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Originally published In Press as doi:10.1074/jbc.M104893200 on January 22, 2002

J. Biol. Chem., Vol. 277, Issue 14, 12237-12245, April 5, 2002
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tBID Homooligomerizes in the Mitochondrial Membrane to Induce Apoptosis*

Michal GrinbergDagger , Rachel SarigDagger , Yehudit ZaltsmanDagger , Dan FrumkinDagger , Nicholas Grammatikakis§, Eitan Reuveny, and Atan GrossDagger ||

From the Departments of Dagger  Biological Regulation and  Biological Chemistry, Weizmann Institute of Science, Rehovot 76100, Israel and the § Department of Microbiology and Immunology, Queen's University, Kingston, Ontario K7L 3N6, Canada

Activation of the tumor necrosis factor R1/Fas receptor results in the cleavage of cytosolic BID to truncated tBID. tBID translocates to the mitochondria to induce the oligomerization of BAX or BAK, resulting in the release of cytochrome c (Cyt c). Here we demonstrate that in tumor necrosis factor alpha -activated FL5.12 cells, tBID becomes part of a 45-kDa cross-linkable mitochondrial complex that does not include BAX or BAK. Using fluorescence resonance energy transfer analysis and co-immunoprecipitation, we demonstrate that tBID-tBID interactions occur in the mitochondria of living cells. Cross-linking experiments using a tBID-GST chimera indicated that tBID forms homotrimers in the mitochondrial membrane. To test the functional consequence of tBID oligomerization, we expressed a chimeric FKBP-tBID molecule. Enforced dimerization of FKBP-tBID by the bivalent ligand FK1012 resulted in Cyt c release, caspase activation, and apoptosis. Surprisingly, enforced dimerization of tBID did not result in the dimerization of either BAX or BAK. Moreover, a tBID BH3 mutant (G94E), which does not interact with or induce the dimerization of either BAX or BAK, formed the 45-kDa complex and induced both Cyt c release and apoptosis. Thus, tBID oligomerization may represent an alternative mechanism for inducing mitochondrial dysfunction and apoptosis.

* This work was supported in part by the Israel Science Foundation, Israel Cancer Research Fund, and a Leukemia and Lymphoma Society fellowship award (to A.G.).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. Tel.: 972-8-9343656; Fax: 972-8-9344116; E-mail: atan.gross@weizmann.ac.il.

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