Afferent regulation of chicken auditory brainstem neurons: Rapid changes in phosphorylation of elongation factor 2

Journal of Comparative Neurology

Volumn 521, Issue 5, 2013, Pages 1165-1183

  Mcbride, Ethan G ^a   Rubel, Edwin W ^a   Wang, Yuan ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Afferent deprivation; Apoptosis; Cell death; Cochlea removal; Nucleus magnocellularis; Protein synthesis

Indexed keywords

ELONGATION FACTOR 2;

ANIMAL TISSUE; ARTICLE; BRAIN STEM; CELL SURVIVAL; COCHLEA; CONTROLLED STUDY; IMMUNOCYTOCHEMISTRY; MAGNOCELLULAR NUCLEUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS REGULATION; RIBOSOME;

ANIMALS; ANIMALS, NEWBORN; AUDITORY PATHWAYS; BRAIN STEM; CELL LINE, TRANSFORMED; CELL SURVIVAL; CHICKENS; COCHLEA; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; NEURONS; PEPTIDE ELONGATION FACTOR 2; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; RNA; SENSORY DEPRIVATION; TIME FACTORS;

EID: 84873882073     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23227     Document Type: Article

References (94)

1. Adams KW, Cooper GM. 2007. Rapid turnover of MCL-1 couples translation to cell survival and apoptosis. J Biol Chem 282: 6192-6200.
2. Antion MD, Hou L, Wong H, Hoeffer CA, Klann E. 2008. mGluR-dependent long-term depression is associated with increased phosphorylation of S6 and synthesis of elongation factor 1a but remains expressed in S6K-deficient mice. Mol Cell Biol 28: 2996-3007.
3. Arora S, Yang J-M, Kinzy TG, Utsumi R, Okamoto T, Kitayama T, Ortiz PA, Hait WN. 2003. Identification and characterization of an inhibitor of eukaryotic elongation factor 2 kinase against human cancer cell lines. Cancer Res 63: 6894-6899.
4. Arora S, Yang J-M, Hait WN. 2005. Identification of the ubiquitin-proteasome pathway in the regulation of the stability of eukaryotic elongation factor-2 kinase. Cancer Res 65: 3806-3810.
5. Autry AE, Adachi M, Nosyreva E, Na ES, Los MF, Cheng P, Kavalali ET, Monteggia LM. 2011. NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature 475: 91-95.
6. Bagaglio DM, Cheng EHC, Gorelick FS, Mitsui K-I, Nairn AC, Hait WN. 1993. Phosphorylation of elongation factor 2 in normal and malignant rat glial cells. Cancer Res 53: 2260-2264.
7. Barrera I, Flores-Méndez M, Hernández-Kelly LC, Cid L, Huerta M, Zinker S, López-Bayghen E, Aguilera J, Ortega A. 2010. Glutamate regulates eEF1A phosphorylation and ribosomal transit time in Bergmann glial cells. Neurochem Int 57: 795-803.
8. Born DE, Rubel EW. 1985. Afferent influences on brain stem auditory nuclei of the chicken: neuron number and size following cochlea removal. J Comp Neurol 231: 435-445.
9. Born DE, Rubel EW. 1988. Afferent influences on brain stem auditory nuclei of the chicken: presynaptic action potentials regulate protein synthesis in nucleus magnocellularis neurons. J Neurosci 8: 901-919.
10. Born DE, Durham D, Rubel EW. 1991. Afferent influences on brainstem auditory nuclei of the chick: Nucleus magnocellularis neuronal activity following cochlea removal. Brain Res 557: 37-47.
11. Browne GJ, Proud CG. 2002. Regulation of peptide-chain elongation in mammalian cells. Eur J Biochem 269: 5360-5368.
12. Bush AL, Hyson RL. 2006. Lithium increases bcl-2 expression in chick cochlear nucleus and protects against deafferentation-induced cell death. Neuroscience 138: 1341-1349.
13. Carlberg U, Nilsson A, Nygård O. 1990. Functional properties of phosphorylated elongation factor 2. Eur J Biochem 191: 639-645.
14. Celis JE, Madsen P, Ryazanov AG. 1990. Increased phosphorylation of elongation factor 2 during mitosis in transformed human amnion cells correlates with a decreased rate of protein synthesis. Proc Natl Acad Sci U S A 87: 4231-4235.
15. Chen JH, Riazy M, Smith EM, Proud CG, Steinbrecher UP, Duronio V. 2009. Oxidized LDL-mediated macrophage survival involves elongation factor-2 kinase. Arterioscler Thromb Vasc 29: 92-98.
16. Chen Z, Gopalakrishnan SM, Bui M-H, Soni NB, Warrior U, Johnson EF, Donnelly JB, Glaser KB. 2011. 1-Benzyl-3-cetyl-2-methylimidazolium iodide (NH125) induces phosphorylation of eukaryotic elongation factor-2 (eEF2). J Biol Chem 286: 43951-43958.
17. Cheng EH, Gorelick FS, Czernik AJ, Bagaglio DM, Hait WN. 1995. Calmodulin-dependent protein kinases in rat glioblastoma. Cell Growth Differ 6: 615.
18. Chotiner J, Khorasani H, Nairn A, O'Dell T, Watson J. 2003. Adenylyl cyclase-dependent form of chemical long-term potentiation triggers translational regulation at the elongation step. Neuroscience 116: 743-752.
19. Clarke PG, Egloff M. 1988. Combined effects of deafferentation and de-efferentation on isthmo-optic neurons during the period of their naturally occurring cell death. Anat Embryol 179: 103-108.
20. Cossenza M, Cadilhe DV, Coutinho RN, Paes-de-Carvalho R, Cossenza M, Cadilhe DV, Coutinho RN, Paes-de-Carvalho R. 2006. Inhibition of protein synthesis by activation of NMDA receptors in cultured retinal cells: a new mechanism for the regulation of nitric oxide production. J Neurochem 97: 1481-1493.
21. Diggle TA, Redpath NT, Heesom KJ, Denton RM. 1998. Regulation of protein-synthesis elongation-factor-2 kinase by cAMP in adipocytes. Biochem J 336: 525-529.
22. Garden G, Canady K, Lurie D, Bothwell M, Rubel E. 1994. A biphasic change in ribosomal conformation during transneuronal degeneration is altered by inhibition of mitochondrial, but not cytoplasmic protein synthesis. J Neurosci 14: 1994-2008.
23. Garden GA, Hartlage-Rübsamen M, Rubel EW, Bothwell MA. 1995a. Protein masking of a ribosomal RNA epitope is an early event in afferent deprivation-induced neuronal death. Mol Cell Neurosci 6: 293-310.
24. Garden GA, Redeker-DeWulf V, Rubel EW. 1995b. Afferent influences on brainstem auditory nuclei of the chicken: regulation of transcriptional activity following cochlea removal. J Comp Neurol 359: 412-423.
25. Grange J, Belly A, Dupas S, Trembleau A, Sadoul R, Goldberg Y. 2009. Specific interaction between Sam68 and neuronal mRNAs: implication for the activity-dependent biosynthesis of elongation factor eEF1A. J Neurosci Res 87: 12-25.
26. 2+/calmodulin-dependent processes such as phosphorylation of elongation factor 2. Skin Pharmacol 1: 84-92.
27. Gschwendt M, Kittstein W, Mieskes G, Marks F. 1989. A type 2A protein phosphatase dephosphorylates the elongation factor 2 and is stimulated by the phorbol ester TPA in mouse epidermis in vivo. FEBS Lett 257: 357-360.
28. Guillery RW. 1973. Quantitative studies of transneuronal atrophy in the dorsal lateral geniculate nucleus of cats and kittens. J Comp Neurol 149: 423-437.
29. Harris JA, Iguchi F, Seidl AH, Lurie DI, Rubel EW. 2008. Afferent deprivation elicits a transcriptional response associated with neuronal survival after a critical period in the mouse cochlear nucleus. J Neurosci 28: 10990-11002.
30. Hartlage-Rübsamen M, Rubel EW. 1996. Influence of mitochondrial protein synthesis inhibition on deafferentation-induced ultrastructural changes in nucleus magnocellularis of developing chicks. J Comp Neurol 371: 448-460.
31. Hashisaki GT, Rubel EW. 1989. Effects of unilateral cochlea removal on anteroventral cochlear nucleus neurons in developing gerbils. J Comp Neurol 283: 5-73.
32. Heil P, Scheich H. 1986. Effects of unilateral and bilateral cochlea removal on 2-deoxyglucose patterns in the chick auditory system. J Comp Neurol 252: 279-301.
33. Hernández G, Altmann M, Lasko P. 2010. Origins and evolution of the mechanisms regulating translation initiation in eukaryotes. Trends Biochem Sci 35: 63-73.
34. Hong-Brown LQ, Brown CR, Huber DS, Lang CH. 2007. Alcohol regulates eukaryotic elongation factor 2 phosphorylation via an AMP-activated protein kinase-dependent mechanism in C2C12 skeletal myocytes. J Biol Chem 282: 3702-3712.
35. Horman S, Browne GJ, Krause U, Patel JV, Vertommen D, Bertrand L, Lavoinne A, Hue L, Proud CG, Rider MH. 2002. Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr Biol 12: 1419-1423.
36. Hyson RL, Rubel EW. 1995. Activity-dependent regulation of a ribosomal RNA epitope in the chick cochlear nucleus. Brain Res 672: 196-204.
37. Iizuka A, Sengoku K, Iketani M, Nakamura F, Sato Y, Matsushita M, Nairn AC, Takamatsu K, Goshima Y, Takei K. 2007. Calcium-induced synergistic inhibition of a translational factor eEF2 in nerve growth cones. Biochem Biophys Res Commun 353: 244-250.
38. Jackson RJ, Hellen CUT, Pestova TV. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Bio 11: 113-127.
39. Jørgensen R, Merrill AR, Andersen GR. 2006. The life and death of translation elongation factor 2. Biochem Soc Trans 34: 1-6.
40. Kalil R. 1980. A quantitative study of the effects of monocular enucleation and deprivation on cell growth in the dorsal lateral geniculate nucleus of the cat. J Comp Neurol 189: 483-524.
41. Kanhema T, Dagestad G, Panja D, Tiron A, Messaoudi E, Håvik B, Ying S, Nairn AC, Sonenberg N, Bramham CR, 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.
42. Karnes HE, Kaiser CL, Durham D. 2009. Deafferentation-induced caspase-3 activation and DNA fragmentation in chick cochlear nucleus neurons. Neuroscience 159: 804-818.
43. Karnes HE, Scaletty PN, Durham D. 2010. Histochemical and fluorescent analyses of mitochondrial integrity in chick auditory neurons following deafferentation. J Am Acad Audiol 21: 204-218.
44. Kaul G, Pattan G, Rafeequi T. 2011. Eukaryotic elongation factor-2 (eEF2): its regulation and peptide chain elongation. Cell Biochem Funct 29: 227-234.
45. Kim HK, Kim Y-B, Kim E-G, Schuman E. 2005. Measurement of dendritic mRNA transport using ribosomal markers. Biochem Biophys Res Commun 328: 895-900.
46. Kuipers SD, Tiron A, Soule J, Messaoudi E, Trentani A, Bramham CR. 2009. Selective survival and maturation of adult-born dentate granule cells expressing the immediate early gene Arc/Arg3.1. PLoS ONE 4: 1-12.
47. Lenz G, Avruch J. 2005. Glutamatergic regulation of the p70S6 kinase in primary mouse neurons. J Biol Chem 280: 38121-38124.
48. Lerner EA, Lerner MR, Janeway CA, Steitz JA. 1981. Monoclonal antibodies to nucleic acid-containing cellular constituents: probes for molecular biology and autoimmune disease. Proc Natl Acad Sci U S A 78: 2737-2741.
49. Lurie DI, Rubel EW. 1994. Astrocyte proliferation in the chick auditory brainstem following cochlea removal. J Comp Neurol 346: 276-288.
50. Marin P, Nastiuk KL, Daniel N, Girault J-A, Czernik AJ, Glowinski J, Nairn AC, Prémont J. 1997. Glutamate-dependent phosphorylation of elongation factor-2 and inhibition of protein synthesis in neurons. J Neurosci 17: 3445-3454.
51. Mitsui K, Brady M, Palfrey HC, Nairn AC. 1993. Purification and characterization of calmodulin-dependent protein kinase III from rabbit reticulocytes and rat pancreas. J Biol Chem 268: 13422-13433.
52. Moore DR. 1990. Auditory brainstem of the ferret: early cessation of developmental sensitivity of neurons in the cochlear nucleus to removal of the cochlea. J Comp Neurol 302: 810-823.
53. Mostafapour SP, Cochran SL, Del Puerto NM, Rubel EW. 2000. Patterns of cell death in mouse anteroventral cochlear nucleus neurons after unilateral cochlea removal. J Comp Neurol 426: 561-571.
54. Mostafapour SP, Del Puerto NM, Rubel EW. 2002. Bcl-2 overexpression eliminates deprivation-induced cell death of brainstem auditory neurons. J Neurosci 22: 4670-4674.
55. Nairn AC, Palfrey HC. 1987. Identification of the major Mr 100, 000 substrate for calmodulin-dependent protein kinase III in mammalian cells as elongation factor-2. J Biol Chem 262: 17299-17303.
56. Nakamoto T. 2009. Evolution and the universality of the mechanism of initiation of protein synthesis. Gene 432: 1-6.
57. Nakamura J, Aoyagi S, Nanchi I, Nakatsuka S-I, Hirata E, Shibata S, Fukuda M, Yamamoto Y, Fukuda I, Tatsumi N, et al. 2009. Overexpression of eukaryotic elongation factor eEF2 in gastrointestinal cancers and its involvement in G2/M progression in the cell cycle. Int J Oncol 34: 1181-1189.
58. Nosyreva E, Kavalali ET. 2010. Activity-dependent augmentation of spontaneous neurotransmission during endoplasmic reticulum stress. J Neurosci 30: 7358-7368.
59. Park S, Park JM, Kim S, Kim J-A, Shepherd JD, Smith-Hicks CL, Chowdhury S, Kaufmann W, Kuhl D, Ryazanov AG, 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.
60. Parmer TG, Ward MD, Yurkow EJ, Vyas VH, Kearney TJ, Hait WN. 1999. Activity and regulation by growth factors of calmodulin-dependent protein kinase III (elongation factor 2-kinase) in human breast cancer. Br J Cancer 79: 59-64.
61. Piccoli G, Verpelli C, Tonna N, Romorini S, Alessio M, Nairn AC, Bachi A, Sala C. 2007. Proteomic analysis of activity-dependent synaptic plasticity in hippocampal neurons. J Proteome Res 6: 3203-3215.
62. Redpath NT, Proud CG. 1993. Cyclic AMP-dependent protein kinase phosphorylates rabbit reticulocyte elongation factor-2 kinase and induces calcium-independent activity. Biochem J 293: 31-34.
63. Redpath NT, Price NT, Severinov KV, Proud CG. 1993. Regulation of elongation factor-2 by multisite phosphorylation. Eur J Biochem 213: 689-699.
64. Redpath NT, Foulstone EJ, Proud CG. 1996. Regulation of translation elongation factor-2 by insulin via a rapamycin-sensitive signalling pathway. EMBO J 15: 2291-2297.
65. Robinson AM, Conley D, Kern R. 2003. Olfactory neurons in bax knockout mice are protected from bulbectomy-induced apoptosis. Neuroreport 14: 1891-1894.
66. Rubel EW, Fritzsch B. 2002. Auditory system development: primary auditory neurons and their targets. Annu Rev Neurosci 25: 51-101.
67. Ryazanov AG, Shestakova EA, Natapov PG. 1988. Phosphorylation of elongation factor 2 by EF-2 kinase affects rate of translation. Nature 334: 170-173.
68. Scheetz AJ, Nairn AC, Constantine-Paton M. 1997. N-methyl-D-aspartate receptor activation and visual activity induce elongation factor-2 phosphorylation in amphibian tecta: a role for N-methyl-D-aspartate receptors in controlling protein synthesis. Proc Natl Acad Sci U S A 94: 14770-14775.
69. Scheetz AJ, Nairn AC, Constantine-Paton M. 2000. NMDA receptor-mediated control of protein synthesis at developing synapses. Nat Neurosci 3: 211-216.
70. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136: 731-745.
71. Steward O, Rubel EW. 1985. Afferent influences on brain stem auditory nuclei of the chicken: cessation of amino acid incorporation as an antecedent to age-dependent transneuronal degeneration. J Comp Neurol 231: 385-395.
72. Sutton MA, Wall NR, Aakalu GN, Schuman EM. 2004. Regulation of dendritic protein synthesis by miniature synaptic events. Science 304: 1979-1983.
73. Sutton MA, Ito HT, Cressy P, Kempf C, Woo JC, Schuman EM. 2006. Miniature neurotransmission stabilizes synaptic function via tonic suppression of local dendritic protein synthesis. Cell 125: 785-799.
74. Sutton MA, Taylor AM, Ito HT, Pham A, Schuman EM. 2007. Postsynaptic decoding of neural activity: eEF2 as a biochemical sensor coupling miniature synaptic transmission to local protein synthesis. Neuron 55: 648-661.
75. Terada N, Patel HR, Takase K, Kohno K, Nairn AC, Gelfand EW. 1994. Rapamycin selectively inhibits translation of mRNAs encoding elongation factors and ribosomal proteins. Proc Natl Acad Sci U S A 91: 11477.
76. Tierney TS, Russell FA, Moore DR. 1997. Susceptibility of developing cochlear nucleus neurons to deafferentation-induced death abruptly ends just before the onset of hearing. J Comp Neurol 378: 295-306.
77. Trune DR. 1982. Influence of neonatal cochlea removal on the development of mouse cochlear nucleus: I. Number, size, and density of its neurons. J Comp Neurol 209: 409-424.
78. Vankirk AM, Byrd CA. 2003. Apoptosis following peripheral sensory deafferentation in the olfactory bulb of adult zebrafish. J Comp Neurol 455: 488-498.
79. Verpelli C, Piccoli G, Zibetti C, Zanchi A, Gardoni F, Huang K, Brambilla D, Di Luca M, Battaglioli E, Sala C. 2010. Synaptic activity controls dendritic spine morphology by modulating eEF2-dependent BDNF synthesis. J Neurosci 30: 5830-5842.
80. Wang L, Wang X, Proud CG. 2000. Activation of mRNA translation in rat cardiac myocytes by insulin involves multiple rapamycin-sensitive steps. Am J Physiol Heart Circ Physiol 278: H1056-H1068.
81. Wang Y, Rubel EW. 2008. Rapid regulation of microtubule-associated protein 2 in dendrites of nucleus laminaris of the chick following deprivation of afferent activity. Neuroscience 154: 381-389.
82. Wang Y, Cunningham DE, Tempel BL, Rubel EW. 2009. Compartment-specific regulation of plasma membrane calcium ATPase type 2 in the chick auditory brainstem. J Comp Neurol 514: 624-640.
83. Weatherill DB, McCamphill PK, Pethoukov E, Dunn TW, Fan X, Sossin WS. 2011. Compartment-specific, differential regulation of eukaryotic elongation factor 2 and its kinase within Aplysia sensory neurons. J Neurochem 117: 841-855.
84. White-Gilbertson S, Rubinchik S, Voelkel-Johnson C. 2008. Transformation, translation and TRAIL: an unexpected intersection. Cytokine Growth Factor Res 19: 167-172.
85. Wilkinson BL, Sadler KA, Hyson RL. 2002. Rapid deafferentation-induced upregulation of bcl-2 mRNA in the chick cochlear nucleus. Brain Res Mol Brain Res 99: 67-74.
86. Wilkinson B, Elam J, Fadool D, Hyson R. 2003. Afferent regulation of cytochrome-c and active caspase-9 in the avian cochlear nucleus. Neuroscience 120: 1071-1079.
87. Willis SN, Fletcher JI, Kaufmann T, Van Delft MF, Chen L, Czabotar PE, Ierino H, Lee EF, Fairlie WD, Bouillet P, et al. 2007. Apoptosis initiated when BH3 ligands engage multiple Bcl-2 homologs, not Bax or Bak. Science 315: 856-859.
88. Wu H, Yang J-M, Jin S, Zhang H, Hait WN. 2006. Elongation factor-2 kinase regulates autophagy in human glioblastoma cells. Cancer Res 66: 3015-3023.
89. Yamaguchi S, Fujii-Taira I, Murakami A, Hirose N, Aoki N, Izawa E-I, Fujimoto Y, Takano T, Matsushima T, Homma KJ. 2008. Up-regulation of microtubule-associated protein 2 accompanying the filial imprinting of domestic chicks (Gallus gallus domesticus). Brain Res Bull 76: 282-288.
90. Yamaguchi S, Katagiri S, Aoki N, Iikubo E, Kitajima T, Matsushima T, Homma KJ. 2011. Molecular function of microtubule-associated protein 2 for filial imprinting in domestic chicks (Gallus gallus domesticus). Neurosci Res 69: 32-40.
91. Zhang Y, Cheng Y, Zhang L, Ren X, Huber-Keener KJ, Lee S, Yun J, Wang HG, Yang JM. 2011. Inhibition of eEF-2 kinase sensitizes human glioma cells to TRAIL and down-regulates Bcl-xL expression. Biochem Biophys Res Commun 414: 129-134.
92. Zirpel L, Rubel EW. 1996. Eighth nerve activity regulates intracellular calcium concentration of avian cochlear nucleus neurons via a metabotropic glutamate receptor. J Neurophysiol 76: 4127-4139.
93. Zirpel L, Lachica EA, Lippe WR. 1995a. Deafferentation increases the intracellular calcium of cochlear nucleus neurons in the embryonic chick. J Neurophysiol 74: 1355-1357.
94. Zirpel L, Lachica EA, Rubel EW. 1995b. Activation of a metabotropic glutamate receptor increases intracellular calcium concentrations in neurons of the avian cochlear nucleus. J Neurosci 15: 214-222.