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Originally published In Press as doi:10.1074/jbc.M211388200 on February 5, 2003

J. Biol. Chem., Vol. 278, Issue 16, 14134-14145, April 18, 2003
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Calcium Influx through Receptor-operated Channel Induces Mitochondria-triggered Paraptotic Cell Death*,

Enrique JambrinaDagger , Roberto AlonsoDagger §, Marta AlcaldeDagger , María del Carmen RodríguezDagger , Antonio Serrano, Carlos Martínez-A., Javier García-SanchoDagger , and Manuel IzquierdoDagger ||

From the Dagger  Instituto de Biología y Genética Molecular, CSIC-Universidad de Valladolid, Facultad de Medicina, Ramón y Cajal 7, 47005 Valladolid, Spain and the  Department of Immunology and Oncology, Centro Nacional de Biotecnología (CNB-CSIC), Campus de Cantoblanco, 28049 Madrid, Spain

We address the specific role of cytoplasmic Ca2+ overload as a cell death trigger by expressing a receptor-operated specific Ca2+ channel, vanilloid receptor subtype 1 (VR1), in Jurkat cells. Ca2+ uptake through the VR1 channel, but not capacitative Ca2+ influx stimulated by the muscarinic type 1 receptor, induced sustained intracellular [Ca2+] rises, exposure of phosphatidylserine, and cell death. Ca2+ influx was necessary and sufficient to induce mitochondrial damage, as assessed by opening of the permeability transition pore and collapse of the mitochondrial membrane potential. Ca2+-induced cell death was inhibited by ruthenium red, protonophore carbonyl cyanide m-chlorophenylhydrazone, or cyclosporin A treatment, as well as by Bcl-2 expression, indicating that this process requires mitochondrial calcium uptake and permeability transition pore opening. Cell death occurred without caspase activation, oligonucleosomal/50-kilobase pair DNA cleavage, or release of cytochrome c or apoptosis inducer factor from mitochondria, but it required oxidative/nitrative stress. Thus, Ca2+ influx triggers a distinct program of mitochondrial dysfunction leading to paraptotic cell death, which does not fulfill the criteria for either apoptosis or necrosis.

* This work was supported by grants from Ministerio de Ciencia y Tecnología/European Union and Plan Nacional de Investigación Científica, Desarrollo e Innovación Tecnológica (FEDER, 1FD97-1725-C02-01 and C02-02) and Comisión Interministerial de Ciencia y Tecnología, Spain, Grant SAF2000-0118-C03-02).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.

The on-line version of this article (available at http://www.jbc.org) contains a video file.

§ Recipient of a fellowship from the Spanish Ministerio de Ciencia y Tecnología.

|| To whom correspondence should be addressed. Tel.: 34-983-423000 (ext. 4589); E-mail: mizdo@ibgm.uva.es.

Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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