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J. Biol. Chem., Vol. 278, Issue 37, 35805-35811, September 12, 2003

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Heterogeneity of the Chondroitin Sulfate Portion of Phosphacan/6B4 Proteoglycan Regulates Its Binding Affinity for Pleiotrophin/Heparin Binding Growth-associated Molecule^*

Nobuaki Maeda  , Jue He , Yuki Yajima ¶, Tadahisa Mikami ¶, Kazuyuki Sugahara ¶ and Tomio Yabe 

From the Department of Developmental Neuroscience, Tokyo Metropolitan Institute for Neuroscience, 2-6 Musashidai, Fuchu, Tokyo 183-8526, and the ^¶Department of Biochemistry, Kobe Pharmaceutical University, Higashinada-ku, Kobe 658-8558, Japan

PTP is a receptor-type protein-tyrosine phosphatase that is synthesized as a chondroitin sulfate proteoglycan and uses pleiotrophin as a ligand. The chondroitin sulfate portion of this receptor is essential for high affinity binding to pleiotrophin. Here, we purified phosphacan, which corresponds to the extracellular domain of PTP, from postnatal day 7 (P7) and P12 rat cerebral cortex (PG-P7 and PG-P12, respectively) and from P20 rat whole brain (PG-P20). The chondroitin sulfate of these preparations displayed immunologically and compositionally different structures. In particular, only PG-P20 reacted with the monoclonal antibody MO-225, which recognizes chondroitin sulfate containing the GlcA(2S)1–3GalNAc(6S) disaccharide unit (D unit). Analysis of the chondroitinase digestion products revealed that GlcA1–3GalNAc(4S) disaccharide unit (A unit) was the major component in these preparations and that PG-P20 contained 1.3% D unit, which was not detected in PG-P7 and PG-P12. Interaction analysis using a surface plasmon resonance biosensor indicated that PG-P20 had 5-fold stronger affinity for pleiotrophin (dissociation constant (K_D) = 0.14 nM) than PG-P7 and PG-P12, although all these preparations showed similar low affinity binding to pleiotrophin after chondroitinase ABC digestion (K_D = 1.4 1.6 nM). We also found that shark cartilage chondroitin sulfate D containing 20% D unit bound to pleiotrophin with moderate affinity (K_D = 2.7 nM), whereas whale cartilage chondroitin sulfate A showed no binding to this growth factor. These results suggest that variation of chondroitin sulfate plays important roles in the regulation of signal transduction in the brain.

Received for publication, May 27, 2003 , and in revised form, July 1, 2003.

^* This study was supported in part by the grants from the Ministry of Education Science, Sports, and Culture of Japan (to N. M. and K. S.), the Takeda Science Foundation (to N. M.), and the Science Research Promotion Fund of Japan Private School Promotion Foundation (to K. S.). 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.

To whom correspondence should be addressed. Tel.: 81-42-325-3881; Fax: 81-42-321-8678; E-mail: maedan{at}tmin.ac.jp.

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