DOI QR코드

DOI QR Code

Thermal effects on antioxidant enzymes response in Tilapia, Oreochromis niloticus exposed Arsenic

Arsenic에 노출된 틸라피아, Oreochromis niloticus의 항산화 효소반응에 미치는 수온의 영향

  • Min, EunYoung (Institute of Fisheries science, PuKyong National University) ;
  • Jeong, Ji Won (National Fishery Products Quality Management Service) ;
  • Kang, Ju-Chan (Department of Aquatic life medicine, Pukyong National University)
  • 민은영 (부경대학교 수산과학연구소) ;
  • 정지원 (국립수산물품질관리원) ;
  • 강주찬 (부경대학교 수산생명의학과)
  • Received : 2014.07.10
  • Accepted : 2014.08.04
  • Published : 2014.08.30

Abstract

The effects of waterborne arsenic (As) exposure on antioxidant defense were studied in liver and gills of tilapia, Oreochromis niloticus under thermal stress. Tilapia were exposed to different As concentrations (0, 200 and $400{\mu}g/L$) at three water-temperatures (WT; 20, 25 and $30^{\circ}C$) for 10 days. In antioxidant response, glutathione (GSH) levels, glutathione reductase (GR), glutathione peroxidase (GPx) and glutathione S-treansferase (GST) activities were significantly decreased depend on WT in the gills after As exposure. Also, the range of fluctuation in these enzymes activities was most significantly increased at $30^{\circ}C$ in the liver of tilapia exposed to As. The present findings suggest that a simultaneous stress by temperature change and As exposure could accelerate the alteration in antioxidant enzymes activities of tilapia.

본 연구에서는 수온변화에 따른 비소 (As) 노출의 영향을 틸라피아 Oreochromis niloticus의 간과 아가미에서 항산화 방어기작 (antioxidant defense system)을 통해 알아보고자 한다. 틸라피아를 수온이 각각, 20, 25 및 $30^{\circ}C$ 일때, 비소 농도 0, 200 및 $400{\mu}g/L$에서 10일간 노출시킨 후, glutathione (GSH) levels, glutathione reductase (GR), glutathione peroxidase (GPx) and glutathione S-treansferase (GST) 효소 활성을 측정하였다. 비소 노출 이후, 틸라피아의 간과 아가미에서 이들 항산화 효소는 수온 변화에 따라 유의하게 변화하였다. 특히, 다른 온도구간에 비하여 수온이 $30^{\circ}C$ 일 때, 비소에 노출된 틸라피아의 간에서 이들 효소의 변동폭은 가장 유의하게 증가하였다. 즉, 본 연구는 틸라피아의 간과 아가미에서 GSH 및 항산화 효소인 GR, GPx 및 GST에 미치는 비소의 영향은 수온 상승이 동반되었을 때, 어류의 산화 스트레스에 대한 방어 기작의 감소를 촉진시켰음을 보여준다.

Keywords

References

  1. An, J.H. and Lee, K.H.: Correlation and hysteresis analysis of air-water temperature in four rivers: Preliminary study for water temperature prediction. Kor. Environ. Pol. Res. 12(2): 17-32, 2013.
  2. Ahmad, I.M.P. and Santos, M.A.: Enzymatic and nonenzymatic antioxidants as an adaption to phagocytic-induced damage in Anguilla anguilla L. following in situ harbor water exposure. Ecotoxicol. Environ. Safe. 2: 290-302, 2004.
  3. Ahmed, M.K., Mamun, Md.H.A., Parvin, E., Akter, M.S. and Khan, M.S.: Arsenic induced toxicity and histopathological changes in gill and liver tissue of freshwater fish, tilapia (Oreochromis mossambicus). Exp. Toxicol. Path., 65: 903-909, 2013. https://doi.org/10.1016/j.etp.2013.01.003
  4. APHA 1992: Standard methods for the examination of water and wastewater, 18th edition. American Public Health Association, Washington, D.C., 1992.
  5. Atli, G. and Canli, M.: Response of antioxidant system of freshwater fish, Oreochromis niolticus to acute and chronic metal (Cd, Cu, Cr, Zn, Fe) exposure. Ecotoxicol. Environ. Safe. 73: 1884-1889, 2010. https://doi.org/10.1016/j.ecoenv.2010.09.005
  6. Bachleitner-Hofmann, T., Gisslinger, B., Grumbeck, E. and Gisslinger, H.: Arsenic trioxide and ascorbic acid: synergy with potential implication for the treatment of acute of myeloid leukaemia. Br. J. Haematol. 112(3): 783-786, 2001. https://doi.org/10.1046/j.1365-2141.2001.02608.x
  7. Baeck, S.K.: Combined effect of Cu and temperature on physiological and biochemical change of rock fish, Sebastes schlegeli. PuKyong National University, Master's Thesis, 2012
  8. Bagnyukova, T.V., Lushchak, O.V., Storey, K.B. and Lushchak, V.I.: Oxidative stress and antioxidant defense responses by goldfish tissues to acute change of temperature form 3 to $23^{\circ}C$. J. Thermal Biol. 32: 227-234, 2007. https://doi.org/10.1016/j.jtherbio.2007.01.004
  9. Bell, J.G., Cowey, C.B. Adron, J.W. and Shanks, A.M.: Some effects of vitamin E and selenium deprivation on tissue enzyme levels and indices of tissue peroxidation in rainbow trout (Salmo gairdneri). Br. J. Natr. 53: 149-157, 1985. https://doi.org/10.1079/BJN19850019
  10. Beutler, E. Red cell metabolism: Manual of biochemical methods (3rd ed.). Grune Stratton, Ic., Orlando, FL 32887, London, 1984.
  11. Chang, Y.J., Hur, J.W., Kim, H.K. and Lee, J.K.: Stress in olive flounder (Paralichthys olivaceus) and fat cod (Hexagrammos otakii) by the sudden drop and rise of water temperature. J. Korean Fish. Soc., 34 (2): 34(2):91-97, 2001.
  12. Cherkasov, A.A., Overton, R.A., Sokolov, Jr. E.P. and Sokolova, I.M.: Temperature-dependent effects of cadmium and purine nucleotides on mitochondrial aconitase from a marine ectotherm, Crassostrea virginica: a role of temperature in oxidative stress and allosteric enzyme regulation. J. Exp. Biol. 210: 46-55, 2007. https://doi.org/10.1242/jeb.02589
  13. Choi, B.S., Kang, D.W., Lee, J.Y., Park, E.S., Hong, Y.P., Yang, J.S., Lee, H.M. and Park, J.D.: Acute toxicity of arsenic in Rats and Mice. K. J. Occup. Environ. Med. 15(4): 323-334, 2003.
  14. Chouchane, S. and Snow, E.T.: In Vitro Effect of Arsenical Compounds on Glutathione-Related Enzymes. Chem. Res. Toxicol. 14(5): 517-522, 2001. https://doi.org/10.1021/tx000123x
  15. Csanaky, I. Nemeti, B. and Gregus, Z.: Dose-dependent biotransformation of arsenite in rats- not. S-adenosylmethionine depletion impairs arsenic methylation at high dose. Toxicol. 183: 77-91, 2003. https://doi.org/10.1016/S0300-483X(02)00444-4
  16. Cui, Y., Du, Y., Lu, M. and Qiang, C.: Antioxidant responses of Chilo suppressalis (Lepidoptera: Pyralidae) larvae exposed to thermal stress. J. Thermal Biol. 36: 292-297, 2011. https://doi.org/10.1016/j.jtherbio.2011.04.003
  17. Culioli, J.L., Calendini, S., Mori, C. and Orsini, A.: Arsenic accumulation in a freshwater fish living in a contaminated river of Corsica, France. Ecotoxicol. Environ. Safe. 72: 1440-1445, 2009. https://doi.org/10.1016/j.ecoenv.2009.03.003
  18. Dringen, R., Gutterer, J.M. and Hirrlinger, J.: Glutathione metabolism in brain metabolic interaction between astrocytes and neurons in the defense against reactive oxygen species. Eur. J. Biochem. 267: 4912-4916, 2000. https://doi.org/10.1046/j.1432-1327.2000.01597.x
  19. Elia, A.C., Dorr, A.J.M., Mantilacci, L., Taticchi, M.I. and Galarini, R.: Effects of mercury on glutathione and glutathione-dependent enzymes in catfish (Icatalurus melas R.). In: Markert B, Friese K (Eds.), Trace Elements- Their distribution and effects in the environment: Trace metals in the environment. Vol. 4, Elsevier Science, Amsterdam, pp. 411-421, 2000.
  20. Elia, A.C., Galarini, R., Taticchi, M.I., Martin Dorr, A.J. and Mantilacci, L.: Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. Ecotoxicol. Environ. Safe. 55: 162-167, 2003. https://doi.org/10.1016/S0147-6513(02)00123-9
  21. Elsie, M.B.S.: Thermal effects on the accumulation of arsenic in green sunfish, Lepomis cyanellus. Arch. Environ. Contam. Toxicol. 4(1): 8-17, 1976. https://doi.org/10.1007/BF02221011
  22. Gallagher, E.P, Canada, A.T. and Di Giulio, R.T.: The protective role of glutathione in chlorothalonil-induced toxicity to channel catfish. Aquat. Toxicol. 23: 155-168, 1992. https://doi.org/10.1016/0166-445X(92)90049-S
  23. Grim, J.M., Miles, D.R.B. and Crockett, E.L.: Temperature acclimation alters oxidative capacities and composition of membrane lipids without influencing activities of enzymatic antioxidants or susceptibility to lipid peroxidation in fish muscle. J. Exp. Biol. 213: 445-452, 2010. https://doi.org/10.1242/jeb.036939
  24. Grim, J.M., Simonik, E.A., Semones, M.C., Kuhn, D.E. and Crockett, E.L.: The glutathione-dependent system of antioxidant defense is not modulated by temperature acclimation in muscle tissues from striped bass, Morne saxatilis. Comp. Biochem. Physiol. 164(A): 383-390, 2013. https://doi.org/10.1016/j.cbpa.2012.11.018
  25. Ha, K.J., Ha, E.H., Yoo, C.S. and Jeon, E.H.: Temperature trends and extreme climate since 1909 at big four cities of Korea. AP. J. Amos. Sci., 40(1): 1-16, 2004.
  26. Habig, W., Pabst, J. and Jakoby, W.B.: Glutahione-Stransferases: The first enzymatic step in mercaptouric acid formation. J. Biol. Chem. 249: 7130-7139, 1974.
  27. Hayes, J.D. and Pulford, D.J.: The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit. Rev. Biochem. Mol. Biol. 30: 445-600, 1995. https://doi.org/10.3109/10409239509083491
  28. Hayes, J.D. and McLellan, L.I.: Glutathione and Glutathione-dependent enzymes represent a Co-ordinately regulated defense against oxidative stress. Free Rad. Res. 31: 273-300, 1999. https://doi.org/10.1080/10715769900300851
  29. Heise, K., Puntarulo, S., Portner, H.O., Abele, D.: Production of reactive oxygen species by isolated mitochondria of the Antarctic bivalve Laternula elliptica (King and Broderip) under heat stress. Comp. Biochem. Physiol. 134(C): 79-90, 2003. https://doi.org/10.1016/S1096-4959(02)00231-2
  30. Hughes, M.F.: Arsenic toxicity and potential mechanisms of action. Toxicol. Lett. 133: 1-16, 2002. https://doi.org/10.1016/S0378-4274(02)00084-X
  31. Jason, M.H. Hong, Z. and Dean, P.J.: Differential oxidation of thioredoxin-1, thioredoxin-2, and glutathione by metal ions. Free Radic. Biol. Med. 40: 138-145, 2006. https://doi.org/10.1016/j.freeradbiomed.2005.09.023
  32. Jezierska, B. and Witeska, M.: The metal uptake and accumulation in fish living in polluted waters. Soil and Water Pollution Monitoring, Protection and Remediation, NATO Science Series, 69: 107-114, 2006. https://doi.org/10.1007/978-1-4020-4728-2_6
  33. John. D.H. and David, J.P.: The glutathione S-transferase supergene family: regulation of GST and the contribution of the isozymes to cancer chemoprotection and drug resistance. Critical reviews in Biochem. Molecul. Biol. 30(6): 445-600, 1995. https://doi.org/10.3109/10409239509083491
  34. Kavitha, P. and Venkateswara, R. J.: Sub-lethal effects of profenofos on tissue-specific antioxidative responses in a Euryhyaline fish, Oreochromis mossambicus. Ecotoxicol. Environ. Saf. 72: 1727-1733, 2009. https://doi.org/10.1016/j.ecoenv.2009.05.010
  35. Kaur, M., Atif, F., Ali, M., Rehman, H. and Raisuddin, S.: Heat stress-induced alterations of antioxidants in the freshwater fish Channa punctate Bloch. J. Fish Biol. 67: 1653-1665, 2005. https://doi.org/10.1111/j.1095-8649.2005.00872.x
  36. Kitchin, K.T. and Ahmad, S.: Oxidative stress as a possible mode of action for arsenic carcinogenesis. Toxicol. Lett. 137: 3-3, 2003. https://doi.org/10.1016/S0378-4274(02)00376-4
  37. Kotsanis, N. and Ilipoulou, G.J.: Arsenic induced liver hyperplasia and kidney fibrosis in rainbow trout (Oncorhynchus mykiss) by microinjection technique: A sensitive animal bioassay for environmental metal-toxicity. Bull. Environ. Contam. Toxicol. 62 (2): 169-178, 1999. https://doi.org/10.1007/s001289900856
  38. Lawson, N.M. and Mason, R.P.: Concentrations of mercury, methylmercury, cadmium, lead, arsenic and selenium in the Rain and Stream water of two contrasting watersheds in Western Maryland. Water Res. 35(17): 4039-4052, 2001. https://doi.org/10.1016/S0043-1354(01)00140-3
  39. Liu, J., Liu, Y., Powell, D.A., Walkes, M.P. and Klassen, C.D.: Multidrug-resistance mdr 1a/1b double knockout mice are more sensitive than wild type mice to acute arsenic toxicity, with higher arsenic accumulation in tissues. Toxicol. 170: 55-62, 2002. https://doi.org/10.1016/S0300-483X(01)00532-7
  40. Liu, H., Zhang, J.F., Shen, H., Wang, X.R. and Wang, W.M.: Impact of Copper and Its EDTA Complex on the Glutathione-Dependent Antioxidant System in Freshwater Fish (Carassius auratus). Bull. Environ. Contam. Toxicol. 74: 1111-1117, 2005. https://doi.org/10.1007/s00128-005-0696-x
  41. Livingstone, D.R.: Contaminant-stimulated reaction oxygen species production and oxidative damage in aquatic organisms. Mar. Pollut. Bull. 42: 656-666, 2001. https://doi.org/10.1016/S0025-326X(01)00060-1
  42. Logue, J.P.T. and Cossins, A.R.: Heat injury and resistance adaptation in fish. J. Ther. Biol. 20: 191-197, 1995. https://doi.org/10.1016/0306-4565(94)00056-O
  43. Maiti, S. and Chatterjee, A.K.: Effects on levels of glutathione and some related enzymes in tissues after an acute arsenic exposure in rats and their relationship to dietary protein deficiency. Arch. Toxicol. 75: 531-537, 2001. https://doi.org/10.1007/s002040100240
  44. Mandal, B.K. and Suzuki, K.T.: Arsenic round the world: a review. Talanta, 58: 201-235, 2002. https://doi.org/10.1016/S0039-9140(02)00268-0
  45. McGeachy, S.M. and Dixon, D.G.: The impact of temperature on the acute toxicity of arsenate and arsenite to rainbow trout (Salomo gairdneri). Ecotoxicol. Environ. Saf. 17(1): 86-93, 1989. https://doi.org/10.1016/0147-6513(89)90012-2
  46. Nam, S.S., Lee, C.W., Ryn, J.R., Park, E.R., Nam, K.C., Rhu, H.I., Jeon, S.H., Na, J.G., Choi, D.I. and Park, K.S.: Effects of Arsenic on the gonadal development in Crucian carp. Kor. J. Environ. Toxicol. 16(2): 51-56, 2001.
  47. Park, M.Y., Chang, Y.J. and Kang, D.Y.: Physiological response of the cultured olive flounder (Paralichthys olivaceus) to the sharp changes of water temperature. J. Aquaculture, 12(3): 221-228, 1999.
  48. Richardson, R.J. and Murphy, S.D.: Effect of glutathione depletion on tissue deposition of methylmercury in rats. Toxicol. Appl. Pharmacol. 31: 505-519, 1975. https://doi.org/10.1016/0041-008X(75)90274-4
  49. Ryan, S.N.: The effect of chronic heat stress on cortisol levels in the Antartic fish Pagothenia borchgrevinki. Experimentia, 51: 768-774, 1995. https://doi.org/10.1007/BF01922428
  50. Seong, K.T., Hwang, J.D., Han, I.S., Go, W.J., Suh, Y.S. and Lee, J.Y.: Characteristic for long-term trends of temperature in the Koreans waters. J. K. Soc. Mar. Environ., 16(4): 353-360, 2010.
  51. Shah, A.Q., Kazi, T.G., Arain, M.B., Jamali, M.K., Afridi, H.I., Jamil, N.J., Baig, J.A. and Kandhro, G.A.: Accumulation of arsenic in different fresh water fish species - potential contribution to high arsenic intakes. Food Chem. 112: 520-524, 2009. https://doi.org/10.1016/j.foodchem.2008.05.095
  52. Shi, H., Hudson, L.G. and Liu, K.J.: Oxidative stress and apoptosis in metal ion-induced carcinogenesis. Free Radic. Biol. Med. 37: 852-593, 2004.
  53. Sorensen, E.M.B.: Toxicity and accumulation of arsenic in green sunfish, Lepomis cyanellus, exposed to arsenate in water. Bull. Environ. Contam. Toxicol. 15: 756-764, 1976. https://doi.org/10.1007/BF01685629
  54. Sorensen, E.M.B.: Arsenic. In: Sorenson, E.M.B. (Ed.), Metal poisoning in Fish. CRC Press, pp. 61-99, 1991.
  55. Sun, Y., Zhang, H., Yu, J., Shen, Y., Yin, H., Liu, H. and Wang, X.: Bioaccumulation and antioxidant responses in goldfish Carassius auratus under HC Orange No 1 exposure. Ecotoxicol. Environ. Safe. 63: 430-437, 2006. https://doi.org/10.1016/j.ecoenv.2005.02.001
  56. Takatsu, A., Kuroiwa, T. and Uchiumi, A.: Arsenic accumulation in organs of the fresh water fish Tribolodon hakonensis. J. Trace Elements Med. Biol. 13: 176-179, 1999. https://doi.org/10.1016/S0946-672X(99)80008-X
  57. Tripathi, N. and Flora, S.J.S.: Effect of some thiol chelators on emzymatic activities in blood, liver and kidneys of acute arsenic (III) exposed mice. Biomed. Environ. Sci. 11: 38-45, 1998.
  58. Tsai, J.W., Huang, Y.H., Chen, W.Y. and Liao, C.M.: Detoxification and bioregulation are critical for long-term waterborne arsenic exposure risk assessment for tilapia. Environ. Monit. Assess. 184: 561-572, 2012. https://doi.org/10.1007/s10661-011-1988-8
  59. Valko, M., Rhodes, C.J., Moncol, J., Izakovic, M. and Mazur, M.: Free-radicals, metals and antioxidants in oxidative stress-induced cancer. Chem. Biol. Interact. 160: 1-40, 2006. https://doi.org/10.1016/j.cbi.2005.12.009
  60. Ventura-Lima, J., de Castro, M.R., Acosta, D., Fattorini, D,, Regoli, F., de Carvalho, L.M., Bohrer, D., Geracitano, L.A., Barros, D.M., Marins, L.F., da Silva, R.S., Bonan, C.D., Bogo, M.R. and Monserrat, J.M.: Effects of arsenic (As) exposure on the antioxidant status of gills of the zebrafish Danio rerio (Cyprinidae). Comp. Biochem. Physiol. Toxicol. Pharmacol. 149(4C): 538-43, 2009. https://doi.org/10.1016/j.cbpc.2008.12.003
  61. Winston, G.W. and Giulio, R.T.: Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat. Toxicol. 19: 137-161, 1991. https://doi.org/10.1016/0166-445X(91)90033-6

Cited by

  1. Influence of Elevated Temperatures on the Physiological Response of Hemolymph from Two Species of the Abalone, Haliotis discus hannai and H. discus discus vol.31, pp.1, 2015, https://doi.org/10.9710/kjm.2015.31.1.1
  2. Oxidative stress and non-specific immune responses in juvenile black sea bream, Acanthopagrus schlegelii, exposed to waterborne zinc vol.20, pp.1, 2017, https://doi.org/10.1186/s41240-017-0056-x
  3. Influence of elevated temperatures on the physiological response of hemolymph from two species of abalone, Haliotis gigantea and Haliotis discus discus (Reeve, 1846) vol.31, pp.3, 2015, https://doi.org/10.9710/kjm.2015.31.3.187
  4. Toxic effects of arsenic on growth, hematological parameters, and plasma components of starry flounder, Platichthys stellatus, at two water temperature conditions vol.22, pp.1, 2019, https://doi.org/10.1186/s41240-019-0116-5