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Erschienen in: The Cerebellum 3/2008

01.09.2008

3′UTR-Dependent Localization of a Purkinje Cell Messenger RNA in Dendrites

verfasst von: Rui Zhang, Xulun Zhang, Feng Bian, Xin-an Pu, Karl Schilling, John Oberdick

Erschienen in: The Cerebellum | Ausgabe 3/2008

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Abstract

Pcp2(L7) is a Purkinje cell-specific GoLoco domain protein that modulates activation of Gαi/o proteins by G protein-coupled receptors. A likely downstream effector of this pathway is the P-type Ca2+ channel, and thereby, the intrinsic electrophysiology of Purkinje cells could be modulated by Pcp2(L7). It has long been known that the Pcp2(L7) mRNA is abundantly localized in dendrites, suggesting the possibility of distal synthesis and local changes in levels of the protein. As a first step to uncover the trafficking and translational mechanisms for this mRNA, we have begun identifying the cis-acting sequences important for its localization in dendrites. Using expression of modified transgenes in vivo, we show that the 3′UTR, only 65 bases long, is necessary in this process.
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1
These results were reported in part at a meeting: Serinagaoglu, Y., Iscru, E.M., Tian, J., Bishop, G.A., Morgan, J.I., Zhu, M.X., Oberdick, J. Sensorimotor behavioral changes and alteration of Purkinje cell firing patterns in Pcp2(L7) null mutant mice. Program No. 986.2. 2005 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2005. Online.
 
Literatur
1.
Zurück zum Zitat Kang H, Schuman EM (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273:1402–1406PubMedCrossRef Kang H, Schuman EM (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273:1402–1406PubMedCrossRef
2.
Zurück zum Zitat Steward O, Wallace C, Lyford G, Worley P (1998) Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21:741–751PubMedCrossRef Steward O, Wallace C, Lyford G, Worley P (1998) Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21:741–751PubMedCrossRef
3.
Zurück zum Zitat Scheetz AJ, Nairn AC, Constantine-Paton M (2000) NMDA receptor-mediated control of protein synthesis at developing synapses. Nat Neurosci 3:211–217PubMedCrossRef Scheetz AJ, Nairn AC, Constantine-Paton M (2000) NMDA receptor-mediated control of protein synthesis at developing synapses. Nat Neurosci 3:211–217PubMedCrossRef
4.
Zurück zum Zitat Tiruchinapalli DM, Oleynikov Y, Kelic S, Shenoy SM, Hartley A, Stanton PK, Singer RH, Bassell GJ (2003) Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and beta-actin mRNA in dendrites and spines of hippocampal neurons. J Neurosci 23:3251–3261PubMed Tiruchinapalli DM, Oleynikov Y, Kelic S, Shenoy SM, Hartley A, Stanton PK, Singer RH, Bassell GJ (2003) Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and beta-actin mRNA in dendrites and spines of hippocampal neurons. J Neurosci 23:3251–3261PubMed
5.
Zurück zum Zitat Steward O, Schuman EM (2001) Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24:299–325PubMedCrossRef Steward O, Schuman EM (2001) Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24:299–325PubMedCrossRef
6.
Zurück zum Zitat Wells DG, Richter JD, Fallon JR (2000) Molecular mechanisms for activity-regulated protein synthesis in the synapto-dendritic compartment. Curr Opin Neurobiol 10:132–137PubMedCrossRef Wells DG, Richter JD, Fallon JR (2000) Molecular mechanisms for activity-regulated protein synthesis in the synapto-dendritic compartment. Curr Opin Neurobiol 10:132–137PubMedCrossRef
7.
Zurück zum Zitat Bian F, Chu T, Schilling K, Oberdick J (1996) Differential mRNA transport and the regulation of protein synthesis: selective sensitivity of Purkinje cell dendritic mRNAs to translational inhibition. Mol Cell Neurosci 7:116–133PubMedCrossRef Bian F, Chu T, Schilling K, Oberdick J (1996) Differential mRNA transport and the regulation of protein synthesis: selective sensitivity of Purkinje cell dendritic mRNAs to translational inhibition. Mol Cell Neurosci 7:116–133PubMedCrossRef
8.
Zurück zum Zitat Siderovski DP, Diversé-Pierlussi MA, De Vries L (1999) The GoLoco motif: a Galphai/o binding motif and potential guanine-nucleotide exchange factor. Trends Biochem Sci 24:340–341PubMedCrossRef Siderovski DP, Diversé-Pierlussi MA, De Vries L (1999) The GoLoco motif: a Galphai/o binding motif and potential guanine-nucleotide exchange factor. Trends Biochem Sci 24:340–341PubMedCrossRef
9.
Zurück zum Zitat Zhang X, Zhang H, Oberdick J (2002) Conservation of the developmentally regulated dendritic localization of a Purkinje cell-specific mRNA that encodes a G-protein modulator: comparison of rodent and human Pcp2(L7) gene structure and expression. Mol Brain Res 105:1–10PubMedCrossRef Zhang X, Zhang H, Oberdick J (2002) Conservation of the developmentally regulated dendritic localization of a Purkinje cell-specific mRNA that encodes a G-protein modulator: comparison of rodent and human Pcp2(L7) gene structure and expression. Mol Brain Res 105:1–10PubMedCrossRef
10.
Zurück zum Zitat Willard FS, McCudden CR, Siderovski DP (2006) G-protein alpha subunit interaction and guanine nucleotide dissociation inhibitor activity of the dual GoLoco motif protein PCP-2 (Purkinje cell protein-2). Cell Signal 18:1226–1234PubMedCrossRef Willard FS, McCudden CR, Siderovski DP (2006) G-protein alpha subunit interaction and guanine nucleotide dissociation inhibitor activity of the dual GoLoco motif protein PCP-2 (Purkinje cell protein-2). Cell Signal 18:1226–1234PubMedCrossRef
11.
Zurück zum Zitat Oberdick J, Levinthal F, Levinthal C (1988) A Purkinje cell differentiation marker shows partial DNA sequence homology to the cellular sis/PDGF2 gene. Neuron 1:367–376PubMedCrossRef Oberdick J, Levinthal F, Levinthal C (1988) A Purkinje cell differentiation marker shows partial DNA sequence homology to the cellular sis/PDGF2 gene. Neuron 1:367–376PubMedCrossRef
12.
Zurück zum Zitat Oberdick J, Smeyne RJ, Mann JR, Zackson S, Morgan JI (1990) A promoter that drives transgene expression in cerebellar Purkinje and retinal bipolar neurons. Science 248:223–226PubMedCrossRef Oberdick J, Smeyne RJ, Mann JR, Zackson S, Morgan JI (1990) A promoter that drives transgene expression in cerebellar Purkinje and retinal bipolar neurons. Science 248:223–226PubMedCrossRef
13.
Zurück zum Zitat Berrebi AS, Oberdick J, Sangameswaran L, Christakos S, Morgan JI, Mugnaini E (1991) Cerebellar Purkinje cell markers are expressed in retinal bipolar neurons. J Comp Neurol 308:630–649PubMedCrossRef Berrebi AS, Oberdick J, Sangameswaran L, Christakos S, Morgan JI, Mugnaini E (1991) Cerebellar Purkinje cell markers are expressed in retinal bipolar neurons. J Comp Neurol 308:630–649PubMedCrossRef
14.
Zurück zum Zitat Vassileva G, Smeyne R, Morgan J (1997) Absence of neuroanatomical and behavioral deficits in L7/Pcp2 null mice. Mol Brain Res 46:333–337PubMedCrossRef Vassileva G, Smeyne R, Morgan J (1997) Absence of neuroanatomical and behavioral deficits in L7/Pcp2 null mice. Mol Brain Res 46:333–337PubMedCrossRef
15.
Zurück zum Zitat Mohn AR, Feddersen RM, Nguyen MS, Koller BH (1997) Phenotypic analysis of mice lacking the highly abundant Purkinje cell and bipolar neuron-specific PCP2 protein. Mol Cell Neurosci 9:63–76PubMedCrossRef Mohn AR, Feddersen RM, Nguyen MS, Koller BH (1997) Phenotypic analysis of mice lacking the highly abundant Purkinje cell and bipolar neuron-specific PCP2 protein. Mol Cell Neurosci 9:63–76PubMedCrossRef
16.
Zurück zum Zitat Kinoshita-Kawada M, Oberdick J, Zhu MX (2004) A Purkinje cell-specific GoLoco domain protein, L7/Pcp2, modulates receptor-mediated inhibition of Cav2.1 Ca2+ channels in a dose-dependent manner. Mol Brain Res 132:73–86PubMedCrossRef Kinoshita-Kawada M, Oberdick J, Zhu MX (2004) A Purkinje cell-specific GoLoco domain protein, L7/Pcp2, modulates receptor-mediated inhibition of Cav2.1 Ca2+ channels in a dose-dependent manner. Mol Brain Res 132:73–86PubMedCrossRef
17.
Zurück zum Zitat Kim JJ, Thompson RF (1997) Cerebellar circuits and synaptic mechanisms involved in classical eyeblink conditioning. Trends Neurosci 20:177–181PubMedCrossRef Kim JJ, Thompson RF (1997) Cerebellar circuits and synaptic mechanisms involved in classical eyeblink conditioning. Trends Neurosci 20:177–181PubMedCrossRef
18.
Zurück zum Zitat De Zeeuw CI, Hansel C, Bian F, Koekkoek SKE, van Alphen AM, Linden DJ, Oberdick J (1998) Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20:495–508PubMedCrossRef De Zeeuw CI, Hansel C, Bian F, Koekkoek SKE, van Alphen AM, Linden DJ, Oberdick J (1998) Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20:495–508PubMedCrossRef
19.
Zurück zum Zitat Raymond JL, Lisberger SG (2000) Hypotheses about the neural trigger for plasticity in the circuit for the vestibulo-ocular reflex. Prog Brain Res 124:235–246PubMedCrossRef Raymond JL, Lisberger SG (2000) Hypotheses about the neural trigger for plasticity in the circuit for the vestibulo-ocular reflex. Prog Brain Res 124:235–246PubMedCrossRef
20.
Zurück zum Zitat Hansel C, Linden DJ, D’Angelo ED (2001) Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat Neurosci 4(5):467–475PubMed Hansel C, Linden DJ, D’Angelo ED (2001) Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat Neurosci 4(5):467–475PubMed
21.
Zurück zum Zitat Blazquez PM, Hirata Y, Highstein SM (2004) The vestibulo-ocular reflex as a model system for motor learning: what is the role of the cerebellum? Cerebellum 3:188–192PubMedCrossRef Blazquez PM, Hirata Y, Highstein SM (2004) The vestibulo-ocular reflex as a model system for motor learning: what is the role of the cerebellum? Cerebellum 3:188–192PubMedCrossRef
22.
Zurück zum Zitat Metzger F, Kapfhammer JP (2003) Protein kinase C: its role in activity-dependent Purkinje cell development and plasticity. Cerebellum 2:206–214PubMedCrossRef Metzger F, Kapfhammer JP (2003) Protein kinase C: its role in activity-dependent Purkinje cell development and plasticity. Cerebellum 2:206–214PubMedCrossRef
23.
Zurück zum Zitat Smeyne RJ, Chu T, Lewin A, Bian F, S-Crisman S, Kunsch C, Lira S, Oberdick J (1995) Local control of granule cell generation by cerebellar Purkinje cells. Mol Cell Neurosci 6:230–251PubMedCrossRef Smeyne RJ, Chu T, Lewin A, Bian F, S-Crisman S, Kunsch C, Lira S, Oberdick J (1995) Local control of granule cell generation by cerebellar Purkinje cells. Mol Cell Neurosci 6:230–251PubMedCrossRef
24.
Zurück zum Zitat Zhang X, Baader S, Bian F, Muller W, Oberdick J (2001) High level Purkinje cell-specific expression of green fluorescent protein in transgenic mice. Histochem Cell Biol 115:455–464PubMed Zhang X, Baader S, Bian F, Muller W, Oberdick J (2001) High level Purkinje cell-specific expression of green fluorescent protein in transgenic mice. Histochem Cell Biol 115:455–464PubMed
25.
Zurück zum Zitat Baader SL, Sanlioglu S, Berrebi AS, Parker-Thornburg J, Oberdick J (1998) Ectopic overexpression of Engrailed-2 in cerebellar Purkinje cells causes restricted cell loss and retarded external germinal layer development at lobule junctions. J Neurosci 18:1763–1773PubMed Baader SL, Sanlioglu S, Berrebi AS, Parker-Thornburg J, Oberdick J (1998) Ectopic overexpression of Engrailed-2 in cerebellar Purkinje cells causes restricted cell loss and retarded external germinal layer development at lobule junctions. J Neurosci 18:1763–1773PubMed
26.
Zurück zum Zitat Wanner I, Baader S, Brich M, Oberdick J, Schilling K (1997) Subcellular localization of specific mRNAs and their protein products in Purkinje cells by combined fluorescence in situ hybrdization and immunocytochemistry. Histochem Cell Biol 108:345–357PubMedCrossRef Wanner I, Baader S, Brich M, Oberdick J, Schilling K (1997) Subcellular localization of specific mRNAs and their protein products in Purkinje cells by combined fluorescence in situ hybrdization and immunocytochemistry. Histochem Cell Biol 108:345–357PubMedCrossRef
27.
Zurück zum Zitat Wanner I, Baader S, Oberdick J, Schilling K (2000) Changing subcellular distribution and activity-dependent utilization of a dendritically localized mRNA in developing Purkinje cells. Mol Cell Neurosci 15:275–287PubMedCrossRef Wanner I, Baader S, Oberdick J, Schilling K (2000) Changing subcellular distribution and activity-dependent utilization of a dendritically localized mRNA in developing Purkinje cells. Mol Cell Neurosci 15:275–287PubMedCrossRef
28.
Zurück zum Zitat Blichenberg A, Schwanke B, Rehbein M, Garner CC, Richter D, Kindler S (1999) Identification of a cis-acting dendritic targeting element in MAP2 mRNAs. J Neurosci 19:8818–8829PubMed Blichenberg A, Schwanke B, Rehbein M, Garner CC, Richter D, Kindler S (1999) Identification of a cis-acting dendritic targeting element in MAP2 mRNAs. J Neurosci 19:8818–8829PubMed
29.
Zurück zum Zitat Mori Y, Imaizumi K, Katayama T, Yoneda T, Tohyama M (2000) Two cis-acting elements in the 3′ untranslated region of a-CaMKII regulate its dendritic targeting. Nat Neurosci 3:1079–1084PubMedCrossRef Mori Y, Imaizumi K, Katayama T, Yoneda T, Tohyama M (2000) Two cis-acting elements in the 3′ untranslated region of a-CaMKII regulate its dendritic targeting. Nat Neurosci 3:1079–1084PubMedCrossRef
30.
Zurück zum Zitat Blichenberg A, Rehbein M, Muller R, Garner CC, Richter D, Kindler S (2001) Identification of a cis-acting dendritic targeting element in the mRNA encoding the a subunit of Ca2+/calmodulin-dependent protein kinase II. Eur J Neurosci 13:1881–1888PubMedCrossRef Blichenberg A, Rehbein M, Muller R, Garner CC, Richter D, Kindler S (2001) Identification of a cis-acting dendritic targeting element in the mRNA encoding the a subunit of Ca2+/calmodulin-dependent protein kinase II. Eur J Neurosci 13:1881–1888PubMedCrossRef
31.
Zurück zum Zitat MacDonald PM, Struhl G (1988) Cis-acting sequences responsible for anterior localization of bicoid mRNA in Drosophila embryos. Nature 336:595–598PubMedCrossRef MacDonald PM, Struhl G (1988) Cis-acting sequences responsible for anterior localization of bicoid mRNA in Drosophila embryos. Nature 336:595–598PubMedCrossRef
32.
Zurück zum Zitat Gavis ER, Lehmann R (1994) Translational regulation of nanos by RNA localization. Nature 369:315–318PubMedCrossRef Gavis ER, Lehmann R (1994) Translational regulation of nanos by RNA localization. Nature 369:315–318PubMedCrossRef
33.
Zurück zum Zitat Ferrandon D, Elphick L, Nusslein-Volhard C, St Johnston D (1994) Staufen protein associates with the 3′YTP of bicoid mRNA to form particles that move in a microtubule-dependent manner. Cell 79:1221–1232PubMedCrossRef Ferrandon D, Elphick L, Nusslein-Volhard C, St Johnston D (1994) Staufen protein associates with the 3′YTP of bicoid mRNA to form particles that move in a microtubule-dependent manner. Cell 79:1221–1232PubMedCrossRef
34.
Zurück zum Zitat Palacios IM, St Johnston D (2001) Getting the message across: the intracellular localization of mRNAs in higher eukaryotes. Annu Rev Cell Dev Biol 17:569–614PubMedCrossRef Palacios IM, St Johnston D (2001) Getting the message across: the intracellular localization of mRNAs in higher eukaryotes. Annu Rev Cell Dev Biol 17:569–614PubMedCrossRef
35.
Zurück zum Zitat Bockers TM, Segger-Junius M, Iglauer P, Bockmann J, Gundelfinger ED, Kreutz MR, Richter D, Kindler S, Kreienkamp H (2004) Differential expression and dendritic transcript localization of Shank family members: identification of a dendritic targeting element in the 3′ untranslated region of Shank1 mRNA. Mol Cell Neurosci 26:182–190PubMedCrossRef Bockers TM, Segger-Junius M, Iglauer P, Bockmann J, Gundelfinger ED, Kreutz MR, Richter D, Kindler S, Kreienkamp H (2004) Differential expression and dendritic transcript localization of Shank family members: identification of a dendritic targeting element in the 3′ untranslated region of Shank1 mRNA. Mol Cell Neurosci 26:182–190PubMedCrossRef
36.
Zurück zum Zitat Serinagaoglu Y, Zhang R, Zhang Y, Zhang L, Hartt G, Young AP, Oberdick J (2007) A promoter element with enhancer properties, and the orphan nuclear receptor RORalpha, are required for Purkinje cell-specific expression of a Gi/o modulator. Mol Cell Neurosci 34:324–342PubMedCrossRef Serinagaoglu Y, Zhang R, Zhang Y, Zhang L, Hartt G, Young AP, Oberdick J (2007) A promoter element with enhancer properties, and the orphan nuclear receptor RORalpha, are required for Purkinje cell-specific expression of a Gi/o modulator. Mol Cell Neurosci 34:324–342PubMedCrossRef
37.
Zurück zum Zitat Simons MJ, Pellionisz A (2006) Genomics, morphogenesis, and biophysics: triangulation of Purkinje cell development. Cerebellum 5:27–35PubMedCrossRef Simons MJ, Pellionisz A (2006) Genomics, morphogenesis, and biophysics: triangulation of Purkinje cell development. Cerebellum 5:27–35PubMedCrossRef
38.
Zurück zum Zitat Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415PubMedCrossRef Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415PubMedCrossRef
39.
Zurück zum Zitat Webb CKm McCudden CR, Willard FS, Kimple RJ, Siderovski DP, Oxford GS (2005) D2 dopamine receptor activation of potassium channels is selectively decoupled by Ga1-dpecific GoLoco motif peptides. J Neurochem 92:1408–1418CrossRef Webb CKm McCudden CR, Willard FS, Kimple RJ, Siderovski DP, Oxford GS (2005) D2 dopamine receptor activation of potassium channels is selectively decoupled by Ga1-dpecific GoLoco motif peptides. J Neurochem 92:1408–1418CrossRef
40.
Zurück zum Zitat Miller S, Yasuda M, Coats JK, Jones Y, Martone ME, Mayford M (2002) Disruption of dendritic translation of CaMKIIa impairs stabilization of synaptic plasticity and memory consolidation. Neuron 36:507–519PubMedCrossRef Miller S, Yasuda M, Coats JK, Jones Y, Martone ME, Mayford M (2002) Disruption of dendritic translation of CaMKIIa impairs stabilization of synaptic plasticity and memory consolidation. Neuron 36:507–519PubMedCrossRef
41.
Zurück zum Zitat Huang YS, Carson JH, Barbarese E, Richter JD (2003) Facilitation of dendritic mRNA transport by CPEB. Genes Dev 17:638–653PubMedCrossRef Huang YS, Carson JH, Barbarese E, Richter JD (2003) Facilitation of dendritic mRNA transport by CPEB. Genes Dev 17:638–653PubMedCrossRef
Metadaten
Titel
3′UTR-Dependent Localization of a Purkinje Cell Messenger RNA in Dendrites
verfasst von
Rui Zhang
Xulun Zhang
Feng Bian
Xin-an Pu
Karl Schilling
John Oberdick
Publikationsdatum
01.09.2008
Verlag
Springer-Verlag
Erschienen in
The Cerebellum / Ausgabe 3/2008
Print ISSN: 1473-4222
Elektronische ISSN: 1473-4230
DOI
https://doi.org/10.1007/s12311-008-0051-y

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