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Primary cilia and dendritic spines: Different but similar signaling compartments

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Molecules and Cells

Abstract

Primary non-motile cilia and dendritic spines are cellular compartments that are specialized to sense and transduce environmental cues and presynaptic signals, respectively. Despite their unique cellular roles, both compartments exhibit remarkable parallels in the general principles, as well as molecular mechanisms, by which their protein composition, membrane domain architecture, cellular interactions, and structural and functional plasticity are regulated. We compare and contrast the pathways required for the generation and function of cilia and dendritic spines, and suggest that insights from the study of one may inform investigations into the other of these critically important signaling structures.

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References

  • Abramoff, M.D., Mullins, R.F., Lee, K., Hoffmann, J.M., Sonka, M., Critser, D.B., Stasheff, S.F., and Stone, E.M. (2013). Human photoreceptor outer segments shorten during light adaptation. Invest. Ophthalmol. Vis. Sci. 54, 3721–3728.

    PubMed  Google Scholar 

  • Adesnik, H., Nicoll, R.A., and England, P.M. (2005). Photoinactivation of native AMPA receptors reveals their real-time trafficking. Neuron 48, 977–985.

    PubMed  CAS  Google Scholar 

  • Allen, N.J., Bennett, M.L., Foo, L.C., Wang, G.X., Chakraborty, C., Smith, S.J., and Barres, B.A. (2012). Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors. Nature 486, 410–414.

    PubMed  CAS  Google Scholar 

  • Allison, D.W., Gelfand, V.I., Spector, I., and Craig, A.M. (1998). Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J. Neurosci. 18, 2423–2436.

    PubMed  CAS  Google Scholar 

  • Anggono, V., and Huganir, R.L. (2012). Regulation of AMPA receptor trafficking and synaptic plasticity. Curr. Opin. Neurobiol. 22, 461–469.

    PubMed  CAS  Google Scholar 

  • Araque, A., Parpura, V., Sanzgiri, R.P., and Haydon, P.G. (1998a). Glutamate-dependent astrocyte modulation of synaptic transmission between cultured hippocampal neurons. Eur. J. Neurosci. 10, 2129–2142.

    PubMed  CAS  Google Scholar 

  • Araque, A., Sanzgiri, R.P., Parpura, V., and Haydon, P.G. (1998b). Calcium elevation in astrocytes causes an NMDA receptor-dependent increase in the frequency of miniature synaptic currents in cultured hippocampal neurons. J. Neurosci. 18, 6822–6829.

    PubMed  CAS  Google Scholar 

  • Araque, A., Parpura, V., Sanzgiri, R.P., and Haydon, P.G. (1999). Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 22, 208–215.

    PubMed  CAS  Google Scholar 

  • Ashby, M.C., Maier, S.R., Nishimune, A., and Henley, J.M. (2006). Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology. J. Neurosci. 26, 7046–7055.

    PubMed  CAS  Google Scholar 

  • Avasthi, P., and Marshall, W.F. (2012). Stages of ciliogenesis and regulation of ciliary length. Differentiation 83, S30–42.

    PubMed  CAS  Google Scholar 

  • Bacaj, T., Tevlin, M., Lu, Y., and Shaham, S. (2008). Glia are essential for sensory organ function in C. elegans. Science 322, 744–747.

    PubMed  CAS  Google Scholar 

  • Basten, S.G., and Giles, R.H. (2013). Functional aspects of primary cilia in signaling, cell cycle and tumorigenesis. Cilia 2, 6.

    PubMed  CAS  Google Scholar 

  • Beattie, E.C., Stellwagen, D., Morishita, W., Bresnahan, J.C., Ha, B.K., Von Zastrow, M., Beattie, M.S., and Malenka, R.C. (2002). Control of synaptic strength by glial TNFalpha. Science 295, 2282–2285.

    PubMed  CAS  Google Scholar 

  • Berbari, N.F., Johnson, A.D., Lewis, J.S., Askwith, C.C., and Mykytyn, K. (2008). Identification of ciliary localization sequences within the third intracellular loop of G protein-coupled receptors. Mol. Biol. Cell 19, 1540–1547.

    PubMed  CAS  Google Scholar 

  • Berbari, N.F., O’Connor, A.K., Haycraft, C.J., and Yoder, B.K. (2009). The primary cilium as a complex signaling center. Curr. Biol. 19, R526–535.

    PubMed  CAS  Google Scholar 

  • Bershteyn, M., Atwood, S.X., Woo, W.M., Li, M., and Oro, A.E. (2010). MIM and cortactin antagonism regulates ciliogenesis and hedgehog signaling. Dev. Cell 19, 270–283.

    PubMed  CAS  Google Scholar 

  • Besschetnova, T.Y., Kolpakova-Hart, E., Guan, Y., Zhou, J., Olsen, B.R., and Shah, J.V. (2010). Identification of signaling pathways regulating primary cilium length and flow-mediated adaptation. Curr. Biol. 20, 182–187.

    PubMed  CAS  Google Scholar 

  • Bhatt, D.H., Zhang, S., and Gan, W.B. (2009). Dendritic spine dynamics. Annu. Rev. Physiol. 71, 261–282.

    PubMed  CAS  Google Scholar 

  • Bibb, C., and Young, R.W. (1974). Renewal of fatty acids in the membranes of visual cell outer segments. J. Cell Biol. 61, 327–343.

    PubMed  CAS  Google Scholar 

  • Blanpied, T.A., Scott, D.B., and Ehlers, M.D. (2002). Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron 36, 435–449.

    PubMed  CAS  Google Scholar 

  • Bloodgood, B.L. and Sabatini, B.L. (2005). Neuronal activity regulates diffusion across the neck of dendritic spines. Science 310, 866–869.

    PubMed  CAS  Google Scholar 

  • Boesze-Battaglia, K., and Albert, A.D. (1990). Cholesterol modulation of photoreceptor function in bovine retinal rod outer segments. J. Biol. Chem. 265, 20727–20730.

    PubMed  CAS  Google Scholar 

  • Boisvieux-Ulrich, E., Laine, M.C., and Sandoz, D. (1990). Cytochalasin D inhibits basal body migration and ciliary elongation in quail oviduct epithelium. Cell Tissue Res. 259, 443–454.

    PubMed  CAS  Google Scholar 

  • Bok, D., and Hall, M.O. (1971). The role of the pigment epithelium in the etiology of inherited retinal dystrophy in the rat. J. Cell Biol. 49, 664–682.

    PubMed  CAS  Google Scholar 

  • Bourne, J.N., and Harris, K.M. (2008). Balancing structure and function at hippocampal dendritic spines. Annu. Rev. Neurosci. 31, 47–67.

    PubMed  CAS  Google Scholar 

  • Bourne, J.N., Sorra, K.E., Hurlburt, J., and Harris, K.M. (2007). Polyribosomes are increased in spines of CA1 dendrites 2 h after the induction of LTP in mature rat hippocampal slices. Hippocampus 17, 1–4.

    PubMed  CAS  Google Scholar 

  • Brady, J.D., Rich, T.C., Le, X., Stafford, K., Fowler, C.J., Lynch, L., Karpen, J.W., Brown, R.L., and Martens, J.R. (2004). Functional role of lipid raft microdomains in cyclic nucleotide-gated channel activation. Mol. Pharmacol. 65, 503–511.

    PubMed  CAS  Google Scholar 

  • Breslow, D.K., Koslover, E., Seydel, F., Spakowitz, A.J., and Nachury, M.V. (2013). An in vitro assay for entry into cilia reveals unique properties of the soluble diffusion barrier. J. Cell Biol. [In press].

    Google Scholar 

  • Burghoorn, J., Dekkers, M.P., Rademakers, S., de Jong, T., Willemsen, R., Swoboda, P., and Jansen, G. (2010). Dauer pheromone and G-protein signaling modulate the coordination of intraflagellar transport kinesin motor proteins in C. elegans. J. Cell Sci. 123, 2077–2084.

    PubMed  CAS  Google Scholar 

  • Calabrese, B., Wilson, M.S., and Halpain, S. (2006). Development and regulation of dendritic spine synapses. Physiology (Bethesda) 21, 38–47.

    CAS  Google Scholar 

  • Carmona, M.A., Murai, K.K., Wang, L., Roberts, A.J., and Pasquale, E.B. (2009). Glial ephrin-A3 regulates hippocampal dendritic spine morphology and glutamate transport. Proc. Natl. Acad. Sci. USA 106, 12524–12529.

    PubMed  CAS  Google Scholar 

  • Castillo, K., Restrepo, D., and Bacigalupo, J. (2010). Cellular and molecular Ca2+ microdomains in olfactory cilia support low signaling amplification of odor transduction. Eur. J. Neurosci. 32, 932–938.

    PubMed  Google Scholar 

  • Chen, Y., and Sabatini, B.L. (2012). Signaling in dendritic spines and spine microdomains. Curr. Opin. Neurobiol. 22, 389–396.

    PubMed  CAS  Google Scholar 

  • Chen, H., Wiegand, R.D., Koutz, C.A., and Anderson, R.E. (1992). Docosahexaenoic acid increases in frog retinal pigment epithelium following rod photoreceptor shedding. Exp. Eye Res. 55, 93–100.

    PubMed  CAS  Google Scholar 

  • Chen, X., Winters, C., Azzam, R., Li, X., Galbraith, J.A., Leapman, R.D., and Reese, T.S. (2008). Organization of the core structure of the postsynaptic density. Proc. Natl. Acad. Sci. USA 105, 4453–4458.

    PubMed  CAS  Google Scholar 

  • Chiba, S., Amagai, Y., Homma, Y., Fukuda, M., and Mizuno, K. (2013). NDR2-mediated Rabin8 phosphorylation is crucial for ciliogenesis by switching binding specificity from phosphatidylserine to Sec15. EMBO J. 32, 874–885.

    PubMed  CAS  Google Scholar 

  • Chih, B., Liu, P., Chinn, Y., Chalouni, C., Komuves, L.G., Hass, P. E., Sandoval, W., and Peterson, A.S. (2012). A ciliopathy complex at the transition zone protects the cilia as a privileged membrane domain. Nat. Cell Biol. 14, 61–72.

    CAS  Google Scholar 

  • Cho, K.O., Hunt, C.A., and Kennedy, M.B. (1992). The rat brain postsynaptic density fraction contains a homolog of the Drosophila discs-large tumor suppressor protein. Neuron 9, 929–942.

    PubMed  CAS  Google Scholar 

  • Cho, S.J., Lee, H., Dutta, S., Song, J., Walikonis, R., and Moon, I.S. (2011). Septin 6 regulates the cytoarchitecture of neurons through localization at dendritic branch points and bases of protrusions. Mol. Cells 32, 89–98.

    PubMed  CAS  Google Scholar 

  • Christensen, S.T., Pedersen, S.F., Satir, P., Veland, I.R., and Schneider, L. (2008). The primary cilium coordinates signaling pathways in cell cycle control and migration during development and tissue repair. Curr. Top. Dev. Biol. 85, 261–301.

    PubMed  CAS  Google Scholar 

  • Christopherson, K.S., Ullian, E.M., Stokes, C.C., Mullowney, C.E., Hell, J.W., Agah, A., Lawler, J., Mosher, D.F., Bornstein, P., and Barres, B.A. (2005). Thrombospondins are astrocyte-secreted proteins that promote CNS synaptogenesis. Cell 120, 421–433.

    PubMed  CAS  Google Scholar 

  • Clarke, L.E., and Barres, B.A. (2013). Emerging roles of astrocytes in neural circuit development. Nat. Rev. Neurosci. 14, 311–321.

    PubMed  CAS  Google Scholar 

  • Cooney, J.R., Hurlburt, J.L., Selig, D.K., Harris, K.M., and Fiala, J.C. (2002). Endosomal compartments serve multiple hippocampal dendritic spines from a widespread rather than a local store of recycling membrane. J. Neurosci. 22, 2215–2224.

    PubMed  CAS  Google Scholar 

  • Corbit, K.C., Aanstad, P., Singla, V., Norman, A.R., Stainier, D.Y., and Reiter, J.F. (2005). Vertebrate Smoothened functions at the primary cilium. Nature 437, 1018–1021.

    PubMed  CAS  Google Scholar 

  • Cornell-Bell, A.H., Finkbeiner, S.M., Cooper, M.S., and Smith, S.J. (1990). Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science 247, 470–473.

    PubMed  CAS  Google Scholar 

  • Craven, S.E., El-Husseini, A.E., and Bredt, D.S. (1999). Synaptic targeting of the postsynaptic density protein PSD-95 mediated by lipid and protein motifs. Neuron 22, 497–509.

    PubMed  CAS  Google Scholar 

  • Czarnecki, P.G., and Shah, J.V. (2012). The ciliary transition zone: from morphology and molecules to medicine. Trends Cell Biol. 22, 201–210.

    PubMed  CAS  Google Scholar 

  • Dansie, L.E., and Ethell, I.M. (2011). Casting a net on dendritic spines: the extracellular matrix and its receptors. Dev. Neurobiol. 71, 956–981.

    PubMed  CAS  Google Scholar 

  • Das, A., and Guo, W. (2011). Rabs and the exocyst in ciliogenesis, tubulogenesis and beyond. Trends Cell Biol. 21, 383–386.

    PubMed  CAS  Google Scholar 

  • Dent, E.W., Merriam, E.B., and Hu, X. (2011). The dynamic cytoskeleton: backbone of dendritic spine plasticity. Curr. Opin. Neurobiol. 21, 175–181.

    PubMed  CAS  Google Scholar 

  • Deretic, D., Huber, L.A., Ransom, N., Mancini, M., Simons, K., and Papermaster, D.S. (1995). rab8 in retinal photoreceptors may participate in rhodopsin transport and in rod outer segment disk morphogenesis. J. Cell Sci. 108, 215–224.

    PubMed  CAS  Google Scholar 

  • Deretic, D., Williams, A.H., Ransom, N., Morel, V., Hargrave, P.A., and Arendt, A. (2005). Rhodopsin C terminus, the site of mutations causing retinal disease, regulates trafficking by binding to ADP-ribosylation factor 4 (ARF4). Proc. Natl. Acad. Sci. USA 102, 3301–3306.

    PubMed  CAS  Google Scholar 

  • Domire, J.S., Green, J.A., Lee, K.G., Johnson, A.D., Askwith, C.C., and Mykytyn, K. (2011). Dopamine receptor 1 localizes to neuronal cilia in a dynamic process that requires the Bardet-Biedl syndrome proteins. Cell Mol. Life Sci. 68, 2951–2960.

    PubMed  CAS  Google Scholar 

  • Dooley, R., Baumgart, S., Rasche, S., Hatt, H., and Neuhaus, E.M. (2009). Olfactory receptor signaling is regulated by the postsynaptic density 95, Drosophila discs large, zona-occludens 1 (PDZ) scaffold multi-PDZ domain protein 1. FEBS J. 276, 7279–7290.

    PubMed  CAS  Google Scholar 

  • Drummond, I.A. (2012). Cilia functions in development. Curr. Opin. Cell Biol. 24, 24–30.

    PubMed  CAS  Google Scholar 

  • Dubreuil, V., Marzesco, A.M., Corbeil, D., Huttner, W.B., and Wilsch-Brauninger, M. (2007). Midbody and primary cilium of neural progenitors release extracellular membrane particles enriched in the stem cell marker prominin-1. J. Cell Biol. 176, 483–495.

    PubMed  CAS  Google Scholar 

  • Edwards, R.B., and Szamier, R.B. (1977). Defective phagocytosis of isolated rod outer segments by RCS rat retinal pigment epithelium in culture. Science 197, 1001–1003.

    PubMed  CAS  Google Scholar 

  • Engert, F., and Bonhoeffer, T. (1999). Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66–70.

    PubMed  CAS  Google Scholar 

  • Eroglu, C., Allen, N.J., Susman, M.W., O’Rourke, N.A., Park, C.Y., Ozkan, E., Chakraborty, C., Mulinyawe, S.B., Annis, D.S., Huberman, A.D., et al. (2009). Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell 139, 380–392.

    PubMed  CAS  Google Scholar 

  • Ethell, I.M., and Pasquale, E.B. (2005). Molecular mechanisms of dendritic spine development and remodeling. Prog. Neurobiol. 75, 161–205.

    PubMed  CAS  Google Scholar 

  • Feng, W., and Zhang, M. (2009). Organization and dynamics of PDZ-domain-related supramodules in the postsynaptic density. Nat. Rev. Neurosci. 10, 87–99.

    PubMed  CAS  Google Scholar 

  • Fiacco, T.A., and McCarthy, K.D. (2006). Astrocyte calcium elevations: properties, propagation, and effects on brain signaling. Glia 54, 676–690.

    PubMed  Google Scholar 

  • Fischer, M., Kaech, S., Knutti, D., and Matus, A. (1998). Rapid actin-based plasticity in dendritic spines. Neuron 20, 847–854.

    PubMed  CAS  Google Scholar 

  • Flannery, R.J., French, D.A., and Kleene, S.J. (2006). Clustering of cyclic-nucleotide-gated channels in olfactory cilia. Biophys. J. 91, 179–188.

    PubMed  CAS  Google Scholar 

  • Follit, J.A., Li, L., Vucica, Y., and Pazour, G.J. (2010). The cytoplasmic tail of fibrocystin contains a ciliary targeting sequence. J. Cell Biol. 188, 21–28.

    PubMed  CAS  Google Scholar 

  • Francesconi, A., and Duvoisin, R.M. (2002). Alternative splicing unmasks dendritic and axonal targeting signals in metabotropic glutamate receptor 1. J. Neurosci. 22, 2196–2205.

    PubMed  CAS  Google Scholar 

  • Francesconi, A., Kumari, R., and Zukin, R.S. (2009). Regulation of group I metabotropic glutamate receptor trafficking and signaling by the caveolar/lipid raft pathway. J. Neurosci. 29, 3590–3602.

    PubMed  CAS  Google Scholar 

  • French, D.A., Badamdorj, D., and Kleene, S.J. (2010). Spatial distribution of calcium-gated chloride channels in olfactory cilia. PLoS ONE 5, e15676.

    PubMed  CAS  Google Scholar 

  • Frost, N.A., Shroff, H., Kong, H., Betzig, E., and Blanpied, T.A. (2010). Single-molecule discrimination of discrete perisynaptic and distributed sites of actin filament assembly within dendritic spines. Neuron 67, 86–99.

    PubMed  CAS  Google Scholar 

  • Fukazawa, Y., Saitoh, Y., Ozawa, F., Ohta, Y., Mizuno, K., and Inokuchi, K. (2003). Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38, 447–460.

    PubMed  CAS  Google Scholar 

  • Gaertig, J., and Wloga, D. (2008). Ciliary tubulin and its post-translational modifications. Curr. Top. Dev. Biol. 85, 83–113.

    PubMed  CAS  Google Scholar 

  • Garcia-Gonzalo, F.R., and Reiter, J.F. (2012). Scoring a backstage pass: mechanisms of ciliogenesis and ciliary access. J. Cell Biol. 197, 697–709.

    PubMed  CAS  Google Scholar 

  • Gaudreault, S.B., Chabot, C., Gratton, J.P., and Poirier, J. (2004). The caveolin scaffolding domain modifies 2-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptor binding properties by inhibiting phospholipase A2 activity. J. Biol. Chem. 279, 356–362.

    PubMed  CAS  Google Scholar 

  • Geng, L., Okuhara, D., Yu, Z., Tian, X., Cai, Y., Shibazaki, S., and Somlo, S. (2006). Polycystin-2 traffics to cilia independently of polycystin-1 by using an N-terminal RVxP motif. J. Cell Sci. 119, 1383–1395.

    PubMed  CAS  Google Scholar 

  • Gerges, N.Z., Backos, D.S., and Esteban, J.A. (2004). Local control of AMPA receptor trafficking at the postsynaptic terminal by a small GTPase of the Rab family. J. Biol. Chem. 279, 43870–43878.

    PubMed  CAS  Google Scholar 

  • Gerges, N.Z., Backos, D.S., Rupasinghe, C.N., Spaller, M.R., and Esteban, J.A. (2006). Dual role of the exocyst in AMPA receptor targeting and insertion into the postsynaptic membrane. EMBO J. 25, 1623–1634.

    PubMed  CAS  Google Scholar 

  • Ghossoub, R., Molla-Herman, A., Bastin, P., and Benmerah, A. (2011). The ciliary pocket: a once-forgotten membrane domain at the base of cilia. Biol. Cell 103, 131–144.

    PubMed  Google Scholar 

  • Gibbons, I.R., and Grimstone, A.V. (1960). On flagellar structure in certain flagellates. J. Biophys. Biochem. Cytol 7, 697–716.

    PubMed  CAS  Google Scholar 

  • Gibbs, D., Kitamoto, J., and Williams, D.S. (2003). Abnormal phagocytosis by retinal pigmented epithelium that lacks myosin VIIa, the Usher syndrome 1B protein. Proc. Natl. Acad. Sci. USA 100, 6481–6486.

    PubMed  CAS  Google Scholar 

  • Gilula, N.B., and Satir, P. (1972). The ciliary necklace. A ciliary membrane specialization. J. Cell Biol. 53, 494–509.

    PubMed  CAS  Google Scholar 

  • Gladding, C.M., and Raymond, L.A. (2011). Mechanisms underlying NMDA receptor synaptic/extrasynaptic distribution and function. Mol. Cell. Neurosci. 48, 308–320.

    PubMed  CAS  Google Scholar 

  • Gong, Z., Son, W., Chung, Y.D., Kim, J., Shin, D.W., McClung, C.A., Lee, Y., Lee, H.W., Chang, D.J., Kaang, B.K., et al. (2004). Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila. J. Neurosci. 24, 9059–9066.

    PubMed  CAS  Google Scholar 

  • Gordon, W.C., Rodriguez de Turco, E.B., and Bazan, N.G. (1992). Retinal pigment epithelial cells play a central role in the conservation of docosahexaenoic acid by photoreceptor cells after shedding and phagocytosis. Curr. Eye Res. 11, 73–83.

    PubMed  CAS  Google Scholar 

  • Gray, E.G., and Guillery, R.W. (1963). A note on the dendritic spine apparatus. J. Anat. 97, 389–392.

    PubMed  CAS  Google Scholar 

  • Green, J.A., and Mykytyn, K. (2010). Neuronal ciliary signaling in homeostasis and disease. Cell Mol. Life Sci. 67, 3287–3297.

    PubMed  CAS  Google Scholar 

  • Gu, J., Firestein, B.L., and Zheng, J.Q. (2008). Microtubules in dendritic spine development. J. Neurosci. 28, 12120–12124.

    PubMed  CAS  Google Scholar 

  • Haber, M., Zhou, L., and Murai, K.K. (2006). Cooperative astrocyte and dendritic spine dynamics at hippocampal excitatory synapses. J. Neurosci. 26, 8881–8891.

    PubMed  CAS  Google Scholar 

  • Halassa, M.M., and Haydon, P.G. (2010). Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu. Rev. Physiol. 72, 335–355.

    PubMed  CAS  Google Scholar 

  • Halpain, S., Hipolito, A., and Saffer, L. (1998). Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin. J. Neurosci. 18, 9835–9844.

    PubMed  CAS  Google Scholar 

  • Hama, H., Hara, C., Yamaguchi, K., and Miyawaki, A. (2004). PKC signaling mediates global enhancement of excitatory synaptogenesis in neurons triggered by local contact with astrocytes. Neuron 41, 405–415.

    PubMed  CAS  Google Scholar 

  • Handel, M., Schulz, S., Stanarius, A., Schreff, M., Erdtmann-Vourliotis, M., Schmidt, H., Wolf, G., and Hollt, V. (1999). Selective targeting of somatostatin receptor 3 to neuronal cilia. Neuroscience 89, 909–926.

    PubMed  CAS  Google Scholar 

  • Hardingham, G.E., and Bading, H. (2010). Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 11, 682–696.

    PubMed  CAS  Google Scholar 

  • Haycraft, C.J., Banizs, B., Aydin-Son, Y., Zhang, Q., Michaud, E.J., and Yoder, B.K. (2005). Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PLoS Genet. 1, e53.

    PubMed  Google Scholar 

  • Heine, M., Groc, L., Frischknecht, R., Beique, J.C., Lounis, B., Rumbaugh, G., Huganir, R.L., Cognet, L., and Choquet, D. (2008). Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 320, 201–205.

    PubMed  CAS  Google Scholar 

  • Hering, H., Lin, C.C., and Sheng, M. (2003). Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. J. Neurosci. 23, 3262–3271.

    PubMed  CAS  Google Scholar 

  • Higginbotham, H., Eom, T.Y., Mariani, L.E., Bachleda, A., Hirt, J., Gukassyan, V., Cusack, C.L., Lai, C., Caspary, T., and Anton, E.S. (2012). Arl13b in primary cilia regulates the migration and placement of interneurons in the developing cerebral cortex. Dev. Cell 23, 925–938.

    PubMed  CAS  Google Scholar 

  • Higginbotham, H., Guo, J., Yokota, Y., Umberger, N.L., Su, C.Y., Li, J., Verma, N., Hirt, J., Ghukasyan, V., Caspary, T., et al. (2013). Arl13b-regulated cilia activities are essential for polarized radial glial scaffold formation. Nat. Neurosci. 16, 1000–1007.

    PubMed  CAS  Google Scholar 

  • Higley, M.J., and Sabatini, B.L. (2012). Calcium signaling in dendritic spines. Cold Spring Harb. Perspect. Biol. 4, a005686.

    PubMed  Google Scholar 

  • Hirrlinger, J., Hulsmann, S., and Kirchhoff, F. (2004). Astroglial processes show spontaneous motility at active synaptic terminals in situ. Eur. J. Neurosci. 20, 2235–2239.

    PubMed  Google Scholar 

  • Hogan, M.C., Manganelli, L., Woollard, J.R., Masyuk, A.I., Masyuk, T.V., Tammachote, R., Huang, B.Q., Leontovich, A.A., Beito, T.G., Madden, B.J., et al. (2009). Characterization of PKD protein-positive exosome-like vesicles. J. Am. Soc. Nephrol. 20, 278–288.

    PubMed  CAS  Google Scholar 

  • Honkura, N., Matsuzaki, M., Noguchi, J., Ellis-Davies, G.C., and Kasai, H. (2008). The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron 57, 719–729.

    PubMed  CAS  Google Scholar 

  • Hotulainen, P., and Hoogenraad, C.C. (2010). Actin in dendritic spines: connecting dynamics to function. J. Cell Biol. 189, 619–629.

    PubMed  CAS  Google Scholar 

  • Hotulainen, P., Llano, O., Smirnov, S., Tanhuanpaa, K., Faix, J., Rivera, C., and Lappalainen, P. (2009). Defining mechanisms of actin polymerization and depolymerization during dendritic spine morphogenesis. J. Cell Biol. 185, 323–339.

    PubMed  CAS  Google Scholar 

  • Hsiao, Y.C., Tuz, K., and Ferland, R.J. (2012). Trafficking in and to the primary cilium. Cilia 1, 4.

    PubMed  CAS  Google Scholar 

  • Hu, J., Wittekind, S.G., and Barr, M.M. (2007). STAM and Hrs down-regulate ciliary TRP receptors. Mol. Biol. Cell 18, 3277–3289.

    PubMed  CAS  Google Scholar 

  • Hu, X., Viesselmann, C., Nam, S., Merriam, E., and Dent, E.W. (2008). Activity-dependent dynamic microtubule invasion of dendritic spines. J. Neurosci. 28, 13094–13105.

    PubMed  CAS  Google Scholar 

  • Hu, Q., Milenkovic, L., Jin, H., Scott, M.P., Nachury, M.V., Spiliotis, E.T., and Nelson, W.J. (2010). A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 329, 436–439.

    PubMed  CAS  Google Scholar 

  • Hu, X., Ballo, L., Pietila, L., Viesselmann, C., Ballweg, J., Lumbard, D., Stevenson, M., Merriam, E., and Dent, E.W. (2011). BDNFinduced increase of PSD-95 in dendritic spines requires dynamic microtubule invasions. J. Neurosci. 31, 15597–15603.

    PubMed  CAS  Google Scholar 

  • Hunnicutt, G.R., Kosfiszer, M.G., and Snell, W.J. (1990). Cell body and flagellar agglutinins in Chlamydomonas reinhardtii: the cell body plasma membrane is a reservoir for agglutinins whose migration to the flagella is regulated by a functional barrier. J. Cell Biol. 111, 1605–1616.

    PubMed  CAS  Google Scholar 

  • Imanishi, M., Endres, N.F., Gennerich, A., and Vale, R.D. (2006). Autoinhibition regulates the motility of the C. elegans intraflagellar transport motor OSM-3. J. Cell Biol. 174, 931–937.

    PubMed  CAS  Google Scholar 

  • Inoue, A., and Okabe, S. (2003). The dynamic organization of postsynaptic proteins: translocating molecules regulate synaptic function. Curr. Opin. Neurobiol. 13, 332–340.

    PubMed  CAS  Google Scholar 

  • Iomini, C., Li, L., Mo, W., Dutcher, S.K., and Piperno, G. (2006). Two flagellar genes, AGG2 and AGG3, mediate orientation to light in Chlamydomonas. Curr. Biol. 16, 1147–1153.

    PubMed  CAS  Google Scholar 

  • Jablonski, M.M., and Iannaccone, A. (2000). Targeted disruption of Muller cell metabolism induces photoreceptor dysmorphogenesis. Glia 32, 192–204.

    PubMed  CAS  Google Scholar 

  • Janich, P., and Corbeil, D. (2007). GM1 and GM3 gangliosides highlight distinct lipid microdomains within the apical domain of epithelial cells. FEBS Lett. 581, 1783–1787.

    PubMed  CAS  Google Scholar 

  • Janke, C., and Bulinski, J.C. (2011). Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions. Nat. Rev. Mol. Cell Biol. 12, 773–786.

    PubMed  CAS  Google Scholar 

  • Jaworski, J., Kapitein, L.C., Gouveia, S.M., Dortland, B.R., Wulf, P.S., Grigoriev, I., Camera, P., Spangler, S.A., Di Stefano, P., Demmers, J., et al. (2009). Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 61, 85–100.

    PubMed  CAS  Google Scholar 

  • Jenkins, P.M., Hurd, T.W., Zhang, L., McEwen, D.P., Brown, R.L., Margolis, B., Verhey, K.J., and Martens, J.R. (2006). Ciliary targeting of olfactory CNG channels requires the CNGB1b subunit and the kinesin-2 motor protein, KIF17. Curr. Biol. 16, 1211–1216.

    PubMed  CAS  Google Scholar 

  • Jin, H., White, S.R., Shida, T., Schulz, S., Aguiar, M., Gygi, S.P., Bazan, J.F., and Nachury, M.V. (2010). The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Cell 141, 1208–1219.

    PubMed  CAS  Google Scholar 

  • Kameda, H., Furuta, T., Matsuda, W., Ohira, K., Nakamura, K., Hioki, H., and Kaneko, T. (2008). Targeting green fluorescent protein to dendritic membrane in central neurons. Neurosci. Res. 61, 79–91.

    PubMed  CAS  Google Scholar 

  • Kaneshiro, E.S., Matesic, D.F., and Jayasimhulu, K. (1984). Characterizations of six ethanolamine sphingophospholipids from Paramecium cells and cilia. J. Lipid Res. 25, 369–377.

    PubMed  CAS  Google Scholar 

  • Kapitein, L.C., Yau, K.W., Gouveia, S.M., van der Zwan, W.A., Wulf, P.S., Keijzer, N., Demmers, J., Jaworski, J., Akhmanova, A., and Hoogenraad, C.C. (2011). NMDA receptor activation sup presses microtubule growth and spine entry. J. Neurosci. 31, 8194–8209.

    PubMed  CAS  Google Scholar 

  • Kaplan, O.I., Doroquez, D.B., Cevik, S., Bowie, R.V., Clarke, L., Sanders, A.A., Kida, K., Rappoport, J.Z., Sengupta, P., and Blacque, O.E. (2012). Endocytosis genes facilitate protein and membrane transport in C. elegans aensory cilia. Curr. Biol. 22, 451–460.

    PubMed  CAS  Google Scholar 

  • Kasai, H., Hayama, T., Ishikawa, M., Watanabe, S., Yagishita, S., and Noguchi, J. (2010). Learning rules and persistence of dendritic spines. Eur. J. Neurosci. 32, 241–249.

    PubMed  Google Scholar 

  • Kaya, K., Ramesha, C.S., and Thompson, G.A., Jr. (1984). Temperatureinduced changes in the hydroxy and non-hydroxy fatty acid-containing sphingolipids abundant in the surface membrane of Tetrahymena pyriformis NT-1. J. Lipid Res. 25, 68–74.

    PubMed  CAS  Google Scholar 

  • Kaye, J.A., Rose, N.C., Goldsworthy, B., Goga, A., and L’Etoile, N.D. (2009). A 3′UTR pumilio-binding element directs translational activation in olfactory sensory neurons. Neuron 61, 57–70.

    PubMed  CAS  Google Scholar 

  • Kee, H.L., Dishinger, J.F., Blasius, T.L., Liu, C.J., Margolis, B., and Verhey, K.J. (2012). A size-exclusion permeability barrier and nucleoporins characterize a ciliary pore complex that regulates transport into cilia. Nat. Cell Biol. 14, 431–437.

    PubMed  CAS  Google Scholar 

  • Keith, D.J., Sanderson, J.L., Gibson, E.S., Woolfrey, K.M., Robertson, H.R., Olszewski, K., Kang, R., El-Husseini, A., and Dell’acqua, M.L. (2012). Palmitoylation of A-kinase anchoring protein 79/150 regulates dendritic endosomal targeting and synaptic plasticity mechanisms. J. Neurosci. 32, 7119–7136.

    PubMed  CAS  Google Scholar 

  • Kennedy, M.J., and Ehlers, M.D. (2011). Mechanisms and function of dendritic exocytosis. Neuron 69, 856–875.

    PubMed  CAS  Google Scholar 

  • Kennedy, M.J., Davison, I.G., Robinson, C.G., and Ehlers, M.D. (2010). Syntaxin-4 defines a domain for activity-dependent exocytosis in dendritic spines. Cell 141, 524–535.

    PubMed  CAS  Google Scholar 

  • Kessels, H.W., and Malinow, R. (2009). Synaptic AMPA receptor plasticity and behavior. Neuron 61, 340–350.

    PubMed  CAS  Google Scholar 

  • Kettenmann, H., Kirchhoff, F., and Verkhratsky, A. (2013). Microglia: new roles for the synaptic stripper. Neuron 77, 10–18.

    PubMed  CAS  Google Scholar 

  • Kharazia, V.N., and Weinberg, R.J. (1997). Tangential synaptic distribution of NMDA and AMPA receptors in rat neocortex. Neurosci. Lett. 238, 41–44.

    PubMed  CAS  Google Scholar 

  • Kim, C.H., and Lisman, J.E. (1999). A role of actin filament in synaptic transmission and long-term potentiation. J. Neurosci. 19, 4314–4324.

    PubMed  CAS  Google Scholar 

  • Kim, E., and Sheng, M. (2004). PDZ domain proteins of synapses. Nat. Rev. Neurosci. 5, 771–781.

    PubMed  CAS  Google Scholar 

  • Kim, E., Naisbitt, S., Hsueh, Y.P., Rao, A., Rothschild, A., Craig, A.M., and Sheng, M. (1997). GKAP, a novel synaptic protein that interacts with the guanylate kinase-like domain of the PSD-95/SAP90 family of channel clustering molecules. J. Cell Biol. 136, 669–678.

    PubMed  CAS  Google Scholar 

  • Kim, J., Lee, J.E., Heynen-Genel, S., Suyama, E., Ono, K., Lee, K., Ideker, T., Aza-Blanc, P., and Gleeson, J.G. (2010a). Functional genomic screen for modulators of ciliogenesis and cilium length. Nature 464, 1048–1051.

    PubMed  CAS  Google Scholar 

  • Kim, S.K., Shindo, A., Park, T.J., Oh, E.C., Ghosh, S., Gray, R.S., Lewis, R.A., Johnson, C.A., Attie-Bittach, T., Katsanis, N., et al. (2010b). Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science 329, 1337–1340.

    PubMed  CAS  Google Scholar 

  • Knodler, A., Feng, S., Zhang, J., Zhang, X., Das, A., Peranen, J., and Guo, W. (2010). Coordination of Rab8 and Rab11 in primary ciliogenesis. Proc. Natl. Acad. Sci. USA 107, 6346–6351.

    PubMed  CAS  Google Scholar 

  • Koleske, A.J. (2013). Molecular mechanisms of dendrite stability. Nat. Rev. Neurosci. 14, 536–550.

    PubMed  CAS  Google Scholar 

  • Konno, D., Ko, J.A., Usui, S., Hori, K., Maruoka, H., Inui, M., Fujikado, T., Tano, Y., Suzuki, T., Tohyama, K., et al. (2002). The postsynaptic density and dendritic raft localization of PSD-Zip70, which contains an N-myristoylation sequence and leucine-zipper motifs. J. Cell Sci. 115, 4695–4706.

    PubMed  CAS  Google Scholar 

  • Kornau, H.C., Schenker, L.T., Kennedy, M.B., and Seeburg, P.H. (1995). Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269, 1737–1740.

    PubMed  CAS  Google Scholar 

  • Korobova, F., and Svitkina, T. (2010). Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol. Biol. Cell 21, 165–176.

    PubMed  CAS  Google Scholar 

  • Kottgen, M., and Walz, G. (2005). Subcellular localization and trafficking of polycystins. Pflugers Arch. 451, 286–293.

    PubMed  Google Scholar 

  • Krucker, T., Siggins, G.R., and Halpain, S. (2000). Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc. Natl. Acad. Sci. USA 97, 6856–6861.

    PubMed  CAS  Google Scholar 

  • Kucukdereli, H., Allen, N.J., Lee, A.T., Feng, A., Ozlu, M.I., Conatser, L.M., Chakraborty, C., Workman, G., Weaver, M., Sage, E.H., et al. (2011). Control of excitatory CNS synaptogenesis by astrocyte-secreted proteins Hevin and SPARC. Proc. Natl. Acad. Sci. USA 108, E440–449.

    PubMed  CAS  Google Scholar 

  • Kuriu, T., Inoue, A., Bito, H., Sobue, K., and Okabe, S. (2006). Differential control of postsynaptic density scaffolds via actindependent and -independent mechanisms. J. Neurosci. 26, 7693–7706.

    PubMed  CAS  Google Scholar 

  • Lattke, M., Magnutzki, A., Walther, P., Wirth, T., and Baumann, B. (2012). Nuclear factor kappaB activation impairs ependymal ciliogenesis and links neuroinflammation to hydrocephalus formation. J. Neurosci. 32, 11511–11523.

    PubMed  CAS  Google Scholar 

  • Lee, J.H., and Gleeson, J.G. (2010). The role of primary cilia in neuronal function. Neurobiol. Dis. 38, 167–172.

    PubMed  CAS  Google Scholar 

  • Lee, J., Moon, S., Cha, Y., and Chung, Y.D. (2010). Drosophila TRPN(=NOMPC) channel localizes to the distal end of mechanosensory cilia. PLoS One 5, e11012.

    PubMed  Google Scholar 

  • Lee, K.F., Soares, C., and Beique, J.C. (2012). Examining form and function of dendritic spines. Neur. Plast. 2012, 704103.

    Google Scholar 

  • Lefebvre, P.A., Nordstrom, S.A., Moulder, J.E., and Rosenbaum, J.L. (1978). Flagellar elongation and shortening in Chlamydomonas. IV. Effects of flagellar detachment, regeneration, and resorption on the induction of flagellar protein synthesis. J. Cell Biol. 78, 8–27.

    PubMed  CAS  Google Scholar 

  • Lehnert, B.P., Baker, A.E., Gaudry, Q., Chiang, A.S., and Wilson, R.I. (2013). Distinct roles of TRP channels in auditory transduction and amplification in Drosophila. Neuron 77, 115–128.

    PubMed  CAS  Google Scholar 

  • Lehre, K.P., and Rusakov, D.A. (2002). Asymmetry of glia near central synapses favors presynaptically directed glutamate escape. Biophys. J. 83, 125–134.

    PubMed  CAS  Google Scholar 

  • Leveille, F., El Gaamouch, F., Gouix, E., Lecocq, M., Lobner, D., Nicole, O., and Buisson, A. (2008). Neuronal viability is controlled by a functional relation between synaptic and extrasynaptic NMDA receptors. FASEB J. 22, 4258–4271.

    PubMed  CAS  Google Scholar 

  • Li, Z., Okamoto, K., Hayashi, Y., and Sheng, M. (2004). The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119, 873–887.

    PubMed  CAS  Google Scholar 

  • Liang, X., Madrid, J., Saleh, H.S., and Howard, J. (2011). NOMPC, a member of the TRP channel family, localizes to the tubular body and distal cilium of Drosophila campaniform and chordotonal receptor cells. Cytoskeleton (Hoboken) 68, 1–7.

    CAS  Google Scholar 

  • Lin, D.T., Makino, Y., Sharma, K., Hayashi, T., Neve, R., Takamiya, K., and Huganir, R.L. (2009). Regulation of AMPA receptor extrasynaptic insertion by 4.1N, phosphorylation and palmitoylation. Nat. Neurosci. 12, 879–887.

    CAS  Google Scholar 

  • Lin, Y.C., Niewiadomski, P., Lin, B., Nakamura, H., Phua, S.C., Jiao, J., Levchenko, A., Inoue, T. Rohatgi, R., and Inoue, T. (2013). Chemically inducible diffusion trap at cilia reveals molecular sieve-like barrier. Nat. Chem. Biol. 9, 437–443.

    PubMed  CAS  Google Scholar 

  • Liu, Q., Tan, G., Levenkova, N., Li, T., Pugh, E.N., Jr., Rux, J.J., Speicher, D.W., and Pierce, E.A. (2007). The proteome of the mouse photoreceptor sensory cilium complex. Mol. Cell. Proteomics 6, 1299–1317.

    PubMed  CAS  Google Scholar 

  • Louvi, A., and Grove, E.A. (2011). Cilia in the CNS: the quiet organelle claims center stage. Neuron 69, 1046–1060.

    PubMed  CAS  Google Scholar 

  • Low, S.H., Roche, P.A., Anderson, H.A., van Ijzendoorn, S.C., Zhang, M., Mostov, K.E., and Weimbs, T. (1998). Targeting of SNAP-23 and SNAP-25 in polarized epithelial cells. J. Biol. Chem. 273, 3422–3430.

    PubMed  CAS  Google Scholar 

  • Makino, H., and Malinow, R. (2009). AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 64, 381–390.

    PubMed  CAS  Google Scholar 

  • Maletic-Savatic, M., Malinow, R., and Svoboda, K. (1999). Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283, 1923–1927.

    PubMed  CAS  Google Scholar 

  • Matsuzaki, M., Honkura, N., Ellis-Davies, G.C., and Kasai, H. (2004). Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761–766.

    PubMed  CAS  Google Scholar 

  • Mayer, U., Kuller, A., Daiber, P.C., Neudorf, I., Warnken, U., Schnolzer, M., Frings, S., and Mohrlen, F. (2008). The proteome of rat olfactory sensory cilia. Proteomics 2, 322–334.

    Google Scholar 

  • Mazelova, J., Ransom, N., Astuto-Gribble, L., Wilson, M.C., and Deretic, D. (2009). Syntaxin 3 and SNAP-25 pairing, regulated by omega-3 docosahexaenoic acid, controls the delivery of rhodopsin for the biogenesis of cilia-derived sensory organelles, the rod outer segments. J. Cell Sci. 122, 2003–2013.

    PubMed  CAS  Google Scholar 

  • Mesland, D.A., Hoffman, J.L., Caligor, E., and Goodenough, U.W. (1980). Flagellar tip activation stimulated by membrane adhesions in Chlamydomonas gametes. J. Cell Biol. 84, 599–617.

    PubMed  CAS  Google Scholar 

  • Milenkovic, L., Scott, M.P., and Rohatgi, R. (2009). Lateral transport of Smoothened from the plasma membrane to the membrane of the cilium. J. Cell Biol. 187, 365–374.

    PubMed  CAS  Google Scholar 

  • Mitchell, D.C., Straume, M., Miller, J.L., and Litman, B.J. (1990). Modulation of metarhodopsin formation by cholesterol-induced ordering of bilayer lipids. Biochemistry 29, 9143–9149.

    PubMed  CAS  Google Scholar 

  • Mitsui, S., Saito, M., Hayashi, K., Mori, K., and Yoshihara, Y. (2005). A novel phenylalanine-based targeting signal directs telencephalin to neuronal dendrites. J. Neurosci. 25, 1122–1131.

    PubMed  CAS  Google Scholar 

  • Miyamoto, A., Wake, H., Moorhouse, A.J., and Nabekura, J. (2013). Microglia and synapse interactions: fine tuning neural circuits and candidate molecules. Front. Cell. Neurosci. 7, 70.

    PubMed  Google Scholar 

  • Miyoshi, K., Kasahara, K., Miyazaki, I., and Asanuma, M. (2009). Lithium treatment elongates primary cilia in the mouse brain and in cultured cells. Biochem. Biophys. Res. Commun. 388, 757–762.

    PubMed  CAS  Google Scholar 

  • Molla-Herman, A., Ghossoub, R., Blisnick, T., Meunier, A., Serres, C., Silbermann, F., Emmerson, C., Romeo, K., Bourdoncle, P., Schmitt, A., et al. (2010). The ciliary pocket: an endocytic membrane domain at the base of primary and motile cilia. J. Cell Sci. 123, 1785–1795.

    PubMed  CAS  Google Scholar 

  • Moritz, O.L., Tam, B.M., Hurd, L.L., Peranen, J., Deretic, D., and Papermaster, D.S. (2001). Mutant rab8 Impairs docking and fusion of rhodopsin-bearing post-Golgi membranes and causes cell death of transgenic Xenopus rods. Mol. Biol. Cell 12, 2341–2351.

    PubMed  CAS  Google Scholar 

  • Mukhopadhyay, S., Lu, Y., Shaham, S., and Sengupta, P. (2008). Sensory signaling-dependent remodeling of olfactory cilia architecture in C. elegans. Dev. Cell 14, 762–774.

    PubMed  CAS  Google Scholar 

  • Mullen, R.J., and LaVail, M.M. (1976). Inherited retinal dystrophy: primary defect in pigment epithelium determined with experimental rat chimeras. Science 192, 799–801.

    PubMed  CAS  Google Scholar 

  • Muller, W., and Connor, J.A. (1992). Ca2+ signalling in postsynaptic dendrites and spines of mammalian neurons in brain slice. J. Physiol. 86, 57–66.

    CAS  Google Scholar 

  • Murai, K.K., Nguyen, L.N., Irie, F., Yamaguchi, Y., and Pasquale, E.B. (2003). Control of hippocampal dendritic spine morphology through ephrin-A3/EphA4 signaling. Nat. Neurosci. 6, 153–160.

    PubMed  CAS  Google Scholar 

  • Nachury, M.V., Seeley, E.S., and Jin, H. (2010). Trafficking to the ciliary membrane: how to get across the periciliary diffusion barrier? Annu. Rev. Cell Dev. Biol. 26, 59–87.

    PubMed  CAS  Google Scholar 

  • Nagerl, U.V., Eberhorn, N., Cambridge, S.B., and Bonhoeffer, T. (2004). Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44, 759–767.

    PubMed  Google Scholar 

  • Nair, K.S., Balasubramanian, N., and Slepak, V.Z. (2002). Signaldependent translocation of transducin, RGS9-1-Gbeta5L complex, and arrestin to detergent-resistant membrane rafts in photo-receptors. Curr. Biol. 12, 421–425.

    PubMed  CAS  Google Scholar 

  • Naisbitt, S., Kim, E., Tu, J.C., Xiao, B., Sala, C., Valtschanoff, J., Weinberg, R.J., Worley, P.F., and Sheng, M. (1999). Shank, a novel family of postsynaptic density proteins that binds to the NMDA receptor/PSD-95/GKAP complex and cortactin. Neuron 23, 569–582.

    PubMed  CAS  Google Scholar 

  • Newman, E.A. (2003a). Glial cell inhibition of neurons by release of ATP. J. Neurosci. 23, 1659–1666.

    PubMed  CAS  Google Scholar 

  • Newman, E.A. (2003b). New roles for astrocytes: regulation of synaptic transmission. Trends Neurosci. 26, 536–542.

    PubMed  CAS  Google Scholar 

  • Newpher, T.M., and Ehlers, M.D. (2009). Spine microdomains for postsynaptic signaling and plasticity. Trends Cell Biol. 19, 218–227.

    PubMed  Google Scholar 

  • Nishida, H., and Okabe, S. (2007). Direct astrocytic contacts regulate local maturation of dendritic spines. J. Neurosci. 27, 331–340.

    PubMed  CAS  Google Scholar 

  • Noel, J., Ralph, G.S., Pickard, L., Williams, J., Molnar, E., Uney, J.B., Collingridge, G.L., and Henley, J.M. (1999). Surface expression of AMPA receptors in hippocampal neurons is regulated by an NSF-dependent mechanism. Neuron 23, 365–376.

    PubMed  CAS  Google Scholar 

  • Noguchi, J., Matsuzaki, M., Ellis-Davies, G.C., and Kasai, H. (2005). Spine-neck geometry determines NMDA receptor-dependent Ca2+ signaling in dendrites. Neuron 46, 609–622.

    PubMed  CAS  Google Scholar 

  • Oishi, I., Kawakami, Y., Raya, A., Callol-Massot, C., and Izpisua Belmonte, J.C. (2006). Regulation of primary cilia formation and left-right patterning in zebrafish by a noncanonical Wnt signaling mediator, duboraya. Nat. Genet. 38, 1316–1322.

    PubMed  CAS  Google Scholar 

  • Okabe, S. (2007). Molecular anatomy of the postsynaptic density. Mol. Cell Neurosci. 34, 503–518.

    PubMed  CAS  Google Scholar 

  • Okamoto, K., Nagai, T., Miyawaki, A., and Hayashi, Y. (2004). Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat. Neurosci. 7, 1104–1112.

    PubMed  CAS  Google Scholar 

  • Ostroff, L.E., Fiala, J.C., Allwardt, B., and Harris, K.M. (2002). Polyribosomes redistribute from dendritic shafts into spines with enlarged synapses during LTP in developing rat hippocampal slices. Neuron 35, 535–545.

    PubMed  CAS  Google Scholar 

  • Ou, Y., Ruan, Y., Cheng, M., Moser, J.J., Rattner, J.B., and van der Hoorn, F.A. (2009). Adenylate cyclase regulates elongation of mammalian primary cilia. Exp. Cell Res. 315, 2802–2817.

    PubMed  CAS  Google Scholar 

  • Ounjai, P., Kim, K.D., Liu, H., Dong, M., Tauscher, A.N., Witkowska, H.E., and Downing, K.H. (2013). Architectural insights into a ciliary partition. Curr. Biol. 23, 339–344.

    PubMed  CAS  Google Scholar 

  • Palay, S.L. (1956). Synapses in the central nervous system. J. Biophys. Biochem. Cytol. 2, 193–202.

    PubMed  CAS  Google Scholar 

  • Panatier, A., Vallee, J., Haber, M., Murai, K.K., Lacaille, J.C., and Robitaille, R. (2011). Astrocytes are endogenous regulators of basal transmission at central synapses. Cell 146, 785–798.

    PubMed  CAS  Google Scholar 

  • Pannasch, U., and Rouach, N. (2013). Emerging role for astroglial networks in information processing: from synapse to behavior. Trends Neurosci. 36, 405–417.

    PubMed  CAS  Google Scholar 

  • Paolicelli, R.C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., Giustetto, M., Ferreira, T.A., Guiducci, E., Dumas, L., et al. (2011). Synaptic pruning by microglia is necessary for normal brain development. Science 333, 1456–1458.

    PubMed  CAS  Google Scholar 

  • Park, M., Penick, E.C., Edwards, J.G., Kauer, J.A., and Ehlers, M.D. (2004). Recycling endosomes supply AMPA receptors for LTP. Science 305, 1972–1975.

    PubMed  CAS  Google Scholar 

  • Park, M., Salgado, J.M., Ostroff, L., Helton, T.D., Robinson, C.G., Harris, K.M., and Ehlers, M.D. (2006). Plasticity-induced growth of dendritic spines by exocytic trafficking from recycling endosomes. Neuron 52, 817–830.

    PubMed  CAS  Google Scholar 

  • Parpura, V., Basarsky, T.A., Liu, F., Jeftinija, K., Jeftinija, S., and Haydon, P.G. (1994). Glutamate-mediated astrocyte-neuron signalling. Nature 369, 744–747.

    PubMed  CAS  Google Scholar 

  • Pasquale, S.M., and Goodenough, U.W. (1987). Cyclic AMP functions as a primary sexual signal in gametes of Chlamydomonas reinhardtii. J. Cell Biol. 105, 2279–2292.

    PubMed  CAS  Google Scholar 

  • Passafaro, M., Piech, V., and Sheng, M. (2001). Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nat. Neurosci. 4, 917–926.

    PubMed  CAS  Google Scholar 

  • Pasti, L., Volterra, A., Pozzan, T., and Carmignoto, G. (1997). Intracellular calcium oscillations in astrocytes: a highly plastic, bidirectional form of communication between neurons and astrocytes in situ. J. Neurosci. 17, 7817–7830.

    PubMed  CAS  Google Scholar 

  • Patterson, M.A., Szatmari, E.M., and Yasuda, R. (2010). AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK-dependent manner during long-term potentiation. Proc. Natl. Acad. Sci. USA 107, 15951–15956.

    PubMed  CAS  Google Scholar 

  • Pazour, G.J., and Bloodgood, R.A. (2008). Targeting proteins to the ciliary membrane. Curr. Top. Dev. Biol. 85, 115–149.

    PubMed  CAS  Google Scholar 

  • Penn, J.S., and Williams, T.P. (1986). Photostasis: regulation of daily photon-catch by rat retinas in response to various cyclic illuminances. Exp. Eye Res. 43, 915–928.

    PubMed  CAS  Google Scholar 

  • Penzes, P., Cahill, M.E., Jones, K.A., VanLeeuwen, J.E., and Woolfrey, K.M. (2011). Dendritic spine pathology in neuropsy-chiatric disorders. Nat. Neurosci. 14, 285–293.

    PubMed  CAS  Google Scholar 

  • Perea, G., and Araque, A. (2005). Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes. J. Neurosci. 25, 2192–2203.

    PubMed  CAS  Google Scholar 

  • Perens, E.A., and Shaham, S. (2005). C. elegans daf-6 encodes a patched-related protein required for lumen formation. Dev. Cell 8, 893–906.

    PubMed  CAS  Google Scholar 

  • Perkins, L.A., Hedgecock, E.M., Thomson, J.N., and Culotti, J.G. (1986). Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev. Biol. 117, 456–487.

    PubMed  CAS  Google Scholar 

  • Petrini, E.M., Lu, J., Cognet, L., Lounis, B., Ehlers, M.D., and Choquet, D. (2009). Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 63, 92–105.

    PubMed  CAS  Google Scholar 

  • Plotnikova, O.V., Pugacheva, E.N., and Golemis, E.A. (2009). Primary cilia and the cell cycle. Methods Cell Biol. 94, 137–160.

    PubMed  CAS  Google Scholar 

  • Pontrello, C.G., and Ethell, I.M. (2009). Accelerators, brakes, and gears of actin dynamics in dendritic spines. Open Neurosci. J. 3, 67–86.

    PubMed  CAS  Google Scholar 

  • Poole, C.A., Flint, M.H., and Beaumont, B.W. (1985). Analysis of the morphology and function of primary cilia in connective tissues: a cellular cybernetic probe? Cell Motil. 5, 175–193.

    PubMed  CAS  Google Scholar 

  • Porter, J.T., and McCarthy, K.D. (1996). Hippocampal astrocytes in situ respond to glutamate released from synaptic terminals. J. Neurosci. 16, 5073–5081.

    PubMed  CAS  Google Scholar 

  • Procko, C., Lu, Y., and Shaham, S. (2011). Glia delimit shape changes of sensory neuron receptive endings in C. elegans. Development 138, 1371–1381.

    PubMed  CAS  Google Scholar 

  • Procko, C., Lu, Y., and Shaham, S. (2012). Sensory organ remodeling in Caenorhabditis elegans requires the zinc-finger protein ZTF-16. Genetics 190, 1405–1415.

    PubMed  CAS  Google Scholar 

  • Quader, H., Cherniack, J., and Filner, P. (1978). Participation of calcium in flagellar shortening and regeneration in Chlamydomonas reinhardii. Exp. Cell Res. 113, 295–301.

    PubMed  CAS  Google Scholar 

  • Racz, B., Blanpied, T.A., Ehlers, M.D., and Weinberg, R.J. (2004). Lateral organization of endocytic machinery in dendritic spines. Nat. Neurosci. 7, 917–918.

    PubMed  CAS  Google Scholar 

  • Rattner, J.B., Sciore, P., Ou, Y., van der Hoorn, F.A., and Lo, I.K. (2010). Primary cilia in fibroblast-like type B synoviocytes lie within a cilium pit: a site of endocytosis. Histol. Histopathol. 25, 865–875.

    PubMed  Google Scholar 

  • Reese, T.S. (1965). Olfactory cilia in the frog. J. Cell Biol. 25, 209–230.

    PubMed  CAS  Google Scholar 

  • Reiter, J.F., Blacque, O.E., and Leroux, M.R. (2012). The base of the cilium: roles for transition fibres and the transition zone in ciliary formation, maintenance and compartmentalization. EMBO Rep. 13, 608–618.

    PubMed  CAS  Google Scholar 

  • Rivera, J.F., Ahmad, S., Quick, M.W., Liman, E.R., and Arnold, D.B. (2003). An evolutionarily conserved dileucine motif in Shal K+ channels mediates dendritic targeting. Nat. Neurosci. 6, 243–250.

    PubMed  CAS  Google Scholar 

  • Rochefort, N.L., and Konnerth, A. (2012). Dendritic spines: from structure to in vivo function. EMBO Rep. 13, 699–708.

    PubMed  CAS  Google Scholar 

  • Roepman, R., and Wolfrum, U. (2007). Protein networks and complexes in photoreceptor cilia. Subcell. Biochem 43, 209–235.

    PubMed  Google Scholar 

  • Rogers, K.K., Wilson, P.D., Snyder, R.W., Zhang, X., Guo, W., Burrow, C.R., and Lipschutz, J.H. (2004). The exocyst localizes to the primary cilium in MDCK cells. Biochem. Biophys. Res. Commun. 319, 138–143.

    PubMed  CAS  Google Scholar 

  • Rohatgi, R., Milenkovic, L., and Scott, M.P. (2007). Patched1 regulates hedgehog signaling at the primary cilium. Science 317, 372–376.

    PubMed  CAS  Google Scholar 

  • Rosenbaum, J.L., and Witman, G.B. (2002). Intraflagellar transport. Nat. Rev. Mol. Cell. Biol. 3, 813–825.

    PubMed  CAS  Google Scholar 

  • Rubio, M.D., Johnson, R., Miller, C.A., Huganir, R.L., and Rumbaugh, G. (2011). Regulation of synapse structure and function by distinct myosin II motors. J. Neurosci. 31, 1448–1460.

    PubMed  CAS  Google Scholar 

  • Ryu, J., Liu, L., Wong, T.P., Wu, D.C., Burette, A., Weinberg, R., Wang, Y.T., and Sheng, M. (2006). A critical role for myosin IIb in dendritic spine morphology and synaptic function. Neuron 49, 175–182.

    PubMed  CAS  Google Scholar 

  • Saarikangas, J., and Barral, Y. (2011). The emerging functions of septins in metazoans. EMBO Rep. 12, 1118–1126.

    PubMed  CAS  Google Scholar 

  • Sabatini, B.L., Oertner, T.G., and Svoboda, K. (2002). The life cycle of Ca(2+) ions in dendritic spines. Neuron 33, 439–452.

    PubMed  CAS  Google Scholar 

  • Schafer, D.P., Lehrman, E.K., Kautzman, A.G., Koyama, R., Mardinly, A.R., Yamasaki, R., Ransohoff, R.M., Greenberg, M.E., Barres, B.A., and Stevens, B. (2012). Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74, 691–705.

    PubMed  CAS  Google Scholar 

  • Schneider, L., Clement, C.A., Teilmann, S.C., Pazour, G.J., Hoffmann, E.K., Satir, P., and Christensen, S.T. (2005). PDGFRalpha signaling is regulated through the primary cilium in fibroblasts. Curr. Biol. 15, 1861–1866.

    PubMed  CAS  Google Scholar 

  • Scholey, J.M. (2008). Intraflagellar transport motors in cilia: moving along the cell’s antenna. J. Cell Biol. 180, 23–29.

    PubMed  CAS  Google Scholar 

  • Schubert, V., and Dotti, C.G. (2007). Transmitting on actin: synaptic control of dendritic architecture. J. Cell Sci. 120, 205–212.

    PubMed  CAS  Google Scholar 

  • Seeger-Nukpezah, T., and Golemis, E.A. (2012). The extracellular matrix and ciliary signaling. Curr. Opin. Cell Biol. 24, 652–661.

    PubMed  CAS  Google Scholar 

  • Senin, II, Hoppner-Heitmann, D., Polkovnikova, O.O., Churumova, V.A., Tikhomirova, N.K., Philippov, P.P., and Koch, K.W. (2004). Recoverin and rhodopsin kinase activity in detergent-resistant membrane rafts from rod outer segments. J. Biol. Chem. 279, 48647–48653.

    PubMed  CAS  Google Scholar 

  • Seno, K., Kishimoto, M., Abe, M., Higuchi, Y., Mieda, M., Owada, Y., Yoshiyama, W., Liu, H., and Hayashi, F. (2001). Light- and guanosine 5′-3-O-(thio)triphosphate-sensitive localization of a G protein and its effector on detergent-resistant membrane rafts in rod photoreceptor outer segments. J. Biol. Chem. 276, 20813–20816.

    PubMed  CAS  Google Scholar 

  • Sfakianos, J., Togawa, A., Maday, S., Hull, M., Pypaert, M., Cantley, L., Toomre, D., and Mellman, I. (2007). Par3 functions in the biogenesis of the primary cilium in polarized epithelial cells. J. Cell Biol. 179, 1133–1140.

    PubMed  CAS  Google Scholar 

  • Shah, A.S., Ben-Shahar, Y., Moninger, T.O., Kline, J.N., and Welsh, M.J. (2009). Motile cilia of human airway epithelia are chemosensory. Science 325, 1131–1134.

    PubMed  CAS  Google Scholar 

  • Shaham, S. (2010). Chemosensory organs as models of neuronal synapses. Nat. Rev. Neurosci. 11, 212–217.

    PubMed  CAS  Google Scholar 

  • Sharma, N., Kosan, Z.A., Stallworth, J.E., Berbari, N.F., and Yoder, B.K. (2011). Soluble levels of cytosolic tubulin regulate ciliary length control. Mol. Biol. Cell 22, 806–816.

    PubMed  CAS  Google Scholar 

  • Sheng, M., and Kim, E. (2011). The postsynaptic organization of synapses. Cold Spring Harb. Perspect. Biol. 3.

  • Shinohara, Y., Hirase, H., Watanabe, M., Itakura, M., Takahashi, M., and Shigemoto, R. (2008). Left-right asymmetry of the hippocampal synapses with differential subunit allocation of glutamate receptors. Proc. Natl. Acad. Sci. USA 105, 19498–19503.

    PubMed  CAS  Google Scholar 

  • Shiraishi, Y., Mizutani, A., Yuasa, S., Mikoshiba, K., and Furuichi, T. (2004). Differential expression of Homer family proteins in the developing mouse brain. J. Comp. Neurol. 473, 582–599.

    PubMed  CAS  Google Scholar 

  • Shirao, T., and Gonzalez-Billault, C. (2013). Actin filaments and microtubules in dendritic spines. J. Neurochem. 126, 155–164.

    PubMed  CAS  Google Scholar 

  • Siekevitz, P. (1985). The postsynaptic density: a possible role in long-lasting effects in the central nervous system. Proc. Natl. Acad. Sci. USA 82, 3494–3498.

    PubMed  CAS  Google Scholar 

  • Silverman, M.A., and Leroux, M.R. (2009). Intraflagellar transport and the generation of dynamic, structurally and functionally diverse cilia. Trends Cell Biol. 19, 306–316.

    PubMed  CAS  Google Scholar 

  • Simons, K., and Toomre, D. (2000). Lipid rafts and signal transduction. Nat. Rev. Mol. Cell Biol. 1, 31–39.

    PubMed  CAS  Google Scholar 

  • Souto-Padron, T., and de Souza, W. (1983). Freeze-fracture localization of filipin-cholesterol complexes in the plasma membrane of Trypanosoma cruzi. J. Parasitol. 69, 129–137.

    PubMed  CAS  Google Scholar 

  • Spacek, J., and Harris, K.M. (1997). Three-dimensional organization of smooth endoplasmic reticulum in hippocampal CA1 dendrites and dendritic spines of the immature and mature rat. J. Neurosci. 17, 190–203.

    PubMed  CAS  Google Scholar 

  • Spacek, J., and Harris, K.M. (2004). Trans-endocytosis via spinules in adult rat hippocampus. J. Neurosci. 24, 4233–4241.

    PubMed  CAS  Google Scholar 

  • Star, E.N., Kwiatkowski, D.J., and Murthy, V.N. (2002). Rapid turnover of actin in dendritic spines and its regulation by activity. Nat. Neurosci. 5, 239–246.

    PubMed  CAS  Google Scholar 

  • Strauss, O. (2005). The retinal pigment epithelium in visual function. Physiol. Rev. 85, 845–881.

    PubMed  CAS  Google Scholar 

  • Svoboda, K., Tank, D.W., and Denk, W. (1996). Direct measurement of coupling between dendritic spines and shafts. Science 272, 716–719.

    PubMed  CAS  Google Scholar 

  • Tada, T., Simonetta, A., Batterton, M., Kinoshita, M., Edbauer, D., and Sheng, M. (2007). Role of Septin cytoskeleton in spine morphogenesis and dendrite development in neurons. Curr. Biol. 17, 1752–1758.

    PubMed  CAS  Google Scholar 

  • Tam, B.M., Moritz, O.L., Hurd, L.B., and Papermaster, D.S. (2000). Identification of an outer segment targeting signal in the COOH terminus of rhodopsin using transgenic Xenopus laevis. J. Cell Biol. 151, 1369–1380.

    PubMed  CAS  Google Scholar 

  • Tao, B., Bu, S., Yang, Z., Siroky, B., Kappes, J.C., Kispert, A., and Guay-Woodford, L.M. (2009). Cystin localizes to primary cilia via membrane microdomains and a targeting motif. J. Am. Soc. Nephrol. 20, 2570–2580.

    PubMed  CAS  Google Scholar 

  • Tao-Cheng, J.H., Dosemeci, A., Gallant, P.E., Miller, S., Galbraith, J.A., Winters, C.A., Azzam, R., and Reese, T.S. (2009). Rapid turnover of spinules at synaptic terminals. Neuroscience 160, 42–50.

    PubMed  CAS  Google Scholar 

  • Tao-Cheng, J.H., Crocker, V.T., Winters, C.A., Azzam, R., Chludzinski, J., and Reese, T.S. (2011). Trafficking of AMPA receptors at plasma membranes of hippocampal neurons. J. Neurosci. 31, 4834–4843.

    PubMed  CAS  Google Scholar 

  • Tardin, C., Cognet, L., Bats, C., Lounis, B., and Choquet, D. (2003). Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J. 22, 4656–4665.

    PubMed  CAS  Google Scholar 

  • Tarrant, S.B., and Routtenberg, A. (1977). The synaptic spinule in the dendritic spine: electron microscopic study of the hippocampal dentate gyrus. Tissue Cell 9, 461–473.

    PubMed  CAS  Google Scholar 

  • Teodoro, R.O., Pekkurnaz, G., Nasser, A., Higashi-Kovtun, M.E., Balakireva, M., McLachlan, I.G., Camonis, J., and Schwarz, T.L. (2013). Ral mediates activity-dependent growth of postsynaptic membranes via recruitment of the exocyst. EMBO J. 32, 2039–2055.

    PubMed  CAS  Google Scholar 

  • Tetley, L. (1986). Freeze-fracture studies on the surface membranes of pleomorphic bloodstream and in vitro transformed procyclic Trypanosoma brucei. Acta Trop. 43, 307–317.

    PubMed  CAS  Google Scholar 

  • Tobin, D., Madsen, D., Kahn-Kirby, A., Peckol, E., Moulder, G., Barstead, R., Maricq, A., and Bargmann, C.I. (2002). Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35, 307–318.

    PubMed  CAS  Google Scholar 

  • Trapp, B.D., Wujek, J.R., Criste, G.A., Jalabi, W., Yin, X., Kidd, G.J., Stohlman, S., and Ransohoff, R. (2007). Evidence for synaptic stripping by cortical microglia. Glia 55, 360–368.

    PubMed  Google Scholar 

  • Travis, A.J., Merdiushev, T., Vargas, L.A., Jones, B.H., Purdon, M.A., Nipper, R.W., Galatioto, J., Moss, S.B., Hunnicutt, G.R., and Kopf, G.S. (2001). Expression and localization of caveolin-1, and the presence of membrane rafts, in mouse and Guinea pig spermatozoa. Dev. Biol. 240, 599–610.

    PubMed  CAS  Google Scholar 

  • Tremblay, M.E., Lowery, R.L., and Majewska, A.K. (2010). Microglial interactions with synapses are modulated by visual experience. PLoS Biol. 8, e1000527.

    PubMed  Google Scholar 

  • Tyler, K.M., Fridberg, A., Toriello, K.M., Olson, C.L., Cieslak, J.A., Hazlett, T.L., and Engman, D.M. (2009). Flagellar membrane localization via association with lipid rafts. J. Cell Sci. 122, 859–866.

    PubMed  CAS  Google Scholar 

  • Ventura, R., and Harris, K.M. (1999). Three-dimensional relationships between hippocampal synapses and astrocytes. J. Neurosci. 19, 6897–6906.

    PubMed  CAS  Google Scholar 

  • Verbich, D., Prenosil, G.A., Chang, P.K., Murai, K.K., and McKinney, R.A. (2012). Glial glutamate transport modulates dendritic spine head protrusions in the hippocampus. Glia 60, 1067–1077.

    PubMed  Google Scholar 

  • Verhey, K.J., Dishinger, J., and Kee, H.L. (2011). Kinesin motors and primary cilia. Biochem. Soc. Trans. 39, 1120–1125.

    PubMed  CAS  Google Scholar 

  • Vieira, O.V., Gaus, K., Verkade, P., Fullekrug, J., Vaz, W.L., and Simons, K. (2006). FAPP2, cilium formation, and compartmentalization of the apical membrane in polarized Madin-Darby canine kidney (MDCK) cells. Proc. Natl. Acad. Sci. USA 103, 18556–18561.

    PubMed  CAS  Google Scholar 

  • Volterra, A., and Meldolesi, J. (2005). Astrocytes, from brain glue to communication elements: the revolution continues. Nat. Rev. Neurosci. 6, 626–640.

    PubMed  CAS  Google Scholar 

  • Wake, H., Moorhouse, A.J., Miyamoto, A., and Nabekura, J. (2013). Microglia: actively surveying and shaping neuronal circuit structure and function. Trends Neurosci. 36, 209–217.

    PubMed  CAS  Google Scholar 

  • Walsh, M.J., and Kuruc, N. (1992). The postsynaptic density: constituent and associated proteins characterized by electrophoresis, immunoblotting, and peptide sequencing. J. Neurochem. 59, 667–678.

    PubMed  CAS  Google Scholar 

  • Wang, X., Iannaccone, A., and Jablonski, M.M. (2004). Contribution of Muller cells toward the regulation of photoreceptor outer segment assembly. Neuron Glia Biol. 1, 291–296.

    PubMed  Google Scholar 

  • Wang, X., Lou, N., Xu, Q., Tian, G.F., Peng, W.G., Han, X., Kang, J., Takano, T., and Nedergaard, M. (2006). Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo. Nat. Neurosci. 9, 816–823.

    PubMed  CAS  Google Scholar 

  • Wang, G., Krishnamurthy, K., and Bieberich, E. (2009a). Regulation of primary cilia formation by ceramide. J. Lipid Res. 50, 2103–2110.

    PubMed  CAS  Google Scholar 

  • Wang, J.S., Estevez, M.E., Cornwall, M.C., and Kefalov, V.J. (2009b). Intra-retinal visual cycle required for rapid and complete cone dark adaptation. Nat. Neurosci. 12, 295–302.

    PubMed  CAS  Google Scholar 

  • Wang, X., Nookala, S., Narayanan, C., Giorgianni, F., Beranova-Giorgianni, S., McCollum, G., Gerling, I., Penn, J.S., and Jablonski, M.M. (2009c). Proteomic analysis of the retina: removal of RPE alters outer segment assembly and retinal protein expression. Glia 57, 380–392.

    PubMed  Google Scholar 

  • Wang, Y., Zhou, Z., Walsh, C.T., and McMahon, A.P. (2009d). Selective translocation of intracellular smoothened to the primary cilium in response to Hedgehog pathway modulation. Proc. Natl. Acad. Sci. USA 106, 2623–2628.

    PubMed  CAS  Google Scholar 

  • Ward, S., Thomson, N., White, J.G., and Brenner, S. (1975). Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J. Comp. Neurol. 160, 313–337.

    PubMed  CAS  Google Scholar 

  • Waters, A.M., and Beales, P.L. (2011). Ciliopathies: an expanding disease spectrum. Pediatr. Nephrol. 26, 1039–1056.

    PubMed  Google Scholar 

  • Wegner, A.M., Nebhan, C.A., Hu, L., Majumdar, D., Meier, K.M., Weaver, A.M., and Webb, D.J. (2008). N-wasp and the arp2/3 complex are critical regulators of actin in the development of dendritic spines and synapses. J. Biol. Chem. 283, 15912–15920.

    PubMed  CAS  Google Scholar 

  • West, A.E., Neve, R.L., and Buckley, K.M. (1997). Identification of a somatodendritic targeting signal in the cytoplasmic domain of the transferrin receptor. J. Neurosci. 17, 6038–6047.

    PubMed  CAS  Google Scholar 

  • Westlake, C.J., Junutula, J.R., Simon, G.C., Pilli, M., Prekeris, R., Scheller, R.H., Jackson, P.K., and Eldridge, A.G. (2007). Identification of Rab11 as a small GTPase binding protein for the Evi5 oncogene. Proc. Natl. Acad. Sci. USA 104, 1236–1241.

    PubMed  CAS  Google Scholar 

  • Westlake, C.J., Baye, L.M., Nachury, M.V., Wright, K.J., Ervin, K.E., Phu, L., Chalouni, C., Beck, J.S., Kirkpatrick, D.S., Slusarski, D. C., et al. (2011). Primary cilia membrane assembly is initiated by Rab11 and transport protein particle II (TRAPPII) complexdependent trafficking of Rabin8 to the centrosome. Proc. Natl. Acad. Sci. USA 108, 2759–2764.

    PubMed  CAS  Google Scholar 

  • Wilson, N.F., Iyer, J.K., Buchheim, J.A., and Meek, W. (2008). Regulation of flagellar length in Chlamydomonas. Semin. Cell Dev. Biol. 19, 494–501.

    PubMed  Google Scholar 

  • Wojtyniak, M., Brear, A.G., O’Halloran, D.M., and Sengupta, P. (2013). Cell- and subunit-specific mechanisms of CNG channel ciliary trafficking and localization in C. elegans. J. Cell Sci. (in press).

    Google Scholar 

  • Wood, C.R., Huang, K., Diener, D.R., and Rosenbaum, J.L. (2013). The cilium secretes bioactive ectosomes. Curr. Biol. 23, 906–911.

    PubMed  CAS  Google Scholar 

  • Xie, Y., Vessey, J.P., Konecna, A., Dahm, R., Macchi, P., and Kiebler, M.A. (2007). The GTP-binding protein Septin 7 is critical for dendrite branching and dendritic-spine morphology. Curr. Biol. 17, 1746–1751.

    PubMed  CAS  Google Scholar 

  • Ye, F., Breslow, D.K., Koslover, E.F., Spakowitz, A.J., Nelson, W.J., and Nachury, M.V. (2013). Single molecule imaging reveals a major role for diffusion in the exploration of ciliary space by signaling receptors. eLife 2, e00654.

    PubMed  Google Scholar 

  • Yoshii, A., Zhao, J.P., Pandian, S., van Zundert, B., and Constantine-Paton, M. (2013). A myosin Va mutant mouse with disruptions in glutamate synaptic development and mature plasticity in visual cortex. J. Neurosci. 33, 8472–8482.

    PubMed  CAS  Google Scholar 

  • Young, R.W. (1967). The renewal of photoreceptor cell outer segments. J. Cell Biol. 33, 61–72.

    PubMed  CAS  Google Scholar 

  • Young, R.W. (1971). Shedding of discs from rod outer segments in the rhesus monkey. J. Ultrastruc. Res. 34, 190–203.

    CAS  Google Scholar 

  • Young, R.W. (1976). Visual cells and the concept of renewal. Invest. Ophthalmol. Vis. Sci. 15, 700–725.

    PubMed  CAS  Google Scholar 

  • Young, R.W., and Droz, B. (1968). The renewal of protein in retinal rods and cones. J. Cell Biol. 39, 169–184.

    PubMed  CAS  Google Scholar 

  • Young, R.W., and Bok, D. (1969). Participation of the retinal pigment epithelium in the rod outer segment renewal process. J. Cell Biol. 42, 392–403.

    PubMed  CAS  Google Scholar 

  • Yudowski, G.A., Puthenveedu, M.A., Leonoudakis, D., Panicker, S., Thorn, K.S., Beattie, E.C., and von Zastrow, M. (2007). Realtime imaging of discrete exocytic events mediating surface delivery of AMPA receptors. J. Neurosci. 27, 11112–11121.

    PubMed  CAS  Google Scholar 

  • Zeng, H., Jia, J., and Liu, A. (2010). Coordinated translocation of mammalian Gli proteins and suppressor of fused to the primary cilium. PLoS One 5, e15900.

    PubMed  CAS  Google Scholar 

  • Zhou, Q., Homma, K.J., and Poo, M.M. (2004). Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44, 749–757.

    PubMed  CAS  Google Scholar 

  • Zhu, Y.C., Li, D., Wang, L., Lu, B., Zheng, J., Zhao, S.L., Zeng, R., and Xiong, Z.Q. (2013). Palmitoylation-dependent CDKL5-PSD-95 interaction regulates synaptic targeting of CDKL5 and den dritic spine development. Proc. Natl. Acad. Sci. USA 110, 9118–9123.

    PubMed  CAS  Google Scholar 

  • Zito, K., Knott, G., Shepherd, G.M., Shenolikar, S., and Svoboda, K. (2004). Induction of spine growth and synapse formation by regulation of the spine actin cytoskeleton. Neuron 44, 321–334.

    PubMed  CAS  Google Scholar 

  • Zuo, X., Guo, W., and Lipschutz, J.H. (2009). The exocyst protein Sec10 is necessary for primary ciliogenesis and cystogenesis in vitro. Mol. Biol. Cell 20, 2522–2529.

    PubMed  CAS  Google Scholar 

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  1. Department of Biology and National Center for Behavioral Genomics, Brandeis University, Waltham, MA, 02454, USA

    Inna V. Nechipurenko, David B. Doroquez & Piali Sengupta

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Nechipurenko, I.V., Doroquez, D.B. & Sengupta, P. Primary cilia and dendritic spines: Different but similar signaling compartments. Mol Cells 36, 288–303 (2013). https://doi.org/10.1007/s10059-013-0246-z

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