Carbonic Anhydrase Activity Responses and Histopathological Changes in Gill and Liver Tissues after Acute Exposure to Chromium in Brown Trout Juveniles

Yeliz Demir; Ertan Oruç; Ahmet Topal

Carbonic Anhydrase Activity Responses and Histopathological Changes in Gill and Liver Tissues after Acute Exposure to Chromium in Brown Trout Juveniles

Year 2016, Volume: 44 Issue: 4, 515 - 523, 01.11.2016

Abstract

Heavy metals are major pollutants in ground, air, marine and fresh water and they cause toxic effects in fish tissues. This study was conducted to determine histopathological effects and changes in carbonic anhy- drase CA enzyme activity in liver and gill tissues of brown trout juveniles exposed to chromium Cr3+ . Fish were exposed to chromium concentrations 1 mg/L and 2 mg/L for 24, 48 and 96h. It was found that CA was significantly inhibited at 48 and 96h of two concentrations p

Keywords

Carbonic anhydrase, histopathology, Liver, gills, chromium

References

1. Y.B. Koca, S. Koca, S. Yıldız, B. Gurcu, E. Osanc, O. Tuncbas, G. Aksoy, Investigation of histopathological and cytogenetic effects on Lepomis gibbosus (Pisces: Perciformes) in the çine stream (Aydın/Turkey) with determination of water pollution, Environ. Toxicol., 20 (2005) 560-571.
2. A.G. Heath, Water Pollution and Fish Physiology, CRC Press, Florida, USA, (1987) 245.
3. G. Atli, Ö. Alptekin, S. Tükel, M. Canli, Response of catalase activity to Ag+, Cd2+, Cr6+, Cu2+ and Zn2+ in five tissues of freshwater fish Oreochromis niloticus, Comp. Biochem. Phys. C., 143 (2006) 218-224.
4. A. Viarengo, Biochemical effects of trace metals, Mar. Pollut. Bull., 16 (1985) 153-158.
5. E.D. Kaya, H. Soyut, S. Beydemir, Carbonic anhydrase activity from the gilthead sea bream (Sparus aurata) liver: The toxicological effects of heavy metals, Environ. Toxicol. Pharmacol., 36 (2013) 514-521.
6. D. Steinhagen, T. Helmus, S. Maurer, R.D. Michael, W. Leibold, J.P. Scharsack, A. Skouras, H.J. Schuberth, Effect of hexavalent carcinogenic chromium on carp Cyprinus carpio immune cells, Dis. Aquat. Org., 62 (2004) 155-161.
7. V. Velma, P.B. Tchounwou, Oxidative stress and DNA damage induced by chromium in liver and kidney of goldfish, Carassius auratus, Biomark, Insights., 25 (2013) 43-51.
8. J.W. Moore, Chromium. In: Inorganic contaminants of surface water: Research and monitoring priorities, New York, NY, Springer-Verlag New York Inc., (1991) 83–97.
9. V. Velma, P.B. Tchounwou, Chromium-induced biochemical, genotoxic and histopathologic effects in liver and kidney of goldfish, Carassius auratus, Mutat. Res., 30 (2010) 43-51.
10. P.S. Rainbow, S.L. White, Comparative accumulating of cobalt by three crustaceans: a decapod, an amphipod and a barnace, Aquat. Toxicol., 16 (1990) 113-126.
11. C.C.C. Cerqueira, M.N. Fernandes, Gill tissue recovery after copper exposure and blood parameter responses in the tropical fish, Prochilodus scrofa. Ecotoxicol. Environ. Saf., 52 (2002) 83-91.
12. M.N. Fernandes, A.F. Mazon, Environmental pollution and fish gill morphology. In: Val AL, Kapoor B.G. (Eds.), Fish Adaptations, Science Publishers, Enfield, (2003) 203–231.
13. D. Ekinci, S. Beydemir, O.I. Kufrevioglu, In vitro inhibitory effects of some heavy metals on human erythrocyte carbonic anhydrases, J. Enzyme Inhib. Med. Chem., 22 (2007) 745-750.
14. H. Soyut, S. Beydemir, Purification and some kinetic properties of carbonic anhydrase from rainbow trout (Oncorhynchus mykiss) liver and metal inhibition, Protein Peptide Lett., 15 (2008) 528-535.
15. H.A. Alici, D. Ekinci, S. Beydemir, Intravenous anesthetics inhibit human paraoxonase-1 (PON1) activity in vitro and in vivo. Clin. Bioch., 41 (2008) 1384-1390.
16. D. Ekinci, S. Beydemir, Evaluation of the impacts of antibiotic drugs on PON 1; a major bioscavenger against cardiovascular diseases, Eur. J. Pharmacol., 617 (2009) 84-89.
17. M. Senturk, D. Ekinci, H.A. Alici, S. Beydemir, Paraoxonase-1, an organophosphate detoxifier and cardioprotective enzyme, is inhibited by anesthetics: An in vitro and in vivo insight, Pest. Biochem. Physiol., 101 (2011) 206-211.
18. H. Soyut, S. Beydemir, S.B. Ceyhun, O. Erdogan, E.D. Kaya, Changes in carbonic anhydrase activity and gene expression of Hsp70 in rainbow trout (Oncorhynchus mykiss) muscle after exposure to some metals, Turk J. Vet. Anim. Sci., 36 (2012) 499- 508.
19. H. Soyut, S. Beydemir, The impact of heavy metals on the activity of carbonic anhydrase from rainbow trout (Oncorhynchus mykiss) kidney, Toxicol. Ind. Health., 28 (2012) 296-305.
20. H. Soyut, E.D. Kaya, S. Beydemir, Impact of antibacterial drugs on human serum paraoxonase-1 (hPON1) activity: an in vitro study, Asian Pac. J. Trop. Biomed., 4 (2014) 603-609.
21. C. Turkes, H. Soyut, S. Beydemir, Effect of calcium channel blockers on paraoxonase-1 (PON1) activity and oxidative stress, Pharmacol. Rep., 66 (2014) 74- 78.
22. C. Turkes, H. Soyut, S. Beydemir, Human serum paraoxonase-1 (hPON1): In vitro inhibition effects of moxifloxacin hydrochloride, levofloxacin hemihidrate, cefepime hydrochloride, cefotaxime sodium, and ceftizoxime sodium, J. Enzyme Inhib. Med. Chem., 30 (2015) 622–628.
23. E.D. Kaya, H. Soyut, S. Beydemir, The toxicological impacts of some heavy metals on carbonic anhydrase from gilthead sea bream (Sparus aurata) gills, Environ. Toxicol. Pharmacol., 39 (2015) 825-832.
24. S. Sender, K. Bottcher, Y. Cetin, G. Gros, Carbonic anhydrase in the gills of seawater- and freshwateracclimated flounders Platichthys flesus: Purification, characterization, and immunohistochemical localization, J. Histochem. Cytochem., 47 (1999) 43- 50.
25. A.M. Vitale, J.M. Monserrat, P. Castilho, E.M. Rodriguez, Inhibitory effects of cadmium on carbonic anhydrase activity and ionic regulation of the estuarine crab Chasmagnathus granulata (Decapoda, Grapsidae). Comp. Biochem. Physiol. C., 122 (1999) 121-129.
26. M.G. Lionetto, M.E. Giordano, S. Vilella, T. Schettino, Inhibition of enzymatic activities by cadmium, Aquat. Toxicol., 48 (2000) 561-571.
27. H. Tohse, Y. Mugiya, Effect of enzyme and anion transport inhibitors on in vitro incorporation of inorganic carbon and calcium into endolymph and otoliths in Salmon (Oncorhynhus masou), Comp. Biochem. Physiol. A., 128 (2001) 177-184.
28. S. Kolayli, F. Karahalil, H. Sahin, B. Dincer, C.T. Supuran, Characterization and inhibition studies of an -carbonic anhydrase from the endangered sturgeon species Acipenser gueldenstaedti, J. Enzyme Inhib. Med. Chem., 26 (2011) 440-444.
29. D. Erdem, E. Yerlikaya, S.B. Ceyhun, R. Demirdag, M. Sentürk, O. Erdogan, O.I. Kufrevioglu, Inhibition effect of some sulfonamides on carbonic anhydrase from european seabass (Dicentrachus labrax), Hacettepe J. Biol. Chem., 39 (2011) 139-144.
30. S.B. Ceyhun, M. Sentürk, E. Yerlikaya, O. Erdogan, O.I. Kufrevioglu, D. Ekinci, Purification and characterization of carbonic anhydrase from the teleost fish Dicentrarchuslabrax (Europeanseabass) liver and toxicological effects of metals on enzyme activity, Environ. Toxicol. Pharmacol., 32 (2011) 69-74.
31. D.G. Stevens, G.A. Chapman, Toxicity of trivalent chromium to early life stages of steelhead trout, Environ. Toxicol. Chem., 3 (1984) 125-133.
32. K.M. Wilbur, N.G. Anderson, Electrometric and colorimetric determination of carbonic anhydrase, J. Biol. Chem., 176 (1948) 147-154.
33. S. De Mora, S.W. Fowler, E. Wyse, S. Azemard, Distribution of heavy metals in marine bivalves, fish and coastal sediments in the Gulf and Gulf of Oman, Mar. Pollut. Bull., 49 (2004) 410-424.
34. H. Hwang, P.G. Green, R.M. Higashi, T.M. Young, Tidal salt marsh sediment in California, USA. Part 2: occurrence and anthropogenic input of trace metals, Chemosphere, 64 (2006) 1899-1909.
35. A. Cicek, A.S. Koparal, Lead, chromium, and cadmium levels in cyprinus carpio and barb plebejus living in the badger dam lake, Turk J. Environ. Conserv., 39 (2001) 3-6.
36. E.F. Kayhan, Bioaccumulate and toxicity of cadmium in seafood, E. U. J. Fish. Aquat. Sci., 23 (2006) 215- 220.
37. Cicik B. The effects on metal accumulation in the liver, gill and muscle tissues of carp (Cyprinus carpio L.) of copper-zinc interaction, Turk J Environ Ecol. 2003;48:32-36.
38. E. Capkin, S. Birincioglu, I. Altinok, Histopathological changes in rainbow trout (Oncorhynchus mykiss) after exposure to sublethal composite nitrogen fertilizers, Ecotoxicol. Environ. Saf., 72 (2009) 1999-2004.
39. J. Mallatt, Fish gill structural changes induced by toxicants and other irritants: a statistical review, Can. J. Fish. Aquat. Sci., 42 (1985) 630-648.
40. D.E. Hinton, D.J. Lauren, Liver structural alterations accompanying chronic toxicity in fishes: potential biomarkers of exposure. In: Biomarkers of Environmental Contaminations. (ed. by J.F. McCarthy, L.R. Shugart), Lewis Publisher, Boca Raton, FL (1990) 17-57.
41. M.M.P. Camargo, C.B.R. Martinez, Histopathology of gills, kidney and liver of a Neotropical fish caged in an urban stream, Neotrop. Ichthyol., 5 (2007) 327-336.
42. J.C. Van Dyk, G.M. Pietersea, J.H. Van Vurena, Histological changes in the liver of Oreochromis mossambicus (Cichlidae) after exposure to cadmium and zinc, Ecotoxicol. Environ. Saf., 66 (2007) 432-40.
43. M. Suiçmez, M. Kayım, D. Köseoğlu, E. Hasdemir, Toxic effects of lead on the liver and gills of oncorhynchus mykiss WALBAUM 1792, Bull. Environ. Contam. Toxicol., 77 (2006) 551-558.
44. H.V. Ghate, L. Mulherkar, Histological changes in the gills of two freshwater prawn species exposed to copper sulphate, Ind. J. Exp. Biol., 17 (1979) 838-840.
45. P. Peebua, M. Kruatrachue, P. Pokethitiyook, S. Singhakaew, Histopathological alterations of Nile tilapia, Oreochromis niloticus in acute and subchronic alachlor exposure, J. Environ. Biol., 29 (2008) 325- 331.
46. E.I. Cengiz, Gill and kidney histopathology in the freshwater fish Cyprinus carpio after acute exposure to deltamethrin, Environ. Toxicol. Pharmacol., 22 (2006) 200-204.
47. G. Alak, M. Atamanalp, A. Topal, H. Arslan, E. Oruç, S. Altun, Histopathological and biochemical effects of humic acid against cadmium toxicity in brown trout gills and muscles, Turk J. Fish. Aquat. Sci., 13 (2013) 315-320.
48. I. Gulcin, S. Beydemir, O. Hisar, Effect of alphatocopheroloil antioxidant enzyme activities and lipid peroxidation in rainbow trout (Oncorhynchus mykiss), Acta Vet. Hung., 53 (2005) 425-433.
49. K. Bottcher, A. Waheed, W.S. Sly, Membraneassociated carbonic anhydrase from the crab gill: Purification, characterization, and comparison with mammalian Cas, Arch. Biochem. Biophys., 312 (1994) 429-435.
50. S.R. Krungkrai, N. Suraveratum, S. Rochanakij, J. Krungkrai, Characterization of carbonic anhydrase in Plasmodium falciparium, Int. J. Parasıtol., 31 (2001) 661-668.
51. S. Beydemir, M. Bulbul, O. Hisar, H. Soyut, T. Yanik, Carbonic anhydrase: affinity purification and kinetic properties from rainbow trout lens, Int. J. Appl. Chem., 2 (2006) 45-55.
52. Y. Zhenyan, X. Liping, L. Seunghwan, Z.A. Rongqing, Novel carbonic anhydrase from the mantle of the pearl oyster (Pinctada fucata), Comp. Biochem. Physiol. B., 143 (2006) 190-194.
53. R.P. Henry, Multiple roles of carbonic anhydrase in cellular transport and metabolism, Annu. Rev. Physiol., 58 (1996) 523-538.
54. C.T. Supuran, Carbonic anhydrases: catalytic and inhibition mechanisms, distribution and physiological roles. In: Supuran CT, Conway J, Smith HJ (Eds.), Carbonic Anhydrase. Its Inhibitors and Activators. CRC Press, London, (2004) 1–23.
55. H. Soyut, S. Beydemir, O. Hisar, Effects of some metals on carbonic anhydrase from brains of rainbow trout, Biol. Trace Elem. Res., 123 (2008) 179-190.

Kahverengi Alabalık Yavrularında Kroma Akut Maruz Kaldıktan Sonra Solungaç ve Karaciğer Dokularında Histolojik Değişiklikler ve Karbonik Anhidraz Aktivitesi Yanıtları

Year 2016, Volume: 44 Issue: 4, 515 - 523, 01.11.2016

Yeliz Demir Ertan Oruç Ahmet Topal

Abstract

A ğır metaller toprak, hava, deniz ve tatlı sularda önemli kirleticilerdir. Balık dokularında toksik etkilere neden olurlar. Bu çalışma, kroma Cr3+ maruz kalmış kahverengi yavru alabalık karaciğer ve solungaç dokularında karbonik anhidraz CA enzim aktivitesindeki değişiklikleri ve histolojik etkileri belirlemek amacıyla yapıldı. Balık 24, 48 ve 96 saat için 1 mg/L ve 2 mg/L derişimlerde kroma maruz bırakıldı. CA iki derişimde, 48 ve 96 saat’ta önemli bir şekilde inhibe olduğu bulundu p

Keywords

Karbonik anhidraz, histopatoloji, karaciğer, solungaçlar, krom

References

1. Y.B. Koca, S. Koca, S. Yıldız, B. Gurcu, E. Osanc, O. Tuncbas, G. Aksoy, Investigation of histopathological and cytogenetic effects on Lepomis gibbosus (Pisces: Perciformes) in the çine stream (Aydın/Turkey) with determination of water pollution, Environ. Toxicol., 20 (2005) 560-571.
2. A.G. Heath, Water Pollution and Fish Physiology, CRC Press, Florida, USA, (1987) 245.
3. G. Atli, Ö. Alptekin, S. Tükel, M. Canli, Response of catalase activity to Ag+, Cd2+, Cr6+, Cu2+ and Zn2+ in five tissues of freshwater fish Oreochromis niloticus, Comp. Biochem. Phys. C., 143 (2006) 218-224.
4. A. Viarengo, Biochemical effects of trace metals, Mar. Pollut. Bull., 16 (1985) 153-158.
5. E.D. Kaya, H. Soyut, S. Beydemir, Carbonic anhydrase activity from the gilthead sea bream (Sparus aurata) liver: The toxicological effects of heavy metals, Environ. Toxicol. Pharmacol., 36 (2013) 514-521.
6. D. Steinhagen, T. Helmus, S. Maurer, R.D. Michael, W. Leibold, J.P. Scharsack, A. Skouras, H.J. Schuberth, Effect of hexavalent carcinogenic chromium on carp Cyprinus carpio immune cells, Dis. Aquat. Org., 62 (2004) 155-161.
7. V. Velma, P.B. Tchounwou, Oxidative stress and DNA damage induced by chromium in liver and kidney of goldfish, Carassius auratus, Biomark, Insights., 25 (2013) 43-51.
8. J.W. Moore, Chromium. In: Inorganic contaminants of surface water: Research and monitoring priorities, New York, NY, Springer-Verlag New York Inc., (1991) 83–97.
9. V. Velma, P.B. Tchounwou, Chromium-induced biochemical, genotoxic and histopathologic effects in liver and kidney of goldfish, Carassius auratus, Mutat. Res., 30 (2010) 43-51.
10. P.S. Rainbow, S.L. White, Comparative accumulating of cobalt by three crustaceans: a decapod, an amphipod and a barnace, Aquat. Toxicol., 16 (1990) 113-126.
11. C.C.C. Cerqueira, M.N. Fernandes, Gill tissue recovery after copper exposure and blood parameter responses in the tropical fish, Prochilodus scrofa. Ecotoxicol. Environ. Saf., 52 (2002) 83-91.
12. M.N. Fernandes, A.F. Mazon, Environmental pollution and fish gill morphology. In: Val AL, Kapoor B.G. (Eds.), Fish Adaptations, Science Publishers, Enfield, (2003) 203–231.
13. D. Ekinci, S. Beydemir, O.I. Kufrevioglu, In vitro inhibitory effects of some heavy metals on human erythrocyte carbonic anhydrases, J. Enzyme Inhib. Med. Chem., 22 (2007) 745-750.
14. H. Soyut, S. Beydemir, Purification and some kinetic properties of carbonic anhydrase from rainbow trout (Oncorhynchus mykiss) liver and metal inhibition, Protein Peptide Lett., 15 (2008) 528-535.
15. H.A. Alici, D. Ekinci, S. Beydemir, Intravenous anesthetics inhibit human paraoxonase-1 (PON1) activity in vitro and in vivo. Clin. Bioch., 41 (2008) 1384-1390.
16. D. Ekinci, S. Beydemir, Evaluation of the impacts of antibiotic drugs on PON 1; a major bioscavenger against cardiovascular diseases, Eur. J. Pharmacol., 617 (2009) 84-89.
17. M. Senturk, D. Ekinci, H.A. Alici, S. Beydemir, Paraoxonase-1, an organophosphate detoxifier and cardioprotective enzyme, is inhibited by anesthetics: An in vitro and in vivo insight, Pest. Biochem. Physiol., 101 (2011) 206-211.
18. H. Soyut, S. Beydemir, S.B. Ceyhun, O. Erdogan, E.D. Kaya, Changes in carbonic anhydrase activity and gene expression of Hsp70 in rainbow trout (Oncorhynchus mykiss) muscle after exposure to some metals, Turk J. Vet. Anim. Sci., 36 (2012) 499- 508.
19. H. Soyut, S. Beydemir, The impact of heavy metals on the activity of carbonic anhydrase from rainbow trout (Oncorhynchus mykiss) kidney, Toxicol. Ind. Health., 28 (2012) 296-305.
20. H. Soyut, E.D. Kaya, S. Beydemir, Impact of antibacterial drugs on human serum paraoxonase-1 (hPON1) activity: an in vitro study, Asian Pac. J. Trop. Biomed., 4 (2014) 603-609.
21. C. Turkes, H. Soyut, S. Beydemir, Effect of calcium channel blockers on paraoxonase-1 (PON1) activity and oxidative stress, Pharmacol. Rep., 66 (2014) 74- 78.
22. C. Turkes, H. Soyut, S. Beydemir, Human serum paraoxonase-1 (hPON1): In vitro inhibition effects of moxifloxacin hydrochloride, levofloxacin hemihidrate, cefepime hydrochloride, cefotaxime sodium, and ceftizoxime sodium, J. Enzyme Inhib. Med. Chem., 30 (2015) 622–628.
23. E.D. Kaya, H. Soyut, S. Beydemir, The toxicological impacts of some heavy metals on carbonic anhydrase from gilthead sea bream (Sparus aurata) gills, Environ. Toxicol. Pharmacol., 39 (2015) 825-832.
24. S. Sender, K. Bottcher, Y. Cetin, G. Gros, Carbonic anhydrase in the gills of seawater- and freshwateracclimated flounders Platichthys flesus: Purification, characterization, and immunohistochemical localization, J. Histochem. Cytochem., 47 (1999) 43- 50.
25. A.M. Vitale, J.M. Monserrat, P. Castilho, E.M. Rodriguez, Inhibitory effects of cadmium on carbonic anhydrase activity and ionic regulation of the estuarine crab Chasmagnathus granulata (Decapoda, Grapsidae). Comp. Biochem. Physiol. C., 122 (1999) 121-129.
26. M.G. Lionetto, M.E. Giordano, S. Vilella, T. Schettino, Inhibition of enzymatic activities by cadmium, Aquat. Toxicol., 48 (2000) 561-571.
27. H. Tohse, Y. Mugiya, Effect of enzyme and anion transport inhibitors on in vitro incorporation of inorganic carbon and calcium into endolymph and otoliths in Salmon (Oncorhynhus masou), Comp. Biochem. Physiol. A., 128 (2001) 177-184.
28. S. Kolayli, F. Karahalil, H. Sahin, B. Dincer, C.T. Supuran, Characterization and inhibition studies of an -carbonic anhydrase from the endangered sturgeon species Acipenser gueldenstaedti, J. Enzyme Inhib. Med. Chem., 26 (2011) 440-444.
29. D. Erdem, E. Yerlikaya, S.B. Ceyhun, R. Demirdag, M. Sentürk, O. Erdogan, O.I. Kufrevioglu, Inhibition effect of some sulfonamides on carbonic anhydrase from european seabass (Dicentrachus labrax), Hacettepe J. Biol. Chem., 39 (2011) 139-144.
30. S.B. Ceyhun, M. Sentürk, E. Yerlikaya, O. Erdogan, O.I. Kufrevioglu, D. Ekinci, Purification and characterization of carbonic anhydrase from the teleost fish Dicentrarchuslabrax (Europeanseabass) liver and toxicological effects of metals on enzyme activity, Environ. Toxicol. Pharmacol., 32 (2011) 69-74.
31. D.G. Stevens, G.A. Chapman, Toxicity of trivalent chromium to early life stages of steelhead trout, Environ. Toxicol. Chem., 3 (1984) 125-133.
32. K.M. Wilbur, N.G. Anderson, Electrometric and colorimetric determination of carbonic anhydrase, J. Biol. Chem., 176 (1948) 147-154.
33. S. De Mora, S.W. Fowler, E. Wyse, S. Azemard, Distribution of heavy metals in marine bivalves, fish and coastal sediments in the Gulf and Gulf of Oman, Mar. Pollut. Bull., 49 (2004) 410-424.
34. H. Hwang, P.G. Green, R.M. Higashi, T.M. Young, Tidal salt marsh sediment in California, USA. Part 2: occurrence and anthropogenic input of trace metals, Chemosphere, 64 (2006) 1899-1909.
35. A. Cicek, A.S. Koparal, Lead, chromium, and cadmium levels in cyprinus carpio and barb plebejus living in the badger dam lake, Turk J. Environ. Conserv., 39 (2001) 3-6.
36. E.F. Kayhan, Bioaccumulate and toxicity of cadmium in seafood, E. U. J. Fish. Aquat. Sci., 23 (2006) 215- 220.
37. Cicik B. The effects on metal accumulation in the liver, gill and muscle tissues of carp (Cyprinus carpio L.) of copper-zinc interaction, Turk J Environ Ecol. 2003;48:32-36.
38. E. Capkin, S. Birincioglu, I. Altinok, Histopathological changes in rainbow trout (Oncorhynchus mykiss) after exposure to sublethal composite nitrogen fertilizers, Ecotoxicol. Environ. Saf., 72 (2009) 1999-2004.
39. J. Mallatt, Fish gill structural changes induced by toxicants and other irritants: a statistical review, Can. J. Fish. Aquat. Sci., 42 (1985) 630-648.
40. D.E. Hinton, D.J. Lauren, Liver structural alterations accompanying chronic toxicity in fishes: potential biomarkers of exposure. In: Biomarkers of Environmental Contaminations. (ed. by J.F. McCarthy, L.R. Shugart), Lewis Publisher, Boca Raton, FL (1990) 17-57.
41. M.M.P. Camargo, C.B.R. Martinez, Histopathology of gills, kidney and liver of a Neotropical fish caged in an urban stream, Neotrop. Ichthyol., 5 (2007) 327-336.
42. J.C. Van Dyk, G.M. Pietersea, J.H. Van Vurena, Histological changes in the liver of Oreochromis mossambicus (Cichlidae) after exposure to cadmium and zinc, Ecotoxicol. Environ. Saf., 66 (2007) 432-40.
43. M. Suiçmez, M. Kayım, D. Köseoğlu, E. Hasdemir, Toxic effects of lead on the liver and gills of oncorhynchus mykiss WALBAUM 1792, Bull. Environ. Contam. Toxicol., 77 (2006) 551-558.
44. H.V. Ghate, L. Mulherkar, Histological changes in the gills of two freshwater prawn species exposed to copper sulphate, Ind. J. Exp. Biol., 17 (1979) 838-840.
45. P. Peebua, M. Kruatrachue, P. Pokethitiyook, S. Singhakaew, Histopathological alterations of Nile tilapia, Oreochromis niloticus in acute and subchronic alachlor exposure, J. Environ. Biol., 29 (2008) 325- 331.
46. E.I. Cengiz, Gill and kidney histopathology in the freshwater fish Cyprinus carpio after acute exposure to deltamethrin, Environ. Toxicol. Pharmacol., 22 (2006) 200-204.
47. G. Alak, M. Atamanalp, A. Topal, H. Arslan, E. Oruç, S. Altun, Histopathological and biochemical effects of humic acid against cadmium toxicity in brown trout gills and muscles, Turk J. Fish. Aquat. Sci., 13 (2013) 315-320.
48. I. Gulcin, S. Beydemir, O. Hisar, Effect of alphatocopheroloil antioxidant enzyme activities and lipid peroxidation in rainbow trout (Oncorhynchus mykiss), Acta Vet. Hung., 53 (2005) 425-433.
49. K. Bottcher, A. Waheed, W.S. Sly, Membraneassociated carbonic anhydrase from the crab gill: Purification, characterization, and comparison with mammalian Cas, Arch. Biochem. Biophys., 312 (1994) 429-435.
50. S.R. Krungkrai, N. Suraveratum, S. Rochanakij, J. Krungkrai, Characterization of carbonic anhydrase in Plasmodium falciparium, Int. J. Parasıtol., 31 (2001) 661-668.
51. S. Beydemir, M. Bulbul, O. Hisar, H. Soyut, T. Yanik, Carbonic anhydrase: affinity purification and kinetic properties from rainbow trout lens, Int. J. Appl. Chem., 2 (2006) 45-55.
52. Y. Zhenyan, X. Liping, L. Seunghwan, Z.A. Rongqing, Novel carbonic anhydrase from the mantle of the pearl oyster (Pinctada fucata), Comp. Biochem. Physiol. B., 143 (2006) 190-194.
53. R.P. Henry, Multiple roles of carbonic anhydrase in cellular transport and metabolism, Annu. Rev. Physiol., 58 (1996) 523-538.
54. C.T. Supuran, Carbonic anhydrases: catalytic and inhibition mechanisms, distribution and physiological roles. In: Supuran CT, Conway J, Smith HJ (Eds.), Carbonic Anhydrase. Its Inhibitors and Activators. CRC Press, London, (2004) 1–23.
55. H. Soyut, S. Beydemir, O. Hisar, Effects of some metals on carbonic anhydrase from brains of rainbow trout, Biol. Trace Elem. Res., 123 (2008) 179-190.

There are 55 citations in total.

Details

Primary Language	English
Journal Section	Research Article
Authors	Yeliz Demir This is me Ertan Oruç This is me Ahmet Topal This is me
Publication Date	November 1, 2016
Published in Issue	Year 2016 Volume: 44 Issue: 4

Cite

APA	Demir, Y., Oruç, E., & Topal, A. (2016). Carbonic Anhydrase Activity Responses and Histopathological Changes in Gill and Liver Tissues after Acute Exposure to Chromium in Brown Trout Juveniles. Hacettepe Journal of Biology and Chemistry, 44(4), 515-523.
AMA	Demir Y, Oruç E, Topal A. Carbonic Anhydrase Activity Responses and Histopathological Changes in Gill and Liver Tissues after Acute Exposure to Chromium in Brown Trout Juveniles. HJBC. November 2016;44(4):515-523.
Chicago	Demir, Yeliz, Ertan Oruç, and Ahmet Topal. “Carbonic Anhydrase Activity Responses and Histopathological Changes in Gill and Liver Tissues After Acute Exposure to Chromium in Brown Trout Juveniles”. Hacettepe Journal of Biology and Chemistry 44, no. 4 (November 2016): 515-23.
EndNote	Demir Y, Oruç E, Topal A (November 1, 2016) Carbonic Anhydrase Activity Responses and Histopathological Changes in Gill and Liver Tissues after Acute Exposure to Chromium in Brown Trout Juveniles. Hacettepe Journal of Biology and Chemistry 44 4 515–523.
IEEE	Y. Demir, E. Oruç, and A. Topal, “Carbonic Anhydrase Activity Responses and Histopathological Changes in Gill and Liver Tissues after Acute Exposure to Chromium in Brown Trout Juveniles”, HJBC, vol. 44, no. 4, pp. 515–523, 2016.
ISNAD	Demir, Yeliz et al. “Carbonic Anhydrase Activity Responses and Histopathological Changes in Gill and Liver Tissues After Acute Exposure to Chromium in Brown Trout Juveniles”. Hacettepe Journal of Biology and Chemistry 44/4 (November 2016), 515-523.
JAMA	Demir Y, Oruç E, Topal A. Carbonic Anhydrase Activity Responses and Histopathological Changes in Gill and Liver Tissues after Acute Exposure to Chromium in Brown Trout Juveniles. HJBC. 2016;44:515–523.
MLA	Demir, Yeliz et al. “Carbonic Anhydrase Activity Responses and Histopathological Changes in Gill and Liver Tissues After Acute Exposure to Chromium in Brown Trout Juveniles”. Hacettepe Journal of Biology and Chemistry, vol. 44, no. 4, 2016, pp. 515-23.
Vancouver	Demir Y, Oruç E, Topal A. Carbonic Anhydrase Activity Responses and Histopathological Changes in Gill and Liver Tissues after Acute Exposure to Chromium in Brown Trout Juveniles. HJBC. 2016;44(4):515-23.

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