Hog1 mitogen-activated protein kinase phosphorylation targets the yeast Fps1 aquaglyceroporin for endocytosis, thereby rendering cells resistant to acetic acid

Molecular and Cellular Biology

Volumn 27, Issue 18, 2007, Pages 6446-6456

  Mollapour, Mehdi ^a   Piper, Peter W ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; AQUAGLYCEROPORIN; CELL SURFACE PROTEIN; HIGH OSMOLARITY GLYCEROL 1; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN FPS1; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; GENE DELETION; GENE MUTATION; NONHUMAN; PKA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; UBIQUITINATION; YEAST;

ACETIC ACID; AQUAPORINS; ENDOCYTOSIS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, FUNGAL; HYDROGEN-ION CONCENTRATION; MEMBRANE PROTEINS; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA;

EID: 34548775911     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.02205-06     Document Type: Article

References (37)

1. Adams, A., D. E. Gottschling, C. A. Kaiser, and T. Stearns. 1997. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Agre, P., and D. Kozono. 2003. Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett. 555:72-78.
3. Amerik, A. Y., J. Nowak, S. Swaminathan, and M. Hochstrasser. 2000. The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol. Biol. Cell 11:3365-3380.
4. Dupre, S., D. Urban-Grimal, and R. Haguenauer-Tsapis. 2004. Ubiquitin and endocytic internalization in yeast and animal cells. Biochim. Biophys. Acta 1695:89-111.
5. Fu, D., A. Libson, L. J. Miercke, C. Weltzman, P. Nollert, J. Krucinski, and R. M. Stroud. 2000. Structure of a glycerol-conducting channel and the basis for its selectivity. Science 290:481-486.
6. Ghaemmaghami, S., W. K. Huh, K. Bower, R. W. Howson, A. Belle, N. Dephoure, E. K. O'Shea, and J. S. Weissman. 2003. Global analysis of protein expression in yeast. Nature 425:737-741.
7. Gietz, R. D., and A. Sugino. 1988. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenised yeast genes lacking six-base-pair restriction sites. Gene 74:527-534.
8. Goldstein, A. L., and J. H. McCusker. 1999. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15:1541-1553.
9. Hedfalk, K., R. M. Bill, J. G. Mullins, S. Karlgren, C. Filipsson, J. Bergstrom, M. J. Tamas, J. Rydstrom, and S. Hohmann. 2004. A regulatory domain in the C-terminal extension of the yeast glycerol channel Fps1p. J. Biol. Chem. 279:14954-14960.
10. Henriques, M., C. Quintas, and M. C. Loureiro-Dias. 1997. Extrusion of benzoic acid in Saccharomyces cerevisiae by an energy-dependent mechanism. Microbiology 143:1877-1883.
11. Hohmann, I., R. M. Bill, I. Kayingo, and B. A. Prior. 2000. Microbial MIP channels. Trends Microbiol. 8:33-38.
12. Hohmann, S. 2002. Osmotic stress signaling and osmoadaptation in yeasts. Microbiol. Mol. Biol Rev. 66:300-372.
13. Karlgren, S., N. Pettersson, B. Nordlander, J. C. Mathai, J. L. Brodsky, M. L. Zeidel, R. M. Bill, and S. Hohmann. 2005. Conditional osmotic stress in yeast: a system to study transport through aquaglyceroporins and osmo-stress signaling. J. Biol. Chem. 280:7186-7193.
14. King, L. S., D. Kozono, and P. Agre. 2004. From structure to disease: the evolving tale of aquaporin biology. Nat. Rev. Mol. Cell. Biol. 5:687-698.
15. Krebs, H. A., D. Wiggins, M. Stubbs, A. Sols, and F. Bedoya. 1983. Studies on the mechanism of the antifungal action of benzoate. Biochem. J. 214:657-663.
16. Luyten, K., J. Albertyn, W. F. Skibbe, B. A. Prior, J. Ramos, J. M. Thevelein, and S. Hohmann. 1995. Fps1, a yeast member of the MIP family of channel proteins, is a facilitator for glycerol uptake and efflux and is inactive under osmotic stress. EMBO J. 14:1360-1371.
17. Millson, S. H., A. Truman, V. King, C. Prodromou, L. Pearl, and P. W. Piper. 2005. A two-hybrid screen of the yeast proteome for Hsp90 interactors uncovers a novel Hsp90 chaperone requirement in activity of a stress-activated MAP kinase, Slt2p(Mpk1p). Eukaryot. Cell. 4:849-860.
18. Millson, S. M., A. Truman, and P. W. Piper. 2003. Vectors for N- or C-terminal positioning of the yeast Gal4p DNA binding or activator domains. BioTechniques 35:60-64.
19. Mollapour, M., and P. W. Piper. 2006. Hog1p MAP kinase determines acetic acid resistance in Saccharomyces cerevisiae. FEMS Yeast Res. 6:1274-1280.
20. Niedenthal, R. K., L. Riles, M. Johnston, and J. H. Hegemann. 1996. Green fluorescent protein as a marker for gene expression and subcellular localisation in budding yeast. Yeast 12:773-786.
21. O'Rourke, S. M., and I. Herskowitz. 2004. Unique and redundant roles for HOG MAPK pathway components as revealed by whole-genome expression analysis. Mol. Biol. Cell. 15:532-542.
22. Pettersson, N., C. Filipsson, E. Becit, L. Brive, and S. Hohmann. 2005. Aquaporins in yeasts and filamentous fungi. Biol. Cell 97:487-500.
23. Piper, P., Y. MahŽ, S. Thompson, R. Pandjaitan, C. Holyoak, R. Egner, M. MŸhlbauer, P. Coote, and K. Kuchler. 1998. The Pdr12 ABC transporter is required for the development of weak organic acid resistance in yeast. EMBO J. 17:4257-4265.
24. Posas, F., and H. Saito. 1997. Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. Science 276:1702-1705.
25. Proft, M., G. Mas, E. de Nadal, A. Vendrell, N. Noriega, K. Struhl, and F. Posas. 2006. The stress-activated Hog1 kinase is a selective transcriptional elongation factor for genes responding to osmotic stress. Mol. Cell. 23:241-250.
26. Proft, M., and K. Struhl. 2004. MAP kinase-mediated stress relief that precedes and regulates the timing of transcriptional induction. Cell 118:351-361.
27. Swaminathan, S., A. Y. Amerik, and M. Hochstrasser. 1999. The Doa4 deubiquitinating enzyme is required for ubiquitin homeostasis in yeast. Mol. Biol. Cell. 10:2583-2594.
28. Tamas, M. J., S. Karlgren, R. M. Bill, K. Hedfalk, L. Allegri, M. Ferreira, J. M. Thevelein, J. Rydstrom, J. G. Mullins, and S. Hohmann. 2003. A short regulatory domain restricts glycerol transport through yeast Fps1p. J. Biol. Chem. 278:6337-6345.
29. Tamas, M. J., K. Luyten, F. C. Sutherland, A Hernandez, J. Albertyn, H. Valadi, H. Li, B. A. Prior, S. G. Kilian, J. Ramos, L. Gustafsson, J. M. Thevelein, and S. Hohmann. 1999. Fps1p controls the accumulation and release of the compatible solute glycerol in yeast osmoregulation. Mol. Microbiol. 31:1087-1104.
30. Tamas, M. J., M. Rep, J. M. Thevelein, and S. Hohmann. 2000. Stimulation of the yeast high osmolarity glycerol (HOG) pathway: evidence for a signal generated by a change in turgor rather than by water stress. FEBS Lett. 472:159-165.
31. Tang, H. Y., A. Munn, and M. Cai. 1997. EH domain proteins Pan1p and End3p are components of a complex that plays a dual role in organization of the cortical actin cytoskeleton and endocytosis in Saccharomyces cerevisiae. Mol. Cell. Biol. 17:4294-4304.
32. Tanoue, T., and E. Nishida. 2003. Molecular recognitions in the MAP kinase cascades. Cell Signal. 15:455-462.
33. Thorsen, M., Y. Di, C. Tangemo, M. Morillas, D. Ahmadpour, C. Van der Does, A. Wagner, E. Johansson, J. Boman, F. Posas, R. Wysocki, and M. J. Tamas. 2006. The MAPK Hog1p modulates Fps1p-dependent arsenite uptake and tolerance in yeast. Mol. Biol. Cell 17:4400-4410.
34. Uetz, P., G. Cagney, D. Lockshon, A. Qureshi-Emili, D. Conover, M. Johnston, and S. Fields. 2000. A protein array for genomewide screens of protein-protein interactions. Nature 403:623-627.
35. Urbe, S. 2005. Ubiquitin and endocytic protein sorting. Essays Biochem. 41:81-98.
36. Wysocki, R., C. C. Chery, D. Wawrzycka, M. Van Hulle, R. Cornelis, J. M. Thevelein, and M. J. Tamas. 2001. The glycerol channel Fps1p mediates the uptake of arsenite and antimonite in Saccharomyces cerevisiae. Mol. Microbiol. 40:1391-1401.
37. Zeuthen, T., B. Wu, S. Pavlovic-Djuranovic, L. M. Holm, N. L. Uzcategui, M. Duszenko, J. F. Kun, J. E. Schultz, and E. Beitz. 2006. Ammonia permeability of the aquaglyceroporins from Plasmodium falciparum, Toxoplasma gondii and Trypansoma brucei. Mol. Microbiol. 61:1598-1608.