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Dendritic localization and a cis-acting dendritic targeting element of Kv4.2 mRNA

  • Jo, Anna (Department of Medicine and Microbiology, College of Medicine, Signaling Disorder Research Center, Chungbuk National University) ;
  • Nam, Yeon-Ju (Department of Medicine and Microbiology, College of Medicine, Signaling Disorder Research Center, Chungbuk National University) ;
  • Oh, Jun-Young (Department of Medicine and Microbiology, College of Medicine, Signaling Disorder Research Center, Chungbuk National University) ;
  • Cheon, Hyo-Soon (Department of Medicine and Microbiology, College of Medicine, Signaling Disorder Research Center, Chungbuk National University) ;
  • Jeromin, Andreas (Banyan Biomarkers, Inc) ;
  • Lee, Jin-A (Department of Biological Engineering, Hannam University) ;
  • Kim, Hyong-Kyu (Department of Medicine and Microbiology, College of Medicine, Signaling Disorder Research Center, Chungbuk National University)
  • Received : 2010.07.12
  • Accepted : 2010.08.16
  • Published : 2010.10.31

Abstract

Kv4.2, a pore-forming $\alpha$-subunit of voltage-gated A-type potassium channels, is expressed abundantly in the soma and dendrites of hippocampal neurons, and is responsible for somatodendritic $I_A$ current. Recent studies have suggested that changes in the surface levels of Kv4.2 potassium channels might be relevant to synaptic plasticity. Although the function and expression of Kv4.2 protein have been extensively studied, the dendritic localization of Kv4.2 mRNA is not well described. In this study, Kv4.2 mRNAs were shown to be localized in the dendrites near postsynaptic regions. The dendritic transport of Kv4.2 mRNAs were mediated by microtubule-based movement. The 500 nucleotides of specific regions within the 3'-untranslated region of Kv4.2 mRNA were found to be necessary and sufficient for its dendritic localization. Collectively, these results suggest that the dendritic localization of Kv4.2 mRNAs might regulate the dendritic surface level of Kv4.2 channels and synaptic plasticity.

Keywords

References

  1. Birnbaum, S. G., Varga, A. W., Yuan, L. L., Anderson, A. E., Sweatt, J. D. and Schrader, L. A. (2004) Structure and function of Kv4-family transient potassium channels. Physiol. Rev. 84, 803-833. https://doi.org/10.1152/physrev.00039.2003
  2. Covarrubias, M., Bhattacharji, A., De Santiago-Castillo, J. A., Dougherty, K., Kaulin, Y. A., Na-Phuket, T. R. and Wang, G. (2008) The neuronal Kv4 channel complex. Neurochem. Res. 33, 1558-1567. https://doi.org/10.1007/s11064-008-9650-8
  3. Hoffman, D. A., Magee, J. C., Colbert, C. M. and Johnston, D. (1997) K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387, 869-875. https://doi.org/10.1038/43119
  4. Watanabe, S., Hoffman, D. A., Migliore, M. and Johnston, D. (2002) Dendritic K+ channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc. Natl. Acad. Sci. U.S.A. 99, 8366-8371. https://doi.org/10.1073/pnas.122210599
  5. Cai, X., Liang, C. W., Muralidharan, S., Kao, J. P., Tang, C. M. and Thompson S. M. (2004) Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 44, 351-364. https://doi.org/10.1016/j.neuron.2004.09.026
  6. Frick, A., Magee, J. and Johnston, D. (2004) LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat. Neurosci. 7, 126-135. https://doi.org/10.1038/nn1178
  7. Chen, X., Yuan, L. L., Zhao, C., Birnbaum, S. G., Frick, A., Jung, W. E., Schwarz, T. L., Sweatt, J. D. and Johnston, D. (2006) Deletion of Kv4.2 gene eliminates dendritic A-type $K^+$ current and enhances induction of long-term potentiation in hippocampal CA1 pyramidal neurons. J. Neurosci. 26, 12143-12151. https://doi.org/10.1523/JNEUROSCI.2667-06.2006
  8. Sheng, M., Tsaur, M. L., Jan, Y. N. and Jan, L. Y. (1992) Subcellular segregation of two A-type K+ channel proteins in rat central neurons. Neuron 9, 271-284. https://doi.org/10.1016/0896-6273(92)90166-B
  9. Maletic-Savatic, M., Lenn, N. J. and Trimmer, J. S. (1995) Differential spatiotemporal expression of K+ channel polypeptides in rat hippocampal neurons developing in situ and in vitro. J. Neurosci. 15, 3840-3851.
  10. Serodio, P. and Rudy, B. (1998) Differential expression of Kv4 $K^+$ channel subunits mediating subthreshold transient $K^+$ (A-type) currents in rat brain. J. Neurophysiol. 79, 1081-1091. https://doi.org/10.1152/jn.1998.79.2.1081
  11. Kim, J., Wei, D. S. and Hoffman, D. A. (2005) Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J. Physiol. 569, 41-57. https://doi.org/10.1113/jphysiol.2005.095042
  12. Tkatch, T., Baranauskas, G. and Surmeier, D. J. (2000) Kv4.2 mRNA abundance and A-type K(+) current amplitude are linearly related in basal ganglia and basal forebrain neurons. J. Neurosci. 20, 579-588.
  13. Lauver, A., Yuan, L. L., Jeromin, A., Nadin, B. M., Rodriguez, J. J., Davies, H. A., Stewart, M. G., Wu, G. Y. and Pfaffinger, P. J. (2006) Manipulating Kv4.2 identifies a specific component of hippocampal pyramidal neuron A-current that depends upon Kv4.2 expression. J. Neurochem. 99, 1207-1223. https://doi.org/10.1111/j.1471-4159.2006.04185.x
  14. Kim, J., Jung, S. C., Clemens, A. M., Petralia, R. S. and Hoffman, D. A. (2007) Regulation of dendritic excitability by activity-dependent trafficking of the A-type K+ channel subunit Kv4.2 in hippocampal neurons. Neuron 54, 933-947. https://doi.org/10.1016/j.neuron.2007.05.026
  15. Lei, Z., Deng, P. and Xu, Z. C. (2008) Regulation of Kv4.2 channels by glutamate in cultured hippocampal neurons. J. Neurochem. 106, 182-192. https://doi.org/10.1111/j.1471-4159.2008.05356.x
  16. Sutton, M. A. and Schuman, E. M. (2005) Local translational control in dendrites and its role in long-term synaptic plasticity. J. Neurobiol. 64, 116-131. https://doi.org/10.1002/neu.20152
  17. Pfeiffer, B. E. and Huber, K. M. (2006) Current advances in local protein synthesis and synaptic plasticity. J. Neurosci. 26, 7147-7150. https://doi.org/10.1523/JNEUROSCI.1797-06.2006
  18. Kang, H. and Schuman, E. M. (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273, 1402-1406. https://doi.org/10.1126/science.273.5280.1402
  19. Huber, K. M., Kayser, M. S. and Bear, M. F. (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288, 1254-1257. https://doi.org/10.1126/science.288.5469.1254
  20. Knowles, R. B. and Kosik, K. S. (1997) Neurotrophin-3 signals redistribute RNA in neurons. Proc. Natl. Acad. Sci. U.S.A. 94, 14804-14808. https://doi.org/10.1073/pnas.94.26.14804
  21. 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.
  22. Muslimov, I. A., Banker, G., Brosius, J. and Tiedge, H. (1998) Activity-dependent regulation of dendritic BC1 RNA in hippocampal neurons in culture. J. Cell Biol. 141, 1601-1611. https://doi.org/10.1083/jcb.141.7.1601
  23. Steward, O., Wallace, C. S., Lyford, G. L. and Worley, P. F. (1998) Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21, 741-751. https://doi.org/10.1016/S0896-6273(00)80591-7
  24. Schacher, S., Wu, F., Panyko, J. D., Sun, Z. Y. and Wang, D. (1999) Expression and branch-specific export of mRNA are regulated by synapse formation and interaction with specific postsynaptic targets. J. Neurosci. 19, 6338-6347.
  25. Steward, O. and Worley, P. F. (2001) A cellular mechanism for targeting newly synthesized mRNAs to synaptic sites on dendrites. Proc. Natl. Acad. Sci. U.S.A. 98, 7062-7068. https://doi.org/10.1073/pnas.131146398
  26. Martin, K. C. and Zukin, R. S. (2006) RNA trafficking and local protein synthesis in dendrites: an overview. J. Neurosci. 26, 7131-7134. https://doi.org/10.1523/JNEUROSCI.1801-06.2006
  27. Raab-Graham, K. F., Haddick, P. C., Jan, Y. N. and Jan, L. Y. (2006) Activity- and mTOR-dependent suppression of Kv1.1 channel mRNA translation in dendrites. Science 314, 144-148. https://doi.org/10.1126/science.1131693
  28. 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. U.S.A. 93, 13250-13255. https://doi.org/10.1073/pnas.93.23.13250
  29. 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. https://doi.org/10.1038/80591
  30. Jambhekar, A. and Derisi, J. L. (2007) Cis-acting determinants of asymmetric, cytoplasmic RNA transport. RNA 13, 625-642. https://doi.org/10.1261/rna.262607
  31. Andreassi, C. and Riccio, A. (2009) To localize or not to localize: mRNA fate is in 3'UTR ends. Trends Cell Biol. 19, 465-474. https://doi.org/10.1016/j.tcb.2009.06.001
  32. Rook, M. S., Lu, M. and Kosik, K. S. (2000) CaMKIIalpha 3' untranslated region-directed mRNA translocation in living neurons: visualization by GFP linkage. J. Neurosci. 20, 6385-6393.
  33. 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.
  34. Ainger, K., Avossa, D., Diana, A. S., Barry, C., Barbarese, E. and Carsonv J. H. (1997) Transport and localization elements in myelin basic protein mRNA. J. Cell Biol. 138, 1077-1087. https://doi.org/10.1083/jcb.138.5.1077
  35. Jeong, J. H., Nam, Y. J., Kim, S. Y., Kim, E. G., Jeong, J. and Kim, H. K. (2007) The transport of Staufen2- containing ribonucleoprotein complexes involves kinesin motor protein and is modulated by mitogen-activated protein kinase pathway. J. Neurochem. 102, 2073-2084. https://doi.org/10.1111/j.1471-4159.2007.04697.x
  36. Goetze, B., Grunewald, B., Baldassa, S. and Kiebler, M. (2004) Chemically controlled formation of a DNA/calcium phosphate coprecipitate: application for transfection of mature hippocampal neurons. J. Neurobiol. 60, 517-525. https://doi.org/10.1002/neu.20073

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