Selective localization of Arc mRNA in dendrites involves activity- and translation-dependent mRNA degradation

Journal of Neuroscience

Volumn 34, Issue 13, 2014, Pages 4481-4493

  Farris, Shannon ^a   Lewandowski, Gail ^a   Cox, Conor D ^a   Steward, Oswald ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Arc Arg3.1; mRNA degradation; mRNA localization; NMDA receptors; Protein synthesis; Synapse

Indexed keywords

MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARC GENE; ARTICLE; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; FEMALE; FLUORESCENCE IN SITU HYBRIDIZATION; GENE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; RAT; RNA DEGRADATION; RNA TRANSLATION; SYNAPSE; SYNAPTIC POTENTIAL;

ARC/ARG3.1; MRNA DEGRADATION; MRNA LOCALIZATION; NMDA RECEPTORS; PROTEIN SYNTHESIS; SYNAPSE;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CYTOSKELETAL PROTEINS; DENDRITES; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION; HIPPOCAMPUS; NERVE TISSUE PROTEINS; NEURONS; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; RNA STABILITY; RNA, MESSENGER; SIGNAL TRANSDUCTION; SYNAPSES; TIME FACTORS; TRANSCRIPTION, GENETIC;

EID: 84897888752     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4944-13.2014     Document Type: Article

References (33)

1. Ashraf SI, McLoon AL, Sclarsic SM, Kunes S (2006) Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124:191-205. CrossRef Medline
2. Banerjee S, Neveu P, Kosik KS (2009) A coordinated local translational control point at the synapse involving relief from silencing and MOV10 degradation. Neuron 64:871-884. CrossRef Medline
3. Batish M, van den Bogaard P, Kramer FR, Tyagi S (2012) Neuronal m RNAs travel singly into dendrites. Proc Natl Acad Sci U S A 109:4645-4650. CrossRef Medline
4. Cochran BH, Reffel AC, Stiles CD (1983) Molecular cloning of gene sequences regulated by platelet-derived growth factor. Cell 33:939-947. CrossRef Medline
5. Durand S, Lykke-Andersen J (2013) Nonsense-mediated m RNA decay occurs during e IF4F-dependent translation in human cells. Nat Struct Mol Biol 20:702-709. CrossRef Medline
6. Gao Y, Tatavarty V, Korza G, Levin MK, Carson JH (2008) Multiplexed dendritic targeting of α calcium calmodulin-dependent protein kinase II, neurogranin, and activity-regulated cytoskeleton-associated protein RNAs by the A2 pathway. Mol Biol Cell 19:2311-2327. CrossRef Medline
7. Giorgi C, Yeo GW, Stone ME, Katz DB, Burge C, Turrigiano G, Moore MJ (2007) The EJC factor e IF4AIII modulates synaptic strength and neuronal protein expression. Cell 130:179-191. CrossRef Medline
8. 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
9. 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
10. 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
11. Håvik B, Røkke H, Bårdsen K, Davanger S, Bramham CR (2003) Bursts of high-frequency stimulation trigger rapid delivery of pre-existing α-Ca MKII m RNA to synapses: a mechanism in dendritic protein synthesis during long-term potentiation in adult awake rats. Eur J Neurosci 17:2679-2689. CrossRef Medline
12. Huang F, Chotiner JK, Steward O (2007) Actin polymerization and ERK phosphorylation are required for Arc/Arg3.1 m RNA targeting to activated synaptic sites on dendrites. J Neurosci 27:9054-9067. CrossRef Medline
13. Kanai Y, Dohmae N, Hirokawa N (2004) Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43:513-525. CrossRef Medline
14. Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030-1038. CrossRef Medline
15. Kiebler MA, Bassell GJ (2006) Neuronal RNA granules: movers and makers. Neuron 51:685-690. CrossRef Medline
16. Laird-Offringa IA, de Wit CL, Elfferich P, van der Eb AJ (1990) Poly(A) tail shortening is the translation-dependent step in c-myc m RNA degradation. Mol Cell Biol 10:6132-6140. CrossRef Medline
17. Lau LF, Nathans D (1987) Expression of a set of growth-related immediate early genes in BALB/c 3T3 cells: coordinate regulation with c-fos or c-myc. Proc Natl Acad Sci U S A 84:1182-1186. CrossRef Medline
18. 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
19. 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
20. 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
21. Mikl M, Vendra G, Kiebler MA (2011) Independent localization of MAP2, Ca MKIIα and β-actin RNAs in low copy numbers. EMBO Rep 12:1077-1084. CrossRef Medline
22. Muddashetty RS, Nalavadi VC, Gross C, Yao X, Xing L, Laur O, Warren ST, Bassell GJ (2011) Reversible inhibition of PSD-95 m RNA translation by mi R-125a, FMRP phosphorylation, and m Glu R signaling. Mol Cell 42: 673-688. CrossRef Medline
23. Nguyen PV, Kandel ER (1996) A macromolecular synthesis-dependent late phase of long-term potentiation requiring c AMP in the medial perforant pathway of rat hippocampal slices. J Neurosci 16:3189-3198. Medline
24. 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 Ca MKIIβ. Cell 149:886-898. CrossRef Medline
25. Park S, Park JM, Kim S, Kim JA, Shepherd JD, Smith-Hicks CL, Chowdhury S, Kaufmann W, Kuhl D, Ryazanov AG, Huganir RL, Linden DJ, Worley PF (2008) Elongation factor 2 and fragile X mental retardation protein control the dynamic translation of Arc/Arg3.1 essential for m Glu R-LTD. Neuron 59:70-83. CrossRef Medline
26. Shan J, Munro TP, Barbarese E, Carson JH, Smith R (2003) A molecular mechanism for m RNA trafficking in neuronal dendrites. J Neurosci 23: 8859-8866. Medline
27. Steward O, Worley PF (2001) Selective targeting of newly synthesized Arc m RNA to active synapses requires NMDA receptor activation. Neuron 30:227-240. CrossRef Medline
28. Steward O, Wallace CS, Lyford GL, Worley PF (1998) Synaptic activation causes the m RNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21:741-751. CrossRef Medline
29. Swanger SA, Bassell GJ (2011) Making and breaking synapses through local m RNA regulation. Curr Opin Genet Dev 21:414-421. CrossRef Medline
30. 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
31. Wallace CS, Lyford GL, Worley PF, Steward O (1998) Differential intracellular sorting of immediate early gene m RNAs depends on signals in the m RNA sequence. J Neurosci 18:26-35. Medline
32. Wang F, Flanagan J, Su N, Wang LC, Bui S, Nielson A, Wu X, Vo HT, Ma XJ, Luo Y (2012) RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues. J Mol Diagn 14:22-29. CrossRef Medline
33. Wilson T, Treisman R (1988) Removal of poly(A) and consequent degradation of c-fos m RNA facilitated by 3' AU-rich sequences. Nature 336:396-399. CrossRef Medline