Regulation of the neuronal proteasome by Zif268 (Egr1)

Journal of Neuroscience

Volumn 26, Issue 5, 2006, Pages 1624-1634

  James, Allan B ^a   Conway, Ann Marie ^a   Morris, Brian J ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

26S proteasome; Egr 1; Immunoproteasome; Lmp2; Plasticity; Proteasome activity

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; HALOPERIDOL; PROTEASOME;

ANIMAL TISSUE; ARTICLE; BINDING SITE; BIOINFORMATICS; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME ACTIVITY; ENZYME SUBUNIT; GENE EXPRESSION REGULATION; GENE INDUCTION; GENETIC TRANSFECTION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RAT; REPORTER GENE; TRANSCRIPTION INITIATION SITE;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; CEREBRAL CORTEX; COMPUTATIONAL BIOLOGY; CYSTEINE ENDOPEPTIDASES; EARLY GROWTH RESPONSE PROTEIN 1; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; IMMEDIATE-EARLY PROTEINS; LONG-TERM POTENTIATION; MALE; MICE; MICE, KNOCKOUT; NEURONS; PC12 CELLS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SUBUNITS; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, WISTAR; TRANS-ACTIVATION (GENETICS);

EID: 32544446276     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4199-05.2006     Document Type: Article

References (101)

1. Bahouth SW, Beauchamp MJ, Vu KN (2002) Reciprocal regulation of beta 1-adrenergic receptor gene transcription by Sp1 and early growth response gene 1: induction of EGR-1 inhibits the expression of the beta 1-adrenergic receptor gene. Mol Pharmacol 61:379-390.
2. Becker AJ, Chen J, Zien A, Sochivko D, Normann S, Schramm J, Elger CE, Wiestler OD, Blumcke I (2003) Correlated stage- and subfield-associated hippocampal gene expression patterns in experimental and human temporal lobe epilepsy. Eur J Neurosci 18:2792-2802.
3. Beckmann AM, Wilce PA (1997) EGR transcription factors in the nervous system. Neurochem Int 31:477-510.
4. Berkers CR, Verdoes M, Lichtman E, Fiebiger E, Kessler BM, Anderson KC, Ploegh HL, Ovaa H, Galardy PJ (2005) Activity probe for in vivo profiling of the specificity of proteasome inhibitor bortezomib. Nat Methods 2:357-362.
5. Blalock EM, Chen K-C, Sharrow K, Herman JP, Porter NM, Foster TC, Landfield PW (2003) Gene microarrays in hippocampal aging: statistical profiling identifies novel processes correlated with cognitive impairment. J Neurosci 23:3807-3819.
6. Boehmer C, Henke G, Schniepp R, Palmada M, Rothstein JD, Broer S, Lang F (2003) Regulation of the glutamate transporter EAAT1 by the ubiquitin ligase Nedd4-2 and SGK1/3 and protein kinase B. J Neurochem 86:1181-1188.
7. Boehmer C, Philippin M, Rajamanickam J, Mack A, Broer S, Palmada M, Lang F (2004) Stimulation of the EAAT4 glutamate transporter by SGK protein kinase isoforms and PKB. Biochem Biophys Res Commun 324:1242-1248.
8. 2 receptors. J Neurosci 17:4536-4544.
9. Campbell DS, Holt CE (2001) Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32:1013-1026.
10. Cao X, Mahendran R, Guy G, Tan Y (1993) Detection and characterization of cellular EGR-1 binding to its recognition site. J Biol Chem 268:16949-16957.
11. Cascio P, Call M, Petre BM, Walz T, Goldberg AL (2002) Properties of the hybrid form of the 26S proteasome containing both 19S and PA28 complexes. EMBO J 21:2636-2645.
12. Cepeda C, Hurst RS, Altemus KL, Flores-Hernandez J, Calvert CR, Jokel ES, Grandy DK, Low MJ, Rubinstein M, Ariano MA, Levine MS (2001) Facilitated glutamatergic transmission in the striatum of D2 dopamine receptor-deficient mice. J Neurophysiol 85:659-670.
13. Chain DG, Schwartz JH, Hegde AN (1999) Ubiquitin-mediated proteolysis in learning and memory. Mol Neurobiol 20:125-142.
14. Chapman NR, Perkins ND (2000) Inhibition of the RelA (p65) NFkB subunit by egr-1. J Biol Chem 275:4719-4725.
15. Chatterjee-Kishore M, Kishore R, Hicklin DJ, Marincola FM, Ferrone S (1998) Different requirements for signal transducer and activator of transcription 1alpha and interferon regulatory factor 1 in the regulation of low molecular mass polypeptide 2 and transporter associated with antigen processing 1 gene expression. J Biol Chem 273:16177-16183.
16. Chowdhary R, Ali RA, Albig W, Doenecke D, Bajic VB (2005) Promoter modeling: the case study of mammalian histone promoters. Bioinformatics 21:2623-2628.
17. Cirelli C, Gutierrez CM, Tononi G (2004) Extensive and divergent effects of sleep and wakefulness on brain gene expression. Neuron 41:35-43.
18. Cogswell PC, Mayo MW, Baldwin Jr AS (1997) Involvement of Egr-1/RelA synergy in distinguishing T cell activation from tumor necrosis factor-alpha-induced NF-kappa B1 transcription. J Exp Med 185:491-498.
19. Cole AJ, Saffen DW, Baraban JM, Worley PF (1989) Rapid increase of an immediate-early gene mRNA in hippocampal neurons by NMDA receptor activation. Nature 340:474-476.
20. 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.
21. Conway A-M, James AB, O'Kane EM, Rakhit S, Morris BJ (2004) Regulation of myosin light chain phosphorylation by RhoB in neuronal cells. Exp Cell Res 300:35-42.
22. Cooper EM, Hudson AW, Amos J, Wagstaff J, Howley PM (2004) Biochemical analysis of Angelman syndrome-associated mutations in the E3 ubiquitin ligase E6-associated protein. J Biol Chem 279:41208-41217.
23. Copertino DW, Edelman GM, Jones FS (1997) Multiple promoter elements differentially regulate the expression of the mouse tenascin gene. Proc Natl Acad Sci USA 94:1846-1851.
24. Davis Jr W, Chen ZJ, Ile KE, Tew KD (2003) Reciprocal regulation of expression of the human adenosine 5′-triphosphate binding cassette, subfamily A, transporter 2 (ABCA2) promoter by the early growth response-1 (EGR-1) and Sp-family transcription factors. Nucleic Acids Res 31:1097-1107.
25. Diaz-Hernandez M, Hernandez F, Martin-Aparicio E, Gomez-Ramos P, Moran MA, Casano JG, Ferrer I, Avila J, Lucas JJ (2003) Neuronal induction of the immunoproteasome in Huntington's disease. J Neurosci 23:11653-11661.
26. Ding Q, Keller JN (2001) Proteasomes and proteasome inhibition in the central nervous system. Free Radic Biol Med 31:574-584.
27. Dinkel A, Aicher W, Haas C, Zipfel P, Peter H, Eibel H (1997) Transcription factor Egr-1 activity down-regulates Fas and CD23 expression in B cells. J Immunol 159:2678-2684.
28. Donahue CP, Jensen RV, Ochiishi T, Eisenstein I, Zhao M, Shors T, Kosik KS (2002) Transcriptional profiling reveals regulated genes in the hippocampus during memory formation. Hippocampus 12:821-833.
29. Ebert SN, Balt SL, Hunter JPB, Gashler A, Sukhatme V, Wong DL (1994) Egr-1 activation of rat adrenal phenylethanolamine N-methyltransferase gene. J Biol Chem 269:20885-20898.
30. Ehlers MD (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6:231-242.
31. El-Khodor BF, Kholodilov NG, Yarygina O, Burke RE (2001) The expression of mRNAs for the proteasome complex is developmentally regulated in the rat mesencephalon. Dev Brain Res 129:47-56.
32. Fenteany G, Schreiber SL (1996) Specific inhibition of the chymotrypsin-like activity of the proteasome induces a bipolar morphology in neuroblastoma cells. Chem Biol 3:905-912.
33. Fruh K, Gossen M, Wang K, Bujard H, Peterson P, Yang Y (1994) Displacement of housekeeping proteasome subunits by MHC-encoded LMPs: a newly discovered mechanism for modulating the multicatalytic proteinase complex. EMBO J 13:3236-3244.
34. Fukada T, Tonks NK (2001) The reciprocal role of Egr-1 and Sp family proteins in regulation of the PTP1B promoter in response to the p210 Bcr-Abl oncoprotein-tyrosine kinase. J Biol Chem 276:25512-25519.
35. Gonzalez-Nicolini V, McGinty JF (2002) Gene expression profile from the striatum of amphetamine-treated rats: a cDNA array and in situ hybridization histochemical study. Brain Res Gene Expr Patterns 1:193-198.
36. Groettrup M, Ruppert T, Kuehn L, Seeger M, Standera S, Koszinowski U, Kloetzel PM (1995) The interferon-gamma-inducible 11 S regulator (PA28) and the LMP2/LMP7 subunits govern the peptide production by the 20 S proteasome in vitro. J Biol Chem 270:23808-23815.
37. Groot M, Boxer LM, Thiel G (2000) Nerve growth factor- and epidermal growth factor-regulated gene transcription in PC12 pheochromocytoma and INS-1 insulinoma cells. Eur J Cell Biol 79:924-935.
38. Guillemot L, Levy A, Raymondjean M, Rothhut B (2001) Angiotensin II-induced transcriptional activation of the cyclin D1 gene is mediated by Egr-1 in CHO-AT1A cells. J Biol Chem 276:39394-39403.
39. Harris JL, Alper PB, Li J, Rechsteiner M, Backes BJ (2001) Substrate specificity of the human proteasome. Chem Biol 8:1131-1141.
40. Hegde AN, Inokuchi K, Pei W, Casadio A, Ghirardi M, Chain DG, Martin KC, Kandel ER, Schwartz JH (1997) Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell 89:115-126.
41. Hisamatsu H, Shimbara N, Saito Y, Kristensen P, Hendil K, Fujiwara T, Takahashi E, Tanahashi N, Tamura T, Ichihara A, Tanaka K (1996) Newly identified pair of proteasomal subunits regulated reciprocally by interferon gamma. J Exp Med 183:1807-1816.
42. Huang R-P, Fan Y, Ni Z, Mercola D, Adamson ED (1997) Reciprocal modulation between Sp1 and Egr1. J Cell Biochem 66:489-499.
43. Huh GS, Boulanger LM, Du H, Riquelme PA, Brotz TM, Shatz CJ (2000) Functional requirement for class I MHC in CNS development and plasticity. Science 290:2155-2159.
44. Hwang L-Y, Lieu PT, Peterson PA, Yang Y (2001) Functional regulation of immunoproteasomes and transporter associated with antigen processing. Immunol Res 24:245-272.
45. James AB, Conway A-M, Thiel G, Morris BJ (2004) Egr1-mediated transcriptional modulation of neuronal target genes: permissive effect of forskolin via cAMP. Cell Signal 16:1355-1362.
46. James AB, Conway A-M, Morris BJ (2005) Genomic profiling of the neuronal target genes of the plasticity-related transcription factor - Zif268. J Neurochem 95:796-810.
47. Jarvis ED, Scharff C, Grossman MR, Ramos JA, Nottebohm F (1998) For whom the bird sings: context-dependent gene expression. Neuron 21:775-788.
48. Jones MW, Errington ML, French PJ, Fine A, Bliss TVP, Garel S, Charnay P, Bozon B, Laroche S, Davis S (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4:289-296.
49. Juo P, Kaplan JM (2004) The anaphase-promoting complex regulates the abundance of GLR-1 glutamate receptors in the ventral nerve cord of C. elegans. Curr Biol 14:2057-2062.
50. Kaczmarek L, Zangenehpour S, Chaudhuri A (1999) Sensory regulation of immediate-early genes c-fos and zif268 in monkey visual cortex at birth and throughout the critical period. Cereb Cortex 9:179-187.
51. Kamalakaran S, Radhakrishnan SK, Beck WT (2005) Identification of estrogen-responsive genes using a genome-wide analysis of promoter elements for transcription factor binding sites. J Biol Chem 280:21491-21497.
52. Kazi A, Daniel KG, Smith DM, Kumar NB, Dou QP (2003) Inhibition of the proteasome activity, a novel mechanism associated with the tumor cell apoptosis-inducing ability of genistein. Biochem Pharmacol 66:965-976.
53. Keefe KA, Gerfen CR (1995) D1-D2 dopamine receptor synergy in striatum: effects of intrastriatal infusions of dopamine agonists and antagonists on immediate early gene expression. Neuroscience 66:903-913.
54. Keller JN, Hanni KB, Markesbery WR (2000) Possible involvement of proteasome inhibition in aging: implications for oxidative stress. Mech Ageing Dev 113:61-70.
55. Kel-Margoulis OV, Tchekmenev D, Kel AE, Goessling E, Hornischer K, Lewicki-Potapov B, Wingender E (2003) Composition-sensitive analysis of the human genome for regulatory signals. In Silico Biol 3:145-171.
56. Levenson J, Weeber E, Selcher JC, Kategaya LS, Sweatt JD, Eskin A (2002) Long-term potentiation and contextual fear conditioning increase neuronal glutamate uptake. Nat Neurosci 5:155-161.
57. Liu C, Calogero A, Ragona G, Adamson E, Mercola D (1996) EGR-1, the reluctant suppression factor. Crit Rev Oncog 7:101-125.
58. Lopez-Salon M, Alonso M, Vianna MRM, Viola H, Mello e Souza T, Izquierdo I, Pasquini JM, Medina JH (2002) The ubiquitin-proteasome cascade is required for mammalian long-term memory formation. Eur J Neurosci 14:1820-1826.
59. Marques L, Brucet M, Lloberas J, Celada A (2004) STAT1 regulates lipopolysaccharide- and TNF-a-dependent expression of transporter associated with antigen processing 1 and low molecular mass polypeptide 2 genes in macrophages by distinct mechanisms. J Immunol 173:1103-1110.
60. Mello CV, Velho TAF, Pinaud R (2004) Song-induced gene expression: a window on song auditory processing and perception. Ann NY Acad Sci 1016:263-281.
61. Mengual E, Arizti P, Rodrigo J, Gimenez-Amaya JM, Castano JG (1996) Immunohistochemical distribution and electron microscopic subcellular localization of the proteasome in the rat CNS. J Neurosci 16:6331-6341.
62. Morris BJ (1995) Stimulation of immediate-early gene expression in striatal neurones by nitric oxide. J Biol Chem 270:24740-24744.
63. Morris BJ (2004) Neuronal plasticity. In: Molecular biology of the neuron, Ed 2 (Davies RW, Morris BJ, eds), pp 357-386. Oxford: Oxford UP.
64. Moss A, Blackburn-Munro G, Garry EM, Blakemore JA, Dickinson T, Resie R, Mitchell R, Fleetwood-Walker SM (2003) A role of the ubiquitin-proteasome system in neuropathic pain. J Neurosci 22:1363-1372.
65. Nguyen TV, Kosofsky BE, Birnbaum R, Cohen BM, Hyman SE (1992) Differential expression of c-fos and zif268 in rat striatum after haloperidol, clozapine, and amphetamine. Proc Natl Acad Sci USA 89:4270-4274.
66. Noda C, Tanahashi N, Shimbara N, Hendil KB, Tanaka K (2000) Tissue distribution of constitutive proteasomes, immunoproteasomes, and PA28 in rats. Biochem Biophys Res Commun 277:348-354.
67. Oberdorf J, Carlson EJ, Skach WR (2001) Redundancy of mammalian proteasome beta subunit function during endoplasmic reticulum associated degradation. Biochemistry 40:13397-13405.
68. Obin M, Mesco E, Gong X, Haas AL, Joseph J, Taylor A (1999) Neurite outgrowth in PC12 cells. Distinguishing the roles of ubiquitylation and ubiquitin-dependent proteolysis. J Biol Chem 274:11789-11795.
69. Pak DTS, Sheng M (2003) Targeted protein degradation and synapse remodelling by an inducible protein kinase. Science 302:1368-1373.
70. Proffitt JA, Blair GE (1997) The MHC-encoded TAP1/LMP2 bidirectional promoter is down-regulated in highly oncogenic adenovirus type 12 transformed cells. FEBS Lett 400:141-144.
71. Quandt K, Frech K, Karas H, Wingender E, Werner T (1995) Matind and Matinspector - new fast and versatile tools for detection of consensus matches in nucleotide-sequence data. Nucleic Acids Res 23:4878-4884.
72. Rezvani K, Mee S, Dawson S, McIlhinney J, Fujita J, Mayer RJ (2003) Proteasomal interactors control activities as diverse as the cell cycle and glutaminergic neurotransmission. Biochem Soc Trans 31:470-473.
73. Richardson CL, Tate WP, Mason SP, Lawlow PA, Dragunow M, Abraham WC (1992) Correlation betwen the induction of an immediate-early gene, zif/268, and long-term potentiation. Brain Res 580:147-154.
74. Schniepp R, Kohler K, Ladewig T, Guenther E, Henke G, Palmada M, Boehmer C, Rothstein JD, Broer S, Lang F (2004) Retinal colocalization and in vitro interaction of the glutamate receptor EAAT3 and the serum- and glucocorticoid-inducible kinase SGK1. Invest Ophthalmol Vis Sci 45:1442-1449.
75. Shen Y, Linden DJ (2005) Long-term potentiation of neuronal glutamate transporters. Neuron 46:715-722.
76. Simpson CS, Morris BJ (1994) Haloperidol and fluphenazine induce junB gene expression in rat striatum and nucleus accumbens. J Neurochem 63:1955-1961.
77. Simpson CS, Morris BJ (2000) Regulation of neuronal cell adhesion molecule (NCAM) expression by NF-kB. J Biol Chem 275:16879-16884.
78. 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.
79. Srivastava S, Weitzmann MN, Kimble RB, Rizzo M, Zahner M, Milbrandt J, Ross FP, Pacifici R (1998) Estrogen blocks M-CSF gene expression and osteoclast formation by regulating phosphorylation of egr1 and its interaction with Sp1. J Clin Invest 102:1850-1859.
80. Tan L, Peng H, Osaki M, Choy BK, Auron PE, Sandell LJ, Goldring MB (2003) Egr-1 mediates transcriptional repression of COL2A1 promoter activity by interleukin-1beta. J Biol Chem 278:17688-17700.
81. Thottassery JV, Sun D, Zambetti GP, Troutman A, Sukhatme VP, Schuetz EG, Schuetz JD (1999) Sp1 and Egr-1 have opposing effects on the regulation of the rat Pgp2/mdr1b gene. J Biol Chem 274:3199-3206.
82. Topilko P, Schneider-Maunoury S, Levi G, Trembleau A, Gourdji D, Driancourt M-A, Rao CV, Charnay P (1998) Multiple pituitary and ovarian defects in Krox-24 (NGFI-A, Egr-1)-targeted mice. Mol Endocrinol 12:107-122.
83. Tsai KJ, Chen SK, Ma YL, Hsu WL, Lee EHY (2002) sgk, a primary glucocorticoid-induced gene, facilitates memory consolidation of spatial learning in rats. Proc Natl Acad Sci USA 99:3990-3995.
84. Tullai JW, Schaffer ME, Mullenbrock S, Kasif S, Cooper GM (2004) Identification of transcription factor binding sites upstream of human genes regulated by the phosphatidylinositol 3-kinase and MEK/ERK signaling pathways. J Biol Chem 279:20167-20177.
85. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116-5121.
86. Virolle T, Krones-Herzig A, Baron V, De Gregorio G, Adamson ED, Mercola D (2003) Egr1 promotes growth and survival of prostate cancer cells. Identification of novel Egr1 target genes. J Biol Chem 278:11802-11810.
87. Waldegger S, Erdel M, Nagl UO, Barth P, Raber G, Steuer S, Utermann G, Paulmichl M, Lang F (1998) Genomic organization and chromosomal localization of the human SGK protein kinase gene. Genomics 51:299-302.
88. Wang C, Dostanic S, Servant N, Chalifour LE (2005) Egr-1 negatively regulates expression of the sodium-calcium exchanger-1 in cardiomyocytes in vitro and in vivo. Cardiovasc Res 65:187-194.
89. Webster M, Goya L, Ge Y, Maiyar A, Firestone G (1993) Characterization of sgk, a novel member of the serine/threonine protein kinase gene family which is transcriptionally induced by glucocorticoids and serum. Mol Cell Biol 13:2031-2040.
90. Whitehouse AS, Tisdale MJ (2003) Increased expression of the ubiquitin-proteasome pathway in murine myotubes by proteolysis-inducing factor (PIF) is associated with activation of the transcription factor NF-kappaB. Br J Cancer 89:1116-1122.
91. Wisden W, Errington ML, Williams S, Dunnett SB, Waters C, Hitchcock D, Evan G, Bliss TVP, Hunt SP (1990) Differential expression of immediate-early genes in the hippocampus and spinal cord. Neuron 4:603-614.
92. Worley PF, Bhat RV, Baraban JM, Erickson CA, Mcnaughton BL, Barnes CA (1993) Thresholds for synaptic activation of transcription factors in hippocampus: correlation with long-term enhancement. J Neurosci 13:4776-4786.
93. Wright KL, White LC, Kelly A, Beck S, Trowsdale J, Ting J-Y (1995) Coordinate regulation of the human TAP1 and LMP2 genes from a shared bidirectional promoter. J Exp Med 181:1459-1471.
94. Xie X, Lu J, Kulbokas EJ, Golub TR, Mootha V, Lindblad-Toh K, Lander ES, Kellis M (2005) Systematic discovery of regulatory motifs in human promoters and 3′ UTRs by comparison of several mammals. Nature 434:338-345.
95. Yang Y, Früh K, Ahn K, Peterson PA (1995) In vivo assembly of the proteasomal complexes, implications for antigen processing. J Biol Chem 270:27687-27694.
96. Yao WD, Gainetdinov RR, Arbuckle MI, Sotnikova TD, Cyr M, Beaulieu JM, Torres GE, Grant SG, Caron MG (2004) Identification of PSD-95 as a regulator of dopamine-mediated synaptic and behavioral plasticity. Neuron 41:625-638.
97. Yu J, de Belle I, Liang H, Adamson ED (2004) Coactivating factors p300 and CBP are transcriptionally crossregulated by Egr1 in prostate cells, leading to divergent responses. Mol Cell 15:83-94.
98. Zhang X, Liu Y (2003) Suppression of HGF receptor gene expression by oxidative stress is mediated through the interplay between Sp1 and Egr-1. Am J Physiol Renal Physiol 284:F1216-F1225.
99. Zhang X, Odom DT, Koo S-H, Conkright MD, Canettieri G, Best J, Chen H, Jenner R, Herbolsheimer E, Jacobsen E, Kadam S, Ecker JR, Emerson B, Hogenesch JB, Unterman T, Young RA, Montminy M (2005) Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci USA 102:4459-4464.
100. Zhao Y, Hegde AN, Martin KC (2003) The ubiquitin proteasome system functions as an inhibitory constraint on synaptic strengthening. Curr Biol 13:887-898.
101. Zheng J, Wu J, Sun Z (2003) An approach to identify over-represented cis-elements in related sequences. Nucleic Acids Res 31:1995-2005.