Tenascin-R promotes assembly of the extracellular matrix of perineuronal nets via clustering of aggrecan

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 369, Issue 1654, 2014, Pages

  Morawski, Markus ^a   Dityatev, Alexander ^b,c,d   Hartlage Rübsamen, Maike ^a   Blosa, Maren ^a   Holzer, Max ^a   Flach, Katharina ^a   Pavlica, Sanja ^a   Dityateva, Galina ^b,c   Brückner, Gert ^a   Schachner, Melitta ^b,e,f  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^d GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^e SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

^f RUTGERS UNIVERSITY   (United States)

Author keywords

Aggregation; Chondroitin sulfate proteoglycans; Inhibitory interneurons; Synaptic; Synaptogenesis

Indexed keywords

AGGREGATION; CLUSTER ANALYSIS; HISTOLOGY; INHIBITOR; MATRIX; NEUROLOGY; PROTEIN; RODENT; STABILIZATION; SULFATE;

AGGRECAN; TENASCIN; TENASCIN R;

ANIMAL; CULTURE TECHNIQUE; EXTRACELLULAR MATRIX; GENETICS; KNOCKOUT MOUSE; METABOLISM; MOUSE; OLIGODENDROGLIA; PHYSIOLOGY;

AGGRECANS; ANIMALS; CELL CULTURE TECHNIQUES; EXTRACELLULAR MATRIX; MICE; MICE, KNOCKOUT; OLIGODENDROGLIA; TENASCIN;

EID: 84907192647     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2014.0046     Document Type: Article

References (47)

1. Brückner G, Grosche J. 2001 Perineuronal nets show intrinsic patterns of extracellular matrix differentiation in organotypic slice cultures. Exp. Brain Res. 137, 83-93. (doi:10.1007/s002210000617)
2. Berghuis P et al. 2004 Brain-derived neurotrophic factor controls functional differentiation and microcircuit formation of selectively isolated fastspiking GABAergic interneurons. Eur. J. Neurosci. 20, 1290-1306. (doi:10.1111/j.1460-9568.2004. 03561.x)
3. John N, Krugel H, Frischknecht R, Smalla K-H, Schultz C, Kreutz M, Gundelfinger E, Seidenbecher C. 2006 Brevican-containing perineuronal nets of extracellular matrix in dissociated hippocampal primary cultures. Mol. Cell. Neurosci. 31, 774-784. (doi:10.1016/j.mcn. 2006.01.011)
4. Dityatev A, Brückner G, Dityateva G, Grosche J, Kleene R, Schachner M. 2007 Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Dev. Neurobiol. 67, 570-588. (doi:10.1002/dneu.20361)
5. Giamanco KA, Morawski M, Matthews RT. 2010 Perineuronal net formation and structure in aggrecan knockout mice. Neuroscience 170, 1314-1327. (doi:10.1016/j.neuroscience.2010.08.032)
6. Lander C, Zhang H, Hockfield S. 1998 Neurons produce a neuronal cell surface-associated chondroitin sulfate proteoglycan. J. Neurosci. 18, 174-183.
7. Matthews R, Kelly G, Zerillo C, Gray G, Tiemeyer M, Hockfield S. 2002 Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J. Neurosci. 22, 7536-7547.
8. Seidenbecher C, Smalla K-H, Fischer N, Gundelfinger E, Kreutz M. 2002 Brevican isoforms associate with neural membranes. J. Neurochem. 83, 738-746. (doi:10.1046/j.1471-4159.2002.01183.x)
9. Yamaguchi Y. 2000 Lecticans: organizers of the brain extracellular matrix. Cell. Mol. Life Sci. 57, 276-289. (doi:10.1007/PL00000690)
10. Guimaraes A, Zaremba S, Hockfield S. 1990 Molecular and morphological changes in the cat lateral geniculate nucleus and visual cortex induced by visual deprivation are revealed by monoclonal antibodies Cat-304 and Cat-301. J. Neurosci. 10, 3014-3024.
11. Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett J, Maffei L. 2002 Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298, 1248-1251. (doi:10.1126/science.1072699)
12. Brückner G, Morawski M, Arendt T. 2008 Aggrecanbased extracellular matrix is an integral part of the human basal ganglia circuit. Neuroscience 151, 489-504. (doi:10.1016/j.neuroscience.2007.10.033)
13. Morawski M, Brückner G, Jäger C, Seeger G, Künzle H, Arendt T. 2010 Aggrecan-based extracellular matrix shows unique cortical features and conserved subcortical principles of mammalian brain organization in the Madagascan lesser hedgehog tenrec (Echinops telfairi Martin, 1838). Neuroscience 165, 831-849. (doi:10.1016/j.neuroscience.2009. 08.018)
14. Blosa M, Sonntag M, Bruckner G, Jager C, Seeger G, Matthews RT, Rubsamen R, Arendt T, Morawski M. 2013 Unique features of extracellular matrix in the mouse medial nucleus of trapezoid bodyimplications for physiological functions. Neuroscience 228, 215-234. (doi:10.1016/j. neuroscience.2012.10.003)
15. Brückner G, Grosche J, Hartlage-Rubsamen M, Schmidt S, Schachner M. 2003 Region and laminaspecific distribution of extracellular matrix proteoglycans, hyaluronan and tenascin-R in the mouse hippocampal formation. J. Chem. Neuroanat. 26, 37-50. (doi:10.1016/S0891-0618(03)00036-X)
16. Aspberg A, Miura R, Bourdoulous S, Shimonaka M, Heinegard D, Schachner M, Ruoslahti E, Yamaguchi Y. 1997 The C-type lectin domains of lecticans, a family of aggregating chondroitin sulfate proteoglycans, bind tenascin-R by protein-protein interactions independent of carbohydrate moiety. Proc. Natl Acad. Sci. USA 94, 10116-10121. (doi:10.1073/pnas.94. 19.10116)
17. Chiquet-Ehrismann R, Tucker RP. 2011 Tenascins and the importance of adhesion modulation. Cold Spring Harb. Perspect. Biol. 3, 1-19. (doi:10.1101/ cshperspect.a004960)
18. Weber P et al. 1999 Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J. Neurosci. 19, 4245-4262.
19. Brückner G, Grosche J, Schmidt S, Hartig W, Margolis RU, Delpech B, Seidenbecher C., Czaniera R, Schachner M. 2000 Postnatal development of perineuronal nets in wild-type mice and in a mutant deficient in tenascin-R. J. Comp. Neurol. 428, 616-629. (doi:10.1002/1096-9861(20001225) 428:4,616::AID-CNE3.3.0.CO;2-K)
20. Zhou XH et al. 2001 Neurocan is dispensable for brain development. Mol. Cell Biol. 21, 5970-5978. (doi:10.1128/MCB.21.17.5970-5978.2001)
21. Brakebusch C et al. 2002 Brevican-deficient mice display impaired hippocampal CA1 long-term potentiation but show no obvious deficits in learning and memory. Mol. Cell. Biol. 22, 7417-7427. (doi:10.1128/MCB.22.21.7417-7427.2002)
22. Hockfield S, Kalb RG, Zaremba S, Fryer H. 1990 Expression of neural proteoglycans correlates with the acquisition of mature neuronal properties in the mammalian brain. Cold Spring Harb. Symp. Quant. Biol. 55, 505-514. (doi:10.1101/SQB.1990.055. 01.049)
23. Morawski M, Bruckner G, Arendt T, Matthews RT. 2012 Aggrecan: beyond cartilage and into the brain. Int. J. Biochem. Cell Biol. 44, 690-693. (doi:10. 1016/j.biocel.2012.01.010)
24. Brückner G, Kacza J, Grosche J. 2004 Perineuronal nets characterized by vital labelling, confocal and electron microscopy in organotypic slice cultures of rat parietal cortex and hippocampus. J. Mol. Histol. 35, 115-122. (doi:10.1023/B:HIJO.0000023374. 22298.50)
25. Brückner G, Schutz A, Hartig W, Brauer K, Paulke BR, Bigl V. 1994 Projection of non-cholinergic basal forebrain neurons ensheathed with perineuronal nets to rat mesocortex. J. Chem. Neuroanat. 8, 11-18. (doi:10.1016/0891-0618(94)90032-9)
26. Adams I, Brauer K, Arélin C, Härtig W, Fine A, Mäder M, Arendt T, Brückner G. 2001 Perineuronal nets in the rhesus monkey and human basal forebrain including basal ganglia. Neuroscience 108, 285-298. (doi:10.1016/S0306-4522(01)00419-5)
27. Morawski M, Brückner G, Jäger C, Seeger G, Arendt T. 2010 Neurons associated with aggrecan-based perineuronal nets are protected against tau pathology in subcortical regions in Alzheimer’s disease. Neuroscience 169, 1347-1363. (doi:10. 1016/j.neuroscience.2010.05.022)
28. Brückner G, Szeoke S, Pavlica S, Grosche J, Kacza J.2006 Axon initial segment ensheathed by extracellular matrix in perineuronal nets. Neuroscience 138, 365-375. (doi:10.1016/j. neuroscience.2005.11.068)
29. Kurokawa T, Tsuda M, Sugino Y. 1976 Purification and characterization of a lectin from Wistaria floribunda seeds. J. Biol. Chem. 251, 5686-5693.
30. Nikonenko A, Schmidt S, Skibo G, Brückner G, Schachner M. 2003 Tenascin-R-deficient mice show structural alterations of symmetric perisomatic synapses in the CA1 region of the hippocampus. J. Comp. Neurol. 456, 338-349. (doi:10.1002/cne. 10537)
31. Morellini F, Sivukhina E, Stoenica L, Oulianova E, Bukalo O, Jakovcevski I, Dityatev A, Irintchev A, Schachner M. 2010 Improved reversal learning and working memory and enhanced reactivity to novelty in mice with enhanced GABAergic innervation in the dentate gyrus. Cereb. Cortex 20, 2712-2727. (doi:10.1093/cercor/bhq017)
32. Saghatelyan AK, Dityatev A, Schmidt S, Schuster T, Bartsch U, Schachner M. 2001 Reduced perisomatic inhibition, increased excitatory transmission, and impaired long-term potentiation in mice deficient for the extracellular matrix glycoprotein tenascin-R. Mol. Cell. Neurosci. 17, 226-240. (doi:10.1006/ mcne.2000.0922)
33. Saghatelyan AK et al. 2003 Recognition molecule associated carbohydrate inhibits postsynaptic GABA(B) receptors: a mechanism for homeostatic regulation of GABA release in perisomatic synapses. Mol. Cell. Neurosci. 24, 271-282. (doi:10.1016/ S1044-7431(03)00163-5)
34. Zacharias U, Rauch U. 2006 Competition and cooperation between tenascin-R, lecticans and contactin 1 regulate neurite growth and morphology. J. Cell Sci. 119, 3456-3466. (doi:10.1242/jcs.03094)
35. Suttkus A, Rohn S, Jager C, Arendt T, Morawski M. 2012 Neuroprotection against iron-induced cell death by perineuronal nets—an in vivo analysis of oxidative stress. Am. J. Neurodegener. Dis. 1, 122-129.
36. Suttkus A, Rohn S, Weigel S, Löckner P, Arendt T, Morawski M. 2014 Aggrecan, link protein and tenascin-R are essential components of the perineuronal net to protect neurons against ironinduced oxidative stress. Cell Death Dis. 5, e1119. (doi:10.1038/cddis.2014.25)
37. Dityatev A, Seidenbecher C., Schachner M. 2010 Compartmentalization from the outside: the extracellular matrix and functional microdomains in the brain. Trends Neurosci. 33, 503-512. (doi:10. 1016/j.tins.2010.08.003)
38. Wang D, Fawcett J. 2012 The perineuronal net and the control of CNS plasticity. Cell Tissue Res. 349, 147-160. (doi:10.1007/s00441-012-1375-y)
39. Van den Oever MC et al. 2010 Extracellular matrix plasticity and GABAergic inhibition of prefrontal cortex pyramidal cells facilitates relapse to heroin seeking. Neuropsychopharmacology 35, 2120-2133. (doi:10.1038/npp.2010.90)
40. Soleman S, Filippov M, Dityatev A, Fawcett J. 2013 Targeting the neural extracellular matrix in neurological disorders. Neuroscience 253, 194-213. (doi:10.1016/j.neuroscience.2013.08.050)
41. Kähler AK et al. 2011 Candidate gene analysis of the human natural killer-1 carbohydrate pathway and perineuronal nets in schizophrenia: B3GAT2 is associated with disease risk and cortical surface area. Biol. Psychiatry 69, 90-96. (doi:10.1016/j. biopsych.2010.07.035)
42. Stoppini L, Buchs PA, Muller D. 1991 A simple method for organotypic cultures of nervous tissue. J. Neurosci. Methods 37, 173-182. (doi:10.1016/ 9 0165-0270(91)90128-M)
43. Lohmann C, Ilic V, Friauf E. 1998 Development of a topographically organized auditory network in slice culture is calcium dependent. J. Neurobiol. 34, 97-112. (doi:10.1002/(SICI)1097-4695(19980205) 34:2,97::AID-NEU1.3.0.CO;2-6)
44. Nörenberg U, Hubert M, Brümmendorf T, Tárnok A, Rathjen FG. 1995 Characterization of functional domains of the tenascin-R (restrictin) polypeptide: cell attachment site, binding with F11, and enhancement of F11-mediated neurite outgrowth by tenascin-R. J. Cell Biol. 130, 473-484. (doi:10. 1083/jcb.130.2.473)
45. Faissner A, Kruse J. 1990 J1/tenascin is a repulsive substrate for central nervous system neurons. Neuron 5, 627-637. (doi:10.1016/0896-6273(90)90217-4)
46. Rigato F, Garwood J, Calco V, Heck N, Faivre-Sarrailh C, Faissner A. 2002 Tenascin-C promotes neurite outgrowth of embryonic hippocampal neurons through the alternatively spliced fibronectin type III BD domains via activation of the cell adhesion molecule F3/contactin. J. Neurosci. 22, 6596-6609.
47. Zacharias U, Leuschner R, Nörenberg U, Rathjen FG. 2002 Tenascin-R induces actin-rich microprocesses and branches along neurite shafts. Mol. Cell. Neurosci. 21, 626-633. (doi:10.1006/mcne. 2002.1203)