AU-rich element-binding protein negatively regulates CCAAT enhancer-binding protein mRNA stability during long-term synaptic plasticity in Aplysia

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 38, 2012, Pages 15520-15525

  Lee, Yong Seok ^a   Choi, Sun Lim ^a   Jun, Heejung ^a   Yim, Se Jeong ^a   Lee, Jin A ^b   Kim, Hyoung F ^a   Lee, Seung Hee ^a   Shim, Jaehoon ^a   Lee, Kyungmin ^c   Jang, Deok Jin ^c   Kaang, Bong Kiun ^a  

^a Seoul National University   (South Korea)

^b Hannam University   (South Korea)

^c Kyungpook National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AU RICH ELEMENT BINDING PROTEIN; BINDING PROTEIN; CCAAT ENHANCER BINDING PROTEIN; MESSENGER RNA; SEROTONIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; APLYSIA; ARTICLE; CONTROLLED STUDY; GENE OVEREXPRESSION; MOLECULAR CLONING; MOTONEURON; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN STABILITY; REPORTER GENE; RNA STABILITY; SENSORY NERVE CELL;

3' UNTRANSLATED REGIONS; ANIMALS; APLYSIA; CCAAT-ENHANCER-BINDING PROTEINS; CLONING, MOLECULAR; GENE EXPRESSION REGULATION; GENES, REPORTER; HEK293 CELLS; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN D; HUMANS; IN SITU HYBRIDIZATION; MODELS, BIOLOGICAL; MODELS, GENETIC; NEURONAL PLASTICITY; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, MESSENGER; SYNAPTIC TRANSMISSION;

APLYSIA;

EID: 84866544096     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1116224109     Document Type: Article

References (46)

1. Kandel ER (2001) The molecular biology of memory storage: A dialogue between genes and synapses. Science 294:1030-1038.
2. Bailey CH, Bartsch D, Kandel ER (1996) Toward a molecular definition of long-term memory storage. Proc Natl Acad Sci USA 93:13445-13452. (Pubitemid 26424140)
3. Lee YS, Bailey CH, Kandel ER, Kaang BK (2008) Transcriptional regulation of long-term memory in the marine snail Aplysia. Mol Brain 1:3.
4. Alberini CM, Ghirardi M, Metz R, Kandel ER (1994) C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia. Cell 76:1099-1114.
5. Hegde AN, et al. (1997) Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell 89:115-126. (Pubitemid 27180591)
6. Alberini CM, Ghirardi M, Huang YY, Nguyen PV, Kandel ER (1995) A molecular switch for the consolidation of long-term memory: cAMP-inducible gene expression. Ann N Y Acad Sci 758:261-286.
7. Lee JA, et al. (2001) Overexpression of and RNA interference with the CCAAT enhancer-binding protein on long-term facilitation of Aplysia sensory to motor synapses. Learn Mem 8:220-226.
8. Yamamoto N, Hegde AN, Chain DG, Schwartz JH (1999) Activation and degradation of the transcription factor C/EBP during long-term facilitation in Aplysia. J Neurochem 73:2415-2423.
9. McCarthy JE, Kollmus H (1995) Cytoplasmic mRNA-protein interactions in eukaryotic gene expression. Trends Biochem Sci 20:191-197.
10. Guhaniyogi J, Brewer G (2001) Regulation of mRNA stability in mammalian cells. Gene 265:11-23. (Pubitemid 32209246)
11. Bevilacqua A, Ceriani MC, Capaccioli S, Nicolin A (2003) Post-transcriptional regulation of gene expression by degradation of messenger RNAs. J Cell Physiol 195:356-372. (Pubitemid 36529864)
12. Mitchell P, Tollervey D (2000) mRNA stability in eukaryotes. Curr Opin Genet Dev 10:193-198. (Pubitemid 30182253)
13. Bolognani F, Perrone-Bizzozero NI (2008) RNA-protein interactions and control of mRNA stability in neurons. J Neurosci Res 86:481-489. (Pubitemid 351204460)
14. Chen CY, Shyu AB (1995) AU-rich elements: Characterization and importance in mRNA degradation. Trends Biochem Sci 20:465-470.
15. Yim SJ, et al. (2006) Regulation of ApC/EBP mRNA by the Aplysia AU-rich element-binding protein, ApELAV, and its effects on 5-hydroxytryptamine-induced long-term facilitation. J Neurochem 98:420-429.
16. Zhang W, et al. (1993) Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol Cell Biol 13:7652-7665. (Pubitemid 23354290)
17. DeMaria CT, Brewer G (1996) AUF1 binding affinity to A+U-rich elements correlates with rapid mRNA degradation. J Biol Chem 271:12179-12184.
18. Wagner BJ, DeMaria CT, Sun Y, Wilson GM, Brewer G (1998) Structure and genomic organization of the human AUF1 gene: Alternative pre-mRNA splicing generates four protein isoforms. Genomics 48:195-202. (Pubitemid 28164499)
19. Laroia G, Cuesta R, Brewer G, Schneider RJ (1999) Control of mRNA decay by heat shock-ubiquitin-proteasome pathway. Science 284:499-502. (Pubitemid 29289625)
20. Laroia G, Sarkar B, Schneider RJ (2002) Ubiquitin-dependent mechanism regulates rapid turnover of AU-rich cytokine mRNAs. Proc Natl Acad Sci USA 99:1842-1846. (Pubitemid 34168977)
21. Lee YS, et al. (2008) Transcriptome analysis and identification of regulators for long-term plasticity in Aplysia kurodai. Proc Natl Acad Sci USA 105:18602-18607.
22. Ma WJ, Cheng S, Campbell C, Wright A, Furneaux H (1996) Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein. J Biol Chem 271:8144-8151. (Pubitemid 26108641)
23. Dearth LR, DeWille J (2003) An AU-rich element in the 3? untranslated region of the C/EBP delta mRNA is important for protein binding during G0 growth arrest. Biochem Biophys Res Commun 304:344-350. (Pubitemid 36444576)
24. Lal A, et al. (2004) Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J 23:3092-3102. (Pubitemid 39093603)
25. Dobi A, et al. (2006) AUF1 is expressed in the developing brain, binds to AT-rich double-stranded DNA, and regulates enkephalin gene expression. J Biol Chem 281:28889-28900. (Pubitemid 44507032)
26. Taubenfeld SM, et al. (2001) Fornix-dependent induction of hippocampal CCAAT enhancer-binding protein [beta] and [delta] Co-localizes with phosphorylated cAMP response element-binding protein and accompanies long-term memory consolidation. J Neurosci 21:84-91. (Pubitemid 32098729)
27. Montarolo PG, Kandel ER, Schacher S (1988) Long-term heterosynaptic inhibition in Aplysia. Nature 333:171-174.
28. Guan Z, et al. (2002) Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 111:483-493. (Pubitemid 35363296)
29. Hambardzumyan D, et al. (2009) AUF1 and Hu proteins in the developing rat brain: Implication in the proliferation and differentiation of neural progenitors. J Neurosci Res 87:1296-1309.
30. Jurado S, et al. (2006) NMDA induces post-transcriptional regulation of alpha2-guanylyl-cyclase-subunit expression in cerebellar granule cells. J Cell Sci 119:1622-1631. (Pubitemid 43732988)
31. Sarkar B, Lu JY, Schneider RJ (2003) Nuclear import and export functions in the different isoforms of the AUF1/heterogeneous nuclear ribonucleoprotein protein family. J Biol Chem 278:20700-20707. (Pubitemid 36806372)
32. Arao Y, Kuriyama R, Kayama F, Kato S (2000) A nuclear matrix-associated factor, SAFB, interacts with specific isoforms of AUF1/hnRNP D. Arch Biochem Biophys 380: 228-236. (Pubitemid 30659091)
33. Martin KC, Barad M, Kandel ER (2000) Local protein synthesis and its role in synapse-specific plasticity. Curr Opin Neurobiol 10:587-592.
34. Schuman EM (1999) mRNA trafficking and local protein synthesis at the synapse. Neuron 23:645-648.
35. Si K, et al. (2003) A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in aplysia. Cell 115:893-904. (Pubitemid 38058500)
36. Miniaci MC, et al. (2008) Sustained CPEB-dependent local protein synthesis is required to stabilize synaptic growth for persistence of long-term facilitation in Aplysia. Neuron 59:1024-1036.
37. Si K, Choi YB, White-Grindley E, Majumdar A, Kandel ER (2010) Aplysia CPEB can form prion-like multimers in sensory neurons that contribute to long-term facilitation. Cell 140:421-435.
38. Liu J, Hu JY, Wu F, Schwartz JH, Schacher S (2006) Two mRNA-binding proteins regulate the distribution of syntaxin mRNA in Aplysia sensory neurons. J Neurosci 26:5204-5214. (Pubitemid 44315302)
39. Alarcon JM, et al. (2004) Selective modulation of some forms of schaffer collateral-CA1 synaptic plasticity in mice with a disruption of the CPEB-1 gene. Learn Mem 11: 318-327. (Pubitemid 38697898)
40. Berger-Sweeney J, Zearfoss NR, Richter JD (2006) Reduced extinction of hippocampaldependent memories in CPEB knockout mice. Learn Mem 13:4-7. (Pubitemid 43200812)
41. Pascale A, et al. (2004) Increase of the RNA-binding protein HuD and posttranscriptional up-regulation of the GAP-43 gene during spatial memory. Proc Natl Acad Sci USA 101:1217-1222. (Pubitemid 38182669)
42. Bolognani F, Merhege MA, Twiss J, Perrone-Bizzozero NI (2004) Dendritic localization of the RNA-binding protein HuD in hippocampal neurons: Association with polysomes and upregulation during contextual learning. Neurosci Lett 371:152-157. (Pubitemid 39440762)
43. Quattrone A, et al. (2001) Posttranscriptional regulation of gene expression in learning by the neuronal ELAV-like mRNA-stabilizing proteins. Proc Natl Acad Sci USA 98:11668-11673. (Pubitemid 32928786)
44. Bolognani F, et al. (2007) Associative and spatial learning and memory deficits in transgenic mice overexpressing the RNA-binding protein HuD. Neurobiol Learn Mem 87:635- 643.
45. Mastushita-Sakai T, White-Grindley E, Samuelson J, Seidel C, Si K (2010) Drosophila Orb2 targets genes involved in neuronal growth, synapse formation, and protein turnover. Proc Natl Acad Sci USA 107:11987-11992.
46. Kim H, et al. (2006) A nucleolar protein ApLLP induces ApC/EBP expression required for long-term synaptic facilitation in aplysia neurons. Neuron 49:707-718. (Pubitemid 43290130)