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J. Biol. Chem., Vol. 279, Issue 51, 53755-53761, December 17, 2004

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Nematode Chondroitin Polymerizing Factor Showing Cell-/Organ-specific Expression Is Indispensable for Chondroitin Synthesis and Embryonic Cell Division^*

Tomomi Izumikawa, Hiroshi Kitagawa¶, Souhei Mizuguchi||, Kazuko H. Nomura||, Kazuya Nomura¶||, Jun-ichi Tamura**, Keiko Gengyo-Ando, Shohei Mitani, and Kazuyuki Sugahara

From the Department of Biochemistry, Kobe Pharmaceutical University, Higashinada-ku, Kobe 658-8558, the ^||Department of Biological Sciences, Faculty of Science, Kyushu University Graduate School, Fukuoka 812-8581, Core Research for Evolutional Science and Technology (CREST) of Japan Science and Technology Agency (JST), Kawaguchi Center Building, 4-1-8, Hon-cho, Kawaguchi, Saitama 332-0012, the ^**Department of Regional Environment, Faculty of Regional Sciences, Tottori University, Tottori 680-8551, and the Department of Physiology, Tokyo Woman's Medical University School of Medicine, Tokyo 162-8666, Japan

Chondroitin polymerization was first demonstrated in vitro when human chondroitin synthase (ChSy) was coexpressed with human chondroitin polymerizing factor (ChPF), which is homologous to ChSy but has little glycosyltransferase activity. To analyze the biological function of chondroitin, the Caenorhabditis elegans ortholog of human ChSy (sqv-5) was recently cloned, and the expression of its product was depleted by RNA-mediated interference (RNAi) and deletion mutagenesis. Blocking of chondroitin synthesis resulted in defects of cytokinesis in early embryogenesis, and eventually, cell division stopped. Here, we cloned the ortholog of human ChPF in C. elegans, PAR2.4. Despite little glycosyltransferase activity of the gene product, chondroitin polymerization was demonstrated as in the case of mammals when PAR2.4 was coexpressed with cChSy in vitro. The worm phenotypes including the reversion of cytokinesis, observed after the depletion of PAR2.4 by RNAi, were very similar to the cChSy (sqv-5)-RNAi phenotypes. Thus, PAR2.4 in addition to cChSy is indispensable for the biosynthesis of chondroitin in C. elegans, and the two cooperate to synthesize chondroitin in vivo. The expression of the PAR2.4 protein was observed in seam cells, which can act as neural stem cells in early embryonic lineages. The expression was also detected in vulva and distal tip cells of the growing gonad arms from L3 through to the young adult stage. These findings are consistent with the notion that chondroitin is involved in the organogenesis of the vulva and maturation of the gonad and also indicative of an involvement in distal tip cell migration and neural development.

Received for publication, August 20, 2004 , and in revised form, October 6, 2004.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AB110823 andAB110824

^* This work was supported in part part by grants from the Science Research Promotion Fund of the Japan Private School Promotion Foundation and the Kato Memorial Bioscience Foundation (to H. K.) and Grants-in-aid for Scientific Research C16590075 (to H. K.) and B16390026 (to K. S.) and Grant-in-aid for Scientific Research on Priority Areas 14082207 (to K. S. and to K. N.) from the Ministry of Education, Science, Culture, and Sports of Japan. 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 a supplemental QuickTime movie.

^¶ Supported by CREST of the JST.

To whom correspondence should be addressed: Dept. of Biochemistry, Kobe Pharmaceutical University, 4-19-1 Motoyamakita-machi, Higashinada-ku, Kobe 658-8558, Japan. Tel.: 81-78-441-7570; Fax: 81-78-441-7571; E-mail: k-sugar{at}kobepharma-u.ac.jp.

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