Potassium deprivation is sufficient to induce a cell death program in Saccharomyces cerevisiae

FEMS Yeast Research

Volumn 10, Issue 5, 2010, Pages 497-507

  Lauff, Diana Beatríz ^a   Santa María, Guillermo E ^a  

^a INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

Author keywords

apoptosis; potassium transport; programmed cell death; Saccharomyces cerevisiae; TRK

Indexed keywords

CALCIUM; CARRIER PROTEIN; CASPASE; EGTAZIC ACID; LIPOCORTIN 5; PHOSPHATIDYLSERINE; PROPIDIUM IODIDE; PROTEIN TRK1; PROTEIN TRK2; PROTEIN YCA1; REACTIVE OXYGEN METABOLITE; RUBIDIUM; SACCHAROMYCES CEREVISIAE PROTEIN; UNCLASSIFIED DRUG; CATION TRANSPORT PROTEIN; CHROMATIN; POTASSIUM; TRK1 PROTEIN, S CEREVISIAE; TRK2 PROTEIN, S CEREVISIAE;

APOPTOSIS; ARTICLE; CALCIUM HOMEOSTASIS; CELL MEMBRANE; CELL MEMBRANE POTENTIAL; CELL VACUOLE; CHROMATIN CONDENSATION; DNA FRAGMENTATION; FUNGUS GROWTH; GENE DELETION; HYPERPOLARIZATION; NONHUMAN; POTASSIUM DEPLETION; POTASSIUM RESTRICTION; POTASSIUM TRANSPORT; SACCHAROMYCES CEREVISIAE; YEAST CELL; CELL DEATH; CHEMISTRY; CHROMATIN; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY;

CALCIUM; CATION TRANSPORT PROTEINS; CELL DEATH; CELL MEMBRANE; CHROMATIN; DNA FRAGMENTATION; GENE DELETION; PHOSPHATIDYLSERINES; POTASSIUM; REACTIVE OXYGEN SPECIES; RUBIDIUM; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 77954475188     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2010.00628.x     Document Type: Article

References (43)

1. Aerts AM, Zabrocki P, François IE et al 2008) Ydc1p ceramidase triggers organelle fragmentation, apoptosis and accelerated ageing in yeast. Cell Mol Life Sci 65 : 1933 1942.
2. Aiking H Tempest DW (1977) Rubidium as a probe for function and transport of potassium in the yeast Candida utilis NCYC 321, grown in chemostat culture. Arch Microbiol 115 : 215 221. (Pubitemid 8222695)
3. + efflux. Antimicrob Agents Ch 52 : 4081 4088.
4. Baev D, Rivetta A, Vylkova S, Sun JN, Zeng GF, Slayman CL Edgerton M (2004) The TRK1 potassium transporter is the critical effector for killing of Candida albicans by the cationic protein, Histatin 5. J Biol Chem 279 : 55060 55072.
5. Bertl A, Ramos J, Ludwig J, Lichtenberg-Fraté H, Reid J, Bihler H, Calero F, Martínez P Ljungdahl PO (2003) Characterization of potassium transport in wild-type and isogenic yeast strains carrying all combinations of trk1, trk2 and tok1 null mutations. Mol Microbiol 47 : 767 780.
6. Bortner CD Cidlowski JA (2007) Cell shrinkage and monovalent cation fluxes: role in apoptosis. Arch Biochem Biophys 462 : 176 188.
7. Camacho M, Ramos J Rodríguez-Navarro A (1981) Potassium requirements of Saccharomyces cerevisiae. Curr Microbiol 6 : 295 299.
8. + transporter from the Trk family in the ectomycorrhizal fungus Hebeloma cylindrosporum. J Biol Chem 282 : 26057 26066.
9. dos Santos Sant'Ana G, da Silva Paes L, Vieira Paiva AF et al 2009) Protective effect of ions against cell death induced by acid stress in Saccharomyces. FEMS Yeast Res 9 : 701 712.
10. 2+ driven by the membrane potential in energy-depleted yeast cells. J Gen Microbiol 133 : 1641 1649.
11. Gaber R, Styles CA Fink GR (1988) TRK1 encodes a plasma membrane protein required for high affinity potassium transport in Saccharomyces cerevisiae. Mol Cell Biol 8 : 2848 2859.
12. Guaragnella N, Pereira C, Sousa MJ, Antonacci L, Passarella S, Côrte-Real M, Marra E Giannattasio S (2006) YCA1 participates in the acetic acid induced yeast programmed cell death also in a manner unrelated to its caspase-like activity. FEBS Lett 580 : 6880 6884.
13. Haro R Rodríguez-Navarro A (2002) Molecular analysis of the mechanism of potassium uptake through the TRK1 transporter of Saccharomyces cerevisiae. Biochim Biophys Acta 1564 : 114 122.
14. Huh G-H, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML, Bressan RA Hasegawa PM (2002) Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. Plant J 29 : 649 659.
15. - sensor. J Gen Physiol 131 : 379 391.
16. Kaiserer L, Oberparleiter C, Weiler-Gorz R, Burgstaller W, Leiter E Marx F (2003) Characterization of the Penicillium chrysogenum antifungal protein PAF. Arch Microbiol 180 : 204 210.
17. Kuroda T, Bihler H, Bashi E, Slayman CL Rivetta A (2004) Chloride channel function in the yeast TRK-potassium transporters. J Membrane Biol 198 : 177 192.
18. Leiter E, Szappanos H, Oberparleiter C, Kaiserer L, Csernoch L, Pusztahelyi T, Emri T, Pócsi I, Salvenmoser W Marx F (2005) Antifungal protein PAF severely affects the integrity of the plasma membrane of Aspergillus nidulans and induces an apoptosis-like phenotype. Antimicrob Agents Ch 49 : 2445 2453.
19. Ludovico P, Sousa MJ, Silva MT, Leão C Côrte-Real M (2001) Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 147 : 2409 2415. (Pubitemid 32899237)
20. Madeo F, Fröhlich E Fröhlich KW (1997) A yeast mutant showing diagnostic markers of early and late apoptosis. J Cell Biol 139 : 729 734.
21. Madeo F, Engelhardt S, Herker E, Lehmann N, Maldener C, Proksch A, Wissing S Fröhlich KU (2002) Apoptosis in yeast: a new model system with applications in cell biology and medicine. Curr Genet 41 : 208 216.
22. Madeo F, Carmona-Gutierrez D, Ring J, Büttner S, Eisenberg T Kroemer G (2009) Caspase-dependent and caspase-independent cell death pathways in yeast. Biochim Biophys Acta 382 : 227 231.
23. Madrid R, Gómez MJ, Ramos J Rodríguez-Navarro A (1998) Ectopic potassium uptake in trk1 trk2 mutants of Saccharomyces cerevisiae correlates with a highly hyperpolarized membrane potential. J Biol Chem 273 : 14838 14844.
24. +-nutrition and enhanced resistance to salt stress. FEBS Lett 582 : 3922 3928.
25. Maresova L Sychrova H (2005) Physiological characterization of Saccharomyces cerevisiae kha1 deletion mutants. Mol Microbiol 55 : 588 600.
26. Maresova L, Muend S, Zhang Y-Q, Sychrova H Rao R (2009) Membrane hyperpolarization drives cation influx and fungicidal activity of amiodarone. J Biol Chem 284 : 2795 2802.
27. Martinac B, Zhut H, Kubalski A, Zhou X, Culbertson M, Busseytt H Kung C (1990) Yeast K1 killer toxin forms ion channels in sensitive yeast spheroplasts and in artificial liposomes. P Natl Acad Sci USA 87 : 6228 6232.
28. Mendoza I, Rubio F, Rodríguez-Navarro A Pardo JM (1994) The protein phosphatase calcineurin is essential for NaCl tolerance of Saccharomyces cerevisiae. J Biol Chem 269 : 8792 8796.
29. Mulet JM, Leube MP, Kron SJ, Ríos G, Fink GR Serrano R (1999) A novel mechanism of ion homeostasis and salt tolerance in yeast: the Hal4 and Hal5 protein kinases modulate the Trk1-Trk2 potassium transporter. Mol Cell Biol 19 : 3328 3337.
30. Navarre C Goffeau A (2000) Membrane hyperpolarization and salt sensitivity induced by deletion of PMP3, a highly conserved small protein of yeast plasma membrane. EMBO J 19 : 2515 2524.
31. 2+ homeostasis in Saccharomyces cerevisiae. FEMS Yeast Res 9 : 832 848.
32. Pereira C, Silva RD, Saraiva L, Johansson B, Sousa MJ Côrte-Real M (2008) Mitochondria-dependent apoptosis in yeast. Biochim Biophys Acta 1783 : 1286 1302.
33. Pozniakovsky AI, Knorre DA, Markova OV, Hyman AA, Skulachev VP Severin FF (2005) Role of mitochondria in the pheromone and amiodarone-induced programmed death of yeast. J Cell Biol 168 : 257 269.
34. Reiter J, Herker E, Madeo F Schmitt MJ (2005) Viral killer toxins induce caspase-mediated apoptosis in yeast. J Cell Biol 168 : 353 358.
35. Rodríguez-Navarro A (2000) Potassium transport in fungi and plants. Biochim Biophys Acta 1469 : 1 30.
36. Ruíz A, Ruiz MC, Sánchez-Garrido MA, Ariño J Ramos J (2004) The Ppz protein phosphatases regulate Trk-independent potassium influx in yeast. FEBS Lett 578 : 58 62.
37. Schauer A, Knauer H, Ruckenstuhl C, Fussi H, Durchschlag M, Potocnik U Fröhlich K-U (2009) Vacuolar functions determine the mode of cell death. Biochim Biophys Acta 1793 : 540 545.
38. Sharon A, Finkelstein A, Shlezinger N Hatam I (2009) Fungal apoptosis: function, genes and gene function. FEMS Microbiol Rev 33 : 833 854.
39. Silva RD, Sotoca R, Johansson B, Ludovico P, Sansonetty F, Silva MT, Peinado JM Corte-Real M (2006) Hyperosmotic stress induces metacaspase- and mitochondria-dependent apoptosis in Saccharomyces cerevisiae. Mol Microbiol 58 : 824 834.
40. Vargas RC, García-Salcedo R, Tenreiro S, Teixeira MC, Fernandes AR, Ramos J Sá-Correia I (2007) Saccharomyces cerevisiae multidrug resistance transporter Qdr2 is implicated in potassium uptake, providing a physiological advantage to quinidine-stressed cells. Eukaryot Cell 6 : 134 142.
41. Vylkova S, Li XS, Berner JC Edgerton M (2006) Distinct antifungal mechanisms: β-defensins require Candida albicans Ssa1 protein, while Trk1p mediates activity of cysteine-free cationic peptides. Antimicrob Agents Ch 50 : 324 331.
42. + and pH homeostasis: implications for salt tolerance, cell wall integrity and cell cycle progression. EMBO J 21 : 920 929.
43. Zheng K, Pan J-W, Ye L et al 2007) Programmed cell death-involved aluminum toxicity in yeast alleviated by antiapoptotic members with decreased calcium signals. Plant Physiol 143 : 38 49.