Nucleolar integrity is required for the maintenance of long-term synaptic plasticity

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Allen, Kim D ^a,b   Gourov, Andrei V ^a   Harte, Christopher ^a   Gao, Peng ^a   Lee, Clarice ^a   Sylvain, Darlene ^a   Splett, Joshua M ^a   Oxberry, William C ^a,c   Van De Nes, Paula S ^a   Troy Regier, Matthew J ^a   Wolk, Jason ^a   Alarcon, Juan M ^a,c   Hernández, A Iván ^a,c  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c Downstate Health Sciences University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; DNA DIRECTED RNA POLYMERASE; FORSKOLIN; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; POLY(ADENOSINE DIPHOSPHATE RIBOSE); RNA 18S; RNA 28S; RNA 5.8S; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PARP1 PROTEIN, MOUSE;

ADULT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; ENZYME INHIBITION; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LEARNING; LONG TERM POTENTIATION; MALE; MEMORY CONSOLIDATION; MOLECULAR BIOLOGY; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOLUS; PROTEIN SYNTHESIS; RAT; REGULATORY MECHANISM; RNA SYNTHESIS; UPREGULATION; ANIMAL; BIOSYNTHESIS; DRUG EFFECTS; GENETICS; LONG TERM MEMORY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SYNAPSE;

ANIMALS; COLFORSIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; GENE EXPRESSION; HIPPOCAMPUS; LONG-TERM POTENTIATION; MAP KINASE SIGNALING SYSTEM; MEMORY, LONG-TERM; MICE; NEURONAL PLASTICITY; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES; RNA, RIBOSOMAL, 28S; SYNAPSES;

EID: 84905474552     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104364     Document Type: Article

References (60)

1. Katz J, Halstead WC (1950) Protein organization and mental function. Comp Psychol Monographs 20: 1-38.
2. Flexner JB, Flexner LB, Stellar E (1963) Memory in mice as affected by intracerebral puromycin. Science 141: 57-59.
3. Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294: 1030-1038.
4. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44: 5-21. (Pubitemid 39348827)
5. Kang H, Schuman EM (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273: 1402-1406. (Pubitemid 26296531)
6. Frey U, Morris RG (1997) Synaptic tagging and long-term potentiation. Nature 385: 533-536. (Pubitemid 27074671)
7. Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, et al. (1997) Synapsespecific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage. Cell 91: 927-938. (Pubitemid 28028772)
8. Klann E, Sweatt JD (2008) Altered protein synthesis is a trigger for long-term memory formation. Neurobiol Learn Mem 89: 247-259. (Pubitemid 351318266)
9. Alberini CM (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89: 121-145.
10. Cohen-Armon M, Visochek L, Katzoff A, Levitan D, Susswein AJ, et al. (2004) Long-term memory requires polyADP-ribosylation. Science 304: 1820-1822. (Pubitemid 38787901)
11. Hernandez AI, Wolk J, Hu JY, Liu J, Kurosu T, et al. (2009) Poly-(ADP-ribose) polymerase-1 is necessary for long-term facilitation in Aplysia. The Journal of neuroscience : the official journal of the Society for Neuroscience 29: 9553-9562.
12. Goldberg S, Visochek L, Giladi E, Gozes I, Cohen-Armon M (2009) PolyADP-ribosylation is required for long-term memory formation in mammals. Journal of neurochemistry 111: 72-79.
13. Fontan-Lozano A, Suarez-Pereira I, Horrillo A, del-Pozo-Martin Y, Hmadcha A, et al. (2010) Histone H1 poly[ADP]-ribosylation regulates the chromatin alterations required for learning consolidation. The Journal of neuroscience : the official journal of the Society for Neuroscience 30: 13305-13313.
14. Guetg C, Scheifele F, Rosenthal F, Hottiger MO, Santoro R (2012) Inheritance of silent rDNA chromatin is mediated by PARP1 via noncoding RNA. Mol Cell 45: 790-800.
15. Boamah EK, Kotova E, Garabedian M, Jarnik M, Tulin AV (2012) Poly(ADP-Ribose) polymerase 1 (PARP-1) regulates ribosomal biogenesis in Drosophila nucleoli. PLoS Genet 8: e1002442.
16. Brewer GJ, Torricelli JR, Evege EK, Price PJ (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J Neurosci Res 35: 567-576. (Pubitemid 23215708)
17. Jiao Y, Sun Z, Lee T, Fusco FR, Kimble TD, et al. (1999) A simple and sensitive antigen retrieval method for free-floating and slide-mounted tissue sections. J Neurosci Methods 93: 149-162.
18. Barber RD, Harmer DW, Coleman RA, Clark BJ (2005) GAPDH as a housekeeping gene: analysis of GAPDH mRNA expression in a panel of 72 human tissues. Physiol Genomics 21: 389-395. (Pubitemid 40898499)
19. Wilson DM 3rd, Bianchi C (1999) Improved immunodetection of nuclear antigens after sodium dodecyl sulfate treatment of formaldehyde-fixed cells. J Histochem Cytochem 47: 1095-1100.
20. Sirri V, Urcuqui-Inchima S, Roussel P, Hernandez-Verdun D (2008) Nucleolus: the fascinating nuclear body. Histochem Cell Biol 129: 13-31. (Pubitemid 50005910)
21. Hernandez-Verdun D (1991) The nucleolus today. J Cell Sci 99 (Pt 3): 465-471.
22. Hernandez-Verdun D (2006) The nucleolus: a model for the organization of nuclear functions. Histochem Cell Biol 126: 135-148.
23. Guetg C, Santoro R (2012) Noncoding RNAs link PARP1 to heterochromatin. Cell Cycle 11: 2217-2218.
24. 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 & development 16: 2108-2119.
25. Chen M, Jiang P (2004) Altered subcellular distribution of nucleolar protein fibrillarin by actinomycin D in HEp-2 cells. Acta Pharmacol Sin 25: 902-906. (Pubitemid 38915448)
26. Goldberg IH, Reich E (1964) Actinomycin Inhibition of Rna Synthesis Directed by DNA. Fed Proc 23: 958-964.
27. Perry RP, Kelley DE (1970) Inhibition of RNA synthesis by actinomycin D: characteristic dose-response of different RNA species. J Cell Physiol 76: 127-139.
28. Toku S, Nabeshima Y, Ogata K (1983) Effects of low dose actinomycin D treatment in vivo on the biosynthesis of ribosomal proteins in rat liver. J Biochem 93: 349-359. (Pubitemid 13073940)
29. Kill IR (1996) Localisation of the Ki-67 antigen within the nucleolus. Evidence for a fibrillarin-deficient region of the dense fibrillar component. J Cell Sci 109 (Pt 6): 1253-1263.
30. Christensen MO, Krokowski RM, Barthelmes HU, Hock R, Boege F, et al. (2004) Distinct effects of topoisomerase I and RNA polymerase I inhibitors suggest a dual mechanism of nucleolar/nucleoplasmic partitioning of topoisomerase I. J Biol Chem 279: 21873-21882. (Pubitemid 38679376)
31. Kalita K, Makonchuk D, Gomes C, Zheng JJ, Hetman M (2008) Inhibition of nucleolar transcription as a trigger for neuronal apoptosis. J Neurochem 105: 2286-2299. (Pubitemid 351782259)
32. Bensaude O (2011) Inhibiting eukaryotic transcription: Which compound to choose? How to evaluate its activity? Transcription 2: 103-108.
33. Hetman M, Pietrzak M (2012) Emerging roles of the neuronal nucleolus. Trends Neurosci 35: 305-314.
34. Desnoyers S, Kaufmann SH, Poirier GG (1996) Alteration of the nucleolar localization of poly(ADP-ribose) polymerase upon treatment with transcription inhibitors. Exp Cell Res 227: 146-153. (Pubitemid 26293425)
35. Drygin D, Rice WG, Grummt I (2010) The RNA polymerase I transcription machinery: an emerging target for the treatment of cancer. Annu Rev Pharmacol Toxicol 50: 131-156.
36. Burger K, Muhl B, Harasim T, Rohrmoser M, Malamoussi A, et al. (2010) Chemotherapeutic drugs inhibit ribosome biogenesis at various levels. J Biol Chem 285: 12416-12425.
37. Haddach M, Pierre F, Regan CF, Borsan C, Michaux J, et al. (2012) Synthesis and SAR of inhibitors of protein kinase CK2: novel tricyclic quinoline analogs. Bioorg Med Chem Lett 22: 45-48.
38. Bywater MJ, Poortinga G, Sanij E, Hein N, Peck A, et al. (2012) Inhibition of RNA polymerase I as a therapeutic strategy to promote cancer-specific activation of p53. Cancer Cell 22: 51-65.
39. Seamon KB, Padgett W, Daly JW (1981) Forskolin: unique diterpene activator of adenylate cyclase in membranes and in intact cells. Proc Natl Acad Sci U S A 78: 3363-3367. (Pubitemid 11059290)
40. Castellucci VF, Kandel ER, Schwartz JH, Wilson FD, Nairn AC, et al. (1980) Intracellular injection of t he catalytic subunit of cyclic AMP-dependent protein kinase simulates facilitation of transmitter release underlying behavioral sensitization in Aplysia. Proc Natl Acad Sci U S A 77: 7492-7496. (Pubitemid 11131157)
41. Bacskai BJ, Hochner B, Mahaut-Smith M, Adams SR, Kaang BK, et al. (1993) Spatially resolved dynamics of cAMP and protein kinase A subunits in Aplysia sensory neurons. Science 260: 222-226. (Pubitemid 23140889)
42. Abel T, Nguyen PV, Barad M, Deuel TA, Kandel ER, et al. (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88: 615-626. (Pubitemid 27152404)
43. Sgambato V, Pages C, Rogard M, Besson MJ, Caboche J (1998) Extracellular signal-regulated kinase (ERK) controls immediate early gene induction on corticostriatal stimulation. J Neurosci 18: 8814-8825. (Pubitemid 28491747)
44. Gobert D, Topolnik L, Azzi M, Huang L, Badeaux F, et al. (2008) Forskolin induction of late-LTP and up-regulation of 5′ TOP mRNAs translation via mTOR, ERK, and PI3K in hippocampal pyramidal cells. Journal of neurochemistry 106: 1160-1174.
45. Castellucci VF, Frost WN, Goelet P, Montarolo PG, Schacher S, et al. (1986) Cell and molecular analysis of long-term sensitization in Aplysia. J Physiol (Paris) 81: 349-357. (Pubitemid 17051247)
46. Schacher S, Castellucci VF, Kandel ER (1988) cAMP evokes long-term facilitation in Aplysia sensory neurons that requires new protein synthesis. Science 240: 1667-1669.
47. Mayer C, Grummt I (2006) Ribosome biogenesis and cell growth: mTOR coordinates transcription by all three classes of nuclear RNA polymerases. Oncogene 25: 6384-6391. (Pubitemid 44582283)
48. Grummt I (2003) Life on a planet of its own: regulation of RNA polymerase I transcription in the nucleolus. Genes Dev 17: 1691-1702.
49. Russell J, Zomerdijk JC (2005) RNA-polymerase-I-directed rDNA transcription, life and works. Trends Biochem Sci 30: 87-96. (Pubitemid 40187301)
50. Paredes S, Maggert KA (2009) Ribosomal DNA contributes to global chromatin regulation. Proc Natl Acad Sci U S A 106: 17829-17834.
51. Vargas JP, Rodriguez F, Liqm JC, Arias JL, Salas C (2000) Spatial learning-induced increase in the argyrophilic nucleolar organizer region of dorsolateral telencephalic neurons in goldfish. Brain research 865: 77-84. (Pubitemid 30256208)
52. Richter JD, Klann E (2009) Making synaptic plasticity and memory last: mechanisms of translational regulation. Genes Dev 23: 1-11.
53. Gomes C, Smith SC, Youssef MN, Zheng JJ, Hagg T, et al. (2011) RNA polymerase 1-driven transcription as a mediator of BDNF-induced neurite outgrowth. J Biol Chem 286: 4357-4363.
54. 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)
55. Day JJ, Sweatt JD (2011) Epigenetic modifications in neurons are essential for formation and storage of behavioral memory. Neuropsychopharmacology 36: 357-358.
56. Day JJ, Sweatt JD (2012) Epigenetic treatments for cognitive impairments. Neuropsychopharmacology 37: 247-260.
57. Pederson T, Tsai RY (2009) In search of nonribosomal nucleolar protein function and regulation. J Cell Biol 184: 771-776.
58. Parlato R, Kreiner G (2013) Nucleolar activity in neurodegenerative diseases: a missing piece of the puzzle? J Mol Med (Berl) 91: 541-547.
59. Pietrzak M, Rempala G, Nelson PT, Zheng JJ, Hetman M (2011) Epigenetic silencing of nucleolar rRNA genes in Alzheimer's disease. PloS one 6: e22585.
60. Kiryk A, Sowodniok K, Kreiner G, Rodriguez-Parkitna J, Sonmez A, et al. (2013) Impaired rRNA synthesis triggers homeostatic responses in hippocampal neurons. Front Cell Neurosci 7: 207.