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Originally published In Press as doi:10.1074/jbc.M206021200 on July 12, 2002

J. Biol. Chem., Vol. 277, Issue 39, 36443-36448, September 27, 2002
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Trafficking of Ganglioside GD3 to Mitochondria by Tumor Necrosis Factor-alpha *

Carmen García-RuizDagger §, Anna ColellDagger , Albert Morales, María Calvo, Carlos Enrich, and José C. Fernández-Checa||**

From the Liver Unit, Instituto de Malalties Digestives, Hospital Clinic i Provincial, the  Department of Cell Biology, School of Medicine, University of Barcelona, Instituto de Investigaciones Biomédicas August Pi Suñer, Barcelona, 08036, Spain, and the || Department of Experimental Pathology, Instituto Investigaciones Biomédicas Barcelona, Consejo Superior de Investigaciones Científicas, Barcelona, 08036, Spain

The interaction of mitochondria with proapoptotic proteins activates apoptosis pathways. Previous findings have identified ganglioside GD3 (GD3) as an emerging apoptotic lipid intermediate that targets mitochondria in response to death signals. Using immunoelectron and laser scanning confocal microscopy, we characterize the trafficking of GD3 to mitochondria in response to tumor necrosis factor-alpha (TNF-alpha ) in rat hepatocytes. In control hepatocytes, GD3 is present predominantly at the plasma membrane as well as in the endosomal/Golgi network, as verified by its colocalization with the asialoglycoprotein receptor. Following TNF-alpha exposure, GD3 undergoes a rapid cellular redistribution with a gradual loss from the plasma membrane before its colocalization with mitochondria. This process is mimicked by acidic sphingomyelinase and ionizing radiation but not by neutral sphingomyelinase or staurosporin. TNF-alpha stimulated the colocalization of GD3 with early and late endosomal markers, Rab 5 and Rab 7, whereas perturbation of plasma membrane cholesterol or actin cytoskeleton or inhibition of glucosylceramide synthase prevented the trafficking of GD3 to mitochondria. Finally, prevention of the TNF-alpha -stimulated neosynthesis of GD3, cyclosporin A, and latrunculin A or filipin protected sensitized hepatocytes from TNF-alpha -mediated cell death. Thus, the intracellular redistribution and mitochondrial targeting of GD3 during TNF-alpha signaling occurs through actin cytoskeleton vesicular trafficking and contributes to TNF-alpha -mediated hepatocellular cell death.

* This work was supported in part by Grant P50 AA11999 from the Research Center for Liver and Pancreatic Diseases funded by the U. S. National Institute on Alcohol Abuse and Alcoholism, Plan Nacional de I+D Grants SAF 99-0138, SAF 2001-2118, and PM99-0166, and Fondo Investigaciones Sanitarias Grant FISS 00-907.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.

Dagger These authors contributed equally to the work.

§ A Sistema Nacional de Salud (SNS) investigator from the Fondo Investigaciones Sanitarias.

** To whom correspondence should be addressed: Liver Unit, Hospital Clinic i Provincial, Villarroel, 170, 08036 Barcelona, Spain. Fax: 34-93-451-5272; E-mail: checa229@yahoo.com.

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