Riboflavin Photosensitized Oxidation of Myoglobin - American

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Riboflavin Photosensitized Oxidation of Myoglobin Juliana M. Grippa,† Andressa de Zawadzki,† Alberto B. Grossi,‡ Leif H. Skibsted,*,‡ and Daniel R. Cardoso*,† †

Instituto de Química de São Carlos, Universidade de São Paulo, Av. Trabalhador São Carlense 400, CP 780, CEP 13560-970, São Carlos, SP, Brazil ‡ Department of Food Science, University of Copenhagen, Rolighedsvej 30, DK-1958 Frederiksberg C, Denmark ABSTRACT: The reaction of the fresh meat pigment oxymyoglobin, MbFe(II)O2, and its oxidized form metmyoglobin, MbFe(III), with triplet-state riboflavin involves the pigment protein, which is oxidatively cleaved or dimerized as shown by SDS− PAGE and Western blotting. The overall rate constant for oxidation of MbFe(II)O2 by 3Rib is (3.0 ± 0.5) × 109 L·mol−1·s−1 and (3.1 ± 0.4) × 109 L·mol−1·s−1 for MbFe(III) in phosphate buffer of pH 7.4 at 25 °C as determined by laser flash photolysis. The high rates are rationalized by ground state hydrophobic interactions as detected as static quenching of fluorescence from singletexcited state riboflavin by myoglobins using time-resolved fluorescence spectroscopy and a Stern−Volmer approach. Binding of riboflavin to MbFe(III) has Ka = (1.2 ± 0.2) × 104 mol·L−1 with ΔH° = −112 ± 22 kJ·mol−1 and ΔS° = −296 ± 75 J·mol−1·K−1. For meat, riboflavin is concluded to be a photosensitizer for protein oxidation but not for discoloration. KEYWORDS: riboflavin, photooxidation, oxymyoglobin, metmyoglobin, protein cross-linking

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INTRODUCTION Riboflavin is present in the aqueous phase of milk, eggs, and muscle based foods and is as vitamin B2 an important nutrient.1 Riboflavin (Rib) or vitamin B2, as well as its biologically active forms, flavin mononucleotide, FMN, and flavin adenine dinucleotide, FAD, are very well-known to actively participate in type I and type II photosensitized oxidation reactions on exposure to visible or UV-A light in tissue or in food and beverages.2−8 The heterocyclic isoalloxazine ring of Rib, FMN, and FAD forms upon light exposure a highly fluorescent singlet state (1Rib, τ = 5 ns in water), which decays by intersystem crossing (Φisc = 0.67) to the highly reactive and long-lived triplet-excited state (τ = 15 μs) with E° = 1.77 V vs NHE in water at ambient temperature.9,10 The long-lived triplet excited state is a powerful oxidant biradical and capable of oxidizing a wide range of biomolecules like proteins, purine and pyrimidine bases, vitamins, and polyphenols with second-order rate constant approaching the diffusion limit in water in so-called type I photooxidation processes.2,6,7 Besides inducing oxidation of a wide number of biomolecules by such direct or protoncoupled electron transfer, triplet-excited riboflavin may also induce type II photooxidation by producing the reactive electrophilic singlet-excited state oxygen, 1O2, through energy transfer in a spin-allowed process (Φ = 0.68, k = 9.8 × 108 L· mol−1·s−1 in water at 25 °C).10,11 In protein rich tissue or food, type I photosensitization is dominating through rapid electron transfer or proton-coupled electron transfer from mainly tyrosine, histidine, tryptophan, and cysteine amino acid side chains of proteins to 3Rib with rates approaching the diffusion limit.12,13 In lipid rich tissue or food, oxygen quenching of 3Rib wins over chemical quenching by lipids, resulting in formation of 1O2 and subsequent type II photosensitized oxidation of lipids.2,14,15,4 Only under anaerobic conditions, type I photooxidation becomes significant © 2014 American Chemical Society

for lipids and now with a slower hydrogen atom transfer from allylic or bis-allylic positions in unsaturated lipids or in sterols to 3Rib.15 However, protein radicals formed in type I sensitized reactions in aqueous phases may subsequently initiate lipid oxidation at water/lipid interfaces coupling lipid phase oxidation with protein oxidation in the aqueous compartments of tissue and aqueous phase of foods.2 Meat and meat products are sensitive to oxidation during processing and storage. Oxidation of lipids thus leads to rancidity, while protein oxidation decreases meat tenderness, and oxidation of meat pigments is recognized as discoloration.16,17 Riboflavin sensitized oxidation has been described for proteins and lipids,12,15 however, a possible role of riboflavin in oxidation of myoglobins as meat pigments has remained unattended. We have accordingly expanded previous studies of riboflavin photosensitized oxidation of lipids and proteins to include oxymyoglobin and metmyoglobin as the fresh meat pigment and its oxidized form, respectively.

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MATERIALS AND METHODS

Chemicals and Materials. Coomassie brilliant blue R-250, 5,5dimethylpyrroline N-oxide (DMPO), EDTA disodium salt, K2HPO4 and KH2PO4, phenol red, riboflavin, Sephadex G-25, sodium chloride, sodium dithionite, TBS-T, Tris·HCl, Tris·Base, and horse heart myoglobin were purchased from Sigma-Aldrich (Sigma-Aldrich, Steinheim, Germany). Myoglobin was further purified and oxymyoglobin synthesized according to the procedure described in the literature.18 Water was purified (18 MΩ·cm) by means of a Milli-Q purification system from Millipore (Billerica, MA). Laser Flash Photolysis. Laser flash photolysis experiments were carried out with an LFP-112 ns laser flash photolysis spectrometer Received: Revised: Accepted: Published: 1153

November 16, 2013 January 14, 2014 January 17, 2014 January 17, 2014 dx.doi.org/10.1021/jf405182f | J. Agric. Food Chem. 2014, 62, 1153−1158

Journal of Agricultural and Food Chemistry

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from Luzchem (Ottawa, Canada) using the third harmonic (355 nm) of a pulsed Q-switched Nd:YAG laser (Brilliant B, Les Ulis, France) attenuated to 14 mJ·cm−2 as the excitation source with 8 ns of pulse duration. Appropriate UV cutoff filters were used to minimize the sample degradation by the monitoring light. The samples were excited in 1.0 cm ×1.0 cm fluorescence cuvettes from Hellma (Mulheim, Germany). The signal from the monochromator/photomultiplier detection system was captured by a Tektronix TDS 2012 digitizer (Beaverton, OR). The laser system and the digitizer were connected to a personal computer via General Purpose Instrumentation Bus (GPIB) and serial interfaces controlling all the experimental parameters and providing suitable processing and data storage capabilities. Each kinetic trace was averaged 16 times, and observed rate constants were determined by fitting the data with MatLab R2008 to exponential decay functions (Mathworks Inc., Natick, MA). All measurements were made with fresh solutions thermostatted at 25.0 ± 0.1 °C and purged with high-purity N2 (White-Martins, Sertãozinho-SP, Brazil) for 60 min before the experiment. Fluorescence Measurements. Fluorescence measurements were carried out using a Hitachi F-7000 fluorescence spectrometer (Hitachi High-Tech, Tokyo, Japan) at 25 °C using a thermostated cell holder. Samples were excited in 1.0 cm ×1.0 cm fluorescence cuvettes from Hellma (Mulheim, Germany), and the emission spectra were recorded for excitation at 445 nm. Fluorescence lifetime measurements were performed with an Optical Building Blocks Corp. Fluorometer (Birmingham, United Kingdom), using the time-resolved mode. The excitation and emission wavelengths were λ = 460 and 530 nm, respectively. Fluorescence decay times were fitted using a monoexponential decay function, and the best fit was obtained by optimized Chi-square residuals and standard deviation parameters. All solutions were deaerated by purging the cuvette with high-purity N2 (WhiteMartins, Sertãozinho-SP, Brazil). Time Resolved Fluorescence Spectroscopy. Time-resolved fluorescence of the sample was measured by time-correlated singlephoton counting using a picosecond spectrometer equipped with Glan-Laser polarizers (Newport, Irvine, CA), a Peltier-cooled PMTMCP from Hamamatsu model R3809U-50 (Hamamatsu, Japan) as the photon detector, and Tennelec-Oxford (Oxford, Abingdon, U.K.) counting electronics. The light pulse was provided by frequency doubling the 200 fs laser pulse of a Mira 900 Ti-sapphire laser pumped by a Verdi 5 W coherent laser (Santa Clara, CA), and the pulse frequency was reduced to 800 kHz using a pulse picker (Conoptics, Danbury, CT). The fluorescence decays were taken in magic angle (λexc = 400 nm) and analyzed by a reconvolution procedure with instrument response function (irf) with exponential decay models, and the goodness of the fit was evaluated by the Chisquare statistical parameters. Steady-state fluorescence was measured on a Hitachi F-7000 spectrofluorometer (Hitachi Hi-Tech, Mito, Japan) at 25 ± 0.1 °C. All solutions were deaerated by purging the cuvette with high-purity N2 (White-Martins, Sertãozinho-SP, Brazil). Steady State Photolysis. An aqueous solution (pH = 7.4, ionic strength 0.2 mol·L−1, 25 ± 0.5 °C) with 40 × 10−6 mol·L−1 riboflavin and 8 × 10−6 mol·L−1 myoglobin was exposed to 436 nm monochromatic light generated by a mercury lamp (HBO 200 w/4 short arc, Osram, Augsburg, Germany) accommodated with a focusing quartz lens, a water-filled heat filter and an Oriel narrow-band interference filter (center wavelength, 436 nm; Oriel Corp., Irvine, CA). The intensity of light, Io, was measured by ferrioxalate actinometry19 and had the average value of 2 × 10−6 einstein·s−1· cm−2. The absorbance measurements were carried out employing a Hitachi U-3501 (Hitachi-Hitech, Japan) spectrophotometer. All solutions were deaerated by purging the cuvette with high-purity N2 (White-Martins, Sertãozinho-SP, Brazil). SDS−PAGE Electrophoresis. Protein containing samples were collected and diluted in SDS sample buffer to a protein concentration of 1 mg·mL−1 (106 mM Tris·HCl, 141 mM Tris·Base, 2% SDS, 10% glycerol, 0.51 mM EDTA, 0.22 mM SERVA Blue G250, 0.175 mM Phenol Red; pH 7.4) and boiled for 5 min. 15 μL was loaded onto Tris-acetate gels (10% polyacrylamide, Invitrogen, Carlsbad, CA) and run at 125 V for 45 min. Gels were stained with 0.1% Coomassie

brilliant blue R-250 colorant. Following destaining, proteins were identified by comparing relative motilities to molecular weight standards (Precision Plus Protein ALL Blue Standards; Bio-Rad, Berkley, CA) run under the same experimental conditions. Western Blotting. 25 μL of protein (1.0 mg·mL−1) from samples added to 25 μL in 4× LDS sample buffer with 50 mM DTT was electrophoresed on 8−12% SDS−polyacrylamide gel under reducing conditions and transferred to polyvinylidene difluoride membranes (0.20 μm pore size; Invitrogen, Carlsbad, CA) using a Nu-PAGE Transfer Buffer (Invitrogen, Carlsbad, CA) with 10% methanol. The membranes were blocked in 5% nonfat dried milk in Tris-buffered saline/Tween-20 (TBS-T; 20 mM Tris, pH 7.5, 150 mM NaCl, 0.3% Tween-20) for 1 h at room temperature. Immunoblotting was performed using a mouse monoclonal affinity-purified antibody (1:1000) to myoglobin, for 24 h at 4 °C in 1% nonfat dried milk in TBS-T. The membrane was then washed three times in TBS-T and incubated with a 1:2000 horseradish peroxidase-conjugated mouse affinity-purified antibody to mouse IgG, (GE Healthcare, Litle Chalfont, U.K.), in TBS-T for 2 h at room temperature. After three washes in TBS-T, proteins were visualized using the enhanced chemiluminescent system model ECL-plus.

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RESULTS AND DISCUSSION Oxidation of meat and meat products involves lipids, proteins, and heme-pigments and leads to rancidity, loss of tenderness, and discoloration.16,17 Oxidation processes in meat are initiated by exposure to light, by iron catalysis, and by enzymatic processes including pseudoperoxidase activity of heme-pigments.20,21 Notably, oxidation of lipids, proteins, and pigments is coupled, and the relative importance of the various initiators under specific conditions still remains an open question. Riboflavin shows strong absorption in the spectral region for which fluorescent light used for retail display has high intensity, see Figure 1. Oxymyoglobin, MbFe(II)O2, and metmyoglobin,

Figure 1. UV−vis absorption spectra for aqueous phosphate buffer pH 7.4 of riboflavin, 27 × 10−6 mol·L−1, metmyoglobin, 8 × 10−6 mol·L−1, and oxymyoglobin, 4.610−6 mol·L−1. Arrows indicate the excitation wavelength for the steady-state photolysis (436 nm) and laser flash photolysis (355 nm).

MbFe(III), both absorb light in the visible region, but since the quantum yield for oxidation of MbFe(II)O2 is very small for visible light and MbFe(III) is not photoreactive, direct photooxidation is of little importance.22 None-heme meat proteins does not absorb visible light, and as for MbFe(II)O2, riboflavin photosensitized processes should rather be considered.2 1154

dx.doi.org/10.1021/jf405182f | J. Agric. Food Chem. 2014, 62, 1153−1158


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apparent value for kq of 4.84 × 1012 L·mol−1·s−1 and similar value for MbFe(II)O2, see Table 1, which both are above the

Riboflavin is highly fluorescent as may be seen from the emission spectra shown in Figure 2A for aqueous solutions of

Table 1. Second-Order Rate Constant of Singlet-Excited State Riboflavin Quenching, 1kq, and of Triplet-Excited State Riboflavin Reductive Quenching, k2, by Myoglobins in Aqueous Phosphate Buffer pH 7.4 (0.2 mol L−1 NaCl) at 25 °C kq (L·mol−1·s−1)a

k2 (L·mol−1·s−1)

6.4 × 1012 4.8 × 1012

3.1 ± 0.4 × 109 3.0 ± 0.5 × 109

1

species metmyoglobin oxymyoglobin

from the Stern−Volmer treatment of the steady-state fluorescence data for dynamic quenching. a

diffusion limit for a second-order process, further confirming that the quenching of 1Rib is static rather than dynamic. The quenching was accordingly rather analyzed accordingly to23 log Io + I = log K a + n × log[MbFe(III)] I in which Ka is the equilibrium constant for

(2)

Rib + n MbFe(III) ⇋ Rib(MbFe(III))n

(3)

and n is the number of quenchers binding to the emitting compound in the ground state. The values determined for Ka and n for the three temperatures, see Figure 3, is collected in Table 2 and provides the thermodynamic parameters ΔH° = −112 ± 22 kJ·mol−1 and ΔS° = −296 ± 75 J·mol−1·K−1 for the reaction of eq 3 using the Van’t Hoff equation. The binding of MbFe(III) to Rib is an exothermic process with a 1:1 stoichiometry, and the static quenching is highest at low temperatures as usually observed for hydrophobic interaction. The good linearity seen for the plot according to eq 2 for each of the three temperatures indicates that the quenching is dominating by the ground state binding of the MbFe(III) to Rib rather than by a dynamic process, as is also in agreement with the values of Ka around 104 mol·L−1. The decrease in entropy for binding of MbFe(III) to Rib could indicate a strong hydrophobic interaction without significant solvent involvement. The isoalloxazine ring of riboflavin is hydrophobic and has the possibility of binding to a hydrophobic surface region of myoglobin. The singlet excited state of riboflavin is too short-lived for bimolecular reactions in contrast to the triplet excited state, 3 Rib, with a lifetime of 15 μs in aqueous solution. The reaction of 3Rib as generated by laser flash photolysis with 355 nm excitation, see Figure 1, with MbFe(II)O2 and MbFe(III) was followed using transient absorption spectroscopy. The decay of 3 Rib, absorbing in the near-infrared region, was increased in rate by the presence of myoglobins as seen from Figure 4 for MbFe(II)O2 and MbFe(III). The rate of decay of 3Rib followed first-order kinetics, and the observed pseudo-first-order rate constant was found to depend on the myoglobin concentration according to

Figure 2. (A) Fluorescence emission spectra of riboflavin, 10 × 10−6 mol·L−1, in aqueous solution pH 7.4 for increasing concentration of metmyoglobin ranging from 1 to 20 × 10−6 mol·L−1. Inset: Stern− Volmer plot, see eq 1. (B) Fluorescence lifetime measurements by time-resolved single photon counting for riboflavin, 18 × 10−6 mol· L−1, in the absence or presence of 7 × 10−6 mol·L−1 metmyoglobin in anaerobic aqueous phosphate buffer pH 7.4, irf = instrument response function.

riboflavin with increasing concentration of MbFe(III). Excitation at 436 nm was used in order to reduce inner-filter effects, compare with Figure 1, and the reduction in fluorescence intensity by the presence of MbFe(III) can rather be assigned to quenching by myoglobin. The fluorescent lifetime was found to have the value of τ = 4.8 ns at 25 °C independent of the presence of MbFe(III) as seen from Figure 2B, in agreement with static rather than dynamic quenching of 1 Rib by MbFe(III). The fluorescence intensity was analyzed according to the Stern−Volmer equation, Io = 1 + kq × t × [MbFe(III)] (1) I in which Io is the fluorescence intensity at 525 nm in the absence of MbFe(III), and I is the intensity for increasing concentration of MbFe(III), see inset in Figure 2A. The observed linearity of the Stern−Volmer plot provided an

kobs = ko + k 2[myoglobin]

(4)

both for MbFe(II)O2 and for MbFe(III), as seen from the insets in Figure 4. The second-order rate constant for reaction of 3Rib with MbFe(III) had the value of k2 = (3.1 ± 0.4) × 109 L·mol−1·s−1 and with MbFe(II)O2 the value of k2 = (3.0 ± 0.5) × 109 L·mol−1·s−1. 3Rib is a strong oxidant, and the reaction 1155



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Figure 4. Triplet-excited riboflavin decay profile probed at 720 nm by transient absorption laser flash photolysis for anaerobic aqueous solution pH 7.4 of 30 × 10−6 mol·L−1 riboflavin with increasing concentration of (A) metmyoglobin and (B) oxymyoglobin. Insets: (A) kobs from exponential fitting of absorption decay versus metmyoglobin concentration according to eq 4. (B) kobs from exponential fitting of absorption decay versus oxymyoglobin concentration according to eq 4

with the myoglobins is an electron-transfer reaction from the protein backbone in myoglobin to 3Rib in agreement with assignment of the reaction of 3Rib with other water-soluble compounds as electron donors. Metmyoglobin was in agreement with this assignment found to be cross-linked using SDS− PAGE electrophoresis24 and at the same time degrading into smaller protein units, see Figure 5. Western blotting confirmed the degradation of MbFe(III) by reaction with 3Rib, see Figure 6. The involvement of radicals in the degradation of myoglobins upon reaction with 3Rib is further confirmed by SDS−PAGE electrophoresis, as addition of DMPO, a nitrone spin-trap, yields significant protection of MbFe(III), indicating that quenching of 3Rib by MbFe(III) involves electron transfer rather than energy transfer. The rate of reaction between 3Rib and each of the two myoglobins is faster by almost a factor of 10 when compared with other proteins like β-casein, β-lactoglobulin, and bovine serum albumin for which the same reaction with 3Rib has been studied.2 The facile reaction seems to be related to the hydrophobic interaction in the ground state between the two reactants as detected by fluorescence quenching of 1Rib by

Figure 3. Quenching of 1Rib fluorescence by metmyoglobin at different temperatures, (A) 15 °C, (B) 25 °C, and (C) 35 °C, plotted according to eq 2 for static quenching.23

Table 2. Association Constant and Binding Number for the Formation of the Metmyoglobin−Riboflavin Ground State Complex in Aqueous Phosphate Buffer pH 7.4 (0.2 mol L−1 NaCl) at Different Temperatures temp (°C)

Ka (L·mol−1)

n

15 ± 0.1 25 ± 0.1 35 ± 0.1

9.1 ± 1 × 104 1.2 ± 0.1 × 104 4.5 ± 2 × 103

0.84 ± 0.01 0.97 ± 0.01 1.12 ± 0.01

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accordingly concluded to be a photosensitizer for protein degradation but not for discoloration.

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AUTHOR INFORMATION

Corresponding Author

*D.R.C.: e-mail, [email protected]; phone, +55 16 33 73 99 76. L.H.S.: e-mail, [email protected]; phone, + 45 35 33 32 21. Notes

The authors declare no competing financial interest. This research is part of the bilateral Brazilian/Danish Food Science Research Program “BEAM - Bread and Meat for the Future” supported by FAPESP (Grant 2011/51555-7) to D.R.C. and by the Danish Research Council for Strategic Research (Grant 11-116064) to L.H.S. D.R.C. thanks CNPq for the research fellowship.

Figure 5. SDS−PAGE profile for aqueous phosphate buffer solution pH 7.4 containing (1) 8 × 10−6 mol·L−1 myoglobin and 30 × 10−6 mol·L −1 riboflavin kept in the dark; (2) 8 × 10 −6 mol·L −1 metmyoglobin, 30 × 10−6 mol·L−1 riboflavin, and 30 × 10−3 mol· L−1 DMPO kept in the dark; (3) 8 × 10−6 mol·L−1 metmyoglobin and 30 × 10−6 mol·L−1 riboflavin exposed to 436 nm light for 1 h; (4) 8 × 10−6 mol·L−1 metmyoglobin, 30 × 10−6 mol·L−1 riboflavin, and 30 × 10−3 mol·L−1 DMPO exposed to 436 nm light for 1 h.

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ACKNOWLEDGMENTS Prof. Marcelo H. Gehlen (IQSC-USP) is acknowledged for the time-resolved single photon counting measurements (FAPESP Grant 2011/18215-8). The student Ceder Alloo is thanked for helping with the SDS−PAGE and Western-blotting experiments.

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MbFe(III). The close interaction between 3Rib and MbFe(III) or MbFe(II)O2 will limit the diffusion distance or requirement of rearrangement prior to electron transfer resulting in the high effective rate approaching the diffusion limit. However, the observation of second-order kinetics for the electron transfer implies that the process is not intramolecular but rather a reaction between two molecules. The heme iron was not affected by the reaction with 3Rib in MbFe(III) or MbFe(II)O2 as the visible spectrum of MbFe(II)O2 did not change during reaction of MbFe(II)O2 with 3Rib. Neither was MbFe(III) oxidized to MbFe(IV)O or reduced to MbFe(II) by 3Rib (data not shown). Oxymyoglobin is light sensitive, but only UV light is of importance for direct photooxidation to yield metmyoglobin, and UV absorbers in the food packing material protect meat color.21 Riboflavin may, however, through photosensitized reactions, oxidize myoglobins, as shown by laser flash photolysis and transient absorption spectroscopy. The very efficient electron transfer between myoglobin and tripletexcited state riboflavin will, however, not affect the heme iron but only the myoglobin protein. For meat, riboflavin is

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Figure 6. Western-blotting gel profile and band intensity for an aqueous solution pH 7.4 containing 8 × 10−6 mol·L−1 myoglobin and 30 × 10−6 mol· L−1 riboflavin. Left lane: sample was kept in the dark. Right lane: sample was exposed to 436 nm light for 1 h. 1157



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