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J. Biol. Chem., Vol. 278, Issue 48, 48422-48433, November 28, 2003

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In Vitro Development of Mouse Embryonic Stem Cells Lacking JNK/Stress-activated Protein Kinase-associated Protein 1 (JSAP1) Scaffold Protein Revealed Its Requirement during Early Embryonic Neurogenesis^*

Ping Xu, Katsuji Yoshioka¶, Daisuke Yoshimura, Yohei Tominaga, Tomoko Nishioka, Michihiko Ito||, and Yusaku Nakabeppu**

From the Division of Neurofunctional Genomics, Department of Immunobiology and Neuroscience, Medical Institute of Bioregulation, Kyushu University and CREST, Japan Science and Technology Corp., Fukuoka 812-8582, Japan, ^¶Division of Cell Cycle Regulation, Department of Molecular and Cellular Biology, Cancer Research Institute, Kanazawa University, Kanazawa, Ishikawa 920-0934, Japan, and ^||Department of Biosciences, School of Science, Kitasato University, Sagamihara, Kanagawa 228-8555, Japan

The Jsap1 gene encodes a scaffold protein for c-Jun N-terminal kinase cascades. We established c-Jun N-terminal kinase (JNK)/stress-activated protein kinase-associated protein 1 (JSAP1)-null mouse embryonic stem cell lines by homologous recombination. The JSAP1-null embryonic stem cells were viable, however, exhibited hyperplasia of the ectoderm during embryoid body formation, and spontaneously differentiated into neurons more efficiently than did wild type. The expression of components of c-Jun N-terminal kinase cascades and a subset of marker mRNAs during early embryogenesis was altered in the JSAP1-null mutants. Retinoic acid dramatically increased the expression of JSAP1 and JNK3, which were co-precipitated with anti-JNK3 in the neuroectoderm of wild type but not JSAP1-null embryoid bodies. In the neurons differentiated from the wild type embryoid bodies, JSAP1 was localized in the soma, neurites, and growth cone-like structure of the neurites, and neurite outgrowth from the JSAP1-null embryoid bodies was apparently less efficient than from wild type. JSAP1 and c-Jun N-terminal kinase 3 were coexpressed in the embryonic ectoderm of E7.5 mouse embryo, whereas Wnt1 and Pax2 were coexpressed with JSAP1 at the midbrain-hindbrain junction in E12.5 mouse embryo, thus suggesting that JSAP1 is required for early embryonic neurogenesis.

Received for publication, July 21, 2003 , and in revised form, August 26, 2003.

^* This work was supported in part by a grant-in-aid for Japan Society for the Promotion of Science fellows from the Ministry of Education, Culture, Sports, Science, and Technology of Japan for JSPS postdoctoral fellowships for foreign researchers 10098480 (to P. X.). 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.

^** To whom correspondence should be addressed. Tel.: 81-92-642-6800; Fax: 81-92-642-6791; E-mail: yusaku{at}bioreg.kyushu-u.ac.jp.

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