisms and fields, particularly those who are analyzing high throughput data, HUGO gene nomenclature for the human orthologs is used throughout. Where human orthologs have not been clearly identified, reference is made to protein families identified in man. WIREs RNA 2013, 4:437–461. doi: 10.1002/wrna.1171 This article is categorized under: RNA Interactions with Proteins and Other Molecules > Protein–RNA Interactions: Functional Implications Translation > Translation Regulation RNA Processing > 3' End Processing

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    Not in our library10.1016/j.cell.2004.10.029

  96. 96.

    Hake LE, Richter JD. CPEB is a specificity factor that mediates cytoplasmic polyadenylation during Xenopus oocyte maturation. Cell. 1994;79:617-627.

    Not in our library10.1016/0092-8674(94)90547-9

  97. 97.

    Ballantyne S, Daniel DL, Wickens M. A dependent pathway of cytoplasmic polyadenylation reactions linked to cell cycle control by c-mos and CDK1 activation. Mol Biol Cell. 1997;8:1633-1648.

    Not in our library10.1091/mbc.8.8.1633

  98. 98.

    Barkoff AF, Dickson KS, Gray NK, Wickens M. Translational control of cyclin B1 mRNA during meiotic maturation: coordinated repression and cytoplasmic polyadenylation. Dev Biol. 2000;220:97-109.

    Not in our library10.1006/dbio.2000.9613

  99. 99.

    Pique M, Lopez JM, Foissac S, Guigo R, Mendez R. A combinatorial code for CPE-mediated translational control. Cell. 2008;132:434-448.

    Not in our library10.1016/j.cell.2007.12.038

  100. 100.

    Igea A, Mendez R. Meiosis requires a translational positive loop where CPEB1 ensues its replacement by CPEB4. EMBO J. 2010;29:2182-2193.

    Not in our library10.1038/emboj.2010.111

  101. 101.

    Mendez R, Barnard D, Richter JD. Differential mRNA translation and meiotic progression require Cdc2-mediated CPEB destruction. EMBO J. 2002;21:1833-1844.

    Not in our library10.1093/emboj/21.7.1833

  102. 102.

    Chen J, Melton C, Suh N, Oh JS, Horner K, Xie F, Sette C, Blelloch R, Conti M. Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. Genes Dev. 2011;25:755-766.

    Not in our library10.1101/gad.2028911

  103. 103.

    Charlesworth A, Wilczynska A, Thampi P, Cox LL, MacNicol AM. Musashi regulates the temporal order of mRNA translation during Xenopus oocyte maturation. EMBO J. 2006;25:2792-2801.

    Not in our library10.1038/sj.emboj.7601159

  104. 104.

    McGrew LL, Richter JD. Translational control by cytoplasmic polyadenylation during Xenopus oocyte maturation: Characterization of cis and trans elements and regulation by cyclin/MPF. EMBO J. 1990;9:3743-3751.

    Not in our library10.1002/j.1460-2075.1990.tb07587.x

  105. 105.

    Vishnu MR, Sumaroka M, Klein PS, Liebhaber SA. The poly(rC)-binding protein αCP2 is a noncanonical factor in X. laevis cytoplasmic polyadenylation. RNA. 2011;17:944-956.

    Not in our library10.1261/rna.2587411

  106. 106.

    Simon R, Tassan J-P, Richter JD. Translational control by poly(A) elongation during Xenopus development: differential repression and enhancement by a novel cytoplasmic polyadenylation element. Genes Dev. 1992;6:2580-2591.

    Not in our library10.1101/gad.6.12b.2580

  107. 107.

    Paris J, Richter JD. Maturation-specific polyadenylation and translational control: diversity of cytoplasmic polyadenylation elements, influence of poly(A) tail size, and formation of stable polyadenylation complexes. Mol Cell Biol. 1990;10:5634-5645.

    Not in our library10.1128/mcb.10.11.5634-5645.1990

  108. 108.

    Sheets MD, Fox CA, Hunt T, Vande Woude G, Wickens M. The 3′-untranslated regions of c-mos and cyclin mRNAs stimulate translation by regulating cytoplasmic polyadenylation. Genes Dev. 1994;8:926-938.

    Not in our library10.1101/gad.8.8.926

  109. 109.

    Tay J, Hodgman R, Richter JD. The control of cyclin B1 mRNA translation during mouse oocyte maturation. Dev Biol. 2000;221:1-9.

    Not in our library10.1006/dbio.2000.9669

  110. 110.

    Oruganty-Das A, Ng T, Udagawa T, Goh EL, Richter JD. Translational control of mitochondrial energy production mediates neuron morphogenesis. Cell Metab. 2012;16:789-800.

    Not in our library10.1016/j.cmet.2012.11.002

  111. 111.

    Mendez R, Hake LE, Andresson T, Littlepage LE, Ruderman JV, Richter JD. Phosphorylation of CPE binding factor by Eg2 regulates translation of c-mos mRNA. Nature. 2000;404:302-307.

    Not in our library10.1038/35005126

  112. 112.

    Novoa I, Gallego J, Ferreira PG, Mendez R. Mitotic cell-cycle progression is regulated by CPEB1 and CPEB4-dependent translational control. Nat Cell Biol. 2010.

    Not in our library10.1038/ncb2046

  113. 113.

    Huang YS, Kan MC, Lin CL, Richter JD. CPEB3 and CPEB4 in neurons: analysis of RNA-binding specificity and translational control of AMPA receptor GluR2 mRNA. EMBO J. 2006;25:4865-4876.

    Not in our library10.1038/sj.emboj.7601322

  114. 114.

    Imai T, Tokunaga A, Yoshida T, Hashimoto M, Mikoshiba K, Weinmaster G, Nakafuku M, Okano H. The neural RNA-binding protein Musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA. Mol Cell Biol. 2001;21:3888-3900.

    Not in our library10.1128/mcb.21.12.3888-3900.2001

  115. 115.

    Charlesworth A, Ridge JA, King LA, MacNicol MC, MacNicol AM. A novel regulatory element determines the timing of Mos mRNA translation during Xenopus oocyte maturation. EMBO J. 2002;21:2798-2806.

    Not in our library10.1093/emboj/21.11.2798

  116. 116.

    Arumugam K, Wang Y, Hardy LL, MacNicol MC, MacNicol AM. Enforcing temporal control of maternal mRNA translation during oocyte cell-cycle progression. EMBO J. 2009;29:387-397.

    Not in our library10.1038/emboj.2009.337

  117. 117.

    Charlesworth A, Cox LL, MacNicol AM. Cytoplasmic polyadenylation element (CPE)- and CPE-binding protein (CPEB)-independent mechanisms regulate early class maternal mRNA translational activation in Xenopus oocytes. J Biol Chem. 2004;279:17650-17659.

    Not in our library10.1074/jbc.m313837200

  118. 118.

    Simon R, Wu L, Richter JD. Cytoplasmic polyadenylation of activin receptor mRNA and the control of pattern formation in Xenopus development. Dev Biol. 1996;179:239-250.

    Not in our library10.1006/dbio.1996.0254

  119. 119.

    Wu L, Good PJ, Richter JD. The 36-kilodalton embryonic-type cytoplasmic polyadenylation element- binding protein in Xenopus laevis is ElrA, a member of the ELAV family of RNA-binding proteins. Mol Cell Biol. 1997;17:6402-6409.

    Not in our library10.1128/mcb.17.11.6402

  120. 120.

    Campbell ZT, Bhimsaria D, Valley CT, Rodriguez-Martinez JA, Menichelli E, Williamson JR, Ansari AZ, Wickens M. Cooperativity in RNA-protein interactions: global analysis of RNA binding specificity. Cell Rep. 2012;1:570-581.

    Not in our library10.1016/j.celrep.2012.04.003

  121. 121.

    Campbell ZT, Menichelli E, Friend K, Wu J, Kimble J, Williamson JR, Wickens M. Identification of a conserved interface between PUF and CPEB proteins. J Biol Chem. 2012;287:18854-18862.

    Not in our library10.1074/jbc.m112.352815

  122. 122.

    Suh N, Crittenden SL, Goldstrohm A, Hook B, Thompson B, Wickens M, Kimble J. FBF and its dual control of gld-1 expression in the Caenorhabditis elegans germline. Genetics. 2009;181:1249-1260.

    Not in our library10.1534/genetics.108.099440

  123. 123.

    Schmid M, Kuchler B, Eckmann CR. Two conserved regulatory cytoplasmic poly(A) polymerases, GLD-4 and GLD-2, regulate meiotic progression in C. elegans. Genes Dev. 2009;23:824-836.

    Not in our library10.1101/gad.494009

  124. 124.

    Suh N, Jedamzik B, Eckmann CR, Wickens M, Kimble J. The GLD-2 poly(A) polymerase activates gld-1 mRNA in the Caenorhabditis elegans germ line. Proc Natl Acad Sci USA. 2006;103:15108-15112.

    Not in our library10.1073/pnas.0607050103

  125. 125.

    Jenkins HT, Malkova B, Edwards TA. Kinked β-strands mediate high-affinity recognition of mRNA targets by the germ-cell regulator DAZL. Proc Natl Acad Sci USA. 2011;108:18266-18271.

    Not in our library10.1073/pnas.1105211108

  126. 126.

    Padmanabhan K, Richter JD. Regulated Pumilio-2 binding controls RINGO/Spy mRNA translation and CPEB activation. Genes Dev. 2006;20:199-209.

    Not in our library10.1101/gad.1383106

  127. 127.

    Collier B, Gorgoni B, Loveridge C, Cooke HJ, Gray NK. The DAZL family proteins are PABP-binding proteins that regulate translation in germ cells. EMBO J. 2005;24:2656-2666.

    Not in our library10.1038/sj.emboj.7600738

  128. 128.

    Moore FL, Jaruzelska J, Fox MS, Urano J, Firpo MT, Turek PJ, Dorfman DM, Pera RA. Human Pumilio-2 is expressed in embryonic stem cells and germ cells and interacts with DAZ (Deleted in AZoospermia) and DAZ-like proteins. Proc Natl Acad Sci USA. 2003;100:538-543.

    Not in our library10.1073/pnas.0234478100

  129. 129.

    Nakahata S, Kawamoto S. Tissue-dependent isoforms of mammalian Fox-1 homologs are associated with tissue-specific splicing activities. Nucleic Acids Res. 2005;33:2078-2089.

    Not in our library10.1093/nar/gki338

  130. 130.

    Yeo GW, Coufal NG, Liang TY, Peng GE, Fu XD, Gage FH. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat Struct Mol Biol. 2009;16:130-137.

    Not in our library10.1038/nsmb.1545

  131. 131.

    Papin C, Rouget C, Mandart E. Xenopus Rbm9 is a novel interactor of XGld2 in the cytoplasmic polyadenylation complex. FEBS J. 2008;275:490-503.

    Not in our library10.1111/j.1742-4658.2007.06216.x

  132. 132.

    Didiot MC, Tian Z, Schaeffer C, Subramanian M, Mandel JL, Moine H. The G-quartet containing FMRP binding site in FMR1 mRNA is a potent exonic splicing enhancer. Nucleic Acids Res. 2008;36:4902-4912.

    Not in our library10.1093/nar/gkn472

  133. 133.

    Zalfa F, Adinolfi S, Napoli I, Kuhn-Holsken E, Urlaub H, Achsel T, Pastore A, Bagni C. Fragile X mental retardation protein (FMRP) binds specifically to the brain cytoplasmic RNAs BC1/BC200 via a novel RNA-binding motif. J Biol Chem. 2005;280:33403-33410.

    Not in our library10.1074/jbc.m504286200

  134. 134.

    Darnell JC, Van Driesche SJ, Zhang C, Hung KY, Mele A, Fraser CE, Stone EF, Chen C, Fak JJ, Chi SW, et al. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell. 2011;146:247-261.

    Not in our library10.1016/j.cell.2011.06.013

  135. 135.

    Ascano M, Mukherjee N, Bandaru P, Miller JB, Nusbaum JD, Corcoran DL, Langlois C, Munschauer M, Dewell S, Hafner M, et al. FMRP targets distinct mRNA sequence elements to regulate protein expression. Nature. 2012;492:382-386.

    Not in our library10.1038/nature11737

  136. 136.

    Kwak JE, Drier E, Barbee SA, Ramaswami M, Yin JC, Wickens M. GLD2 poly(A) polymerase is required for long-term memory. Proc Natl Acad Sci USA. 2008;105:14644-14649.

    Not in our library10.1073/pnas.0803185105

  137. 137.

    Costa A, Wang Y, Dockendorff TC, Erdjument-Bromage H, Tempst P, Schedl P, Jongens TA. The Drosophila fragile X protein functions as a negative regulator in the orb autoregulatory pathway. Dev Cell. 2005;8:331-342.

    Not in our library10.1016/j.devcel.2005.01.011

  138. 138.

    Kwak JE, Wang L, Ballantyne S, Kimble J, Wickens M. Mammalian GLD-2 homologs are poly(A) polymerases. Proc Natl Acad Sci USA. 2004;101:4407-4412.

    Not in our library10.1073/pnas.0400779101

  139. 139.

    Benoit P, Papin C, Kwak JE, Wickens M, Simonelig M. PAP- and GLD-2-type poly(A) polymerases are required sequentially in cytoplasmic polyadenylation and oogenesis in Drosophila. Development. 2008;135:1969-1979.

    Not in our library10.1242/dev.021444

  140. 140.

    Gebauer F, Richter JD. Cloning and characterization of a Xenopus poly(A) polymerase. Mol Cell Biol. 1995;15:1422-1430.

    Not in our library10.1128/mcb.15.3.1422

  141. 141.

    Bilger A, Fox CA, Wahle E, Wickens M. Nuclear polyadenylation factors recognize cytoplasmic polyadenylation elements. Genes Dev. 1994;8:1106-1116.

    Not in our library10.1101/gad.8.9.1106

  142. 142.

    Zhao WQ, Manley JL. Complex alternative RNA processing generates an unexpected diversity of poly(A) polymerase isoforms. Mol Cell Biol. 1996;16:2378-2386.

    Not in our library10.1128/mcb.16.5.2378

  143. 143.

    Nakanishi T, Kubota H, Ishibashi N, Kumagai S, Watanabe H, Yamashita M, Kashiwabara S, Miyado K, Baba T. Possible role of mouse poly(A) polymerase mGLD-2 during oocyte maturation. Dev Biol. 2006;289:115-126.

    Not in our library10.1016/j.ydbio.2005.10.017

  144. 144.

    Nakanishi T, Kumagai S, Kimura M, Watanabe H, Sakurai T, Kimura M, Kashiwabara S, Baba T. Disruption of mouse poly(A) polymerase mGLD-2 does not alter polyadenylation status in oocytes and somatic cells. Biochem Biophys Res Commun. 2007;364:14-19.

    Not in our library10.1016/j.bbrc.2007.09.096

  145. 145.

    Burns DM, D'Ambrogio A, Nottrott S, Richter JD. CPEB and two poly(A) polymerases control miR-122 stability and p53 mRNA translation. Nature. 2011;473:105-108.

    Not in our library10.1038/nature09908

  146. 146.

    Choi HS, Lee SH, Kim H, Lee Y. Germ cell-specific gene 1 targets testis-specific poly(A) polymerase to the endoplasmic reticulum through protein-protein interactions. FEBS Lett. 2008;582:1203-1209.

    Not in our library10.1016/j.febslet.2008.01.065

  147. 147.

    Kashiwabara S, Zhuang T, Yamagata K, Noguchi J, Fukamizu A, Baba T. Identification of a novel isoform of poly(A) polymerase, TPAP, specifically present in the cytoplasm of spermatogenic cells. Dev Biol. 2000;228:106-115.

    Not in our library10.1006/dbio.2000.9894

  148. 148.

    Kashiwabara S, Noguchi J, Zhuang T, Ohmura K, Honda A, Sugiura S, Miyamoto K, Takahashi S, Inoue K, Ogura A, et al. Regulation of spermatogenesis by testis-specific, cytoplasmic poly(A) polymerase TPAP. Science. 2002;298:1999-2002.

    Not in our library10.1126/science.1074632

  149. 149.

    Kashiwabara SI, Nakanishi T, Kimura M, Baba T. Non-canonical poly(A) polymerase in mammalian gametogenesis. Biochim Biophys Acta. 2008;1779:230-238.

    Not in our library10.1016/j.bbagrm.2008.01.004

  150. 150.

    Zhuang T, Kashiwabara S, Noguchi J, Baba T. Transgenic expression of testis-specific poly(A) polymerase TPAP in wild-type and TPAP-deficient mice. J Reprod Dev. 2004;50:207-213.

    Not in our library10.1262/jrd.50.207

  151. 151.

    Fernandez-Miranda G, Mendez R. The CPEB-family of proteins, translational control in senescence and cancer. Ageing Res Rev. 2012;11:460-472.

    Not in our library10.1016/j.arr.2012.03.004

  152. 152.

    Wang XP, Cooper NG. Comparative in silico analyses of cpeb1-4 with functional predictions. Bioinform Biol Insights. 2010;4:61-83.

    Not in our library10.4137/bbi.s5087

  153. 153.

    Hake LE, Mendez R, Richter JD. Specificity of RNA binding by CPEB: requirement for RNA recognition motifs and a novel zinc finger. Mol Cell Biol. 1998;18:685-693.

    Not in our library10.1128/mcb.18.2.685

  154. 154.

    Stebbins-Boaz B, Hake LE, Richter JD. CPEB controls the cytoplasmic polyadenylation of cyclin, Cdk2 and c-mos mRNAs and is necessary for oocyte maturation in Xenopus. EMBO J. 1996;15:2582-2592.

    Not in our library

  155. 155.

    Groisman I, Huang YS, Mendez R, Cao Q, Richter JD. Translational control of embryonic cell division by CPEB and maskin. Cold Spring Harb Symp Quant Biol. 2001;66:345-351.

    Not in our library10.1101/sqb.2001.66.345

  156. 156.

    Tay J, Richter JD. Germ cell differentiation and synaptonemal complex formation are disrupted in CPEB knockout mice. Dev Cell. 2001;1:201-213.

    Not in our library10.1016/s1534-5807(01)00025-9

  157. 157.

    Castagnetti S, Ephrussi A. Orb and a long poly(A) tail are required for efficient oskar translation at the posterior pole of the Drosophila oocyte. Development. 2003;130:835-843.

    Not in our library10.1242/dev.00309

  158. 158.

    Jin SW, Arno N, Cohen A, Shah A, Xu Q, Chen N, Ellis RE. In Caenorhabditis elegans, the RNA-binding domains of the cytoplasmic polyadenylation element binding protein FOG-1 are needed to regulate germ cell fates. Genetics. 2001;159:1617-1630.

    Not in our library10.1093/genetics/159.4.1617

  159. 159.

    Luitjens C, Gallegos M, Kraemer B, Kimble J, Wickens M. CPEB proteins control two key steps in spermatogenesis in C. elegans. Genes Dev. 2000;14:2596-2609.

    Not in our library10.1101/gad.831700

  160. 160.

    Chang JS, Tan L, Schedl P. The Drosophila CPEB homolog, orb, is required for oskar protein expression in oocytes. Dev Biol. 1999;215:91-106.

    Not in our library10.1006/dbio.1999.9444

  161. 161.

    Juge F, Zaessinger S, Temme C, Wahle E, Simonelig M. Control of poly(A) polymerase level is essential to cytoplasmic polyadenylation and early development in Drosophila. EMBO J. 2002;21:6603-6613.

    Not in our library10.1093/emboj/cdf633

  162. 162.

    Dickson KS, Bilger A, Ballantyne S, Wickens MP. The cleavage and polyadenylation specificity factor in Xenopus laevis oocytes is a cytoplasmic factor involved in regulated polyadenylation. Mol Cell Biol. 1999;19:5707-5717.

    Not in our library10.1128/mcb.19.8.5707

  163. 163.

    Kim JH, Richter JD. Opposing polymerase-deadenylase activities regulate cytoplasmic polyadenylation. Mol Cell. 2006;24:173-183.

    Not in our library10.1016/j.molcel.2006.08.016

  164. 164.

    van EttenJ, Schagat TL, Hrit J, Weidmann C, Brumbaugh J, Coon JJ, Goldstrohm AC. Human Pumilio proteins recruit multiple deadenylases to efficiently repress messenger RNAs. J Biol Chem. 2012;287:36370-36383.

    Not in our library10.1074/jbc.m112.373522

  165. 165.

    Friend K, Brook M, Bezirci FB, Sheets MD, Gray NK, Seli E. Embryonic poly(A)-binding protein (ePAB) phosphorylation is required for Xenopus oocyte maturation. Biochem J. 2012;445:93-100.

    Not in our library10.1042/bj20120304

  166. 166.

    Mendez R, Murthy KG, Ryan K, Manley JL, Richter JD. Phosphorylation of CPEB by Eg2 mediates the recruitment of CPSF into an active cytoplasmic polyadenylation complex. Mol Cell. 2000;6:1253-1259.

    Not in our library10.1016/s1097-2765(00)00121-0

  167. 167.

    Barnard DC, Cao Q, Richter JD. Differential phosphorylation controls Maskin association with eukaryotic translation initiation factor 4E and localization on the mitotic apparatus. Mol Cell Biol. 2005;25:7605-7615.

    Not in our library10.1128/mcb.25.17.7605-7615.2005

  168. 168.

    Kim JH, Richter JD. RINGO/cdk1 and CPEB mediate poly(A) tail stabilization and translational regulation by ePAB. Genes Dev. 2007;21:2571-2579.

    Not in our library10.1101/gad.1593007

  169. 169.

    Cao Q, Richter JD. Dissolution of the maskin-eIF4E complex by cytoplasmic polyadenylation and poly(A)-binding protein controls cyclin B1 mRNA translation and oocyte maturation. EMBO J. 2002;21:3852-3862.

    Not in our library10.1093/emboj/cdf353

  170. 170.

    Hägele S, Kuhn U, Boning M, Katschinski DM. Cytoplasmic polyadenylation-element-binding protein (CPEB)1 and 2 bind to the HIF-1α mRNA 3′-UTR and modulate HIF-1α protein expression. Biochem J. 2009;417:235-246.

    Not in our library10.1042/bj20081353

  171. 171.

    Nairismagi ML, Vislovukh A, Meng Q, Kratassiouk G, Beldiman C, Petretich M, Groisman R, Fuchtbauer EM, Harel-Bellan A, Groisman I. Translational control of TWIST1 expression in MCF-10A cell lines recapitulating breast cancer progression. Oncogene. 2012;13:4960-4966.

    Not in our library10.1038/onc.2011.650

  172. 172.

    Dickson KS, Thompson SR, Gray NK, Wickens M. Poly(A) polymerase and the regulation of cytoplasmic polyadenylation. J Biol Chem. 2001;276:41810-41816.

    Not in our library10.1074/jbc.m103030200

  173. 173.

    Nakahata S, Kotani T, Mita K, Kawasaki T, Katsu Y, Nagahama Y, Yamashita M. Involvement of Xenopus Pumilio in the translational regulation that is specific to cyclin B1 mRNA during oocyte maturation. Mech Dev. 2003;120:865-880.

    Not in our library10.1016/s0925-4773(03)00160-6

  174. 174.

    Tucker M, Staples RR, Valencia-Sanchez MA, Muhlrad D, Parker R. Ccr4p is the catalytic subunit of a Ccr4p/Pop2p/Notp mRNA deadenylase complex in Saccharomyces cerevisiae. EMBO J. 2002;21:1427-1436.

    Not in our library10.1093/emboj/21.6.1427

  175. 175.

    Wreden C, Verrotti AC, Schisa JA, Lieberfarb ME, Strickland S. Nanos and pumilio establish embryonic polarity in Drosophila by promoting posterior deadenylation of hunchback mRNA. Development. 1997;124:3015-3023.

    Not in our library10.1242/dev.124.15.3015

  176. 176.

    Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A, Schultz J, Rick JM, Michon AM, Cruciat CM, et al. Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature. 2002;415:141-147.

    Not in our library10.1038/415141a

  177. 177.

    Hodgman R, Tay J, Mendez R, Richter JD. CPEB phosphorylation and cytoplasmic polyadenylation are catalyzed by the kinase IAK1/Eg2 in maturing mouse oocytes. Development. 2001;128:2815-2822.

    Not in our library10.1242/dev.128.14.2815

  178. 178.

    Tay J, Hodgman R, Sarkissian M, Richter JD. Regulated CPEB phosphorylation during meiotic progression suggests a mechanism for temporal control of maternal mRNA translation. Genes Dev. 2003;17:1457-1462.

    Not in our library10.1101/gad.1071403

  179. 179.

    Keady BT, Kuo P, Martinez SE, Yuan L, Hake LE. MAPK interacts with XGef and is required for CPEB activation during meiosis in Xenopus oocytes. J Cell Sci. 2007;120:1093-1103.

    Not in our library10.1242/jcs.03416

  180. 180.

    Kuo P, Runge E, Lu X, Hake LE. XGef influences XRINGO/CDK1 signaling and CPEB activation during Xenopus oocyte maturation. Differentiation. 2010;81:133-140.

    Not in our library10.1016/j.diff.2010.11.001

  181. 181.

    Frank-Vaillant M, Haccard O, Thibier C, Ozon R, Arlot-Bonnemains Y, Prigent C, Jessus C. Progesterone regulates the accumulation and the activation of Eg2 kinase in Xenopus oocytes. J Cell Sci. 2000;113:1127-1138.

    Not in our library10.1242/jcs.113.7.1127

  182. 182.

    Ma C, Cummings C, Liu XJ. Biphasic activation of Aurora-A kinase during the meiosis I- meiosis II transition in Xenopus oocytes. Mol Cell Biol. 2003;23:1703-1716.

    Not in our library10.1128/mcb.23.5.1703-1716.2003

  183. 183.

    Maton G, Thibier C, Castro A, Lorca T, Prigent C, Jessus C. Cdc2-cyclin B triggers H3 kinase activation of Aurora-A in Xenopus oocytes. J Biol Chem. 2003;278:21439-21449.

    Not in our library10.1074/jbc.m300811200

  184. 184.
  185. 185.

    Vardy L, Pesin JA, Orr-Weaver TL. Regulation of Cyclin A protein in meiosis and early embryogenesis. Proc Natl Acad Sci USA. 2009;106:1838-1843.

    Not in our library10.1073/pnas.0813237106

  186. 186.

    Bouvet P, Omilli F, Arlot-Bonnemains Y, Legagneux V, Roghi C, Bassez T, Osborne HB. The deadenylation conferred by the 3′ untranslated region of a developmentally controlled mRNA in Xenopus embryos is switched to polyadenylation by deletion of a short sequence element. Mol Cell Biol. 1994;14:1893-1900.

    Not in our library10.1128/mcb.14.3.1893-1900.1994

  187. 187.

    Rouhana L, Wickens M. Autoregulation of GLD-2 cytoplasmic poly(A) polymerase. RNA. 2007;13:188-199.

    Not in our library10.1261/rna.333507

  188. 188.

    Tan L, Chang JS, Costa A, Schedl P. An autoregulatory feedback loop directs the localized expression of the Drosophila CPEB protein Orb in the developing oocyte. Development. 2001;128:1159-1169.

    Not in our library10.1242/dev.128.7.1159

  189. 189.

    Wong LC, Schedl P. Cup blocks the precocious activation of the orb autoregulatory loop. PLoS One. 2011;6:e28261.

    Not in our library10.1371/journal.pone.0028261

  190. 190.

    Reverte CG, Ahearn MD, Hake LE. CPEB degradation during Xenopus oocyte maturation requires a PEST domain and the 26S proteasome. Dev Biol. 2001;231:447-458.

    Not in our library10.1006/dbio.2001.0153

  191. 191.

    Setoyama D, Yamashita M, Sagata N. Mechanism of degradation of CPEB during Xenopus oocyte maturation. Proc Natl Acad Sci USA. 2007;104:18001-18006.

    Not in our library10.1073/pnas.0706952104

  192. 192.

    Lin CL, Huang YT, Richter JD. Transient CPEB dimerization and translational control. RNA. 2012;18:1050-1061.

    Not in our library10.1261/rna.031682.111

  193. 193.

    Sagata N, Oskarsson M, Copeland T, Brumbaugh J, Vande Woude GF. Function of c-mos proto-oncogene product in meiotic maturation in Xenopus oocytes. Nature. 1988;335:519-525.

    Not in our library10.1038/335519a0

  194. 194.

    Sheets MD, Wu M, Wickens M. Polyadenylation of c-mos mRNA as a control point in Xenopus meiotic maturation. Nature. 1995;374:511-516.

    Not in our library10.1038/374511a0

  195. 195.

    De Moor CH, Richter JD. The Mos pathway regulates cytoplasmic polyadenylation in Xenopus oocytes. Mol Cell Biol. 1997;17:6419-6426.

    Not in our library10.1128/mcb.17.11.6419

  196. 196.

    Belloc E, Pique M, Mendez R. Sequential waves of polyadenylation and deadenylation define a translation circuit that drives meiotic progression. Biochem Soc Trans. 2008;36:665-670.

    Not in our library10.1042/bst0360665

  197. 197.

    Racki WJ, Richter JD. CPEB controls oocyte growth and follicle development in the mouse. Development. 2006;133:4527-4537.

    Not in our library10.1242/dev.02651

  198. 198.

    Gebauer F, Xu W, Cooper GM, Richter JD. Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J. 1994;13:5712-5720.

    Not in our library10.1002/j.1460-2075.1994.tb06909.x

  199. 199.

    Seli E, Lalioti MD, Flaherty SM, Sakkas D, Terzi N, Steitz JA. An embryonic poly(A)-binding protein (ePAB) is expressed in mouse oocytes and early preimplantation embryos. Proc Natl Acad Sci USA. 2005;102:367-372.

    Not in our library10.1073/pnas.0408378102

  200. 200.

    Guzeloglu-Kayisli O, Pauli S, Demir H, Lalioti MD, Sakkas D, Seli E. Identification and characterization of human embryonic poly(A) binding protein (EPAB). Mol Hum Reprod. 2008;14:581-588.

    Not in our library10.1093/molehr/gan047

  201. 201.

    Guzeloglu-Kayisli O, Lalioti MD, Aydiner F, Sasson I, Ilbay O, Sakkas D, Lowther KM, Mehlmann LM, Seli E. Embryonic poly(A)-binding protein (EPAB) is required for oocyte maturation and female fertility in mice. Biochem J. 2012;446:47-58.

    Not in our library10.1042/bj20120467

  202. 202.

    Wang H, Li Y, Wang Y, Han ZG, Cai B. C9orf100, a new member of the Dbl-family guanine nucleotide exchange factors, promotes cell proliferation and migration in hepatocellular carcinoma. Mol Med Report. 2012;5:1169-1174.

    Not in our library10.3892/mmr.2012.783

  203. 203.

    Reverte CG, Yuan L, Keady BT, Lacza C, Attfield KR, Mahon GM, Freeman B, Whitehead IP, Hake LE. XGef is a CPEB-interacting protein involved in Xenopus oocyte maturation. Dev Biol. 2003;255:383-398.

    Not in our library10.1016/s0012-1606(02)00089-1

  204. 204.

    Martinez SE, Yuan L, Lacza C, Ransom H, Mahon GM, Whitehead IP, Hake LE. XGef mediates early CPEB phosphorylation during Xenopus oocyte meiotic maturation. Mol Biol Cell. 2005;16:1152-1164.

    Not in our library10.1091/mbc.e04-07-0585

  205. 205.

    Ferby I, Blazquez M, Palmer A, Eritja R, Nebreda AR. A novel p34(cdc2)-binding and activating protein that is necessary and sufficient to trigger G(2)/M progression in Xenopus oocytes. Genes Dev. 1999;13:2177-2189.

    Not in our library10.1101/gad.13.16.2177

  206. 206.

    Sakakibara S, Nakamura Y, Yoshida T, Shibata S, Koike M, Takano H, Ueda S, Uchiyama Y, Noda T, Okano H. RNA-binding protein Musashi family: roles for CNS stem cells and a subpopulation of ependymal cells revealed by targeted disruption and antisense ablation. Proc Natl Acad Sci USA. 2002;99:15194-15199.

    Not in our library10.1073/pnas.232087499

  207. 207.

    Gunter KM, McLaughlin EA. Translational control in germ cell development: a role for the RNA-binding proteins Musashi-1 and Musashi-2. IUBMB Life. 2011;63:678-685.

    Not in our library10.1002/iub.499

  208. 208.

    Wu X, Viveiros MM, Eppig JJ, Bai Y, Fitzpatrick SL, Matzuk MM. Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nat Genet. 2003;33:187-191.

    Not in our library10.1038/ng1079

  209. 209.

    Hu J, Wang F, Zhu X, Yuan Y, Ding M, Gao S. Mouse ZAR1-like (XM_359149) colocalizes with mRNA processing components and its dominant-negative mutant caused two-cell-stage embryonic arrest. Dev Dyn. 2010;239:407-424.

    Not in our library10.1002/dvdy.22170

  210. 210.

    Brook M, Smith JW, Gray NK. The DAZL and PABP families: RNA-binding proteins with interrelated roles in translational control in oocytes. Reproduction. 2009;137:595-617.

    Not in our library10.1530/rep-08-0524

  211. 211.

    Reynolds N, Collier B, Bingham V, Gray NK, Cooke HJ. Translation of the synaptonemal complex component Sycp3 is enhanced in vivo by the germ cell specific regulator Dazl. RNA. 2007;13:974-981.

    Not in our library10.1261/rna.465507

  212. 212.

    Kosaka K, Kawakami K, Sakamoto H, Inoue K. Spatiotemporal localization of germ plasm RNAs during zebrafish oogenesis. Mech Dev. 2007;124:279-289.

    Not in our library10.1016/j.mod.2007.01.003

  213. 213.

    Wiszniak SE, Dredge BK, Jensen KB. HuB (elavl2) mRNA is restricted to the germ cells by post-transcriptional mechanisms including stabilisation of the message by DAZL. PLoS One. 2011;6:e20773.

    Not in our library10.1371/journal.pone.0020773

  214. 214.

    Zeng M, Lu Y, Liao X, Li D, Sun H, Liang S, Zhang S, Ma Y, Yang Z. DAZL binds to 3′UTR of Tex19.1 mRNAs and regulates Tex19.1 expression. Mol Biol Rep. 2009;36:2399-2403.

    Not in our library10.1007/s11033-009-9470-1

  215. 215.

    Osborne HB, Duval C, Ghoda L, Omilli F, Bassez T, Coffino P. Expression and post-transcriptional regulation of ornithine decarboxylase during early Xenopus development. Eur J Biochem. 1991;202:575-581.

    Not in our library10.1111/j.1432-1033.1991.tb16410.x

  216. 216.

    Slevin MK, Gourronc F, Hartley RS. ElrA binding to the 3′UTR of cyclin E1 mRNA requires polyadenylation elements. Nucleic Acids Res. 2007;35:2167-2176.

    Not in our library10.1093/nar/gkm084

  217. 217.

    Paillard L, Maniey D, Lachaume P, Legagneux V, Osborne HB. Identification of a C-rich element as a novel cytoplasmic polyadenylation element in Xenopus embryos. Mech Dev. 2000;93:117-125.

    Not in our library10.1016/s0925-4773(00)00279-3

  218. 218.

    Gravina P, Campioni N, Loreni F, Pierandrei-Amaldi P, Cardinali B. Complementary DNA analysis, expression and subcellular localization of hnRNP E2 gene in Xenopus laevis. Gene. 2002;290:193-201.

    Not in our library10.1016/s0378-1119(02)00561-9

  219. 219.

    Kim KW, Nykamp K, Suh N, Bachorik JL, Wang L, Kimble J. Antagonism between GLD-2 binding partners controls gamete sex. Dev Cell. 2009;16:723-733.

    Not in our library10.1016/j.devcel.2009.04.002

  220. 220.

    Eckmann CR, Crittenden SL, Suh N, Kimble J. GLD-3 and control of the mitosis/meiosis decision in the germline of Caenorhabditis elegans. Genetics. 2004;168:147-160.

    Not in our library10.1534/genetics.104.029264

  221. 221.

    Eckmann CR, Kraemer B, Wickens M, Kimble J. GLD-3, a bicaudal-C homolog that inhibits FBF to control germline sex determination in C. elegans. Dev Cell. 2002;3:697-710.

    Not in our library10.1016/s1534-5807(02)00322-2

  222. 222.

    Nakel K, Hartung SA, Bonneau F, Eckmann CR, Conti E. Four KH domains of the C. elegans bicaudal-C ortholog GLD-3 form a globular structural platform. RNA. 2010;16:2058-2067.

    Not in our library10.1261/rna.2315010

  223. 223.

    Chicoine J, Benoit P, Gamberi C, Paliouras M, Simonelig M, Lasko P. Bicaudal-C recruits CCR4-NOT deadenylase to target mRNAs and regulates oogenesis, cytoskeletal organization, and its own expression. Dev Cell. 2007;13:691-704.

    Not in our library10.1016/j.devcel.2007.10.002

  224. 224.

    Rybarska A, Harterink M, Jedamzik B, Kupinski AP, Schmid M, Eckmann CR. GLS-1, a novel P granule component, modulates a network of conserved RNA regulators to influence germ cell fate decisions. PLoS Genet. 2009;5:e1000494.

    Not in our library10.1371/journal.pgen.1000494

  225. 225.

    Weiss J, Hurley LA, Harris RM, Finlayson C, Tong M, Fisher LA, Moran JL, Beier DR, Mason C, Jameson JL. ENU mutagenesis in mice identifies candidate genes for hypogonadism. Mamm Genome. 2012;23:346-355.

    Not in our library10.1007/s00335-011-9388-5

  226. 226.

    Coll O, Villalba A, Bussotti G, Notredame C, Gebauer F. A novel, noncanonical mechanism of cytoplasmic polyadenylation operates in Drosophila embryogenesis. Genes Dev. 2010;24:129-134.

    Not in our library10.1101/gad.568610

  227. 227.

    Brawerman G, Diez J. Metabolism of the polyadenylate sequence of nuclear RNA and messenger RNA in mammalian cells. Cell. 1975;5:271-280.

    Not in our library10.1016/0092-8674(75)90102-6

  228. 228.

    Watanabe T, Yachi K, Ohta T, Fukushima T, Yoshino A, Katayama Y, Shinojima Y, Terui T, Nagase H. Non-promoter hypermethylation of zygote arrest 1 (ZAR1) in human brain tumors. Brain Tumor Pathol. 2011;28:199-202.

    Not in our library10.1007/s10014-011-0019-3

  229. 229.

    Shinojima Y, Terui T, Hara H, Kimura M, Igarashi J, Wang X, Kawashima H, Kobayashi Y, Muroi S, Hayakawa S, et al. Identification and analysis of an early diagnostic marker for malignant melanoma: ZAR1 intra-genic differential methylation. J Dermatol Sci. 2010;59:98-106.

    Not in our library10.1016/j.jdermsci.2010.04.016

  230. 230.

    Ezeh UI, Turek PJ, Reijo RA, Clark AT. Human embryonic stem cell genes OCT4, NANOG, STELLAR, and GDF3 are expressed in both seminoma and breast carcinoma. Cancer. 2005;104:2255-2265.

    Not in our library10.1002/cncr.21432

  231. 231.

    Du L, Richter JD. Activity-dependent polyadenylation in neurons. RNA. 2005;11:1340-1347.

    Not in our library10.1261/rna.2870505

  232. 232.

    Huang YS, Jung MY, Sarkissian M, Richter JD. N-methyl-D-aspartate receptor signaling results in Aurora kinase-catalyzed CPEB phosphorylation and α CaMKII mRNA polyadenylation at synapses. EMBO J. 2002;21:2139-2148.

    Not in our library10.1093/emboj/21.9.2139

  233. 233.

    Wells DG, Dong X, Quinlan EM, Huang YS, Bear MF, Richter JD, Fallon JR. A role for the cytoplasmic polyadenylation element in NMDA receptor-regulated mRNA translation in neurons. J Neurosci. 2001;21:9541-9548.

    Not in our library10.1523/jneurosci.21-24-09541.2001

  234. 234.

    Wu L, Wells D, Tay J, Mendis D, Abbott MA, Barnitt A, Quinlan E, Heynen A, Fallon JR, Richter JD. CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of α-CaMKII mRNA at synapses. Neuron. 1998;21:1129-1139.

    Not in our library10.1016/s0896-6273(00)80630-3

  235. 235.

    Zearfoss NR, Alarcon JM, Trifilieff P, Kandel E, Richter JD. A molecular circuit composed of CPEB-1 and c-Jun controls growth hormone-mediated synaptic plasticity in the mouse hippocampus. J Neurosci. 2008;28:8502-8509.

    Not in our library10.1523/jneurosci.1756-08.2008

  236. 236.

    Huang YS, Carson JH, Barbarese E, Richter JD. Facilitation of dendritic mRNA transport by CPEB. Genes Dev. 2003;17:638-653.

    Not in our library10.1101/gad.1053003

  237. 237.

    Bestman JE, Cline HT. The relationship between dendritic branch dynamics and CPEB-labeled RNP granules captured in vivo. Front Neural Circuits. 2009;3:10.

    Not in our library10.3389/neuro.04.010.2009

  238. 238.

    Bestman JE, Cline HT. The RNA binding protein CPEB regulates dendrite morphogenesis and neuronal circuit assembly in vivo. Proc Natl Acad Sci USA. 2008;105:20494-20499.

    Not in our library10.1073/pnas.0806296105

  239. 239.

    Atkins CM, Davare MA, Oh MC, Derkach V, Soderling TR. Bidirectional regulation of cytoplasmic polyadenylation element-binding protein phosphorylation by Ca2+/calmodulin-dependent protein kinase II and protein phosphatase 1 during hippocampal long-term potentiation. J Neurosci. 2005;25:5604-5610.

    Not in our library10.1523/jneurosci.5051-04.2005

  240. 240.

    Atkins CM, Nozaki N, Shigeri Y, Soderling TR. Cytoplasmic polyadenylation element binding protein-dependent protein synthesis is regulated by calcium/calmodulin-dependent protein kinase II. J Neurosci. 2004;24:5193-5201.

    Not in our library10.1523/jneurosci.0854-04.2004

  241. 241.

    Udagawa T, Swanger SA, Takeuchi K, Kim JH, Nalavadi V, Shin J, Lorenz LJ, Zukin RS, Bassell GJ, Richter JD. Bidirectional control of mRNA translation and synaptic plasticity by the cytoplasmic polyadenylation complex. Mol Cell. 2012;47:253-266.

    Not in our library10.1016/j.molcel.2012.05.016

  242. 242.

    Aslam N, Shouval HZ. Regulation of cytoplasmic polyadenylation can generate a bistable switch. BMC Syst Biol. 2012;6:12.

    Not in our library10.1186/1752-0509-6-12

  243. 243.

    Si K, Giustetto M, Etkin A, Hsu R, Janisiewicz AM, Miniaci MC, Kim JH, Zhu H, Kandel ER. A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in aplysia. Cell. 2003;115:893-904.

    Not in our library10.1016/s0092-8674(03)01021-3

  244. 244.

    Si K, Lindquist S, Kandel ER. A neuronal isoform of the aplysia CPEB has prion-like properties. Cell. 2003;115:879-891.

    Not in our library10.1016/s0092-8674(03)01020-1

  245. 245.

    Si K, Choi YB, White-Grindley E, Majumdar A, Kandel ER. Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation. Cell. 2010;140:421-435.

    Not in our library10.1016/j.cell.2010.01.008

  246. 246.

    Kruttner S, Stepien B, Noordermeer JN, Mommaas MA, Mechtler K, Dickson BJ, Keleman K. Drosophila CPEB Orb2A mediates memory independent of Its RNA-binding domain. Neuron. 2012;76:383-395.

    Not in our library10.1016/j.neuron.2012.08.028

  247. 247.

    Kondrashov A, Meijer HA, Barthet-Barateig A, Parker HN, Khurshid A, Tessier S, Sicard M, Knox AJ, Pang L, De Moor CH. Inhibition of polyadenylation reduces inflammatory gene induction. RNA. 2012;18:2236-2250.

    Not in our library10.1261/rna.032391.112

  248. 248.

    Wong YY, Moon A, Duffin R, Barthet-Barateig A, Meijer HA, Clemens MJ, De Moor CH. Cordycepin inhibits protein synthesis and cell adhesion through effects on signal transduction. J Biol Chem. 2010;285:2610-2621.

    Not in our library10.1074/jbc.m109.071159

  249. 249.

    Hafer N, Xu S, Bhat KM, Schedl P. The Drosophila CPEB protein Orb2 has a novel expression pattern and is important for asymmetric cell division and nervous system function. Genetics. 2011;189:907-921.

    Not in our library10.1534/genetics.110.123646

  250. 250.

    Keleman K, Kruttner S, Alenius M, Dickson BJ. Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat Neurosci. 2007;10:1587-1593.

    Not in our library10.1038/nn1996

  251. 251.

    Jones KJ, Korb E, Kundel MA, Kochanek AR, Kabraji S, McEvoy M, Shin CY, Wells DG. CPEB1 regulates β-catenin mRNA translation and cell migration in astrocytes. Glia. 2008;56:1401-1413.

    Not in our library10.1002/glia.20707

  252. 252.

    Kundel M, Jones KJ, Shin CY, Wells DG. Cytoplasmic polyadenylation element-binding protein regulates neurotrophin-3-dependent β-catenin mRNA translation in developing hippocampal neurons. J Neurosci. 2009;29:13630-13639.

    Not in our library10.1523/jneurosci.2910-08.2009

  253. 253.

    McEvoy M, Cao G, Llopis PM, Kundel M, Jones K, Hofler C, Shin C, Wells DG. Cytoplasmic polyadenylation element binding protein 1-mediated mRNA translation in Purkinje neurons is required for cerebellar long-term depression and motor coordination. J Neurosci. 2007;27:6400-6411.

    Not in our library10.1523/jneurosci.5211-06.2007

  254. 254.

    Vessey JP, Schoderboeck L, Gingl E, Luzi E, Riefler J, Di LF, Karra D, Thomas S, Kiebler MA, Macchi P. Mammalian Pumilio 2 regulates dendrite morphogenesis and synaptic function. Proc Natl Acad Sci USA. 2010;107:3222-3227.

    Not in our library10.1073/pnas.0907128107

  255. 255.

    Kuo MW, Wang SH, Chang JC, Chang CH, Huang LJ, Lin HH, Yu AL, Li WH, Yu J. A novel puf-A gene predicted from evolutionary analysis is involved in the development of eyes and primordial germ-cells. PLoS One. 2009;4:e4980.

    Not in our library10.1371/journal.pone.0004980

  256. 256.

    Menon KP, Andrews S, Murthy M, Gavis ER, Zinn K. The translational repressors Nanos and Pumilio have divergent effects on presynaptic terminal growth and postsynaptic glutamate receptor subunit composition. J Neurosci. 2009;29:5558-5572.

    Not in our library10.1523/jneurosci.0520-09.2009

  257. 257.

    Chen G, Li W, Zhang QS, Regulski M, Sinha N, Barditch J, Tully T, Krainer AR, Zhang MQ, Dubnau J. Identification of synaptic targets of Drosophila pumilio. PLoS Comput Biol. 2008;4:e1000026.

    Not in our library10.1371/journal.pcbi.1000026

  258. 258.

    Baines RA. Neuronal homeostasis through translational control. Mol Neurobiol. 2005;32:113-121.

    Not in our library10.1385/mn:32:2:113

  259. 259.
  260. 260.

    Ye B, Petritsch C, Clark IE, Gavis ER, Jan LY, Jan YN. Nanos and Pumilio are essential for dendrite morphogenesis in Drosophila peripheral neurons. Curr Biol. 2004;14:314-321.

    Not in our library10.1016/j.cub.2004.01.052

  261. 261.

    Alarcon JM, Hodgman R, Theis M, Huang YS, Kandel ER, Richter JD. Selective modulation of some forms of schaffer collateral-CA1 synaptic plasticity in mice with a disruption of the CPEB-1 gene. Learn Mem. 2004;11:318-327.

    Not in our library10.1101/lm.72704

  262. 262.

    Berger-Sweeney J, Zearfoss NR, Richter JD. Reduced extinction of hippocampal-dependent memories in CPEB knockout mice. Learn Mem. 2006;13:4-7.

    Not in our library10.1101/lm.73706

  263. 263.

    Theis M, Si K, Kandel ER. Two previously undescribed members of the mouse CPEB family of genes and their inducible expression in the principal cell layers of the hippocampus. Proc Natl Acad Sci USA. 2003;100:9602-9607.

    Not in our library10.1073/pnas.1133424100

  264. 264.

    Pavlopoulos E, Trifilieff P, Chevaleyre V, Fioriti L, Zairis S, Pagano A, Malleret G, Kandel ER. Neuralized1 activates CPEB3: a function for nonproteolytic ubiquitin in synaptic plasticity and memory storage. Cell. 2011;147:1369-1383.

    Not in our library10.1016/j.cell.2011.09.056

  265. 265.

    Wang CF, Huang YS. Calpain 2 activated through N-Methyl-D-aspartic acid receptor signaling cleaves CPEB3 and abrogates CPEB3-repressed translation in neurons. Mol Cell Biol. 2012;32:3321-3332.

    Not in our library10.1128/mcb.00296-12

  266. 266.

    Vogler C, Spalek K, Aerni A, Demougin P, Muller A, Huynh KD, Papassotiropoulos A, de Quervain DJ. CPEB3 is associated with human episodic memory. Front Behav Neurosci. 2009;3:4.

    Not in our library10.3389/neuro.08.004.2009

  267. 267.

    Hosoda N, Funakoshi Y, Hirasawa M, Yamagishi R, Asano Y, Miyagawa R, Ogami K, Tsujimoto M, Hoshino S. Anti-proliferative protein Tob negatively regulates CPEB3 target by recruiting Caf1 deadenylase. EMBO J. 2011;30:1311-1323.

    Not in our library10.1038/emboj.2011.37

  268. 268.

    Sasayama T, Marumoto T, Kunitoku N, Zhang D, Tamaki N, Kohmura E, Saya H, Hirota T. Over-expression of Aurora-A targets cytoplasmic polyadenylation element binding protein and promotes mRNA polyadenylation of Cdk1 and cyclin B1. Genes Cells. 2005;10:627-638.

    Not in our library10.1111/j.1365-2443.2005.00870.x

  269. 269.

    Cao Q, Kim JH, Richter JD. CDK1 and calcineurin regulate Maskin association with eIF4E and translational control of cell cycle progression. Nat Struct Mol Biol. 2006;13:1128-1134.

    Not in our library10.1038/nsmb1169

  270. 270.

    Groisman I, Jung MY, Sarkissian M, Cao Q, Richter JD. Translational control of the embryonic cell cycle. Cell. 2002;109:473-483.

    Not in our library10.1016/s0092-8674(02)00733-x

  271. 271.

    Pederson T, Robbins E. RNA synthesis in HeLa cells. Pattern in hypertonic medium and its similarity to synthesis during G2-prophase. J Cell Biol. 1970;47:734-744.

    Not in our library10.1083/jcb.47.3.734

  272. 272.

    Burns DM, Richter JD. CPEB regulation of human cellular senescence, energy metabolism, and p53 mRNA translation. Genes Dev. 2008;22:3449-3460.

    Not in our library10.1101/gad.1697808

  273. 273.

    Groisman I, Ivshina M, Marin V, Kennedy NJ, Davis RJ, Richter JD. Control of cellular senescence by CPEB. Genes Dev. 2006;20:2701-2712.

    Not in our library10.1101/gad.1438906

  274. 274.

    Berndt H, Harnisch C, Rammelt C, Stohr N, Zirkel A, Dohm JC, Himmelbauer H, Tavanez JP, Huttelmaier S, Wahle E. Maturation of mammalian H/ACA box snoRNAs: PAPD5-dependent adenylation and PARN-dependent trimming. RNA. 2012;18:958-972.

    Not in our library10.1261/rna.032292.112

  275. 275.

    Lin CL, Evans V, Shen S, Xing Y, Richter JD. The nuclear experience of CPEB: implications for RNA processing and translational control. RNA. 2010;16:338-348.

    Not in our library10.1261/rna.1779810

  276. 276.

    Kan MC, Oruganty-Das A, Cooper-Morgan A, Jin G, Swanger S, Bassell G, Florman H, Van LK, Richter JD. CPEB4 is a cell survival protein retained in the nucleus upon ischemia or endoplasmic reticulum calcium depletion. Mol Cell Biol. 2010;30:5658-5671.

    Not in our library10.1128/mcb.00716-10

  277. 277.

    Ernoult-Lange M, Wilczynska A, Harper M, Aigueperse C, Dautry F, Kress M, Weil D. Nucleocytoplasmic traffic of CPEB1 and accumulation in Crm1 nucleolar bodies. Mol Biol Cell. 2009;20:176-187.

    Not in our library10.1091/mbc.e08-09-0904

  278. 278.

    Kojima S, Sher-Chen EL, Green CB. Circadian control of mRNA polyadenylation dynamics regulates rhythmic protein expression. Genes Dev. 2012;26:2724-2736.

    Not in our library10.1101/gad.208306.112

  279. 279.

    Okano H, Kawahara H, Toriya M, Nakao K, Shibata S, Imai T. Function of RNA-binding protein Musashi-1 in stem cells. Exp Cell Res. 2005;306:349-356.

    Not in our library10.1016/j.yexcr.2005.02.021

  280. 280.

    Clarke RB. Isolation and characterization of human mammary stem cells. Cell Prolif. 2005;38:375-386.

    Not in our library10.1111/j.1365-2184.2005.00357.x

  281. 281.

    Todaro M, Francipane MG, Medema JP, Stassi G. Colon cancer stem cells: promise of targeted therapy. Gastroenterology. 2010;138:2151-2162.

    Not in our library10.1053/j.gastro.2009.12.063

  282. 282.

    Yen TH, Wright NA. The gastrointestinal tract stem cell niche. Stem Cell Rev. 2006;2:203-212.

    Not in our library10.1007/s12015-006-0048-1

  283. 283.

    Cervello I, Mirantes C, Santamaria X, Dolcet X, Matias-Guiu X, Simon C. Stem cells in human endometrium and endometrial carcinoma. Int J Gynecol Pathol. 2011;30:317-327.

    Not in our library10.1097/pgp.0b013e3182102754

  284. 284.

    de Andres-Aguayo L, Varas F, Graf T. Musashi 2 in hematopoiesis. Curr Opin Hematol. 2012;19:268-272.

    Not in our library10.1097/moh.0b013e328353c778

  285. 285.

    Kawahara H, Imai T, Imataka H, Tsujimoto M, Matsumoto K, Okano H. Neural RNA-binding protein Musashi1 inhibits translation initiation by competing with eIF4G for PABP. J Cell Biol. 2008;181:639-653.

    Not in our library10.1083/jcb.200708004

  286. 286.

    Quenault T, Lithgow T, Traven A. PUF proteins: repression, activation and mRNA localization. Trends Cell Biol. 2011;21:104-112.

    Not in our library10.1016/j.tcb.2010.09.013

  287. 287.

    Kim SY, Kim JY, Malik S, Son W, Kwon KS, Kim C. Negative regulation of EGFR/MAPK pathway by Pumilio in Drosophila melanogaster. PLoS One. 2012;7:e34016.

    Not in our library10.1371/journal.pone.0034016

  288. 288.

    Bermudez O, Jouandin P, Rottier J, Bourcier C, Pages G, Gimond C. Post-transcriptional regulation of the DUSP6/MKP-3 phosphatase by MEK/ERK signalling and hypoxia. J Cell Physiol. 2010;226:276-284.

    Not in our library10.1002/jcp.22339

  289. 289.
  290. 290.

    Bouvrette DJ, Sittaramane V, Heidel JR, Chandrasekhar A, Bryda EC. Knockdown of bicaudal C in zebrafish (Danio rerio) causes cystic kidneys: a nonmammalian model of polycystic kidney disease. Comp Med. 2010;60:96-106.

    Not in our library

  291. 291.

    Cogswell C, Price SJ, Hou X, Guay-Woodford LM, Flaherty L, Bryda EC. Positional cloning of jcpk/bpk locus of the mouse. Mamm Genome. 2003;14:242-249.

    Not in our library10.1007/s00335-002-2241-0

  292. 292.

    Kraus MR, Clauin S, Pfister Y, Di MM, Ulinski T, Constam D, Bellanne-Chantelot C, Grapin-Botton A. Two mutations in human BICC1 resulting in Wnt pathway hyperactivity associated with cystic renal dysplasia. Hum Mutat. 2012;33:86-90.

    Not in our library10.1002/humu.21610

  293. 293.

    Maisonneuve C, Guilleret I, Vick P, Weber T, Andre P, Beyer T, Blum M, Constam DB. Bicaudal C, a novel regulator of Dvl signaling abutting RNA-processing bodies, controls cilia orientation and leftward flow. Development. 2009;136:3019-3030.

    Not in our library10.1242/dev.038174

  294. 294.

    Ryan S, Verghese S, Cianciola NL, Cotton CU, Carlin CR. Autosomal recessive polycystic kidney disease epithelial cell model reveals multiple basolateral epidermal growth factor receptor sorting pathways. Mol Biol Cell. 2010;21:2732-2745.

    Not in our library10.1091/mbc.e09-12-1059

  295. 295.

    Fu Y, Kim I, Lian P, Li A, Zhou L, Li C, Liang D, Coffey RJ, Ma J, Zhao P, et al. Loss of Bicc1 impairs tubulomorphogenesis of cultured IMCD cells by disrupting E-cadherin-based cell-cell adhesion. Eur J Cell Biol. 2010;89:428-436.

    Not in our library10.1016/j.ejcb.2010.01.002

  296. 296.

    Nagaoka K, Udagawa T, Richter JD. CPEB-mediated ZO-1 mRNA localization is required for epithelial tight-junction assembly and cell polarity. Nat Commun. 2012;3:675.

    Not in our library10.1038/ncomms1678

  297. 297.

    Kiessling F, Kartenbeck J, Haller C. Cell-cell contacts in the human cell line ECV304 exhibit both endothelial and epithelial characteristics. Cell Tissue Res. 1999;297:131-140.

    Not in our library10.1007/s004410051340

  298. 298.

    Paffenholz R, Kuhn C, Grund C, Stehr S, Franke WW. The arm-repeat protein NPRAP (neurojungin) is a constituent of the plaques of the outer limiting zone in the retina, defining a novel type of adhering junction. Exp Cell Res. 1999;250:452-464.

    Not in our library10.1006/excr.1999.4534

  299. 299.

    Bouvrette DJ, Price SJ, Bryda EC. K homology domains of the mouse polycystic kidney disease-related protein, Bicaudal-C (Bicc1), mediate RNA binding in vitro. Nephron Exp Nephrol. 2008;108:e27-e34.

    Not in our library10.1159/000112913

  300. 300.

    Piazzon N, Maisonneuve C, Guilleret I, Rotman S, Constam DB. Bicc1 links the regulation of cAMP signaling in polycystic kidneys to microRNA-induced gene silencing. J Mol Cell Biol. 2012;4:398-408.

    Not in our library10.1093/jmcb/mjs027

  301. 301.

    Tran U, Zakin L, Schweickert A, Agrawal R, Doger R, Blum M, De Robertis EM, Wessely O. The RNA-binding protein bicaudal C regulates polycystin 2 in the kidney by antagonizing miR-17 activity. Development. 2010;137:1107-1116.

    Not in our library10.1242/dev.046045

  302. 302.

    von Roretz C, Di MS, Mazroui R, Gallouzi IE. Turnover of AU-rich-containing mRNAs during stress: a matter of survival. Wiley Interdiscip Rev RNA. 2011;2:336-347.

    Not in our library10.1002/wrna.55

  303. 303.

    Makeyev AV, Liebhaber SA. The poly(C)-binding proteins: a multiplicity of functions and a search for mechanisms. RNA. 2002;8:265-278.

    Not in our library10.1017/s1355838202024627

  304. 304.

    Ostareck-Lederer A, Ostareck DH. Control of mRNA translation and stability in haematopoietic cells: The function of hnRNPs K and E1/E2. Biol Cell. 2004;96:407-411.

    Not in our library10.1016/j.biolcel.2004.03.010

  305. 305.

    Eiring AM, Harb JG, Neviani P, Garton C, Oaks JJ, Spizzo R, Liu S, Schwind S, Santhanam R, Hickey CJ, et al. miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts. Cell. 2010;140:652-665.

    Not in our library10.1016/j.cell.2010.01.007

  306. 306.

    Ji X, Kong J, Carstens RP, Liebhaber SA. The 3′ untranslated region complex involved in stabilization of human α-globin mRNA assembles in the nucleus and serves an independent role as a splice enhancer. Mol Cell Biol. 2007;27:3290-3302.

    Not in our library10.1128/mcb.02289-05

  307. 307.

    de Hoog CL, Foster LJ, Mann M. RNA and RNA binding proteins participate in early stages of cell spreading through spreading initiation centers. Cell. 2004;117:649-662.

    Not in our library10.1016/s0092-8674(04)00456-8

  308. 308.

    Yang Q, Gilmartin GM, Doublie S. Structural basis of UGUA recognition by the Nudix protein CFI(m)25 and implications for a regulatory role in mRNA 3′ processing. Proc Natl Acad Sci USA. 2010;107:10062-10067.

    Not in our library10.1073/pnas.1000848107

  309. 309.

    McPheeters DS, Cremona N, Sunder S, Chen HM, Averbeck N, Leatherwood J, Wise JA. A complex gene regulatory mechanism that operates at the nexus of multiple RNA processing decisions. Nat Struct Mol Biol. 2009;16:255-264.

    Not in our library10.1038/nsmb.1556

  310. 310.

    Houseley J, Tollervey D. The nuclear RNA surveillance machinery: the link between ncRNAs and genome structure in budding yeast? Biochim Biophys Acta. 2008;1779:239-246.

    Not in our library10.1016/j.bbagrm.2007.12.008

  311. 311.

    Katoh T, Sakaguchi Y, Miyauchi K, Suzuki T, Kashiwabara S, Baba T, Suzuki T. Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev. 2009;23:433-438.

    Not in our library10.1101/gad.1761509

  312. 312.

    Shcherbik N, Wang M, Lapik YR, Srivastava L, Pestov DG. Polyadenylation and degradation of incomplete RNA polymerase I transcripts in mammalian cells. EMBO Rep. 2010;11:106-111.

    Not in our library10.1038/embor.2009.271

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