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Amino Acids

, Volume 32, Issue 4, pp 543–551 | Cite as

Sulfenic acid in human serum albumin

  • S. Carballal
  • B. Alvarez
  • L. Turell
  • H. Botti
  • B. A. Freeman
  • R. Radi
Review Article

Summary.

Sulfenic acid (RSOH) is a central intermediate in both the reversible and irreversible redox modulation by reactive species of an increasing number of proteins involved in signal transduction and enzymatic pathways. In this paper we focus on human serum albumin (HSA), the most abundant plasma protein, proposed to serve antioxidant functions in the vascular compartment. Sulfenic acid in HSA has been previously detected using different methods after oxidation of its single free thiol Cys34 through one- or two-electron mechanisms. Since recent evidence suggests that sulfenic acid in HSA is stabilized within the protein environment, this derivative represents an appropriate model to examine protein sulfenic acid biochemistry, structure and reactivity. Sulfenic acid in HSA could be involved in mixed disufide formation, supporting a role of HSA-Cys34 as an important redox regulator in extracellular compartments.

Keywords: Thiol – Human serum albumin – Sulfenic acid – Peroxynitrite – Hydrogen peroxide – Free radicals 

Abbreviations:

HSA

human serum albumin

HSA-SH

the thiol of HSA

BSA

bovine serum albumin

SH/HSA

amount of thiol per albumin molecule

RSOH

sulfenic acid

NBD-Cl

7-chloro-4-nitrobenzo-2-oxa-1,3-diazol

DTNB

5,5′-dithio-bis(2-nitrobenzoic acid)

dimedone

5,5-dimethyl-1,3-cyclohexanedione

GSH

glutathione

GSSG

glutathione disulfide

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References

  1. Allison, WS 1976Formation and reactions of sulfenic acids in proteinsAcc Chem Res9293299CrossRefGoogle Scholar
  2. Alvarez, B, Ferrer-Sueta, G, Freeman, BA, Radi, R 1999Kinetics of peroxynitrite reaction with amino acids and human serum albuminJ Biol Chem274842848PubMedCrossRefGoogle Scholar
  3. Andersson, A, Isaksson, A, Brattstrom, L, Hultberg, B 1993Homocysteine and other thiols determined in plasma by HPLC and thiol-specific postcolumn derivatizationClin Chem3915901597PubMedGoogle Scholar
  4. Biteau, B, Labarre, J, Toledano, MB 2003ATP-dependent reduction of cysteine-sulphinic acid by S. cerevisiae sulphiredoxinNature425980984PubMedCrossRefGoogle Scholar
  5. Bito, R, Hino, S, Baba, A, Tanaka, M, Watabe, H, Kawabata, H 2005Degradation of oxidative stress-induced denatured albumin in rat liver endothelial cellsAm J Physiol Cell Physiol289C531C542PubMedCrossRefGoogle Scholar
  6. Bonini, MG, Augusto, O 2001Carbon dioxide stimulates the production of thiyl, sulfinyl, and disulfide radical anion from thiol oxidation by peroxynitriteJ Biol Chem27697499754PubMedCrossRefGoogle Scholar
  7. Boschi-Muller, S, Azza, S, Sanglier-Cianferani, S, Talfournier, F, Van Dorsselear, A, Branlant, G 2000A sulfenic acid enzyme intermediate is involved in the catalytic mechanism of peptide methionine sulfoxide reductase from Escherichia coliJ Biol Chem2753590835913PubMedCrossRefGoogle Scholar
  8. Brigelius-Flohe, R 1999Tissue-specific functions of individual glutathione peroxidasesFree Radic Biol Med27951965PubMedCrossRefGoogle Scholar
  9. Bryk, R, Griffin, P, Nathan, C 2000Peroxynitrite reductase activity of bacterial peroxiredoxinsNature407211215PubMedCrossRefGoogle Scholar
  10. Budanov, AV, Sablina, AA, Feinstein, E, Koonin, EV, Chumakov, PM 2004Regeneration of peroxiredoxins by p53-regulated sestrins, homologs of bacterial AhpDScience304596600PubMedCrossRefGoogle Scholar
  11. Carballal, S, Radi, R, Kirk, MC, Barnes, S, Freeman, BA, Alvarez, B 2003Sulfenic acid formation in human serum albumin by hydrogen peroxide and peroxynitriteBiochemistry4299069914PubMedCrossRefGoogle Scholar
  12. Carter, DC, He, XM 1990Structure of human serum albuminScience249302303PubMedCrossRefGoogle Scholar
  13. Carter, DC, He, XM, Munson, SH, Twigg, PD, Gernert, KM, Broom, MB, Miller, TY 1989Three-dimensional structure of human serum albuminScience24411951198PubMedCrossRefGoogle Scholar
  14. Cha, MK, Kim, IH 2006Disulfide between Cys392 and Cys438 of human serum albumin is redox-active, which is responsible for the thioredoxin-supported lipid peroxidase activityArch Biochem Biophys4451925PubMedGoogle Scholar
  15. Claiborne, A, Mallett, TC, Yeh, JI, Luba, J, Parsonage, D 2001Structural, redox, and mechanistic parameters for cysteine-sulfenic acid function in catalysis and regulationAdv Protein Chem58215276PubMedCrossRefGoogle Scholar
  16. Claiborne, A, Miller, H, Parsonage, D, Ross, RP 1993Protein-sulfenic acid stabilization and function in enzyme catalysis and gene regulationFaseb J714831490PubMedGoogle Scholar
  17. Claiborne, A, Yeh, JI, Mallett, TC, Luba, J, Crane, EJ,3rd, Charrier, V, Parsonage, D 1999Protein-sulfenic acids: diverse roles for an unlikely player in enzyme catalysis and redox regulationBiochemistry381540715416PubMedCrossRefGoogle Scholar
  18. DeLano WL (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA, USA. http://www.pymol.org
  19. DeMaster, EG, Quast, BJ, Redfern, B, Nagasawa, HT 1995Reaction of nitric oxide with the free sulfhydryl group of human serum albumin yields a sulfenic acid and nitrous oxideBiochemistry341149411499PubMedCrossRefGoogle Scholar
  20. Denu, JM, Tanner, KG 1998Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulationBiochemistry3756335642PubMedCrossRefGoogle Scholar
  21. Di Simplicio, P, Frosali, S, Priora, R, Summa, D, Cherubini Di Simplicio, F, Di Giuseppe, D, Di Stefano, A 2005Biochemical and biological aspects of protein thiolation in cells and plasmaAntioxid Redox Signal7951963PubMedCrossRefGoogle Scholar
  22. Ellis, HR, Poole, LB 1997aNovel application of 7-chloro-4-nitrobenzo-2-oxa-1,3-diazole to identify cysteine sulfenic acid in the AhpC component of alkyl hydroperoxide reductaseBiochemistry361501315018CrossRefGoogle Scholar
  23. Ellis, HR, Poole, LB 1997bRoles for the two cysteine residues of AhpC in catalysis of peroxide reduction by alkyl hydroperoxide reductase from Salmonella typhimuriumBiochemistry361334913356CrossRefGoogle Scholar
  24. Era, S, Hamaguchi, T, Sogami, M, Kuwata, K, Suzuki, E, Miura, K, Kawai, K, Kitazawa, Y, Okabe, H, Noma, A,  et al. 1988Further studies on the resolution of human mercapt- and nonmercaptalbumin and on human serum albumin in the elderly by high-performance liquid chromatographyInt J Pept Protein Res31435442PubMedCrossRefGoogle Scholar
  25. Era, S, Kuwata, K, Imai, H, Nakamura, K, Hayashi, T, Sogami, M 1995Age-related change in redox state of human serum albuminBiochim Biophys Acta12471216PubMedGoogle Scholar
  26. Finkel, T 2000Redox-dependent signal transductionFEBS Lett4765254PubMedCrossRefGoogle Scholar
  27. Gatti, RM, Radi, R, Augusto, O 1994Peroxynitrite-mediated oxidation of albumin to the protein-thiyl free radicalFEBS Lett348287290PubMedCrossRefGoogle Scholar
  28. Giles, GI, Jacob, C 2002Reactive sulfur species: an emerging concept in oxidative stressBiol Chem383375388PubMedCrossRefGoogle Scholar
  29. Halliwell, B 1988Albumin an important extracellular antioxidant?Biochem Pharmacol37569571PubMedCrossRefGoogle Scholar
  30. Halliwell, B, Gutteridge, JM 1990The antioxidants of human extracellular fluidsArch Biochem Biophys28018PubMedCrossRefGoogle Scholar
  31. Hansen, JM, Go, YM, Jones, DP 2006aNuclear and mitochondrial compartmentation of oxidative stress and redox signalingAnnu Rev Pharmacol Toxicol46215234CrossRefGoogle Scholar
  32. Hansen, JM, Zhang, H, Jones, DP 2006bDifferential oxidation of thioredoxin-1, thioredoxin-2, and glutathione by metal ionsFree Radic Biol Med40138145CrossRefGoogle Scholar
  33. He, XM, Carter, DC 1992Atomic structure and chemistry of human serum albuminNature358209215PubMedCrossRefGoogle Scholar
  34. Imai, H, Hayashi, T, Negawa, T, Nakamura, K, Tomida, M, Koda, K, Tajima, T, Koda, Y, Suda, K, Era, S 2002Strenuous exercise-induced change in redox state of human serum albumin during intensive kendo trainingJpn J Physiol52135140PubMedCrossRefGoogle Scholar
  35. Inayama, T, Kumagai, Y, Sakane, M, Saito, M, Matsuda, M 1996Plasma protein-bound sulfhydryl group oxidation in humans following a full marathon raceLife Sci59573578PubMedCrossRefGoogle Scholar
  36. Janatova, J, Fuller, JK, Hunter, MJ 1968The heterogeneity of bovine albumin with respect to sulfhydryl and dimer contentJ Biol Chem24336123622PubMedGoogle Scholar
  37. Kawai, K, Yoh, M, Hayashi, T, Imai, H, Negawa, T, Tomida, M, Sogami, M, Era, S 2001Effect of diabetic retinopathy on redox state of aqueous humor and serum albumin in patients with senile cataractTokai J Exp Clin Med269399PubMedGoogle Scholar
  38. Keire, DA, Strauss, E, Guo, W, Noszal, B, Rabenstein, DL 1992Kinetics and equilibria of thiol/disulfide interchange reactions of selected biological thiols and related molecules with oxidized glutathioneJ Org Chem57123127CrossRefGoogle Scholar
  39. Kice, JL, Cleveland, JP 1973Nucleophilic substitution reactions involving sulfenic acids and sulfenyl derivatives. Nucleophile- and acid-catalyzed oxygen-18 exchange of phenyl benzenethiolsulfinateJ Amer Chem Soc95104109CrossRefGoogle Scholar
  40. Koppenol, WH, Moreno, JJ, Pryor, WA, Ischiropoulos, H, Beckman, JS 1992Peroxynitrite, a cloaked oxidant formed by nitric oxide and superoxideChem Res Toxicol5834842PubMedCrossRefGoogle Scholar
  41. Kratochwil, NA, Ivanov, AI, Patriarca, M, Parkinson, JA, Gouldsworthy, AM, Murdoch, P, Sadler, PJ 1999Surprising reactions of iodo Pt(IV) and Pt(II) complexes with human albumin: detection of Cys34 sulfenic acidJ Am Chem Soc12181938203CrossRefGoogle Scholar
  42. Leto, S, Yiengst, MJ, Barrows, CH,Jr 1970The effect of age and protein deprivation on the sulfhydryl content of serum albuminJ Gerontol2548PubMedGoogle Scholar
  43. Liu, L, Hausladen, A, Zeng, M, Que, L, Heitman, J, Stamler, JS 2001A metabolic enzyme for S-nitrosothiol conserved from bacteria to humansNature410490494PubMedCrossRefGoogle Scholar
  44. Mansoor, MA, Svardal, AM, Ueland, PM 1992Determination of the in vivo redox status of cysteine, cysteinylglycine, homocysteine, and glutathione in human plasmaAnal Biochem200218229PubMedCrossRefGoogle Scholar
  45. Moriarty-Craige, SE, Jones, DP 2004Extracellular thiols and thiol/disulfide redox in metabolismAnnu Rev Nutr24481509PubMedCrossRefGoogle Scholar
  46. Noel, JK, Hunter, MJ 1972Bovine mercaptalbumin and non-mercaptalbumin monomers. Interconversions and structural differencesJ Biol Chem24773917406PubMedGoogle Scholar
  47. Paget, MS, Buttner, MJ 2003Thiol-based regulatory switchesAnnu Rev Genet3791121PubMedCrossRefGoogle Scholar
  48. Peshenko, IV, Shichi, H 2001Oxidation of active center cysteine of bovine 1-Cys peroxiredoxin to the cysteine sulfenic acid form by peroxide and peroxynitriteFree Radic Biol Med31292303PubMedCrossRefGoogle Scholar
  49. Peters, T 1996All about albumin: biochemistry, genetics and medical applicationsAcademic PressSan DiegoGoogle Scholar
  50. Poole, LB, Zeng, BB, Knaggs, SA, Yakubu, M, King, SB 2005Synthesis of chemical probes to map sulfenic acid modifications on proteinsBioconjug Chem1616241628PubMedCrossRefGoogle Scholar
  51. Quijano, C, Alvarez, B, Gatti, RM, Augusto, O, Radi, R 1997Pathways of peroxynitrite oxidation of thiol groupsBiochem J322167173PubMedGoogle Scholar
  52. Radi, R, Beckman, JS, Bush, KM, Freeman, BA 1991aPeroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxideJ Biol Chem26642444250Google Scholar
  53. Radi, R, Bush, KM, Cosgrove, TP, Freeman, BA 1991bReaction of xanthine oxidase-derived oxidants with lipid and protein of human plasmaArch Biochem Biophys286117125CrossRefGoogle Scholar
  54. Raftery, MJ, Yang, Z, Valenzuela, SM, Geczy, CL 2001Novel intra- and inter-molecular sulfinamide bonds in S100A8 produced by hypochlorite oxidationJ Biol Chem2763339333401PubMedCrossRefGoogle Scholar
  55. Sahoo, R, Dutta, T, Das, A, Sinha Ray, S, Sengupta, R, Ghosh, S 2006Effect of nitrosative stress on Schizosaccharomyces pombe: inactivation of glutathione reductase by peroxynitriteFree Radic Biol Med40625631PubMedCrossRefGoogle Scholar
  56. Salmeen, A, Andersen, JN, Myers, MP, Meng, TC, Hinks, JA, Tonks, NK, Barford, D 2003Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediateNature423769773PubMedCrossRefGoogle Scholar
  57. Salmeen, A, Barford, D 2005Functions and mechanisms of redox regulation of cysteine-based phosphatasesAntioxid Redox Signal7560577PubMedCrossRefGoogle Scholar
  58. Saurin, AT, Neubert, H, Brennan, JP, Eaton, P 2004Widespread sulfenic acid formation in tissues in response to hydrogen peroxideProc Natl Acad Sci USA1011798217987PubMedCrossRefGoogle Scholar
  59. Schafer, FQ, Buettner, GR 2001Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione coupleFree Radic Biol Med3011911212PubMedCrossRefGoogle Scholar
  60. Schnitzer, JE, Sung, A, Horvat, R, Bravo, J 1992Preferential interaction of albumin-binding proteins, gp30 and gp18, with conformationally modified albumins. Presence in many cells and tissues with a possible role in catabolismJ Biol Chem2672454424553PubMedGoogle Scholar
  61. Stamler, JS, Simon, DI, Osborne, JA, Mullins, ME, Jaraki, O, Michel, T, Singel, DJ, Loscalzo, J 1992S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compoundsProc Natl Acad Sci USA89444448PubMedCrossRefGoogle Scholar
  62. Stewart, AJ, Blindauer, CA, Berezenko, S, Sleep, D, Tooth, D, Sadler, PJ 2005Role of Tyr84 in controlling the reactivity of Cys34 of human albuminFebs J272353362PubMedCrossRefGoogle Scholar
  63. Sugio, S, Kashima, A, Mochizuki, S, Noda, M, Kobayashi, K 1999Crystal structure of human serum albumin at 2.5 A resolutionProtein Eng12439446PubMedCrossRefGoogle Scholar
  64. Surdhar, PS, Armstrong, DA 1986Redox potentials of some sulfur-containing radicalsJ Phys Chem9059155917CrossRefGoogle Scholar
  65. Takakura, K, Beckman, JS, MacMillan-Crow, LA, Crow, JP 1999Rapid and irreversible inactivation of protein tyrosine phosphatases PTP1B, CD45, and LAR by peroxynitriteArch Biochem Biophys369197207PubMedCrossRefGoogle Scholar
  66. Tomida, M, Ishimaru, J, Hayashi, T, Nakamura, K, Murayama, K, Era, S 2003The redox states of serum and synovial fluid of patients with temporomandibular joint disordersJpn J Physiol53351355PubMedCrossRefGoogle Scholar
  67. Torchinsky, YM 1981Sulfur in proteinsPergamon Press LtdOxfordGoogle Scholar
  68. Trujillo, M, Budde, H, Pineyro, MD, Stehr, M, Robello, C, Flohe, L, Radi, R 2004Trypanosoma brucei and Trypanosoma cruzi tryparedoxin peroxidases catalytically detoxify peroxynitrite via oxidation of fast reacting thiolsJ Biol Chem2793417534182PubMedCrossRefGoogle Scholar
  69. Trujillo, M, Radi, R 2002Peroxynitrite reaction with the reduced and the oxidized forms of lipoic acid: new insights into the reaction of peroxynitrite with thiolsArch Biochem Biophys3979198PubMedCrossRefGoogle Scholar
  70. van der Vliet, A, Hoen, PA, Wong, PS, Bast, A, Cross, CE 1998Formation of S-nitrosothiols via direct nucleophilic nitrosation of thiols by peroxynitrite with elimination of hydrogen peroxideJ Biol Chem2733025530262PubMedCrossRefGoogle Scholar
  71. van Montfort, RL, Congreve, M, Tisi, D, Carr, R, Jhoti, H 2003Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1BNature423773777PubMedCrossRefGoogle Scholar
  72. Wilson, JM, Wu, D, Motiu-DeGrood, R, Hupe, DJ 1980A spectrophotometric method for studying the rates of reaction of disulfides with protein thiol groups applied to bovine serum albuminJ Am Chem Soc102359363CrossRefGoogle Scholar
  73. Wink, DA, Nims, RW, Darbyshire, JF, Christodoulou, D, Hanbauer, I, Cox, GW, Laval, F, Laval, J, Cook, JA, Krishna, MC,  et al. 1994Reaction kinetics for nitrosation of cysteine and glutathione in aerobic nitric oxide solutions at neutral pH. Insights into the fate and physiological effects of intermediates generated in the NO/O2 reactionChem Res Toxicol7519525PubMedCrossRefGoogle Scholar
  74. Winterbourn, CC, Metodiewa, D 1999Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxideFree Radic Biol Med27322328PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • S. Carballal
    • 1
    • 2
    • 3
  • B. Alvarez
    • 1
    • 3
  • L. Turell
    • 1
    • 3
  • H. Botti
    • 2
    • 3
  • B. A. Freeman
    • 4
  • R. Radi
    • 2
    • 3
  1. 1.Laboratorio de Enzimología, Facultad de CienciasUniversidad de la RepúblicaMontevideoUruguay
  2. 2.Departamento de Bioquímica, Facultad de MedicinaUniversidad de la RepúblicaMontevideoUruguay
  3. 3.Center for Free Radical and Biomedical ResearchUniversidad de la RepúblicaMontevideoUruguay
  4. 4.Department of PharmacologyUniversity of Pittsburgh Medical CenterPittsburghUSA

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