Regulated spatial organization and sensitivity of cytosolic protein oxidation in Caenorhabditis elegans

Nature Communications

Volumn 5, Issue , 2014, Pages

  Romero Aristizabal, Catalina ^a   Marks, Debora S ^a   Fontana, Walter ^a   Apfeld, Javier ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUFFER; CYSTEINE; DISULFIDE; GLUTATHIONE; INSULIN; PROTEIN; THIOL; OXYGEN; THIOL DERIVATIVE;

GERM CELL; OXIDATION; PROTEIN; REDOX CONDITIONS; SENSOR; SPATIOTEMPORAL ANALYSIS; SULFIDE; THIOL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CHROMATOPHORE; CONTROLLED STUDY; DISULFIDE BOND; GENE INTERACTION; INTRACELLULAR SPACE; NONHUMAN; OXIDATION; OXIDATION REDUCTION POTENTIAL; SENSITIVITY ANALYSIS; SENSOR; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; CYTOSOL; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; METABOLISM; OXIDATION REDUCTION REACTION; PHARYNX; PHYSIOLOGY; TRANSGENE;

CAENORHABDITIS ELEGANS;

ANIMALS; CAENORHABDITIS ELEGANS; CYSTEINE; CYTOSOL; DISULFIDES; GENE EXPRESSION REGULATION; GLUTATHIONE; INSULIN; MICROSCOPY, FLUORESCENCE; OXIDATION-REDUCTION; OXYGEN; PHARYNX; SIGNAL TRANSDUCTION; SULFHYDRYL COMPOUNDS; TRANSGENES;

EID: 84923288540     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms6020     Document Type: Article

References (56)

1. Gilbert, H. F. Molecular and cellular aspects of thiol-disulfide exchange. Adv. Enzymol. Relat. Areas Mol. Biol. 63, 69-172 (1990
2. Gilbert, H. F. Biological disulfides: The third messenger? Modulation of phosphofructokinase activity by thiol/disulfide exchange. J. Biol. Chem. 257, 12086-12091 (1982
3. Corcoran, A. & Cotter, T. G. Redox regulation of protein kinases. FEBS J. 280, 1944-1965 (2013
4. Fuller, W. et al. Regulation of the cardiac sodium pump. Cell. Mol. Life Sci. 70, 1357-1380 (2013
5. Yang, Y., Jin, X. & Jiang, C. S-glutathionylation of ion channels: Insights into the regulation of channel functions, thiol modification crosstalk and mechanosensing. Antioxid. Redox Signal. 6, 937-951 (2013
6. de Keizer, P. L., Burgering, B. M. & Dansen, T. B. Forkhead box o as a sensor, mediator, and regulator of redox signaling. Antioxid. Redox Signal. 14, 1093-1106 (2011
7. Pastore, A. & Piemonte, F. S-Glutathionylation signaling in cell biology: Progress and prospects. Eur. J. Pharm. Sci. 46, 279-292 (2012
8. Sakai, J. et al. Reactive oxygen species-induced actin glutathionylation controls actin dynamics in neutrophils. Immunity 37, 1037-1049 (2012
9. Xiong, Y., Uys, J. D., Tew, K. D. & Townsend, D. M. S-glutathionylation: From molecular mechanisms to health outcomes. Antioxid. Redox Signal. 15, 233-270 (2011
10. Sabens Liedhegner, E. A., Gao, X. H. & Mieyal, J. J. Mechanisms of altered redox regulation in neurodegenerative diseases-focus on S-glutathionylation. Antioxid. Redox Signal. 16, 543-566 (2012
11. Mieyal, J. J., Gallogly, M. M., Qanungo, S., Sabens, E. A. & Shelton, M. D. Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid. Redox Signal. 10, 1941-1988 (2008
12. Sanchez-Gomez, F. J., Espinosa-Diez, C., Dubey, M., Dikshit, M. & Lamas, S. S-glutathionylation: Relevance in diabetes and potential role as a biomarker. Biol. Chem. 394, 1263-1280 (2013
13. Holmgren, A. Thioredoxin and glutaredoxin systems. J. Biol. Chem. 264, 13963-13966 (1989
14. Meyer, Y., Buchanan, B. B., Vignols, F. & Reichheld, J. P. Thioredoxins and glutaredoxins: Unifying elements in redox biology. Annu Rev. Genet. 43, 335-367 (2009
15. Jones, D. P. Radical-free biology of oxidative stress. Am J. Physiol. Cell Physiol. 295, C849-C868 (2008
16. Moosmann, B. & Behl, C. Mitochondrially encoded cysteine predicts animal lifespan. Aging Cell 7, 32-46 (2008
17. Meyer, A. J. & Dick, T. P. Fluorescent protein-based redox probes. Antioxid. Redox Signal. 13, 621-650 (2010
18. Meyer, A. J. et al. Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J. 52, 973-986 (2007
19. Schwarzlander, M. et al. Confocal imaging of glutathione redox potential in living plant cells. J. Microsc. 231, 299-316 (2008
20. Ostergaard, H., Tachibana, C. & Winther, J. R. Monitoring disulfide bond formation in the eukaryotic cytosol. J. Cell Biol. 166, 337-345 (2004
21. Gutscher, M. et al. Real-time imaging of the intracellular glutathione redox potential. Nat. Methods 5, 553-559 (2008
22. Albrecht, S. C., Barata, A. G., Grosshans, J., Teleman, A. A. & Dick, T. P. In vivo mapping of hydrogen peroxide and oxidized glutathione reveals chemical and regional specificity of redox homeostasis. Cell Metab. 14, 819-829 (2011
23. Cannon, M. B. & Remington, S. J. Re-engineering redox-sensitive green fluorescent protein for improved response rate. Protein Sci. 15, 45-57 (2006
24. Hanson, G. T. et al. Investigating mitochondrial redox potential with redoxsensitive green fluorescent protein indicators. J. Biol. Chem. 279, 13044-13053 (2004
25. Kosower, N. S. & Kosower, E. M. Diamide: An oxidant probe for thiols. Methods Enzymol. 251, 123-133 (1995
26. Liao, V. H. & Yu, C. W. Caenorhabditis elegans gcs-1 confers resistance to arsenic-induced oxidative stress. Biometals 18, 519-528 (2005
27. Mango, S. E. The C. elegans pharynx: A model for organogenesis. WormBook 1-26 (2007
28. Honda, Y. & Honda, S. The daf-2 gene network for longevity regulates oxidative stress resistance and Mn-superoxide dismutase gene expression in Caenorhabditis elegans. Faseb J. 13, 1385-1393 (1999
29. Holzenberger, M. et al. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 421, 182-187 (2003
30. Kimura, K. D., Tissenbaum, H. A., Liu, Y. & Ruvkun, G. daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277, 942-946 (1997
31. Patel, D. S. et al. Clustering of genetically defined allele classes in the Caenorhabditis elegans DAF-2 insulin/IGF-1 receptor. Genetics 178, 931-946 (2008
32. Ogg, S. et al. The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389, 994-999 (1997
33. Lin, K., Dorman, J. B., Rodan, A. & Kenyon, C. daf-16: An HNF-3/forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278, 1319-1322 (1997
34. Ramsay, J. O. & Silverman, B. W. Functional Data Analysis 2nd edn (Springer, 2006
35. Schafer, F. Q. & Buettner, G. R. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 30, 1191-1212 (2001
36. Bachi, A., Dalle-Donne, I. & Scaloni, A. Redox proteomics: Chemical principles, methodological approaches and biological/biomedical promises. Chem. Rev. 113, 596-698 (2013
37. Clark, W. M. Studies on oxidation-reduction. I. Introduction. Public Health Rep. 38, 443-445 (1923
38. Meister, A. Glutathione metabolism and its selective modification. J. Biol. Chem. 263, 17205-17208 (1988
39. Luersen, K. et al. The glutathione reductase GSR-1 determines stress tolerance and longevity in Caenorhabditis elegans. PLoS ONE 8, e60731 (2013
40. Arkblad, E. L. et al. A Caenorhabditis elegans mutant lacking functional nicotinamide nucleotide transhydrogenase displays increased sensitivity to oxidative stress. Free Radic. Biol. Med. 38, 1518-1525 (2005
41. Bass, R., Ruddock, L. W., Klappa, P. & Freedman, R. B. A major fraction of endoplasmic reticulum-located glutathione is present as mixed disulfides with protein. J. Biol. Chem. 279, 5257-5262 (2004
42. Winterbourn, C. C. & Metodiewa, D. Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. Free Radic. Biol. Med. 27, 322-328 (1999
43. Morgan, B. et al. Multiple glutathione disulfide removal pathways mediate cytosolic redox homeostasis. Nat. Chem. Biol. 9, 119-125 (2013
44. Nagy, P., Winterbourn, C. C. & James, C. F. in: Advances in Molecular Toxicology (ed James, C. F.) Chapter 6 (Elsevier, 2010
45. Brigelius-Flohe, R. & Flohe, L. Basic principles and emerging concepts in the redox control of transcription factors. Antioxid. Redox Signal. 15, 2335-2381 (2011
46. Ghaemmaghami, S. et al. Global analysis of protein expression in yeast. Nature 425, 737-741 (2003
47. Milo, R., Jorgensen, P., Moran, U., Weber, G. & Springer, M. BioNumbers-the database of key numbers in molecular and cell biology. Nucleic Acids Res. 38, D750-D753 (2010
48. Maughan, D. W., Henkin, J. A. & Vigoreaux, J. O. Concentrations of glycolytic enzymes and other cytosolic proteins in the diffusible fraction of a vertebrate muscle proteome. Mol. Cell. Proteomics 4, 1541-1549 (2005
49. Stone, J. R. & Yang, S. Hydrogen peroxide: A signaling messenger. Antioxid. Redox Signal. 8, 243-270 (2006
50. Appenzeller-Herzog, C. Glutathione-and non-glutathione-based oxidant control in the endoplasmic reticulum. J. Cell Sci. 124, 847-855 (2011
51. Aslund, F., Zheng, M., Beckwith, J. & Storz, G. Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc. Natl Acad. Sci. USA 96, 6161-6165 (1999
52. Moreland, K. in Diverging color maps for scientific visualization. Proceedings of the 5th International Symposium on Visual Computing 92-103 (Springer-Verlag, 2009
53. Wardman, P. Reduction potentials of one-electron couples involving free radicals in aqueous solution. J. Phys. Chem. Ref. Data 18, 1637-1755 (1989
54. Pfeiffer, J., Johnson, D. & Nehrke, K. Oscillatory transepithelial H(+) flux regulates a rhythmic behavior in C. elegans. Curr. Biol. 18, 297-302 (2008
55. Johnson, D., Allman, E. & Nehrke, K. Regulation of acid-base transporters by reactive oxygen species following mitochondrial fragmentation. Am J. Physiol. Cell Physiol. 302, C1045-C1054 (2012
56. Ramsay, J. O., Hooker, G. & Graves, S. Functional Data Analysis with R and MATLAB (Springer, 2009).