Regulation of Rap GTPases in mammalian neurons (original) (raw)

Acknowledgments:

B.S. was supported by the Cluster of Excellence Cells in Motion.

Funding: DFG (Grant/Award Number: ‘EXC 1003 – CiM’).

References

Ang, X.L., Seeburg, D.P., Sheng, M., and Harper, J.W. (2008). Regulation of postsynaptic RapGAP SPAR by Polo-like kinase 2 and the SCFβ-TRCP ubiquitin ligase in hippocampal neurons. J. Biol. Chem. 283, 29424–29432.10.1074/jbc.M802475200 Search in Google Scholar PubMed PubMed Central

Antoine-Bertrand, J., Duquette, P.M., Alchini, R., Kennedy, T.E., Fournier, A.E., and Lamarche-Vane, N. (2016). p120RasGAP protein mediates Netrin-1 protein-induced cortical axon outgrowth and guidance. J. Biol. Chem. 291, 4589–4602.10.1074/jbc.M115.674846 Search in Google Scholar PubMed PubMed Central

Araki, Y., Zeng, M., Zhang, M., and Huganir, R.L. (2015). Rapid dispersion of SynGAP from synaptic spines triggers AMPA receptor insertion and spine enlargement during LTP. Neuron 85, 173–189.10.1016/j.neuron.2014.12.023 Search in Google Scholar PubMed PubMed Central

Asha, H., de Ruiter, N.D., Wang, M.G., and Hariharan, I.K. (1999). The Rap1 GTPase functions as a regulator of morphogenesis in vivo. EMBO J. 18, 605–615.10.1093/emboj/18.3.605 Search in Google Scholar PubMed PubMed Central

Azoulay-Alfaguter, I., Strazza, M., and Mor, A. (2015). Chaperone-mediated specificity in Ras and Rap signaling. Crit. Rev. Biochem. Mol. Biol. 50, 194–202.10.3109/10409238.2014.989308 Search in Google Scholar PubMed

Bailey, C.H., Kandel, E.R., and Harris, K.M. (2015). Structural components of synaptic plasticity and memory consolidation. Cold Spring Harb. Perspect. Biol. 7, a021758.10.1101/cshperspect.a021758 Search in Google Scholar PubMed PubMed Central

Ballif, B.A., Arnaud, L., Arthur, W.T., Guris, D., Imamoto, A., and Cooper, J.A. (2004). Activation of a Dab1/CrkL/C3G/Rap1 pathway in Reelin-stimulated neurons. Curr. Biol. 14, 606–610.10.1016/j.cub.2004.03.038 Search in Google Scholar PubMed

Baron, J., Blex, C., Rohrbeck, A., Rachakonda, S.K., Birnbaumer, L., Ahnert-Hilger, G., and Brunk, I. (2013). The alpha-subunit of the trimeric GTPase Go2 regulates axonal growth. J. Neurochem. 124, 782–794.10.1111/jnc.12123 Search in Google Scholar PubMed PubMed Central

Beggs, H., Schahin-Reed, D., Zang, K., Goebbels, S., Nave, K., Gorski, J., Jones, K., Sretavan, D., and Reichardt, L. (2003). FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40, 501–514.10.1016/S0896-6273(03)00666-4 Search in Google Scholar

Beranger, F., Goud, B., Tavitian, A., and de Gunzburg, J. (1991). Association of the Ras-antagonistic Rap1/Krev-1 proteins with the Golgi complex. Proc. Natl. Acad. Sci. USA 88, 1606–1610.10.1073/pnas.88.5.1606 Search in Google Scholar PubMed PubMed Central

Berg, T.J., Gastonguay, A.J., Lorimer, E.L., Kuhnmuench, J.R., Li, R., Fields, A.P., and Williams, C.L. (2010). Splice variants of SmgGDS control small GTPase prenylation and membrane localization. J. Biol. Chem. 285, 35255–35266.10.1074/jbc.M110.129916 Search in Google Scholar PubMed PubMed Central

Bilasy, S.E., Satoh, T., Ueda, S., Wei, P., Kanemura, H., Aiba, A., Terashima, T., and Kataoka, T. (2009). Dorsal telencephalon-specific RA-GEF-1 knockout mice develop heterotopic cortical mass and commissural fiber defect. Eur. J. Neurosci. 29, 1994–2008.10.1111/j.1460-9568.2009.06754.x Search in Google Scholar PubMed

Bilasy, S.E., Satoh, T., Terashima, T., and Kataoka, T. (2011). RA-GEF-1 (Rapgef2) is essential for proper development of the midline commissures. Neurosci. Res. 71, 200–209.10.1016/j.neures.2011.08.004 Search in Google Scholar PubMed

Bithell, A., Alberta, J., Hornby, F., Stiles, C.D., and Williams, B.P. (2003). Expression of the guanine nucleotide exchange factor, mr-gef, is regulated during the differentiation of specific subsets of telencephalic neurons. Brain Res. Dev. Brain. Res. 146, 107–118.10.1016/j.devbrainres.2003.09.017 Search in Google Scholar PubMed

Bivona, T.G., Wiener, H.H., Ahearn, I.M., Silletti, J., Chiu, V.K., and Philips, M.R. (2004). Rap1 up-regulation and activation on plasma membrane regulates T cell adhesion. J. Cell. Biol. 164, 461–470.10.1083/jcb.200311093 Search in Google Scholar PubMed PubMed Central

Bock, H.H. and Herz, J. (2003). Reelin activates SRC family tyrosine kinases in neurons. Curr. Biol. 13, 18–26.10.1016/S0960-9822(02)01403-3 Search in Google Scholar

Bos, J.L., de Rooij, J., and Reedquist, K.A. (2001). Rap1 signalling: adhering to new models. Nat. Rev. Mol. Cell. Biol. 2, 369–377.10.1038/35073073 Search in Google Scholar PubMed

Bos, J.L., Rehmann, H., and Wittinghofer, A. (2007). GEFs and GAPs: critical elements in the control of small G proteins. Cell 129, 865–877.10.1016/j.cell.2007.05.018 Search in Google Scholar PubMed

Bruurs, L.J. and Bos, J.L. (2014). Mechanisms of isoform specific Rap2 signaling during enterocytic brush border formation. PLoS One 9, e106687.10.1371/journal.pone.0106687 Search in Google Scholar PubMed PubMed Central

Cahill, M.E., Bagot, R.C., Gancarz, A.M., Walker, D.M., Sun, H., Wang, Z.J., Heller, E.A., Feng, J., Kennedy, P.J., Koo, J.W., et al. (2016). Bidirectional synaptic structural plasticity after chronic cocaine administration occurs through Rap1 small GTPase signaling. Neuron 89, 566–582.10.1016/j.neuron.2016.01.031 Search in Google Scholar PubMed PubMed Central

Carlisle, H.J., Manzerra, P., Marcora, E., and Kennedy, M.B. (2008). SynGAP regulates steady-state and activity-dependent phosphorylation of cofilin. J. Neurosci. 28, 13673–13683.10.1523/JNEUROSCI.4695-08.2008 Search in Google Scholar PubMed PubMed Central

Chen, H.J., Rojas-Soto, M., Oguni, A., and Kennedy, M.B. (1998). A synaptic Ras-GTPase activating protein (p135 SynGAP) inhibited by CaM kinase II. Neuron 20, 895–904.10.1016/S0896-6273(00)80471-7 Search in Google Scholar PubMed

Cherfils, J. and Zeghouf, M. (2013). Regulation of small GTPases by GEFs, GAPs, and GDIs. Physiol. Rev. 93, 269–309.10.1152/physrev.00003.2012 Search in Google Scholar PubMed

Chrzanowska-Wodnicka, M., White, G.C., 2nd, Quilliam, L.A., and Whitehead, K.J. (2015). Small GTPase Rap1 is essential for mouse development and formation of functional vasculature. PLoS One 10, e0145689.10.1371/journal.pone.0145689 Search in Google Scholar PubMed PubMed Central

Clement, J.P., Aceti, M., Creson, T.K., Ozkan, E.D., Shi, Y., Reish, N.J., Almonte, A.G., Miller, B.H., Wiltgen, B.J., Miller, C.A., et al. (2012). Pathogenic SYNGAP1 mutations impair cognitive development by disrupting maturation of dendritic spine synapses. Cell 151, 709–723.10.1016/j.cell.2012.08.045 Search in Google Scholar PubMed PubMed Central

Consonni, S.V., Gloerich, M., Spanjaard, E., and Bos, J.L. (2012). cAMP regulates DEP domain-mediated binding of the guanine nucleotide exchange factor Epac1 to phosphatidic acid at the plasma membrane. Proc. Natl. Acad. Sci. USA 109, 3814–3819.10.1073/pnas.1117599109 Search in Google Scholar PubMed PubMed Central

Crittenden, J.R., Bergmeier, W., Zhang, Y., Piffath, C.L., Liang, Y., Wagner, D.D., Housman, D.E., and Graybiel, A.M. (2004). CalDAG-GEFI integrates signaling for platelet aggregation and thrombus formation. Nat. Med. 10, 982–986.10.1038/nm1098 Search in Google Scholar PubMed

Dai, Y., Walker, S.A., de Vet, E., Cook, S., Welch, H.C., and Lockyer, P.J. (2011). Ca2+-dependent monomer and dimer formation switches CAPRI Protein between Ras GTPase-activating protein (GAP) and RapGAP activities. J. Biol. Chem. 286, 19905–19916.10.1074/jbc.M110.201301 Search in Google Scholar PubMed PubMed Central

de Rooij, J., Zwartkruis, F.J.T., Verheijen, M.H.G., Cool, R.H., Nijman, S.M.B., Wittinghofer, A., and Bos, J.L. (1998). Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396, 474–477.10.1038/24884 Search in Google Scholar PubMed

de Rooij, J., Boenink, N.M., van Triest, M., Cool, R.H., Wittinghofer, A., and Bos, J.L. (1999). PDZ-GEF1, a guanine nucleotide exchange factor specific for Rap1 and Rap2. J. Biol. Chem. 274, 38125–38130.10.1074/jbc.274.53.38125 Search in Google Scholar PubMed

de Rooij, J., Rehmann, H., van Triest, M., Cool, R.H., Wittinghofer, A., and Bos, J.L. (2000). Mechanism of regulation of the Epac family of cAMP-dependent RapGEFs. J. Biol. Chem. 275, 20829–20836.10.1074/jbc.M001113200 Search in Google Scholar PubMed

Dolnik, A., Kanwal, N., Mackert, S., Halbedl, S., Proepper, C., Bockmann, J., Schoen, M., Boeckers, T.M., Kuhl, S.J., and Schmeisser, M.J. (2016). Sipa1l3/SPAR3 is targeted to postsynaptic specializations and interacts with the Fezzin ProSAPiP1/Lzts3. J. Neurochem. 136, 28–35.10.1111/jnc.13353 Search in Google Scholar PubMed

Dower, N.A., Stang, S.L., Bottorff, D.A., Ebinu, J.O., Dickie, P., Ostergaard, H.L., and Stone, J.C. (2000). RasGRP is essential for mouse thymocyte differentiation and TCR signaling. Nat. Immunol. 1, 317–321.10.1038/79766 Search in Google Scholar PubMed

Fansa, E.K., Dvorsky, R., Zhang, S.C., Fiegen, D., and Ahmadian, M.R. (2013). Interaction characteristics of Plexin-B1 with Rho family proteins. Biochem. Biophys. Res. Commun. 434, 785–790.10.1016/j.bbrc.2013.04.012 Search in Google Scholar PubMed

Fernandes, H.B., Riordan, S., Nomura, T., Remmers, C.L., Kraniotis, S., Marshall, J.J., Kukreja, L., Vassar, R., and Contractor, A. (2015). Epac2 mediates cAMP-dependent potentiation of neurotransmission in the hippocampus. J. Neurosci. 35, 6544–6553.10.1523/JNEUROSCI.0314-14.2015 Search in Google Scholar PubMed PubMed Central

Franco, S.J., Martinez-Garay, I., Gil-Sanz, C., Harkins-Perry, S.R., and Müller, U. (2011). Reelin regulates cadherin function via Dab1/Rap1 to control neuronal migration and lamination in the neocortex. Neuron 69, 482–497.10.1016/j.neuron.2011.01.003 Search in Google Scholar PubMed PubMed Central

Frische, E.W., Pellis-van Berkel, W., van Haaften, G., Cuppen, E., Plasterk, R.H., Tijsterman, M., Bos, J.L., and Zwartkruis, F.J. (2007). RAP-1 and the RAL-1/exocyst pathway coordinate hypodermal cell organization in Caenorhabditis elegans. EMBO J. 26, 5083–5092.10.1038/sj.emboj.7601922 Search in Google Scholar PubMed PubMed Central

Frotscher, M. (2010). Role for Reelin in stabilizing cortical architecture. Trends. Neurosci. 33, 407–414.10.1016/j.tins.2010.06.001 Search in Google Scholar PubMed

Fu, Z., Lee, S.H., Simonetta, A., Hansen, J., Sheng, M., and Pak, D.T. (2007). Differential roles of Rap1 and Rap2 small GTPases in neurite retraction and synapse elimination in hippocampal spiny neurons. J. Neurochem. 100, 118–131.10.1111/j.1471-4159.2006.04195.x Search in Google Scholar PubMed

Fukuyama, T., Ogita, H., Kawakatsu, T., Fukuhara, T., Yamada, T., Sato, T., Shimizu, K., Nakamura, T., Matsuda, M., and Takai, Y. (2005). Involvement of the c-Src-Crk-C3G-Rap1 signaling in the nectin-induced activation of Cdc42 and formation of adherens junctions. J Biol Chem. 280, 815–825.10.1074/jbc.M411099200 Search in Google Scholar PubMed

Gao, P., Sultan, K.T., Zhang, X.J., and Shi, S.H. (2013). Lineage-dependent circuit assembly in the neocortex. Development 140, 2645–2655.10.1242/dev.087668 Search in Google Scholar PubMed PubMed Central

Gasper, R., Sot, B., and Wittinghofer, A. (2010). GTPase activity of Di-Ras proteins is stimulated by Rap1GAP proteins. Small GTPases 1, 133–141.10.4161/sgtp.1.3.14742 Search in Google Scholar PubMed PubMed Central

Gekel, I. and Neher, E. (2008). Application of an Epac activator enhances neurotransmitter release at excitatory central synapses. J. Neurosci. 28, 7991–8002.10.1523/JNEUROSCI.0268-08.2008 Search in Google Scholar PubMed PubMed Central

Gil-Sanz, C., Franco, S.J., Martinez-Garay, I., Espinosa, A., Harkins-Perry, S., and Muller, U. (2013). Cajal-Retzius cells instruct neuronal migration by coincidence signaling between secreted and contact-dependent guidance cues. Neuron 79, 461–477.10.1016/j.neuron.2013.06.040 Search in Google Scholar PubMed PubMed Central

Gloerich, M. and Bos, J.L. (2011). Regulating Rap small G-proteins in time and space. Trends Cell Biol. 21, 615–623.10.1016/j.tcb.2011.07.001 Search in Google Scholar PubMed

Gloerich, M., ten Klooster, J.P., Vliem, M.J., Koorman, T., Zwartkruis, F.J., Clevers, H., and Bos, J.L. (2012). Rap2A links intestinal cell polarity to brush border formation. Nat. Cell Biol. 14, 793–801.10.1038/ncb2537 Search in Google Scholar PubMed

Golec, D.P., Dower, N.A., Stone, J.C., and Baldwin, T.A. (2013). RasGRP1, but not RasGRP3, is required for efficient thymic beta-selection and ERK activation downstream of CXCR4. PLoS One 8, e53300.10.1371/journal.pone.0053300 Search in Google Scholar PubMed PubMed Central

Gotoh, T., Hattori, S., Nakamura, S., Kitayama, H., Noda, M., Takai, Y., Kaibuchi, K., Matsui, H., Hatase, O., Takahashi, H., et al. (1995). Identification of Rap1 as a target for the Crk SH3 domain-binding guanine nucleotide-releasing factor C3G. Mol. Cell. Biol. 15, 6746–6753.10.1128/MCB.15.12.6746 Search in Google Scholar PubMed PubMed Central

Graus-Porta, D., Blaess, S., Senften, M., Littlewood-Evans, A., Damsky, C., Huang, Z., Orban, P., Klein, R., Schittny, J., and Müller, U. (2001). Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31, 367–379.10.1016/S0896-6273(01)00374-9 Search in Google Scholar

Greenlees, R., Mihelec, M., Yousoof, S., Speidel, D., Wu, S.K., Rinkwitz, S., Prokudin, I., Perveen, R., Cheng, A.S., Ma, A., et al. (2015). Mutations in SIPA1L3 cause eye defects through disruption of cell polarity and cytoskeleton organization. Hum. Mol. Genet. 24, 5789–5804.10.1093/hmg/ddv298 Search in Google Scholar PubMed

Gupta, A., Tsai, L.H., and Wynshaw-Boris, A. (2002). Life is a journey: a genetic look at neocortical development. Nat. Rev. Genet. 3, 342–355.10.1038/nrg799 Search in Google Scholar PubMed

Hattori, M., Tsukamoto, N., Nur-e-Kamal, M.S., Rubinfeld, B., Iwai, K., Kubota, H., Maruta, H., and Minato, N. (1995). Molecular cloning of a novel mitogen-inducible nuclear protein with a Ran GTPase-activating domain that affects cell cycle progression. Mol. Cell. Biol. 15, 552–560.10.1128/MCB.15.1.552 Search in Google Scholar PubMed PubMed Central

Herz, J. and Chen, Y. (2006). Reelin, lipoprotein receptors and synaptic plasticity. Nat. Rev. Neurosci. 7, 850–859.10.1038/nrn2009 Search in Google Scholar PubMed

Hisata, S., Sakisaka, T., Baba, T., Yamada, T., Aoki, K., Matsuda, M., and Takai, Y. (2007). Rap1-PDZ-GEF1 interacts with a neurotrophin receptor at late endosomes, leading to sustained activation of Rap1 and ERK and neurite outgrowth. J. Cell Biol. 178, 843–860.10.1083/jcb.200610073 Search in Google Scholar PubMed PubMed Central

Hoffmeister, M., Riha, P., Neumuller, O., Danielewski, O., Schultess, J., and Smolenski, A.P. (2008). Cyclic nucleotide-dependent protein kinases inhibit binding of 14-3-3 to the GTPase-activating protein Rap1GAP2 in platelets. J. Biol. Chem. 283, 2297–2306.10.1074/jbc.M706825200 Search in Google Scholar PubMed

Homayouni, R., Magdaleno, S., Keshvara, L., Rice, D.S., and Curran, T. (2003). Interaction of Disabled-1 and the GTPase activating protein Dab2IP in mouse brain. Brain Res. Mol. Brain Res. 115, 121–129.10.1016/S0169-328X(03)00176-1 Search in Google Scholar

Hota, P.K. and Buck, M. (2012). Plexin structures are coming: opportunities for multilevel investigations of semaphorin guidance receptors, their cell signaling mechanisms, and functions. Cell. Mol. Life Sci. 69, 3765–3805.10.1007/s00018-012-1019-0 Search in Google Scholar PubMed

Hotulainen, P. and Hoogenraad, C.C. (2010). Actin in dendritic spines: connecting dynamics to function. J. Cell. Biol. 189, 619–629.10.1083/jcb.201003008 Search in Google Scholar PubMed PubMed Central

Huelsmann, S., Hepper, C., Marchese, D., Knoll, C., and Reuter, R. (2006). The PDZ-GEF dizzy regulates cell shape of migrating macrophages via Rap1 and integrins in the Drosophila embryo. Development 133, 2915–2924.10.1242/dev.02449 Search in Google Scholar PubMed

Hussain, N.K., Hsin, H., Huganir, R.L., and Sheng, M. (2010). MINK and TNIK differentially act on Rap2-mediated signal transduction to regulate neuronal structure and AMPA receptor function. J. Neurosci. 30, 14786–14794.10.1523/JNEUROSCI.4124-10.2010 Search in Google Scholar PubMed PubMed Central

Ichiba, T., Hashimoto, Y., Nakaya, M., Kuraishi, Y., Tanaka, S., Kurata, T., Mochizuki, N., and Matsuda, M. (1999). Activation of C3G guanine nucleotide exchange factor for Rap1 by phosphorylation of tyrosine 504. J. Biol. Chem. 274, 14376–14381.10.1074/jbc.274.20.14376 Search in Google Scholar PubMed

Iwashita, S., Kobayashi, M., Kubo, Y., Hinohara, Y., Sezaki, M., Nakamura, K., Suzuki-Migishima, R., Yokoyama, M., Sato, S., Fukuda, M., et al. (2007). Versatile roles of R-Ras GAP in neurite formation of PC12 cells and embryonic vascular development. J. Biol. Chem. 282, 3413–3417.10.1074/jbc.C600293200 Search in Google Scholar PubMed

Iwig, J.S., Vercoulen, Y., Das, R., Barros, T., Limnander, A., Che, Y., Pelton, J.G., Wemmer, D.E., Roose, J.P., and Kuriyan, J. (2013). Structural analysis of autoinhibition in the Ras-specific exchange factor RasGRP1. Elife 2, e00813.10.7554/eLife.00813 Search in Google Scholar PubMed PubMed Central

Janoueix-Lerosey, I., Polakis, P., Tavitian, A., and de Gunzburg, J. (1992). Regulation of the GTPase activity of the ras-related rap2 protein. Biochem. Biophys. Res. Commun. 189, 455–464.10.1016/0006-291X(92)91580-J Search in Google Scholar PubMed

Jeyabalan, N. and Clement, J.P. (2016). SYNGAP1: mind the Gap. Front. Cell. Neurosci. 10, 32.10.3389/fncel.2016.00032 Search in Google Scholar PubMed PubMed Central

Jin, T.G., Satoh, T., Liao, Y., Song, C., Gao, X., Kariya, K., Hu, C.D., and Kataoka, T. (2001). Role of the CDC25 homology domain of phospholipase Cε in amplification of Rap1-dependent signaling. J. Biol. Chem. 276, 30301–30307.10.1074/jbc.M103530200 Search in Google Scholar PubMed

Jongbloets, B.C. and Pasterkamp, R.J. (2014). Semaphorin signalling during development Development 141, 3292–3297.10.1242/dev.105544 Search in Google Scholar PubMed

Jordan, J.D., Carey, K.D., Stork, P.J., and Iyengar, R. (1999). Modulation of rap activity by direct interaction of Gα(o) with Rap1 GTPase-activating protein. J. Biol. Chem. 274, 21507–21510.10.1074/jbc.274.31.21507 Search in Google Scholar PubMed

Jossin, Y. and Cooper, J. (2011). Reelin, Rap1 and N-cadherin orient the migration of multipolar neurons in the developing neocortex. Nat. Neurosci. 14, 697–703.10.1038/nn.2816 Search in Google Scholar PubMed PubMed Central

Jossin, Y. and Goffinet, A.M. (2001). Reelin does not directly influence axonal growth. J. Neurosci. 21, RC183.10.1523/JNEUROSCI.21-23-j0001.2001 Search in Google Scholar PubMed PubMed Central

Kawabe, H., Neeb, A., Dimova, K., Young, S.M., Jr., Takeda, M., Katsurabayashi, S., Mitkovski, M., Malakhova, O.A., Zhang, D.E., Umikawa, M., et al. (2010). Regulation of Rap2A by the ubiquitin ligase Nedd4-1 controls neurite development. Neuron 65, 358–372.10.1016/j.neuron.2010.01.007 Search in Google Scholar PubMed PubMed Central

Kawasaki, H., Springett, G.M., Mochizuki, N., Toki, S., Nakaya, M., Matsuda, M., Housman, D.E., and Graybiel, A.M. (1998a). A family of cAMP-binding proteins that directly activate Rap1. Science 282, 2275–2279.10.1126/science.282.5397.2275 Search in Google Scholar PubMed

Kawasaki, H., Springett, G.M., Toki, S., Canales, J.J., Harlan, P., Blumenstiel, J.P., Chen, E.J., Bany, I.A., Mochizuki, N., Ashbacher, A., et al. (1998b). A Rap guanine nucleotide exchange factor enriched highly in the basal ganglia. Proc. Natl. Acad. Sci. USA 95, 13278–13283.10.1073/pnas.95.22.13278 Search in Google Scholar PubMed PubMed Central

Kielland, A., Bochorishvili, G., Corson, J., Zhang, L., Rosin, D.L., Heggelund, P., and Zhu, J.J. (2009). Activity patterns govern synapse-specific AMPA receptor trafficking between deliverable and synaptic pools. Neuron 62, 84–101.10.1016/j.neuron.2009.03.001 Search in Google Scholar PubMed PubMed Central

Kim, J.H., Liao, D., Lau, L.F., and Huganir, R.L. (1998). SynGAP: a synaptic RasGAP that associates with the PSD-95/SAP90 protein family. Neuron 20, 683–691.10.1016/S0896-6273(00)81008-9 Search in Google Scholar PubMed

Kim, J.H., Lee, H.K., Takamiya, K., and Huganir, R.L. (2003). The role of synaptic GTPase-activating protein in neuronal development and synaptic plasticity. J. Neurosci. 23, 1119–1124.10.1523/JNEUROSCI.23-04-01119.2003 Search in Google Scholar PubMed PubMed Central

Knox, A.L. and Brown, N.H. (2002). Rap1 GTPase regulation of adherens junction positioning and cell adhesion. Science 295, 1285–1288.10.1126/science.1067549 Search in Google Scholar PubMed

Knuesel, I., Elliott, A., Chen, H.J., Mansuy, I.M., and Kennedy, M.B. (2005). A role for synGAP in regulating neuronal apoptosis. Eur. J. Neurosci. 21, 611–621.10.1111/j.1460-9568.2005.03908.x Search in Google Scholar PubMed

Kruger, R.P., Aurandt, J., and Guan, K.L. (2005). Semaphorins command cells to move. Nat. Rev. Mol. Cell. Biol. 6, 789–800.10.1038/nrm1740 Search in Google Scholar PubMed

Kuiperij, H.B., de Rooij, J., Rehmann, H., van Triest, M., Wittinghofer, A., Bos, J.L., and Zwartkruis, F.J. (2003). Characterisation of PDZ-GEFs, a family of guanine nucleotide exchange factors specific for Rap1 and Rap2. Biochim. Biophys. Acta 1593, 141–149.10.1016/S0167-4889(02)00365-8 Search in Google Scholar

Kuo, G., Arnaud, L., Kronstad-O’Brien, P., and Cooper, J.A. (2005). Absence of Fyn and Src causes a reeler-like phenotype. J. Neurosci. 25, 8578–8586.10.1523/JNEUROSCI.1656-05.2005 Search in Google Scholar PubMed PubMed Central

Kupzig, S., Bouyoucef-Cherchalli, D., Yarwood, S., Sessions, R., and Cullen, P.J. (2009). The ability of GAP1IP4BP to function as a Rap1 GTPase-activating protein (GAP) requires its Ras GAP-related domain and an arginine finger rather than an asparagine thumb. Mol. Cell. Biol. 29, 3929–3940.10.1128/MCB.00427-09 Search in Google Scholar PubMed PubMed Central

Lee, K.J., Lee, Y., Rozeboom, A., Lee, J.Y., Udagawa, N., Hoe, H.S., and Pak, D.T. (2011). Requirement for Plk2 in orchestrated ras and rap signaling, homeostatic structural plasticity, and memory. Neuron 69, 957–973.10.1016/j.neuron.2011.02.004 Search in Google Scholar PubMed PubMed Central

Lee, G.H., Kim, S.H., Homayouni, R., and D’Arcangelo, G. (2012). Dab2ip regulates neuronal migration and neurite outgrowth in the developing neocortex. PLoS One 7, e46592.10.1371/journal.pone.0046592 Search in Google Scholar PubMed PubMed Central

Lee, K., Kobayashi, Y., Seo, H., Kwak, J.H., Masuda, A., Lim, C.S., Lee, H.R., Kang, S.J., Park, P., Sim, S.E., et al. (2015). Involvement of cAMP-guanine nucleotide exchange factor II in hippocampal long-term depression and behavioral flexibility. Mol. Brain 8, 38.10.1186/s13041-015-0130-1 Search in Google Scholar PubMed PubMed Central

Levy, R.J., Kvajo, M., Li, Y., Tsvetkov, E., Dong, W., Yoshikawa, Y., Kataoka, T., Bolshakov, V.Y., Karayiorgou, M., and Gogos, J.A. (2015). Deletion of Rapgef6, a candidate schizophrenia susceptibility gene, disrupts amygdala function in mice. Transl. Psychiatry 5, e577.10.1038/tp.2015.75 Search in Google Scholar PubMed PubMed Central

Li, Y., Asuri, S., Rebhun, J.F., Castro, A.F., Paranavitana, N.C., and Quilliam, L.A. (2006). The RAP1 guanine nucleotide exchange factor Epac2 couples cyclic AMP and Ras signals at the plasma membrane. J. Biol. Chem. 281, 2506–2514.10.1074/jbc.M508165200 Search in Google Scholar PubMed

Liao, Y., Satoh, T., Gao, X., Jin, T.G., Hu, C.D., and Kataoka, T. (2001). RA-GEF-1, a guanine nucleotide exchange factor for Rap1, is activated by translocation induced by association with Rap1*GTP and enhances Rap1-dependent B-Raf activation. J. Biol. Chem. 276, 28478–28483.10.1074/jbc.M101737200 Search in Google Scholar PubMed

Liu, C., Takahashi, M., Li, Y.P., Song, S., Dillon, T.J., Shinde, U., and Stork, P.J.S. (2008). Ras is required for the cyclic AMP-dependent activation of Rap1 via Epac2. Mol. Cell. Biol. 28, 7109–7125.10.1128/MCB.01060-08 Search in Google Scholar PubMed PubMed Central

Liu, A., Zhou, Z., Dang, R., Zhu, Y., Qi, J., He, G., Leung, C., Pak, D., Jia, Z., and Xie, W. (2016). Neuroligin 1 regulates spines and synaptic plasticity via LIMK1/cofilin-mediated actin reorganization. J. Cell. Biol. 212, 449–463.10.1083/jcb.201509023 Search in Google Scholar PubMed PubMed Central

Lockyer, P.J., Kupzig, S., and Cullen, P.J. (2001). CAPRI regulates Ca2+-dependent inactivation of the Ras-MAPK pathway. Curr. Biol. 11, 981–986.10.1016/S0960-9822(01)00261-5 Search in Google Scholar PubMed

Maruoka, H., Konno, D., Hori, K., and Sobue, K. (2005). Collaboration of PSD-Zip70 with its binding partner, SPAR, in dendritic spine maturity. J. Neurosci. 25, 1421–1430.10.1523/JNEUROSCI.3920-04.2005 Search in Google Scholar PubMed PubMed Central

Mayanagi, T., Yasuda, H., and Sobue, K. (2015). PSD-Zip70 deficiency causes prefrontal hypofunction associated with glutamatergic synapse maturation defects by dysregulation of Rap2 activity. J. Neurosci. 35, 14327–14340.10.1523/JNEUROSCI.2349-15.2015 Search in Google Scholar PubMed PubMed Central

McAvoy, T., Zhou, M.M., Greengard, P., and Nairn, A.C. (2009). Phosphorylation of Rap1GAP, a striatally enriched protein, by protein kinase A controls Rap1 activity and dendritic spine morphology. Proc. Natl. Acad. Sci. USA 106, 3531–3536.10.1073/pnas.0813263106 Search in Google Scholar PubMed PubMed Central

Meng, J. and Casey, P.J. (2002). Activation of Gz attenuates Rap1-mediated differentiation of PC12 cells. J. Biol. Chem. 277, 43417–43424.10.1074/jbc.M204074200 Search in Google Scholar PubMed

Meyer, G. (2010). Building a human cortex: the evolutionary differentiation of Cajal-Retzius cells and the cortical hem. J. Anat. 217, 334–343.10.1111/j.1469-7580.2010.01266.x Search in Google Scholar PubMed PubMed Central

Mochizuki, N., Ohba, Y., Kiyokawa, E., Kurata, T., Murakami, T., Ozaki, T., Kitabatake, A., Nagashima, K., and Matsuda, M. (1999). Activation of the ERK/MAPK pathway by an isoform of rap1GAP associated with Gα(i). Nature 400, 891–894.10.1038/23738 Search in Google Scholar PubMed

Morozov, A., Muzzio, I.A., Bourtchouladze, R., Van-Strien, N., Lapidus, K., Yin, D., Winder, D.G., Adams, J.P., Sweatt, J.D., and Kandel, E.R. (2003). Rap1 couples cAMP signaling to a distinct pool of p42/44MAPK regulating excitability, synaptic plasticity, learning, and memory. Neuron 39, 309–325.10.1016/S0896-6273(03)00404-5 Search in Google Scholar PubMed

Munoz-Llancao, P., Henriquez, D.R., Wilson, C., Bodaleo, F., Boddeke, E.W., Lezoualc’h, F., Schmidt, M., and Gonzalez-Billault, C. (2015). Exchange protein directly activated by cAMP (EPAC) regulates neuronal polarization through Rap1B. J. Neurosci. 35, 11315–11329.10.1523/JNEUROSCI.3645-14.2015 Search in Google Scholar PubMed PubMed Central

Muro, R., Nitta, T., Okada, T., Ideta, H., Tsubata, T., and Suzuki, H. (2015). The Ras GTPase-activating protein Rasal3 supports survival of naive T cells. PLoS One 10, e0119898.10.1371/journal.pone.0119898 Search in Google Scholar PubMed PubMed Central

Nagai, T., Nakamuta, S., Kuroda, K., Nakauchi, S., Nishioka, T., Takano, T., Zhang, X., Tsuboi, D., Funahashi, Y., Nakano, T., et al. (2016). Phosphoproteomics of the dopamine pathway enables discovery of Rap1 activation as a reward signal in vivo. Neuron 89, 550–565.10.1016/j.neuron.2015.12.019 Search in Google Scholar PubMed

Nakamura, T., Yasuda, S., Nagai, H., Koinuma, S., Morishita, S., Goto, A., Kinashi, T., and Wada, N. (2013). Longest neurite-specific activation of Rap1B in hippocampal neurons contributes to polarity formation through RalA and Nore1A in addition to PI3-kinase. Genes Cells 18, 1020–1031.10.1111/gtc.12097 Search in Google Scholar PubMed

Nonaka, H., Takei, K., Umikawa, M., Oshiro, M., Kuninaka, K., Bayarjargal, M., Asato, T., Yamashiro, Y., Uechi, Y., Endo, S., et al. (2008). MINK is a Rap2 effector for phosphorylation of the postsynaptic scaffold protein TANC1. Biochem. Biophys. Res. Commun. 377, 573–578.10.1016/j.bbrc.2008.10.038 Search in Google Scholar PubMed

Ntantie, E., Gonyo, P., Lorimer, E.L., Hauser, A.D., Schuld, N., McAllister, D., Kalyanaraman, B., Dwinell, M.B., Auchampach, J.A., and Williams, C.L. (2013). An adenosine-mediated signaling pathway suppresses prenylation of the GTPase Rap1B and promotes cell scattering. Sci. Signal. 6, ra39.10.1126/scisignal.2003374 Search in Google Scholar PubMed PubMed Central

Ogawa, M., Miyata, T., Nakajima, K., Yagyu, K., Seike, M., Ikenaka, K., Yamamoto, H., and Mikoshiba, K. (1995). The Reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14, 899–912.10.1016/0896-6273(95)90329-1 Search in Google Scholar PubMed

Ohba, Y., Ikuta, K., Ogura, A., Matsuda, J., Mochizuki, N., Nagashima, K., Kurokawa, K., Mayer, B.J., Maki, K., Miyazaki, J., et al. (2001). Requirement for C3G-dependent Rap1 activation for cell adhesion and embryogenesis. EMBO J. 20, 3333–3341.10.1093/emboj/20.13.3333 Search in Google Scholar PubMed PubMed Central

Ohshima, T., Hirasawa, M., Tabata, H., Mutoh, T., Adachi, T., Suzuki, H., Saruta, K., Iwasato, T., Itohara, S., Hashimoto, M., et al. (2007). Cdk5 is required for multipolar-to-bipolar transition during radial neuronal migration and proper dendrite development of pyramidal neurons in the cerebral cortex. Development 134, 2273–2282.10.1242/dev.02854 Search in Google Scholar PubMed

Oinuma, I., Katoh, H., and Negishi, M. (2004). Molecular dissection of the semaphorin 4D receptor plexin-B1-stimulated R-Ras GTPase-activating protein activity and neurite remodeling in hippocampal neurons. J. Neurosci. 24, 11473–11480.10.1523/JNEUROSCI.3257-04.2004 Search in Google Scholar PubMed PubMed Central

Pak, D.T. and Sheng, M. (2003). Targeted protein degradation and synapse remodeling by an inducible protein kinase. Science 302, 1368–1373.10.1126/science.1082475 Search in Google Scholar PubMed

Pak, D.T., Yang, S., Rudolph-Correia, S., Kim, E., and Sheng, M. (2001). Regulation of dendritic spine morphology by SPAR, a PSD-95-associated RapGAP. Neuron 31, 289–303.10.1016/S0896-6273(01)00355-5 Search in Google Scholar

Pan, B.X., Vautier, F., Ito, W., Bolshakov, V.Y., and Morozov, A. (2008). Enhanced cortico-amygdala efficacy and suppressed fear in absence of Rap1. J. Neurosci. 28, 2089–2098.10.1523/JNEUROSCI.5156-07.2008 Search in Google Scholar PubMed PubMed Central

Paridaen, J.T. and Huttner, W.B. (2014). Neurogenesis during development of the vertebrate central nervous system. EMBO Rep. 15, 351–364.10.1002/embr.201438447 Search in Google Scholar PubMed PubMed Central

Park, T.J. and Curran, T. (2008). Crk and Crk-like play essential overlapping roles downstream of disabled-1 in the Reelin pathway. J. Neurosci. 28, 13551–13562.10.1523/JNEUROSCI.4323-08.2008 Search in Google Scholar PubMed PubMed Central

Pascoe, H.G., Wang, Y., and Zhang, X. (2015). Structural mechanisms of plexin signaling. Prog. Biophys. Mol. Biol. 118, 161–168.10.1016/j.pbiomolbio.2015.03.006 Search in Google Scholar PubMed PubMed Central

Pellis-van Berkel, W., Verheijen, M.H., Cuppen, E., Asahina, M., de Rooij, J., Jansen, G., Plasterk, R.H., Bos, J.L., and Zwartkruis, F.J. (2005). Requirement of the Caenorhabditis elegans RapGEF pxf-1 and rap-1 for epithelial integrity. Mol. Biol. Cell 16, 106–116.10.1091/mbc.e04-06-0492 Search in Google Scholar PubMed PubMed Central

Pena, V., Hothorn, M., Eberth, A., Kaschau, N., Parret, A., Gremer, L., Bonneau, F., Ahmadian, M.R., and Scheffzek, K. (2008). The C2 domain of SynGAP is essential for stimulation of the Rap GTPase reaction. EMBO Rep. 9, 350–355.10.1038/embor.2008.20 Search in Google Scholar PubMed PubMed Central

Pizon, V., Desjardins, M., Bucci, C., Parton, R.G., and Zerial, M. (1994). Association of Rap1a and Rap1b proteins with late endocytic/phagocytic compartments and Rap2a with the Golgi complex. J. Cell Sci. 107, 1661–1670.10.1242/jcs.107.6.1661 Search in Google Scholar PubMed

Polakis, P.G., Rubinfeld, B., Evans, T., and McCormick, F. (1991). Purification of a plasma membrane-associated GTPase-activating protein specific for rap1/Krev-1 from HL60 cells. Proc. Natl. Acad. Sci. USA 88, 239–243.10.1073/pnas.88.1.239 Search in Google Scholar PubMed PubMed Central

Qiao, S. and Homayouni, R. (2015). Dab2IP regulates neuronal positioning, Rap1 activity and integrin signaling in the developing cortex. Dev. Neurosci. 37, 131–141.10.1159/000369092 Search in Google Scholar PubMed PubMed Central

Qiao, S., Kim, S.H., Heck, D., Goldowitz, D., LeDoux, M.S., and Homayouni, R. (2013). Dab2IP GTPase activating protein regulates dendrite development and synapse number in cerebellum. PLoS One 8, e53635.10.1371/journal.pone.0053635 Search in Google Scholar PubMed PubMed Central

Radha, V., Rajanna, A., and Swarup, G. (2004). Phosphorylated guanine nucleotide exchange factor C3G, induced by pervanadate and Src family kinases localizes to the Golgi and subcortical actin cytoskeleton. BMC Cell Biol. 5, 31.10.1186/1471-2121-5-31 Search in Google Scholar PubMed PubMed Central

Radha, V., Mitra, A., Dayma, K., and Sasikumar, K. (2011). Signalling to actin: role of C3G, a multitasking guanine-nucleotide-exchange factor. Biosci. Rep. 31, 231–244.10.1042/BSR20100094 Search in Google Scholar PubMed

Rebhun, J.F., Castro, A.F., and Quilliam, L.A. (2000). Identification of guanine nucleotide exchange factors (GEFs) for the Rap1 GTPase. Regulation of MR-GEF by M-Ras-GTP interaction. J. Biol. Chem. 275, 34901–34908.10.1074/jbc.M005327200 Search in Google Scholar PubMed

Rehmann, H., Das, J., Knipscheer, P., Wittinghofer, A., and Bos, J.L. (2006). Structure of the cyclic-AMP-responsive exchange factor Epac2 in its auto-inhibited state. Nature 439, 625–628.10.1038/nature04468 Search in Google Scholar PubMed

Reuther, G.W., Lambert, Q.T., Rebhun, J.F., Caligiuri, M.A., Quilliam, L.A., and Der, C.J. (2002). RasGRP4 is a novel Ras activator isolated from acute myeloid leukemia. J. Biol. Chem. 277, 30508–30514.10.1074/jbc.M111330200 Search in Google Scholar PubMed

Richter, M., Murai, K.K., Bourgin, C., Pak, D.T., and Pasquale, E.B. (2007). The EphA4 receptor regulates neuronal morphology through SPAR-mediated inactivation of Rap GTPases. J. Neurosci. 27, 14205–14215.10.1523/JNEUROSCI.2746-07.2007 Search in Google Scholar PubMed PubMed Central

Rohm, B., Rahim, B., Kleiber, B., Hovatta, I., and Püschel, A.W. (2000). The semaphorin 3A receptor may directly regulate the activity of small GTPases. FEBS Lett. 486, 68–72.10.1016/S0014-5793(00)02240-7 Search in Google Scholar PubMed

Roy, B.C., Kohu, K., Matsuura, K., Yanai, H., and Akiyama, T. (2002). SPAL, a Rap-specific GTPase activating protein, is present in the NMDA receptor-PSD-95 complex in the hippocampus. Genes Cells 7, 607–617.10.1046/j.1365-2443.2002.00546.x Search in Google Scholar PubMed

Saito, Y., Oinuma, I., Fujimoto, S., and Negishi, M. (2009). Plexin-B1 is a GTPase activating protein for M-Ras, remodelling dendrite morphology. EMBO Rep. 10, 614–621.10.1038/embor.2009.63 Search in Google Scholar PubMed PubMed Central

Sawada, Y., Tamada, M., Dubin-Thaler, B.J., Cherniavskaya, O., Sakai, R., Tanaka, S., and Sheetz, M.P. (2006). Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127, 1015–1026.10.1016/j.cell.2006.09.044 Search in Google Scholar PubMed PubMed Central

Schmeisser, M.J., Grabrucker, A.M., Bockmann, J., and Boeckers, T.M. (2009). Synaptic cross-talk between N-methyl-D-aspartate receptors and LAPSER1-β-catenin at excitatory synapses. J. Biol. Chem. 284, 29146–29157.10.1074/jbc.M109.020628 Search in Google Scholar PubMed PubMed Central

Schmid, M.T., Weinandy, F., Wilsch-Brauninger, M., Huttner, W.B., Cappello, S., and Gotz, M. (2014). The role of α-E-catenin in cerebral cortex development: radial glia specific effect on neuronal migration. Front. Cell. Neurosci. 8, 215.10.3389/fncel.2014.00215 Search in Google Scholar PubMed PubMed Central

Schuld, N.J., Vervacke, J.S., Lorimer, E.L., Simon, N.C., Hauser, A.D., Barbieri, J.T., Distefano, M.D., and Williams, C.L. (2014). The chaperone protein SmgGDS interacts with small GTPases entering the prenylation pathway by recognizing the last amino acid in the CAAX motif. J. Biol. Chem. 289, 6862–6876.10.1074/jbc.M113.527192 Search in Google Scholar PubMed PubMed Central

Schultess, J., Danielewski, O., and Smolenski, A.P. (2005). Rap1GAP2 is a new GTPase-activating protein of Rap1 expressed in human platelets. Blood 105, 3185–3192.10.1182/blood-2004-09-3605 Search in Google Scholar PubMed

Schwamborn, J.C. and Püschel, A.W. (2004). The sequential activity of the GTPases Rap1B and Cdc42 determines neuronal polarity. Nat. Neurosci. 7, 923–929.10.1038/nn1295 Search in Google Scholar PubMed

Scrima, A., Thomas, C., Deaconescu, D., and Wittinghofer, A. (2008). The Rap-RapGAP complex: GTP hydrolysis without catalytic glutamine and arginine residues. EMBO J. 27, 1145–1153.10.1038/emboj.2008.30 Search in Google Scholar PubMed PubMed Central

Seeburg, D.P., Feliu-Mojer, M., Gaiottino, J., Pak, D.T., and Sheng, M. (2008). Critical role of CDK5 and Polo-like kinase 2 in homeostatic synaptic plasticity during elevated activity. Neuron 58, 571–583.10.1016/j.neuron.2008.03.021 Search in Google Scholar PubMed PubMed Central

Sekine, K., Kawauchi, T., Kubo, K., Honda, T., Herz, J., Hattori, M., Kinashi, T., and Nakajima, K. (2012). Reelin controls neuronal positioning by promoting cell-matrix adhesion via inside-out activation of integrin α5β1. Neuron 76, 353–369.10.1016/j.neuron.2012.07.020 Search in Google Scholar PubMed PubMed Central

Shah, B., Lutter, D., Bochenek, M.L., Kato, K., Tsytsyura, Y., Glyvuk, N., Sakakibara, A., Klingauf, J., Adams, R.H., and Puschel, A.W. (2016a). C3G/Rapgef1 is required in multipolar neurons for the transition to a bipolar morphology during cortical development. PLoS One 11, e0154174.10.1371/journal.pone.0154174 Search in Google Scholar PubMed PubMed Central

Shah, B., Lutter, D., Tsytsyura, Y., Glyvuk, N., Sakakibara, A., Klingauf, J., and Püschel, A.W. (2016b). Rap1 GTPases are master regulators of neural cell polarity in the developing neocortex. Cereb. Cortex. pii: bhv341. [Epub ahead of print].10.1093/cercor/bhv341 Search in Google Scholar PubMed

Sot, B., Behrmann, E., Raunser, S., and Wittinghofer, A. (2013). Ras GTPase activating (RasGAP) activity of the dual specificity GAP protein Rasal requires colocalization and C2 domain binding to lipid membranes. Proc. Natl. Acad. Sci. USA 110, 111–116.10.1073/pnas.1201658110 Search in Google Scholar PubMed PubMed Central

Spilker, C. and Kreutz, M.R. (2010). RapGAPs in brain: multipurpose players in neuronal Rap signalling. Eur. J. Neurosci. 32, 1–9.10.1111/j.1460-9568.2010.07273.x Search in Google Scholar PubMed

Spilker, C., Acuna Sanhueza, G.A., Bockers, T.M., Kreutz, M.R., and Gundelfinger, E.D. (2008). SPAR2, a novel SPAR-related protein with GAP activity for Rap1 and Rap2. J. Neurochem. 104, 187–201.10.1111/j.1471-4159.2007.04991.x Search in Google Scholar PubMed

Stornetta, R.L. and Zhu, J.J. (2011). Ras and Rap signaling in synaptic plasticity and mental disorders. Neuroscientist 17, 54–78.10.1177/1073858410365562 Search in Google Scholar PubMed PubMed Central

Takahashi, M., Dillon, T.J., Liu, C., Kariya, Y., Wang, Z., and Stork, P.J. (2013). Protein kinase A-dependent phosphorylation of Rap1 regulates its membrane localization and cell migration. J. Biol. Chem. 288, 27712–27723.10.1074/jbc.M113.466904 Search in Google Scholar PubMed PubMed Central

Tamada, M., Sheetz, M.P., and Sawada, Y. (2004). Activation of a signaling cascade by cytoskeleton stretch. Dev. Cell 7, 709–718.10.1016/j.devcel.2004.08.021 Search in Google Scholar PubMed

Tissir, F. and Goffinet, A.M. (2003). Reelin and brain development. Nat. Rev. Neurosci. 4, 496–505.10.1038/nrn1113 Search in Google Scholar PubMed

Toki, S., Kawasaki, H., Tashiro, N., Housman, D.E., and Graybiel, A.M. (2001). Guanine nucleotide exchange factors CalDAG-GEFI and CalDAG-GEFII are colocalized in striatal projection neurons. J. Comp. Neurol. 437, 398–407.10.1002/cne.1291 Search in Google Scholar PubMed

Tomoda, T., Kim, J.H., Zhan, C., and Hatten, M.E. (2004). Role of Unc51.1 and its binding partners in CNS axon outgrowth. Genes Dev. 18, 541–558.10.1101/gad.1151204 Search in Google Scholar PubMed PubMed Central

Tran, T.S., Kolodkin, A.L., and Bharadwaj, R. (2007). Semaphorin regulation of cellular morphology. Annu. Rev. Cell. Dev. Biol. 23, 263–292.10.1146/annurev.cellbio.22.010605.093554 Search in Google Scholar PubMed

Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J., Hammer, R., Richardson, J., and Herz, J. (1999). Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97, 689–701.10.1016/S0092-8674(00)80782-5 Search in Google Scholar

Uechi, Y., Bayarjargal, M., Umikawa, M., Oshiro, M., Takei, K., Yamashiro, Y., Asato, T., Endo, S., Misaki, R., Taguchi, T., et al. (2009). Rap2 function requires palmitoylation and recycling endosome localization. Biochem. Biophys. Res. Commun. 378, 732–737.10.1016/j.bbrc.2008.11.107 Search in Google Scholar PubMed

Uesugi, K., Oinuma, I., Katoh, H., and Negishi, M. (2009). Different requirement for Rnd GTPases of R-Ras GAP activity of Plexin-C1 and Plexin-D1. J. Biol. Chem. 284, 6743–6751.10.1074/jbc.M805213200 Search in Google Scholar PubMed PubMed Central

van den Berghe, N., Cool, R.H., Horn, G., and Wittinghofer, A. (1997). Biochemical characterization of C3G: an exchange factor that discriminates between Rap1 and Rap2 and is not inhibited by Rap1A(S17N). Oncogene 15, 845–850.10.1038/sj.onc.1201407 Search in Google Scholar PubMed

Vazquez, L.E., Chen, H.J., Sokolova, I., Knuesel, I., and Kennedy, M.B. (2004). SynGAP regulates spine formation. J. Neurosci. 24, 8862–8872.10.1523/JNEUROSCI.3213-04.2004 Search in Google Scholar PubMed PubMed Central

Voss, A.K., Gruss, P., and Thomas, T. (2003). The guanine nucleotide exchange factor C3G is necessary for the formation of focal adhesions and vascular maturation. Development 130, 355–367.10.1242/dev.00217 Search in Google Scholar PubMed

Voss, A.K., Britto, J.M., Dixon, M.P., Sheikh, B.N., Collin, C., Tan, S.S., and Thomas, T. (2008). C3G regulates cortical neuron migration, preplate splitting and radial glial cell attachment. Development 135, 2139–2149.10.1242/dev.016725 Search in Google Scholar PubMed

Walkup, W.G.t., Washburn, L., Sweredoski, M.J., Carlisle, H.J., Graham, R.L., Hess, S., and Kennedy, M.B. (2015). Phosphorylation of synaptic GTPase-activating protein (synGAP) by Ca2+/calmodulin-dependent protein kinase II (CaMKII) and cyclin-dependent kinase 5 (CDK5) alters the ratio of its GAP activity toward Ras and Rap GTPases. J. Biol. Chem. 290, 4908–4927.10.1074/jbc.M114.614420 Search in Google Scholar PubMed PubMed Central

Wang, Z., Tseng, C.P., Pong, R.C., Chen, H., McConnell, J.D., Navone, N., and Hsieh, J.T. (2002). The mechanism of growth-inhibitory effect of DOC-2/DAB2 in prostate cancer. Characterization of a novel GTPase-activating protein associated with N-terminal domain of DOC-2/DAB2. J. Biol. Chem. 277, 12622–12631.10.1074/jbc.M110568200 Search in Google Scholar PubMed

Wang, H., Singh, S.R., Zheng, Z., Oh, S.W., Chen, X., Edwards, K., and Hou, S.X. (2006). Rap-GEF signaling controls stem cell anchoring to their niche through regulating DE-cadherin-mediated cell adhesion in the Drosophila testis. Dev. Cell 10, 117–126.10.1016/j.devcel.2005.11.004 Search in Google Scholar PubMed

Wang, Y., He, H., Srivastava, N., Vikarunnessa, S., Chen, Y.B., Jiang, J., Cowan, C.W., and Zhang, X. (2012). Plexins are GTPase-activating proteins for Rap and are activated by induced dimerization. Sci. Signal. 5, ra6.10.1126/scisignal.2002636 Search in Google Scholar PubMed PubMed Central

Wang, Y., Pascoe, H.G., Brautigam, C.A., He, H., and Zhang, X. (2013). Structural basis for activation and non-canonical catalysis of the Rap GTPase activating protein domain of plexin. eLife 2, e01279.10.7554/eLife.01279.020 Search in Google Scholar

Wei, P., Satoh, T., Edamatsu, H., Aiba, A., Setsu, T., Terashima, T., Kitazawa, S., Nakao, K., Yoshikawa, Y., Tamada, M., et al. (2007). Defective vascular morphogenesis and mid-gestation embryonic death in mice lacking RA-GEF-1. Biochem. Biophys. Res. Commun. 363, 106–112.10.1016/j.bbrc.2007.08.149 Search in Google Scholar PubMed

Wendholt, D., Spilker, C., Schmitt, A., Dolnik, A., Smalla, K.H., Proepper, C., Bockmann, J., Sobue, K., Gundelfinger, E.D., Kreutz, M.R., et al. (2006). ProSAP-interacting protein 1 (ProSAPiP1), a novel protein of the postsynaptic density that links the spine-associated Rap-Gap (SPAR) to the scaffolding protein ProSAP2/Shank3. J. Biol. Chem. 281, 13805–13816.10.1074/jbc.M601101200 Search in Google Scholar PubMed

Woolfrey, K.M., Srivastava, D.P., Photowala, H., Yamashita, M., Barbolina, M.V., Cahill, M.E., Xie, Z., Jones, K.A., Quilliam, L.A., Prakriya, M., et al. (2009). Epac2 induces synapse remodeling and depression and its disease-associated forms alter spines. Nat. Neurosci. 12, 1275–1284.10.1038/nn.2386 Search in Google Scholar PubMed PubMed Central

Worzfeld, T. and Offermanns, S. (2014). Semaphorins and plexins as therapeutic targets. Nat. Rev. Drug Discov. 13, 603–621.10.1038/nrd4337 Search in Google Scholar PubMed

Wu, D., Tadano, M., Edamatsu, H., Masago-Toda, M., Yamawaki-Kataoka, Y., Terashima, T., Mizoguchi, A., Minami, Y., Satoh, T., and Kataoka, T. (2003). Neuronal lineage-specific induction of phospholipase Cepsilon expression in the developing mouse brain. Eur. J. Neurosci. 17, 1571–1580.10.1046/j.1460-9568.2003.02591.x Search in Google Scholar PubMed

Xie, Z., Huganir, R.L., and Penzes, P. (2005). Activity-dependent dendritic spine structural plasticity is regulated by small GTPase Rap1 and its target AF-6. Neuron 48, 605–618.10.1016/j.neuron.2005.09.027 Search in Google Scholar PubMed

Yaman, E., Gasper, R., Koerner, C., Wittinghofer, A., and Tazebay, U.H. (2009). RasGEF1A and RasGEF1B are guanine nucleotide exchange factors that discriminate between Rap GTP-binding proteins and mediate Rap2-specific nucleotide exchange. FEBS J. 276, 4607–4616.10.1111/j.1742-4658.2009.07166.x Search in Google Scholar PubMed

Yang, Y., Shu, X., Liu, D., Shang, Y., Wu, Y., Pei, L., Xu, X., Tian, Q., Zhang, J., Qian, K., et al. (2012). EPAC null mutation impairs learning and social interactions via aberrant regulation of miR-124 and Zif268 translation. Neuron 73, 774–788.10.1016/j.neuron.2012.02.003 Search in Google Scholar PubMed PubMed Central

Ye, T., Ip, J.P., Fu, A.K., and Ip, N.Y. (2014). Cdk5-mediated phosphorylation of RapGEF2 controls neuronal migration in the developing cerebral cortex. Nat. Commun. 5, 4826.10.1038/ncomms5826 Search in Google Scholar PubMed PubMed Central

Zanata, S.M., Hovatta, I., Rohm, B., and Püschel, A.W. (2002). Antagonistic effects of Rnd1 and RhoD GTPases regulate receptor activity in Semaphorin 3A-induced cytoskeletal collapse. J. Neurosci. 22, 471–477.10.1523/JNEUROSCI.22-02-00471.2002 Search in Google Scholar PubMed PubMed Central

Zhu, J.J., Qin, Y., Zhao, M., Van Aelst, L., and Malinow, R. (2002). Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell 110, 443–455.10.1016/S0092-8674(02)00897-8 Search in Google Scholar PubMed

Zhu, Y., Pak, D., Qin, Y., McCormack, S.G., Kim, M.J., Baumgart, J.P., Velamoor, V., Auberson, Y.P., Osten, P., van Aelst, L., et al. (2005). Rap2-JNK removes synaptic AMPA receptors during depotentiation. Neuron 46, 905–916.10.1016/j.neuron.2005.04.037 Search in Google Scholar PubMed

Zhu, M., Fuller, D.M., and Zhang, W. (2012). The role of Ras guanine nucleotide releasing protein 4 in Fc epsilonRI-mediated signaling, mast cell function, and T cell development. J. Biol. Chem. 287, 8135–8143.10.1074/jbc.M111.320580 Search in Google Scholar PubMed PubMed Central

Zhu, J., Shang, Y., and Zhang, M. (2016). Mechanistic basis of MAGUK-organized complexes in synaptic development and signalling. Nat. Rev. Neurosci. 17, 209–223.10.1038/nrn.2016.18 Search in Google Scholar PubMed

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