Hostname: page-component-848d4c4894-xfwgj Total loading time: 0 Render date: 2024-06-30T06:07:46.293Z Has data issue: false hasContentIssue false
  • English
  • Français

N-methyl-d-aspartate receptor independent changes in expression of polysialic acid-neural cell adhesion molecule despite blockade of homosynaptic long-term potentiation and heterosynaptic long-term depression in the awake freely behaving rat dentate gyrus

Published online by Cambridge University Press:  13 August 2009

Jose J. Rodríguez ,
Glenn M. Dallérac ,
Masashi Tabuchi ,
Heather A. Davies ,
Frances M. Colyer ,
Michael G. Stewart  and
Valérie Doyère
Jose J. Rodríguez*
Affiliation:
Faculty of Life Sciences, The University of Manchester, Manchester, UK Institute of Experimental Medicine, ASCR, Prague, Czech Republic
Glenn M. Dallérac
Affiliation:
NAMC, CNRS-UMR8620, Université Paris-Sud, Orsay, France
Masashi Tabuchi
Affiliation:
Faculty of Life Sciences, The University of Manchester, Manchester, UK
Heather A. Davies
Affiliation:
Department of Life Sciences, The Open University, Milton Keynes, UK
Frances M. Colyer
Affiliation:
Department of Life Sciences, The Open University, Milton Keynes, UK
Michael G. Stewart
Affiliation:
Department of Life Sciences, The Open University, Milton Keynes, UK
Valérie Doyère*
Affiliation:
NAMC, CNRS-UMR8620, Université Paris-Sud, Orsay, France
*
Correspondence should be addressed to: V. Doyère, CNRS-UMR8620, NAMC, Université Paris-Sud, Bat. 446, 91405 Orsay, France phone: +33 (0)169 154 987 email: valerie.doyere@u-psud.fr; J. J. Rodríguez, Faculty of Life Sciences, The University of Manchester, AV Hill Building, Room 2.002, Oxford Road, Manchester M13 9PT, UK phone: +44 (0)161 275 7324 email: Jose.Rodriguez-arellano@manchester.ac.uk
Correspondence should be addressed to: V. Doyère, CNRS-UMR8620, NAMC, Université Paris-Sud, Bat. 446, 91405 Orsay, France phone: +33 (0)169 154 987 email: valerie.doyere@u-psud.fr; J. J. Rodríguez, Faculty of Life Sciences, The University of Manchester, AV Hill Building, Room 2.002, Oxford Road, Manchester M13 9PT, UK phone: +44 (0)161 275 7324 email: Jose.Rodriguez-arellano@manchester.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

Investigations examining the role of polysialic acid (PSA) on the neural cell adhesion molecule (NCAM) in synaptic plasticity have yielded inconsistent data. Here, we addressed this issue by determining whether homosynaptic long-term potentiation (LTP) and heterosynaptic long-term depression (LTD) induce changes in the distribution of PSA-NCAM in the dentate gyrus (DG) of rats in vivo. In addition, we also examined whether the observed modifications were initiated via the activation of N-methyl-d-aspartate (NMDA) receptors. Immunocytochemical analysis showed an increase in PSA-NCAM positive cells both at 2 and 24 h following high-frequency stimulation of either medial or lateral perforant paths, leading to homosynaptic LTP and heterosynaptic LTD, respectively, in the medial molecular layer of the DG. Analysis of sub-cellular distribution of PSA-NCAM by electron microscopy showed decreased PSA dendritic labelling in LTD rats and a sub-cellular relocation towards the spines in LTP rats. Importantly, these modifications were found to be independent of the activation of NMDA receptors. Our findings suggest that strong activation of the granule cells up-regulates PSA-NCAM synthesis which then incorporates into activated synapses, representing NMDA-independent plastic processes that act synergistically on LTP/LTD mechanisms without participating in their expression.

Keywords

Adhesion moleculeshippocampussynaptic plasticity
Type
Research Article
Information
Neuron Glia Biology , Volume 4 , Special Issue 3: Cell Adhesion and Extracellular Matrix Molecules in Synaptic Plasticity , August 2008 , pp. 169 - 178
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abraham, W.C., Logan, B., Wolff, A. and Benuskova, L. (2007) “Heterosynaptic” LTD in the dentate gyrus of anesthetized rat requires homosynaptic activity. Journal of Neurophysiology 98, 1048–1051.CrossRefGoogle ScholarPubMed
Abraham, W.C. and McNaughton, N. (1984) Differences in synaptic transmission between medial and lateral components of the perforant path. Brain Research 303, 251–260.CrossRefGoogle ScholarPubMed
Angata, K. and Fukuda, M. (2003) Polysialyltransferases: major players in polysialic acid synthesis on the neural cell adhesion molecule. Biochimie 85, 195–206.CrossRefGoogle ScholarPubMed
Arami, S., Jucker, M., Schachner, M. and Welzl, H. (1996) The effect of continuous intraventricular infusion of L1 and NCAM antibodies on spatial learning in rats. Behavioural Brain Research 81, 81–87.CrossRefGoogle ScholarPubMed
Becker, C.G., Artola, A., Gerardy-Schahn, R., Becker, T., Welzl, H. and Schachner, M. (1996) The polysialic acid modification of the neural cell adhesion molecule is involved in spatial learning and hippocampal long-term potentiation. Journal of Neuroscience Research 45, 143–152.3.0.CO;2-A>CrossRefGoogle ScholarPubMed
Bouzioukh, F., Tell, F., Jean, A. and Rougon, G. (2001) NMDA receptor and nitric oxide synthase activation regulate polysialylated neural cell adhesion molecule expression in adult brainstem synapses. Journal of Neuroscience 21, 4721–4730.CrossRefGoogle ScholarPubMed
Bruses, J.L., Oka, S. and Rutishauser, U. (1995) NCAM-associated polysialic acid on ciliary ganglion neurons is regulated by polysialytransferase levels and interaction with muscle. Journal of Neuroscience 15, 8310–8319.CrossRefGoogle ScholarPubMed
Bruses, J.L. and Rutishauser, U. (1998) Regulation of neural cell adhesion molecule polysialylation: evidence for nontranscriptional control and sensitivity to an intracellular pool of calcium. Journal of Cell Biology 140, 1177–1186.CrossRefGoogle Scholar
Chan, J., Aoki, C. and Pickel, V.M. (1990) Optimization of differential immunogold-silver and peroxidase labelling with maintenance of ultrastructure in brain sections before plastic embedding. Journal of Neuroscience Methods 33, 113–127.CrossRefGoogle ScholarPubMed
Deisseroth, K., Bito, H. and Tsien, R.W. (1996) Signaling from synapse to nucleus: postsynaptic CREB phosphorylation during multiple forms of hippocampal synaptic plasticity. Neuron 16, 89–101.CrossRefGoogle ScholarPubMed
Dityatev, A., Dityateva, G. and Schachner, M. (2000) Synaptic strength as a function of post- versus presynaptic expression of the neural cell adhesion molecule NCAM. Neuron 26, 207–217.CrossRefGoogle ScholarPubMed
Doyere, V., Srebro, B. and Laroche, S. (1997) Heterosynaptic LTD and depotentiation in the medial perforant path of the dentate gyrus in the freely moving rat. Journal of Neurophysiology 77, 571–578.CrossRefGoogle ScholarPubMed
Eckhardt, M., Bukalo, O., Chazal, G., Wang, L., Goridis, C., Schachner, M. et al. (2000) Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. Journal of Neuroscience 20, 5234–5244.CrossRefGoogle ScholarPubMed
Eyre, M.D., Richter-Levin, G., Avital, A. and Stewart, M.G. (2003) Morphological changes in hippocampal dentate gyrus synapses following spatial learning in rats are transient. European Journal of Neuroscience 17, 1973–1980.CrossRefGoogle ScholarPubMed
Florian, C., Foltz, J., Norreel, J.C., Rougon, G. and Roullet, P. (2006) Post-training intrahippocampal injection of synthetic poly-alpha-2,8-sialic acid-neural cell adhesion molecule mimetic peptide improves spatial long-term performance in mice. Learning & Memory 13, 335–341.CrossRefGoogle ScholarPubMed
Foley, A.G., Hedigan, K., Roullet, P., Moricard, Y., Murphy, K.J., Sara, S.J. et al. (2003) Consolidation of memory for odour-reward association requires transient polysialylation of the neural cell adhesion molecule in the rat hippocampal dentate gyrus. Journal of Neuroscience Research 74, 570–576.CrossRefGoogle ScholarPubMed
Fox, G.B., O'Connell, A.W., Murphy, K.J. and Regan, C.M. (1995) Memory consolidation induces a transient and time-dependent increase in the frequency of neural cell adhesion molecule polysialylated cells in the adult rat hippocampus. Journal of Neurochemistry 65, 2796–2799.CrossRefGoogle ScholarPubMed
Fux, C.M., Krug, M., Dityatev, A., Schuster, T. and Schachner, M. (2003) NCAM180 and glutamate receptor subtypes in potentiated spine synapses: an immunogold electron microscopic study. Molecular and Cellular Neurosciences 24, 939–950.CrossRefGoogle ScholarPubMed
Gascon, E., Vutskits, L. and Kiss, J.Z. (2007) Polysialic acid-neural cell adhesion molecule in brain plasticity: from synapses to integration of new neurons. Brain Research and Reviews 56, 101–118.CrossRefGoogle ScholarPubMed
Hammond, M.S., Sims, C., Parameshwaran, K., Suppiramaniam, V., Schachner, M. and Dityatev, A. (2006) Neural cell adhesion molecule-associated polysialic acid inhibits NR2B-containing N-methyl-d-aspartate receptors and prevents glutamate-induced cell death. Journal of Biological Chemistry 281, 34859–34869.CrossRefGoogle ScholarPubMed
Hardingham, G.E., Arnold, F.J. and Bading, H. (2001) Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nature Neuroscience 4, 261–267.CrossRefGoogle ScholarPubMed
Hsu, S.M., Raine, L. and Fanger, H. (1981) The use of antiavidin antibody and avidin-biotin-peroxidase complex in immunoperoxidase technics. American Journal of Clinical Pathology 75, 816–821.CrossRefGoogle ScholarPubMed
Kiss, J.Z. and Muller, D. (2001) Contribution of the neural cell adhesion molecule to neuronal and synaptic plasticity. Reviews in the Neurosciences 12, 297–310.CrossRefGoogle ScholarPubMed
Lopez-Fernandez, M.A., Montaron, M.F., Varea, E., Rougon, G., Venero, C., Abrous, D.N. et al. (2007) Upregulation of polysialylated neural cell adhesion molecule in the dorsal hippocampus after contextual fear conditioning is involved in long-term memory formation. Journal of Neuroscience 27, 4552–4561.CrossRefGoogle ScholarPubMed
Markram, K., Gerardy-Schahn, R. and Sandi, C. (2007) Selective learning and memory impairments in mice deficient for polysialylated NCAM in adulthood. Neuroscience 144, 788–796.CrossRefGoogle ScholarPubMed
Mezey, S., Doyere, V., De Souza, I., Harrison, E., Cambon, K., Kendal, C.E. et al. (2004) Long-term synaptic morphometry changes after induction of long-term potentiation and long-term depression in the dentate gyrus of awake rats are not simply mirror phenomena. European Journal of Neuroscience 19, 2310–2318.CrossRefGoogle Scholar
Mikkonen, M., Soininen, H., Tapiola, T., Alafuzoff, I. and Miettinen, R. (1999) Hippocampal plasticity in Alzheimer's disease: changes in highly polysialylated NCAM immunoreactivity in the hippocampal formation. European Journal of Neuroscience 11, 1754–1764.CrossRefGoogle ScholarPubMed
Mileusnic, R., Lancashire, C. and Rose, S.P. (1999) Sequence-specific impairment of memory formation by NCAM antisense oligonucleotides. Learning & Memory 6, 120–127.CrossRefGoogle ScholarPubMed
Miranda, R., Blanco, E., Begega, A., Santin, L.J. and Arias, J.L. (2006) Reversible changes in hippocampal CA1 synapses associated with water maze training in rats. Synapse 59, 177–181.CrossRefGoogle ScholarPubMed
Muller, D., Wang, C., Skibo, G., Toni, N., Cremer, H., Calaora, V. et al. (1996) PSA-NCAM is required for activity-induced synaptic plasticity. Neuron 17, 413–422.CrossRefGoogle ScholarPubMed
Nacher, J., Blasco-Ibanez, J.M. and McEwen, B.S. (2002) Non-granule PSA-NCAM immunoreactive neurons in the rat hippocampus. Brain Research 930, 1–11.CrossRefGoogle ScholarPubMed
Nacher, J., Rosell, D.R., Alonso-Llosa, G. and McEwen, B.S. (2001) NMDA receptor antagonist treatment induces a long-lasting increase in the number of proliferating cells, PSA-NCAM-immunoreactive granule neurons and radial glia in the adult rat dentate gyrus. European Journal of Neuroscience 13, 512–520.CrossRefGoogle ScholarPubMed
Nakagawa, S., Kim, J.E., Lee, R., Chen, J., Fujioka, T., Malberg, J. et al. (2002) Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. Journal of Neuroscience 22, 9868–9876.CrossRefGoogle ScholarPubMed
Nixon, K., Kim, D.H., Potts, E.N., He, J. and Crews, F.T. (2008) Distinct cell proliferation events during abstinence after alcohol dependence: microglia proliferation precedes neurogenesis. Neurobiology of Disease 31, 218–229.CrossRefGoogle ScholarPubMed
Paxinos, G. and Watson, C. (1998) The Rat Nervous System. New York: Academic Press, Spiral Bound.Google Scholar
Peters, A., Palay, S.L. and Webster, H.D. (1991) The Fine Structure of the Nervous System. 3rd ed.New York: Oxford University Press.Google Scholar
Pickel, V.M., Johnson, E., Carson, M. and Chan, J. (1992) Ultrastructure of spared dopamine terminals in caudate-putamen nuclei of adult rats neonatally treated with intranigral 6-hydroxydopamine. Developmental Brain Research 70, 75–86.CrossRefGoogle ScholarPubMed
Platano, D., Fattoretti, P., Balietti, M., Giorgetti, B., Casoli, T., Di Stefano, G. et al. (2008) Synaptic remodeling in hippocampal CA1 region of aged rats correlates with better memory performance in passive avoidance test. Rejuvenation Research 11, 341–348.CrossRefGoogle ScholarPubMed
Reynolds, E.S. (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Journal of Cell Biology 17, 208.CrossRefGoogle ScholarPubMed
Rougon, G. (1993) Structure, metabolism and cell biology of polysialic acids. European Journal of Cell Biology 61, 197–207.Google ScholarPubMed
Roullet, P., Mileusnic, R., Rose, S.P. and Sara, S.J. (1997) Neural cell adhesion molecules play a role in rat memory formation in appetitive as well as aversive tasks. Neuroreport 8, 1907–1911.CrossRefGoogle ScholarPubMed
Rutishauser, U. (2008) Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nature Reviews. Neuroscience 9, 26–35.CrossRefGoogle ScholarPubMed
Rutishauser, U. and Landmesser, L. (1996) Polysialic acid in the vertebrate nervous system: a promoter of plasticity in cell-cell interactions. Trends in Neurosciences 19, 422–427.CrossRefGoogle ScholarPubMed
Schachner, M. (1997) Neural recognition molecules and synaptic plasticity. Current Opinion in Cell Biology 9, 627–634.CrossRefGoogle ScholarPubMed
Schuster, T., Krug, M., Hassan, H. and Schachner, M. (1998) Increase in proportion of hippocampal spine synapses expressing neural cell adhesion molecule NCAM180 following long-term potentation. Journal of Neurobiology 37, 359–372.3.0.CO;2-4>CrossRefGoogle Scholar
Schuster, T., Krug, M., Stalder, M., Hackel, N., Gerardy-Schahn, R. and Schachner, M. (2001) Immunoelectron microscopic localization of the neural recognition molecules L1, NCAM, and its isoform NCAM180, the NCAM-associated polysialic acid, beta1 integrin and the extracellular matrix molecule tenascin-R in synapses of the adult rat hippocampus. Journal of Neurobiology 49, 142–158.CrossRefGoogle ScholarPubMed
Seki, T. and Arai, Y. (1993) Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neuroscience Research 17, 265–290.CrossRefGoogle ScholarPubMed
Sheng, M., Thompson, M.A. and Greenberg, M.E. (1991) CREB: a Ca(2+)-regulated transcription factor phosphorylated by calmodulin-dependent kinases. Science 252, 1427–1430.CrossRefGoogle Scholar
Singh, J. and Kaur, G. (2007) Transcriptional regulation of polysialylated neural cell adhesion molecule expression by NMDA receptor activation in retinoic acid-differentiated SH-SY5Y neuroblastoma cultures. Brain Research 1154, 8–21.CrossRefGoogle ScholarPubMed
Stewart, M.G., Medvedev, N.I., Popov, V.I., Schoepfer, R., Davies, H.A., Murphy, K. et al. (2005) Chemically induced long-term potentiation increases the number of perforated and complex postsynaptic densities but does not alter dendritic spine volume in CA1 of adult mouse hippocampal slices. European Journal of Neuroscience 21, 3368–3378.CrossRefGoogle Scholar
Stoenica, L., Senkov, O., Gerardy-Schahn, R., Weinhold, B., Schachner, M. and Dityatev, A. (2006) In vivo synaptic plasticity in the dentate gyrus of mice deficient in the neural cell adhesion molecule NCAM or its polysialic acid. European Journal of Neuroscience 23, 2255–2264.CrossRefGoogle ScholarPubMed
Vaithianathan, T., Matthias, K., Bahr, B., Schachner, M., Suppiramaniam, V., Dityatev, A. et al. (2004) Neural cell adhesion molecule-associated polysialic acid potentiates alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor currents. Journal of Biological Chemistry 279, 47975–47984.CrossRefGoogle ScholarPubMed
Venero, C., Herrero, A.I., Touyarot, K., Cambon, K., Lopez-Fernandez, M.A., Berezin, V. et al. (2006) Hippocampal up-regulation of NCAM expression and polysialylation plays a key role on spatial memory. European Journal of Neuroscience 23, 1585–1595.CrossRefGoogle Scholar
Wang, C., Pralong, W.F., Schulz, M.F., Rougon, G., Aubry, J.M., Pagliusi, S. et al. (1996) Functional N-methyl-D-aspartate receptors in O-2A glial precursor cells: a critical role in regulating polysialic acid-neural cell adhesion molecule expression and cell migration. Journal of Cell Biology 135, 1565–1581.CrossRefGoogle Scholar