Synaptic strength is bidirectionally controlled by opposing activity-dependent regulation of nedd4-1 and USP8

Journal of Neuroscience

Volumn 34, Issue 50, 2014, Pages 16637-16649

  Scudder, Samantha L ^a   Goo, Marisa S ^a   Cartier, Anna E ^b   Molteni, Alice ^a   Schwarz, Lindsay A ^c   Wright, Rebecca ^d   Patrick, Gentry N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ICB International Inc   (United States)

^c STANFORD UNIVERSITY   (United States)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

AMPA receptors; Deubiquitination; E3 ubiquitin ligase; Endocytosis; Lysosome; Ubiquitin

Indexed keywords

AMPA RECEPTOR; BICUCULLINE; GLYCINE; RECOMBINANT DNA; UBIQUITIN PROTEIN LIGASE NEDD4; UBIQUITIN THIOLESTERASE; ESCRT PROTEIN; NEDD4 UBIQUITIN PROTEIN LIGASES; PROTEINASE; UBIQUITIN PROTEIN LIGASE; USP8 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENZYME REGULATION; GENETIC TRANSFECTION; HIPPOCAMPAL NEURONAL CULTURE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; NERVE CELL PLASTICITY; NEWBORN; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; RAT; SYNAPTIC EFFICACY; UBIQUITINATION; WESTERN BLOTTING; ANIMAL; CELL CULTURE; FEMALE; HEK293 CELL LINE; MALE; MOUSE; PHYSIOLOGY; PROTEIN TRANSPORT; SYNAPSE;

ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; ENDOPEPTIDASES; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; FEMALE; HEK293 CELLS; HUMANS; MALE; MICE; PROTEIN TRANSPORT; RATS; SYNAPSES; UBIQUITIN THIOLESTERASE; UBIQUITIN-PROTEIN LIGASES;

EID: 84916608455     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2452-14.2014     Document Type: Article

References (41)

1. Carlin RK, Grab DJ, Cohen RS, Siekevitz P (1980) Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J Cell Biol 86:831-845. CrossRef Medline
2. Cho KO, Hunt CA, Kennedy MB (1992) The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9:929-942. CrossRef Medline
3. Davis GW (2013) Homeostatic signaling and the stabilization of neural function. Neuron 80:718-728. CrossRef Medline
4. 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. CrossRef Medline
5. Djakovic SN, Marquez-Lona EM, Jakawich SK, Wright R, Chu C, Sutton MA, Patrick GN (2012) Phosphorylation of Rpt6 regulates synaptic strength in hippocampal neurons. J Neurosci 32:5126-5131. CrossRef Medline
6. Dunn R, Klos DA, Adler AS, Hicke L (2004) The C2 domain of the Rsp5 ubiquitin ligase binds membrane phosphoinositides and directs ubiquitination of endosomal cargo. J Cell Biol 165:135-144. CrossRef Medline
7. Ehlers MD (2000) Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 28:511-525. CrossRef Medline
8. Ehlers MD (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6:231-242. CrossRef Medline
9. Fu AK, Hung KW, Fu WY, Shen C, Chen Y, Xia J, Lai KO, Ip NY (2011) APC(Cdh1) mediates EphA4-dependent downregulation of AMPA receptors in homeostatic plasticity. Nat Neurosci 14:181-189. CrossRef Medline
10. Hicke L (1997) Ubiquitin-dependent internalization and down-regulation of plasma membrane proteins. FASEB J 11:1215-1226. Medline
11. Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19: 141-172. CrossRef Medline
12. Hou Q, Gilbert J, Man HY (2011) Homeostatic regulation of AMPA receptor trafficking and degradation by light-controlled single-synaptic activation. Neuron 72:806-818. CrossRef Medline
13. Huganir RL, Nicoll RA (2013) AMPARs and synaptic plasticity: the last 25 years. Neuron 80:704-717. CrossRef Medline
14. Kowalski JR, Juo P (2012) The role of deubiquitinating enzymes in synaptic function and nervous system diseases. Neural Plast 2012:892-749. CrossRef Medline
15. Kumar S, Tomooka Y, Noda M (1992) Identification of a set of genes with developmentally down-regulated expression in the mouse brain. Biochem Biophys Res Commun 185:1155-1161. CrossRef Medline
16. Kumar S, Harvey KF, Kinoshita M, Copeland NG, Noda M, Jenkins NA (1997) cDNA cloning, expression analysis, and mapping of the mouse Nedd4 gene. Genomics 40:435-443. CrossRef Medline
17. Lee SH, Simonetta A, Sheng M (2004) Subunit rules governing the sorting of internalized AMPA receptors in hippocampal neurons. Neuron 43: 221-236. CrossRef Medline
18. Lin A, Hou Q, Jarzylo L, Amato S, Gilbert J, Shang F, Man HY (2011) Nedd4-mediated AMPA receptor ubiquitination regulates receptor turnover and trafficking. J Neurochem 119:27-39. CrossRef Medline
19. Lin JW, Ju W, Foster K, Lee SH, Ahmadian G, Wyszynski M, Wang YT, Sheng M (2000) Distinct molecular mechanisms and divergent endocytotic pathways of AMPA receptor internalization. Nat Neurosci 3:1282-1290. CrossRef Medline
20. Lu W, Roche KW (2012) Posttranslational regulation of AMPA receptor trafficking and function. Curr Opin Neurobiol 22:470-479. CrossRef Medline
21. Lussier MP, Nasu-Nishimura Y, Roche KW (2011) Activity-dependent ubiquitination of the AMPA receptor subunit GluA2. J Neurosci 31:3077-3081. CrossRef Medline
22. Mabb AM, Ehlers MD (2010) Ubiquitination in postsynaptic function and plasticity. Annu Rev Cell Dev Biol 26:179-210. CrossRef Medline
23. Mabb AM, Je HS, Wall MJ, Robinson CG, Larsen RS, Qiang Y, Corrêa SA, Ehlers MD (2014) Triad3A regulates synaptic strength by ubiquitination of Arc. Neuron 82:1299-1316. CrossRef Medline
24. Meijer IM, Kerperien J, Sotoca AM, van Zoelen EJ, van Leeuwen JE (2013) The Usp8 deubiquitination enzyme is post-translationally modified by tyrosine and serine phosphorylation. Cell Signal 25:919-930. CrossRef Medline
25. Mizuno E, Kitamura N, Komada M (2007) 14-3-3-dependent inhibition of the deubiquitinating activity of UBPY and its cancellation in the M phase. Exp Cell Res 313:3624-3634. CrossRef Medline
26. Nalefski EA, Falke JJ (1996) The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci 5:2375-2390. CrossRef Medline
27. Patrick GN (2006) Synapse formation and plasticity: recent insights from the perspective of the ubiquitin proteasome system. Curr Opin Neurobiol 16:90-94. CrossRef Medline
28. Pickart CM (2004) Back to the future with ubiquitin. Cell 116:181-190. CrossRef Medline
29. Piper RC, Luzio JP (2007) Ubiquitin-dependent sorting of integral membrane proteins for degradation in lysosomes. Curr Opin Cell Biol 19:459-465. CrossRef Medline
30. Plant PJ, Yeger H, Staub O, Howard P, Rotin D (1997) The C2 domain of the ubiquitin protein ligase Nedd4 mediates Ca2-dependent plasma membrane localization. J Biol Chem 272:32329-32336. CrossRef Medline
31. Plant PJ, Lafont F, Lecat S, Verkade P, Simons K, Rotin D (2000) Apical membrane targeting of Nedd4 is mediated by an association of its C2 domain with annexin XIIIb. J Cell Biol 149:1473-1484. CrossRef Medline
32. Pozo K, Goda Y (2010) Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66:337-351. CrossRef Medline
33. Schwarz LA, Hall BJ, Patrick GN (2010) Activity-dependent ubiquitination of GluA1 mediates a distinct AMPA receptor endocytosis and sorting pathway. J Neurosci 30:16718-16729. CrossRef Medline
34. Seeburg DP, Feliu-Mojer M, Gaiottino J, Pak DT, Sheng M (2008) Critical role of CDK5 and Polo-like kinase 2 in homeostatic synaptic plasticity during elevated activity. Neuron 58:571-583. CrossRef Medline
35. Shepherd JD, Huganir RL (2007) The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu Rev Cell Dev Biol 23:613-643. CrossRef Medline
36. Shin SM, Zhang N, Hansen J, Gerges NZ, Pak DT, Sheng M, Lee SH (2012) GKAP orchestrates activity-dependent postsynaptic protein remodeling and homeostatic scaling. Nat Neurosci 15:1655-1666. CrossRef Medline
37. Todi SV, Paulson HL (2011) Balancing act: deubiquitinating enzymes in the nervous system. Trends Neurosci 34:370-382. CrossRef Medline
38. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892-896. CrossRef Medline
39. Wang J, Peng Q, Lin Q, Childress C, Carey D, Yang W (2010) Calcium activates Nedd4 E3 ubiquitin ligases by releasing the C2 domainmediated auto-inhibition. J Biol Chem 285:12279-12288. CrossRef Medline
40. Wright MH, Berlin I, Nash PD (2011) Regulation of endocytic sorting by ESCRT-DUB-mediated deubiquitination. Cell Biochem Biophys 60:39-46. CrossRef Medline
41. Yamada T, Yang Y, Bonni A (2013) Spatial organization of ubiquitin ligase pathways orchestrates neuronal connectivity. Trends Neurosci 36:218-226. CrossRef Medline