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Differential involvement of β3 integrin in pre- and postsynaptic forms of adaptation to chronic activity deprivation

Published online by Cambridge University Press:  16 September 2009

Lorenzo A. Cingolani*
Affiliation:
MRC Laboratory for Molecular Cell Biology and Cell Biology Unit, UCL, Gower Street, WC1E 6BT London, UK
Yukiko Goda*
Affiliation:
MRC Laboratory for Molecular Cell Biology and Cell Biology Unit, UCL, Gower Street, WC1E 6BT London, UK Department of Neuroscience, Physiology and Pharmacology, UCL, Gower Street, WC1E 6BT, London, UK
*
Correspondence should be addressed to: Lorenzo A. Cingolani or Yukiko Goda, MRC Laboratory for Molecular Cell Biology and Cell Biology Unit, UCL, Gower Street, London WC1E 6BT, UK phone: +44 20 76793531 fax: +44 20 76797805 emails: l.cingolani@ucl.ac.uk; y.goda@ucl.ac.uk
Correspondence should be addressed to: Lorenzo A. Cingolani or Yukiko Goda, MRC Laboratory for Molecular Cell Biology and Cell Biology Unit, UCL, Gower Street, London WC1E 6BT, UK phone: +44 20 76793531 fax: +44 20 76797805 emails: l.cingolani@ucl.ac.uk; y.goda@ucl.ac.uk

Abstract

Neuronal networks can adapt to global changes in activity levels through compensatory modifications in pre- and postsynaptic parameters of synaptic transmission. These forms of synaptic plasticity are known as synaptic homeostasis, and are thought to require specific cellular interactions and signaling across the entire neuronal network. However, the molecular mechanisms underlying synaptic homeostasis have so far been investigated mostly in primary cultures of dissociated neurons, a preparation that lacks the specificity of in vivo circuitry. Here, we show that there are critical differences in the properties of synaptic homeostasis between dissociated neuronal cultures and organotypic slices, a preparation that preserves more precisely in vivo connectivity. Moreover, the cell adhesion molecule β3 integrin, which regulates excitatory synaptic strength, is specifically required for a postsynaptic form of synaptic homeostasis called synaptic scaling in both dissociated cultures and organotypic slices. Conversely, another form of synaptic homeostasis that involves changes in presynaptic quantal content occurs independently of β3 integrin. Our findings define the differential involvement of β3 integrin in two forms of synaptic homeostasis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2009

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References

Aoto, J., Nam, C.I., Poon, M.M., Ting, P. and Chen, L. (2008) Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron 60, 308320.Google Scholar
Bausch, S.B., He, S., Petrova, Y., Wang, X.M. and McNamara, J.O. (2006) Plasticity of both excitatory and inhibitory synapses is associated with seizures induced by removal of chronic blockade of activity in cultured hippocampus. Journal of Neurophysiology 96, 21512167.Google Scholar
Bennett, M.R. and Kearns, J.L. (2000) Statistics of transmitter release at nerve terminals. Progress in Neurobiology 60, 545606.Google Scholar
Branco, T., Staras, K., Darcy, K.J. and Goda, Y. (2008) Local dendritic activity sets release probability at hippocampal synapses. Neuron 59, 475485.Google Scholar
Buckby, L.E., Jensen, T.P., Smith, P.J. and Empson, R.M. (2006) Network stability through homeostatic scaling of excitatory and inhibitory synapses following inactivity in CA3 of rat organotypic hippocampal slice cultures. Molecular and Cellular Neurosciences 31, 805816.Google Scholar
Burrone, J., O'Byrne, M. and Murthy, V.N. (2002) Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature 420, 414418.Google Scholar
Chan, C.S., Weeber, E.J., Kurup, S., Sweatt, J.D. and Davis, R.L. (2003) Integrin requirement for hippocampal synaptic plasticity and spatial memory. Journal of Neuroscience 23, 71077116.Google Scholar
Chavis, P. and Westbrook, G. (2001) Integrins mediate functional pre- and postsynaptic maturation at a hippocampal synapse. Nature 411, 317321.Google Scholar
Cingolani, L.A., Thalhammer, A., Yu, L.M., Catalano, M., Ramos, T., Colicos, M.A. et al. (2008) Activity-dependent regulation of synaptic AMPA receptor composition and abundance by beta3 integrins. Neuron 58, 749762.Google Scholar
De Simoni, A., Griesinger, C.B. and Edwards, F.A. (2003) Development of rat CA1 neurones in acute versus organotypic slices: role of experience in synaptic morphology and activity. Journal of Physiology 550, 135147.Google Scholar
Desai, N.S., Cudmore, R.H., Nelson, S.B. and Turrigiano, G.G. (2002) Critical periods for experience-dependent synaptic scaling in visual cortex. Nature Neuroscience 5, 783789.Google Scholar
Echegoyen, J., Neu, A., Graber, K.D. and Soltesz, I. (2007) Homeostatic plasticity studied using in vivo hippocampal activity-blockade: synaptic scaling, intrinsic plasticity and age-dependence. PLoS ONE 2, e700.Google Scholar
Galvan, C.D., Wenzel, J.H., Dineley, K.T., Lam, T.T., Schwartzkroin, P.A., Sweatt, J.D. et al. (2003) Postsynaptic contributions to hippocampal network hyperexcitability induced by chronic activity blockade in vivo. European Journal of Neuroscience 18, 18611872.Google Scholar
Gao, B., Saba, T.M. and Tsan, M.F. (2002) Role of alpha(v)beta(3)-integrin in TNF-alpha-induced endothelial cell migration. American Journal of Physiology. Cell Physiology 283, C1196C1205.Google Scholar
Goel, A., Jiang, B., Xu, L.W., Song, L., Kirkwood, A. and Lee, H.K. (2006) Cross-modal regulation of synaptic AMPA receptors in primary sensory cortices by visual experience. Nature Neuroscience 9, 10011003.Google Scholar
Hodivala-Dilke, K.M., McHugh, K.P., Tsakiris, D.A., Rayburn, H., Crowley, D., Ullman-Cullere, M. et al. (1999) Beta3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. Journal of Clinical Investigation 103, 229238.Google Scholar
Huang, Z., Shimazu, K., Woo, N.H., Zang, K., Muller, U., Lu, B. et al. (2006) Distinct roles of the beta 1-class integrins at the developing and the mature hippocampal excitatory synapse. Journal of Neuroscience 26, 1120811219.Google Scholar
Hynes, R.O. (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110, 673687.Google Scholar
Ibata, K., Sun, Q. and Turrigiano, G.G. (2008) Rapid synaptic scaling induced by changes in postsynaptic firing. Neuron 57, 819826.Google Scholar
Kang, W.S., Choi, J.S., Shin, Y.J., Kim, H.Y., Cha, J.H., Lee, J.Y. et al. (2008) Differential regulation of osteopontin receptors, CD44 and the alpha(v) and beta(3) integrin subunits, in the rat hippocampus following transient forebrain ischemia. Brain Research 1228, 208216.Google Scholar
Karmarkar, U.R. and Buonomano, D.V. (2006) Different forms of homeostatic plasticity are engaged with distinct temporal profiles. European Journal of Neuroscience 23, 15751584.Google Scholar
Kim, J. and Tsien, R.W. (2008) Synapse-specific adaptations to inactivity in hippocampal circuits achieve homeostatic gain control while dampening network reverberation. Neuron 58, 925937.Google Scholar
Kirov, S.A., Goddard, C.A. and Harris, K.M. (2004) Age-dependence in the homeostatic upregulation of hippocampal dendritic spine number during blocked synaptic transmission. Neuropharmacology 47, 640648.Google Scholar
Lauri, S.E., Lamsa, K., Pavlov, I., Riekki, R., Johnson, B.E., Molnar, E. et al. (2003) Activity blockade increases the number of functional synapses in the hippocampus of newborn rats. Molecular and Cell Neurosciences 22, 107117.Google Scholar
Maffei, A., Nataraj, K., Nelson, S.B. and Turrigiano, G.G. (2006) Potentiation of cortical inhibition by visual deprivation. Nature 443, 8184.Google Scholar
Maffei, A., Nelson, S.B. and Turrigiano, G.G. (2004) Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nature Neuroscience 7, 13531359.Google Scholar
Maffei, A. and Turrigiano, G.G. (2008) Multiple modes of network homeostasis in visual cortical layer 2/3. Journal of Neuroscience 28, 43774384.CrossRefGoogle ScholarPubMed
Moulder, K.L., Jiang, X., Taylor, A.A., Olney, J.W. and Mennerick, S. (2006) Physiological activity depresses synaptic function through an effect on vesicle priming. Journal of Neuroscience 26, 66186626.Google Scholar
Moulder, K.L., Meeks, J.P., Shute, A.A., Hamilton, C.K., de Erausquin, G. and Mennerick, S. (2004) Plastic elimination of functional glutamate release sites by depolarization. Neuron 42, 423435.Google Scholar
Murthy, V.N., Schikorski, T., Stevens, C.F. and Zhu, Y. (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32, 673682.Google Scholar
Nishimura, S.L., Boylen, K.P., Einheber, S., Milner, T.A., Ramos, D.M. and Pytela, R. (1998) Synaptic and glial localization of the integrin alphavbeta8 in mouse and rat brain. Brain Research 791, 271282.CrossRefGoogle ScholarPubMed
Okuda, T., Yu, L.M., Cingolani, L.A., Kemler, R. and Goda, Y. (2007) beta-Catenin regulates excitatory postsynaptic strength at hippocampal synapses. Proceedings of the National Academy of Sciences of the U.S.A. 104, 1347913484.Google Scholar
Pinkstaff, J.K., Detterich, J., Lynch, G. and Gall, C. (1999) Integrin subunit gene expression is regionally differentiated in adult brain. Journal of Neuroscience 19, 15411556.Google Scholar
Pinkstaff, J.K., Lynch, G. and Gall, C.M. (1998) Localization and seizure-regulation of integrin beta 1 mRNA in adult rat brain. Brain Research. Molecular Brain Research 55, 265276.Google Scholar
Rabinowitch, I. and Segev, I. (2008) Two opposing plasticity mechanisms pulling a single synapse. Trends in Neuroscience 31, 377383.Google Scholar
Rich, M.M. and Wenner, P. (2007) Sensing and expressing homeostatic synaptic plasticity. Trends in Neuroscience 30, 119125.Google Scholar
Rutherford, L.C., Nelson, S.B. and Turrigiano, G.G. (1998) BDNF has opposite effects on the quantal amplitude of pyramidal neuron and interneuron excitatory synapses. Neuron 21, 521530.Google Scholar
Shi, Y. and Ethell, I.M. (2006) Integrins control dendritic spine plasticity in hippocampal neurons through NMDA receptor and Ca2+/calmodulin-dependent protein kinase II-mediated actin reorganization. Journal of Neuroscience 26, 18131822.Google Scholar
Stellwagen, D. and Malenka, R.C. (2006) Synaptic scaling mediated by glial TNF-alpha. Nature 440, 10541059.CrossRefGoogle ScholarPubMed
Thiagarajan, T.C., Lindskog, M. and Tsien, R.W. (2005) Adaptation to synaptic inactivity in hippocampal neurons. Neuron 47, 725737.CrossRefGoogle ScholarPubMed
Turrigiano, G.G. (2008) The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135, 422435.Google Scholar
Turrigiano, G.G., Leslie, K.R., Desai, N.S., Rutherford, L.C. and Nelson, S.B. (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892896.Google Scholar
Turrigiano, G.G. and Nelson, S.B. (2004) Homeostatic plasticity in the developing nervous system. Nature Reviews Neuroscience 5, 97107.Google Scholar
Tyler, W.J. and Pozzo-Miller, L. (2003) Miniature synaptic transmission and BDNF modulate dendritic spine growth and form in rat CA1 neurones. Journal of Physiology 553, 497509.Google Scholar
Wierenga, C.J., Walsh, M.F. and Turrigiano, G.G. (2006) Temporal regulation of the expression locus of homeostatic plasticity. Journal of Neurophysiology 96, 21272133.Google Scholar