Poly-(ADP-ribose) polymerase-1 is necessary for long-term facilitation in Aplysia

Journal of Neuroscience

Volumn 29, Issue 30, 2009, Pages 9553-9562

  Hernández, A Iván ^a,b,c   Wolk, Jason ^a   Hu, Jiang Yuan ^a   Liu, Jinming ^a   Kurosu, Takeshi ^a,d   Schwartz, James H ^a   Schacher, Samuel ^a  

^a NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^b SUNY DOWNSTATE MEDICAL CENTER   (United States)

^c SUNY Downstate Medical Center   (United States)

^d Thai National Institute of Health   (Thailand)

Author keywords

[No Author keywords available]

Indexed keywords

3 AMINOBENZAMIDE; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; RIBOSOME PROTEIN; RIBOSOME RNA; SEROTONIN; UBIQUITIN CONJUGATING ENZYME E2;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; APLYSIA; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME REGULATION; GANGLION; GENE EXPRESSION REGULATION; LONG TERM MEMORY; MOLECULAR CLONING; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA ANALYSIS; RNA GENE; SENSORIMOTOR FUNCTION; SENSORY NERVE CELL; SYNAPSE;

ANIMALS; APLYSIA; BASE SEQUENCE; BENZAMIDES; CELLS, CULTURED; ENZYME INHIBITORS; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM POTENTIATION; MOLECULAR SEQUENCE DATA; MOTOR NEURONS; PHENANTHRENES; POLY(ADP-RIBOSE) POLYMERASES; RIBOSOMAL PROTEINS; RNA, MESSENGER; RNA, RIBOSOMAL; SENSORY RECEPTOR CELLS; SEROTONIN; SYNAPSES; TIME FACTORS; UBIQUITIN-CONJUGATING ENZYMES;

EID: 68049119933     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1512-09.2009     Document Type: Article

References (70)

1. Aalfs JD, Kingston RE (2000) What does 'chromatin remodeling' mean? Trends Biochem Sci 25:548-555.
2. 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. (Pubitemid 24106389)
3. Bartsch D, Ghirardi M, Casadio A, Giustetto M, Karl KA, Zhu H, Kandel ER (2000) Enhancement of memory-related long-term facilitation by ApAF, a novel transcription factor that acts downstream from both CREB1 and CREB2. Cell 103:595-608. (Pubitemid 30954003)
4. Barzilai A, Kennedy TE, Sweatt JD, Kandel ER (1989) 5-HT modulates protein synthesis and the expression of specific proteins during long-term facilitation in Aplysia sensory neurons. Neuron 2:1577-1586.
5. Bergold PJ, Beushausen SA, Sacktor TC, Cheley S, Bayley H, Schwartz JH (1992) A regulatory subunit of the cAMP-dependent protein kinase down-regulated in Aplysia sensory neurons during long-term sensitization. Neuron 8:387-397.
6. Buonomano DV, Byrne JH (1990) Long-term synaptic changes produced by a cellular analog of classical conditioning in Aplysia. Science 249:420-423. (Pubitemid 20248871)
7. Chain DG, Hegde AN, Yamamoto N, Liu-Marsh B, Schwartz JH (1995) Persistent activation of cAMP-dependent protein kinase by regulated proteolysis suggests a neuron-specific function of the ubiquitin system in Aplysia. J Neurosci 15:7592-7603.
8. Chain DG, Casadio A, Schacher S, Hegde AN, Valbrun M, Yamamoto N, Goldberg AL, Bartsch D, Kandel ER, Schwartz JH (1999) Mechanisms for generating the autonomous cAMP-dependent protein kinase required for long-term facilitation in Aplysia. Neuron 22:147-156. (Pubitemid 29070101)
9. Cohen-Armon M (2007) PARP-1 activation in the ERK signaling pathway. Trends Pharmacol Sci 28:556-560.
10. Cohen-Armon M, Visochek L, Katzoff A, Levitan D, Susswein AJ, Klein R, Valbrun M, Schwartz JH (2004) Long-term memory requires polyADPribosylation. Science 304:1820-1822.
11. Cohen-Armon M, Visochek L, Rozensal D, Kalal A, Geistrikh I, Klein R, Bendetz-Nezer S, Yao Z, Seger R (2007) DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol Cell 25:297-308. (Pubitemid 46127778)
12. Dale N, Kandel ER, Schacher S (1987) Serotonin produces long-term changes in the excitability of Aplysia sensory neurons in culture that depend on new protein synthesis. J Neurosci 7:2232-2238.
13. D'Amours D, Desnoyers S, D'Silva I, Poirier GG (1999) Poly(ADPribosyl) ation reactions in the regulation of nuclear functions. Biochem J 342:249-268. (Pubitemid 29425344)
14. Davis HP, Squire LR (1984) Protein synthesis and memory: a review. Psychol Bull 96:518-559.
15. de Murcia G, Ménissier de Murcia J (1994) Poly(ADP-ribose) polymerase: a molecular nick-sensor. Trends Biochem Sci 19:172-176.
16. Fioravante D, Liu RY, Byrne JH (2008) The ubiquitin-proteasome system is necessary for long-term synaptic depression in Aplysia. J Neurosci 28:10245-10256.
17. Fromont-Racine M, Senger B, Saveanu C, Fasiolo F (2003) Ribosome assembly in eukaryotes. Gene 313:17-42.
18. Fulton D, Kemenes I, Andrew RJ, Benjamin PR (2005) A single timewindow for protein synthesis-dependent long-term memory formation after one-trial appetitive conditioning. Eur J Neurosci 21:1347-1358. (Pubitemid 40516633)
19. Giustetto M, Hegde AN, Si K, Casadio A, Inokuchi K, Pei W, Kandel ER, Schwartz JH (2003) Axonal transport of eukaryotic translation elongation factor 1alpha mRNA couples transcription in the nucleus to long-term facilitation at the synapse. Proc Natl Acad Sci U S A 100: 13680-13685. (Pubitemid 37444799)
20. Grummt I (2003) Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev 17:1691-1702.
21. Guan Z, Giustetto M, Lomvardas S, Kim JH, Miniaci MC, Schwartz JH, Thanos D, Kandel ER (2002) Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 111:483-493. (Pubitemid 35363296)
22. Guan Z, Kim JH, Lomvardas S, Holick K, Xu S, Kandel ER, Schwartz JH (2003) p38 MAP kinase mediates both short-term and long-term synaptic depression in Aplysia. J Neurosci 23:7317-7325. (Pubitemid 36999521)
23. Ha HC, Hester LD, Snyder SH (2002) Poly(ADP-ribose) polymerase-1 dependence of stress-induced transcription factors and associated gene expression in glia. Proc Natl Acad Sci U S A 99:3270-3275.
24. Hattar S, Lyons LC, Eskin A (2002) Circadian regulation of a transcription factor, ApC/EBP, in the eye of Aplysia californica. J Neurochem 83:1401-1411.
25. 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. (Pubitemid 27180591)
26. Homburg S, Visochek L, Moran N, Dantzer F, Priel E, Asculai E, Schwartz D, Rotter V, Dekel N, Cohen-Armon M (2000) A fast signal-induced activation of Poly(ADP-ribose) polymerase: a novel downstream target of phospholipase c. J Cell Biol 150:293-307. (Pubitemid 30491354)
27. Hu JY, Glickman L, Wu F, Schacher S (2004) Serotonin regulates the secretion and autocrine action of a neuropeptide to activate MAPK required for long-term facilitation in Aplysia. Neuron 43:373-385. (Pubitemid 39061129)
28. Hu JY, Chen Y, Schacher S (2007) Protein kinase C regulates local synthesis and secretion of a neuropeptide required for activity-dependent long-term synaptic plasticity. J Neurosci 27:8927-8939. (Pubitemid 47292757)
29. Hyson RL, Rubel EW (1995) Activity-dependent regulation of a ribosomal RNA epitope in the chick cochlear nucleus. Brain Res 672:196-204.
30. Jones CB, McIntosh J, Huang H, Graytock A, HoytDG (2001) Regulation of bleomycin-induced DNA breakage and chromatin structure in lung endothelial cells by integrins and poly(ADP-ribose) polymerase. Mol Pharmacol 59:69-75. (Pubitemid 32043087)
31. Jordan BA, Fernholz BD, Khatri L, Ziff EB (2007) Activity-dependent AIDA-1 nuclear signaling regulates nucleolar numbers and protein synthesis in neurons. Nat Neurosci 10:427-435. (Pubitemid 46494588)
32. Ju BG, Solum D, Song EJ, Lee KJ, Rose DW, Glass CK, RosenfeldMG (2004) Activating the PARP-1 sensor component of the groucho/ TLE1 corepressor complex mediates a CaMKinase IIdelta-dependent neurogenic gene activation pathway. Cell 119:815-829. (Pubitemid 40017688)
33. Ju BG, Lunyak VV, Perissi V, Garcia-Bassets I, Rose DW, Glass CK, Rosenfeld MG (2006) A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription. Science 312:1798-1802. (Pubitemid 43962898)
34. Kameshita I, Matsuda Z, Taniguchi T, Shizuta Y (1984) Poly (ADP-ribose) synthetase. Separation and identification of three proteolytic fragments as the substrate-binding domain, the DNA-binding domain, and the automodification domain. J Biol Chem 259:4770-4776. (Pubitemid 14144197)
35. Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030-1038. (Pubitemid 33041851)
36. Kandel ER, Schwartz JH (1982) Molecular biology of learning: modulation of transmitter release. Science 218:433-443.
37. Kauppinen TM, Swanson RA (2007) The role of poly(ADP-ribose) polymerase-1 in CNS disease. Neuroscience 145:1267-1272.
38. Kauppinen TM, Chan WY, Suh SW, Wiggins AK, Huang EJ, Swanson RA (2006) Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal-regulated kinases 1/2. Proc Natl Acad Sci U S A 103:7136-7141.
39. Kim MY, Zhang T, Kraus WL (2005) Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes Dev 19:1951-1967.
40. Klann E, Sweatt JD (2008) Altered protein synthesis is a trigger for long-term memory formation. Neurobiol Learn Mem 89:247-259. (Pubitemid 351318266)
41. Krishnakumar R, Gamble MJ, Frizzell KM, Berrocal JG, Kininis M, KrausWL (2008) Reciprocal binding of PARP-1 and histone H1 at promoters specifies transcriptional outcomes. Science 319:819-821. (Pubitemid 351225873)
42. Levenson JM, Sweatt JD (2006) Epigenetic mechanisms: a common theme in vertebrate and invertebrate memory formation. Cell Mol Life Sci 63:1009-1016.
43. Lyons LC, Collado MS, Khabour O, Green CL, Eskin A (2006) The circadian clock modulates core steps in long-term memory formation in Aplysia. J Neurosci 26:8662-8671.
44. Mauelshagen J, Parker GR, Carew TJ (1996) Dynamics of induction and expression of long-term synaptic facilitation in Aplysia. J Neurosci 16:7099-7108. (Pubitemid 26382887)
45. Meder VS, Boeglin M, de Murcia G, Schrieber V (2005) PARP-1 and PARP-2 interact with nucleophosmin/B23 and accumulate in transcriptionally active nucleoli. J Cell Sci 118:211-222. (Pubitemid 40277117)
46. Miniaci MC, Kim JH, Puthanveettil SV, Si K, Zhu H, Kandel ER, Bailey CH (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.
47. Montarolo PG, Goelet P, Castellucci VF, Morgan J, Kandel ER, Schacher S (1986) A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234:1249-1254. (Pubitemid 17232366)
48. Montarolo PG, Kandel ER, Schacher S (1988) Long-term heterosynaptic inhibition in Aplysia. Nature 333:171-174.
49. Moroz LL, Edwards JR, Puthanveettil SV, Kohn AB, Ha T, Heyland A, Knudsen B, Sahni A, Yu F, Liu L, Jezzini S, Lovell P, Iannucculli W, Chen M, Nguyen T, Sheng H, Shaw R, Kalachikov S, Panchin YV, Farmerie W, Russo JJ, Ju J, Kandel ER (2006) Neuronal transcriptome of Aplysia: neuronal compartments and circuitry. Cell 127:1453-1467.
50. Narlikar GJ, Fan HY, Kingston RE (2002) Cooperation between complexes that regulate chromatin structure and transcription. Cell 108:475-487.
51. Noel F, Nuñez-Regueiro M, Cook R, Byrne JH, Eskin A (1993) Long-term changes in synthesis of intermediate filament protein, actin and other proteins in pleural sensory neurons of Aplysia produced by an in vitro analogue of sensitization training. Brain Res Mol Brain Res 19:203-210.
52. Noel F, Koumenis C, Nunez-Regueiro M, Raju U, Byrne JH, Eskin A (1994) Effects on protein synthesis produced by pairing depolarization with serotonin, an analogue of associative learning in Aplysia. Proc Natl Acad Sci U S A 91:4150-4154. (Pubitemid 24143390)
53. Ogino H, Nozaki T, Gunji A, Maeda M, Suzuki H, Ohta T, Murakami Y, Nakagama H, Sugimura T, Masutani M (2007) Loss of Parp-1 affects gene expression profile in a genome-wide manner in ES cells and liver cells. BMC Genomics 8:41. (Pubitemid 46389837)
54. Pavri R, Lewis B, Kim TK, Dilworth FJ, Erdjument-Bromage H, Tempst P, de Murcia G, Evans R, Chambon P, ReinbergD (2005) PARP-1 determines specificity in a retinoid signaling pathway via direct modulation of mediator. Mol Cell 18:83-96. (Pubitemid 40444650)
55. Perry RP (1981) RNA processing comes of age. J Cell Biol 91:28s-38s.
56. Polesskaya OO, Haroutunian V, Davis KL, Hernandez I, Sokolov BP (2003) Novel putative nonprotein-coding RNA gene from 11q14 displays decreased expression in brains of patients with schizophrenia. J Neurosci Res 74:111-122. (Pubitemid 37176674)
57. Russell J, Zomerdijk JC (2005) RNA-polymerase-I-directed rDNA transcription, life and works. Trends Biochem Sci 30:87-96. (Pubitemid 40187301)
58. Schreiber V, Dantzer F, Ame JC, de Murcia G (2006) Poly(ADP-ribose): novel functions for an old molecule. Nat Rev Mol Cell Biol 7:517-528. (Pubitemid 44036457)
59. Sharma SK, Carew TJ (2004) The roles of MAPK cascades in synaptic plasticity and memory in Aplysia: facilitatory effects and inhibitory constraints. Learn Mem 11:373-378.
60. Sokolov BP, Prockop DJ (1994) A rapid and simple PCR-based method for isolation of cDNAs from differentially expressed genes. Nucleic Acids Res 22:4009-4015.
61. Sossin WS, Sacktor TC, Schwartz JH (1994) Persistent activation of protein kinase C during the development of long-term facilitation in Aplysia. Learn Mem 1:189-202.
62. Spence J, Gali RR, Dittmar G, Sherman F, Karin M, Finley D (2000) Cell cycle-regulated modification of the ribosome by a variant multiubiquitin chain. Cell 102:67-76.
63. Sutton MA, Carew TJ (2000) Parallel molecular pathways mediate expression of distinct forms of intermediate-term facilitation at tail sensory-motor synapses in Aplysia. Neuron 26:219-231.
64. Sutton MA, Bagnall MW, Sharma SK, Shobe J, Carew TJ (2004) Intermediate-term memory for site-specific sensitization in Aplysia is maintained by persistent activation of protein kinase C. J Neurosci 24:3600-3609.
65. Tulin A, Spradling A (2003) Chromatin loosening by poly(ADP)-ribose polymerase (PARP) at Drosophila puff loci. Science 299:560-562.
66. Tulin A, Stewart D, Spradling AC (2002) The Drosophila heterochromatic gene encoding poly(ADP-ribose) polymerase (PARP) is required to modulate chromatin structure during development. Genes Dev 16:2108-2119.
67. Vargas JP, Rodríguez F, López JC, Arias JL, Salas C (2000) Spatial learning-induced increase in the argyrophilic nucleolar organizer region of dorsolateral telencephalic neurons in goldfish. Brain Res 865:77-84.
68. Virág L, Szabó C (2002) The therapeutic potential of poly(ADP-ribose) polymerase inhibitors. Pharmacol Rev 54:375-429.
69. Visochek L, Steingart RA, Vulih-Shultzman I, Klein R, Priel E, Gozes I, Cohen-Armon M (2005) PolyADP-ribosylation is involved in neurotrophic activity. J Neurosci 25:7420-7428.
70. Zwartjes RE, West H, Hattar S, Ren X, Noel F, Nuñez-Regueiro M, MacPhee K, Homayouni R, Crow MT, Byrne JH, Eskin A (1998) Identification of specific mRNAs affected by treatments producing long-term facilitation in Aplysia. Learn Mem 4:478-495. (Pubitemid 28223974)