Compartment-specific, differential regulation of eukaryotic elongation factor 2 and its kinase within Aplysia sensory neurons

Journal of Neurochemistry

Volumn 117, Issue 5, 2011, Pages 841-855

  Weatherill, Daniel B ^a   McCamphill, Patrick K ^a   Pethoukov, Eugenia ^a   Dunn, Tyler W ^a   Fan, Xiaotang ^a   Sossin, Wayne S ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Aplysia; compartment specific; elongation; eukaryotic elongation factor 2; eukaryotic elongation factor 2 kinase; long term facilitation

Indexed keywords

ALANINE; ELONGATION FACTOR 2; ELONGATION FACTOR 2 KINASE; S6 KINASE; SERINE; SEROTONIN;

APLYSIA; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE MUTATION; GENE OVEREXPRESSION; INTERNAL RIBOSOME ENTRY SITE; INTRACELLULAR SPACE; NEURITE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REGULATORY MECHANISM; SENSORY NERVE CELL; SOMATIC CELL; TRANSLATION REGULATION;

ANIMALS; APLYSIA; BLOTTING, WESTERN; CAENORHABDITIS ELEGANS PROTEINS; CELLS, CULTURED; CLONING, MOLECULAR; ELONGATION FACTOR 2 KINASE; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, FLUORESCENCE; NEURITES; PEPTIDE ELONGATION FACTOR 2; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBOSOMAL PROTEIN S6 KINASES; SENSORY RECEPTOR CELLS; SEROTONIN; TRANSCRIPTION FACTORS;

APLYSIA; EUKARYOTA;

EID: 79955651138     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07251.x     Document Type: Article

References (45)

1. Barzilai A., Kennedy T. E., Sweatt J. D., and, Kandel E. R., (1989) 5-HT modulates protein synthesis and the expression of specific proteins during long-term facilitation in Aplysia sensory neurons. Neuron 2, 1577-1586.
2. Belelovsky K., Elkobi A., Kaphzan H., Nairn A. C., and, Rosenblum K., (2005) A molecular switch for translational control in taste memory consolidation. Eur. J. Neurosci. 22, 2560-2568. (Pubitemid 41758998)
3. Browne G. J., and, Proud C. G., (2002) Regulation of peptide-chain elongation in mammalian cells. Eur. J. Biochem. 269, 5360-5368. (Pubitemid 35365525)
4. Browne G. J., and, Proud C. G., (2004) A novel mTOR-regulated phosphorylation site in elongation factor 2 kinase modulates the activity of the kinase and its binding to calmodulin. Mol. Cell. Biol. 24, 2986-2997. (Pubitemid 38381287)
5. Browne G. J., Finn S. G., and, Proud C. G., (2004) Stimulation of the AMP-activated protein kinase leads to activation of eukaryotic elongation factor 2 kinase and to its phosphorylation at a novel site, serine 398. J. Biol. Chem. 279, 12220-12231. (Pubitemid 38445787)
6. Carroll M., Warren O., Fan X., and, Sossin W. S., (2004) 5-HT stimulates eEF2 dephosphorylation in a rapamycin-sensitive manner in Aplysia neurites. J. Neurochem. 90, 1464-1476. (Pubitemid 39223649)
7. Carroll M., Dyer J., and, Sossin W. S., (2006) Serotonin increases phosphorylation of synaptic 4EBP through TOR, but eukaryotic initiation factor 4E levels do not limit somatic cap-dependent translation in aplysia neurons. Mol. Cell. Biol. 26, 8586-8598. (Pubitemid 44748590)
8. Casadio A., Martin K. C., Giustetto M., Zhu H., Chen M., Bartsch D., Bailey C. H., and, Kandel E. R., (1999) A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99, 221-237. (Pubitemid 29491788)
9. Chotiner J. K., Khorasani H., Nairn A. C., O'Dell T. J., and, Watson J. B., (2003) Adenylyl cyclase-dependent form of chemical long-term potentiation triggers translational regulation at the elongation step. Neuroscience 116, 743-752. (Pubitemid 36160570)
10. Costa-Mattioli M., Sossin W. S., Klann E., and, Sonenberg N., (2009) Translational control of long-lasting synaptic plasticity and memory. Neuron 61, 10-26.
11. Davidkova G., and, Carroll R. C., (2007) Characterization of the role of microtubule-associated protein 1B in metabotropic glutamate receptor-mediated endocytosis of AMPA receptors in hippocampus. J. Neurosci. 27, 13273-13278. (Pubitemid 350220475)
12. Diggle T. A., Subkhankulova T., Lilley K. S., Shikotra N., Willis A. E., and, Redpath N. T., (2001) Phosphorylation of elongation factor-2 kinase on serine 499 by cAMP-dependent protein kinase induces Ca2+/calmodulin-independent activity. Biochem. J. 353, 621-626. (Pubitemid 32158330)
13. Dyer J. R., Michel S., Lee W., Castellucci V. F., Wayne N. L., and, Sossin W. S., (2003) An activity-dependent switch to cap-independent translation triggered by eIF4E dephosphorylation. Nat. Neurosci. 6, 219-220. (Pubitemid 36278278)
14. Erwin D. H., and, Davidson E. H., (2002) The last common bilaterian ancestor. Development 129, 3021-3032. (Pubitemid 34879063)
15. Fernandez J., Yaman I., Huang C., et al. (2005) Ribosome stalling regulates IRES-mediated translation in eukaryotes, a parallel to prokaryotic attenuation. Mol. Cell 17, 405-416. (Pubitemid 40193311)
16. Gupta K. C., and, Ono E., (1997) Stimulation of Sendai virus C' protein synthesis by cycloheximide. Biochem. J. 321 (Pt 3), 811-818.
17. Hay N., and, Sonenberg N., (2004) Upstream and downstream of mTOR. Genes Dev. 18, 1926-1945. (Pubitemid 39071573)
18. Hu J. Y., Wu F., and, Schacher S., (2006) Two signaling pathways regulate the expression and secretion of a neuropeptide required for long-term facilitation in Aplysia. J. Neurosci. 26, 1026-1035. (Pubitemid 43239577)
19. Kandel E. R., (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294, 1030-1038. (Pubitemid 33041851)
20. Kanhema T., Dagestad G., Panja D., et al. (2006) Dual regulation of translation initiation and peptide chain elongation during BDNF-induced LTP in vivo: evidence for compartment-specific translation control. J. Neurochem. 99, 1328-1337. (Pubitemid 44730089)
21. Kelleher R. J. 3rd, Govindarajan A., and, Tonegawa S., (2004) Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44, 59-73. (Pubitemid 39348830)
22. Khan A., Pepio A. M., and, Sossin W. S., (2001) Serotonin activates S6 kinase in a rapamycin-sensitive manner in Aplysia synaptosomes. J. Neurosci. 21, 382-391. (Pubitemid 32107429)
23. Knebel A., Haydon C. E., Morrice N., and, Cohen P., (2002) Stress-induced regulation of eukaryotic elongation factor 2 kinase by SB 203580-sensitive and -insensitive pathways. Biochem. J. 367, 525-532. (Pubitemid 35216829)
24. Nairn A. C., Bhagat B., and, Palfrey H. C., (1985) Identification of calmodulin-dependent protein kinase III and its major Mr 100,000 substrate in mammalian tissues. Proc. Natl Acad. Sci. USA 82, 7939-7943. (Pubitemid 16169471)
25. Nakhost A., Dyer J. R., Pepio A. M., Fan X., and, Sossin W. S., (1999) Protein kinase C phosphorylated at a conserved threonine is retained in the cytoplasm. J. Biol. Chem. 274, 28944-28949.
26. Oldfield S., and, Proud C. G., (1993) Phosphorylation of elongation factor-2 from the lepidopteran insect, Spodoptera frugiperda. FEBS Lett. 327, 71-74. (Pubitemid 23216841)
27. Park S., Park J. M., Kim S., et al. (2008) Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of Arc/Arg3.1 essential for mGluR-LTD. Neuron 59, 70-83. (Pubitemid 351905855)
28. Pinkstaff J. K., Chappell S. A., Mauro V. P., Edelman G. M., and, Krushel L. A., (2001) Internal initiation of translation of five dendritically localized neuronal mRNAs. Proc. Natl Acad. Sci. USA 98, 2770-2775. (Pubitemid 32209558)
29. Ryazanov A. G., and, Davydova E. K., (1989) Mechanism of elongation factor 2 (EF-2) inactivation upon phosphorylation. Phosphorylated EF-2 is unable to catalyze translocation. FEBS Lett. 251, 187-190. (Pubitemid 19182729)
30. Ryazanov A. G., Pavur K. S., and, Dorovkov M. V., (1999) Alpha-kinases: a new class of protein kinases with a novel catalytic domain. Curr. Biol. 9, R43-R45. (Pubitemid 29083519)
31. Schalm S. S., and, Blenis J., (2002) Identification of a conserved motif required for mTOR signaling. Curr. Biol. 12, 632-639. (Pubitemid 34315846)
32. 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. (Pubitemid 30140781)
33. Shobe J. L., Zhao Y., Stough S., Ye X., Hsuan V., Martin K. C., and, Carew T. J., (2009) Temporal phases of activity-dependent plasticity and memory are mediated by compartmentalized routing of MAPK signaling in aplysia sensory neurons. Neuron 61, 113-125.
34. Smith E. M., and, Proud C. G., (2008) cdc2-cyclin B regulates eEF2 kinase activity in a cell cycle- and amino acid-dependent manner. EMBO J. 27, 1005-1016. (Pubitemid 351508149)
35. Sonenberg N., and, Hinnebusch A. G., (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136, 731-745.
36. Sossin W. S., (2003) Phosphopeptide-specific antibodies to protein kinase C. Methods Mol. Biol. 233, 233-244.
37. Sossin W. S., (2008) Molecular memory traces. Prog. Brain Res. 169, 3-25.
38. Sutton M. A., Taylor A. M., Ito H. T., Pham A., and, Schuman E. M., (2007) Postsynaptic decoding of neural activity: eEF2 as a biochemical sensor coupling miniature synaptic transmission to local protein synthesis. Neuron 55, 648-661. (Pubitemid 47223643)
39. Verpelli C., Piccoli G., Zanchi A., Gardoni F., Huang K., Brambilla D., Di Luca M., Battaglioli E., and, Sala C., (2010) Synaptic activity controls dendritic spine morphology by modulating eEF2-dependent BDNF synthesis. J. Neurosci. 30, 5830-5842.
40. Walden W. E., and, Thach R. E., (1986) Translational control of gene expression in a normal fibroblast. Characterization of a subclass of mRNAs with unusual kinetic properties. Biochemistry 25, 2033-2041. (Pubitemid 16036016)
41. Wang X., and, Proud C. G., (2009) Nutrient control of TORC1, a cell-cycle regulator. Trends Cell Biol. 19, 260-267.
42. Wang X., Li W., Williams M., Terada N., Alessi D. R., and, Proud C. G., (2001) Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase. EMBO J. 20, 4370-4379. (Pubitemid 32772031)
43. Weatherill D. B., Dyer J., and, Sossin W. S., (2010) Ribosomal protein S6 kinase is a critical downstream effector of the target of rapamycin complex 1 for long-term facilitation in Aplysia. J. Biol. Chem. 285, 12255-12267.
44. Yanow S. K., Manseau F., Hislop J., Castellucci V. F., and, Sossin W. S., (1998) Biochemical pathways by which serotonin regulates translation in the nervous system of Aplysia. J. Neurochem. 70, 572-583. (Pubitemid 28079346)
45. Ziv N. E., and, Spira M. E., (1995) Axotomy induces a transient and localized elevation of the free intracellular calcium concentration to the millimolar range. J. Neurophysiol. 74, 2625-2637. (Pubitemid 26012320)