How does the protein environment optimize the thermodynamics of thiol sulfenylation? Insights from model systems to QM/MM calculations on human 2-Cys peroxiredoxin

Journal of Biomolecular Structure and Dynamics

Volumn 33, Issue 3, 2015, Pages 584-596

  Oláh, Julianna ^a   Van Bergen, Laura ^b   De Proft, Frank ^b   Roos, Goedele ^b,c  

^a BUDAPEST UNIVERSITY OF TECHNOLOGY AND ECONOMICS   (Hungary)

^b VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^c Brussels Center for Redox Biology   (Belgium)

Author keywords

Ligand effect; Peroxiredoxin; QM MM; Redox chemistry; Sulfenylation

Indexed keywords

CYSTEINE; PEROXIREDOXIN; SULFENIC ACID DERIVATIVE; SULFONIC ACID DERIVATIVE; THIOL; THIOREDOXIN PEROXIDASE; THIOREDOXIN PEROXIDASE B; UNCLASSIFIED DRUG; PRDX2 PROTEIN, HUMAN;

ARTICLE; ENZYME ACTIVE SITE; HYDROGEN BOND; MOLECULAR MECHANICS; OXIDATION REDUCTION POTENTIAL; PROTEIN MODIFICATION; QUANTUM MECHANICS; SULFENYLATION; THERMODYNAMICS; CHEMISTRY; HUMAN; MOLECULAR DYNAMICS; OXIDATION REDUCTION REACTION; QUANTUM THEORY;

CATALYTIC DOMAIN; CYSTEINE; HUMANS; HYDROGEN BONDING; MOLECULAR DYNAMICS SIMULATION; OXIDATION-REDUCTION; PEROXIREDOXINS; QUANTUM THEORY; THERMODYNAMICS;

EID: 84919843680     PISSN: 07391102     EISSN: 15380254     Source Type: Journal    
DOI: 10.1080/07391102.2014.907543     Document Type: Article

References (38)

1. Billiet, L., Geerlings, P., Messens, J., & Roos, G. (2012). The thermodynamics of thiol sulfenylation. Free Radical Biology and Medicine, 52, 1473-1485.
2. Brooks, B. R., Brooks, C. L., 3rd, Mackerell, A. D., Jr, Nilsson, L., Petrella, R. J., Roux, B., ... Karplus, M. (2009). CHARMM: The biomolecular simulation program. Journal of Computational Chemistry, 30, 1545-1614.
3. Budde, H., Flohe, L., Hecht, H. J., Hofmann, B., Stehr, M., Wissing, J., & Lunsdorf, H. (2003). Kinetics and redoxsensitive oligomerisation reveal negative subunit cooperativity in tryparedoxin peroxidase of Trypanosoma brucei brucei. Biological Chemistry, 384, 619-633.
4. Cox, A. G., Winterbourn, C. C., & Hampton, M. B. (2010). Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. Biochemical Journal, 425, 313-325.
5. Ferrer-Sueta, G., Manta, B., Botti, H., Radi, R., Trujillo, M., & Denicola, A. (2011). Factors affecting protein thiol reactivity and specificity in peroxide reduction. Chemical Research in Toxicology, 24, 434-450.
6. Flohe, L. (2010). Changing paradigms in thiology: From antioxidant defense toward redox regulation. Methods in Enzymology, 473, 1-39.
7. Flohe, L., Budde, H., Bruns, K., Castro, H., Clos, J., Hofmann, B., ... Hecht, H. J. (2002). Tryparedoxin peroxidase of leishmania donovani: Molecular cloning, heterologous expression, specificity, and catalytic mechanism. Archives of Biochemistry and Biophysics, 400, 148-148.
8. Foloppe, N., & Nilsson, L. (2004). The glutaredoxin -C-P-Y-Cmotif: Influence of peripheral residues. Structure, 12, 289-300.
9. Foloppe, N., Sagemark, J., Nordstrand, K., Berndt, K. D., & Nilsson, L. (2001). Structure, dynamics and electrostatics of the active site of glutaredoxin 3 from Escherichia coli: Comparison with functionally related proteins. Journal of Molecular Biology, 310, 449-470.
10. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuceria, G. E., Robb, M. A., Cheeseman, J. R., ... Fox, D. J. (2009). Gaussian 09, Revision A.1. Wallingford, CT: Gaussian.
11. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuceria, G. E., Robb, M. A., Cheeseman, J. R., ... Pople, J. R. (2003). Gaussian 03, Revision A,1. Wallingford, CT: Gaussian.
12. Grimme, S., Antony, J., Ehrlich, S., & Krieg, H. (2010). A consistent and accurate ab initio parametrization of density functional dispersion correction (DFT-D) for the 94 elements H-Pu. Journal of Chemical Physics, 132, 154104.
13. Hall, A., Karplus, P. A., & Poole, L. B. (2009). Typical 2-Cys peroxiredoxins - Structures, mechanisms and functions. FEBS Journal, 276, 2469-2477.
14. Ho, J. M., & Coote, M. L. (2010). A universal approach for continuum solvent pK a calculations: Are we there yet? Theoretical Chemistry Accounts, 125, 3-21.
15. Ho, J., Coote, M. L., Cramer, C. J., & Truhlar, D. G. (in press). Theoretical calculation of reduction potentials. In B. Speiser & O. Hammerich (Eds.), Organic electrochemistry (5th ed.). Boca Raton, FL: CRC Press.
16. Ho, J., Klamt, A., & Coote, M. L. (2010). Comment on the correct use of continuum solvent models. The Journal of Physical Chemistry A, 114, 13442-13444.
17. Lamkemeyer, P., Laxa, M., Collin, V., Li, W., Finkemeier, I., Schottler, M. A., ... Dietz, K. J. (2006). Peroxiredoxin Q of Arabidopsis thaliana is attached to the thylakoids and functions in context of photosynthesis. The Plant Journal, 45, 968-981.
18. Lonsdale, R., Olah, J., Mulholland, A. J., & Harvey, J. N. (2011). Does compound I vary significantly between isoforms of cytochrome P450? Journal of the American Chemical Society, 133, 15464-15474.
19. MacKerell, A. D., Jr, Banavali, N., & Foloppe, N. (2000). Development and current status of the CHARMM force field for nucleic acids. Biopolymers, 56, 257-265.
20. Nagy, P., Karton, A., Betz, A., Peskin, A. V., Pace, P., O'Reilly, R. J., ... Winterbourn, C. C. (2011). Model for the exceptional reactivity of peroxiredoxins 2 and 3 with hydrogen peroxide: A kinetic and computational study. Journal of Biological Chemistry, 286, 18048-18055.
21. Olsson, M. H., Søndergaard, C. R., Rostkowski, M., & Jensen, J. H. (2011). PROPKA3: Consistent treatment of internal and surface residues in empirical pKa predictions. Journal of Chemical Theory and Computation, 7, 525-537.
22. Parsonage, D., Youngblood, D. S., Sarma, G. N., Wood, Z. A., Karplus, P. A., & Poole, L. B. (2005). Analysis of the link between enzymatic activity and oligomeric state in AhpC, a bacterial peroxiredoxin. Biochemistry, 44, 10583-10592.
23. Peskin, A. V., Low, F. M., Paton, L. N., Maghzal, G. J., Hampton, M. B., &Winterbourn, C. C. (2007). The high reactivity of peroxiredoxin 2 with H2O2 is not reflected in its reaction with other oxidants and thiol reagents. Journal of Biological Chemistry, 282, 11885-11892.
24. Poole, L. B. (2007). The catalytic mechanism of peroxiredoxins. Subcellular Biochemistry, 44, 61-81.
25. Poole, L. B., Karplus, P. A., & Claiborne, A. (2004). Protein sulfenic acids in redox signaling. Annual Review of Pharmacology and Toxicology, 44, 325-347.
26. Roos, G., De Proft, F., & Geerlings, P. (2013). Electron capture by the thiyl radical and disulfide bond: Ligand effects on the reduction potential. Chemistry - A European Journal, 19, 5050-5060.
27. Roos, G., Foloppe, N., & Messens, J. (2013). Understanding the pKa of redox cysteines: The key role of hydrogen bonding. Antioxidants & Redox Signaling, 18, 94-127.
28. Roos, G., Foloppe, N., Van Laer, K., Wyns, L., Nilsson, L., Geerlings, P., & Messens, J. (2009). How thioredoxin dissociates its mixed disulfide. PLoS Computational Biology, 5, e1000461.
29. Roos, G., & Messens, J. (2011). Protein sulfenic acid formation: From cellular damage to redox regulation free radic. Biology and Medicine, 51, 314-326.
30. Schroder, E., Littlechild, J. A., Lebedev, A. A., Errington, N., Vagin, A. A., & Isupov, M. N. (2000). Crystal structure of decameric 2-Cys peroxiredoxin from human erythrocytes at 1.7 Å resolution. Structure, 8, 605-615.
31. Sharma, P. K., Chu, Z. T., Olsson, M. H., & Warshel, A. (2007). A new paradigm for electrostatic catalysis of radical reactions in vitamin B12 enzymes. Proceedings of the National Academy of Sciences, 104, 9661-9666.
32. Strickland, N., Mulholland, A. J., & Harvey, J. N. (2006). The Fe-CO bond energy in myoglobin: A QM/MM study of the effect of tertiary structure. Biophysical Journal, 90, L27-L29.
33. Tomasi, J., Mennucci, B., & Cammi, R. (2005). Quantum mechanical continuum solvation models. Chemical Reviews, 105, 2999-3094.
34. Trujillo, M., Clippe, A., Manta, B., Ferrer-Sueta, G., Smeets, A., Declercq, J. P., ... Radi, R. (2007). Pre-steady state kinetic characterization of human peroxiredoxin 5: Taking advantage of Trp84 fluorescence increase upon oxidation. Archives of Biochemistry and Biophysics, 467, 95-106.
35. van der Kamp, M. W. (2008). Modelling reactions and dynamics of claisen enzymes (PhD thesis). University Bristol.
36. Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., ... Mackerell, A. D. Jr. (2010). CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. Journal of Computational Chemistry, 31, 671-690.
37. Winterbourn, C. C., & Hampton, M. B. (2008). Thiol chemistry and specificity in redox signaling. Free Radical Biology and Medicine, 45, 549-561.
38. Wood, Z. A., Schroder, E., Robin Harris, J., & Poole, L. B. (2003). Structure, mechanism and regulation of peroxiredoxins. Trends in Biochemical Sciences, 28, 32-40.