Abstract
It has been shown that defects in cell fusion during mating can trigger programmed cell death in the yeast Saccharomyces cerevisiae. We wished to test whether defects in nuclear migration during cell fusion have the same effect. A partial pedigree analysis of nine kar1 × KAR1 crosses of two different types (four α KAR1 × a kar1 and five α kar1 × a KAR1 crosses) was carried out, and quantitative estimates of the frequencies of different mother/daughter (m/d) classes were obtained. The kar1 mutation affects nuclear congression and delays nuclear fusion. In each cross tested, the nucleus that entered the first bud tended to be the one contributed by the cell that carried the wild-type allele of KAR1. If budding was delayed by nutrient limitation, the kar1 nucleus could be rescued, indicating that the primary effect of the kar1 mutation is that it slows spindle action. Many m/d classes appear as a result of the degradation of one of the nuclei in the heterokaryon. Loss of nuclei in heterokaryons was accompanied by an accumulation of reactive oxygen species (ROS), and by abnormalities in nuclear structure revealed by TUNEL (terminal transferase-mediated dUTP nick end-labeling) analysis, DAPI staining and by histone-GFP fluorescence patterns which suggested an apoptosis-like process. Often only one nucleus was degraded, and ROS accumulation was restricted to one half of the zygote. We therefore suggest that the data obtained can be explained by apoptosis-like death of a half-cell (cell body).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguilaniu H, Gustafsson L, Rigoulet M, Nystrom T (2003) Asymmetric inheritance of oxidatively damaged proteins during cytokinesis. Science 299:1751–1753
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Physiol Plant Mol Biol 55:379–399
Baluska F, Volkmann D, Barlow PW (2004a) Eukaryotic cells and their cell bodies: cell theory revised. Ann Bot 94:9–32
Baluska F, Volkmann D, Barlow PW (2004b) Cell bodies in a cage. Nature 428:371
Bettiga M, Calzani L, Orlandi I, Alberghina L, Vai M (2004) Involvement of the yeast metacaspase Yca1 in ubp10Δ-programmed cell death. FEMS Yeast Res 5:141–147
Burhans WC, Weinberger M, Marchetti MA, Ramachandran L, D’Urso G, Huberman JA (2003) Apoptosis-like yeast cell death in response to DNA damage and replication defects. Mutat Res 532:227–243
Fahrenkrog B, Sauder U, Aebi U (2004) The S. cerevisiae HtrA-like protein Nma111p is a nuclear serine protease that mediates yeast apoptosis. J Cell Sci 117:115–126
Fannjiang Y, Cheng W-C, Lee SJ, Qi B, Pevsner J, McCaffery JM, Hill RB, Basanez G, Hardwick JM (2004) Mitochondrial fission proteins regulate programmed cell death in yeast. Genes Dev 18:2785–2797
Frohlich K-U, Madeo F (2001) Apoptosis in yeast: a new model for aging research. Exp Gerontol 37:27–31
Granot D, Levine A, Dor-Hefetz E (2003) Sugar-induced apoptosis in yeast cells. FEMS Yeast Res 4:7–13
Guimares CA, Linden R (2004) Programmed cell death: apoptosis and alternative death styles. Eur J Biochem 271:1638–1650
Helfant AH (2002) Composition of the spindle body of Saccharomyces cerevisiae and the proteins involved in its duplication. Curr Genet 40:291–301
Herker E, Jungwirth H, Lehmann KA, Maldener C, Frohlich K-U, Wissing S, Buttner S, Fehr M, Sigrist S, Madeo F (2004) Chronological aging leads to apoptosis in yeast. J Cell Biol 164:501–507
Koc A, Gasch AP, Rutherford JC, Kim H-Y, Gladyshev VN (2004) Methionine sulfoxide reductase regulation of yeast lifespan reveals reactive oxygen species-dependent and -independent components of aging. Proc Natl Acad Sci USA 101:7999–8004
Lancashire WE, Mattoon JR (1979) Cytoduction: a tool for mitochondrial genetic studies in yeast. Mol Gen Genet 170:333–344
Laun P, Pichova A, Madeo F, Fuchs J, Ellinger A, Kohlwein S, Dawes I, Frohlich K-U, Breitenbach M (2001) Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Mol Microbiol 39:1166–1173
Ligr M, Madeo F, Frohlich E, Hilt W, Frohlich K-U, Wolf DH (1998) Mammaliam Bax triggers apoptotic changes in yeast. FEBS Lett 438:61–65
Ludovico P, Sousa MJ, Silva MT, Leao C, Corte-Real M (2001) Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid. Microbiology 147:2409–2415
Madeo F, Frohlich E, Frohlich KU (1997) A yeast mutant showing diagnostic markers of early and late apoptosis. J Cell Biol 139:729–734
Madeo F, Frohlich E, Ligr M, Grey M, Sigrist SJ, Wolf DH, Frohlich K-U (1999) Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol 145:757–767
Madeo F, Engelhardt S, Hecker E, Lehmann N, Maldener C, Proksch H, Wissing S, Frohlich K-U (2002a) Apoptosis in yeast: a new model system with applications in cell biology and medicine. Curr Genet 41:208–216
Madeo F, Herker E, Maldener C, Wissing S, Lachelt S, Herlan M, Fehr M, Lauber K, Sigrist SJ, Wesselborg S, Frohlich K-U (2002b) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9:911–917
Moraitis C, Curran BP (2004) Reactive oxygen species may influence the heat shock response and stress tolerance in the yeast Saccharomyces cerevisiae. Yeast 21:313–323
Nevzglyadova OV, Artyomov AV, Gaivoronski AA, Soidla TR (2002) Concealed nuclei in Saccharomyces strains. FEMS Yeast Res 2:471–479
Nevzglyadova OV, Artyomov AV, Mikhailova EV, Soidla TR (2004) The impact of manipulations with cytoplasmically inherited factors on nuclear transmission and degradation in yeast heterokaryons. Curr Genet 45:273–282
Pereira G, Grueneberg U, Knop M, Schiebel E (1999) Interaction of the yeast γ-tubulin complex-binding protein Spc72p with Kar1p is essential for microtubule function during karyogamy. EMBO J 18:4180–4195
Rose MD (1996) Nuclear fusion in the yeast Saccharomyces cerevisiae. Annu Rev Cell Biol 12:663–695
Rose MD, Fink GR (1987) KAR1, a gene required for function of both intranuclear and extranuclear microtubules in yeast. Cell 48:1047–1060
Sachs L (1972) Statistische Auswertungsmethoden. Springer, Berlin-Heidelberg-New York
Severin FF, Hyman AA (2002) Pheromone induces programmed cell death in S. cerevisiae. Curr Biol 12:R233–R235
Sherman F, Fink GR, Hicks JB (1986) Laboratory course manual for methods in yeast genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor
Skulachev VP (2002) Programmed death phenomena: from organelle to organism. Ann NY Acad Sci 959:214–237
Thorpe GW, Fong CS, Alic N, Higgins VJ, Dawes IW (2004) Cells have distinct mechanisms to maintain protection against different reactive oxygen species: oxidative-stress-response genes. Proc Natl Acad Sci USA 101:6564–6569
Vallen EA, Hiller MA, Scherson TY, Rose MD (1992a) Separate domains of KAR1 mediate distinct functions in mitosis and nuclear fusion. J Cell Biol 117:1277–1287
Vallen EA, Scherson TY, Roberts T, van Zee K, Rose MD (1992b) Asymmetric mitotic segregation of the yeast spindle pole body. Cell 69:505–515
Wissing S, et al (2004) An AIF orthologue regulates apoptosis in yeast. J Cell Biol 166:969–974
Wysocki R, Kron SJ (2004) Yeast cell death during DNA damage arrest is independent of caspase or reactive oxygen species. J Cell Biol 166:311–316
Acknowledgements
This work was partly supported by the INTAS grant 2001-2347 to O.V. Nevzglyadova and the Russian MCB RAS grant. The work was carried out in compliance with the current Russian Federation laws regulating genetic experimentation.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by C. Hollenberg
Rights and permissions
About this article
Cite this article
Nevzglyadova, O.V., Artyomov, A.V., Mikhailova, E.V. et al. Bud selection and apoptosis-like degradation of nuclei in yeast heterokaryons: a KAR1 effect. Mol Genet Genomics 274, 419–427 (2005). https://doi.org/10.1007/s00438-005-0036-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-005-0036-1