Ubiquitin-dependent regulation of the synapse

Annual Review of Neuroscience

Volumn 27, Issue , 2004, Pages 223-246

  DiAntonio, Aaron ^a   Hicke, Linda ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Axon guidance; Proteasome; Protein degradation; Synaptic plasticity; Synaptic transmission

Indexed keywords

BINDING PROTEIN; LIGASE; UBIQUITIN;

APLYSIA; CONFORMATION; COVALENT BOND; NERVE CELL; NERVE CELL PLASTICITY; NERVE ENDING; NERVOUS SYSTEM; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN STABILITY; REVIEW; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; CENTRAL NERVOUS SYSTEM; CYSTEINE ENDOPEPTIDASES; GROWTH CONES; HUMANS; MULTIENZYME COMPLEXES; NERVE TISSUE PROTEINS; NEURAL PATHWAYS; NEURONAL PLASTICITY; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; SYNAPSES; SYNAPTIC TRANSMISSION; UBIQUITIN;

EID: 3943055513     PISSN: 0147006X     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.neuro.27.070203.144317     Document Type: Review

References (99)

1. Aravamudan B, Broadie K. 2003. Synaptic Drosophila UNC-13 is regulated by antagonistic G-protein pathways via a proteasome-dependent degradation mechanism. J. Neurobiol. 54:417-38
2. Beal R, Deveraux Q, Xia G, Rechsteiner M, Pickart C. 1996. Surface hydrophobic residues of multiubiquitin chains essential for proteolytic targeting. Proc. Natl. Acad. Sci. USA 93:861-66
3. Bedford FK, Kittler JT, Muller E, Thomas P, Uren JM, et al. 2001. GABA(A) receptor cell surface number and subunit stability are regulated by the ubiquitin-like protein Plic-1. Nat. Neurosci. 4:908-16
4. Ben-Neriah Y. 2002. Regulatory functions of ubiquitination in the immune system. Nat. Immunol. 3:20-26
5. Brittis PA, Lu Q, Flanagan JG. 2002. Axonal protein synthesis provides a mechanism for localized regulation at an intermediate target. Cell 110:223-35
6. Buchberger A. 2002. From UBA to UBX: new words in the ubiquitin vocabulary. Trends Cell Biol. 12:216-21
7. Burbea M, Dreier L, Dittman JS, Grunwald ME, Kaplan JM. 2002. Ubiquitin and AP180 regulate the abundance of GLR-1 glutamate receptors at postsynaptic elements in C. elegans. Neuron 35:107-20
8. Buttner C, Sadtler S, Leyendecker A, Laube B, Griffon N, et al. 2001. Ubiquitination precedes internalization and proteolytic cleavage of plasma membrane-bound glycine receptors. J. Biol. Chem. 276:42978-85
9. Campbell DS, Holt CE. 2001. Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32:1013-26
10. Chen X, Zhang B, Fischer JA. 2002. A specific protein substrate for a deubiquitinating enzyme: Liquid facets is the substrate of fat facets. Genes Dev. 16:289-94
11. Chin LS, Vavalle JP, Li L. 2002. Staring, a novel E3 ubiquitin-protein ligase that targets syntaxin 1 for degradation. J. Biol. Chem. 277:35071-79
12. Coscoy L, Sanchez DJ, Ganem D. 2001. A novel class of herpesvirus-encoded membrane-bound E3 ubiquitin ligases regulates endocytosis of proteins involved in immune recognition. J. Cell Biol. 155:1265-74
13. Davies BA, Topp JD, Sfeir AJ, Katzmann DJ, Carney DS, et al. 2003. Vps9p CUE domain ubiquitin binding is required for efficient endocytic protein traffic. J. Biol. Chem. 278:19826-33
14. DiAntonio A, Haghighi AP, Portman SL, Lee JD, Amaranto AM, Goodman CS. 2001. Ubiquitination-dependent mechanisms regulate synaptic growth and function. Nature 412:449-52
15. Di Fiore PP, Polo S, Hofmann K. 2003. When ubiquitin meets ubiquitin receptors: a signalling connection. Nat. Rev. Mol. Cell Biol. 4:491-97
16. Doherty P, Williams G, Williams EJ. 2000. CAMs and axonal growth: a critical evaluation of the role of calcium and the MAPK cascade. Mol. Cell Neurosci. 16:283-95
17. Dunn R, Hicke L. 2001. Multiple roles for Rsp5p-dependent ubiquitination at the internalization step of endocytosis. J. Biol. Chem. 276:25974-81
18. Ehlers MD. 2003. Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 6:231-42
19. Fisk HA, Yaffe MP. 1999. A role for ubiquitination in mitochondrial inheritance in Saccharomyces cerevisiae. J. Cell Biol. 145:1199-208
20. Galan JM, Haguenauer-Tsapis R. 1997. Ubiquitin Lys63 is involved in ubiquitination and endocytosis of a yeast plasma membrane protein. EMBO J. 16:5847-54
21. Giasson BI, Lee VM. 2003. Are ubiquitination pathways central to Parkinson's disease? Cell 114:1-8
22. Glickman MH, Ciechanover A. 2002. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82:373-428
23. Gregory RC, Taniguchi T, D'Andrea AD. 2003. Regulation of the Fanconi anemia pathway by monoubiquitination. Semin. Cancer Biol. 13:77-82
24. Guo Q, Xie J, Dang CV, Liu ET, Bishop JM. 1998. Identification of a large Myc-binding protein that contains RCC1-like repeats. Proc. Natl. Acad. Sci. USA 95:9172-77
25. Hatakeyama S, Yada M, Matsumoto M, Ishida N, Nakayama KI. 2001. U box proteins as a new family of ubiquitin-protein ligases. J. Biol. Chem. 276:33111-20
26. Hegde AN, DiAntonio A. 2002. Ubiquitin and the synapse. Nat. Rev. Neurosci. 3:854-61
27. 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 90:7436-40
28. Hegde AN, Inokuchi K, Pei W, Casadio A, Ghirardi M, et al. 1997. Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell 89:115-26
29. Helliwell SB, Losko S, Kaiser CA. 2001. Components of a ubiquitin ligase complex specify polyubiquitination and intracellular trafficking of the general amino acid permease. J. Cell Biol. 153:649-62
30. Hicke L, Dunn R. 2003. Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19:141-72
31. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S. 2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135-41
32. Huang Y, Baker RT, Fischer-Vize JA. 1995. Control of cell fate by a deubiquitinating enzyme encoded by the fat facets gene. Science 270:1828-31
33. Huber AB, Kolodkin AL, Ginty DD, Cloutier JF. 2003. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu. Rev. Neurosci. 26:509-63
34. Huibregtse JM, Scheffner M, Beaudenon S, Howley PM. 1995. A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl. Acad. Sci. USA 92:2563-67
35. Jefferis GS, Marin EC, Watts RJ, Luo L. 2002. Development of neuronal connectivity in Drosophila antennal lobes and mushroom bodies. Curr. Opin. Neurobiol. 12:80-86
36. Jiang C, Schuman EM. 2002. Regulation and function of local protein synthesis in neuronal dendrites. Trends Biochem. Sci. 27:506-13
37. Jiang YH, Armstrong D, Albrecht U, Atkins CM, Noebels JL, et al. 1998. Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation [see comments]. Neuron 21:799-811
38. Joazeiro CA, Weissman AM. 2000. RING finger proteins: mediators of ubiquitin ligase activity. Cell 102:549-52
39. Kandel ER. 2001. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030-38
40. Kantor DB, Kolodkin AL. 2003. Curbing the excesses of youth: molecular insights into axonal pruning. Neuron 38:849-52
41. Katzmann DJ, Odorizzi G, Emr SD. 2002. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3:893-905
42. Keleman K, Rajagopalan S, Cleppien D, Teis D, Paiha K, et al. 2002. Comm sorts Robo to control axon guidance at the Drosophila midline. Cell 110:415-27
43. Kidd T, Bland KS, Goodman CS. 1999. Slit is the midline repellent for the Robo receptor in Drosophila. Cell 96:785-94
44. Kidd T, Russell C, Goodman CS, Tear G. 1998. Dosage-sensitive and complementary functions of roundabout and commissureless control axon crossing of the CNS midline. Neuron 20:25-33
45. Kishino T, Lalande M, Wagstaff J. 1997. UBE3A/E6-AP mutations cause Angelman syndrome. Nat. Genet. 15:70-73
46. Klapisz E, Sorokina I, Lemeer S, Pijnenburg M, Verkleij AJ, van Bergen en Henegouwen PM. 2002. A ubiquitin-interacting motif (UIM) is essential for Eps15 and Eps15R ubiquitination. J. Biol. Chem. 277:30746-53
47. Korey CA, Van Vactor D. 2000. From the growth cone surface to the cytoskeleton: one journey, many paths. J. Neurobiol. 44:184-93
48. Liu Y, Fallon L, Lashuel HA, Liu Z, Lansbury PT Jr. 2002. The UCH-L1 gene encodes two opposing enzymatic activities that affect alpha-synuclein degradation and Parkinson's disease susceptibility. Cell 111:209-18
49. Lopez-Salon M, Alonso M, Vianna MR, Viola H, Souza TME, et al. 2001. The ubiquitin-proteasome cascade is required for mammalian long-term memory formation. Eur. J. Neurosci. 14:1820-26
50. Mack TG, Reiner M, Beirowski B, Mi W, Emanuelli M, et al. 2001. Wallerian degeneration of injured axons and synapses is delayed by a Ube4b/Nmnat chimeric gene. Nat. Neurosci. 4:1199-206
51. Malinow R, Malenka RC. 2002. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25:103-26
52. Matsuura T, Sutcliffe JS, Fang P, Galjaard RJ, Jiang YH, et al. 1997. De novo truncating mutations in E6-AP ubiquitin-protein ligase gene (UBE3A) in Angelman syndrome. Nat. Genet. 15:74-77
53. Mayer RJ, Laszlo L, Middleton A, Landon M, Hope J, Lowe J. 1992. Ubiquitin, lysosomes and neurodegenerative diseases. Biochem. Soc. Trans. 20:645-48
54. Mizuno E, Kawahata K, Kato M, Kitamura N, Komada M. 2003. STAM proteins bind ubiquitinated proteins on the early endosome via the VHS domain and ubiquitin-interacting motif. Mol. Biol. Cell 14:3675-89
55. Mizuno Y, Hattori N, Mori H, Suzuki T, Tanaka K. 2001. Parkin and Parkinson's disease. Curr. Opin. Neurol. 14:477-82
56. Moss A, Blackburn-Munro G, Garry EM, Blakemore JA, Dickinson T, et al. 2002. A role of the ubiquitin-proteasome system in neuropathic pain. J. Neurosci. 22:1363-72
57. Muralidhar MG, Thomas JB. 1993. The Drosophila bendless gene encodes a neural protein related to ubiquitin-conjugating enzymes. Neuron 11:253-66
58. Muratani M, Tansey WP. 2003. How the ubiquitin-proteasome system controls transcription. Nat. Rev. Mol. Cell Biol. 4:192-201
59. Murphey RK, Froggett SJ, Caruccio P, Shan-Crofts X, Kitamoto T, Godenschwege TA. 2003. Targeted expression of shibire ts and semaphorin 1a reveals critical periods for synapse formation in the giant fiber of Drosophila. Development 130:3671-82
60. Myat A, Henry P, McCabe V, Flintoft L, Rotin D, Tear G. 2002. Drosophila Nedd4, a ubiquitin ligase, is recruited by commissureless to control cell surface levels of the roundabout receptor. Neuron 35:447-59
61. Naze P, Vuillaume I, Destee A, Pasquier F, Sablonniere B. 2002. Mutation analysis and association studies of the ubiquitin carboxy-terminal hydrolase L1 gene in Huntington's disease. Neurosci. Lett. 328:1-4
62. Oh CE, McMahon R, Benzer S, Tanouye MA. 1994. bendless, a Drosophila gene affecting neuronal connectivity, encodes a ubiquitin-conjugating enzyme homolog. J. Neurosci. 14:3166-79
63. Oldham CE, Mohney RP, Miller SL, Hanes RN, O'Bryan JP. 2002. The ubiquitin-interacting motifs target the endocytic adaptor protein epsin for ubiquitination. Curr. Biol. 12:1112-16
64. O'Leary DD, Koester SE. 1993. Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex. Neuron 10:991-1006
65. Patrick GN, Bingol B, Weld HA, Schuman EM. 2003. Ubiquitin-mediated proteasome activity is required for agonist-induced endocytosis of GluRs. Curr. Biol. 13:2073-81
66. Peng J, Schwartz D, Elias JE, Thoreen CC, Cheng D, et al. 2003. A proteomics approach to understanding protein ubiquitination. Nat. Biotechnol. 21:921-26
67. Pickart CM. 2001. Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70:503-33
68. Polo S, Sigismund S, Faretta M, Guidi M, Capua MR, et al. 2002. A single motif responsible for ubiquitin recognition and monoubiquitination in endocytic proteins. Nature 416:451-55
69. Raiborg C, Rusten TE, Stenmark H. 2003. Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 15:446-55
70. Rotin D, Staub O, Haguenauer-Tsapis R. 2000. Ubiquitination and endocytosis of plasma membrane proteins: role of Nedd4/Rsp5p family of ubiquitin-protein ligases. J. Membr. Biol. 176:1-17
71. Saigoh K, Wang YL, Suh JG, Yamanishi T, Sakai Y, et al. 1999. Intragenic deletion in the gene encoding ubiquitin carboxy-terminal hydrolase in gad mice. Nat. Genet. 23:47-51
72. Sanes JR, Lichtman JW. 1999. Development of the vertebrate neuromuscular junction. Annu. Rev. Neurosci. 22:389-442
73. Schaefer AM, Hadwiger GD, Nonet ML. 2000. rpm-1, a conserved neuronal gene that regulates targeting and synaptogenesis in C. elegans. Neuron 26:345-56
74. Schnell JD, Hicke L. 2003. Non-traditional functions of ubiquitin and ubiquitin-binding proteins. J. Biol. Chem. 278:35857-60
75. Schwartz DC, Hochstrasser M. 2003. A superfamily of protein tags: ubiquitin, SUMO and related modifiers. Trends Biochem. Sci. 28:321-28
76. Sheng M. 2001. Molecular organization of the postsynaptic specialization. Proc. Natl. Acad. Sci. USA 98:7058-61
77. Shih SC, Katzmann KJ, Schnell JD, Sutanto M, Emr SC, Hicke LH. 2002. Epsins and Vps27/Hrs contain ubiquitin-binding domains that function in receptor endocytosis. Nat. Cell Biol. 4:389-93
78. Shih SC, Prag G, Francis SA, Sutanto MA, Hurley JH, Hicke L. 2003. A ubiquitin-binding motif required for intramolecular ubiquitylation, the CUE domain. EMBO J. 22:1273-81
79. Sloper-Mould KE, Pickart CM, Hicke L. 2001. Distinct functional surface regions on ubiquitin. J. Biol. Chem. 276:30483-89
80. Speese SD, Trotta N, Rodesch CK, Aravamudan B, Broadie K. 2003. The ubiquitin proteasome system acutely regulates presynaptic protein turnover and synaptic efficacy. Curr. Biol. 13:899-910
81. Sudol M, Hunter T. 2000. NeW wrinkles for an old domain. Cell 103:1001-4
82. Terrell J, Shih S, Dunn R, Hicke L. 1998. A function for monoubiquitination in the internalization of a G protein-coupled receptor. Mol. Cell 1:193-202
83. Thomas JB, Wyman RJ. 1984. Mutations altering synaptic connectivity between identified neurons in Drosophila. J. Neurosci. 4:530-38
84. Truman JW. 1990. Metamorphosis of the central nervous system of Drosophila. J. Neurobiol. 21:1072-84
85. Turrigiano GG. 1999. Homeostatic plasticity in neuronal networks: the more things change, the more they stay the same. Trends Neurosci. 22:221-27
86. van Kerkhof P, Govers R, Alves Dos Santos CM, Strous GJ. 2000. Endocytosis and degradation of the growth hormone receptor are proteasome-dependent. J. Biol. Chem. 275:1575-80
87. Wan HI, DiAntonio A, Fetter RD, Bergstrom K, Strauss R, Goodman CS. 2000. Highwire regulates synaptic growth in Drosophila. Neuron 26:313-29
88. Watts RJ, Hoopfer ED, Luo L. 2003. Axon pruning during Drosophila metamorphosis: evidence for local degeneration and requirement of the ubiquitin-proteasome system. Neuron 38:871-85
89. Weissman A. 2001. Themes and variations on ubiquitylation. Nat. Rev. Mol. Cell Biol. 2:169-78
90. Wendland B. 2002. Epsins: adaptors in endocytosis? Nat. Rev. Mol. Cell Biol. 3:971-77
91. West AE, Chen WG, Dalva MB, Dolmetsch RE, Kernhauser JM, et al. 2001. Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. USA 98:11024-31
92. Wheeler TC, Chin LS, Li Y, Roudabush FL, Li L. 2002. Regulation of synaptophysin degradation by mammalian homologues of seven in absentia. J. Biol. Chem. 277:10273-82
93. Wilson SM, Bhattacharyya B, Rachel RA, Coppola V, Tessarollo L, et al. 2002. Synaptic defects in ataxia mice result from a mutation in Usp14, encoding a ubiquitin-specific protease. Nat. Genet. 32:420-25
94. Wolf B, Seeger MA, Chiba A. 1998. Commissureless endocytosis is correlated with initiation of neuromuscular synaptogenesis. Development 125:3853-63
95. Yu TW, Bargmann CI. 2001. Dynamic regulation of axon guidance. Nat. Neurosci. 4(Suppl.):1169-76
96. Zhai Q, Wang J, Kim A, Liu Q, Watts R, et al. 2003. Involvement of the ubiquitin-proteasome system in the early stages of Wallerian degeneration. Neuron 39:217-25
97. Zhang LI, Poo MM. 2001. Electrical activity and development of neural circuits. Nat. Neurosci. 4(Suppl.):1207-14
98. Zhao Y, Hegde AN, Martin KC. 2003. The ubiquitin proteasome system functions as an inhibitory constraint on synaptic strengthening. Curr. Biol. 13:887-98
99. Zhen M, Huang X, Bamber B, Jin Y. 2000. Regulation of presynaptic terminal organization by C. elegans RPM-1, a putative guanine nucleotide exchanger with a RING-H2 finger domain. Neuron 26:331-43