CPEB: a life in translation.

Nearly two decades ago, Xenopus oocytes were found to contain mRNAs harboring a small sequence in their 3' untranslated regions that control cytoplasmic polyadenylation and translational activation during development. This cytoplasmic polyadenylation element (CPE) is the binding platform for CPE-binding protein (CPEB), which promotes polyadenylation-induced translation. Since then, the biochemistry and biology of CPEB has grown rather substantially: mechanistically, CPEB nucleates a complex of factors that regulates poly(A) elongation through, of all things, a deadenylating enzyme; biologically, CPEB mediates many processes including germ-cell development, cell division and cellular senescence, and synaptic plasticity and learning and memory. These observations underscore the growing complexities of CPEB involvement in cell function.

[1]  J. Richter,et al.  Regulated CPEB phosphorylation during meiotic progression suggests a mechanism for temporal control of maternal mRNA translation. , 2003, Genes & development.

[2]  E. Kandel,et al.  A Neuronal Isoform of the Aplysia CPEB Has Prion-Like Properties , 2003, Cell.

[3]  Q. Cao,et al.  Dissolution of the maskin–eIF4E complex by cytoplasmic polyadenylation and poly(A)‐binding protein controls cyclin B1 mRNA translation and oocyte maturation , 2002, The EMBO journal.

[4]  Jong Heon Kim,et al.  CDK1 and calcineurin regulate Maskin association with eIF4E and translational control of cell cycle progression , 2006, Nature Structural &Molecular Biology.

[5]  J. Steitz,et al.  Metazoan oocyte and early embryo development program: a progression through translation regulatory cascades. , 2006, Genes & development.

[6]  Q. Cao,et al.  Translational Control of the Embryonic Cell Cycle , 2002, Cell.

[7]  M. Bear,et al.  Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. , 2000, Science.

[8]  D. Weil,et al.  The translational regulator CPEB1 provides a link between dcp1 bodies and stress granules , 2005, Journal of Cell Science.

[9]  N. Sharpless,et al.  ROS as a tumour suppressor? , 2006, Nature Cell Biology.

[10]  O. Steward,et al.  Synaptic Regulation of Translation of Dendritic mRNAs , 2006, The Journal of Neuroscience.

[11]  M. McCall,et al.  Photoreceptor regulated expression of Ca(2+)/calmodulin-dependent protein kinase II in the mouse retina. , 2000, Brain research. Molecular brain research.

[12]  M. Matzuk,et al.  The Art and Artifact of GDF9 Activity: Cumulus Expansion and the Cumulus Expansion-Enabling Factor1 , 2005, Biology of reproduction.

[13]  E. Schuman,et al.  Dendritic Protein Synthesis, Synaptic Plasticity, and Memory , 2006, Cell.

[14]  N. Sharpless,et al.  The Regulation of INK4/ARF in Cancer and Aging , 2006, Cell.

[15]  J. Richter,et al.  Reduced extinction of hippocampal-dependent memories in CPEB knockout mice. , 2006, Learning & memory.

[16]  J. Steitz,et al.  AU-Rich-Element-Mediated Upregulation of Translation by FXR1 and Argonaute 2 , 2007, Cell.

[17]  C. Lacza,et al.  XGef mediates early CPEB phosphorylation during Xenopus oocyte meiotic maturation. , 2005, Molecular biology of the cell.

[18]  Roger J. Davis,et al.  Control of cellular senescence by CPEB. , 2006, Genes & development.

[19]  Jonathan S Weissman,et al.  Dissection and Design of Yeast Prions , 2004, PLoS biology.

[20]  Wael Tadros,et al.  Setting the stage for development: mRNA translation and stability during oocyte maturation and egg activation in Drosophila , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[21]  I. Vernos,et al.  Function and regulation of Maskin, a TACC family protein, in microtubule growth during mitosis , 2005, The Journal of cell biology.

[22]  Yi-shuian Huang,et al.  Facilitation of dendritic mRNA transport by CPEB. , 2003, Genes & development.

[23]  Yi-shuian Huang,et al.  CPEB3 and CPEB4 in neurons: analysis of RNA‐binding specificity and translational control of AMPA receptor GluR2 mRNA , 2006, The EMBO journal.

[24]  R. Heald,et al.  A Rae1-Containing Ribonucleoprotein Complex Is Required for Mitotic Spindle Assembly , 2005, Cell.

[25]  R. Méndez,et al.  Progesterone and insulin stimulation of CPEB-dependent polyadenylation is regulated by Aurora A and glycogen synthase kinase-3. , 2004, Genes & development.

[26]  P. Pandolfi,et al.  The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis , 2004, Nature Medicine.

[27]  Yan Wang,et al.  The Drosophila fragile X protein functions as a negative regulator in the orb autoregulatory pathway. , 2005, Developmental cell.

[28]  M. Tuite,et al.  Propagation of yeast prions , 2003, Nature Reviews Molecular Cell Biology.

[29]  Alan G Hinnebusch,et al.  eIF3: a versatile scaffold for translation initiation complexes. , 2006, Trends in biochemical sciences.

[30]  Y Nagahama,et al.  Biochemical Identification of Xenopus Pumilio as a Sequence-specific Cyclin B1 mRNA-binding Protein That Physically Interacts with a Nanos Homolog, Xcat-2, and a Cytoplasmic Polyadenylation Element-binding Protein* , 2001, The Journal of Biological Chemistry.

[31]  Martin M. Matzuk,et al.  Intercellular Communication in the Mammalian Ovary: Oocytes Carry the Conversation , 2002, Science.

[32]  E. Kandel,et al.  Selective modulation of some forms of schaffer collateral-CA1 synaptic plasticity in mice with a disruption of the CPEB-1 gene. , 2004, Learning & memory.

[33]  D. Wells,et al.  Rapid, Activity-Induced Increase in Tissue Plasminogen Activator Is Mediated by Metabotropic Glutamate Receptor-Dependent mRNA Translation , 2004, The Journal of Neuroscience.

[34]  W. Filipowicz,et al.  Relief of microRNA-Mediated Translational Repression in Human Cells Subjected to Stress , 2006, Cell.

[35]  Nahum Sonenberg,et al.  Interaction of eIF4G with poly(A)-binding protein stimulates translation and is critical for Xenopus oocyte maturation , 2000, Current Biology.

[36]  R. Méndez,et al.  Translational control by CPEB: a means to the end , 2001, Nature Reviews Molecular Cell Biology.

[37]  Yi-shuian Huang,et al.  N‐methyl‐D‐aspartate receptor signaling results in Aurora kinase‐catalyzed CPEB phosphorylation and αCaMKII mRNA polyadenylation at synapses , 2002, The EMBO journal.

[38]  D. Belin,et al.  Transient translational silencing by reversible mRNA deadenylation , 1992, Cell.

[39]  S. Lowe,et al.  Intrinsic tumour suppression , 2004, Nature.

[40]  J. Campisi Suppressing Cancer: The Importance of Being Senescent , 2005, Science.

[41]  K. Ryan,et al.  Symplekin and xGLD-2 Are Required for CPEB-Mediated Cytoplasmic Polyadenylation , 2004, Cell.

[42]  D. Barford,et al.  Argonaute: A scaffold for the function of short regulatory RNAs. , 2006, Trends in biochemical sciences.

[43]  Eric R. Kandel,et al.  Two previously undescribed members of the mouse CPEB family of genes and their inducible expression in the principal cell layers of the hippocampus , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[44]  C. Sherr,et al.  Principles of Tumor Suppression , 2004, Cell.

[45]  Joel D. Richter,et al.  Differential Phosphorylation Controls Maskin Association with Eukaryotic Translation Initiation Factor 4E and Localization on the Mitotic Apparatus , 2005, Molecular and Cellular Biology.

[46]  S. Lowe,et al.  Senescence comes of age , 2005, Nature Medicine.

[47]  J. Campisi Senescent Cells, Tumor Suppression, and Organismal Aging: Good Citizens, Bad Neighbors , 2005, Cell.

[48]  M. Mayford,et al.  Disruption of Dendritic Translation of CaMKIIα Impairs Stabilization of Synaptic Plasticity and Memory Consolidation , 2002, Neuron.

[49]  M. Wickens,et al.  Vertebrate GLD2 poly(A) polymerases in the germline and the brain. , 2005, RNA.

[50]  J. Richter,et al.  Selective translation of mRNAs at synapses , 2002, Current Opinion in Neurobiology.

[51]  R. Weinberg,et al.  The signals and pathways activating cellular senescence. , 2005, The international journal of biochemistry & cell biology.

[52]  N. Sharpless,et al.  RAS unplugged: negative feedback and oncogene-induced senescence. , 2006, Cancer cell.

[53]  J. H. Schwartz,et al.  The cytoplasmic polyadenylation element binding protein and polyadenylation of messenger RNA in Aplysia neurons , 2003, Brain Research.

[54]  Yi-shuian Huang,et al.  Amyloid Precursor Proteins Anchor CPEB to Membranes and Promote Polyadenylation-Induced Translation , 2005, Molecular and Cellular Biology.

[55]  R. Méndez,et al.  Differential mRNA translation and meiotic progression require Cdc2‐mediated CPEB destruction , 2002, The EMBO journal.

[56]  H. Piwnica-Worms,et al.  Maturation-specific polyadenylation: in vitro activation by p34cdc2 and phosphorylation of a 58-kD CPE-binding protein. , 1991, Genes & development.

[57]  M. Wickens,et al.  Autoregulation of GLD-2 cytoplasmic poly(A) polymerase. , 2006, RNA.

[58]  M. Wickens,et al.  19 Translational Control in Development , 2007 .

[59]  E. Quinlan,et al.  CPEB-Mediated Cytoplasmic Polyadenylation and the Regulation of Experience-Dependent Translation of α-CaMKII mRNA at Synapses , 1998, Neuron.

[60]  J. Richter,et al.  CPEB controls oocyte growth and follicle development in the mouse , 2006, Development.

[61]  Ted Abel,et al.  Molecular mechanisms of memory acquisition, consolidation and retrieval , 2001, Current Opinion in Neurobiology.

[62]  Yasushi Shigeri,et al.  Cytoplasmic Polyadenylation Element Binding Protein-Dependent Protein Synthesis Is Regulated by Calcium/Calmodulin-Dependent Protein Kinase II , 2004, The Journal of Neuroscience.

[63]  J. Richter,et al.  Germ cell differentiation and synaptonemal complex formation are disrupted in CPEB knockout mice. , 2001, Developmental cell.

[64]  A. Hyman,et al.  Aurora A phosphorylation of TACC3/maskin is required for centrosome-dependent microtubule assembly in mitosis , 2005, The Journal of cell biology.

[65]  N. Sonenberg,et al.  Regulation of cap-dependent translation by eIF4E inhibitory proteins , 2005, Nature.

[66]  Eric R. Kandel,et al.  A Neuronal Isoform of CPEB Regulates Local Protein Synthesis and Stabilizes Synapse-Specific Long-Term Facilitation in Aplysia , 2003, Cell.

[67]  J. Richter,et al.  Regulated Pumilio-2 binding controls RINGO/Spy mRNA translation and CPEB activation. , 2006, Genes & development.

[68]  Jonathan S Weissman,et al.  Multiple Gln/Asn-Rich Prion Domains Confer Susceptibility to Induction of the Yeast [PSI+] Prion , 2001, Cell.

[69]  A. Sachs,et al.  Poly(A) tail metabolism and function in eucaryotes. , 1993, The Journal of biological chemistry.

[70]  E. Schuman,et al.  A Requirement for Local Protein Synthesis in Neurotrophin-Induced Hippocampal Synaptic Plasticity , 1996, Science.

[71]  J. Richter,et al.  Opposing polymerase-deadenylase activities regulate cytoplasmic polyadenylation. , 2006, Molecular cell.

[72]  L. Hake,et al.  CPEB degradation during Xenopus oocyte maturation requires a PEST domain and the 26S proteasome. , 2001, Developmental biology.

[73]  J. Richter,et al.  Translational Control by Neuroguidin, a Eukaryotic Initiation Factor 4E and CPEB Binding Protein , 2006, Molecular and Cellular Biology.

[74]  L. Tong,et al.  Polyadenylation factor CPSF-73 is the pre-mRNA 3'-end-processing endonuclease , 2006, Nature.

[75]  N. Standart,et al.  A conserved role of a DEAD box helicase in mRNA masking. , 2001, RNA.

[76]  E. Klann,et al.  Translational control of synaptic plasticity and learning and memory , 2007 .

[77]  Yi-shuian Huang,et al.  CPEB, Maskin, and Cyclin B1 mRNA at the Mitotic Apparatus Implications for Local Translational Control of Cell Division , 2000, Cell.

[78]  Michael B. Mathews,et al.  Translational control in biology and medicine , 2007 .

[79]  Christel Rouget,et al.  Cytoplasmic CstF-77 Protein Belongs to a Masking Complex with Cytoplasmic Polyadenylation Element-binding Protein in Xenopus Oocytes* , 2006, Journal of Biological Chemistry.