Estimation of kinetic parameters related to biochemical interactions between hydrogen peroxide and signal transduction proteins

Frontiers in Chemistry

Volumn 2, Issue OCT, 2014, Pages

  Brito, Paula M ^a,b,c   Antunes, Fernando ^d  

^a RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^b INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^c UNIVERSITY OF BEIRA INTERIOR   (Portugal)

^d UNIVERSITY OF LISBON   (Portugal)

Author keywords

Kinetics; Protein tyrosine phosphatases; PTP1B; Rate constant; Redox regulation; Redox signaling; SHP 2

Indexed keywords

EID: 84949283967     PISSN: None     EISSN: 22962646     Source Type: Journal    
DOI: 10.3389/fchem.2014.00082     Document Type: Article

References (55)

1. Adimora, N. J., Jones, D. P., and Kemp, M. L. (2010). A model of redox kinetics implicates the thiol proteome in cellular hydrogen peroxide responses. Antioxid. Redox Signal. 13, 731-743. doi: 10.1089/ars.2009.2968
2. Alves, R., Antunes, F., and Salvador, A. (2006). Tools for kinetic modeling of biochemical networks. Nat. Biotechnol. 24, 667-672. doi: 10.1038/nbt0606-667
3. 2 gradients across biomembranes. FEBS Lett. 475, 121-126. doi: 10.1016/S0014-5793(00)01638-0
4. Barrett, W. C., DeGnore, J. P., Konig, S., Fales, H. M., Keng, Y. F., Zhang, Z. Y., et al. (1999). Regulation of PTP1B via glutathionylation of the active site cysteine 215. Biochemistry (Mosc.) 38, 6699-6705. doi: 10.1021/bi990240v
5. Benfeitas, R., Selvaggio, G., Antunes, F., Coelho, P. M. B. M., and Salvador, A. (2014). Hydrogen peroxide metabolism and sensing in human erythrocytes: a validated kinetic model and reappraisal of the role of peroxiredoxin II. Free Radic. Biol. Med. 74, 35-49. doi: 10.1016/j.freeradbiomed.2014.06.007
6. Bienert, G. P., Møller, A. L. B., Kristiansen, K. A., Schulz, A., Møller, I. M., Schjoerring, J. K., et al. (2007). Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J. Biol. Chem. 282, 1183-1192. doi: 10.1074/jbc.M603761200
7. 2 in Saccharomyces cerevisiae. J. Biol. Chem. 279, 6501-6506. doi: 10.1074/jbc.M311818200
8. Brigelius-Flohé, R., and Flohé, L. (2011). Basic principles and emerging concepts in the redox control of transcription factors. Antioxid. Redox Signal. 15, 2335-2381. doi: 10.1089/ars.2010.3534
9. Buettner, G. R., Wagner, B. A., and Rodgers, V. G. J. (2013). Quantitative redox biology: an approach to understanding the role of reactive species in defining the cellular redox environment. Cell Biochem. Biophys. 67, 477-483. doi: 10.1007/s12013-011-9320-3
10. 2-domain-containing protein tyrosine phosphatases by two backdoor cysteines. Biochemistry (Mosc.) 48, 1399-1409. doi: 10.1021/bi801973z
11. Chen, K., Kirber, M. T., Xiao, H., Yang, Y., and Keaney, J. F. (2008). Regulation of ROS signal transduction by NADPH oxidase 4 localization. J. Cell Biol. 181, 1129-1139. doi: 10.1083/jcb.200709049
12. 2: de novo synthesis versus nuclear translocation. Methods Enzymol. 528, 157-171. doi: 10.1016/B978-0-12-405881-1.00009-4
13. 2 in the induction of NF-κ B-dependent selective gene expression. Methods Enzymol. 528, 173-188. doi: 10.1016/B978-0-12-405881-1.00010-0
14. Dagnell, M., Frijhoff, J., Pader, I., Augsten, M., Boivin, B., Xu, J., et al. (2013). Selective activation of oxidized PTP1B by the thioredoxin system modulates PDGF-? receptor tyrosine kinase signaling. Proc. Natl. Acad. Sci. U.S.A. 110, 13398-13403. doi: 10.1073/pnas.1302891110
15. Denu, J. M., and Tanner, K. G. (1998). Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. Biochemistry (Mosc.) 37, 5633-5642. doi: 10.1021/bi973035t
16. 2: relevance in inflammation and synergy with TNF-alpha. J. Immunol. 178, 3893-3902. doi: 10.4049/jimmunol.178.6.3893
17. Ferrer-Sueta, G., Manta, B., Botti, H., Radi, R., Trujillo, M., and Denicola, A. (2011). Factors affecting protein thiol reactivity and specificity in peroxide reduction. Chem. Res. Toxicol. 24, 434-450. doi: 10.1021/tx100413v
18. Fisher-Wellman, K. H., and Neufer, P. D. (2012). Linking mitochondrial bioenergetics to insulin resistance via redox biology. Trends Endocrinol. Metab. 23, 142-153. doi: 10.1016/j.tem.2011.12.008
19. Flohe, L. (1979). Glutathione peroxidase: fact and fiction. Ciba Found. Symp. 65, 95-122.
20. 2 in studies of signal transduction. Free Radic. Biol. Med. 42, 926-932. doi: 10.1016/j.freeradbiomed.2007.01.011
21. Forman, H. J., Maiorino, M., and Ursini, F. (2010). Signaling functions of reactive oxygen species. Biochemistry (Mosc.) 49, 835-842. doi: 10.1021/bi9020378
22. Forstrom, J. W., and Tappel, A. L. (1979). Donor substrate specificity and thiol reduction of glutathione disulfide peroxidase. J. Biol. Chem. 254, 2888-2891.
23. Haque, A., Andersen, J. N., Salmeen, A., Barford, D., and Tonks, N. K. (2011). Conformation-sensing antibodies stabilize the oxidized form of PTP1B and inhibit its phosphatase activity. Cell 147, 185-198. doi: 10.1016/j.cell.2011.08.036
24. Huang, B. K., and Sikes, H. D. (2014). Quantifying intracellular hydrogen peroxide perturbations in terms of concentration. Redox Biol. 2, 955-962. doi: 10.1016/j.redox.2014.08.001
25. Irani, K., Xia, Y., Zweier, J. L., Sollott, S. J., Der, C. J., Fearon, E. R., et al. (1997). Mitogenic signaling mediated by oxidatnts in ras-transformed fibroblasts. Science 275, 1649-1652. doi: 10.1126/science.275.5306.1649
26. Iwakami, S., Misu, H., Takeda, T., Sugimori, M., Matsugo, S., Kaneko, S., et al. (2011). Concentration-dependent dual effects of hydrogen peroxide on insulin signal transduction in H4IIEC hepatocytes. PLoS ONE 6:e27401. doi: 10.1371/journal.pone.0027401
27. LaButti, J., Chowdhury, G., Reilly, T. J., and Gates, K. S. (2007). Redox regulation of protein tyrosine phosphatase 1B (PTP1B) by peroxymonophosphate (= O3POOH). J. Am. Chem. Soc. 129:5320. doi: 10.1021/ja070194j
28. Lee, S. R., Kwon, K. S., Kim, S. R., and Rhee, S. G. (1998). Reversible inactivation of protein-tyrosine phosphatase 1B in A431 cells stimulated with epidermal growth factor. J. Biol. Chem. 273, 15366-15372. doi: 10.1074/jbc.273.25.15366
29. Le Moan, N., Clement, G., Le Maout, S., Tacnet, F., and Toledano, M. B. (2006). The Saccharomyces cerevisiae proteome of oxidized protein thiols: contrasted functions for the thioredoxin and glutathione pathways. J. Biol. Chem. 281, 10420-10430. doi: 10.1074/jbc.M513346200
30. Mahadev, K., Zilbering, A., Zhu, L., and Goldstein, B. J. (2001). Insulin-stimulated hydrogen peroxide reversibly inhibits protein-tyrosine phosphatase 1b in vivo and enhances the early insulin action cascade. J. Biol. Chem. 276, 21938-21942. doi: 10.1074/jbc.C100109200
31. 2 permeation through cytoplasmic and peroxisomal membranes: comparison with experimental data. Biochim. Biophys. Acta 1673, 149-159. doi: 10.1016/j.bbagen.2004.04.011
32. 2 delivery to cells: steady-state versus bolus addition. Methods Enzymol. 526, 159-173. doi: 10.1016/B978-0-12-405883-5.00010-7
33. 2: latency concepts and gradients. Methods Enzymol. 527, 3-19. doi: 10.1016/B978-0-12-405882-8.00001-5
34. Marinho, H. S., Real, C., Cyrne, L., Soares, H., and Antunes, F. (2014). Hydrogen peroxide sensing, signaling and regulation of transcription factors. Redox Biol. 2, 535-562. doi: 10.1016/j.redox.2014.02.006
35. Martínez-Acedo, P., Núñez, E., Gómez, F. J. S., Moreno, M., Ramos, E., Izquierdo-álvarez, A., et al. (2012). A novel strategy for global analysis of the dynamic thiol redox proteome. Mol. Cell. Proteomics 11, 800-813. doi: 10.1074/mcp.M111.016469
36. Meng, T.-C., Fukada, T., and Tonks, N. K. (2002). Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell 9, 387-399. doi: 10.1016/S1097-2765(02)00445-8
37. Miller, E. W., Dickinson, B. C., and Chang, C. J. (2010). Aquaporin-3 mediates hydrogen peroxide uptake to regulate downstream intracellular signaling. Proc. Natl. Acad. Sci. U.S.A. 107, 15681-15686. doi: 10.1073/pnas.1005776107
38. Mishina, N. M., Tyurin-Kuzmin, P. A., Markvicheva, K. N., Vorotnikov, A. V., Tkachuk, V. A., Laketa, V., et al. (2011). Does cellular hydrogen peroxide diffuse or act locally? Antioxid. Redox Signal. 14, 1-7. doi: 10.1089/ars.2010.3539
39. Oakley, F. D., Abbott, D., Li, Q., and Engelhardt, J. F. (2009). Signaling components of redox active endosomes: the redoxosomes. Antioxid. Redox Signal. 11, 1313-1333. doi: 10.1089/ARS.2008.2363
40. Oliveira-Marques, V., Silva, T., Cunha, F., Covas, G., Marinho, H. S., Antunes, F., et al. (2013). A quantitative study of the cell-type specific modulation of c-Rel by hydrogen peroxide and TNF-α Redox Biol. 1, 347-352. doi: 10.1016/j.redox.2013.05.004
41. Parsons, Z. D., and Gates, K. S. (2013). Thiol-dependent recovery of catalytic activity from oxidized protein tyrosine phosphatases. Biochemistry (Mosc.) 52, 6412-6423. doi: 10.1021/bi400451m
42. Paulsen, C. E., Truong, T. H., Garcia, F. J., Homann, A., Gupta, V., Leonard, S. E., et al. (2012). Peroxide-dependent sulfenylation of the EGFR catalytic site enhances kinase activity. Nat. Chem. Biol. 8, 57-64. doi: 10.1038/nchembio.736
43. Rasband, W. (1997). ImageJ, U. S. National Institutes of Health. Bethesda, MD. Available online at: http://rsb.info.nih.gov/ij/, 1997-2006
44. Rawat, S. J., Creasy, C. L., Peterson, J. R., and Chernoff, J. (2013). The tumor suppressor Mst1 promotes changes in the cellular redox state by phosphorylation and inactivation of peroxiredoxin-1 protein. J. Biol. Chem. 288, 8762-8771. doi: 10.1074/jbc.M112.414524
45. Rinna, A., Torres, M., and Forman, H. J. (2006). Stimulation of the alveolar macrophage respiratory burst by ADP causes selective glutathionylation of protein tyrosine phosphatase 1B. Free Radic. Biol. Med. 41, 86-91. doi: 10.1016/j.freeradbiomed.2006.03.010
46. 2 generation: redox signalling and oxidative stress. J. Biol. Chem. 289, 8735-8741. doi: 10.1074/jbc.R113.544635
47. Tanner, J. J., Parsons, Z. D., Cummings, A. H., Zhou, H., and Gates, K. S. (2011). Redox regulation of protein tyrosine phosphatases: structural and chemical aspects. Antioxid. Redox Signal. 15, 77-97. doi: 10.1089/ars.2010.3611
48. Trindade, D. F., Cerchiaro, G., and Augusto, O. (2006). A role for peroxymonocarbonate in the stimulation of biothiol peroxidation by the bicarbonate/carbon dioxide pair. Chem. Res. Toxicol. 19, 1475-1482. doi: 10.1021/tx060146x
49. Tschopp, J., and Schroder, K. (2010). NLRP3 inflammasome activation: the convergence of multiple signalling pathways on ROS production? Nat. Rev. Immunol. 10, 210-215. doi: 10.1038/nri2725
50. Van Eunen, K., Bouwman, J., Daran-Lapujade, P., Postmus, J., Canelas, A. B., Mensonides, F. I. C., et al. (2010). Measuring enzyme activities under standardized in vivo-like conditions for systems biology. FEBS J. 277, 749-760. doi: 10.1111/j.1742-4658.2009.07524.x
51. Van Eunen, K., Kiewiet, J. A. L., Westerhoff, H. V., and Bakker, B. M. (2012). Testing biochemistry revisited: how in vivo metabolism can be understood from in vitro enzyme kinetics. PLoS Comput Biol 8:e1002483. doi: 10.1371/journal.pcbi.1002483
52. Voit, E. (1991). Canonical Nonlinear Modeling: S-System Approach to Understanding Complexity. New York, NY: Van Nostrand Reinhold.
53. Winterbourn, C. C., and Hampton, M. B. (2008). Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 45, 549-561. doi: 10.1016/j.freeradbiomed.2008.05.004
54. 2 accumulation for cell signaling. Cell 140, 517-528. doi: 10.1016/j.cell.2010.01.009
55. 2-Mediated Inactivation of Protein Tyrosine Phosphatases. J. Am. Chem. Soc. 133, 15803-15805. doi: 10.1021/ja2077137