In vitro interceptive and reparative effects of myo-inositol against copper-induced oxidative damage and antioxidant system disturbance in primary cultured fish enterocytes

Aquatic Toxicology

Volumn 132-133, Issue , 2013, Pages 100-110

  Jiang, Wei Dan ^a   Liu, Yang ^a   Jiang, Jun ^a   Hu, Kai ^a   Li, Shu Hong ^a   Feng, Lin ^a   Zhou, Xiao Qiu ^a  

^a SICHUAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

Antioxidant; Carp; Copper; Enterocyte; Intestine; Myo Inositol

Indexed keywords

ALKALINE PHOSPHATASE; CARBONYL DERIVATIVE; CATALASE; COPPER; COPPER ZINC SUPEROXIDE DISMUTASE; GLUTATHIONE; GLUTATHIONE REDUCTASE; INOSITOL; INOSITOL TRISPHOSPHATE; LACTATE DEHYDROGENASE; MALONALDEHYDE; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ANTIOXIDANT; CONCENTRATION (COMPOSITION); COPPER; EUKARYOTE; FISH CULTURE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DAMAGE; CELL PROTECTION; CELL REGENERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; ENZYME RELEASE; ENZYME REPRESSION; FISH; IN VITRO STUDY; INTESTINE CELL; LIPID PEROXIDATION; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN METABOLISM;

ANIMALS; ANTIOXIDANTS; CARPS; COPPER; ENTEROCYTES; INOSITOL; INTESTINES; OXIDATION-REDUCTION; OXIDATIVE STRESS; WATER POLLUTANTS, CHEMICAL;

EID: 84874768458     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.02.005     Document Type: Article

References (81)

1. Agnoletto M.H., Guecheva T.N., Dondé F., Oliveira A.F.D., Franke F., Cassini C., Salvador M., Henriques J.A.P., Saffi J. Association of low repair efficiency with high hormone receptors expression and SOD activity in breast cancer patients. Clinical Biochemistry 2007, 40:1252-1258.
2. Al-Subiai S.N., Jha A.N., Moody A.J. Contamination of bivalve haemolymph samples by adductor muscle components: implications for biomarker studies. Ecotoxicology 2009, 18:334-342.
3. Aoe H., Masuda I. Water-soluble vitamin requirements of carp: II. Requirements for p-aminobenzoic and inositol. Bulletin of the Japanese Society of Scientific Fisheries 1967, 33:674-680.
4. 2+ in five tissues of freshwater fish Oreochromis niloticus. Comparative Biochemistry and Physiology, Part C 2006, 143:218-224.
5. Attia A.A., Elmazoudy R.H., El-Shenawy N.S. Antioxidant role of propolis extract against oxidative damage of testicular tissue induced by insecticide chlorpyrifos in rats. Pesticide Biochemistry and Physiology 2012, 10.1016/j.pestbp.2012.04.002.
6. Baltaci{dotless}oĝlu E., Akali{dotless}n F.A., Alver A., Deĝer O., Karabulut E. Protein carbonyl levels in serum and gingival in patients with chronic periodontitis. Archives of Oral Biology 2008, 53:716-722.
7. Benzie I.F. Evolution of antioxidant defence mechanisms. European Journal of Nutrition 2000, 39:53-61.
8. Bhor V.M., Raghuram N., Sivakami S. Oxidative damage and altered antioxidant enzyme activities in the small intestine of streptozotocin-induced diabetic rats. International Journal of Biochemistry and Cell Biology 2004, 36:29-97.
9. Bicho A.H., Ferreira G., Ferreira K.G. Chloride channels in the eel intestine. Journal of Experimental Biology 1999, 202:39-46.
10. Bielmyer G.K., Gatlin D., Isely J.J., Tomasso J., Klaine S.J. Response of hybrid striped bass to waterborne and dietary copper in freshwater and saltwater. Comparative Biochemistry and Physiology. Part C: Comparative Pharmacology 2005, 140:131-137.
11. Bohr V.A. Repair of oxidative DNA damage in nuclear and mitochondrial DNA, and some changes with aging in mammalian cells. Free Radical Biology and Medicine 2002, 33:29-36.
12. Bopp S.K., Abicht H.K., Knauer K. Copper-induced oxidative stress in rainbow trout gill cells. Aquatic Toxicology 2008, 86:197-204.
13. Borges L.P., Nogueira C.W., Panatieri R.B., Rocha J.B.T., Zeni G. Acute liver damage induced by 2-nitropropane in rats: effect of diphenyl diselenide on antioxidant defenses. Chemico-Biological Interactions 2006, 160:99-107.
14. Bradford M.M. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye-binding. Analytical Biochemistry 1976, 72:248-254.
15. Cabrini L., Bergami R., Fiorentini D., Marchetti M., Landi L., Tolomelli B. Vitamin B6 deficiency affects antioxidant defenses in rat liver and heart. Biochemistry and Molecular Biology International 1998, 46:689-697.
16. Chen J., Zhou X.-Q., Feng L., Liu Y., Jiang J. Effects of glutamine on hydrogen peroxide-induced oxidative damage in intestinal epithelial cells of Jian carp (Cyprinus carpio var. Jian). Aquaculture 2009, 288:285-289.
17. Datkhile K.D., Mukhopadhyaya R., Dongre T.K., Nath B.B. Increased level of superoxide dismutase (SOD) activity in larvae of Chironomus ramosus (Diptera: Chironomidae) subjected to ionizing radiation. Comparative Biochemistry and Physiology. Part C: Comparative Pharmacology 2009, 149:500-506.
18. Ekwall B., Silano V., Paganuzzi-Stammati A., Zucco F. Toxicity tests with mammalian cell cultures. Scope 1990, Published by John Wiley and Sons Ltd, (Chapter 7).
19. Grosell M., McDonald M.D., Wood C.M., Walsh P.J. Effects of prolonged copper exposure in the marine gulf toadfish (Opsanus beta). I. Hydromineral balance and plasma nitrogenous waste products. Aquatic Toxicology 2004, 68:249-262.
20. Halliwell B., Whiteman M. Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean?. British Journal de Pharmacologie 2004, 142:231-255.
21. Holub B.J. The cellular forms and functions of the inositol phospholipids and their metabolic derivatives. Nutrition Reviews 1987, 45:65-71.
22. Hoyle I., Shaw B.J., Handy R.D. Dietary copper exposure in the African walking catfish, Clarias gariepinus: transient osmoregulatory disturbances and oxidative stress. Aquatic Toxicology 2007, 83:62-72.
23. Hu M.L., Chen Y.K., Lin Y.F. The antioxidant and prooxidant activity of some B vitamins and vitamin-like compounds. Chemico-Biological Interactions 1995, 97:63-73.
24. Iizuka M., Sasaki K., Hirai Y., Shindo K., Konno S., Itou H., Ohshima S., Horie Y., Watanabe S. Morphogenic protein epimorphin protects intestinal epithelial cells from oxidative stress by the activation of EGF receptor and MEK/ERK, PI3 kinase/Akt signals. American Journal of Physiology - Gastrointestinal and Liver 2007, 292:39-52.
25. Jarrett S.G., Boulton M.E. Antioxidant up-regulation and increased nuclear DNA protection play key roles in adaptation to oxidative stress in epithelial cells. Free Radical Biology and Medicine 2005, 38:1382-1391.
26. Jiang, J., 2005. Effects of glutamine on the growth and metabolism of enterocytes in Jian carp (Cyprinus carpio var. Jian). Master thesis, Sichuan Agricultural University, Ya'an, China.
27. Jiang J., Zheng T., Zhou X.-Q., Liu Y., Feng L. Influence of glutamine and vitamin E on growth and antioxidant capacity of fish enterocytes. Aquaculture Nutrition 2009, 15:409-414.
28. Jiang W.-D., Feng L., Liu Y., Jiang J., Zhou X.-Q. Growth, digestive capacity and intestinal microflora of juvenile Jian carp (Cyprinus carpio var. Jian) fed graded levels of dietary inositol. Aquaculture Research 2009, 40:955-962.
29. Jiang W.-D., Feng L., Liu Y., Jiang J., Hu K., Li S.-H., Zhou X.-Q. Lipid peroxidation, protein oxidant and antioxidant status of muscle, intestine and hepatopancreas for juvenile Jian carp (Cyprinus carpio var. Jian) fed graded levels of myo-inositol. Food Chemistry 2010, 120:692-697.
30. Jiang W.-D., Wu P., Kuang S.-Y., Liu Y., Jiang J., Hu K., Li S.-H., Tang L., Feng L., Zhou X.-Q. Myo-inositol prevents copper-induced oxidative damage and changes in antioxidant capacity in various organs and the enterocytes of juvenile Jian carp (Cyprinus carpio var. Jian). Aquatic Toxicology 2011, 105:543-551.
31. Jiang W.-D., Kuang S.-Y., Liu Y., Jiang J., Hu K., Li S.-H., Tang L., Feng L., Zhou X.-Q. Effects of myo-inositol on proliferation, differentiation, oxidative status and antioxidant capacity of carp enterocytes in primary culture. Aquaculture Nutrition 2013, 19:45-53.
32. Kamunde C., Grosell M., Higgs D., Wood C.M. Copper metabolism in actively growing rainbow trout (Oncorhynchus mykiss): interactions between dietary and waterborne copper uptake. Journal of Experimental Biology 2002, 205:279-290.
33. Kapoor R., Kakkar P. Protective role of morin, a flavoniod, against high glucose induced oxidative stress mediated apoptosis in primary rat hepatocytes. PLoS ONE 2012, 7(8):e41663. 10.1371/journal.pone.0041663.
34. Ketterer B., Meyer D.J. Glutathione transferases: a possible role in the detoxication and repair of DNA and lipid hydroperoxides. Mutation Research 1989, 214:33-40.
35. Kim S.D., Kang J.C. Effect of dietary copper exposure on accumulation, growth and hematological parameters of the juvenile rockfish, Sebastes schlegeli. Marine Environment Research 2004, 58:65-82.
36. Kohen R., Nyska A. Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicologic Pathology 2002, 6:620-650.
37. Krogdahl Å., McKellep A.M.B., Baeverfjord G. Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.). Aquaculture Nutrition 2003, 9:361-371.
38. Lanza C., Raimondo S., Vergani L., Catena N., Sénès F., Tos P., Geuna S. Expression of antioxidant molecules after peripheral nerve injury and regeneration. Journal of Neuroscience Research 2012, 90:842-848.
39. Letelier M.E., Lepe A.M., Faundez M., Salazar J., Marin R., Aracena P., Speisky H. Possible mechanisms underlying copper-induced damage in biological membranes leading to cellular toxicity. Chemico-Biological Interactions 2005, 151:71-82.
40. Li M., Hu C., Zhu Q., Chen L., Kong Z., Liu Z. Copper and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in the microalga Pavlova viridis (Prymnesiophyceae). Chemosphere 2006, 62:565-572.
41. Li Q., Ai Q., Mai K., Xu W., Zheng Y. In vitro effects of arachidonic acid on immune functions of head kidney macrophages isolated from yellow croaker (Larmichths crocea). Aquaculture 2012, 330-333:47-53.
42. Lora J., Alonso F.J., Segura J.A., Lobo C., Márquez J., Matés J.M. Antisense glutaminase inhibition decreases glutathione antioxidant capacity and increases apoptosis in Ehrlich ascitic tumour cells. European Journal of Biochemistry 2004, 271:4298-4306.
43. Lushchak V.I., Lushchak L.P., Mota A.A., Hermes-Lima M. Oxidative stress and antioxidant defenses in goldfish Carassius auratus during anoxia and reoxygenation. American Journal of Physiology 2001, 280:100-107.
44. Mansell D., Veiga N., Torres J., Etchells L.L., Bryce R.A., Kremer C., Freeman S. Conformational study of the natural iron chelator myo-inositol 1,2,3-triphosphate using restrained/flexible analogues and computational analysis. Tetrahedron 2010, 66:8949-8957.
45. Mattie M.D., Freedman J.H. Copper-inducible transcription: regulation by metal- and oxidative stress-responsive pathways. American Journal of Physiology - Cell Physiology 2004, 286:C293-C301.
46. McElwee M.K., Song M.O., Freedman J.H. Copper activation of NF-kB signaling in HepG2 cells. Journal of Molecular Biology 2009, 393:1013-1021.
47. Moller P., Loft S. Interventions with antioxidants and nutrients in relation to oxidative DNA damage and repair. Mutation Research: Fundamental and Molecular Mechanisms of Mutagenesis 2004, 551:79-89.
48. Moren M., Suontama J., Hemre G.-I., Karlsen Ø., Olsen R.E., Mundheim H., Julshamn K. Element concentrations in meals from krill and amphipods - possible alternative protein sources in complete diets for farmed fish. Aquaculture 2006, 261:174-181.
49. Mulier B., Rahman I., Watchorn T., Donaldson K., MacNee W., Jeffery P.K. Hydrogen peroxide-induced epithelial injury: the protective role of intracellular nonprotein thiols (NPSH). European Respiratory Journal 1998, 11:384-391.
50. Mustafa S.A., Davies S.J., Jha A.J. Determination of hypoxia and dietary copper mediated sub-lethal toxicity in carp, Cyprinus carpio, at different levels of biological organization. Chemosphere 2012, 87:413-422.
51. Nagashima R., Sugiyama C., Yoneyama M., Kuramoto N., Kawada K., Ogita K. Acoustic overstimulation facilitates the expression of glutamate-cysteine ligase catalytic subunit probably through enhanced DNA binding of activator protein-1 and/or NF-kB in the murine cochlea. Neurochemistry International 2007, 51:209-215.
52. Olsen R.E., Sundell K., Mayhew T.M., Myklebust R., Ringø E. Acute stress alters intestinal function of rainbow trout, Oncorhynchus mykiss (Walbaum). Aquaculture 2005, 250:480-495.
53. Pacifici R.E., Davies K.J.A. Protein, lipid and DNA repair systems in oxidative stress: the free-radical theory of aging revisited. Gerontology 1991, 37:166-180.
54. Papaleo E., Unfer V., Baillargeon J.P., Chiu T.T. Contribution of myo-inositol to reproduction. European Journal of Obstetrics, Gynecology, and Reproductive Biology 2009, 147:120-123.
55. Ramos A.A., Pereira-Wilson C., Collins A.R. Protective effects of ursolic acid and luteolin against oxidative DNA damage include enhancement of DNA repair in Caco-2 cells. Mutation Research: Fundamental and Molecular Mechanisms of Mutagenesis 2010, 692:6-11.
56. Rushworth S.A., Ogborne R.M., Charalambos C.A., O'Connell M.A. Role of protein kinase C δ in curcumin-induced antioxidant response element-mediated gene expression in human monocytes. Biochemical and Biophysical Research Communications 2006, 341:1007-1016.
57. Sanchez W., Palluel O., Meunier L., Coquery M., Porcher J.M., Ait-Aissa S. Copper-induced oxidative stress in three-spined stickleback: relationship with hepatic metal levels. Environmental Toxicology and Pharmacology 2005, 19:177-183.
58. Sandrini J.Z., Bianchini A., Trindade G.S., Nery L.E.M., Marins L.F.F. Reactive oxygen species generation and expression of DNA repair-related genes after copper exposure in zebrafish (Danio rerio) ZFL cells. Aquatic Toxicology 2009, 95:285-291.
59. Santoro M., Caffaratti E., Salas-Peregrin J.M., Korecz L., Rockenbauer A., Luis F.S. Signorella kinetics and mechanism of the chromic oxidation of myo-inositol. Polyhedron 2007, 26:169-177.
60. Scherz-Shouval R., Elazar Z. ROS, mitochondria and the regulation of autophagy. Trends in Cell Biology 2007, 17:422-427.
61. Shiau S.Y., Su S.L. Dietary inositol requirement for juvenile grass shrimp, Penaeus monodon. Aquaculture 2004, 241:1-8.
62. Shiau S.Y., Su S.L. Juvenile tilapia (Oreochromis niloticus×Oreochromis aureus) requires dietary myo-inositol for maximal growth. Aquaculture 2005, 243:273-277.
63. Sies H. Oxidative stress: introductory remarks. Oxidative Stress 1985, 1-8. Academic Press, London. H. Sies (Ed.).
64. Sies H. Strategies of antioxidant defense. European Journal of Biochemistry 1993, 215:213-219.
65. Singh A.K., Mehtab S., Jain A.K. Selective electrochemical sensor for copper (II) ion based on chelating ionophores. Analytica Chimica Acta 2006, 575:25-31.
66. Spiers I.D., Barker C.J., Chung S.-K., Chang Y.-T., Freeman S., Gardiner J.M., Hirst P.H., Lambert P.A., Michell R.H., Poyner D.R., Schwalbe C.H., Smith A.W., Solomons K.R.H. Synthesis and iron binding studies of myo-inositol 1,2,3-trisphosphate and (±)-myo-inositol 1,2-bisphosphate, and iron binding studies of all myo-inositol tetrakisphosphates. Carbohydrate Research 1996, 282:81-99.
67. Srivastava S., Mishra S., Tripathi R.D., Dwivedi S., Gupta D.K. Copper-induced oxidative stress and responses of antioxidants and phytochelatins in Hydrilla verticillata (L.f.) Royle. Aquatic Toxicology 2006, 80:405-415.
68. 2-induced oxidative stress in human keratinocytes and mouse fibroblasts. Burns 2006, 32:973-979.
69. Upadhyay R., Panda S.K. Zinc reduces copper toxicity induced oxidative stress by promoting antioxidant defense in freshly grown aquatic duckweed Spirodela polyrhiza L. Journal of Hazardous Materials 2010, 175:1081-1084.
70. Uriu-Adams J.Y., Keen C.L. Copper, oxidative stress, and human health. Molecular Aspects of Medicine 2005, 26:268-298.
71. Valenca S.S., Beerra F.S., Romana-Souza B., Paiva R.O., Costa A.M.A., Porto L.C. Supplementation with vitamins C and E improves mouse lung repair. Journal of Nutritional Biochemistry 2008, 19:604-611.
72. Van-Kuijk F.J.G.M., Sevanian A., Handelman G.J., Dratz E.A. A new role for phospholipase A2: protection of membranes from lipid peroxidation damage. Trends in Biochemical Sciences 1987, 12:31-34.
73. Vardi N., Parlakpinar H., Ozturk F., Ates B., Gul M., Cetin A., Erdogan A., Otlu A. Potent protective effect of apricot and b-carotene on methotrexate-induced intestinal oxidative damage in rats. Food and Chemical Toxicology 2008, 46:3015-3022.
74. Vieira L.R., Gravato C., Soares A.M.V.M., Morgado F., Guilhermino L. Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: linking biomarkers to behaviour. Chemosphere 2009, 76:1416-1427.
75. Villanueva J., Vanacore R., Goicoechea O., Amthauer R. Intestinal alkaline phosphatase of the fish Cyprinus carpio: regional distribution and membrane association. Journal of Experimental Zoology 1997, 279:347-355.
76. Wang X., Hai C.X., Liang X., Yu S.X., Zhang W., Li Y.L. The protective effects of Acanthopanax senticosus Harms aqueous extracts against oxidative stress: role of Nrf2 and antioxidant enzymes. Journal of Ethnopharmacology 2010, 127:424-432.
77. Wang W.-X., Onsanit S., Dang F. Dietary bioavailability of cadmium, inorganic mercury, and zinc to a marine fish: effects of food composition and type. Aquaculture 2012, 356-357:98-104.
78. Weldy C.S., Luttrell I.P., White C.C., Morgan-Stevenson V., Bammler T.K., Beyer R.P., Afsharinejad Z., Kim F., Chitaley K., Kavanagh T.J. Glutathione (GSH) and the GSH synthesis gene Gclm modulate vascular reactivity in mice. Free Radical Biology and Medicine 2012, 53:1264-1278.
79. Winston G.W., Di-Giulio R.T. Prooxidant and antioxidant mechanisms in aquatic organisms. Aquatic Toxicology 1991, 19:137-161.
80. Xie L., Buchwalter D.B. Cadmiun exposure route affects antioxidant responses in the mayfly Centroptilum triangulifer. Aquatic Toxicology 2011, 105:199-205.
81. Zhang X.-D., Zhu Y.-F., Cai L.-S., Wu T.-X. Effects of fasting on the meat quality and antioxidant defenses of market-size farmed large yellow croaker (Pseudosciaena crocea). Aquaculture 2008, 280:136-139.