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    Joel Richter PhD

    TitleProfessor
    InstitutionUniversity of Massachusetts Medical School
    DepartmentProgram in Molecular Medicine
    AddressUniversity of Massachusetts Medical School
    373 Plantation Street
    Worcester MA 01605
    Phone508-856-8615
      Other Positions
      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentBiochemistry and Molecular Pharmacology

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentInterdisciplinary Graduate Program

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentMD/PhD Program

      InstitutionUMMS - Graduate School of Biomedical Sciences
      DepartmentNeuroscience

      InstitutionUMMS - Programs, Centers and Institutes
      DepartmentRNA Therapeutics Institute

        Overview 
        Narrative

        Academic Background

        Ph. D. (1979) Arizona State University

        J_Richter_photo

        What we do...

        We study the molecular biology of mRNA translational control by cytoplasmic polyadenylation and how this process influences interesting biological phenomena including early animal development, cellular senescence/growth control, neuron synaptic plasticity, learning, and memory, and neurologic disease.

        Translational control by 3’ end formation

        Many inactive mRNAs have short poly(A) tails and only when the tails are elongated does translation ensue. A key factor that regulates polyadenylation-induced translation is the RNA binding protein CPEB (Cytoplasmic Polyadenylation Element Binding Protein). CPEB binds specific 3’UTR cis elements in mRNAs and recruits unusual poly(A) polymerases and translation factors that extend poly(A) tails in the cytoplasm and promote translation.

        One poly(A) polymerase also monoadenylates and stabilizes specific miRNAs, adding an important and unexpected layer of translational control by 3’ end formation.

        Early animal development

        Maternal (masked) mRNAs in oocytes have short poly(A) tails, which are elongated when the cells re-enter the meiotic divisions and prepare for fertilization. This cytoplasmic polyadenylation induces translation, and the biochemistry of these events in most easily studied in oocytes of the frog Xenopus. The importance of CPEB for germ cell development is demonstrated by the observation that meiosis does not proceed beyond the pachytene stage in CPEB knockout mice.

        Figure

        Schematic Diagram
        Figure 1. The mRNA binding protein CPEB associates with the UUUUUAU cytoplasmic polyadenylation element (CPE) in 3’ UTRs. CPEB also binds the non-canonical poly(A) polymerase Gld2, the deadenylase PARN, the AAUAAA poly(A) cleavage site factors CPSF, the scaffold protein symplekin, and the translation inhibitor factor maskin. PARN activity removes the poly(A) tail as soon as it is added by Gld2. Maskin represses translation buy binding the cap-binding factor eIF4E. In response to environmental cues, the kinase Aurora A phosphorylates CPEB, which leads to the expulsion of PARN and Gld2-catalyzed cytoplasmic polyadenylation. The newly elongated poly(A) tail is bound by poly(A) binding protein (PABP), which in turn binds eIF4G and helps it bind eIF4E in place of maskin. eIF4G, via eIF3, positions the 40S ribosomal subunit on the 5’ end of the mRNA where it begins to scan for an AUG initiation codon.

        Senescence and growth control

        Senescence is a mechanism cells employ to exit the cell cycle as a guard against malignant transformation. Primary mouse cells that lack the CPEB gene do not senesce but instead are immortal. Similarly, primary human cells from which CPEB is depleted also bypass senescence and exhibit the Warburg Effect, an alteration in bioenergetics often employed by cancer cells to survive in an inhospitable environment.

        CPEB knockout mice display defects in the polarity of mammary epithelial cells, which is recapitulated in vitro with mouse mammary cells depleted of CPEB. This loss of polarity is due to the mis-localization of the mRNA encoding ZO-1, a tight junction protein. When CPEB-depleted mammary cells lose polarity, they undergo an epithelial to mesenchyme transition (EMT), which often presages enhanced metastatic potential. Indeed, CPEB-depleted mammary cells are highly metastatic.

        Figure

        Schematic Diagram
        Figure 2. Mouse mammary epithelial cells grown in suspension form a polarized 3 dimensional architecture with a central cavity and a basal external surface. ZO-1, a tight junction protein (red), is apically localized. In CPEB-depleted cells, the polarity is lost and no central cavity is formed; ZO-1 staining is randomly distributed. The blue (DAPI) staining identifies nuclei.

        Synaptic plasticity, learning and memory, and neuronal metabolism

        CPEB and the cytoplasmic polyadenylation complex reside at postsynaptic sites of neurons in the mammalian central nervous system. In dendrites, they control local mRNA polyadenylation-induced translation in response to synaptic stimulation. Synaptic plasticity, the ability of synapses to undergo long-lasting biochemical and morphological changes in response to stimulation, forms the underlying basis of learning and memory. CPEB knockout mice are defective for synaptic plasticity and hippocampal-dependent memory formation. Hippocampal neurons depleted of other components of the cytoplasmic polyadenylation complex with lentivirus-based shRNAs also display defects in synaptic plasticity, indicating that polyadenylation-induced translation forms an essential mechanism to control translation and higher cognitive function.

        Neurons derived from CPEB knockout mice have alterations in metabolism in that ATP production by mitochondria is compromised. This deficit in ATP reduces dendrite arborization and is observed in both neurons cultured in vitro and neurons expressing an shRNA for CPEB in vivo.

        Figure

        Figure 3. Cultured mouse hippocampal neurons form neurite extensions with filipodia extending from growth cones. The CPEB-associated translational control protein neuroguidin forms puncta in the neurites and filipodia.

        Figure

        Figure 4. Rat hippocampus was injected with lentivirus expressing shRNA for the unusual poly(A) polymerase Gld2 as well as GFP. The sectioned hippocampus shows GFP fluorescence in the dentate gyrus region of the hippocampus.

        Neurologic disease

        The Fragile X Syndrome (FXS) is the most common heritable form of mental retardation and the most common monogenic form of autism. FXS is caused by a triplet repeat expansion in and transcriptional silencing of the FMR1 gene. FMR1 encodes FMRP, an RNA binding protein that normally represses translation in the brain. In the absence of FMRP, aberrantly high translation likely causes FXS in both humans and a mouse model. Restoration of normal translation occurs in FMRP/CPEB double knockout mice. Moreover, rescue of synapse function and learning and memory also occurs in FMRP/CPEB double knockout mice, suggesting that CPEB might be a novel therapeutic to reverse FXS.



        Rotation Projects

        Potential Rotation Projects

        1. The program of early development in all animals is regulated at the level of messenger RNA translation. We investigate regulated mRNA translation in oocytes and embryos of Xenopus and the mouse. Xenopus oocytes are used to study the molecular mechanisms of mRNA translation, and to assess the influence of translational control on various aspects of oogenesis and embryogenesis. We use the mouse to make targeted gene knockouts of translation factors and examine the effects on early mammalian development.


        2. Recent work has demonstrated that the Xenopus embryonic cell cycle is regulated is regulated at the level of mRNA translation. Further work suggests that mRNA translational may also control the mammalian somatic cell cycle. We employ FACS analysis to examine HeLa and MCF7 breast cancer cell cycle progression following transfection of cDNAs for dominant negative mutant forms of specific translation factors.


        3. Synaptic plasticity, which probably underlies learning and long term memory storage in the central nervous system, is regulated at least in part by mRNA translational control in dendrites. One protein that controls translation in Xenopus and mouse oocytes, CPEB, is present in dendrites and appears to be important for learning and memory. Similarly, axon guidance is also influenced by mRNA translational control, and CPEB and associated factors may be involved here as well. For these studies, we employ cultured hippocampal neurons, knockout mice, and Drosophila, which offers a genetic approach to these problems.


        Bibliographic 
        selected publications
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        1. Udagawa T, Farny NG, Jakovcevski M, Kaphzan H, Alarcon JM, Anilkumar S, Ivshina M, Hurt JA, Nagaoka K, Nalavadi VC, Lorenz LJ, Bassell GJ, Akbarian S, Chattarji S, Klann E, Richter JD. Genetic and acute CPEB1 depletion ameliorate fragile X pathophysiology. Nat Med. 2013 Oct 20.
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        2. Swanger SA, He YA, Richter JD, Bassell GJ. Dendritic GluN2A Synthesis Mediates Activity-Induced NMDA Receptor Insertion. J Neurosci. 2013 May 15; 33(20):8898-908.
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        3. D'Ambrogio A, Nagaoka K, Richter JD. Translational control of cell growth and malignancy by the CPEBs. Nat Rev Cancer. 2013 Apr; 13(4):283-90.
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        4. Oruganty-Das A, Ng T, Udagawa T, Goh EL, Richter JD. Translational control of mitochondrial energy production mediates neuron morphogenesis. Cell Metab. 2012 Dec 5; 16(6):789-800.
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        5. D'Ambrogio A, Gu W, Udagawa T, Mello CC, Richter JD. Specific miRNA Stabilization by Gld2-Catalyzed Monoadenylation. Cell Rep. 2012 Dec 27; 2(6):1537-45.
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        6. Nechama M, Lin CL, Richter JD. An Unusual Two-Step Control of CPEB Destruction by Pin1. Mol Cell Biol. 2013 Jan; 33(1):48-58.
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        7. Darnell JC, Richter JD. Cytoplasmic RNA-Binding Proteins and the Control of Complex Brain Function. Cold Spring Harb Perspect Biol. 2012; 4(8).
          View in: PubMed
        8. 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 Jun 20.
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        9. Lin CL, Huang YT, Richter JD. Transient CPEB dimerization and translational control. RNA. 2012 May; 18(5):1050-61.
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        10. 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.
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        11. Alexandrov IM, Ivshina M, Jung DY, Friedline R, Ko HJ, Xu M, O'Sullivan-Murphy B, Bortell R, Huang YT, Urano F, Kim JK, Richter JD. Cytoplasmic Polyadenylation Element Binding Protein Deficiency Stimulates PTEN and Stat3 mRNA Translation and Induces Hepatic Insulin Resistance. PLoS Genet. 2012 Jan; 8(1):e1002457.
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        12. Liu-Yesucevitz L, Bassell GJ, Gitler AD, Hart AC, Klann E, Richter JD, Warren ST, Wolozin B. Local RNA translation at the synapse and in disease. J Neurosci. 2011 Nov 9; 31(45):16086-93.
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        13. Richter JD, Lasko P. Translational control in oocyte development. Cold Spring Harb Perspect Biol. 2011; 3(9).
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        14. Darnell JC, Van Driesche SJ, Zhang C, Hung KY, Mele A, Fraser CE, Stone EF, Chen C, Fak JJ, Chi SW, Licatalosi DD, Richter JD, Darnell RB. FMRP Stalls Ribosomal Translocation on mRNAs Linked to Synaptic Function and Autism. Cell. 2011 Jul 22; 146(2):247-61.
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        15. Richter JD, Treisman JE. Not just the messenger: RNA takes control. Curr Opin Genet Dev. 2011 Aug; 21(4):363-5.
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        16. Groppo R, Richter JD. CPEB Control of NF-{kappa}B Nuclear Localization and Interleukin-6 Production Mediates Cellular Senescence. Mol Cell Biol. 2011 Jul; 31(13):2707-14.
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        17. 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 May 5; 473(7345):105-8.
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        18. Richter JD. Translational control of synaptic plasticity. Biochem Soc Trans. 2010 Dec 1; 38(6):1527-30.
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        19. Kan MC, Oruganty-Das A, Cooper-Morgan A, Jin G, Swanger SA, Bassell GJ, Florman H, van Leyen K, Richter JD. CPEB4 is a cell survival protein retained in the nucleus upon ischemia or endoplasmic reticulum calcium depletion. Mol Cell Biol. 2010 Dec; 30(24):5658-71.
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        20. Lin CL, Evans V, Shen S, Xing Y, Richter JD. The nuclear experience of CPEB: implications for RNA processing and translational control. RNA. 2010 Feb; 16(2):338-48.
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        21. Cao Q, Padmanabhan K, Richter JD. Pumilio 2 controls translation by competing with eIF4E for 7-methyl guanosine cap recognition. RNA. 2010 Jan; 16(1):221-7.
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        22. Costa-Mattioli M, Sonenberg N, Richter JD. Chapter 8 translational regulatory mechanisms in synaptic plasticity and memory storage. Prog Mol Biol Transl Sci. 2009; 90:293-311.
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        23. Zukin RS, Richter JD, Bagni C. Signals, synapses, and synthesis: how new proteins control plasticity. Front Neural Circuits. 2009; 3:14.
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        24. Groppo R, Richter JD. Translational control from head to tail. Curr Opin Cell Biol. 2009 Jun; 21(3):444-51.
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        25. Lin AC, Tan CL, Lin CL, Strochlic L, Huang YS, Richter JD, Holt CE. Cytoplasmic polyadenylation and cytoplasmic polyadenylation element-dependent mRNA regulation are involved in Xenopus retinal axon development. Neural Dev. 2009; 4:8.
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        26. Richter JD, Klann E. Making synaptic plasticity and memory last: mechanisms of translational regulation. Genes Dev. 2009 Jan 1; 23(1):1-11.
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        27. Burns DM, Richter JD. CPEB regulation of human cellular senescence, energy metabolism, and p53 mRNA translation. Genes Dev. 2008 Dec 15; 22(24):3449-60.
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        28. 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 Aug 20; 28(34):8502-9.
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        29. Richter JD. Think you know how miRNAs work? Think again. Nat Struct Mol Biol. 2008 Apr; 15(4):334-6.
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        30. Richter JD. Breaking the code of polyadenylation-induced translation. Cell. 2008 Feb 8; 132(3):335-7.
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        31. Kim JH, Richter JD. Measuring CPEB-mediated cytoplasmic polyadenylation-deadenylation in Xenopus laevis oocytes and egg extracts. Methods Enzymol. 2008; 448:119-38.
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        32. Kim JH, Richter JD. RINGO/cdk1 and CPEB mediate poly(A) tail stabilization and translational regulation by ePAB. Genes Dev. 2007 Oct 15; 21(20):2571-9.
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        33. Richter JD. CPEB: a life in translation. Trends Biochem Sci. 2007 Jun; 32(6):279-85.
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        34. Richter JD, Fallon JR. Synapses go nucle(ol)ar. Nat Neurosci. 2007 Apr; 10(4):399-400.
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        35. Tung JJ, Padmanabhan K, Hansen DV, Richter JD, Jackson PK. Translational unmasking of Emi2 directs cytostatic factor arrest in meiosis II. Cell Cycle. 2007 Mar 15; 6(6):725-31.
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        36. Huang YS, Richter JD. Analysis of mRNA translation in cultured hippocampal neurons. Methods Enzymol. 2007; 431:143-62.
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        37. Nottrott S, Simard MJ, Richter JD. Human let-7a miRNA blocks protein production on actively translating polyribosomes. Nat Struct Mol Biol. 2006 Dec; 13(12):1108-14.
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        38. 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 Dec; 13(12):1128-34.
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        39. Kim JH, Richter JD. Opposing polymerase-deadenylase activities regulate cytoplasmic polyadenylation. Mol Cell. 2006 Oct 20; 24(2):173-83.
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        40. Racki WJ, Richter JD. CPEB controls oocyte growth and follicle development in the mouse. Development. 2006 Nov; 133(22):4527-37.
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        41. 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 Oct 18; 25(20):4865-76.
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        42. Groisman I, Ivshina M, Marin V, Kennedy NJ, Davis RJ, Richter JD. Control of cellular senescence by CPEB. Genes Dev. 2006 Oct 1; 20(19):2701-12.
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        43. Zeissig S, Bürgel N, Günzel D, Richter J, Mankertz J, Wahnschaffe U, Kroesen AJ, Zeitz M, Fromm M, Schulzke JD. Changes in expression and distribution of claudin 2, 5 and 8 lead to discontinuous tight junctions and barrier dysfunction in active Crohn's disease. Gut. 2007 Jan; 56(1):61-72.
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        44. Jung MY, Lorenz L, Richter JD. Translational control by neuroguidin, a eukaryotic initiation factor 4E and CPEB binding protein. Mol Cell Biol. 2006 Jun; 26(11):4277-87.
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        45. Padmanabhan K, Richter JD. Regulated Pumilio-2 binding controls RINGO/Spy mRNA translation and CPEB activation. Genes Dev. 2006 Jan 15; 20(2):199-209.
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        46. Berger-Sweeney J, Zearfoss NR, Richter JD. Reduced extinction of hippocampal-dependent memories in CPEB knockout mice. Learn Mem. 2006 Jan-Feb; 13(1):4-7.
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        47. Cao Q, Huang YS, Kan MC, Richter JD. Amyloid precursor proteins anchor CPEB to membranes and promote polyadenylation-induced translation. Mol Cell Biol. 2005 Dec; 25(24):10930-9.
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        48. 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 Sep; 25(17):7605-15.
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        49. Du L, Richter JD. Activity-dependent polyadenylation in neurons. RNA. 2005 Sep; 11(9):1340-7.
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        50. Richter JD, Sonenberg N. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature. 2005 Feb 3; 433(7025):477-80.
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        51. Barnard DC, Ryan K, Manley JL, Richter JD. Symplekin and xGLD-2 are required for CPEB-mediated cytoplasmic polyadenylation. Cell. 2004 Nov 24; 119(5):641-51.
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        52. Richter JD. RNA transport (partly) revealed! Neuron. 2004 Aug 19; 43(4):442-3.
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        53. Huang YS, Richter JD. Regulation of local mRNA translation. Curr Opin Cell Biol. 2004 Jun; 16(3):308-13.
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        54. 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 May-Jun; 11(3):318-27.
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        55. Sarkissian M, Mendez R, Richter JD. Progesterone and insulin stimulation of CPEB-dependent polyadenylation is regulated by Aurora A and glycogen synthase kinase-3. Genes Dev. 2004 Jan 1; 18(1):48-61.
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        56. 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 Jun 15; 17(12):1457-62.
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        57. Huang YS, Carson JH, Barbarese E, Richter JD. Facilitation of dendritic mRNA transport by CPEB. Genes Dev. 2003 Mar 1; 17(5):638-53.
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        58. 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 Jul 15; 21(14):3852-62.
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        59. Richter JD, Lorenz LJ. Selective translation of mRNAs at synapses. Curr Opin Neurobiol. 2002 Jun; 12(3):300-4.
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        60. Groisman I, Jung MY, Sarkissian M, Cao Q, Richter JD. Translational control of the embryonic cell cycle. Cell. 2002 May 17; 109(4):473-83.
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        61. Huang YS, Jung MY, Sarkissian M, Richter JD. N-methyl-D-aspartate receptor signaling results in Aurora kinase-catalyzed CPEB phosphorylation and alpha CaMKII mRNA polyadenylation at synapses. EMBO J. 2002 May 1; 21(9):2139-48.
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        62. Mendez R, Barnard D, Richter JD. Differential mRNA translation and meiotic progression require Cdc2-mediated CPEB destruction. EMBO J. 2002 Apr 2; 21(7):1833-44.
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        63. Cattaruzza M, Berger MM, Ochs M, Fayyazi A, Füzesi L, Richter J, Hecker M. Deformation-induced endothelin B receptor-mediated smooth muscle cell apoptosis is matrix-dependent. Cell Death Differ. 2002 Feb; 9(2):219-26.
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        64. Tay J, Richter JD. Germ cell differentiation and synaptonemal complex formation are disrupted in CPEB knockout mice. Dev Cell. 2001 Aug; 1(2):201-13.
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        65. Richter JD, Theurkauf WE. Development. The message is in the translation. Science. 2001 Jul 6; 293(5527):60-2.
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        66. Mendez R, Richter JD. Translational control by CPEB: a means to the end. Nat Rev Mol Cell Biol. 2001 Jul; 2(7):521-9.
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        67. 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 Jul; 128(14):2815-22.
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        68. Richter JD. Think globally, translate locally: what mitotic spindles and neuronal synapses have in common. Proc Natl Acad Sci U S A. 2001 Jun 19; 98(13):7069-71.
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        69. 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; 66:345-51.
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        70. de Moor CH, Richter JD. Translational control in vertebrate development. Int Rev Cytol. 2001; 203:567-608.
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        71. 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 Nov; 6(5):1253-9.
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        72. Groisman I, Huang YS, Mendez R, Cao Q, Theurkauf W, Richter JD. CPEB, maskin, and cyclin B1 mRNA at the mitotic apparatus: implications for local translational control of cell division. Cell. 2000 Oct 27; 103(3):435-47.
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        73. Irwin RS, Richter JE. Gastroesophageal reflux and chronic cough. Am J Gastroenterol. 2000 Aug; 95(8 Suppl):S9-14.
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        74. Tay J, Hodgman R, Richter JD. The control of cyclin B1 mRNA translation during mouse oocyte maturation. Dev Biol. 2000 May 1; 221(1):1-9.
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        75. 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 Mar 16; 404(6775):302-7.
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        76. Stebbins-Boaz B, Cao Q, de Moor CH, Mendez R, Richter JD. Maskin is a CPEB-associated factor that transiently interacts with elF-4E. Mol Cell. 1999 Dec; 4(6):1017-27.
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        77. Richter JD. Cytoplasmic polyadenylation in development and beyond. Microbiol Mol Biol Rev. 1999 Jun; 63(2):446-56.
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        78. de Moor CH, Richter JD. Cytoplasmic polyadenylation elements mediate masking and unmasking of cyclin B1 mRNA. EMBO J. 1999 Apr 15; 18(8):2294-303.
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        79. Walker J, Minshall N, Hake L, Richter J, Standart N. The clam 3' UTR masking element-binding protein p82 is a member of the CPEB family. RNA. 1999 Jan; 5(1):14-26.
          View in: PubMed
        80. 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 alpha-CaMKII mRNA at synapses. Neuron. 1998 Nov; 21(5):1129-39.
          View in: PubMed
        81. Kuge H, Brownlee GG, Gershon PD, Richter JD. Cap ribose methylation of c-mos mRNA stimulates translation and oocyte maturation in Xenopus laevis. Nucleic Acids Res. 1998 Jul 1; 26(13):3208-14.
          View in: PubMed
        82. 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 Nov; 17(11):6402-9.
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        83. de Moor CH, Richter JD. The Mos pathway regulates cytoplasmic polyadenylation in Xenopus oocytes. Mol Cell Biol. 1997 Nov; 17(11):6419-26.
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