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Molecular and Cellular Biology, August 2000, p. 5454-5468, Vol. 20, No. 15
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

BNIP3 and Genetic Control of Necrosis-Like Cell Death through the Mitochondrial Permeability Transition Pore

C. Vande Velde,1 J. Cizeau,1 D. Dubik,1 J. Alimonti,1 T. Brown,1 S. Israels,1 R. Hakem,2 and A. H. Greenberg1,*

The Manitoba Institute of Cell Biology, University of Manitoba, Winnipeg, Manitoba R3E 0V9,1 and The Amgen Institute, Ontario Cancer Institute, University of Toronto, Toronto, Ontario M5G 2C1,2 Canada

Received 7 January 2000/Returned for modification 22 February 2000/Accepted 3 May 2000

Many apoptotic signaling pathways are directed to mitochondria, where they initiate the release of apoptogenic proteins and open the proposed mitochondrial permeability transition (PT) pore that ultimately results in the activation of the caspase proteases responsible for cell disassembly. BNIP3 (formerly NIP3) is a member of the Bcl-2 family that is expressed in mitochondria and induces apoptosis without a functional BH3 domain. We report that endogenous BNIP3 is loosely associated with mitochondrial membrane in normal tissue but fully integrates into the mitochondrial outer membrane with the N terminus in the cytoplasm and the C terminus in the membrane during induction of cell death. Surprisingly, BNIP3-mediated cell death is independent of Apaf-1, caspase activation, cytochrome c release, and nuclear translocation of apoptosis-inducing factor. However, cells transfected with BNIP3 exhibit early plasma membrane permeability, mitochondrial damage, extensive cytoplasmic vacuolation, and mitochondrial autophagy, yielding a morphotype that is typical of necrosis. These changes were accompanied by rapid and profound mitochondrial dysfunction characterized by opening of the mitochondrial PT pore, proton electrochemical gradient (Delta psi m) suppression, and increased reactive oxygen species production. The PT pore inhibitors cyclosporin A and bongkrekic acid blocked mitochondrial dysregulation and cell death. We propose that BNIP3 is a gene that mediates a necrosis-like cell death through PT pore opening and mitochondrial dysfunction.

* Corresponding author. Mailing address: Manitoba Institute of Cell Biology, University of Manitoba, 100 Olivia Street, Winnipeg, MB R3E 0V9, Canada. Phone: (204) 787-2112. Fax: (204) 787-2190. E-mail: agreenb{at}cc.umanitoba.ca.

Molecular and Cellular Biology, August 2000, p. 5454-5468, Vol. 20, No. 15
0270-7306/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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