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Molecular Neurobiology

, Volume 25, Issue 2, pp 149–165 | Cite as

Candidate RNA-binding proteins regulating extrasomatic mRNA targeting and translation in mammalian neurons

  • Stefan KindlerEmail author
  • Michaela Monshausen
Article

Abstract

In mammalian neurons, long-lasting changes in the efficacy of individual synapses depend on the synthesis of new proteins. To maintain specificity, neuronal cells have to ensure that these newly synthesized proteins accumulate at the appropriate subpopulation of synapses. One way that neurons have solved this challenge appears to be the local translation of extrasomatic mRNAs in dendrites and at postsynaptic sites. Mechanisms, which regulate the targeting, translation, and stability of dendritic mRNAs, involve an organized interaction between cis-acting elements of localized transcripts and trans-acting RNA-binding proteins. The molecular identity and cellular functions of trans-acting factors that are likely to play an important role in post-transcriptional processing of extrasomatic transcripts in mammalian neurons are now being elucidated.

Index Entries

Dendritic RNA sorting extrasomatic translation ribonucleoprotein particle trans-acting factor synaptic activity 

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References

  1. 1.
    Frey U. and Morris R. G. (1998) Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci. 21, 181–188.PubMedGoogle Scholar
  2. 2.
    Abbott L. F. and Nelson S. B. (2000) Synaptic plasticity: taming the beast. Nat. Neurosci. 3(Suppl), 1178–1183.PubMedGoogle Scholar
  3. 3.
    Martin S. J., Grimwood P. D., and Morris R. G. (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci. 23, 649–711.PubMedGoogle Scholar
  4. 4.
    Schuman E. M. (1999) mRNA trafficking and local protein synthesis at the synapse. Neuron 23, 645–648.PubMedGoogle Scholar
  5. 5.
    Luscher C., Nicoll R. A., Malenka R. C., and Muller D. (2000) Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat. Neurosci. 3, 545–550.PubMedGoogle Scholar
  6. 6.
    Wells D. G., Richter J. D., and Fallon J. R. (2000) Molecular mechanisms for activity-regulated protein synthesis in the synapto-dendritic compartment. Curr. Opin. Neurobiol. 10, 132–137.PubMedGoogle Scholar
  7. 7.
    Steward O. and Schuman E. M. (2001) Protein synthesis at synaptic sites on dendrites. Annu. Rev. Neurosci. 24, 299–325.PubMedGoogle Scholar
  8. 8.
    Tiedge H., Bloom F. E., and Richter D. (2001) Molecular kinesis in cellular function and plasticity. Proc. Natl. Acad. Sci. USA 98, 6997–6998.PubMedGoogle Scholar
  9. 9.
    Steward O. and Levy W. B. (1982) Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J. Neurosci. 2, 284–291.PubMedGoogle Scholar
  10. 10.
    Steward O. and Reeves T. M. (1988) Proteinsynthetic machinery beneath postynaptic sites on CNS neurons: association between polyribosomes and other organelles at the synaptic site. J. Neurosci. 8, 176–184.PubMedGoogle Scholar
  11. 11.
    Torre E. R. and Steward O. (1992) Demonstration of local protein synthesis within dendrites using a new cell culture system that permits the isolation of living axons and dendrites from their cell bodies. J. Neurosci. 12, 762–772.PubMedGoogle Scholar
  12. 12.
    Crino P. B. and Eberwine J. (1996) Molecular characterization of the dendritic growth cone: regulated mRNA transport and local protein synthesis. Neuron 17, 1173–1187.PubMedGoogle Scholar
  13. 13.
    Kacharmina J. E., Job C., Crino P., and Eberwine J. (2000) Stimulation of glutamate receptor protein synthesis and membrane insertion within isolated neuronal dendrites. Proc. Natl. Acad. Sci. USA 97, 11,545–11,550.Google Scholar
  14. 14.
    Aakalu G., Smith W. B., Nguyen N., Jiang C., and Schuman E. M. (2001) Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30, 489–502.PubMedGoogle Scholar
  15. 15.
    Kiebler M. A. and DesGroseillers L. (2000) Molecular insights into mRNA transport and local translation in the mammalian nervous system. Neuron 25, 19–28.PubMedGoogle Scholar
  16. 16.
    Burgin K. E., Waxham M. N., Rickling S., Westgate S. A., Mobley W. C., and Kelly P. T. (1990) In situ hybridization histochemistry of Ca2+/calmodulin-dependent protein kinase in developing rat brain. J. Neurosci. 10, 1788–1798.PubMedGoogle Scholar
  17. 17.
    Garner C. C., Tucker R. B., and Matus A. (1988) Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites. Nature 336, 674–677.PubMedGoogle Scholar
  18. 18.
    Bruckenstein D. A., Lein P. J., Higgins D., and Fremeau R. T., Jr. (1990) Distinct spatial localization of specific mRNAs in cultured sympathetic neurons. Neuron 5, 809–819.PubMedGoogle Scholar
  19. 19.
    Kleiman R., Banker G., and Steward O. (1990) Differential subcellular localization of particular mRNAs in hippocampal neurons in culture. Neuron 5, 821–830.PubMedGoogle Scholar
  20. 20.
    Link W., Konietzko U., Kauselmann G., Krug M., Schwanke B., Frey U., and Kuhl D. (1995) Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc. Natl. Acad. Sci. USA 92, 5734–5738.PubMedGoogle Scholar
  21. 21.
    Lyford G. L., Yamagata K., Kaufmann W. E., Barnes C. A., Sanders L. K., Copeland N. G., et al. (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14, 433–445.PubMedGoogle Scholar
  22. 22.
    Herb A., Wisden W., Catania M., Marechal D., Dresse A., and Seeburg P. (1997) Prominent dendritic localization in forebrain neurons of a novel mRNA and its product, dendrin. Mol. Cell. Neurosci. 8, 367–374.PubMedGoogle Scholar
  23. 23.
    Mohr E., Morris J. F., and Richter D. (1995) Differential subcellular mRNA targeting: deletion of a single nucleotide prevents the transport to axons but not to dendrites of rat hypothalamic magnocellular neurons. Proc. Natl. Acad. Sci. USA 92, 4377–4381.PubMedGoogle Scholar
  24. 24.
    Severt W. L., Biber T. U., Wu X., Hecht N. B., DeLorenzo R. J., and Jakoi E. R. (1999) The suppression of testis-brain RNA binding protein and kinesin heavy chain disrupts mRNA sorting in dendrites. J. Cell Sci. 112, 3691–3702.PubMedGoogle Scholar
  25. 25.
    Jansen R. P. (2001) mRNA localization: message on the move. Nat. Rev. Mol. Cell Biol. 2, 247–256.PubMedGoogle Scholar
  26. 26.
    Blichenberg A., Schwanke B., Rehbein M., Garner C. C., Richter D., and Kindler S. (1999) Identification of a cis-acting dendritic targeting element in MAP2 mRNAs. J. Neurosci. 19, 8818–8829.PubMedGoogle Scholar
  27. 27.
    Wu L., Wells D., Tay J., Mendis D., Abbott M. A., Barnitt A., et al. (1998) CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of alpha-CaMKII mRNA at synapses. Neuron 21, 1129–1139.PubMedGoogle Scholar
  28. 28.
    Mori Y., Imaizumi K., Katayama T., Yoneda T., and Tohyama M. (2000) Two cis-acting elements in the 3′ untranslated region of alpha-CaMKII regulate its dendritic targeting. Nat. Neurosci. 3, 1079–1084.PubMedGoogle Scholar
  29. 29.
    Blichenberg A., Rehbein M., Muller R., Garner C. C., Richter D., and Kindler S. (2001) Identification of a cis-acting dendritic targeting element in the mRNA encoding the alpha subunit of Ca2+/calmodulin-dependent protein kinase II. Eur. J. Neurosci. 13, 1881–1888.PubMedGoogle Scholar
  30. 30.
    Prakash N., Fehr S., Mohr E., and Richter D. (1997) Dendritic localization of rat vasopressin mRNA: ultrastructural analysis and mapping of targeting elements. Eur. J. Neurosci. 9, 523–532.PubMedGoogle Scholar
  31. 31.
    Schüpbach T. and Wieschaus E. (1986) Germline autonomy of maternal-effect mutations altering the embryonic body pattern of Drosophila. Dev. Biol. 113, 443–448.PubMedGoogle Scholar
  32. 32.
    Winslow G. M., Carroll S. B., and Scott M. P. (1988) Maternal-effect genes that alter the fate map of the Drosophila blastoderm embryo. Dev. Biol. 129, 72–83.PubMedGoogle Scholar
  33. 33.
    St Johnston D., Beuchle D., and Nusslein-Volhard C. (1991) Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66, 51–63.PubMedGoogle Scholar
  34. 34.
    Micklem D. R., Adams J., Grunert S., and St. Johnston D. (2000) Distinct roles of two conserved Staufen domains in oskar mRNA localization and translation. EMBO J. 19, 1366–1377.PubMedGoogle Scholar
  35. 35.
    Campos-Ortega J. A. (1997) Asymmetric division: dynastic intricacies of neuroblast division. Curr. Biol. 7, R726–728.PubMedGoogle Scholar
  36. 36.
    Li P., Yang X., Wasser M., Cai Y., and Chia W. (1997) Inscuteable and Staufen mediate asymmetric localization and segregation of prospero RNA during Drosophila neuroblast cell divisions. Cell 90, 437–447.PubMedGoogle Scholar
  37. 37.
    Broadus J., Fuerstenberg S., and Doe C. Q. (1998) Staufen-dependent localization of prospero mRNA contributes to neuroblast daughter-cell fate. Nature 391, 792–795.PubMedGoogle Scholar
  38. 38.
    St Johnston D., Brown N. H., Gall J. G., and Jantsch M. (1992) A conserved double-stranded RNA-binding domain. Proc. Natl. Acad. Sci. USA 89, 10,979–10,983.Google Scholar
  39. 39.
    Ramos A., Grunert S., Adams J., Micklem D. R., Proctor M. R., Freund S., et al. (2000) RNA recognition by a Staufen double-stranded RNA-binding domain. EMBO J. 19, 997–1009.PubMedGoogle Scholar
  40. 40.
    Schuldt A. J., Adams J. H., Davidson C. M., Micklem D. R., Haseloff J., St. Johnston D., and Brand A. H. (1998) Miranda mediates asymmetric protein and RNA localization in the developing nervous system. Genes Dev. 12, 1847–1857.PubMedGoogle Scholar
  41. 41.
    Kiebler M. A., Hemraj I., Verkade P., Kohrmann M., Fortes P., Marion R. M., et al. (1999) The mammalian staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons: implications for its involvement in mRNA transport. J. Neurosci. 19, 288–297.PubMedGoogle Scholar
  42. 42.
    Marion R. M., Fortes P., Beloso A., Dotti C., and Ortin J. (1999) A human sequence homologue of Staufen is an RNA-binding protein that is associated with polysomes and localizes to the rough endoplasmic reticulum. Mol. Cell. Biol. 19, 2212–2219.PubMedGoogle Scholar
  43. 43.
    Wickham L., Duchaine T., Luo M., Nabi I. R., and DesGroseillers L. (1999) Mammalian Staufen is a double-stranded-RNA- and tubulin-binding protein which localizes to the rough endoplasmic reticulum. Mol. Cell. Biol. 19, 2220–2230.PubMedGoogle Scholar
  44. 44.
    Monshausen M., Putz U., Rehbein M., Schweizer M., DesGroseillers L., Kuhl D., Richter D., and Kindler S. (2001) Two rat brain Staufen isoforms differentially bind RNA. J. Neurochem. 76, 155–165.PubMedGoogle Scholar
  45. 45.
    Duchaine T., Wang H. J., Luo M., Steinberg S. V., Nabi I. R., and DesGroseillers L. (2000) A novel murine Staufen isoform modulates the RNA content of Staufen complexes. Mol. Cell. Biol. 20, 5592–5601.PubMedGoogle Scholar
  46. 46.
    Köhrmann M., Luo M., Kaether C., DesGroseillers L., Dotti C. G., and Kiebler M. A. (1999) Microtubule-dependent recruitment of staufen-green fluorescent protein into large RNA-containing granules and subsequent dendritic transport in living hippocampal neurons. Mol. Biol. Cell 10, 2945–2953.PubMedGoogle Scholar
  47. 47.
    Knowles R. B., Sabry J. H., Martone M. E., Deerinck T. J., Ellisman M. H., Bassell G. J., and Kosik K. S. (1996) Translocation of RNA granules in living neurons. J. Neurosci. 16, 7812–7820.PubMedGoogle Scholar
  48. 48.
    Oliver G., Sosa-Pineda B., Geisendorf S., Spana E. P., Doe C. Q., and Gruss P. (1993) Prox 1, a prospero-related homeobox gene expressed during mouse development. Mech. Dev. 44, 3–16.PubMedGoogle Scholar
  49. 49.
    Jin P. and Warren S. T. (2000) Understanding the molecular basis of fragile X syndrome. Hum. Mol. Genet. 9, 901–908.PubMedGoogle Scholar
  50. 50.
    Hinds H. L., Ashley C. T., Sutcliffe J. S., Nelson D. L., Warren S. T., Housman D. E., and Schalling M. (1993) Tissue specific expression of FMR-1 provides evidence for a functional role in fragile X syndrome. Nat. Genet. 3, 36–43.PubMedGoogle Scholar
  51. 51.
    Ashley C. T., Jr., Wilkinson K. D., Reines D., and Warren S. T. (1993) FMR1 protein: conserved RNP family domains and selective RNA binding. Science 262, 563–566.PubMedGoogle Scholar
  52. 52.
    Siomi H., Siomi M. C., Nussbaum R. L., and Dreyfuss G. (1993) The protein product of the fragile X gene, FMR1, has characteristics of an RNA-binding protein. Cell 74, 291–298.PubMedGoogle Scholar
  53. 53.
    De Boulle K., Verkerk A. J., Reyniers E., Vits L., Hendrickx J., Van Roy B., Van den Bos F., et al. (1993) A point mutation in the FMR-1 gene associated with fragile X mental retardation. Nat. Genet. 3, 31–35.PubMedGoogle Scholar
  54. 54.
    Siomi M. C., Siomi H., Sauer W. H., Srinivasan S., Nussbaum R. L., and Dreyfuss G. (1995) FXR1, an autosomal homolog of the fragile X mental retardation gene. EMBO J. 14, 2401–2408.PubMedGoogle Scholar
  55. 55.
    Zhang Y., O’Connor J. P., Siomi M. C., Srinivasan S., Dutra A., Nussbaum R. L., and Dreyfuss G. (1995) The fragile X mental retardation syndrome protein interacts with novel homologs FXR1 and FXR2. EMBO J. 14, 5358–5366.PubMedGoogle Scholar
  56. 56.
    Hoogeveen A. T. and Oostra B. A. (1997) The fragile X syndrome. J. Inherit. Metab. Dis. 20, 139–151.PubMedGoogle Scholar
  57. 57.
    Brown V., Small K., Lakkis L., Feng Y., Gunter C., Wilkinson K. D., and Warren S. T. (1998) Purified recombinant Fmrp exhibits selective RNA binding as an intrinsic property of the fragile X mental retardation protein. J. Biol. Chem. 273, 15521–15527.PubMedGoogle Scholar
  58. 58.
    Adinolfi S., Bagni C., Musco G., Gibson T., Mazzarella L., and Pastore A. (1999) Dissecting FMR1, the protein responsible for fragile X syndrome, in its structural and functional domains. RNA 5, 1248–1258.PubMedGoogle Scholar
  59. 59.
    Tamanini F., Meijer N., Verheij C., Willems P.J., Galjaard H., Oostra B. A., and Hoogeveen A. T. (1996) FMRP is associated to the ribosomes via RNA. Hum. Mol. Genet. 5, 809–813.PubMedGoogle Scholar
  60. 60.
    Corbin F., Bouillon M., Fortin A., Morin S., Rousseau F., and Khandjian E. W. (1997) The fragile X mental retardation protein is associated with poly(A)+mRNA in actively translating polyribosomes. Hum. Mol. Genet. 6, 1465–1472.PubMedGoogle Scholar
  61. 61.
    Eberhart D. E., Malter H. E., Feng Y., and Warren S. T. (1996) The fragile X mental retardaprotein protein is a ribonucleoprotein containing both nuclear localization and nuclear export signals. Hum. Mol. Genet. 5, 1083–1091.PubMedGoogle Scholar
  62. 62.
    Feng Y., Absher D., Eberhart D. E., Brown V., Malter H. E., and Warren S. T. (1997) FMRP associates with polyribosomes as an mRNP, and the 1304N mutation of severe fragile X syndrome abolishes this association. Mol. Cell 1, 109–118.PubMedGoogle Scholar
  63. 63.
    Laggerbauer B., Ostareck D., Keidel E., Ostareck-Lederer A., and Fischer U. (2001) Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum. Mol. Genet. 10, 329–338.PubMedGoogle Scholar
  64. 64.
    Bardoni B., Schenck A., and Mandel J. L. (1999) A novel RNA-binding nuclear protein that interacts with the fragile X mental retardation (FMR1) protein. Hum. Mol. Genet. 8, 2557–2566.PubMedGoogle Scholar
  65. 65.
    Ceman S., Brown V., and Warren S. T. (1999) Isolation of an FMRP-associated messenger ribonucleoprotein particle and identification of nucleolin and the fragile X-related proteins as components of the complex. Mol. Cell. Biol. 19, 7925–7932.PubMedGoogle Scholar
  66. 66.
    Li Z., Zhang Y., Ku L., Wilkinson K. D., Warren S. T., and Feng Y. (2001) The fragile X mental retardation protein inhibits translation via interacting with mRNA. Nucleic Acids Res. 29, 2276–2283.PubMedGoogle Scholar
  67. 67.
    Feng Y., Gutekunst C. A., Eberhart D. E., Yi H., Warren S. T., and Hersch S. M. (1997) Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J. Neurosci. 17, 1539–1547.PubMedGoogle Scholar
  68. 68.
    Weiler I. J., Irwin S. A., Klintsova A. Y., Spencer C. M., Brazelton A. D., Miyashiro K., et al. (1997) Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proc. Natl. Acad. Sci. USA 94, 5395–5400.PubMedGoogle Scholar
  69. 69.
    DiMarco S., Ceman S., Torre E., and Warren S. (1999) FMRP is a phosphoprotein and a substrate of the Fes non-receptor typrosine kinase. Am. J. Hum. Genet. 65 (suppl.), A269.Google Scholar
  70. 70.
    Tamanini F., Bontekoe C., Bakker C. E., van Unen L., Anar B., Willemsen R., et al. (1999) Different targets for the fragile X-related proteins revealed by their distinct nuclear localizations. Hum. Mol. Genet. 8, 863–869.PubMedGoogle Scholar
  71. 71.
    Hinton V. J., Brown W. T., Wisniewski K., and Rudelli R. D. (1991) Analysis of neocortex in three males with the fragile X syndrome. Am. J. Med. Genet. 41, 289–294.PubMedGoogle Scholar
  72. 72.
    Comery T. A., Harris J. B., Willems P. J., Oostra B. A., Irwin S. A., Weiler I. J., and Greenough W. T. (1997) Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc. Natl. Acad. Sci. USA 94, 5401–5404.PubMedGoogle Scholar
  73. 73.
    Steward O., Bakker C. E., Willems P. J., and Oostra B. A. (1998) No evidence for disruption of normal patterns of mRNA localization in dendrites or dendritic transport of recently synthesized mRNA in FMR1 knockout mice, a model for human fragile-X mental retardation syndrome. Neuroreport 9, 477–481.PubMedGoogle Scholar
  74. 74.
    Campos A. R., Grossman D., and White K. (1985) Mutant alleles at the locus elav in Drosophila melanogaster lead to nervous system defects. A developmental-genetic analysis. J. Neurogenet. 2, 197–218.PubMedGoogle Scholar
  75. 75.
    Robinow S. and White K. (1991) Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J. Neurobiol. 22, 443–461.PubMedGoogle Scholar
  76. 76.
    Keene J. D. (1999) Why is Hu where? Shuttling of early-response-gene messenger RNA subsets. Proc. Natl. Acad. Sci. USA 96, 5–7.PubMedGoogle Scholar
  77. 77.
    Brennan C. M. and Steitz J. A. (2001) HuR and mRNA stability. Cell Mol. Life Sci. 58, 266–277.PubMedGoogle Scholar
  78. 78.
    Keene J. D. (2001) Ribonucleoprotein infrastructure regulating the flow of genetic information between the genome and the proteome. Proc. Natl. Acad. Sci. USA 98, 7018–7024.PubMedGoogle Scholar
  79. 79.
    Burd C. G. and Dreyfuss G. (1994) Conserved structures and diversity of functions of RNA-binding proteins. Science 265, 615–621.PubMedGoogle Scholar
  80. 80.
    Chung S., Eckrich M., Perrone-Bizzozero N., Kohn D. T., and Furneaux H. (1997) The Elavlike proteins bind to a conserved regulatory element in the 3′-untranslated region of GAP-43 mRNA. J. Biol. Chem. 272, 6593–6598.PubMedGoogle Scholar
  81. 81.
    Gao F. B. and Keene J. D. (1996) Hel-N1/Hel-N2 proteins are bound to poly(A)+mRNA in granular RNP structures and are implicated in neuronal differentiation. J. Cell Sci. 109, 579–589.PubMedGoogle Scholar
  82. 82.
    Antic D. and Keene J. D. (1998) Messenger ribonucleoprotein complexes containing human ELAV proteins: interactions with cytoskeleton and translation apparatus. J. Cell Sci. 111, 183–197.PubMedGoogle Scholar
  83. 83.
    Fan X. C. and Steitz J. A. (1998) HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc. Natl. Acad. Sci. USA 95, 15293–15298.PubMedGoogle Scholar
  84. 84.
    Fan X. C. and Steitz J. A. (1998) Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17, 3448–3460.PubMedGoogle Scholar
  85. 85.
    Aranda-Abreu G. E., Behar L., Chung S., Furneaux H., and Ginzburg I. (1999) Embryonic lethal abnormal vision-like RNA-binding proteins regulate neurite outgrowth and tau expression in PC12 cells. J. Neurosci. 19, 6907–6917.PubMedGoogle Scholar
  86. 86.
    Landry C. F., Watson J. B., Kashima T., and Campagnoni A. T. (1994) Cellular influences on RNA sorting in neurons and glia: an in situ hybridization histochemical study. Brain Res. Mol. Brain Res. 27, 1–11.PubMedGoogle Scholar
  87. 87.
    Litman P., Barg J., Rindzoonski L., and Ginzburg I. (1993) Subcellular localization of tau mRNA in differentiating neuronal cell culture: implications for neuronal polarity. Neuron 10, 627–638.PubMedGoogle Scholar
  88. 88.
    Aarts L. H., Schotman P., Verhaagen J., Schrama L. H., and Gispen W. H. (1998) The role of the neural growth associated protein B-50/GAP-43 in morphogenesis. Adv. Exp. Med. Biol. 446, 85–106.PubMedGoogle Scholar
  89. 89.
    Antic D., Lu N., and Keene J. D. (1999) ELAV tumor antigen, Hel-N1, increases translation of neurofilament M mRNA and induces formation of neurites in human teratocarcinoma cells. Genes Dev. 13, 449–461.PubMedGoogle Scholar
  90. 90.
    Lenz S. E., Henschel Y., Zopf D., Voss B., and Gundelfinger E. D. (1992) VILIP, a cognate protein of the retinal calcium binding proteins visinin and recoverin, is expressed in the developing chicken brain. Brain Res. Mol. Brain Res. 15, 133–140.PubMedGoogle Scholar
  91. 91.
    Lenz S. E., Jiang S., Braun K., and Gundelfinger E. D. (1996) Localization of the neural calcium-binding protein VILIP (visinin-like protein) in neurons of the chick visual system and cerebellum. Cell Tissue Res. 283, 413–424.PubMedGoogle Scholar
  92. 92.
    Lenz S. E., Zuschratter W., and Gundelfinger E. D. (1996) Distribution of visinin-like protein (VILIP) immunoreactivity in the hippocampus of the Monogolian gerbil (Meriones unguiculatus). Neurosci. Lett. 206, 133–136.PubMedGoogle Scholar
  93. 93.
    Bernstein H. G., Baumann B., Danos P., Diekmann S., Bogerts B., Gundelfinger E. D., and Braunewell K. H. (1999) Regional and cellular distribution of neural visinin-like protein immunoreactivities (VILIP-1 and VILIP-3) in human brain. J. Neurocytol. 28, 655–662.PubMedGoogle Scholar
  94. 94.
    Braunewell K. H. and Gundelfinger E. D. (1997) Low level expression of calcium-sensor protein VILIP induces cAMP-dependent differentiation in rat C6 glioma cells. Neurosci. Lett. 234, 139–142.PubMedGoogle Scholar
  95. 95.
    Braunewell K. H., Spilker C., Behnisch T., and Gundelfinger E. D. (1997) The neuronal calcium-sensor protein VILIP modulates cyclic AMP accumulation in stably transfected C6 glioma cells: amino-terminal myristoylation determines functional activity. J. Neurochem. 68, 2129–2139.PubMedGoogle Scholar
  96. 96.
    Mathisen P. M., Johnson J. M., Kawczak J. A., and Tuohy V. K. (1999) Visinin-like protein (VILIP) is a neuron-specific calcium-dependent double-stranded RNA-binding protein. J. Biol. Chem. 274, 31,571–31,576.Google Scholar
  97. 97.
    Tongiorgi E., Righi M., and Cattaneo A. (1997) Activity-dependent dendritic targeting of BDNF and TrkB mRNAs in hippocampal neurons. J. Neurosci. 17, 9492–9505.PubMedGoogle Scholar
  98. 98.
    Lenz S. E., Braunewell K. H., Weise C., Nedlina-Chittka A., and Gundelfinger E. D. (1996) The neuronal EF-hand Ca(2+)-binding protein VILIP: interaction with cell membrane and actin-based cytoskeleton. Biochem. Biophys. Res. Commun. 225, 1078–1083.PubMedGoogle Scholar
  99. 99.
    Kislauskis E. H., Zhu X., and Singer R. H. (1994) Sequences responsible for intracellular localization of beta-actin messenger RNA also affect cell phenotype. J. Cell Biol. 127, 441–451.PubMedGoogle Scholar
  100. 100.
    Ross A. F., Oleynikov Y., Kislauskis E. H., Taneja K. L., and Singer R. H. (1997) Characterization of a beta-actin mRNA zipcode-binding protein. Mol. Cell. Biol. 17, 2158–2165.PubMedGoogle Scholar
  101. 101.
    Nielsen J., Christiansen J., Lykke-Andersen J., Johnsen A. H., Wewer U. M., and Nielsen F. C. (1999) A family of insulin-like growth factor II mRNA-binding proteins represses translation in late development. Mol. Cell. Biol. 19, 1262–1270.PubMedGoogle Scholar
  102. 102.
    Deshler J. O., Highett M. I., and Schnapp B. J. (1997) Localization of Xenopus Vg1 mRNA by Vera protein and the endoplasmic reticulum. Science 276, 1128–1131.PubMedGoogle Scholar
  103. 103.
    Havin L., Git A., Elisha Z., Oberman F., Yaniv K., Schwartz S. P., et al. (1998) RNA-binding protein conserved in both microtubule-and microfilament- based RNA localization. Genes Dev. 12, 1593–1598.PubMedGoogle Scholar
  104. 104.
    Bernstein P. L., Herrick D. J., Prokipcak R. D., and Ross J. (1992) Control of c-myc mRNA half-life in vitro by a protein capable of binding to a coding region stability determinant. Genes Dev. 6, 642–654.PubMedGoogle Scholar
  105. 105.
    Doyle G. A., Betz N. A., Leeds P. F., Fleisig A. J., Prokipcak R. D., and Ross J. (1998) The c-myc coding region determinant-binding protein: a member of a family of KH domain RNA-binding proteins. Nucleic Acids Res. 26, 5036–5044.PubMedGoogle Scholar
  106. 106.
    Bassell G. J., Zhang H., Byrd A. L., Femino A. M., Singer R. H., Taneja K. L., et al. (1998) Sorting of beta-actin mRNA and protein to neurites and growth cones in culture. J. Neurosci. 18, 251–265.PubMedGoogle Scholar
  107. 107.
    Zhang H. L., Singer R. H., and Bassell G. J. (1999) Neurotrophin regulation of beta-actin mRNA and protein localization within growth cones. J. Cell Biol. 147, 59–70.PubMedGoogle Scholar
  108. 108.
    Aoki K., Suzuki K., Sugano T., Tasaka T., Nakahara K., Kuge O., et al. (1995) A novel gene, Translin, encodes a recombination hotspot binding protein associated with chromosomal translocations. Nat. Genet. 10, 167–174.PubMedGoogle Scholar
  109. 109.
    Kwon Y. K. and Hecht N. B. (1991) Cytoplasmic protein binding to highly conserved sequences in the 3′ untranslated region of mouse protamine 2 mRNA, a translationally regulated transcript of male germ cells. Proc. Natl. Acad. Sci. USA 88, 3584–3588.PubMedGoogle Scholar
  110. 110.
    Kwon Y. K. and Hecht N. B. (1993) Binding of a phosphoprotein to the 3′ untranslated region of the mouse protamine 2 mRNA temporally represses its translation. Mol. Cell. Biol. 13, 6547–6557.PubMedGoogle Scholar
  111. 111.
    Wu X. Q., Gu W., Meng X., and Hecht N. B. (1997) The RNA-binding protein, TB-RBP, is the mouse homologue of translin, a recombination protein associated with chromosomal translocations. Proc. Natl. Acad. Sci. USA 94, 5640–5645.PubMedGoogle Scholar
  112. 112.
    Wu X. Q., Xu L., and Hecht N. B. (1998) Dimerization of the testis brain RNA-binding protein (translin) is mediated through its C-terminus and is required for DNA- and RNA-binding. Nucleic Acids Res. 26, 1675–1680.PubMedGoogle Scholar
  113. 113.
    Aoki K., Suzuki K., Ishida R., and Kasai M. (1999) The DNA binding activity of Translin is mediated by a basic region in the ring-shaped structure conserved in evolution. FEBS Lett. 443, 363–366.PubMedGoogle Scholar
  114. 114.
    Chennathukuzhi V. M., Kurihara Y., Bray J. D., and Hecht N. B. (2001) Trax (translin-associated factor x), a primarily cytoplasmic protein, inhibits the binding of tb-rbp (translin) to RNA. J. Biol. Chem. 276, 13256–13263.PubMedGoogle Scholar
  115. 115.
    Finkenstadt P. M., Kang W. S., Jeon M., Taira E., Tang W., and Baraban J. M. (2000) Somatodendritic localization of Translin, a component of the Translin/Trax RNA binding complex. J. Neurochem. 75, 1754–1762.PubMedGoogle Scholar
  116. 116.
    Han J. R., Yiu G. K., and Hecht N. B. (1995) Testis/brain RNA-binding protein attaches translationally repressed and transported mRNAs to microtubules. Proc. Natl. Acad. Sci. USA 92, 9550–9554.PubMedGoogle Scholar
  117. 117.
    Wu X. Q. and Hecht N. B. (2000) Mouse testis brain ribonucleic acid-binding protein/translin colocalizes with microtubules and is immunoprecipitated with messenger ribonucleic acids encoding myelin basic protein, alpha calmodulin kinase II, and protamines 1 and 2. Biol. Reprod. 62, 720–725.PubMedGoogle Scholar
  118. 118.
    Kobayashi S., Takashima A., and Anzai K. (1998) The dendritic translocation of translin protein in the form of BC1 RNA protein particles in developing rat hippocampal neurons in primary culture. Biochem. Biophys. Res. Commun. 253, 448–453.PubMedGoogle Scholar
  119. 119.
    Wu X. Q., Petrusz P., and Hecht N. B. (1999) Testis-brain RNA-binding protein (Translin) is primarily expressed in neurons of the mouse brain. Brain Res. 819, 174–178.PubMedGoogle Scholar
  120. 120.
    Morales C. R., Wu X. Q., and Hecht N. B. (1998) The DNA/RNA-binding protein, TB-RBP, moves from the nucleus to the cytoplasm and through intercellular bridges in male germ cells. Dev. Biol. 201, 113–123.PubMedGoogle Scholar
  121. 121.
    Castro A., Peter M., Magnaghi-Jaulin L., Vigneron S., Loyaux D., Lorca T., and Labbe J. C. (2000) Part of Xenopus translin is localized in the centrosomes during mitosis. Biochem. Biophys. Res. Commun. 276, 515–523.PubMedGoogle Scholar
  122. 122.
    Tiedge H., Fremeau R. T., Jr., Weinstock P. H., Arancio O., and Brosius J. (1991) Dendritic location of neural BC1 RNA. Proc. Natl. Acad. Sci. USA 88, 2093–2097.PubMedGoogle Scholar
  123. 123.
    Muramatsu T., Ohmae A., and Anzai K. (1998) BC1 RNA protein particles in mouse brain contain two y-,h-element-binding proteins, translin and a 37 kDa protein. Biochem. Biophys. Res. Commun. 247, 7–11.PubMedGoogle Scholar
  124. 124.
    Mendez R. and Richter J. D. (2001) Translational control by cpeb: a means to the end. Nat. Rev. Mol. Cell Biol. 2, 521–529.PubMedGoogle Scholar
  125. 125.
    Richter J. D. (2001) Think globally, translate locally: what mitotic spindles and neuronal synapses have in common. Proc. Natl. Acad. Sci. USA 98, 7069–7071.PubMedGoogle Scholar
  126. 126.
    Hake L. E., Mendez R., and Richter J. D. (1998) Specificity of RNA binding by CPEB: requirement for RNA recognition motifs and a novel zinc finger. Mol. Cell. Biol. 18, 685–693.PubMedGoogle Scholar
  127. 127.
    Gebauer F. and Richter J. D. (1995) Cloning and characterization of a Xenopus poly(A) polymerase. Mol. Cell. Biol. 15, 1422–1430.PubMedGoogle Scholar
  128. 128.
    Andresson T. and Ruderman J. V. (1998) The kinase Eg2 is a component of the Xenopus oocyte progesterone-activated signaling pathway. EMBO J. 17, 5627–5637.PubMedGoogle Scholar
  129. 129.
    Silva A. J., Paylor R., Wehner J. M., and Tonegawa S. (1992) Impaired spatial learning in alpha-calcium-calmodulin kinase II mutant mice. Science 257, 206–211.PubMedGoogle Scholar
  130. 130.
    Silva A. J., Stevens C. F., Tonegawa S., and Wang Y. (1992) Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science 257, 201–206.PubMedGoogle Scholar
  131. 131.
    Ouyang Y., Rosenstein A., Kreiman G., Schuman E. M., and Kennedy M. B. (1999) Tetanic stimulation leads to increased accumulation of Ca(2+)/calmodulin-dependent protein kinase II via dendritic protein synthesis in hippocampal neurons. J. Neurosci. 19, 7823–7833.PubMedGoogle Scholar
  132. 132.
    Scheetz A. J., Nairn A. C., and Constantine-Paton M. (2000) NMDA receptor-mediated control of protein synthesis at developing synapses. Nat. Neurosci. 3, 211–216.PubMedGoogle Scholar
  133. 133.
    Mohr E., Prakash N., Vieluf K., Fuhrmann C., Buck F., and Richter D. (2001) Vasopressin mRNA localization in nerve cells: characterization of cis-acting elements and trans-acting factors. Proc. Natl. Acad. Sci. USA 98, 7072–7079.PubMedGoogle Scholar
  134. 134.
    Görlach M., Burd C. G., and Dreyfuss G. (1994) The mRNA poly(A)-binding protein: localization, abundance, and RNA-binding specificity. Exp. Cell. Res. 211, 400–407.PubMedGoogle Scholar
  135. 135.
    Preiss T., Muckenthaler M., and Hentze M. W. (1998) Poly(A)-tail-promoted translation in yeast: implications for translational control. RNA 4, 1321–1331.PubMedGoogle Scholar
  136. 136.
    Coller J. M., Gray N. K., and Wickens M. P. (1998) mRNA stabilization by poly(A) binding protein is independent of poly(A) and requires translation. Genes Dev. 12, 3226–3235.PubMedGoogle Scholar
  137. 137.
    Shafit-Zagardo B. and Kalcheva N. (1998) Making sense of the multiple MAP-2 transcripts and their role in the neuron. Mol. Neurobiol. 16, 149–162.PubMedGoogle Scholar
  138. 138.
    Kindler S., Mohr E., Rehbein M., and Richter D. (2001) Extrasomatic targeting of MAP2, vasopressin and oxytocin mRNAs in mammalian neurons, in Results and Problems in Cell Differentiation: Cell Polarity and Subcellular RNA Localization (Richter D., ed.), Springer, Heidelberg, Germany, pp. 83–104.Google Scholar
  139. 139.
    Rehbein M., Kindler S., Horke S., and Richter D. (2000) Two trans-acting rat-brain proteins, MARTA1 and MARTA2, interact specifically with the dendritic targeting element in MAP2 mRNAs. Brain Res. Mol. Brain Res. 79, 192–201.PubMedGoogle Scholar
  140. 140.
    Mayford M., Baranes D., Podsypanina K., and Kandel E. R. (1996) The 3′-untranslated region of CaMKII alpha is a cis-acting signal for the localization and translation of mRNA in dendrites. Proc. Natl. Acad. Sci. USA 93, 13250–13255.PubMedGoogle Scholar

Copyright information

© Humana Press Inc 2002

Authors and Affiliations

  1. 1.Institute for Cell Biochemistry and Clinical Neurobiology, University Hospital EppendorfUniversity of HamburgHamburgGermany
  2. 2.Biology DepartmentMassachusetts Institute of TechnologyCambridge

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