Abstract
Although questioned for a long time, accumulating evidence now strongly supports the presence of apoptotic processes in lower eukaryotes. Especially in fungi, both yeasts and filamentous fungi, more and more examples of an apoptotic cell death programme emerged during the past decade. This work revealed that, although fungal apoptosis shares significant similarity with mammalian apoptosis, the mechanistic details involved in the regulation and execution are different. Here we summarise current knowledge about apoptosis in yeasts and in filamentous fungi and we focus on a comprehensive description and evaluation of the role in development and ageing. Specific emphasis is laid on the impact of apoptosis in host--pathogen interactions, sexual development and lifespan control. In addition, we evaluate the differences between fungal and mammalian apoptosis.
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References
Ahn SH, Cheung WL, Hsu JY, Diaz RL, Smith MM, Allis CD (2005a) Sterile 20 kinase phosphorylates histone H2B at serine 10 during hydrogen peroxide-induced apoptosis in S. cerevisiae. Cell 120:25–36
Ahn SH, Henderson KA, Keeney S, Allis CD (2005b) H2B (Ser10) phosphorylation is induced during apoptosis and meiosis in S. cerevisiae. Cell Cycle 4:780–783
Almeida T, Marques M, Mojzita D, Amorim MA, Silva RD, Almeida B, Rodrigues P, Ludovico P, Hohmann S, Moradas-Ferreira P, Corte-Real M, Costa V (2008) Isc1p plays a key role in hydrogen peroxide resistance and chronological lifespan through modulation of iron levels and apoptosis. Mol Biol Cell 19:865–876
Barhoom S, Sharon A (2007) Bcl-2 proteins link programmed cell death with growth and morphogenetic adaptations in the fungal plant pathogen Colletotrichum gloeosporioides. Fungal Genet Biol 44:32–43
Belcour L, Begel O, Mosse MO, Vierny-Jamet C (1981) Mitochondrial DNA amplification in senescent cultures of Podospora anserina: Variability between the retained, amplified sequences. Curr Genet 3:13–21
Belcour L, Begel O, Picard-Bennoun M (1991) A site-specific deletion in mitochondrial DNA of Podospora is under the control of nuclear genes. Proc Natl Acad Sci USA 88:3579–3583
Bok JW, Chung D, Balajee SA, Marr KA, Andes D, Nielsen KF, Frisvad JC, Kirby KA, Keller NP (2006) GliZ, a transcriptional regulator of gliotoxin biosynthesis, contributes to Aspergillus fumigatus virulence. Infect Immun 74:6761–6768
Borghouts C, Kimpel E, Osiewacz HD (1997) Mitochondrial DNA rearrangements of Podospora anserina are under the control of the nuclear gene grisea. Proc Natl Acad Sci USA 94:10768–10773
Borghouts C, Osiewacz HD (1998) GRISEA, a copper-modulated transcription factor from Podospora anserina involved in senescence and morphogenesis, is an ortholog of MAC1 in Saccharomyces cerevisiae. Mol Gen Genet 260:492–502
Borghouts C, Kerschner S, Osiewacz HD (2000) Copper-dependence of mitochondrial DNA rearrangements in Podospora anserina. Curr Genet 37:268–275
Borghouts C, Werner A, Elthon T, Osiewacz HD (2001) Copper-modulated gene expression and senescence in the filamentous fungus Podospora anserina. Mol Cell Biol 21:390–399
Büttner S, Eisenberg T, Carmona-Gutierrez D, Ruli D, Knauer H, Ruckenstuhl C, Sigrist C, Wissing S, Kollroser M, Fröhlich KU, Sigrist S, Madeo F (2007) Endonuclease G regulates budding yeast life and death. Mol Cell 25:233–246
Chen C, Dickman MB (2005) Proline suppresses apoptosis in the fungal pathogen Colletotrichum trifolii. Proc Natl Acad Sci USA 102:3459–3464
Cory S, Adams JM (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2:647–656
Cummings DJ, Belcour L, Grandchamp C (1979) Mitochondrial DNA from Podospora anserina. II. Properties of mutant DNA and multimeric circular DNA from senescent cultures. Mol Gen Genet 171:239–250
Davies DR, Bindschedler LV, Strickland TS, Bolwell GP (2006) Production of reactive oxygen species in Arabidopsis thaliana cell suspension cultures in response to an elicitor from Fusarium oxysporum: implications for basal resistance. J Exp Bot 57:1817–1827
Degterev A, Boyce M, Yuan J (2003) A decade of caspases. Oncogene 22:8543–8567
Dufour E, Boulay J, Rincheval V, Sainsard-Chanet A (2000) A causal link between respiration and senescence in Podospora anserina. Proc Natl Acad Sci USA 97:4138–4143
Eisenberg T, Büttner S, Kroemer G, Madeo F (2007) The mitochondrial pathway in yeast apoptosis. Apoptosis 12:1011–1023
Fabrizio P, Battistella L, Vardavas R, Gattazzo C, Liou LL, Diaspro A, Dossen JW, Gralla EB, Longo VD (2004) Superoxide is a mediator of an altruistic aging program in Saccharomyces cerevisiae. J Cell Biol 166:1055–1067
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 WC, 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
Forman HJ, Torres M (2002) Reactive oxygen species and cell signaling: respiratory burst in macrophage signaling. Am J Respir Crit Care Med 166:S4–S8
Galgoczy L, Papp T, Lukacs G, Leiter E, Pocsi I, Vagvolgyi C (2007) Interactions between statins and Penicillium chrysogenum antifungal protein (PAF) to inhibit the germination of sporangiospores of different sensitive Zygomycetes. FEMS Microbiol Lett 270:109–115
Glass NL, Dementhon K (2006) Non-self recognition and programmed cell death in filamentous fungi. Curr Opin Microbiol 9:553–558
Gonzalez IJ, Desponds C, Schaff C, Mottram JC, Fasel N (2007) Leishmania major metacaspase can replace yeast metacaspase in programmed cell death and has arginine-specific cysteine peptidase activity. Int J Parasitol 37:161–172
Gourlay CW, Ayscough KR (2005) Identification of an upstream regulatory pathway controlling actin-mediated apoptosis in yeast. J Cell Sci 118:2119–2132
Gourlay CW, Carpp LN, Timpson P, Winder SJ, Ayscough KR (2004) A role for the actin cytoskeleton in cell death and aging in yeast. J Cell Biol 164:803–809
Greenberg JT, Yao N (2004) The role and regulation of programmed cell death in plant–pathogen interactions. Cell Microbiol 6:201–211
Gun LD, Shin SY, Maeng CY, Jin ZZ, Kim KL, Hahm KS (1999) Isolation and characterization of a novel antifungal peptide from Aspergillus niger. Biochem Biophys Res Commun 263:646–651
Gwinn MR, Vallyathan V (2006) Respiratory burst: role in signal transduction in alveolar macrophages. J Toxicol Environ Health B Crit Rev 9:27–39
Haarer BK, Amberg DC (2004) Old yellow enzyme protects the actin cytoskeleton from oxidative stress. Mol Biol Cell 15:4522–4531
Hajjeh RA, Sofair AN, Harrison LH, Lyon GM, Arthington-Skaggs BA, Mirza SA, Phelan M, Morgan J, Lee-Yang W, Ciblak MA, Benjamin LE, Sanza LT, Huie S, Yeo SF, Brandt ME, Warnock DW (2004) Incidence of bloodstream infections due to Candida species and in vitro susceptibilities of isolates collected from 1998 to 2000 in a population-based active surveillance program. J Clin Microbiol 42:1519–1527
Hamann A, Brust D, Osiewacz HD (2007) Deletion of putative apoptosis factors leads to lifespan extension in the fungal ageing model Podospora anserina. Mol Microbiol 65:948–958
Hauptmann P, Lehle L (2008) Kex1 protease is involved in yeast cell death induced by defective N-glycosylation, acetic acid and during chronological aging. J Biol Chem 283:19151–19163
Heeren G, Jarolim S, Laun P, Rinnerthaler M, Stolze K, Perrone GG, Kohlwein SD, Nohl H, Dawes IW, Breitenbach M (2004) The role of respiration, reactive oxygen species and oxidative stress in mother cell-specific ageing of yeast strains defective in the RAS signalling pathway. FEMS Yeast Res 5:157–167
Hengartner MO (2000) The biochemistry of apoptosis. Nature 407:770–776
Herker E, Jungwirth H, Lehmann KA, Maldener C, Fröhlich KU, Wissing S, Büttner S, Fehr M, Sigrist S, Madeo F (2004) Chronological aging leads to apoptosis in yeast. J Cell Biol 164:501–507
Hornby JM, Jensen EC, Lisec AD, Tasto JJ, Jahnke B, Shoemaker R, Dussault P, Nickerson KW (2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microbiol 67:2982–2992
Ito S, Ihara T, Tamura H, Tanaka S, Ikeda T, Kajihara H, Dissanayake C, bdel-Motaal FF, El-Sayed MA (2007) alpha-Tomatine, the major saponin in tomato, induces programmed cell death mediated by reactive oxygen species in the fungal pathogen Fusarium oxysporum. FEBS Lett 581:3217–3222
Jamet-Vierny C, Contamine V, Boulay J, Zickler D, Picard M (1997) Mutations in genes encoding the mitochondrial outer membrane proteins Tom70 and Mdm10 of Podospora anserina modify the spectrum of mitochondrial DNA rearrangements associated with cellular death. Mol Cell Biol 17:6359–6366
Jürgensmeier JM, Krajewski S, Armstrong RC, Wilson GM, Oltersdorf T, Fritz LC, Reed JC, Ottilie S (1997) Bax- and Bak-induced cell death in the fission yeast Schizosaccharomyces pombe. Mol Biol Cell 8:325–339
Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26:239–257
Kim BY, Lee KS, Choo YM, Kim I, Je YH, Woo SD, Lee SM, Park HC, Sohn HD, Jin BR (2008) Insect transferrin functions as an antioxidant protein in a beetle larva. Comp Biochem Physiol B Biochem Mol Biol. 150:16–169
Klassen R, Meinhardt F (2003) Structural and functional analysis of the killer element pPin1-3 from Pichia inositovora. Mol Genet Genomics 270:190–199
Klassen R, Meinhardt F (2005) Induction of DNA damage and apoptosis in Saccharomyces cerevisiae by a yeast killer toxin. Cell Microbiol 7:393–401
Klassen R, Teichert S, Meinhardt F (2004) Novel yeast killer toxins provoke S-phase arrest and DNA damage checkpoint activation. Mol Microbiol 53:263–273
Kleckner N, Zickler D, Jones GH, Dekker J, Padmore R, Henle J, Hutchinson J (2004) A mechanical basis for chromosome function. Proc Natl Acad Sci USA 101:12592–12597
Koonin EV, Aravind L (2002) Origin and evolution of eukaryotic apoptosis: the bacterial connection. Cell Death Differ 9:394–404
Krause F, Scheckhuber CQ, Werner A, Rexroth S, Reifschneider NH, Dencher NA, Osiewacz HD (2004) Supramolecular organization of cytochrome c oxidase- and alternative oxidase-dependent respiratory chains in the filamentous fungus Podospora anserina. J Biol Chem 279:26453–26461
Krause F, Scheckhuber CQ, Werner A, Rexroth S, Reifschneider NH, Dencher NA, Osiewacz HD (2006) OXPHOS Supercomplexes: respiration and life-span control in the aging model Podospora anserina. Ann NY Acad Sci 1067:106–115
Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87:99–163
Kück U, Stahl U, Esser K (1981) Plasmid-like DNA is part of mitochondrial DNA in Podospora anserina. Curr Genet 3:151–156
Kück U, Osiewacz HD, Schmidt U, Kappelhoff B, Schulte E, Stahl U, Esser K (1985) The onset of senescence is affected by DNA rearrangements of a discontinuous mitochondrial gene in Podospora anserina. Curr Genet 9:373–382
Kweon YO, Paik YH, Schnabl B, Qian T, Lemasters JJ, Brenner DA (2003) Gliotoxin-mediated apoptosis of activated human hepatic stellate cells. J Hepatol 39:38–46
Laun P, Pichova A, Madeo F, Fuchs J, Ellinger A, Kohlwein S, Dawes I, Fröhlich KU, Breitenbach M (2001) Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Mol Microbiol 39:1166–1173
Leiter E, Szappanos H, Oberparleiter C, Kaiserer L, Csernoch L, Pusztahelyi T, Emri T, Pocsi I, Salvenmoser W, Marx F (2005) Antifungal protein PAF severely affects the integrity of the plasma membrane of Aspergillus nidulans and induces an apoptosis-like phenotype. Antimicrob Agents Chemother 49:2445–2453
Li W, Sun L, Liang Q, Wang J, Mo W, Zhou B (2006) Yeast AMID homologue Ndi1p displays respiration-restricted apoptotic activity and is involved in chronological aging. Mol Biol Cell 17:1802–1811
Liang Q, Zhou B (2007) Copper and manganese induce yeast apoptosis via different pathways. Mol Biol Cell 18:4741–4749
Liang Q, Li W, Zhou B (2008) Caspase-independent apoptosis in yeast. Biochim Biophys Acta 1783: 1311–1319
Longo VD, Ellerby LM, Bredesen DE, Valentine JS, Gralla EB (1997) Human Bcl-2 reverses survival defects in yeast lacking superoxide dismutase and delays death of wild-type yeast. J Cell Biol 137:1581–1588
Lorin S, Dufour E, Boulay J, Begel O, Marsy S, Sainsard-Chanet A (2001) Overexpression of the alternative oxidase restores senescence and fertility in a long-lived respiration-deficient mutant of Podospora anserina. Mol Microbiol 42:1259–1267
Lu BC (2000) The control of meiosis progression in the fungus Coprinus cinereus by light/dark cycles. Fungal Genet Biol 31:33–41
Lu BC, Gallo N, Kues U (2003) White-cap mutants and meiotic apoptosis in the basidiomycete Coprinus cinereus. Fungal Genet Biol 39:82–93
Ludovico P, Rodrigues F, Almeida A, Silva MT, Barrientos A, 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
Maas MF, de Boer HJ, Debets AJ, Hoekstra RF (2004) The mitochondrial plasmid pAL2-1 reduces calorie restriction mediated life span extension in the filamentous fungus Podospora anserina. Fungal Genet Biol 41:865–871
Maas MF, Hoekstra RF, Debets AJ (2007) A mitochondrial mutator plasmid that causes senescence under dietary restricted conditions. BMC Genet 8:9
Madeo F, Fröhlich E, Fröhlich KU (1997) A yeast mutant showing diagnostic markers of early and late apoptosis. J Cell Biol 139:729–734
Madeo F, Herker E, Maldener C, Wissing S, Lächelt S, Herlan M, Fehr M, Lauber K, Sigrist SJ, Wesselborg S, Fröhlich KU (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9:911–917
Manon S, Chaudhuri B, Guerin M (1997) Release of cytochrome c and decrease of cytochrome c oxidase in Bax-expressing yeast cells, and prevention of these effects by coexpression of Bcl-xL. FEBS Lett 415:29–32
Marek SM, Wu J, Louise GN, Gilchrist DG, Bostock RM (2003) Nuclear DNA degradation during heterokaryon incompatibility in Neurospora crassa. Fungal Genet Biol 40:126–137
Marx F, Binder U, Leiter E, Pocsi I (2008) The Penicillium chrysogenum antifungal protein PAF, a promising tool for the development of new antifungal therapies and fungal cell biology studies. Cell Mol Life Sci 65:445–454
Mousavi SA, Robson GD (2003) Entry into the stationary phase is associated with a rapid loss of viability and an apoptotic-like phenotype in the opportunistic pathogen Aspergillus fumigatus. Fungal Genet Biol 39:221–229
Mousavi SA, Robson GD (2004) Oxidative and amphotericin B-mediated cell death in the opportunistic pathogen Aspergillus fumigatus is associated with an apoptotic-like phenotype. Microbiology 150:1937–1945
Odat O, Matta S, Khalil H, Kampranis SC, Pfau R, Tsichlis PN, Makris AM (2007) Old yellow enzymes, highly homologous FMN oxidoreductases with modulating roles in oxidative stress and programmed cell death in yeast. J Biol Chem 282:36010–36023
Osiewacz HD, Esser K (1984) The mitochondrial plasmid of Podospora anserina: a mobile intron of a mitochondrial gene. Curr Genet 8:299–305
Pahl HL, Krauss B, Schulze-Osthoff K, Decker T, Traenckner EB, Vogt M, Myers C, Parks T, Warring P, Mühlbacher A, Czernilofsky AP, Baeuerle PA (1996) The immunosuppressive fungal metabolite gliotoxin specifically inhibits transcription factor NF-κB. J Exp Med 183:1829–1840
Pereira C, Camougrand N, Manon S, Sousa MJ, Corte-Real M (2007) ADP/ATP carrier is required for mitochondrial outer membrane permeabilization and cytochrome c release in yeast apoptosis. Mol Microbiol 66:571–582
Pinan-Lucarré B, Paoletti M, Dementhon K, Coulary-Salin B, Clave C (2003) Autophagy is induced during cell death by incompatibility and is essential for differentiation in the filamentous fungus Podospora anserina. Mol Microbiol 47:321–333
Pinan-Lucarré B, Balguerie A, Clave C (2005) Accelerated cell death in Podospora autophagy mutants. Eukaryot Cell 4:1765–1774
Pinan-Lucarré B, Paoletti M, Clave C (2007) Cell death by incompatibility in the fungus Podospora. Semin Cancer Biol 17:101–111
Reiter J, Herker E, Madeo F, Schmitt MJ (2005) Viral killer toxins induce caspase-mediated apoptosis in yeast. J Cell Biol 168:353–358
Ribot C, Hirsch J, Balzergue S, Tharreau D, Notteghem JL, Lebrun MH, Morel JB (2008) Susceptibility of rice to the blast fungus, Magnaporthe grisea. J Plant Physiol 165:114–124
Richie DL, Miley MD, Bhabhra R, Robson GD, Rhodes JC, Askew DS (2007) The Aspergillus fumigatus metacaspases CasA and CasB facilitate growth under conditions of endoplasmic reticulum stress. Mol Microbiol 63:591–604
Rinnerthaler M, Jarolim S, Heeren G, Palle E, Perju S, Klinger H, Bogengruber E, Madeo F, Braun RJ, Breitenbach-Koller L, Breitenbach M, Laun P (2006) MMI1 (YKL056c, TMA19), the yeast orthologue of the translationally controlled tumor protein (TCTP) has apoptotic functions and interacts with both microtubules and mitochondria. Biochim Biophys Acta 1757:631–638
Saelens X, Festjens N, Vande WL, van GM, van LG, Vandenabeele P (2004) Toxic proteins released from mitochondria in cell death. Oncogene 23:2861–2874
Scheckhuber CQ, Erjavec N, Tinazli A, Hamann A, Nyström T, Osiewacz HD (2007) Reducing mitochondrial fission results in increased life span and fitness of two fungal ageing models. Nat Cell Biol 9:99–105
Schmitt MJ, Breinig F (2006) Yeast viral killer toxins: lethality and self-protection. Nat Rev Microbiol 4:212–221
Schrick K, Garvik B, Hartwell LH (1997) Mating in Saccharomyces cerevisiae: the role of the pheromone signal transduction pathway in the chemotropic response to pheromone. Genetics 147:19–32
Sellem CH, Lemaire C, Lorin S, Dujardin G, Sainsard-Chanet A (2005) Interaction between the oxa1 and rmp1 genes modulates respiratory complex assembly and life span in Podospora anserina. Genetics 169:1379–1389
Sellem CH, Marsy S, Boivin A, Lemaire C, Sainsard-Chanet A (2007) A mutation in the gene encoding cytochrome c1 leads to a decreased ROS content and to a long-lived phenotype in the filamentous fungus Podospora anserina. Fungal Genet Biol 44:648–658
Semighini CP, Hornby JM, Dumitru R, Nickerson KW, Harris SD (2006a) Farnesol-induced apoptosis in Aspergillus nidulans reveals a possible mechanism for antagonistic interactions between fungi. Mol Microbiol 59:753–764
Semighini CP, Savoldi M, Goldman GH, Harris SD (2006b) Functional characterization of the putative Aspergillus nidulans poly(ADP-ribose) polymerase homolog PrpA. Genetics 173:87–98
Semighini CP, Murray N, Harris SD (2008) Inhibition of Fusarium graminearum growth and development by farnesol. FEMS Microbiol Lett 279:259–264
Severin FF, Hyman AA (2002) Pheromone induces programmed cell death in S. cerevisiae. Curr Biol 12:R233–R235
Silar P, Picard M (1994) Increased longevity of EF-1 alpha high-fidelity mutants in Podospora anserina. J Mol Biol 235:231–236
Silva RD, Sotoca R, Johansson B, Ludovico P, Sansonetty F, Silva MT, Peinado JM, Corte-Real M (2005) Hyperosmotic stress induces metacaspase- and mitochondria-dependent apoptosis in Saccharomyces cerevisiae. Mol Microbiol 58:824–834
Stahl U, Lemke PA, Tudzynski P, Kück U, Esser K (1978) Evidence for plasmid like DNA in a filamentous fungus, the ascomycete Podospora anserina. Mol Gen Genet 162:341–343
Stumpferl SW, Stephan O, Osiewacz HD (2004) Impact of a disruption of a pathway delivering copper to mitochondria on Podospora anserina metabolism and life span. Eukaryotic Cell 3:200–211
Suen YK, Fung KP, Lee CY, Kong SK (2001) Gliotoxin induces apoptosis in cultured macrophages via production of reactive oxygen species and cytochrome c release without mitochondrial depolarization. Free Radic Res 35:1–10
Szappanos H, Szigeti GP, Pal B, Rusznak Z, Szucs G, Rajnavolgyi E, Balla J, Balla G, Nagy E, Leiter E, Pocsi I, Marx F, Csernoch L (2005) The Penicillium chrysogenum-derived antifungal peptide shows no toxic effects on mammalian cells in the intended therapeutic concentration. Naunyn Schmiedebergs Arch Pharmacol 371:122–132
Szappanos H, Szigeti GP, Pal B, Rusznak Z, Szucs G, Rajnavolgyi E, Balla J, Balla G, Nagy E, Leiter E, Pocsi I, Hagen S, Meyer V, Csernoch L (2006) The antifungal protein AFP secreted by Aspergillus giganteus does not cause detrimental effects on certain mammalian cells. Peptides 27:1717–1725
Theis T, Wedde M, Meyer V, Stahl U (2003) The antifungal protein from Aspergillus giganteus causes membrane permeabilization. Antimicrob Agents Chemother 47:588–593
Thrane C, Kaufmann U, Stummann BM, Olsson S (2004) Activation of caspase-like activity and poly (ADP-ribose) polymerase degradation during sporulation in Aspergillus nidulans. Fungal Genet Biol 41:361–368
Tudzynski P, Esser K (1979) Chromosomal and extrachromosomal control of senescence in the ascomycete Podospora anserina. Mol Gen Genet 173:71–84
Uren AG, O'Rourke K, Aravind LA, Pisabarro MT, Seshagiri S, Koonin EV, Dixit VM (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
Vachova L, Palkova Z (2007) Caspases in yeast apoptosis-like death: facts and artefacts. FEMS Yeast Res 7:12–21
Vercammen D, van de CB, De JG, Eeckhout D, Casteels P, Vandepoele K, Vandenberghe I, Van BJ, Inze D, Van BF (2004) Type II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J Biol Chem 279:45329–45336
Walczak H, Krammer PH (2000) The CD95 (APO-1/Fas) and the TRAIL (APO-2L) apoptosis systems. Exp Cell Res 256:58–66
Walter D, Wissing S, Madeo F, Fahrenkrog B (2006) The inhibitor-of-apoptosis protein Bir1p protects against apoptosis in S. cerevisiae and is a substrate for the yeast homologue of Omi/HtrA2. J Cell Sci 119: 1843–1851
Watanabe N, Lam E (2005) Two Arabidopsis metacaspases AtMCP1b and AtMCP2b are arginine/lysine-specific cysteine proteases and activate apoptosis-like cell death in yeast. J Biol Chem 280:14691–14699
Wissing S, Ludovico P, Herker E, Büttner S, Engelhardt SM, Decker T, Link A, Proksch A, Rodrigues F, Corte-Real M, Fröhlich KU, Manns J, Cande C, Sigrist SJ, Kroemer G, Madeo F (2004) An AIF orthologue regulates apoptosis in yeast. J Cell Biol 166:969–974
Zhang NN, Dudgeon DD, Paliwal S, Levchenko A, Grote E, Cunningham KW (2006) Multiple signaling pathways regulate yeast cell death during the response to mating pheromones. Mol Biol Cell 17:3409–3422
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The authors gratefully acknowledge the European Commission (LSHM-CT-2004-512020) and the Deutsche Forschungsgemeinschaft (Bonn, Germany) for supporting experimental work referenced from the authors' laboratory.
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Brust, D., Hamann, A., Osiewacz, H.D. (2009). Apoptosis in Fungal Development and Ageing. In: Anke, T., Weber, D. (eds) Physiology and Genetics. The Mycota, vol 15. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-00286-1_4
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