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Alterations in mitochondrial morphology ofSchizosaccharomyces pombe induced by cell-death promoting agents

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Abstract

The effect of the yeast cell-death inducing agents, Bax and acetic acid, on mitochondrial structure ofSchizosaccharomyces pombe was studied. Comparison of mitochondrial structures in cells grown on different substrates and visualized with different probes revealed variations in their morphology. Cells grown on respiratory C sources as well as in the presence of antimycin A exhibited punctuated mitochondria when visualized with mitochondrially targeted green fluorescent protein, while they still appeared as tubular structures when stained with DiOC6(3). Both expression of Bax and acetic acid treatment induced fragmentation and aggregation of mitochondrial network, which could be prevented by coexpression of Bcl-XL. Aberrant mitochondrial morphology generated by either Bax or acetic acid was not accompanied with the loss of mitochondrial genome (mtDNA), indicating that alterations of mitochondrial morphology following death stimuli follow different mechanisms than those involved in mitochondrial inheritance mutants.

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Abbreviations

DAPI:

4′,6-diamidino-2-phenylindole

DiOC6(3):

3-hexyl-2-[3″-(3′-hexyl-2′(3′H)benzoxazolylidene)-l″-propenyl]benzoxazolium iodide (see formula)

FCS:

fermentable carbon source(s)

MT:

mitochondrial(ly)

mtGFP:

MT-targeted green fluorescent protein

NCS:

nonfermentable carbon source(s)

References

  • Bleazard W., McCaffery J.M., King E.J., Bale S., Mozdy A., Tieu Q., Nunnari J., Shaw J.M.: The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast.Nature Cell Biol. 1, 298–304 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Boldogh I.R., Pon L.A.: Assaying actin-binding activity of mitochondria in yeast.Meth.Cell Biol. 65, 159–173 (2001).

    Article  CAS  Google Scholar 

  • Boldogh I.R., Ramcharan S.L., Yang H.C., Pon L.A.: A type V myosin (Myo2p) and a Rab-like G-protein (Ypt11p) are required for retention of newly inherited mitochondria in yeast cells during cell division.Mol.Biol.Cell 15, 3994–4002 (2004).

    Article  PubMed  CAS  Google Scholar 

  • 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).

    Article  PubMed  CAS  Google Scholar 

  • Forsburg S.L.: Comparison ofSchizosaccharomyces pombe expression systems.Nucl.Acids Res. 21, 2955–2956 (1993).

    Article  PubMed  CAS  Google Scholar 

  • 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).

    Article  PubMed  CAS  Google Scholar 

  • Guan K., Farh L., Marshall T.K., Deschenes R.J.: Normal mitochondrial structure and genome maintenance in yeast requires the dynamin-like product of theMGM1 gene.Curr.Genet. 24, 141–148 (1993).

    Article  PubMed  CAS  Google Scholar 

  • Jensen R.E.: Control of mitochondrial shape.Curr.Opin.Cell Biol. 17, 384–388 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Jones B.A., Fangman W.L.: Mitochondrial DNA maintenance in yeast requires a protein containing a region related to the GTP-binding domain of dynamin.Genes Dev. 6, 380–389 (1992).

    Article  PubMed  CAS  Google Scholar 

  • Jurgensmeier J.M., Krajewski S., Armstrong R.C., Wilson G.M., Oltersdorf T., Fritz L.C., Reed J.C., Ottilie S.: Bax-and Bak-induced cell death in the fission yeastSchizosaccharomyces pombe.Mol.Biol.Cell 8, 325–339 (1997).

    PubMed  CAS  Google Scholar 

  • 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).

    Article  PubMed  CAS  Google Scholar 

  • Lang B., Burger G., Doxiadis I., Thomas D.Y., Bandlow W., Kaudewitz F.: A simple method for the large-scale preparation of mitochondria from microorganisms.Analyst.Biochem. 77, 110–121 (1977).

    Article  CAS  Google Scholar 

  • Ludovico P., Sousa M.J., Silva M.T., Leao C., Corte-Real M.:Saccharomyces cerevisiae commits to a programmed cell death process in response to acetic acid.Microbiology 147, 2409–2415 (2001).

    PubMed  CAS  Google Scholar 

  • Madeo F., Herker E., Wissing S., Jungwirth H., Eisenberg T., Frohlich K.U.: Apoptosis in yeast.Curr.Opin.Microbiol. 7, 655–660 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Maundrell K.:nmt1 of fission yeast. A highly transcribed gene completely repressed by thiamine.J.Biol.Chem. 265, 10857–10864 (1990).

    PubMed  CAS  Google Scholar 

  • Moore A.L., Walters A.J., Thorpe J., Fricaud A.C., Watts F.Z.:Schizosaccharomyces pombe mitochondria: morphological, respiratory and protein import characteristics.Yeast 8, 923–933 (1992).

    Article  PubMed  CAS  Google Scholar 

  • Moreno S., Klar A., Nurse P.: Molecular genetic analysis of fission yeastSchizosaccharomyces pombe.Meth.Enzymol. 194, 795–823 (1991).

    Article  PubMed  CAS  Google Scholar 

  • Nunnari J., Marshall W.F., Straight A., Murray A., Sedat J.W., Walter P.: Mitochondrial transmission during mating inSaccharomyces cerevisiae is determined by mitochondrial fusion and fission and the intramitochondrial segregation of mitochondrial DNA.Mol.Biol.Cell 8, 1233–1242 (1997).

    PubMed  CAS  Google Scholar 

  • Okamoto K., Shaw J.M.: Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes.Ann.Rev.Genet. 39, 503–536 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Ono T., Isobe K., Nakada K., Hayashi J.I.: Human cells are protected from mitochondrial dysfunction by complementation of DNA products in fused mitochondria.Nat.Genet. 28, 272–275 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Pelloquin L., Belenguer P., Menon Y., Ducommun B.: Identification of a fission yeast dynamin-related protein involved in mitochondrial DNA maintenance.Biochem.Biophys.Res.Commun. 251, 720–726 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Pelloquin L., Belenguer P., Menon Y., Gas N., Ducommun B.: Fission yeast Msp1 is a mitochondrial dynamin-related protein.J.Cell Sci. 112 (Pt 22), 4151–4161 (1999).

    PubMed  CAS  Google Scholar 

  • Perfettini J.L., Roumier T., Kroemer G.: Mitochondrial fusion and fission in the control of apoptosis.Trends Cell Biol. 15, 179–183 (2005).

    Article  PubMed  CAS  Google Scholar 

  • Rapaport D., Brunner M., Neupert W., Westermann B.: Fzolp is a mitochondrial outer membrane protein essential for the biogenesis of functional mitochondria inSaccharomyces cerevisiae.J.Biol.Chem. 273, 20150–20155 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J., Fritsch E.F., Maniatis T.:Molecular Cloning: a Laboratory Manual. Cold Spring Harbor Laboratory Press, New York 1989.

    Google Scholar 

  • Sato T., Hanada M., Bodrug S., Irie S., Iwama N., Boise L.H., Thompson C.B., Golemis E., Fong L., Wang H.G., Reed J.C.: Interactions among members of the Bcl-2 protein family analyzed with a yeast two-hybrid system.Proc.Nat.Acad.Sci.USA 91, 9238–9242 (1994).

    Article  PubMed  CAS  Google Scholar 

  • Scott S.V., Cassidy-Stone A., Meeusen S.L., Nunnari J.: Staying in aerobic shape: how the structural integrity of mitochondria and mitochondrial DNA is maintained.Curr.Opin.Cell Biol. 15, 482–488 (2003).

    Article  PubMed  CAS  Google Scholar 

  • Skulachev V.P.: Mitochondrial filaments and clusters as intracellular power-transmitting cables.Trends Biochem.Sci. 26, 23–29 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Trancikova A., Weisova P., Kissova I. Zeman I., Kolarov J.: Production of reactive oxygen species and loss of viability in yeast mitochondrial mutants: protective effect of Bcl-XL.FEMS Yeast Res. 5, 149–156 (2004).

    Article  PubMed  CAS  Google Scholar 

  • Trezeguet V., Zeman I., David C., Lauquin G.J., Kolarov J.: Expression of the ADP/ATP carrier encoding genes in aerobic yeasts; phenotype of an ADP/ATP carrier deletion mutant ofSchizosaccharomyces pombe.Biochim.Biophys.Acta 1410, 229–236 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Uchida N., Suzuki K., Saiki R., Kainou T., Tanaka K., Matsuda H., Kawamukai M.: Phenotypes of fission yeast defective in ubiquinone production due to disruption of the gene forp-hydroxybenzoate polyprenyl diphosphate transferase.J.Bacteriol. 182, 6933–6939 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Yaffe M.P.: Dynamic mitochondria.Nature Cell Biol. 1, E149-E150 (1999).

    Article  PubMed  CAS  Google Scholar 

  • Yaffe M.P., Harata D., Verde F., Eddison M., Toda T., Nurse P.: Microtubules mediate mitochondrial distribution in fission yeast.Proc.Nat.Acad.Sci.USA 93, 11664–11668 (1996).

    Article  PubMed  CAS  Google Scholar 

  • Zha H., Fisk H.A., Yaffe M.P., Mahajan N., Herman B., Reed J.C.: Structure-function comparisons of the pro-apoptotic protein Bax in yeast and mammalian cells.Mol.Cell Biol. 16, 6494–6508 (1996).

    PubMed  CAS  Google Scholar 

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Correspondence to P. Polčic.

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This work was supported by grants from theAgency for Support of Research and Development no. APVT-20-012404 and no. APVT-20-017202 and fromNATO no. RIG 981468.

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Pevala, V., Kolarov, J. & Polčic, P. Alterations in mitochondrial morphology ofSchizosaccharomyces pombe induced by cell-death promoting agents. Folia Microbiol 52, 381–390 (2007). https://doi.org/10.1007/BF02932093

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