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J. Biol. Chem., Vol. 281, Issue 26, 17789-17800, June 30, 2006

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Composition of Perineuronal Net Extracellular Matrix in Rat Brain

A DIFFERENT DISACCHARIDE COMPOSITION FOR THE NET-ASSOCIATED PROTEOGLYCANS^*

Sarama Sathyaseelan Deepa, Daniela Carulli, Clare Galtrey, Kate Rhodes, Junko Fukuda, Tadahisa Mikami, Kazuyuki Sugahara, and James W. Fawcett¹

From the Centre for Brain Repair, Cambridge University, Forvie Site, Cambridge CB2 2PY, United Kingdom and the Department of Biochemistry, Kobe Pharmaceutical University, Higashinada-ku, Kobe 658-558, Japan

We developed a method to extract differentially chondroitin sulfate proteoglycans (CSPGs) that are diffusely present in the central nervous system (CNS) matrix and CSPGs that are present in the condensed matrix of perineuronal nets (PNNs). Adult rat brain was sequentially extracted with Tris-buffered saline (TBS), TBS-containing detergent, 1 M NaCl, and 6 M urea. Extracting tissue sections with these buffers showed that the diffuse and membrane-bound CSPGs were extracted in the first three buffers, but PNN-associated CSPGs remained and were only removed by 6 M urea. Most of the CSPGs were extracted to some degree with all the buffers, with neurocan, brevican, aggrecan, and versican particularly associated with the stable urea-extractable PNNs. The CSPGs in stable complexes only extractable in urea buffer are found from postnatal day 7–14 coinciding with PNN formation. Disaccharide composition analysis indicated a different glycosaminoglycan (GAG) composition for PGs strongly associated with extracellular matrix (ECM). For CS/dermatan sulfate (DS)-GAG the content of nonsulfated, 6-O-sulfated, 2,6-O-disulfated, and 4,6-O-disulfated disaccharides were higher and for heparan sulfate (HS)-GAG, the content of 6-O-sulfated, 2-N-, 6-O-disulfated, 2-O-, 2-N-disulfated, and 2-O-, 2-N-, 6-O-trisulfated disaccharides were higher in urea extract compared with other buffer extracts. Digestions with chondroitinase ABC and hyaluronidase indicated that aggrecan, versican, neurocan, brevican, and phosphacan are retained in PNNs through binding to hyaluronan (HA). A comparison of the brain and spinal cord ECM with respect to CSPGs indicated that the PNNs in both parts of the CNS have the same composition.

Received for publication, January 18, 2006 , and in revised form, March 17, 2006.

^* The work at Cambridge University was supported by the Wellcome Trust, the UK Medical Research Council, the Christopher Reeve Foundation, and the Henry Smith Charity. The work at Kobe Pharmaceutical University was supported in part by HAITEKU from the Japan Private School Promotion Foundation, Core Research for Evolutional Science and Technology (CREST) of the Japan Science and Technology (JST) Corporation, and grantsin-aid for Scientific Research from the Ministry of Education, Science, Culture, and Sports of Japan (MEXT). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ To whom correspondence should be addressed: Centre for Brain Repair, Cambridge University, Forvie Site, Cambridge CB2 2PY, UK. Tel.: 44-1223-331188; Fax: 44-1223-331174; E-mail: jf108{at}cam.ac.uk.

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