Advertisement

Brain Structure and Function

, Volume 224, Issue 2, pp 521–532 | Cite as

A possible postsynaptic role for SNAP-25 in hippocampal synapses

  • S. Hussain
  • H. Ringsevjen
  • M. Schupp
  • Ø. Hvalby
  • J. B. Sørensen
  • V. Jensen
  • S. DavangerEmail author
Original Article
  • 169 Downloads

Abstract

The SNARE protein SNAP-25 is well documented as regulator of presynaptic vesicle exocytosis. Increasing evidence suggests roles for SNARE proteins in postsynaptic trafficking of glutamate receptors as a basic mechanism in synaptic plasticity. Despite these indications, detailed quantitative subsynaptic localization studies of SNAP-25 have never been performed. Here, we provide novel electron microscopic data of SNAP-25 localization in postsynaptic spines. In addition to its expected presynaptic localization, we show that the protein is also present in the postsynaptic density (PSD), the postsynaptic lateral membrane and on small vesicles in the postsynaptic cytoplasm. We further investigated possible changes in synaptic SNAP-25 protein expression after hippocampal long-term potentiation (LTP). Quantitative analysis of immunogold-labeled electron microscopy sections did not show statistically significant changes of SNAP-25 gold particle densities 1 h after LTP induction, indicating that local trafficking of SNAP-25 does not play a role in the early phases of LTP. However, the strong expression of SNAP-25 in postsynaptic plasma membranes suggests a function of the protein in postsynaptic vesicle exocytosis and a possible role in hippocampal synaptic plasticity.

Keywords

SNARE proteins Electron microscopy LTP Synaptic plasticity Hippocampus 

Notes

Acknowledgements

We thank Karen Marie Gujord, Jorunn Knutsen, Bjørg Riber, Johannes Helm and Bashir Hakim for their expert technical assistance. We thank Finn-Mogens S. Haug for assistance with immunogold quantification and statistics. The University of Oslo, and the European Union Projects QLG3-CT-2001-02089 (KARTRAP) and LSCHM-CT-2005-005320 (GRIPANNT) supported this work. The authors declare that they have no competing interests.

Compliance with ethical standards

Ethical approval

Experimental protocols were approved by the Institutional Animal Care and Use Committee and conform to National Institutes of Health guidelines for the care and use of animals, as well as international laws on protection of laboratory animals, with the approval of a local bioethical committee and under the supervision of a veterinary commission for animal care and comfort of the University of Oslo and the University of Copenhagen. The animals were treated in accordance with the guidelines of the Norwegian Committees and Danish Animal Health Inspectorate on Animal Experimentation (Norwegian/Danish Animal Welfare Act and European Communities Council, Directive of 24 November 1986–86/609/EEC). Every effort was made to minimize the number of animals used and their sufferings. This article does not contain any studies with human participants performed by any of the authors.

References

  1. Bark IC, Wilson MC (1994) Human cDNA clones encoding two different isoforms of the nerve terminal protein SNAP-25. Gene 139(2):291–292Google Scholar
  2. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232(2):331–356Google Scholar
  3. Bronk P, Deak F, Wilson MC, Liu X, Sudhof TC, Kavalali ET (2007) Differential effects of SNAP-25 deletion on Ca2+—dependent and Ca2+—independent neurotransmission. J Neurophysiol 98(2):794–806.  https://doi.org/10.1152/jn.00226.2007 Google Scholar
  4. Chen YA, Scheller RH (2001) SNARE-mediated membrane fusion. Nat Rev Mol Cell Biol 2(2):98–106.  https://doi.org/10.1038/35052017 Google Scholar
  5. Delgado-Martinez I, Nehring RB, Sorensen JB (2007) Differential abilities of SNAP-25 homologs to support neuronal function. J Neurosci 27(35):9380–9391.  https://doi.org/10.1523/JNEUROSCI.5092-06.2007 Google Scholar
  6. Duc C, Catsicas S (1995) Ultrastructural localization of SNAP-25 within the rat spinal cord and peripheral nervous system. J Comp Neurol 356(1):152–163.  https://doi.org/10.1002/cne.903560111 Google Scholar
  7. Fossati G, Morini R, Corradini I, Antonucci F, Trepte P, Edry E, Sharma V, Papale A, Pozzi D, Defilippi P, Meier JC, Brambilla R, Turco E, Rosenblum K, Wanker EE, Ziv NE, Menna E, Matteoli M (2015) Reduced SNAP-25 increases PSD-95 mobility and impairs spine morphogenesis. Cell Death Differ 22(9):1425–1436.  https://doi.org/10.1038/cdd.2014.227 Google Scholar
  8. Garbelli R, Inverardi F, Medici V, Amadeo A, Verderio C, Matteoli M, Frassoni C (2008) Heterogeneous expression of SNAP-25 in rat and human brain. J Comp Neurol 506(3):373–386.  https://doi.org/10.1002/cne.21505 Google Scholar
  9. Gu Y, Huganir RL (2016) Identification of the SNARE complex mediating the exocytosis of NMDA receptors. Proc Natl Acad Sci USA 113(43):12280–12285.  https://doi.org/10.1073/pnas.1614042113 Google Scholar
  10. Hagiwara A, Fukazawa Y, Deguchi-Tawarada M, Ohtsuka T, Shigemoto R (2005) Differential distribution of release-related proteins in the hippocampal CA3 area as revealed by freeze-fracture replica labeling. J Comp Neurol 489(2):195–216.  https://doi.org/10.1002/cne.20633 Google Scholar
  11. Haglerød C, Kapic A, Boulland JL, Hussain S, Holen T, Skare O, Laake P, Ottersen OP, Haug FM, Davanger S (2009) Protein interacting with C kinase 1 (PICK1) and GluR2 are associated with presynaptic plasma membrane and vesicles in hippocampal excitatory synapses. Neuroscience 158(1):242–252Google Scholar
  12. Hohenstein AC, Roche PA (2001) SNAP-29 is a promiscuous syntaxin-binding SNARE. Biochem Biophys Res Commun 285(2):167–171.  https://doi.org/10.1006/bbrc.2001.5141 Google Scholar
  13. Holderith N, Lorincz A, Katona G, Rozsa B, Kulik A, Watanabe M, Nusser Z (2012) Release probability of hippocampal glutamatergic terminals scales with the size of the active zone. Nat Neurosci 15(7):988–997.  https://doi.org/10.1038/nn.3137 Google Scholar
  14. Holt M, Varoqueaux F, Wiederhold K, Takamori S, Urlaub H, Fasshauer D, Jahn R (2006) Identification of SNAP-47, a novel Qbc-SNARE with ubiquitous expression. J Biol Chem 281(25):17076–17083.  https://doi.org/10.1074/jbc.M513838200 Google Scholar
  15. Hussain S, Davanger S (2011) The discovery of the soluble N-ethylmaleimide-sensitive factor attachment protein receptor complex and the molecular regulation of synaptic vesicle transmitter release: the 2010 Kavli prize in neuroscience. Neuroscience.  https://doi.org/10.1016/j.neuroscience.2011.05.057 Google Scholar
  16. Hussain S, Davanger S (2015) Postsynaptic VAMP/synaptobrevin facilitates differential vesicle trafficking of GluA1 and GluA2 AMPA receptor subunits. PLoS One 10(10):e0140868.  https://doi.org/10.1371/journal.pone.0140868 Google Scholar
  17. Hussain S, Ringsevjen H, Egbenya DL, Skjervold TL, Davanger S (2016) SNARE protein syntaxin-1 colocalizes closely with NMDA Receptor subunit NR2B in postsynaptic spines in the hippocampus. Front Mol Neurosci 9:10.  https://doi.org/10.3389/fnmol.2016.00010 Google Scholar
  18. Hussain S, Egbenya DL, Lai YC, Dosa ZJ, Sorensen JB, Anderson AE, Davanger S (2017) The calcium sensor synaptotagmin 1 is expressed and regulated in hippocampal postsynaptic spines. Hippocampus.  https://doi.org/10.1002/hipo.22761 Google Scholar
  19. Jurado S, Goswami D, Zhang Y, Molina AJ, Sudhof TC, Malenka RC (2013) LTP requires a unique postsynaptic SNARE fusion machinery. Neuron 77(3):542–558.  https://doi.org/10.1016/j.neuron.2012.11.029 Google Scholar
  20. Kerti K, Lorincz A, Nusser Z (2012) Unique somato-dendritic distribution pattern of Kv4.2 channels on hippocampal CA1 pyramidal cells. Eur J Neurosci 35(1):66–75.  https://doi.org/10.1111/j.1460-9568.2011.07907.x Google Scholar
  21. Lau CG, Takayasu Y, Rodenas-Ruano A, Paternain AV, Lerma J, Bennett MV, Zukin RS (2010) SNAP-25 is a target of protein kinase C phosphorylation critical to NMDA receptor trafficking. J Neurosci 30(1):242–254.  https://doi.org/10.1523/JNEUROSCI.4933-08.2010 Google Scholar
  22. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25:103–126.  https://doi.org/10.1146/annurev.neuro.25.112701.142758 Google Scholar
  23. Mandolesi G, Vanni V, Cesa R, Grasselli G, Puglisi F, Cesare P, Strata P (2009) Distribution of the SNAP25 and SNAP23 synaptosomal-associated protein isoforms in rat cerebellar cortex. Neuroscience 164(3):1084–1096.  https://doi.org/10.1016/j.neuroscience.2009.08.067 Google Scholar
  24. Mathiisen TM, Nagelhus EA, Jouleh B, Torp T, Frydenlund DS, Mylonakou MN, Amiry-Moghaddam M, Covolan L, Utvik JK, Riber B, Gujord KM, Knutsen J, Skare Ø, Laake P, Davanger S, Haug FM, Rinvik E, Ottersen OP (2006) Postembedding immunogold cytochemistry of membrane molecules and amino acid transmitters in the central nervous system. In: Zaborszky L, Wouterlood FG, Lanciego JL (eds) Neuroanatomical tract-tracing 3: molecules, neurons, and systems. Springer, New York, pp 72–108Google Scholar
  25. Megias M, Emri Z, Freund TF, Gulyas AI (2001) Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102(3):527–540Google Scholar
  26. Ravichandran V, Chawla A, Roche PA (1996) Identification of a novel syntaxin- and synaptobrevin/VAMP-binding protein, SNAP-23, expressed in non-neuronal tissues. J Biol Chem 271(23):13300–13303Google Scholar
  27. Risinger C, Blomqvist AG, Lundell I, Lambertsson A, Nassel D, Pieribone VA, Brodin L, Larhammar D (1993) Evolutionary conservation of synaptosome-associated protein 25 kDa (SNAP-25) shown by Drosophila and Torpedo cDNA clones. J Biol Chem 268(32):24408–24414Google Scholar
  28. Roberts LA, Morris BJ, O’Shaughnessy CT (1998) Involvement of two isoforms of SNAP-25 in the expression of long-term potentiation in the rat hippocampus. Neuroreport 9(1):33–36Google Scholar
  29. Sadoul K, Lang J, Montecucco C, Weller U, Regazzi R, Catsicas S, Wollheim CB, Halban PA (1995) SNAP-25 is expressed in islets of Langerhans and is involved in insulin release. J Cell Biol 128(6):1019–1028Google Scholar
  30. Selak S, Paternain AV, Aller MI, Pico E, Rivera R, Lerma J (2009) A role for SNAP25 in internalization of kainate receptors and synaptic plasticity. Neuron 63(3):357–371.  https://doi.org/10.1016/j.neuron.2009.07.017 Google Scholar
  31. Stuchlik A (2014) Dynamic learning and memory, synaptic plasticity and neurogenesis: an update. Front Behav Neurosci 8:106.  https://doi.org/10.3389/fnbeh.2014.00106 Google Scholar
  32. Tafoya LC, Mameli M, Miyashita T, Guzowski JF, Valenzuela CF, Wilson MC (2006) Expression and function of SNAP-25 as a universal SNARE component in GABAergic neurons. J Neurosci 26(30):7826–7838.  https://doi.org/10.1523/JNEUROSCI.1866-06.2006 Google Scholar
  33. Takamori S, Holt M, Stenius K, Lemke EA, Gronborg M, Riedel D, Urlaub H, Schenck S, Brugger B, Ringler P, Muller SA, Rammner B, Grater F, Hub JS, De Groot BL, Mieskes G, Moriyama Y, Klingauf J, Grubmuller H, Heuser J, Wieland F, Jahn R (2006) Molecular anatomy of a trafficking organelle. Cell 127(4):831–846.  https://doi.org/10.1016/j.cell.2006.10.030 Google Scholar
  34. Tao-Cheng JH, Du J, McBain CJ (2000) Snap-25 is polarized to axons and abundant along the axolemma: an immunogold study of intact neurons. J Neurocytol 29(1):67–77Google Scholar
  35. Tomasoni R, Repetto D, Morini R, Elia C, Gardoni F, Di Luca M, Turco E, Defilippi P, Matteoli M (2013) SNAP-25 regulates spine formation through postsynaptic binding to p140Cap. Nat Commun 4:2136.  https://doi.org/10.1038/ncomms3136 Google Scholar
  36. Walch-Solimena C, Blasi J, Edelmann L, Chapman ER, von Mollard GF, Jahn R (1995) The t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling. J Cell Biol 128(4):637–645Google Scholar
  37. Washbourne P, Thompson PM, Carta M, Costa ET, Mathews JR, Lopez-Bendito G, Molnar Z, Becher MW, Valenzuela CF, Partridge LD, Wilson MC (2002) Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci 5(1):19–26.  https://doi.org/10.1038/nn783 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018
Corrected Publication 2018

Authors and Affiliations

  1. 1.Division of Anatomy, Department of Molecular Medicine, Institute of Basic Medical SciencesUniversity of OsloOsloNorway
  2. 2.Division of Physiology, Department of Molecular Medicine, Institute of Basic Medical SciencesUniversity of OsloOsloNorway
  3. 3.Department of Neuroscience, Faculty of Health and Medical SciencesUniversity of CopenhagenCopenhagenDenmark
  4. 4.Laboratory of Synaptic Plasticity, Division of AnatomyInstitute of Basic Medical SciencesOsloNorway

Personalised recommendations