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J. Biol. Chem., Vol. 281, Issue 4, 2033-2043, January 27, 2006

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Stress-induced Response, Localization, and Regulation of the Pmk1 Cell Integrity Pathway in Schizosaccharomyces pombe^*

Marisa Madrid1, Teresa Soto, Hou Keat Khong2, Alejandro Franco3, Jero Vicente, Pilar Pérez, Mariano Gacto4, and José Cansado

From the Departamento de Genética y Microbiología, University of Murcia, Murcia 30071, Spain and Instituto de Microbiología Bioquímica, CSIC/Departamento de Microbiología y Genética, University of Salamanca, Salamanca 37007, Spain

Mitogen-activated protein kinase (MAPK) signaling pathways are critical for the sensing and response of eukaryotic cells to extracellular changes. In Schizosaccharomyces pombe, MAPK Pmk1/Spm1 has been involved in cell wall construction, morphogenesis, cytokinesis, and ion homeostasis, as part of the so-called cell integrity pathway together with MAPK kinase kinase Mkh1 and MAPK kinase Pek1. We show that Pmk1 is activated in multiple stress situations, including hyper- or hypotonic stress, glucose deprivation, presence of cell wall-damaging compounds, and oxidative stress induced by hydrogen peroxide or pro-oxidants. The stress-induced activation of Pmk1 was completely dependent on Mkh1 and Pek1 function, supporting a nonbranched pathway in the regulation of MAPK activation. Fluorescence microscopy revealed that Mkh1, Pek1, and Pmp1 (a protein phosphatase that inactivates Pmk1) are cytoplasmic proteins. Mkh1 and Pek1 were also found at the septum, whereas Pmk1 localized in both cytoplasm and nucleus as well as in the mitotic spindle and septum during cytokinesis. Interestingly, Pmk1 subcellular localization was unaffected by stress or the absence of Mkh1 and Pek1, suggesting that its activation by the Mkh1-Pek1 cascade takes place at the cytoplasm and/or septum and that the active and inactive forms of this kinase cross the nuclear membrane. Cdc42 GTPase and its effectors, p21-activated kinases Pak2 and Pak1, are not upstream elements controlling the basal level or the stress-induced activation of Pmk1. However, Sty1 MAPK was essential for proper Pmk1 deactivation after hypertonic stress in a process regulated by Atf1 transcription factor. These results provide the first evidence for the existence of cross-talk between two MAPK cascades during the stress response in fission yeast.

Received for publication, June 14, 2005 , and in revised form, November 16, 2005.

^* This work was supported in part by Ministerio de Educación y Ciencia (Spain) Grant BFU2005-01401/BMC (to J. C.) and Fundación Séneca (Spain) Grant 00475/PI/04. 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.

¹ Fellow of the Ministerio de Educación, Cultura y Deporte.

² Fellow of the Agencia Española de Cooperación Internacional (Spain).

³ Present address: Division of Yeast Genetics, National Institute for Medical Research, London NW7 1AA, United Kingdom.

⁴ To whom correspondence should be addressed: Dept. of Genetics and Microbiology, Facultad de Biología, University of Murcia, Campus Universitario de Espinardo, Murcia 30071, Spain. Tel.: 34-968367132; Fax: 34-968363963; E-mail: maga{at}um.es.

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