Folia Microbiologica

, 52:479 | Cite as

Apoptosis and aging in mitochondrial morphology mutants ofS. cerevisiae

Article

Abstract

Cell viability during chronological aging and after apoptotic stimuli in some yeast mutants with altered mitochondrial morphology was followed; a function for the corresponding genes in the apoptotic process was assessed.MDM30 andDNM1, the genes encoding an F-box protein and the dynamin-related GTPase, respectively, are involved in triggering aging and apoptosis. In contrast,YME1, encoding a subunit of the mitochondrial inner membrane i-AAA proteinase complex, has a protective role in these processes.FIS1, the mitochondrial fission gene, might play a protective role after an apoptotic insult while it seems to promote cell death in aging cells.

Abbreviations

GFP

green fluorescent protein(s)

PNPase

polyribonucleotide nucleotidyltransferase (EC 2.7.7.8)

MT

mitochondrial

References

  1. Arnold I., Wagner-Ecker M., Ansorge W., Langer T.: Evidence for a novel mitochondria-to-nucleus signaling pathway in respiring cells lacking i-AAA protease and the ABC-transporter Md11.Gene 367, 74–88 (2006).PubMedCrossRefGoogle Scholar
  2. Breckenridge D.G., Stojanovic M., Marcellus R.C., Shore G.C.: Caspase cleavage product of BAP31 induces mitochondrial fission through endoplasmic reticulum calcium signals, enhancing cytochromec release to the cytosol.J.Cell Biol. 160, 1115–1127 (2003).PubMedCrossRefGoogle Scholar
  3. Chan D.C.: Mitochondria: dynamic organelles in disease, aging, and development.Cell 125, 1241–1252 (2006).PubMedCrossRefGoogle Scholar
  4. Chen H.W., Rainey R.N., Balatoni C.E., Dawson D.W., Troke J.J., Wasiak S., Hong J.S., Mcbride H.M., Koehler C.M., Teitell M.A., French S.W.: Mammalian polynucleotide phosphorylase is an intermembrane space RNase that maintains mitochondrial homeostasis.Mol.Cell.Biol. 26, 8475–8487 (2006).PubMedCrossRefGoogle Scholar
  5. Durr M., Escobar-Henriques M., Merz S., Geimer S., Langer T., Westermann B.: Nonredundant roles of mitochondria-associated F-box proteins Mfb1 and Mdm30 in maintenance of mitochondrial morphology in yeast.Mol.Biol.Cell 17, 3745–3755 (2006).PubMedCrossRefGoogle Scholar
  6. Escobar-Henriques M., Westermann B., Langer T.: Regulation of mitochondrial fusion by the F-box protein Mdm30 involves proteasome-independent turnover of Fzol.J.Cell Biol. 173, 645–650 (2006).PubMedCrossRefGoogle Scholar
  7. Fannjiang Y., Cheng W.C., Lee S.J., Qi B., Pevsner J., Mccaffery J.M., Hill R.B., Basanez G., Hardwick J.M.: Mitochondrial fission proteins regulate programmed cell death in yeast.Genes Dev. 18, 2785–2797 (2004).PubMedCrossRefGoogle Scholar
  8. Frank S., Gaume B., Bergmann-Leitner E.S., Leitner W.W., Robert E.G., Catez F., Smith C.L., Youle R.J.: The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis.Dev.Cell 1, 515–525 (2001).PubMedCrossRefGoogle Scholar
  9. Fritz S., Weinbach N., Westermann B.: Mdm30 is an F-box protein required for maintenance of fusion-competent mitochondria in yeast.Mol.Biol.Cell 14, 2303–2313 (2003).PubMedCrossRefGoogle Scholar
  10. Hales K.G., Fuller M.T.: Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase.Cell 90, 121–129 (1997).PubMedCrossRefGoogle Scholar
  11. Heath-Engel H.M., Shore G.C.: Mitochondrial membrane dynamics, cristae remodeling and apoptosis.Biochim.Biophys.Acta 1763, 549–560 (2006).PubMedCrossRefGoogle Scholar
  12. Jagasia R., Grote P., Westermann B., Conradt B.: DRP-1-mediated mitochondrial fragmentation during EGL-1-induced cell death inC. elegans.Nature 433, 754–760 (2005).PubMedCrossRefGoogle Scholar
  13. James D.I., Parone P.A., Mattenberger Y., Martinou J.C.: hFis1, a novel component of the mammalian mitochondrial fission machinery.J.Biol.Chem. 278, 36373–36379 (2003).PubMedCrossRefGoogle Scholar
  14. Juhola M.K., Shah Z.H., Grivell L.A., Jacobs H.T.: The mitochondrial inner membrane AAA metalloprotease family in metazoans.FEBS Lett. 481, 91–95 (2000).PubMedCrossRefGoogle Scholar
  15. Karbowski M., Lee Y.J., Gaume B., Jeong S.Y., Frank S., Nechushtan A., Santel A., Fuller M., Smith C.L., Youle R.J.: Spatial and temporal association of Bax with mitochondrial fission sites, Drp1, and Mfn2 during apoptosis.J.Cell Biol. 159, 931–938 (2002).PubMedCrossRefGoogle Scholar
  16. Labrousse A.M., Shurland D.L., Van Der Bliek A.M.: Contribution of the GTPase domain to the subcellular localization of dynamin in the nematodeCaenorhabditis elegans.Mol.Biol.Cell 9, 3227–3239 (1998).PubMedGoogle Scholar
  17. Lee Y.J., Jeong S.Y., Karbowski M., Smith C.L., Youle R.J.: Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis.Mol.Biol.Cell 15, 5001–5011 (2004).PubMedCrossRefGoogle Scholar
  18. Leonhard K., Herrmann J.M., Stuart R.A., Mannhaupt G., Neupert W., Langer T.: AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria.EMBO J. 15, 4218–4229 (1996).PubMedGoogle Scholar
  19. Leonhard K., Stiegler A., Neupert W., Langer T.: Chaperone-like activity of the AAA domain of the yeast Ymel AAA protease.Nature 398, 348–351 (1999).PubMedCrossRefGoogle Scholar
  20. Leszczyniecka M., Desalle R., Kang D.C., Fisher P.B.: The origin of polynucleotide phosphorylase domains.Mol.Phylogenet.Evol. 31, 123–130 (2004).PubMedCrossRefGoogle Scholar
  21. Longo V.D., Mitteldorf J., Skulachev V.P.: Programmed and altruistic ageing.Nature Rev.Genet. 6, 866–872 (2005).CrossRefPubMedGoogle Scholar
  22. Ludovico P., Madeo F., Silva M.: Yeast programmed cell death: an intricate puzzle.IUBMB Life 57, 129–135 (2005).PubMedCrossRefGoogle Scholar
  23. Manon S., Priault M., Camougrand N.: Mitochondrial AAA-type protease Yme1p is involved in Bax effects on cytochrome-c oxidase.Biochem.Biophys.Res.Commun. 289, 1314–1319 (2001).PubMedCrossRefGoogle Scholar
  24. Mazzoni C., Herker E., Palermo V., Jungwirth H., Eisenberg T., Madeo F., Falcone C.: Yeast caspase 1 links messenger RNA stability to apoptosis in yeast.EMBO Rep. 6, 1076–1081 (2005).PubMedCrossRefGoogle Scholar
  25. Mozdy A.D., Mccaffery J.M., Shaw J.M.: Dnm1p GTPase-mediated mitochondrial fission is a multi-step process requiring the novel integral membrane component Fis1p.J.Cell Biol. 151, 367–380 (2000).PubMedCrossRefGoogle Scholar
  26. Muratani M., Kung C., Shokat K.M., Tansey W.P.: The F box protein Dsg1/Mdm30 is a transcriptional coactivator that stimulates Gal4 turnover and cotranscriptional mRNA processing.Cell 120, 887–899 (2005).PubMedCrossRefGoogle Scholar
  27. Rainey R.N., Glavin J.D., Chen H.W., French S.W., Teitell M.A., Koehler C.M.: A new function in translocation for the mitochondrial i-AAA protease Yme1: import of polynucleotide phosphorylase into the intermembrane space.Mol.Cell Biol. 26, 8488–8497 (2006).PubMedCrossRefGoogle Scholar
  28. Shaw J.M., Nunnari J.: Mitochondrial dynamics and division in budding yeast.Trends Cell Biol. 12, 178–184 (2002).PubMedCrossRefGoogle Scholar
  29. Sugioka R., Shimizu S., Tsujimoto Y.: Fzo1, a protein involved in mitochondrial fusion, inhibits apoptosis.J.Biol.Chem. 279, 52726–52734 (2004).PubMedCrossRefGoogle Scholar
  30. Weber E.R., Hanekamp T., Thorsness P.E.: Biochemical and functional analysis of theYME1 gene product, an ATP and zinc-dependent mitochondrial protease fromS. cerevisiae.Mol.Biol.Cell 7, 307–317 (1996).PubMedGoogle Scholar
  31. Westermann B., Neupert W.: Mitochondria-targeted green fluorescent proteins: convenient tools for the study of organelle biogenesis inSaccharomyces cerevisiae.Yeast 16, 1421–1427 (2000).PubMedCrossRefGoogle Scholar
  32. Yaffe M.P.: The cutting edge of mitochondrial fusion.Nature Cell Biol. 5, 497–499 (2003).PubMedCrossRefGoogle Scholar

Copyright information

© Institute of Microbiology, Academy of Sciences of the Czech Republic 2007

Authors and Affiliations

  1. 1.Department of Cell and Developmental Biology, Pasteur Institute-Cenci Bolognetti FoundationUniversity of Rome “La Sapienza”RomeItaly

Personalised recommendations