Yeast protein expression profile during acetic acid-induced apoptosis indicates causal involvement of the TOR pathway

Proteomics

Volumn 9, Issue 3, 2009, Pages 720-732

  Almeida, Bruno ^a   Ohlmeier, Steffen ^b   Almeida, Agostinho J ^a   Madeo, Frank ^c   Leão, Cecília ^a   Rodrigues, Fernando ^a   Ludovico, Paula ^a  

^a UNIVERSITY OF MINHO   (Portugal)

^b UNIVERSITY OF OULU   (Finland)

^c Institute of Molecular Biosciences   (Austria)

Author keywords

Acetic acid; Amino acid starvation; GAAC system; TOR pathway; Yeast apoptosis

Indexed keywords

ACETIC ACID; AMINO ACID; DNA NUCLEOTIDYLEXOTRANSFERASE; PHOSPHATASE; PROTEIN GCN2; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GCN4; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CARBOHYDRATE METABOLISM; CELL CYCLE; CONTROLLED STUDY; NICK END LABELING; NONHUMAN; NUCLEOTIDE METABOLISM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MALNUTRITION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION INITIATION;

ACETIC ACID; APOPTOSIS; BLOTTING, WESTERN; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, FUNGAL; MASS SPECTROMETRY; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

EID: 60549114895     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200700816     Document Type: Article

References (40)

1. Ludovico, P., Madeo, F., Silva, M., Yeast programmed cell death: an intricate puzzle. IUBMB Life 2005, 57, 129-135.
2. Madeo, F., Herker, E., Wissing, S., Jungwirth, H. et al., Apoptosis in yeast. Curr. Opin. Microbiol. 2004, 7, 655-660.
3. Madeo, F., Frohlich, E., Frohlich, K. U., A yeast mutant showing diagnostic markers of early and late apoptosis. J. Cell. Biol. 1997, 739, 729-734.
4. Weinberger, M., Ramachandran, L., Feng, L., Sharma, K. et al., Apoptosis in budding yeast caused by defects in initiation of DNA replication. J. Cell. Sci. 2005, 178, 3543-3553.
5. Laun, P., Ramachandran, L., Jarolim, S., Herker, E. et al.,A comparison of the aging and apoptotic transcriptome of Saccharomyces cerevisiae. FEMS Yeast Res. 2005, 5, 1261-1272.
6. Ruvolo, P. P., Deng, X., May, W. S., Phosphorylation of Bcl2 and regulation of apoptosis. Leukemia 2001, 75, 515-522.
7. Ludovico, P., Sousa, M. J., Silva, M. T., Leao, C., Corte-Real, M., Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 2001, 747, 2409-2415.
8. Fannjiang, Y., Cheng, W. C., Lee, S. J., Qi, B. et al., Mitochondrial fission proteins regulate programmed cell death in yeast. Genes Dev. 2004, 78, 2785-2797.
9. Wissing, S., Ludovico, P., Herker, E., Buttner, S. et al.,An AIF orthologue regulates apoptosis in yeast. J. Cell. Biol. 2004, 766, 969-974.
10. Ludovico, P., Rodrigues, F., Almeida, A., Silva, M. T. et al., Cytochrome c release and mitochondria involvement in programmed cell death induced by acetic acid in Saccharomyces cerevisiae. Mol. Biol. Cell 2002, 73, 2598-2606.
11. Ohlmeier, S., Kastaniotis, A. J., Hiltunen, J. K., Bergmann, U., The yeast mitochondrial proteome, a study of fermentative and respiratory growth. J. Biol. Chem. 2004, 279, 3956-3979.
12. Almeida, B., Sampaio-Marques, B., Carvalho, J., Silva, M. T. et al., An atypical active cell death process underlies the fungicidal activity of ciclopirox olamine against the yeast Saccharomyces cerevisiae. FEMS Yeast Res. 2007, 7, 404-412.
13. Ludovico, P., Sansonetty, F., Silva, M. T., Corte-Real, M., Acetic acid induces a programmed cell death process in the food spoilage yeast Zygosaccharomyces bailii. FEMS Yeast Res. 2003, 3, 91-96.
14. Proud, C. G., The multifaceted role of mTOR in cellular stress responses. DNA Repair (Amst) 2004, 3, 927-934.
15. Eklund, H., Uhlin, U., Farnegardh, M., Logan, D. T., Nordlund, P., Structure and function of the radical enzyme ribonucleotide reductase. Prog. Biophys. Mol. Biol. 2001, 77, 177-268.
16. Carroll, C. W., Altman, R., Schieltz, D., Yates, J. R., Kellogg, D., The septins are required for the mitosis-specific activation of the Gin4 kinase. J. Cell. Biol. 1998, 143, 709-717.
17. Barral, Y., Parra, M., Bidlingmaier, S., Snyder, M., Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast. Genes Dev. 1999, 13, 176-187.
18. Mirande, M., Waller, J. P., The yeast lysyl-tRNA synthetase gene. Evidence for general amino acid control of its expression and domain structure of the encoded protein. J. Biol. Chem. 1988, 263, 18443-18451.
19. Dickinson, J. R., Salgado, L. E., Hewlins, M. J., The catabolism of amino acids to long chain and complex alcohols in Saccharomyces cerevisiae. J. Biol. Chem. 2003, 278, 8028-8034.
20. Forsberg, H., Hammar, M., Andreasson, C., Moliner, A., Ljungdahl, P. O., Suppressors of ssy1 and ptr3 null mutations define novel amino acid sensor-independent genes in Saccharomyces cerevisiae. Genetics 2001, 158, 973-988.
21. Lee, Y. D., Elledge, S. J., Control of ribonucleotide reductase localization through an anchoring mechanism involving Wtm1. Genes Dev. 2006, 20, 334-344.
22. Barbet, N. C., Schneider, U., Helliwell, S. B., Stansfield, I. et al., TOR controls translation initiation and early G1 progression in yeast. Mol. Biol. Cell 1996, 7, 25-42.
23. Shamji, A. F., Kuruvilla, F. G., Schreiber, S. L., Partitioning the transcriptional program induced by rapamycin among the effectors of the Tor proteins. Curr. Biol. 2000, 70, 1574-1581.
24. Jiang, Y., Broach, J. R., Tor proteins and protein phosphatase 2A reciprocally regulate Tap42 in controlling cell growth in yeast. EMBO J. 1999, 18, 2782-2792.
25. Zabrocki, P., Van Hoof, C., Goris, J., Thevelein, J. M. et al., Protein phosphatase 2A on track for nutrient-induced signalling in yeast. Mol. Microbiol. 2002, 43, 835-842.
26. Hinnebusch, A. G., Natarajan, K., Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot. Cell 2002, 1, 22-32.
27. Matsuo, R., Kubota, H., Obata, T., Kito, K. et al., The yeast eIF4E-associated protein Eap1p attenuates GCN4 translation upon TOR-inactivation. FEBS Lett. 2005, 579, 2433-2438.
28. Buzzard, K. A., Giaccia, A. J., Killender, M., Anderson, R. L., Heat shock protein 72 modulates pathways of stress-induced apoptosis. J. Biol. Chem. 1998, 273, 17147-17153.
29. Gurbuxani, S., Schmitt, E., Cande, C., Parcellier, A. et al., Heat shock protein 70 binding inhibits the nuclear import of apoptosis-inducing factor. Oncogene 2003, 22, 6669-6678.
30. Bauer, B. E., Rossington, D., Mollapour, M., Mamnun, Y. et al., 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. 2003, 270, 3189-3195.
31. Gomes, P., Sampaio-Marques, B., Ludovico, P., Rodrigues, F., Leao, C., Low auxotrophy-complementing amino acid concentrations reduce yeast chronological life span. Mech. Ageing Dev. 2007, 128, 383-391.
32. Eisler, H., Frohlich, K. U., Heidenreich, E., Starvation for an essential amino acid induces apoptosis and oxidative stress in yeast. Exp. Cell Res. 2004, 300, 345-353.
33. Powers, R. W., 3rd, Kaeberlein, M., Caldwell, S. D., Kennedy, B. K., Fields, S., Extension of chronological life span in yeast by decreased TOR pathway signaling. Genes Dev. 2006, 20, 174-184.
34. Di Como, C. J., Arndt, K. T., Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev. 1996, 10, 1904-1916.
35. Wang, H., Wang, X., Jiang, Y., Interaction with Tap42 is required for the essential function of Sit4 and type 2A phosphatases. Mol. Biol. Cell 2003, 14, 4342-4351.
36. Jiang, Y., Regulation of the cell cycle by protein phosphatase 2A in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 2006, 70, 440-449.
37. Loewith, R., Jacinto, E., Wullschleger, S., Lorberg, A. et al., Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 2002, 10, 457-468.
38. De Virgilio, C., Loewith, R., The TOR signalling network from yeastto man. Int. J. Biochem. Cell Biol. 2006, 38, 1476-1481.
39. Magherini, F., Tani, C., Gamberi, T., Caselli, A. et al., Protein expression profiles in Saccharomyces cerevisiae during apoptosis induced by H2O2. Proteomics 2007, 7, 1434-1445.
40. Almeida, B., Buttner, S., Ohlmeier, S., Silva, A., et al., NO-mediated apoptosis in yeast. J. Cell. Sci. 2007, 120, 3279-3288.