Molecular mechanisms of Saccharomyces cerevisiae stress adaptation and programmed cell death in response to acetic acid

Frontiers in Microbiology

Volumn 4, Issue FEB, 2013, Pages

  Giannattasio, Sergio ^a   Guaragnella, Nicoletta ^a   Ždralević, Maša ^a   Marra, Ersilia ^a  

^a CNR   (Italy)

Author keywords

Acetic acid; Cell adaptation; Mitochondrial retrograde pathway; Programmed cell death; Yeast

Indexed keywords

SACCHAROMYCES CEREVISIAE;

EID: 84875904201     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00033     Document Type: Review

References (95)

1. Almeida, B.,Ohlmeier, S., Almeida, A. J., Madeo, F., Leao, C., Rodrigues, F., et al. (2009).Yeast protein expression profile during acetic acid-induced apoptosis indicates causal involvementof theTORpathway.Proteomics 9, 720-732.
2. Antonelli,A., Castellari, L., Zambonelli, C., and Carnacini, A. (1999). Yeast influence on volatile composition of wines. J. Agric. Food Chem. 47,1139- 1144.
3. Arneborg, N., Jespersen, L., and 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.
4. Burtner, C. R., Murakami, C. J., Kennedy, B. K., and Kaeberlein, M. (2009). A molecular mechanism of chronological aging in yeast. Cell Cycle 8, 1256-1270.
5. Butow, R. A., and Avadhani, N. G. (2004). Mitochondrial signaling: the retrograde response. Mol. Cell 14, 1-15.
6. Carmelo,V.,Santos,H.,and Sa-Correia, I. (1997). Effect of extracellular acidification on the activity of plasma membraneATPaseandonthecytosolic and vacuolar pH of Saccharomyces cerevisiae. Biochim. Biophys. Acta 1325,63-70.
7. Carmona-Gutierrez, D., Eisenberg, T., Buttner, S., Meisinger, C., Kroemer, G., and Madeo, F. (2010). Apoptosis in yeast: triggers, pathways, subroutines. Cell Death Differ. 17, 763-773.
8. Casal, M., Cardoso, H., and Leao, C. (1996). Mechanisms regulating the transport of acetic acid in Saccharomyces cerevisiae. Microbiology 142(Pt 6), 1385-1390.
9. Casal, M., Paiva, S., Andrade, R. P., Gancedo, C., and Leao, C. (1999). The lactate-proton symport of Saccharomyces cerevisiae is encoded by JEN1. J. Bacteriol. 181,2620-2623.
10. Colombo, S., Ma, P., Cauwenberg, L., Winderickx, J., Crauwels, M., Teunissen, A., et al. (1998). Involvement of distinct G-proteins, Gpa2 and Ras, in glucose and intracellular acidification-induced cAMP signalling in the yeast Saccharomyces cerevisiae. EMBO J. 17, 3326- 3341.
11. Eisenberg, T., Buttner, S., Kroemer, G., and Madeo, F. (2007). The mito chondrial pathway in yeastapoptosis. Apoptosis 12, 1011-1023.
12. Fernandes, A. R., Mira, N. P., Vargas, R. C., Canelhas, I., and Sa-Correia, I. (2005). Saccharomyces cerevisiae adaptation to weak acids involves the transcription factor Haa1p and Haa1p-regulated genes. Biochem. Biophys. Res. Commun. 337,95-103.
13. Fleet, G. H. (2007). Yeasts in foods and beverages: impact on product quality andsafety. Curr. Opin. Biotechnol. 18, 170-175.
14. Fuchs, B. B., and Mylonakis, E. (2009). Our paths might cross: the role of the fungal cell wall integrity pathway in stress response and cross talk with other stress response pathways. Eukaryot. Cell 8,1616-1625.
15. Garay-Arroyo, A., Covarrubias, A. A., Clark, I., Nino, I., Gosset, G., and Martinez, A. (2004). Response to different environmental stress conditions of industrial and laboratory Saccharomyces cerevisiae strains. Appl. Microbiol. Biotechnol. 63, 734-741.
16. Gasch, A. P., and Werner-Washburne, M. (2002). The genomics of yeast responses to environmental stress and starvation. Funct. Integr. Genomics 2, 181-192.
17. Giannattasio, S., Atlante, A., Antonacci, L.,Guaragnella,N.,Lattanzio,P.,Passarella, S., et al. (2008). Cytochrome c is released from coupled mitochondria of yeast en route to acetic acid induced programmed cell death and can work as an electron donor and a ROS scavenger. FEBS Lett. 582, 1519-1525.
18. Giannattasio, S., Guaragnella, N., Corte-Real, M., Passarella, S., and Marra, E. (2005a). Acid stress adaptation protects Saccharomyces cerevisiae from acetic acid-induced programmed cell death. Gene 354, 93-98.
19. Giannattasio, S., Liu, Z., Thornton, J., and Butow, R. A. (2005b). Retrograderesponsetomitochondrialdys function is separable from TOR1/2 regulation of retrograde gene expression. J. Biol. Chem. 280, 42528- 42535.
20. Guaragnella, N., Antonacci, L., Giannattasio, S., Marra, E., and Passarella, S. (2008). Catalase T and Cu,Zn superoxide dismutase in the acetic acid-induced programmed cell death in Saccharomyces cerevisiae. FEBS Lett. 582, 210-214.
21. Guaragnella, N., Antonacci, L., Passarella, S., Marra, E., and Giannattasio, S. (2007). Hydrogen peroxide and superoxide anion production during acetic acid-induced yeast programmed cell death. Folia Microbiol. 7 237-240.
22. Guaragnella, N., Antonacci, L., Passarella, S., Marra, E., and Giannattasio, S. (2011a). Achievements and perspectives in yeast acetic acid-induced programmed cell death pathways. Biochem. Soc. Trans. 39, 1538-1543.
23. Guaragnella, N., Passarella, S., Marra, E., and Giannattasio, S. (2011b). Cytochrome c Trp65Ser substitution results in inhibition of acetic acid induced programmed cell death in Saccharomyces cerevisiae. Mitochondrion 11,987-991.
24. Guaragnella, N., Bobba, A., Passarella, S., Marra, E., and Giannattasio, S. (2010a). Yeast acetic acid-induced programmed cell death can occur without cytochrome c release which requires metacaspase YCA1. FEBS Lett. 584, 224-228.
25. Guaragnella, N., Passarella, S., Marra, E., and Giannattasio, S. (2010b). Knock-out of metacaspase and/or cytochrome c results in the activation of a ROS-independent acetic acid-induced programmed cell death pathway in yeast. FEBS Lett. 584, 3655-3660.
26. Guaragnella, N., Pereira, C., Sousa, M. J., Antonacci, L., Passarella, S., Corte-Real, M., et al. (2006). YCA1 participatesintheaceticacidinduced yeastprogrammedcelldeathalsoina manner unrelated to its caspase-like activity. FEBS Lett. 580,6880-6884.
27. Guaragnella, N., Ždralević, M., Antonacci, L., Passarella, S., Marra, E., and Giannattasio, S. (2012). The role of mitochondria in yeast programmed cell death. Front. Oncol. 2:70. doi: 10.3389/fonc.2012.00070
28. Hatzixanthis, K., Mollapour, M., Seymour, I., Bauer, B. E., Krapf, G., Schuller, C., et al. (2003). Moderately lipophilic carboxylate compounds are the selective inducers of the Saccharomyces cerevisiae Pdr12p ATP binding cassette transporter.Yeast 20, 575-585.
29. Hohmann, S. (2009). Control of high osmolaritysignallingintheyeastSaccharomyces cerevisiae. FEBS Lett. 583, 4025-4029.
30. Jazwinski, S. M., and Kriete, A. (2012).Theyeastretrograderesponse as a model of intracellular signaling of mitochondrial dysfunction. Front. Physiol. 3:139. doi: 10.3389/fphys.2012.00139
31. Jazwinsky,M.S. (2003)."Mitochondria, metabolism and aging in yeast," in Model Systems in Aging, eds T. Nyström and H. D. Osiewacz (Berlin Heidelberg: Springer-Verlag), 39-59.
32. Jia, Y., Rothermel, B., Thornton, J., and Butow, R. A. (1997). A basic helix-loop-helix-leucine zipper transcription complex in yeast functions in a signaling pathway from mitochondria to the nucleus. Mol. Cell. Biol. 17,1110-1117.
33. Klinke, H. B., Thomsen, A. B., and Ahring, B. K. (2004). Inhibition of ethanol-producingyeastandbacteria by degradation products produced during pre-treatment of biomass. Appl. Microbiol. Biotechnol. 66, 10-26.
34. Komeili, A., Wedaman, K. P., O'shea, E. K., and Powers, T. (2000). Mechanism of metabolic control. Target of rapamycinsignalinglinksnitrogen quality to the activity of the Rtg1 and Rtg3transcriptionfactors.J.CellBiol. 151, 863-878.
35. Lambert,R.J.,andStratford,M. (1999). Weak-acid preservatives: modelling microbial inhibition and response. J. Appl. Microbiol. 86,157-164.
36. Lastauskiene, E., and Citavicius, D. (2008). Influence of RAS genes on yeast Saccharomyces cerevisiae cell viability in acidic environment. Biologija 54, 150-155.
37. Leadsham, J. E., and Gourlay, C. W. (2010). cAMP/PKA signaling balances respiratory activity with mitochondria dependent apoptosis via transcriptional regulation. BMC Cell Biol. 11:92. doi: 10.1186/1471-2121-11-92
38. Lee, R. E., Brunette, S., Puente, L. G., and Megeney, L. A. (2010). Metacaspase Yca1 is required for clearance of insoluble protein aggregates. Proc. Natl. Acad. Sci. U.S.A. 107, 13348-13353.
39. Lee, R. E., Puente, L. G., Kaern, M., and Megeney, L. A. (2008). A nondeath role of the yeast metacaspase: Yca1palterscellcycledynamics.PLoS ONE 3:e2956. doi: 10.1371/journal.pone.0002956
40. Lee, Y. J., Jang, J. W., Kim, K. J., and Maeng, P. J. (2011). TCA cycleindependent acetate metabolism via the glyoxylate cycle in Saccharomyces cerevisiae. Yeast 28, 153-166.
41. Liao, X. S., Small, W. C., Srere, P. A., and Butow, R. A. (1991). Intramito chondrial functions regulate nonmitochondrial citrate synthase (CIT2) expression in Saccharomyces cerevisiae. Mol. Cell. Biol. 11,38-46.
42. Liu, Z., and Butow, R. A. (2006). Mito-chondrial retrograde signaling.Annu. Rev. Genet. 40,159-185.
43. Liu, Z., Sekito, T., Epstein, C. B., and Butow,R. A. (2001). RTG-dependent mitochondria to nucleus signaling is negatively regulated by the seven WD-repeat protein Lst8p. EMBO J. 20,7209-7219.
44. Liu,Z.,Sekito,T.,Spirek,M.,Thornton, J., and Butow, R. A. (2003). Retrograde signaling is regulated by the dynamic interaction between Rtg2p and Mks1p. Mol. Cell 12,401-411.
45. Liu, Z., Spirek, M., Thornton, J., and Butow,R. A. (2005). A novel degronmediated degradation of the RTG pathway regulator, Mks1p, by SCF-Grr1. Mol. Biol. Cell 16, 4893-4904.
46. Liu, Z. L., and Blaschek, H. P. (2010). "Biomass conversion inhibitors and in situ detoxification," in Biomass to Biofuels: Strategies for Global Industries, eds A. Vertes, N. Qureshi, H. Yukawa, and H. Blaschek. (Oxford: John Wiley & Sons,Ltd.), 233-259.
47. Ludovico, P., Rodrigues, F., Almeida, A., Silva, M. T., Barrientos, A., and Corte-Real, M. (2002). Cytochrome c release and mitochondria involvement in programmed cell death induced by acetic acid in Saccharomyces cerevisiae. Mol. Biol. Cell 13, 2598-2606.
48. Ludovico, P., Sansonetty, F., Silva, M. T., and Corte-Real, M. (2003). Acetic acidinducesaprogrammedcelldeath process in the food spoilage yeast Zygosaccharomyces bailii. FEMS Yeast Res. 3,91-96.
49. Ludovico, P., Sousa, M. J., Silva, M. T., Leao, C., and Corte-Real, M. (2001). Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 147, 2409-2415.
50. Madeo, F., Frohlich, E., and Frohlich, K.U. (1997).Ayeastmutantshowing diagnostic markers of early and late apoptosis. J. Cell Biol. 139, 729-734.
51. Madeo, F., Frohlich, E., Ligr, M., Grey, M., Sigrist, S. J., Wolf, D. H., et al. (1999). Oxygen stress: a regulator of apoptosis in yeast. J. Cell Biol. 145, 757-767.
52. Madeo, F., Herker, E., Maldener, C., Wissing, S., Lachelt, S., Herlan, M., et al. (2002). A caspase-related protease regulates apoptosis in yeast. Mol. Cell 9, 911-917.
53. Martinez-Munoz, G. A., and Kane, P. (2008). Vacuolar and plasma membrane proton pumps collaborate to achieve cytosolic pH homeostasis in yeast. J. Biol. Chem. 283, 20309- 20319.
54. Mira,N.P.,Becker,J.D.,andSa-Correia, I. (2010a). Genomic expression programinvolvingtheHaa1p-regulonin Saccharomyces cerevisiae response to acetic acid. OMICS 14,587-601.
55. Mira, N. P., Palma, M., Guerreiro, J. F., and Sa-Correia, I. (2010b). Genomewide identification of Saccharomyces cerevisiaegenesrequiredfortolerance to acetic acid. Microb. Cell Fact. 9,79.
56. Mira, N. P., Teixeira, M. C., and Sa-Correia, I. (2010c). Adaptive response and tolerance to weak acids in Saccharomyces cerevisiae: a genome-wide view. OMICS 14, 525-540.
57. Mira, N. P., Henriques, S. F., Keller, G., Teixeira, M. C., Matos, R. G., Arraiano, C. M., et al. (2011). Identificationof aDNA-bindingsiteforthe transcription factor Haa1, required for Saccharomyces cerevisiae response toaceticacidstress. NucleicAcidsRes. 39,6896-6907.
58. Mitchell,A.,Romano,G. H.,Groisman, B., Yona, A., Dekel, E., Kupiec, M., et al. (2009). Adaptive prediction of environmental changes by microorganisms. Nature 460,220-224.
59. Mollapour, M., and Piper, P. W. (2006). Hog1p mitogen-activated protein kinase determines acetic acid resistance in Saccharomyces cerevisiae. FEMS Yeast Res. 6, 1274- 1280.
60. Mollapour, M., and Piper, P. W. (2007). Hog1 mitogen-activated protein kinase phosphorylation targets the yeast Fps1 aquaglyceroporin for endocytosis, thereby rendering cells resistanttoaceticacid.Mol.Cell.Biol. 27,6446-6456.
61. Mollapour, M., Shepherd, A., and Piper, P. W. (2008). Novel stress responses facilitate Saccharomyces cerevisiae growth in the presence of the monocarboxylate preservatives. Yeast 25,169-177.
62. Mollapour,M.,Shepherd,A.,and Piper, P. W. (2009). Presence of the Fps1p aquaglyceroporin channel is essential for Hog1p activation, but suppresses Slt2(Mpk1)p activation, with acetic acid stress of yeast. Microbiology 155, 3304-3311.
63. Mroczek,S.,and Kufel,J. (2008).Apoptotic signals induce specific degradation of ribosomal RNA in yeast. Nucleic Acids Res. 36, 2874-2888.
64. Orzechowski Westholm, J., Tronnersjo, S., Nordberg, N., Olsson, I., Komorowski, J., and Ronne, H. (2012). Gis1 and Rph1 regulate glycerol and acetate metabolism in glucose depleted yeast cells. PLoS ONE 7:e31577. doi: 10.1371/journal.pone.0031577
65. Paiva, S., Devaux, F., Barbosa, S., Jacq, C., and Casal, M. (2004). Ady2p is essential for the acetate permease activity in the yeast Saccharomyces cerevisiae. Yeast 21, 201-210.
66. Pereira, C., Camougrand, N., Manon, S., Sousa, M. J., and Corte-Real, M. (2007). ADP/ATP carrier is required for mitochondrial outer membrane permeabilization and cytochrome c releaseinyeastapoptosis.Mol.Microbiol. 66,571-582.
67. Pereira, C., Silva, R. D., Saraiva, L., Johansson, B., Sousa, M. J., and Corte-Real, M. (2008). Mitochondria-dependent apoptosis in yeast. Biochim. Biophys. Acta 1783, 1286-1302.
68. Phillips, A. J., Crowe, J. D., and Ramsdale, M. (2006). Ras pathway signaling accelerates programmed cell death in the pathogenic fungus Candida albicans. Proc. Natl. Acad. Sci. U.S.A. 103, 726-731.
69. Pinto, I., Cardoso, H., Leao, C., and Van Uden, N. (1989). High enthalpy and low enthalpy death in Saccharomyces cerevisiae induced by acetic acid. Biotechnol. Bioeng. 33, 1350- 1352.
70. Piper, P., Calderon, C. O., Hatzixanthis, K., and Mollapour, M. (2001). Weak acid adaptation: the stress response that confers yeasts with resistance to organic acid food preservatives. Microbiology 147, 2635-2642.
71. Piper,P.W. (1999).Yeastsuperoxidedismutase mutants reveal a pro-oxidant action of weak organic acid food preservatives. Free Radic. Biol. Med. 27, 1219-1227.
72. Piper,P.W. (2011)."Resistanceof yeasts to wek organic acid food preservatives," in Advances in Applied Microbiology, eds A. Laskin, G. Gadd, and S. Sariaslani (Burlington: Academic Press), 97-113.
73. Pizarro, F., Vargas, F. A., and Agosin, E. (2007).Asystemsbiologyperspective of wine fermentations. Yeast 24, 977-991.
74. Pretorius, I. S. (2000). Tailoring wine yeast for the new millennium: novel approachestotheancientartofwinemaking. Yeast 16,675-729.
75. Pretorius, I. S., and Bauer, F. F. (2002). Meeting the consumer challenge through genetically customized wine-yeast strains. Trends Biotechnol. 20, 426-432.
76. Ribeiro, G. F., Corte-Real, M., and Johansson, B. (2006). Characterization of DNA damage in yeast apoptosis induced by hydrogen peroxide, acetic acid, and hyperosmotic shock. Mol. Biol. Cell 17,4584-4591.
77. Rodrigues, F., Sousa, M. J., Ludovico, P., Santos, H., Corte-Real, M., and Leao, C. (2012). The fate of acetic acid during glucose Co-metabolism by the spoilage yeast Zygosaccharomyces bailii. PLoS ONE 7:e52402. doi: 10.1371/journal.pone.0052402
78. Rolland, F., Winderickx, J., and Thevelein, J. M. (2002). Glucosesensing and -signalling mechanisms in yeast. FEMS Yeast Res. 2, 183-201.
79. Ruiz-Roig, C., Noriega, N., Duch, A., Posas, F., and De Nadal, E. (2012). The Hog1 SAPK controls the Rtg1/Rtg3 transcriptional complex activity by multiple regulatory mechanisms. Mol. Biol. Cell 23, 4286-4296.
80. Schuller, C., Mamnun, Y. M., Mollapour, M., Krapf, G., Schuster, M., Bauer, B. E., et al. (2004). Global phenotypic analysis and transcriptional profiling defines the weak acid stress response regulon in Saccharomyces cerevisiae. Mol. Biol. Cell 15, 706-720.
81. Sekito, T., Thornton, J., and Butow, R. A. (2000). Mitochondria-to-nuclear signaling is regulated by the subcellular localization of the transcription factors Rtg1p and Rtg3p. Mol. Biol. Cell 11,2103-2115.
82. Sousa, M. J., Rodrigues, F., Corte-Real, M.,andLeao,C. (1998). Mechanisms underlying the transport and intracellular metabolism of acetic acid in the presence of glucose in the yeast Zygosaccharomyces bailii. Microbiology 144(Pt 3),665-670.
83. Srinivasan, V., Kriete, A., Sacan, A., andJazwinski,S.M. (2010).Comparing the yeast retrograde response and NF-kappaB stress responses: implications for aging. Aging Cell 9, 933-941.
84. Stratford, M. (2006). "Food and beverage spoilage yeasts.," in Yeasts in Food and Beverages, ed. A. Querol and G. Fleet (Berlin: Springer), 335-379.
85. Stratford, M., and Anslow, P. A. (1996). Comparison of the inhibitory action on Saccharomyces cerevisiae of weakacid preservatives, uncouplers, and medium-chain fatty acids. FEMS Microbiol. Lett. 142, 53-58.
86. Stratford, M., and Anslow, P. A. (1998). Evidence that sorbic acid does not inhibit yeast as a classic 'weak acid preservative'.Lett.Appl.Microbiol.27, 203-206.
87. Tulha, J., Faria-Oliveira, F., Lucas, C., andFerreira,C. (2012). Programmed cell death in Saccharomyces cerevisiae is hampered by the deletion of GUP1 gene. BMC Microbiol. 12:80. doi: 10.1186/1471-2180-12-80
88. Ullah, A., Orij, R., Brul, S., and Smits,G.J. (2012).Quantitativeanalysis of the modes of growth inhibition by weak organic acids in yeast. Appl. Environ. Microbiol. 78, 8377- 8387.
89. Uren, A. G., O'rourke, K., Aravind, L. A., Pisabarro, M. T., Seshagiri, S., Koonin, E. V., et al. (2000). Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell 6, 961-967.
90. Vilela-Moura, A., Schuller, D., Mendes-Faia, A., and Corte-Real, M. (2008). Reduction of volatile acidity of wines by selected yeast strains. Appl. Microbiol. Biotechnol. 80, 881-890.
91. Vilela-Moura, A., Schuller, D., Mendes-Faia, A., Silva, R. D., Chaves, S. R., Sousa, M. J., et al. (2010). The impact of acetate metabolism on yeast fermentative performance and wine quality: reduction of volatile acidity of grape musts and wines. Appl. Microbiol. Biotechnol. 89, 271-280.
92. Weinberger, M., Mesquita, A., Caroll, T., Marks, L., Yang, H., Zhang, Z., et al. (2010). Growth signaling promotes chronological aging in budding yeast by inducing superoxide anions that inhibit quiescence. Aging (Albany NY) 2, 709-726.
93. Wilkinson, D., and Ramsdale, M. (2011). Proteases and caspase-like activity in the yeast Saccharomyces cerevisiae. Biochem. Soc. Trans. 39, 1502-1508.
94. Ždralević, M., Guaragnella, N., Antonacci, L., Marra, E., and Giannattasio, S. (2012). Yeast as a tool to study signaling pathways in mitochondrial stress response and cytoprotection. ScientificWorldJournal 2012, 912147.
95. Zhang, J. G., Liu, X. Y., He, X. P., Guo, X. N., Lu, Y., and Zhang, B. R. (2011). Improvement of acetic acid tolerance and fermentation performance of Saccharomyces cerevisiae by disruption of the FPS1 aquaglyceroporin gene. Biotechnol. Lett. 33,277-284.