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J. Biol. Chem., Vol. 279, Issue 40, 41594-41602, October 1, 2004

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A Cooperative Role for Atf1 and Pap1 in the Detoxification of the Oxidative Stress Induced by Glucose Deprivation in Schizosaccharomyces pombe^*

Marisa Madrid, Teresa Soto, Alejandro Franco, Vanessa Paredes, Jero Vicente, Elena Hidalgo¶, Mariano Gacto||, and José Cansado

From the Department of Genetics and Microbiology, Facultad de Biología, University of Murcia, 30071 Murcia, and the ^¶Cell Signaling Unit, Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, 08003 Barcelona, Spain

In Schizosaccharomyces pombe, glucose concentrations below a certain threshold trigger the stress-activated protein kinase (SAPK) signal transduction pathway and promote increased transcription of Atf1-dependent genes coding for the general stress response. Removal of glucose specifically induces the nuclear accumulation of green fluorescent protein-labeled Pap1 (GFP-Pap1) and the expression of genes dependent on this transcription factor. In contrast, depletion of the nitrogen source triggers the SAPK pathway but does not activate Pap1-dependent gene transcription, indicating that carbon stress rather than growth arrest leads to an endogenous oxidative condition that favors nuclear accumulation of Pap1. The reductant agents glutathione or N-acetylcysteine suppress the nuclear accumulation of GFP-Pap1 induced by glucose deprivation without inhibiting the activation of the MAPK Sty1. In addition, cells expressing a mutant GFP-Pap1 unable to accumulate into the nucleus upon hydrogen peroxide-mediated oxidative stress failed to show this protein into the nucleus in the absence of glucose. These results support the concept of a concerted action between the SAPK pathway and the Pap1 transcription factor during glucose exhaustion by which glucose limitation induces activation of the SAPK pathway prior to the oxidative stress caused by glucose deprivation. The ensuing induction of Atf1-dependent genes (catalase) decreases the level of hydroperoxides allowing Pap1 nuclear accumulation and function. Congruent with this interpretation, glucose-depleted cells show higher adaptive response to exogenous oxidative stress than those maintained in the presence of glucose.

Received for publication, May 18, 2004 , and in revised form, July 2, 2004.

^* This work was supported in part by Grant BMC 2002-01104 from the Ministerio de Ciencia y Tecnología (MCYT, Spain) (to J. C.). 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.

A predoctoral fellow from the Ministerio de Educación, Cultura y Deporte (Spain).

^|| To whom correspondence should be addressed: Dept. of Genetics and Microbiology, Facultad de Biología, University of Murcia, Campus Universitario de Espinardo, 30071 Murcia, Spain. Tel.: 34-968367132; Fax: 34-968363963; E-mail: maga{at}um.es.

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