Biological Chemistry of Hydrogen Peroxide
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1 Biological Chemistry of Hydrogen Peroxide Christine Winterbourn Department of Pathology University of Otago, Christchurch New Zealand
2 Hydrogen Peroxide Intermediate in reduction of oxygen to water A major biological reactive oxygen species e - O 2.- O 2 e - oxygen superoxide radical Often (incorrectly) considered synonymously with ROS Widely considered as transmitter of redox signals H 2 O 2 hydrogen peroxide e - OH. e - hydroxyl radical H 2 O water
3 Hydrogen Peroxide Strong 2 electron oxidant: E o (ph 7) H 2 O 2 / H 2 O = 1.32 V For comparison HOCl / Cl - = 1.08 V and ONOO - / NO 2- = 1.20 V Reactions slow due to high activation energy Activation energy kinetics Relative rates with GSH: H 2 O 2 : ONOO - : HOCl ΔE o thermodynamics
4 Hydrogen Peroxide Modest 1 electron oxidant: 1 electron reduction gives very strong oxidant (hydroxyl radical) H 2 O 2 OH H 2 O E o (ph 7) 0.32 V 2.31 V
5 Hydrogen Peroxide Uncharged Diffusible Penetrates membranes Membrane transport may be facilitated by aquaporin(s)
6 Sources of Hydrogen Peroxide Indirect via superoxide dismutation Mitochondrial electron transport chain NADPH oxidases (NOXs and DUOXs) Auto-oxidation of heme proteins (hemoglobin, nitric oxide synthase) Redox cycling and autoxidizable xenobiotics Direct enzymatic sources - flavoproteins Peroxisomes eg β-oxidation of acyl-coa Polyamine oxidase Urate oxidase Endoplasmic reticulum eg Ero1 Radiation - UV and γ
7 Does SOD increase hydrogen peroxide production? 2O H + O 2 + H 2 O 2 NO. Increasing the dismutation rate does not increase the amount of product formed. There are provisos SOD increases [H 2 O 2 ] by preventing 2O reductant 2O 2 + product SOD decreases [H 2 O 2 ] by preventing 2O oxidant 2H 2 O 2 + product SOD increases [H 2 O 2 ] by displacing an unfavorable equilibrium semiquinone + O 2 quinone + O - 2
8 Does SOD increase hydrogen peroxide production? 2O H + O 2 + H 2 O 2 NO. Increasing the dismutation rate does not increase the amount of product. There are provisos SOD increases [H 2 O 2 ] by preventing 2O reductant 2O 2 + product SOD decreases [H 2 O 2 ] by preventing 2O oxidant 2H 2 O 2 + product SOD increases [H 2 O 2 ] by displacing an unfavorable equilibrium semiquinone + O 2 quinone + O - 2 SOD
9 Defenses against Hydrogen Peroxide Catalase heme enzyme mainly peroxisomes 2H 2 O 2 O 2 + H 2 O Glutathione peroxidase selenoproteins H 2 O 2 + 2GSH GSSG + 2H 2 O GSSG + NADPH + H + 2GSH + NADP + Peroxiredoxins thiol proteins H 2 O 2 + 2PrxSH PrxSSPrx + 2H 2 O PrxSSPrx + Trx(SH) 2 2PrxSH + Trx(SS) Trx(SS) + NADPH + H + Trx(SH) 2 + NADP + H 2 O 2 rate constants in range M -1 s -1
10 Rate Constants and Kinetics A + B products Second order reaction Rate = k [A].[ B] where k is rate constant; units M -1 s -1 Pseudo first order reaction if one reactant (B) is in excess Rate = k [A] Half life (t 1/2 ) = 0.7 / k seconds Diffusion controlled reaction ( OH reactions) k ~ M -1 s -1 in presence of 1 mm B, t 1/2 ~ 1 microsecond If k = 1 M -1 s -1, t 1/2 ~ 10 min
11 Reactions of Hydrogen Peroxide One electron oxidations - involve transition metals - generate hydroxyl radicals or higher oxidation states of metal - initiators of free radical processes Fenton reaction ligand- Fe 2+ + H 2 O 2 [ ligand- Fe(IV)=O ] + H 2 O ferryl H + ligand-fe 3+ + OH Imlay, Ann Rev Biochem 77, 755 (2008)
12 Fenton reaction Fe 2+ + H 2 O 2 Fe 3+ + OH Generates highly reactive, indiscriminate, hydroxyl radical. Fe 2+ recycled by reductants, eg ascorbate, GSH. Rate constant typically 5-20 x 10 3 M -1 s -1 If metal bound to protein or DNA, site- localized oxidation can occur. Protection by sequestering metal ions, eg transferrin, ferritin.
13 Reactions with Heme Peroxidases Fast reactions - rate constants typically ~10 8 M -1 s -1 Activate H 2 O 2 to generate more reactive 1e and 2e oxidants Major mechanism for radical generation. Mammalian examples Myeloperoxidase Eosinophil peroxidase Lactoperoxidase Thyroid peroxidase Vascular peroxidase Surrogate peroxidases Hemoglobin Myoglobin Cytochromes Davies et al, ARS 10, 1199 (2008)
14 Myeloperoxidase Neutrophil protein, important for antimicrobial activity, contributes to tissue damage in inflammation. HOCl Cl - MP 3+ H + +R H 2 O 2 RH Compound I RH R + H + Compound II R examples Tyrosine Nitrite Polyphenols Serotonin Ascorbate
15 Two Electron Reactions of Hydrogen Peroxide Generally slow Selenium and sulfur centres most reactive Few biological substrates are competitive Rate constants (M -1 s -1 ) GPxs peroxiredoxins oxyr Tyr phosphatases GSH Met
16 Activation of H 2 O 2 by reaction with bicarbonate H 2 O 2 + HCO 3 - HCO H 2 O peroxymonocarbonate Peroxymonocarbonate is ~100 fold more reactive than H 2 O 2 BUT K ~ 0.35 so at physiological bicarbonate HCO 4- : H 2 O 2 = 0.02 AND Forward reaction is slow so rate of conversion of H 2 O 2 to HCO 4- is only 3% per min Medinas et al IUBMB Life 59, 255 (2007)
17 Hydrogen Peroxide and Redox Signaling Many cellular responses to oxidative stress or receptor activation transmitted by redox signals. Receptor binding can cause NOX activation. Hydrogen peroxide implicated as transmitter of signal. Thiol proteins considered to be oxidant sensitive targets. Most thiols react slowly with H 2 O 2. How does redox signaling occur?
18 Identifying Physiological Targets Determined by reaction rates and concentrations. Reactions occur in competition. Reactions that occur in isolation will not all be sufficiently favorable to occur in cells. For two substrates, the ratio of the amounts of oxidant reacting with each is given by k 1 [substrate 1] k 2 [substrate 2]
19 Thiol Chemistry Reaction of Cys with H 2 O 2 Slow reaction (ph 7.4) Cys-SH + H 2 O 2 Cys-SOH + H 2 O k = 2.4 M -1 s -1 How to facilitate reaction: Change protein environment to ionize thiol k ~ 26 M -1 s -1
20 Slow reaction (ph 7.4) Reaction of Cys with H 2 O 2 Cys-SH + H 2 O 2 Cys-SOH + H 2 O k = 2.4 M -1 s -1 How to facilitate reaction: Change protein environment to ionise thiol k ~ 26 M -1 s -1 Activate H 2 O 2 through protein interaction k = M -1 s -1
21 Thiol Oxidation by H 2 O 2 k M -1 s -1 GSH 1 2 mm Protein tyrosine µm phosphatases GAPDH ~ µm Peroxiredoxins > µm Estimated concentration
22 Simulation of potential cellular targets for H 2 O 2 GPx1 Based on rate constants and estimated cellular concentrations (k[substrate]) and assuming homogeneous system (Winterbourn Nat Chem Biol 4, 278 (2008)
23 Slow reaction (ph 7.4) Reaction of Cys with H 2 O 2 Cys-SH + H 2 O 2 Cys-SOH + H 2 O k = 2.4 M -1 s -1 How to facilitate reaction: Change protein environment to ionise thiol k ~ 26 M -1 s -1 Activate H 2 O 2 through protein interaction k = M -1 s -1 Oxidation via intermediary H 2 O 2 + R 1 SH R 1 SOH + R 2 SH R 2 SOH
24 Slow reaction (ph 7.4) Reaction of Cys with H 2 O 2 Cys-SH + H 2 O 2 Cys-SOH + H 2 O k = 2.4 M -1 s -1 How to facilitate reaction: Decrease ph Cys-S - + H 2 O 2 k = 26 M -1 s -1 Change protein environment to ionise thiol k ~ 26 M -1 s -1 Activate H 2 O 2 through protein interaction k = M -1 s -1 Oxidation via intermediary H 2 O 2 + R 1 SH R 1 SOH + R 2 SH R 2 SOH Form association with H 2 O 2 generator Winterbourn & Hampton FRBM 45, 549 (2008)
25 Examples Fast reacting thiol protein OxyR bacterial transcription factor responsive to H 2 O 2 Oxidation via intermediary YAP1- yeast transcription factor transactivated by peroxiredoxin GPx3 D'Autréaux B, Toledano MB. Nat Rev Mol Cell Biol 8, 813 (2007)
26 Peroxiredoxins Ubiquitous family of thiol proteins Present in cells at high concentration Highly reactive with H 2 O 2 2-cys and 1-cys forms Recycled by thioredoxin or GSH 22kD Monomers associate to form decamers Hall et al FEBS J 276, 2469 (2009)
27 2-Cys Peroxiredoxin / Thioredoxin Cycle Sp H S r H H 2 O 2 SOH S r H H 2 O 2 SO 2 H S r H S r H S p H S r H SOH S r H SO 2 H Thioredoxin, Thioredoxin reductase, NADPH S S S S
28 2-Cys Peroxiredoxin / Thioredoxin Cycle Sp H S r H H 2 O 2 SOH S r H H 2 O 2 SO 2 H S r H S r H S p H S r H SOH S r H SO 2 H ProteinSH Thioredoxin, Thioredoxin reductase, NADPH S S S S S r H S-SPr
29 Decamer / dimer distribution depends on oxidation state oxidation 5 Barranco-Medina et al FEBS Lett 583, 1809 (2009) Dissociation constants (K D ) Reduced Prx ~1 µm Reduced < Disulfide >> Hyperoxidized Have potential to transmit signals through both redox and conformational changes
30 Real Time Detection of Cellular Hydrogen Peroxide Production Peroxidase based Extracellular H 2 O 2 + HRP + detector detector radical coloured or fluorescent product eg Amplex red Dihydrorhodamine Dihydrodichlorofluorescein (DCF) Phenol red Amplex red Caution Radical scavengers and superoxide inhibit by scavenging detector radical
31 Hydrogen Peroxide Production by Stimulated Neutrophils Efficient detection requires SOD 1.2 H2O2 production over 15 min phenol red homovanillic acid scopoletin no SOD SOD Kettle, Carr & Winterbourn, FRBM 17, 161 (1994)
32 Detection of Intracellular Hydrogen Peroxide Production Dihydrodichlorofluorescein (DCF) DCF-diacetate DCF H 2 O 2 DCF radical DCF ox fluorescent intracellular hydrolysis transition metal or peroxidase
33 Detection of Intracellular Hydrogen Peroxide Production Dihydrodichlorofluorescein (DCF) DCF-diacetate DCF H 2 O 2 DCF radical DCF ox fluorescent intracellular hydrolysis transition metal or peroxidase Cautions DCF does not react with H 2 O 2. Potential catalysts include heme proteins, low mol wt Fe or Cu, cyt c. Also oxidized by ONOO -, HOCl, other radicals. Radical scavengers react with detector radical. Undergoes photo-oxidation. Pitfalls Not specific for H 2 O 2. Change in response could be due to catalyst (eg cyt c, lysosomal Fe) or radical scavenger (eg GSH, total thiol, added antioxidant) without any change in oxidant production.
34 Detection of Intracellular Hydrogen Peroxide Production Alternative probes Boronates Chang et al. J. Am. Chem. Soc. 2004, 126, Advantages Direct reaction with H 2 O 2. Non-radical process. Cautions Reaction is slow (low k). Also reacts with OONO -, HOCl.
35 HyPer - Detection of Intracellular Hydrogen Peroxide Production green fluorescent protein probes genetically encoded circularly permuted YFP inserted in regulatory region of oxyr HS- HSoxyR YFP H 2 O 2 S- S- Growth factor-treated cells (32 min) Advantages Specificity for H 2 O 2 High reactivity Targetable ph insensitive Belousov et al, Nat Methods. 3, 281(2006) Cautions Reversible (Trx)
36 Detection of Intracellular Hydrogen Peroxide Production RoGFP - genetically encoded modified GFP SH SH S S Conformational change alters fluorescent properties Meyer & Dick, ARS 13, 621 (2010)
37 RoGFP Thiol groups have low reactivity with H 2 O 2 Link to highly reactive sensor Yeast peroxiredoxin that transmits H 2 O 2 signal to YAP1 Advantages Specificity and high reactivity for H 2 O 2 Targetable Ratiometric Adaptable to other sensors Cautions Reversible (Trx) ph dependent
38 Hydrogen Peroxide Major biological reactive oxygen species. Participates in radical and non-radical reactions. These contribute to oxidative damage and redox signaling. Understanding of molecular mechanisms of redox signaling still limited. Critical use of probes needed to quantify and localize cellular H 2 O 2 production.
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