Antineoplasic Drug Methotrexate Redox Mechanism Using a Glassy Carbon Electrode
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1 Antineoplasic Drug Methotrexate Redox Mechanism Using a Glassy Carbon Electrode A. D. R. Pontinha, a S. M. A. Jorge, a, b V. C. Diculescu, a M. Vivan, c A. M. Oliveira-Brett* a a Departamento de Química, Faculdade de CiÞncias e Tecnologia, Universidade de Coimbra, , Coimbra, Portugal tel/fax: b Departamento de Química e Bioquímica, Instituto de BiociÞncias, UNESP, , Botucatu, SP, Brasil c Hospital da Universidade de Coimbra, 3000 Coimbra, Portugal * brett@ci.uc.pt Received: September 30, 2011;& Accepted: January 20, 2012 Abstract Methotrexate (MTX) is an antimetabolite of folic acid indicated in the treatment of a variety of cancers. The electrochemical behaviour of MTX on a glassy carbon electrode was investigated. The MTX oxidation is a complex, ph-dependent, diffusion-controlled irreversible process and proceeds with the transfer of two electrons and two protons and the formation of one electroactive product, 7-hydroxymethotrexate that undergoes a reversible redox reaction. The MTX reduction is a ph-dependent, quasi-reversible process and involves the transfer of two electrons and two protons leading to the formation of an electroactive product. Keywords: Glassy carbon, Methotrexate, Oxidation, Reduction DOI: /elan Introduction Antimetabolites are a group of drugs that have become very important for cancer chemotherapy being highly effective in targeting and inhibiting the enzymes involved in malignant cell lines [1]. Methotrexate (MTX), N- [4{[2,4-diamino-6-pteridinyl-methyl]-methylamino}benzoyl] glutamic acid (Scheme 1) is an antimetabolite of folic acid that acts by competitively binding to the enzyme dehydrofolate reductase [2,3]. This process interrupts the formation of purines and pyrimidines within the cell, inhibiting DNA synthesis, but it may also interfere with protein synthesis blocking the conversion of some aminoacids [3,4]. It is used to treat severe lymphatic leukemia, choriocarcinoma, non-hodgkins lymphoma, bone carcinoma, as well as head, neck, breast, and lung tumors [5 8]. It is also employed as an alternative treatment for psoriasis and rheumatoid arthritis [9]. Several side effects were observed using MTX in treatments such as renal insufficiency, hypoalbuminemia, gastrointestinal lesions, marrow suppression, hepatic failure and pancytopenia [10]. The diversity of drug secondary effects is a major problem in clinical medicine and drug development, showing the need to identify the factors associated with variable drug sensitivity. From this point of view, the quantitative determination of MTX in biological samples [11] has emerged as a very important topic and high-performance liquid chromatography (HPLC) [12 14], fluorimetry [15] Scheme 1. Chemical structure of MTX. and spectrophotometry [16] have been used for this purpose. Adsorptive stripping voltammetry of MTX was carried out using a multivariate strategy by means of experimental design tools [17,18], and MTX was determined at submicromolar concentration in human blood plasma and urine [19,20]. Studies on the electrochemical reduction behaviour of MTX have been undertaken using mercury meniscus modified silver solid amalgam electrode [21] and the static mercury drop electrode [22 25], but since the mercury drop electrode is limited to the negative potential range only the reduction mechanism of MTX was investigated. A systematic investigation of the oxidation and reduction mechanism of MTX has not been yet undertaken. Electroanalytical methods are fast, highly sensitive and can allow direct measurement in biological samples with very little or no sample pretreatment. They have been successfully used for the detection and determination of several pharmaceutical drugs [26 29], and the use of solid Electroanalysis 2012, 24, No. 4, Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim 917
2 electrodes in general, and various forms of carbon in particular, has greatly increased in recent years. The present study is concerned with the investigation of MTX oxidation and reduction mechanisms, on a glassy carbon electrode over a wide ph range, using cyclic (CV), differential pulse (DP) and square-wave (SW) voltammetry, which will provide very important and useful data concerning the formation and redox behaviour of MTX metabolites. 2 Experimental 2.1 Materials and Reagents Methotrexate was obtained from Sigma and used without further purification. A stock solution of 200 mm MTX was prepared daily in different ph buffers. Solutions of different concentrations of MTX were obtained by dilution of the appropriate volume in supporting electrolyte. All supporting electrolyte solutions (Table 1) [30], were prepared using analytical grade reagents and purified water from a Millipore Milli-Q system (conductivity 0.1 mscm 1 ). DP voltammograms in the supporting electrolyte were recorded using a clean GCE until a steady state baseline voltammogram was obtained. Nitrogen saturated solutions were obtained by bubbling high purity N 2 for a minimum of 10 min in the solution and continuing with a flow of pure gas over the solution during voltammetric experiments. Microvolumes were measured using EP-10 and EP-100 Plus Motorized Microliter Pippettes (Rainin Instrument Co. Inc., Woburn, USA). The ph measurements were carried out with a Crison microph 2001 ph-meter with an Ingold combined glass electrode. All experiments were done at room temperature (25 18C). 2.2 Voltammetric Parameters and Electrochemical Cells Voltammetric experiments were carried out using a mautolab running with GPES 4.9 software, Eco-Chemie, Utrecht, The Netherlands. The measurements were carried out using a three-electrode system in a 0.5 ml onecompartment electrochemical cell of capacity 2 ml (Cypress System Inc., USA). GCE (d = 1.5 mm) was the Table 1. Supporting electrolyte solutions [30]. ph Composition 2.0 HCl+KCl 3.4 HAcO + NaAcO 4.3 HAcO + NaAcO 5.4 HAcO + NaAcO 6.1 NaH 2 PO 4 + Na 2 HPO NaH 2 PO 4 + Na 2 HPO NaH 2 PO 4 + Na 2 HPO NH 3 +NH 4 Cl 10.5 NH 3 +NH 4 Cl 12.0 NaOH + KCl working electrode, Pt wire the counter electrode and the Ag/AgCl (3 M KCl) reference electrode. The experimental conditions for DP voltammetry were: pulse amplitude 50 mv, pulse width 70 ms and scan rate 5 mv s 1. For SW voltammetry a frequency of 50 Hz and a potential increment of 2 mv, corresponding to an effective scan rate of 100 mvs 1 were used. The GCE was polished using diamond spray, particle size 3 mm (Kemet, UK) before each electrochemical experiment. After polishing, it was rinsed thoroughly with Milli-Q water. Following this mechanical treatment, the GCE was placed in supporting electrolyte and differential pulse voltammograms were recorded until a steady state baseline voltammogram was obtained. This procedure ensured very reproducible experimental results. 2.3 Acquisition and Presentation of Voltammetric Data All the DP voltammograms presented were backgroundsubtracted and baseline-corrected using the moving average application with a step window of 5 mv included in GPES version 4.9 software. This mathematical treatment improves the visualization and identification of peaks over the baseline without introducing any artefact, although the peak intensity is, in some cases, reduced (< 10%) relative to that of the untreated curve. This mathematical treatment of the original voltammograms was used in the presentation of all experimental voltammograms for a better and clearer identification of the peaks. Nevertheless, the values for peak current presented in all plots were determined from the original untreated voltammograms after subtraction of the baseline. 3 Results and Discussion The electrochemical behaviour of MTX was investigated in N 2 saturated ph M acetate buffer by CV at scan rate 100 mv s 1, using a GCE. The CVs were recorded in the interval between 0.5 V and V, starting from 0.0 V towards the positive potential limit (Figure 1A) and from 0.0 V towards the negative potential limit (Figure 1B). The results showed that MTX undergoes oxidation, peak 1 a, and reduction, peak 3 c, in a complex redox process. Electroactive products after MTX oxidation, peaks 2 a 2 c, and after MTX reduction, peak 4 a, were obtained. A similar behaviour was observed in all supporting electrolytes. Since the oxidation and reduction of MTX occur independently of each other they were investigated separately. 3.1 Oxidation Cyclic Voltammetry A. D. R. Pontinha et al. The oxidation behaviour of MTX was studied by CV in a 30 mm MTX in ph M acetate buffer solution at a Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim Electroanalysis 2012, 24, No. 4,
3 Antineoplasic Drug Methotrexate Redox Mechanism Using a GCE Fig. 2. CVs in N 2 saturated solutions of 30 mm MTX in ph M acetate buffer; ( ) first and ( ) second scan at v= 100 mv s 1. Fig. 1. CVs in a N 2 saturated solution of 30 mm MTX in ph M acetate buffer recorded between 0.5 V and V, starting from 0.00 V: (A) in the positive direction and (B) in the negative direction, ( ) first and ( ) second scans at v=100 mv s 1. scan rate v=100 mv s 1, in the interval 0.50 V and V, starting from 0.0 V towards 0.50 V (Figure 2). On the first CV no cathodic peak was observed but after reversing the scan direction at V two anodic peak 1 a, at E p1 a =+0.77 V, and peak 1 a, at E p1 a = V, occurred (Figure 2). On the second CV obtained without cleaning the GCE surface, a new reduction peak 2 c, at E p2c = 0.43 V, appeared and after changing the scan direction the corresponding anodic peak 2 a,ate p2a = 0.40 V, occurred. These peaks are due to the reversible reaction of the MTX oxidation product formed at the GCE surface during the first scan. The decrease of peaks 1 a and 1 a currents observed on the second scan is explained by the adsorption of MTX oxidation products at the electrode surface. The concentration of MTX adsorbed onto the GCE surface in ph M acetate buffer electrolyte solution was calculated from the CV in Figure 2 using the equation G MTX = Q (n F A) 1, where the charge Q = C, from the area under the peak, the number of electrons transferred n = 2 (see Section 3.1.2), the Faraday constant F=96485 C mol 1 and the electrode area A= cm 2. The MTX total surface concentration of G MTX = molcm 2 was obtained. Similar experiments were carried out in supporting electrolytes with different ph values. The CVs obtained showed the same behaviour confirming the irreversibility of peaks 1 a and 1 a and the reversibility of MTX oxidation product peak 2 c, which with increasing ph was shifted to more negative potentials. The product formed after MTX oxidation was reversibly reduced, peaks 2 c 2 a (Figures 1 and 2A). CV was used in order to characterise the ph behaviour of these processes. Both peaks are ph dependent their potentials shifted to more negative values with increasing ph. The relationship is linear and the slope of 59 mv per ph unit shows that the same number of electrons and protons is involved in the redox mechanism of MTX oxidation product. Considering that the difference between peaks potential and their potential at half height is j E p E p/2 j = 56.6/n 30 mv, the redox process of MTX oxidation product occurs with transfer of two electrons and two protons Differential Pulse Voltammetry and ph Effect A ph study of MTX oxidation was carried out by DP voltammetry in 30 mm MTX solutions for electrolytes with 2.0 <ph < One main oxidation peak occurred on the first DP voltammogram in all supporting electrolytes. Two consecutive charge transfer reactions were observed for 3.4<pH <10.5 (Figure 3A). In the first DP voltammogram at ph 6.1, peak 1 a occurred at E p1 a =+0.75 V and peak 1 a, ate p1 a =+0.90 V (Figure 3B). Electroanalysis 2012, 24, No. 4, Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim 919
4 A. D. R. Pontinha et al. Fig. 3. DP voltammograms base-line corrected in 30 mm MTX: A) 3D plot of the first scan as a function of ph of the supporting electrolyte and B) in ph M phosphate buffer; first ( ), second ( ) and third (----) scans. The occurrence of these two oxidation peaks is explained considering that the MTX molecule that diffuses from the bulk solution and can adsorb on the electrode surface in a planar or in a perpendicular position but the MTX electroactive centre is the same. In the planar position, the aromatic ring is parallel to the electrode surface, facilitating the electron transfer and the oxidation potential is lower, peak 1 a. In the perpendicular orientation to the electrode surface, the oxidation process is more difficult and occurs at a higher potential, peak 1 a. The MTX molecules adsorbed in the monolayer have the possibility of movement and different orientations on the GCE surface, being responsible for the occurrence of peaks 1 a and 1 a. After scanning the potential, the MTX molecules are rearranged on the electrode surface and on the second and third scans, obtained in the same conditions without cleaning the electrode surface, only one oxidation peak 1 a appeared [31] (Figure 3B). Successive DP voltammograms were recorded in all electrolytes and a similar behaviour was observed. Fig. 4. (A) 3D plot of second scan of base-line corrected DPVs in 30 mm MTX as a function of ph of the supporting electrolyte. (B) Plot of E pa (&) and I pa (*) of second scan of peak 1 a vs. ph. The orientation of the adsorbed MTX molecules was not dependent on the solution concentration. Peaks 1 a and 1 a always occurred in DP voltammograms in different concentrated solutions of mm, using a clean GCE surface, and a similar behaviour has been observed [31 and references therein]. For this reason, the second DP voltammogram of peak 1 a was selected to study the ph-dependence of MTX oxidation (Figure 4A). Increasing the ph of the supporting electrolyte, the potential of peak 1 a shifted to more negative values, and a linear dependence was found for ph < 5.4 following the equation E p1a = ph (Figure 4B). The slope of 60 mv per ph unit indicated that the MTX oxidation processes involve the same number of electrons and protons. The width at half-height peak 1 a was found to be W 1/2 ~ 61 mv for the lowest concentration used (0.2 mm), close to the theoretical value for the transfer of two electrons [32], so the oxidation of MTX occurs with the transfer of two electrons and two protons. The current of the peak 1 a showed a maximum value at around ph 4.3 (Figure 4B). For ph >5.4, the oxidation process of MTX does not depend on the ph of the supporting electrolyte. This Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim Electroanalysis 2012, 24, No. 4,
5 Antineoplasic Drug Methotrexate Redox Mechanism Using a GCE effect is specific to an electrochemical reaction in which the transfer of electrons is followed by the chemical deprotonation of the oxidation product and allowed the determination of pk a ~ 5.4 of MTX oxidation product. Three values of pk a, associated to the different groups, are described [11]. The value of pk a ~5.4 determined is only related with the redox behaviour of MTX oxidation product. 3.2 Reduction Cyclic Voltammetry The reduction of MTX at a GCE was initially investigated by CV, in N 2 saturated solutions of 30 mm MTX ph M acetate buffer, at a scan rate v=100 mv s 1, starting from 0.0 V towards V and reversing until 1.30 V (Figure 5). On the first positive-going scan, no peak was observed but on the negative-going scan a cathodic peak 3 c, at E p3c = 0.57 V, occurred. Changing the scan direction, the corresponding anodic peak 3 a, at E p3a = 0.52 V, appeared. On the second CV, a new anodic peak 4 a, at E p4a =+0.57 V, was only observed by CV, corresponding to the oxidation of MTX reduction product (Figure 5). The small peaks are due to the electroactive functional groups (carbonyl, carboxyl, etc) onto the GCE surface. CVs were also obtained in N 2 saturated solutions of 30 mm MTX at a scan rate v=100 mv s 1 in supporting electrolytes with different ph values. The oxidation peak 4 a only appeared for ph <7.0, and the potential shifted to more negative values with increasing ph, in a linear relationship with the slope of 59 mv per ph unit, showing that the mechanism involves the same number of electrons and protons. The difference between peak potential and the half-wave potential, j E pa E p/2a j ~51 mv, so two electrons were transferred. Therefore, it can be concluded Fig. 6. (A) 3D plot of reduction of base-line corrected DP voltammograms in N 2 saturated 30 mm MTX as a function of ph of the supporting electrolyte. (B) Plot of E pc (&) of peak 3 c vs. ph. that oxidation of MTX reduction product at peak 4 a occurs with the transfer of two electrons and two protons Differential Pulse Voltammetry and ph Effect Fig. 5. CVs in N 2 saturated solutions of 30 mm MTX in ph M acetate buffer; ( ) first and ( ) second scan at v= 100 mv s 1. The ph study of MTX reduction process was carried out by DP voltammetry in 30 mm MTX solutions in N 2 saturated electrolytes with 2.0 < ph < 12.0 (Figure 6A). The DP voltammograms showed the reduction peak 3 c in all supporting electrolytes. The peak 3 c potential was shifted with increasing ph to more negative potentials. The dependence with ph was linear and following the relationship E p3c (V) = ph (Figure 6B). The slope of 60 mv per ph unit shows that the same number of electrons and protons is involved in the reduction mechanism of MTX. The width Electroanalysis 2012, 24, No. 4, Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim 921
6 A. D. R. Pontinha et al. The great advantage of SWV is the possibility to see during only one scan if the electron transfer reaction is reversible or not. Since the current is sampled in both positive and negative-going pulses, peaks corresponding to the oxidation and reduction of the electroactive species at the electrode surface can be obtained at the same time, greater speed of analysis, lower consumption of the electroactive species in relation with DP voltammetry, and reduced problems with poisoning of the electrode surface [32]. The reversibility of peak 3 c was confirmed by plotting the forward and backward components of the total current (Figure 7). 3.3 Redox Mechanism Fig. 7. SW voltammogram in a N 2 saturated solution of 30 mm MTX in ph M acetate buffer; f = 50 Hz, DE s =2mV, pulse amplitude 100 mv, v eff = 50 mv s 1 ; I t : total current, I f : forward current, I b : backward current. at half-height of peak 3 c was always W 1/2 = 60 mv, which suggests that the reduction of MTX occurs with two electrons and two protons Square Wave Voltammetry SW voltammetry showed similar features to DP voltammograms and CV. The first SW voltammogram in a N 2 saturated solution of 30 mm MTX in ph M phosphate buffer, showed the MTX reduction peak 3 c, at E p3c = 0.65 V (Figure 7). The results obtained indicated that the oxidation and reduction of MTX follows two distinct redox processes that involve the formation of electroactive products. The oxidation of MTX, peak 1 a, is irreversible and corresponds to the electro-oxidation of the pyrazine moiety involving a mechanism of two electrons and two protons (Scheme 2A). The oxidation product is 7-hydroxymethotrexate (7-OH-MTX) [14] which is in vivo the main MTX metabolite. The results obtained showed that 7-OH-MTX is reduced, peaks 2 c 2 a, similarly to other pteridine compounds [28] in a two electron two proton mechanism. The reduction of MTX, cathodic peak 3 c (Figure 5), involves the transfer of two electrons and two protons corresponding to the reduction of the diamino-pteridinyl moiety to yield a 5,8-dihydro derivative as in other pteridine compounds, which undergoes, peaks 4 a, a two electrons and two protons electrochemical irreversible oxida- Scheme 2. Proposed redox mechanism of MTX: A) oxidation and B) reduction Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim Electroanalysis 2012, 24, No. 4,
7 Antineoplasic Drug Methotrexate Redox Mechanism Using a GCE tion (Scheme 2B). The formation the 5,8-dihydro derivative has also been reported in the literature [28]. 4 Conclusions The study of the redox behaviour of different organic compounds using electrochemical techniques can provide valuable insights into the biological redox reactions of these molecules and of their metabolites. The electrochemical investigation of MTX redox behaviour was carried out in a wide ph range and showed that MTX undergoes oxidation and reduction at a GCE. The oxidation of MTX is an irreversible process that occurs with the transfer of two electrons and two protons and the formation of 7-hydroxymethotrexate. This process is ph-dependent for electrolytes with ph < 5.4 and leads to the formation of an electroactive product that adsorbs on the electrode surface and undergoes reversible redox reaction. The reduction of MTX is a reversible, ph-dependent process which involves the transfer of two electrons and two protons, with the formation of an electroactive product that undergoes irreversible oxidation. Acknowledgements Financial support from Fundażo para a CiÞncia e Tecnologia (FCT), PhD Grant SFRH/BD/46026/2008 (A. D. R. Pontinha), Post-Doctoral Grant SFRH/BPD/36110/2007 (V. C. Diculescu), Projects PTDC/QUI/098562/2008 and PTDC/SAU-BEB/104643/2008, POCI 2010 (co-financed by the European Community Fund FEDER), and CEMUC-R (Research Unit 285), and CAPES-Brasil, Post-Doctoral Grant/ (S. M. A. Jorge), is gratefully acknowledged. References [1] M. C. Perry, in The Chemotherapy Source Book, Lippincott, Williams & Wilkins, Pennsylvania, USA 1996, pp [2] R. S. Vardanyan, V. J. Hruby, in Synthesis of Essential Drugs, (Eds: R. S. Vardanyan, V. J. Hruby), Elsevier, Amsterdam, The Netherlands 2006, pp [3] M. Krajinovic, A. Moghrabi, Pharmacogenomics 2004, 5, 819. [4] W. A. Bleyer, Cancer 1978, 41, 36. [5] W. A. Bleyer, Cancer Treat. Rev. 1977, 4, 87. [6] M. Chow, H. Rubin, Proc. Natl. Acad. Sci. USA 1998, 95, [7] H.-P. Lipp, J. T. Hartmann, in: Side Effects of Drugs Annual, Vol. 29 (Ed: J. K. Aronson), Elsevier, Amsterdam, The Netherlands 2007, pp [8] S. Manfrida, S. Chiesa, L. Teofili, B. Diletto, S. Hohaus, A. Fiorentino, B. De Bari, V. Frascino, C. Aristei, M. Balducci, Eur. J. Cancer Supplements 2010, 8, 22. [9] P. J. Mease, B. S. Goffe, J. Metz, A. VanderStoep, B. Finck, D. J. Burge, Lancet 2000, 356, 385. [10] I. J. Cohen, Med. Hypotheses 2007, 68, [11] F. M. Rubino, J. Chromatogr. B 2001, 764, 217. [12] T. Hirai, S. Matsumoto, I. Kishi, J. Chromatogr. B 1997, 690, 267. [13] H. Aboleneen, J. Simpson, D. Backes, J. Chromatogr. B 1996, 681, 317. [14] F. Palmisano, T. R. I. Cataldi, P. G. Zambonin, J. Chromatogr. B 1985, 344, 249. [15] I. D. Merµs, A. E. Mansilla, F. S. López, M. J.R. Gómez, Talanta 2001, 55, 623. [16] S. M. Sabry, M. Abdel-Hady, M. Elsayed, O. T. Fahmy, H. M. Maher, J. Pharm. Biomed. Anal. 2003, 32, 409. [17] S. Pinzauti, P. Gratteri, S. Furlanetto, P. Mura, E. Dreassi, R. Phan-Tan-Luu, J. Pharm. Biomed. Anal. 1996, 41, 881. [18] F. Wang, Y. Wu, J. Liu, B. Ye, Electrochim. Acta 2009, 54, [19] A. Temizer, A. N. Onar, Talanta 1988, 35, 805. [20] L. Gao, Y. Wu, J. Liu, Y. Baoxian, J. Electroanal. Chem. 2007, 610, 131. [21] R. Selesovska, L. Bandzuchova, T. Navratil, Electroanalysis 2011, 23, 177. [22] B.-X. Ye, S. Qu, F. Wang, L. Li, J. Chin. Chem. Soc. 2005, 52, [23] R. C. Gurira, L. D. Bowers, J. Electroanal. Chem. 1983, 146, 109. [24] R. C. Gurira, L. D. Bowers, J. Electroanal. Chem. 1987, 220, 323. [25] A. J. M. Ordieres, A. C. García, J. M. F. Alvarez, P. T. Blanco, Anal. Chim. Acta 1990, 233, 281. [26] S. M. A. Jorge, A. D. R. Pontinha, A. M. Oliveira-Brett, Electroanalysis 2010, 22, 625. [27] A. D. R. Pontinha, S. C. B. Oliveira, A. M. Oliveira-Brett, Electroanalysis 2008, 20, [28] V. C. Diculescu, A. Militaru, A. Shah, R. Qureshi, L. Tugulea, A. M. Oliveira Brett, J. Electroanal. Chem. 2010, 647, 1. [29] S. C. B. Oliveira, M. Vivan, A. M. Oliveira-Brett, Electroanalysis 2008, 20, [30] D. D. Perrin, B. Dempsey, in Buffers for ph and Metal Ion Control, Chapman and Hall Laboratory Manuals, London [31] Y. Wang, S. R. Belding, E. I. Rogers, R. G. Compton, J. Electroanal. Chem. 2011, 650, 196. [32] C. M. A. Brett, A. M. Oliveira-Brett, in Electrochemistry: Principles, Methods and Applications, Oxford Science University Publications, Oxford, UK Electroanalysis 2012, 24, No. 4, Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim 923
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