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J. Biol. Chem., Vol. 279, Issue 23, 24514-24520, June 4, 2004

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Chicken Leukemia Inhibitory Factor Maintains Chicken Embryonic Stem Cells in the Undifferentiated State^*

Hiroyuki Horiuchi¶, Airo Tategaki||, Yusuke Yamashita, Hikaru Hisamatsu, Mari Ogawa||, Takashi Noguchi, Masayoshi Aosasa||, Tsuyoshi Kawashima||, Sachiko Akita, Norihisa Nishimichi, Naoko Mitsui**, Shuichi Furusawa, and Haruo Matsuda

From the Department of Molecular and Applied Biosciences, Graduate School of Biosphere Science, Laboratory of Immunobiology, Hiroshima University, Higashi-Hiroshima 739-8528, Japan, the ^||Hiroshima Prefectural Institute of Industrial Science and Technology, Hiroshima Industrial Promotion Organization, 3-10-32 Kagamiyama, Higashi-Hiroshima 739-0046, Japan, and the ^**Research and Development Institute, Towakagaku Co. Ltd., 3-13-26 Kagamiyama, Higashi-Hiroshima, 739-0046, Japan

Mouse embryonic stem (ES) cells can be maintained in an undifferentiated state in the presence of leukemia inhibitory factor (LIF), a member of the interleukin-6 cytokine family. In other mammals, this is not possible with LIF alone. Chicken ES-like cells (blastodermal cells) have only been cultured with mouse LIF because chicken LIF was not available. However the culture system is imperfect and chicken ES-like cells equivalent to mouse ES cells were not observed. In the present study, we cloned the cDNA-encoding chicken LIF using mRNA subtraction and RACE methodology. The chicken LIF cDNA encodes a protein with 40% sequence identity to mouse LIF. It has 211 amino acids including a putative N-terminal signal peptide of 24 residues. Chicken blastodermal cells were cultured in the presence of bacterially expressed chicken LIF or mouse LIF. The expression of alkaline phosphatase and embryonal carcinoma cell monoclonal antibody-1 and stage-specific embryonic antigen-1 and the activation of STAT3 were examined, all of which are indices of the undifferentiated state. Exposure in the blastodermal cells to recombinant chicken LIF but not to mouse LIF maintained the expression of these various markers. After 9 days of incubation, the blastodermal cells formed cystic embryoid bodies in the presence of mouse LIF but not in the presence of recombinant chicken LIF. We conclude that chicken LIF is able to maintain chicken ES cell cultures in the undifferentiated state.

Received for publication, December 4, 2003 , and in revised form, March 11, 2004.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) BD187371.

^* This work was supported by grants-in-aid for Cooperative Link of Unique Science and Technology for Economy Revitalization from the Ministry of Education, Culture, Sports, Science and Technology of Japan, the Biotechnology Cluster in Central Hiroshima of Hiroshima Prefecture in Japan, and the Program for Promotion of Basic Research Activities for Innovative Biosciences 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.

These authors contributed equally to this work.

^¶ To whom correspondence should be addressed: Dept. of Molecular and Applied Biosciences, Laboratory of Immunobiology, Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima 739-8528, Japan. Tel./Fax: 81-824-24-7970; E-mail: hhori10{at}Hiroshima-u.ac.jp.

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