Abstract
FSH1 belongs to the family of serine hydrolases in yeast and is homologous to the human ovarian tumor suppressor gene (OVAC2). Our preliminary results showed that cells lacking Fsh1p exhibit an increase in cell growth, and a decrease in the expression of AIF1 and NUC1 (apoptosis responsive genes) when compared to the wild type cells. Growth inhibition of cells overexpressing FSH1 is due to induction of cell death associated with cell death markers typical of mammalian apoptosis namely DNA fragmentation, phosphatidylserine externalization, ROS accumulation, Cytochrome c release, and altered mitochondrial membrane potential. When wild type cells were overexpressed with FSH1 there was up regulation of AIF1 level when compared to control cells suggesting that overexpression of FSH1 regulated cell death in yeast.
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Abbreviations
- FSH:
-
Family of serine hydrolase
- S. cerevisiae :
-
Saccharomyces cerevisiae
- MMP:
-
Mitochondrial membrane potential
References
Acosta-Zaldıvar M, Andres MT, Rego A, Pereira CS, Fierro JF, Corte-Real M (2016) Human lactoferrin triggers a mitochondrial- and caspases dependent regulated cell death in Saccharomyces cerevisiae. Apoptosis 21:163–173
Amigoni L, Frigerio G, Martegani E, Colombo S (2016) Involvement of Aif1 in apoptosis triggered by lack of Hxk2 in the yeast Saccharomyces cerevisiae. FEMS Yeast Res 16(3):fow16. https://doi.org/10.1093/femsyr/fow016
Azizi AA, Gelpi E, Yang JW, Rupp B, Godwin AK, Slater C, Slavc I, Lubec G (2006) Mass spectrometric identification of serine hydrolase OVCA2 in the medulloblastoma cell line DAOY. Cancer Lett 241(2):235–249
Baxter SM, Rosenblum JS, Knutson S, Nelson MR, Montimurro JS, DiGennaro JA, Speir JA, Burbaum JJ, Fetrow JS (2004) Synergistic computational and experimental proteomics approaches for more accurate detection of active serine hydrolases in yeast. Mol Cell Proteom 3:209–225
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Büttner S, Eisenberg T, Carmona-Gutierrez D, Ruli D, Knauer H, Ruckenstuhl C, Sigrist C, Wissing S, Kollroser M, Fröhlich KU, Sigrist S, Madeo F (2007) Endonuclease G regulates budding yeast life and death. Mol Cell 25:233–246
Carmona-Gutierrez D, Bauer MA, Zimmermann A, Aguilera A, Austriaco N, Ayscough K et al (2018) Guidelines and recommendations on yeast cell death nomenclature. Microbial Cell 5:4–31
Gietz D, St Jean A, Woods RA, Schiestl RH (1992) Improved method for high-efficiency transformation of intact yeast cells. Nucleic Acids Res 20:1425
Gowsalya R, Ravi C, Kannan M, Nachiappan V (2019) FSH3 mediated cell death is dependent on NUC1 in Saccharomyces cerevisiae. FEMS Yeast Res 19(3):foz017. https://doi.org/10.1093/femsyr/foz017
Guaragnella N, Bobba A, Passarella S (2010) Yeast acetic acid induced programmed cell death can occur without cytochrome c release which requires metacaspase YCA1. FEBS Lett 584:224–228
Herker E, Jungwrth H, Lehmann KA, Maldene C, Frohlich KU, Wissing S, Buttner S, Fehr M, Sigrist S, Madeo F (2004) Chronological aging leads to apoptosis in yeast. J Cell Biol 164:501–507
Khan MA, Chock PB, Stadtman ER (2005) Knockout of caspase-like gene, YCA1, abrogates apoptosis and elevates oxidized proteins in Saccharomyces cerevisiae. PNAS 102:17326–17331
Koning AJ, Lum PY, Williams JM, Wright R (1993) DiOC6 staining reveals organelle structure and dynamics in living yeast cells. Cell Motil Cytoskelet 25:111–128
Laun P, Pichova A, Madeo F, Fuchs J, Ellinger A, Kohlwein S, Dawes I, Fröhlich KU, Breitenbach M (2001) Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis. Mol Microbiol 39:1166–1173
Lee BI, Lee DJ, Cho KJ, Kim GW (2005) Early nuclear translocation of endonuclease G and subsequent DNA fragmentation after transient focal cerebral ischemia in mice. Neurosci Lett 386:23–27
Li LY, Luo X, Wang X (2001) Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 412:95–99
Ligr M, Madeo F, Frohlich E, Hilt W, Frohlich KU, Wolf DH (1998) Mammalian Bax triggers apoptotic changes in yeast. FEBS Lett 38:61–65
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
Ly JD, Grubb D, Lawen A (2003) The mitochondrial membrane potential (∆ψm) in apoptosis; an update. Apoptosis 8:115–128
Madeo F, Frohlich E, Frohlich KU (1997) A yeast mutant showing diagnostic markers of early and late apoptosis. J Cell Biol 139:729–734
Madeo F, Frohlich E, Ligr M, Grey M, Sigrist SJ, Wolf DH, Frohlich KU (1999) Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol 145:757–767
Madeo F, Herker E, Maldener C, Wissing S, Lachelt S, Herlan M, Fehr M, Lauber K, Sigrist SJ, Wesselborg S, Frohlich KU (2002) A caspase-related protease regulates apoptosis in yeast. Mol Cell 9:911–917
Madeo F, Herker E, Wissing S, Jungwirth H, Eisenberg T, Frohlich KU (2004) Apoptosis in yeast. Curr Opin Microbiol 7:655–660
Madeo F, Carmona-Gutierrez D, Ring J (2009) Caspase-dependent and caspase-independent cell death pathways in yeast. Biochem Biophys Res Commun 382:227–231
Mazzoni C, Falcone C (2008) Caspase-dependent apoptosis in yeast. Biochim Biophys Acta 1783:1320–1327
Miramar MD, Costantini P, Ravagnan L, Saraiva LM, Haouzi D, Brothers G, Penninger JM, Peleato ML, Kroemer G, Susin SA (2001) NADH oxidase activity of mitochondrial apoptosis-inducing factor. J Biol Chem 276:16391–16398
Montague JW Jr, Hughes FM, Cidlowski JA (1997) Native recombinant cyclophilins A, B, and C degrade DNA independently of peptidylprolyl cis-trans- isomerase activity. Potential roles cyclophilins in apoptosis. J Biol Chem 272:6677–6684
Muzaffar S, Chattoo BB (2017) Apoptosis-inducing factor (Aif1) mediates anacardic acid-induced apoptosis in Saccharomyces cerevisiae. Apoptosis 22:463–474
Quevillon-Cheruel S, Leulliot N, Graille M, Hervouet N, Coste F, Bénédetti H, Zelwer C, Janin J, Van Tilbeurgh H (2005) Crystal structure of yeast YHR049W/FSH1, a member of the serine hydrolase family. Protein Sci 14:1350–1356
Schafer P, Scholz SR, Gimadutdinow O, Cymerman IA, Bujnicki JM, Ruiz-Carrillo A, Pingoud A, Meiss G (2004) Structural and functional characterization of mitochondrial Endo G, a sugar non-specific nuclease which plays an important role during apoptosis. J Mol Biol 338:217–228
Simon H-U, Haj-Yehia A, Levi-Schaffer F (2000) Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5:415–418
Sousa CA, Soares HMVM, Soares EV (2019) Nickel oxide nanoparticles trigger caspase- and mitochondria-dependent apoptosis in the yeast Saccharomyces cerevisiae. Chem Res Toxicol 32:245–254
Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM, Kroemer G (1999) Molecular characterization of mitochondrial apoptosis-inducing factor. Nature 397:441–446
Vahsen N, Cande C, Briere JJ (2004) AIF deficiency compromises oxidative phosphorylation. EMBO J 23:4679–4689
Wissing S, Ludovico P, Herker E (2004) An AIF orthologue regulates apoptosis in yeast. J Cell Biol 166:969–974
Zaim J, Speina E, Kierzek AM (2005) Identification of new genes regulated by the Crt1 transcription factor, an effector of the DNA damage checkpoint pathway in Saccharomyces cerevisiae. J Biol Chem 280:28–37
Acknowledgements
We thank Prof. Ram Rajasekharan (Central Food Technological Research Institute, Mysore, India) for providing yeast strains and reagents. We thank the infrastructure facilities from DST-FIST, Department of Biochemistry, Life Sciences & DST-PURSE facilities, of Bharathidasan University.
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VN and RG designed the experiments, RG, CR and MA performed the experiments.VN and RG wrote the manuscript. All the authors discussed the results and concluded the manuscript.
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Gowsalya, R., Ravi, C., Arul, M. et al. FSH1 overexpression triggers apoptosis in Saccharomyces cerevisiae. Antonie van Leeuwenhoek 112, 1775–1784 (2019). https://doi.org/10.1007/s10482-019-01310-7
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DOI: https://doi.org/10.1007/s10482-019-01310-7