Mitophagy Improves Ethanol Tolerance in Yeast: Regulation by Mitochondrial Reactive Oxygen Species in Saccharomyces cerevisiae
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Ethanol often accumulates during the process of wine fermentation, and mitophagy has critical role in ethanol output. However, the relationship between mitophagy and ethanol stress is still unclear. In this study, the expression of ATG11 and ATG32 genes exposed to ethanol stress was accessed by real-time quantitative reverse transcription polymerase chain reaction (qRT-PCR). The result indicated that ethanol stress induced expression of the ATG11 and ATG32 genes. The colony sizes and the alcohol yield of atg11 and atg32 were also smaller and lower than those of wild type strain under ethanol whereas the mortality of mutants is higher. Furthermore, compared with wild type, the membrane integrity and the mitochondrial membrane potential of atg11 and atg32 exhibited greater damage following ethanol stress. In addition, a greater proportion of mutant cells were arrested at the G1/G0 cell cycle. There was more aggregation of peroxide hydrogen (H2O2) and superoxide anion (O2 •-) in mutants. These changes in H2O2 and O2 •- in yeasts were altered by reductants or inhibitors of scavenging enzyme by means of regulating the expression of ATG11 and ATG32 genes. Inhibitors of the mitochondrial electron transport chain (mtETC) also increased production of H2O2 and O2 •- by enhancing expression of the ATG11 and ATG32 genes. Further results showed that activator or inhibitor of autophagy also activated or inhibited mitophagy by altering production of H2O2 and O2 •. Therefore, ethanol stress induces mitophagy which improves yeast the tolerance to ethanol and the level of mitophagy during ethanol stress is regulated by ROS derived from mtETC.
Abstract
Ethanol often accumulates during the process of wine fermentation, and mitophagy has critical role in ethanol output. However, the relationship between mitophagy and ethanol stress is still unclear. In this study, the expression of ATG11 and ATG32 genes exposed to ethanol stress was accessed by real-time quantitative reverse transcription polymerase chain reaction (qRT-PCR). The result indicated that ethanol stress induced expression of the ATG11 and ATG32 genes. The colony sizes and the alcohol yield of atg11 and atg32 were also smaller and lower than those of wild type strain under ethanol whereas the mortality of mutants is higher. Furthermore, compared with wild type, the membrane integrity and the mitochondrial membrane potential of atg11 and atg32 exhibited greater damage following ethanol stress. In addition, a greater proportion of mutant cells were arrested at the G1/G0 cell cycle. There was more aggregation of peroxide hydrogen (H2O2) and superoxide anion (O2 •-) in mutants. These changes in H2O2 and O2 •- in yeasts were altered by reductants or inhibitors of scavenging enzyme by means of regulating the expression of ATG11 and ATG32 genes. Inhibitors of the mitochondrial electron transport chain (mtETC) also increased production of H2O2 and O2 •- by enhancing expression of the ATG11 and ATG32 genes. Further results showed that activator or inhibitor of autophagy also activated or inhibited mitophagy by altering production of H2O2 and O2 •. Therefore, ethanol stress induces mitophagy which improves yeast the tolerance to ethanol and the level of mitophagy during ethanol stress is regulated by ROS derived from mtETC.
참고문헌 (48)
- Muller FL, "Complex III releases superoxide to both sides of the inner mitochondrial membrane", J. Biol. Chem, 279, pp.49064~49073 (2004)
- Fedoseeva IV, "The role of flavin-containing enzymes in mitochondrial membrane hyperpolarization and ROS production in respiring Saccharomyces cerevisiae cells under heatshock conditions", Sci. Rep, 7, pp.2586~ (2017)
- Miller A, "Superoxide dismutases : ancient enzymes and new insights", FEBS. Lett, 586, pp.585~595 (2012)
- 권영연, "Mitochondrial Efficiency-Dependent Viability of Saccharomyces cerevisiae Mutants Carrying Individual Electron Transport Chain Component Deletions", Molecules and Cells, 38(12), pp.1054~1063 (2015), 한국분자세포생물학회
- Zyrina AN, "Mitochondrial superoxide dismutase and Yap1p act as a signaling module contributing to ethanol tolerance of the yeast Saccharomyces cerevisiae", Appl. Environ. Microbiol., 83, pp.e02759~ (2017)
- Magrì A, "Overexpression of human SOD1 in VDAC1-less yeast restores mitochondrial functionality modulating beta-barrel outer membrane protein genes", Biochim. Biophys. Acta, 1857, pp.789~798 (2016)
- Knuppertz L, "Stress-dependent opposing roles for mitophagy in aging of the ascomycete Podospora anserina", Autophagy, 13, pp.1037~1052 (2017)
- Rattanawong K, "Cu", Zn-superoxide dismutase and glutathione are involved in response to oxidative stress induced by protein denaturing effect of alachlorin Saccharomy cescerevisiae, 2015, pp.89, 963~971
- Tomoyuki Fukuda, "Mechanisms and Physiological Roles of Mitophagy in Yeast", Molecules and Cells, 41(1), pp.35~44 (2018), 한국분자세포생물학회
- Kanki T, "Mitophagy in yeast : molecular mechanisms and physiological role", Biochim. Biophys. Acta, 1853, pp.2756~2765 (2015)
- Fan P, "Molecular regulation mechanisms and interactions between reactive oxygen species and mitophagy", DNA Cell Biol, 38, pp.10~22 (2019)
- Müller M, "Mitophagy and mitochondrial dynamics in Saccharomyces cerevisiae", Biochim. Biophys. Acta, 1853, pp.2766~2774 (2015)
- Kurihara Y, "Mitophagy plays an essential role in reducing mitochondrial production of reactive oxygen species and mutation of mitochondrial DNA by maintaining mitochondrial quantity and quality in yeast", J. Biol. Chem, 287, pp.3265~3272 (2012)
- Tsukada M, "Isolation and characterization of autophagydefective mutants of Saccharomyces cerevisiae", FEBS. Lett, 333, pp.169~174 (1993)
- 유승민, "A Molecular Approach to Mitophagy and Mitochondrial Dynamics", Molecules and Cells, 41(1), pp.18~26 (2018), 한국분자세포생물학회
- Xia X, "A pseudo-receiver domain in Atg32 is required for mitophagy", Autohhagy, 14, pp.1620~1628 (2018)
- Aihara M, "Tor and the Sin3-Rpd3 complex regulate expression of the mitophagy receptor protein Atg32 in yeast", J. Cell Sci, 127, pp.3184~3196 (2014)
- Furukawa K, "The PP2A-like protein phosphatase Ppg1 and the Far complex cooperatively counteract CK2-mediated phosphorylation of Atg32 to inhibit mitophagy", Cell Rep, 23, pp.3579~3590 (2018)
- Shan YT, "Progress on function of ATG11", Prog. Biochem. Biophys, 46, pp.796~803 (2019)
- Zientara-Rytter K, "Pex3 and Atg37 compete to regulate the interaction between the pexophagy receptor, Atg30, and the Hrr25 kinase", Autophagy, 14, pp.368~384 (2018)
- Chen S, "ER-phagy requires Lnp1, a protein that stabilizes rearrangements of the ER network", Proc. Natl. Acad. Sci. USA, 115, pp.E6237~E6244 (2018)
- Eapena VV, "A pathway of targeted autophagy is induced by DNA damage in budding yeas", Proc. Natl. Acad. Sci. USA, 116, pp.E1158~E1167 (2017)
- Waliullah TM, "Rim15 and Sch9 kinases are involved in induction of autophagic degradation of ribosomes in budding yeast", Biosci. Biotech. Biochem, 81, pp.307~310 (2017)
- Takagi H, "Proline accumulation protects Saccharomyces cerevisiae cells in stationary phase from ethanol stress by reducing reactive oxygen species levels", Yeast, 33, pp.355~363 (2016)
- Noctor G, "Ascorbate and glutathione : keeping active oxygen under control", Annu. Rev. Plant Physiol. Plant Mol. Biol, 49, pp.249~279 (1998)
- Tesnière C, "Responses of Saccharomyces cerevisiae to nitrogen starvation in wine alcoholic fermentation", Appl. Microbiol. Biotechnol, 99, pp.7025~7034 (2015)
- Timón-Gómez A, "Regulation of the stress-activated degradation of mitochondrial respiratory complexes in yeast", Front. Microbiol, 9, pp.106~ (2018)
- Shiroma S, "Enhancement of ethanol fermentation in Saccharomyces cerevisiae sake yeast by disrupting mitophagy function", Appl. Environ. Microbiol, 80, pp.1002~1012 (2014)
- Hong-juan Jing, "Ethanol Induces Autophagy Regulated by Mitochondrial ROS in Saccharomyces cerevisiae", Journal of Microbiology and Biotechnology, 28(12), pp.1982~1991 (2018), 한국미생물·생명공학회
- Mendes-Ferreira A, "Accumulation of nonsuperoxide anion reactive oxygen species mediates nitrogen-limited alcoholic fermentation by Saccharomyces cerevisiae", Appl. Environ. Microbiol, 76, pp.7918~7824 (2010)
- Almeida B, "An atypical active cell death process underlies the fungicidal activity of ciclopirox olamine against the yeast Saccharomyces cerevisiae", FEMS Yeast Res, 7, pp.404~412 (2007)
- Kainz K, "Methods to assess autophagy and chronological aging in yeast", Methods Enzymol, 588, pp.367~394 (2017)
- Ludovico P, "Cytochrome c release and mitochondria involvement in programmed cell death induced by acetic acid in Saccharomyces cerevisiae", Mol. Biol. Cell, 13, pp.2598~2606 (2002)
- Ludovico P, "Assessment of mitochondrial membrane potential in yeast cell populations by flow cytometry", Microbiology, 147, pp.3335~3343 (2001)
- Schmittgen TD, "Analyzing real-time PCR data by the comparative CT method", Nat. Protoc, 3, pp.1101~1108 (2008)
- Wagner-Vogel G, "Uniparental mitochondrial DNA inheritance is not affected in Ustilago maydis Δatg11 mutants blocked in mitophagy", BMC Microbiol, 15, pp.23~ (2015)
- Ma M, "Mechanisms of ethanol tolerance in Saccharomyces cerevisiae", Appl. Microbiol. Biotechnol, 87, pp.829~845 (2010)
- Charoenbhakdi S, "Vacuolar H+-ATPase protects Saccharomyces cerevisiae cells against ethanol-induced oxidative and cell wall stresses", Appl. Environ. Microbiol, 82, pp.3121~3130 (2016)
- Dog?an A, "Improvements of tolerance to stress conditions by genetic engineering in Saccharomyces cerevisiae during ethanol production", Appl. Biochem. Biotechnol, 174, pp.28~42 (2014)
- Lin Y, "Ethanol fermentation from biomass resources : current state and prospects", Appl. Microbiol. Biotechnol, 69, pp.627~642 (2006)
- Zorova LD, "Mitochondrial membrane potential", Analytic. Biochem, 552, pp.50~59 (2018)
- An Z, "Autophagy is required for G1", G0 quiescence in response to nitrogen starvation in Saccharomyces cerevisiae, 2014, pp.10, 1702~1711
- Kim S, "Elucidation of ethanol tolerance mechanisms in saccharomyces cerevisiae by global metabolite profiling", Biotechnol. J, 11, pp.1221~1229 (2016)
- Deffieu M, "Glutathione participates in the regulation of mitophagy in yeast", J. Biol. Chem, 284, pp.14828~14837 (2009)
- Okamoto K, "Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy", Dev. Cell, 17, pp.87~97 (2009)
- Lazarou M, "The ubiquitin kinase PINK1 recruits autophagy receptors to induce mitophagy", Nature, 524, pp.309~314 (2015)
- Bin-Umera MA, "Elimination of damaged mitochondria through mitophagy reduces mitochondrial oxidative stress and increases tolerance to trichothecenes", Proc. Natl. Acad. Sci. USA, 111, pp.11798~11803 (2014)
- Yao Z, "An unconventional pathway for mitochondrial protein egradation", Autophagy, 12, pp.1971~1972 (2016)
