Copper alters the effect of temperature on mitochondrial bioenergetics in rainbow trout, Oncorhynchus mykiss

Archives of Environmental Contamination and Toxicology

Volumn 66, Issue 3, 2014, Pages 430-440

  Sappal, Ravinder ^a   MacDougald, Michelle ^a   Stevens, Don ^a   Fast, Mark D ^a   Kamunde, Collins ^a  

^a UNIVERSITY OF PRINCE EDWARD ISLAND   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; TRICARBOXYLIC ACID; UBIQUINOL CYTOCHROME C REDUCTASE;

ANIMAL EXPERIMENT; ARTICLE; BIOENERGY; BREATHING RATE; CELL ENERGY; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME ACTIVITY; HIGH TEMPERATURE; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATION; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RAINBOW TROUT; TEMPERATURE;

ONCORHYNCHUS MYKISS;

ANIMALS; CELL RESPIRATION; COPPER; ENERGY METABOLISM; MITOCHONDRIA; ONCORHYNCHUS MYKISS; TEMPERATURE; WATER POLLUTANTS, CHEMICAL;

EID: 84899493870     PISSN: 00904341     EISSN: 14320703     Source Type: Journal    
DOI: 10.1007/s00244-013-9985-2     Document Type: Article

References (64)

1. Abele D, Heise K, Pörtner HO, Puntarulo S (2002) Temperature-dependence of mitochondrial function and production of reactive oxygen species in the intertidal mud clam Mya arenaria. J Exp Biol 205:1831-1841 (Pubitemid 34853435)
2. Adiele RC, Stevens D, Kamunde C (2010) Reciprocal enhancement of uptake and toxicity of cadmium and calcium in rainbow trout (Oncorhynchus mykiss) liver mitochondria. Aquat Toxicol 96:319-327
3. Adiele RC, Stevens D, Kamunde C (2012) Differential inhibition of electron transport chain enzyme complexes by cadmium and calcium in isolated rainbow trout (Oncorhynchus mykiss) hepatic mitochondria. Toxicol Sci 127:110-119
4. Almeida VMF, Buck LT, Hochachka PW (1994) Substrate and acute temperature effects on turtle heart and liver mitochondria. Am J Physiol 266:R858-R862
5. Altshuler I, Demiri B, Xu S, Constantin A, Yan ND, Cristescu ME (2011) An integrated multi-disciplinary approach for studying multiple stressors in freshwater ecosystems: Daphnia as a model organism. Integr Comp Biol 51:623-633
6. 2+-promoted mitochondrial permeability transition: a comparison with other heavy metals. Acta Biochim Pollut 51:545-551
7. Belyaeva EA, Korotkova SM, Saris N-E (2011) In vitro modulation of heavy metal-induced rat liver mitochondria dysfunction: a comparison of copper and mercury with cadmium. J Trace Elem Med Biol 25:63-73
8. Blier PU, Guderley HE (1993) Mitochondrial activity in rainbow trout red muscle: the effect of temperature on the ADP-dependence of ATP synthesis. J Exp Biol 176:145-157
9. Boveris A, Oshino N, Chance B (1972) The cellular production of hydrogen peroxide. Biochem J 128:617-630
10. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
11. Brand MD, Chien LF, Ainscow EK, Rolfe DFS, Porter RK (1994) The causes and functions of mitochondrial proton leak. Biochim Biophys Acta 1187:132-139 (Pubitemid 24267043)
12. Chavez-Crooker P, Garrido N, Ahearn GA (2002) Copper transport by lobster (Homarus americanus) hepatopancreatic mitochondria. J Exp Biol 205:405-413 (Pubitemid 34853805)
13. Cherkasov AS, Biswas PK, Ridings DM, Ringwood AH, Sokolova IM (2006a) Effects of acclimation temperature and cadmium exposure on cellular energy budgets in the marine mollusk Crassostrea virginica: linking cellular and mitochondrial responses. J Exp Biol 209:1274-1284
14. Cherkasov AS, Ringwood AH, Sokolova IM (2006b) Combined effects of temperature acclimation and cadmium exposure on mitochondrial function in eastern oysters Crassostrea virginica Gmelin (Bivalvia: Ostreidae). Environ Toxicol Chem 25:2461-2469 (Pubitemid 44763304)
15. Christensen MR, Graham MD, Vinebrooke RD, Findlay DL, Paterson MJ, Turner MA(2006) Multiple anthropogenic stressors cause ecological surprises in boreal lakes. Global Change Biol 12:2316-2322 (Pubitemid 44857706)
16. Collins S, McCoy K, Catapane EJ, Carroll MA (2010) The effects of copper and copper blocking agents on gill mitochondrial O2 utilization of Crassostrea virginica. In Vivo 32:14-19
17. Couture P, Kumar PR (2003) Impairment of metabolic capacities in copper and cadmium contaminated wild yellow perch (Perca flavescens). Aquat Toxicol 64:107-120 (Pubitemid 37323807)
18. Currie RJ, Bennett WA, Beitinger TL (1998) Critical thermal minima and maxima of three freshwater game-fish species acclimated to constant temperatures. Environ Biol Fishes 51:187-200 (Pubitemid 28118081)
19. Dufour S, Rousse N, Canioni P, Diolez P (1996) Top-down control analysis of temperature effect on oxidative phosphorylation. Biochem J 314:743-751
20. Echtay KS, Murphy MP, Smith RAJ, Talbot DA, Brand MD (2002) Superoxide activates mitochondrial uncoupling protein 2 from the matrix side. Studies using targeted antioxidants. J Biol Chem 277:47129-47135 (Pubitemid 36159222)
21. Estabrook RW (1967) Mitochondrial respiratory control and the polarographic measurements in mitochondria. Methods Enzymol 10:41-47
22. Finstad B, Staurnes M, Reite OB (1988) Effect of low temperature on sea-water tolerance in rainbow trout, Salmo gairdneri. Aquaculture 72:319-328
23. Folt CL, Chen CY, Moore MV, Burnaford J (1999) Synergism and antagonism among multiple stressors. Limnol Oceanogr 44:864-877 (Pubitemid 29235730)
24. Garceau N, Pichaud N, Couture P (2010) Inhibition of goldfish mitochondrial metabolism by in vitro exposure to Cd, Cu and Ni. Aquat Toxicol 98:107-112
25. Guderley H (2011) Mitochondria and temperature. In: Farrell AP (ed) Encyclopedia of fish physiology: Energetics, interactions with the environment, lifestyles, and applications. Academic, New York, pp 1709-1716
26. Guderley H, Johnston IA (1996) Plasticity of fish muscle mitochondria with thermal acclimation. J Exp Biol 199:1311-1317 (Pubitemid 26263639)
27. Guderley H, St-Pierre J (2002) Going with the flow or life in the fast lane: contrasting mitochondrial responses to thermal change. J Exp Biol 205:2237-2249
28. Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Oxford University Press, Oxford
29. Hardewig I, Peck LS, Pörtner HO (1999) Thermal sensitivity of mitochondrial function in the Antarctic Notothenioid, Lepidonotothen nudifrons. J Comp Physiol B 169:597-604 (Pubitemid 30018248)
30. Heron P, Cousins K, Boyd C, Daya S (2001) Paradoxical effects of copper and manganese on brain mitochondrial function. Life Sci 68:1575-1583 (Pubitemid 32245585)
31. Heugens EHW, Hendriks AJ, Dekker T, van Straalen NM, Admiraal W (2001) A review of the effects of multiple stressors on aquatic organisms and analysis of uncertainty factors for use in risk assessment. Crit Rev Toxicol 31:247-284 (Pubitemid 32565568)
32. Intergovernmental Panel on Climate Change (2007) Impacts, adaptation and vulnerability. In: Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (eds) Contribution of Working Group II to the Fourth Assessment Report of the IPCC Cambridge University Press, Cambridge
33. Ivanina AV, Cherkasov AS, Sokolova IM (2008) Effects of cadmium on cellular protein and glutathione synthesis and expression of stress proteins in eastern oysters, Crassostrea virginica Gmelin. J Exp Biol 211:577-586 (Pubitemid 351428885)
34. Ivanina AV, Beniash E, Etzkorn M, Meyers TB, Ringwood AH, Sokolova IM (2013) Short-term acute hypercapnia affects cellular responses to trace metals in the hard clams Mercenaria mercenaria. Aquat Toxicol 140-141:123-133
35. Jastroch M, Divakaruni AS, Mookerjee S, Treberg JR, Brand MD (2010) Mitochondrial proton and electron leaks. Essays Biochem 47:53-67
36. Kamunde C, MacPhail R (2008) Bioaccumulation and hepatic speciation of copper in rainbow trout (Oncorhynchus mykiss) during chronic waterborne copper exposure. Arch Environ Contam Toxicol 54:493-503 (Pubitemid 351362170)
37. Kraffe E, Marty Y, Guderley H (2007) Changes in mitochondrial oxidative capacities during thermal acclimation of rainbow trout Oncorhynchus mykiss : roles of membrane proteins, phospholipids and their fatty acid compositions. J Exp Biol 210:149-165 (Pubitemid 46160840)
38. Krumschnabel G, Manzl C, Berger C, Hofer B (2005) Oxidative stress, mitochondrial permeability transition, and cell death in Cu-exposed trout hepatocytes. Toxicol Appl Pharmacol 209:62-73 (Pubitemid 41547218)
39. Lannig G, Flores JF, Sokolova IM (2006) Temperature dependent stress response in oysters, Crassostrea virginica: pollution decreases temperature tolerance in oysters. Aquat Toxicol 79:278-287 (Pubitemid 44403929)
40. Lauer MM, de Oliveira CB, Yano NLI, Bianchini A (2012) Copper effects on key metabolic enzymes and mitochondrial membrane potential in gills of the estuarine crab Neohelice granulata at different salinities. Comp Biochem Physiol C 156:140-147
41. Linder MC (1991) Biochemistry of copper. In: Frieden E (ed) Biochemistry of the elements series. Elsevier, New York, pp 43-52
42. Luvisetto S, Schmehl I, Intravaia E, Conti E, Azzone GF (1992) Mechanism of loss of thermodynamic control in mitochondria due to hyperthyroidism and temperature. J Biol Chem 267:15348-15355
43. Manzl C, Ebner H, Kock G, Dallinger R, Krumschnabel G (2003) Copper, but not cadmium, is acutely toxic for trout hepatocytes: short-term effects on energetics and ion homeostasis. Toxicol Appl Pharmacol 191:235-244 (Pubitemid 37108687)
44. Mark FC, Lucassen M, Strobel A, Barrera-Oro E, Koschnick N, Zane L et al (2012) Mitochondrial function in Antarctic Notothenioids with ND6 translocation. PLoS ONE 7:e31860
45. Meyer JS, Clearwater SJ, Doser TA, Rogaczewski MJ, Hansen JA (2007) Effects of water chemistry on the bioavailability and toxicity of waterborne cadmium, copper, nickel, lead, and zinc to freshwater organisms. SETAC Press, Pensacola
46. Moyes CD, Buck LT, Hochachka PW (1988) Temperature effects on pH of mitochondria isolated from carp red muscle. Am J Physiol 254:R611-R615
47. Onukwufor JO, MacDonald N, Kibenge F, Stevens D, Kamunde C (2013) Hypoxia-cadmium interactions on rainbow trout (Oncorhynchus mykiss) mitochondrial bioenergetics: Attenuation of hypoxia-induced proton leak by low doses of cadmium. J Exp Biol. doi:10.1242/jeb.093344
48. Parker N, Vidal-Puig A, Brand MD (2008) Stimulation of mitochondrial proton conductance by hydroxynonenal requires a high membrane potential. Biosci Rep 28:83-88
49. Pena MMO, Lee J, Thiele DJ (1999) A delicate balance: homeostatic control of copper uptake and distribution. J Nutr 129:1251-1260 (Pubitemid 29304971)
50. Pörtner HO (2012) Integrating climate-related stressor effects on marine organisms: unifying principles linking molecule to ecosystem level changes. Mar Ecol Progr Ser 470:273-290
51. Pörtner HO, Hardewig I, Peck LS (1999a) Mitochondrial function and critical temperature in the Antarctic bivalve, Laternula elliptica. Comp Biochem Physiol A 124:179-189 (Pubitemid 29509778)
52. Pörtner HO, van Dijk PLM, Hardewig I, Sommer A (1999b) Levels of metabolic cold adaptation: trade-offs in eurythermal and stenothermal ectotherms. In: Davison W, Williams CH (eds) Antarctic ecosystems: models for wider ecological understanding. Caxton Press, Christchurch, pp 109-122
53. 2+. Toxicology 143:263-273
54. Pye V (1973) Acute temperature change and the oxidation rates of ectotherm mitochondria. In: Wieser W (ed) Effects of temperature on ectothermic organisms. Springer, New York, pp 83-95
55. Sala OE, Chapin FS, Armesto JJ, Berlow E, Bloomfield J, Dirzo R et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770-1774 (Pubitemid 30143956)
56. + with mitochondria. Acta Chem Scand 45:1042-1046
57. Schulte PM, Healy TM, Fangue NA (2011) Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr Comp Biol 51:691-702
58. 2+ Toxicity inhibition of mitochondrial dehydrogenases in vitro and in vivo. Ann Neurol 55:645-653
59. Sokol RJ, Twedt D, McKim JM Jr, Devereaux MW, Karrer FM, Kam I et al (1994) Oxidant injury to hepatic mitochondria in patients with Wilson's disease and Bedlington terriers with copper toxicosis. Gastroenterology 107:1788-1798 (Pubitemid 24357635)
60. Sokolova IM (2004) Cadmium effects on mitochondrial function are enhanced by increased temperatures in a marine poikilotherm, Crassostrea virginica Gmelin (Bivalvia: Ostreidae). J Exp Biol 207:2639-2648
61. Sokolova IM, Lannig G (2008) Interactive effects of metal pollution and temperature on metabolism in aquatic ectotherms: implications of global climate change. Climate Res 37:181-201
62. Spinazzi M, Casarin A, Pertegato V, Salviati L, Angelini C (2012) Assessment of mitochondrial respiratory chain enzymatic activities on tissues and cultured cells. Nat Prot 7:1235-1246
63. Strubelt O, Kremer J, Tilse A, Keogh J, Pentz R, Younes M (1996) Comparative studies on the toxicity of mercury, cadmium, and copper toward the isolated perfused rat liver. J Toxicol Environ Health 47:267-283
64. Wallace KB, Starkov AA (2000) Mitochondrial targets of drug toxicity. Annu Rev Pharmacol Toxicol 40:353-388 (Pubitemid 30340687)