Postsynaptic density scaffold SAP102 regulates cortical synapse development through EphB and PAK signaling pathway

Journal of Neuroscience

Volumn 33, Issue 11, 2013, Pages 5040-5052

  Murata, Yasunobu ^a   Constantine Paton, Martha ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; EPHRIN RECEPTOR; EPHRIN RECEPTOR B2; GREEN FLUORESCENT PROTEIN; P21 ACTIVATED KINASE; POSTSYNAPTIC DENSITY PROTEIN 95; SAP102 PROTEIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; BIOTINYLATION; BRAIN CORTEX; DENDRITE; DOWN REGULATION; EMBRYO; FEMALE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTOGENESIS; VISUAL CORTEX; WESTERN BLOTTING;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; BIOTINYLATION; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EMBRYO, MAMMALIAN; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LENTIVIRUS; MALE; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; NEURONS; NEUROPEPTIDES; POST-SYNAPTIC DENSITY; RATS; RECEPTORS, EPH FAMILY; RECEPTORS, N-METHYL-D-ASPARTATE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SYNAPSES; SYNAPTOSOMES; TRANSFECTION; VISUAL CORTEX;

EID: 84874845902     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2896-12.2013     Document Type: Article

References (72)

1. Allen KM, Gleeson JG, Bagrodia S, Partington MW, MacMillan JC, Cerione RA, Mulley JC, Walsh CA (1998) PAK3 mutation in nonsyndromic X-linked mental retardation. Nat Genet 20:25-30. CrossRef Medline
2. Banker G, Goslin K (1991) Culturing nerve cells. Cambridge, MA: MIT.
3. Béïque JC, Lin D-T, Kang MG, Aizawa H, Takamiya K, Huganir RL (2006) Synapse-specific regulation of AMPA receptor function by PSD-95. Proc Natl Acad Sci U S A 103:19535-19540. CrossRef Medline
4. Bienvenu T, des Portes V, McDonell N, Carrié A, Zemni R, Couvert P, Ropers HH, Moraine C, van Bokhoven H, Fryns JP, Allen K, Walsh CA, Boué J, Kahn A, Chelly J, Beldjord C (2000) Missense mutation in PAK3, R67C, causes X-linked nonspecific mental retardation. Am J Med Genet 93:294-298. CrossRef Medline
5. Boda B, Alberi S, Nikonenko I, Node-Langlois R, Jourdain P, Moosmayer M, Parisi-Jourdain L, Muller D (2004) The mental retardation protein PAK3 contributes to synapse formation and plasticity in hippocampus. J Neurosci 24:10816-10825. CrossRef Medline
6. Boda B, Dubos A, Muller D (2010) Signaling mechanisms regulating synapse formation and function in mental retardation. Curr Opin Neurobiol 20:519-527. CrossRef Medline
7. Bouvier D, Corera AT, Tremblay ME, Riad M, Chagnon M, Murai KK, Pasquale EB, Fon EA, Doucet G (2008) Presynaptic and post-synaptic localization of EphA4 and EphB2 in adult mouse forebrain. J Neurochem 106:682-695. CrossRef Medline
8. Chen BS, Thomas EV, Sanz-Clemente A, Roche KW (2011) NMDA receptor-dependent regulation of dendritic spine morphology by SAP102 splice variants. J Neurosci 31:89-96. CrossRef Medline
9. Cheng D, Hoogenraad CC, Rush J, Ramm E, Schlager MA, Duong DM, Xu P, Wijayawardana SR, Hanfelt J, Nakagawa T, Sheng M, Peng J (2006) Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Mol Cell Proteomics 5:1158-1170. CrossRef Medline
10. Cuthbert PC, Stanford LE, Coba MP, Ainge JA, Fink AE, Opazo P, Delgado JY, Komiyama NH, O'Dell TJ, Grant SG (2007) Synapse-associated protein 102/dlgh3 couples theNMDAreceptor to specific plasticity pathways and learning strategies. J Neurosci 27:2673-2682. CrossRef Medline
11. Dalva MB, Takasu MA, Lin MZ, Shamah SM, Hu L, Gale NW, Greenberg ME (2000) Eph B receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103:945-956. CrossRef Medline
12. Dittgen T, Nimmerjahn A, Komai S, Licznerski P, Waters J, Margrie TW, Helmchen F, Denk W, Brecht M, Osten P (2004) Lentivirus-based genetic manipulations of cortical neurons and their optical and electrophysiological monitoring in vivo. Proc Natl Acad Sci U S A 101:18206-18211. CrossRef Medline
13. Ehlers MD (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6:231-242. CrossRef Medline
14. Ehrlich I, Klein M, Rumpel S, Malinow R (2007) PSD-95 is required for activity-driven synapse stabilization. Proc Natl Acad Sci U S A 104:4176-4181. CrossRef Medline
15. El-Husseini AE, Schnell E, Chetkovich DM, Nicoll RA, Bredt DS (2000) PSD-95 involvement in maturation of excitatory synapses. Science 290: 1364-1368. Medline
16. Elias GM, Nicoll RA (2007) Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins. Trends Cell Biol 17:343-352. CrossRef Medline
17. Elias GM, Funke L, Stein V, Grant SG, Bredt DS, Nicoll RA (2006) Synapsespecific and developmentally regulated targeting of AMPA receptors by a family of MAGUK scaffolding proteins. Neuron 52:307-320. CrossRef Medline
18. Elias GM, Elias LA, Apostolides PF, Kriegstein AR, Nicoll RA (2008) Differential trafficking of AMPA and NMDA receptors by SAP102 and PSD-95 underlies synapse development. Proc Natl Acad Sci U S A 105:20953-20958. CrossRef Medline
19. Ethell IM, Irie F, Kalo MS, Couchman JR, Pasquale EB, Yamaguchi Y (2001) EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron 31:1001-1013. CrossRef Medline
20. Funke L, Dakoji S, Bredt DS (2005) Membrane-associated guanylate kinases regulate adhesion and plasticity at cell junctions. Annu Rev Biochem 74:219-245. CrossRef Medline
21. Futai K, Kim MJ, Hashikawa T, Scheiffele P, Sheng M, Hayashi Y (2007) Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin. Nat Neurosci 10:186-195. CrossRef Medline
22. Gerrow K, Romorini S, Nabi SM, Colicos MA, Sala C, El-Husseini A (2006) A performed complex of postsynaptic proteins is involved in excitatory synapse development. Neuron 49:547-562. CrossRef Medline
23. Gray JA, Shi Y, Usui H, During MJ, Sakimura K, Nicoll RA (2011) Distinct modes of AMPA receptor suppression at developing synapses by GluN2A and GluN2B: single-cell NMDA receptor subunit deletion in vivo. Neuron 71:1085-1101. CrossRef Medline
24. Henkemeyer M, Itkis OS, Ngo M, Hickmott PW, Ethell IM (2003) Multiple Eph B receptor tyrosine kinases shape dendritic spines in the hippocampus. J Cell Biol 163:1313-1326. CrossRef Medline
25. Humeau Y, Gambino F, Chelly J, Vitale N (2009) X-linked mental retardation: focus on synaptic function and plasticity. J Neurochem 109:1-14. CrossRef Medline
26. Irie F, Yamaguchi Y (2002) Eph B receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP. Nat Neurosci 5:1117-1118. CrossRef Medline
27. Kayser MS, McClelland AC, Hughes EG, Dalva MB (2006) Intracellular and trans-synaptic regulation of glutamatergic synaptogenesis by Eph B receptors. J Neurosci 26:12152-12164. CrossRef Medline
28. Kayser MS, Nolt MJ, Dalva MB (2008) Eph B receptors couple dendritic filopodia motility to synapse formation. Neuron 59:56-69. CrossRef Medline
29. Kiraly DD, Lemtiri-Chlieh F, Levine ES, Mains RE, Eipper BA (2011) Kalirin binds the NR2B subunit of the NMDA receptor, altering its synaptic localization and function. J Neurosci 31:12554-12565. CrossRef Medline
30. Klein R (2009) Bidirectional modulation of synaptic functions by Eph/ephrin signaling. Nat Neurosci 12:15-20. CrossRef Medline
31. Kreis P, Barnier JV (2009) PAK signalling in neuronal physiology. Cell Signal 21:384-393. CrossRef Medline
32. Lai KO, Ip NY (2009) Synapse development and plasticity: roles of ephrin/ Eph receptor signaling. Curr Opin Neurobiol 19:275-283. CrossRef Medline
33. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295:868-872. CrossRef Medline
34. Lu W, Constantine-Paton M (2004) Eye opening rapidly induces synaptic potentiation and refinement. Neuron 43:237-249. CrossRef Medline
35. Ma XM (2010) Kalirin-7 is a key player in the formation of excitatory synapses in hippocampal neurons. ScientificWorldJournal 10:1655-1666. CrossRef Medline
36. Ma XM, Huang J, Wang Y, Eipper BA, Mains RE (2003) Kalirin, a multifunctional Rho guanine nucleotide exchange factor, is necessary for maintenance of hippocampal pyramidal neuron dendrites and dendritic spines. J Neurosci 23:10593-10603. Medline
37. Ma XM, Kiraly DD, Gaier ED, Wang Y, Kim EJ, Levine ES, Eipper BA, Mains RE (2008) Kalirin-7 is required for synaptic structure and function. J Neurosci 28:12368-12382. CrossRef Medline
38. Meng J, Meng Y, Hanna A, Janus C, Jia Z (2005) Abnormal long-lasting synaptic plasticity and cognition in mice lacking the mental retardation gene Pak3. J Neurosci 25:6641-6650. CrossRef Medline
39. Nadif Kasri N, Nakano-Kobayashi A, Malinow R, Li B, Van Aelst L (2009) The Rho-linked mental retardation protein oligophrenin-1 controls synapse maturation and plasticity by stabilizing AMPA receptors. Genes Dev 23:1289-1302. CrossRef Medline
40. Nakagawa T, Futai K, Lashuel HA, Lo I, Okamoto K, Walz T, Hayashi Y, Sheng M (2004) Quaternary structure, protein dynamics, and synaptic function of SAP97 controlled by L27 domain interactions. Neuron 44: 453-467. CrossRef Medline
41. Nodé-Langlois R, Muller D, Boda B (2006) Sequential implication of the mental retardation proteins ARHGEF6 and PAK3 in spine morphogenesis. J Cell Sci 119:4986-4993. CrossRef Medline
42. Nolt MJ, Lin Y, Hruska M, Murphy J, Sheffler-Colins SI, Kayser MS, Passer J, Bennett MV, Zukin RS, Dalva MB (2011) Eph B controls NMDA receptor function and synaptic targeting in a subunit-specific manner. J Neurosci 31:5353-5364. CrossRef Medline
43. Oh D, Han S, Seo J, Lee JR, Choi J, Groffen J, Kim K, Cho YS, Choi HS, Shin H, Woo J, Won H, Park SK, Kim SY, Jo J, Whitcomb DJ, Cho K, Kim H, Bae YC, Heisterkamp N, et al. (2010) Regulation of synaptic Rac1 activity, long-term potentiation maintenance, and learning and memory by BCR and ABR Rac GTPase-activating proteins. J Neurosci 30:14134-14144. CrossRef Medline
44. Penzes P, Jones KA (2008) Dendritic spine dynamics-a key role for kalirin-7. Trends Neurosci 31:419-427. CrossRef Medline
45. Penzes P, Johnson RC, Alam MR, Kambampati V, Mains RE, Eipper BA (2000) An isoform of kalirin, a brain-specific GDP/GTP exchange factor, is enriched in the postsynaptic density fraction. J Biol Chem 275:6395-6403. CrossRef Medline
46. Penzes P, Johnson RC, Sattler R, Zhang X, Huganir RL, Kambampati V, Mains RE, Eipper BA (2001) The neuronal Rho-GEF Kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron 29:229-242. CrossRef Medline
47. Penzes P, Beeser A, Chernoff J, Schiller MR, Eipper BA, Mains RE, Huganir RL (2003) Rapid induction of dendritic spine morphogenesis by transsynaptic ephrinB-Eph B receptor activation of the Rho-GEF kalirin. Neuron 37:263-274. CrossRef Medline
48. Petralia RS, Sans N, Wang YX, Wenthold RJ (2005) Ontogeny of postsynaptic density proteins at glutamatergic synapses. Mol Cell Neurosci 29: 436-452. CrossRef Medline
49. Phillips MA, Colonnese MT, Goldberg J, Lewis LD, Brown EN, Constantine-Paton M (2011) A synaptic strategy for consolidation of convergent visuotopic maps. Neuron 71:710-724. CrossRef Medline
50. Ramakers GJ (2002) Rho proteins, mental retardation and the cellular basis of cognition. Trends Neurosci 25:191-199. CrossRef Medline
51. Rauner C, Köhr G (2011) Triheteromeric NR1/NR2A/NR2B receptors constitute the major N-methyl-D-aspartate receptor population in adult hippocampal synapses. J Biol Chem 286:7558-7566. CrossRef Medline
52. Rejeb I, Saillour Y, Castelnau L, Julien C, Bienvenu T, Taga P, Chaabouni H, Chelly J, Ben Jemaa L, Bahi-Buisson N (2008) Anovel splice mutation in PAK3 gene underlying mental retardation with neuropsychiatric features. Eur J Hum Genet 16:1358-1363. CrossRef Medline
53. Ropers HH (2010) Genetics of early onset cognitive impairment. Annu Rev Genomics Hum Genet 11:161-187. CrossRef Medline
54. Rubinson DA, Dillon CP, Kwiatkowski AV, Sievers C, Yang L, Kopinja J, Rooney DL, Zhang M, Ihrig MM, McManus MT, Gertler FB, Scott ML, Van Parijs L (2003) A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice byRNA interference. Nat Genet 33:401-406. CrossRef Medline
55. Saneyoshi T, Wayman G, Fortin D, Davare M, Hoshi N, Nozaki N, Natsume T, Soderling TR (2008) Activity-dependent synaptogenesis: regulation by a CaM-kinase kinase/CaM-kinase I/betaPIX signaling complex. Neuron 57:94-107. CrossRef Medline
56. Sans N, Petralia RS, Wang YX, Blahos J 2nd, Hell JW, Wenthold RJ (2000) A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J Neurosci 20:1260-1271. Medline
57. Scherer SW, Dawson G (2011) Risk factors for autism: translating genomic discoveries into diagnostics. Hum Genet 130:123-148. CrossRef Medline
58. Schlüter OM, Xu W, Malenka RC (2006) Alternative N-terminal domains of PSD-95 and SAP97 govern activity-dependent regulation of synaptic AMPA receptor function. Neuron 51:99-111. CrossRef Medline
59. Sheng M, Hoogenraad CC (2007) The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem 76:823-847. CrossRef Medline
60. Takasu MA, Dalva MB, Zigmond RE, Greenberg ME (2002) Modulation of NMDA receptor-dependent calcium influx and gene expression through Eph B receptors. Science 295:491-495. CrossRef Medline
61. Tarpey P, Parnau J, Blow M, Woffendin H, Bignell G, Cox C, Cox J, Davies H, Edkins S, Holden S, Korny A, Mallya U, Moon J, O'Meara S, Parker A, Stephens P, Stevens C, Teague J, Donnelly A, Mangelsdorf M, et al. (2004) Mutations in the DLG3 gene cause nonsyndromic X-linked mental retardation. Am J Hum Genet 75:318-324. CrossRef Medline
62. Tolias KF, Bikoff JB, Kane CG, Tolias CS, Hu L, Greenberg ME (2007) The Rac1 guanine nucleotide exchange factor Tiam1 mediates Eph B receptordependent dendritic spine development. Proc Natl Acad Sci U S A 104: 7265-7270. CrossRef Medline
63. van Zundert B, Yoshii A, Constantine-Paton M (2004) Receptor compartmentalization and trafficking at glutamate synapses: a developmental proposal. Trends Neurosci 27:428-437. CrossRef Medline
64. Washbourne P, Liu XB, Jones EG, McAllister AK (2004) Cycling of NMDA receptors during trafficking in neurons before synapse formation. J Neurosci 24:8253-8264. CrossRef Medline
65. Xie Z, Srivastava DP, Photowala H, Kai L, Cahill ME, Woolfrey KM, Shum CY, Surmeier DJ, Penzes P (2007) Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 56:640-656. CrossRef Medline
66. Yoshii A, Constantine-Paton M (2007) BDNF induces transport of PSD-95 to dendrites through PI3K-AKT signaling after NMDA receptor activation. Nat Neurosci 10:702-711. CrossRef Medline
67. Yoshii A, Sheng MH, Constantine-Paton M (2003) Eye opening induces a rapid dendritic localization of PSD-95 in central visual neurons. Proc Natl Acad Sci U S A 100:1334-1339. CrossRef Medline
68. Yoshii A, Murata Y, Kim J, Zhang C, Shokat KM, Constantine-Paton M (2011) Trk B and protein kinaseM{zeta} regulate synaptic localization of PSD-95 in developing cortex. J Neurosci 31:11894-11904. CrossRef Medline
69. Zanni G, van Esch H, Bensalem A, Saillour Y, Poirier K, Castelnau L, Ropers HH, de Brouwer AP, Laumonnier F, Fryns JP, Chelly J (2010) A novel mutation in the DLG3 gene encoding the synapse-associated protein 102 (SAP102) causes nonsyndromic mental retardation. Neurogenetics 11: 251-255. CrossRef Medline
70. Zhang H, Webb DJ, Asmussen H, Niu S, Horwitz AF (2005) A GIT1/PIX/ Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC. J Neurosci 25:3379-3388. CrossRef Medline
71. Zheng CY, Petralia RS, Wang YX, Kachar B, Wenthold RJ (2010) SAP102 is a highly mobile MAGUK in spines. J Neurosci 30:4757-4766. CrossRef Medline
72. Zheng CY, Seabold GK, Horak M, Petralia RS (2011) MAGUKs, synaptic development, and synaptic plasticity. Neuroscientist 17:493-512. CrossRef Medline