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J. Biol. Chem., Vol. 279, Issue 46, 48404-48409, November 12, 2004

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Autophagy Gene Disruption Reveals a Non-vacuolar Cell Death Pathway in Dictyostelium^*

Artemis Kosta, Céline Roisin-Bouffay¶||, Marie-Françoise Luciani¶, Grant P. Otto**, Richard H. Kessin**, and Pierre Golstein

From the Centre d'Immunologie INSERM/CNRS/Université de la Mediterranée de Marseille-Luminy, Case 906, Avenue de Luminy, 13288 Marseille Cedex 9, France and the ^**Department of Anatomy and Cell Biology, Columbia University, New York, New York 10032

Types of cell death include apoptosis, necrosis, and autophagic cell death. The latter can be defined as death of cells containing autophagosomes, autophagic bodies, and/or vacuoles. Are autophagy and vacuolization causes, consequences, or side effects in cell death with autophagy? Would control of autophagy suffice to control this type of cell death? We disrupted the atg1 autophagy gene in Dictyostelium discoideum, a genetically tractable model for developmental autophagic vacuolar cell death. The procedure that induced autophagy, vacuolization, and death in wild-type cells led in atg1 mutant cells to impaired autophagy and to no vacuolization, demonstrating that atg1 is required for vacuolization. Unexpectedly, however, cell death still took place, with a non-vacuolar and centrally condensed morphology. Thus, a cell death mechanism that does not require vacuolization can operate in this cell death model showing conspicuous vacuolization. The revelation of non-vacuolar cell death in this protist by autophagy gene disruption is reminiscent of caspase inhibition revealing necrotic cell death in animal cells. Thus, hidden alternative cell death pathways may be found across kingdoms and for diverse types of cell death.

Received for publication, August 4, 2004 , and in revised form, August 11, 2004.

^* This work was supported by institutional grants from INSERM and CNRS and specific grants from Association pour la Recherche contre le Cancer, Ministere de la Recherche et de la Technologie, and the European Community 5th Framework Program. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Supported by an INSERM poste vert.

^¶ Both authors contributed equally to this work.

^|| Supported by the European Community.

To whom correspondence should be addressed: Centre d'Immunologie INSERM/CNRS/Université de la Mediterranée, Case 906, Campus de Luminy, Ave. de Luminy, 13288 Marseille Cedex 9, France. Tel.: 33-0-4-91-26-94-68; Fax: 33-0-4-91-26-94-30; E-mail: golstein{at}ciml.univ-mrs.fr.

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