Skip to main content
SpringerLink
Log in

Differential expression of several molecules of the extracellular matrix in functionally and developmentally distinct regions of rat spinal cord

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

We have examined the regional distribution of several chondroitin sulfate proteoglycans (neurocan, brevican, versican, aggrecan, phosphacan), of their glycosaminoglycan moieties, and of tenascin-R in the spinal cord of adult rat. The relationships of these molecules with glial and neuronal populations, identified with appropriate markers, were investigated by using multiple fluorescence labeling combined with confocal microscopy. The results showed that the distribution of the examined molecules was similar at all spinal cord levels but displayed area-specific differences along the dorso-ventral axis, delimiting functionally and developmentally distinct areas. In the gray matter, laminae I and II lacked perineuronal nets (PNNs) of extracellular matrix and contained low levels of chondroitin sulfate glycosaminoglycans (CS-GAGs), brevican, and tenascin-R, possibly favoring the maintenance of local neuroplastic properties. Conversely, CS-GAGs, brevican, and phosphacan were abundant, with numerous thick PNNs, in laminae III-VIII and X. Motor neurons (lamina IX) were surrounded by PNNs that contained all molecules investigated but displayed various amounts of CS-GAGs. Double-labeling experiments showed that the presence of PNNs could not be unequivocally related to specific classes of neurons, such as motor neurons or interneurons identified by their expression of calcium-binding proteins (parvalbumin, calbindin, calretinin). However, a good correlation was found between PNNs rich in CS-GAGs and the neuronal expression of the Kv3.1b subunit of the potassium channel, a marker of fast-firing neurons. This observation confirms the correlation between the electrophysiological properties of these neurons and the specific composition of their microenvironment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Akopians A, Runyan SA, Phelps PE (2003) Expression of L1 decreases during postnatal development of rat spinal cord. J Comp Neurol 467:375–388

    PubMed  CAS  Google Scholar 

  • Amiry-Moghaddam M, Ottersen OP (2003) The molecular basis of water transport in the brain. Nat Rev Neurosci 4:991–1001

    Article  PubMed  CAS  Google Scholar 

  • Angelov DN, Walther M, Streppel M, Guntinas-Lichius O, Neiss WF, Probstmeier R, Pesheva P (1998) Tenascin-R is antiadhesive for activated microglia that induce downregulation of the protein after peripheral nerve injury: a new role in neuronal protection. J Neurosci 18:6218–6229

    PubMed  CAS  Google Scholar 

  • Asher RA, Morgenstern DA, Fidler PS, Adcock KH, Oohira A, Braistead JE, Levine JM, Margolis RU, Rogers JH, Fawcett JW (2000) Neurocan is upregulated in injured brain and in cytokine-treated astrocytes. J Neurosci 20:2427–2438

    PubMed  CAS  Google Scholar 

  • Asher RA, Morgenstern DA, Shearer MC, Adcock KH, Pesheva P, Fawcett JW (2002) Versican is upregulated in CNS injury and is a product of oligodendrocyte lineage cells. J Neurosci 22:2225–2236

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Bandtlow CE, Zimmermann DR (2000) Proteoglycans in the developing brain: new conceptual insights for old proteins. Physiol Rev 80:1267–1290

    PubMed  CAS  Google Scholar 

  • Baranauskas G, Tkatch T, Nagata K, Yeh JZ, Surmeier DJ (2003) Kv3.4 subunits enhance the repolarizing efficiency of Kv3.1 channels in fast-spiking neurons. Nat Neurosci 6:258–266

    PubMed  CAS  Google Scholar 

  • Berardi N, Pizzorusso T, Maffei L (2004) Extracellular matrix and visual cortical plasticity: freeing the synapse. Neuron 44:905–908

    PubMed  CAS  Google Scholar 

  • Bertolotto A, Manzardo E, Guglielmone R (1996) Immunohistochemical mapping of perineuronal nets containing chondroitin unsulfated proteoglycan in the central nervous system. Cell Tissue Res 283:283–295

    PubMed  CAS  Google Scholar 

  • Bignami A, Asher R, Perides G, Rahemtulla F (1992) The extracellular matrix of cerebral gray matter. Golgi’s pericellular net and Nissl’s nervoesen Grau revisited. J Dev Neurosci 10:291–299

    CAS  Google Scholar 

  • Bogen O, Dreger M, Gillen C, Schröder W, Hucho F (2005) Identification of versican as an isolectin B4-binding glycoprotein from mammalian spinal cord tissue. FEBS J 272:1090–1102

    PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    PubMed  CAS  Google Scholar 

  • Brauer K, Werner L, Leibnitz L (1982) Perineuronal nets of glia. J Hirnforsch 23:701–708

    PubMed  CAS  Google Scholar 

  • Brook GA, Schmitt AB, Nacimiento W, Weis J, Schröder JM, Noth J (1998) Distribution of B-50 (GAP-43) mRNA and protein in the normal adult human spinal cord. Acta Neuropathol 9:378–386

    Google Scholar 

  • Brückner G, Brauer K, Härtig W, Wolff JR, Rickmann MJ, Derouiche A, Delpech B, Girard N, Oertel WH, Reichenbach A (1993) Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia 8:183–200

    PubMed  Google Scholar 

  • Brückner G, Bringmann A, Köppe G, Härtig W, Brauer K (1996a) In vivo and in vitro labelling of perineuronal nets in rat brain. Brain Res 720:84–92

    PubMed  Google Scholar 

  • Brückner G, Härtig W, Kacza J, Seeger G, Welt K, Brauer K (1996b) Extracellular matrix organization in various regions of rat brain grey matter. J Neurocytol 25:333–346

    PubMed  Google Scholar 

  • Brückner G, Hausen D, Härtig W, Drlicek M, Arendt T, Brauer K (1999) Cortical areas abundant in extracellular matrix chondroitin sulphate proteoglycans are less affected by cytoskeletal changes in Alzheimer’s disease. Neuroscience 92:791–805

    PubMed  Google Scholar 

  • Brückner G, Grosche J, Schmidt S, Härtig 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

    PubMed  Google Scholar 

  • Brückner G, Grosche J, Hartlage-Rübsamen M, Schmidt S, Schachner M (2003) Region and lamina-specific distribution of extracellular matrix proteoglycans, hyaluronan and tenascin-R in the mouse hippocampal formation. J Chem Neuroanat 26:37–50

    PubMed  Google Scholar 

  • Bukalo O, Schachner M, Dityatev A (2001) Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience 104:359–369

    PubMed  CAS  Google Scholar 

  • Carden MJ, Trojanowski JQ, Schlaerpfer WW, Lee VMY (1987) Two-stage expression of neurofilament polypeptides during rat neurogenesis with early establishment of adult phosphorylation patterns. J Neurosci 7:3489–3504

    PubMed  CAS  Google Scholar 

  • Carr PA, Alvarez FJ, Leman EA, Fyffe REW (1998) Calbindin D28k expression in immunohistochemically identified Renshaw cells. NeuroReport 9:2657–2661

    PubMed  CAS  Google Scholar 

  • Carulli D, Rhodes KE, Brown DJ, Bonnert TP, Pollack SJ, Oliver K, Strata P, Fawcett JW (2006) Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components. J Comp Neurol 494:559–577

    PubMed  CAS  Google Scholar 

  • Caterson B, Christner JE, Baker JR, Couchman JR (1985) Production and characterization of monoclonal antibodies directed against connective tissue proteoglycans. Fed Proc 44:386–393

    PubMed  CAS  Google Scholar 

  • Celio MR, Chiquet-Ehrismann R (1993) “Perineuronal nets” around cortical interneurons expressing parvalbumin are rich in tenascin. Neurosci Lett 162:137–140

    PubMed  CAS  Google Scholar 

  • Celio MR, Blümcke I (1994) Perineuronal nets-A specialized form of extracellular matrix in the adult nervous system. Brain Res Rev 19:128–145

    PubMed  CAS  Google Scholar 

  • Celio MR, Spreafico R, De Biasi S, Vitellaro-Zuccarello L (1998) Perineuronal nets: past and present. Trends Neurosci 21:510–515

    PubMed  CAS  Google Scholar 

  • Coggeshall RE, Reynolds ML, Woolf CJ (1991) Distribution of the growth associated protein GAP-43 in the central processes of axotomized primary afferents in the adult spinal cord; presence of growth cone-like structures. Neurosci Lett 131:37–41

    PubMed  CAS  Google Scholar 

  • Cremer H, Chazal G, Carleton A, Gordis C, Vincent JD, Lledo PMN (1997) NCAM is essential for axonal growth and fasciculation in the hippocampus. Mol Cell Neurosci 8:323–335

    PubMed  CAS  Google Scholar 

  • Cremer H, Chazal G, Lledo PM, Rougon G, Montaron MF, Mayo W, Le Moal M, Abrous DN (2000) PSA-NCAM: an important regulator of hippocampal plasticity. Int J Dev Neurosci 18:213–220

    PubMed  CAS  Google Scholar 

  • Davies JE, Tang X, Denning JW, Archibald SJ, Davies SJA (2004) Decorin suppresses neurocan, brevican, phosphacan and NG2 expression and promotes axon growth across adult rat spinal cord injuries. Eur J Neurosci 19:1226–1242

    PubMed  Google Scholar 

  • Engel M, Maurel P, Margolis RU, Margolis RK (1996) Chondroitin sulfate proteoglycans in the developing central nervous system. I. Cellular sites of synthesis of neurocan and phosphacan. J Comp Neurol 366:34–43

    PubMed  CAS  Google Scholar 

  • Friedlander DR, Milev P, Karthikeyan L, Margolis RK, Margolis RU (1994) The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth. J Cell Biol 125:669–680

    PubMed  CAS  Google Scholar 

  • Garwood J, Heck N, Reichardt F, Faissner A (2003) Phosphacan short isoform, a novel non-proteoglycan variant of phosphacan/receptor protein tyrosine phosphatase-β, interacts with neuronal receptors and promotes neurite outgrowth. J Biol Chem 278:24164–24173

    PubMed  CAS  Google Scholar 

  • Gross MK, Dottori M, Goulding M (2002) Lbx1 specifies somatosensory association interneurons in the dorsal spinal cord. Neuron 34:535–549

    PubMed  CAS  Google Scholar 

  • Haas CA, Rauch U, Thon N, Merten T, Deller T (1999) Entorhinal cortex lesion in adult rats induces the expression of the neuronal chondroitin sulfate proteoglycan neurocan in reactive astrocytes. J Neurosci 19:9953–9963

    PubMed  CAS  Google Scholar 

  • Hagihara K, Miura R, Berglund E, Ranscht B, Yamaguchi Y (1999) Immunohistochemical evidence for the brevican-tenascin-R interaction: colocalization in perineuronal nets suggest a physiological role for the interaction in the adult rat brain. J Comp Neurol 410:256–264

    PubMed  CAS  Google Scholar 

  • Härtig W, Brauer K, Brückner G (1992) Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons. NeuroReport 3:869–872

    Article  PubMed  Google Scholar 

  • Härtig W, Derouiche A, Welt K, Brauer K, Grosche J, Mäder M, Reichenbach A, Brückner G (1999) Cortical neurons immunoreactive for potassium channel Kv3.1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations. Brain Res 842:15–29

    PubMed  Google Scholar 

  • Härtig W, Singer A, Grosche J, Brauer K, Ottersen OP, Brückner G (2001) Perineuronal nets in the rat medial nucleus of the trapezoid body surround neurons immunoreactive for various amino acids, calcium binding proteins and the potassium channel subunit Kv3.1b. Brain Res 899:123–133

    PubMed  Google Scholar 

  • Haunsø A, Celio MR, Margolis RK, Menoud PA (1999) Phosphacan immunoreactivity is associated with perineuronal nets around parvalbumin-expressing neurons. Brain Res 834:219–222

    PubMed  Google Scholar 

  • Hockfield S, McKay RDG (1983) A surface antigen expressed by a subset of neurons in the vertebrate central nervous system. Proc Natl Acad Sci USA 80:5758–5761

    PubMed  CAS  Google Scholar 

  • 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 Harbor Symp Quant Biol 55:505–514

    PubMed  CAS  Google Scholar 

  • Horn AK, Brückner G, Härtig W, Messoudi A (2003) Saccadic omnipause and burst neurons in monkey and human are ensheathed by perineuronal nets but differ in their expression of calcium-binding proteins. J Comp Neurol 455:341–352

    PubMed  CAS  Google Scholar 

  • Jessell TM (1988) Adhesion molecules and the hierarchy of neural development. Neuron 1:3–13

    PubMed  CAS  Google Scholar 

  • Jessel TM (2000) Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 1:20–29

    Google Scholar 

  • Jones LL, Margolis RU, Tuszynski MH (2003) The chondroitin sulfate proteoglycans neurocan, brevican, phosphacan, and versican are differentially regulated following spinal cord injury. Exp Neurol 182:399–411

    PubMed  CAS  Google Scholar 

  • Joosten EA (1994) Developmental expression of N-CAM epitopes in the rat spinal cord during corticospinal tract axon outgrowth and target innervation. Brain Res Dev Brain Res 78:226–236

    PubMed  CAS  Google Scholar 

  • Kalb RG, Hockfield S (1988) Molecular evidence for early activity-dependent development of hamster motor neurons. J Neurosci 8:2350–2360

    PubMed  CAS  Google Scholar 

  • Kalb RG, Hockfield S (1990) Large diameter primary afferent input is required for expression of the Cat-301 proteoglycan on the surface of motor neurons. Neuroscience 34:391–401

    PubMed  CAS  Google Scholar 

  • Kalb RG, Hockfield S (1992) Activity-dependent development of spinal cord motor neurons. Brain Res Rev 17:283–289

    PubMed  CAS  Google Scholar 

  • Kalb RG, Hockfield S (1994) Electrical activity in the neuromuscular unit can influence the molecular development of motor neurons. Dev Biol 162:539–548

    PubMed  CAS  Google Scholar 

  • Lemmon V, Farr KL, Lagenaur C (1989) L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron 2:1597–1603

    PubMed  CAS  Google Scholar 

  • Lemons ML, Sandy JD, Anderson DK, Howland DR (2001) Intact aggrecan and fragments generated by both aggrecanase and metalloproteinase-like activities are present in the developing and adult rat spinal cord and their relative abundance is altered by injury. J Neurosci 21:4772–4781

    PubMed  CAS  Google Scholar 

  • Maeda N, Hakamana H, Oohira A, Noda M (1995) Purification, characterization and developmental expression of a brain-specific chondroitin sulfate, 6B4 proteoglycan/phosphacan. Neuroscience 6:23–35

    Google Scholar 

  • Maeda N, He J, Yajima Y, Mikami T, Sugahara K, Yabe T (2003) Heterogeneity of the chondroitin sulfate portion of phosphacan/6B4 proteoglycan regulates its binding affinity for pleiotrophin/heparin binding growth-associated molecule. J Biol Chem 278:35805–35811

    PubMed  CAS  Google Scholar 

  • Mannion RJ, Doubell TP, Coggeshall RE, Woolf CJ (1996) Collateral sprouting of injured primary afferent A–fibers into the superficial dorsal horn of the adult rat spinal cord after topical capsaicin treatment to the sciatic nerve. J Neurosci 16:5189–5195

    PubMed  CAS  Google Scholar 

  • Matsui F, Nishizuka M, Yasuda Y, Aono S, Watanabe E, Oohira A (1998) Occurrence of a N-terminal proteolytic fragment of neurocan, not a C-terminal half, in a perineuronal net in the adult rat cerebrum. Brain Res 790:45–51

    PubMed  CAS  Google Scholar 

  • Matsui F, Nishizuka M, Oohira A (1999) Proteoglycans in perineuronal nets. Acta Histochem Cytochem 32:141–147

    CAS  Google Scholar 

  • Matthews RT, Kelly GM, Zerillo CA, Gray G, Tiemeyer M, Hockfield S (2002) Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets. J Neurosci 22:7536–7547

    PubMed  CAS  Google Scholar 

  • Maurel P, Rauch U, Flad M, Margolis RK, Margolis RU (1994) Phosphacan, a chondroitin sulfate proteoglycan of brain that interacts with neurons and neural cell-adhesion molecules, is an extracellular variant of a receptor-type protein tyrosine phosphatase. Proc Natl Acad Sci USA 91:2512–2516

    PubMed  CAS  Google Scholar 

  • McKeon RJ, Hoke A, Silver J (1995) Injury-induced proteoglycans inhibit the potential for laminin mediated axon growth on astrocytic scars. Exp Neurol 136:32–43

    PubMed  CAS  Google Scholar 

  • McKeon RG, Jurynec MJ, Buck CR (1999) The chondroitin sulfate proteoglycans neurocan and phosphacan are expressed by reactive astrocytes in the chronic CNS glial scar. J Neurosci 15:10778–10788

    Google Scholar 

  • Milev P, Friedlander DR, Sakurai T, Karthikeyan L, Flad M, Margolis RK, Grumet M, Margolis RU (1994) Interactions of the chondroitin sulfate proteoglycan phosphacan, the extracellular domain of a receptor-type protein tyrosine phosphatase, with neurons, glia, and neuronal cell adhesion molecules. J Cell Biol 127:1703–1715

    PubMed  CAS  Google Scholar 

  • Milev P, Maurel P, Haring M, Margolis RK, Margolis RU (1996) TAG-1/axonin-1 is a high-affinity ligand of neurocan, phosphacan/protein-tyrosine phosphatase-ζ/β, and N-CAM. J Biol Chem 271:15716–15723

    PubMed  CAS  Google Scholar 

  • Morawski M, Brückner MK, Riederer P, Brückner G, Arendt T (2004) Perineuronal nets potentially protect against oxidative stress. Exp Neurol 188:309–315

    PubMed  CAS  Google Scholar 

  • Morris NP, Henderson Z (2000) Perineuronal nets ensheath fast-spiking, parvalbumin-immunoreactive neurons in the medial septum/diagonal band complex. Eur J Neurosci 12:828–838

    PubMed  CAS  Google Scholar 

  • Müller T, Brohmann H, Pierani A, Heppenstal PA, Lewin GR, Jessel TM, Birchmeier C (2002) The homeodomain factor Lxb1 distinguishes two major programs of neuronal differentiation in the dorsal spinal cord. Neuron 34:551–562

    PubMed  Google Scholar 

  • Murakami T, Tsubouchi Y, Tsubouchi M, Ohtsuka A, Taguchi T (1993) The occurrence of rat spinal cord neurons with strongly negatively-charged surface coats. Arch Histol Cytol 56:501–504

    PubMed  CAS  Google Scholar 

  • Murakami T, Ohtsuka A, Ono K (1996) Neurons with perineuronal sulfated proteoglycans in the mouse brain and spinal cord: their distribution and reactions to lectins Vicia villosa agglutinin and Golgi’s silver nitrate. Arch Histol Cytol 59:219–231

    PubMed  CAS  Google Scholar 

  • Nacimiento W, Topper R, Fischer A, Oestreicher AB, Nacimiento AC, Gispen WH, Noth J, Kreutzberg GW (1993) Immunocytochemistry of B-50 (GAP-43) in the spinal cord and in dorsal root ganglia of the adult cat. J Neurocytol 22:413–424

    PubMed  CAS  Google Scholar 

  • Nakatsuka T, Park J-S, Kumamoto E, Tamaki T, Yoshimura M (1999) Plastic changes in sensory inputs to rat substantia gelatinosa neurons following peripheral inflammation. Pain 82:39–47

    PubMed  CAS  Google Scholar 

  • Ojima H, Sakai M, Ohyama J (1998) Molecular heterogeneity of Vicia villosa-recognized perineuronal nets surrounding pyramidal and nonpyramidal neurons in the guinea pig cerebral cortex. Brain Res 786:274–280

    PubMed  CAS  Google Scholar 

  • Okamoto M, Mori S, Ichimura M, Endo H (1994) Chondroitin sulfate proteoglycans protect cultured rat’s cortical and hippocampal neurons from delayed cell death induced by excitotoxic amino acids. Neurosci Lett 172:51–54

    PubMed  CAS  Google Scholar 

  • Perides G, Erickson HP, Rahentmulla F, Bignami A (1993) Colocalization of tenascin with versican, a hyaluronate binding chondroitin sulfate proteoglycan. Anat Embryol 188:467–479

    PubMed  CAS  Google Scholar 

  • Pesheva P, Spiess E, Schachner M (1989) J1-160 and J1-180 are oligodendrocyte-secreted nonpermissive substrates for cell adhesion. J Cell Biol 109:1765–1778

    PubMed  CAS  Google Scholar 

  • Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1248–1251

    PubMed  CAS  Google Scholar 

  • Ratcliffe CF, Qu Y, McKormick KA, Tibbs VC, Dixon, Jack E, Scheuer T, Catteral WA (2000) A sodium channel signaling complex: modulation by associated receptor protein tyrosine phosphatase β. Nat Neurosci 3:437–444

    PubMed  CAS  Google Scholar 

  • Rauch U, Ping G, Janetzko A, Flaccus A, Hilgenberg L, Tekotte H, Margolis RK, Margolis RU (1991) Isolation and characterization of chondroitin sulfate and chondroitin/keratan sulfate proteoglycans of brain identified with monoclonal antibodies. J Biol Chem 266:14785–14801

    PubMed  CAS  Google Scholar 

  • Ren K, Ruda MA (1994) A comparative study of the calcium-binding proteins calbindin-D28k, calretinin and parvalbumin in the rat spinal cord. Brain Res Rev 19:163–179

    PubMed  CAS  Google Scholar 

  • Rhodes KE, Fawcett JF (2004) Chondroitin sulphate proteoglycans: preventing plasticity or protecting the CNS? J Anat 204:33–48

    PubMed  CAS  Google Scholar 

  • Rudy B, McBain CJ (2001) Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing. Trends Neurosci 24:517–526

    PubMed  CAS  Google Scholar 

  • Runyan SA, Roy R, Zhong H, Phelps PE (2005) L1 CAM expression in the superfical dorsal horn is derived from the dorsal root ganglion. J Comp Neurol 485:267–279

    PubMed  CAS  Google Scholar 

  • Sakurai T, Friedlander DR, Grumet M (1996) Expression of polypeptide variants of receptor-type protein tyrosine phosphatase β: the secreted form, phosphacan, increases dramatically during embryonic development and modulates glial cell behavior in vitro. J Neurosci Res 43:694–706

    PubMed  CAS  Google Scholar 

  • Schüppel K, Brauer K, Härtig W, Grosche J, Earley B, Leonard BE, Brückner G (2002) Perineuronal nets of extracellular matrix around hippocampal interneurons resist destruction by activated microglia in trimethyltin-treated rats. Brain Res 958:448–453

    PubMed  Google Scholar 

  • Schwarzacher SW, Vuksic M, Haas CM, Burbach GJ, Sloviter RS, Deller T (2006) Neuronal hyperactivity induces astrocytic expression of neurocan in the adult rat hippocampus. Glia 53:704–714

    PubMed  Google Scholar 

  • Seidenbecher CI, Smalla KH, Fisher N, Gundelfinger ED, Kreutz MR (2002) Brevican isoforms associate with neural membranes. J Neurochem 83:738–746

    PubMed  CAS  Google Scholar 

  • Seki T, Arai Y (1993) Highly polysialylated NCAM expression in the developing and adult rat spinal cord. Dev Brain Res 73:141–145

    CAS  Google Scholar 

  • Smith-Thomas LC, Stevens J, Fok-Seang J, Faissner A, Rogers JH, Fawcett JW (1995) Increased axon regeneration in astrocytes grown in the presence of proteoglycan synthesis inhibitors. J Cell Sci 108:1307–1315

    PubMed  CAS  Google Scholar 

  • Soares S, Traka M, Boxberg Y von, Bouquet C, Karagogeos D, Nothias F (2005) Neuronal and glial expression of the adhesion molecule TAG-1 is regulated after peripheral nerve lesion or neurodegeneration of adult nervous system. Eur J Neurosci 21:1169–1180

    PubMed  Google Scholar 

  • Spicer SS, Naegele JR, Schulte BA (1996) Differentiation of glycoconjugates localized to sensory terminals and selected sites in brain. J Comp Neurol 365:217–231

    PubMed  CAS  Google Scholar 

  • Takahashi-Iwanaga H, Murakami T, Abe K (1998) Three-dimensional microanatomy of perineuronal nets enveloping motor neurons in the rat spinal cord. J Neurocytol 27:817–827

    PubMed  CAS  Google Scholar 

  • Vitellaro-Zuccarello L, Meroni A, Amadeo A, De Biasi S (2001) Chondroitin sulfate proteoglycans in the rat thalamus: expression during postnatal development and correlation with calcium-binding proteins in adults. Cell Tissue Res 306:15–26

    PubMed  CAS  Google Scholar 

  • Vitellaro-Zuccarello L, Mazzetti S, Bosisio P, Monti C, De Biasi S (2005) Distribution of aquaporin 4 in rodent spinal cord: relationship with astrocyte markers and chondroitin sulfate proteoglycans. Glia 51:148–159

    PubMed  Google Scholar 

  • Westling J, Gottschall PE, Thompson VP, Cockburn A, Perides G, Zimmermann DR, Sandy JD (2004) ADAMTS4 (aggrecanase-1) cleaves human brain versican V2 at Glu405-Gln406 to generate glial hyaluronate binding protein. Biochem J 377:787–795

    PubMed  CAS  Google Scholar 

  • Wintergerst ES, Vogt Weisenhorn DM, Rathjen FG, Riederer BM, Lambert S, Celio MR (1996) Temporal and spatial appearance of the membrane cytoskeleton and perineuronal nets in the rat neocortex. Neurosci Lett 209:173–176

    PubMed  CAS  Google Scholar 

  • Woolf CJ, Shortland P, Coggeshall RE (1992) Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355:75–78

    PubMed  CAS  Google Scholar 

  • Xiao ZC, Ragsdale DS, Malhotra JD, Mattei LN, Braun PE, Schachner M, Isom LL (1999) Tenascin-R is a functional modulator of sodium channel subunits. J Biol Chem 274:26511–26517

    PubMed  CAS  Google Scholar 

  • Yamaguchi Y (2000) Lecticans: organisers of the brain extracellular matrix. Cell Mol Life Sci 57:276–289

    PubMed  CAS  Google Scholar 

  • Yasuhara O, Akiyama A, McGeer EB, McGeer PL (1994). Immunohistochemical localization of hyaluronic acid in rat and human brain. Brain Res 635:269–282

    PubMed  CAS  Google Scholar 

  • Zuo J, Neubauer D, Dyess K, Ferguson TA, Muir D (1998) Degradation of chondroitin sulfate proteoglycan enhances the neurite-promoting potential of spinal cord tissue. Exp Neurol 154:654–662

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

Confocal microscopy was carried out at the Centro Interdipartimentale di Microscopia Avanzata (CIMA) of the University of Milan. The phosphacan/RPTPζ/β  monoclonal antibodies (3F8, 3H1 and 2B49) and the versican (12C5) monoclonal antibody were obtained from the Developmental Studies Hybridoma Bank.

Author information

Authors and Affiliations

  1. Dip. Scienze Biomolecolari e Biotecnologie, Università degli Studi di Milano, Via Celoria 26, 20133, Milan, Italy

    Laura Vitellaro-Zuccarello, Paola Bosisio, Samanta Mazzetti, Claudia Monti & Silvia De Biasi

Authors
  1. Laura Vitellaro-Zuccarello
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paola Bosisio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Samanta Mazzetti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Claudia Monti
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Silvia De Biasi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura Vitellaro-Zuccarello.

Additional information

This paper is dedicated to Prof. Aurelio Bairati on the occasion of his retirement from his professorship at the University of Milan.

This work was supported by grants from the Italian Ministry of Education, University and Research (COFIN 03 and 05) and the University of Milan (FIRST).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vitellaro-Zuccarello, L., Bosisio, P., Mazzetti, S. et al. Differential expression of several molecules of the extracellular matrix in functionally and developmentally distinct regions of rat spinal cord. Cell Tissue Res 327, 433–447 (2007). https://doi.org/10.1007/s00441-006-0289-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-006-0289-y

Keywords

Search

Navigation