Abstract
It is well known that synaptic plasticity is the cellular mechanism underlying learning and memory. Activity-dependent synaptic changes in electrical properties and morphology, including synaptogenesis, lead to alterations of synaptic strength, which is associated with long-term potentiation (LTP). Brain-derived neurotrophic factor (BDNF)/tropomyosin-related kinase B (TrkB) signaling is involved in learning and memory formation by regulating synaptic plasticity. The phosphatidylinositol 3-kinase (PI3-K)/Akt pathway is one of the key signaling cascades downstream BDNF/TrkB and is believed to modulate N-methyl-d-aspartate (NMDA) receptor-mediated synaptic plasticity. However, the molecular mechanism underlying the connection between these two key players in synaptic plasticity remains largely unknown. Girders of actin filament (Girdin), an Akt substrate that directly binds to actin filaments, has been shown to play a role in neuronal migration and neuronal development. Recently, we identified Girdin as a key molecule involved in regulating long-term memory. It was demonstrated that phosphorylation of Girdin by Akt contributed to the maintenance of LTP by linking the BDNF/TrkB signaling pathway with NMDA receptor activity. These findings indicate that Girdin plays a pivotal role in a variety of processes in the CNS. Here, we review recent advances in our understanding about the roles of Girdin in the CNS and focus particularly on neuronal migration and memory.
Acknowledgments
This study was supported, in part, by the following funding sources: Grants-in-aid for Scientific Research (no. 15H01284, 26293053, 26670121) from the Japan Society for the Promotion of Science; ‘Integrated Research on Neuropsychiatric Disorders’ carried out under the SRPBS from MEXT; and a grant from the Smoking Research Foundation, Japan. Ministry of Education, Culture, Sports, Science, and Technology.
Conflict of interest statement: The authors declare no competing financial interests.
References
Alonso, M., Vianna, M.R., Depino, A.M., Mello e Souza, T., Pereira, P., Szapiro, G., Viola, H., Pitossi, F., Izquierdo, I., and Medina, J.H. (2002). BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation. Hippocampus 12, 551–560.10.1002/hipo.10035Search in Google Scholar PubMed
Asai, M., Asai, N., Murata, A., Yokota, H., Ohmori, K., Mii, S., Enomoto, A., Murakumo, Y., and Takahashi, M. (2012). Similar phenotypes of Girdin germ-line and conditional knockout mice indicate a crucial role for Girdin in the nestin lineage. Biochem. Biophys. Res. Commun. 426, 533–538.10.1016/j.bbrc.2012.08.122Search in Google Scholar PubMed
Atkins, C.M., Selcher, J.C., Petraitis, J.J., Trzaskos, J.M., and Sweatt, J.D. (1998). The MAPK cascade is required for mammalian associative learning. Nat. Neurosci. 1, 602–609.10.1038/2836Search in Google Scholar PubMed
Balu, D.T., Carlson, G.C., Talbot, K., Kazi, H., Hill-Smith, T.E., Easton, R.M., Birnbaum, M.J., and Lucki, I. (2012). Akt1 deficiency in schizophrenia and impairment of hippocampal plasticity and function. Hippocampus 22, 230–240.10.1002/hipo.20887Search in Google Scholar PubMed PubMed Central
Barria, A., Derkach, V., and Soderling, T. (1997). Identification of the Ca2+/calmodulin-dependent protein kinase II regulatory phosphorylation site in the α-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate-type glutamate receptor. J. Biol. Chem. 272, 32727–32730.10.1074/jbc.272.52.32727Search in Google Scholar PubMed
Bhandari, D., Lopez-Sanchez, I., To, A., Lo, I.C., Aznar, N., Leyme, A., Gupta, V., Niesman, I., Maddox, A.L., Garcia-Marcos, M., et al. (2015). Cyclin-dependent kinase 5 activates guanine nucleotide exchange factor GIV/Girdin to orchestrate migration-proliferation dichotomy. Proc. Natl. Acad. Sci. USA 112, E4874–E4883.10.1073/pnas.1514157112Search in Google Scholar PubMed PubMed Central
Bliss, T.V. and Lomo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of perforant path. J. Physiol. (Lond.) 232, 331–356.10.1113/jphysiol.1973.sp010273Search in Google Scholar PubMed PubMed Central
Blum, S., Moore, A.N., Adams, F., and Dash, P.K. (1999). A mitogen-activated protein kinase cascade in the CA1/CA2 subfield of the dorsal hippocampus is essential for long-term spatial memory. J. Neurosci. 19, 3535–3544.10.1523/JNEUROSCI.19-09-03535.1999Search in Google Scholar
Brambilla, R., Gnesutta, N., Minichiello, L., White, G., Roylance, A.J., Herron, C.E., Ramsey, M., Wolfer, D.P., Cestari, V., Rossi-Arnaud, C., et al. (1997). A role for the Ras signaling pathway in synaptic transmission and long-term memory. Nature 390, 281–286.10.1038/36849Search in Google Scholar PubMed
Burnouf, S., Martire, A., Derisbourg, M., Laurent, C., Belarbi, K., Leboucher, A., Fernandez-Gomez, F.J., Troquier, L., Eddarkaoui, S., Grosjean, M.E., et al. (2013). NMDA receptor dysfunction contributes to impaired brain-derived neurotrophic factor-induced facilitation of hippocampal synaptic transmission in a Tau transgenic model. Aging Cell 12, 11–23.10.1111/acel.12018Search in Google Scholar PubMed
Connor, B., Young, D., Yan, Q., Faull, R.L., Synek, B., and Dragunow, M. (1997). Brain-derived neurotrophic factor is reduced in Alzheimer’s disease. Brain Res. Mol. Brain Res. 49, 71–81.10.1016/S0169-328X(97)00125-3Search in Google Scholar
Cuesto, G., Enriquez-Barreto, L., Caramés, C., Cantarero, M., Gasull, X., Sandi, C., Ferrús, A., Acebes, Á., and Morales, M. (2011). Phosphoinositide-3-kinase activation controls synaptogenesis and spinogenesis in hippocampal neurons. J. Neurosci. 31, 2721–2733.10.1523/JNEUROSCI.4477-10.2011Search in Google Scholar PubMed PubMed Central
Dahl, J.P., Wang-Dunlop, J., Gonzales, C., Goad, M.E., Mark, R.J., and Kwak, S.P. (2003). Characterization of the WAVE1 knock-out mouse: implications for CNS development. J. Neurosci. 23, 3343–3352.10.1523/JNEUROSCI.23-08-03343.2003Search in Google Scholar
Derkach, V.A., Oh, M.C., Guire, E.S., and Soderling, T.R. (2007). Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat. Rev. Neurosci. 8, 101–113.10.1038/nrn2055Search in Google Scholar PubMed
Dillon, C. and Goda, Y. (2005). The actin cytoskeleton: integrating form and function at the synapse. Annu. Rev. Neurosci. 28, 25–55.10.1146/annurev.neuro.28.061604.135757Search in Google Scholar PubMed
Duguid, I. and Sjöström, P.J. (2006). Novel presynaptic mechanisms for coincidence detection in synaptic plasticity. Curr. Opin. Neurobiol. 16, 312–322.10.1016/j.conb.2006.05.008Search in Google Scholar PubMed
English, J.D. and Sweatt, J.D. (1996). Activation of p42 mitogen-activated protein kinase in hippocampal long term potentiation. J. Biol. Chem. 271, 24329–24332.10.1074/jbc.271.40.24329Search in Google Scholar PubMed
English, J.D. and Sweatt, J.D. (1997). A requirement for the mitogen-activated protein kinase cascade in hippocampal long term potentiation. J. Biol. Chem. 272, 19103–19106.10.1074/jbc.272.31.19103Search in Google Scholar PubMed
Enomoto, A., Murakami, H., Asai, N., Morone, N., Watanabe, T., Kawai, K., Murakumo, Y., Usukura, J., Kaibuchi, K., and Takahashi, M. (2005). Akt/PKB regulates actin organization and cell motility via Girdin/APE. Dev. Cell 9, 389–402.10.1016/j.devcel.2005.08.001Search in Google Scholar PubMed
Enomoto, A., Asai, N., Namba, T., Wang, Y., Kato, T., Tanaka, M., Tatsumi, H., Taya, S., Tsuboi, D., Kuroda, K., et al. (2009). Roles of disrupted-in-schizophrenia 1-interacting protein Girdin in postnatal development of the dentate gyrus. Neuron 63, 774–787.10.1016/j.neuron.2009.08.015Search in Google Scholar PubMed
Gao, C., Frausto, S.F., Guedea, A.L., Tronson, N.C., Jovasevic, V., Leaderbrand, K., Corcoran, K.A., Guzmán, Y.F., Swanson, G.T., and Radulovic, J. (2011). IQGAP1 regulates NR2A signaling, spine density, and cognitive processes. J. Neurosci. 31, 8533–8542.10.1523/JNEUROSCI.1300-11.2011Search in Google Scholar
Garcia-Marcos, M., Ghosh, P., and Farquhar, M.G. (2009). GIV is a nonreceptor GEF for G alpha I with a unique motif that regulates Akt signaling. Proc. Natl. Acad. Sci. USA 106, 3178–3183.10.1073/pnas.0900294106Search in Google Scholar
Ghosh, P., Garcia-Marcos, M., Bornheimer, S.J., and Farquhar, M.G. (2008). Activation of Gαi3 triggers cell migration via regulation of GIV. J. Cell. Biol. 182, 381–393.10.1083/jcb.200712066Search in Google Scholar
Hayashi, Y., Shi, S.H., Esteban, J.A., Piccini, A., Poncer, J.C., and Malinow, R. (2000). Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262–2267.10.1126/science.287.5461.2262Search in Google Scholar
Hering, H. and Sheng, M. (2003). Activity-dependent redistribution and essential role of cortactin in dendritic spine morphogenesis. J. Neurosci. 23, 11759–11769.10.1523/JNEUROSCI.23-37-11759.2003Search in Google Scholar
Horwood, J.M., Dufour, F., Laroche, S., and Davis, S. (2006). Signaling mechanisms mediated by the phosphoinositide 3-kinase/Akt cascade in synaptic plasticity and memory in the rat. Eur. J. Neurosci. 23, 3375–3384.10.1111/j.1460-9568.2006.04859.xSearch in Google Scholar
Ito, T., Komeima, K., Yasuma, T., Enomoto, A., Asai, N., Asai, M., Iwase, S., Takahashi, M., and Terasaki, H. (2013). Girdin and its phosphorylation dynamically regulate neonatal vascular development and pathological neovascularization in the retina. Am. J. Pathol. 182, 586–596.10.1016/j.ajpath.2012.10.012Search in Google Scholar
Jiang, P., Enomoto, A., Jijiwa, M., Kato, T., Hasegawa, T., Ishida, M., Sato, T., Asai, N., Murakumo, Y., and Takahashi, M. (2008). An actin-binding protein Girdin regulates the motility of breast cancer cells. Cancer Res. 68, 1310–1318.10.1158/0008-5472.CAN-07-5111Search in Google Scholar
Karege, F., Perret, G., Bondolfi, G., Schwald, M., Bertschy, G., and Aubry, J.M. (2002). Decreased serum brain-derived neurotrophic factor level in major depressed patients. Psychiatry Res. 109, 143–148.10.1016/S0165-1781(02)00005-7Search in Google Scholar
Kelleher, R.J. 3rd, Govindarajan, A., Jung, H.Y., Kang, H., and Tonegawa, S. (2004). Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116, 467–479.10.1016/S0092-8674(04)00115-1Search in Google Scholar
Kim, Y., Sung, J.Y., Ceglia, I., Lee, K.W., Ahn, J.H., Halford, J.M., Kim, A.M., Kwak, S.P., Park, J.B., Ho Ryu, S., et al. (2006). Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature 442, 814–817.10.1038/nature04976Search in Google Scholar
Kim, I.H., Racz, B., Wang, H., Burianek, L., Weinberg, R., Yasuda, R., Wetsel, W.C., and Soderling, S.H. (2013). Disruption of Arp2/3 results in asymmetric structural plasticity of dendritic spine and progressive synaptic and behavioral abnormalities. J. Neurosci. 33, 6081–6092.10.1523/JNEUROSCI.0035-13.2013Search in Google Scholar
Kitamura, T., Asai, N., Enomoto, A., Maeda, K., Kato, T., Ishida, M., Jiang, P., Watanabe, T., Usukura, J., and Kondo, T. (2008). Regulation of VEGF-mediated angiogenesis by the Akt/PKB substrate Girdin. Nat. Cell Biol. 10, 329–337.10.1038/ncb1695Search in Google Scholar
Lavezzari, G., McCallum, J., Lee, R., and Roche, K.W. (2003). Differential binding of the AP-2 adaptor complex and PSD-95 to the C-terminus of the NMDA receptor subunit NR2B regulates surface expression. Neuropharmacology 45, 729–737.10.1016/S0028-3908(03)00308-3Search in Google Scholar
Lee, H.Y., Takamiya, K., Han, J.S., Man, H., Kim, C.H., Rumbaugh, G., Yu, S., Ding, L., He, C., Petralia, R.S., et al. (2003). Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112, 631–643.10.1016/S0092-8674(03)00122-3Search in Google Scholar
Lein, E.S., Hawrylycz, M.J., Ao, N., Ayres, M., Bensinger, A., Bernard, A., Boe, A.F., Boguski, M.S., Brockway, K.S., and Byrnes, E.J. (2007). Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168–176.10.1038/nature05453Search in Google Scholar
Le-Niculescu, H., Niesman, I., Fischer, T., DeVries, L., and Farquhar, M.G. (2005). Identification and characterization of GIV, a novel Galpha i/s-interacting protein found on COPI, endoplasmic reticulum-Golgi transport vesicles. J. Biol. Chem. 280, 22012–22020.10.1074/jbc.M501833200Search in Google Scholar
Lin, S.Y., Wu, K., Levine, E.S., Mount, H.T., Suen, P.C., and Black, I.B. (1998). BDNF acutely increases tyrosine phosphorylation of the NMDA receptor subunit 2B in cortical and hippocampal postsynaptic densities. Brain Res. Mol. Brain Res. 55, 20–27.10.1016/S0169-328X(97)00349-5Search in Google Scholar
Lin, C., Ear, J., Pavlova, Y., Mittal, Y., Kufareva, I., Ghassemian, M., Abagyan, R., Garcia-Marcos, M., and Ghosh, P. (2011). Tyrosine phosphorylation of the Galpha-interacting protein GIV promotes activation of phosphoinositide 3-kinase during cell migration. Sci. Signal. 4, ra64.10.1126/scisignal.2002049Search in Google Scholar PubMed PubMed Central
Linnarsson, S., Björklund, A., and Ernfors, P. (1997). Learning deficit in BDNF mutant mice. Eur. J. Neurosci. 9, 2581–2587.10.1111/j.1460-9568.1997.tb01687.xSearch in Google Scholar PubMed
Lopez-Sanchez, I., Kalogriopoulos, N., Lo, I.C., Kabir, F., Midde, K., Wang, H., and Ghosh, P. (2015). Focal adhesions are foci for tyrosine-based signal transduction via GIV/Girdin and G proteins. Mol. Biol. Cell. 26, 4313–4324.10.1091/mbc.E15-07-0496Search in Google Scholar
Lu, Y.M., Roder, J.C., Davidow, J., and Salter, M.W. (1998). Src activation in the induction of long-term potentiation in CA1 hippocampal neurons. Science 279, 1363–1367.10.1126/science.279.5355.1363Search in Google Scholar
Mammen, A.L., Kameyama, K., Roche, K.W., and Huganir, R.L. (1997). Phosphorylation of the alpha-amino-3-hydroxy- 5-methylisoxazole4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II. J. Biol. Chem. 272, 32528–32533.10.1074/jbc.272.51.32528Search in Google Scholar
Minichiello, L., Korte, M., Wolfer, D., Kühn, R., Unsicker, K., Cestari, V., Rossi-Arnaud, C., Lipp, H.P., Bonhoeffer, T., and Klein, R. (1999). Essential role for TrkB receptors in hippocampus-mediated learning. Neuron 24, 401–414.10.1016/S0896-6273(00)80853-3Search in Google Scholar
Mizuno, M., Yamada, K., Olariu, A., Nawa, H., and Nabeshima, T. (2000). Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J. Neurosci. 20, 7116–7121.10.1523/JNEUROSCI.20-18-07116.2000Search in Google Scholar
Mizuno, M., Yamada, K., Takei, N., Tran, M.H., He, J., Nakajima, A., and Nabeshima, T. (2003a). Phosphatidylinositol 3-kinase: a molecule mediating BDNF-dependent spatial memory formation. Mol. Psychiatry 8, 217–224.10.1038/sj.mp.4001215Search in Google Scholar
Mizuno, M., Yamada, K., He, J., Nakajima, A., and Nabeshima, T. (2003b). Involvement of BDNF receptor TrkB in spatial memory formation. Learn. Mem. 10, 108–115.10.1101/lm.56003Search in Google Scholar
Monyer, H., Brunashev, N., Laurie, D.J., Sakmann, B., and Seeburg, P.H. (1994). Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12, 529–540.10.1016/0896-6273(94)90210-0Search in Google Scholar
Mu, J.S., Li, W.P., Yao, Z.B., and Zhou, X.F. (1999). Deprivation of edogenous brain-derived neurotrophic factor results in impairment of spatial learning and memory in adult rats. Brain Res. 835, 259–265.10.1016/S0006-8993(99)01592-9Search in Google Scholar
Munkholm, K., Vinberg, M., and Kessing, L.V. (2016). Peripheral blood brain-derived neurotrophic factor in bipolar disorder: a comprehensive systematic review and meta-analysis. Mol. Psychiatry. 21, 216–228.10.1038/mp.2015.54Search in Google Scholar PubMed
Murakoshi, H. and Yasuda, R. (2012). Postsynaptic signaling during plasticity of dendritic spine. Trends Neurosci. 35, 135–143.10.1016/j.tins.2011.12.002Search in Google Scholar
Muramatsu, A., Enomoto, A., Kato, T., Weng, L., Kuroda, K., Asai, N., Asai, M., Mii, S., and Takahashi, M. (2015). Potential involvement of kinesin-1 in the regulation of subcellular localization of Girdin. Biochem. Biophys. Res. Commun. 463, 999–1005.10.1016/j.bbrc.2015.06.049Search in Google Scholar
Nakai, T., Nagai, T., Tanaka, M., Itoh, N., Asai, N., Enomoto, A., Asai, M., Yamada, S., Saifullah, A.B., Sokabe, M., et al. (2014). Girdin phosphorylation is crucial for synaptic plasticity and memory: a potential role in the interaction of BDNF/TrkB/Akt signaling with NMDA receptor. J. Neurosci. 34, 14995–15008.10.1523/JNEUROSCI.2228-14.2014Search in Google Scholar
Nakazawa, T., Komai, S., Watabe, A.M., Kiyama, Y., Fukaya, M., Arima-Yoshida, F., Horai, R., Sudo, K., Ebine, K., Delawary, M., et al. (2006). NR2B tyrosine phosphorylation modulates fear learning as well as amygdaloid synaptic plasticity. EMBO J. 25, 2867–2877.10.1038/sj.emboj.7601156Search in Google Scholar
Neves-Pereira, M., Cheung, J.K., Pasdar, A., Zhang, F., Breen, G., Yates, P., Sinclair, M., Crombie, C., Walker, N., and St Clair, D.M. (2005). BDNF gene is a risk factor for schizophrenia in a Scottish population. Mol. Psychiatry 10, 208–212.10.1038/sj.mp.4001575Search in Google Scholar
Ohara, K., Enomoto, A., Kato, T., Hashimoto, T., Isotani-Sakakibara, M., Asai, N., Ishida-Takagishi, M., Weng, L., Nakayama, M., Watanabe, T., et al. (2012). Involvement of Girdin in the determination of cell polarity during cell migration. PLoS One 7, e36681.10.1371/journal.pone.0036681Search in Google Scholar
Patterson, S.L., Abel, T., Deuel, T.A., Martin, K.C., Rose, J.C., and Kandel, E.R. (1996). Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16, 1137–1145.10.1016/S0896-6273(00)80140-3Search in Google Scholar
Pitman, R.M. (1984). The versatile synapse. J. Exp. Biol. 112, 199–224.10.1242/jeb.112.1.199Search in Google Scholar PubMed
Prybylowski, K., Chang, K., Sans, N., Kan, L., Vicini, S., and Wenthold, R.J. (2005). The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2. Neuron 47, 845–857.10.1016/j.neuron.2005.08.016Search in Google Scholar PubMed PubMed Central
Salter, M.W. and Kalia, L.V. (2004). Src kinases: a hub for NMDA receptor regulation. Nat. Rev. Neurosci. 5, 317–328.10.1038/nrn1368Search in Google Scholar PubMed
Sanna, P.P., Cammalleri, M., Berton, F., Simpson, C., Lutjens, R., Bloom, F.E., and Francesconi, W. (2002). 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, 3359–3365.10.1523/JNEUROSCI.22-09-03359.2002Search in Google Scholar
Shi, S., Hayashi, Y., Esteban, J.A., and Malinow, R. (2001). Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105, 331–343.10.1016/S0092-8674(01)00321-XSearch in Google Scholar
Shipton, O.A. and Paulsen, O. (2013). GluN2A and GluN2B subunit-containing NMDA receptors in hippocampal plasticity. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 369, 20130163.10.1098/rstb.2013.0163Search in Google Scholar
Sklar, P., Gabriel, S.B., Mclnnis, M.G., Bennett, P., Lim, Y., Tsan, G., Schaffner, S., Kirov, G., Jones, I., Owen, M., et al. (2002). Family-based association study of 76 candidate genes in bipolar disorder: BDNF is a potential risk locus. Brain-derived neutrophic factor. Mol. Psychiatry 7, 579–593.10.1038/sj.mp.4001058Search in Google Scholar
Soderling, S.H., Guire, E.S., Kaech, S., White, J., Zhang, F., Schutz, K., Langeberg, L.K., Banker, G., Raber, J., and Scott, J.D. (2007). A WAVE-1 and WRP signaling complex regulates spine density, synaptic plasticity, and memory. J. Neurosci. 27, 355–365.10.1523/JNEUROSCI.3209-06.2006Search in Google Scholar
Sun, X., Zhao, Y., and Wolf, M.E. (2005). Dopamine receptor stimulation modulates AMPA receptor synaptic insertion in prefrontal cortex neurons. J. Neurosci. 25, 7342–7351.10.1523/JNEUROSCI.4603-04.2005Search in Google Scholar
Sutton, M.A. and Schuman, E.M. (2006). Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127, 49–58.10.1016/j.cell.2006.09.014Search in Google Scholar
Turrigiano, G.G. and Nelson, S.B. (2000). Hebb and homeostasis in neuronal plasticity. Curr. Opin. Neurobiol. 10, 358–364.10.1016/S0959-4388(00)00091-XSearch in Google Scholar
Vissel, B., Krupp, J.J., Heinemann, S.F., and Westbrook, G.L. (2001). A use-dependent tyrosine phosphorylation of NMDA receptor is independent of ion flux. Nat. Neurosci. 4, 587–596.10.1038/88404Search in Google Scholar PubMed
Wang, Y., Kaneko, N., Asai, N., Enomoto, A., Isotani-Sakakibara, M., Kato, T., Asai, M., Murakumo, Y., Otha, H., Hikita, T., et al. (2011). Girdin is an intrinsic regulator of neuroblast chain migration in the rostral migratory stream of the postnatal brain. J. Neurosci. 31, 8109–8122.10.1523/JNEUROSCI.1130-11.2011Search in Google Scholar PubMed PubMed Central
Watanabe, M., Inoue, Y., Sakimura, K., and Mishina, M. (1992). Developmental changes in distribution of NMDA receptor channel subunit mRNAs. Neuroreport 3, 1138–1140.10.1097/00001756-199212000-00027Search in Google Scholar PubMed
Weickert, C.S., Hyde, T.M., Lipska, B.K., Herman, M.M., Weinberger, D.R., and Kleinman, J.E. (2003). Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia. Mol. Psychiatry 8, 592–610.10.1038/sj.mp.4001308Search in Google Scholar PubMed
Weng, L., Enomoto, A., Ishida-Takagishi, M., Asai, N., and Takahashi, M. (2010). Girding for migratory cues: roles of the Akt substrate Girdin in cancer progression and angiogenesis. Cancer Sci. 101, 836–842.10.1111/j.1349-7006.2009.01487.xSearch in Google Scholar PubMed
Weng, L., Enomoto, A., Miyoshi, H., Takahashi, K., Asai, N., Morone, N., Jiang, P., An, J., Kato, T., Kuroda, K., et al. (2014). Regulation of cargo-selective endocytosis by dynamin 2 GTPase-activating protein girdin. EMBO J. 33, 2098–2112.10.15252/embj.201488289Search in Google Scholar PubMed PubMed Central
Yamada, K. and Nabeshima, T. (2003). Brain-derived neurotrophic factor/TrkB signaling in memory processes. J. Pharmacol. Sci. 91, 267–270.10.1254/jphs.91.267Search in Google Scholar PubMed
Zafra, F., Hengerer, B., Leibrock, J., Thoenen, H., and Lindholm, D. (1990). Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J. 9, 3545–3550.10.1002/j.1460-2075.1990.tb07564.xSearch in Google Scholar PubMed PubMed Central
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