Oxidative stress and metabolic responses to copper in freshwater- and seawater-acclimated killifish, Fundulus heteroclitus

Aquatic Toxicology

Volumn 161, Issue , 2015, Pages 242-252

  Ransberry, Victoria E ^a   Morash, Andrea J ^c   Blewett, Tamzin A ^a   Wood, Chris M ^a,b   McClelland, Grant B ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c CSIRO   (Australia)

Author keywords

Catalase; Copper; Freshwater; Killifish; Metabolism; Oxygen consumption rate; Protein carbonyls; Salinity

Indexed keywords

CARBONYL DERIVATIVE; CATALASE; COPPER; HEMOGLOBIN; LACTIC ACID; SUPEROXIDE DISMUTASE; FRESH WATER; SEA WATER; WATER POLLUTANT;

BIOACCUMULATION; COPPER; ECOTOXICOLOGY; METABOLISM; OXIDATION; PROTEIN; SALINITY; TELEOST; TOXICITY;

ACCLIMATIZATION; ADULT; AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CARBOHYDRATE METABOLISM; CARCASS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; COPPER METABOLISM; DOWN REGULATION; FRESHWATER SPECIES; FUNDULUS HETEROCLITUS; GILL; HEMATOCRIT; HEMOGLOBIN BLOOD LEVEL; INTESTINE; LACTATE BLOOD LEVEL; LIVER; METABOLIC REGULATION; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; SALINITY; SEA; TOXICITY TESTING; UPREGULATION; ANIMAL; DRUG EFFECTS; ENZYME ACTIVATION; ENZYMOLOGY; FUNDULIDAE; METABOLISM; PHYSIOLOGY; TOXICITY; WATER POLLUTANT;

CYPRINODONTOIDEI; FUNDULUS HETEROCLITUS;

ANIMALS; COPPER; ENZYME ACTIVATION; FRESH WATER; FUNDULIDAE; GILLS; INTESTINES; LIVER; OXIDATIVE STRESS; SALINITY; SEAWATER; SUPEROXIDE DISMUTASE; WATER POLLUTANTS, CHEMICAL;

EID: 84923584565     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2015.02.013     Document Type: Article

References (78)

1. Almroth B.C., Albertsson E., Sturve J., Förlin L. Oxidative stress, evident in antioxidant defences and damage products: in rainbow trout caged outside a sewage treatment plant. Ecotoxicol. Environ. Saf. 2008, 70:370-378.
2. Antognelli C., Romani R., Baldracchini F., De Santis A., Andreani G., Talesa V. Different activity of glyoxalase system enzymes in specimens of Sparus auratus exposed to sublethal copper concentrations. Chem. Biol. Interact. 2003, 142:297-305.
3. Bagnyukova T.V., Chahrak O.I., Lushchak V.I. Coordinated response of goldfish antioxidant defenses to environmental stress. Aquat. Toxicol. 2006, 78:325-331.
4. Beaumont M.W., Butler P.J., Taylor E.W. Exposure of brown trout to a sublethal concentration of copper in soft acidic water: effects upon gas exchange and ammonia accumulation. J. Exp. Biol. 2003, 206:153-162.
5. Blanchard J., Grosell M. Copper toxicity across salinities from freshwater to seawater in the euryhaline fish Fundulus heteroclitus: is copper an ionoregulatory toxicant in high salinities?. Aquat. Toxicol. 2006, 80:131-139.
6. Blewett T., MacLatchy D.L., Wood C.M. The effects of temperature and salinity on 17-α-ethynylestradiol uptake and its relationship to oxygen consumption in the model euryhaline teleost (Fundulus heteroclitus). Aquat. Toxicol. 2013, 127:61-71.
7. Bopp S.K., Abicht H.K., Knauer K. Copper-induced oxidative stress in rainbow trout gill cells. Aquat. Toxicol. 2008, 86:197-204.
8. Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 7:248-254.
9. Bury N.R., Walker P.A., Glover C.N. Nutritive metal uptake in teleost fish. J. Exp. Biol. 2003, 206:11-23.
10. Campbell P.G.C. Interactions between trace metals and aquatic organisms: a critique ofthe free-ion activity model in metal speciation and bioavailability. Aquatic Systems 1995, 45-102. IUPAC, John Wiley and Sons, New York. A. Tessier, D.R. Turner (Eds.).
11. Capkova M., Houstek J., Hansikova H., Hainer V., Kunesova M., Zeman J. Activities of cytochrome c oxidase and citrate synthase in lymphocytes of obese and normal-weight subjects. Int. J. Obes. 2002, 26:1110-1117.
12. Carvalho C.S., Fernandes M.N. Effect of temperature on copper toxicity and hematological responses in the neotropical fish Prochilodus scrofa at low and high pH. Aquaculture 2006, 251:109-117.
13. Carvalho C.S., Fernandes M.N. Effect of copper on liver key enzymes of anaerobic glucose metabolism from freshwater tropical fish Prochilodus lineatus. Comp. Biochem. Physiol. A 2008, 151:437-442.
14. Cerqueira C.C.C., Fernandes M.N. Gill tissue recovery after copper exposure and blood parameter responses in the tropical fish, Prochilodus scrofa. Ecotoxicol. Environ. Saf. 2002, 52:83-89.
15. Cheney M.A., Criddle R.S. Heavy metal effects on the metabolic activity of Elliptio complanata: a calorimetric method. J. Environ. Qual. 1996, 25:235-240.
16. Connell D., Lam P., Richardson B., Wu R. Introduction to Ecotoxicology 1999, Blackwell Science, Australia.
17. Costa F.O., Neuparth T., Costa M.H., Theodorakis C.W., Shugart L.R. Detection of DNA strand breakage in a marine amphipod by agarose gel electrophoresis: exposure to X-rays and copper. Biomarkers 2002, 7:451-463.
18. Couture P., Kumar P.R. Impairment of metabolic capacities in copper and cadmium contaminated wild yellow perch (Perca flavescens). Aquat. Toxicol. 2003, 64:107-130.
19. Craig P.M., Wood C.M., McClelland G.B. Oxidative stress response and gene expression with acute copper exposure in zebrafish (Danio rerio). Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293(5):1882-1892.
20. Craig P.M., Hogstrand C., Wood C.M., McClelland G.B. Gene expression endpoints following chronic waterborne copper exposure in a genomic model organism, the zebrafish, Danio rerio. Physiol. Genom. 2009, 40(1):23-33.
21. Cyriac P.J., Antony A., Nambisan P.N.K. Hemoglobin and hematocrit values in the fish Oreochromis mossambicus (Peters) after short term exposure to copper and mercury. Bull. Environ. Contam. Toxicol. 1989, 43:315-320.
22. De Boeck G., Smet H., Blust R. The effect of sublethal levels of copper on oxygen consumption and ammonia excretion in the common carp, Cyprinus carpio. Aquat. Toxicol. 1995, 32:27-141.
23. Depledge M.H. Disruption of circulatory and respiratory activity in the shore crab, Carcinus maenas (L.) exposed to heavy metal pollution. Comp. Biochem. Physiol. C 1984, 78(2):445-459.
24. Dethloff G.M., Schlenk D., Hamm J.T., Bailey H.C. Alterations in physiological parameters of rainbow trout (Oncorhynchus mykiss) with exposure to copper and copper/zinc mixtures. Ecotoxicol. Environ. Saf. 1999, 42:253-264.
25. Dorval J., Hontela A. Role of glutathione redox cycle and catalase in defense against oxidative stress induced by endosulfan in adrenocortical cells of rainbow trout (Oncorhynchus mykiss). Toxicol. Appl. Pharmacol. 2003, 192:191-200.
26. Eyckmans M., Celis N., Horemans N., Blust R., De Boeck G. Exposure to waterborne copper reveals differences in oxidative stress response in three freshwater fish species. Aquat. Toxicol. 2011, 103:112-120.
27. Genz J., Taylor J.R., Grosell M. Effects of salinity on intestinal bicarbonate secretion and compensatory regulation of acid-base balance in Opsanus beta. J. Exp. Biol. 2008, 211:2327-2335.
28. Grosell M., Wood C.M. Copper uptake across rainbow trout gills: mechanisms of apical entry. J. Exp. Biol. 2002, 205:1179-1188.
29. Grosell M., Hansen H.J.M., Rosenkilde P., Hansen H.J. Cu uptake, metabolism and elimination in fed and starved European eels (Anguilla anguilla) during adaptation to water-borne Cu exposure. Comp. Biochem. Physiol. C 1998, 120:295-305.
30. Grosell M., Nielsen C., Bianchini A. Sodium turnover rate determines sensitivity to acute copper and silver exposure in freshwater animals. Comp. Biochem. Physiol. C 2002, 133:287-303.
31. +-ATPase activity in osmoregulatory tissues. Aquat. Toxicol. 2004, 68:249-262.
32. Grosell M., Blanchard J., Brix K.V., Gerdes R. Physiology is pivotal for interactions between salinity and acute toxicity to fish and invertebrates. Aquat. Toxicol. 2007, 82:162-172.
33. Grosell M. Copper 2012, vol. 31A:53-133. Elsevier, San Diego.
34. Gul S., Belge-Kurutas E., Yildiz E., Sahan A., Doran F. Pollution correlated modifications of liver antioxidant systems and histopathology of fish (Cyprinidae) living in Seyhan Dam Lake. Turkey Environ. Int. 2004, 30:605-609.
35. Halliwell B., Gutteridge J.M.C. Free Radicals in Biology and Medicine 2001, Oxford University Press, New York. third ed.
36. Hansen J.I., Mustafa T., Depledge M. Mechanisms of copper toxicity in the shore crab, Carcinus maenas II. Effects of key metabolic enzymes, metabolites and energy charge potential. Mar. Biol. 1992, 114:259-264.
37. Hughes G.M., Shelton G. The mechanism of gill ventilation in three freshwater teleosts. J. Exp. Biol. 1958, 35:807-823.
38. Hughes G.M. The dimensions of fish gills in relation to their function. J. Exp. Biol. 1966, 45:177-195.
39. Isani G., Cattani O., Carpene E., Cortesi P. Kinetic properties of liver and muscle pyruvate kinase of a marine teleost: sea bass (Dicentrarchus labrax L). Comp. Biochem. Physiol. B 1994, 107:616-624.
40. Kamunde C., Clayton C., Wood C. Waterborne versus dietary copper uptake in rainbow trout and the effects of previous waterborne copper exposure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2002, 283:R69-R78.
41. Kraemer L.D., Campbell P.G.C., Hare L. Dynamics of Cu, Cd, and Zn accumulation in organs and subcellular fractions in field transplanted juvenile yellow perch (Perca flavescens). Environ. Pollut. 2005, 138:324-337.
42. Krumschnabel G., Manzl C., Berger C., Hofer B. Oxidative stress mitochondrial permeability transition, and cell death in Cu-exposed trout hepatocytes. Toxicol. Appl. Pharmacol. 2005, 209:62-73.
43. La Fontaine S., Mercer J.F. Trafficking of the copper-ATPases, ATP7A and ATP7B:role in copper homeostasis. Arch. Biochem. Biophys. 2007, 463:149-167.
44. Larsen E.H., Sørensen J.B., Sørensen J.N. Analysis of the sodium recirculation theory of solute-coupled water transport in small intestine. J. Physiol. 2002, 542:33-50.
45. Larsson A., Haux C., Sjöbeck M. Fish physiology and metal pollution: results and experiences from laboratory and field studies. Ecotoxicol. Environ. Saf. 1985, 9:250-281.
46. Lauren D.J., McDonald D.G. Acclimation to copper by rainbow trout, Salmo gairdneri: physiology. Can. J. Fish. Aquat. Sci. 1987, 44(1):99-104.
47. Loretz C.A. Electrophysiology of ion transport in teleost intestinal cells. Cellular and Molecular Approaches to Fish Ionic Regulation 1995, 25-56. London Academic Press, London. C.M. Wood, T.J. Shuttleworth (Eds.).
48. Loro V.L., Jorge M.B., da Silva K.R., Wood C.M. Oxidative stress parameters and antioxidant response to sublethal waterborne zinc in a euryhaline teleost Fundulus heteroclitus: protective effects of salinity. Aquat. Toxicol. 2012, 110-111:187-193.
49. Loro V.L., Nogueira L., Nadella S.R., Wood C.M. Zinc bioaccumulation and ionoregulatory impacts in Fundulus heteroclitus exposed to sublethal waterborne zinc at different salinities. Comp. Biochem. Physiol. C 2014, 166:96-104.
50. Lushchak V.I. Environmentally induced oxidative stress in aquatic animals. Aquat. Toxicol. 2011, 101:13-30.
51. Main W.P.L., Ross C., Bielmyer G.K. Copper accumulation and oxidative stress in the sea anemone, Aiptasia pallida, after waterborne copper exposure. Comp. Biochem. Physiol. 2010, 151C:216-221.
52. Manduzio H., Monsinjon T., Rocher B., Leboulenger F., Galap C. Characterization of inducible isoform of the Cu/Zn superoxide dismutase in the blue mussel Mytilus edulis. Aquat. Toxicol. 2003, 64:73-83.
53. Marshall W.S., Grosell M. Ion transport, osmoregulation, and acid-base balance. The Physiology of Fishes 2005, 177-230. CRC Press, Boca Raton. third ed. D.H. Evans, J.B. Claiborne (Eds.).
54. Martínez-Álvarez R.M., Morales A.E., Sanz A. Antioxidant defenses in fish: biotic and abiotic factors. Rev. Fish Biol. Fish. 2005, 15:75-88.
55. Mazon A.F., Fernandes M.N. Toxicity and differential tissue accumulation of copper in the tropical freshwater fish, Prochilodus scrofa (Prochilodontidae). Bull. Environ. Contam. Toxicol. 1999, 63:797-804.
56. Mazon A.F., Monteiro E.A.S., Pinheiro G.H.D., Fernandes M.N. Hematological and physiological changes induced by short-term exposure to copper in the freshwater fish, Prochilodus scrofa. Braz. J. Biol. 2002, 62:621-631.
57. McClelland G.B., Craig P.M., Dhekney K., Dipardo S. Temperature- and exercise-induced gene expression and metabolic enzyme changes in skeletal muscle of adult zebrafish (Danio rerio). J. Physiol. 2006, 577:739-751.
58. McDonald D.G., Wood C.M. Branchial mechanisms of acclimation to metals in freshwater fish. Fish Ecophysiology 1993, 297-321. Chapman and Hall, London, (Chapter 12). J. Cliff Rankin, F.B. Jensen (Eds.).
59. Nadella S.R., Fitzpatrick J.L., Franklin N., Bucking C.P., Smith S., Wood C.M. Toxicity of dissolved Cu, Zn, Ni and Cd to developing embryos of the blue mussel (Mytilus trossolus) and the protective effect of dissolved organic carbon. Comp. Biochem. Physiol. C 2009, 149:340-348.
60. Niyogi S., Wood C. Biotic ligand model: a flexible tool for developing site-specific water quality guidelines for metals. Environ. Sci. Technol. 2004, 38:6177-6192.
61. Paris-Palacios S., Biagianti-Risbourg S., Vernet G. Biochemical and (ultra) structural hepatic perturbations of Brachydanio rerio (Teleostei, Cyprinidae) exposed to two sublethal concentrations of copper sulfate. Aquat. Toxicol. 2000, 50:109-124.
62. Pedrajas J.R., Peinado J., Lopez-Barea J. Oxidative stress in fish exposed to model xenobiotics. Oxidatively modified forms of Cu, Zn superoxide dismutase as potential biomarkers. Chem. Biol. Interact. 1995, 98:267-282.
63. 2+. Toxicology 2000, 143:263-273.
64. Radi A., Matkovics B. Effects of metal ions on the antioxidant enzyme activities: protein contents and lipid peroxidation of carp tissues. Comp. Biochem. Physiol. C 1988, 90:69-72.
65. Sampaio F.G., Boijink C.L., Oba E.T., dos Santos L.R.B., Kalini A.L., Rantin F.T. Antioxidant defenses and biochemical changes in pacu (Piaractus mesopotamicus) in response to single and combined copper and hypoxia exposure. Comp. Biochem. Physiol. Part C 2008, 147:43-51.
66. Sanchez W., Palluel O., Meunier L., Coquery M., Porcher J.M., Aït-Aïssa S. Copper-induced oxidative stress in three-spined stickleback: relationship with hepatic metal levels. Environ. Toxicol. Pharmacol. 2005, 19:177-183.
67. Schippers M.-P., Rukas R., Smith R.W., Wang J., Smolen K., McClelland G.B. Lifetime performance in foraging honeybees: behaviour and physiology. J. Exp. Biol. 2006, 209:3828-3836.
68. Scott G.R., Baker D.W., Schulte P.M., Wood C.M. Physiological and molecular mechanisms of osmoregulatory plasticity in killifish after seawater transfer. J. Exp. Biol. 2008, 211:2450-2459.
69. Streyer L. Biochemistry 1981, Freeman & Co., San Francisco. second ed.
70. 2O. Bull. VURH Vodnany 1982, 2:26-29. [In Czech].
71. 4 on carp. J. Environ. Sci. Health Part B, Pestic. Food Contam. Agric. Wastes 1996, 31:627-635.
72. Toyota Y., Okabe S., Kanamori S., Kitano Y. The determination of Mn, Fe, Ni, Cu and Zn in seawater by atomic absorption spectrometry after coprecipitation with lanthanum hydroxide. J. Oceanogr. Soc. Japan. 1982, 38:357-361.
73. Viant M.R., Walton J.H., TenBrook P.L., Tjeerdema R.S. Sublethal actions of copper in abalone (Haliotis rufescens) as characterized by in vivo 31P NMR. Aquat. Toxicol. 2002, 57:139-151.
74. Vutukuru S.S., Chintada S., Madhavi K.R., Venkateswara Rao J., Anjaneyulu Y. Acute effects of copper on superoxide dismutase, catalase and lipid peroxidation in the freshwater teleost fish Esomus danricus. Fish Physiol. Biochem. 2006, 32:221-229.
75. Wendelaar-Bonga S.E., Lock R.C.A. Toxicants and osmoregulation in fish. Neth. J. Zool. 1992, 42:478-493.
76. Witeska M., Kondera E., Lipionoga J., Jastrzebska A. Changes in oxygen consumption rate and red blood parameters in common carp Cyprinus carpio L. after acute copper and cadmium exposures. Fresen. Environ. Bull. 2010, 19(1):115-122.
77. Wood C.M. An introduction to metals in fish physiology and toxicology: Basic principles 2012, vol 31A:1-51. Elsevier, San Diego.
78. Wright D.A. Trace-metal and major ion interactions in aquatic animals. Mar. Pollut. Bull. 1995, 31:8-18.