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LC-MS/MS-Based, Label-Free, Peptide-Centric, Quantitative Proteomics of the H2O2 Stimulon in Wild-Type S. Cerevisiae Cells vs Those Deleted for the H2O2 Sensor, Ccp1

Title:

LC-MS/MS-Based, Label-Free, Peptide-Centric, Quantitative Proteomics of the H2O2 Stimulon in Wild-Type S. Cerevisiae Cells vs Those Deleted for the H2O2 Sensor, Ccp1

Sadeghian, Tanaz (2022) LC-MS/MS-Based, Label-Free, Peptide-Centric, Quantitative Proteomics of the H2O2 Stimulon in Wild-Type S. Cerevisiae Cells vs Those Deleted for the H2O2 Sensor, Ccp1. Masters thesis, Concordia University.

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Abstract

Reactive oxygen species (ROS) such as hydrogen peroxide (H2O2) can be harmful to cells. However, cells adapt to sublethal doses of H2O2 by the enhancement of antioxidant synthesis and shifting their carbon flux to NADPH generation. Cytochrome c peroxidase (Ccp1) is a heme-based protein located in the intermembrane space of yeast mitochondria that functions as a sensor of H2O2. To fully explore the H2O2-sensing role of Ccp1, we compared the H2O2 stimulon in wt and ccp1Δ Saccharomyces cerevisiae cells (BY4741 strain) using label-free peptide-centric, quantitative proteomics. Cells were grown to mid-log phase, challenged with 0.4 mM H2O2, and whole-cell lysates were prepared 10 and 60 min later for three biological replicates. All the proteins in each lysate were concentrated into a single band on a 6% stacking gel for tryptic digestion and peptide analysis by nanoLC-MS/MS. A total of 2222 proteins were quantified and identified from their unique peptides (14,642) in the biological replicates. The stimulated and repressed proteins were analyzed using an abundance ratio (R) calculated by Proteome Discoverer v2.4, and Ccp1’s role was evaluated through the examination of proteins up- and downregulated following H2O2 challenge. Our results suggest that Ccp1 influences the abundance of key antioxidant enzymes such as Ctt1, Trx2 and Prx1 by effecting the levels of transcription factors involved in H2O2 signaling, including Yap1 and Hsf1. Ccp1 deletion alters the abundance of proteins that are important in NADPH production such as Rki1 and Sol3. These proteomics results combined with published biochemical data provide new insights into how Ccp1 contributes to the coordination of cellular defensive mechanisms and the shifts in metabolic pathways following H2O2 challenge.

Divisions:Concordia University > Faculty of Arts and Science > Chemistry and Biochemistry
Item Type:Thesis (Masters)
Authors:Sadeghian, Tanaz
Institution:Concordia University
Degree Name:M. Sc.
Program:Chemistry
Date:July 2022
Thesis Supervisor(s):English, Ann
ID Code:990957
Deposited By: Tanaz Sadeghian
Deposited On:27 Oct 2022 14:24
Last Modified:27 Oct 2022 14:24

References:

(1) Veal, E. A.; Day, A. M.; Morgan, B. A. Hydrogen Peroxide Sensing and Signaling. Mol. Cell 2007, 26 (1), 1–14.
(2) Collinson, L. P.; Dawes, I. W. Inducibility of the Response of Yeast Cells to Peroxide Stress. Microbiology 1992, 138 (2), 329–335.
(3) Farrugia, G.; Balzan, R. Oxidative Stress and Programmed Cell Death in Yeast. Front. Oncol. 2012, 2, 64.
(4) Jamieson, D. J. Oxidative Stress Responses of the Yeast Saccharomyces Cerevisiae. Yeast 1998, 14 (16), 1511–1527.
(5) Lou, M. F. Redox Regulation in the Lens. Prog. Retin. Eye Res. 2003, 22 (5), 657–682.
(6) Atamna, H.; Mackey, J.; Dhahbi, J. M. Mitochondrial Pharmacology: Electron Transport Chain Bypass as Strategies to Treat Mitochondrial Dysfunction. Biofactors 2012, 38 (2), 158–166.
(7) Kohen, R.; Nyska, A. Invited Review: Oxidation of Biological Systems: Oxidative Stress Phenomena, Antioxidants, Redox Reactions, and Methods for Their Quantification. Toxicol. Pathol. 2002, 30 (6), 620–650.
(8) Sies, H. Physiological Society Symposium: Impaired Endothelial and Smooth Muscle Cell Function in Oxidative Stress. Exp. Physiol. 1997, 82 (2), 291–295.
(9) Gasch, A. P.; Werner-Washburne, M. The Genomics of Yeast Responses to Environmental Stress and Starvation. Funct. Integr. Genomics 2002, 2 (4), 181–192.
(10) Slater, A. F.; Stefan, C.; Nobel, I.; Orrenius, S. The Role of Intracellular Oxidants in Apoptosis. Biochim. Biophys. Acta BBA-Mol. Basis Dis. 1995, 1271 (1), 59–62.
(11) Forman, H. J. Use and Abuse of Exogenous H2O2 in Studies of Signal Transduction. Free Radic. Biol. Med. 2007, 42 (7), 926–932.
(12) Sousa-Lopes, A.; Antunes, F.; Cyrne, L.; Marinho, H. Decreased Cellular Permeability to H2O2 Protects Saccharomyces Cerevisiae Cells in Stationary Phase against Oxidative Stress. FEBS Lett. 2004, 578 (1–2), 152–156.
(13) Martins Jr, D. Genetic Intervention and Biochemical Analysis of Antioxidant Enzyme Function and Their Post-Translational Modifications in Yeast. 2014.
(14) Kathiresan, M. Biochemical and Mass Spectrometric Analysis of Yeast Cytochrome c Peroxidase in Vitro and in Vivo Gives Insights into Its Biological Functions as a H2O2 Sensor and Heme Donor Protein. 2015.
(15) Kathiresan, M.; Martins, D.; English, A. M. Respiration Triggers Heme Transfer from Cytochrome c Peroxidase to Catalase in Yeast Mitochondria. Proc. Natl. Acad. Sci. 2014, 111 (49), 17468–17473.
(16) Mulford, K.; Fassler, J. Association of the Skn7 and Yap1 Transcription Factors in the Saccharomyces Cerevisiae Oxidative Stress Response. Eukaryot. Cell 2011, 10 (6), 761–769.
(17) Martins, D.; English, A. M. Catalase Activity Is Stimulated by H2O2 in Rich Culture Medium and Is Required for H2O2 Resistance and Adaptation in Yeast. Redox Biol. 2014, 2, 308–313.
(18) Spencer, J.; Phister, T. G.; Smart, K. A.; Greetham, D. Tolerance of Pentose Utilising Yeast to Hydrogen Peroxide-Induced Oxidative Stress. BMC Res. Notes 2014, 7 (1), 1–12.
(19) Dastpeyman, S. Spatiotemporal Tracking of Heme-Bound and Heme-Free Yeast Cytochrome c Peroxidase in Live Cells and Probing Its Regulation of the H2O2 Stimulon at the Proteome Level, Concordia University, 2020.
(20) Sablina, A. A.; Budanov, A. V.; Ilyinskaya, G. V.; Agapova, L. S.; Kravchenko, J. E.; Chumakov, P. M. The Antioxidant Function of the P53 Tumor Suppressor. Nat. Med. 2005, 11 (12), 1306–1313.
(21) Poljak, A.; Dawes, I. W.; Ingelse, B. A.; Duncan, M. W.; Smythe, G. A.; Grant, C. M. Oxidative Damage to Proteins in Yeast Cells Exposed to Adaptive Levels of H2O2. Redox Rep. 2003, 8 (6), 371–377.
(22) Semchyshyn, H. M.; Valishkevych, B. V. Hormetic Effect of H2O2 in Saccharomyces Cerevisiae: Involvement of TOR and Glutathione Reductase. Dose-Response 2016, 14 (2), 1559325816636130.
(23) Bienert, G. P.; Schjoerring, J. K.; Jahn, T. P. Membrane Transport of Hydrogen Peroxide. Biochim. Biophys. Acta BBA-Biomembr. 2006, 1758 (8), 994–1003.
(24) Fomenko, D. E.; Koc, A.; Agisheva, N.; Jacobsen, M.; Kaya, A.; Malinouski, M.; Rutherford, J. C.; Siu, K.-L.; Jin, D.-Y.; Winge, D. R. Thiol Peroxidases Mediate Specific Genome-Wide Regulation of Gene Expression in Response to Hydrogen Peroxide. Proc. Natl. Acad. Sci. 2011, 108 (7), 2729–2734.
(25) Kaput, J.; Goltz, S.; Blobel, G. Nucleotide Sequence of the Yeast Nuclear Gene for Cytochrome c Peroxidase Precursor. Functional Implications of the Pre Sequence for Protein Transport into Mitochondria. J. Biol. Chem. 1982, 257 (24), 15054–15058.
(26) Van de Water, K.; Sterckx, Y. G.; Volkov, A. N. The Low-Affinity Complex of Cytochrome c and Its Peroxidase. Nat. Commun. 2015, 6 (1), 1–12.
(27) Poulos, T. L.; Freer, S. T.; Alden, R. A.; Edwards, S. L.; Skogland, U.; Takio, K.; Eriksson, B.; Xuong, N.-H.; Yonetani, T.; Kraut, J. The Crystal Structure of Cytochrome c Peroxidase. J. Biol. Chem. 1980, 255 (2), 575–580.
(28) Erman, J. E.; Vitello, L. B. Yeast Cytochrome c Peroxidase: Mechanistic Studies via Protein Engineering. Biochim. Biophys. Acta BBA-Protein Struct. Mol. Enzymol. 2002, 1597 (2), 193–220.
(29) Kaput, J.; Brandriss, M. C.; Prussak-Wieckowska, T. In Vitro Import of Cytochrome c Peroxidase into the Intermembrane Space: Release of the Processed Form by Intact Mitochondria. J. Cell Biol. 1989, 109 (1), 101–112.
(30) Erman, J. E.; Vitello, L. B.; Mauro, J. M.; Kraut, J. Detection of an Oxyferryl Porphyrin. Pi.-Cation-Radical Intermediate in the Reaction between Hydrogen Peroxide and a Mutant Yeast Cytochrome c Peroxidase. Evidence for Tryptophan-191 Involvement in the Radical Site of Compound I. Biochemistry 1989, 28 (20), 7992–7995.
(31) Martins, D.; Kathiresan, M.; English, A. M. Cytochrome c Peroxidase Is a Mitochondrial Heme-Based H2O2 Sensor That Modulates Antioxidant Defense. Free Radic. Biol. Med. 2013, 65, 541–551.
(32) Kwon, M.; Chong, S.; Han, S.; Kim, K. Oxidative Stresses Elevate the Expression of Cytochrome c Peroxidase in Saccharomyces Cerevisiae. Biochim. Biophys. Acta BBA-Gen. Subj. 2003, 1623 (1), 1–5.
(33) Minard, K. I.; McAlister-Henn, L. Antioxidant Function of Cytosolic Sources of NADPH in Yeast. Free Radic. Biol. Med. 2001, 31 (6), 832–843.
(34) Charizanis, C.; Juhnke, H.; Krems, B.; Entian, K.-D. The Mitochondrial Cytochrome c Peroxidase Ccp1 of Saccharomyces Cerevisiae Is Involved in Conveying an Oxidative Stress Signal to the Transcription Factor Pos9 (Skn7). Mol. Gen. Genet. MGG 1999, 262 (3), 437–447.
(35) Picazo, C.; Molin, M. Impact of Hydrogen Peroxide on Protein Synthesis in Yeast. Antioxidants 2021, 10 (6), 952.
(36) Veal, E. A.; Ross, S. J.; Malakasi, P.; Peacock, E.; Morgan, B. A. Ybp1 Is Required for the Hydrogen Peroxide-Induced Oxidation of the Yap1 Transcription Factor. J. Biol. Chem. 2003, 278 (33), 30896–30904.
(37) Delaunay, A.; Pflieger, D.; Barrault, M.-B.; Vinh, J.; Toledano, M. B. A Thiol Peroxidase Is an H2O2 Receptor and Redox-Transducer in Gene Activation. Cell 2002, 111 (4), 471–481.
(38) Simaan, H.; Lev, S.; Horwitz, B. A. Oxidant-Sensing Pathways in the Responses of Fungal Pathogens to Chemical Stress Signals. Front. Microbiol. 2019, 10, 567.
(39) He, X.; Fassler, J. S. Identification of Novel Yap1p and Skn7p Binding Sites Involved in the Oxidative Stress Response of Saccharomyces Cerevisiae. Mol. Microbiol. 2005, 58 (5), 1454–1467.
(40) Solís, E. J.; Pandey, J. P.; Zheng, X.; Jin, D. X.; Gupta, P. B.; Airoldi, E. M.; Pincus, D.; Denic, V. Defining the Essential Function of Yeast Hsf1 Reveals a Compact Transcriptional Program for Maintaining Eukaryotic Proteostasis. Mol. Cell 2016, 63 (1), 60–71.
(41) Raitt, D. C.; Johnson, A. L.; Erkine, A. M.; Makino, K.; Morgan, B.; Gross, D. S.; Johnston, L. H. The Skn7 Response Regulator of Saccharomyces Cerevisiae Interacts with Hsf1 in Vivo and Is Required for the Induction of Heat Shock Genes by Oxidative Stress. Mol. Biol. Cell 2000, 11 (7), 2335–2347.
(42) Lee, J.; Godon, C.; Lagniel, G.; Spector, D.; Garin, J.; Labarre, J.; Toledano, M. B. Yap1 and Skn7 Control Two Specialized Oxidative Stress Response Regulons in Yeast. J. Biol. Chem. 1999, 274 (23), 16040–16046.
(43) Hasan, R.; Leroy, C.; Isnard, A.; Labarre, J.; Boy‐Marcotte, E.; Toledano, M. B. The Control of the Yeast H2O2 Response by the Msn2/4 Transcription Factors. Mol. Microbiol. 2002, 45 (1), 233–241.
(44) Ma, M.; Liu, Z. L. Comparative Transcriptome Profiling Analyses during the Lag Phase Uncover YAP1, PDR1, PDR3, RPN4, and HSF1 as Key Regulatory Genes in Genomic Adaptation to the Lignocellulose Derived Inhibitor HMF for Saccharomyces Cerevisiae. BMC Genomics 2010, 11 (1), 1–19.
(45) Szatkowska, R.; Garcia-Albornoz, M.; Roszkowska, K.; Holman, S. W.; Furmanek, E.; Hubbard, S. J.; Beynon, R. J.; Adamczyk, M. Glycolytic Flux in Saccharomyces Cerevisiae Is Dependent on RNA Polymerase III and Its Negative Regulator Maf1. Biochem. J. 2019, 476 (7), 1053–1082.
(46) Nanyan, M.; Takagi, H. Proline Homeostasis in Saccharomyces Cerevisiae: How Does the Stress-Responsive Transcription Factor Msn2 Play a Role? Front. Genet. 2020, 11, 438.
(47) Boisnard, S.; Lagniel, G.; Garmendia-Torres, C.; Molin, M.; Boy-Marcotte, E.; Jacquet, M.; Toledano, M. B.; Labarre, J.; Chédin, S. H2O2 Activates the Nuclear Localization of Msn2 and Maf1 through Thioredoxins in Saccharomyces Cerevisiae. Eukaryot. Cell 2009, 8 (9), 1429–1438.
(48) Jacquel, B.; Matifas, A.; Charvin, G. A Trade-off between Stress Resistance and Tolerance Underlies the Adaptive Response to Hydrogen Peroxide. bioRxiv 2021.
(49) Domon, B.; Aebersold, R. Mass Spectrometry and Protein Analysis. science 2006, 312 (5771), 212–217.
(50) Neverova, I.; Van Eyk, J. E. Role of Chromatographic Techniques in Proteomic Analysis. J. Chromatogr. B 2005, 815 (1–2), 51–63.
(51) Park, K.; Yoon, J. Y.; Lee, S.; Paek, E.; Park, H.; Jung, H.-J.; Lee, S.-W. Isotopic Peak Intensity Ratio Based Algorithm for Determination of Isotopic Clusters and Monoisotopic Masses of Polypeptides from High-Resolution Mass Spectrometric Data. Anal. Chem. 2008, 80 (19), 7294–7303.
(52) Zhang, Y.; Fonslow, B. R.; Shan, B.; Baek, M.-C.; Yates III, J. R. Protein Analysis by Shotgun/Bottom-up Proteomics. Chem. Rev. 2013, 113 (4), 2343–2394.
(53) Smolka, M.; Zhou, H.; Aebersold, R. Quantitative Protein Profiling Using Two-Dimensional Gel Electrophoresis, Isotope-Coded Affinity Tag Labeling, and Mass Spectrometry. Mol. Cell. Proteomics 2002, 1 (1), 19–29.
(54) Ciborowski, P.; Silberring, J. Proteomic Profiling and Analytical Chemistry: The Crossroads; Elsevier, 2016.
(55) Magdeldin, S.; Enany, S.; Yoshida, Y.; Xu, B.; Zhang, Y.; Zureena, Z.; Lokamani, I.; Yaoita, E.; Yamamoto, T. Basics and Recent Advances of Two Dimensional-Polyacrylamide Gel Electrophoresis. Clin. Proteomics 2014, 11 (1), 1–10.
(56) Yerlekar, A.; Dudhe, P. A Review on Study and Comparison between 2D Gel Electrophoresis and Mass Spectrometry. IOSR J Comput Eng 2014, 16, 97e104.
(57) Matthiesen, R. Mass Spectrometry Data Analysis in Proteomics; Springer, 2007; Vol. 367.
(58) Schey, K. L.; Grey, A. C.; Nicklay, J. J. Mass Spectrometry of Membrane Proteins: A Focus on Aquaporins. Biochemistry 2013, 52 (22), 3807–3817.
(59) Sap, K. A.; Demmers, J. A. Labeling Methods in Mass Spectrometry Based Quantitative Proteomics, Integrative Proteomics, Dr. Hon-Chiu Leung (Ed.), ISBN: 978-953-51-0070-6, InTech. InTech Doi 2012, 10, 32489.
(60) Zhu, W.; Smith, J. W.; Huang, C.-M. Mass Spectrometry-Based Label-Free Quantitative Proteomics. J. Biomed. Biotechnol. 2009, 2010.
(61) Matthiesen, R. Mass Spectrometry Data Analysis in Proteomics; Springer, 2007; Vol. 367.
(62) Megger, D. A.; Bracht, T.; Meyer, H. E.; Sitek, B. Label-Free Quantification in Clinical Proteomics. Biochim. Biophys. Acta BBA-Proteins Proteomics 2013, 1834 (8), 1581–1590.
(63) Kalli, A.; Smith, G. T.; Sweredoski, M. J.; Hess, S. Evaluation and Optimization of Mass Spectrometric Settings during Data-Dependent Acquisition Mode: Focus on LTQ-Orbitrap Mass Analyzers. J. Proteome Res. 2013, 12 (7), 3071–3086.
(64) Guan, S.; Taylor, P. P.; Han, Z.; Moran, M. F.; Ma, B. Data Dependent–Independent Acquisition (Ddia) Proteomics. J. Proteome Res. 2020, 19 (8), 3230–3237.
(65) Röst, H. L.; Rosenberger, G.; Navarro, P.; Gillet, L.; Miladinović, S. M.; Schubert, O. T.; Wolski, W.; Collins, B. C.; Malmström, J.; Malmström, L. OpenSWATH Enables Automated, Targeted Analysis of Data-Independent Acquisition MS Data. Nat. Biotechnol. 2014, 32 (3), 219–223.
(66) Proteome Discoverer Guide v2.4.
(67) Vreeke, G. J.; Lubbers, W.; Vincken, J.-P.; Wierenga, P. A. A Method to Identify and Quantify the Complete Peptide Composition in Protein Hydrolysates. Anal. Chim. Acta 2022, 339616.
(68) Mallick, P.; Kuster, B. Proteomics: A Pragmatic Perspective. Nat. Biotechnol. 2010, 28 (7), 695–709.
(69) Hodge, K.; Ten Have, S.; Hutton, L.; Lamond, A. I. Cleaning up the Masses: Exclusion Lists to Reduce Contamination with HPLC-MS/MS. J. Proteomics 2013, 88, 92–103.
(70) Dowell, J. A.; Frost, D. C.; Zhang, J.; Li, L. Comparison of Two-Dimensional Fractionation Techniques for Shotgun Proteomics. Anal. Chem. 2008, 80 (17), 6715–6723.
(71) Siepen, J. A.; Keevil, E.-J.; Knight, D.; Hubbard, S. J. Prediction of Missed Cleavage Sites in Tryptic Peptides Aids Protein Identification in Proteomics. J. Proteome Res. 2007, 6 (1), 399–408.
(72) Saveliev, S.; Bratz, M.; Zubarev, R.; Szapacs, M.; Budamgunta, H.; Urh, M. Trypsin/Lys-C Protease Mix for Enhanced Protein Mass Spectrometry Analysis. Nat. Methods 2013, 10 (11), i–ii.
(73) Datta, S.; Mertens, B. J. Statistical Analysis of Proteomics, Metabolomics, and Lipidomics Data Using Mass Spectrometry; Springer, 2017.
(74) Käll, L.; Storey, J. D.; MacCoss, M. J.; Noble, W. S. Posterior Error Probabilities and False Discovery Rates: Two Sides of the Same Coin. J. Proteome Res. 2008, 7 (01), 40–44.
(75) Risk, B. A.; Edwards, N. J.; Giddings, M. C. A Peptide-Spectrum Scoring System Based on Ion Alignment, Intensity, and Pair Probabilities. J. Proteome Res. 2013, 12 (9), 4240–4247.
(76) Aggarwal, S.; Yadav, A. K. False Discovery Rate Estimation in Proteomics. In Statistical Analysis in Proteomics; Springer, 2016; pp 119–128.
(77) Ham, B. M.; Yang, F.; Jayachandran, H.; Jaitly, N.; Monroe, M. E.; Gritsenko, M. A.; Livesay, E. A.; Zhao, R.; Purvine, S. O.; Orton, D. The Influence of Sample Preparation and Replicate Analyses on HeLa Cell Phosphoproteome Coverage. J. Proteome Res. 2008, 7 (6), 2215–2221.
(78) Piehowski, P. D.; Petyuk, V. A.; Orton, D. J.; Xie, F.; Moore, R. J.; Ramirez-Restrepo, M.; Engel, A.; Lieberman, A. P.; Albin, R. L.; Camp, D. G. Sources of Technical Variability in Quantitative LC–MS Proteomics: Human Brain Tissue Sample Analysis. J. Proteome Res. 2013, 12 (5), 2128–2137.
(79) Tabb, D. L.; Vega-Montoto, L.; Rudnick, P. A.; Variyath, A. M.; Ham, A.-J. L.; Bunk, D. M.; Kilpatrick, L. E.; Billheimer, D. D.; Blackman, R. K.; Cardasis, H. L. Repeatability and Reproducibility in Proteomic Identifications by Liquid Chromatography− Tandem Mass Spectrometry. J. Proteome Res. 2010, 9 (2), 761–776.
(80) Bartlett, J.; Frost, C. Reliability, Repeatability and Reproducibility: Analysis of Measurement Errors in Continuous Variables. Ultrasound Obstet. Gynecol. Off. J. Int. Soc. Ultrasound Obstet. Gynecol. 2008, 31 (4), 466–475.
(81) Välikangas, T.; Suomi, T.; Elo, L. L. A Systematic Evaluation of Normalization Methods in Quantitative Label-Free Proteomics. Brief. Bioinform. 2018, 19 (1), 1–11.
(82) Cox, J.; Hein, M. Y.; Luber, C. A.; Paron, I.; Nagaraj, N.; Mann, M. Accurate Proteome-Wide Label-Free Quantification by Delayed Normalization and Maximal Peptide Ratio Extraction, Termed MaxLFQ. Mol. Cell. Proteomics 2014, 13 (9), 2513–2526.
(83) Altman, D. G.; Bland, J. M. How to Obtain the P Value from a Confidence Interval. Bmj 2011, 343.
(84) Belle, A.; Tanay, A.; Bitincka, L.; Shamir, R.; O’Shea, E. K. Quantification of Protein Half-Lives in the Budding Yeast Proteome. Proc. Natl. Acad. Sci. 2006, 103 (35), 13004–13009.
(85) Godon, C.; Lagniel, G.; Lee, J.; Buhler, J.-M.; Kieffer, S.; Perrot, M.; Boucherie, H.; Toledano, M. B.; Labarre, J. The H2O2 Stimulon in Saccharomyces Cerevisiae. J. Biol. Chem. 1998, 273 (35), 22480–22489.
(86) Kirkman, H. N.; Galiano, S.; Gaetani, G. The Function of Catalase-Bound NADPH. J. Biol. Chem. 1987, 262 (2), 660–666.
(87) Luikenhuis, S.; Perrone, G.; Dawes, I. W.; Grant, C. M. The Yeast Saccharomyces Cerevisiae Contains Two Glutaredoxin Genes That Are Required for Protection against Reactive Oxygen Species. Mol. Biol. Cell 1998, 9 (5), 1081–1091.
(88) Brachmann, C.; Kaduhr, L.; Jüdes, A.; Ravichandran, K. E.; West, J. D.; Glatt, S.; Schaffrath, R. Redox Requirements for Ubiquitin-like Urmylation of Ahp1, a 2-Cys Peroxiredoxin from Yeast. Redox Biol. 2020, 30, 101438.
(89) Roger, F.; Picazo, C.; Reiter, W.; Libiad, M.; Asami, C.; Hanzén, S.; Gao, C.; Lagniel, G.; Welkenhuysen, N.; Labarre, J. Peroxiredoxin Promotes Longevity and H2O2-Resistance in Yeast through Redox-Modulation of Protein Kinase A. Elife 2020, 9, e60346.
(90) Nyström, T.; Yang, J.; Molin, M. Peroxiredoxins, Gerontogenes Linking Aging to Genome Instability and Cancer. Genes Dev. 2012, 26 (18), 2001–2008.
(91) Biteau, B.; Labarre, J.; Toledano, M. B. ATP-Dependent Reduction of Cysteine–Sulphinic Acid by S. Cerevisiae Sulphiredoxin. Nature 2003, 425 (6961), 980–984.
(92) Gulshan, K.; Thommandru, B.; Moye-Rowley, W. S. Proteolytic Degradation of the Yap1 Transcription Factor Is Regulated by Subcellular Localization and the E3 Ubiquitin Ligase Not4. J. Biol. Chem. 2012, 287 (32), 26796–26805.
(93) Delaunay, A.; Isnard, A.; Toledano, M. B. H2O2 Sensing through Oxidation of the Yap1 Transcription Factor. EMBO J. 2000, 19 (19), 5157–5166.
(94) Chen, L.-H.; Lin, C.-H.; Chung, K.-R. Roles for SKN7 Response Regulator in Stress Resistance, Conidiation and Virulence in the Citrus Pathogen Alternaria Alternata. Fungal Genet. Biol. 2012, 49 (10), 802–813.
(95) Kathiresan, M.; English, A. Targeted Proteomics Identify Metabolism-Dependent Interactors of Yeast Cytochrome c Peroxidase: Implications in Stress Response and Heme Trafficking. Metallomics 2016, 8 (4), 434–443.
(96) Benaroudj, N.; Goldberg, A. L. Trehalose Accumulation during Cellular Stress Protects Cells and Cellular Proteins from Damage by Oxygen Radicals. J. Biol. Chem. 2001, 276 (26), 24261–24267.
(97) Jamieson, D. J. Oxidative Stress Responses of the Yeast Saccharomyces Cerevisiae. Yeast 1998, 14 (16), 1511–1527.
(98) Parrou, J. L.; Teste, M.-A.; François, J. Effects of Various Types of Stress on the Metabolism of Reserve Carbohydrates in Saccharomyces Cerevisiae: Genetic Evidence for a Stress-Induced Recycling of Glycogen and Trehalose. Microbiology 1997, 143 (6), 1891–1900.
(99) Swart, C.; Martínez-Jaime, S.; Gorka, M.; Zander, K.; Graf, A. Hit-Gel: Streamlining in-Gel Protein Digestion for High-Throughput Proteomics Experiments. Sci. Rep. 2018, 8 (1), 1–8.
(100) Wiśniewski, J. R.; Wegler, C.; Artursson, P. Multiple-Enzyme-Digestion Strategy Improves Accuracy and Sensitivity of Label-and Standard-Free Absolute Quantification to a Level That Is Achievable by Analysis with Stable Isotope-Labeled Standard Spiking. J. Proteome Res. 2018, 18 (1), 217–224.
(101) Shenton, D.; Smirnova, J. B.; Selley, J. N.; Carroll, K.; Hubbard, S. J.; Pavitt, G. D.; Ashe, M. P.; Grant, C. M. Global Translational Responses to Oxidative Stress Impact upon Multiple Levels of Protein Synthesis. J. Biol. Chem. 2006, 281 (39), 29011–29021.
(102) Fernandes, P. N.; Mannarino, S. C.; Silva, C. G.; Pereira, M. D.; Panek, A. D.; Eleutherio, E. C. Oxidative Stress Response in Eukaryotes: Effect of Glutathione, Superoxide Dismutase and Catalase on Adaptation to Peroxide and Menadione Stresses in Saccharomyces Cerevisiae. Redox Rep. 2007, 12 (5), 236–244.
(103) Ng, C.-H.; Tan, S.-X.; Perrone, G. G.; Thorpe, G. W.; Higgins, V. J.; Dawes, I. W. Adaptation to Hydrogen Peroxide in Saccharomyces Cerevisiae: The Role of NADPH-Generating Systems and the SKN7 Transcription Factor. Free Radic. Biol. Med. 2008, 44 (6), 1131–1145.
(104) Yamamoto, A.; Ueda, J.; Yamamoto, N.; Hashikawa, N.; Sakurai, H. Role of Heat Shock Transcription Factor in Saccharomyces Cerevisiae Oxidative Stress Response. Eukaryot. Cell 2007, 6 (8), 1373–1379.
(105) François, J.; Parrou, J. L. Reserve Carbohydrates Metabolism in the Yeast Saccharomyces Cerevisiae. Fems Microbiol. Rev. 2001, 25 (1), 125–145.
(106) Vogel, C.; Silva, G. M.; Marcotte, E. M. Protein Expression Regulation under Oxidative Stress. Mol. Cell. Proteomics 2011, 10 (12).
(107) Jiang, D.; Jarrett, H. W.; Haskins, W. E. Methods for Proteomic Analysis of Transcription Factors. J. Chromatogr. A 2009, 1216 (41), 6881–6889.
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Research related to the current document (at the CORE website)
- Research related to the current document (at the CORE website)
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