In vivo changes in carbonic anhydrase activity and histopathology of gill and liver tissues after acute exposure to chlorpyrifos in rainbow trout

Topal, Ahmet; Atamanalp, Muhammed; Oruç, Ertan; Demir, Yeliz; Beydemir, Şükrü; Işık, Alparslan

doi:10.2478/10004-1254-65-2014-2547

Abstract

Chlorpyrifos is an organophosphate pesticide widely used in agriculture and aquaculture. This study investigated its effects on carbonic anhydrase (CA) enzyme activity and histopathology of rainbow trout gill and liver. The fish were exposed to 2.25 (25 % of 96 h LC₅₀), 4.5 (50 % of 96 h LC₅₀), and 6.75 μg L^-1 (75 % of 96 h LC₅₀) of chlorpyrifos for 24, 48, 72, and 96 h. CA activity was measured in liver and gills and histopathological changes were examined by light microscopy. The most common liver changes at most of the chlorpyrifos concentrations were hyperaemia and degenerative changes. Gill tissues were characterised by lamellar hyperaemia, lamellar oedemas, clumping, cellular degeneration, hyperplasia, and lamellar atrophy. CA enzyme activity in the gills decreased at all concentrations at 48, 72, and 96 h after exposure to chlorpyrifos (p<0.05). Similarly, there was a time-dependent decrease in CA activity at all of the concentrations in liver tissues (p<0.05). The present study indicated that chlorpyrifos inhibits CA enzyme activity and causes histopathological damage in gill and liver tissues

References

1. Narra MR. Tissue-specific recovery of oxidative and antioxidant effects of chlorpyrifos in the freshwater crab, Barytelphusa guerini. Arch Environ Contam Toxicol 2014;67:158-66. doi: 10.1007/s00244-014-0010-110.1007/s00244-014-0010-124595736
Search in Google Scholar
2. Qin G, Liu T, Guo Y, Zhang X, Ma E, Zhang J. Effects of chlorpyrifos on glutathione S-transferase in migratory locust, Locusta migratoria. Pestic Biochem Physiol 2014;109:1-5. doi: 10.1016/j.pestbp.2013.12.00810.1016/j.pestbp.2013.12.00824581378
Search in Google Scholar
3. Fu Y, Li M, Liu C, Qu JP, Zhu WJ, Xing HJ, Xu SW, Li S. Effect of atrazine and chlorpyrifos exposure on cytochrome P450 contents and enzyme activities in common carp gills. Ecotoxicol Environ Saf 2013;94:28-36. doi: 10.1016/j. ecoenv.2013.04.018
Search in Google Scholar
4. Ismail M, Khan QM, Ali R, Ali T, Mobeen A. Genotoxicity of chlorpyrifos in freshwater fish Labeo rohita using Alkaline Single-Cell Gel Electrophoresis (Comet) assay. Drug Chem Toxicol 2014;37:466-71. doi: 10.3109/01480545.2014.88709310.3109/01480545.2014.88709324524247
Search in Google Scholar
5. Khalil F, Kang IJ, Undap S, Tasmin R, Qiu X, Shimasaki Y, Oshima Y. Alterations in social behavior of Japanese medaka (Oryzias latipes) in response to sublethal chlorpyrifos exposure. Chemosphere 2013;92:125-30. doi: 10.1016/j. chemosphere.2013.02.042
Search in Google Scholar
6. Mishra A, Devi Y. Histopathological alterations in the brain (optic tectum) of the freshwater teleost Channa punctatus in response to acute and subchronic exposure to the pesticide Chlorpyrifos. Acta Histochem 2014;116:176-81. doi: 10.1016/j.acthis.2013.07.00110.1016/j.acthis.2013.07.00123948667
Search in Google Scholar
7. Salazar-Lugo R, Mata C, Oliveros A, Rojas LM, Lemus M, Villarroel E. Histopathological changes in gill, liver and kidney of neotropical fish Colossoma macropomum exposed to paraquat at different temperatures. Environ Toxicol Pharmacol 2011;31: 490-5. doi: 10.1016/j.etap.2011.02.00210.1016/j.etap.2011.02.00221787721
Search in Google Scholar
8. Uner N, Oruç EÖ, Sevgiler Y, Sahin N, Durmaz H, Usta D. Effects of diazinon on acetylcholinesterase activity and lipid peroxidation in the brain of Oreochromis niloticus. Environ Toxicol Pharmacol 2006;21:241-5. doi: 10.1016/j. etap.2005.08.007
Search in Google Scholar
9. Demirdağ R, Yerlikaya E, Aksakal E, Küfrevioğlu OI, Ekinci D. Influence of pesticides on the pH regulatory enzyme, carbonic anhydrase, from European Seabass liver and bovine erythrocytes. Environ Toxicol Pharmacol 2012;34:218-22. doi: 10.1016/j.etap.2012.04.00710.1016/j.etap.2012.04.00722561108
Search in Google Scholar
10. Ma J, Liu Y, Niu D, Li X. Effects of chlorpyrifos on the t r a n s c r i p t i o n o f C Y P 3 A c D N A , a c t i v i t y o f acetylcholinesterase, and oxidative stress response of goldfish (Carassius auratus). Environ Toxicol 2013; Epub Nov 4 doi: 10.1002/tox.2191810.1002/tox.2191824190793
Search in Google Scholar
11. Kokushi E, Uno S, Pal S, Koyama J. Effects of chlorpyrifos on the metabolome of the freshwater carp, Cyprinus carpio. Environ Toxicol 2013; Epub Aug 30 doi: 10.1002/tox.2190310.1002/tox.2190323997021
Search in Google Scholar
12. Xing H, Li S, Wang Z, Gao X, Xu S, Wang X. Oxidative stress response and histopathological changes due to atrazine and chlorpyrifos exposure in common carp. Pestic Biochem P h y s i o l 2 0 1 2 ; 1 0 3 : 7 4 - 8 0 . d o i : 1 0 . 1 0 1 6 / j . chemosphere.2012.02.049
Search in Google Scholar
13. Xing H, Li S, Wang Z, Gao X, Xu S, Wang X. Histopathological changes and antioxidant response in brain and kidney of common carp exposed to atrazine and chlorpyrifos. Chemosphere 2012;88:377-83. doi: 10.1016/j. chemosphere.2012.02.049
Search in Google Scholar
14. Kavitha P, Rao JV. Toxic effects of chlorpyrifos on antioxidant enzymes and target enzyme acetylcholinesterase interaction in mosquito fish, Gambusia affinis. Environ Toxicol Pharmacol 2008;26:192-8. doi: 10.1016/j. etap.2008.03.010
Search in Google Scholar
15. Ali D, Nagpure NS, Kumar S, Kumar R, Kushwaha B, Lakra WS. Assessment of genotoxic and mutagenic effects of chlorpyrifos in freshwater fish Channa punctatus (Bloch) using micronucleus assay and alkaline single-cell gel electrophoresis. Food Chem Toxicol 2009;47:650-6. doi: 10.1016/j.fct.2008.12.02110.1016/j.fct.2008.12.02119141310
Search in Google Scholar
16. Tilton FA, Tilton SC, Bammler TK, Beyer RP, Stapleton PL, Scholz NL, Gallagher EP. Transcriptional impact of organophosphate and metal mixtures on olfaction: copper dominates the chlorpyrifos-induced response in adult zebrafish. Aquat Toxicol 2011;102:205-15. doi: 10.1016/j. aquatox.2011.01.012
Search in Google Scholar
17. Ural MS. Chlorpyrifos-induced changes in oxidant/ antioxidant status and haematological parameters of Cyprinus carpio: Ameliorative effect of lycopene. Chemosphere 2013;90:2059-64. doi: 10.1016/j. chemosphere.2012.12.006
Search in Google Scholar
18. Ferrari A, Venturino A, Pechén de D’Angelo AM. Muscular and brain cholinesterase sensitivities to azinphos methyl and carbaryl in the juvenile rainbow trout Oncorhynchus mykiss. Comp Biochem Physiol C Toxicol Pharmacol. 2007;146:308-13. doi: 10.1016/j.cbpc.2007.04.00210.1016/j.cbpc.2007.04.00217509940
Search in Google Scholar
19. Ozaki A, Sakamoto T, Khoo S, Nakamura K, Coimbra MRM, Akutsu T, Okamoto N. Quantitative trait loci (QTLs) associated with resistance/susceptibility to infectious pancreatic necrosis virus (IPNV) in rainbow trout (Oncorhynchus mykiss). Mol Gen Genomics 2001;265:23-31. PMID: 1137086910.1007/s00438000039211370869
Search in Google Scholar
20. Balaydın HT, Soyut H, Ekinci D, Göksu S, Beydemir S, M e n z e k A , S a h i n E . S y n t h e s i s a n d c a r b o n i c anhydraseinhibitory properties of novel bromophenols including natural products. J Enzyme Inhib Med Chem 2012;27:43-50. doi: 10.3109/14756366.2011.57413110.3109/14756366.2011.574131
Search in Google Scholar
21. Postel R, Sonnenberg A. Carbonic anhydrase 5 regulates acid-base homeostasis in zebrafish. PLoS One 2012;7(6):e39881. doi: 10.1371/journal.pone.003988110.1371/journal.pone.0039881
Search in Google Scholar
22. Çoban TA, Beydemir S, Gülçin I, Ekinci D. Morphine inhibits erythrocyte carbonic anhydrase in vitro and in vivo. Biol Pharm Bull 2007;30:2257-61. doi: 10.1248/bpb.30.225710.1248/bpb.30.2257
Search in Google Scholar
23. Doğan S. The in vitro effects of some pesticides on carbonic anhydrase activity of Oncorhynchus mykiss and Cyprinus carpio fish. J Hazard Mater 2006;132:171-6. doi:10.1016/j. jhazmat.2005.10.006
Search in Google Scholar
24. Kaya ED, Söyüt H, Beydemir S. Carbonic anhydrase activity from the gilthead seabream (Sparus aurata) liver: The toxicological effects of heavy metals. Environ Toxicol Pharmacol 2013;36:514-21. doi: 10.1016/j.etap.2013.05.01910.1016/j.etap.2013.05.019
Search in Google Scholar
25. Capkin E, Birincioglu S, Altinok I. Histopathological changes in rainbow trout (Oncorhynchus mykiss) after exposure to sublethal composite nitrogen fertilizers. Ecotoxicol Environ Saf 2009;72:1999-2004. doi: 10.1016/j.ecoenv.2009.05.00710.1016/j.ecoenv.2009.05.007
Search in Google Scholar
26. U.S. Environmental Protection Agency (US EPA). Ambient water quality criteria for chlorpyrifos - 1986. Washington (DC): US EPA; 1986.
Search in Google Scholar
27. Wilbur KM, Anderson NG. Electrometric and colorimetric determination of carbonic anhydrase. J Biol Chem 1948;176:147-54. PMID: 1888615210.1016/S0021-9258(18)51011-5
Search in Google Scholar
28. Ghorashi S, Shajeei H, Vaezi G, Shamoushaki MMN, Babakhani A. Histopathological studies on kidneys and gills of Onchorhynchus mykiss exposed to sublethal concentration P h y s i o l 2 0 1 2 ; 1 0 3 : 7 4 - 8 0 . d o i : 1 0 . 1 0 1 6 / j . chemosphere.2012.02.049
Search in Google Scholar
13. Xing H, Li S, Wang Z, Gao X, Xu S, Wang X. Histopathological changes and antioxidant response in brain and kidney of common carp exposed to atrazine and chlorpyrifos. Chemosphere 2012;88:377-83. doi: 10.1016/j. chemosphere.2012.02.049
Search in Google Scholar
14. Kavitha P, Rao JV. Toxic effects of chlorpyrifos on antioxidant enzymes and target enzyme acetylcholinesterase interaction in mosquito fish, Gambusia affinis. Environ Toxicol Pharmacol 2008;26:192-8. doi: 10.1016/j. etap.2008.03.010
Search in Google Scholar
15. Ali D, Nagpure NS, Kumar S, Kumar R, Kushwaha B, Lakra WS. Assessment of genotoxic and mutagenic effects of chlorpyrifos in freshwater fish Channa punctatus (Bloch) using micronucleus assay and alkaline single-cell gel electrophoresis. Food Chem Toxicol 2009;47:650-6. doi: 10.1016/j.fct.2008.12.02110.1016/j.fct.2008.12.02119141310
Search in Google Scholar
16. Tilton FA, Tilton SC, Bammler TK, Beyer RP, Stapleton PL, Scholz NL, Gallagher EP. Transcriptional impact of organophosphate and metal mixtures on olfaction: copper dominates the chlorpyrifos-induced response in adult zebrafish. Aquat Toxicol 2011;102:205-15. doi: 10.1016/j. aquatox.2011.01.012
Search in Google Scholar
17. Ural MS. Chlorpyrifos-induced changes in oxidant/ antioxidant status and haematological parameters of Cyprinus carpio: Ameliorative effect of lycopene. Chemosphere 2013;90:2059-64. doi: 10.1016/j. chemosphere.2012.12.006
Search in Google Scholar
18. Ferrari A, Venturino A, Pechén de D’Angelo AM. Muscular and brain cholinesterase sensitivities to azinphos methyl and carbaryl in the juvenile rainbow trout Oncorhynchus mykiss. Comp Biochem Physiol C Toxicol Pharmacol. 2007;146:308-13. doi: 10.1016/j.cbpc.2007.04.00210.1016/j.cbpc.2007.04.00217509940
Search in Google Scholar
19. Ozaki A, Sakamoto T, Khoo S, Nakamura K, Coimbra MRM, Akutsu T, Okamoto N. Quantitative trait loci (QTLs) associated with resistance/susceptibility to infectious pancreatic necrosis virus (IPNV) in rainbow trout (Oncorhynchus mykiss). Mol Gen Genomics 2001;265:23-31. PMID: 1137086910.1007/s004380000392
Search in Google Scholar
20. Balaydın HT, Soyut H, Ekinci D, Göksu S, Beydemir S, M e n z e k A , S a h i n E . S y n t h e s i s a n d c a r b o n i c anhydraseinhibitory properties of novel bromophenols including natural products. J Enzyme Inhib Med Chem 2012;27:43-50. doi: 10.3109/14756366.2011.57413110.3109/14756366.2011.574131
Search in Google Scholar
21. Postel R, Sonnenberg A. Carbonic anhydrase 5 regulates acid-base homeostasis in zebrafish. PLoS One 2012;7(6):e39881. doi: 10.1371/journal.pone.003988110.1371/journal.pone.0039881
Search in Google Scholar
22. Çoban TA, Beydemir S, Gülçin I, Ekinci D. Morphine inhibits erythrocyte carbonic anhydrase in vitro and in vivo. Biol Pharm Bull 2007;30:2257-61. doi: 10.1248/bpb.30.225710.1248/bpb.30.2257
Search in Google Scholar
23. Doğan S. The in vitro effects of some pesticides on carbonic anhydrase activity of Oncorhynchus mykiss and Cyprinus carpio fish. J Hazard Mater 2006;132:171-6. doi:10.1016/j. jhazmat.2005.10.006
Search in Google Scholar
24. Kaya ED, Söyüt H, Beydemir S. Carbonic anhydrase activity from the gilthead seabream (Sparus aurata) liver: The toxicological effects of heavy metals. Environ Toxicol Pharmacol 2013;36:514-21. doi: 10.1016/j.etap.2013.05.01910.1016/j.etap.2013.05.019
Search in Google Scholar
25. Capkin E, Birincioglu S, Altinok I. Histopathological changes in rainbow trout (Oncorhynchus mykiss) after exposure to sublethal composite nitrogen fertilizers. Ecotoxicol Environ Saf 2009;72:1999-2004. doi: 10.1016/j.ecoenv.2009.05.00710.1016/j.ecoenv.2009.05.007
Search in Google Scholar
26. U.S. Environmental Protection Agency (US EPA). Ambient water quality criteria for chlorpyrifos - 1986. Washington (DC): US EPA; 1986.
Search in Google Scholar
27. Wilbur KM, Anderson NG. Electrometric and colorimetric determination of carbonic anhydrase. J Biol Chem 1948;176:147-54. PMID: 1888615210.1016/S0021-9258(18)51011-5
Search in Google Scholar
28. Ghorashi S, Shajeei H, Vaezi G, Shamoushaki MMN, Babakhani A. Histopathological studies on kidneys and gills of Onchorhynchus mykiss exposed to sublethal concentration trout, Oncorhynchus mykiss. Tissue Cell 2010;42:158-64. doi: 10.1016/j.tice.2010.03.00410.1016/j.tice.2010.03.00420430411
Search in Google Scholar
37. Pal S, Kokushi E, Koyama J, Uno S, Ghosh AR. Histopathological alterations in gill, liver and kidney of common carp exposed to chlorpyrifos. J Environ Sci Health B 2012;47:180-95. doi: 10.1080/03601234.2012.63228510.1080/03601234.2012.63228522375590
Search in Google Scholar
38. Kaya H, Çelik EŞ, Gürkan M, Yılmaz S, Akbulut M. Effects of subchronic exposure to phosalone on oxidative stress and histopathological alterations in common carp (Cyprinus carpio, L., 1758). J Toxicol Environ Health A 2013;76:853-64. doi: 10.1080/15287394.2013.82313610.1080/15287394.2013.82313624053362
Search in Google Scholar
39. del Carmen Alvarez M, Fuiman LA. Environmental levels of atrazine and its degradation products impair survival skills and growth of red drum larvae. Aquat Toxicol 2005;74:229-41. doi: org/10.1016/j.aquatox.2005.05.01410.1016/j.aquatox.2005.05.01416009435
Search in Google Scholar
40. Mallatt J. Fish gill structural changes induced by toxicants and other irritants: a statistical review. Can J Fish Aquat Sci 1985;42:630-48. doi: 10.1139/f85-08310.1139/f85-083
Search in Google Scholar
41. Hinton DE, Lauren DJ. Liver structural alterations accompanying chronic toxicity in fishes: potential biomarkers of exposure. In: McCarthy JF, Shugart LR, editors. Biomarkers of environmental contaminations. Boca Raton (FL): Lewis Publisher; 17-57, 1990.
Search in Google Scholar
42. Camargo MMP, Martinez CBR. Histopathology of gills, kidney and liver of a Neotropical fish caged in an urban stream. Neotrop Ichthyol 2007;5:327-36. doi. org/10.1590/ S1679-6225200700030001310.1590/S1679-62252007000300013
Search in Google Scholar
43. Peebua P, Kruatrachue M, Pokethitiyook P, Singhakaew S. Histopathological alterations of Nile tilapia, Oreochromis niloticus in acute and subchronic alachlor exposure. J Environ Biol 2008;29:325-31. PMID: 18972686
Search in Google Scholar
44. Ba-Omar TA, Al-Jardani S, Victor R. Effects of pesticide temephos on the gills of Aphanius dispar (Pisces: Cyprinodontidae). Tissue Cell 2011;43:29-38. doi: 10.1016/j. tice.2010.11.002
Search in Google Scholar

In vivo changes in carbonic anhydrase activity and histopathology of gill and liver tissues after acute exposure to chlorpyrifos in rainbow trout

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