pubs.acs.org/Langmuir © 2010 American Chemical Society
Peroxide Decoloration of CI Acid Orange 7 Catalyzed by Manganese Chlorophyll Derivatives at the Surfaces of Micelles and Lipid Bilayers Shuichi Ishigure,† Tatsuro Mitsui,† Shingo Ito,† Yuji Kondo,† Shigeki Kawabe,† Masaharu Kondo, † Takehisa Dewa,† Hiroyuki Mino,‡ Shigeru Itoh,‡ and Mamoru Nango*,† †
Department of Life and Materials Engineering, Nagoya Institute of Technology, Gokiso-cho, Showa-ku, Nagoya, Aichi 466-8555, Japan, and ‡Division of Material Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku Nagoya, Aichi 464-8602, Japan Received December 4, 2009. Revised Manuscript Received January 18, 2010
Manganese-substituted chlorophyll a derivatives (MnChls) were synthesized. We first report peroxidative oxidation of an azo dye, CI Acid Orange 7, catalyzed by MnChls at the surfaces of micelles and lipid bilayers with hydrogen peroxide (H2O2) under mild conditions (pH 8.0, 25 °C). Peroxide decoloration depended upon the structures of MnChls, surfactants, lipids, and the presence of imidazole. Surprisingly, a largest decoloration rate was observed for MnChls dimer, MnPChlide a-K(MnPChlide a)-His 5 in cetyltrimethylammonium bromide (CTAB) micellar solution, especially when imidazole was present: this observation is analogous to the decoloration using horseradish peroxidase (HRP). Interestingly, the dimer complexes showed enhanced decoloration in comparison to the corresponding MnChls monomer in the micellar solution. In contrast, the MnChls monomer showed enhanced decoloration in comparison with the MnChls dimer in liposomal suspensions. Further, the imidazole residue covalently linked to the MnChls plays an important role in increasing the decoloration in both micellar and liposomal suspensions as well as in addition of imidazole into the solutions. It is interesting that the electron paramagnetic resonance (EPR) spectra of MnPChlide a ME 2, MnPChlide a-His 3, and MnMPMME-His 7 have 16 peaks around g = 2 in Egg PC or DMPC liposomal suspension with H2O2, which is typical of a mixed-valence Mn(III)-Mn(IV) complex with coupling between two ions. The higher decoloration performance obtained by the monomer porphyrin compounds at the surface of the lipid bilayers appears to be related to the stability of this mixed-valence Mn(III)-Mn(IV) species formed in the lipid bilayers. This finding should provide useful information to note that MnChls, which are easily found in a number of biological systems, are involved in functions such as hydrogen peroxide decomposition in bacteria and the oxidation of water during photosynthesis as well as the peroxidases function such as the peroxidative decoloration as bleaching agents.
Introduction The porphyrin model is useful for providing insights into possible reactions of porphyrin complexes. In these models, porphyrin pigments play a key role in oxidative electron-transfer systems such as peroxidases and cytochromes.1-6 It has been reported that many oxidation systems, metalloporphyrins, can be used to mimic cytochrome P-450-dependent monooxygenases and peroxidases, and the quantitative epoxidations of alkenes and alkane hydroxylation can be catalyzed by synthetic porphyrin complexes.5-7 It is interesting to note that binuclear and multinuclear manganese containing enzymes, which are found in a number of biological systems, are involved in functions such as *Corresponding author: Tel þ81-52-735-5226; Fax þ81-52-735-5208; e-mail
[email protected]. (1) Nango, M.; Hikita, T.; Nakano, T.; Yamada, T.; Nagata, M.; Kurono, Y.; Ohtsuka, T. Langmuir 1998, 14, 407–416. (2) Yamada, T.; Kikushima, S.; Hikita, T.; Yabuki, S.; Nagata, M.; Umemura, R.; Kondo, M.; Ohtsuka, T.; Nango, M. Thin Solid Films 2005, 474, 310–321. (3) Nango, M.; Iwasaki, T.; Takeuchi, Y.; Kurono, Y.; Tokuda, J.; Oura, R. Langmuir 1998, 14, 3272–3278. (4) Kondo, M.; Kawashima, N.; Mitsui, T.; Ito, S.; Ishigure, S.; Hashimoto, T.; Umemura, R.; Dewa, T.; Yamashita, K.; Mino, H.; Itoh, S.; Nango, M. Chem. Lett. 2005, 34, 1592–1593. (5) Collman, J. P.; Kodadek, T.; Raybuck, S. A.; Meunier, B. Proc. Natl. Acad. Sci. U.S.A. 1983, 80, 7039–7041. (6) Nolte, R. J. M.; Razenberg, J. A. S. J.; Schurman, R. J. Am. Chem. Soc. 1986, 108, 2751–2752. (7) Battioni, P.; Renaud, J. P.; Bartoli, J. F.; Reina-Artiles, M.; Fort, M.; Mansuy, D. J. Am. Chem. Soc. 1988, 110, 8462–8470. (8) Pessiki, P. J.; Dismukes, G. C. J. Am. Chem. Soc. 1994, 116, 898–903.
7774 DOI: 10.1021/la904574m
hydrogen peroxide (H2O2) decomposition in bacteria8 and the oxidation of water during photosynthesis.9 Further, some peroxidases such as lignin peroxidase, manganese peroxidase, and horseradish peroxidase have been used to catalyze the decoloration of azo dyes because not only are they more active than those bleaching agents currently available but also environmentally safe.10-12 Hage et al. reported that non-heme manganese ion complex catalyzed the low-temperature decoloration of tea-colored cotton when hydrogen peroxide was used as a bleaching agent,13 and Namboodri et al. reported the decoloration of dyes with hot peroxide catalyzed by a copper phthalocyanine-based reactive blue 21 dye.14 Recently, Sheriff et al. reported that selective dye oxidation using in situ generated hydrogen peroxide catalyzed by manganese(II) ions.15 Hodges et al. reported the results of kinetic and mechanistic investigations focusing on the oxidation of 1-arylazohydroxynaphthalene-6-sulfonate dyes by 3-chloroperoxybenzoic acid in the presence of the sterically (9) Naruta, Y.; Sasayama, M.; Sasaki, T. Angew. Chem., Int. Ed. Engl. 1994, 33, 1839–1841. (10) Chivukula, M.; Spadarao, J. T.; Renganathan, V. Biochemistry 1995, 34, 7765–7772. (11) Heinfling, A.; Martı´ nez, M. J.; Martı´ nez, A. T.; Bergbauer, M.; Szewzyk, U. Appl. Environ. Microbiol. 1998, 64, 2788–2793. (12) Zhu, M.; Huang, X.; Shen, H. Talanta 2001, 53, 927–935. (13) Hage, R.; Iburg, J. E.; Kerschner, J.; Koek, J. H.; Lempers, E. L. M.; Martens, R. J.; Racherla, U. S.; Russell, S. W.; Swarthoff, T.; van Vliet, M. R.; Warnaar, J. B.; van der Wolf, L.; Krijnen, B. Nature 1994, 369, 637–639. (14) Namboodri, C. G.; Walsh, W. K. Am. Dyest. Rep. 1995, 84, 86–95. (15) Sheriff, T. S.; Cope, S.; Ekwegh, M. Dalton Trans. 2007, 5119–5122.
Published on Web 02/25/2010
Langmuir 2010, 26(11), 7774–7782
Ishigure et al.
Article Chart 1. Structure of Manganese Chlorophyll a Derivatives and Manganese Porphyrin Derivatives
Chart 2. Structure of Azo Dye
hindered anionic oxoiron(IV) tetra(2,6-dichloro-3-sulfonatophenyl)porphyrin in aqueous solution.16 In previous papers, we reported the peroxide decoloration of azo dyes catalyzed by manganese porphyrins.3,4,17 However, fewer studies, if any, have investigated the catalytic effect of chlorophyll complexes upon the peroxidative decoloration of azo dyes with decomposition of H2O2 under mild conditions such as neutral pH at 25 °C. In this study, we first report the peroxidative oxidation of the azo dye (Chart 2) catalyzed by manganese chlorophyll a derivatives (Chart 1) in various micellar solutions and liposomal suspensions (16) Hodges, G. R.; Lindsay, Smith J. R.; Oakes, J. J. Chem. Soc., Perkin Trans. 1998, 2, 617–627. (17) Tokuda, J.; Oura, R.; Nango, M. Textile Res. J. 1999, 69, 956–960.
Langmuir 2010, 26(11), 7774–7782
(Scheme 1) with decomposition of hydrogen peroxide under mild conditions. Manganese chlorophyll a derivatives (MnChls), manganese-substituted chlorophyll a (MnChl a) 1, MnPChlide a ME 2, MnPChlide a-His 3, MnPChlide a-K(MnPChlide a)-OMe 4, and MnPChlide a-K(MnPChlide a)-His 5 (Chart 1), were synthesized. MnChls with hydorgen peroxide (H2O2) efficiently catalyzed the peroxide oxidation of CI Acid Orange 7 in micellar solutions and liposomal suspensions under mild conditions; in these reactions, the imidazole residue covalently linked to the MnChls played an important role in increasing decoloration. Electron paramagnetic resonance (EPR) spectra of MnChls were also measured to elucidate the catalytic mechanism of the MnChls for decoloration. A key aspect of the peroxidative decoloration is its usefulness in providing in insights into the catalytic effect of porphyrin structures on decoloration at the surface of the micelllar and lipid bilayers. MnChls were selected because of their environmental safety, usefulness, well-defined biological properties, and industrial applications. Future detergents will be routinely required to contain bleaching agents that are not only more active than those currently available but are also environmentally safe and cost-effective. DOI: 10.1021/la904574m
7775
Article
Ishigure et al. Scheme 1. Decoloration of the Azo Dye Catalyzed by Manganese Chlorophyll Derivatives in Micllar or Liposomal Solutions
Hydrogen peroxide, a traditional bleaching agent, loses its activity as the washing temperature decreases. It is considered that manganese or ferric complexes are relatively more favorable for catalytic bleaching than hydrogen peroxide alone.3,10,17 Thus, studying the catalytic effect of MnChls on the rate of decoloration of azo dyes by hydrogen peroxide is useful for providing insights into the favorable catalytic bleaching properties of horseradish peroxidase (HRP) as well as binuclear and multinuclear manganese-containing enzymes, which are easily found in a number of biological systems, are involved in functions such as hydrogen peroxide decomposition in bacteria and the oxidation of water during photosynthesis.
Materials and Methods General Materials. All reactions and chromatographic separations were carried out at minimum room light. Tetrahydrofuran (THF) and triethylamine were distilled and stored over molecular sieves. The other solvents used in this study were at least of spectral grade. The silica gel used for column chromatography was silica gel, 70-230 mesh, 60 A˚, obtained from Aldrich. 1H NMR spectra were obtained using the Varian Gemini-300 NMR spectrometer, with tetramethylsilane used as an internal standard for CDCl3. The UV absorption spectra were recorded on Hitachi U-3500 spectrophotometers. Mass spectra (MS) were obtained in R-cyano-4-hydroxycinnamic acid (CHCA), using a matrix-assisted laser desorption/ionization mode-time of flight (MALDITOF) mass spectrometer (Perseptive Biosystems Voyager RN). Hydrogen peroxide was provided by Mitubishigasu Chemicals as a 31% solution. The pH was adjusted with tris(hydroxymethyl)aminomethane and 1.0 N HCl(aq). The azo dye, CI Acid Orange 7, was provided by Tokyo Kasei and purified by recrystallization from aqueous ethanol. Triton X-100 and sodium dodecyl sulfate (SDS) were obtained from Nacalai Tesque, Inc. Cetyltrimethylammonium bromide (CTAB) was obtained from Wako Pure Chemical Industries, Ltd. Egg yolk phosphatidylcholine (Egg PC) and dimyristoylphosphatidylcholine (DMPC) were gifts from Nippon Fine Chemical Co. Peroxidative Decoloration of Azo Dye.3 The peroxide oxidation of azo dyes by hydrogen peroxide in the presence of MnChls and manganese porphyrin derivatives (MnPorphyrins) was evaluated by determining the decoloration curve of the dye in aqueous solution (1 10-2 [M] Tris-HCl buffer) at pH 8.0 at 25 °C. The required amount of an aqueous solution of the azo dye adjusted to the desired pH was added to 25 mL of the bleaching solution at 25 °C so as to obtain the initial concentrations of the azo dye of 1 10-4 M. MnChls solubilized by surfactants or lipids were mixed with the azo dye in aqueous solution, and hydrogen peroxide was finally added to mixture solution of MnChls and the 7776 DOI: 10.1021/la904574m
azo dye. To obtain each decoloration curve, each of the solutions was placed as quickly as possible in a covered optical quartz cell, and the concentration of the coloring matter in the bleaching solution was determined by a spectrophotometric method using a Hitachi U-3500 spectrophotometer equipped with a thermostat; the concentration was measured at appropriate time intervals and the desired temperature. At the absorption maximum of the coloring matter, there is no interference from products formed during decomposition. Under these conditions, the calibration line follows Beer’s law. Absorptions of CI Acid Orange 7 was measured at 484 nm.
Preparation of Liposomal Membrane Containing Manganese Chlorophyll a Derivatives or Manganese Porphyrin Derivatives. Manganese chlorophyll a derivativrs (MnChls) or
manganese porphyrin derivatives (MnPorphyrins) (2.4 μmol) and Egg PC (143 μmol) (MnPorphyrin/lipid = 1/60, mol/mol) in choloroform was transferred to a flask. The organic solvent was removed using rotary evaporator, resulting in a thin lipid film containing MnChls or MnPorphyrins. The last traces of solvent were then removed under reduced pressure using vacuum pump for 12 h. To the dried film was added 2.5 mL of 10 mM Tris-HCl buffer (pH 8.0), and the mixture was vortexed for 2 min. The liposomal suspension was subjected to five freeze/thaw cycles (77 K/325 K) and was then sonicated for 10 min in an ice bath conditions to make small unilamellar vesicles. After sonication, the liposomal suspension was purified by gel filtration (Sephadex G-50). After gel filtration, liposomal membrane containing MnChls and MnPorphyrins was obtained. The concentrations of MnChls and MnPorphyrins are calculated by a UV/vis spectrometer to ajust sample concentration for catalytic and EPR experiments. Cyclic Voltammogram Measurement. Cyclic voltammogram (CV) measurements were conducted using a Hokuto Denko HZ-3000. A standard Ag/AgCl electrode served as reference electrode, glassy carbon served as the working electrode, and platinum functioned as the counter electrode. Solutions containing MnChls or MnPorphyrins were prepared in DMSO containing 0.1 M tetra-n-butylammomium perchlorate (TBAP). The solutions were degassed by argon bubbling. The data are summarized in Table 2. Electric Paramagnetic Resonance Measurement. The EPR was measured on a Bruker ESP 300E spectrometer at 9.487 GHz. Solutions containing MnChls and MnPorphyrins were prepared in Egg PC liposomal suspension. The solutions were degassed by argon bubbling and cooled by liquid helium. EPR measurements were performed in quartz tubes (d = 5 mm, l = 150 mm) placed into a dewar with liquid helium. While studying the temperature dependence of the micropower saturation, the likely influence of the modulation field amplitude on P1/2 was examined. The data are summarized in Table 5. Langmuir 2010, 26(11), 7774–7782
Ishigure et al.
Article Scheme 2. Synthesis of Chlorophyll a Derivatives
Results and Discussion Synthesis and Characterization of Manganese Chlorophyll a Derivatives. Synthetic sequences leading to the compounds, manganese chlorophyll a derivatives (MnChls), MnChl a 1, MnPChlide a ME 2, MnPChlide a-His 3, MnPChlide aK(MnPChlide a)-OMe 4, and MnPChlide a-K(MnPChlide a)His 5 (Chart 1), were prepared by the following synthetic sequence of steps as shown in Scheme 2. Pheophytin a, PPheide a ME, PPheide a-His, PPheide a-K(PPheide a)-OMe, and PPheide aK(PPheide a)-His were prepared from Chl a as described in the Supporting Information. Characterization and verification of the compounds synthesized were performed by mean of UV/vis Langmuir 2010, 26(11), 7774–7782
absorption, 1H NMR spectroscopies, and MALDI-TOF mass spectroscopies. The manganese complexes were prepared as described in previous papers.3,4 MALDI-TOF data showed the presence of a characteristic MnChls, as shown in the Supporting Information. Tables 1 and 2 show the absorption maximum of Soret and Qy bands and CV potential values of MnChls in the absence and presence of imidazole. When imidazole coordinates to Mn, the λmax of Soret and Qy bands and CV potential are changed. Table 1 presents that the Soret and Qy bands are red-shifted by around 1 -3 nm (except for the Soret band of MnPChlide aK(MnPChlide a)-OMe 4, which is shifted by 12 nm), depending on the structures of MnChls and the concentration of imidazole. For DOI: 10.1021/la904574m
7777
Article
Ishigure et al.
Table 1. λmax of Manganese(III) Chlorophyll a Derivatives in the Presence of Imidazole in CTAB Micelle Solution at 25 °C and pH 8.0a λmax/nm catalyst
imidazole/mM
Soret band
Table 3. Rate Constants for Decoloration Reaction of CI Acid Orange 7 Catalyzed by Manganese Chlorophyll a Derivatives and Manganese Porphyrin Derivatives with H2O2 at 25 °C and pH 8.0a kobs ( 102 min-1)
Qy band
surfactant none 367 683 10 369 683 100 370 685 3 none 364 685 10 367 685 100 367 686 4 none 358 688 10 363 691 100 370 690 5 none 364 688 a [CTAB] = 8.0 10-4 M, [2] = [3] = 1.0 10-5 M, and [4] = [5] = 5.0 10-6 M. 2
Table 2. Redox Potential of Manganese Chlorophyll a Derivatives and Manganese Porphyrin Derivatives in the DMSO Solution at Room Temperaturea catalyst
imidazole/M
redox potential/V vs Ag/AgCl (0.1 M KClaq) Mn(II)/Mn(III)
0 -0.296 0 -0.264 2 -0.302 5 -0.350 3 0 -0.259 4 0 -0.265 2 -0.314 5 -0.336 6 0 -0.456 2 -0.496 5 -0.520 7 0 -0.463 8 0 -0.475 a [1]=[2]=[3]=[7] =[6] = 5.0 10-3 M and [4] = [8] = 2.5 10-3 M.
catalyst
CTAB
Triton X-100
example, the Qy band of MnPChlide a ME 2 is red-shifted by 2 nm due to the presence of 100 mM imizazole, consistent with MnPChlide a-His 3, implying that the Mn atom of the MnChls coordinated with the N atom of imizazole.3 The CV potential values of MnChls become negative with increasing the presence of imidazole as shown in Table 2, this is an observation that is consistent with the red shift of the Soret or Qy band as shown Table 1.3 A higher oxidation potential was observed for MnPChlide a ME 2 than for MnMPDME 6. 7778 DOI: 10.1021/la904574m
SDS
Egg PC
DMPC
1 252 1.75 2 188 124 88.1 53.5 67.9 3 438 191 264 4 608 5.76 2.79b 0.247b 1.06 6 27.9b b 5.11 7 215 c d d 0.84 0.07 0.42 1.33 none a [CI Acid Orange 7] = 1.0 10-4 M, [H2O2] = 3.0 10-2 M, [CTAB] = 8.0 10-4 M, [Triton X-100] = 1.5 10-4 M, [SDS] = 1.0 10-3 M, [Egg PC] = 9.0 10-4 M, [DMPC] = 9.0 10-4 M. b Cited from ref 4. c Control data no catalyst with H2O2. d Cited from ref 25.
Table 4. Rate Constants for Decoloration Reaction of CI Acid Orange 7 Catalyzed by Manganese Chlorophyll a Derivatives and Manganese Porphyrin Derivatives with H2O2 at 25 °C and pH 8.0a kobs ( 102 min-1)
1 2
Figure 1. Plot of ln(C0/Ct) against decoloration time for CI Acid Orange 7 catalyzed by MnPChlide a ME 2 in micellar solution at 25 °C and pH 8.0 ([CI Acid Orange 7] = 1.0 10-4 M, [H2O2] = 3.0 10-2 M, [2] = 1.0 10-5 M, [Triton X-100] = 1.5 10-4 M, [SDS] = 1.0 10-3 M, [CTAB] = 8.0 10-4 M): CTAB (circles), SDS (triangles), Triton X-100 (squares), only H2O2 without 2 (cross).
lipid
imidazole/mM catalyst
none
10
1 252 2 188 827 3 438 941 4 608 1019 5 777 1113 797 6 27.9b 646 7 215b 705 8 165b b 957 9 389 c HRP 1100 a [CI Acid Orange 7] = 1.0 10-4 M, [H2O2] = 3.0 10-2 M, [CTAB] = 8.0 10-4 M, [1] = [2] = [3] = [6] = [7] = 1.0 10-5 M, [4] = [5] = [8] = [9] = 5.0 10-6 M, and [HRP] = 1.0 10-5 M. b Cited from ref 4. c Without CTAB.
Peroxidative Decoloration of Azo Dye in Micellar Solutions. Effect of Surfactants. To examine the effects of surfactants and the porphyrin structures on the chemoselectivity variations in the peroxide oxidation, we investigated the decoloration of CI Acid Orange 7 catalyzed by MnChls in micellar solutions, as shown in Scheme 1. For example, Figure 1 shows that for various micellar solutions semilogarithmic plots of C0/Ct against decoloration time gave a straight line passing through the origin in case of CI Acid Orange 7 in the presence and absence of MnPChlide a ME 2. C0 and Ct are the dye concentrations in the initial solution and at time t, respectively. The decoloration of azo dye was evidently observed in the presence of 2 with surfactants. The decoloration rates were first order with respect to the dye concentration for the times as shown in Figure 1. Equation 1 provides numerical values that can be used later to compare the compounds and the influence of various conditions, such as pH and temperature: lnðC0 =Ct Þ ¼ kobs t
ð1Þ
The rate constant kobs based on first-order kinetics is given in units of min-1 and summarized in Tables 3 and 4. The effect of surfactants on the decoloration rate of the dye has been examined at pH 8.0 to provide an insight into the charge effect of the dye-surfactant interaction as shown in Figure 1 and Table 3. These results presented that the decoloration rate increased in the Langmuir 2010, 26(11), 7774–7782
Ishigure et al.
Article
Figure 2. EPR spectra of manganese chlorophyll derivatives, 1 (a), 2 (b), 3 (c), and 4 (d) and manganese porphyrin derivatives, 6 (e) and 7 (f)
in Egg PC liposomal solution at pH 8.0, 5 K. [1] = [2] = [3] = [6] = [7] = 1 10-3 M, [4] = 5 10-4 M, and [H2O2] = 1.5 M. The spectra prior to H2O2 addition are given in black, with the spectra after H2O2 presented in red. Table 5. EPR Spectra of Manganese Chlorophyll a Derivatives and Manganese Porphyrin Derivatives in Egg PC or DMPC Liposome Solution at 5 K and pH 8.0a catalyst surfactant split width/G A1/G
A2/G
A1/A2 J/cm-1
Egg PC 6 510 Egg PC 16 1083 146 70 2.1 -15.3 DMPC 16 1088 148 70 2.1 3 Egg PC 16 1085 147 70 2.1 -45.0 DMPC 16 1087 147 70 2.1 4 Egg PC 6 518 6 Egg PC 6 510 7 Egg PC 16 1071 145 69 2.1 -25.5 a [1] = [2] = [3] = [6] = [7] = 1 10-3 M, [4] = 5 10-4 M, [H2O2] = 1.5 M,and [Egg PC] = [DMPC] = 0.1 M. 1 2
order CTAB (cation) > Triton X-100 (neutral) > SDS (anion). The decoloration rate on CTAB and Triton X-100 depended upon it is concentration, where the maximum decoloration rate was observed at the critical micelle concentration. Enhanced decoloration of the dye was observed in the CTAB micelle in Langmuir 2010, 26(11), 7774–7782
comparison to those in Triton X-100 and SDS, indicating that the role of CTAB could be important for favoring complex formation between MnChls and azo dyes, with hydrogen peroxide getting oxidized. This result indicates that the decoloration rates depend on the electrostatic interaction between the dye (anion) and the hydrophilic part of the surfactant, consistent with the result as described previously.3,4,17 Mitsuishi et al. reported that the interactions between methyl orange anion and dodecyltrimethylammonium cation were hindered due to the presence of sodium chloride.18 Their observation is also consistent with our present results. Effect of Strucutures of Manganese Chlorophyll a Derivatives. Table 4 shows that in CTAB micellar solutions the decoloration rates increase in the order MnMPDME 6 < MnMPMME-K(MnMPMME)-OMe 8 < MnPChlide a ME 2 < MnMPMME-His 7 < MnChl a 1 < MnMPMME-K(MnMPMME)-His 9 < MnPChlide a-His 3 < MnPChlide (18) Mitsuishi, M.; Yoshida, D.; Urata, S.; Hamada, K.; Ishiwatari, T. J. Soc. Fiber Sci. Tech. Jpn 1993, 49, 176–181.
DOI: 10.1021/la904574m
7779
Article
a-K(MnPChlide a)-OMe 4 < MnPChlide a- K(MnPChlide a)-His 5. The decoloration rate depended on the structures of the porphyrin derivatives. Comparing the decoloration rate and the structures of these MnChl a 1 or manganese chlorophyll derivatives, an enhanced decoloration rate was observed for MnChl a 1 in comparison with MnPChlide a ME 2. This result indicates that the phytol group contributes to increasing the rate, suggesting that the phytol group plays an important role in hydrophobic domain formation with CTAB through the hydrophobic interaction in the micellar reaction. Further, in these chlorophyll derivatives, the imidazole residue covalently linked to the MnChls for MnPChlide a-His 3 and MnPChlide a-K(MnPChlide a)-His 9 plays an important role in increasing decoloration due to coordination between the Mn atom in the porphyrin ring and the imidazole group of MnPChlide a-His 3. This coordination causes the red shift of the Soret band of MnChls and the decrease in the CV potential values as shown in Tables 1 and 2. This imidazole moiety can effectively enhance the decoloration as described previously.3,4 Surprisingly, the MnChls dimer 4 and 5 enhance decoloration much more effectively than the corresponding MnChls monomer; this result is consistent with the result obtained for MnPorphyrins dimer 8 and 9.4 Alternatively, a large increased rate was observed for MnPChlide a ME 2 compared with MnMPDME 6 in CTAB micellar solution, as shown in Table 4, in which a high oxidation potential was observed for MnPChlide a ME 2 (-0.264 V) than for MnMPDME 6 (-0.456 V) as described in Table 2. This high oxidation potential of CV is likely to contributes to the enhanced rate for MnPChlide a ME 2 in comparison to the rate for MnMPMDME 6.3,4 Peroxidative Decoloration of Azo Dye in Liposomal Suspensions. The effects of lipids and the structures of MnChls and MnPorphyrins on the peroxidative decoloration of CI Acid Orange 7 catalyzed by MnChls and MnPorphyrins in liposomal suspensions were investigated, as shown in Scheme 1. The decoloration rates in Egg PC solution increased in the order MnMPDME 6 < MnChl a 1 < MnMPMME-His 7 < MnPChlide a-K(MnPChlide a)-OMe 4 , MnPChlide a ME 2 < MnPChlide a-His 3, as shown in Table 3. Interestingly, less enhanced decoloration, if at all, was observed in liposomal suspension for MnChl a 1 and MnPChlide a-K(MnPChlide a)OMe 4 in comparison with MnPChlide a ME 2. This result is quite different from the order in CTAB micellar solutions and can probably be attributed to the decrease of the mobility due to the phytol group of MnChl a 1 or the large size of the dimer molecules in MnPChlide a-K(MnPChlide a)-OMe 4 in comparison with the corresponding monomer derivatives, which contributes to the decreased rate in the lipid bilayers. A similar enhanced rate was observed for MnPChlide a-His 3 in comparison with the case for MnPChlide a ME 2 in a liposomal suspension; this result is consistent with the data for micellar solution and indicates again that coordination between the Mn atom in the porphyrin ring and the imidazole group in MnChls plays an important role in enhancement of the decoloration rate.3,4 The precise mechanism governing the peroxide decoloration of dyes with hydrogen peroxide in such micellar solution and liposomal suspension is not fully understood, but it is thought to be due to hydroxyl radical, reacting with the organic coloring agent and destroying the chromophore at the surface of micellar and lipid bilayers.3,4 For example, after the decomposition of CI Acid Orange 7, the dye decoloration products were 4-sulfophenyldiazene, 4-nitrosobenzenesulfonic acid, and quinone intermediates.3,10 It is interesting to note that the 7780 DOI: 10.1021/la904574m
Ishigure et al.
decoloration rate depended on the surfactants, structures of the MnChls, lipids, and the presence of imidazole, as shown in Tables 3 and 4. Furthermore, as is apparent from Table 3, the decoloration rates increase in the order Egg PC < DMPC. Egg PC extracted from egg yolk is a mixture and bearing verious acyl chains (Tm ∼ - 10 ( 5 °C), while the synthetic phospholipid, DMPC, is single component with saturated acyl chain (Tm ∼ 23.6 ( 1.5 °C). Yoshimoto et al. reported that the packing density of phosphatidylcholine (PC) molecules influences the reactivity19 in which hydrogen peroxide was more easily decomposed at the surface of DMPC lipid bilayers than at the surface of unsaturated phospholipid bilayers. Therefore, the interface of liposomal membrane plays a key role in the catalytic reaction. Effect of Ligand. The rate of decoloration of CI Acid Orange 7 with hydrogen peroxide catalyzed by MnChls was examined in the presence of imidazole (10 mM) at pH 8.0, as shown in Table 4. The decoloration rate increased with the addition of imidazole for MnChls in micellar solutions. A similar addition effect of imidazole on decoloration was observed in liposomal suspensions. It is interesting to note that the effect of imidazole effect on the decoloration rate depended on the structures of MnChls in liposomal suspension as well as in micellar solutions. Surprisingly, the largest decoloration rate was observed for MnPChlide aK(MnPChlide a)-His 5 in CTAB micellar solution, especially when imidazole was present; this result is analogous to of the results obtained horseradish peroxidase (HRP) as shown in Table 4. Thus, interactions between these MnChls and imidazole play a crucial role in influencing the decoloration rate at the surface of lipid as well as micellar bilayers. The probable role of imidazole is that it coordinates with Mn as a ligand and also works as the base catalyst,7 in which manganese porphyrins decompose H2O2 and transfer more or less than one oxygen atom to the azo dye presumably via a high valent MndO intermediate such as Mn(IV)dO in the bleaching solution when imidazole is present. As an axial Mn ligand, imidazole plays an important role by favoring the heterolytic cleavage of H2O2, which yields the MndO intermediate and H2O, over a possible homolytic cleavage, which may yield a hydroxyl radical; in addition, imidazole favors monooxygenation of azo dye over H2O2 dismutation at the level of an imidazole-MndO intermediate. Its role as a base catalyst could be important for the formation of a MndO intermediate from Mn(III) and H2O2. These results imply that the hydroxyl radicals react with the organic azo coloring agent, destroying the chromophore.3,10 However, further investigations will be necessary to determine the various roles indicated by imidazole in oxidations by H2O2 catalyzed by MnChls. Electron Paramagnetic Spectroscopy Measurement. Characterization of High Valence Manganese Complex. All the manganese chlorophyll a derivatives proved to be excellent catalysts under mild conditions, suggesting the formation of similar active species of MnChls with decomposition of H2O2. The mechanism of catalyzed decoloration was further investigated by EPR in micellar solution and liposomal suspensions. Figures 2 and 3 show X-band EPR spectra at 5 K for MnChls, MnChl a 1, MnPChlide a ME 2, MnPChlide a-His 3, and MnPChlide a-K(MnPChlide a)-OMe 4, and for MnPorphyrins, MnMPDME 6 and MnMPMME-His 7, in Egg PC and DMPC liposomal suspensions. Table 5 presents detailed EPR spectral data, including the hyperfine valence constant, hyperfine (19) Yoshimoto, M.; Miyazaki, Y.; Umemoto, A.; Walde, P.; Kuboi, R.; Nakao, K. Langmuir 2007, 23(18), 9416–9422.
Langmuir 2010, 26(11), 7774–7782
Ishigure et al.
Article
Figure 3. EPR spectra of manganese chlorophyll derivatives, 2 (a) and 3 (b) in Egg PC (black line) and DMPC (red line) liposomal solution at pH 8.0, 5 K. [Catalyst] = 1 10-3 M, [H2O2] = 1.5 M.
Figure 4. Semilogarithmic plot of P1/2 vs 1/T. [Catalyst] = 1 10-3 M, [H2O2] = 1.5 M; 2 (triangles), 3 (squares), and 7 (circles).
bandwidth, and representative microwave saturation, for MnChls and MnPorphyrins in Egg PC and DMPC liposome in 1 10-2 M Tris-HCl buffer with pH 8.0. Figure 2 and Table 5 show that when H2O2 was added, EPR spectra of MnPChlide a ME 2, MnPChlide a-His 3, and MnMPMME-His 7 contained 16 peaks around g = 2 in Egg PC or DMPC liposomal suspension, which are typical of a mixed-valence complex with coupling between two ions.20,21 No detectable change in 16 peaks was observed for MnChl a 1, MnPChlide a-K(MnPChlide a)-OMe 4, and MnMPDME 6 in the liposomal suspensions. These results suggest that MnPChlide a ME 2, MnPChlide a-His 3, and MnMPMME-His 7 react with H2O via electron transfer, yielding a mixed-valence Mn complex in the lipid bilayers. Furthermore, the 16 peaks obtained for MnPChlide a-His 3 or MnMPMME-His 7 were clearer than those for MnPChlide a ME 2 or MnMPDME 6, respectively, indicating that the imidazole moiety of the compound contributes to the formation of the mixed-valence Mn complex. In contrast, MnChls and MnPorphyrins did not provide such EPR spectra in micellar solutions with H2O2 under this condition. Interestingly, Figure 3 shows that the EPR spectra of MnPChlide a ME 2 and MnPChlide a-His 3 contained 16 peaks in DMPC liposomal suspension as well as in Egg PC when H2O2 was added; the peaks were more clearly observed for DMPC liposomal suspension than for the Egg PC liposomal suspension. This result indicates that molecular packing by DMPC lipid bilayers influences on the formation of a mixed-valence Mn complex; this is consistent with the effective decomposition of H2O2 at the surface of the DMPC lipid bilayers.19 (20) Bryliakov, K. P.; Kholdeeva, O. A.; Vanina, M. P.; Talsi, E. P. J. Mol. Catal. A 2002, 178, 47–53. (21) Dismukes, G. C.; Sheats, J. E.; Smegali, J. A. J. Am. Chem. Soc. 1987, 109, 7202–7203.
Langmuir 2010, 26(11), 7774–7782
Table 5 shows that the ratio of the hyperfine valence constant data (A1/A2) equals 2.1 for manganese complexes. Talsi et al. indicate that the ratio of Mn(III)-Mn(IV) complexes corresponds to A1/A2 = 2/1, while the ratio of Mn(II)-Mn(III) complexes corresponds to A1/A2 = 7/4.20 Thus, these hyperfine valence constants imply that the mixed-valence Mn complexes formed from for MnMPMME-His 7, MnPChlide a ME 2, and MnPChlide a-His 3 are likely to be Mn(III)-Mn(IV) complexes rather than Mn(II)-Mn(III) complexes. Dismukes et al. reported that the Mn(III)-Mn(IV) complex has a total hyperfine bandwidth of 1070 G, while the Mn(II)-Mn(III) complex has a bandwidth of 1410 G.21 Table 5 shows that the bandwidth for MnPChlide a ME 2, MnPChlide a-His 3, and MnMPMME-His 7 is between 1071 and 1088 G, which corresponds the bandwidth of an Mn(III)-Mn(IV) complex. Stability of the Mixed-Valence Manganese(III)-Manganese(IV) Complex. Figure 4 shows the semilogarithmic plots of P1/2 vs 1/T prepared from the representative microwave saturation data in the temperature range of 4-30 K for manganese complexes. According to eq 222,23 P1=2 µ 1=T1 ¼ expð-Δ=kTÞ
ð2Þ
P1/2 is the microwave power for half-saturation, T1 is the spin-lattice relaxation time, Δ is the zero-field splitting constant (Δ = -3J), k is the Boltzmann constant, and T is the temparature. J (cm-1) values are summarized in Table 5. The J values in Table 5 indicate that the stability of the mixedvalence Mn species(as shown in Supporting Information Chart S1) formed21,24 in the lipid bilayers can be evaluated. The absolute values increase in the order MnPChlide a ME 2 < MnMPMMEHis 7 < MnPChlide a-His 3. The larger value observed for MnPChlide a-His 3 than for MnMPMME-His 7 indicates that Mn(III)-Mn(IV) complexes of the MnChls are more stable than the MnPorphyrins. In addition, a larger value is also observed for MnPChlide a-His 3 than for MnPChlide ME 2, thereby indicating that Mn(III)-Mn(IV) complexes of MnPChlide a-His 3 are more stable than those of MnPChlide a ME 2 and implying that the histidine residue contributes to the stability of the mixed-valence Mn species. These results are consistent with the results obtained for the X-band EPR spectra described above (Figure 2). (22) Yim, M. B.; Kuo, L. C.; Makinen, M. W. J. Magn. Reson. 1982, 46, 247– 256. (23) Sarrou, J.; Ioannidis, N.; Deligiannakis, Y.; Petrouleas, V. Biochemistry 1998, 37, 3581–3587. (24) Mukhopadhyay, S.; Mandal, S. K.; Bhaduri, S.; Armstrong, W. H. Chem. Rev. 2004, 104, 3981–4026. (25) Tokuda, J.; Ohura, R.; Nango, M. Textile Res. J. 1999, 69, 456–462.
DOI: 10.1021/la904574m
7781
Article
Altogether, the EPR results suggest that the higher decoloration performance obtained by these monomer porphyrin compounds at the surface of the lipid bilayers appears to be related to the stability of this mixed-valence Mn(III)-Mn(IV) species formed in the lipid bilayers.
Conclusion MnChls, MnPChlide a ME 2, MnPChlide a-His 3, MnPChlide a-K-(MnPChlide a)-OMe 4, and MnPChlide a-K(MnPChlide a)His 5, and Mn-substituted chlorophyll a (MnChl a) 1 (Chart 1) were synthesized. MnChls with H2O2 in the presence of imidazole efficiently catalyzed the peroxide oxidation of azo dyes (Chart 2) in micellar solutions and liposomal suspensions under mild conditions such as pH 8.0 and 25 °C. The peroxidation depended upon the structures of surfactant, lipids, and MnChls and the presence of imidazole. The effects of surfactant, lipids, and the chlorophyll structures on the peroxidation are discussed. The kinetics of the decoloration of the azo dye by hydrogen peroxide catalyzed by MnChls in the presence and absence of imidazole were evaluated. Interestingly, the imidazole residue covalently linked with the Mn complexes and the added imidazole play an important role in increasing the decoloration in both micellar solutions and liposomal suspensions. The dimer complexes enhanced decoloration in comparison with the corresponding monomer derivatives in the micellar solution. In contrast, the
7782 DOI: 10.1021/la904574m
Ishigure et al.
MnChls monomer showed enhanced decoloration in comparison with the MnChls dimer in liposomal suspensions. Furthermore, when H2O2 was added, the EPR spectra of MnMPMME-His 7, MnPChlide a ME 2, and MnPChlide a-His 3 presented the typical of mixed-valence Mn(III)-Mn(IV) complexes with coupling between two ions. The higher decoloration performance obtained by these monomer porphyrin compounds in the liposomal suspension appears to be related to the stability of this mixed-valence Mn(III)-Mn(IV) species formed in lipid bilayers. This finding should provide useful information to note that MnChls, which are easily found in a number of biological systems, are involved in functions such as hydrogen peroxide decomposition in bacteria and the oxidation of water during photosynthesis as well as the peroxidases function such as the peroxidative decoloration as bleaching agents. Acknowledgment. M.N. thanks Dr Alastair T. Gardiner, University of Glasgow, for helpful discussions. The present work was partially supported by a Grand-in-Aid from the Ministry of Education, Science and Culture, Japan. Supporting Information Available: The structure of [Mn(III)-Mn(IV)] μ-oxo chlorophyll dimer on EPR conditions (Chart S1) and experimental details. This material is available free of charge via the Internet at http://pubs.acs.org.
Langmuir 2010, 26(11), 7774–7782
