Programmed Cell Death in the Yeast <span class='italic'>Saccharomyces cerevisiae</span>

doi:10.1017/CBO9780511976094.033

33 - Programmed Cell Death in the Yeast Saccharomyces cerevisiae

from Part III - Cell Death in Nonmammalian Organisms

Published online by Cambridge University Press: 07 September 2011

Valter D. Longo and

Edited by

Douglas R. Green: Affiliation:
St. Jude Children's Research Hospital, Memphis, Tennessee
Valter D. Longo: Affiliation:
University of Southern California
Cristina Mazzoni: Affiliation:
University of Rome
John C. Reed: Affiliation:
Sanford-Burnham Medical Research Institute, La Jolla, California

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Summary

The yeast Saccharomyces cerevisiae is one of the most studied model systems for molecular and cellular biology. In 1996, it became the first eukaryotic organism to have a completely sequenced genome (Dujon, 1996; Goffeau et al., 1996), which led to a number of valuable and widely accessed databases. Among its features is the short generation time (usually 90–120 minutes) and the ability to grow at various temperatures in relatively inexpensive media. Moreover, many of its genes are well characterized, thanks in part to its amenability to modifications such as gene disruption, gene marking, mutations, or gene-dosage modifications. Because of these advantageous features, it has become the model organism of choice for many investigators in fields ranging from basic biology to biomedical research.

Type: Chapter
Information: Apoptosis
Physiology and Pathology
, pp. 389 - 396

DOI: https://doi.org/10.1017/CBO9780511976094.033 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2011

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References

Ahn, S. H., Henderson, K. A., Keeney, S. and Allis, C. D. (2005). H2B (Ser10) phosphorylation is induced during apoptosis and meiosis in S. cerevisiae. Cell Cycle 4, 780–3.

Allen, C., Buttner, S., Aragon, A. D., Thomas, J. A., Meirelles, O., Jaetao, J. E., Benn, D., Ruby, S. W., Veenhuis, M., Madeo, F. and Werner-Washburne, M. (2006). Isolation of quiescent and nonquiescent cells from yeast stationary-phase cultures. J Cell Biol 174, 89–100.

Almeida, B., Buttner, S., Ohlmeier, S., Silva, A., Mesquita, A., Sampaio-Marques, B., Osorio, N. S., Kollau, A., Mayer, B., Leao, C., Laranjinha, J., Rodrigues, F., Madeo, F. and Ludovico, P. (2007). NO-mediated apoptosis in yeast. J Cell Sci 120, 3279–88.

Almeida, B., Silva, A., Mesquita, A., Sampaio-Marques, B., Rodrigues, F. and Ludovico, P. (2008). Drug-induced apoptosis in yeast. Biochim Biophys Acta 1783, 1436–48.

Braun, R. J. and Zischka, H. (2008). Mechanisms of Cdc48/VCP-mediated cell death – from yeast apoptosis to human disease. Biochim Biophys Acta 1783, 1418–35.

Cannon, J. F., Gibbs, J. B. and Tatchell, K. (1986). Suppressors of the ras2 mutation of Saccharomyces cerevisiae. Genetics 113, 247–64.

Dujon, B. (1996). The yeast genome project: what did we learn? Trends Genet 12, 263–70.

Fabrizio, P., Battistella, L., Vardavas, R., Gattazzo, C., Liou, L. L., Diaspro, A., Dossen, J. W., Gralla, E. B. and Longo, V. D. (2004a). Superoxide is a mediator of an altruistic aging program in Saccharomyces cerevisiae. J Cell Biol 166, 1055–67.

Fabrizio, P., Gattazzo, C., Battistella, L., Wei, M., Cheng, C., McGrew, K. and Longo, V. D. (2005). Sir2 blocks extreme life-span extension. Cell 123, 655–67.

Fabrizio, P., Liou, L. L., Moy, V. N., Diaspro, A., Valentine, J. S., Gralla, E. B. and Longo, V. D. (2003). SOD2 functions downstream of Sch9 to extend longevity in yeast. Genetics 163, 35–46.

Fabrizio, P., Pletcher, S. D., Minois, N., Vaupel, J. W. and Longo, V. D. (2004b). Chronological aging-independent replicative life span regulation by Msn2/Msn4 and Sod2 in Saccharomyces cerevisiae. FEBS Lett 557, 136–42.

Fabrizio, P., Pozza, F., Pletcher, S. D., Gendron, C. M. and Longo, V. D. (2001). Regulation of longevity and stress resistance by Sch9 in yeast. Science 292, 288–90.

Fahrenkrog, B., Sauder, U. and Aebi, U. (2004). The S. cerevisiae HtrA-like protein Nma111p is a nuclear serine protease that mediates yeast apoptosis. J Cell Sci 117, 115–26.

Fannjiang, Y., Cheng, W. C., Lee, S. J., Qi, B., Pevsner, J., McCaffery, J. M., Hill, R. B., Basanez, G. and Hardwick, J. M. (2004). Mitochondrial fission proteins regulate programmed cell death in yeast. Genes Dev 18, 2785–97.

Foland, T. B., Dentler, W. L., Suprenant, K. A., Gupta, M. L., Jr. and Himes, R. H. (2005). Paclitaxel-induced microtubule stabilization causes mitotic block and apoptotic-like cell death in a paclitaxel-sensitive strain of Saccharomyces cerevisiae. Yeast 22, 971–8.

Forman, M. S., Mackenzie, I. R., Cairns, N. J., Swanson, E., Boyer, P. J., Drachman, D. A., Jhaveri, B. S., Karlawish, J. H., Pestronk, A., Smith, T. W., Tu, P. H., Watts, G. D., Markesbery, W. R., Smith, C. D. and Kimonis, V. E. (2006). Novel ubiquitin neuropathology in frontotemporal dementia with valosin-containing protein gene mutations. J Neuropathol Exp Neurol 65, 571–81.

Frohlich, K. U., Fussi, H. and Ruckenstuhl, C. (2007). Yeast apoptosis–from genes to pathways. Semin Cancer Biol 17, 112–21.

Goffeau, A., Barrell, B. G., Bussey, H., Davis, R. W., Dujon, B., Feldmann, H., Galibert, F., Hoheisel, J. D., Jacq, C., Johnston, M., Louis, E. J., Mewes, H. W., Murakami, Y., Philippsen, P., Tettelin, H. and Oliver, S. G. (1996). Life with 6000 genes. Science 274, 546, 563–7.

Hanada, M., Aime-Sempe, C., Sato, T. and Reed, J. C. (1995). Structure-function analysis of Bcl-2 protein. Identification of conserved domains important for homodimerization with Bcl-2 and heterodimerization with Bax. J Biol Chem 270, 11962–9.

Herker, E., Jungwirth, H., Lehmann, K. A., Maldener, C., Frohlich, K. U., Wissing, S., Buttner, S., Fehr, M., Sigrist, S. and Madeo, F. (2004). Chronological aging leads to apoptosis in yeast. J Cell Biol 164, 501–7.

Higashiyama, H., Hirose, F., Yamaguchi, M., Inoue, Y. H., Fujikake, N., Matsukage, A. and Kakizuka, A. (2002). Identification of ter94, Drosophila VCP, as a modulator of polyglutamine-induced neurodegeneration. Cell Death Differ 9, 264–73.

Hirabayashi, M., Inoue, K., Tanaka, K., Nakadate, K., Ohsawa, Y., Kamei, Y., Popiel, A. H., Sinohara, A., Iwamatsu, A., Kimura, Y., Uchiyama, Y., Hori, S. and Kakizuka, A. (2001). VCP/p97 in abnormal protein aggregates, cytoplasmic vacuoles, and cell death, phenotypes relevant to neurodegeneration. Cell Death Differ 8, 977–84.

Huang, M. E., Rio, A. G., Nicolas, A. and Kolodner, R. D. (2003). A genomewide screen in Saccharomyces cerevisiae for genes that suppress the accumulation of mutations. Proc Natl Acad Sci U S A 100, 11529–34.

Hubbers, C. U., Clemen, C. S., Kesper, K., Boddrich, A., Hofmann, A., Kamarainen, O., Tolksdorf, K., Stumpf, M., Reichelt, J., Roth, U., Krause, S., Watts, G., Kimonis, V., Wattjes, M. P., Reimann, J., Thal, D. R., Biermann, K., Evert, B. O., Lochmuller, H., Wanker, E. E., Schoser, B. G., Noegel, A. A. and Schroder, R. (2007). Pathological consequences of VCP mutations on human striated muscle. Brain 130, 381–93.

Imamura, S., Ojima, N. and Yamashita, M. (2003). Cold-inducible expression of the cell division cycle gene CDC48 and its promotion of cell proliferation during cold acclimation in zebrafish cells. FEBS Lett 549, 14–20.

Ivanovska, I. and Hardwick, J. M. (2005). Viruses activate a genetically conserved cell death pathway in a unicellular organism. J Cell Biol 170, 391–9.

Lamb, J. R., Fu, V., Wirtz, E. and Bangs, J. D. (2001). Functional analysis of the trypanosomal AAA protein TbVCP with trans-dominant ATP hydrolysis mutants. J Biol Chem 276, 21512–20.

Li, W., Sun, L., Liang, Q., Wang, J., Mo, W. and Zhou, B. (2006). Yeast AMID homologue Ndi1p displays respiration-restricted apoptotic activity and is involved in chronological aging. Mol Biol Cell 17, 1802–11.

Liang, Q., Li, W. and Zhou, B. (2008). Caspase-independent apoptosis in yeast. Biochim Biophys Acta 1783, 1311–9.

Ligr, M., Madeo, F., Frohlich, E., Hilt, W., Frohlich, K. U. and Wolf, D. H. (1998). Mammalian Bax triggers apoptotic changes in yeast. FEBS Lett 438, 61–5.

Longo, V. D., Ellerby, L. M., Bredesen, D. E., Valentine, J. S. and Gralla, E. B. (1997). Human Bcl-2 reverses survival defects in yeast lacking superoxide dismutase and delays death of wild-type yeast. J Cell Biol 137, 1581–8.

Longo, V. D., Gralla, E. B. and Valentine, J. S. (1996). Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae. Mitochondrial production of toxic oxygen species in vivo. J Biol Chem 271, 12275–80.

Longo, V. D., Mitteldorf, J. and Skulachev, V. P. (2005). Programmed and altruistic ageing. Nat Rev Genet 6, 866–72.

Low, C. P., Liew, L. P., Pervaiz, S. and Yang, H. (2005). Apoptosis and lipoapoptosis in the fission yeast Schizosaccharomyces pombe. FEMS Yeast Res 5, 1199–206.

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, 2409–15.

Madeo, F., Frohlich, E. and Frohlich, K. U. (1997). A yeast mutant showing diagnostic markers of early and late apoptosis. J Cell Biol 139, 729–34.

Madeo, F., Frohlich, E., Ligr, M., Grey, M., Sigrist, S. J., Wolf, D. H. and Frohlich, K. U. (1999). Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol 145, 757–67.

Madeo, F., Herker, E., Maldener, C., Wissing, S., Lachelt, S., Herlan, M., Fehr, M., Lauber, K., Sigrist, S. J., Wesselborg, S. and Frohlich, K. U. (2002). A caspase-related protease regulates apoptosis in yeast. Mol Cell 9, 911–7.

Matsuyama, S., Llopis, J., Deveraux, Q. L., Tsien, R. Y. and Reed, J. C. (2000). Changes in intramitochondrial and cytosolic pH: early events that modulate caspase activation during apoptosis. Nat Cell Biol 2, 318–25.

Mazzoni, C. and Falcone, C. (2008). Caspase-dependent apoptosis in yeast. Biochim Biophys Acta 1783, 1320–7.

Mazzoni, C., Herker, E., Palermo, V., Jungwirth, H., Eisenberg, T., Madeo, F. and Falcone, C. (2005). Yeast caspase 1 links messenger RNA stability to apoptosis in yeast. EMBO Rep 6, 1076–81.

Mazzoni, C., Mancini, P., Verdone, L., Madeo, F., Serafini, A., Herker, E. and Falcone, C. (2003). A truncated form of KlLsm4p and the absence of factors involved in mRNA decapping trigger apoptosis in yeast. Mol Biol Cell 14, 721–9.

Palermo, V., Falcone, C. and Mazzoni, C. (2007). Apoptosis and aging in mitochondrial morphology mutants of S. cerevisiae. Folia Microbiol (Praha) 52, 479–83.

Pozniakovsky, A. I., Knorre, D. A., Markova, O. V., Hyman, A. A., Skulachev, V. P. and Severin, F. F. (2005). Role of mitochondria in the pheromone- and amiodarone-induced programmed death of yeast. J Cell Biol 168, 257–69.

Priault, M., Chaudhuri, B., Clow, A., Camougrand, N. and Manon, S. (1999). Investigation of bax-induced release of cytochrome c from yeast mitochondria permeability of mitochondrial membranes, role of VDAC and ATP requirement. Eur J Biochem 260, 684–91.

Qiu, J., Yoon, J. H. and Shen, B. (2005). Search for apoptotic nucleases in yeast: role of Tat-D nuclease in apoptotic DNA degradation. J Biol Chem 280, 15370–9.

Reiter, J., Herker, E., Madeo, F. and Schmitt, M. J. (2005). Viral killer toxins induce caspase-mediated apoptosis in yeast. J Cell Biol 168, 353–8.

Roux, A. E., Quissac, A., Chartrand, P., Ferbeyre, G. and Rokeach, L. A. (2006). Regulation of chronological aging in Schizosaccharomyces pombe by the protein kinases Pka1 and Sck2. Aging Cell 5, 345–57.

Sato, T., Hanada, M., Bodrug, S., Irie, S., Iwama, N., Boise, L. H., Thompson, C. B., Golemis, E., Fong, L., Wang, H. G. and et al. (1994). Interactions among members of the Bcl-2 protein family analyzed with a yeast two-hybrid system. Proc Natl Acad Sci U S A 91, 9238–42.

Schmitt, M. J. and Breinig, F. (2006). Yeast viral killer toxins: lethality and self-protection. Nat Rev Microbiol 4, 212–21.

Severin, F. F. and Hyman, A. A. (2002). Pheromone induces programmed cell death in S. cerevisiae. Curr Biol 12, R233–5.

Shirogane, T., Fukada, T., Muller, J. M., Shima, D. T., Hibi, M. and Hirano, T. (1999). Synergistic roles for Pim-1 and c-Myc in STAT3-mediated cell cycle progression and antiapoptosis. Immunity 11, 709–19.

Silva, R. D., Sotoca, R., Johansson, B., Ludovico, P., Sansonetty, F., Silva, M. T., Peinado, J. M. and Corte-Real, M. (2005). Hyperosmotic stress induces metacaspase- and mitochondria-dependent apoptosis in Saccharomyces cerevisiae. Mol Microbiol 58, 824–34.

Teparic, R., Stuparevic, I. and Mrsa, V. (2004). Increased mortality of Saccharomyces cerevisiae cell wall protein mutants. Microbiology 150, 3145–50.

Vachova, L. and Palkova, Z. (2005). Physiological regulation of yeast cell death in multicellular colonies is triggered by ammonia. J Cell Biol 169, 711–7.

Wilson, M. A., St. Amour, C. V., Collins, J. L., Ringe, D. and Petsko, G. A. (2004). The 1.8-A resolution crystal structure of YDR533Cp from Saccharomyces cerevisiae: a member of the DJ-1/ThiJ/PfpI superfamily. Proc Natl Acad Sci U S A 101, 1531–6.

Wissing, S., Ludovico, P., Herker, E., Buttner, S., Engelhardt, S. M., Decker, T., Link, A., Proksch, A., Rodrigues, F., Corte-Real, M., Frohlich, K. U., Manns, J., Cande, C., Sigrist, S. J., Kroemer, G. and Madeo, F. (2004). An AIF orthologue regulates apoptosis in yeast. J Cell Biol 166, 969–74.

Zhang, N. N., Dudgeon, D. D., Paliwal, S., Levchenko, A., Grote, E. and Cunningham, K. W. (2006). Multiple signaling pathways regulate yeast cell death during the response to mating pheromones. Mol Biol Cell 17, 3409–22.

Zhang, Q., Chieu, H. K., Low, C. P., Zhang, S., Heng, C. K. and Yang, H. (2003). Schizosaccharomyces pombe cells deficient in triacylglycerols synthesis undergo apoptosis upon entry into the stationary phase. J Biol Chem 278, 47145–55.