Cadmium affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity

Authors

  • LIONEL GARNIER,

    1. Commissariat à l’Energie Atomique, Centre de Cadarache, DSV-DEVM, Laboratoire de Radiobiologie Végétale, 13108 Saint-Paul lez Durance Cedex, France,
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  • FRANÇOISE SIMON-PLAS,

    1. Laboratoire de Phytopharmacie et de Biochimie des Interactions Cellulaires, UMR 692, Institut National de la Recherche Agronomique, 21065 Dijon, Cedex, France and
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  • PATRICE THULEAU,

    1. Signaux et Messages Cellulaires chez les Végétaux, Centre National de la Recherche Scientifique, Université Paul Sabatier UMR5546, BP 17 Auzeville, F-31326 Castanet-Tolosan, France
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  • JEAN-PIERRE AGNEL,

    1. Commissariat à l’Energie Atomique, Centre de Cadarache, DSV-DEVM, Laboratoire de Radiobiologie Végétale, 13108 Saint-Paul lez Durance Cedex, France,
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  • JEAN-PIERRE BLEIN,

    1. Laboratoire de Phytopharmacie et de Biochimie des Interactions Cellulaires, UMR 692, Institut National de la Recherche Agronomique, 21065 Dijon, Cedex, France and
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  • RAOUL RANJEVA,

    1. Signaux et Messages Cellulaires chez les Végétaux, Centre National de la Recherche Scientifique, Université Paul Sabatier UMR5546, BP 17 Auzeville, F-31326 Castanet-Tolosan, France
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  • JEAN-LUC MONTILLET

    Corresponding author
    1. Commissariat à l’Energie Atomique, Centre de Cadarache, DSV-DEVM, Laboratoire de Radiobiologie Végétale, 13108 Saint-Paul lez Durance Cedex, France,
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Jean-Luc Montillet. Fax: +33 4 42 25 23 64; e-mail: jean-luc.montillet@cea.fr

ABSTRACT

Cadmium is suspected to exert its toxic action on cells through oxidative damage. However, the transition metal is unable to directly generate reactive oxygen species (ROS) via redox reactions with molecular oxygen in a biological environment. Here, we show that bright yellow-2 (BY-2) tobacco cells exposed to millimolar concentrations of CdCl2 developed cell death within 2–3 h. The death process was preceded by two successive waves of ROS differing in their nature and subcellular localization. Firstly, these consisted in the transient NADPH oxidase-dependent accumulation of H2O2 followed by the accumulation of O2−. in mitochondria. A third wave of ROS consisting in fatty acid hydroperoxide accumulation was concomitant with cell death. Accumulation of H2O2 was preceded by an increase in cytosolic free calcium concentration originating from internal pools that was essential to activate the NADPH oxidase. The cell line gp3, impaired in NADPH oxidase activity, and that was unable to accumulate H2O2 in response to Cd2+, was nevertheless poisoned by the metal. Therefore, this first wave of ROS was not sufficient to trigger all the cadmium-dependent deleterious effects. However, we show that the accumulation of O2−. of mitochondrial origin and membrane peroxidation are key players in Cd2+-induced cell death.

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