Impaired synaptic clustering of postsynaptic density proteins and altered signal transmission in hippocampal neurons, and disrupted learning behavior in PDZ1 and PDZ2 ligand binding-deficient PSD-95 knockin mice

Molecular Brain

Volumn 5, Issue 1, 2012, Pages

  Nagura, Hitoshi ^a,b   Ishikawa, Yasuyuki ^c   Kobayashi, Katsunori ^d   Takao, Keizo ^e   Tanaka, Tomo ^a   Nishikawa, Kouki ^b   Tamura, Hideki ^c   Shiosaka, Sadao ^c   Suzuki, Hidenori ^d   Miyakawa, Tsuyoshi ^f   Fujiyoshi, Yoshinori ^b   Doi, Tomoko ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NAGOYA UNIVERSITY   (Japan)

^c NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^d NIPPON MEDICAL SCHOOL   (Japan)

^e NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^f FUJITA HEALTH UNIVERSITY   (Japan)

Author keywords

Behavioral test battery; Dentate gyrus; PDZ domain; PSD 95; PSD MAGUK; Synaptic clustering; Synaptic transmission

Indexed keywords

COMPLEMENTARY DNA; LIGAND; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POSTSYNAPTIC DENSITY PROTEIN 95;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; LEARNING; LIGAND BINDING; LONG TERM DEPRESSION; LONG TERM MEMORY; LONG TERM POTENTIATION; MALE; MEMORY DISORDER; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; SYNAPTIC EFFICACY; WORKING MEMORY;

AGING; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; FEAR; GENE KNOCK-IN TECHNIQUES; GREEN FLUORESCENT PROTEINS; GUANYLATE KINASE; HIPPOCAMPUS; LEARNING; LIGANDS; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MEMBRANE PROTEINS; MEMORY; MICE; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; NEURONS; PROTEIN STRUCTURE, TERTIARY; SYNAPSES; SYNAPTIC TRANSMISSION;

MUS;

EID: 84871503854     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-5-43     Document Type: Article

References (50)

1. PDZ domain proteins of synapses. Kim E, Sheng M, Nat Rev Neurosci 2004 5 771 781 15378037
2. Integration of biochemical signalling in spines. Kennedy MB, Beale HC, Carlisle HJ, Washburn LR, Nat Rev Neurosci 2005 6 423 434 15928715
3. Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Funke L, Dakoji S, Bredt DS, Annu Rev Biochem 2005 74 219 245 10.1146/annurev.biochem.74.082803.133339 15952887
4. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH, Science 1995 269 1737 1740 10.1126/science.7569905 7569905
5. Interaction of transmembrane AMPA receptor regulatory proteins with multiple membrane associated guanylate kinases. Dakoji S, Tomita S, Karimzadegan S, Nicoll RA, Bredt DS, Neuropharmacology 2003 45 849 856 10.1016/S0028- 3908(03)00267-3 14529722
6. The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Jackson AC, Nicoll RA, Neuron 2011 70 178 199 10.1016/j.neuron.2011.04.007 21521608
7. Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Cheng D, Hoogenraad CC, Rush J, Ramm E, Schlager MA, Duong DM, Xu P, Wijayawardana SR, Hanfelt J, Nakagawa T, Sheng M, Peng J, Mol Cell Proteomics 2006 5 1158 1170 10.1074/mcp.D500009-MCP200 16507876
8. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, He Y, Ramsay MF, Morris RG, Morrison JH, O'Dell TJ, Grant SG, Nature 1998 396 433 439 10.1038/24790 9853749
9. Synapse-specific and developmentally regulated targeting of AMPA receptors by a family of MAGUK scaffolding proteins. Elias GM, Funke L, Stein V, Grant SG, Bredt DS, Nicoll RA, Neuron 2006 52 307 320 10.1016/j.neuron.2006.09. 012 17046693
10. Synapse-specific regulation of AMPA receptor function by PSD-95. Beique JC, Lin DT, Kang MG, Aizawa H, Takamiya K, Huganir RL, Proc Natl Acad Sci USA 2006 103 19535 19540 10.1073/pnas.0608492103 17148601
11. Opposing effects of PSD-93 and PSD-95 on long-term potentiation and spike timing-dependent plasticity. Carlisle HJ, Fink AE, Grant SG, O'Dell TJ, J Physiol 2008 586 5885 5900 10.1113/jphysiol.2008.163469 18936077
12. Differential trafficking of AMPA and NMDA receptors by SAP102 and PSD-95 underlies synapse development. Elias GM, Elias LA, Apostolides PF, Kriegstein AR, Nicoll RA, Proc Natl Acad Sci USA 2008 105 20953 20958 10.1073/pnas. 0811025106 19104036
13. PSD-95 and PSD-93 play critical but distinct roles in synaptic scaling up and down. Sun Q, Turrigiano GG, J Neurosci 2011 31 6800 6808 10.1523/JNEUROSCI.5616-10.2011 21543610
14. PSD-95-like membrane associated guanylate kinases (PSD-MAGUKs) and synaptic plasticity. Xu W, Curr Opin Neurobiol 2011 21 306 312 10.1016/j.conb.2011.03.001 21450454
15. Molecular dissociation of the role of PSD-95 in regulating synaptic strength and LTD. Xu W, Schluter OM, Steiner P, Czervionke BL, Sabatini B, Malenka RC, Neuron 2008 57 248 262 10.1016/j.neuron.2007.11.027 18215622
16. Ligand binding of the second PDZ domain regulates clustering of PSD-95 with the Kv1.4 potassium channel. Imamura F, Maeda S, Doi T, Fujiyoshi Y, J Biol Chem 2002 277 3640 3646 10.1074/jbc.M106940200 11723117
17. Ligand binding of PDZ domains has various roles in the synaptic clustering of SAP102 and PSD-95. Minatohara K, Ichikawa S, Seki T, Fujiyoshi Y, Doi T, Neurosci Lett 2013 533 44 49 23178474
18. The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Cho KO, Hunt CA, Kennedy MB, Neuron 1992 9 929 942 10.1016/0896-6273(92)90245-9 1419001
19. Essential contribution of the ligand-binding beta B/beta C loop of PDZ1 and PDZ2 in the regulation of postsynaptic clustering, scaffolding, and localization of postsynaptic density-95. Nonaka M, Doi T, Fujiyoshi Y, Takemoto-Kimura S, Bito H, J Neurosci 2006 26 763 774 10.1523/JNEUROSCI.2489-05. 2006 16421296
20. A developmental change in NMDA receptor-associated proteins at hippocampal synapses. Sans N, Petralia RS, Wang YX, Blahos J 2nd, Hell JW, Wenthold RJ, J Neurosci 2000 20 1260 1271 10648730
21. Ontogeny of postsynaptic density proteins at glutamatergic synapses. Petralia RS, Sans N, Wang YX, Wenthold RJ, Mol Cell Neurosci 2005 29 436 452 10.1016/j.mcn.2005.03.013 15894489
22. Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. Tomita S, Chen L, Kawasaki Y, Petralia RS, Wenthold RJ, Nicoll RA, Bredt DS, J Cell Biol 2003 161 805 816 10.1083/jcb.200212116 12771129
23. Heterogeneity of release probability, facilitation, and depletion at central synapses. Dobrunz LE, Stevens CF, Neuron 1997 18 995 1008 10.1016/S0896-6273(00)80338-4 9208866
24. Conditional calcineurin knockout mice exhibit multiple abnormal behaviors related to schizophrenia. Miyakawa T, Leiter LM, Gerber DJ, Gainetdinov RR, Sotnikova TD, Zeng H, Caron MG, Tonegawa S, Proc Natl Acad Sci USA 2003 100 8987 8992 10.1073/pnas.1432926100 12851457
25. Behavioral profile of wild mice in the elevated plus-maze test for anxiety. Holmes A, Parmigiani S, Ferrari PF, Palanza P, Rodgers RJ, Physiol Behav 2000 71 509 516 10.1016/S0031-9384(00)00373-5 11239669
26. GKAP, a novel synaptic protein that interacts with the guanylate kinase-like domain of the PSD-95/SAP90 family of channel clustering molecules. Kim E, Naisbitt S, Hsueh YP, Rao A, Rothschild A, Craig AM, Sheng M, J Cell Biol 1997 136 669 678 10.1083/jcb.136.3.669 9024696
27. Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Naisbitt S, Kim E, Tu JC, Xiao B, Sala C, Valtschanoff J, Weinberg RJ, Worley PF, Sheng M, Neuron 1999 23 569 582 10.1016/S0896-6273(00)80809-0 10433268
28. Dlg1 binds GKAP to control dynein association with microtubules, centrosome positioning, and cell polarity. Manneville JB, Jehanno M, Etienne-Manneville S, J Cell Biol 2010 191 585 598 10.1083/jcb.201002151 21041448
29. Synapse-associated protein 102/dlgh3 couples the NMDA receptor to specific plasticity pathways and learning strategies. Cuthbert PC, Stanford LE, Coba MP, Ainge JA, Fink AE, Opazo P, Delgado JY, Komiyama NH, O'Dell TJ, Grant SG, J Neurosci 2007 27 2673 2682 10.1523/JNEUROSCI.4457-06.2007 17344405
30. Heteromultimerization and NMDA receptor-clustering activity of Chapsyn-110, a member of the PSD-95 family of proteins. Kim E, Cho KO, Rothschild A, Sheng M, Neuron 1996 17 103 113 10.1016/S0896-6273(00)80284-6 8755482
31. Structural basis of long-term potentiation in single dendritic spines. Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H, Nature 2004 429 761 766 10.1038/nature02617 15190253
32. Synaptic accumulation of PSD-95 and synaptic function regulated by phosphorylation of serine-295 of PSD-95. Kim MJ, Futai K, Jo J, Hayashi Y, Cho K, Sheng M, Neuron 2007 56 488 502 10.1016/j.neuron.2007.09.007 17988632
33. A critical role for PSD-95/AKAP interactions in endocytosis of synaptic AMPA receptors. Bhattacharyya S, Biou V, Xu W, Schluter O, Malenka RC, Nat Neurosci 2009 12 172 181 10.1038/nn.2249 19169250
34. Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins. Elias GM, Nicoll RA, Trends Cell Biol 2007 17 343 352 10.1016/j.tcb.2007.07.005 17644382
35. TARP gamma-8 controls hippocampal AMPA receptor number, distribution and synaptic plasticity. Rouach N, Byrd K, Petralia RS, Elias GM, Adesnik H, Tomita S, Karimzadegan S, Kealey C, Bredt DS, Nicoll RA, Nat Neurosci 2005 8 1525 1533 10.1038/nn1551 16222232
36. Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin. Futai K, Kim MJ, Hashikawa T, Scheiffele P, Sheng M, Hayashi Y, Nat Neurosci 2007 10 186 195 10.1038/nn1837 17237775
37. Synchronous and asynchronous transmitter release at nicotinic synapses are differentially regulated by postsynaptic PSD-95 proteins. Neff RA 3rd, Conroy WG, Schoellerman JD, Berg DK, J Neurosci 2009 29 15770 15779 10.1523/JNEUROSCI.4951-09.2009 20016093
38. Association of mouse Dlg4 (PSD-95) gene deletion and human DLG4 gene variation with phenotypes relevant to autism spectrum disorders and Williams' syndrome. Feyder M, Karlsson RM, Mathur P, Lyman M, Bock R, Momenan R, Munasinghe J, Scattoni ML, Ihne J, Camp M, Graybeal C, Strathdee D, Begg A, Alvarez VA, Kirsch P, Rietschel M, Cichon S, Walter H, Meyer-Lindenberg A, Grant SG, Holmes A, Am J Psychiatry 2010 167 1508 1517 10.1176/appi.ajp.2010.10040484 20952458
39. Advances in autism genetics: on the threshold of a new neurobiology. Abrahams BS, Geschwind DH, Nat rev genetics 2008 9 341 355 10.1038/nrg2346
40. Genetic variation in C57BL/6 ES cell lines and genetic instability in the Bruce4 C57BL/6 ES cell line. Hughes ED, Qu YY, Genik SJ, Lyons RH, Pacheco CD, Lieberman AP, Samuelson LC, Nasonkin IO, Camper SA, Van Keuren ML, Saunders TL, Mamm Genome 2007 18 549 558 10.1007/s00335-007-9054-0 17828574
41. Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. Carlin RK, Grab DJ, Cohen RS, Siekevitz P, J Cell Biol 1980 86 831 845 10.1083/jcb.86.3.831 7410481
42. Identification and verification of novel rodent postsynaptic density proteins. Jordan BA, Fernholz BD, Boussac M, Xu C, Grigorean G, Ziff EB, Neubert TA, Mol Cell Proteomics 2004 3 857 871 10.1074/mcp.M400045-MCP200 15169875
43. Proteomic analysis revealed a novel synaptic proline-rich membrane protein (PRR7) associated with PSD-95 and NMDA receptor. Murata Y, Doi T, Taniguchi H, Fujiyoshi Y, Biochem Biophys Res Commun 2005 327 183 191 10.1016/j.bbrc.2004.11.154 15629447
44. Role of neuropsin in formation and maturation of Schaffer-collateral L1cam-immunoreactive synaptic boutons. Nakamura Y, Tamura H, Horinouchi K, Shiosaka S, J Cell Sci 2006 119 1341 1349 10.1242/jcs.02862 16537644
45. Neuropsin (KLK8)-dependent and -independent synaptic tagging in the Schaffer-collateral pathway of mouse hippocampus. Ishikawa Y, Horii Y, Tamura H, Shiosaka S, J Neurosci 2008 28 843 849 10.1523/JNEUROSCI.4397-07.2008 18216192
46. Hyperactivity and intact hippocampus-dependent learning in mice lacking the M1 muscarinic acetylcholine receptor. Miyakawa T, Yamada M, Duttaroy A, Wess J, J Neurosci 2001 21 5239 5250 11438599
47. Impact of brain-behavior phenotyping of genetically-engineered mice on research of neuropsychiatric disorders. Takao K, Yamasaki N, Miyakawa T, Neurosci Res 2007 58 124 132 10.1016/j.neures.2007.02.009 17524507
48. Comprehensive behavioral analysis of calcium/calmodulin-dependent protein kinase IV knockout mice. Takao K, Tanda K, Nakamura K, Kasahara J, Nakao K, Katsuki M, Nakanishi K, Yamasaki N, Toyama K, Adachi M, Umeda M, Araki T, Fukunaga K, Kondo H, Sakagami H, Miyakawa T, PLoS One 2010 5 9460 10.1371/journal.pone.0009460 20209163
49. Relaxin-3-deficient mice showed slight alteration in anxiety-related behavior. Watanabe Y, Tsujimura A, Takao K, Nishi K, Ito Y, Yasuhara Y, Nakatomi Y, Yokoyama C, Fukui K, Miyakawa T, Tanaka M, Front Behav Neurosci 2011 5 50 21887138
50. Synaptic E3 ligase SCRAPPER in contextual fear conditioning: extensive behavioral phenotyping of Scrapper heterozygote and overexpressing mutant mice. Yao I, Takao K, Miyakawa T, Ito S, Setou M, PLoS One 2011 6 17317 10.1371/journal.pone.0017317 21390313