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Plant Biol (Stuttg) 2006; 8(4): 407-418
DOI: 10.1055/s-2006-923961
Review Article

Georg Thieme Verlag Stuttgart KG · New York

Concepts and Approaches Towards Understanding the Cellular Redox Proteome

E. Ströher1 , K.-J. Dietz1
  • 1Faculty of Biology - W5-134, Bielefeld University, Universitätsstraße 25, 33501 Bielefeld, Germany
Weitere Informationen

Publikationsverlauf

Received: September 23, 2005

Accepted: January 25, 2006

Publikationsdatum:
11. Mai 2006 (online)

   Lizenzen und Reprints

Abstract

The physiological activity of a significant subset of cell proteins is modified by the redox state of regulatory thiols. The cellular redox homeostasis depends on the balance between oxidation of thiols through oxygen and reactive oxygen species and reduction by thiol-disulfide transfer reactions. Novel and improved methodology has been designed during recent years to address the level of thiol/disulfide regulation on a genome-wide scale. The approaches are either based on gel electrophoresis or on chromatographic techniques coupled to high end mass spectrometry. The review addresses diagonal 2D‐SDS-PAGE, targeted identification of specific redox-interactions, affinity chromatography with thioredoxins and glutaredoxins, gel-based and non-gel based labelling techniques with fluorophores (such as Cy3, Cy5, ICy), radioisotopes, or with isotope-coded affinity tags (ICAT), differential gel electrophoresis (DIGE) and combined fractional diagonal chromatography (COFRADIC). The extended methodological repertoire promises fast and new insight into the intricate regulation network of the redox proteome of animals, bacteria, and plants.

Key words

2D gel electrophoresis - affinity chromatography - protein thiol - redox proteome - redox regulation - thioredoxin

References

  • 1 Anderson L. E., Manabe K.. Disulfide-linked peptides in the chloroplast thylakoid membrane.  Biochimica et Biophysica Acta. (1979);  579 1-9
    PubMedGoogle Scholar
  • 2 Apel K., Hirt H.. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction.  Annual Review of Plant Biology. (2004);  55 373-399
    CrossrefPubMedGoogle Scholar
  • 3 Baier M., Dietz K. J.. Chloroplasts as source and target of cellular redox regulation: a discussion on chloroplast redox signals in the context of plant physiology.  Journal of Experimental Botany. (2005);  56 1449-1462
    CrossrefPubMedGoogle Scholar
  • 4 Balmer Y., Koller A., del Val G., Manieri W., Schürmann P., Buchanan B. B.. Proteomics gives insight into the regulatory function of chloroplast thioredoxins.  Proceedings of the National Academy of Sciences of the USA. (2003);  100 370-375
    CrossrefPubMedGoogle Scholar
  • 6 Balmer Y., Vensel W. H., Tanaka C. K., Hurkman W. J., Gelhaye E., Rouhier N., Jacquot J. P., Manieri W., Schürmann P., Droux M., Buchanan B. B.. Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria.  Proceedings of the National Academy of Sciences of the USA. (2004 a);  101 2642-2647
    CrossrefPubMedGoogle Scholar
  • 5 Balmer Y., Koller A., del Val G., Schürmann P., Buchanan B. B.. Proteomics uncovers proteins interacting electrostatically with thioredoxin in chloroplasts.  Photosynthesis Research. (2004 b);  79 275-280
    CrossrefPubMedGoogle Scholar
  • 7 Brandes H. K., Larimer F. W., Geck M. K., Stringer C. D., Schürmann P., Hartman F. C.. Direct identification of the primary nucleophile of thioredoxin f.  Journal of Biological Chemistry. (1993);  268 18411-18414
    PubMedGoogle Scholar
  • 8 Buchanan B. B., Balmer Y.. Redox regulation: a broadening horizon.  Annual Review of Plant Biology. (2005);  56 187-220
    CrossrefPubMedGoogle Scholar
  • 9 Capitani G., Markovic-Housley Z., DelVal G., Morris M., Jansonius J. N., Schürmann P.. Crystal structures of two functionally different thioredoxins in spinach chloroplasts.  Journal of Molecular Biology. (2000);  302 135-154
    CrossrefPubMedGoogle Scholar
  • 10 Chan H. L., Gharbi S., Gaffney P. R., Cramer R., Waterfield M. D., Timms J. F.. Proteomic analysis of redox- and ErbB2-dependent changes in mammary luminal epithelial cells using cysteine- and lysine-labelling two-dimensional difference gel electrophoresis.  Proteomics. (2005);  5 2908-2926
    CrossrefPubMedGoogle Scholar
  • 11 Collin V., Issakidis-Bourguet E., Marchand C., Hirasawa M., Lancelin J. M., Knaff D. B., Miginiac-Maslow M.. The Arabidopsis plastidial thioredoxins: new functions and new insights into specificity.  Journal of Biological Chemistry. (2003);  278 23747-23752
    CrossrefPubMedGoogle Scholar
  • 12 Collin V., Lamkemeyer P., Miginiac-Maslow M., Hirasawa M., Knaff D. B., Dietz K. J., Issakidis-Bourguet E.. Characterization of plastidial thioredoxins from Arabidopsis belonging to the new y-type.  Plant Physiology. (2004);  136 4088-4095
    CrossrefPubMedGoogle Scholar
  • 13 Cummings R. C., Andon N. L., Haynes P. A., Park M., Fischer W. H., Schubert D.. Protein disulfide bond formation in the cytoplasm during oxidative stress.  The Journal of Biological Chemistry. (2004);  279 21749-21758
    CrossrefPubMedGoogle Scholar
  • 14 del Val G., Yee B. C., Lozano R. M., Buchanan B. B., Ermel R. W., Lee Y. M., Frick O. L.. Thioredoxin treatment increases digestibility and lowers allergenicity of milk.  Journal of Allergy and Clinical Immunology. (1999);  103 690-697
    CrossrefPubMedGoogle Scholar
  • 15 Dietz K. J.. Plant peroxiredoxins.  Annual Review of Plant Biology. (2003);  54 93-107
    CrossrefPubMedGoogle Scholar
  • 16 Dietz K. J.. Plant thiol enzymes and thiol homeostasis in relation to thiol-dependent redox regulation and oxidative stress. Smirnoff, N., ed. Antioxidants and Reactive Oxygen Species in Plants. Oxford; Blackwell Publishing (2005): 25-52
    Google Scholar
  • 17 Dietz K. J., Link G., Pistorius E. K., Scheibe R.. Redox regulation in oxigenic photosynthesis.  Progress in Botany. (2002);  63 207-245
    PubMedGoogle Scholar
  • 18 Finkemeier I., Goodman M., Lamkemeyer P., Kandlbinder A., Sweetlove L. J., Dietz K. J.. The mitochondrial type II peroxiredoxin F is essential for redox homeostasis and root growth of Arabidopsis thaliana under stress.  Journal of Biological Chemistry. (2005);  280 12168-12180
    PubMedGoogle Scholar
  • 19 Gelhaye E., Rouhier N., Gerard J., Jolivet Y., Gualberto J., Navrot N., Ohlsson P. I., Wingsle G., Hirasawa M., Knaff D. B., Wang H., Dizengremel P., Meyer Y., Jacquot J. P.. A specific form of thioredoxin h occurs in plant mitochondria and regulates the alternative oxidase.  Proceedings of the National Academy of Sciences of the USA. (2004);  101 14545-14550
    CrossrefPubMedGoogle Scholar
  • 20 Gelhaye E., Rouhier N., Navrot N., Jacquot J. P.. The plant thioredoxin system.  Cellular and Molecular Life Sciences. (2005);  62 24-35
    CrossrefPubMedGoogle Scholar
  • 21 Gevaert K., Ghesquiere B., Staes A., Martens L., Van Damme J., Thomas G. R., Vandekerckhove J.. Reversible labelling of cysteine-containing peptides allows their specific chromatographic isolation for non-gel proteome studies.  Proteomics. (2004);  4 897-908
    CrossrefPubMedGoogle Scholar
  • 22 Gilles-Gonzalez M. A., Gonzalez G.. Heme-based sensors: defining characteristics, recent developments, and regulatory hypotheses.  Journal of Inorganic Biochemistry. (2005);  99 1-22
    CrossrefPubMedGoogle Scholar
  • 23 Gobin P., Ng P. K. W., Buchanan B. B., Kobrehel K.. Sulfhydryl-disulfide changes in proteins of developing wheat grain.  Plant Physiology and Biochemistry. (1997);  35 777-783
    PubMedGoogle Scholar
  • 24 Gygi S. P., Rist B., Gerber S. A., Turecek F., Gelb M. H., Aebersold R.. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags.  Nature Biotechnology. (1999);  17 994-999
    PubMedGoogle Scholar
  • 25 Hofmann B., Hecht H. J., Flohe L.. Peroxiredoxins.  Biological Chemistry. (2002);  383 347-364
    CrossrefPubMedGoogle Scholar
  • 26 Holtzapffel R. C., Castelli J., Finnegan P. M., Millar A. H., Whelan J., Day D. A.. A tomato alternative oxidase protein with altered regulatory properties.  Biochimica et Biophysica Acta. (2003);  1606 153-162
    PubMedGoogle Scholar
  • 27 Jacquot J. P., Lancelin J.-M., Meyer Y.. Transley review. No. 94. Thioredoxins: structure and function in plant cells.  New Phytologist. (1997);  136 543-570
    CrossrefPubMedGoogle Scholar
  • 28 Jansson S., Andersen B., Scheller H. V.. Nearest-neighbor analysis of higher-plant photosystem I holocomplex.  Plant Physiology. (1996);  112 409-420
    CrossrefPubMedGoogle Scholar
  • 29 Katti S. K., Robbins A. H., Yang Y., Wells W. W.. Crystal structure of thioltransferase at 2.2 Å resolution.  Protein Science. (1995);  4 1998-2005
    PubMedGoogle Scholar
  • 30 Kobrehel K., Wong J. H., Balogh A., Kiss F., Yee B. C., Buchanan B. B.. Specific reduction of wheat storage proteins by thioredoxin h.  Plant Physiology. (1992);  99 919-924
    PubMedGoogle Scholar
  • 31 König J., Baier M., Horling F., Kahmann U., Harris G., Schürmann P., Dietz K. J.. The plant-specific function of 2-Cys peroxiredoxin-mediated detoxification of peroxides in the redox-hierarchy of photosynthetic electron flux.  Proceedings of the National Academy of Sciences of the USA. (2002);  99 5738-5743
    CrossrefPubMedGoogle Scholar
  • 32 Kumar J. K., Tabor S., Richardson C. C.. Proteomic analysis of thioredoxin-targeted proteins in Escherichia coli.  Proceedings of the National Academy of Sciences of the USA. (2004);  101 3759-3764
    CrossrefPubMedGoogle Scholar
  • 33 Kumar R. A., Koc A., Cerny R. L., Gladyshev V. N.. Reaction mechanism, evolutionary analysis, and role of zinc in Drosophila methionine-R-sulfoxide reductase.  Journal of Biological Chemistry. (2002);  277 37527-37535
    CrossrefPubMedGoogle Scholar
  • 34 Laloi C., Rayapuram N., Chartier Y., Grienenberger J. M., Bonnard G., Meyer Y.. Identification and characterization of a mitochondrial thioredoxin system in plants.  Proceedings of the National Academy of Sciences of the USA. (2001);  98 14144-14149
    CrossrefPubMedGoogle Scholar
  • 35 Lemaire S. D., Guillon B., Le Marechal P., Keryer E., Miginiac-Maslow M., Decottignies P.. New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii.  Proceedings of the National Academy of Sciences of the USA. (2004);  101 7475-7480
    CrossrefPubMedGoogle Scholar
  • 36 Lindahl M., Florencio FJ.. Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different.  Proceedings of the National Academy of Sciences of the USA. (2003);  100 16107-16112
    CrossrefPubMedGoogle Scholar
  • 37 Maeda K., Finnie C., Svensson B.. Cy5 maleimide labelling for sensitive detection of free thiols in native protein extracts: identification of seed proteins targeted by barley thioredoxin h isoforms.  Biochemical Journal. (2004);  378 497-507
    CrossrefPubMedGoogle Scholar
  • 38 Maeda K., Finnie C., Svensson B.. Identification of thioredoxin h-reducible disulphides in proteomes by differential labelling of cysteines: insight into recognition and regulation of proteins in barley seeds by thioredoxin h.  Proteomics. (2005);  5 1634-1644
    CrossrefPubMedGoogle Scholar
  • 39 Marchand C., Le Marechal P., Meyer Y., Miginiac-Maslow M., Issakidis-Bourguet E., Decottignies P.. New targets of Arabidopsis thioredoxins revealed by proteomic analysis.  Proteomics. (2004);  4 2696-2706
    CrossrefPubMedGoogle Scholar
  • 40 Marouga R., David S., Hawkins E.. The development of the DIGE system: 2D fluorescence difference gel analysis technology.  Analytical and Bioanalytical Chemistry. (2005);  382 669-678
    CrossrefPubMedGoogle Scholar
  • 41 Marx C., Wong J. H., Buchanan B. B.. Thioredoxin and germinating barley: targets and protein redox changes.  Planta. (2003);  216 454-460
    PubMedGoogle Scholar
  • 42 Matsuo T., Graham D., Patterson B. D., Hockley D. B.. An electrophoretic method to detect cold-induced dissociation of proteins in crude extracts of higher plants.  Analytical Biochemistry. (1994);  223 181-184
    CrossrefPubMedGoogle Scholar
  • 43 Millenaar F. F., Lambers H.. The alternative oxidase: in vivo regulation and function.  Plant Biology. (2003);  5 2-15
    Artikel in Thieme ConnectPubMedGoogle Scholar
  • 44 Miranda-Vizuete A., Sadek C. M., Jimenez A., Krause W. J., Sutovsky P., Oko R.. The mammalian testis-specific thioredoxin system.  Antioxidants and Redox Signaling. (2004);  6 25-40
    CrossrefPubMedGoogle Scholar
  • 45 Mora-Garcia S., Rodriguez-Suarez R., Wolosiuk R. A.. Role of electrostatic interactions on the affinity of thioredoxin for target proteins. Recognition of chloroplast fructose-1,6-bisphosphatase by mutant Escherichia coli thioredoxins.  Journal of Biological Chemistry. (1998);  273 16273-16280
    CrossrefPubMedGoogle Scholar
  • 46 Motohashi K., Kondoh A., Stumpp M. T., Hisabori T.. Comprehensive survey of proteins targeted by chloroplast thioredoxin.  Proceedings of the National Academy of Sciences of the USA. (2001);  98 11224-11229
    CrossrefPubMedGoogle Scholar
  • 47 Narikawa R., Okamoto S., Ikeuchi M., Ohmori M.. Molecular evolution of PAS domain-containing proteins of filamentous cyanobacteria through domain shuffling and domain duplication.  DNA Research. (2004);  11 69-81
    CrossrefPubMedGoogle Scholar
  • 48 Rigaut G., Shevchenko A., Rutz B., Wilm M., Mann M., Seraphin B.. A generic protein purification method for protein complex characterization and proteome exploration.  Nature Biotechnology. (1999);  17 1030-1032
    CrossrefPubMedGoogle Scholar
  • 49 Rouhier N., Gelhaye E., Jacquot J. P.. Glutaredoxin-dependent peroxiredoxin from poplar. Protein-protein interaction and catalytic mechanism.  The Journal of Biological Chemistry. (2002);  277 13609-13614
    CrossrefPubMedGoogle Scholar
  • 50 Rouhier N., Gelhaye E., Jacquot J. P.. Plant glutaredoxins: still mysterious reducing systems.  Cellular and Molecular Life Sciences. (2004);  61 1266-1277
    CrossrefPubMedGoogle Scholar
  • 51 Rouhier N., Villarejo A., Srivastava M., Gelhaye E., Keech O., Droux M., Finkemeier I., Samuelsson G., Dietz K. J., Jacquot J. P., Wingsle G.. Identification of plant glutaredoxin targets.  Antioxidants and Redox Signaling. (2005);  7 919-929
    PubMedGoogle Scholar
  • 52 Sanchez S., Arenas J., Abel A., Criado M. T., Ferreiros C. M.. Analysis of outer membrane protein complexes and heat-modifiable proteins in Neisseria strains using two-dimensional diagonal electrophoresis.  Journal of Proteome Research. (2004);  4 91-95
    PubMedGoogle Scholar
  • 53 Schafer F. Q., Buettner G. R.. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple.  Free Radical Biology and Medicine. (2001);  30 1191-1212
    CrossrefPubMedGoogle Scholar
  • 54 Scheibe R.. Malate valves to balance cellular energy supply.  Physiologia Plantarum. (2004);  120 21-26
    CrossrefPubMedGoogle Scholar
  • 55 Schürmann P.. Redox signaling in the chloroplast: the ferredoxin/thioredoxin system.  Antioxidants and Redox Signaling. (2003);  5 69-78
    PubMedGoogle Scholar
  • 56 Schürmann P., Jacquot J. P.. Plant thioredoxin systems revisited.  Annual Review of Plant Physiology and Plant Molecular Biology. (2000);  51 371-400
    CrossrefPubMedGoogle Scholar
  • 57 Sethuraman M., McComb M. E., Heibeck T., Costello C. E., Cohen R. A.. Isotope-coded affinity tag approach to identify and quantify oxidant-sensitive protein thiols.  Molecular and Cellular Proteomics. (2004 a);  3 273-278
    PubMedGoogle Scholar
  • 58 Sethuraman M., McComb M. E., Huang H., Huang S., Heibeck T., Costello C. E., Cohen R. A.. Isotope-coded affinity tag (ICAT) approach to redox proteomics: identification and quantitation of oxidant-sensitive cysteine thiols in complex protein mixtures.  Journal of Proteome Research. (2004 b);  3 1228-1233
    CrossrefPubMedGoogle Scholar
  • 59 Stork T., Michel K. P., Pistorius E. K., Dietz K. J.. Bioinformatic analysis of the genomes of the cyanobacteria Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942 for the presence of peroxiredoxins and their transcript regulation under stress.  Journal of Experimental Botany. (2005);  56 3193-3206
    CrossrefPubMedGoogle Scholar
  • 60 Taylor B. L., Zhulin I. B.. PAS domains: internal sensors of oxygen, redox potential, and light.  Microbiology and Molecular Biology Reviews. (1999);  63 479-506
    PubMedGoogle Scholar
  • 61 Verdoucq L., Vignols F., Jacquot J. P., Chartier Y., Meyer Y.. In vivo characterization of a thioredoxin h target protein defines a new peroxiredoxin family.  Journal of Biological Chemistry. (1999);  274 19714-19722
    CrossrefPubMedGoogle Scholar
  • 62 Weis M., Cotgreave I. C., Moore G. A., Norbeck K., Moldeus P.. Accessibility of hepatocyte protein thiols to monobromobimane.  Biochimica et Biophysica Acta. (1993);  1176 13-19
    PubMedGoogle Scholar
  • 63 Wong J. H., Balmer Y., Cai N., Tanaka C. K., Vensel W. H., Hurkman W. J., Buchanan B. B.. Unraveling thioredoxin-linked metabolic processes of cereal starchy endosperm using proteomics.  FEBS Letters. (2003);  547 151-156
    CrossrefPubMedGoogle Scholar
  • 65 Wong J. H., Cai N., Tanaka C. K., Vensel W. H., Hurkamn W. J., Buchanan B. B.. Thioredoxin reduction alters the solubility of proteins of wheat starchy endosperm: an early event in cereal germination.  Plant and Cell Physiology. (2004 a);  45 407-415
    CrossrefPubMedGoogle Scholar
  • 64 Wong J. H., Cai N., Balmer Y., Tanaka C. K., Vensel W. H., Hurkman W. J., Buchanan B. B.. Thioredoxin targets of developing wheat seeds identified by complementary proteomic approaches.  Phytochemistry. (2004 b);  65 1629-1640
    CrossrefPubMedGoogle Scholar
  • 66 Xing S. P., Rosso M. G., Zachgo S.. ROXY1, a member of the plant glutaredoxin family, is required for petal development in Arabidopsis thaliana.  Development. (2005);  132 1555-1565
    CrossrefPubMedGoogle Scholar
  • 68 Yano H., Wong J. H., Lee Y. M., Cho M. J., Buchanan B. B.. A strategy for the identification of proteins targeted by thioredoxin.  Proceedings of the National Academy of Sciences of the USA. (2001 a);  98 4794-4799
    CrossrefPubMedGoogle Scholar
  • 67 Yano H., Wong J. H., Cho M. J., Buchanan B. B.. Redox changes accompanying the degradation of seed storage proteins in germinating rice.  Plant and Cell Physiology. (2001 b);  42 879-883
    CrossrefPubMedGoogle Scholar
  • 69 Zhang S., Scheller H. V.. Light-harvesting complex II binds to several small subunits of photosystem I.  Journal of Biological Chemistry. (2003);  279 3180-3187
    CrossrefPubMedGoogle Scholar

K.-J. Dietz

Faculty of Biology - W5-134
Bielefeld University

Universitätsstraße 25

33501 Bielefeld

Germany

eMail: karl-josef.dietz@uni-bielefeld.de

Editor: B. Schulz

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