Modulation of network activity and induction of homeostatic synaptic plasticity by enzymatic removal of heparan sulfates

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1654, 2014, Pages

  Korotchenko, Svetlana ^a,b   Cingolani, Lorenzo A ^a   Kuznetsova, Tatiana ^a   Bologna, Luca Leonardo ^c,d,e   Chiappalone, Michela ^a   Dityatev, Alexander ^a,b,f  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b LOBACHEVSKY STATE UNIVERSITY OF NIZHNY NOVGOROD   (Russian Federation)

^c INSERM   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e CNRS   (France)

^f GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

Author keywords

AMPA receptor; Burst; Heparan sulfate proteoglycans; Neural network; Seizure; Synaptic upscaling

Indexed keywords

AMPLITUDE; ARTIFICIAL NEURAL NETWORK; ENZYME ACTIVITY; FREQUENCY ANALYSIS; GENE EXPRESSION; HOMEOSTASIS; MATURATION; MOLECULAR ANALYSIS; PHENOTYPIC PLASTICITY; RODENT; SULFATE;

EID: 84907192429     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0134     Document Type: Article

References (30)

1. Maeda N, Ishii M, Nishimura K, Kamimura K. 2011 Functions of chondroitin sulfate and heparan sulfate in the developing brain. Neurochem. Res. 36, 1228-1240. (doi:10.1007/s11064-010-0324-y)
2. Kirn-Safran C, Farach-Carson MC, Carson DD. 2009 Multifunctionality of extracellular and cell surface heparan sulfate proteoglycans. Cell Mol. Life Sci. 66, 3421-3434. (doi:10.1007/s00018-009-0096-1)
3. Fico A, Maina F, Dono R. 2011 Fine-tuning of cell signaling by glypicans. Cell Mol. Life Sci. 68, 923-929. (doi:10.1007/s00018-007-7471-6)
4. Dityatev A, Dityateva G, Sytnyk V, Delling M, Toni N, Nikonenko I, Muller D, Schachner M. 2004 Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses. J. Neurosci. 24, 9372-9382. (doi:10.1523/JNEUROSCI.1702-04.2004)
5. Allen NJ, Bennett ML, Foo LC, Wang GX, Chakraborty C, Smith SJ, Barres BA. 2012 Astrocyte glypicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors. Nature 486, 410-414. (doi:10.1038/nature11059)
6. Lauri SE, Kaukinen S, Kinnunen T, Ylinen A, Imai S, Kaila K, Taira T, Rauvala H. 1999 Regulatory role and molecular interactions of a cell-surface heparan sulfate proteoglycan (N-syndecan) in hippocampal long-term potentiation. J. Neurosci. 19, 1226-1235.
7. Irie F, Badie-Mahdavi H, Yamaguchi Y. 2012 Autism-like socio-communicative deficits and stereotypies in mice lacking heparan sulfate. Proc. Natl Acad. Sci. USA 109, 5052-5056. (doi:10.1073/ pnas.1117881109)
8. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB. 1998 Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892-896. (doi:10.1038/36103)
9. Dityatev A, Schachner M, Sonderegger P. 2010 The dual role of the extracellular matrix in synaptic plasticity and homeostasis. Nat. Rev. Neurosci. 11, 735-746. (doi:10.1038/nrn2898)
10. Gundelfinger ED, Frischknecht R, Choquet D, Heine M. 2010 Converting juvenile into adult plasticity: a role for the brain’s extracellular matrix. Eur. J. Neurosci. 31, 2156-2165. (doi:10.1111/j.14609568.2010.07253.x)
11. Thalhammer A, Cingolani LA. 2014 Cell adhesion and homeostatic synaptic plasticity. Neuropharmacology 78, 23-30. (doi:10.1016/j. neuropharm.2013.03.015)
12. Cingolani LA, Goda Y. 2008 Differential involvement of beta3 integrin in pre and postsynaptic forms of adaptation to chronic activity deprivation. Neuron Glia Biol. 4, 179-187. (doi:10.1017/S1740925X 0999024X)
13. Groth RD, Lindskog M, Thiagarajan TC, Li L, Tsien RW. 2011 Beta Ca2þ/CaM-dependent kinase type II triggers upregulation of GluA1 to coordinate adaptation to synaptic inactivity in hippocampal neurons. Proc. Natl Acad. Sci. USA 108, 828-833. (doi:10.1073/pnas.1018022108).
14. Coultrap SJ, Bayer KU. 2012 CaMKII regulation in information processing and storage. Trends Neurosci. 35, 607-618. (doi:10.1016/j.tins.2012.05.003)
15. Barria A, Derkach V, Soderling T. 1997 Identification of the Ca2þ/calmodulin-dependent protein kinase II regulatory phosphorylation site in the alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate-type glutamate receptor. J. Biol. Chem. 272, 32 727-32730. (doi:10.1074/jbc.272.52.32727)
16. Levisohn PM. 2007 The autism-epilepsy connection. Epilepsia 48(Suppl. 9), 33-35. (doi:10.1111/j.1528-1167.2007.01399.x)
17. Thiagarajan TC, Lindskog M, Tsien RW. 2005 Adaptation to synaptic inactivity in hippocampal neurons. Neuron 47, 725-737. (doi:10.1016/j. neuron.2005.06.037)
18. Wondolowski J, Dickman D. 2013 Emerging links between homeostatic synaptic plasticity and neurological disease. Front Cell Neurosci. 7, 223. (doi:10.3389/fncel.2013.00223)
19. Kim J, Tsien RW. 2008 Synapse-specific adaptations to inactivity in hippocampal circuits achieve homeostatic gain control while dampening network reverberation. Neuron 58, 925-937. (doi:10.1016/j. neuron.2008.05.009)
20. Valenzuela JC, Heise C, Franken G, Singh J, Schweitzer B, Seidenbecher CI, Frischknecht R. 2014 Hyaluronan-based extracellular matrix under conditions of homeostatic plasticity. Phil. Trans. R. Soc. B 369, 20130606. (doi:10.1098/rstb.2013.0606)
21. Knaus HG, Scheffauer F, Romanin C, Schindler HG, Glossmann H. 1990 Heparin binds with high affinity to voltage-dependent L-type Ca2þ channels. Evidence for an agonistic action. J. Biol. Chem. 265, 11156-11166.
22. Kochlamazashvili G et al. 2010 The extracellular matrix molecule hyaluronic acid regulates hippocampal synaptic plasticity by modulating postsynaptic L-type Ca2þ channels. Neuron 67, 116-128. (doi:10.1016/j.neuron.2010.05.030)
23. Vedunova M, Sakharnova T, Mitroshina E, Perminova M, Pimashkin A, Zakharov Y, Dityatev A, Mukhina I. 2013 Seizure-like activity in hyaluronidase-treated dissociated hippocampal cultures. Front. Cell Neurosci. 7, 149. (doi:10.3389/fncel.2013.00149)
24. Faye C, Moreau C, Chautard E, Jetne R, Fukai N, Ruggiero F, Humphries MJ, Olsen BR, Ricard-Blum S. 2009 Molecular interplay between endostatin, integrins, and heparan sulfate. J. Biol. Chem. 284, 22029-22040. (doi:10.1074/jbc.M109.002840)
25. Menegon A, Verderio C, Leoni C, Benfenati F, Czernik AJ, Greengard P, Matteoli M, Valtorta F. 2002 Spatial and temporal regulation of Ca2þ/ calmodulin-dependent protein kinase II activity in developing neurons. J. Neurosci. 22, 7016-7026.
26. Potter SM, DeMarse TB. 2001 A new approach to neural cell culture for long-term studies. J. Neurosci. Methods 110, 17-24. (doi:10.1016/S0165-0270(01)00412-5)
27. Jiang J, Wu X, Tang H, Luo G. 2013 Apolipoprotein E mediates attachment of clinical hepatitis C virus to hepatocytes by binding to cell surface heparan sulfate proteoglycan receptors. PLoS ONE 8, e67982. (doi:10.1371/journal.pone.0067982)
28. Bologna LL, Pasquale V, Garofalo M, Gandolfo M, Baljon PL, Maccione A, Martinoia S, Chiappalone M. 2010 Investigating neuronal activity by SPYCODE multi-channel data analyzer. Neural Netw. 23, 685-697. (doi:10.1016/j.neunet.2010.05.002)
29. Maccione A, Gandolfo M, Massobrio P, Novellino A, Martinoia S, Chiappalone M. 2009 A novel algorithm for precise identification of spikes in extracellularly recorded neuronal signals. J. Neurosci. Methods 177, 241-249. (doi:10.1016/j.jneumeth.2008.09.026)
30. Pasquale V, Martinoia S, Chiappalone M. 2010 A self-adapting approach for the detection of bursts and network bursts in neuronal cultures. J. Comput. Neurosci. 29, 213-229. (doi:10.1007/s10827-009-0175-1)