This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Mulet, J. M.
Right arrow Articles by Serrano, R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Mulet, J. M.
Right arrow Articles by Serrano, R.

 Previous Article  |  Next Article 

Molecular and Cellular Biology, May 1999, p. 3328-3337, Vol. 19, No. 5
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

A Novel Mechanism of Ion Homeostasis and Salt Tolerance in Yeast: the Hal4 and Hal5 Protein Kinases Modulate the Trk1-Trk2 Potassium Transporter

Jose M. Mulet,1 Martin P. Leube,1,dagger Stephen J. Kron,2,Dagger Gabino Rios,1 Gerald R. Fink,2 and Ramon Serrano1,*

Instituto de Biologia Molecular y Celular de Plantas, Universidad Politecnica de Valencia-C.S.I.C., 46022 Valencia, Spain,1 and Whitehead Institute for Biomedical Research, Cambridge, Massachusetts 02142-14792

Received 20 November 1998/Returned for modification 22 December 1998/Accepted 28 January 1999

The regulation of intracellular ion concentrations is a fundamental property of living cells. Although many ion transporters have been identified, the systems that modulate their activity remain largely unknown. We have characterized two partially redundant genes from Saccharomyces cerevisiae, HAL4/SAT4 and HAL5, that encode homologous protein kinases implicated in the regulation of cation uptake. Overexpression of these genes increases the tolerance of yeast cells to sodium and lithium, whereas gene disruptions result in greater cation sensitivity. These phenotypic effects of the mutations correlate with changes in cation uptake and are dependent on a functional Trk1-Trk2 potassium transport system. In addition, hal4 hal5 and trk1 trk2 mutants exhibit similar phenotypes: (i) they are deficient in potassium uptake; (ii) their growth is sensitive to a variety of toxic cations, including lithium, sodium, calcium, tetramethylammonium, hygromycin B, and low pH; and (iii) they exhibit increased uptake of methylammonium, an indicator of membrane potential. These results suggest that the Hal4 and Hal5 protein kinases activate the Trk1-Trk2 potassium transporter, increasing the influx of potassium and decreasing the membrane potential. The resulting loss in electrical driving force reduces the uptake of toxic cations and improves salt tolerance. Our data support a role for regulation of membrane potential in adaptation to salt stress that is mediated by the Hal4 and Hal5 kinases.

* Corresponding author. Mailing address: Instituto de Biologia Molecular y Celular de Plantas, Universidad Politecnica de Valencia-C.S.I.C., Camino de Vera s/n, 46022 Valencia, Spain. Phone: 34-96-3877860. Fax: 34-96-3877859. E-mail: serrano{at}ibmcp.upv.es.

dagger Present address: PlantTec Biotechnologie GmbH, 14473 Potsdam, Germany.

Dagger Present address: Center for Molecular Oncology, University of Chicago, Chicago, IL 60637-5419.

Molecular and Cellular Biology, May 1999, p. 3328-3337, Vol. 19, No. 5
0270-7306/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Paumi, C. M., Chuk, M., Chevelev, I., Stagljar, I., Michaelis, S. (2008). Negative Regulation of the Yeast ABC Transporter Ycf1p by Phosphorylation within Its N-terminal Extension. J. Biol. Chem. 283: 27079-27088 [Abstract] [Full Text]  
  • Fulgenzi, F. R., Peralta, M. L., Mangano, S., Danna, C. H., Vallejo, A. J., Puigdomenech, P., Santa-Maria, G. E. (2008). The Ionic Environment Controls the Contribution of the Barley HvHAK1 Transporter to Potassium Acquisition. Plant Physiol. 147: 252-262 [Abstract] [Full Text]  
  • Morton, C. O., Hayes, A., Wilson, M., Rash, B. M., Oliver, S. G., Coote, P. (2007). Global Phenotype Screening and Transcript Analysis Outlines the Inhibitory Mode(s) of Action of Two Amphibian-Derived, {alpha}-Helical, Cationic Peptides on Saccharomyces cerevisiae. Antimicrob. Agents Chemother. 51: 3948-3959 [Abstract] [Full Text]  
  • Perez-Valle, J., Jenkins, H., Merchan, S., Montiel, V., Ramos, J., Sharma, S., Serrano, R., Yenush, L. (2007). Key Role for Intracellular K+ and Protein Kinases Sat4/Hal4 and Hal5 in the Plasma Membrane Stabilization of Yeast Nutrient Transporters. Mol. Cell. Biol. 27: 5725-5736 [Abstract] [Full Text]  
  • Ali, R., Zielinski, R. E., Berkowitz, G. A. (2006). Expression of plant cyclic nucleotide-gated cation channels in yeast. J Exp Bot 57: 125-138 [Abstract] [Full Text]  
  • Yenush, L., Merchan, S., Holmes, J., Serrano, R. (2005). pH-Responsive, Posttranslational Regulation of the Trk1 Potassium Transporter by the Type 1-Related Ppz1 Phosphatase. Mol. Cell. Biol. 25: 8683-8692 [Abstract] [Full Text]  
  • Thornton, G., Wilkinson, C. R. M., Toone, W. M., Jones, N. (2005). A novel pathway determining multidrug sensitivity in Schizosaccharomyces pombe. GENES CELLS 10: 941-951 [Abstract] [Full Text]  
  • Manlandro, C. M. A., Haydon, D. H., Rosenwald, A. G. (2005). Ability of Sit4p To Promote K+ Efflux via Nha1p Is Modulated by Sap155p and Sap185p. Eukaryot Cell 4: 1041-1049 [Abstract] [Full Text]  
  • Wang, L.-y., Shimada, K., Morishita, M., Shiozaki, K. (2005). Response of Fission Yeast to Toxic Cations Involves Cooperative Action of the Stress-Activated Protein Kinase Spc1/Sty1 and the Hal4 Protein Kinase. Mol. Cell. Biol. 25: 3945-3955 [Abstract] [Full Text]  
  • Kim, S.-Y., Craig, E. A. (2005). Broad Sensitivity of Saccharomyces cerevisiae Lacking Ribosome-Associated Chaperone Ssb or Zuo1 to Cations, Including Aminoglycosides. Eukaryot Cell 4: 82-89 [Abstract] [Full Text]  
  • Lisman, Q., Urli-Stam, D., Holthuis, J. C. M. (2004). HOR7, a Multicopy Suppressor of the Ca2+-induced Growth Defect in Sphingolipid Mannosyltransferase-deficient Yeast. J. Biol. Chem. 279: 36390-36396 [Abstract] [Full Text]  
  • Li, M., Martin, S. J., Bruno, V. M., Mitchell, A. P., Davis, D. A. (2004). Candida albicans Rim13p, a Protease Required for Rim101p Processing at Acidic and Alkaline pHs. Eukaryot Cell 3: 741-751 [Abstract] [Full Text]  
  • Munson, A. M., Haydon, D. H., Love, S. L., Fell, G. L., Palanivel, V. R., Rosenwald, A. G. (2004). Yeast ARL1 encodes a regulator of K+ influx. J. Cell Sci. 117: 2309-2320 [Abstract] [Full Text]  
  • Ali, R., Brett, C. L., Mukherjee, S., Rao, R. (2004). Inhibition of Sodium/Proton Exchange by a Rab-GTPase-activating Protein Regulates Endosomal Traffic in Yeast. J. Biol. Chem. 279: 4498-4506 [Abstract] [Full Text]  
  • Merchan, S., Bernal, D., Serrano, R., Yenush, L. (2004). Response of the Saccharomyces cerevisiae Mpk1 Mitogen-Activated Protein Kinase Pathway to Increases in Internal Turgor Pressure Caused by Loss of Ppz Protein Phosphatases. Eukaryot Cell 3: 100-107 [Abstract] [Full Text]  
  • Matsumoto, T. K., Ellsmore, A. J., Cessna, S. G., Low, P. S., Pardo, J. M., Bressan, R. A., Hasegawa, P. M. (2002). An Osmotically Induced Cytosolic Ca2+ Transient Activates Calcineurin Signaling to Mediate Ion Homeostasis and Salt Tolerance of Saccharomyces cerevisiae. J. Biol. Chem. 277: 33075-33080 [Abstract] [Full Text]  
  • Williams-Hart, T., Wu, X., Tatchell, K. (2002). Protein Phosphatase Type 1 Regulates Ion Homeostasis in Saccharomyces cerevisiae. Genetics 160: 1423-1437 [Abstract] [Full Text]  
  • De Craene, J.-O., Soetens, O., Andre, B. (2001). The Npr1 Kinase Controls Biosynthetic and Endocytic Sorting of the Yeast Gap1 Permease. J. Biol. Chem. 276: 43939-43948 [Abstract] [Full Text]  
  • Erez, O., Kahana, C. (2001). Screening for Modulators of Spermine Tolerance Identifies Sky1, the SR Protein Kinase of Saccharomyces cerevisiae, as a Regulator of Polyamine Transport and Ion Homeostasis. Mol. Cell. Biol. 21: 175-184 [Abstract] [Full Text]  
  • Goossens, A., de la Fuente, N., Forment, J., Serrano, R., Portillo, F. (2000). Regulation of Yeast H+-ATPase by Protein Kinases Belonging to a Family Dedicated to Activation of Plasma Membrane Transporters. Mol. Cell. Biol. 20: 7654-7661 [Abstract] [Full Text]  
  • Siniossoglou, S., Hurt, E. C., Pelham, H. R. B. (2000). Psr1p/Psr2p, Two Plasma Membrane Phosphatases with an Essential DXDX(T/V) Motif Required for Sodium Stress Response in Yeast. J. Biol. Chem. 275: 19352-19360 [Abstract] [Full Text]  
  • Masuda, C. A., Ramirez, J., Pena, A., Montero-Lomeli, M. (2000). Regulation of Monovalent Ion Homeostasis and pH by the Ser-Thr Protein Phosphatase SIT4 in Saccharomyces cerevisiae. J. Biol. Chem. 275: 30957-30961 [Abstract] [Full Text]  
  • Simon, E., Clotet, J., Calero, F., Ramos, J., Arino, J. (2001). A Screening for High Copy Suppressors of the sit4 hal3 Synthetically Lethal Phenotype Reveals a Role for the Yeast Nha1 Antiporter in Cell Cycle Regulation. J. Biol. Chem. 276: 29740-29747 [Abstract] [Full Text]  
  • Goossens, A., Dever, T. E., Pascual-Ahuir, A., Serrano, R. (2001). The Protein Kinase Gcn2p Mediates Sodium Toxicity in Yeast. J. Biol. Chem. 276: 30753-30760 [Abstract] [Full Text]  
  • Crespo, J. L., Daicho, K., Ushimaru, T., Hall, M. N. (2001). The GATA Transcription Factors GLN3 and GAT1 Link TOR to Salt Stress in Saccharomyces cerevisiae. J. Biol. Chem. 276: 34441-34444 [Abstract] [Full Text]  
  • Halfter, U., Ishitani, M., Zhu, J.-K. (2000). The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc. Natl. Acad. Sci. USA 97: 3735-3740 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»