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J. Biol. Chem., Vol. 281, Issue 26, 18257-18263, June 30, 2006

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Identification and Characterization of Versican/PG-M Aggregates in Cartilage^*

Kazu Matsumoto, Nobuhiro Kamiya, Keittisak Suwan, Fukiko Atsumi, Katsuji Shimizu, Tamayuki Shinomura^¶, Yoshihiko Yamada^||, Koji Kimata, and Hideto Watanabe¹

From the Institute for Molecular Science of Medicine, Aichi Medical University, Nagakute, Aichi 480-1195, Japan, Department of Orthopaedic Surgery, Gifu University School of Medicine, Gifu 500-8705, Japan, ^¶Tissue Regeneration, Department of Hard Tissue Engineering, Tokyo Medical and Dental University, Tokyo 113-8549, Japan, and ^||Craniofacial Developmental Biology and Regeneration Branch, NIDCR, National Institutes of Health, Bethesda, Maryland 20892-4370

Versican/PG-M is a large chondroitin sulfate proteoglycan of the extracellular matrix with a common domain structure to aggrecan and is present in cartilage at low levels. Here, we characterized cartilage versican during development and growth. Immunostaining showed that versican was mainly localized in the interterritorial zone of the articular surface at 2 weeks in mice, whereas aggrecan was in the pericellular zone of prehypertrophic and hypertrophic cells of the growth plate. Although its transcription level rapidly diminished during growth, versican remained in the articular cartilage. Biochemical analysis of normal articular cartilage and aggrecan-null cartilage from cmd (cartilage matrix deficiency)/cmd mice revealed that versican was present as a proteoglycan aggregate with both link protein and hyaluronan. Chondroitin sulfate chains of versican digested with chondroitinase ABC contained 71% nonsulfated and 28% 4-sulfated unsaturated disaccharides, whereas those of aggrecan contained 25% nonsulfated and 70% 4-sulfated. Link protein overexpression in chondrocytic N1511 cells at the early stage of differentiation, in which versican is expressed, enhanced versican deposition in the matrix and prevented subsequent aggrecan deposition. These results suggest that versican is present as an aggregate distinct from the aggrecan aggregate and may play specific roles in the articular surface.

Received for publication, September 20, 2005 , and in revised form, April 26, 2006.

^* This work was supported by a grant-in-aid for scientific research on priority areas (KAKENHI to H. W.) and a grant-in-aid for scientific research (KAKENHI to H. W.). 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: Inst. for Molecular Science of Medicine, Aichi Medical University, Karimata 21, Yazako, Nagakute, Aichi-gun, Aichi 480-1195, Japan. Tel.: 81-561-62-3311 (ext. 2086); Fax: 81-561-63-3532; E-mail: wannabee{at}aichi-med-u.ac.jp.

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