Oxidative stress response in canine in vitro liver, kidney and intestinal models with seven potential dietary ingredients

Toxicology Letters

Volumn 241, Issue , 2016, Pages 49-59

  Choi, Kyoungju ^a   Ortega, Maria T ^a   Jeffery, Brett ^b   Riviere, Jim E ^a   Monteiro Riviere, Nancy A ^a  

^a KANSAS STATE UNIVERSITY   (United States)

^b Mars Global Food Safety Center   (China)

Author keywords

Dietary ingredients; In vitro canine culture systems; Multiple organ derived cells; Organ specific oxidative stress

Indexed keywords

CATECHIN; CHLOROPHYLL; CINEOLE; DENATONIUM BENZOATE; EPIGALLOCATECHIN GALLATE; FOOD ADDITIVE; HUMULON; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SODIUM COPPER CHLOROPHYLLIN; SUPEROXIDE; TETRAHYDROISOHUMULONE; UNCLASSIFIED DRUG; XYLITOL; ANTIOXIDANT; OXIDIZING AGENT;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; CELL CULTURE; CELL FUNCTION; CONTROLLED STUDY; DOG; FOOD COMPOSITION; FOOD POISONING; IN VITRO STUDY; INTESTINE CELL; KIDNEY PROXIMAL TUBULE; LIVER CELL; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; TEA; ANIMAL; BONE MARROW CELL; CHEMISTRY; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; FOOD; FOOD ANALYSIS; INTESTINE; KIDNEY; LIVER; MESENCHYMAL STROMA CELL; METABOLISM;

ANIMALS; ANTIOXIDANTS; BONE MARROW CELLS; CELLS, CULTURED; DOGS; DOSE-RESPONSE RELATIONSHIP, DRUG; FOOD; FOOD ANALYSIS; HEPATOCYTES; INTESTINES; KIDNEY; KIDNEY TUBULES, PROXIMAL; LIVER; MESENCHYMAL STROMAL CELLS; OXIDANTS; OXIDATIVE STRESS;

EID: 84947725653     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2015.11.012     Document Type: Article

References (77)

1. Abdel-Rahman A., Anyangwe N., Carlacci L., Casper S., Danam R.P., Enongene E., Erives G., Fabricant D., Gudi R., Jilmas C.J., Hines C.J., Hines F., Howard P., Levy D., Lin Y., Moore R.J., Pfeiler E., Thurmond T.S., Turujman S., Walker N.J. The safety and regulation of natural products used as foods and food ingredients. Toxicol. Sci. 2011, 123(2):333-348.
2. Acevedo-Morantes C.Y., Meléndez E., Singh S.P., Ramírez-Vick J.E. Cytotoxicity and reactive oxygen species generated by ferrocenium and ferrocene on MCF7 and MCF10a cell lines. J. Cancer Sci. Ther. 2012, 4(9):271-275.
3. Barth R. The Chemistry of the Beer: The Science in the Suds 2013, Wiley-Blackwell, Ames, IA. 1st ed.
4. Bjornsson E., Olsson R. Serious adverse liver reactions associated with herbal weight-loss supplements. J. Hepatol. 2007, 47(2):295-297.
5. Boloor K.K., Kamat J.P., Devasagayam T.P. Chlorophyllin as a protector of mitochondrial membranes against gamma-radiation and photosensitization?. Toxicology 2000, 155(1-3):63-71.
6. Bolisetty S., Jaimes E.A. Mitochondria and reactive oxygen species Physiology and Pathophysiology. Int. J. Mol. Sci. 2013, 14:6306-6344.
7. Cattoor K., Remon J., Boussery K., Bocxlaer J.V., Bracke M., Keukeleire D.D., Deforce D., Heyerick A. Bioavailability of hop-derived iso-α-acids and reduced derivatives. Food Funct. 2011, 2(7):412-422.
8. Chappel C.I., Smith S.Y., Chagnon M. Subchronic toxicity study of tetrahydroisohumulone and hexahydroisohumulone in the beagle dog. Food Chem. Toxicol. 1998, 36:915-922.
9. Chernomorsky S., Rancourt R., Virdi K., Segelman A., Poretz R.D. Antimutagenicity, cytotoxicity and composition of chlorophyllin copper complex. Cancer Lett. 1997, 120(2):141-147.
10. Cho N., Yang H., Lee M., Huh J., Kim H.W., Kim H.P., Sung S.H. Neuroprotective benzyl benzoate glycosides from Disporum viridescens roots in HT22 hippocampal neuronal cells. J. Nat. Prod. 2013, 76(12):2291-2297. 10.1021/np400676b.
11. Cho, S., 2013. GRAS notification of Shangdong Longlive Biotechnology, LTD.'s xylooligo-saccharides. Available:. http://file:///E:/KJ%20Choi/2015_2014/KSU/Mas%20project/GRAS/GRAS%20for%20xylitol%20uses.pdf.
12. Choi K., Pfund W.P., Andersen M.E., Thomas R.S., Clewell H.J., LeCluyse E.L. Development of 3D dynamic flow model of human liver and its application to prediction of metabolic clearance of 7-ethoxycoumarin. Tissue Eng. Part C: Methods 2014, 20(8):641-651.
13. Clerch L.B., Wright A.E., Coalson J.J. Lung manganese superoxide dismutase protein expression increases in the baboon model of bronchopulmonary dysplasia and is regulated at a posttranscriptional level. Pediatr. Res. 1996, 39:253-258.
14. Crespy V., Williamson G. Review of the health effects of green tea catechins in in vivo animal models. J. Nutr. 2004, 134(Suppl. 12):3431S-3440S.
15. De Vincenzi M., Silano M., De Vincenzi A., Maialetti F., Scazzocchio B. Constituents of aromatic plants: eucalyptol. Fitoterapia 2002, 73:269-275.
16. 1 Could be prevented by sodium copper chlorophyllin-implication to their genotoxic mechanism. Food Chem. 2015, 170:455-462.
17. Dörsam B., Wu C.F., Efferth T., Kaina B., Fahrer J. The eucalyptus oil ingredient 1,8-cineol induces oxidative DNA damage. Arch. Toxicol. 2014, 89(5):797-805.
18. 2-induced clastogenicity, genotoxicity and mutagenicity by chlorophyllin administration in mice brain, liver, and bone marrow cells. Toxicol. Sci. 2014, 142:21-32.
19. European Commission (EC), 2002. Opinion of scientific committee on food on eucalyptol. Available:. http://file:///E:/KJ%20Choi/2015_2014/KSU/Mas%20project/GRAS/GRAS%20for%20eucalyptol%20uses.pdf.
20. Food and Drug Administration (FDA), 2015. Pet food. Available:. http://www.fda.gov/animalveterinary/products/animalfoodfeeds/petfood/ucm2006475.
21. Food and Drug Administration (FDA), 2001. Agency response letter GRAS notice No. GRN 000063. Available:. http://www.fda.gov/Food/IngredientsPackagingLabeling/GRAS/NoticeInventory/ucm153973.htm.
22. Food and Drug Administration (FDA), 2002. Listing of color additives exempt from certification; sodium copper chlorophyllin. Available:. http://www.fda.gov/ohrms/dockets/98fr/00c-0929-nfr0001-vol1.pdf.
23. Garza K.M., Soto K.F., Murr L.E. Cytotoxicity and reactive oxygen species generation from aggregated carbon and carbonaceous nanoparticulate materials. Int. J. Nanomed. 2008, 3(1):83-94.
24. Goodin M.G., Bray B.J., Rosengren R.J. Sex- and strain-dependent effect of epigallocatechin gallate (EGCG) and epicatechin gallate (ECG) in the mouse. Food Chem. Toxicol. 2006, 44(9):1496-1504.
25. Graham H.N. Green tea composition, consumption, and polyphenol chemistry. Prev. Med. 1992, 21(3):334-350.
26. Haigis M.C., Yankner B.A. The aging stress response. Mol. Cell 2010, 40(2):333-344.
27. Hansen S.R., Janssen C., Beasley V.R. Denatonium benzoate as a deterrent to ingestion of toxic substances: toxicity and efficacy. Vet. Hum. Toxicol. 1993, 35(3):234-236.
28. Haniu H., Saito N., Matsuda Y., Usui Y., Aoki K., Shimizu M., Ogihara N., Hara K., Takanashi S., Okamoto M., Nakamura K., Ishigaki N., Tsukahara T., Kato H. Manufacturing strategy for multiwalled carbon nanotubes as a biocompatible and innovative material. J. Nanotechnol. 2012, 2012(2012):6. Article ID 937819. http://dx.doi.org/10.1155/2012/937819.
29. Hwang J., Ha J., Park I., Lee S., Baik H., Kim Y., Park O. Apoptotic effect of EGCG in HT-29 colon cancer cells via AMPK signaling pathway. Cancer Lett 2007, 247(1):115-121.
30. The Health Canada Pest Management Regulatory Agency, 2012. Re-evaluation Decision RVD2012-06, Denatonium Benzoate. Available at:. http://www.hc-sc.gc.ca/cps-spc/pubs/pest/_decisions/rvd2012-06/index-eng.php.
31. Inacio J.D.F., Canto-Cavalheiro M.M., Almeida-Amaral E.E. In vitro and in vivo effects of EGCG on leishmania amazonesis. J. Nat. Prod. 2013, 76:1993-1996.
32. Javaid A., Bonkovsky H.L. Hepatotoxicity due to extracts of Chinese green tea (Camellia sinensis): a growing concern. J. Hepatol. 2006, 45:334-335.
33. Kalaiselvi P., Rajashree K., Bharathi Priya L., Padma V.V. Cytoprotective effect of epigallocatechin-3-gallate against deoxynivalenol-induced toxicity through anti-oxidative and anti-inflammatory mechanisms in HT-29 cells. Food Chem. Toxicol. 2013, 56:110-118.
34. Kapetanovic I.M., Crowell J.A., Krishnaraj R., Zakharov A., Lindeblad M., Lyubimov A. Exposure and toxicity of green tea polyphenols in fasted and non-fasted dogs. Toxicology 2009, 260(1-3):28-36.
35. Khan N., Afaq F., Saleem M., Ahmad N., Mukhtar H. Targeting multiple signaling pathways by green tea polyphenol (-)-epigallocatechin-3-gallate. Cancer Res. 2006, 66(5):2500-2505.
36. Kovar K.A., Gropper B., Friess D., Ammon H.P.T. Blood levels of 1,8-cineole and locomotor activity of mice after inhalation and oral administration of rosemary oil. Planta Med. 1987, 53(4):315-318.
37. Koci J., Jeffery B., Riviere J.E., Monteiro-Riviere N.A. In vitro safety assessment of food ingredients in canine primary renal proximal tubule cells. Toxicol. In Vitro 2015, 29(2):289-298.
38. Lambert J.D., Kennett M.J., Sang S., Reuhl K.R., Ju J., Yang C.S. Hepatotoxicity of high oral dose (-)-epigallocatechin-3-gallate in mice. Food Chem. Toxicol. 2010, 48:409-416.
39. Lee M.J., Maliakal P., Chen L., Meng X., Bondoc F.Y., Prabhu S., Lambert G., Mohr S., Yang C.S. Pharmacokinetics of tea catechins after ingestion of green tea and (-)-epigallocatechin-3-gallate by humans: formation of different metabolites and individual variability. Cancer Epidemiol. Biomarkers Prev. 2002, 11(10 Pt. 1):1025-1032.
40. Lee R.J., Kofonow J.M., Rosen P.L., Siebert A.P., Chen B., Doghramji L., Xiong G., Adappa N.D., Palmer J.N., Kennedy D.W., Kreindler J.L., Margolskee R.F., Cohen N.A. Bitter and sweet taste receptors regulate human upper respiratory innate immunity. J. Clin. Invest. 2014, 124(3):1393-1405.
41. Machado M., Dinis A.M., Santos-Rosa M., Alves V., Salgueiro L., Cavaleiro C., Sousa M.C. Activity of Thymus capitellatus volatile extract, 1,8-cineole and borneol against Leishmania species. Vet. Parasitol. 2014, 200(1-2):39-49.
42. Mahinka, S.P., 2007. Generally recongnized as safe status of green tea catechin. Available:. http://file:///E:/KJ%20Choi/2015_2014/KSU/Mas%20project/GRAS/GRAS%20for%20green%20tea%20uses.pdf.
43. Miyata M., Kurogi M., Oda M., Saitoh O. Effect of five taste ligands on the release of CCK from an enteroendocrine cell line, STC-1. Biomed. Res. 2014, 35(2):171-176.
44. Monteiro-Riviere N.A., Ortega M.T., Choi K., Koci J., Lin Z., Jeffrey B., Riviere J.E. Comparative in vitro cytotoxicity of 20 potential food ingredients in canine liver, kidney and bone marrow stem cell derived mesenchymal and enterocyte-like cells. Appl. In Vitro Toxicol. 2015, Advance Access published. 10.1089/aivt.2015.0020.
45. Namikoshi T., Tomita N., Fujimoto S., Haruna Y., Ohzeki M., Komai N., Sasaki T., Yoshida A., Kashihara N. Isohumulones derived from hops ameliorate renal injury via an anti-oxidative effect in Dahl salt-sensitive rats. Hypertens. Res. 2007, 30(2):175-184.
46. Nasri H., Ahmadi A., Baradaran A., Nasri P., Hajian S., Pour-Arian A., Kohi G., Rafieian-Kopaei M. A biochemical study on ameliorative effect of green tea (Camellia sinensis) extract against contrast media induced acute kidney injury. J. Renal Inj. Prev. 2014, 3(1):47-49.
47. Ortega M.T., Jeffery B., Riviere J.E., Monteiro-Riviere N.A. Toxicological effects of pet food ingredients on canine bone marrow-derived mesenchymal stem cells and enterocyte-like cells. J. Appl. Toxicol. 2015, 14(May). Advance Access published. 10.1002/jat.3158.
48. Osowski A., Pietrzak M., Wieczorek Z., Wieczorek J. Natural compounds in the human diet and their ability to bind mutagens prevents DNA-mutagen intercalation. J. Toxicol. Environ. Health Part A 2010, 73(17-18):1141-1149.
49. Ozkan A., Erdoğan A. Membrane and DNA damaging/protective effects of eugenol, eucalyptol, terpinen-4-ol, and camphor at various concentrations on parental and drug-resistant H1299 cells. Turk. J. Biol. 2013, 37:405-413.
50. Patel S., Wiggins J. Eucalyptus oil poisoning. Arch. Dis. Child. 1980, 55(5):405-406.
51. Paravicini T.M., Touyz R.M. Redox signaling in hypertension. Cardiovas. Res. 2006, 71:247-258.
52. Park K.K., Park J.H., Jung Y.J., Chung W.Y. Inhibitory effects of chlorophyllin, hemin and tetrakis (4-benzoic acid) porphyrin on oxidative DNA damage and mouse skin inflammation induced by 12-O-tetradecanoylphorbol-13-acetate as a possible anti-tumor promoting mechanism. Mutat. Res. 2003, 542(1-2):89-97.
53. Poppenga R.H. Herbal medicine: potential for intoxication and interactions with conventional drugs. Clin. Tech. Small Anim. Pract. 2002, 17(1):6-18.
54. Pujalté I., Passagne I., Brouillaud B., Tréguer M., Durand E., Ohayon-Courtès C., Azou Cytotoxicity and oxidative stress induced by different metallic nanoparticles on human kidney cells. Part. Fibre Toxicol. 2011, 8:10. 10.1186/1743-8977-8-10.
55. Ray P.D., Huang B.W., Tsuij Y. Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell. Signal. 2012, 24(5):981-990.
56. Riley P., Moore D., Ahmed F., Sharif M.O., Worthington H.V. Xylitol-containing products for preventing dental caries in children and adults. Cochrane Database Syst. Rev. 2015, 26(3). CD010743. 10.1002/14651858.cd010743.pub2.
57. Schiffrin E.L., Lipman M.L., Mann J.F.E. Cardiovascular involvement in general medical conditions: chronic kidney disease effects on the cardiovascular system. Circulation 2007, 116:85-97.
58. Schnitzler P., Schön K., Reichling J. Antiviral activity of Australian tea tree oil and eucalyptus oil against herpes simplex virus in cell culture. Die Pharmazie 2001, 56(4):343-347.
59. Shuhendler A.J., Pu K., Cui L., Uetrecht J.P., Rao J. Real-time imaging of oxidative and nitrosative stress in the liver of live animals for drug-toxicity testing. Nat. Biotechnol. 2014, 32(4):373-380.
60. Shukla V., Mishra S.K., Pant H.C. Oxidative stress in neurodegeration. Adv. Pharmacol. Sci. 2011, 2011:572634. 10.1155/2011/572634.
61. Siddiqui M.A., Ahmad J., Farshori N.N., Saquib Q., Jahan S., Kashyap M.P., Ahamed M., Musarrat J., Al-Khedhairy A.A. Rotenone-induced oxidative stress and apoptosis in human liver HepG2 cells. Mol. Cell. Biochem. 2013, 384(1-2):59-69.
62. Srivastava S., Chan C. Hydrogen peroxide and hydroxyl radicals mediate palmitate-induced cytotoxicity to hepatoma cells: relation to mitochondrial permeability transition. Free Radic. Res. 2007, 41(1):38-49.
63. Stoicov C., Saffari R., Houghton J. Green tea inhibits Helicobacter growth in vivo and in vitro. Int. J. Antimicrob. Agents 2009, 33(5):473-478.
64. Takahashi K., Ibidera K., Akiba Y. Effect of dietary xylitol on growth and inflammatory responses in immune stimulated chickens. Br. Poult. Sci. 1999, 40(4):552-554.
65. Takaishi M., Fujita F., Uchida K., Yamamoto S., Sawada S.M., Hatai U.C., Shimizu M., Tominaga M. 1,8-Cineole, a TRPM8 agonist, is a novel natural antagonist of human TRPA1. Mol. Pain 2012, 8(86):1-12.
66. Thomson M., Al-Qattan K., Mansour M.H., Ali M. Green tea attenuates oxidative stress and downregulates the expression of angiotensin II AT1 receptor in renal and hepatic tissues of streptozotocin-induced diabetic rats. Evid. Based Complement. Altern. Med. 2012, 2012:409047. 10.1155/2012/409047.
67. Trachootham D., Alexandre J., Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach?. Nat. Rev. Drug Discov. 2009, 8(7):579-591.
68. Tumolo T., Lanfer-Marquez U.M. Copper chlorophyllin: a food colorant with bioactive properties?. Food Res. Int. 2012, 46(2):451-459.
69. Uehara T., Miyoshi T., Tsuchiya N., Masuno K., Okada M., Inoue S., Torii M., Yamate J., Maruyama T. Comparative analysis of gene expression between renal cortex and papilla in nedaplatin-induced nephrotoxicity in rats. Hum. Exp. Toxicol. 2007, 26(10):767-780.
70. US Consumer Product Safety Commission, 1992. Final report study of aversive agents. Available:. http://https://www.cpsc.gov//PageFiles/96066/aversive.pdf.
71. Xia Z., He Y., Yu J. Experimental acute toxicity of xylitol in dogs. J. Vet. Pharmacol. Ther. 2009, 32(5):465-469.
72. Yamaguchi N., Satoh-Yamaguchi K., Ono M. In vitro evaluation of antibacterial, anticollagenase, and antioxidant activities of hop components (Humulus lupulus) addressing acne vulgaris_Phytomedicine. Phytomedicine 2009, 16(4):369-376.
73. Yamamoto K., Wang J., Yamamoto S., Tobe H. Suppression of cyclooxygenase-2 gene transcription by humulone of beer hop extract studied with reference to glucocorticoid. FEBS Lett. 2000, 465:103-106.
74. Yazdani M., Paulsen R.E., Gjøen T., Hylland K. Reactive oxygen species and cytotoxicity in rainbow trout hepatocytes: effects of medium and incubation time. Bull. Environ. Contam. Toxicol. 2014, 94(2):193-198.
75. Yokozawa T., Noh J.S., Park C.H. Green tea polyphenols for the protection against renal damage caused by oxidative stress. Evid. Based Complement. Altern. Med. 2012, 1-12. 10.1155/2012/845917.
76. Zanoli P., Rivasi M., Zavatti M., Brusiani F., Baraldi M. New insight in the neuropharmacological activity of Humulus lupulus L. J. Ethnopharmacol. 2005, 102:102-106.
77. Zhang L.W., Koci J., Jeffery B., Riviere J.E., Monteiro-Riviere N.A. Safety assessment of potential food ingredients in canine primary hepatocytes. Food Chem. Toxicol. 2015, 78:105-115.