Protein sulfenic acid formation: from cellular damage to redox regulation.

Protein sulfenic acid formation has long been regarded as unwanted damage caused by reactive oxygen species (ROS). However, over the past 10 years, accumulating evidence has shown that the reversible oxidation of cysteine thiol groups to sulfenic acid functions as a redox-based signal transduction mechanism. Here, we review the mechanisms of sulfenic acid formation by ROS. We present some of the most important roles played by sulfenic acids in living cells as well as the pathways that regulate sulfenic acid formation. We highlight the experimental tools that have been developed to study the cellular sulfenome and show how computational approaches might help to better understand the mechanisms of sulfenic acid formation.

[1]  J. S. Francisco,et al.  General-acid-catalyzed reactions of hypochlorous acid and acetyl hypochlorite with chlorite ion. , 2000, Inorganic chemistry.

[2]  Patrizia Rizzu,et al.  Mutations in the DJ-1 Gene Associated with Autosomal Recessive Early-Onset Parkinsonism , 2002, Science.

[3]  J. Fetrow,et al.  The Requirement of Reversible Cysteine Sulfenic Acid Formation for T Cell Activation and Function1 , 2007, The Journal of Immunology.

[4]  N. Zhang,et al.  The reaction of superoxide radical anion with dithiothreitol: a chain process , 1991 .

[5]  Cong-Zhao Zhou,et al.  Glutathionylation‐triggered conformational changes of glutaredoxin Grx1 from the yeast Saccharomyces cerevisiae , 2008, Proteins.

[6]  Douglas S Rehder,et al.  Cysteine sulfenic acid as an intermediate in disulfide bond formation and nonenzymatic protein folding. , 2010, Biochemistry.

[7]  L. Flohé,et al.  Kinetics of peroxiredoxins and their role in the decomposition of peroxynitrite. , 2007, Sub-cellular biochemistry.

[8]  S. Rhee,et al.  Reduction of Cysteine Sulfinic Acid by Sulfiredoxin Is Specific to 2-Cys Peroxiredoxins* , 2005, Journal of Biological Chemistry.

[9]  P. Karplus,et al.  Analysis of the link between enzymatic activity and oligomeric state in AhpC, a bacterial peroxiredoxin. , 2005, Biochemistry.

[10]  R. Hondal,et al.  Differing views of the role of selenium in thioredoxin reductase , 2011, Amino Acids.

[11]  Kate S Carroll,et al.  Expanding the functional diversity of proteins through cysteine oxidation. , 2008, Current opinion in chemical biology.

[12]  J. Helmann,et al.  The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[13]  C. Rodrigues-Pousada,et al.  Two redox centers within Yap1 for H2O2 and thiol-reactive chemicals signaling. , 2003, Free radical biology & medicine.

[14]  H. Sies,et al.  Oxidation of glutathione by the superoxide radical to the disulfide and the sulfonate yielding singlet oxygen. , 1983, European journal of biochemistry.

[15]  Jacquelyn S. Fetrow,et al.  PREX: PeroxiRedoxin classification indEX, a database of subfamily assignments across the diverse peroxiredoxin family , 2010, Nucleic Acids Res..

[16]  Paul H. Bessette,et al.  Reduction of the periplasmic disulfide bond isomerase, DsbC, occurs by passage of electrons from cytoplasmic thioredoxin , 1997, Journal of bacteriology.

[17]  Michael Schrader,et al.  Peroxisomes and oxidative stress. , 2006, Biochimica et biophysica acta.

[18]  J. Schneider,et al.  Arsenic(III) species inhibit oxidative protein folding in vitro. , 2009, Biochemistry.

[19]  U. Jakob,et al.  Chaperone Activity with a Redox Switch , 1999, Cell.

[20]  L. Poole,et al.  Identification of cysteine sulfenic acid in AhpC of alkyl hydroperoxide reductase. , 2002, Methods in enzymology.

[21]  M. Ashby,et al.  Thiocyanate is an efficient endogenous scavenger of the phagocytic killing agent hypobromous acid. , 2006, Chemical research in toxicology.

[22]  Rafael Radi,et al.  Factors affecting protein thiol reactivity and specificity in peroxide reduction. , 2011, Chemical research in toxicology.

[23]  D. Liebler,et al.  Provided for Non-commercial Research and Educational Use Only. Not for Reproduction, Distribution or Commercial Use. Use of Dimedone-based Chemical Probes for Sulfenic Acid Detection: Methods to Visualize and Identify Labeled Proteins Author's Personal Copy , 2022 .

[24]  A. Caccuri,et al.  Proton release upon glutathione binding to glutathione transferase P1-1: kinetic analysis of a multistep glutathione binding process. , 1998, Biochemistry.

[25]  T. Niki,et al.  The Crystal Structure of DJ-1, a Protein Related to Male Fertility and Parkinson's Disease* , 2003, Journal of Biological Chemistry.

[26]  L. Poole,et al.  The catalytic mechanism of peroxiredoxins. , 2007, Sub-cellular biochemistry.

[27]  L. Poole,et al.  Novel application of 7-chloro-4-nitrobenzo-2-oxa-1,3-diazole to identify cysteine sulfenic acid in the AhpC component of alkyl hydroperoxide reductase. , 1997, Biochemistry.

[28]  M. J. Wood,et al.  Formation, reactivity, and detection of protein sulfenic acids. , 2010, Chemical research in toxicology.

[29]  G. Church,et al.  Cloning and sequencing of thiol-specific antioxidant from mammalian brain: alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[30]  S. Rhee,et al.  Characterization of Mammalian Sulfiredoxin and Its Reactivation of Hyperoxidized Peroxiredoxin through Reduction of Cysteine Sulfinic Acid in the Active Site to Cysteine* , 2004, Journal of Biological Chemistry.

[31]  L. Flohé Changing paradigms in thiology from antioxidant defense toward redox regulation. , 2010, Methods in enzymology.

[32]  Kate S Carroll,et al.  Mining the thiol proteome for sulfenic acid modifications reveals new targets for oxidation in cells. , 2009, ACS chemical biology.

[33]  Stefano Toppo,et al.  A comparison of thiol peroxidase mechanisms. , 2011, Antioxidants & redox signaling.

[34]  R. Armstrong,et al.  Mechanistic imperatives for the evolution of glutathione transferases. , 1998, Current opinion in chemical biology.

[35]  C. Winterbourn,et al.  The High Reactivity of Peroxiredoxin 2 with H2O2 Is Not Reflected in Its Reaction with Other Oxidants and Thiol Reagents* , 2007, Journal of Biological Chemistry.

[36]  T. C. Bruice,et al.  The Structure of Anthraquinone-1-sulfenic Acid (Fries' Acid) and Related Compounds , 1959 .

[37]  C. Winterbourn,et al.  Mitochondrial peroxiredoxin involvement in antioxidant defence and redox signalling. , 2010, The Biochemical journal.

[38]  M. Enescu,et al.  Mechanism of cysteine oxidation by a hydroxyl radical: a theoretical study. , 2006, Chemphyschem : a European journal of chemical physics and physical chemistry.

[39]  R. E. Huber,et al.  Comparison of the chemical properties of selenocysteine and selenocystine with their sulfur analogs. , 1967, Archives of biochemistry and biophysics.

[40]  H. Forman Use and abuse of exogenous H2O2 in studies of signal transduction. , 2007, Free radical biology & medicine.

[41]  H. Lilie,et al.  The redox-switch domain of Hsp33 functions as dual stress sensor , 2007, Nature Structural &Molecular Biology.

[42]  P. Karplus,et al.  Peroxiredoxin Evolution and the Regulation of Hydrogen Peroxide Signaling , 2003, Science.

[43]  A J Sinskey,et al.  Oxidized redox state of glutathione in the endoplasmic reticulum. , 1992, Science.

[44]  G. Buettner The pecking order of free radicals and antioxidants: lipid peroxidation, alpha-tocopherol, and ascorbate. , 1993, Archives of biochemistry and biophysics.

[45]  M. Davies,et al.  Hypochlorous acid-mediated oxidation of lipid components and antioxidants present in low-density lipoproteins: absolute rate constants, product analysis, and computational modeling. , 2003, Chemical research in toxicology.

[46]  L. Flohé,et al.  Glutathione peroxidase: A selenoenzyme , 1973, FEBS letters.

[47]  T. Taira,et al.  DJ-1, a novel oncogene which transforms mouse NIH3T3 cells in cooperation with ras. , 1997, Biochemical and biophysical research communications.

[48]  Carla Mattos,et al.  Structural mechanism of oxidative regulation of the phosphatase Cdc25B via an intramolecular disulfide bond. , 2005, Biochemistry.

[49]  E. Knapp,et al.  One-electron reduction potential for oxygen- and sulfur-centered organic radicals in protic and aprotic solvents. , 2005, Journal of the American Chemical Society.

[50]  Goedele Roos,et al.  Enzymatic catalysis: the emerging role of conceptual density functional theory. , 2009, The journal of physical chemistry. B.

[51]  Kate S. Carroll,et al.  Profiling protein thiol oxidation in tumor cells using sulfenic acid-specific antibodies , 2009, Proceedings of the National Academy of Sciences.

[52]  K. Rokutan,et al.  Protein S-thiolation and dethiolation during the respiratory burst in human monocytes. A reversible post-translational modification with potential for buffering the effects of oxidant stress. , 1996, Journal of immunology.

[53]  M. Davies,et al.  Absolute rate constants for the reaction of hypochlorous acid with protein side chains and peptide bonds. , 2001, Chemical research in toxicology.

[54]  M. Enescu,et al.  A computational study of thiolate and selenolate oxidation by hydrogen peroxide. , 2005, Chemphyschem : a European journal of chemical physics and physical chemistry.

[55]  Michael Reth,et al.  Hydrogen peroxide as second messenger in lymphocyte activation , 2002, Nature Immunology.

[56]  P Andrew Karplus,et al.  Structural evidence that peroxiredoxin catalytic power is based on transition-state stabilization. , 2010, Journal of molecular biology.

[57]  W. Lowther,et al.  Protein Engineering of the Quaternary Sulfiredoxin·Peroxiredoxin Enzyme·Substrate Complex Reveals the Molecular Basis for Cysteine Sulfinic Acid Phosphorylation* , 2009, The Journal of Biological Chemistry.

[58]  M. J. Wood,et al.  A genetically encoded probe for cysteine sulfenic acid protein modification in vivo. , 2007, Biochemistry.

[59]  J. Collet,et al.  Structure, function, and mechanism of thioredoxin proteins. , 2010, Antioxidants & redox signaling.

[60]  J. Collet,et al.  Pathways of disulfide bond formation in Escherichia coli. , 2006, The international journal of biochemistry & cell biology.

[61]  H. Forman,et al.  Signaling functions of reactive oxygen species. , 2010, Biochemistry.

[62]  R. Friesner,et al.  Computing Redox Potentials in Solution: Density Functional Theory as A Tool for Rational Design of Redox Agents , 2002 .

[63]  B. Remington,et al.  Cysteine pKa depression by a protonated glutamic acid in human DJ-1. , 2008, Biochemistry.

[64]  Wenbo Zhou,et al.  DJ-1 Up-regulates Glutathione Synthesis during Oxidative Stress and Inhibits A53T α-Synuclein Toxicity* , 2005, Journal of Biological Chemistry.

[65]  S. Patai,et al.  The chemistry of peroxides , 2006 .

[66]  Miles Congreve,et al.  Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B , 2003, Nature.

[67]  R. Fisher,et al.  Crystal structure of S‐glutathiolated carbonic anhydrase III , 2000, FEBS letters.

[68]  G. Storz,et al.  Oxidative stress. , 1999, Current opinion in microbiology.

[69]  J. Imlay,et al.  Balance between Endogenous Superoxide Stress and Antioxidant Defenses , 1998, Journal of bacteriology.

[70]  R. Armstrong,et al.  Structure, catalytic mechanism, and evolution of the glutathione transferases. , 1997, Chemical research in toxicology.

[71]  J. Denu,et al.  Specific and reversible inactivation of protein tyrosine phosphatases by hydrogen peroxide: evidence for a sulfenic acid intermediate and implications for redox regulation. , 1998, Biochemistry.

[72]  M. Trujillo,et al.  Pre-steady state kinetic characterization of human peroxiredoxin 5: taking advantage of Trp84 fluorescence increase upon oxidation. , 2007, Archives of biochemistry and biophysics.

[73]  D. Parsonage,et al.  Protein‐sulfenic acid stabilization and function in enzyme catalysis and gene regulation , 1993, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[74]  G. Petsko,et al.  The oxidation state of DJ-1 regulates its chaperone activity toward alpha-synuclein. , 2006, Journal of molecular biology.

[75]  L. Flohé,et al.  Kinetics and Redox-Sensitive Oligomerisation Reveal Negative Subunit Cooperativity in Tryparedoxin Peroxidase of Trypanosoma brucei brucei , 2003, Biological chemistry.

[76]  T. Creighton,et al.  Kinetic role of a meta-stable native-like two-disulphide species in the folding transition of bovine pancreatic trypsin inhibitor. , 1984, Journal of molecular biology.

[77]  P. Wardman,et al.  Kinetic factors that control the fate of thiyl radicals in cells. , 1995, Methods in enzymology.

[78]  Mark A. Wilson,et al.  The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[79]  R. Radi,et al.  Sulfenic acid--a key intermediate in albumin thiol oxidation. , 2009, Journal of chromatography. B, Analytical technologies in the biomedical and life sciences.

[80]  T. Dawson,et al.  DJ-1 gene deletion reveals that DJ-1 is an atypical peroxiredoxin-like peroxidase , 2007, Proceedings of the National Academy of Sciences.

[81]  W. Lowther,et al.  Provided for Non-commercial Research and Educational Use Only. Not for Reproduction, Distribution or Commercial Use , 2022 .

[82]  J. Fetrow,et al.  Fluorescent and affinity-based tools to detect cysteine sulfenic acid formation in proteins. , 2007, Bioconjugate chemistry.

[83]  Paul H. Bessette,et al.  In Vivo and in Vitro Function of theEscherichia coli Periplasmic Cysteine Oxidoreductase DsbG* , 1999, The Journal of Biological Chemistry.

[84]  J. Helmann,et al.  Bacillithiol is an antioxidant thiol produced in Bacilli , 2009, Nature chemical biology.

[85]  Robert A. LaRossa,et al.  DNA Microarray-Mediated Transcriptional Profiling of the Escherichia coli Response to Hydrogen Peroxide , 2001, Journal of bacteriology.

[86]  M. Trujillo,et al.  Kinetic studies on peroxynitrite reduction by peroxiredoxins. , 2008, Methods in enzymology.

[87]  R. Glockshuber,et al.  A single dipeptide sequence modulates the redox properties of a whole enzyme family. , 1998, Folding & design.

[88]  S. Rhee,et al.  Identification of a New Type of Mammalian Peroxiredoxin That Forms an Intramolecular Disulfide as a Reaction Intermediate* , 2000, The Journal of Biological Chemistry.

[89]  L. Rice,et al.  Unexpected Inhibition of Peptidoglycan LD-Transpeptidase from Enterococcus faecium by the β-Lactam Imipenem* , 2007, Journal of Biological Chemistry.

[90]  M. Toledano,et al.  ATP-dependent reduction of cysteine–sulphinic acid by S. cerevisiae sulphiredoxin , 2003, Nature.

[91]  R. Wait,et al.  Protein Sulfenation as a Redox Sensor , 2007, Molecular & Cellular Proteomics.

[92]  J. Imlay Cellular defenses against superoxide and hydrogen peroxide. , 2008, Annual review of biochemistry.

[93]  M. A. Edeling,et al.  Crystal structures of the DsbG disulfide isomerase reveal an unstable disulfide , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[94]  H. Gilbert Molecular and cellular aspects of thiol-disulfide exchange. , 2006, Advances in enzymology and related areas of molecular biology.

[95]  M. Cha,et al.  Thioredoxin-linked peroxidase from human red blood cell: evidence for the existence of thioredoxin and thioredoxin reductase in human red blood cell. , 1995, Biochemical and biophysical research communications.

[96]  J. Davies,et al.  Coenzyme A Disulfide Reductase, the Primary Low Molecular Weight Disulfide Reductase from Staphylococcus aureus , 1998, The Journal of Biological Chemistry.

[97]  S. Toppo,et al.  Catalytic mechanisms and specificities of glutathione peroxidases: variations of a basic scheme. , 2009, Biochimica et biophysica acta.

[98]  Goedele Roos,et al.  The Activation of Electrophile, Nucleophile and Leaving Group during the Reaction Catalysed by pI258 Arsenate Reductase , 2006, Chembiochem : a European journal of chemical biology.

[99]  M. Davies,et al.  Hypochlorite-induced oxidation of amino acids, peptides and proteins , 2003, Amino Acids.

[100]  R. Glockshuber,et al.  The redox properties of protein disulfide isomerase (DsbA) of Escherichia coli result from a tense conformation of its oxidized form. , 1993, Journal of molecular biology.

[101]  M. Davies,et al.  Kinetic analysis of the reactions of hypobromous acid with protein components: implications for cellular damage and use of 3-bromotyrosine as a marker of oxidative stress. , 2004, Biochemistry.

[102]  M. Ashby,et al.  Reactive sulfur species: kinetics and mechanisms of the oxidation of cysteine by hypohalous acid to give cysteine sulfenic acid. , 2007, Journal of the American Chemical Society.

[103]  N. Tonks,et al.  Protein tyrosine phosphatases: from genes, to function, to disease , 2006, Nature Reviews Molecular Cell Biology.

[104]  H. Schlegel,et al.  Oxidation of Amines and Sulfides with Hydrogen Peroxide and Alkyl Hydrogen Peroxide. The Nature of the Oxygen-Transfer Step , 1994 .

[105]  Kate S. Carroll,et al.  A chemical approach for detecting sulfenic acid-modified proteins in living cells. , 2008, Molecular bioSystems.

[106]  J. Helmann,et al.  Oxidant‐dependent switching between reversible and sacrificial oxidation pathways for Bacillus subtilis OhrR , 2008, Molecular microbiology.

[107]  W. Lowther,et al.  Structure of the sulphiredoxin–peroxiredoxin complex reveals an essential repair embrace , 2008, Nature.

[108]  K. Rokutan,et al.  Phagocytosis and stimulation of the respiratory burst by phorbol diester initiate S-thiolation of specific proteins in macrophages. , 1991, Journal of immunology.

[109]  S. Barnes,et al.  Sulfenic acid formation in human serum albumin by hydrogen peroxide and peroxynitrite. , 2003, Biochemistry.

[110]  K. Davies,et al.  Calcium and oxidative stress: from cell signaling to cell death. , 2002, Molecular immunology.

[111]  Z. A. Wood,et al.  Structure, mechanism and regulation of peroxiredoxins. , 2003, Trends in biochemical sciences.

[112]  J. Tanner,et al.  Redox regulation of protein tyrosine phosphatases: structural and chemical aspects. , 2011, Antioxidants & redox signaling.

[113]  C. Winterbourn Superoxide as an intracellular radical sink. , 1993, Free radical biology & medicine.

[114]  L. Valgimigli,et al.  The redox chemistry of sulfenic acids. , 2010, Journal of the American Chemical Society.

[115]  B. Freeman,et al.  Sulfenic acid in human serum albumin , 2006, Amino Acids.

[116]  J. Helmann,et al.  A complex thiolate switch regulates the Bacillus subtilis organic peroxide sensor OhrR , 2007, Proceedings of the National Academy of Sciences.

[117]  S. Rhee,et al.  Peroxiredoxin, a Novel Family of Peroxidases , 2001, IUBMB life.

[118]  H. Forman Reactive oxygen species and α,β‐unsaturated aldehydes as second messengers in signal transduction , 2010, Annals of the New York Academy of Sciences.

[119]  Michael P. Myers,et al.  Redox regulation of protein tyrosine phosphatase 1B involves a sulphenyl-amide intermediate , 2003, Nature.

[120]  P. Karplus,et al.  Substrate specificity and redox potential of AhpC, a bacterial peroxiredoxin , 2008, Proceedings of the National Academy of Sciences.

[121]  Silvio C. E. Tosatto,et al.  The catalytic site of glutathione peroxidases. , 2008, Antioxidants & redox signaling.

[122]  Vincenzo Bonifati,et al.  Genetics of parkinsonism. , 2007, Parkinsonism & related disorders.

[123]  J. Rudolph,et al.  Catalytic and chemical competence of regulation of cdc25 phosphatase by oxidation/reduction. , 2003, Biochemistry.

[124]  B. Freeman,et al.  Reactivity of sulfenic acid in human serum albumin. , 2008, Biochemistry.

[125]  Kap-Seok Yang,et al.  Reversing the Inactivation of Peroxiredoxins Caused by Cysteine Sulfinic Acid Formation , 2003, Science.

[126]  Walter Thiel,et al.  QM/MM studies of enzymes. , 2007, Current opinion in chemical biology.

[127]  K. Rokutan,et al.  S-thiolation of individual human neutrophil proteins including actin by stimulation of the respiratory burst: evidence against a role for glutathione disulfide. , 1994, Archives of biochemistry and biophysics.

[128]  Hao Hu,et al.  Free energies of chemical reactions in solution and in enzymes with ab initio quantum mechanics/molecular mechanics methods. , 2008, Annual review of physical chemistry.

[129]  P. Karplus,et al.  Structural changes common to catalysis in the Tpx peroxiredoxin subfamily. , 2009, Journal of molecular biology.

[130]  Kate S. Carroll,et al.  A Periplasmic Reducing System Protects Single Cysteine Residues from Oxidation , 2009, Science.

[131]  M. Trujillo,et al.  Thiol and sulfenic acid oxidation of AhpE, the one-cysteine peroxiredoxin from Mycobacterium tuberculosis: kinetics, acidity constants, and conformational dynamics. , 2009, Biochemistry.

[132]  Mark A. Wilson,et al.  The oxidation state of DJ-1 regulates its chaperone activity toward α-synuclein , 2006 .

[133]  P. Karplus,et al.  AhpF and other NADH:peroxiredoxin oxidoreductases, homologues of low Mr thioredoxin reductase. , 2000, European journal of biochemistry.

[134]  S. Rhee,et al.  Irreversible inactivation of glutathione peroxidase 1 and reversible inactivation of peroxiredoxin II by H2O2 in red blood cells. , 2010, Antioxidants & redox signaling.

[135]  Goedele Roos,et al.  Origin of the pKa Perturbation of N-Terminal Cysteine in α- and 310-Helices: A Computational DFT Study , 2006 .

[136]  M. Rigoulet,et al.  Mitochondrial ROS generation and its regulation: mechanisms involved in H(2)O(2) signaling. , 2011, Antioxidants & redox signaling.

[137]  L. Poole,et al.  Redox regulation and trapping sulfenic acid in the peroxide-sensitive human mitochondrial branched chain aminotransferase. , 2008, Methods in molecular biology.

[138]  C. Winterbourn,et al.  Reactivity of biologically important thiol compounds with superoxide and hydrogen peroxide. , 1999, Free radical biology & medicine.

[139]  R. Okazaki,et al.  Synthesis, Structure, and Reactions of a Sulfenic Acid Bearing a Novel Bowl-Type Substituent: The First Synthesis of a Stable Sulfenic Acid by Direct Oxidation of a Thiol , 1997 .

[140]  P. B. Chock,et al.  Regulation of PTP1B via glutathionylation of the active site cysteine 215. , 1999, Biochemistry.

[141]  Goedele Roos,et al.  How Thioredoxin Dissociates Its Mixed Disulfide , 2009, PLoS Comput. Biol..

[142]  P Andrew Karplus,et al.  Structure-based Insights into the Catalytic Power and Conformational Dexterity of Peroxiredoxins , 2022 .

[143]  Tsuyoshi Inoue,et al.  Oxidation of archaeal peroxiredoxin involves a hypervalent sulfur intermediate , 2008, Proceedings of the National Academy of Sciences.

[144]  A. Saurin,et al.  Widespread sulfenic acid formation in tissues in response to hydrogen peroxide , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[145]  Mark A. Wilson,et al.  Formation of a Stabilized Cysteine Sulfinic Acid Is Critical for the Mitochondrial Function of the Parkinsonism Protein DJ-1* , 2009, Journal of Biological Chemistry.

[146]  G. Storz,et al.  Activation of the OxyR transcription factor by reversible disulfide bond formation. , 1998, Science.

[147]  Molly M Gallogly,et al.  Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. , 2008, Antioxidants & redox signaling.

[148]  A. Holmgren,et al.  Substitution of the conserved tryptophan 31 in Escherichia coli thioredoxin by site-directed mutagenesis and structure-function analysis. , 1991, The Journal of biological chemistry.

[149]  S. Rhee,et al.  Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. , 2005, Free radical biology & medicine.

[150]  C. Winterbourn,et al.  Thiol chemistry and specificity in redox signaling. , 2008, Free radical biology & medicine.

[151]  L. Folkes,et al.  Reactivity of hydrogen sulfide with peroxynitrite and other oxidants of biological interest. , 2011, Free radical biology & medicine.

[152]  C. Winterbourn,et al.  Reconciling the chemistry and biology of reactive oxygen species. , 2008, Nature chemical biology.

[153]  M. J. Wood,et al.  Molecular Mechanism of Oxidative Stress Perception by the Orp1 Protein* , 2007, Journal of Biological Chemistry.

[154]  M. Trujillo,et al.  The peroxidase and peroxynitrite reductase activity of human erythrocyte peroxiredoxin 2. , 2009, Archives of biochemistry and biophysics.

[155]  P. Karplus,et al.  Protein sulfenic acids in redox signaling. , 2004, Annual review of pharmacology and toxicology.

[156]  R. Brigelius-Flohé Tissue-specific functions of individual glutathione peroxidases. , 1999, Free radical biology & medicine.

[157]  Kate S. Carroll,et al.  Chemical Dissection of an Essential Redox Switch in Yeast , 2022 .

[158]  R. Radi,et al.  Oxidation of the albumin thiol to sulfenic acid and its implications in the intravascular compartment. , 2009, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[159]  H. Schlegel,et al.  Nature of the transition structure for oxygen atom transfer from a hydroperoxide. Theoretical comparison between water oxide and ammonia oxide , 1991 .

[160]  M. Coote,et al.  A universal approach for continuum solvent pKa calculations: are we there yet? , 2009 .