Immunohistochemical evidence for the brevican-tenascin-R interaction: Colocalization in perineuronal nets suggests a physiological role for the interaction in the adult rat brain

Journal of Comparative Neurology

Volumn 410, Issue 2, 1999, Pages 256-264

  Hagihara, Kazuki ^a   Miura, Ryu ^a   Kosaki, Rika ^a   Berglund, Erik ^a   Ranscht, Barbara ^a   Yamaguchi, Yu ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

Brevican; Chondroitin sulfate proteoglycan; Lecticans; Perineuronal nets; Tenscin R; Versican

Indexed keywords

BREVICAN; FIBRONECTIN; LECTIN; MONOCLONAL ANTIBODY; POLYCLONAL ANTIBODY; PROTEOCHONDROITIN SULFATE; TENASCIN; VERSICAN;

ADOLESCENT; ANIMAL TISSUE; ARTICLE; CEREBELLUM NUCLEUS; COCHLEAR NUCLEUS; GIGANTOCELLULAR RETICULAR NUCLEUS; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; NONHUMAN; OCULOMOTOR NUCLEUS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; RED NUCLEUS; RHOMBENCEPHALON; SUPERIOR OLIVARY NUCLEUS; TRIGEMINAL NUCLEUS; VESTIBULAR NUCLEUS;

AGE FACTORS; ANIMALS; ANTIBODIES, MONOCLONAL; BINDING SITES; BRAIN; CELL CULTURE TECHNIQUES; CHONDROITIN SULFATES; EXTRACELLULAR SPACE; IMMUNOHISTOCHEMISTRY; LECTINS; LECTINS, C-TYPE; LIGANDS; MALE; NERVE NET; NERVE TISSUE PROTEINS; NEURAL PATHWAYS; PRESYNAPTIC TERMINALS; PROTEOCHONDROITIN SULFATES; RATS; RATS, SPRAGUE-DAWLEY; RETICULAR FORMATION; TENASCIN;

EID: 0033606849     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990726)410:2<256::AID-CNE7>3.0.CO;2-5     Document Type: Article

References (44)

1. Angelov DN, Walter M, Streppel M, Gunthinas-Litchis 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.
2. Aspberg A, Miura R, Bourdoulous S, Shimonaka M, Heinegård 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.
3. Barsony J, Marx SJ. 1990. Immunocytology on microwave-fixed cells reveals rapid and agonist-specific changes in subcellular accumulation patterns for cAMP or cGMP. Proc Natl Acad Sci USA 87:1188-1192.
4. Bertolotto A, Manzardo E, Guiglielmone R. 1996. Immunohistochemical mapping of perineuronal nets containing chondroitin sulfate proteoglycan in the rat central nervous system. Cell Tissue Res 283:283-295.
5. Bignami A, Asher R, Perides G. 1992. Co-localization of hyaluronic acid and chondroitin sulfate proteoglycans in rat cerebral cortex. Brain Res 579:173-177.
6. Bignami A, Perides G, Rahemtulla F. 1993. Versican, a hyaluronate-binding proteoglycan of embryonal precartilaginous mesenchyma, is mainly expressed postnatally in rat brain. J Neurosci Res 34:97-106.
7. Blümcke I, Eggli P, Celio MR. 1995. Relationship between astrocytic processes and "perineuronal nets" in rat neocortex. Glia 15:131-140.
8. Bode-Lesniewska B, Dours-Zimmermann MT, Odermatt BF, Briner J, Heitz PU, Zimmermann DR. 1996. Distribution of the large aggregating proteoglycan versican in adult human tissues. J Histochem Cytochem 44:303-312.
9. 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.
10. Carbonetto S, Gruver MM, Turner DC. 1983. Nerve fiber growth in culture on fibronectin, collagen, and glycosaminoglycan substrates. J Neurosci 3:2324-2335.
11. Celio MR, Blümcke I. 1994. Perineuronal nets: a specialized form of extracellular matrix in the adult nervous system. Brain Res Rev 19:128-145.
12. Celio MR, Rathjen F. 1993. Restrictin occurs in "perineuronal nets" of the adult rat brain. Soc Neurosci Abstr 19:689.
13. Doege K, Sasaki M, Horigan E, Hassel JR, Yamada Y. 1987. Complete primary structure of the rat cartilage proteoglycan core protein deduced from cDNA clones. J Biol Chem 262:17757-17767.
14. Friedlander DR, Milev P, Karthikeyan L, Margolis RK, Margolis RU. 1994. The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecule Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neunte outgrowth. J Cell Biol 125:669-680.
15. Fryer HJL, Kelly GM, Molinaro L, Hockfield S. 1992. The high molecular weight Cat-301 chondroitin sulfate proteoglycan from brain is related to the large aggregating proteoglycan from cartilage, aggrecan. J Biol Chem 267:9874-9883.
16. Gersten DM, Marchalonis JJ. 1978. A rapid, novel method for the solid-phase derivatization of IgG antibodies for immune-affinity chromatography. J Immunol Methods 24:305-309.
17. Girard N, Courel MN, Delpech A, Brückner G, Delpech B. 1992. Staining of hyaluronan in rat cerebellum with a hyaluronectin-antihyaluronectin immune complex. Histochem J 24:21-24.
18. Herndon ME, Lander AD. 1990. A diverse set of developmentally regulated proteoglycans is expressed in the rat central nervous system. Neuron 4:949-961.
19. Hockfield S, Kalb RG, Zaremba S, Frey 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.
20. Krueger RC Jr, Hennig AK, Schwartz NB. 1992. Two immunologically and developmentally distinct chondroitin sulfate proteoglycans in embryonic chick brain. J Biol Chem 267:12149-12161.
21. LeBaron RG. 1996. Versican. Perspect Dev Neurobiol 3:261-271.
22. Li H, Domowicz M, Hennig A, Schwartz NB. 1996. S103L reactive chondroitin sulfate proteoglycan (aggrecan) mRNA expressed in developing chick brain and cartilage is encoded by a single gene. Brain Res Mol Brain Res 36:309-321.
23. Margolis RK, Margolis RU. 1993. Nervous tissue proteoglycans. Experientia 49:429-446.
24. Milev P, Maurel P, Chiba A, Mevissen M, Popp S, Yamaguchi Y, Margolis RK, Margolis RU. 1998. Differential regulation of expression of hyaluronan-binding proteoglycans in developing brain: aggrecan, versican, neurocan, and brevican. Biochem Biophys Res Commun 247:207-212.
25. Murakami T, Ohtsuka A, Taguchi T. 1994. Neurons with intensely negatively charged extracellular matrix in the human visual cortex. Arch Histol Cytol 57:509-522.
26. Murakami T, Ohtsuka A, Taguchi T, Piao DX. 1995. Perineuronal sulfated proteoglycans and dark neurons in the brain and spinal cord: a histochemical and electron microscopic study of newborn and adult mice. Arch Histol Cytol 58:557-565.
27. Paxinos G, Watson C. 1986. The rat brain in stereotaxic coordinates. 2nd ed. San Diego: Academic Press.
28. Pendes G, Lane WS, Andrews D, Dahl D, Bignami A. 1989. Isolation and partial characterization of a glial hyaluronate-binding protein. J Biol Chem 264:5881-5987.
29. 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.
30. Rauch U, Karthikeyan L, Maurel P, Margolis RU, Margolis RK. 1992. Cloning and primary structure of neurocan, a developmentally regulated, aggregating chondroitin sulfate proteoglycan of brain. J Biol Chem 267:19536-19547.
31. Ruoslahti E. 1996. Brain extracellular matrix. Glycobiology 6:489-492.
32. Schachner M, Taylor J, Bartsch U, Pesheva P. 1994. The perplexing multifunctionality of janusin, a tenascin-related molecule. Perspect Dev Neurobiol 2:33-41.
33. Schwartz NB, Domowicz M, Krueger RC Jr, Li H, Mangoura K. 1996. Brain aggrecan. Perspect Dev Neurobiol 3:291-306.
34. Seidenbecher CI, Richter K, Rauch U, Fässler R, Garner CC, Gundelfinger ED. 1995. Brevican, a chondroitin sulfate proteoglycan of rat brain, occurs as secreted and cell surface glycosylphosphatidylinositol-anchored isoforms. J Biol Chem 270:27206-27212.
35. Snow DM, Lemmon V, Carrino DA, Caplan AI, Silver J. 1990. Sulfated proteoglycans in astroglial barriers inhibit neurite outgrowth in vitro. Exp Neurobiol 109:111-130.
36. Sur M, Frost DO, Hockfield S. 1988. Expression of a surface-associated antigen on Y-cells in the cat lateral geniculate nucleus is regulated by visual experience. J Neurosci 8:874-882.
37. Verna JM, Fichard A, Saxod R. 1989. Influence of glycosaminoglycans on neurite morphology and outgrowth patterns in vitro. Int J Dev Neurosci 7:389-399.
38. 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.
39. Yamada H, Watanabe K, Shimonaka M, Yamaguchi Y 1994. Molecular cloning of brevican, a novel brain proteoglycan of the aggrecan/versican family. J Biol Chem 267:10119-10126.
40. Yamada H, Fredette B, Shitara K, Hagihara K, Miura R, Ranscht B, Stallcup WB, Yamaguchi Y. 1997. The brain chondroitin sulfate proteoglycan brevican associates with astrocytes ensheathing cerebellar glomeruli and inhibits neurite outgrowth from granule neurons. J Neurosci 17:7784-7795.
41. Yamaguchi Y. 1996. Brevican: a major proteoglycan in adult brain. Perspect Dev Neurobiol 3:307-317.
42. Yasuhara O, Akiyama A, McGeer EB, McGeer PL. 1994. Immunohistochemical localization of hyaluronic acid in rat and human brain. Brain Res 635:269-282.
43. Zaremba S, Guimaraes A, Kalb RG, Hockfield S. 1989. Characterization of an activity dependent neuronal surface proteoglycan identified with monoclonal antibody Cat-301. Neuron 2:1207-1219.
44. Zimmermann DR, Ruoslahti E. 1989. Multiple domains of the large fibroblast proteoglycan, versican. EMBO J 8:2975-2981.