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J. Biol. Chem., Vol. 281, Issue 16, 11431-11440, April 21, 2006

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Essential Roles of 3'-Phosphoadenosine 5'-Phoshosulfate Synthase in Embryonic and Larval Development of the Nematode Caenorhabditis elegans^*

Katsufumi Dejima, Akira Seko^¶, Katsuko Yamashita^¶, Keiko Gengyo-Ando^||, Shohei Mitani^||, Tomomi Izumikawa^**, Hiroshi Kitagawa^**, Kazuyuki Sugahara^**, Souhei Mizuguchi, and Kazuya Nomura¹

From the Department of Biology, Faculty of Sciences 33, Kyushu University, Fukuoka 812-8581, Japan, CREST, Kawaguchi Center Bldg., 4-1-8 Hon-cho, Kawaguchi, Saitama 332-0012, Japan, the ^¶Department of Biochemistry, Sasaki Institute, Tokyo 101-0062, Japan, ^||Department of Physiology, Tokyo Women's Medical University School of Medicine, Tokyo 162-8666, Japan, ^**Department of Biochemistry, Kobe Pharmaceutical University, Higashinada-ku, Kobe 658-8558, Japan

Sulfation of biomolecules, which is widely observed from bacteria to humans, plays critical roles in many biological processes. All sulfation reactions in all organisms require activated sulfate, 3'-phosphoadenosine 5'-phosphosulfate (PAPS), as a universal donor. In animals, PAPS is synthesized from ATP and inorganic sulfate by the bifunctional enzyme, PAPS synthase. In mammals, genetic defects in PAPS synthase 2, one of two PAPS synthase isozymes, cause dwarfism disorder, but little is known about the consequences of the complete loss of PAPS synthesis. To define the developmental role of sulfation, we cloned a Caenorhabditis elegans PAPS synthase-homologous gene, pps-1, and depleted expression of its product by isolating the deletion mutant and by RNA-mediated interference. PPS-1 protein exhibits specific activity to form PAPS in vitro, and disruption of the pps-1 gene by RNAi causes pleiotropic developmental defects in muscle patterning and epithelial cell shape changes with a decrease in glycosaminoglycan sulfation. Additionally, the pps-1 null mutant exhibits larval lethality. These data suggest that sulfation is essential for normal growth and integrity of epidermis in C. elegans. Furthermore, reporter analysis showed that pps-1 is expressed in the epidermis and several gland cells but not in neurons and muscles, indicating that PAPS in the neurons and muscles is provided by other cells.

Received for publication, February 16, 2006

^* This work was supported by a grant-in-aid for young scientists (B) (to S. M.) and a grant-in-aid for JSPS Fellows (to K. D.) from MEXT, Japan. It is also supported in part by the Core Research for Evolutional Science and Technology Program of the Japan Science and Technology Corp. (to K. N. and K. S.), Grant-in-aid for Scientific Research 16590075 (to H. K.), and Grant-in-Aid for Scientific Research on Priority Areas 14082207 (to K. N., K. Y., and K. S.) from MEXT, 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.

¹ To whom correspondence should be addressed. E-mail: knomuscb{at}mbox.nc.kyushu-u.ac.jp.

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