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J. Biol. Chem., Vol. 282, Issue 32, 23070-23080, August 10, 2007

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PLAP-1/Asporin, a Novel Negative Regulator of Periodontal Ligament Mineralization^*

Satoru Yamada, Miki Tomoeda, Yasuhiro Ozawa, Shinya Yoneda, Yoshimitsu Terashima, Kazuhiko Ikezawa, Shiro Ikegawa, Masahiro Saito^¶, Satoru Toyosawa^||, and Shinya Murakami¹

From the Departments of Periodontology and ^||Oral Pathology, Osaka University Graduate School of Dentistry, Suita, Osaka 565-0871, Japan, Laboratory for Bone and Joint Disease, Single Nucleotide Polymorphisms Research Center, The Institute of Physical and Chemical Research (RIKEN), Minato-ku, Tokyo 108-8639, Japan, and ^¶Department of Oral Medicine, Division of Operative Dentistry and Endodontics, Kanagawa Dental College, Yokosuka 238-8580, Japan

Periodontal ligament-associated protein-1 (PLAP-1)/asporin is a recently identified novel member of the small leucine-rich repeat proteoglycan family. PLAP-1/asporin is involved in chondrogenesis, and its involvement in the pathogenesis of osteoarthritis has been suggested. We report that PLAP-1/asporin is also expressed specifically and predominantly in the periodontal ligament (PDL) and that it negatively regulates the mineralization of PDL cells. In situ hybridization analysis revealed that PLAP-1/asporin was expressed specifically not only in the PDL of an erupted tooth but also in the dental follicle, which is the progenitor tissue of the PDL during tooth development. Overexpression of PLAP-1/asporin in mouse PDL-derived clone cells interfered with both naturally and bone morphogenetic protein 2 (BMP-2)-induced mineralization of the PDL cells. On the other hand, knockdown of PLAP-1/asporin transcript levels by RNA interference enhanced BMP-2-induced differentiation of PDL cells. Furthermore co-immunoprecipitation assays showed a direct interaction between PLAP-1/asporin and BMP-2 in vitro, and immunohistochemistry staining revealed the co-localization of PLAP-1/asporin and BMP-2 at the cellular level. These results suggest that PLAP-1/asporin plays a specific role(s) in the periodontal ligament as a negative regulator of cytodifferentiation and mineralization probably by regulating BMP-2 activity to prevent the periodontal ligament from developing non-physiological mineralization such as ankylosis.

Received for publication, December 6, 2006 , and in revised form, May 7, 2007.

^* This work was supported by Grants-in-aid 17390560 and 17390561 from the Japan Society for the Promotion of Science and was a part of the 21st Century Center of Excellence entitled "Origination of Frontier BioDentistry" at Osaka University Graduate School of Dentistry supported by the Ministry of Education, Culture, Sports, Science and Technology. 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Table 1.

¹ To whom correspondence should be addressed: Dept. of Periodontology, Osaka University Graduate School of Dentistry, 1-8 Yamadaoka, Suita, Osaka 565-0871, Japan. Tel.: 81-6-6879-2930; Fax: 81-6-6879-2934; E-mail: ipshinya{at}dent.osaka-u.ac.jp.

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