Involvement of cAMP-guanine nucleotide exchange factor II in hippocampal long-term depression and behavioral flexibility

Molecular Brain

Volumn 8, Issue 1, 2015, Pages

  Lee, Kyungmin ^a   Kobayashi, Yuki ^b   Seo, Hyunhyo ^a   Kwak, Ji Hye ^a   Masuda, Akira ^b   Lim, Chae Seok ^d   Lee, Hye Ryeon ^d   Kang, Sukjae Joshua ^d   Park, Pojeong ^d   Sim, Su Eon ^d   Kogo, Naomi ^b   Kawasaki, Hiroaki ^c   Kaang, Bong Kiun ^d   Itohara, Shigeyoshi ^b  

^a Kyungpook National University School of Medicine   (South Korea)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^c FUKUOKA UNIVERSITY   (Japan)

^d Seoul National University   (South Korea)

Author keywords

Knockout mice; Reversal learning; Spatial memory; Synaptic plasticity

Indexed keywords

CYCLIC AMP; GUANINE NUCLEOTIDE EXCHANGE FACTOR; GUANINE NUCLEOTIDE EXCHANGE FACTOR II; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; UNCLASSIFIED DRUG; RAPGEF4 PROTEIN, MOUSE;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOMATION; COGNITION; CONTROLLED STUDY; FEMALE; GENE DELETION; HIPPOCAMPAL CA1 REGION; KNOCKOUT MOUSE; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MORRIS WATER MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRESYNAPTIC INHIBITION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHAFFER COLLATERAL PATHWAY; SPATIAL LEARNING; SPATIAL MEMORY; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; BRAIN; C57BL MOUSE; DEFICIENCY; ELECTRIC SHOCK; HIPPOCAMPUS; LEARNING; METABOLISM;

ANIMALIA; MUS;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; ELECTROSHOCK; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HIPPOCAMPUS; LEARNING; LONG-TERM POTENTIATION; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES;

EID: 84934956108     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/s13041-015-0130-1     Document Type: Article

References (44)

1. de Rooij J, Zwartkruis FJ, Verheijen MH, Cool RH, Nijman SM, Wittinghofer A, et al. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature. 1998;396:474-7.
2. Kawasaki H, Springett GM, Mochizuki N, Toki S, Nakaya M, Matsuda M, et al. A family of cAMP-binding proteins that directly activate Rap1. Science. 1998;282:2275-9.
3. Huang CC, Hsu KS. 2006. Presynaptic mechanism underlying cAMP-induced synaptic potentiation in medial prefrontal cortex pyramidal neurons. Mol Pharmacol. 2006;69:846-56.
4. Gekel I, Neher E. Application of an Epac activator enhances neurotransmitter release at excitatory central synapses. J Neurosci. 2008;28:7991-8002.
5. Gelinas JN, Banko JL, Peters MM, Klann E, Weeber EJ, Nguyen PV. Activation of exchange protein activated by cyclic-AMP enhances long-lasting synaptic potentiation in the hippocampus. Learn Mem. 2008;15:403-11.
6. Zhu JJ, Qin Y, Zhao M, Van Aelst L, Malinow R. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell. 2002;110:443-55.
7. Ostroveanu A, Van Der Zee EA, Eisel UL, Schmidt M, Nijholt IM. Exchange protein activated by cyclic AMP 2 (Epac2) plays a specific and time-limited role in memory retrieval. Hippocampus. 2010;20:1018-26.
8. Srivastava DP, Jones KA, Woolfrey KM, Burgdorf J, Russell TA, Kalmbach A, et al. Social, communication, and cortical structural impairments in Epac2-deficient mice. J Neurosci. 2012;32:11864-78.
9. Yang Y, Shu X, Liu D, Shang Y, Wu Y, Pei L, et al. EPAC null mutation impairs learning and social interactions via aberrant regulation of miR-124 and Zif268 translation. Neuron. 2012;73:774-88.
10. Manabe T, Wyllie DJ, Perkel DJ, Nicoll RA. Modulation of synaptic transmission and long-term potentiation: effects on paired pulse facilitation and EPSC variance in the CA1 region of the hippocampus. J Neurophysiol. 1993;70:1451-9.
11. Zhu Y, Pak D, Qin Y, McCormack SG, Kim MJ, Baumgart JP, et al. Rap2-JNK removes synaptic AMPA receptors during depotentiation. Neuron. 2005;46:905-16.
12. Dudek SM, Bear MF. Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A. 1992;89:4363-7.
13. Krackow S, Vannoni E, Codita A, Mohammed AH, Cirulli F, Branchi I, et al. Consistent behavioral phenotype differences between inbred mouse strains in the IntelliCage. Genes Brain Behav. 2010;9:722-31.
14. Voikar V, Colacicco G, Gruber O, Vannoni E, Lipp HP, Wolfer DP. Conditioned response suppression in the IntelliCage: assessment of mouse strain differences and effects of hippocampal and striatal lesions on acquisition and retention of memory. Behav Brain Res. 2010;213:304-12.
15. Weible AP, Rowland DC, Pang R, Kentros C. Neural correlates of novel object and novel location recognition behavior in the mouse anterior cingulate cortex. J Neurophysiol. 2009;102:2055-68.
16. Kemp A, Manahan-Vaughan D. Hippocampal long-term depression: master or minion in declarative memory processes? Trends Neurosci. 2007;30:111-8.
17. Nicholls RE, Alarcon JM, Malleret G, Carroll RC, Grody M, Vronskaya S, et al. Transgenic mice lacking NMDAR-dependent LTD exhibit deficits in behavioral flexibility. Neuron. 2008;58:104-17.
18. Kim JI, Lee HR, Sim SE, Baek J, Yu NK, Choi JH, et al. PI3Kγ is required for NMDA receptor-dependent long-term depression and behavioral flexibility. Nat Neurosci. 2011;14:1447-54.
19. Kandel ER, Schwartz JH. Molecular biology of learning: modulation of transmitter release. Science. 1982;218:433-43.
20. Woolfrey KM, Srivastava DP, Photowala H, Yamashita M, Barbolina MV, Cahill ME, et al. Epac2 induces synapse remodeling and depression and its disease-associated forms alter spines. Nat Neurosci. 2009;12:1275-84.
21. Tzounopoulos T, Janz R, Sudhof TC, Nicoll RA, Malenka RC. A role for cAMP in long-term depression at hippocampal mossy fiber synapses. Neuron. 1998;21:837-45.
22. Trudeau LE, Fang Y, Haydon PG. Modulation of an early step in the secretory machinery in hippocampal nerve terminals. Proc Natl Acad Sci U S A. 1998;95:7163-8.
23. Cheung U, Atwood HL, Zucker RS. 2006. Presynaptic effectors contributing to cAMP-induced synaptic potentiation in Drosophila. J Neurobiol. 2006;66:273-80.
24. Zhong N, Zucker RS. 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;25:208-14.
25. Kaneko M, Takahashi T. Presynaptic mechanism underlying cAMP-dependent synaptic potentiation. J Neurosci. 2006;24:5202-8.
26. Jordan BA, Fernholz BD, Boussac M, Xu C, Grigorean G, Ziff EB, et al. Identification and verification of novel rodent postsynaptic density proteins. Mol Cell Proteomics. 2004;3:857-71.
27. Ster J, de Bock F, Bertaso F, Abitbol K, Daniel H, Bockaert J, et al. Epac mediates PACAP-dependent long-term depression in the hippocampus. J Physiol. 2009;587:101-13.
28. Gerlai R. Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype? Trends Neurosci. 1996;19:177-81.
29. Peirce JL, Derr R, Shendure J, Kolata T, Silver LM. A major influence of sex-specific loci on alcohol preference in C57Bl/6 and DBA/2 inbred mice. Mamm Genome. 1998;9:942-8.
30. Sandberg R, Yasuda R, Pankratz DG, Carter TA, Del Rio JA, Wodicka L, et al. Regional and strain-specific gene expression mapping in the adult mouse brain. Proc Natl Acad Sci U S A. 2000;97:11038-43.
31. Pavlidis P, Noble WS. Analysis of strain and regional variation in gene expression in mouse brain. Genome Biol. 2001;2:RESEARCH0042.1-15.
32. Kraus P, Xing X, Lim SL, Fun ME, Sivakamasundari V, Yap SP, et al. Mouse strain specific gene expression differences for illumina microarray expression profiling in embryos. BMC Res Notes. 2012;14:232.
33. Fiering S, Epner E, Robinson K, Zhuang Y, Telling A, Hu M, et al. Targeted deletion of 5'HS2 of the murine beta-globin LCR reveals that it is not essential for proper regulation of the beta-globin locus. Genes Dev. 1995;9:2203-13.
34. Olson EN, Arnold HH, Rigby PW, Wold BJ. Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell. 1996;85:1-4.
35. Kanki H, Suzuki H, Itohara S. High-efficiency CAG-FLPe deleter mice in C57BL/6 J background. Exp Anim. 2006;55:137-41.
36. Manahan-Vaughan D, Braunewell KH. Novelty acquisition is associated with induction of hippocampal long-term depression. Proc Natl Acad Sci U S A. 1999;96:8739-44.
37. Etkin A, Alarcón JM, Weisberg SP, Touzani K, Huang YY, Nordheim A, et al. A role in learning for SRF: deletion in the adult forebrain disrupts LTD and the formation of an immediate memory of a novel context. Neuron. 2006;50:127-43.
38. Ge Y, Dong Z, Bagot RC, Howland JG, Phillips AG, Wong TP, et al. Hippocampal long-term depression is required for the consolidation of spatial memory. Proc Natl Acad Sci U S A. 2010;107:16697-702.
39. Kawase E, Suemori H, Takahashi N, Okazaki K, Hashimoto K, Nakatsuji N. Strain difference in establishment of mouse embryonic stem (ES) cell lines. Int J Dev Biol. 1994;38:385-90.
40. Sano Y, Syuzo-Takabatake A, Nakaya T, Saito Y, Tomita S, Itohara S, et al. Enhanced amyloidogenic metabolism of the amyloid beta-protein precursor in the X11L-deficient mouse brain. J Biol Chem. 2006;281:37853-60.
41. Matsukawa H, Akiyoshi-Nishimura S, Zhang Q, Luján R, Yamaguchi K, Goto H, et al. Netrin-G/NGL complexes encode functional synaptic diversification. J Neurosci. 2014;34:15779-92.
42. Anderson WW, Collingridge GL. Capabilities of the WinLTP data acquisition program extending beyond basic LTP experimental functions. J Neurosci Methods. 2007;162:346-56.
43. Nishiyama H, Knopfel T, Endo S, Itohara S. Glial protein S100B modulates long-term neuronal synaptic plasticity. Proc Natl Acad Sci U S A. 2002;99:4037-42.
44. Kobayashi Y, Sano Y, Vannoni E, Goto H, Suzuki H, Oba A, et al. Genetic dissection of medial habenula-interpeduncular nucleus pathway function in mice. Front Behav Neurosci. 2013;7:17.