Skip to content
1887

Microbiology Society logo Microbiology

Volume 154, Issue 9

Mitochondrial involvement in aspirin-induced apoptosis in yeast Free

Abstract

We have previously reported that aspirin induces apoptosis in manganese superoxide dismutase (MnSOD)-deficient cells when cultivated on the non-fermentable carbon source ethanol. Here, we investigated the role of mitochondria in aspirin-induced apoptosis. We report that aspirin had an inhibitory effect on cellular respiration, and caused the release of most of the mitochondrial cytochrome and a dramatic drop in the mitochondrial membrane potential (ΔΨ). Also, aspirin reduced the intracellular cytosolic pH in the MnSOD-deficient cells growing in ethanol medium, but this did not seem to be the initial trigger that committed these cells to aspirin-induced apoptosis. Furthermore, loss of ΔΨ was not required for aspirin-induced release of cytochrome , since the initial release of cytochrome occurred prior to the disruption of the ΔΨ. It is thus possible that cytochrome release does not involve the early onset of the mitochondrial permeability transition, but only an alteration of the permeability of the outer mitochondrial membrane.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): C-SNARF-1-AM, 5-(and-6-)-carboxy-seminaphthorhodafluor-1-acetoxymethyl ester , CuZnSOD, copper/zinc superoxide dismutase , FCCP, carbonylcyanide-p-trifluoromethoxyphenylhydrazone , MnSOD, manganese superoxide dismutase , NAO, 10-N-nonyl acridine orange , pHi, intracellular pH , Rh123, rhodamine 123 , ROS, reactive oxygen species and ΔΨm, mitochondrial membrane potential
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2008/017228-0
2008-09-01
2025-03-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/9/2740.html?itemId=/content/journal/micro/10.1099/mic.0.2008/017228-0&mimeType=html&fmt=ahah

References

  1. Adams S. S., Cobb R. 1958; A possible basis for the anti-inflammatory activity of salicylates and other non-hormonal anti-rheumatic drugs. Nature 181:773–774
     [Google Scholar]
  2. Ahn S. H., Cheung W. L., Hsu J. Y., Diaz R. L., Smith M. M., Allis C. D. 2005; Sterile 20 kinase phosphorylates histone H2B at serine 10 during hydrogen peroxide-induced apoptosis in S. cerevisiae . Cell 120:25–36
     [Google Scholar]
  3. Balzan R., Sapienza K., Galea D. R., Vassallo N., Frey H., Bannister W. H. 2004; Aspirin commits yeast cells to apoptosis depending on carbon source. Microbiology 150:109–115
     [Google Scholar]
  4. Büttner S., Eisenberg T., Carmona-Gutierrez D., Ruli D., Knauer H., Ruckenstuhl C., Sigrist C., Wissing S., Kollroser M. other authors 2007; Endonuclease G regulates budding yeast life and death. Mol Cell 25:233–246
     [Google Scholar]
  5. Castano E., Dalmau M., Barragan M., Pueyo G., Bartrons R., Gil J. 1999; Aspirin induces cell death and caspase-dependent phosphatidylserine externalization in HT-29 human colon adenocarcinoma cells. Br J Cancer 81:294–299
     [Google Scholar]
  6. Chan A. T., Giovannucci E. L., Schernhammer E. S., Colditz G. A., Hunter D. J., Willett W. C., Fuch C. S. 2004; A prospective study of aspirin use and the risk for colorectal adenoma. Ann Intern Med 140:157–166
     [Google Scholar]
  7. 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
     [Google Scholar]
  8. Fannjiang Y., Cheng W. C., Lee S. J., Qi B., Pevsner J., McCaffery J. M., Hill R. B., Basanez G., Hardwick J. M. 2004; Mitochondrial fission proteins regulate programmed cell death in yeast. Genes Dev 18:2785–2797
     [Google Scholar]
  9. Gao J., Niwa K., Sun W., Takemura M., Lian Z., Onogi K., Seishima M., Mori H., Tamaya T. 2004; Non-steroidal anti-inflammatory drugs inhibit cellular proliferation and up-regulate cyclooxygenase-2 protein expression in endometrial cancer cells. Cancer Sci 95:901–907
     [Google Scholar]
  10. Glick B. S., Pon L. A. 1995; Isolation of highly purified mitochondria from Saccharomyces cerevisiae . Methods Enzymol 260:213–223
     [Google Scholar]
  11. Haworth R. S., Fliegel L. 1993; Intracellular pH in Schizosaccharomyces pombe – comparison with Saccharomyces cerevisiae . Mol Cell Biochem 124:131–140
     [Google Scholar]
  12. Haworth R. S., Lemire B. D., Crandall D., Cragoe E. J. Jr, Fliegel L. 1991; Characterisation of proton fluxes across the cytoplasmic membrane of the yeast Saccharomyces cerevisiae . Biochim Biophys Acta 1098:79–89
     [Google Scholar]
  13. He H., Xia H. H., Wang J. D., Gu Q., Lin M. C., Zou B., Lam S. K., Chan A. O., Yuen M. F. other authors 2006; Inhibition of human telomerase reverse transcriptase by nonsteroidal antiinflammatory drugs in colon carcinoma. Cancer 106:1243–1249
     [Google Scholar]
  14. Karagiannis J., Young P. G. 2001; Intracellular pH homeostasis during cell-cycle progression and growth state transition in Schizosaccharomyces pombe . J Cell Sci 114:2929–2941
     [Google Scholar]
  15. Kune G. A., Kune S., Watson L. F. 1988; Colorectal cancer risk, chronic illnesses, operations, and medications: case control results from the Melbourne Colorectal Cancer Study. Cancer Res 48:4399–4404
     [Google Scholar]
  16. Li P., Nijhawan D., Budihardjo I., Srinivasula S. M., Ahmad M., Alnemri E. S., Wang X. 1997; Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479–489
     [Google Scholar]
  17. Longo V. D., Liou L. L., Valentine J. S., Gralla E. B. 1999; Mitochondrial superoxide decreases yeast survival in stationary phase. Arch Biochem Biophys 365:131–142
     [Google Scholar]
  18. Ludovico P., Sansonetty F., Côrte-Real M. 2001; Assessment of mitochondrial membrane potential in yeast cell populations by flow cytometry. Microbiology 147:3335–3343
     [Google Scholar]
  19. Ludovico P., Rodrigues F., Almeida A., Silva M. T., Barrientos A., Côrte-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
     [Google Scholar]
  20. Madeo F., Frohlich E., Frohlich K.-U. 1997; A yeast mutant showing diagnostic markers of early and late apoptosis. J Cell Biol 139:729–734
     [Google Scholar]
  21. Madeo F., Frohlich E., Ligr M., Grey M., Sigrist S. J., Wolf D. H., Frohlich K.-U. 1999; Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol 145:757–767
     [Google Scholar]
  22. Madeo F., Herker E., Maldener C., Wissing S., Lächelt S., Herlan M., Fehr M., Lauber K., Sigrist S. J. other authors 2002; A caspase-related protease regulates apoptosis in yeast. Mol Cell 9:911–917
     [Google Scholar]
  23. Madshus I. H. 1988; Regulation of intracellular pH in eukaryotic cells. Biochem J 250:1–8
     [Google Scholar]
  24. 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
     [Google Scholar]
  25. Massari P., Ho Y., Wetzler L. M. 2000; Neisseria meningitidis porin PorB interacts with mitochondria and protects cells from apoptosis. Proc Natl Acad Sci U S A 97:9070–9075
     [Google Scholar]
  26. Matsuyama S., Reed J. C. 2000; Mitochondria-dependent apoptosis and cellular pH regulation. Cell Death Differ 7:1155–1165
     [Google Scholar]
  27. Nulton-Persson A. C., Szweda L. I., Sadek H. A. 2004; Inhibition of cardiac mitochondrial respiration by salicylic acid and acetylsalicylate. J Cardiovasc Pharmacol 44:591–595
     [Google Scholar]
  28. Oh K. W., Qian T., Brenner D. A., Lemasters J. J. 2003; Salicylate enhances necrosis and apoptosis mediated by the mitochondrial permeability transition. Toxicol Sci 73:44–52
     [Google Scholar]
  29. Opitz N., Merten E., Acker H. 1994; Evidence for redistribution-associated intracellular pK′ shifts of the pH-sensitive fluoroprobe carboxy-SNARF-1. Pflugers Arch 427:332–342
     [Google Scholar]
  30. Ott M., Norberg E., Walter K. M., Schreiner P., Kemper C., Rapaport D., Zhivotovsky B., Orrenius S. 2007; The mitochondrial TOM complex is required for tBid/Bax-induced cytochrome c release. J Biol Chem 282:27633–27639
     [Google Scholar]
  31. Pampulha M. E., Loureiro-Dias M. C. 1989; Combined effect of acetic acid, pH and ethanol on intracellular pH of fermenting yeast. Appl Microbiol Biotechnol 31:547–550
     [Google Scholar]
  32. Pearce L. L., Epperly M. W., Greenberger J. S., Pitt B. R., Peterson J. 2001; Identification of respiratory complexes I and III as mitochondrial sites of damage following exposure to ionizing radiation and nitric oxide. Nitric Oxide 5:128–136
     [Google Scholar]
  33. Piper P., Calderon C. O., Hatzixanthis K., Mollapour M. 2001; Weak acid adaptation: the stress response that confers yeasts with resistance to organic acid food preservatives. Microbiology 147:2635–2642
     [Google Scholar]
  34. Pique M., Barragan M., Dalmau M., Bellosillo B., Pons G., Gil J. 2000; Aspirin induces apoptosis through mitochondrial cytochrome c release. FEBS Lett 480:193–196
     [Google Scholar]
  35. Power J. J., Dennis M. S., Redlak M. J., Miller T. A. 2004; Aspirin-induced mucosal cell death in human gastric cells: evidence supporting an apoptotic mechanism. Dig Dis Sci 49:1518–1525
     [Google Scholar]
  36. Pozniakovsky A. I., Knorre D. A., Markova O. V., Hyman A. A., Skulachev V. P., Severin F. F. 2005; Role of mitochondria in the pheromone- and amiodarone-induced programmed death of yeast. J Cell Biol 168:257–269
     [Google Scholar]
  37. Press W. H., Teukolsky S. A., Vetterling W. T., Flannery B. P. 1996 Numerical Recipes in C , 2nd edn. Cambridge: Cambridge University Press;
     [Google Scholar]
  38. Priault M., Chaudhuri B., Clow A., Camougrand N., Manon S. 1999; Investigation of bax-induced release of cytochrome c from yeast mitochondria permeability of mitochondrial membranes, role of VDAC and ATP requirement. Eur J Biochem 260:684–691
     [Google Scholar]
  39. Qiao L., Hanif R., Sphicas E., Shiff S. J., Rigas B. 1998; Effect of aspirin on induction of apoptosis in HT-29 human colon adenocarcinoma cells. Biochem Pharmacol 55:53–64
     [Google Scholar]
  40. Redlak M. J., Power J. J., Miller T. A. 2005; Role of mitochondria in aspirin-induced apoptosis in human gastric epithelial cells. Am J Physiol Gastrointest Liver Physiol 289:G731–G738
     [Google Scholar]
  41. Sapienza K., Balzan R. 2005; Metabolic aspects of aspirin-induced apoptosis in yeast. FEMS Yeast Res 5:1207–1213
     [Google Scholar]
  42. Schwenger P., Alpert D., Skolnik E. Y., Vilcek J. 1998; Activation of p38 mitogen-activated protein kinase by sodium salicylate leads to inhibition of tumor necrosis factor-induced I κ B α phosphorylation and degradation. Mol Cell Biol 18:78–84
     [Google Scholar]
  43. Severin F. F., Hyman A. A. 2002; Pheromone induces programmed cell death in S. cerevisiae . Curr Biol 12:R233–R235
     [Google Scholar]
  44. Silva R. D., Sotoca R., Johansson B., Ludovico P., Sansonetty F., Silva M. T., Peinado J. M., Côrte-Real M. 2005; Hyperosmotic stress induces metacaspase- and mitochondria-dependent apoptosis in Saccharomyces cerevisiae . Mol Microbiol 58:824–834
     [Google Scholar]
  45. Somasundaram S., Rafi S., Hayllar J., Sigthorsson G., Jacob M., Price A. B., Macpherson A., Mahmod T., Scott D. other authors 1997; Mitochondrial damage: a possible mechanism of the “topical” phase of NSAID induced injury to the rat intestine. Gut 41:344–353
     [Google Scholar]
  46. Stark L. A., Dunlop M. G. 2005; Nucleolar sequestration of RelA (p65) regulates NF- κ B-driven transcription and apoptosis. Mol Cell Biol 25:5985–6004
     [Google Scholar]
  47. Starkov A. A., Fiskum G. 2003; Regulation of brain mitochondrial H2O2 production by membrane potential and NAD(P)H redox state. J Neurochem 86:1101–1107
     [Google Scholar]
  48. Uyemura S. A., Santos A. C., Mingatto F. E., Jordani M. C., Curti C. 1997; Diclofenac sodium and mefenamic acid: potent inducers of the membrane permeability transition in renal cortex mitochondria. Arch Biochem Biophys 342:231–235
     [Google Scholar]
  49. Votyakova T. V., Reynolds I. J. 2001; ΔΨm-Dependent and -independent production of reactive oxygen species by rat brain mitochondria. J Neurochem 79:266–277
     [Google Scholar]
  50. Waterhouse N. J., Goldstein J. C., von Ahsen O., Schuler M., Newmeyer D. D., Green D. R. 2001; Cytochrome c maintains mitochondrial transmembrane potential and ATP generation after outer mitochondrial membrane permeabilization during the apoptotic process. J Cell Biol 153:319–328
     [Google Scholar]
  51. Wissing S., Ludovico P., Herker E., Büttner S., Engelhardt S. M., Decker T., Link A., Proksch A., Rodrigues F. other authors 2004; An AIF orthologue regulates apoptosis in yeast. J Cell Biol 166:969–974
     [Google Scholar]
/content/journal/micro/10.1099/mic.0.2008/017228-0
Loading
Mitochondrial involvement in aspirin-induced apoptosis in yeast
Microbiology 154, 2740 (2008); https://doi.org/10.1099/mic.0.2008/017228-0
/content/journal/micro/10.1099/mic.0.2008/017228-0
/content/journal/micro/10.1099/mic.0.2008/017228-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error