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Translation elongation factor-1A1 (eEF1A1) localizes to the spine by domain III

  • Cho, Sun-Jung (Department of Anatomy, Dongguk University College of Medicine) ;
  • Lee, Hyun-Sook (Department of Anatomy, Dongguk University College of Medicine) ;
  • Dutta, Samikshan (Department of Anatomy, Dongguk University College of Medicine) ;
  • Seog, Dae-Hyun (Department of Biochemistry, College of Medicine, Inje University) ;
  • Moon, Il-Soo (Department of Anatomy, Dongguk University College of Medicine)
  • Received : 2011.09.26
  • Accepted : 2011.12.15
  • Published : 2012.04.30

Abstract

In vertebrates, there are two variants of eukaryotic peptide elongation factor 1A (eEF1A; formerly eEF-$1{\alpha}$), eEF1A1 and eEF1A2, which have three well-conserved domains ($D_I$, $D_{II}$, and $D_{III}$). In neurons, eEF1A1 is the embryonic type, which is expressed during embryonic development as well as the first two postnatal weeks. In the present study, EGFP-tagged eEF1A1 truncates were expressed in cortical neurons isolated from rat embryo (E18-19). Live cell images of transfected neurons showed that $D_{III}$-containing EGFP-fusion proteins (EGFP-$D_{III}$, -$D_{II-III}$, -$D_{I-III}$) formed clusters that were confined within somatodendritic domains, while $D_{III}$-missing ones (EGFP-$D_I$, -$D_{II}$, -$D_{I-II}$) and control EGFP were homogeneously dispersed throughout the neuron including axons. In dendrites, EGFP-$D_{III}$ was targeted to the heads of spine- and filopodia-like protrusions, where it was colocalized with $SynGAP{\alpha}$, a postsynaptic marker. Our data indicate that $D_{III}$ of eEF1A1 mediates formation of clusters and localization to spines.

Keywords

References

  1. Merrick, W. C. and Nyborg, J. (2000) The protein biosynthesis elongation cycle. In Translational Control of Gene Expression, Sonenberg, N., Hershey, J. W. B. and Mathews, M. B., (eds.), pp. 89-125, Cold Spring Harbor Laboratory Press, New York, USA.
  2. Mateyak, M. K. and Kinzy, T. G. (2010) eEF1A: Thinking outside the ribosome. J. Biol. Chem. 285, 21209-21213. https://doi.org/10.1074/jbc.R110.113795
  3. Liu, G., Tang, J., Edmonds, B. T., Murray, J., Levin, S., Condeelis, J. (1996) F-actin sequesters elongation factor 1alpha from interaction with aminoacyl-tRNA in a pH-dependent reaction. J. Cell Biol. 135, 953-963. https://doi.org/10.1083/jcb.135.4.953
  4. Moore, R. C. and Cyr, R. J. (2000) Association between elongation factor-1alpha and microtubules in vivo is domain dependent and conditional. Cell Motil. Cytoskeleton 45, 279-292. https://doi.org/10.1002/(SICI)1097-0169(200004)45:4<279::AID-CM4>3.0.CO;2-4
  5. Gross, S. R. and Kinzy, T. G. (2005) Translation elongation factor 1A is essential for regulation of the actin cytoskeleton and cell morphology. Nat. Struct. Mol. Biol. 12, 772-778. https://doi.org/10.1038/nsmb979
  6. Bunai, F., Ando, K., Ueno, H. and Numata, O. (1996) Tetrahymena eukaryotic translation elongation factor 1A (eEF1A) bundles filamentous actin through dimer formation. J. Biochem. 140, 393-399.
  7. Chuang, S. M., Chen, L., Lambertson, D., Anand, M., Kinzy, T. G. and Madura, K. (2005) Proteasome-mediated degradation of cotranslationally damaged proteins involves translation elongation factor 1A. Mol. Cell Biol. 25, 403-413. https://doi.org/10.1128/MCB.25.1.403-413.2005
  8. McClatchy, D. B., Fang, G. and Levey, A. I. (2006) Elongation factor 1A family regulates the recycling of the M4 muscarinic acetylcholine receptor. Neurochem. Res. 31, 975-988. https://doi.org/10.1007/s11064-006-9103-1
  9. Ruest, L. B., Marcotte, R. and Wang, E. (2002) Peptide elongation factor eEF1A-2/S1 expression in cultured differentiated myotubes and its protective effect against caspase-3-mediated apoptosis. J. Biol. Chem. 277, 5418-5425. https://doi.org/10.1074/jbc.M110685200
  10. Chang, R. and Wang, E. (2007) Mouse translation elongation factor eEF1A-2 interacts with Prdx-I to protect cells against apoptotic death induced by oxidative stress. J. Cell. Biochem. 100, 267-278. https://doi.org/10.1002/jcb.20969
  11. Kahns, S., Lund, A., Kristensen, P., Knudsen, C. R., Clark, B. F., Cavallius, J. and Merrick, W. C. (1998) The elongation factor 1 A-2 isoform from rabbit: cloning of the cDNA and characterization of the protein. Nucleic Acids Res. 26, 1884-1890. https://doi.org/10.1093/nar/26.8.1884
  12. Kristensen, P., Lund, A., Clark, B. F., Cavallius, J. and Merrick, W. C. (1998) Purification and characterisation of a tissue specific elongation factor 1 alpha (EF-1 alpha 2) from rabbit muscle. Biochem. Biophys. Res. Commun. 245, 810-814. https://doi.org/10.1006/bbrc.1998.8510
  13. Lee, S., Francoeur, A. M., Liu, S. and Wang, E. (1992) Tissue-specific expression in mammalian brain, heart, and muscle of S1, a member of the elongation factor-1 alpha gene family. J. Biol. Chem. 267, 24064-24068.
  14. Knudsen, S. M., Frydenberg, J., Clark, B. F. and Leffers, H. (1993) Tissue-dependent variation in the expression of elongation factor-1 alpha isoforms: isolation and characterisation of a cDNA encoding a novel variant of human elongation-factor 1 alpha. Eur. J. Biochem. 215, 549-554. https://doi.org/10.1111/j.1432-1033.1993.tb18064.x
  15. Chambers, D. M., Peters, J. and Abbott, C. M. (1998) The lethal mutation of the mouse wasted (wst) is a deletion that abolishes expression of a tissue-specific isoform of translation elongation factor 1alpha, encoded by the Eef1a2 gene. Proc. Natl. Acad. Sci. U.S.A. 95, 4463-4468. https://doi.org/10.1073/pnas.95.8.4463
  16. Newbery, H. J., Loh, D. H., O'Donoghue, J. E., Tomlinson, V. A., Chau, Y. Y., Boyd, J. A., Bergmann, J. H., Brownstein, D. and Abbott, C. M. (2007) Translation elongation factor eEF1A2 is essential for post-weaning survival in mice. Biol. Chem. 282, 28951-28959. https://doi.org/10.1074/jbc.M703962200
  17. Lee, S., Wolfraim, L. A. and Wang, E. (1993) Differential expression of S1 and elongation factor-1 alpha during rat development. J. Biol. Chem. 268, 24453-24459.
  18. Khalyfa, A., Bourbeau, D., Chen, E., Petroulakis, E., Pan, J., Xu, S. and Wang, E. (2001) Characterization of elongation factor-1A (eEF1A-1) and eEF1A-2/S1 protein expression in normal and wasted mice. J. Biol. Chem. 276, 22915-22922. https://doi.org/10.1074/jbc.M101011200
  19. Pan, J., Ruest, L. B., Xu, S. and Wang, E. (2004) Immunocharacterization of the switch of peptide elongation factors eEF1A-1/EF-1alpha and eEF1A-2/S1 in the central nervous system during mouse development. Brain Res. Dev. Brain Res. 149, 1-8.
  20. Phillips, G. R., Florens, L., Tanaka, H., Khaing, Z. Z., Fidler, L., Yates, J. R. 3rd. and Colman, D. R. (2005) Proteomic comparison of two fractions derived from the transsynaptic scaffold. J. Neurosci. Res. 816, 762-775.
  21. Li, K. W., Hornshaw, M. P., Van Der Schors, R. C., Watson, R., Tate, S., Casetta, B., Jimenez, C. R., Gouwenberg, Y., Gundelfinger, E. D., Smalla, K. H. and Smit, A. B. (2004) Proteomics analysis of rat brain postsynaptic density. Implications of the diverse protein functional groups for the integration of synaptic physiology. J. Biol. Chem. 279, 987-1002. https://doi.org/10.1074/jbc.M303116200
  22. Cho, S. J., Jung, J. S., Ko, B. H., Jin, I. and Moon, I. S. (2004) Presence of translation elongation factor-1A (eEF1A) in the excitatory postsynaptic density of rat cerebral cortex. Neurosci. Lett. 366, 29-33. https://doi.org/10.1016/j.neulet.2004.05.036
  23. Bluem, R., Schmidt, E., Corvey, C., Karas, M., Schlicksupp, A., Kirsch, J. and Kuhse, J. (2007) Components of the translational machinery are associated with juvenile glycine receptors and are redistributed to the cytoskeleton upon aging and synaptic activity. J. Biol. Chem. 282, 37783-37793. https://doi.org/10.1074/jbc.M708301200
  24. Dotti, C. G., Sullivan, C. A. and Banker, G. A. (1988) The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8, 1454-1468.
  25. Chen, H. J., Rojas-Soto, M., Oguni, A. and Kennedy, M. B. (1998) A synaptic Ras-GTPase activating protein (p135 SynGAP) inhibited by CaM kinase II. Neuron 20, 895-904. https://doi.org/10.1016/S0896-6273(00)80471-7
  26. Vazquez, L. E., Chen, H. J., Sokolova, I., Knuesel, I. and Kennedy, M. B. (2004) SynGAP regulates spine formation. J. Neurosci. 24, 8862-8872. https://doi.org/10.1523/JNEUROSCI.3213-04.2004
  27. Andersen, G. R., Nissen, P. and Nyborg, J. (2003) Elongation factors in protein biosynthesis. Trends Biochem. Sci. 28, 434-441. https://doi.org/10.1016/S0968-0004(03)00162-2
  28. Demma, M., Warren, V., Hock, R., Dharmawardhane, S. and Condeelis, J. (1990) Isolation of an abundant 50,000-dalton actin filament bundling protein from Dictyostelium amoebae. J. Biol. Chem. 265, 2286-2291.
  29. Yang, F., Demma, M., Warren, V., Dharmawardhane, S. and Condeelis, J. (1990) Identification of an actin-binding protein from Dictyostelium as elongation factor 1a. Nature 347, 494-496. https://doi.org/10.1038/347494a0
  30. Edmonds, B. T., Murray, J., and Condeelis, J. (1995) pH regulation of the F-actin binding properties of Dictyostelium elongation factor 1 alpha. J. Biol. Chem. 270, 15222-15230. https://doi.org/10.1074/jbc.270.25.15222
  31. Korobova, F. and Svitkina T. (2010) Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol. Biol. Cell 21, 165-176. https://doi.org/10.1091/mbc.E09-07-0596
  32. Liu, G., Grant, W. M., Persky, D., Latham, V. M. Jr., Singer, R. H. and Condeelis, J. (2002) Interactions of elongation factor 1alpha with F-actin and beta-actin mRNA: implications for anchoring mRNA in cell protrusions. Mol. Biol. Cell 13, 579-592. https://doi.org/10.1091/mbc.01-03-0140
  33. Morita, K., Bunai, F. and Numata, O. (2008) Roles of three domains of Tetrahymena eEF1A in bundling F-actin. Zoolog. Sci. 25, 22-29. https://doi.org/10.2108/zsj.25.22
  34. Anand, N., Murthy, S., Amann, G., Wernick, M., Porter, L. A., Cukier, I. H., Collins, C., Gray, J. W., Diebold, J., Demetrick, D. J. and Lee, J. M. (2002) Protein elongation factor eEF1A2 is a putative oncogene in ovarian cancer. Nat. Genet. 31, 301-305. https://doi.org/10.1038/ng904
  35. Abbott, C. M., Newbery, H. J., Squires, C. E., Brownstein, D., Griffiths, L. A. and Soares, D. C. (2009) eEF1A2 and neuronal degeneration. Biochem. Soc. Trans. 37, 1293-1297. https://doi.org/10.1042/BST0371293
  36. Carlson, B. M., Borisov, A. B., Dedkov, E. I., Khalyfa, A., Kostrominova, T. Y., Macpherson, P. C., Wang, E. and Faulkner, J. A. (2002) Effects of long-term denervation on skeletal muscle in old rats. J. Gerontol. Sect. A Biol. Sci. Med. Sci. 57, B366-374. https://doi.org/10.1093/gerona/57.10.B366
  37. Khalyfa, A., Carlson, B. M., Dedkov, E. I. and Wang, E. (2003) Changes in protein levels of elongation factors, eEF1A-1 and eEF1A-2/S1, in long-term denervated rat muscle. Restor. Neurol. Neurosci. 21, 47-53.
  38. Cingolani, L. A. and Goda, Y. (2008) Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat. Rev. Neurosci. 9, 344-356. https://doi.org/10.1038/nrn2373
  39. Tropea, D., Majewska, A. K., Garcia, R. and Sur, M. (2010) Structural dynamics of synapses in vivo correlate with functional changes during experience-dependent plasticity in visual cortex. J. Neurosci. 30, 11086-11095. https://doi.org/10.1523/JNEUROSCI.1661-10.2010
  40. Brewer, G. J., Torricelli, J. R., Evege, E. K. and Price, P. J. (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35, 567-576. https://doi.org/10.1002/jnr.490350513
  41. Goslin, K., Assmussen, H. and Banker, G. (1998) Rat hippocampal neurons in low density culture; in Culturing Nerve Cells, 2nd ed, Banker, G. and Goslin, K (eds.), pp. 339-370, MIT Press, Cambridge, London, England.
  42. Moon, I. S., Cho, S. J., Jin, I. and Walikonis, R. (2007) A simple method for combined fluorescence in situ hybridization and immunocytochemistry. Mol. Cells 24, 76-82.

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