p250GAP, a novel brain-enriched GTPase-activating protein for Rho family GTPases, is involved in the N-methyl-D-aspartate receptor signaling

Molecular Biology of the Cell

Volumn 14, Issue 7, 2003, Pages 2921-2934

  Nakazawa, Takanobu ^a   Watabe, Ayako M ^a   Tezuka, Tohru ^a   Yoshida, Yutaka ^a   Yokoyama, Kazumasa ^a   Umemori, Hisashi ^a   Inoue, Akihiro ^b   Okabe, Shigeo ^b   Manabe, Toshiya ^b,c   Yamamoto, Tadashi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^c KOBE UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN PROTEIN; GLUTAMATE RECEPTOR; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN P250GAP; PROTEIN SUBUNIT; RHO FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BRAIN CORTEX; BRAIN SLICE; CELL DENSITY; CORPUS STRIATUM; DENDRITIC SPINE; DEPHOSPHORYLATION; GENE OVEREXPRESSION; HIPPOCAMPUS; HUMAN; HUMAN CELL; HYDROLYSIS; NERVE CELL PLASTICITY; NEUROBLASTOMA CELL; NUCLEOTIDE SEQUENCE; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; THALAMUS;

ACTINS; AMINO ACID SEQUENCE; ANIMALS; BRAIN; CELLS, CULTURED; GTPASE-ACTIVATING PROTEINS; HUMANS; MICE; MOLECULAR SEQUENCE DATA; NEURITES; NEURONS; RECEPTORS, N-METHYL-D-ASPARTATE; RHO GTP-BINDING PROTEINS; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 12444340440     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-09-0623     Document Type: Article

References (65)

1. Allison, D.W., Gelfand, V.I., Spector, I., and Craig, A.M. (1998). Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J. Neurosci. 18, 2423-2436.
2. Barrett, T., Xiao, B., Dodson, E.J., Doson, G., Ludbrook, S.B., Nurmahomed, K., Gamblin, S.J., Musacchio, A., Smerdon, S.J., and Eccleston, J.F. (1997). The structure of the GTPase-activating domain from p50rhoGAP. Nature 385, 458-461.
3. Bateman, J., Shu, H., and Van Vactor, D. (2000). The guanine nucleotide exchange factor Trio mediates axonal development in the Drosophila embryo. Neuron 26, 93-106.
4. Bito, H., Furuyashiki, T., Ishihara, H., Shibasaki, Y., Ohashi, K., Mizuno, K., Maekawa, M., Ishizaki, T., and Narumiya, S. (2000). A critical role for a Rho-associated kinase, p160ROCK, in determining axon outgrowth in mammalian CNS neurons. Neuron 26, 431-441.
5. Brouns, M.R., Matheson, S.F., Hu, K.Q., Delalle, I., Caviness, V.S., Silver, J., Bronson, R.T., and Settleman, J. (2000). The adhesion signaling molecule p190 RhoGAP is required for morphogenetic processes in neural development. Development 127, 4891-4903.
6. Brouns, M.R., Matheson, S.F., and Settleman, J. (2001). p190 RhoGAP is the principal Src substrate in brain and regulate axon outgrowth, guidance and fasciculation. Nat. Cell Biol. 3, 361-367.
7. Carlin, R.J., Shelton, D.L., Segal, R.A., and Shatz, C.J. (1980). Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J. Cell Biol. 86, 831-843.
8. Engert, F., and Bonhoeffer, T. (1999). Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70.
9. English, J.D., and Sweatt, J.D. (1996). Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J. Biol. Chem. 271, 24329-24332.
10. Feldman, D.E., and Knudsen, E.I. (1998). Experience-dependent plasticity and the maturation of glutamatergic synapses. Neuron 20, 1067-1071.
11. Fiala, J.C., Feinberg, M., Popov, V., and Harris, K.M. (1998). Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J. Neurosci. 18, 8900-8911.
12. Fischer, M., Kaech, S., Knutti, D., and Matus, A. (1998). Rapid actin-based plasticity in dendritic spines. Neuron 20, 847-854.
13. Fischer, M., Kaech, S., Wagner, U., Brinkhaus, H., and Matus, A. (2000). Glutamate receptors regulate actin-based plasticity in dendritic spines. Nat. Neurosci. 3, 887-894.
14. Gomez, L.L., Alam, S., Smith, K.E., Horne, E., and Dell'Acqua, M.L. (2002). 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, 7027-7044.
15. Hall, A. (1998). G proteins and small GTPases: distant relatives keep in touch. Science 279, 509-514.
16. Halpain, S., Hipolito, A., and Saffer, L. (1998). Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin. J. Neurosci. 18, 9835-9844.
17. Hering, H., and Sheng, M. (2001). Dendritic spines: structure, dynamics and regulation. Nat. Rev. Neurosci. 2, 880-888.
18. Husi, H., Ward, M.A., Choudhary, J.S., Blackstock, W.P., and Grant, S.G.N. (2000). Proteomic analysis of NMDA receptor-adhesion protein signaling complexes. Nat. Neurosci. 3, 661-669.
19. Jalink, K., van Corven, E.J., Hengeveld, T., Morii, N., Narumiya, S., and Moolenaar, W.H. (1994). Inhibition of lysophosphatidate- and thrombin-indiced neurite retraction and neuronal cell rounding by ADP ribosylation of the small GTP-binding protein Rho. J. Cell Biol. 126, 801-810.
20. James, P., Halladay, J., and Craig, E.A. (1996). Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144, 1425-1436.
21. Kaech, S., Fischer, M., Doll, T., and Matus, A. (1997). Isoform specificity in the relationship of actin to dendritic spines. J. Neurosci. 17, 9565-9572.
22. Kennedy, M.B. (2000). Signal-processing machines at the postsynaptic density. Science 290, 750-754.
23. Kim, C.H., and Lisman, J.E. (1999). A role of actin filament in synaptic transmission and long-term potentiation. J. Neurosci. 19, 4314-4324.
24. Lamarche, N., and Hall, A. (1994). GAPs for Rho-related GTPases. Trends Genet. 10, 436-440.
25. Lamarche-Vane, N., and Hall, A. (1998). CdGAP, a novel proline-rich GTPase-activating protein for Cdc42 and Rac. J. Biol. Chem. 273, 29172-29177.
26. Lee, T., Winter, C., Martickke, S.S., Lee, A., and Luo, L. (2000). Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 25, 307-316.
27. Li, R., Zhang, B., and Zheng, Y. (1997). Structural determinants required for the interaction between Rho GTPases and the GTPases-activating domain of p190. J. Biol. Chem. 272, 32830-32835.
28. Li, Z., Van Aelst, L., and Cline, H.T. (2000). Rho GTPases regulate distinct aspects of dendritic arbor growth in Xenopus central neurons in vivo. Nat. Neurosci. 3, 217-225.
29. Lendvai, B., Sterrn, E.A., Chen, B., and Svoboda, K. (2000). Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404, 876-881.
30. Luo, L. (2000). Rho GTPases in neuronal morphogenesis. Nat. Rev. Neurosci. 1, 173-180.
31. Luo, L., Hensch, T.K., Ackerman, L., Barbel, S., Jan, L.Y., and Jan, Y.N. (1996). Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines. Nature 379, 837-840.
32. Maletic-Savatic, M., Malinow, R., and Svoboda, K. (1999). Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923-1927.
33. Matus, A., Ackermann, M., Pehling, G., Byers, H.R., and Fujiwara, K. (1982). High actin concentrations in brain dendritic spines and postsynaptic densities. Proc. Natl. Acad. Sci. USA 79, 7590-7594.
34. Moon, S.Y., Zang, H., and Zheng, Y. (2003). Characterization of a brain specific Rho GTPase-activating protein, p200RhoGAP. J. Biol. Chem. 278, 4151-4159.
35. Nakamura, T., Komiya, M., Sone, K., Hirose, E., Gotoh, N., Morii, H., Ohta, Y., and Mori, N. (2002). Grit, a GTPase-activating protein for the Rho family, regulates neurite extension through association with the TrkA receptor and N-Shc and CrkL/Crk adaptor molecules. Mol. Cell. Biol. 22, 8721-8734.
36. Nakayama, A.Y., Harms, M.B., and Luo, L. (2000). Small GTPases Rac and Rho in the maintenance of dendritic spines and branches in hippocampal pyramidal neurons. J. Neurosci. 20, 5329-5338.
37. Nakazawa, T., Komai, S., Tezuka, T., Hisatsune, C., Umemori, H., Semba, K., Mishina, M., Manabe, T., and Yamamoto, T. (2001). Characterization of Fyn-mediated tyrosine phoshorylation sites on GluRε2 (NR2B) subunit of the N-methyl-D-aspartate receptor. J. Biol. Chem. 276, 693-699.
38. Nobes, C.D., and Hall, A. (1995). Rho, Rac, CDC42, GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62.
39. Okabe, S., Kim, H.D., Miwa, A., Kuriu, T., and Okado, H. (1999). Continual remodeling of postsynaptic density and its regulation by synaptic activity. Nat. Neurosci. 2, 804-811.
40. Okabe, T., Nakamura, T., Nishimura, Y.N., Kohu, K., Ohwada, S., Morishita, Y., and Akiyama, T. (2003). RICS, a novel GTPase-activating protein for Cdc42 and Rac1, is involved in the β-catenin-N-cadherin and NMDA receptor signaling. J. Biol. Chem. 278, 9920-9927.
41. Parnass, Z., Tashiro, A., and Yuste, R. (2000). Analysis of spine morphological plasticity in developing hippocampal pyramidal neurons. Hippocampus 10, 561-568.
42. Penzes, P., Johnson, R.C., Sattler, R., Zhang, X., Huganir, R.L., Kambampati, V., Mains, R.E., and Eipper, B.A. (2001). The neuronal Rho-GEF Kalirin-7 interacts with PDZ domain-containing proteins and regulates dendritic morphogenesis. Neuron 29, 229-242.
43. Reid, T., Furuyashiki, T., Ishizaki, T., Watanabe, G., Watanabe, N., Fujisawa, K., Morii, N., Madaule, P., and Narumiya, S. (1996). Rhotekin, a new putative target for Rho bearing homology to a serine/threonine kinase, PKN, and Rhophilin in the Rho-binding domain. J. Biol. Chem. 271, 13556-13560.
44. Ridley, A.J., and Hall, A. (1992). The small GTP-binding protein Rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
45. Rosenmund, C., and Westbrook, G.L. (1993). Calcium-induced actin depolymerization reduces NMDA channel activity. Neuron 10, 805-814.
46. Ruchhoeft, M.L., Ohnuma, S.I., McNeil, L., Holt, C.E., and Harris, W.A. (1999). The neuronal architecture of Xenopus retinal ganglion cells is sculpted by Rho-family GTPases in vivo. J. Neurosci. 19, 8454-8463.
47. Sasaki, T., and Takai, Y. (1998). The Rho small G protein family-Rho GDI system as a temporal and spatial determinant for cytoskeletal control. Biochem. Biophys. Res. Commun. 245, 641-645.
48. Scannevin, R.H., and Huganir, R.L. (2000). Postsynaptic organization and regulation of excitatory synapses. Nat. Rev. Neurosci. 1, 133-141.
49. Shamah, S.M., et al. (2001). EphA receptors regulate growth cone dynamics through the novel guanine nucleotide exchange factor Ephexin. Cell 105, 233-244.
50. Sheng, M., and Pak, D.T. (2000). Ligand-gated ion channel interactions with cytoskeletal and signaling proteins. Annu. Rev. Physiol. 62, 755-778.
51. Sorra, K.E., and Harris, K.M. (1998). Stability in synapse number and size at 2 hr after long-term potentiation in hippocampal area CA1. J. Neurosci. 15, 658-671.
52. Takeuchi, M., Kuramochi, S., Fusaki, N., Nada, S., Kawamura-Tsuzuku, J., Matsuda, S., Semba, K., Toyoshima, K., Okada, M., and Yamamoto, T. (1993). Functional and physical interaction of protein-tyrosine kinases Fyn and Csk in the T-cell signaling system. J. Biol. Chem. 268, 27413-27419.
53. Tashiro, A., Minden, A., and Yuste, R. (2000). Regulation of dendritic spine morphology by the Rho family small GTPases: antagonistic roles of Rac and Rho. Cereb. Cortex 10, 927-938.
54. Tavalin, S.J., Colledge, M., Hell, J.W., Langeberg, L.K., Huganir, R.L., and Scott, J.D. (2002). Regulation of GluR1 by the A-kinase anchoring protein 79 (AKAP79) signaling complex shares properties with long-term depression. J. Neurosci. 22, 3044-3051.
55. Threadgill, R., Bobb, K., and Ghosh, A. (1997). Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron 19, 625-634.
56. Toni, N., Buchs, P.A., Nikonenko, I., Bron, C.R., and Muller, D. (1999). LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402, 421-425.
57. Van Aelst, L., and D'Souza-Schorey, C. (1997). Rho GTPases and signaling networks. Genes Dev. 11, 2295-2322.
58. Watanabe, M., Inoue, Y., Sakimura, K., and Mishina, M. (1992). Developmental changes in distribution of NMDA receptor channel subunit mRNA. Neuroreport 3, 1138-1140.
59. Whitehead, I.P., Campbell, S., Rossman, K.L., and Der, C.J. (1997). Dbl family proteins. Biochem. Biophys. Acta 1332, F1-F23.
60. Wong, W.T., Faulkner-Jones, B.E., Sanes, J.R., and Wong, R.O. (2000). Rapid dendritic remodeling in the developing retina: dependence on neurotransmission and reciprocal regulation by Rac and Rho. J. Neurosci. 20, 5024-5036.
61. Wyszynski, M., Kharazia, V., Shanghvi, R., Rao, A., Beggs, A.H., Craig, A.M., Weinberg, R., and Sheng, M. (1998). Differential regional expression and ultrastructural localization of alpha-actinin-2, a putative NMDA receptor-anchoring protein, in rat brain. J. Neurosci. 18, 1383-1392.
62. Yamaguchi, Y., Katoh, H., Yasui, H., Mori, K., and Negishi, M. (2001). RhoA inhibits the nerve growth factor-induced Rac1 activation through Rho-associated kinase-dependent pathway. J. Biol. Chem. 276, 18977-18983.
63. Yoshida, Y., et al. (2000). Negative regulation of BMP/Smad signaling by Tob in osteoblasts. Cell 103, 1085-1097.
64. Yuste, R., and Bonhoeffer, T. (2001). Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu. Rev. Neurosci. 24, 1071-1089.
65. Zipkin, I.D., Kindt, R.M., and Kenyon, C.J. (1997). Role of a new Rho family member in cell migration and axon guidance in C. elegans. Cell 90, 883-894.