Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Reviews in the Neurosciences

Editor-in-Chief: Huston, Joseph P.

Editorial Board: Topic, Bianca / Adeli, Hojjat / Buzsaki, Gyorgy / Crawley, Jacqueline / Crow, Tim / Gold, Paul / Holsboer, Florian / Korth, Carsten / Li, Jay-Shake / Lubec, Gert / McEwen, Bruce / Pan, Weihong / Pletnikov, Mikhail / Robbins, Trevor / Schnitzler, Alfons / Stevens, Charles / Steward, Oswald / Trojanowski, John


IMPACT FACTOR 2018: 2.157
5-year IMPACT FACTOR: 2.935

CiteScore 2017: 2.81

SCImago Journal Rank (SJR) 2017: 0.980
Source Normalized Impact per Paper (SNIP) 2017: 0.804

Online
ISSN
2191-0200
See all formats and pricing
More options …
Volume 27, Issue 5

Issues

Molecular mechanism linking BDNF/TrkB signaling with the NMDA receptor in memory: the role of Girdin in the CNS

Norimichi Itoh
  • Department of Neuropsychopharmacology and Hospital Pharmacy, Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya, Aichi 466-8560, Japan
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Atsushi Enomoto
  • Department of Pathology, Nagoya University Graduate School of Medicine, 65 Tsurumai, Showa, Nagoya, Aichi 466-8550, Japan
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Taku Nagai
  • Department of Neuropsychopharmacology and Hospital Pharmacy, Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya, Aichi 466-8560, Japan
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Masahide Takahashi
  • Department of Pathology, Nagoya University Graduate School of Medicine, 65 Tsurumai, Showa, Nagoya, Aichi 466-8550, Japan
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Kiyofumi Yamada
  • Corresponding author
  • Department of Neuropsychopharmacology and Hospital Pharmacy, Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya, Aichi 466-8560, Japan
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2016-03-01 | DOI: https://doi.org/10.1515/revneuro-2015-0072

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.

Keywords: BDNF/TrkB signaling; Girdin; memory; NR2B; PI3-K/Akt signaling; synaptic plasticity

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.Google Scholar

  • 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.Google Scholar

  • 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.Google Scholar

  • 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.Google Scholar

  • 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.Google Scholar

  • 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.Google Scholar

  • 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.Google Scholar

  • 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.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.Google Scholar

  • 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.Google Scholar

  • 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.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.Google Scholar

  • 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.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.Google Scholar

  • Dillon, C. and Goda, Y. (2005). The actin cytoskeleton: integrating form and function at the synapse. Annu. Rev. Neurosci. 28, 25–55.Google Scholar

  • Duguid, I. and Sjöström, P.J. (2006). Novel presynaptic mechanisms for coincidence detection in synaptic plasticity. Curr. Opin. Neurobiol. 16, 312–322.Google Scholar

  • 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.Google Scholar

  • 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.Google Scholar

  • 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.Google Scholar

  • 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.Google Scholar

  • 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.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.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.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.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.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.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.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.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.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.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.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.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.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.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.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.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.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.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.Google Scholar

  • Linnarsson, S., Björklund, A., and Ernfors, P. (1997). Learning deficit in BDNF mutant mice. Eur. J. Neurosci. 9, 2581–2587.Google Scholar

  • 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.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.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.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.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.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.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.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.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.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.Google Scholar

  • Murakoshi, H. and Yasuda, R. (2012). Postsynaptic signaling during plasticity of dendritic spine. Trends Neurosci. 35, 135–143.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.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.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.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.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.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.Google Scholar

  • Pitman, R.M. (1984). The versatile synapse. J. Exp. Biol. 112, 199–224.Google Scholar

  • 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.Google Scholar

  • Salter, M.W. and Kalia, L.V. (2004). Src kinases: a hub for NMDA receptor regulation. Nat. Rev. Neurosci. 5, 317–328.Google Scholar

  • 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.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.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.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.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.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.Google Scholar

  • Sutton, M.A. and Schuman, E.M. (2006). Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127, 49–58.Google Scholar

  • Turrigiano, G.G. and Nelson, S.B. (2000). Hebb and homeostasis in neuronal plasticity. Curr. Opin. Neurobiol. 10, 358–364.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.Google Scholar

  • 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.Google Scholar

  • Watanabe, M., Inoue, Y., Sakimura, K., and Mishina, M. (1992). Developmental changes in distribution of NMDA receptor channel subunit mRNAs. Neuroreport 3, 1138–1140.Google Scholar

  • 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.Google Scholar

  • 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.Google Scholar

  • 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.Google Scholar

  • Yamada, K. and Nabeshima, T. (2003). Brain-derived neurotrophic factor/TrkB signaling in memory processes. J. Pharmacol. Sci. 91, 267–270.Google Scholar

  • 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.Google Scholar

About the article

Corresponding author: Kiyofumi Yamada, Department of Neuropsychopharmacology and Hospital Pharmacy, Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya, Aichi 466-8560, Japan, e-mail:

aNorimichi Itoh and Atsushi Enomoto: These authors contributed equally to this work.


Received: 2015-12-21

Accepted: 2016-01-14

Published Online: 2016-03-01

Published in Print: 2016-07-01


Conflict of interest statement: The authors declare no competing financial interests.


Citation Information: Reviews in the Neurosciences, Volume 27, Issue 5, Pages 481–490, ISSN (Online) 2191-0200, ISSN (Print) 0334-1763, DOI: https://doi.org/10.1515/revneuro-2015-0072.

Export Citation

©2016 by De Gruyter.Get Permission

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
Magdalena Miranda, Brianne A. Kent, Juan Facundo Morici, Francisco Gallo, Lisa M. Saksida, Timothy J. Bussey, Noelia Weisstaub, and Pedro Bekinschtein
Neurobiology of Learning and Memory, 2018
[3]
Song Li, Jie Cai, Zhi-Bo Feng, Zi-Run Jin, Bo-Heng Liu, Hong-Yan Zhao, Hong-Bo Jing, Tian-Jiao Wei, Guan-Nan Yang, Ling-Yu Liu, Yan-Jun Cui, and Guo-Gang Xing
Neurochemical Research, 2017

Comments (0)

Please log in or register to comment.
Log in