Sustained transcription of the immediate early gene arc in the dentate gyrus after spatial exploration

Journal of Neuroscience

Volumn 33, Issue 4, 2013, Pages 1631-1639

  Ramirez Amaya, Victor ^a   Angulo Perkins, Arafat ^a   Chawla, Monica K ^c   Barnes, Carol A ^c   Rosi, Susanna ^b  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; DACTINOMYCIN; MESSENGER RNA;

ANIMAL TISSUE; ANIMLA EXPERIMENT; ARTICLE; CANNULATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENTATE GYRUS; EXPLORATORY BEHAVIOR; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC TRANSCRIPTION; GRANULE CELL; HIPPOCAMPAL CA1 REGION; IMMEDIATE EARLY GENE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPATIAL DISCRIMINATION; SYNAPTIC TRANSMISSION; TRANSCRIPTION REGULATION;

ANIMALS; CYTOSKELETAL PROTEINS; DENTATE GYRUS; EXPLORATORY BEHAVIOR; GENE EXPRESSION REGULATION; GENES, IMMEDIATE-EARLY; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; NEURONS; RATS; RATS, WISTAR; RNA, MESSENGER; SPATIAL BEHAVIOR; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84872715007     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2916-12.2013     Document Type: Article

References (53)

1. Aicardi G., Argilli E, Cappello S, Santi S, Riccio M, Thoenen H, Canossa M (2004) Induction for long-term potentiation and depression is reflected by corresponding changes in secretion of endogenous brain-derived neurotrophic factor. Proc Natl Acad Sci U S A 101:15788-15792. CrossRef Medline
2. Alme CB., Buzzetti RA, Marrone DF, Leutgeb JK, Chawla MK, Schaner MJ, Bohanick JD., Khoboko T, Leutgeb S, Moser EI, Moser MB, McNaughton BL, Barnes CA. (2010). Hippocampal granule cells opt for early retirement. Hippocampus 20:1109-1123. CrossRef Medline
3. Barnes CA., McNaughton BL. (1980). Physiological compensation for loss of afferent synapses in rat hippocampal granule cells during senescence. J Physiol 309:473-485. Medline
4. Bekinschtein P., Cammarota M, Katche C, Slipczuk L, Rossato JI, Goldin A, Izquierdo I., Medina JH. (2008). BDNF is essential to promote persistence of long-term memory storage. Proc Natl Acad Sci U S A 105:2711-2716. CrossRef Medline
5. Bingol B., Sheng M. (2011). Deconstruction for reconstruction: the role of proteolysis in neural plasticity and disease. Neuron 69:22-32. CrossRef Medline
6. Bramham CR., Messaoudi E. (2005). BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog Neurobiol 76:99-125. CrossRef Medline
7. Bramham CR., Alme MN, Bittins M, Kuipers SD, Nair RR, Pai B, Panja D, Schubert M., Soule J, Tiron A, Wibrand K. (2010). The Arc of synaptic memory. Exp Brain Res 200:125-140. CrossRef Medline
8. Chawla MK., Guzowski JF, Ramirez-Amaya V, Lipa P, Hoffman KL, Marriott LK, Worley PF, McNaughton BL, Barnes CA. (2005). Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 15:579-586. CrossRef Medline
9. Cole AJ., Saffen DW, Baraban JM, Worley PF. (1989). Rapid increase of an immediate early gene messenger RNA in hippocampal neurons by synaptic NMDA receptor activation. Nature 340:474-476. CrossRef Medline
10. Czerniawski J., Ree F, Chia C, Ramamoorthi K, Kumata Y, Otto TA. (2011). The importance of having Arc: expression of the immediate-early gene Arc is required for hippocampus-dependent fear conditioning and blocked by NMDA receptor antagonism. J Neurosci 31:11200-11207. CrossRef Medline
11. El-Sayed M, Hofman-Bang J, Mikkelsen JD. (2011). Effect of brain-derived neurotrophic factor on activity-regulated cytoskeleton-associated protein gene expression in primary frontal cortical neurons. Comparison with NMDA and AMPA. Eur J Pharmacol 660:351-357. CrossRef Medline
12. Fletcher BR., Baxter MG, Guzowski JF, Shapiro ML, Rapp PR. (2007). Selective cholinergic depletion of the hippocampus spares both behaviorally induced Arc transcription and spatial learning and memory. Hippocampus 17:227-234. CrossRef Medline
13. Giorgi C., Yeo GW, Stone ME, Katz DB, Burge C, Turrigiano G, Moore MJ (2007) The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 130:179-191. CrossRef Medline
14. Greer PL., Hanayama R, Bloodgood BL, Mardinly AR, Lipton DM, Flavell SW, Kim TK., Griffith EC, Waldon Z, Maehr R, Ploegh HL, Chowdhury S, Worley PF., Steen J, Greenberg ME. (2010). The Angelman Syndrome protein Ube3A regulates synapse development by ubiquitinating Arc. Cell 140:704-716. CrossRef Medline
15. Guzowski JF., McNaughton BL, Barnes CA, Worley PF. (1999). Environmentspecific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat Neurosci 2:1120-1124. CrossRef Medline
16. Guzowski JF., Lyford GL, Stevenson GD, Houston FP, McGaugh JL, Worley PF, Barnes CA. (2000). Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 20:3993-4001. Medline
17. Guzowski JF., Miyashita T, Chawla MK, Sanderson J, Maes LI, Houston FP, Lipa P., McNaughton BL, Worley PF, Barnes CA. (2006). Recent behavioral history modifies coupling between cell activity and Arc gene transcription in hippocampal CA1 neurons. Proc Natl Acad Sci U S A 103: 1077-1082. CrossRef Medline
18. Holahan MR., Routtenberg A. (2007). Post-translational synaptic protein modification as substrate for long-lasting, remote memory: an initial test. Hippocampus 17:93-97. CrossRef Medline
19. Hopkins ME., Bucci DJ. (2010). BDNF expression in perirhinal cortex is associated with exercise-induced improvement in object recognition memory. Neurobiol Learn Mem 94:278-284. CrossRef Medline
20. Jung MW., McNaughton BL. (1993). Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3:165-182. CrossRef Medline
21. Kang H., Welcher AA, Shelton D, Schuman EM. (1997). Neurotrophins and time: different roles for TrkB signaling in hippocampal long-term potentiation. Neuron 19:653-664. CrossRef Medline
22. Lanahan A., Worley P. (1998). Immediate-early genes and synaptic function. Neurobiol Learn Mem 70:37-43. CrossRef Medline
23. Leutgeb JK., Leutgeb S, Moser MB, Moser EI. (2007). Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science 315:961-966. CrossRef Medline
24. Link W., Konietzko U, Kauselmann G, Krug M, Schwanke B, Frey U, Kuhl D (1995) Somatodendritic expression of an immediate early gene is regulated by synaptic activity. Proc Natl Acad Sci U S A 92:5734-5738. CrossRef Medline
25. Lyford GL., Yamagata K, Kaufmann WE, Barnes CA, Sanders LK, Copeland NG, Gilbert DJ, Jenkins NA, Lanahan AA, Worley PF. (1995). Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeletonassociated protein that is enriched in neuronal dendrites. Neuron 14:433-445. CrossRef Medline
26. Maquat LE. (2004). Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat Rev Mol Cell Biol 5:89-99. CrossRef Medline
27. Marrone DF., Satvat E, Shaner MJ, Worley PF, Barnes CA. (2012). Attenuated long-term Arc expression in the aged fascia dentata. Neurobiol Aging 33:979-990. CrossRef Medline
28. Martin KC. (2001). Arc mRNA dynamics: return to sender-the NMDA receptor provides the targeting address for Arc mRNA. Trends Neurosci 24:621-623. CrossRef Medline
29. Martínez-Moreno A, Rodríguez-Durán LF, EscobarML. (2011). Late protein synthesis-dependent phases in CTA long-term memory: BDNF requirement. Front Behav Neurosci 5:61. Medline
30. McNaughton BL., MorrisRGM. (1987). Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408-415. CrossRef
31. Messaoudi E., Ying SW, Kanhema T, Croll SD, Bramham CR. (2002). Brainderived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo. J Neurosci 22:7453-7461. Medline
32. Messaoudi E., Kanhema T, Soulé J, Tiron A, Dagyte G, da Silva B, Bramham CR. (2007). Sustained Arc/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo. J Neurosci 27:10445-10455. CrossRef Medline
33. Miranda MI., Bermúdez-Rattoni F. (1999). Reversible inactivation of the nucleus basalis magnocellularis induces disruption of cortical acetylcholine release and acquisition, but not retrieval, of aversive memories. Proc Natl Acad Sci U S A 96:6478-6482. CrossRef Medline
34. Miyashita T., Kubik S, Lewandowski G, Guzowski JF. (2008). Networks of neurons, networks of genes: an integrated view of memory consolidation. Neurobiol Learn Mem 89:269-284. CrossRef Medline
35. Morgan JI., Curran T. (1989). Stimulus-transcription coupling in neurons: role of cellular immediate-early genes. Trends Neurosci 12:459-462. CrossRef Medline
36. Okuno H., Akashi K, Ishii Y, Yagishita-Kyo N, Suzuki K, Nonaka M, Kawashima T, Fujii H, Takemoto-Kimura S, Abe M, Natsume R, Chowdhury S, Sakimura K, Worley PF, Bito H. (2012). Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIβ. Cell 149:886-898. CrossRef Medline
37. Paxinos G., Watson C. (1998). The rat brain in stereotaxic coordinates, Ed 4. San Diego, CA: Academic.
38. Penner MR., Roth TL, Barnes CA, Sweatt JD. (2010). An epigenetic hypothesis of aging-related cognitive dysfunction. Front Aging Neurosci 2:9, 2010 Mar 12. Medline
39. Plath N., Ohana O, Dammermann B, Errington ML, Schmitz D, Gross C, Mao X, Engelsberg A, Mahlke C, Welzl H, Kobalz U, Stawrakakis A, Fernandez E, Waltereit R, Bick-Sander A, Therstappen E, Cooke SF, Blanquet V, Wurst W., Salmen B, et al. (2006). Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52:437-444. CrossRef Medline
40. Ramírez-Amaya V, Vazdarjanova A, Mikhael D, Rosi S, Worley PF, Barnes CA. (2005). Spatial exploration-induced Arc mRNA and protein expression: evidence for selective, network-specific reactivation. J Neurosci 25: 1761-1768. CrossRef Medline
41. Rosi S., Ramirez-Amaya V, Vazdarjanova A, Worley PF, Barnes CA, Wenk GL (2005) Neuroinflammation alters the hippocampal pattern of behaviorally induced Arc expression. J Neurosci 25:723-7231. CrossRef Medline
42. Rosi S., Ramirez-Amaya V, Vazdarjanova A, Esparza EE, Larkin PB, Fike JR, Wenk GL, Barnes CA. (2009). Accuracy of hippocampal network activity is disrupted by neuroinflammation: rescue by memantine. Brain 132:2464-2477. CrossRef Medline
43. Sandoval CJ., Martínez-Claros M, Bello-Medina PC, Pérez O, Ramírez-Amaya V. (2011). When are new hippocampal neurons, born in the adult brain, integrated into the network that processes spatial information? PLoS One 6:e17689. CrossRef Medline
44. Santi S., Cappello S, Riccio M, Bergami M, Aicardi G, Schenk U, Matteoli M, Canossa M. (2006). Hippocampal neurons recycle BDNF for activitydependent secretion and LTP maintenance. EMBO J 25:4372-4380. CrossRef Medline
45. Sarter M., Bruno JP, Givens B. (2003). Attentional functions of cortical cholinergic inputs: what does it mean for learning and memory? Neurobiol Learn Mem 80:245-256. CrossRef Medline
46. Shen J., Kudrimoti HS, McNaughton BL, Barnes CA. (1998). Reactivation of neuronal ensembles in hippocampal dentate gyrus during sleep after spatial experience. J Sleep Res 7:6-16. CrossRef Medline
47. Shen K., Teruel MN, Connor JH, Shenolikar S, Meyer T. (2000). Molecular memory by reversible translocation of calcium/calmodulin-dependent protein kinase II. Nat Neurosci 3:881-886. CrossRef Medline
48. Shepherd JD., Bear MF. (2011). New views of Arc, a master regulator of synaptic plasticity. Nat Neurosci 14:279-284. CrossRef Medline
49. Steward O., Worley PF. (2001). Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron 30:227-240. CrossRef Medline
50. Teber I., Köhling R, Speckmann EJ, Barnekow A, Kremerskothen J. (2004). Muscarinic acetylcholine receptor stimulation induces expression of the activity-regulated cytoskeleton-associatedgene (ARC). Brain Res Mol Brain Res 121:131-136. Medline
51. Trifilieff P., Herry C, Vanhoutte P, Caboche J, Desmedt A, Riedel G, Mons N, Micheau J. (2006). Foreground contextual fear memory consolidation requires two independent phases of hippocampal ERK/CREB activation. Learn Mem 13:349-358. CrossRef Medline
52. Vazdarjanova A., Guzowski JF. (2004). Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J Neurosci 24:6489-6496. CrossRef Medline
53. Vazdarjanova A., McNaughton BL, Barnes CA, Worley PF, Guzowski JF (2002) Experience-dependent coincident expression of the effector immediate-early genes arc and Homer 1a in hippocampal and neocortical neuronal networks. J Neurosci 22:10067-10071. Medline