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Molecular and Cellular Biology, April 2005, p. 3140-3150, Vol. 25, No. 8
0270-7306/05/$08.00+0     doi:10.1128/MCB.25.8.3140-3150.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Wing-to-Leg Homeosis by Spineless Causes Apoptosis Regulated by Fish-lips, a Novel Leucine-Rich Repeat Transmembrane Protein{dagger}

Takashi Adachi-Yamada,1,2,3*,{ddagger} Toshiyuki Harumoto,2,{ddagger} Kayoko Sakurai,4,{ddagger} Ryu Ueda,5 Kaoru Saigo,6 Michael B. O'Connor,7,8 and Hiroshi Nakato4,7*

Department of Earth and Planetary System Sciences, Graduate School of Science and Technology,1 Department of Sciences for Natural Environment, Faculty of Human Development, SORST,2 Japan Science and Technology Agency, Kobe University, Kobe,3 Department of Biology, Faculty of Science, Tokyo Metropolitan University, Hachioji,4 Genetic Strains Research Center, National Institute of Genetics, Mishima,5 Department of Biophysics and Biochemistry, Graduate School of Science, University of Tokyo, Tokyo, Japan,6 Department of Genetics, Cell Biology, and Development,7 Howard Hughes Medical Institute, University of Minnesota, Minneapolis, Minnesota8

Received 24 May 2004/ Returned for modification 6 July 2004/ Accepted 21 December 2004

Growth, patterning, and apoptosis are mutually interactive during development. For example, cells that select an abnormal fate in a developing field are frequently removed by apoptosis. An important issue in this process that needs to be resolved is the mechanism used by cells to discern their correct fate from an abnormal fate. In order to examine this issue, we developed an animal model that expresses the dioxin receptor homolog Spineless (Ss) ectopically in the Drosophila wing. The presence of mosaic clones ectopically expressing ss results in a local transformation of organ identity, homeosis, from wing into a leg or antenna. The cells with misspecified fates subsequently activate c-Jun N-terminal kinase to undergo apoptosis in an autonomous or nonautonomous manner depending on their position within the wing, suggesting that a cell-cell interaction is, at least in some cases, involved in the detection of misspecified cells. Similar position dependence is commonly observed when various homeotic genes controlling the body segments are ectopically expressed. The autonomous and nonautonomous apoptosis caused by ss is regulated by a novel leucine-rich repeat family transmembrane protein, Fish-lips (Fili) that interacts with surrounding normal cells. These data support a mechanism in which the lack of some membrane proteins helps to recognize the presence of different cell types and direct these cells to an apoptotic fate in order to exclude them from the normal developing field.

* Corresponding authors. Mailing address for T. Adachi-Yamada: Department of Earth and Planetary System Sciences, Graduate School of Science and Technology, Kobe University, Kobe 657-8501, Japan. Phone: 81-78-803-7743. Fax: 81-78-803-7743. E-mail: yamadach{at}kobe-u.ac.jp. Mailing address for H. Nakato: Department of Genetics, Cell Biology, and Development, University of Minnesota, Minneapolis, MN 55455. Phone: (612) 625-1727. Fax: (612) 626-5652. E-mail: nakat003{at}umn.edu.

{dagger} Supplemental material for this article may be found at http://mcb.asm.org/.

{ddagger} T.A.-Y., T.H., and K.S. contributed equally to this study.

Molecular and Cellular Biology, April 2005, p. 3140-3150, Vol. 25, No. 8
0022-538X/05/$08.00+0     doi:10.1128/MCB.25.8.3140-3150.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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