Bisphenol S Interacts with Catalase and Induces Oxidative Stress in Mouse Liver and Renal Cells

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 34, 2016, Pages 6630-6640

  Zhang, Rui ^a   Liu, Rutao ^a   Zong, Wansong ^b  

^a SHANDONG UNIVERSITY   (China)

^b SHANDONG NORMAL UNIVERSITY   (China)

Author keywords

bisphenol S; catalase; hepatocyte; oxidative stress; renal cell; spectroscopy

Indexed keywords

BINS; CELL DEATH; CELLS; CONSUMER PRODUCTS; HYDROGEN BONDS; MAMMALS; OXIDATIVE STRESS; PHENOLS; SPECTROSCOPY; TOXICITY;

BISPHENOL S; CATALASE; DIRECT INTERACTIONS; FOOD PACKAGING INDUSTRY; HEPATOCYTES; HYDROPHOBIC FORCES; MOLECULAR DOCKING; RENAL CELL;

CYTOLOGY;

4,4' ISOPROPYLIDENEDIPHENOL; BENZHYDRYL DERIVATIVE; CATALASE; ENDOCRINE DISRUPTOR; PHENOL DERIVATIVE; PROTEIN BINDING;

ANIMAL; C57BL MOUSE; CELL CULTURE; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; KIDNEY; LIVER; LIVER CELL; MALE; METABOLISM; MOLECULAR DOCKING; MOUSE; OXIDATIVE STRESS; PROTEIN MOTIF;

AMINO ACID MOTIFS; ANIMALS; BENZHYDRYL COMPOUNDS; CATALASE; CELL SURVIVAL; CELLS, CULTURED; ENDOCRINE DISRUPTORS; HEPATOCYTES; KIDNEY; LIVER; MALE; MICE; MICE, INBRED C57BL; MOLECULAR DOCKING SIMULATION; OXIDATIVE STRESS; PHENOLS; PROTEIN BINDING;

EID: 84984821893     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.6b02656     Document Type: Article

References (59)

1. Liao, C.; Kannan, K. Concentrations and profiles of bisphenol A and other bisphenol analogues in foodstuffs from the United States and their implications for human exposure J. Agric. Food Chem. 2013, 61, 4655-4662 10.1021/jf400445n
2. Dolinoy, D. C.; Huang, D.; Jirtle, R. L. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 13056-13061 10.1073/pnas.0703739104
3. Oz, F.; Seyyar, E. Formation of heterocyclic aromatic amines and migration level of bisphenol-A in sous-vide-cooked trout fillets at different cooking temperatures and cooking levels J. Agric. Food Chem. 2016, 64, 3070-3082 10.1021/acs.jafc.5b05716
4. Melero, J. A.; van Grieken, R.; Morales, G. Advances in the synthesis and catalytic applications of organosulfonic-functionalized mesostructured materials Chem. Rev. 2006, 106, 3790-3812 10.1021/cr050994h
5. Kaiser, J. Controversy continues after panel rules on bisphenol A Science 2007, 317, 884-885 10.1126/science.317.5840.884a
6. Yin, H.; Cui, L.; Ai, S.; Fan, H.; Zhu, L. Electrochemical determination of bisphenol A at Mg-Al-CO 3 layered double hydroxide modified glassy carbon electrode Electrochim. Acta 2010, 55, 603-610 10.1016/j.electacta.2009.09.020
7. Vandenberg, L. N.; Chahoud, I.; Heindel, J. J.; Padmanabhan, V.; Paumgartten, F. J.; Schoenfelder, G. Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A Environ. Health Perspect. 2010, 118, 1055-1070 10.1289/ehp.0901716
8. Ye, X.; Wong, L. Y.; Kramer, J.; Zhou, X.; Jia, T.; Calafat, A. M. Urinary concentrations of bisphenol A and three other bisphenols in convenience samples of U.S. adults during 2000-2014 Environ. Sci. Technol. 2015, 49, 11834-11839 10.1021/acs.est.5b02135
9. Audran, X.; Brehm, D. Proposed Bisphenol A Ban in Food Packaging Would Impact US Exports to France; USDA GAIN Report FR 9090, 2.6; 2012
10. VinÌas, R.; Watson, C. S. Bisphenol S disrupts estradiol-induced nongenomic signaling in a rat pituitary cell line: effects on cell functions Environ. Health Perspect. (Online) 2013, 121, 352 10.1289/ehp.1205826
11. Wang, Y.-Q.; Zhang, H.-M. Effects of bisphenol S on the structures and activities of trypsin and pepsin J. Agric. Food Chem. 2014, 62, 11303-11311 10.1021/jf504347w
12. Zimmerman, J. B.; Anastas, P. T. Toward substitution with no regrets Science 2015, 347, 1198-1199 10.1126/science.aaa0812
13. Liao, C.; Liu, F.; Kannan, K. Bisphenol S, a new bisphenol analogue, in paper products and currency bills and its association with bisphenol A residues Environ. Sci. Technol. 2012, 46, 6515-6522 10.1021/es300876n
14. Liao, C.; Liu, F.; Guo, Y.; Moon, H.-B.; Nakata, H.; Wu, Q.; Kannan, K. Occurrence of eight bisphenol analogues in indoor dust from the United States and several Asian countries: implications for human exposure Environ. Sci. Technol. 2012, 46, 9138-9145 10.1021/es302004w
15. Kinch, C. D.; Ibhazehiebo, K.; Jeong, J.-H.; Habibi, H. R.; Kurrasch, D. M. Low-dose exposure to bisphenol A and replacement bisphenol S induces precocious hypothalamic neurogenesis in embryonic zebrafish Proc. Natl. Acad. Sci. U. S. A. 2015, 112, 1475-1480 10.1073/pnas.1417731112
16. Ike, M.; Chen, M.; Danzl, E.; Sei, K.; Fujita, M. Biodegradation of a variety of bisphenois under aerobic and anaerobic conditions Water Sci. Technol. 2006, 53, 153-160 10.2166/wst.2006.189
17. Danzl, E.; Sei, K.; Soda, S.; Ike, M.; Fujita, M. Biodegradation of bisphenol A, bisphenol F and bisphenol S in seawater Int. J. Environ. Res. Public Health 2009, 6, 1472-1484 10.3390/ijerph6041472
18. Wang, Y.-Q.; Zhang, H.-M.; Cao, J.; Tang, B.-P. Binding of a new bisphenol analogue, bisphenol S to bovine serum albumin and calf thymus DNA J. Photochem. Photobiol., B 2014, 138, 182-190 10.1016/j.jphotobiol.2014.06.002
19. Mathew, M.; Sreedhanya, S.; Manoj, P.; Aravindakumar, C.; Aravind, U. K. Exploring the interaction of bisphenol-S with serum albumins: a better or worse alternative for bisphenol A? J. Phys. Chem. B 2014, 118, 3832-3843 10.1021/jp500404u
20. Ji, K.; Hong, S.; Kho, Y.; Choi, K. Effects of bisphenol s exposure on endocrine functions and reproduction of zebrafish Environ. Sci. Technol. 2013, 47, 8793-8800 10.1021/es400329t
21. Patel, S. J.; Milwid, J. M.; King, K. R.; Bohr, S.; Iracheta-Vellve, A.; Li, M.; Vitalo, A.; Parekkadan, B.; Jindal, R.; Yarmush, M. L. Gap junction inhibition prevents drug-induced liver toxicity and fulminant hepatic failure Nat. Biotechnol. 2012, 30, 179-183 10.1038/nbt.2089
22. Livingstone, D. R. Organic xenobiotic metabolism in marine invertebrates Adv. Comp. Environ. Physiol. 1991, 7, 45-185 10.1007/978-3-642-75897-3-2
23. Ye, X.; Wong, L.-Y.; Kramer, J.; Zhou, X.; Jia, T.; Calafat, A. M. Urinary concentrations of bisphenol A and three other bisphenols in convenience samples of US adults during 2000-2014 Environ. Sci. Technol. 2015, 49, 11834-11839 10.1021/acs.est.5b02135
24. Loew, O. A new enzyme of general occurrence in organisms Science 1900, 11, 701-702 10.1126/science.11.279.701
25. Syed, D. N.; Mukhtar, H. Gender bias in skin cancer: role of catalase revealed J. Invest. Dermatol. 2012, 132, 512-514 10.1038/jid.2011.423
26. Wang, J.; Hao, M.; Liu, C.; Liu, R. Cadmium induced apoptosis in mouse primary hepatocytes: the role of oxidative stress-mediated ERK pathway activation and the involvement of histone H3 phosphorylation RSC Adv. 2015, 5, 31798-31806 10.1039/C5RA03210E
27. Gupta, S.; Verfaillie, C.; Chmielewski, D.; Kren, S.; Eidman, K.; Connaire, J.; Heremans, Y.; Lund, T.; Blackstad, M.; Jiang, Y. Isolation and characterization of kidney-derived stem cells J. Am. Soc. Nephrol. 2006, 17, 3028-3040 10.1681/ASN.2006030275
28. Nakagawa, Y.; Tayama, S. Metabolism and cytotoxicity of bisphenol A and other bisphenols in isolated rat hepatocytes Arch. Toxicol. 2000, 74, 99-105 10.1007/s002040050659
29. Carvalho, M.; RemiaÌo, F.; Milhazes, N.; Borges, F.; Fernandes, E.; Carvalho, F.; Bastos, M. L. The toxicity of N-methyl-α-methyldopamine to freshly isolated rat hepatocytes is prevented by ascorbic acid and N-acetylcysteine Toxicology 2004, 200, 193-203 10.1016/j.tox.2004.03.016
30. Al Maruf, A.; Lip, H.; Wong, H.; O'Brien, P. J. Protective effects of ferulic acid and related polyphenols against glyoxal- or methylglyoxal-induced cytotoxicity and oxidative stress in isolated rat hepatocytes Chem.-Biol. Interact. 2015, 234, 96-104 10.1016/j.cbi.2014.11.007
31. Goth, L. A simple method for determination of serum catalase activity and revision of reference range Clin. Chim. Acta 1991, 196, 143-151 10.1016/0009-8981(91)90067-M
32. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248-254 10.1016/0003-2697(76)90527-3
33. Zamzami, N.; Kroemer, G. The mitochondrion in apoptosis: how Pandora's box opens Nat. Rev. Mol. Cell Biol. 2001, 2, 67-71 10.1038/35048073
34. Idriss, H. T.; Naismith, J. H. TNFα and the TNF receptor superfamily: structure-function relationship(s) Microsc. Res. Tech. 2000, 50, 184-195 10.1002/1097-0029(20000801)50:3<184::AID-JEMT2>3.0.CO;2-H
35. Zhang, K.; Kaufman, R. J. From endoplasmic-reticulum stress to the inflammatory response Nature 2008, 454, 455-462 10.1038/nature07203
36. Reid, T. J.; Murthy, M.; Sicignano, A.; Tanaka, N.; Musick, W.; Rossmann, M. Structure and heme environment of beef liver catalase at 2.5 A resolution Proc. Natl. Acad. Sci. U. S. A. 1981, 78, 4767-4771 10.1073/pnas.78.8.4767
37. Cao, Z.; Liu, R.; Dong, Z.; Yang, X.; Chen, Y. The effect of sarafloxacin on Cu/ZnSOD structure and activity Spectrochim. Acta, Part A 2015, 136, 601-606 10.1016/j.saa.2014.09.073
38. Teng, Y.; Liu, R. Insights into potentially toxic effects of 4-aminoantipyrine on the antioxidant enzyme copper-zinc superoxide dismutase J. Hazard. Mater. 2013, 262, 318-324 10.1016/j.jhazmat.2013.08.047
39. Pan, X.; Qin, P.; Liu, R.; Wang, J. Characterizing the interaction between tartrazine and two serum albumins by a hybrid spectroscopic approach J. Agric. Food Chem. 2011, 59, 6650-6656 10.1021/jf200907x
40. Hao, F.; Jing, M.; Zhao, X.; Liu, R. Spectroscopy, calorimetry and molecular simulation studies on the interaction of catalase with copper ion J. Photochem. Photobiol., B 2015, 143, 100-106 10.1016/j.jphotobiol.2015.01.003
41. Guo, M.; Lü, W.-J.; Li, M.-H.; Wang, W. Study on the binding interaction between carnitine optical isomer and bovine serum albumin Eur. J. Med. Chem. 2008, 43, 2140-2148 10.1016/j.ejmech.2007.11.006
42. Van De Weert, M. Fluorescence quenching to study protein-ligand binding: common errors J. Fluoresc. 2010, 20, 625-629 10.1007/s10895-009-0572-x
43. Lu, D.; Zhao, X.; Zhao, Y.; Zhang, B.; Zhang, B.; Geng, M.; Liu, R. Binding of Sudan II and Sudan IV to bovine serum albumin: comparison studies Food Chem. Toxicol. 2011, 49, 3158-3164 10.1016/j.fct.2011.09.011
44. Congdon, R. W.; Muth, G. W.; Splittgerber, A. G. The binding interaction of Coomassie blue with proteins Anal. Biochem. 1993, 213, 407-413 10.1006/abio.1993.1439
45. Alcala, J. R.; Gratton, E.; Prendergast, F. G. Fluorescence lifetime distributions in proteins Biophys. J. 1987, 51, 597 10.1016/S0006-3495(87)83384-2
46. Seidel, C. A.; Schulz, A.; Sauer, M. H. Nucleobase-specific quenching of fluorescent dyes. 1. Nucleobase one-electron redox potentials and their correlation with static and dynamic quenching efficiencies J. Phys. Chem. 1996, 100, 5541-5553 10.1021/jp951507c
47. Li, H.; Zhao, M.; Su, G.; Lin, L.; Wang, Y. Effect of soy sauce on serum uric acid levels in hyperuricemic rats and identification of flazin as a potent xanthine oxidase inhibitor J. Agric. Food Chem. 2016, 64, 4725-4734 10.1021/acs.jafc.6b01094
48. Wang, J.; Wang, J.; Xu, C.; Liu, R.; Chen, Y. Molecular mechanism of catalase activity change under sodium dodecyl sulfate-induced oxidative stress in the mouse primary hepatocytes J. Hazard. Mater. 2016, 307, 173-183 10.1016/j.jhazmat.2015.11.060
49. Zsila, F.; Bikádi, Z.; Simonyi, M. Probing the binding of the flavonoid, quercetin to human serum albumin by circular dichroism, electronic absorption spectroscopy and molecular modelling methods Biochem. Pharmacol. 2003, 65, 447-456 10.1016/S0006-2952(02)01521-6
50. Xie, X.; Wang, Z.; Zhou, X.; Wang, X.; Chen, X. Study on the interaction of phthalate esters to human serum albumin by steady-state and time-resolved fluorescence and circular dichroism spectroscopy J. Hazard. Mater. 2011, 192, 1291-1298 10.1016/j.jhazmat.2011.06.038
51. Cao, Z.; Liu, R.; Yang, B. Potential toxicity of sarafloxacin to catalase: spectroscopic, ITC and molecular docking descriptions Spectrochim. Acta, Part A 2013, 115, 457-463 10.1016/j.saa.2013.06.093
52. Shaikh, S.; Seetharamappa, J.; Kandagal, P.; Manjunatha, D.; Ashoka, S. Spectroscopic investigations on the mechanism of interaction of bioactive dye with bovine serum albumin Dyes Pigm. 2007, 74, 665-671 10.1016/j.dyepig.2006.04.010
53. Wang, Y.; Zhang, H.; Cao, J.; Zhou, Q. Interaction of methotrexate with trypsin analyzed by spectroscopic and molecular modeling methods J. Mol. Struct. 2013, 1051, 78-85 10.1016/j.molstruc.2013.07.048
54. Ding, F.; Liu, W.; Diao, J.-X.; Sun, Y. Characterization of Alizarin Red S binding sites and structural changes on human serum albumin: a biophysical study J. Hazard. Mater. 2011, 186, 352-359 10.1016/j.jhazmat.2010.11.002
55. Bi, S.; Ding, L.; Tian, Y.; Song, D.; Zhou, X.; Liu, X.; Zhang, H. Investigation of the interaction between flavonoids and human serum albumin J. Mol. Struct. 2004, 703, 37-45 10.1016/j.molstruc.2004.05.026
56. Ibrahim, N.; Ibrahim, H.; Kim, S.; Nallet, J.-P.; Nepveu, F. Interactions between antimalarial indolone-N-oxide derivatives and human serum albumin Biomacromolecules 2010, 11, 3341-3351 10.1021/bm100814n
57. Ross, P. D.; Subramanian, S. Thermodynamics of protein association reactions: forces contributing to stability Biochemistry 1981, 20, 3096-3102 10.1021/bi00514a017
58. Mu, Y.; Lin, J.; Liu, R. Interaction of sodium benzoate with trypsin by spectroscopic techniques Spectrochim. Acta, Part A 2011, 83, 130-135 10.1016/j.saa.2011.07.092
59. Li, H.; Pu, J.; Wang, Y.; Liu, C.; Yu, J.; Li, T.; Wang, R. Comparative study of the binding of trypsin with bifendate and analogs by spectrofluorimetry Spectrochim. Acta, Part A 2013, 115, 1-11 10.1016/j.saa.2013.06.025