The Rac1-GEF Tiam1 couples the NMDA receptor to the activity-dependent development of dendritic arbors and spines

Neuron

Volumn 45, Issue 4, 2005, Pages 525-538

  Tolias, Kimberley F ^a,b   Bikoff, Jay B ^a,b   Burette, Alain ^c   Paradis, Suzanne ^a,b   Harrar, Dana ^a,b   Tavazoie, Sohail ^b   Weinberg, Richard J ^c,d   Greenberg, Michael E ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN; RAC1 PROTEIN; TIAM1 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE;

EID: 13844253719     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2005.01.024     Document Type: Article

References (84)

1. D.R. Alessi, M. Andjelkovic, B. Caudwell, P. Cron, N. Morrice, P. Cohen, and B.A. Hemmings Mechanism of activation of protein kinase B by insulin and IGF-1 EMBO J. 15 1996 6541 6551
2. T. Bonhoeffer, and R. Yuste Spine motility: Phenomenology, mechanisms, and function Neuron 35 2002 1019 1027
3. D.S. Bredt, and R.A. Nicoll AMPA receptor trafficking at excitatory synapses Neuron 40 2003 361 379
4. T.R. Brummelkamp, R. Bernards, and R. Agami A system for stable expression of short interfering RNAs in mammalian cells Science 296 2002 550 553
5. D.A. Cantrell Phosphoinositide 3-kinase signalling pathways J. Cell Sci. 114 2001 1439 1445
6. C.L. Carpenter, and L.C. Cantley Phosphoinositide kinases Curr. Opin. Cell Biol. 8 1996 153 158
7. T.O. Chan, S.E. Rittenhouse, and P.N. Tsichlis AKT/PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide- dependent phosphorylation Annu. Rev. Biochem. 68 1999 965 1014
8. C.Y. Chung, G. Potikyan, and R.A. Firtel Control of cell polarity and chemotaxis by Akt/PKB and PI3 kinase through the regulation of PAKa Mol. Cell 7 2001 937 947
9. P.B. Crino, and J. Eberwine Molecular characterization of the dendritic growth cone: regulated mRNA transport and local protein synthesis Neuron 17 1996 1173 1187
10. S. Cull-Candy, S. Brickley, and M. Farrant NMDA receptor subunits: diversity, development and disease Curr. Opin. Neurobiol. 11 2001 327 335
11. M.B. Dalva, M.A. Takasu, M.Z. Lin, S.M. Shamah, L. Hu, N.W. Gale, and M.E. Greenberg EphB receptors interact with NMDA receptors and regulate excitatory synapse formation Cell 103 2000 945 956
12. M.I. Daw, Z.A. Bortolotto, E. Saulle, S. Zaman, G.L. Collingridge, and J.T. Isaac Phosphatidylinositol 3 kinase regulates synapse specificity of hippocampal long-term depression Nat. Neurosci. 5 2002 835 836
13. E. Ehler, F. van Leeuwen, J.G. Collard, and P.C. Salinas Expression of Tiam-1 in the developing brain suggests a role for the Tiam-1-Rac signaling pathway in cell migration and neurite outgrowth Mol. Cell. Neurosci. 9 1997 1 12
14. I.N. Fleming, C.M. Elliott, F.G. Buchanan, C.P. Downes, and J.H. Exton Ca2+/calmodulin-dependent protein kinase II regulates Tiam1 by reversible protein phosphorylation J. Biol. Chem. 274 1999 12753 12758
15. I.N. Fleming, A. Gray, and C.P. Downes Regulation of the Rac1-specific exchange factor Tiam1 involves both phosphoinositide 3-kinase-dependent and -independent components Biochem. J. 351 2000 173 182
16. Y. Fukazawa, Y. Saitoh, F. Ozawa, Y. Ohta, K. Mizuno, and K. Inokuchi Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo Neuron 38 2003 447 460
17. M. Garcia-Gallo, J. Renart, and M. Diaz-Guerra The NR1 subunit of the N-methyl-D-aspartate receptor can be efficiently expressed alone in the cell surface of mammalian cells and is required for the transport of the NR2A subunit Biochem. J. 356 2001 539 547
18. B. Gaudilliere, Y. Konishi, N. de la Iglesia, G. Yao, and A. Bonni A CaMKII-NeuroD signaling pathway specifies dendritic morphogenesis Neuron 41 2004 229 241
19. E.M. Genot, C. Arrieumerlou, G. Ku, B.M. Burgering, A. Weiss, and I.M. Kramer The T-cell receptor regulates Akt (protein kinase B) via a pathway involving Rac1 and phosphatidylinositide 3-kinase Mol. Cell. Biol. 20 2000 5469 5478
20. A.C. Gingras, B. Raught, and N. Sonenberg Regulation of translation initiation by FRAP/mTOR Genes Dev. 15 2001 807 826
21. M. Goldin, M. Segal, and E. Avignone Functional plasticity triggers formation and pruning of dendritic spines in cultured hippocampal networks J. Neurosci. 21 2001 186 193
22. L.L. Gomez, S. Alam, K.E. Smith, E. Horne, and M.L. Dell'Acqua Regulation of A-kinase anchoring protein 79/150-cAMP-dependent protein kinase postsynaptic targeting by NMDA receptor activation of calcineurin and remodeling of dendritic actin J. Neurosci. 22 2002 7027 7044
23. I.C. Grunwald, M. Korte, D. Wolfer, G.A. Wilkinson, K. Unsicker, H.P. Lipp, T. Bonhoeffer, and R. Klein Kinase-independent requirement of EphB2 receptors in hippocampal synaptic plasticity Neuron 32 2001 1027 1040
24. X. Guo, Y. Lin, C. Horbinski, K.M. Drahushuk, I.J. Kim, P.L. Kaplan, P. Lein, T. Wang, and D. Higgins Dendritic growth induced by BMP-7 requires Smad1 and proteasome activity J. Neurobiol. 48 2001 120 130
25. N. Hay, and N. Sonenberg Upstream and downstream of mTOR Genes Dev. 18 2004 1926 1945
26. J.T. Henderson, J. Georgiou, Z. Jia, J. Robertson, S. Elowe, J.C. Roder, and T. Pawson The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function Neuron 32 2001 1041 1056
27. E.J. Huang, and L.F. Reichardt Neurotrophins: roles in neuronal development and function Annu. Rev. Neurosci. 24 2001 677 736
28. T. Kawauchi, K. Chihama, Y. Nabeshima, and M. Hoshino The in vivo roles of STEF/Tiam1, Rac1 and JNK in cortical neuronal migration EMBO J. 22 2003 4190 4201
29. R.J. Kelleher 3rd, A. Govindarajan, and S. Tonegawa Translational regulatory mechanisms in persistent forms of synaptic plasticity Neuron 44 2004 59 73
30. C.H. Kim, and J.E. Lisman A role of actin filament in synaptic transmission and long-term potentiation J. Neurosci. 19 1999 4314 4324
31. K. Kotani, K. Yonezawa, K. Hara, H. Ueda, Y. Kitamura, H. Sakaue, A. Ando, A. Chavanieu, B. Calas, and F. Grigorescu Involvement of phosphoinositide 3-kinase in insulin- or IGF-1-induced membrane ruffling EMBO J. 13 1994 2313 2321
32. S.C. Kozma, and G. Thomas Regulation of cell size in growth, development and human disease: PI3K, PKB and S6K Bioessays 24 2002 65 71
33. G. Krapivinsky, L. Krapivinsky, Y. Manasian, A. Ivanov, R. Tyzio, C. Pellegrino, Y. Ben-Ari, D.E. Clapham, and I. Medina The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and RasGRF1 Neuron 40 2003 775 784
34. J.M. Lambert, Q.T. Lambert, G.W. Reuther, A. Malliri, D.P. Siderovski, J. Sondek, J.G. Collard, and C.J. Der Tiam1 mediates Ras activation of Rac by a PI(3)K-independent mechanism Nat. Cell Biol. 4 2002 621 625
35. Z. Li, L. Van Aelst, and H.T. Cline Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo Nat. Neurosci. 3 2000 217 225
36. Z. Li, C.D. Aizenman, and H.T. Cline Regulation of rho GTPases by crosstalk and neuronal activity in vivo Neuron 33 2002 741 750
37. C.H. Lin, S.H. Yeh, K.T. Lu, T.H. Leu, W.C. Chang, and P.W. Gean A role for the PI-3 kinase signaling pathway in fear conditioning and synaptic plasticity in the amygdala Neuron 31 2001 841 851
38. H. Lin, R. Huganir, and D. Liao Temporal dynamics of NMDA receptor-induced changes in spine morphology and AMPA receptor recruitment to spines Biochem. Biophys. Res. Commun. 316 2004 501 511
39. J. Lisman, H. Schulman, and H. Cline The molecular basis of CaMKII function in synaptic and behavioural memory Nat. Rev. Neurosci. 3 2002 175 190
40. L. Luo Actin cytoskeleton regulation in neuronal morphogenesis and structural plasticity Annu. Rev. Cell Dev. Biol. 18 2002 601 635
41. L. Luo, T.K. Hensch, L. Ackerman, S. Barbel, L.Y. Jan, and Y.N. Jan Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines Nature 379 1996 837 840
42. H.Y. Man, Q. Wang, W.Y. Lu, W. Ju, G. Ahmadian, L. Liu, S. D'Souza, T.P. Wong, C. Taghibiglou, and J. Lu Activation of PI3-kinase is required for AMPA receptor insertion during LTP of mEPSCs in cultured hippocampal neurons Neuron 38 2003 611 624
43. A. Matus Actin-based plasticity in dendritic spines Science 290 2000 754 758
44. Y. Meng, Y. Zhang, V. Tregoubov, C. Janus, L. Cruz, M. Jackson, W.Y. Lu, J.F. MacDonald, J.Y. Wang, D.L. Falls, and Z. Jia Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice Neuron 35 2002 121 133
45. S. Merlot, and R.A. Firtel Leading the way: Directional sensing through phosphatidylinositol 3-kinase and other signaling pathways J. Cell Sci. 116 2003 3471 3478
46. F. Michiels, J.C. Stam, P.L. Hordijk, R.A. van der Kammen, L. Ruuls-Van Stalle, C.A. Feltkamp, and J.G. Collard Regulated membrane localization of Tiam1, mediated by the NH2-terminal pleckstrin homology domain, is required for Rac-dependent membrane ruffling and C-Jun NH2-terminal kinase activation J. Cell Biol. 137 1997 387 398
47. S.Y. Moon, and Y. Zheng Rho GTPase-activating proteins in cell regulation Trends Cell Biol. 13 2003 13 22
48. A.Y. Nakayama, M.B. Harms, and L. Luo Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons J. Neurosci. 20 2000 5329 5338
49. I. Nikonenko, P. Jourdain, S. Alberi, N. Toni, and D. Muller Activity-induced changes of spine morphology Hippocampus 12 2002 585 591
50. L.E. Ostroff, J.C. Fiala, B. Allwardt, and K.M. Harris Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices Neuron 35 2002 535 545
51. A. Palmer, and R. Klein Multiple roles of ephrins in morphogenesis, neuronal networking, and brain function Genes Dev. 17 2003 1429 1450
52. P. Penzes, R.C. Johnson, M.R. Alam, V. Kambampati, R.E. Mains, and B.A. Eipper An isoform of kalirin, a brain-specific GDP/GTP exchange factor, is enriched in the postsynaptic density fraction J. Biol. Chem. 275 2000 6395 6403
53. P. Penzes, R.C. Johnson, R. Sattler, X. Zhang, R.L. Huganir, V. Kambampati, R.E. Mains, and B.A. Eipper The neuronal Rho-GEF Kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis Neuron 29 2001 229 242
54. I. Perez-Otano, C.T. Schulteis, A. Contractor, S.A. Lipton, J.S. Trimmer, N.J. Sucher, and S.F. Heinemann Assembly with the NR1 subunit is required for surface expression of NR3A-containing NMDA receptors J. Neurosci. 21 2001 1228 1237
55. M.S. Perkinton, J.K. Ip, G.L. Wood, A.J. Crossthwaite, and R.J. Williams Phosphatidylinositol 3-kinase is a central mediator of NMDA receptor signalling to MAP kinase (Erk1/2), Akt/PKB and CREB in striatal neurones J. Neurochem. 80 2002 239 254
56. F. Polleux, T. Morrow, and A. Ghosh Semaphorin 3A is a chemoattractant for cortical apical dendrites Nature 404 2000 567 573
57. G.J. Ramakers Rho proteins, mental retardation and the cellular basis of cognition Trends Neurosci. 25 2002 191 199
58. D.A. Rubinson, C.P. Dillon, A.V. Kwiatkowski, C. Sievers, L. Yang, J. Kopinja, M. Zhang, M.T. McManus, F.B. Gertler, M.L. Scott, and L. Van Parijs A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference Nat. Genet. 33 2003 401 406
59. E.E. Sander, S. van Delft, J.P. ten Klooster, T. Reid, R.A. van der Kammen, F. Michiels, and J.G. Collard Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase J. Cell Biol. 143 1998 1385 1398
60. P.P. Sanna, M. Cammalleri, F. Berton, C. Simpson, R. Lutjens, F.E. Bloom, and W. Francesconi Phosphatidylinositol 3-kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region J. Neurosci. 22 2002 3359 3365
61. A. Schmidt, and A. Hall Guanine nucleotide exchange factors for Rho GTPases: turning on the switch Genes Dev. 16 2002 1587 1609
62. N. Sestan, S. Artavanis-Tsakonas, and P. Rakic Contact-dependent inhibition of cortical neurite growth mediated by notch signaling Science 286 1999 741 746
63. L.M. Shaw, I. Rabinovitz, H.H. Wang, A. Toker, and A.M. Mercurio Activation of phosphoinositide 3-OH kinase by the α6β4 integrin promotes carcinoma invasion Cell 91 1997 949 960
64. D.A. Sholl Dendritic organization in the neurons of the visual and motor cortices of the cat J. Anat. 87 1953 387 406
65. W.C. Sin, K. Haas, E.S. Ruthazer, and H.T. Cline Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases Nature 419 2002 475 480
66. M. Sone, M. Hoshino, E. Suzuki, S. Kuroda, K. Kaibuchi, H. Nakagoshi, K. Saigo, Y. Nabeshima, and C. Hama Still life, a protein in synaptic terminals of Drosophila homologous to GDP-GTP exchangers Science 275 1997 543 547
67. M. Sone, E. Suzuki, M. Hoshino, D. Hou, H. Kuromi, M. Fukata, S. Kuroda, K. Kaibuchi, Y. Nabeshima, and C. Hama Synaptic development is controlled in the periactive zones of Drosophila synapses Development 127 2000 4157 4168
68. J.C. Stam, E.E. Sander, F. Michiels, F.N. van Leeuwen, H.E. Kain, R.A. van der Kammen, and J.G. Collard Targeting of Tiam1 to the plasma membrane requires the cooperative function of the N-terminal pleckstrin homology domain and an adjacent protein interaction domain J. Biol. Chem. 272 1997 28447 28454
69. O. Steward, and E.M. Schuman Protein synthesis at synaptic sites on dendrites Annu. Rev. Neurosci. 24 2001 299 325
70. O. Steward, and E.M. Schuman Compartmentalized synthesis and degradation of proteins in neurons Neuron 40 2003 347 359
71. M.A. Takasu, M.B. Dalva, R.E. Zigmond, and M.E. Greenberg Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors Science 295 2002 491 495
72. Y. Tang, H. Zhou, A. Chen, R.N. Pittman, and J. Field The Akt proto-oncogene links Ras to Pak and cell survival signals J. Biol. Chem. 275 2000 9106 9109
73. S.J. Tang, G. Reis, H. Kang, A.C. Gingras, N. Sonenberg, and E.M. Schuman A rapamycin-sensitive signaling pathway contributes to long-term synaptic plasticity in the hippocampus Proc. Natl. Acad. Sci. USA 99 2002 467 472
74. A. Tashiro, and R. Yuste Regulation of dendritic spine motility and stability by Rac1 and Rho kinase: evidence for two forms of spine motility Mol. Cell. Neurosci. 26 2004 429 440
75. X. Tian, T. Gotoh, K. Tsuji, E.H. Lo, S. Huang, and L.A. Feig Developmentally regulated role for Ras-GRFs in coupling NMDA glutamate receptors to Ras, Erk and CREB EMBO J. 23 2004 1567 1575
76. K.F. Tolias, L.C. Cantley, and C.L. Carpenter Rho family GTPases bind to phosphoinositide kinases J. Biol. Chem. 270 1995 17656 17659
77. L. Van Aelst, and H.T. Cline Rho GTPases and activity-dependent dendrite development Curr. Opin. Neurobiol. 14 2004 297 304
78. O.D. Weiner, P.O. Neilsen, G.D. Prestwich, M.W. Kirschner, L.C. Cantley, and H.R. Bourne A PtdInsP(3)- and Rho GTPase-mediated positive feedback loop regulates neutrophil polarity Nat. Cell Biol. 4 2002 509 513
79. A.E. West, W.G. Chen, M.B. Dalva, R.E. Dolmetsch, J.M. Kornhauser, A.J. Shaywitz, M.A. Takasu, X. Tao, and M.E. Greenberg Calcium regulation of neuronal gene expression Proc. Natl. Acad. Sci. USA 98 2001 11024 11031
80. A.E. West, E.C. Griffith, and M.E. Greenberg Regulation of transcription factors by neuronal activity Nat. Rev. Neurosci. 3 2002 921 931
81. K.L. Whitford, V. Marillat, E. Stein, C.S. Goodman, M. Tessier-Lavigne, A. Chedotal, and A. Ghosh Regulation of cortical dendrite development by Slit-Robo interactions Neuron 33 2002 47 61
82. R.O. Wong, and A. Ghosh Activity-dependent regulation of dendritic growth and patterning Nat. Rev. Neurosci. 3 2002 803 812
83. Z. Xia, H. Dudek, C.K. Miranti, and M.E. Greenberg Calcium influx via the NMDA receptor induces immediate early gene transcription by a MAP kinase/ERK-dependent mechanism J. Neurosci. 16 1996 5425 5436
84. H.Y. Yun, M. Gonzalez-Zulueta, V.L. Dawson, and T.M. Dawson Nitric oxide mediates N-methyl-D-aspartate receptor-induced activation of p21ras Proc. Natl. Acad. Sci. USA 95 1998 5773 5778