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J. Biol. Chem., Vol. 283, Issue 3, 1705-1712, January 18, 2008

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Involvement of p90 Ribosomal S6 Kinase in Termination of Cell Cycle Arrest during Development of Artemia-encysted Embryos^*

Jie-Qiong Dai, Xiao-Jing Zhu, Feng-Qi Liu, Jian-Hai Xiang^¶, Hiromichi Nagasawa^||, and Wei-Jun Yang¹

From the Institute of Cell Biology and Genetics, College of Life Sciences, Zhejiang University, Zhejiang 310058, China, College of Life Sciences, Nankai University, Tianjin 300071, China, ^¶Institute of Oceanology, Chinese Academy of Sciences, Shandong 266071, China, and ^||Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo 113-8657, Japan

Artemia has evolved a unique developmental pattern of encysted embryos to cope with various environmental threats. Cell divisions totally cease during the preemergence developmental stage from gastrula to prenauplius. The molecular mechanism of this, however, remains unknown. Our study focuses on the involvement of p90 ribosomal S6 kinase (RSK), a family of serine/threonine kinase-mediating signal transduction downstream of mitogen-activated protein kinase cascades, in the termination of cell cycle arrest during the post-embryonic development of Artemia-encysted gastrula. With immunochemistry, morphology, and cell cycle analysis, the identified Artemia RSK was established to be specifically activated during the post-embryonic and early larval developmental stages when arrested cells of encysted embryos resumed mitoses. In vivo knockdown of RSK activity by RNA interference, kinase inhibition, and antibody neutralization consistently induced defective larvae with distinct gaps between the exoskeleton and internal tissues. In these abnormal individuals, mitoses were detected to be largely inhibited in the affected regions. These results display the requirement of RSK activity during Artemia development and suggest its role in termination of cell cycle (G₂/M phase) arrest and promotion of mitogenesis. Our findings may, thus, provide insights into the regulation of cell division during Artemia post-embryonic development and reveal further aspects of RSK functions.

Received for publication, September 19, 2007 , and in revised form, November 1, 2007.

The nucleotide sequence(s) reported in this paper has been submitted to the Gen-Bank^TM/EBI Data Bank with accession number(s) EF427895.

^* This work was supported by National Natural Sciences Foundation of China Grant 30225034. 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: Institute of Cell Biology and Genetics, College of Life Sciences, Zhejiang University, Zijingang Campus, Hangzhou, Zhejiang 310058, China. Tel.: 86-0571-88273176; Fax: 86-0571-88273176; E-mail: w_jyang{at}cls.zju.edu.cn.

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