Advertisement

Theoretical Chemistry Accounts

, Volume 129, Issue 1, pp 93–103 | Cite as

Reduction mechanism in class A methionine sulfoxide reductases: a theoretical chemistry investigation

  • E. Thiriot
  • G. Monard
  • S. Boschi-Muller
  • G. Branlant
  • M. F. Ruiz-López
Regular Article

Abstract

Ab initio calculations at the B3LYP/6–311 ++G(2df,2p) and B3LYP/6–31G(d) level have been carried out to investigate the reaction mechanism of methionine sulfoxide reductases of class A. These enzymes reduce oxidized methionine in vivo and therefore play an important role in repairing protein damage caused by the oxidative stress. Our calculations have been carried out for a model reaction in a model active site. Several reaction mechanisms have been explored that can roughly be described as (2H+ + 2e) or (H+ + e). The results suggest that the actual reaction mechanism is of the (2H+ + 2e) type corresponding to a more or less asynchronous-concerted double-proton transfer reaction leading to the formation of methionine (dimethylthioether in our model) and a sulfenic acid Cys-SOH. The Michaelis complex would involve one deprotonated Cys and one protonated Glu residues in the active site, this protonation state being mandatory to stabilize the sulfoxide substrate. Then, proton transfer from Glu to the substrate takes place, followed by proton transfer from one Tyr residue and fast reorganization of the system. The overall activation energy barrier is estimated to fall in the range 7–9 kcal/mol, much lower than the predicted barrier in DMSO solution (29.6 kcal/mol) reported before.

Keywords

Methionine sulfoxide reductase Oxidative stress Enzymatic catalysis Sulfoxide Ab initio calculations 

Notes

Acknowledgments

The authors thank the PRST “Bioingénierie” and the French Ministry of Research (ACI IMPBio program, project SIRE) for financial support. They also thank the French facility CINES for providing computational resources.

Supplementary material

214_2011_901_MOESM1_ESM.pdf (132 kb)
Supplementary material 1 (PDF 132 kb)

References

  1. 1.
    Lowther WT, Brot N, Weissbach H, Matthews BW (2000) Biochemistry 39:13307CrossRefGoogle Scholar
  2. 2.
    Boschi-Muller S, Azza S, Sanglier-Cianferani S, Talfournier F, van Dorsselear A, Branlant G (2000) J Biol Chem 275:35908CrossRefGoogle Scholar
  3. 3.
    Tête-Favier F, Cobessi D, Boschi-Muller S, Azza S, Branlant G, Aubry A (2000) Structure Fold Des 8:1167CrossRefGoogle Scholar
  4. 4.
    Moskovitz J, Bar-Noy S, Williams WM, Requena J, Berlett BS, Stadtman ER (2001) Proc Natl Acad Sci USA 98:12920CrossRefGoogle Scholar
  5. 5.
    Boschi-Muller S, Azza S, Branlant G (2001) Protein Sci 10:2272CrossRefGoogle Scholar
  6. 6.
    Kumar RA, Koc A, Cerny RL, Gladyshev VN (2002) J Biol Chem 277:37527CrossRefGoogle Scholar
  7. 7.
    Lowther WT, Weissbach H, Etienne F, Brot N, Matthews BW (2002) Nat Struct Biol 9:348Google Scholar
  8. 8.
    Olry A, Boschi-Muller S, Marraud M, Sanglier-Cianferani S, van Dorsselear A, Branlant G (2002) J Biol Chem 277:12016CrossRefGoogle Scholar
  9. 9.
    Taylor AB, Benglis DM Jr, Dhandayuthapani S, Hart PJ (2003) J Bacteriol 185:4119CrossRefGoogle Scholar
  10. 10.
    Antoine M, Boschi-Muller S, Branlant G (2003) J Biol Chem 278:45352CrossRefGoogle Scholar
  11. 11.
    Kim H-Y, Gladyshev VN (2004) Mol Biol Cell 15:1055CrossRefGoogle Scholar
  12. 12.
    Olry A, Boschi-Muller S, Branlant G (2004) Biochemistry 43:11616CrossRefGoogle Scholar
  13. 13.
    Coudevylle NT A, Azza S, Boschi-Muller S, Branlant G, Cung M-T (2004) J Biomol NMR 30:363CrossRefGoogle Scholar
  14. 14.
    Boschi-Muller S, Olry A, Antoine M, Branlant G (2005) Biochim Biophys Acta 1703:231Google Scholar
  15. 15.
    Lin Z, Johnson LC, Weissbach H, Brot N, Lively MO, Lowther WT (2007) Proc Natl Acad Sci USA 104:9597CrossRefGoogle Scholar
  16. 16.
    Gruez A, Libiad M, Boschi-Muller S, Branlant G (2010) J Biol Chem 285:25033CrossRefGoogle Scholar
  17. 17.
    Yiannios CN, Karabinos JV (1963) J Org Chem 28:3246CrossRefGoogle Scholar
  18. 18.
    Wallace TJ (1964) J Am Chem Soc 86:2018CrossRefGoogle Scholar
  19. 19.
    Wallace TJ, Mahon JJ (1964) J Am Chem Soc 86:4099CrossRefGoogle Scholar
  20. 20.
    Wallace TJ, Mahon JJ (1965) J Org Chem 30:1502CrossRefGoogle Scholar
  21. 21.
    Epstein WW, Sweat FW (1967) Chem Rev 67:247CrossRefGoogle Scholar
  22. 22.
    Lowe OG (1975) J Org Chem 40:2096CrossRefGoogle Scholar
  23. 23.
    Lowe OG (1976) J Org Chem 41:2061CrossRefGoogle Scholar
  24. 24.
    Madesclaire M (1988) Tetrahedron 44:6537CrossRefGoogle Scholar
  25. 25.
    Arterburn JB, Perry MC, Nelson SL, Dible BR, Holguin MS (1997) J Am Chem Soc 119:9309CrossRefGoogle Scholar
  26. 26.
    Abu-Omar MM, Khan SI (1998) Inorg Chem 37:4979CrossRefGoogle Scholar
  27. 27.
    Arnáiz FJ, Aguado R, Pedrosa MR, De Cian A (2003) Inorg Chim Acta 347:33CrossRefGoogle Scholar
  28. 28.
    Hirano M, Yakabe S, Monobe H, Morimoto T (1998) J Chem Research (S) (8):472–473Google Scholar
  29. 29.
    Balta B, Monard G, Ruiz-López MF, Antoine M, Gand A, Boschi-Muller S, Branlant G (2006) J Phys Chem A 110:7628CrossRefGoogle Scholar
  30. 30.
    Becke AD (1993) J Chem Phys 98:5648CrossRefGoogle Scholar
  31. 31.
    Lee C, Yang W, Parr RG (1988) Phys Rev B 37:785CrossRefGoogle Scholar
  32. 32.
    Tomasi J, Bonaccorsi R, Cami R, Olivares del Valle FJ (1991) J Mol Struct Theochem 234:401CrossRefGoogle Scholar
  33. 33.
    Tomasi J, Persico M (1994) Chem Rev 94:2027CrossRefGoogle Scholar
  34. 34.
    Breneman CM, Wiberg KB (1990) J Comp Chem 11:361CrossRefGoogle Scholar
  35. 35.
    Mayer I (1983) Chem Phys Lett 97:270CrossRefGoogle Scholar
  36. 36.
    Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery Jr JA, Vreven T, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski VG, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen W, Wong MW, Gonzalez C, Pople JA (2004) Gaussian 03, revision C.02. Gaussian Inc., WallingfordGoogle Scholar
  37. 37.
    Antoine M, Gand A, Boschi-Muller S, Branlant G (2006) J Biol Chem 281:39062CrossRefGoogle Scholar
  38. 38.
    Thiriot E (2008) Thesis, Nancy University, Vandoeuvre-lès-Nancy, FranceGoogle Scholar
  39. 39.
    Ranaivoson FM, Antoine M, Kauffmann B, Boschi-Muller S, Aubry A, Branlant G, Favier F (2008) J Mol Biol 377:268CrossRefGoogle Scholar
  40. 40.
    Perrin DD, Dempsey B, Serjeant EP (1981) pKa Prediction for organic acids and bases. Chapman & Hall, LondonGoogle Scholar
  41. 41.
    Li H, Robertson AD, Jensen JH (2005) Proteins Struct Funct. Genet 61:704Google Scholar
  42. 42.
    Bas DC, Rogers DM, Jensen JH (2008) Proteins Struct Funct. Genet 73:765Google Scholar
  43. 43.
    Boschi-Muller S, Gand A, Branlant G (2008) Arch Biochem Biophys 474:266CrossRefGoogle Scholar
  44. 44.
    Cardey B, Enescu M (2005) Chem Phys Chem 6:1175Google Scholar
  45. 45.
    Cardey B, Enescu M (2007) J Phys Chem A 111:673CrossRefGoogle Scholar
  46. 46.
    Fu Y, Liu L, Yu H-Z, Wand Y-M, Guo Q-X (2005) J Mol Struct Theochem 127:7227Google Scholar
  47. 47.
    Forni LG, Willson RL (1986) Biochem J 240:897Google Scholar
  48. 48.
    Vorontsov AV (2008) Russ Chem Rev 77:909CrossRefGoogle Scholar
  49. 49.
    Lewis A, Bumpus JA, Truhlar DG, Cramer CJ (2004) J Chem Educ 81:596CrossRefGoogle Scholar
  50. 50.
    Lewis A, Bumpus JA, Truhlar DG, Cramer CJ (2007) J Chem Educ 84:934Google Scholar
  51. 51.
    Kelly CP, Cramer CJ, Truhlar DG (2007) J Phys Chem B 111:408CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • E. Thiriot
    • 1
  • G. Monard
    • 1
  • S. Boschi-Muller
    • 2
  • G. Branlant
    • 2
  • M. F. Ruiz-López
    • 1
  1. 1.Theoretical Chemistry and Biochemistry Group, SRSMCNancy UniversityVandoeuvre-lès-NancyFrance
  2. 2.Molecular and Structural Enzymology Group, AREMSNancy UniversityVandoeuvre-lès-NancyFrance

Personalised recommendations