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J. Biol. Chem., Vol. 282, Issue 32, 23275-23283, August 10, 2007

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Functional Implication of Nucleolin in the Mouse First Molar Development^*

Ming Xie, Ieyoshi Kobayashi¹, Tamotsu Kiyoshima, Haruyoshi Yamaza^¶, Jun-ya Honda^||, Keiko Takahashi^**, Norio Enoki^**, Akifumi Akamine, and Hidetaka Sakai

From the Laboratory of Oral Pathology and Medicine and the Department of Endodontology and Operative Dentistry, Kyushu University, Graduate School of Dental Science, Fukuoka 812-8582, the ^¶Division of Experimental Medicine, Pathology, and Gerontology, Department of Respiratory and Digestive Medicine, Nagasaki University School of Medicine, Nagasaki 852-8523, and the ^||Department of Orthodontics and the ^**Department of Fixed Prothodontics, Kyushu University, Graduate School of Dental Science, Fukuoka 812-8582, Japan

We examined the functional implication of nucleolin in the mouse first molar development. Both the nucleolin mRNA and protein expressions were demonstrated in the odontogenic epithelial cells in the early stage and in the inner enamel epithelial layer in the late stage. The expression pattern of nucleolin corresponded to the proliferating cells in the tooth germ, thus showing that nucleolin could possibly be related to cell proliferation. No in situ signal of nucleolin was found in the primary enamel knot (PEK). Furthermore, nucleolin protein was demonstrated in the PEK by immunohistochemistry. The existence of nucleolin protein in the PEK may possibly be related to the apoptosis in the PEK cells. An inhibition assay using the hemagglutinating virus of Japan-liposome containing nucleolin antisense phosphorothioated oligonucleotide (AS S-ODN) in cultured mouse mandibles at embryonic day (E) 11.0 showed a marked growth inhibition of tooth germ. Moreover, no developmental arrest was found in the cultured tooth germ at E15.0 treated with nucleolin AS S-ODN. Real time PCR was performed to examine the mRNA expression of nucleolin-related genes, and a significant reduction in the midkine mRNA expression was thus observed in the mouse mandible after being treated with nucleolin AS S-ODN. This inhibition assay indicated that nucleolin could thus be involved in the early stage of tooth germ initiation and morphogenesis, possibly by regulating the midkine expression.

Received for publication, November 21, 2006 , and in revised form, April 20, 2007.

^* This work was supported in part by Grant-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan 17390487 (to H. S.) and 18590169 (to I. K.). 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 Figs. 1–3.

¹ To whom correspondence and reprint requests should be addressed: Laboratory of Oral Pathology and Medicine, Kyushu University, Graduate School of Dental Science, Fukuoka 812-8582, Japan. Tel.: 81-92-642-6328; Fax: 81-92-642-6329; E-mail: ikoba{at}dent.kyushu-u.ac.jp.

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