Proteasome modulates positive and negative translational regulators in long-term synaptic plasticity

Journal of Neuroscience

Volumn 34, Issue 9, 2014, Pages 3171-3182

  Dong, Chenghai ^a   Bach, Svitlana V ^a   Haynes, Kathryn A ^a   Hegde, Ashok N ^a  

^a WAKE FOREST UNIVERSITY HEALTH SCIENCES   (United States)

Author keywords

Activator; Late phase LTP; Protein synthesis; Proteolysis; Repressor; Ubiquitin

Indexed keywords

BRAIN PROTEIN; ELONGATION FACTOR 1ALPHA; INITIATION FACTOR 4E; INITIATION FACTOR 4E BINDING PROTEIN 2; LACTONE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL KINASE; POLYADENYLIC ACID BINDING PROTEIN; PROTEASOME; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; MALE; MOLECULAR INTERACTION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS REGULATION; RADIOIMMUNOPRECIPITATION; TRANSLATION REGULATION;

ACTIVATOR; LATE-PHASE LTP; PROTEIN SYNTHESIS; PROTEOLYSIS; REPRESSOR; UBIQUITIN;

ANIMALS; ELECTRIC STIMULATION; EUKARYOTIC INITIATION FACTOR-4E; EUKARYOTIC INITIATION FACTOR-4G; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MICE; MICE, INBRED C57BL; NEURONS; PATCH-CLAMP TECHNIQUES; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEASOME INHIBITORS; SIGNAL TRANSDUCTION; SIROLIMUS; SYNAPSES; TOR SERINE-THREONINE KINASES;

EID: 84894491283     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3291-13.2014     Document Type: Article

References (50)

1. Banko JL, Poulin F, Hou L, DeMaria CT, Sonenberg N, Klann E (2005) The translation repressor 4E-BP2 is critical for eIF4F complex formation, synaptic plasticity, and memory in the hippocampus. J Neurosci 25:9581-9590. CrossRef Medline
2. Bolduc FV, Bell K, Cox H, Broadie KS, Tully T (2008) Excess protein synthesis in Drosophila fragile X mutants impairs long-term memory. Nat Neurosci 11:1143-1145. CrossRef Medline
3. Byrne JH, Baxter DA, Buonomano DV, Cleary LJ, Eskin A, Goldsmith JR, McClendon E, Nazif FA, Noel F, Scholz KP (1991) Neural and molecular bases of nonassociative and associative learning in Aplysia. Ann N Y Acad Sci 627:124-149. CrossRef Medline
4. Chain DG, Casadio A, Schacher S, Hegde AN, Valbrun M, Yamamoto N, Goldberg AL, Bartsch D, Kandel ER, Schwartz JH (1999) Mechanisms for generating the autonomous cAMP-dependent protein kinase required for long-term facilitation in Aplysia. Neuron 22:147-156. CrossRef Medline
5. Cracco JB, Serrano P, Moskowitz SI, Bergold PJ, Sacktor TC (2005) Protein synthesis-dependent LTP in isolated dendrites of CA1 pyramidal cells. Hippocampus 15:551-556. CrossRef Medline
6. Dennissen FJ, Kholod N, van Leeuwen FW (2012) The ubiquitin proteasome system in neurodegenerative diseases: culprit, accomplice or victim? Prog Neurobiol 96:190-207. CrossRef Medline
7. Dick LR, Cruikshank AA, Grenier L, Melandri FD, Nunes SL, Stein RL (1996) Mechanistic studies on the inactivation of the proteasome by lactacystin: a central role for clasto-lactacystin beta-lactone. J Biol Chem 271:7273-7276. CrossRef Medline
8. Dong C, Upadhya SC, Ding L, Smith TK, Hegde AN (2008) Proteasome inhibition enhances the induction and impairs the maintenance of latephase long-term potentiation. LearnMem15:335-347. CrossRef Medline
9. Fenteany G, Standaert RF, Lane WS, Choi S, Corey EJ, Schreiber SL (1995) Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268:726-731. CrossRef Medline
10. Fioravante D, Byrne JH (2011) Protein degradation and memory formation. Brain Res Bull 85:14-20. CrossRef Medline
11. Fonseca R, Vabulas RM, Hartl FU, Bonhoeffer T, Nägerl UV (2006) A balance of protein synthesis and proteasome-dependent degradation determines the maintenance of LTP. Neuron 52:239-245. CrossRef Medline
12. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385:533-536. CrossRef Medline
13. Frey U, Krug M, Reymann KG, MatthiesH (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. CrossRef Medline
14. Gingras AC, Raught B, Sonenberg N (1999) eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68:913-963. CrossRef Medline
15. Gkogkas CG, Khoutorsky A, Ran I, Rampakakis E, Nevarko T, Weatherill DB, Vasuta C, Yee S, Truitt M, Dallaire P, Major F, Lasko P, Ruggero D, Nader K, Lacaille JC, Sonenberg N (2013) Autism-related deficits via dysregulated eIF4E-dependent translational control. Nature 493:371-377. CrossRef Medline
16. Gobert D, Topolnik L, Azzi M, Huang L, Badeaux F, Desgroseillers L, Sossin WS, Lacaille JC (2008) Forskolin induction of late-LTP and upregulation of 5́ TOP mRNAs translation via mTOR, ERK, and PI3K in hippocampal pyramidal cells. J Neurochem 106:1160-1174. CrossRef Medline
17. Gong B, Cao Z, Zheng P, Vitolo OV, Liu S, Staniszewski A, Moolman D, Zhang H, Shelanski M, Arancio O (2006) Ubiquitin hydrolase Uch-L1 rescues beta-amyloid-induced decreases in synaptic function and contextual memory. Cell 126:775-788. CrossRef Medline
18. Hay N, Sonenberg N (2004) Upstream and downstream of mTOR. Genes Dev 18:1926-1945. CrossRef Medline
19. Hegde AN (2004) Ubiquitin-proteasome-mediated local protein degradation and synaptic plasticity. Prog Neurobiol 73:311-357. CrossRef Medline
20. Hegde AN (2010) The ubiquitin-proteasome pathway and synaptic plasticity. Learn Mem 17:314-327. CrossRef Medline
21. Hernandez PJ, Abel T (2008) The role of protein synthesis in memory consolidation: progress amid decades of debate. Neurobiol Learn Mem 89: 293-311. CrossRef Medline
22. Jarome TJ, Helmstetter FJ (2013) The ubiquitin-proteasome system as a critical regulator of synaptic plasticity and long-term memory formation. Neurobiol Learn Mem 105:107-116. CrossRef Medline
23. Kandel ER, Schwartz JH (1982) Molecular biology of learning: modulation of transmitter release. Science 218:433-443. CrossRef Medline
24. Karpova A, Mikhaylova M, Thomas U, Knöpfel T, Behnisch T (2006) Involvement of protein synthesis and degradation in long-term potentiation of Schaffer collateral CA1 synapses. J Neurosci 26:4949-4955. CrossRef Medline
25. Kelleher RJ, 3rd, Govindarajan A, Jung HY, Kang H, Tonegawa S (2004a) Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116:467-479. CrossRef Medline
26. Kelleher RJ 3rd, Govindarajan A, Tonegawa S (2004b) Translational regulatory mechanisms in persistent forms of synaptic plasticity. Neuron 44: 59-73. CrossRef Medline
27. Khaleghpour K, Kahvejian A, De Crescenzo G, Roy G, Svitkin YV, Imataka H, O'Connor-McCourt M, Sonenberg N (2001) Dual interactions of the translational repressor Paip2 with poly(A) binding protein. Mol Cell Biol 21:5200-5213. CrossRef Medline
28. Koiwai K, Maezawa S, Hayano T, Iitsuka M, Koiwai O (2008) BPOZ-2 directly binds to eEF1A1 to promote eEF1A1 ubiquitylation and degradation and prevent translation. Genes Cells 13:593-607. CrossRef Medline
29. Lantz B (2013) The impact of sample non-normality on ANOVA and alternative methods. Br J Math Stat Psychol 66:224-244. CrossRef Medline
30. McMahon R, Zaborowska I, Walsh D (2011) Noncytotoxic inhibition of viral infection through eIF4F-independent suppression of translation by 4EGi-1. J Virol 85:853-864. CrossRef Medline
31. Meyuhas O (2000) Synthesis of the translational apparatus is regulated at the translational level. Eur J Biochem 267:6321-6330. CrossRef Medline
32. Moerke NJ, Aktas H, Chen H, Cantel S, Reibarkh MY, Fahmy A, Gross JD, Degterev A, Yuan J, Chorev M, Halperin JA, Wagner G (2007) Smallmolecule inhibition of the interaction between the translation initiation factors eIF4E and eIF4G. Cell 128:257-267. CrossRef Medline
33. Murata T, Shimotohno K (2006) Ubiquitination and proteasome-dependent degradation ofhumaneukaryotic translation initiation factor 4E. J BiolChem 281:20788-20800. CrossRef Medline
34. Negrutskii BS, El'skaya AV (1998) Eukaryotic translation elongation factor 1 alpha: structure, expression, functions, and possible role in aminoacyltRNA channeling. Prog Nucleic Acid Res Mol Biol 60:47-78. Medline
35. Nguyen PV, Abel T, Kandel ER (1994) Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265:1104-1107. CrossRef Medline
36. Opazo P, Watabe AM, Grant SG, O'Dell TJ (2003) Phosphatidylinositol 3-kinase regulates the induction of long-term potentiation through extracellular signal-related kinase-independent mechanisms. J Neurosci 23: 3679-3688. Medline
37. Pause A, Belsham GJ, Gingras AC, Donzé O, Lin TA, Lawrence JC Jr, Sonenberg N (1994) Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5́-cap function. Nature 371:762-767. CrossRef Medline
38. Pestova TV, Lorsch JR, Hellen CU (2007) The mechanism of translation initiation in eukaryotes. In: Translational control in biology and medicine (Mathews M, Sonenberg N, Hershey JWB, eds), pp 87-128. Cold Spring Harbor, N. Y: Cold Spring Harbor Laboratory.
39. Santini E, Huynh TN, MacAskill AF, Carter AG, Pierre P, Ruggero D, Kaphzan H, Klann E (2013) Exaggerated translation causes synaptic and behavioural aberrations associated with autism. Nature 493:411-415. CrossRef Medline
40. Sossin WS (2008) Defining memories by their distinct molecular traces. Trends Neurosci 31:170-175. CrossRef Medline
41. Steward O, Schuman EM (2001) Protein synthesis at synaptic sites on dendrites. Annu Rev Neurosci 24:299-325. CrossRef Medline
42. Tang G, Leppla SH (1999) Proteasome activity is required for anthrax lethal toxin to kill macrophages. Infect Immun 67:3055-3060. Medline
43. Thoreen CC, Chantranupong L, Keys HR, Wang T, Gray NS, Sabatini DM (2012) A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 485:109-113. CrossRef Medline
44. Tsokas P, Ma T, Iyengar R, Landau EM, Blitzer RD (2007) Mitogenactivated protein kinase upregulates the dendritic translation machinery in long-term potentiation by controlling the mammalian target of rapamycin pathway. J Neurosci 27:5885-5894. CrossRef Medline
45. Vickers CA, Dickson KS, Wyllie DJ (2005) Induction and maintenance of late-phase long-term potentiation in isolated dendrites of rat hippocampal CA1 pyramidal neurones. J Physiol 568:803-813. CrossRef Medline
46. Wang SH, Morris RG (2010) Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu Rev Psychol 61:49-79, C1-4. CrossRef Medline
47. Woo NH, Nguyen PV (2003) Protein synthesis is required for synaptic immunity to depotentiation. J Neurosci 23:1125-1132. Medline
48. Yanagiya A, Suyama E, Adachi H, Svitkin YV, Aza-Blanc P, Imataka H, Mikami S, Martineau Y, Ronai ZA, Sonenberg N (2012) Translational homeostasis via the mRNA cap-binding protein, eIF4E. Mol Cell 46:847-858. CrossRef Medline
49. Yoshida M, Yoshida K, Kozlov G, Lim NS, De Crescenzo G, Pang Z, Berlanga JJ, Kahvejian A, Gehring K, Wing SS, SonenbergN (2006) Poly(A) binding protein (PABP) homeostasis is mediated by the stability of its inhibitor, Paip2. EMBO J 25:1934-1944. CrossRef Medline
50. Zoncu R, Efeyan A, Sabatini DM (2011) mTOR: from growth signal integration to cancer, diabetes and ageing. Nat Rev Mol Cell Biol 12:21-35. CrossRef Medline