Protein homeostasis and synaptic plasticity

EMBO Journal

Volumn 29, Issue 16, 2010, Pages 2746-2752

  Cajigas, Iván J ^a   Will, Tristan ^a   Schuman, Erin M ^a  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

Author keywords

local protein degradation; local translation; mRNA localization; neuron; synaptic strength

Indexed keywords

MESSENGER RNA; NERVE PROTEIN;

EXPERIMENTAL STUDY; HIPPOCAMPUS; HOMEOSTASIS; LONG TERM DEPRESSION; NERVE CELL PLASTICITY; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; RNA TRANSLATION; ANIMAL; HUMAN; METABOLISM; NERVE CELL; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; HUMANS; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NEURONS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 77955790177     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.173     Document Type: Review

References (75)

1. Andreassi C, Riccio A (2009) To localize or not to localize: mRNA fate is in 3UTR ends. Trends Cell Biol 19: 465-474
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. Banerjee S, Neveu P, Kosik KS (2009) A coordinated local transla-tional control point at the synapse involving relief from silencing and MOV10 degradation. Neuron 64: 871-884
4. Banko JL, Hou L, Poulin F, Sonenberg N, Klann E (2006) Regulation of eukaryotic initiation factor 4E by converging signaling pathways during metabotropic glutamate receptor-dependent long-term depression. J Neurosci 26: 2167-2173
5. Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM (1998) Localization of ASH1 mRNA particles in living yeast. Mol Cell 2: 437-445
6. Bingol B, Schuman EM (2006) Activity-dependent dynamics and sequestration of proteasomes in dendritic spines. Nature 441: 1144-1148
7. Bingol B, Wang CF, Arnott D, Cheng D, Peng J, Sheng M (2010) Autophosphorylated CaMKIIalpha acts as a scaffold to recruit proteasomes to dendritic spines. Cell 140: 567-578
8. Blichenberg A, Rehbein M, Muller R, Garner CC, Richter D, Kindler S (2001) Identification of a cis-acting dendritic targeting element in the mRNA encoding the alpha subunit of Ca2+/calmodulin-dependent protein kinase II. Eur J Neurosci 13: 1881-1888
9. Bodian D (1965) A suggestive relationship of nerve cell Rna with specific synaptic sites. Proc Natl Acad Sci USA 53: 418-425
10. Bramham CR, Wells DG (2007) Dendritic mRNA: transport, translation and function. Nat Rev Neurosci 8: 776-789
11. Cannon WB (1932) The Wisdom of the Body. Vo l. W. W.: New York
12. Chowdhury S, Shepherd JD, Okuno H, Lyford G, Petralia RS, Plath N, Kuhl D, Huganir RL, Worley PF (2006) Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 52: 445-459
13. Colledge M, Snyder EM, Crozier RA, Soderling JA, Jin Y, Langeberg LK, Lu H, Bear MF, Scott JD (2003) Ubiquitination regulates PSD-95 degradation and AMPA receptor surface expression. Neuron 40: 595-607
14. Costa-Mattioli M, Gobert D, Harding H, Herdy B, Azzi M, Bruno M, Bidinosti M, Ben Mamou C, Marcinkiewicz E, Yoshida M, Imataka H, Cuello AC, Seidah N, Sossin W, Lacaille JC, Ron D, Nader K, Sonenberg N (2005) Translational control of hippocampal synap-tic plasticity and memory by the eIF2alpha kinase GCN2. Nature 436: 1166-1173
15. 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
16. Djagaeva I, Doronkin S (2009) Dual regulation of dendritic morphogenesis in Drosophila by the COP9 signalosome. PLoS One 4: e7577
17. Djakovic SN, Schwarz LA, Barylko B, DeMartino GN, Patrick GN (2009) Regulation of the proteasome by neuronal activity and calcium/calmodulin- dependent protein kinase II. J Biol Chem 284: 26655-26665
18. Dong C, Upadhya SC, Ding L, Smith TK, Hegde AN (2008) Proteasome inhibition enhances the induction and impairs the maintenance of late-phase long-term potentiation. Learn Mem 15: 335-347
19. Ehlers MD (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6: 231-242
20. Elsea SH, Mykytyn K, Ferrell K, Coulter KL, Das P, Dubiel W, Patel PI, Metherall JE (1999) Hemizygosity for the COP9 signalosome subunit gene, SGN3, in the Smith-Magenis syndrome. Am J Med Genet 87: 342-348
21. Eom T, Antar LN, Singer RH, Bassell GJ (2003) Localization of a beta-actin messenger ribonucleoprotein complex with zipcode-binding protein modulates the density of dendritic filopodia and filopodial synapses. J Neurosci 23: 10433-10444
22. Evans T, Rosenthal ET, Youngblom J, Distel D, Hunt T (1983) Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell 33: 389-396
23. Fatt P, Katz B (1952) Spontaneous subthreshold activity at motor nerve endings. J Physiol 117: 109-128
24. Flexner JB, Flexner LB, Stellar E (1963) Memory in mice as affected by intracerebral puromycin. Science 141: 57-59
25. Fonseca R, Vabulas RM, Hartl FU, Bonhoeffer T, Nagerl UV (2006) A balance of protein synthesis and proteasome-dependent degradation determines the maintenance of LTP. Neuron 52: 239-245
26. Frey U, Morris RG (1997) Synaptic tagging and long-term potentia-tion. Nature 385: 533-536
27. Greer PL, Hanayama R, Bloodgood BL, Mardinly AR, Lipton DM, Flavell SW, Kim TK, Griffith EC, Waldon Z, Maehr R, Ploegh HL, Chowdhury S, Worley PF, Steen J, Greenberg ME (2010) The Angelman syndrome protein Ube3A regulates synapse development by ubiquitinating arc. Cell 140: 704-716
28. Grooms SY, Noh KM, Regis R, Bassell GJ, Bryan MK, Carroll RC, Zukin RS (2006) Activity bidirectionally regulates AMPA receptor mRNA abundance in dendrites of hippocampal neurons. J Neurosci 26: 8339-8351
29. Hegde AN, Goldberg AL, Schwartz JH (1993) Regulatory subunits of cAMP-dependent protein kinases are degraded after conjugation to ubiquitin: a molecular mechanism underlying long-term synaptic plasticity. Proc Natl Acad Sci USA 90: 7436-7440
30. Hershkowitz M, Wilson JE, Glassman E (1975) The incorporation of radioactive amino acids into brain subcellular proteins during training. J Neurochem 25: 687-694
31. Hou L, Antion MD, Hu D, Spencer CM, Paylor R, Klann E (2006) Dynamic translational and proteasomal regulation of fragile X mental retardation protein controls mGluR-dependent long-term depression. Neuron 51: 441-454
32. Huang YY, Kandel ER (2005) Theta frequency stimulation induces a local form of late phase LTP in the CA1 region of the hippocampus. Learn Mem 12: 587-593
33. Huber KM, Kayser MS, Bear MF (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288: 1254-1257
34. Huttelmaier S, Zenklusen D, Lederer M, Dictenberg J, Lorenz M, Meng X, Bassell GJ, Condeelis J, Singer RH (2005) Spatial regulation of beta-actin translation by Src-dependent phospho-rylation of ZBP1. Nature 438: 512-515
35. Johnson CH, Roeber JF, Hastings JW (1984) Circadian changes in enzyme concentration account for rhythm of enzyme activity in gonyaulax. Science 223: 1428-1430
36. Johnstone O, Lasko P (2001) Translational regulation and RNA localization in Drosophila oocytes and embryos. Annu Rev Genet 35: 365-406
37. Kacharmina JE, Job C, Crino P, Eberwine J (2000) Stimulation of glutamate receptor protein synthesis and membrane insertion within isolated neuronal dendrites. Proc Natl Acad Sci USA 97: 11545-11550
38. Kang H, Schuman EM (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273: 1402-1406
39. Karpova A, Mikhaylova M, Thomas U, Knopfel T, Behnisch T (2006) Involvement of protein synthesis and degradation in long-term potentiation of Schaffer collateral CA1 synapses. J Neurosci 26: 4949-4955
40. Kelleher III RJ, 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
41. Krug M, Lossner B, Ott T (1984) Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res Bull 13: 39-42
42. Laggerbauer B, Ostareck D, Keidel EM, Ostareck-Lederer A, Fischer U (2001) Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum Mol Genet 10: 329-338
43. Li Z, Zhang Y, Ku L, Wilkinson KD, Warren ST, Feng Y (2001) The fragile X mental retardation protein inhibits translation via interacting with mRNA. Nucleic Acids Res 29: 2276-2283
44. Lin AC, Holt CE (2007) Local translation and directional steering in axons. EMBO J 26: 3729-3736
45. Linden DJ (1996) A protein synthesis-dependent late phase of cerebellar long-term depression. Neuron 17: 483-490
46. Long RM, Singer RH, Meng X, Gonzalez I, Nasmyth K, Jansen RP (1997) Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 277: 383-387
47. Lopez-Salon M, Alonso M, Vianna MR, Viola H, Mello e Souza T, Izquierdo I, Pasquini JM, Medina JH (2001) The ubiquitin-protea-some cascade is required for mammalian long-term memory formation. Eur J Neurosci 14: 1820-1826
48. Luke-Glaser S, Roy M, Larsen B, Le Bihan T, Metalnikov P, Tyers M, Peter M, Pintard L (2007) CIF-1, a shared subunit of the COP9/signalosome and eukaryotic initiation factor 3 complexes, regulates MEL-26 levels in the Caenorhabditis elegans embryo. Mol Cell Biol 27: 4526-4540
49. Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, Chen M, Bailey CH, Kandel ER (1997) Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91: 927-938
50. Martin KC, Ephrussi A (2009) mRNA localization: gene expression in the spatial dimension. Cell 136: 719-730
51. Meister G, Landthaler M, Peters L, Chen PY, Urlaub H, Luhrmann R, Tuschl T (2005) Identification of novel argonaute-associated proteins. Curr Biol 15: 2149-2155
52. Miller S, Yasuda M, Coats JK, Jones Y, Martone ME, Mayford M (2002) Disruption of dendritic translation of CaMKIIalpha impairs stabilization of synaptic plasticity and memory consolidation. Neuron 36: 507-519
53. Minshull J, Pines J, Golsteyn R, Standart N, Mackie S, Colman A, Blow J, Ruderman JV, Wu M, Hunt T (1989) The role of cyclin synthesis, modification and destruction in the control of cell division. J Cell Sci Suppl 12: 77-97
54. Mori Y, Imaizumi K, Katayama T, Yoneda T, Tohyama M (2000) Two cis-acting elements in the 3 untranslated region of alpha-CaMKII regulate its dendritic targeting. Nat Neurosci 3: 1079-1084
55. Park S, Park JM, Kim S, Kim JA, Shepherd JD, Smith-Hicks CL, Chowdhury S, Kaufmann W, Kuhl D, Ryazanov AG, Huganir RL, Linden DJ, Worley PF (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
56. Patrick GN, Bingol B, Weld HA, Schuman EM (2003) Ubiquitin-mediated proteasome activity is required for agonist-induced endocytosis of GluRs. Curr Biol 13: 2073-2081
57. Princiotta MF, Finzi D, Qian SB, Gibbs J, Schuchmann S, Buttgereit F, Bennink JR, Yewdell JW (2003) Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity 18: 343-354
58. Rial Verde EM, Lee-Osbourne J, Worley PF, Malinow R, Cline HT (2006) Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission. Neuron 52: 461-474
59. Rock KL, Goldberg AL (1999) Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu Rev Immunol 17: 739-779
60. Sajikumar S, Navakkode S, Sacktor TC, Frey JU (2005) Synaptic tagging and cross-tagging: the role of protein kinase Mzeta in maintaining long-term potentiation but not long-term depression. J Neurosci 25: 5750-5756
61. Schubert U, Anton LC, Gibbs J, Norbury CC, Yewdell JW, Bennink JR (2000) Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature 404: 770-774
62. Sha Z, Brill LM, Cabrera R, Kleifeld O, Scheliga JS, Glickman MH, Chang EC, Wolf DA (2009) The eIF3 interactome reveals the translasome, a supercomplex linking protein synthesis and degradation machineries. Mol Cell 36: 141-152
63. Shashoua VE (1976) Identification of specific changes in the pattern of brain protein synthesis after training. Science 193: 1264-1266
64. Smith WB, Starck SR, Roberts RW, Schuman EM (2005) Dopaminergic stimulation of local protein synthesis enhances surface expression of GluR1 and synaptic transmission in hippocampal neurons. Neuron 45: 765-779
65. Stanton PK, Sarvey JM (1984) Blockade of long-term potentiation in rat hippocampal CA1 region by inhibitors of protein synthesis. J Neurosci 4: 3080-3088
66. Steward O, Levy WB (1982) Preferential localization of polyribo-somes under the base of dendritic spines in granule cells of the dentate gyrus. J Neurosci 2: 284-291
67. 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
68. Sutton MA, Wall NR, Aakalu GN, Schuman EM (2004) Regulation of dendritic protein synthesis by miniature synaptic events. Science 304: 1979-1983
69. Tarpey PS, Raymond FL, O'Meara S, Edkins S, Teague J, Butler A, Dicks E, Stevens C, Tofts C, Avis T, Barthorpe S, Buck G, Cole J, Gray K, Halliday K, Harrison R, Hills K, Jenkinson A, Jones D, Menzies A et al (2007) Mutations in CUL4B, which encodes a ubiquitin E3 ligase subunit, cause an X-linked mental retardation syndrome associated with aggressive outbursts, seizures, relative macrocephaly, central obesity, hypogonadism, pes cavus, and tremor. Am J Hum Genet 80: 345-352
70. Tiruchinapalli DM, Oleynikov Y, Kelic S, Shenoy SM, Hartley A, Stanton PK, Singer RH, Bassell GJ (2003) Activity-dependent trafficking and dynamic localization of zipcode binding protein 1 and beta-actin mRNA in dendrites and spines of hippocampal neurons. J Neurosci 23: 3251-3261
71. 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(Part 3): 803-813
72. Wang DO, Kim SM, Zhao Y, Hwang H, Miura SK, Sossin WS, Martin KC (2009) Synapse-and stimulus-specific local translation during long-term neuronal plasticity. Science 324: 1536-1540
73. Waung MW, Pfeiffer BE, Nosyreva ED, Ronesi JA, Huber KM (2008) Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocy-tosis rate. Neuron 59: 84-97
74. Zhang HL, Eom T, Oleynikov Y, Shenoy SM, Liebelt DA, Dictenberg JB, Singer RH, Bassell GJ (2001) Neurotrophin-induced transport of a beta-actin mRNP complex increases beta-actin levels and stimulates growth cone motility. Neuron 31: 261-275
75. Zou Y, Liu Q, Chen B, Zhang X, Guo C, Zhou H, Li J, Gao G, Guo Y, Yan C, Wei J, Shao C, Gong Y (2007) Mutation in CUL4B, which encodes a member of cullin-RING ubiquitin ligase complex, causes X-linked mental retardation. Am J Hum Genet 80: 561-566