Hog1p mitogen-activated protein kinase determines acetic acid resistance in Saccharomyces cerevisiae

FEMS Yeast Research

Volumn 6, Issue 8, 2006, Pages 1274-1280

  Mollapour, Mehdi ^a   Piper, Peter W ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Acetic acid; Hog1p; MAP kinase signaling; Saccharomyces cerevisiae; Weak organic acid stress

Indexed keywords

ACETIC ACID; GLUCOSE; GLYCEROL; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN HOG1P; PROTEIN SLT2P; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; FUNGUS MUTANT; NONHUMAN; OSMOTIC STRESS; PH; PROTEIN ANALYSIS; SACCHAROMYCES CEREVISIAE;

ACETIC ACID; GENE EXPRESSION REGULATION, FUNGAL; GLYCEROL; HYDROGEN-ION CONCENTRATION; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 33751278445     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1111/j.1567-1364.2006.00118.x     Document Type: Article

References (47)

1. Adams A, Gottschling DE, Kaiser CA & Stearns T (1997) Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Albertyn J, Hohmann S, Thevelein JM & Prior BA (1994) GPD1, which encodes glycerol-3-phosphate dehydrogenase, is essential for growth under osmotic stress in Saccharomyces cerevisiae, and its expression is regulated by the high-osmolarity glycerol response pathway. Mol Cell Biol 14: 4135-4144.
3. Alonso-Monge R, Real E, Wojda I, Bebelman JP, Mager WH & Siderius M (2001) Hyperosmotic stress response and regulation of cell wall integrity in Saccharomyces cerevisiae share common functional aspects. Mol Microbiol 41: 717-730.
4. +-dependent glycerol 3-phosphate dehydrogenase encoded by GPD1 and GPD2 have distinct roles in osmoadaptation and redox regulation. EMBO J 16: 2179-2187.
5. Arneborg N, Jesperson L & Jakobsen M (2000) Individual cells of Saccharomyces cerevisiae and Zygosaccharomyces bailii exhibit different short-term intracellular pH responses to acetic acid. Arch Microbiol 174: 125-128.
6. Bauer BE, Rossington D, Mollapour M, Mamnun Y, Kuchler K & Piper PW (2003) Weak organic acid stress inhibits aromatic amino acid uptake by yeast, causing a strong influence of amino acid auxotrophies on the phenotypes of membrane transporter mutants. Eur J Biochem 270: 3189-3195.
7. Bell M & Engelberg D (2003) Phosphorylation of Tyr-176 of the yeast MAPK Hog1/p38 is not vital for Hog1 biological activity. J Biol Chem 278: 14603-14606.
8. Bonilla M & Cunningham KW (2003) Mitogen-activated protein kinase stimulation of Ca(2+) signaling is required for survival of endoplasmic reticulum stress in yeast. Mol Biol Cell 14: 4296-4305.
9. Canagarajah BJ, Khokhlatchev A, Cobb MH & Goldsmith EJ (1997) Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 90: 859-869.
10. Casal M, Cardoso H & Leao C (1996) Mechanisms regulating the transport of acetic acid in Saccharomyces cerevisiae. Microbiology 142: 1385-1390.
11. Cássio F, Leão C & van Uden N (1987) Transport of lactate and other short-chain monocarboxylates in the yeast Saccharomyces cerevisiae. Appl Environ Microbiol 53: 509-513.
12. Davenport KR, Sohaskey M, Kamada Y, Levin DE & Gustin MC (1995) A second osmosensing signal transduction pathway in yeast. Hypotonic shock activates the PKC1 protein kinase-regulated cell integrity pathway. J Biol Chem 270: 30157-30161.
13. Ferrigno P, Posas F, Koepp D, Saito H & Silver PA (1998) Regulated nucleo/cytoplasmic exchange of HOG1 MAPK requires the importin beta homologs NMD5 and XPO1. EMBO J 17: 5606-5614.
14. Fleet G (1992) Spoilage yeasts. Crit Rev Biotechnol 12: 1-44.
15. García R, Bermejo C, Grau C, Pérez R, Rodríguez- Peña JM, François J, Nombela C & Arroyo J (2004) The global transcriptional response to transient cell wall damage in Saccharomyces cerevisiae and its regulation by the cell integrity signaling pathway. J Biol Chem 279: 15183-15195.
16. García-Rodríguez LJ, Valle R, Durán A & Roncero C (2005) Cell integrity signaling activation in response to hyperosmotic shock in yeast. FEBS Lett 579: 6186-6190.
17. Giannattasio S, Guaragnella N, Corte-Real M, Passarella S & Marra E (2005) Acid stress adaptation protects Saccharomyces cerevisiae from acetic acid-induced programmed cell death. Gene 354: 94-98.
18. Harrison JC, Bardes ESG, Ohya Y & Lew DJ (2001) A role for the Pkc1p/Mpk1p kinase cascade in the morphogenesis checkpoint. Nat Cell Biol 3: 417-420.
19. Hatzixanthis K, Mollapour M, Seymour I, Bauer EB, Krapf G, Schüller C, Kuchler K & Piper PW (2003) Moderately lipophilic carboxylate compounds are the selective inducers of the Saccharomyces cerevisiae Pdr12p ATP-binding cassette transporter. Yeast 20: 575-585.
20. Hohmann S (2002) Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev 66: 300-372.
21. Kamada Y, Jung US, Piotrowski J & Levin DE (1995) The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev 9: 1559-1571.
22. Kapteyn JC, ter Riet B, Vink E, Blad S, de Nobel H, van den Ende H & Klis FM (2000) Low external pH induces HOG1-dependent changes in the organisation of the Saccharomyces cerevisiae cell wall. Mol Microbiol 39: 469-479.
23. Ketela T, Green R & Bussey H (1999) Saccharomyces cerevisiae mid2p is a potential cell wall stress sensor and upstream activator of the PKC1-MPK1 cell integrity pathway. J Bacteriol 181: 3330-3340.
24. Lawrence CL, Botting CH, Antrobus R & Coote PJ (2004) Evidence of a new role for the high-osmolarity glycerol mitogen-activated protein kinase pathway in yeast: regulating adaptation to citric acid stress. Mol Cell Biol 24: 3307-3323.
25. 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.
26. Ludovico P, Sansonetty F, Silva MT & Côrte-Real M (2003) Acetic acid induces a programmed cell death process in the food spoilage yeast Zygosaccharomyces bailii. FEMS Yeast Res 3: 91-96.
27. Maeda T, Wurgler-Murphy SM & Saito H (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369: 242-245.
28. Martin H, Rodriguez-Pachon JM, Ruiz C, Nombela C & Molina M (2000) Regulatory mechanisms for modulation of signaling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae. J Biol Chem 275: 1511-1519.
29. Norbeck J, Pahlman AK, Akhtar N, Blomberg A & Adler L (1996) Purification and characterization of two isoenzymes of DL-glycerol-3-phosphatase from Saccharomyces cerevisiae. Identification of the corresponding GPP1 and GPP2 genes and evidence for osmotic regulation of Gpp2p expression by the osmosensing mitogen-activated protein kinase signal transduction pathway. J Biol Chem 271: 13875-13881.
30. O'Rourke SM & Herskowitz I (2004) Unique and redundant roles for HOG MAPK pathway components as revealed by whole-genome expression analysis. Mol Biol Cell 15: 532-542.
31. Paiva S, Devaux F, Barbosa S, Jacq C & Casal M (2004) Ady2p is essential for the acetate permease activity in the yeast Saccharomyces cerevisiae. Yeast 21: 201-210.
32. Pampulha ME & Loureiro-Dias MC (2000) Energetics of the effect of acetic acid on growth of Saccharomyces cerevisiae. FEMS Microbiol Lett 184: 69-72.
33. Piper P (1994) Measurement of Transcription. IRL Press, Oxford, UK.
34. Piper P, Ortiz CC, Hatzixanthis K & Mollapour M (2001) Weak acid adaptation: the stress response that confers yeasts with resistance to organic acid food preservatives. Microbiology 147: 2635-2642.
35. Pretorius IS (2000) Tailoring wine yeast for the new millennium: novel approaches to the ancient art of winemaking. Yeast 16: 675-729.
36. Proft M & Struhl K (2004) MAP kinase-mediated stress relief that precedes and regulates the timing of transcriptional induction. Cell 118: 351-361.
37. Reinoso-Martín C, Schuller C, Schuetzer-Muehlbauer M & Kuchler K (2003) The yeast protein kinase C cell integrity pathway mediates tolerance to the antifungal drug caspofungin through activation of Slt2p mitogen-activated protein kinase signaling. Eukaryot Cell 2: 1200-1210.
38. Siderius M, Rots E & Mager WH (1997) High-osmolarity signalling in Saccharomyces cerevisiae is modulated in a carbon-source-dependent fashion. Microbiology 143: 3241-3250.
39. Sousa MJ, Rodrigues F, CôrteReal M & Leão C (1998) Mechanisms underlying the transport and intracellular metabolism of acetic acid in the presence of glucose in the yeast Zygosaccharomyces bailii. Microbiology 144: 665-670.
40. Staleva L, Hall A & Orlow SJ (2004) Oxidative stress activates FUS1 and RLM1 transcription in the yeast Saccharomyces cerevisiae in an oxidant-dependent manner. Mol Biol Cell 15: 5574-5582.
41. Steels H, James SA, Roberts IN & Stratford M (1999) Zygosaccharomyces lentus: a significant new osmophilic, preservative-resistant spoilage yeast, capable of growth at low temperature. J Appl Microbiol 87: 520-527.
42. Steels H, James SA, Roberts IN & Stratford M (2000) Sorbic acid resistance: the inoculum effect. Yeast 16: 1173-1183.
43. Steels H, James SA, Bond CJ, Roberts IN & Stratford M (2002) Zygosaccharomyces kombuchaensis: the physiology of a new species related to the spoilage yeasts Zygosaccharomyces lentus and Zygosaccharomyces bailii. FEMS Yeast Res 2: 113-121.
44. Tamas MJ, Rep M, Thevelein JM & Hohmann S (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.
45. Tanoue T & Nishida E (2003) Molecular recognitions in the MAP kinase cascades. Cell Signal 15: 455-462.
46. Tao W, Deschenes RJ & Fassler JS (1999) Intracellular glycerol levels modulate the activity of Sln1p, a Saccharomyces cerevisiae two-component regulator. J Biol Chem 274: 360-367.
47. Zarzov P, Mazzoni C & Mann C (1996) The SLT2(MPK1) MAP kinase is activated during periods of polarized cell growth in yeast. EMBO J 15: 83-91.