'Silent' priming of translation-dependent LTP by β-adrenergic receptors involves phosphorylation and recruitment of AMPA receptors

Learning and Memory

Volumn 17, Issue 12, 2010, Pages 627-638

  Tenorio, Gustavo ^a   Connor, Steven A ^a   Guévremont, Diane ^b   Abraham, Wickliffe C ^b   Williams, Joanna ^b   O'Dell, Thomas J ^c   Nguyen, Peter V ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; BETA ADRENERGIC RECEPTOR; CYCLIC AMP DEPENDENT PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL SURFACE; CONTROLLED STUDY; ENZYME ACTIVATION; HIPPOCAMPUS; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ADRENERGIC BETA-AGONISTS; ADRENERGIC BETA-ANTAGONISTS; ANIMALS; BIOPHYSICS; CARBAZOLES; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; ISOPROTERENOL; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; PATCH-CLAMP TECHNIQUES; PHOSPHORYLATION; PROPRANOLOL; PYRROLES; RECEPTORS, ADRENERGIC, BETA; RECEPTORS, AMPA; SERINE;

EID: 78649574898     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.1974510     Document Type: Article

References (66)

1. Abel T, Nguyen PV, Barad M, Deuel TA, Kandel ER, Bourtchouladze R. 1997. Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88: 615-626.
2. Abraham WC. 2008. Metaplasticity - tuning synapses and networks for plasticity. Nat Rev Neurosci 9: 387-399.
3. Abraham WC, Bear MF. 1996. Metaplasticity: The plasticity of synaptic plasticity. Trends Neurosci 19: 126-130.
4. Abraham WC, Williams JM. 2008. LTP maintenance and its protein synthesis-dependence. Neurobiol Learn Mem 89: 260-268.
5. Alberini CM. 2008. The role of protein synthesis during the labile phases of memory: Revisiting the skepticism. Neurobiol Learn Mem 89: 234-246.
6. Banko JL, Hou L, Klann E. 2004. NMDA receptor activation results in PKA- and ERK-dependent Mnkl activation and increased eIF4E phosphorylation in hippocampal area CA1. J Neurochem 91: 462-470.
7. Beretta L, Gingras AC, Svitkin YV, Hall MN, Sonenberg N. 1996. Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J 15: 658-664.
8. Berridge CW, Waterhouse BD. 2003. The locus coeruleus-noradrenergic system: Modulation of behavioral state and state-dependent cognitive processes. Brain Res Rev 42: 33-84.
9. Bliss TV, Collingridge GL. 1993. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 361: 31-39.
10. Bliss TV, Lomo T. 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232: 331-356.
11. Borgdorff AJ, Choquet D. 2002. Regulation of AMPA receptor lateral movements. Nature 417: 649-653.
12. Bradshaw KD, Emptage NJ, Bliss TV. 2003. A role for dendritic protein synthesis in hippocampal late LTP. Eur J Neurosci 18: 3150-3152.
13. Christie BR, Abraham WC. 1992. Priming of associative long-term depression in the dentate gyrus by theta frequency synaptic activity. Neuron 9: 79-84.
14. Cohen AS, Abraham WC. 1996. Facilitation of long-term potentiation by prior activation of metabotropic glutamate receptors. J Neurophysiol 76: 953-962.
15. Cohen AS, Coussens CM, Raymond CR, Abraham WC. 1999. Long-lasting increase in cellular excitability associated with the priming of LTP induction in rat hippocampus. J Neurophysiol 82: 3139-3148.
16. Collingridge GL, Kehl SJ, McLennan H. 1983. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol 334: 33-46.
17. Dudai Y. 2009. Predicting not to predict too much: How the cellular machinery of memory anticipates the uncertain future. Philos Trans R Soc Lond B Biol Sci 364: 1255-1262.
18. Duvarci S, Nader K, LeDoux JE. 2005. Activation of extracellular signal-regulated kinase-mitogen-activated protein kinase cascade in the amygdala is required for memory reconsolidation of auditory fear conditioning. Eur J Neurosci 21: 283-289.
19. Frey U, Krug M, Reymann KG, Matthies H. 1988. Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res 452: 57-65.
20. Fujii S, Saito K, Miyakawa H, Ito K, Kato H. 1991. Reversal of long-term potentiation (depotentiation) induced by tetanus stimulation of the input to CA1 neurons of guinea pig hippocampal slices. Brain Res 555: 112-122.
21. Gao C, Sun X, Wolf ME. 2006. Activation of D1 dopamine receptors increases surface expression of AMPA receptors and facilitates their synaptic incorporation in cultured hippocampal neurons. J Neurochem 98: 1664-1677.
22. Gelinas JN, Nguyen PV. 2005. Beta-adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation. J Neurosci 25: 3294-3303.
23. Gelinas JN, Nguyen PV. 2007. Neuromodulation of hippocampal synaptic plasticity, learning, and memory by noradrenaline. Cent Nerv Syst Agents Med Chem 7: 17-33.
24. Gelinas JN, Banko JL, Hou L, Sonenberg N, Weeber EJ, Klann E, Nguyen PV. 2007. ERK and mTOR signaling couple beta-adrenergic receptors to translation initiation machinery to gate induction of protein synthesis-dependent long-term potentiation. J Biol Chem 282: 27527-27535.
25. Giovannini MG. 2006. The role of the extracellular signal-regulated kinase pathway in memory encoding. Rev Neurosci 17: 619-634.
26. Gobert D, Topolnik L, Azzi M, Huang L, Badeaux F, Desgroseillers L, Sossin WS, Lacaille JC. 2008. Forskolin induction of late-LTP and up-regulation of 5′ TOP mRNAs translation via mTOR, ERK, and PI3K in hippocampal pyramidal cells. J Neurochem 106: 1160-1174.
27. Hernandez PJ, Abel T. 2008. The role of protein synthesis in memory consolidation: Progress amid decades of debate. Neurobiol Learn Mem 89: 293-311.
28. Hu H, Real E, Takamiya K, Kang MG, Ledoux J, Huganir RL, Malinow R. 2007. Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell 131: 160-173.
29. Huang CC, Liang YC, Hsu KS. 1999. A role for extracellular adenosine in time-dependent reversal of long-term potentiation by low-frequency stimulation at hippocampal CA1 synapses. J Neurosci 19: 9728-9738.
30. Huang YY, Colino A, Selig DK, Malenka RC. 1992. The influence of prior synaptic activity on the induction of long-term potentiation. Science 255: 730-733.
31. Johnston D, Wu SM-S. 1995. Foundations of cellular neurophysiology. MIT Press, Cambridge, MA.
32. Kandel ER. 2001. The molecular biology of memory storage: A dialogue between genes and synapses. Science 294: 1030-1038.
33. Katsuki H, Izumi Y, Zorumski CF. 1997. Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J Neurophysiol 77: 3013-3020.
34. Kelleher RJ 3rd, Govindarajan A, Jung HY, Kang H, Tonegawa S. 2004. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116: 467-479.
35. Kelly A, Laroche S, Davis S. 2003. Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory. J Neurosci 23: 5354-5360.
36. Klann E, Antion MD, Banko JL, Hou L. 2004. Synaptic plasticity and translation initiation. Learn Mem 11: 365-372.
37. Man HY, Sekine-Aizawa Y, Huganir RL. 2007. Regulation of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit. Proc Natl Acad Sci 104: 3579-3584.
38. Mellentin C, Jahnsen H, Abraham WC. 2007. Priming of long-term potentiation mediated by ryanodine receptor activation in rat hippocampal slices. Neuropharmacology 52: 118-125.
39. Moncada D, Viola H. 2007. Induction of long-term memory by exposure to novelty requires protein synthesis: Evidence for a behavioral tagging. J Neurosci 27: 7476-7481.
40. Morris RG, Davis S, Butcher SP. 1990. Hippocampal synaptic plasticity and NMDA receptors: A role in information storage? Philos Trans R Soc Lond B Biol Sci 329: 187-204.
41. Nayak A, Zastrow DJ, Lickteig R, Zahniser NR, Browning MD. 1998. Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis. Nature 394: 680-683.
42. Nguyen PV, Kandel ER. 1996. A macromolecular synthesis-dependent late phase of long-term potentiation requiring cAMP in the medial perforant pathway of rat hippocampal slices. J Neurosci 16: 3189-3198.
43. Nguyen PV, Kandel ER. 1997. Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learn Mem 4: 230-243.
44. O'Connor JJ, Rowan MJ, Anwyl R. 1994. Long-lasting enhancement of NMDA receptor-mediated synaptic transmission by metabotropic glutamate receptor activation. Nature 367: 557-559.
45. O'Dell TJ, Kandel ER. 1994. Low-frequency stimulation erases LTP through an NMDA receptor-mediated activation of protein phosphatases. Learn Mem 1: 129-139.
46. O'Dell TJ, Connor SA, Gelinas JN, Nguyen PV. 2010. Viagra for your synapses: Enhancement of hippocampal long-term potentiation by activation of beta-adrenergic receptors. Cell Signal 22: 728-736.
47. Oh MC, Derkach VA, Guire ES, Soderling TR. 2006. Extrasynaptic membrane trafficking regulated by GluR1 serine 845 phosphorylation primes AMPA receptors for long-term potentiation. J Biol Chem 281: 752-758.
48. Panja D, Dagyte G, Bidinosti M, Wibrand K, Kristiansen AM, Sonenberg N, Bramham CR. 2009. Novel translational control in Arc-dependent long term potentiation consolidation in vivo. J Biol Chem 284: 31498-31511.
49. Pinkstaff JK, Chappell SA, Mauro VP, Edelman GM, Krushel LA. 2001. Internal initiation of translation of five dendritically localized neuronal mRNAs. Proc Natl Acad Sci 98: 2770-2775.
50. Pyronnet S, Imataka H, Gingras AC, Fukunaga R, Hunter T, Sonenberg N. 1999. Human eukaryotic translation initiation factor 4G (eIF4G) recruits Mnk1 to phosphorylate eIF4E. EMBO J 18: 270-279.
51. Raymond CR, Thompson VL, Tate WP, Abraham WC. 2000. Metabotropic glutamate receptors trigger homosynaptic protein synthesis to prolong long-term potentiation. J Neurosci 20: 969-976.
52. Routtenberg A, Rekart JL. 2005. Post-translational protein modification as the substrate for long-lasting memory. Trends Neurosci 28: 12-19.
53. Sajikumar S, Li Q, Abraham WC, Xiao ZC. 2009. Priming of short-term potentiation and synaptic tagging/capture mechanisms by ryanodine receptor activation in rat hippocampal CA1. Learn Mem 16: 178-186.
54. Staubli U, Lynch G. 1990. Stable depression of potentiated synaptic responses in the hippocampus with 1-5 Hz stimulation. Brain Res 513: 113-118.
55. Straube T, Korz V, Balschun D, Frey JU. 2003. Requirement of beta-adrenergic receptor activation and protein synthesis for LTP-reinforcement by novelty in rat dentate gyrus. J Physiol 552: 953-960.
56. Sun X, Zhao Y, Wolf ME. 2005. Dopamine receptor stimulation modulates AMPA receptor synaptic insertion in prefrontal cortex neurons. J Neurosci 25: 7342-7351.
57. Sweatt JD. 2004. Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 14: 311-317.
58. Tang SJ, Reis G, Kang H, Gingras AC, Sonenberg N, Schuman EM. 2002. A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus. Proc Natl Acad Sci 99: 467-472.
59. Tardin C, Cognet L, Bats C, Lounis B, Choquet D. 2003. Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J 22: 4656-4665.
60. Thomas MJ, Moody TD, Makhinson M, O'Dell TJ. 1996. Activity-dependent beta-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron 17: 475-482.
61. Vanhoose AM, Winder DG. 2003. NMDA and beta1-adrenergic receptors differentially signal phosphorylation of glutamate receptor type 1 in area CA1 of hippocampus. J Neurosci 23: 5827-5834.
62. Waskiewicz AJ, Johnson JC, Penn B, Mahalingam M, Kimball SR, Cooper JA. 1999. Phosphorylation of the cap-binding protein eukaryotic translation initiation factor 4E by protein kinase Mnk1 in vivo. Mol Cell Biol 19: 1871-1880.
63. Williams JM, Mason-Parker SE, Abraham WC, Tate WP. 1998. Biphasic changes in the levels of N-methyl-D-aspartate receptor-2 subunits correlate with the induction and persistence of long-term potentiation. Mol Brain Res 60: 21-27.
64. Williams JM, Guévremont D, Mason-Parker SE, Luxmanan C, Tate WP, Abraham WC. 2007. Differential trafficking of AMPA and NMDA receptors during long-term potentiation in awake adult animals. J Neurosci 27: 14171-14178.
65. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, Kandel ER. 1999. ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron 24: 715-726.
66. Woo NH, Nguyen PV. 2003. Protein synthesis is required for synaptic immunity to depotentiation. J Neurosci 23: 1125-1132.