Binding patterns and structure-affinity relationships of food azo dyes with lysozyme: A multitechnique approach

Journal of Agricultural and Food Chemistry

Volumn 61, Issue 50, 2013, Pages 12415-12428

  Peng, Wei ^a,b   Ding, Fei ^b,c   Peng, Yu Kui ^a   Jiang, Yu Ting ^d   Zhang, Li ^b  

^a NORTHWEST A F UNIVERSITY   (China)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

^c Massachusetts Institute of Technology Cambridge   (United States)

^d UNIVERSITY OF OTTAWA   (Canada)

Author keywords

circular dichroism; fluorescence; food azo dye; lysozyme; molecular modeling; structure affinity relationship

Indexed keywords

COMPUTATIONAL ANALYSIS; FLUORESCENCE EMISSION; FLUORESCENCE EMISSION SPECTRA; MULTI-TECHNIQUE APPROACH; PHYSIOLOGICAL CONDITION; STRUCTURE-AFFINITY RELATIONSHIPS; SYNCHRONOUS FLUORESCENCE; TIME-RESOLVED FLUORESCENCE;

AMINO ACIDS; AZO DYES; AZOBENZENE; BINDING ENERGY; DICHROISM; EMISSION SPECTROSCOPY; ENERGY TRANSFER; FLUORESCENCE; HYDROGEN BONDS; MOLECULAR MODELING; PHYSIOLOGICAL MODELS; PROTEINS; TOXICITY;

ENZYMES;

FOOD DYE; LYSOZYME;

ARTICLE; CHEMICAL MODEL; CHEMICAL PHENOMENA; CHEMISTRY; CIRCULAR DICHROISM; ENZYME STABILITY; HUMAN; KINETICS; PROTEIN BINDING;

CIRCULAR DICHROISM; ENZYME STABILITY; FOOD COLORING AGENTS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; KINETICS; MODELS, CHEMICAL; MURAMIDASE; PROTEIN BINDING;

EID: 84890734208     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf4039327     Document Type: Article

References (80)

1. Ferreira, G. R.; Garcia, H. C.; Couri, M. R. C.; Santos, H. F. D.; de Oliveira, L. F. C. On the azo/hydrazo equilibrium in Sudan I azo dye derivatives J. Phys. Chem. A 2013, 117, 642-649
2. Almeida, M. R.; Stephani, R.; Santos, H. F. D.; de Oliveira, L. F. C. Spectroscopic and theoretical study of the "azo"-dye E124 in condensate phase: Evidence of a dominant hydrazo form J. Phys. Chem A 2010, 114, 526-534
3. Hsu, C.-A.; Wen, T.-N.; Su, Y.-C.; Jiang, Z.-B.; Chen, C.-W.; Shyur, L.-F. Biological degradation of anthroquinone and azo dyes by a novel laccase from Lentinus sp Environ. Sci. Technol. 2012, 46, 5109-5117
4. Kobylewski, S.; Jacobson, M. F. Toxicology of food dyes Int. J. Occup. Environ. Health. 2012, 18, 220-246
5. Cheung, W.; Shadi, I. T.; Xu, Y.; Goodacre, R. Quantitative analysis of the banned food dye Sudan-1 using surface enhanced Raman scattering with multivariate chemometrics J. Phys. Chem. C 2010, 114, 7285-7290
6. Seiber, J. N.; Kleinschmidt, L. From detrimental to beneficial constituents in foods: Tracking the publication trends in JAFC J. Agric. Food Chem. 2012, 60, 6644-6647
7. Radomski, J. L. Toxicology of food colors Annu. Rev. Pharmacol. 1974, 14, 127-137
8. Swanson, J. M.; Kinsbourne, M. Food dyes impair performance of hyperactive children on a laboratory learning test Science 1980, 207, 1485-1487
9. Bateman, B.; Warner, J. O.; Hutchinson, E.; Dean, T.; Rowlandson, P.; Gant, C.; Grundy, J.; Fitzgerald, C.; Stevenson, J. The effects of a double blind, placebo controlled, artificial food colourings and benzoate preservative challenge on hyperactivity in a general population sample of preschool children Arch. Dis. Child. 2004, 89, 506-511
10. McCann, D.; Barrett, A.; Cooper, A.; Crumpler, D.; Dalen, L.; Grimshaw, K.; Kitchin, E.; Lok, K.; Porteous, L.; Prince, E.; Sonuga-Barke, E.; Warner, J. O.; Stevenson, J. Food additives and hyperactive behaviour in 3-year-old and 8/9-year-old children in the community: a randomised, double-blinded, placebo-controlled trial Lancet 2007, 370, 1560-1567
11. Brown, M. A.; DeVito, S. C. Predicting azo dye toxicity Crit. Rev. Environ. Sci. Technol. 1993, 23, 249-324
12. Hashem, M. M.; Atta, A. H.; Arbid, M. S.; Nada, S. A.; Asaad, G. F. Immunological studies on Amaranth, Sunset Yellow and Curcumin as food colouring agents in albino rats Food Chem. Toxicol. 2010, 48, 1581-1586
13. Brown, J. P.; Roehm, G. W.; Brown, R. J. Mutagenicity testing of certified food colors and related azo, xanthene and triphenylmethane dyes with the Salmonella/microsome system Mutat. Res., Fundam. Mol. Mech. Mutagen. 1978, 56, 249-271
14. Chung, K.-T.; Fulk, G. E.; Andrews, A. W. Mutagenicity testing of some commonly used dyes Appl. Environ. Microbiol. 1981, 42, 641-648
15. Chung, K.-T. The significance of azo-reduction in the mutagenesis and carcinogenesis of azo dyes Mutat. Res., Rev. Genet. Toxicol. 1983, 114, 269-281
16. Malachová, K.; Pavlícková, Z.; Novotný, C.; Svobodová, K.; Lednická, D.; Musílková, E. Reduction in the mutagenicity of synthetic dyes by successive treatment with activated sludge and the ligninolytic fungus, Irpex lacteus Environ. Mol. Mutagen. 2006, 47, 533-540
17. Sharma, S.; Sharma, S.; Upreti, N.; Sharma, K. P. Monitoring toxicity of an azo dye methyl red and a heavy metal Cu, using plant and animal bioassays Toxicol. Environ. Chem. 2009, 91, 109-120
18. Bonser, G. M.; Bradshaw, L.; Clayson, D. B.; Jull, J. W. A further study of the carcinogenic properties of ortho hydroxy-amines and related compounds by bladder implantation in the mouse Br. J. Cancer 1956, 10, 539-546
19. Chung, K.-T.; Stevens, S. E., Jr. The reduction of azo dyes by the intestinal microflora Crit. Rev. Microbiol. 1992, 18, 175-190
20. Tsuda, S.; Murakami, M.; Matsusaka, N.; Kano, K.; Taniguchi, K.; Sasaki, Y. F. DNA damage induced by red food dyes orally administered to pregnant and male mice Toxicol. Sci. 2001, 61, 92-99
21. Combes, R. D.; Haveland-Smith, R. B. A review of the genotoxicity of food, drug and cosmetic colours and other azo, triphenylmethane and xanthenes dyes Mutat. Res., Rev. Genet. Toxicol. 1982, 98, 101-243
22. Yadav, A.; Kumar, A.; Dwivedi, P. D.; Tripathi, A.; Das, M. In vitro studies on immunotoxic potential of Orange II in splenocytes Toxicol. Lett. 2012, 208, 239-245
23. Nuin, E.; Andreu, I.; Torres, M. J.; Jiménez, M. C.; Miranda, M. A. Enhanced photosafety of cinacalcet upon complexation with serum albumin J. Phys. Chem. B 2011, 115, 1158-1164
24. Bolel, P.; Mahapatra, N.; Halder, M. Optical spectroscopic exploration of binding of Cochineal Red A with two homologous serum albumins J. Agric. Food Chem. 2012, 60, 3727-3734
25. Son, I.; Shek, Y. L.; Dubins, D. N.; Chalikian, T. V. Volumetric characterization of tri- N -acetylglucosamine binding to lysozyme Biochemistry 2012, 51, 5784-5790
26. Fleming, A. On a remarkable bacteriolytic element found in tissues and secretions Proc. R. Soc. Lond. B: Biol. Sci. 1922, 93, 306-317
27. Kirby, A. J. The lysozyme mechanism sorted-after 50 years Nat. Struct. Biol. 2001, 8, 737-739
28. Haas, M.; Kluppel, A. C. A.; Wartna, E. S.; Moolenaar, F.; Meijer, D. K. F.; de Jong, P. E.; de Zeeuw, D. Drug-targeting to the kidney: renal delivery and degradation of a naproxen-lysozyme conjugate in vivo Kidney Int. 1997, 52, 1693-1699
29. Phillips, R. A. Kidney Annu. Rev. Physiol. 1949, 11, 493-526
30. Rennick, B. R. Renal excretion of drugs: tubular transport and metabolism Annu. Rev. Pharmacol. 1972, 12, 141-156
31. Morrissey, K. M.; Stocker, S. L.; Wittwer, M. B.; Xu, L.; Giacomini, K. M. Renal transporters in drug development Annu. Rev. Pharmacol. Toxicol. 2013, 53, 503-529
32. Lowry, O. H.; Rosebrough, N. J.; Farr, A. L.; Randall, R. J. Protein measurement with the Folin phenol reagent J. Biol. Chem. 1951, 193, 265-275
33. Greenfield, N. J. Using circular dichroism spectra to estimate protein secondary structure Nat. Protoc. 2006, 1, 2876-2890
34. Lakowicz, J. R. Principles of Fluorescence Spectroscopy, 3 rd ed.; Springer Science + Business Media: New York, NY, 2006; pp 97-330.
35. Bi, S. Y.; Ding, L.; Tian, Y.; Song, D. Q.; Zhou, X.; Liu, X.; Zhang, H. Q. Investigation of the interaction between flavonoids and human serum albumin J. Mol. Struct. 2004, 703, 37-45
36. Monti, S.; Manet, I.; Marconi, G. Combination of spectroscopic and computational methods to get an understanding of supramolecular chemistry of drugs: from simple host systems to biomolecules Phys. Chem. Chem. Phys. 2011, 13, 20893-20905
37. Greenfield, N. J. Using circular dichroism collected as a function of temperature to determine the thermodynamics of protein unfolding and binding interactions Nat. Protoc. 2006, 1, 2527-2535
38. Lloyd, J. B. F. Synchronized excitation of fluorescence emission spectra Nat. Phys. Sci. 1971, 231, 64-65
39. Fuller, C. W.; Miller, J. N. Silver Medal lectures Proc. Anal. Div. Chem. Soc. 1979, 16, 199-208
40. Abou-Zied, O. K. Spectroscopy of hydroxyphenyl benzazoles in solution and human serum albumin: detecting flexibility, specificity and high affinity of the warfarin drug binding site RSC Adv. 2013, 3, 8747-8755
41. Lehrer, S. S. Solute perturbation of protein fluorescence. The quenching of the tryptophyl fluorescence of model compounds and of lysozyme by iodide ion Biochemistry 1971, 10, 3254-3263
42. Paul, B. K.; Guchhait, N. A spectral deciphering of the binding interaction of an intramolecular charge transfer fluorescence probe with a cationic protein: thermodynamic analysis of the binding phenomenon combined with blind docking study Photochem. Photobiol. Sci. 2011, 10, 980-991
43. De-Llanos, R.; Sánchez-Cortes, S.; Domingo, C.; García-Ramos, J. V.; Sevilla, P. Surface plasmon effects on the binding of antitumoral drug emodin to bovine serum albumin J. Phys. Chem. C 2011, 115, 12419-12429
44. Mitra, P.; Banerjee, M.; Biswas, S.; Basu, S. Protein interactions of Merocyanine 540: spectroscopic and crystallographic studies with lysozyme as a model protein J. Photochem. Photobiol. B: Biol. 2013, 121, 46-56
45. Chodera, J. D.; Mobley, D. L. Entropy-enthalpy compensation: role and ramifications in biomolecular ligand recognition and design Annu. Rev. Biophys. 2013, 42, 121-142
46. Ross, P. D.; Subramanian, S. Thermodynamics of protein association reactions: forces contributing to stability Biochemistry 1981, 20, 3096-3102
47. Abou-Zied, O. K.; Al-Lawatia, N.; Elstner, M.; Steinbrecher, T. B. Binding of hydroxyquinoline probes to human serum albumin: combining molecular modeling and Förster's resonance energy transfer spectroscopy to understand flexible ligand binding J. Phys. Chem. B 2013, 117, 1062-1074
48. Kragh-Hansen, U. Structure and ligand binding properties of human serum albumin Dan. Med. Bull 1990, 37, 57-84
49. Froehlich, E.; Mandeville, J. S.; Jennings, C. J.; Sedaghat-Herati, R.; Tajmir-Riahi, H. A. Dendrimers bind human serum albumin J. Phys. Chem. B 2009, 113, 6986-6993
50. Imoto, T.; Forster, L. S.; Rupley, J. A.; Tanaka, F. Fluorescence of lysozyme: emissions from tryptophan residues 62 and 108 and energy migration Proc. Natl. Acad. Sci. U.S.A. 1971, 69, 1151-1155
51. Stryer, L. Fluorescence spectroscopy of proteins Science 1968, 162, 526-533
52. Stryer, L. The interaction of a naphthalene dye with apomyoglobin and apohemoglobin: a fluorescent probe of non-polar binding sites J. Mol. Biol. 1965, 13, 482-495
53. Blake, C. C. F.; Koenig, D. F.; Mair, G. A.; North, A. C. T.; Phillips, D. C.; Sarma, V. R. Structure of hen egg-white lysozyme: a three-dimensional Fourier synthesis at 2 Å resolution Nature 1965, 206, 757-761
54. Beechem, J. M.; Brand, L. Time-resolved fluorescence of proteins Annu. Rev. Biochem. 1985, 54, 43-71
55. Stryer, L. Fluorescence energy transfer as a spectroscopic ruler Annu. Rev. Biochem. 1978, 47, 819-846
56. Miller, J. N. Fluorescence energy transfer methods in bioanalysis Analyst 2005, 130, 265-270
57. Clegg, R. M. The vital contributions of Perrin and Förster Biophoton. Int. 2004, 11, 42-45
58. Bonan, S.; Fedrizzi, G.; Menotta, S.; Elisabetta, C. Simultaneous determination of synthetic dyes in foodstuffs and beverages by high-performance liquid chromatography coupled with diode-array detector Dyes Pigm. 2013, 99, 36-40
59. Seiber, J. N.; Kleinschmidt, L. A. Contributions of pesticide residue chemistry to improving food and environmental safety: Past and present accomplishments and future challenges J. Agric. Food Chem. 2011, 59, 7536-7543
60. Armbrust, K.; Burns, M.; Crossan, A. N.; Fischhoff, D. A.; Hammond, L. E.; Johnston, J. J.; Kennedy, I.; Rose, M. T.; Seiber, J. N.; Solomon, K. Perspectives on communicating risks of chemicals J. Agric. Food Chem. 2013, 61, 4676-4691
61. Yadav, A.; Kumar, A.; Tripathi, A.; Das, M. Sunset yellow FCF, a permitted food dye, alters functional responses of splenocytes at non-cytotoxic dose Toxicol. Lett. 2013, 217, 197-204
62. Iranfar, H.; Rajabi, O.; Salari, R.; Chamani, J. Probing the interaction of human serum albumin with ciprofloxacin in the presence of silver nanoparticles of three sizes: Multispectroscopic and ζ potential investigation J. Phys. Chem. B 2012, 116, 1951-1964
63. Mansouri, M.; Pirouzi, M.; Saberi, M. R.; Ghaderabad, M.; Chamani, J. Investigation on the interaction between cyclophosphamide and lysozyme in the presence of three different kind of cyclodextrins: Determination of the binding mechanism by spectroscopic and molecular modeling techniques Molecules 2013, 18, 789-813
64. Teilum, K.; Olsen, J. G.; Kragelund, B. B. Protein stability, flexibility and function Biochim. Biophys. Acta, Proteins Proteomics 2011, 1814, 969-976
65. Sattar, Z.; Iranfar, H.; Asoodeh, A.; Saberi, M. R.; Mazhari, M.; Chamani, J. Interaction between holo transferrin and HSA-PPIX complex in the presence of lomefloxacin: An evaluation of PPIX aggregation in protein-protein interactions Spectrochim. Acta, Part A 2012, 97, 1089-1100
66. Bourassa, P.; Bariyanga, J.; Tajmir-Riahi, H. A. Binding sites of resveratrol, genistein, and curcumin with milk α- and β-caseins J. Phys. Chem. B 2013, 117, 1287-1295
67. Kanakis, C. D.; Tarantilis, P. A.; Polissiou, M. G.; Tajmir-Riahi, H. A. Probing the binding sites of resveratrol, genistein, and curcumin with milk β -lactoglobulin J. Biomol. Struct. Dyn. 2012, 12, 1455-1466
68. Tsuda, S.; Matsusaka, N.; Madarame, H.; Ueno, S.; Susa, N.; Ishida, K.; Kawamura, N.; Sekihashi, K.; Sasaki, Y. F. The comet assay in eight mouse organs: results with 24 azo compounds Mutat. Res., Genet. Toxicol. Environ. Mutagen. 2000, 465, 11-26
69. Amin, K. A.; Hameid, H. A., II; Elsttar, A. H. A. Effect of food azo dyes tartrazine and carmoisine on biochemical parameters related to renal, hepatic function and oxidative stress biomarkers in young male rats Food Chem. Toxicol. 2010, 48, 2994-2999
70. Tarantal, A. F.; Chen, H.; Shi, T. T.; Lu, C.-H.; Fang, A. B.; Buckley, S.; Kolb, M.; Gauldie, J.; Warburton, D.; Shi, W. Overexpression of transforming growth factor-β1 in fetal monkey lung results in prenatal pulmonary fibrosis Eur. Respir. J. 2010, 36, 907-914
71. Mayi, T. H.; Daoudi, M.; Derudas, B.; Gross, B.; Bories, G.; Wouters, K.; Brozek, J.; Caiazzo, R.; Raverdi, V.; Pigeyre, M.; Allavena, P.; Mantovani, A.; Pattou, F.; Staels, B.; Chinetti-Gbaguidi, G. Human adipose tissue macrophages display activation of cancer-related pathways J. Biol. Chem. 2012, 287, 21904-21913
72. Levy, Y.; Onuchic, J. N. Water mediation in protein folding and molecular recognition Annu. Rev. Biophys. Biomol. Struct. 2006, 35, 389-415
73. Shaban, Z.; El-Shazly, S.; Ishizuka, M.; Kimura, K.; Kazusaka, A.; Fujita, S. PPAR α -dependent modulation of hepatic CYP1A by clofibric acid in rats Arch. Toxicol. 2004, 78, 496-507
74. Stiborová, M.; Martínek, V.; Schmeiser, H. H.; Frei, E. Modulation of CYP1A1-mediated oxidation of carcinogenic azo dye Sudan I and its binding to DNA by cytochrome b5 Neuroendocrinol. Lett. 2006, 27, 35-39
75. Stiborová, M.; Dračínská, H.; Martínek, V.; Svášková, D.; Hodek, P.; Milichovský, J.; Hejduková, Ž.; Brotánek, J.; Schmeiser, H. H.; Frei, E. Induced expression of cytochrome P450 1A and NAD(P)H:quinone oxidoreductase determined at mRNA, protein, and enzyme activity levels in rats exposed to the carcinogenic azo dye 1-phenylazo-2-naphthol (Sudan I) Chem. Res. Toxicol. 2013, 26, 290-299
76. Zhang, Y. Z.; Görner, H. Photoprocesses of chlorine e6 bound to lysozyme or bovin serum albumin Dyes Pigm. 2009, 83, 174-179
77. Zhang, Y. Z.; Görner, H. Photoprocesses of xanthene dyes bound to lysozyme or serum albumin Photochem. Photobiol. 2009, 85, 677-685
78. Morgan, D. L.; Dunnick, J. K.; Goehl, T.; Jokinen, M. P.; Matthews, H. B.; Zeiger, E.; Mennear, J. H. Summary of the National Toxicology Program benzidine dye initiative Environ. Health Perspect. 1994, 102, 63-78
79. Feng, J. H.; Cerniglia, C. E.; Chen, H. Z. Toxicological significance of azo dye metabolism by human intestinal microbiota Front. Biosci., Elite Ed. 2012, 4, 568-586
80. Stingley, R. L.; Zou, W.; Heinze, T. M.; Chen, H. Z.; Cerniglia, C. E. Metabolism of azo dyes by human skin microbiota J. Med. Microbiol. 2010, 59, 108-114