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Originally published In Press as doi:10.1074/jbc.M108410200 on November 7, 2001

J. Biol. Chem., Vol. 277, Issue 5, 3560-3567, February 1, 2002
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Misexpression of the Eyes Absent Family Triggers the Apoptotic Program*

S. Wesley ClarkDagger §, Brian E. FeeDagger , and John L. ClevelandDagger §

From the Dagger  Department of Biochemistry, St. Jude Children's Research Hospital, Memphis, Tennessee 38105 and the § Department of Molecular Sciences, The University of Tennessee Health Science Center, Memphis, Tennessee 38163

Genetic studies in Drosophila and mice have shown that eyes absent (eya) is an important and conserved transcriptional regulator of development. Along with eyeless/Pax6, sine oculis, and dachshund, eya genes function as master regulators in eye development and can induce ectopic eye formation. Furthermore, the loss-of-function mutants of these genes in the fly causes partial or complete loss of the compound eye, and this is associated with inappropriate apoptosis. Conversely, ectopic eyeless expression in the context of eyes absent or sine oculis mutations results in apoptosis, suggesting that the proper ratio of these factors regulates apoptosis. Here we report that enforced expression of fly eya or of one of its mammalian homologs, Eya2, triggers rapid apoptosis in interleukin-3-dependent 32D.3 murine myeloid cells, which express Eya family members but not Pax6. Eya-induced cell death overrides survival factors and has many features typical of apoptosis, including plasma and mitochondrial membrane changes and caspase activation. Eya-induced apoptosis is blocked by Bcl-2 overexpression but not by the broad-spectrum caspase inhibitor z-VAD.fmk, suggesting that mitochondria are a major target in Eya-induced apoptosis. These results support the concept that inappropriate changes in the steady state levels of Eya proteins may trigger programmed cell deaths during development.

* This work was supported by grants from National Institutes of Health, National Cancer Institute and National Institute of Diabetes and Digestive and Kidney Diseases (to J. L. C.). This work was also supported by the Cancer Center Support Grant CA-21765 and by the American Lebanese Syrian Associated Charities of St. Jude Children's Research Hospital.The costs of publication of this article were defrayed in part by the payment of page charges. The 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: Dept. of Biochemistry, St. Jude Children's Research Hospital, 332 N. Lauderdale, Memphis, TN 38105. Tel.: 901-495-2398; Fax: 901-525-8025; E-mail: john.cleveland@stjude.org.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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