Proteome-wide Light/Dark Modulation of Thiol Oxidation in Cyanobacteria Revealed by Quantitative Site-Specific Redox Proteomics

Guo, Jia; Nguyen, Amelia Y.; Dai, Ziyu; Su, Dian; Gaffrey, Matthew J.; Moore, Ronald J.; Jacobs, Jon M.; Monroe, Matthew E.; Smith, Richard D.; Koppenaal, David W.; Pakrasi, Himadri B.; Qian, Weijun

doi:10.1074/mcp.M114.041160

Title: Proteome-wide Light/Dark Modulation of Thiol Oxidation in Cyanobacteria Revealed by Quantitative Site-Specific Redox Proteomics

Journal Article · Mon Dec 01 00:00:00 EST 2014 · Molecular & Cellular Proteomics. MCP

DOI:https://doi.org/10.1074/mcp.M114.041160· OSTI ID:1640887

Guo, Jia ^[1]; Nguyen, Amelia Y. ^[2]; Dai, Ziyu ^[1]; Su, Dian ^[1]; Gaffrey, Matthew J. ^[1]; Moore, Ronald J. ^[1]; Jacobs, Jon M. ^[1];

^[1];

^[1]; Koppenaal, David W. ^[1]; Pakrasi, Himadri B. ^[3];

^[1]

BATTELLE (PACIFIC NW LAB)
WASHINGTON UNIVERSITY
Washington University in St. Louis

Reversible protein thiol oxidation is an essential regulatory mechanism of photosynthesis, metabolism, and gene expression in photosynthetic organisms. Herein, we present the first proteome-wide quantitative site-specific profiling of in vivo dynamics of thiol oxidation modulated by light/dark in cyanobacterium Synechocystis sp. PCC 6803, an oxygenic photosynthetic prokaryote. Our proteomic approach integrates resin-assisted enrichment with isobaric labeling to enable site-specific and quantitative measurements of reversibly oxidized thiols. The redox dynamics of ~2,200 cysteine sites from 1,060 proteins under different conditions (light, dark, and in the presence of a photosystem II inhibitor DCMU) were quantified. The results revealed broad proteome-wide changes in thiol oxidation in many key biological processes including photosynthesis, carbon fixation, and glycolysis. Moreover, the redox sensitivity data provides a good prediction of potential functional cysteine sites for proteins of interest. Together, our findings provided significant novel insights into the broad redox regulation of photosynthetic organisms.

Cite

Export

Save

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

DOE Contract Number:: AC05-76RL01830

OSTI ID:: 1640887

Report Number(s):: PNNL-SA-100244

Journal Information:: Molecular & Cellular Proteomics. MCP, Vol. 13, Issue 12

Country of Publication:: United States

Language:: English

References (76)

REDOX REGULATION: A Broadening Horizon Buchanan, Bob B.; Balmer, Yves Annual Review of Plant Biology, Vol. 56, Issue 1 https://doi.org/10.1146/annurev.arplant.56.032604.144246	journal	June 2005
Redox Regulation in Photosynthetic Organisms: Signaling, Acclimation, and Practical Implications Foyer, Christine H.; Noctor, Graham Antioxidants & Redox Signaling, Vol. 11, Issue 4 https://doi.org/10.1089/ars.2008.2177	journal	April 2009
Disulfide bond formation network in the three biological kingdoms, bacteria, fungi and mammals: Cellular network for disulfide bond formation Sato, Yoshimi; Inaba, Kenji FEBS Journal, Vol. 279, Issue 13 https://doi.org/10.1111/j.1742-4658.2012.08593.x	journal	June 2012
Unbiased identification of cysteine S-nitrosylation sites on proteins Derakhshan, Behrad; Wille, Pamela C.; Gross, Steven S. Nature Protocols, Vol. 2, Issue 7 https://doi.org/10.1038/nprot.2007.210	journal	June 2007
Identification of S-nitrosylation motifs by site-specific mapping of the S-nitrosocysteine proteome in human vascular smooth muscle cells Greco, T. M.; Hodara, R.; Parastatidis, I. Proceedings of the National Academy of Sciences, Vol. 103, Issue 19 https://doi.org/10.1073/pnas.0600729103	journal	April 2006
Protein S-nitrosylation: purview and parameters Hess, Douglas T.; Matsumoto, Akio; Kim, Sung-Oog Nature Reviews Molecular Cell Biology, Vol. 6, Issue 2 https://doi.org/10.1038/nrm1569	journal	February 2005
Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity Paulsen, Candice E.; Truong, Thu H.; Garcia, Francisco J. Nature Chemical Biology, Vol. 8, Issue 1 https://doi.org/10.1038/nchembio.736	journal	December 2011
Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different Lindahl, M.; Florencio, F. J. Proceedings of the National Academy of Sciences, Vol. 100, Issue 26, p. 16107-16112 https://doi.org/10.1073/pnas.2534397100	journal	December 2003
Dating the cyanobacterial ancestor of the chloroplast Falcón, Luisa I.; Magallón, Susana; Castillo, Amanda The ISME Journal, Vol. 4, Issue 6 https://doi.org/10.1038/ismej.2010.2	journal	March 2010
Cyanobacteria: an emerging source for drug discovery Singh, Rahul Kunwar; Tiwari, Shree Prakash; Rai, Ashwani K. The Journal of Antibiotics, Vol. 64, Issue 6 https://doi.org/10.1038/ja.2011.21	journal	April 2011
Detailing the optimality of photosynthesis in cyanobacteria through systems biology analysis Nogales, J.; Gudmundsson, S.; Knight, E. M. Proceedings of the National Academy of Sciences, Vol. 109, Issue 7 https://doi.org/10.1073/pnas.1117907109	journal	January 2012
Bioengineering of carbon fixation, biofuels, and biochemicals in cyanobacteria and plants Rosgaard, Lisa; de Porcellinis, Alice Jara; Jacobsen, Jacob H. Journal of Biotechnology, Vol. 162, Issue 1 https://doi.org/10.1016/j.jbiotec.2012.05.006	journal	November 2012
Redox Control of psbA Gene Expression in the Cyanobacterium Synechocystis PCC 6803. Involvement of the Cytochrome b ₆ /f Complex Alfonso, Miguel; Perewoska, Irène; Kirilovsky, Diana Plant Physiology, Vol. 122, Issue 2 https://doi.org/10.1104/pp.122.2.505	journal	February 2000
Essential Role of Glutathione in Acclimation to Environmental and Redox Perturbations in the Cyanobacterium Synechocystis sp. PCC 6803 Cameron, Jeffrey C.; Pakrasi, Himadri B. Plant Physiology, Vol. 154, Issue 4 https://doi.org/10.1104/pp.110.162990	journal	October 2010
Potential regulation of gene expression in photosynthetic cells by redox and energy state: approaches towards better understanding Pfannschmidt, T.; Bräutigam, K.; Wagner, R. Annals of Botany, Vol. 103, Issue 4 https://doi.org/10.1093/aob/mcn081	journal	May 2008
The Glutathione/Glutaredoxin System Is Essential for Arsenate Reduction in Synechocystis sp. Strain PCC 6803 Lopez-Maury, L.; Sanchez-Riego, A. M.; Reyes, J. C. Journal of Bacteriology, Vol. 191, Issue 11 https://doi.org/10.1128/JB.01798-08	journal	March 2009
Resin-assisted enrichment of thiols as a general strategy for proteomic profiling of cysteine-based reversible modifications Guo, Jia; Gaffrey, Matthew J.; Su, Dian Nature Protocols, Vol. 9, Issue 1 https://doi.org/10.1038/nprot.2013.161	journal	December 2013
Disulphide proteomes and interactions with thioredoxin on the track towards understanding redox regulation in chloroplasts and cyanobacteria Lindahl, Marika; Kieselbach, Thomas Journal of Proteomics, Vol. 72, Issue 3 https://doi.org/10.1016/j.jprot.2009.01.003	journal	April 2009
Protein S-nitrosylation: a physiological signal for neuronal nitric oxide Jaffrey, Samie R.; Erdjument-Bromage, Hediye; Ferris, Christopher D. Nature Cell Biology, Vol. 3, Issue 2 https://doi.org/10.1038/35055104	journal	January 2001
Thiol redox proteomics seen with fluorescent eyes: The detection of cysteine oxidative modifications by fluorescence derivatization and 2-DE Izquierdo-Álvarez, Alicia; Martínez-Ruiz, Antonio Journal of Proteomics, Vol. 75, Issue 2 https://doi.org/10.1016/j.jprot.2011.09.013	journal	December 2011
Use of Dimedone-Based Chemical Probes for Sulfenic Acid Detection Nelson, Kimberly J.; Klomsiri, Chananat; Codreanu, Simona G. Methods in Enzymology https://doi.org/10.1016/S0076-6879(10)73004-4	book	January 2010
Protein Thiol Modifications Visualized In Vivo Leichert, Lars I.; Jakob, Ursula PLoS Biology, Vol. 2, Issue 11 https://doi.org/10.1371/journal.pbio.0020333	journal	October 2004
Quantifying changes in the thiol redox proteome upon oxidative stress in vivo Leichert, L. I.; Gehrke, F.; Gudiseva, H. V. Proceedings of the National Academy of Sciences, Vol. 105, Issue 24 https://doi.org/10.1073/pnas.0707723105	journal	February 2008
Isotope-coded Affinity Tag Approach to Identify and Quantify Oxidant-sensitive Protein Thiols Sethuraman, Mahadevan; McComb, Mark E.; Heibeck, Tyler Molecular & Cellular Proteomics, Vol. 3, Issue 3 https://doi.org/10.1074/mcp.T300011-MCP200	journal	January 2004
Proteome-wide Quantification and Characterization of Oxidation-Sensitive Cysteines in Pathogenic Bacteria Deng, Xin; Weerapana, Eranthie; Ulanovskaya, Olesya Cell Host & Microbe, Vol. 13, Issue 3 https://doi.org/10.1016/j.chom.2013.02.004	journal	March 2013
Quantitative reactivity profiling predicts functional cysteines in proteomes Weerapana, Eranthie; Wang, Chu; Simon, Gabriel M. Nature, Vol. 468, Issue 7325 https://doi.org/10.1038/nature09472	journal	November 2010
Live Cell Chemical Profiling of Temporal Redox Dynamics in a Photoautotrophic Cyanobacterium Sadler, Natalie C.; Melnicki, Matthew R.; Serres, Margrethe H. ACS Chemical Biology, Vol. 9, Issue 1 https://doi.org/10.1021/cb400769v	journal	October 2013
Mass Spectrometry-Based Quantitative Proteomics for Dissecting Multiplexed Redox Cysteine Modifications in Nitric Oxide-Protected Cardiomyocyte Under Hypoxia Pan, Kuan-Ting; Chen, Yi-Yun; Pu, Tsung-Hsien Antioxidants & Redox Signaling, Vol. 20, Issue 9 https://doi.org/10.1089/ars.2013.5326	journal	March 2014
Proteomic Quantification and Site-Mapping of S -Nitrosylated Proteins Using Isobaric iodoTMT Reagents Qu, Zhe; Meng, Fanjun; Bomgarden, Ryan D. Journal of Proteome Research, Vol. 13, Issue 7 https://doi.org/10.1021/pr401179v	journal	June 2014
Identification and Quantification of S-Nitrosylation by Cysteine Reactive Tandem Mass Tag Switch Assay Murray, Christopher I.; Uhrigshardt, Helge; O'Meally, Robert N. Molecular & Cellular Proteomics, Vol. 11, Issue 2 https://doi.org/10.1074/mcp.M111.013441	journal	November 2011
High-Throughput Comparative Proteome Analysis Using a Quantitative Cysteinyl-peptide Enrichment Technology Liu, Tao; Qian, Wei-Jun; Strittmatter, Eric F. Analytical Chemistry, Vol. 76, Issue 18 https://doi.org/10.1021/ac049485q	journal	September 2004
Proteomic analysis of S-nitrosylation and denitrosylation by resin-assisted capture Forrester, Michael T.; Thompson, J. Will; Foster, Matthew W. Nature Biotechnology, Vol. 27, Issue 6 https://doi.org/10.1038/nbt.1545	journal	May 2009
Simple Conditions for Growth of Unicellular Blue-Green Algae on Plates Allen, Mary Mennes Journal of Phycology, Vol. 4, Issue 1 https://doi.org/10.1111/j.1529-8817.1968.tb04667.x	journal	March 1968
Enhanced Detection of Low Abundance Human Plasma Proteins Using a Tandem IgY12-SuperMix Immunoaffinity Separation Strategy Qian, Wei-Jun; Kaleta, David T.; Petritis, Brianne O. Molecular & Cellular Proteomics, Vol. 7, Issue 10 https://doi.org/10.1074/mcp.M800008-MCP200	journal	July 2008
Chemically Etched Open Tubular and Monolithic Emitters for Nanoelectrospray Ionization Mass Spectrometry Kelly, Ryan T.; Page, Jason S.; Luo, Quanzhou Analytical Chemistry, Vol. 78, Issue 22, p. 7796-7801 https://doi.org/10.1021/ac061133r	journal	November 2006
Spectral Probabilities and Generating Functions of Tandem Mass Spectra: A Strike against Decoy Databases Kim, Sangtae; Gupta, Nitin; Pevzner, Pavel A. Journal of Proteome Research, Vol. 7, Issue 8 https://doi.org/10.1021/pr8001244	journal	August 2008
Probability-Based Evaluation of Peptide and Protein Identifications from Tandem Mass Spectrometry and SEQUEST Analysis: The Human Proteome Qian, Wei-Jun; Liu, Tao; Monroe, Matthew E. Journal of Proteome Research, Vol. 4, Issue 1 https://doi.org/10.1021/pr0498638	journal	February 2005
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A. Nature Protocols, Vol. 4, Issue 1 https://doi.org/10.1038/nprot.2008.211	journal	December 2008
Enzymatic assembly of DNA molecules up to several hundred kilobases Gibson, Daniel G.; Young, Lei; Chuang, Ray-Yuan Nature Methods, Vol. 6, Issue 5, p. 343-345 https://doi.org/10.1038/nmeth.1318	journal	April 2009
Quantitative site-specific reactivity profiling of S-nitrosylation in mouse skeletal muscle using cysteinyl peptide enrichment coupled with mass spectrometry Su, Dian; Shukla, Anil K.; Chen, Baowei Free Radical Biology and Medicine, Vol. 57 https://doi.org/10.1016/j.freeradbiomed.2012.12.010	journal	April 2013
Proteomic identification and quantification of S-glutathionylation in mouse macrophages using resin-assisted enrichment and isobaric labeling Su, Dian; Gaffrey, Matthew J.; Guo, Jia Free Radical Biology and Medicine, Vol. 67 https://doi.org/10.1016/j.freeradbiomed.2013.12.004	journal	February 2014
Tandem Mass Tags: A Novel Quantification Strategy for Comparative Analysis of Complex Protein Mixtures by MS/MS Thompson, Andrew; Schäfer, Jürgen; Kuhn, Karsten Analytical Chemistry, Vol. 75, Issue 8 https://doi.org/10.1021/ac0262560	journal	April 2003
Targeted Quantitation of Site-Specific Cysteine Oxidation in Endogenous Proteins Using a Differential Alkylation and Multiple Reaction Monitoring Mass Spectrometry Approach Held, Jason M.; Danielson, Steven R.; Behring, Jessica B. Molecular & Cellular Proteomics, Vol. 9, Issue 7 https://doi.org/10.1074/mcp.M900643-MCP200	journal	March 2010
Quantitative In Vivo Redox Sensors Uncover Oxidative Stress as an Early Event in Life Knoefler, Daniela; Thamsen, Maike; Koniczek, Martin Molecular Cell, Vol. 47, Issue 5 https://doi.org/10.1016/j.molcel.2012.06.016	journal	September 2012
Inhibitors in the functional dissection of the photosynthetic electron transport system Trebst, Achim Photosynthesis Research, Vol. 92, Issue 2 https://doi.org/10.1007/s11120-007-9213-x	journal	July 2007
Structural Basis of Redox Signaling in Photosynthesis: Structure and Function of Ferredoxin:thioredoxin Reductase and Target Enzymes Dai, Shaodong; Johansson, Kenth; Miginiac-Maslow, Myroslawa Photosynthesis Research, Vol. 79, Issue 3 https://doi.org/10.1023/B:PRES.0000017194.34167.6d	journal	January 2004
Redox Proteomics: Chemical Principles, Methodological Approaches and Biological/Biomedical Promises Bachi, Angela; Dalle-Donne, Isabella; Scaloni, Andrea Chemical Reviews, Vol. 113, Issue 1 https://doi.org/10.1021/cr300073p	journal	November 2012
Diurnal Rhythms Result in Significant Changes in the Cellular Protein Complement in the Cyanobacterium Cyanothece 51142 Stöckel, Jana; Jacobs, Jon M.; Elvitigala, Thanura R. PLoS ONE, Vol. 6, Issue 2 https://doi.org/10.1371/journal.pone.0016680	journal	February 2011
Genome-Wide Dynamic Transcriptional Profiling of the Light-to-Dark Transition in Synechocystis sp. Strain PCC 6803 Gill, R. T.; Katsoulakis, E.; Schmitt, W. Journal of Bacteriology, Vol. 184, Issue 13 https://doi.org/10.1128/JB.184.13.3671-3681.2002	journal	July 2002
DNA Microarray Analysis of Redox-Responsive Genes in the Genome of the Cyanobacterium Synechocystis sp. Strain PCC 6803 Hihara, Yukako; Sonoike, Kintake; Kanehisa, Minoru Journal of Bacteriology, Vol. 185, Issue 5 https://doi.org/10.1128/JB.185.5.1719-1725.2003	journal	March 2003
Membrane proteins from the cyanobacteriumSynechocystis sp. PCC 6803 interacting with thioredoxin Mata-Cabana, Alejandro; Florencio, Francisco J.; Lindahl, Marika PROTEOMICS, Vol. 7, Issue 21 https://doi.org/10.1002/pmic.200700410	journal	November 2007
Selecting thioredoxins for disulphide proteomics: Target proteomes of three thioredoxins from the cyanobacterium Synechocystis sp. PCC 6803 Pérez-Pérez, María Esther; Florencio, Francisco J.; Lindahl, Marika PROTEOMICS, Vol. 6, Issue S1 https://doi.org/10.1002/pmic.200500215	journal	April 2006
The Disulfide Proteome and Other Reactive Cysteine Proteomes: Analysis and Functional Significance Lindahl, Marika; Mata-Cabana, Alejandro; Kieselbach, Thomas Antioxidants & Redox Signaling, Vol. 14, Issue 12 https://doi.org/10.1089/ars.2010.3551	journal	June 2011
Redox Regulation of Thylakoid Protein Kinases and Photosynthetic Gene Expression Rochaix, Jean-David Antioxidants & Redox Signaling, Vol. 18, Issue 16 https://doi.org/10.1089/ars.2012.5110	journal	June 2013
Redox Signaling in the Chloroplast: The Ferredoxin/Thioredoxin System Schürmann, Peter Antioxidants & Redox Signaling, Vol. 5, Issue 1 https://doi.org/10.1089/152308603321223559	journal	February 2003
Bifunctional enzyme FBPase/SBPase is essential for photoautotrophic growth in cyanobacterium Synechocystis sp. PCC 6803 Yan, Chunlan; Xu, Xudong Progress in Natural Science, Vol. 18, Issue 2 https://doi.org/10.1016/j.pnsc.2007.09.003	journal	February 2008
Regulation of CO2 assimilation in oxygenic photosynthesis: The ferredoxin/thioredoxin system Buchanan, Bob B. Archives of Biochemistry and Biophysics, Vol. 288, Issue 1 https://doi.org/10.1016/0003-9861(91)90157-E	journal	July 1991
Molecular Characterization and Redox Regulation of Phosphoribulokinase from the Cyanobacterium Synechococcus sp. PCC 7942 Kobayashi, Daisuke; Tamoi, Masahiro; Iwaki, Toshio Plant and Cell Physiology, Vol. 44, Issue 3 https://doi.org/10.1093/pcp/pcg048	journal	March 2003
Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria Balmer, Y.; Vensel, W. H.; Tanaka, C. K. Proceedings of the National Academy of Sciences, Vol. 101, Issue 8 https://doi.org/10.1073/pnas.0308583101	journal	February 2004
Thiol-Based Redox Switches in Eukaryotic Proteins Brandes, Nicolas; Schmitt, Sebastian; Jakob, Ursula Antioxidants & Redox Signaling, Vol. 11, Issue 5 https://doi.org/10.1089/ars.2008.2285	journal	May 2009
Structure of NADP-dependent glyceraldehyde-3-phosphate dehydrogenase from Synechococcus PCC7942 complexed with NADP Kitatani, Tomoya; Nakamura, Yoshihiro; Wada, Kei Acta Crystallographica Section F Structural Biology and Crystallization Communications, Vol. 62, Issue 4 https://doi.org/10.1107/S1744309106007378	journal	March 2006
Localization and function of ferredoxin:NADP+ reductase bound to the phycobilisomes of Synechocystis van Thor, J. J. The EMBO Journal, Vol. 18, Issue 15 https://doi.org/10.1093/emboj/18.15.4128	journal	August 1999
Dark inactivation of ferredoxin-NADP reductase and cyclic electron flow under far-red light in sunflower leaves Talts, Eero; Oja, Vello; Rämma, Heikko Photosynthesis Research, Vol. 94, Issue 1 https://doi.org/10.1007/s11120-007-9224-7	journal	July 2007
The role of cysteine residues of spinach ferredoxin-NADP+ reductase as assessed by site-directed mutagenesis Aliverti, Alessandro; Piubelli, Luciano; Zanetti, Giuliana Biochemistry, Vol. 32, Issue 25 https://doi.org/10.1021/bi00076a010	journal	June 1993
Peroxiredoxins in Plants and Cyanobacteria Dietz, Karl-Josef Antioxidants & Redox Signaling, Vol. 15, Issue 4 https://doi.org/10.1089/ars.2010.3657	journal	August 2011
Peroxiredoxins are conserved markers of circadian rhythms Edgar, Rachel S.; Green, Edward W.; Zhao, Yuwei Nature, Vol. 485, Issue 7399 https://doi.org/10.1038/nature11088	journal	May 2012
Response to Oxidative Stress Involves a Novel Peroxiredoxin Gene in the Unicellular Cyanobacterium Synechocystis sp. PCC 6803 Kobayashi, Mari; Ishizuka, Tomokazu; Katayama, Mitsunori Plant and Cell Physiology, Vol. 45, Issue 3 https://doi.org/10.1093/pcp/pch034	journal	March 2004
A Comprehensive Analysis of the Peroxiredoxin Reduction System in the Cyanobacterium Synechocystis sp. Strain PCC 6803 Reveals that All Five Peroxiredoxins Are Thioredoxin Dependent Perez-Perez, M. E.; Mata-Cabana, A.; Sanchez-Riego, A. M. Journal of Bacteriology, Vol. 191, Issue 24 https://doi.org/10.1128/JB.00831-09	journal	October 2009
Redox regulation of chloroplastic glucose-6-phosphate dehydrogenase: A new role for f-type thioredoxin Née, Guillaume; Zaffagnini, Mirko; Trost, Paolo FEBS Letters, Vol. 583, Issue 17 https://doi.org/10.1016/j.febslet.2009.07.035	journal	July 2009
A comparison of gene organization in the zwf region of the genomes of the cyanobacteria Synechococcus sp. PCC 7942 and Anabaena sp. PCC 7120 Newman, Julie; Karakaya, Haydar; Scanlan, David J. FEMS Microbiology Letters, Vol. 133, Issue 1-2 https://doi.org/10.1111/j.1574-6968.1995.tb07882.x	journal	November 1995
The Unique Cyanobacterial Protein OpcA Is an Allosteric Effector of Glucose-6-phosphate Dehydrogenase in Nostoc punctiforme ATCC 29133 Hagen, Kari D.; Meeks, John C. Journal of Biological Chemistry, Vol. 276, Issue 15 https://doi.org/10.1074/jbc.M010472200	journal	January 2001
Quantitative Phosphoproteomics Reveals Widespread Full Phosphorylation Site Occupancy During Mitosis Olsen, J. V.; Vermeulen, M.; Santamaria, A. Science Signaling, Vol. 3, Issue 104 https://doi.org/10.1126/scisignal.2000475	journal	January 2010
Integrated proteomic analysis of post-translational modifications by serial enrichment Mertins, Philipp; Qiao, Jana W.; Patel, Jinal Nature Methods, Vol. 10, Issue 7 https://doi.org/10.1038/nmeth.2518	journal	June 2013
Proteomic Analysis of Lysine Acetylation Sites in Rat Tissues Reveals Organ Specificity and Subcellular Patterns Lundby, Alicia; Lage, Kasper; Weinert, Brian T. Cell Reports, Vol. 2, Issue 2 https://doi.org/10.1016/j.celrep.2012.07.006	journal	August 2012
Redox Control of the Activity of Phosphoglycerate Kinase in Synechocystis sp. PCC6803 Tsukamoto, Yu; Fukushima, Yuriko; Hara, Satoshi Plant and Cell Physiology, Vol. 54, Issue 4 https://doi.org/10.1093/pcp/pct002	journal	January 2013
Protochlorophyllide oxidoreductase: A homology model examined by site-directed mutagenesis Townley, Helen E.; Sessions, Richard B.; Clarke, Anthony R. Proteins: Structure, Function, and Genetics, Vol. 44, Issue 3 https://doi.org/10.1002/prot.1098	journal	January 2001

Similar Records

Global Proteomics Reveal An Atypical Strategy for Carbon/Nitrogen Assimilation by a Cyanobacterium Under Diverse Environmental Perturbations

Journal Article · Wed Dec 01 00:00:00 EST 2010 · Molecular & Cellular Proteomics. MCP, 9(12):2678-89 · OSTI ID:1640887

Wegener, Kimberly M; Singh, Abhay K; Jacobs, Jon M; +8 more

Recapitulating the Structural Evolution of Redox Regulation in Adenosine 5′-Phosphosulfate Kinase from Cyanobacteria to Plants

Journal Article · Thu Aug 20 00:00:00 EDT 2015 · Journal of Biological Chemistry · OSTI ID:1640887

Herrmann, Jonathan; Nathin, David; Lee, Soon Goo; +2 more

Resin Assisted Capture Coupled with Isobaric Tandem Mass Tag Labeling for Multiplexed Quantification of Protein Thiol Oxidation

Journal Article · Mon Jun 21 00:00:00 EDT 2021 · Journal of Visualized Experiments (JoVE) · OSTI ID:1640887

Gaffrey, Matthew J.; Day, Nicholas J.; Li, Xiaolu; +1 more

Related Subjects

redox proteomics
photosynthesis
Synechocystis 6803
resin assisted enrichment
protein thiols
thiol oxidation
thiol redox switches

Title: Proteome-wide Light/Dark Modulation of Thiol Oxidation in Cyanobacteria Revealed by Quantitative Site-Specific Redox Proteomics

Citation Formats

References (76)

Similar Records

Related Subjects