1932

Abstract

The cytoplasmic polyadenylation element binding (CPEB) proteins are sequence-specific mRNA binding proteins that control translation in development, health, and disease. CPEB1, the founding member of this family, has become an important model for illustrating general principles of translational control by cytoplasmic polyadenylation in gametogenesis, cancer etiology, synaptic plasticity, learning, and memory. Although the biological functions of the other members of this protein family in vertebrates are just beginning to emerge, it is already evident that they, too, mediate important processes, such as cancer etiology and higher cognitive function. In , the CPEB proteins Orb and Orb2 play key roles in oogenesis and in neuronal function, as do related proteins in and . We review the biochemical features of the CPEB proteins, discuss their activities in several biological systems, and illustrate how understanding CPEB activity in model organisms has an important impact on neurological disease.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-101011-155831
2014-10-06
2024-10-12
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/30/1/annurev-cellbio-101011-155831.html?itemId=/content/journals/10.1146/annurev-cellbio-101011-155831&mimeType=html&fmt=ahah

Literature Cited

  1. Alarcon J, Hodgman R, Theis M, Huang YS, Kandel ER, Richter JD. 2004. Selective modulation of some forms of Schaffer collateral-CA1 synaptic plasticity in mice with a disruption of the CPEB-1 gene. Learn. Mem. 11:318–27 [Google Scholar]
  2. Alexandrov IM, Ivshina M, Jung DY, Friedline R, Ko HJ. et al. 2012. Cytoplasmic polyadenylation element binding protein deficiency stimulates PTEN and Stat3 mRNA translation and induces hepatic insulin resistance. PLOS Genet. 8:1e1002457 [Google Scholar]
  3. Austin J, Kimble J. 1987. glp-1 is required in the germ line for regulation of the decision between mitosis and meiosis in C. elegans. Cell 51:589–99 [Google Scholar]
  4. Austin J, Kimble J. 1989. Transcript analysis of glp-1 and lin-12, homologous genes required for cell interactions during development of C. elegans. Cell 58:565–71 [Google Scholar]
  5. Barnard DC, Cao Q, Richter JD. 2005. Differential phosphorylation controls Maskin association with eukaryotic translation initiation factor 4E and localization on the mitotic apparatus. Mol. Cell. Biol. 25:7605–15 [Google Scholar]
  6. Barnard DC, Ryan K, Manley JL, Richter JD. 2004. Symplekin and xGLD-2 are required for CPEB-mediated cytoplasmic polyadenylation. Cell 119:641–51 [Google Scholar]
  7. Barton MK, Kimble J. 1990. fog-1, a regulatory gene required for specification of spermatogenesis in the germ line of Caenorhabditis elegans. Genetics 125:29–39 [Google Scholar]
  8. Bava FA, Eliscovich C, Ferreira PG, Miñana B, Ben-Dov C. et al. 2013. CPEB1 coordinates alternative 3′ UTR formation with translational regulation. Nature 495:121–25 [Google Scholar]
  9. Benoit B, He CH, Zhang F, Votruba SM, Tadros W. et al. 2009. An essential role for the RNA-binding protein Smaug during the Drosophila maternal-to-zygotic transition. Development 136:923–32 [Google Scholar]
  10. Benoit P, Papin C, Kwak JE, Wickens M, Simonelig M. 2008. PAP- and GLD-2-type poly(A) polymerases are required sequentially in cytoplasmic polyadenylation and oogenesis in Drosophila. Development 135:1969–79 [Google Scholar]
  11. Berger-Sweeney J, Zearfoss NR, Richter JD. 2006. Reduced extinction of hippocampal-dependent memories in CPEB knockout mice. Learn. Mem. 13:4–7 [Google Scholar]
  12. Bestman JE, Cline HT. 2008. The RNA binding protein CPEB regulates dendrite morphogenesis and neuronal circuit assembly in vivo. Proc. Natl. Acad. Sci. USA 105:20494–99 [Google Scholar]
  13. Boag PR, Nakamura A, Blackwell TK. 2005. A conserved RNA-protein complex component involved in physiological germline apoptosis regulation in C. elegans. Development 132:4975–86 [Google Scholar]
  14. Bogen O, Alessandri-Haber N, Chu C, Gear RW, Levine JD. 2012. Generation of a pain memory in the primary afferent nociceptor triggered by PKCε activation of CPEB. J. Neurosci. 32:2018–26 [Google Scholar]
  15. Burns DM, D'Ambrogio A, Nottrott S, Richter JD. 2011. CPEB and two poly(A) polymerases control miR-122 stability and p53 mRNA translation. Nature 473:105–8 [Google Scholar]
  16. Burns DM, Richter J. 2008. CPEB regulation of human cellular senescence, energy metabolism, and p53 mRNA translation. Genes Dev. 22:3449–60 [Google Scholar]
  17. Campbell ZT, Menichelli E, Friend K, Wu J, Kimble J. et al. 2012. Identification of a conserved interface between PUF and CPEB proteins. J. Biol. Chem. 287:18854–62 [Google Scholar]
  18. Cao Q, Kim JH, Richter JD. 2006. CDK1 and calcineurin regulate Maskin association with eIF4E and translational control of cell cycle progression. Nat. Struct. Mol. Biol. 13:1128–34 [Google Scholar]
  19. Cao Q, Richter JD. 2002. Dissolution of the Maskin-eIF4E complex by cytoplasmic polyadenylation and poly(A)-binding protein controls cyclin B1 mRNA translation and oocyte maturation. EMBO J. 21:3852–62 [Google Scholar]
  20. Carpenter AT. 1975. Electron microscopy of meiosis in Drosophila melanogaster females. I. Structure, arrangement, and temporal change of the synaptonemal complex in wild-type. Chromosoma 51:157–82 [Google Scholar]
  21. Castagnetti S, Ephrussi A. 2003. Orb and a long poly(A) tail are required for oskar translation at the posterior pole of the Drosophila oocyte. Development 130:835–43 [Google Scholar]
  22. Chang JS, Tan L, Schedl P. 1999. The Drosophila CPEB homolog, Orb, is required for Oskar protein expression in oocytes. Dev. Biol. 215:91–106 [Google Scholar]
  23. Chang JS, Tan L, Wolf MR, Schedl P. 2001. Functioning of the Drosophila Orb gene in gurken mRNA localization and translation. Development 128:3169–77 [Google Scholar]
  24. Chao HW, Tsai LY, Lu YL, Lin PY, Huang WH. et al. 2013. Deletion of CPEB3 enhances hippocampus-dependent memory via increasing expressions of PSD95 and NMDA receptors. J. Neurosci. 33:17008–22 [Google Scholar]
  25. Chen J, Melton C, Suh N, Oh JS, Homer K. et al. 2011. Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. Genes Dev. 25:755–66 [Google Scholar]
  26. Chen PJ, Huang YS. 2012. CPEB2-eEF2 interaction impedes HIF-1α RNA translation. EMBO J. 31:959–71 [Google Scholar]
  27. Cheung LS, Schüpbach T, Shvartsman SV. 2011. Pattern formation by receptor tyrosine kinases: analysis of the Gurken gradient in Drosophila oogenesis. Curr. Opin. Genet. Dev. 21:719–25 [Google Scholar]
  28. Chicoine J, Benoit P, Gamberi C, Paliouras M, Simonelig M, Lasko P. 2007. Bicaudal-C recruits CCR4-NOT deadenylase to target mRNAs and regulates oogenesis, cytoskeletal organization, and its own expression. Dev. Cell 13:691–704 [Google Scholar]
  29. Christerson LB, McKearin DM. 1994. Orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis. Genes Dev. 8:614–28 [Google Scholar]
  30. Costa A, Pazman C, Sinsimer KS, Wong LC, McLeod I. et al. 2013. Rasputin functions as a positive regulator of Orb in Drosophila oogenesis. PLOS ONE 8:9e72864 [Google Scholar]
  31. Costa A, Wand Y, Dockendorf TC, Erdjument-Bromage H, Tempst P. et al. 2005. The Drosophila fragile X protein functions as a negative regulator in the Orb autoregulatory pathway. Dev. Cell 8:331–42 [Google Scholar]
  32. Crittenden SL, Bernstein DS, Bachorik JL, Thompson BE, Gallegos M. et al. 2002. A conserved RNA-binding protein controls germline stem cells in Caenorhabditis elegans. Nature 417:660–63 [Google Scholar]
  33. Cui J, Sackton KL, Horner VL, Kumar KE, Wolfner MF. 2008. Wispy, the Drosophila homolog of GLD-2, is required during oogenesis and egg activation. Genetics 178:2017–29 [Google Scholar]
  34. D'Ambrogio A, Gu W, Udegawa T, Mello CC, Richter JD. 2012. Specific miRNA stabilization by Gld2-catalyzed monoadenylation. Cell Rep. 27:1537–45 [Google Scholar]
  35. D'Ambrogio A, Nagaoka K, Richter JD. 2013. Translational control of cell growth and malignancy by the CPEBs. Nat. Rev. Cancer 13:283–90 [Google Scholar]
  36. Darnell JC, Klann E. 2013. The translation of translational control by FMRP: therapeutic targets for FXS. Nat. Neurosci. 16:1530–36 [Google Scholar]
  37. Darnell JC, Richter JD. 2012. Cytoplasmic RNA-binding proteins and the control of complex brain function. Cold Spring Harb. Perspect. Biol. 4:8a012344 [Google Scholar]
  38. Darnell JC, Van Driesche SJ, Zhang C, Hung KY, Mele A. et al. 2011. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146:247–61 [Google Scholar]
  39. DePace AH, Santoso A, Hillner P, Weissman JS. 1998. A critical role for amino-terminal glutamine/asparagine repeats in the formation and propagation of a yeast prion. Cell 93:1241–52 [Google Scholar]
  40. Du L, Richter JD. 2005. Activity-dependent polyadenylation in neurons. RNA 11:1340–47 [Google Scholar]
  41. Eckmann CR, Crittenden SL, Suh N, Kimble J. 2004. GLD-3 and control of the mitosis/meiosis decision in the germline of Caenorhabditis elegans. Genetics 168:147–60 [Google Scholar]
  42. Eliscovich C, Peset I, Vernos I, Méndez R. 2008. Spindle-localized CPE-mediated translation controls meiotic chromosome segregation. Nat. Cell Biol. 10:858–65 [Google Scholar]
  43. Feng Y, Gutekunst CA, Eberhart DE, Yi H, Warren ST, Hersch SM. 1997. Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J. Neurosci. 17:1539–47 [Google Scholar]
  44. Ferby I, Blazquez M, Palmer A, Eritja R, Nebreda AR. 1999. A novel p34cdc2-binding and activating protein that is necessary and sufficient to trigger G2/M progression in Xenopus oocytes. Genes Dev. 13:2177–89 [Google Scholar]
  45. Ferrari LF, Bogen O, Levine JD. 2013. Role of nociceptor αCaMKII in transition from acute to chronic pain (hyperalgesic priming) in male and female rats. J. Neurosci. 33:11002–11 [Google Scholar]
  46. Groisman I, Huang YS, Méndez R, Cao Q, Theurkauf W, Richter JD. 2000. CPEB, Maskin, and cyclin B1 mRNA at the mitotic apparatus: implications for local translational control of cell division. Cell 103:435–47 [Google Scholar]
  47. Groisman I, Ivshina M, Marin V, Kennedy NJ, Davis RJ, Richter JD. 2006. Control of cellular senescence by CPEB. Genes Dev. 20:2701–12 [Google Scholar]
  48. Groisman I, Jung MY, Sarkissian M, Cao Q, Richter JD. 2002. Translational control of the embryonic cell cycle. Cell 109:473–83 [Google Scholar]
  49. Groppo R, Richter JD. 2011. CPEB control of NF-κB nuclear localization and interleukin-6 production mediates cellular senescence. Mol. Cell. Biol. 31:2707–14 [Google Scholar]
  50. Hafer N, Xu S, Bhat KM, Schedl P. 2011. The Drosophila CPEB protein Orb2 has a novel expression pattern and is important for asymmetric cell division and nervous system function. Genetics 189:907–21 [Google Scholar]
  51. Hägele S, Kühn U, Böning M, Katschinski DM. 2009. 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. 417:235–46 [Google Scholar]
  52. Hansen D, Wilson-Berry L, Dang T, Schedl T. 2004. Control of the proliferation versus meiotic development decision in the C. elegans germline through regulation of GLD-1 protein accumulation. Development 131:93–104 [Google Scholar]
  53. Hasegawa E, Karashima T, Sumiyoshi E, Yamamoto M. 2006. C. elegans CPB-3 interacts with DAZ-1 and functions in multiple steps of germline development. Dev. Biol. 295:689–99 [Google Scholar]
  54. Heinrich SU, Lindquist S. 2011. Protein-only mechanism induces self-perpetuating changes in the activity of neuronal Aplysia cytoplasmic polyadenylation element binding protein (CPEB). Proc. Natl. Acad. Sci. USA 108:2999–3004 [Google Scholar]
  55. Huang YS, Carson JH, Barbarese E, Richter JD. 2003. Facilitation of dendritic mRNA transport by CPEB. Genes Dev. 17:638–53 [Google Scholar]
  56. Huang YS, Jung MY, Sarkissian M, Richter JD. 2002. N-methyl-d-aspartate receptor signaling results in Aurora kinase-catalyzed CPEB phosphorylation and αCaMKII mRNA polyadenylation at synapses. EMBO J. 21:2139–48 [Google Scholar]
  57. Huang YS, Kan MC, Lin CL, Richter JD. 2006. CPEB3 and CPEB4 in neurons: analysis of RNA-binding specificity and translational control of AMPA receptor GluR2 mRNA. EMBO J. 25:4865–76 [Google Scholar]
  58. Huynh J-R, St. Johnston D. 2000. The role of BicD, Egl, Orb and the microtubules in the restriction of meiosis in the Drosophila oocyte. Development 127:2785–94 [Google Scholar]
  59. Jin S-W, Arno N, Cohen A, Shah A, Xu Q. et al. 2001a. In Caenorhabditis elegans, the RNA-binding domains of the cytoplasmic polyadenylation element binding protein FOG-1 are needed to regulate germ cell fates. Genetics 159:1617–30 [Google Scholar]
  60. Jin S-W, Kimble J, Ellis RE. 2001b. Regulation of cell fate in Caenorhabditis elegans by a novel cytoplasmic polyadenylation element binding protein. Dev. Biol. 229:537–53 [Google Scholar]
  61. Juge F, Zaessinger S, Temme C, Wahle E, Simonelig M. 2002. Control of poly(A) polymerase level is essential to cytoplasmic polyadenylation and early development in Drosophila. EMBO J. 21:6603–13 [Google Scholar]
  62. Jungkamp AC, Stoeckius M, Mecenas D, Grün D, Mastrobuoni G. et al. 2011. In vivo and transcriptome-wide identification of RNA binding protein target sites. Mol. Cell 44:828–40 [Google Scholar]
  63. Kadyk LC, Kimble J. 1998. Genetic regulation of entry into meiosis in Caenorhabditis elegans. Development 125:1803–13 [Google Scholar]
  64. Kan MC, Oruganty-Das A, Cooper-Morgan A, Jin G, Swanger SA. et al. 2010. CPEB4 is a cell survival protein retained in the nucleus upon ischemia or endoplasmic reticulum calcium depletion. Mol. Cell. Biol. 30:5658–71 [Google Scholar]
  65. Kandel ER. 2001. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030–38 [Google Scholar]
  66. Kandel ER. 2012. The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Mol. Brain 5:14 [Google Scholar]
  67. Kang H, Schuman EM. 1996. A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273:1402–6 [Google Scholar]
  68. Katoh T, Sakaguchi Y, Miyauchi K, Suzuki T, Kashiwabara S. et al. 2009. Selective stabilization of mammalian microRNAs by 3′ adenylation mediated by the cytoplasmic poly(A) polymerase GLD-2. Genes Dev. 23:433–38 [Google Scholar]
  69. Keleman K, Krüttner S, Alenius M, Dickson BJ. 2007. Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat. Neurosci. 10:1587–93 [Google Scholar]
  70. Kelleher RJ 3rd, Bear MF. 2008. The autistic neuron: Troubled translation?. Cell 135:401–6 [Google Scholar]
  71. Kim JH, Richter JD. 2006. Opposing polymerase-deadenylase activities regulate cytoplasmic polyadenylation. Mol. Cell 24:173–83 [Google Scholar]
  72. Kim JH, Richter JD. 2007. RINGO/cdk1 and CPEB mediate poly(A) tail stabilization and translational regulation by ePAB. Genes Dev. 21:2571–79 [Google Scholar]
  73. King RC. 1970. Ovarian Development in Drosophila melanogaster. New York: Academic [Google Scholar]
  74. Krüttner S, Stepien B, Noordermeer JN, Mommaas MA, Mechtler K. et al. 2012. Drosophila CPEB Orb2A mediates memory independent of its RNA-binding domain. Neuron 76:383–95 [Google Scholar]
  75. Lamont LB, Crittenden SL, Bernstein D, Wickens M, Kimble J. 2004. FBF-1 and FBF-2 regulate the size of the mitotic region in the C. elegans germline. Dev. Cell 7:697–707 [Google Scholar]
  76. Lamont LB, Kimble J. 2007. Developmental expression of FOG-1/CPEB protein and its control in the Caenorhabditis elegans hermaphroditic germ line. Dev. Dyn. 236:871–79 [Google Scholar]
  77. Lantz V, Chang JS, Horabin JI, Bopp D, Schedl P. 1994. The Drosophila orb RNA-binding protein is required for the formation of the egg chamber and establishment of polarity. Genes Dev. 8:598–613 [Google Scholar]
  78. Lee MH, Schedl T. 2001. Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development. Genes Dev. 15:2408–20 [Google Scholar]
  79. Lin CL, Huang YT, Richter JD. 2012. Transient CPEB dimerization and translational control. RNA 18:1050–61 [Google Scholar]
  80. Luitjens C, Gallegos M, Kraemer B, Kimble J, Wickens M. 2000. CPEB proteins control two key steps in spermatogenesis in C. elegans. Genes Dev. 14:2596–609 [Google Scholar]
  81. Majumdar A, Cesario WC, White-Grindley E, Jiang H, Ren F. et al. 2012. Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory. Cell 148:515–29 [Google Scholar]
  82. Marin VA, Evans TC. 2003. Translational repression of a C. elegans Notch mRNA by the STAR/KH domain protein GLD-1. Development 130:2623–32 [Google Scholar]
  83. Markussen F-H, Michon A-M, Breitwieser W, Ephrussi A. 1995. Translational control of oskar generates Short OSK, the isoform that induces pole plasm assembly. Development 121:3723–32 [Google Scholar]
  84. Maruyama R, Endo S, Sugimoto A, Yamamoto M. 2005. Caenorhabditis elegans DAZ-1 is expressed in proliferating germ cells and directs proper nuclear organization and cytoplasmic core formation during oogenesis. Dev. Biol. 277:142–54 [Google Scholar]
  85. Mastushita-Sakai T, White-Grindley E, Samuelson J, Seidel C, Si K. 2010. Drosophila Orb2 targets genes involved in neuronal growth, synapse formation, and protein turnover. Proc. Natl. Acad. Sci. USA 107:11987–92 [Google Scholar]
  86. Mayford M, Siegelbaum SA, Kandel ER. 2012. Synapses and memory storage. Cold Spring Harb. Perspect. Biol. 4:6a005751 [Google Scholar]
  87. Méndez R, Barnard D, Richter JD. 2002. Differential mRNA translation and meiotic progression require Cdc2-mediated CPEB destruction. EMBO J. 21:1833–44 [Google Scholar]
  88. Méndez R, Hake LE, Andresson T, Littlepage LE, Ruderman JV, Richter JD. 2000a. Phosphorylation of CPE binding factor by Eg2 regulates translation of c-mos mRNA. Nature 404:302–7 [Google Scholar]
  89. Méndez R, Murthy KG, Ryan K, Manley JL, Richter JD. 2000b. Phosphorylation of CPEB by Eg2 mediates the recruitment of CPSF into an active cytoplasmic polyadenylation complex. Mol. Cell 6:1253–59 [Google Scholar]
  90. Méndez R, Richter JD. 2001. Translational control by CPEB: a means to the end. Nat. Rev. Mol. Cell Biol. 2:521–29 [Google Scholar]
  91. Menichelli E, Wu J, Campbell ZT, Wickens M, Williamson JR. 2013. Biochemical characterization of the Caenorhabditis elegans FBF·CPB-1 translational regulation complex identifies conserved protein interaction hotspots. J. Mol. Biol. 425:725–37 [Google Scholar]
  92. Miller MA, Olivas WM. 2011. Roles of Puf proteins in mRNA degradation and translation. Wiley Interdiscip. Rev. RNA 2:471–92 [Google Scholar]
  93. Miniaci MC, Kim JH, Puthanveettil SV, Si K, Zhu H. et al. 2008. Sustained CPEB-dependent local protein synthesis is required to stabilize synaptic growth for persistence of long-term facilitation in Aplysia. Neuron 59:1024–36 [Google Scholar]
  94. Morgan CT, Noble D, Kimble J. 2013. Mitosis-meiosis and sperm-oocyte fate decisions are separable regulatory events. Proc. Natl. Acad. Sci. USA 110:3411–16 [Google Scholar]
  95. Murata T, Nagaso H, Kashiwabara S, Baba T, Okano H, Yokoyama KK. 2001. The hiiragi gene encodes a poly(A) polymerase, which controls the formation of the wing margin in Drosophila melanogaster. Dev. Biol. 233:137–47 [Google Scholar]
  96. Nagaoka K, Udagawa T, Richter JD. 2012. CPEB-mediated ZO-1 mRNA localization is required for epithelial tight-junction assembly and cell polarity. Nat. Commun. 3:675 [Google Scholar]
  97. Nairismägi ML, Vislovukh A, Meng Q, Kratassiouk G, Beldiman C. et al. 2012. Translational control of TWIST1 expression in MCF-10A cell lines recapitulating breast cancer progression. Oncogene 31:4960–66 [Google Scholar]
  98. Nebreda AR, Ferby I. 2000. Regulation of the meiotic cell cycle in oocytes. Curr. Opin. Cell Biol. 12:666–75 [Google Scholar]
  99. Nechama M, Lin CL, Richter JD. 2013. An unusual two-step control of CPEB destruction by Pin1. Mol. Cell. Biol. 33:48–58 [Google Scholar]
  100. Neuman-Silberberg FS, Schüpbach T. 1996. The Drosophila TGF-α-like protein Gurken: expression and cellular localization during Drosophila oogenesis. Mech. Dev. 59:105–13 [Google Scholar]
  101. Ortega AD, Willers IM, Sala S, Cuezva JM. 2010. Human GeBP1 interacts with β-F1-ATPase mRNA and inhibits its translation. J. Cell Sci. 123:2685–96 [Google Scholar]
  102. Ortiz-Zapater E, Pineda D, Martínez-Bosch N, Fernández-Miranda G, Iglesias M. et al. 2011. Key contribution of CPEB4-mediated translational control to cancer progression. Nat. Med. 18:83–90 [Google Scholar]
  103. Oruganty-Das A, Ng T, Udagawa T, Goh EL, Richter JD. 2012. Translational control of mitochondrial energy production mediates neuron morphogenesis. Cell Metab. 16:789–800 [Google Scholar]
  104. Padmanabhan K, Richter JD. 2006. Regulated Pumilio-2 binding controls RINGO/Spy mRNA translation and CPEB activation. Genes Dev. 20:199–209 [Google Scholar]
  105. Pai TP, Chen CC, Lin HH, Chin AL, Lai JS. et al. 2013. Drosophila ORB protein in two mushroom body output neurons is necessary for long-term memory formation. Proc. Natl. Acad. Sci. USA 110:7898–903 [Google Scholar]
  106. Pavlopoulos E, Trifilieff P, Chevaleyre V, Fioriti L, Zairis S. et al. 2011. Neuralized1 activates CPEB3: a function for nonproteolytic ubiquitin in synaptic plasticity and memory storage. Cell 147:1369–83 [Google Scholar]
  107. Piqué M, López JM, Foissac S, Guigó R, Méndez R. 2008. A combinatorial code for CPE-mediated translational control. Cell 132:434–48 [Google Scholar]
  108. Racki WJ, Richter JD. 2006. CPEB controls oocyte growth and follicle development in the mouse. Development 133:4527–37 [Google Scholar]
  109. Raveendra BL, Siemer AB, Puthanveettil SV, Hendrickson WA, Kandel ER, McDermott AE. 2013. Characterization of prion-like conformational changes of the neuronal isoform of Aplysia CPEB. Nat. Struct. Mol. Biol. 20:495–501 [Google Scholar]
  110. Reverte CG, Aheam MD, Hake LE. 2001. CPEB degradation during Xenopus oocyte maturation requires a PEST domain and the 26S proteasome. Dev. Biol. 231:447–58 [Google Scholar]
  111. Richter JD. 2001. Think globally, translate locally: what mitotic spindles and neuronal synapses have in common. Proc. Natl. Acad. Sci. USA 98:7069–71 [Google Scholar]
  112. Richter JD, Klann E. 2009. Making synaptic plasticity and memory last: mechanisms of translational regulation. Genes Dev. 23:1–11 [Google Scholar]
  113. Richter JD, Sonenberg N. 2005. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433:477–80 [Google Scholar]
  114. Roth S, Schüpbach T. 1994. The relationship between ovarian and embryonic dorsoventral patterning in Drosophila. Development 120:2245–57 [Google Scholar]
  115. Rybarska A, Harterink M, Jedamzik B, Kupinski AP, Schmid M, Eckmann CR. 2009. GLS-1, a novel P granule component, modulates a network of conserved RNA regulators to influence germ cell fate decisions. PLOS Genet. 5:5e1000494 [Google Scholar]
  116. Sarkissian M, Méndez R, Richter JD. 2004. Progesterone and insulin stimulation of CPEB-dependent polyadenylation is regulated by Aurora A and glycogen synthase kinase-3. Genes Dev. 18:48–61 [Google Scholar]
  117. Scherzinger E, Lurz R, Turmaine M, Mangiarini L, Hollenbach B. et al. 1997. Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 90:549–56 [Google Scholar]
  118. Schmid M, Küchler B, Eckmann CR. 2009. Two conserved regulatory poly(A) polymerases, GLD-4 and GLD-2, regulate meiotic progression in C. elegans. Genes Dev. 23:824–36 [Google Scholar]
  119. Setoyama D, Yamashita M, Sagata N. 2007. Mechanism of degradation of CPEB during Xenopus oocyte maturation. Proc. Natl. Acad. Sci. USA 104:18001–6 [Google Scholar]
  120. Shin CY, Kundel M, Wells DG. 2004. Rapid, activity-induced increase in tissue plasminogen activator is mediated by metabotropic glutamate receptor-dependent mRNA translation. J. Neurosci. 24:9425–33 [Google Scholar]
  121. Si K, Choi YB, White-Grindley E, Majumdar A, Kandel ER. 2010. Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation. Cell 140:421–35 [Google Scholar]
  122. Si K, Giustetto M, Etkin A, Hsu R, Janisiewicz AM. et al. 2003a. A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in Aplysia. Cell 115:893–904 [Google Scholar]
  123. Si K, Lindquist S, Kandel ER. 2003b. A neuronal isoform of the Aplysia CPEB has prion-like properties. Cell 115:879–91 [Google Scholar]
  124. Silva AJ, Paylor R, Wehner JM, Tonegawa S. 1992. Impaired spatial learning in α-calcium-calmodulin kinase II mutant mice. Science 257:206–11 [Google Scholar]
  125. Stebbins-Boaz B, Cao Q, de Moor CH, Méndez R, Richter JD. 1999. Maskin is a CPEB-associated factor that transiently interacts with elF-4E. Mol. Cell 4:1017–27 [Google Scholar]
  126. Stefani G, Fraser CE, Darnell JC, Darnell RB. 2004. Fragile X mental retardation protein is associated with translating polyribosomes in neuronal cells. J. Neurosci. 24:7272–76 [Google Scholar]
  127. Suh N, Jedamzik B, Eckmann CR, Wickens M, Kimble J. 2006. The GLD-2 poly(A) polymerase activates gld-1 mRNA in the Caenorhabditis elegans germ line. Proc. Natl. Acad. Sci. USA 103:15108–12 [Google Scholar]
  128. Sutton MA, Schuman EM. 2006. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 125:785–99 [Google Scholar]
  129. Swan A, Schüpbach T. 2007. The Cdc20 (Fzy)/Cdh1-related protein, Cort, cooperates with Fzy in cyclin destruction and anaphase progression in meiosis I and II in Drosophila. Development 134:891–99 [Google Scholar]
  130. Swanger SA, He YA, Richter JD, Bassell GJ. 2013. Dendritic GluN2A synthesis mediates activity-induced NMDA receptor insertion. J. Neurosci. 33:8898–908 [Google Scholar]
  131. Tam WL, Weinberg RA. 2013. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nat. Med. 19:1438–49 [Google Scholar]
  132. Tan L, Chang JS, Costa A, Schedl P. 2001. An autoregulatory feedback loop directs the localized expression of the Drosophila CPEB protein Orb in the developing oocyte. Development 128:1159–69 [Google Scholar]
  133. Tay J, Hodgman R, Sarkissian M, Richter JD. 2003. Regulated CPEB phosphorylation during meiotic progression suggests a mechanism for temporal control of maternal mRNA translation. Genes Dev. 17:1457–62 [Google Scholar]
  134. Tay J, Richter JD. 2001. Germ cell differentiation and synaptonemal complex formation are disrupted in CPEB knockout mice. Dev. Cell 1:201–13 [Google Scholar]
  135. Thompson BE, Bernstein DE, Bachorik JL, Petcherski AG, Wickens M, Kimble J. 2005. Dose-dependent control of proliferation and sperm specification by FOG-1/CPEB. Development 132:3471–81 [Google Scholar]
  136. Tsai LY, Chang YW, Lin PY, Chou HJ, Liu TJ. et al. 2013. CPEB4 knockout mice exhibit normal hippocampus-related synaptic plasticity and memory. PLOS ONE 8:12e84978 [Google Scholar]
  137. Udagawa T, Farny NG, Jakovcevski M, Kaphzan H, Alarcon JM. et al. 2013. Genetic and acute CPEB1 depletion ameliorate fragile X pathophysiology. Nat. Med. 19:1473–77 [Google Scholar]
  138. Udagawa T, Swanger SA, Takeuchi K, Kim JH, Nalavadi V. et al. 2012. Bidirectional control of mRNA translation and synaptic plasticity by the cytoplasmic polyadenylation complex. Mol. Cell 47:253–66 [Google Scholar]
  139. Wang L, Eckmann CR, Kadyk LC, Wickens M, Kimble J. 2002. A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans. Nature 419:312–16 [Google Scholar]
  140. Wong LC, Schedl P. 2011. Cup blocks the precocious activation of the orb autoregulatory loop. PLOS ONE 6:12e28261 [Google Scholar]
  141. Wright JE, Gaidatzis D, Senften M, Farley BM, Westhof E. et al. 2011. A quantitative RNA code for mRNA target selection by the germline fate determinant GLD-1. EMBO J. 30:533–45 [Google Scholar]
  142. Wu L, Wells D, Tay J, Mendis D, Abbott MA. et al. 1998. CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of α-CaMKII at synapses. Neuron 21:1129–39 [Google Scholar]
  143. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA. et al. 2004. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117:927–39 [Google Scholar]
  144. Yochem J, Greenwald I. 1989. glp-1 and lin-12, genes implicated in distinct cell-cell interactions in C. elegans, encode similar transmembrane proteins. Cell 58:553–63 [Google Scholar]
  145. Zearfoss NR, Alarcon JM, Trifilieff P, Kandel E, Richter JD. 2008. A molecular circuit composed of CPEB-1 and c-Jun controls growth hormone-mediated synaptic plasticity in the mouse hippocampus. J. Neurosci. 28:8502–9 [Google Scholar]
  146. Zhang B, Gallegos M, Puoti A, Durkin E, Fields S. et al. 1997. A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line. Nature 390:477–84 [Google Scholar]
/content/journals/10.1146/annurev-cellbio-101011-155831
Loading
/content/journals/10.1146/annurev-cellbio-101011-155831
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error