EPAC Null Mutation Impairs Learning and Social Interactions via Aberrant Regulation of miR-124 and Zif268 Translation

Neuron

Volumn 73, Issue 4, 2012, Pages 774-788

  Yang, Ying ^a,b   Shu, Xiaogang ^b   Liu, Dan ^a   Shang, You ^b,c   Wu, Yan ^b,c   Pei, Lei ^a   Xu, Xin ^b   Tian, Qing ^a   Zhang, Jian ^b   Qian, Kun ^b   Wang, Ya Xian ^d   Petralia, Ronald S ^d   Tu, Weihong ^b   Zhu, Ling Qiang ^a   Wang, Jian Zhi ^a   Lu, Youming ^a,b  

^a BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^d NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPAC1 PROTEIN; EPAC2 PROTEIN; EXCHANGE PROTEIN DIRECTLY ACTIVATED BY CAMP; GUANINE NUCLEOTIDE EXCHANGE FACTOR; RAP1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPAC GENE; EPAC1 GENE; EPAC2 GENE; EXCITATORY POSTSYNAPTIC POTENTIAL; FOREBRAIN; GENE; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSCRIPTION; KNOCKOUT MOUSE; LEARNING; LONG TERM POTENTIATION; MALE; MEMORY DISORDER; MIR 124 GENE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA TRANSLATION; SOCIAL INTERACTION; SPATIAL LEARNING; SYNAPSE; ZIF268 GENE;

ANALYSIS OF VARIANCE; ANIMALS; BIOPHYSICS; CHROMATIN IMMUNOPRECIPITATION; CORPUS STRIATUM; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; EARLY GROWTH RESPONSE PROTEIN 1; ELECTRIC STIMULATION; EXPLORATORY BEHAVIOR; GENE EXPRESSION PROFILING; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HIPPOCAMPUS; INTERPERSONAL RELATIONS; LEARNING DISORDERS; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MICE; MICE, TRANSGENIC; MICRORNAS; MICROSCOPY, ELECTRON; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PATCH-CLAMP TECHNIQUES; PROTEIN BIOSYNTHESIS; RAP1 GTP-BINDING PROTEINS; REACTION TIME; SIGNAL TRANSDUCTION; SILVER STAINING; TRANSFECTION;

EID: 84863154673     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.02.003     Document Type: Article

References (58)

1. Arvanitis D.N., Jungas T., Behar A., Davy A. Ephrin-B1 reverse signaling controls a posttranscriptional feedback mechanism via miR-124. Mol. Cell. Biol. 2010, 30:2508-2517.
2. Bacchelli E., Blasi F., Biondolillo M., Lamb J.A., Bonora E., Barnby G., Parr J., Beyer K.S., Klauck S.M., Poustka A., et al. Screening of nine candidate genes for autism on chromosome 2q reveals rare nonsynonymous variants in the cAMP-GEFII gene. Mol. Psychiatry 2003, 8:916-924. International Molecular Genetic Study of Autism Consortium (IMGSAC).
3. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004, 116:281-297.
4. Baumgärtel K., Genoux D., Welzl H., Tweedie-Cullen R.Y., Koshibu K., Livingstone-Zatchej M., Mamie C., Mansuy I.M. Control of the establishment of aversive memory by calcineurin and Zif268. Nat. Neurosci. 2008, 11:572-578.
5. Benito E., Barco A. CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci. 2010, 33:230-240.
6. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
7. Bos J.L. Epac proteins: multi-purpose cAMP targets. Trends Biochem. Sci. 2006, 31:680-686.
8. Bozon B., Davis S., Laroche S. A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 2003, 40:695-701.
9. Cao X., Pfaff S.L., Gage F.H. A functional study of miR-124 in the developing neural tube. Genes Dev. 2007, 21:531-536.
10. Chepurny O.G., Leech C.A., Kelley G.G., Dzhura I., Dzhura E., Li X., Rindler M.J., Schwede F., Genieser H.G., Holz G.G. Enhanced Rap1 activation and insulin secretagogue properties of an acetoxymethyl ester of an Epac-selective cyclic AMP analog in rat INS-1 cells: studies with 8-pCPT-2'-O-Me-cAMP-AM. J. Biol. Chem. 2009, 284:10728-10736.
11. Clark A.M., Goldstein L.D., Tevlin M., Tavaré S., Shaham S., Miska E.A. The microRNA miR-124 controls gene expression in the sensory nervous system of Caenorhabditis elegans. Nucleic Acids Res. 2010, 38:3780-3793.
12. Custer K.L., Austin N.S., Sullivan J.M., Bajjalieh S.M. Synaptic vesicle protein 2 enhances release probability at quiescent synapses. J. Neurosci. 2006, 26:1303-1313.
13. de Rooij J., Zwartkruis F.J., Verheijen M.H., Cool R.H., Nijman S.M., Wittinghofer A., Bos J.L. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 1998, 396:474-477.
14. Edmonds B., Gibb A.J., Colquhoun D. Mechanisms of activation of glutamate receptors and the time course of excitatory synaptic currents. Annu. Rev. Physiol. 1995, 57:495-519.
15. Farnsworth C.L., Marshall M.S., Gibbs J.B., Stacey D.W., Feig L.A. Preferential inhibition of the oncogenic form of RasH by mutations in the GAP binding/" effector" domain. Cell 1991, 64:625-633.
16. Fischbach S.J., Carew T.J. MicroRNAs in memory processing. Neuron 2009, 63:714-716.
17. Fujimoto K., Shibasaki T., Yokoi N., Kashima Y., Matsumoto M., Sasaki T., Tajima N., Iwanaga T., Seino S. Piccolo, a Ca2+ sensor in pancreatic beta-cells. Involvement of cAMP-GEFII.Rim2. Piccolo complex in cAMP-dependent exocytosis. J. Biol. Chem. 2002, 277:50497-50502.
18. Geschwind D.H., Levitt P. Autism spectrum disorders: developmental disconnection syndromes. Curr. Opin. Neurobiol. 2007, 17:103-111.
19. Hall J., Thomas K.L., Everitt B.J. Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nat. Neurosci. 2000, 3:533-535.
20. He L., Hannon G.J. MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 2004, 5:522-531.
21. Impey S., McCorkle S.R., Cha-Molstad H., Dwyer J.M., Yochum G.S., Boss J.M., McWeeney S., Dunn J.J., Mandel G., Goodman R.H. Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell 2004, 119:1041-1054.
22. 2+ regulators in neurotransmitter release. Neuron 1999, 24:1003-1016.
23. Jones M.W., Errington M.L., French P.J., Fine A., Bliss T.V., Garel S., Charnay P., Bozon B., Laroche S., Davis S. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat. Neurosci. 2001, 4:289-296.
24. Kaeser P.S., Deng L., Wang Y., Dulubova I., Liu X., Rizo J., Südhof T.C. RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 2011, 144:282-295.
25. Kawasaki H., Springett G.M., Mochizuki N., Toki S., Nakaya M., Matsuda M., Housman D.E., Graybiel A.M. A family of cAMP-binding proteins that directly activate Rap1. Science 1998, 282:2275-2279.
26. Kelleher R.J., Bear M.F. The autistic neuron: troubled translation?. Cell 2008, 135:401-406.
27. Kelleher R.J., Govindarajan A., Jung H.Y., Kang H., Tonegawa S. Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 2004, 116:467-479.
28. Kessels H.W., Malinow R. Synaptic AMPA receptor plasticity and behavior. Neuron 2009, 61:340-350.
29. Krichevsky A.M., King K.S., Donahue C.P., Khrapko K., Kosik K.S. A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 2003, 9:1274-1281.
30. Levy S.E., Mandell D.S., Schultz R.T. Autism. Lancet 2009, 374:1627-1638.
31. Lim L.P., Lau N.C., Garrett-Engele P., Grimson A., Schelter J.M., Castle J., Bartel D.P., Linsley P.S., Johnson J.M. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433:769-773.
32. 2+)-permeable AMPA receptor channels primes cell death in transient forebrain ischemia. Neuron 2004, 43:43-55.
33. Liu C., Takahashi M., Li Y., Dillon T.J., Kaech S., Stork P.J. The interaction of Epac1 and Ran promotes Rap1 activation at the nuclear envelope. Mol. Cell. Biol. 2010, 30:3956-3969.
34. Malenka R.C., Nicoll R.A. Long-term potentiation-a decade of progress?. Science 1999, 285:1870-1874.
35. Nicoll R.A., Malenka R.C. Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 1995, 377:115-118.
36. Ouyang M., Zhang L., Zhu J.J., Schwede F., Thomas S.A. Epac signaling is required for hippocampus-dependent memory retrieval. Proc. Natl. Acad. Sci. USA 2008, 105:11993-11997.
37. Peng P.L., Zhong X., Tu W., Soundarapandian M.M., Molner P., Zhu D., Lau L., Liu S., Liu F., Lu Y. ADAR2-dependent RNA editing of AMPA receptor subunit GluR2 determines vulnerability of neurons in forebrain ischemia. Neuron 2006, 49:719-733.
38. Rajasethupathy P., Fiumara F., Sheridan R., Betel D., Puthanveettil S.V., Russo J.J., Sander C., Tuschl T., Kandel E. Characterization of small RNAs in Aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 2009, 63:803-817.
39. Ramocki M.B., Zoghbi H.Y. Failure of neuronal homeostasis results in common neuropsychiatric phenotypes. Nature 2008, 455:912-918.
40. Rehmann H., Prakash B., Wolf E., Rueppel A., de Rooij J., Bos J.L., Wittinghofer A. Structure and regulation of the cAMP-binding domains of Epac2. Nat. Struct. Biol. 2003, 10:26-32.
41. Renaudineau S., Poucet B., Laroche S., Davis S., Save E. Impaired long-term stability of CA1 place cell representation in mice lacking the transcription factor zif268/egr1. Proc. Natl. Acad. Sci. USA 2009, 106:11771-11775.
42. Sakaba T., Neher E. Direct modulation of synaptic vesicle priming by GABA(B) receptor activation at a glutamatergic synapse. Nature 2003, 424:775-778.
43. Schratt G.M., Tuebing F., Nigh E.A., Kane C.G., Sabatini M.E., Kiebler M., Greenberg M.E. A brain-specific microRNA regulates dendritic spine development. Nature 2006, 439:283-289.
44. Schwamborn J.C., Püschel A.W. The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat. Neurosci. 2004, 7:923-929.
45. Sehrawat S., Cullere X., Patel S., Italiano J., Mayadas T.N. Role of Epac1, an exchange factor for Rap GTPases, in endothelial microtubule dynamics and barrier function. Mol. Biol. Cell 2008, 19:1261-1270.
46. Silverman J.L., Yang M., Lord C., Crawley J.N. Behavioural phenotyping assays for mouse models of autism. Nat. Rev. Neurosci. 2010, 11:490-502.
47. Soderling T.R., Derkach V.A. Postsynaptic protein phosphorylation and LTP. Trends Neurosci. 2000, 23:75-80.
48. Stark A., Brennecke J., Bushati N., Russell R.B., Cohen S.M. Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3'UTR evolution. Cell 2005, 123:1133-1146.
49. Stork P.J.S. Does Rap1 deserve a bad Rap?. Trends Biochem. Sci. 2003, 28:267-275.
50. Tu W., Xu X., Peng L., Zhong X., Zhang W., Soundarapandian M.M., Balel C., Wang M., Jia N., Zhang W., et al. DAPK1 interaction with NMDA receptor NR2B subunits mediates brain damage in stroke. Cell 2010, 140:222-234.
51. Visvanathan J., Lee S., Lee B., Lee J.W., Lee S.K. The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev. 2007, 21:744-749.
52. Walsh C.A., Morrow E.M., Rubenstein J.L.R. Autism and brain development. Cell 2008, 135:396-400.
53. Wang J., Liu S., Fu Y., Wang J.H., Lu Y. Cdk5 activation induces hippocampal CA1 cell death by directly phosphorylating NMDA receptors. Nat. Neurosci. 2003, 6:1039-1047.
54. West A.E., Chen W.G., Dalva M.B., Dolmetsch R.E., Kornhauser J.M., Shaywitz A.J., Takasu M.A., Tao X., Greenberg M.E. Calcium regulation of neuronal gene expression. Proc. Natl. Acad. Sci. USA 2001, 98:11024-11031.
55. Woolfrey K.M., Srivastava D.P., Photowala H., Yamashita M., Barbolina M.V., Cahill M.E., Xie Z., Jones K.A., Quilliam L.A., Prakriya M., Penzes P. Epac2 induces synapse remodeling and depression and its disease-associated forms alter spines. Nat. Neurosci. 2009, 12:1275-1284.
56. Zhang C.L., Katoh M., Shibasaki T., Minami K., Sunaga Y., Takahashi H., Yokoi N., Iwasaki M., Miki T., Seino S. The cAMP sensor Epac2 is a direct target of antidiabetic sulfonylurea drugs. Science 2009, 325:607-610.
57. Zhong N., Zucker R.S. cAMP acts on exchange protein activated by cAMP/cAMP-regulated guanine nucleotide exchange protein to regulate transmitter release at the crayfish neuromuscular junction. J. Neurosci. 2005, 25:208-214.
58. Zhu J.J., Qin Y., Zhao M., Van Aelst L., Malinow R. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 2002, 110:443-455.