Skip to main content

Advertisement

SpringerLink
Log in

Necrosis in yeast

  • Unusual Model Systems for Cell Death Research
  • Published:
Apoptosis Aims and scope Submit manuscript

Abstract

Necrosis was long regarded as an accidental cell death process resulting from overwhelming cellular injury such as chemical or physical disruption of the plasma membrane. Such a definition, however, proved to be inapplicable to many necrotic scenarios. The discovery that genetic manipulation of several proteins either protected or enhanced necrotic cell death argued in favor of a regulated and hence programmed process, as it is the case for apoptosis. For more than a decade, yeast has served as a model for apoptosis research; recently, evidence accumulated that it also harbors a necrotic program. Here, we summarize the current knowledge about factors that control necrotic cell death in yeast. Mitochondria, aging and a low pH are positive regulators of this process while cellular polyamines (e.g. spermidine) and endonuclease G as well as homeostatic organelles like the vacuole or peroxisomes are potent inhibitors of necrosis. Physiological necrosis may stimulate intercellular signaling via the release of necrotic factors that promote viability of healthy cells and, thus, assure survival of the clone. Together, the data obtained in yeast argue for the existence of a necrotic program, which controls longevity and whose physiological function may thus be aging.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Baehrecke EH (2002) How death shapes life during development. Nat Rev Mol Cell Biol 3:779–787

    PubMed  Google Scholar 

  2. Mayhew TM, Myklebust R, Whybrow A, Jenkins R (1999) Epithelial integrity, cell death and cell loss in mammalian small intestine. Histol Histopathol 14:257–267

    PubMed  Google Scholar 

  3. Holler N, Zaru R, Micheau O et al (2000) Fas triggers an alternative, caspase-8-independent cell death pathway using the kinase RIP as effector molecule. Nat Immunol 1:489–495

    PubMed  Google Scholar 

  4. Walker NI, Harmon BV, Gobe GC, Kerr JF (1988) Patterns of cell death. Methods Achiev Exp Pathol 13:18–54

    PubMed  Google Scholar 

  5. Zong WX, Thompson CB (2006) Necrotic death as a cell fate. Genes Dev 20:1–15

    PubMed  Google Scholar 

  6. Golstein P, Kroemer G (2007) Cell death by necrosis: towards a molecular definition. Trends Biochem Sci 32:37–43

    PubMed  Google Scholar 

  7. Festjens N, Vanden Berghe T, Vandenabeele P (2006) Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta 1757:1371–1387

    PubMed  Google Scholar 

  8. Syntichaki P, Tavernarakis N (2002) Death by necrosis. Uncontrollable catastrophe, or is there order behind the chaos? EMBO Rep 3:604–609

    PubMed  Google Scholar 

  9. Syntichaki P, Tavernarakis N (2003) The biochemistry of neuronal necrosis: rogue biology? Nat Rev Neurosci 4:672–684

    PubMed  Google Scholar 

  10. Galluzzi L, Kepp O, Kroemer G (2009) RIP kinases initiate programmed necrosis. J Mol Cell Biol 1:8–10

    PubMed  Google Scholar 

  11. Artal-Sanz M, Samara C, Syntichaki P, Tavernarakis N (2006) Lysosomal biogenesis and function is critical for necrotic cell death in Caenorhabditis elegans. J Cell Biol 173:231–239

    PubMed  Google Scholar 

  12. Samara C, Syntichaki P, Tavernarakis N (2008) Autophagy is required for necrotic cell death in Caenorhabditis elegans. Cell Death Differ 15:105–112

    PubMed  Google Scholar 

  13. Vanlangenakker N, Berghe TV, Krysko DV, Festjens N, Vandenabeele P (2008) Molecular mechanisms and pathophysiology of necrotic cell death. Curr Mol Med 8:207–220

    PubMed  Google Scholar 

  14. Akiyama H, Barger S, Barnum S et al (2000) Inflammation and Alzheimer’s disease. Neurobiol Aging 21:383–421

    PubMed  Google Scholar 

  15. Tavernarakis N (2007) Cardiomyocyte necrosis: alternative mechanisms, effective interventions. Biochim Biophys Acta 1773:480–482

    PubMed  Google Scholar 

  16. Proskuryakov SY, Konoplyannikov AG, Gabai VL (2003) Necrosis: a specific form of programmed cell death? Exp Cell Res 283:1–16

    PubMed  Google Scholar 

  17. Kroemer G, Martin SJ (2005) Caspase-independent cell death. Nat Med 11:725–730

    PubMed  Google Scholar 

  18. Degterev A, Huang Z, Boyce M et al (2005) Chemical inhibitor of nonapoptotic cell death with therapeutic potential for ischemic brain injury. Nat Chem Biol 1:112–119

    PubMed  Google Scholar 

  19. Madeo F, Frohlich E, Frohlich KU (1997) A yeast mutant showing diagnostic markers of early and late apoptosis. J Cell Biol 139:729–734

    PubMed  Google Scholar 

  20. Madeo F, Frohlich E, Ligr M et al (1999) Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol 145:757–767

    PubMed  Google Scholar 

  21. Carmona-Gutierrez D, Eisenberg T, Buttner S, Meisinger C, Kroemer G, Madeo F (2010) Apoptosis in yeast: triggers, pathways, subroutines. Cell Death Differ (in press)

  22. Madeo F, Carmona-Gutierrez D, Ring J, Buttner S, Eisenberg T, Kroemer G (2009) Caspase-dependent and caspase-independent cell death pathways in yeast. Biochem Biophys Res Commun 382:227–231

    PubMed  Google Scholar 

  23. Almeida B, Silva A, Mesquita A, Sampaio-Marques B, Rodrigues F, Ludovico P (2008) Drug-induced apoptosis in yeast. Biochim Biophys Acta 1783:1436–1448

    PubMed  Google Scholar 

  24. Wissing S, Ludovico P, Herker E et al (2004) An AIF orthologue regulates apoptosis in yeast. J Cell Biol 166:969–974

    PubMed  Google Scholar 

  25. 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

    PubMed  Google Scholar 

  26. Buttner S, Eisenberg T, Carmona-Gutierrez D et al (2007) Endonuclease G regulates budding yeast life and death. Mol Cell 25:233–246

    PubMed  Google Scholar 

  27. Madeo F, Herker E, Maldener C et al (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9:911–917

    PubMed  Google Scholar 

  28. Eisenberg T, Buttner S, Kroemer G, Madeo F (2007) The mitochondrial pathway in yeast apoptosis. Apoptosis 12:1011–1023

    PubMed  Google Scholar 

  29. Pozniakovsky AI, Knorre DA, Markova OV, Hyman AA, Skulachev VP, Severin FF (2005) Role of mitochondria in the pheromone- and amiodarone-induced programmed death of yeast. J Cell Biol 168:257–269

    PubMed  Google Scholar 

  30. 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

    PubMed  Google Scholar 

  31. Ahn SH, Cheung WL, Hsu JY, Diaz RL, Smith MM, Allis CD (2005) Sterile 20 kinase phosphorylates histone H2B at serine 10 during hydrogen peroxide-induced apoptosis in S. cerevisiae. Cell 120:25–36

    PubMed  Google Scholar 

  32. Ahn SH, Diaz RL, Grunstein M, Allis CD (2006) Histone H2B deacetylation at lysine 11 is required for yeast apoptosis induced by phosphorylation of H2B at serine 10. Mol Cell 24:211–220

    PubMed  Google Scholar 

  33. Carmona-Gutierrez D, Madeo F (2006) Yeast unravels epigenetic apoptosis control: deadly chat within a histone tail. Mol Cell 24:167–169

    PubMed  Google Scholar 

  34. Fabrizio P, Battistella L, Vardavas R et al (2004) Superoxide is a mediator of an altruistic aging program in Saccharomyces cerevisiae. J Cell Biol 166:1055–1067

    PubMed  Google Scholar 

  35. Herker E, Jungwirth H, Lehmann KA et al (2004) Chronological aging leads to apoptosis in yeast. J Cell Biol 164:501–507

    PubMed  Google Scholar 

  36. Laun P, Pichova A, Madeo F et al (2001) Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Mol Microbiol 39:1166–1173

    PubMed  Google Scholar 

  37. Buttner S, Eisenberg T, Herker E, Carmona-Gutierrez D, Kroemer G, Madeo F (2006) Why yeast cells can undergo apoptosis: death in times of peace, love, and war. J Cell Biol 175:521–525

    PubMed  Google Scholar 

  38. 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

    PubMed  Google Scholar 

  39. Liang Q, Zhou B (2007) Copper and manganese induce yeast apoptosis via different pathways. Mol Biol Cell 18:4741–4749

    PubMed  Google Scholar 

  40. Phillips AJ, Sudbery I, Ramsdale M (2003) Apoptosis induced by environmental stresses and amphotericin B in Candida albicans. Proc Natl Acad Sci USA 100:14327–14332

    PubMed  Google Scholar 

  41. 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

    PubMed  Google Scholar 

  42. Lieberthal W, Levine JS (1996) Mechanisms of apoptosis and its potential role in renal tubular epithelial cell injury. Am J Physiol 271:F477–F488

    PubMed  Google Scholar 

  43. Hauptmann P, Riel C, Kunz-Schughart LA, Frohlich KU, Madeo F, Lehle L (2006) Defects in N-glycosylation induce apoptosis in yeast. Mol Microbiol 59:765–778

    PubMed  Google Scholar 

  44. Dudgeon DD, Zhang N, Ositelu OO, Kim H, Cunningham KW (2008) Nonapoptotic death of Saccharomyces cerevisiae cells that is stimulated by Hsp90 and inhibited by calcineurin and Cmk2 in response to endoplasmic reticulum stresses. Eukaryot Cell 7:2037–2051

    PubMed  Google Scholar 

  45. Lewis J, Devin A, Miller A et al (2000) Disruption of hsp90 function results in degradation of the death domain kinase, receptor-interacting protein (RIP), and blockage of tumor necrosis factor-induced nuclear factor-kappaB activation. J Biol Chem 275:10519–10526

    PubMed  Google Scholar 

  46. Vanden Berghe T, Kalai M, van Loo G, Declercq W, Vandenabeele P (2003) Disruption of HSP90 function reverts tumor necrosis factor-induced necrosis to apoptosis. J Biol Chem 278:5622–5629

    Google Scholar 

  47. Truman AW, Millson SH, Nuttall JM, Mollapour M, Prodromou C, Piper PW (2007) In the yeast heat shock response, Hsf1-directed induction of Hsp90 facilitates the activation of the Slt2 (Mpk1) mitogen-activated protein kinase required for cell integrity. Eukaryot Cell 6:744–752

    PubMed  Google Scholar 

  48. Zhao R, Houry WA (2007) Molecular interaction network of the Hsp90 chaperone system. Adv Exp Med Biol 594:27–36

    PubMed  Google Scholar 

  49. Blanco R, Carrasco L, Ventoso I (2003) Cell killing by HIV-1 protease. J Biol Chem 278:1086–1093

    PubMed  Google Scholar 

  50. Lenardo MJ, Angleman SB, Bounkeua V et al (2002) Cytopathic killing of peripheral blood CD4(+) T lymphocytes by human immunodeficiency virus type 1 appears necrotic rather than apoptotic and does not require env. J Virol 76:5082–5093

    PubMed  Google Scholar 

  51. Plymale DR, Tang DS, Comardelle AM, Fermin CD, Lewis DE, Garry RF (1999) Both necrosis and apoptosis contribute to HIV-1-induced killing of CD4 cells. Aids 13:1827–1839

    PubMed  Google Scholar 

  52. Badley AD, Roumier T, Lum JJ, Kroemer G (2003) Mitochondrion-mediated apoptosis in HIV-1 infection. Trends Pharmacol Sci 24:298–305

    PubMed  Google Scholar 

  53. Galluzzi L, Blomgren K, Kroemer G (2009) Mitochondrial membrane permeabilization in neuronal injury. Nat Rev Neurosci 10:481–494

    PubMed  Google Scholar 

  54. Kroemer G, Galluzzi L, Brenner C (2007) Mitochondrial membrane permeabilization in cell death. Physiol Rev 87:99–163

    PubMed  Google Scholar 

  55. Skulachev VP (2006) Bioenergetic aspects of apoptosis, necrosis and mitoptosis. Apoptosis 11:473–485

    PubMed  Google Scholar 

  56. Galluzzi L, Kroemer G (2009) Shigella targets the mitochondrial checkpoint of programmed necrosis. Cell Host Microbe 5:107–109

    PubMed  Google Scholar 

  57. Carneiro LA, Travassos LH, Soares F et al (2009) Shigella induces mitochondrial dysfunction and cell death in nonmyleoid cells. Cell Host Microbe 5:123–136

    PubMed  Google Scholar 

  58. Keyhani E, Khavari-Nejad S, Keyhani J, Attar F (2009) Acriflavine-mediated apoptosis and necrosis in yeast Candida utilis. Ann N Y Acad Sci 1171:284–291

    PubMed  Google Scholar 

  59. Sripriya P, Vedantam LV, Podile AR (2009) Involvement of mitochondria and metacaspase elevation in harpin Pss-induced cell death of Saccharomyces cerevisiae. J Cell Biochem 107:1150–1159

    PubMed  Google Scholar 

  60. Buttner S, Bitto A, Ring J et al (2008) Functional mitochondria are required for alpha-synuclein toxicity in aging yeast. J Biol Chem 283:7554–7560

    PubMed  Google Scholar 

  61. Balzan R, Sapienza K, Galea DR, Vassallo N, Frey H, Bannister WH (2004) Aspirin commits yeast cells to apoptosis depending on carbon source. Microbiology 150:109–115

    PubMed  Google Scholar 

  62. Sapienza K, Balzan R (2005) Metabolic aspects of aspirin-induced apoptosis in yeast. FEMS Yeast Res 5:1207–1213

    PubMed  Google Scholar 

  63. Braun RJ, Zischka H, Madeo F et al (2006) Crucial mitochondrial impairment upon CDC48 mutation in apoptotic yeast. J Biol Chem 281:25757–25767

    PubMed  Google Scholar 

  64. Schulze-Osthoff K, Bakker AC, Vanhaesebroeck B, Beyaert R, Jacob WA, Fiers W (1992) Cytotoxic activity of tumor necrosis factor is mediated by early damage of mitochondrial functions. Evidence for the involvement of mitochondrial radical generation. J Biol Chem 267:5317–5323

    PubMed  Google Scholar 

  65. Kalai M, Van Loo G, Vanden Berghe T et al (2002) Tipping the balance between necrosis and apoptosis in human and murine cells treated with interferon and dsRNA. Cell Death Differ 9:981–994

    PubMed  Google Scholar 

  66. Yan SF, Ramasamy R, Schmidt AM (2008) Mechanisms of disease: advanced glycation end-products and their receptor in inflammation and diabetes complications. Nat Clin Pract Endocrinol Metab 4:285–293

    PubMed  Google Scholar 

  67. Oya T, Hattori N, Mizuno Y et al (1999) Methylglyoxal modification of protein. Chemical and immunochemical characterization of methylglyoxal-arginine adducts. J Biol Chem 274:18492–18502

    PubMed  Google Scholar 

  68. Corman B, Duriez M, Poitevin P et al (1998) Aminoguanidine prevents age-related arterial stiffening and cardiac hypertrophy. Proc Natl Acad Sci USA 95:1301–1306

    PubMed  Google Scholar 

  69. Buttner S, Carmona-Gutierrez D, Vitale I et al (2007) Depletion of endonuclease G selectively kills polyploid cells. Cell Cycle 6:1072–1076

    PubMed  Google Scholar 

  70. Launay S, Hermine O, Fontenay M, Kroemer G, Solary E, Garrido C (2005) Vital functions for lethal caspases. Oncogene 24:5137–5148

    PubMed  Google Scholar 

  71. Modjtahedi N, Giordanetto F, Madeo F, Kroemer G (2006) Apoptosis-inducing factor: vital and lethal. Trends Cell Biol 16:264–272

    PubMed  Google Scholar 

  72. Syntichaki P, Samara C, Tavernarakis N (2005) The vacuolar H+ -ATPase mediates intracellular acidification required for neurodegeneration in C. elegans. Curr Biol 15:1249–1254

    PubMed  Google Scholar 

  73. Hitomi J, Christofferson DE, Ng A et al (2008) Identification of a molecular signaling network that regulates a cellular necrotic cell death pathway. Cell 135:1311–1323

    PubMed  Google Scholar 

  74. Kroemer G, Jaattela M (2005) Lysosomes and autophagy in cell death control. Nat Rev Cancer 5:886–897

    PubMed  Google Scholar 

  75. Yamashima T, Oikawa S (2009) The role of lysosomal rupture in neuronal death. Prog Neurobiol 89:343–358

    PubMed  Google Scholar 

  76. Yamashima T (2004) Ca2+ -dependent proteases in ischemic neuronal death: a conserved ‘calpain-cathepsin cascade’ from nematodes to primates. Cell Calcium 36:285–293

    PubMed  Google Scholar 

  77. Yamashima T, Tonchev AB, Tsukada T et al (2003) Sustained calpain activation associated with lysosomal rupture executes necrosis of the postischemic CA1 neurons in primates. Hippocampus 13:791–800

    PubMed  Google Scholar 

  78. Schauer A, Knauer H, Ruckenstuhl C et al (2009) Vacuolar functions determine the mode of cell death. Biochim Biophys Acta 1793:540–545

    PubMed  Google Scholar 

  79. Syntichaki P, Xu K, Driscoll M, Tavernarakis N (2002) Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans. Nature 419:939–944

    PubMed  Google Scholar 

  80. Yamashima T, Kohda Y, Tsuchiya K et al (1998) Inhibition of ischaemic hippocampal neuronal death in primates with cathepsin B inhibitor CA-074: a novel strategy for neuroprotection based on ‘calpain-cathepsin hypothesis’. Eur J Neurosci 10:1723–1733

    PubMed  Google Scholar 

  81. Nakayama M, Ishidoh K, Kayagaki N et al (2002) Multiple pathways of TWEAK-induced cell death. J Immunol 168:734–743

    PubMed  Google Scholar 

  82. Zeh HJ III, Lotze MT (2005) Addicted to death: invasive cancer and the immune response to unscheduled cell death. J Immunother 28:1–9

    PubMed  Google Scholar 

  83. Schrader M, Fahimi HD (2004) Mammalian peroxisomes and reactive oxygen species. Histochem Cell Biol 122:383–393

    PubMed  Google Scholar 

  84. Schrader M, Fahimi HD (2006) Peroxisomes and oxidative stress. Biochim Biophys Acta 1763:1755–1766

    PubMed  Google Scholar 

  85. Baumgart E, Vanhorebeek I, Grabenbauer M et al (2001) Mitochondrial alterations caused by defective peroxisomal biogenesis in a mouse model for Zellweger syndrome (PEX5 knockout mouse). Am J Pathol 159:1477–1494

    PubMed  Google Scholar 

  86. Jungwirth H, Ring J, Mayer T et al (2008) Loss of peroxisome function triggers necrosis. FEBS Lett 582:2882–2886

    PubMed  Google Scholar 

  87. Bener Aksam E, Jungwirth H, Kohlwein SD et al (2008) Absence of the peroxiredoxin Pmp20 causes peroxisomal protein leakage and necrotic cell death. Free Radic Biol Med 45:1115–1124

    PubMed  Google Scholar 

  88. Fabrizio P, Longo VD (2007) The chronological life span of Saccharomyces cerevisiae. Methods Mol Biol 371:89–95

    PubMed  Google Scholar 

  89. Allen C, Buttner S, Aragon AD et al (2006) Isolation of quiescent and nonquiescent cells from yeast stationary-phase cultures. J Cell Biol 174:89–100

    PubMed  Google Scholar 

  90. Eisenberg T, Knauer H, Schauer A et al (2009) Induction of autophagy by spermidine promotes longevity. Nat Cell Biol 11:1305–1314

    PubMed  Google Scholar 

  91. Scaffidi P, Misteli T, Bianchi ME (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418:191–195

    PubMed  Google Scholar 

  92. Nishimura K, Shiina R, Kashiwagi K, Igarashi K (2006) Decrease in polyamines with aging and their ingestion from food and drink. J Biochem 139:81–90

    PubMed  Google Scholar 

  93. Scalabrino G, Ferioli ME (1984) Polyamines in mammalian ageing: an oncological problem, too? A review. Mech Ageing Dev 26:149–164

    PubMed  Google Scholar 

  94. Lovaas E, Carlin G (1991) Spermine: an anti-oxidant and anti-inflammatory agent. Free Radic Biol Med 11:455–461

    PubMed  Google Scholar 

  95. Zhang M, Wang H, Tracey KJ (2000) Regulation of macrophage activation and inflammation by spermine: a new chapter in an old story. Crit Care Med 28:N60–N66

    PubMed  Google Scholar 

  96. Galluzzi L, Aaronson SA, Abrams J et al (2009) Guidelines for the use and interpretation of assays for monitoring cell death in higher eukaryotes. Cell Death Differ 16:1093–1107

    PubMed  Google Scholar 

  97. Ludovico P, Madeo F, Silva M (2005) Yeast programmed cell death: an intricate puzzle. IUBMB Life 57:129–135

    PubMed  Google Scholar 

  98. Phillips AJ, Crowe JD, Ramsdale M (2006) Ras pathway signaling accelerates programmed cell death in the pathogenic fungus Candida albicans. Proc Natl Acad Sci USA 103:726–731

    PubMed  Google Scholar 

  99. Chautan M, Chazal G, Cecconi F, Gruss P, Golstein P (1999) Interdigital cell death can occur through a necrotic and caspase-independent pathway. Curr Biol 9:967–970

    PubMed  Google Scholar 

  100. Smith KG, Strasser A, Vaux DL (1996) CrmA expression in T lymphocytes of transgenic mice inhibits CD95 (Fas/APO-1)-transduced apoptosis, but does not cause lymphadenopathy or autoimmune disease. EMBO J 15:5167–5176

    PubMed  Google Scholar 

  101. Shirogane T, Fukada T, Muller JM, Shima DT, Hibi M, Hirano T (1999) Synergistic roles for Pim-1 and c-Myc in STAT3-mediated cell cycle progression and antiapoptosis. Immunity 11:709–719

    PubMed  Google Scholar 

  102. Longo VD (2004) Ras: the other pro-aging pathway. Sci Aging Knowl Environ 2004:pe36

    Google Scholar 

  103. Longo VD (1999) Mutations in signal transduction proteins increase stress resistance and longevity in yeast, nematodes, fruit flies, and mammalian neuronal cells. Neurobiol Aging 20:479–486

    PubMed  Google Scholar 

  104. Fabrizio P, Liou LL, Moy VN et al (2003) SOD2 functions downstream of Sch9 to extend longevity in yeast. Genetics 163:35–46

    PubMed  Google Scholar 

  105. Baines CP, Kaiser RA, Purcell NH et al (2005) Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434:658–662

    PubMed  Google Scholar 

  106. Nakagawa T, Shimizu S, Watanabe T et al (2005) Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 434:652–658

    PubMed  Google Scholar 

  107. Matouschek A, Rospert S, Schmid K, Glick BS, Schatz G (1995) Cyclophilin catalyzes protein folding in yeast mitochondria. Proc Natl Acad Sci USA 92:6319–6323

    PubMed  Google Scholar 

  108. 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

    PubMed  Google Scholar 

  109. Wang KK (2000) Calpain and caspase: can you tell the difference? Trends Neurosci 23:20–26

    PubMed  Google Scholar 

  110. Liu X, Van Vleet T, Schnellmann RG (2004) The role of calpain in oncotic cell death. Annu Rev Pharmacol Toxicol 44:349–370

    PubMed  Google Scholar 

  111. Futai E, Maeda T, Sorimachi H, Kitamoto K, Ishiura S, Suzuki K (1999) The protease activity of a calpain-like cysteine protease in Saccharomyces cerevisiae is required for alkaline adaptation and sporulation. Mol Gen Genet 260:559–568

    PubMed  Google Scholar 

  112. Mason DA, Shulga N, Undavai S, Ferrando-May E, Rexach MF, Goldfarb DS (2005) Increased nuclear envelope permeability and Pep4p-dependent degradation of nucleoporins during hydrogen peroxide-induced cell death. FEMS Yeast Res 5:1237–1251

    PubMed  Google Scholar 

  113. Picard D (2002) Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci 59:1640–1648

    PubMed  Google Scholar 

  114. Zong WX, Ditsworth D, Bauer DE, Wang ZQ, Thompson CB (2004) Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev 18:1272–1282

    PubMed  Google Scholar 

  115. Faraone-Mennella MR, De Maio A, Petrella A et al (2005) Yeast (ADPribosyl)ation: revisiting a controversial question. J Cell Biochem 94:1258–1266

    PubMed  Google Scholar 

  116. Van Herreweghe F, Mao J, Chaplen FW et al (2002) Tumor necrosis factor-induced modulation of glyoxalase I activities through phosphorylation by PKA results in cell death and is accompanied by the formation of a specific methylglyoxal-derived AGE. Proc Natl Acad Sci USA 99:949–954

    PubMed  Google Scholar 

  117. Longo VD (2003) The Ras and Sch9 pathways regulate stress resistance and longevity. Exp Gerontol 38:807–811

    PubMed  Google Scholar 

  118. Inoue Y, Kimura A (1996) Identification of the structural gene for glyoxalase I from Saccharomyces cerevisiae. J Biol Chem 271:25958–25965

    PubMed  Google Scholar 

  119. Benli M, Doring F, Robinson DG, Yang X, Gallwitz D (1996) Two GTPase isoforms, Ypt31p and Ypt32p, are essential for Golgi function in yeast. EMBO J 15:6460–6475

    PubMed  Google Scholar 

  120. Carlsson P, Mahlapuu M (2002) Forkhead transcription factors: key players in development and metabolism. Dev Biol 250:1–23

    PubMed  Google Scholar 

  121. Supekova L, Supek F, Nelson N (1995) The Saccharomyces cerevisiae VMA10 is an intron-containing gene encoding a novel 13-kDa subunit of vacuolar H(+)-ATPase. J Biol Chem 270:13726–13732

    PubMed  Google Scholar 

  122. Teng X, Hardwick JM (2009) Reliable method for detection of programmed cell death in yeast. Methods Mol Biol 559:335–342

    PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to the European Union for grant Apo-Sys (FP7) to F. M. and T. E. and to the Austrian Science Fund (FWF) for grant S-9304-B05 and “Lipotox” to F. M. and D. C.-G. and for grant T-414-B09 to S. B. (Hertha-Firnberg fellowship). N. T. acknowledges funding support by grants from EMBO, the European Research Council (ERC), and the European Commission Framework Programmes 6 and 7.

Author information

Authors and Affiliations

  1. Institute of Molecular Biosciences, University of Graz, 8010, Graz, Austria

    Tobias Eisenberg, Didac Carmona-Gutierrez, Sabrina Büttner & Frank Madeo

  2. Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, 70013, Heraklion, Crete, Greece

    Nektarios Tavernarakis

Authors
  1. Tobias Eisenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Didac Carmona-Gutierrez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sabrina Büttner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nektarios Tavernarakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Frank Madeo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frank Madeo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Eisenberg, T., Carmona-Gutierrez, D., Büttner, S. et al. Necrosis in yeast. Apoptosis 15, 257–268 (2010). https://doi.org/10.1007/s10495-009-0453-4

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10495-009-0453-4

Keywords

Search

Navigation