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Inhibition effects of some pesticides and heavy metals on carbonic anhydrase enzyme activity purified from horse mackerel (Trachurus trachurus) gill tissues

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Abstract

The gill tissue is the main site of metabolic enzymes or compensation, with the kidney tissue playing a supporting role. At the gill tissue, carbonic anhydrase enzymes (CAs) catalyze the hydration of CO2 to HCO3− and H+ for production to the H2O. In this work, the CA enzyme was purified from horse mackerel (Trachurus trachurus) gill with a specific activity of 21,381.42 EU/mg, purification fold of 150.61, total activity of 2347.68 EU/mL, and a yield of 16.13% using sepharose 4B-L-tyrosine-sulfanilamide affinity gel chromatography. For recording the enzyme purity, gel electrophoresis was performed, and single band was seen. The molecular weight of this enzyme was found approximately 35 kDa. Also, the inhibitory effects of different pesticides such as thiram, clofentezine, propineb, deltamethrin, azoxystrobin, and thiophanate and heavy metal ions such as Fe2+, Cu2+, Co2+, Pb2+ Hg2+, and As3+ on horse mackerel gill tissue CA enzyme activities were investigated. Our results indicated that these pesticides and metal ions showed inhibitory effects at low nanomolar and millimolar concentrations for fish gill CA enzymes, respectively.

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References

  • Abbaci A, Azzouz N, Bouznit Y (2014) A new copper doped montmorillonite modified carbon paste electrode for propineb detection. Appl Clay Sci 90:130–134

    Article  CAS  Google Scholar 

  • Aslan HE, Demir Y, Özaslan MS, Türkan F, Beydemir Ş, Küfrevioğlu ÖI (2018) The behavior of some chalcones on acetylcholinesterase and carbonic anhydrase activity. Drug Chem Toxicol:1–7

  • Atmaca U, Kaya R, Karaman HS, Çelik M, Gülçin İ (2019) Synthesis of oxazolidinone from enantiomerically enriched allylic alcohols and determination of their molecular docking and biologic activities. Bioorg Chem 88:102980

    Article  CAS  Google Scholar 

  • Bayindir S, Caglayan C, Karaman M, Gülcin İ (2019) The green synthesis and molecular docking of novel N-substituted rhodanines as effective inhibitors for carbonic anhydrase and acetylcholinesterase enzymes. Bioorg Chem 103096

  • Bayrak Ç, Taslimi P, Gülçin İ, Menzek A (2017) The first synthesis of 4-phenylbutenone derivative bromophenols including natural products and their inhibition profiles for carbonic anhydrase, acetylcholinesterase and butyrylcholinesterase enzymes. Bioorg Chem 72:359–366

    Article  CAS  Google Scholar 

  • Beydemir Ş, Demir Y (2017) Antiepileptic drugs: impacts on human serum paraoxonase-1. J Biochem Mol Toxicol 31:e21889

    Article  CAS  Google Scholar 

  • Boztas M, Cetinkaya Y, Topal M, Il G, Menzek A, Sahin E, Tanc M, Supuran CT (2014) Synthesis and carbonic anhydrase isoenzymes I, II, IX, and XII inhibitory effects of dimethoxybromophenol derivatives incorporating cyclopropane moieties. J Med Chem 58:640–650

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. AnBio 72:248–254

    CAS  Google Scholar 

  • Burmaoglu S, Yilmaz AO, Polat MF, Kaya R, Gulcin İ, Algul O (2019) Synthesis and biological evaluation of novel tris-chalcones as potent carbonic anhydrase, acetylcholinesterase, butyrylcholinesterase and α-glycosidase inhibitors. Bioorg Chem 85:191–197

    Article  CAS  Google Scholar 

  • Bustaffa E, Stoccoro A, Bianchi F, Migliore L (2014) Genotoxic and epigenetic mechanisms in arsenic carcinogenicity. Arch Toxicol 88:1043–1067

    Article  CAS  Google Scholar 

  • Butler S, Kelly H, Mueller T, Kruger G, Cochran A, Raper T (2018) Influence of droplet size and azoxystrobin insensitivity on frogeye leaf spot management in soybean. Crop Protect 112:149–158

    Article  CAS  Google Scholar 

  • Caglayan C (2019) The effects of naringin on different cyclophosphamide-induced organ toxicities in rats: investigation of changes in some metabolic enzyme activities. Environ Sci Pollut Res:1–10

  • Caglayan C, Gulcin İ (2018) The toxicological effects of some avermectins on goat liver carbonic anhydrase enzyme. J Biochem Mol Toxicol 32:e22010

    Article  CAS  Google Scholar 

  • Caglayan C, Demir Y, Kucukler S, Taslimi P, Kandemir FM, Gulçin İ (2019a) The effects of hesperidin on sodium arsenite-induced different organ toxicity in rats on metabolic enzymes as antidiabetic and anticholinergics potentials: a biochemical approach. J Food Biochem 43:e12720

    Article  CAS  Google Scholar 

  • Caglayan C, Kandemir FM, Yildirim S, Kucukler S, Eser G (2019b) Rutin protects mercuric chloride-induced nephrotoxicity via targeting of aquaporin 1 level, oxidative stress, apoptosis and inflammation in rats. J Trace Elem Med Biol 54:69–78

    Article  CAS  Google Scholar 

  • Ceyhun SB, Şentürk M, Ekinci D, Erdoğan O, Çiltaş A, Kocaman EM (2010) Deltamethrin attenuates antioxidant defense system and induces the expression of heat shock protein 70 in rainbow trout. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 152:215–223

    Google Scholar 

  • Ceyhun SB, Sentürk M, Yerlikaya E, Erdoğan O, Küfrevioğlu Oİ, Ekinci D (2011) Purification and characterization of carbonic anhydrase from the teleost fish Dicentrarchus labrax (European seabass) liver and toxicological effects of metals on enzyme activity. Environ Toxicol Pharmacol 32(1):69–74

    Article  CAS  Google Scholar 

  • Demir Y, Beydemir Ş (2015) Purification, refolding, and characterization of recombinant human paraoxonase-1. Turk J Chem 39:764–776

    Article  CAS  Google Scholar 

  • 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 J Biol Chem 44:515–523

    Google Scholar 

  • Demir Y, Şenol Kotan M, Dikbaş N, Beydemir Ş (2017) Phytase from Weissella halotolerans: purification, partial characterisation and the effect of some metals. Int J Food Prop 20:2127–2137

    CAS  Google Scholar 

  • Erdemir F, Celepci DB, Aktaş A, Gök Y, Kaya R, Taslimi P, Demir Y, Gulçin İ (2019) Novel 2-aminopyridine liganded Pd(II) N-heterocyclic carbene complexes: synthesis, characterization, crystal structure and bioactivity properties. Bioorg Chem 91:103134

    Article  CAS  Google Scholar 

  • Gado AM, Aldahmash BA (2013) Antioxidant effect of Arabic gum against mercuric chloride-induced nephrotoxicity. Drug Des Devel Ther 7:1245

    Article  Google Scholar 

  • Gündoğdu S, Türkeş C, Arslan M, Demir Y, Beydemir Ş (2019) New Isoindole-1,3-dione substituted sulfonamides as potent inhibitors of carbonic anhydrase and Acetylcholinesterase: design, synthesis, and biological evaluation. ChemistrySelect 4(45):13347–13355

    Article  CAS  Google Scholar 

  • Huseynova M, Taslimi P, Medjidov A, Farzaliyev V, Aliyeva M, Gondolova G, Şahin O, Yalçın B, Sujayev A, Orman EB (2018) Synthesis, characterization, crystal structure, electrochemical studies and biological evaluation of metal complexes with thiosemicarbazone of glyoxylic acid. Polyhedron 155:25–33

    Article  CAS  Google Scholar 

  • Jaishankar M, Tseten T, Anbalagan N, Mathew BB, Beeregowda KN (2014) Toxicity, mechanism and health effects of some heavy metals. Interdiscip Toxicol 7:60–72

    Article  CAS  Google Scholar 

  • Jarvis P, Quy K, Macadam J, Edwards M, Smith M (2018) Intake of lead (Pb) from tap water of homes with leaded and low lead plumbing systems. ScTEn 644:1346–1356

    CAS  Google Scholar 

  • Kaya ED, Söyüt H, Beydemir Ş (2013) Carbonic anhydrase activity from the gilthead sea bream (Sparus aurata) liver: the toxicological effects of heavy metals. Environ Toxicol Pharmacol 36:514–521

    Article  CAS  Google Scholar 

  • Khan A, Ahmad L, Khan MZ (2012) Hemato-biochemical changes induced by Pyrethroid insecticides in avian, fish and mammalian species. Int J Agric Biol 14

  • Kirici M, Demir Y, Beydemir S, Atamanalp M (2016) The effect of Al3 and Hg2 on glucose 6-phosphate dehydrogenase from Capoeta Umbla kidney. Appl Ecol Environ Res 14:253–264

    Article  Google Scholar 

  • Kirici M, Turk C, Caglayan C, Kirici M (2017) Toxic effects of copper sulphate pentahydrate on antioxidant enzyme activities and lipid peroxidation of freshwater fish Capoeta umbla (Heckel, 1843) tissues. Appl Ecol Environ Res 15:1685–1696

    Article  Google Scholar 

  • Koksal Z, Kalin R, Gulcin I, Ozdemir H (2018) Inhibitory effects of selected pesticides on peroxidases purified by affinity chromatography. Int J Food Prop 21:385–394

    Article  CAS  Google Scholar 

  • Kose LP, Gülçin İ, Özdemir H, Atasever A, Alwasel SH, Supuran CT (2016) The effects of some avermectins on bovine carbonic anhydrase enzyme. J Enzyme Inhib Med Chem 31:773–778

    Article  CAS  Google Scholar 

  • Krämer W, Schirmer U, Jeschke P, Witschel M (2012) Modern crop protection compounds, 3 volume set, 1. John Wiley & Sons, Hoboken

    Google Scholar 

  • Kucuk M, Gulcin İ (2016) Purification and characterization of the carbonic anhydrase enzyme from Black Sea trout (Salmo trutta Labrax Coruhensis) kidney and inhibition effects of some metal ions on enzyme activity. Environ Toxicol Pharmacol 44:134–139

    Article  CAS  Google Scholar 

  • Kucukoglu K, Gul HI, Taslimi P, Gulcin I, Supuran CT. (2019) Investigation of inhibitory properties of some hydrazone compounds on hCA I, hCA II and AChE enzymes. Bioorg Chem 86:316–321

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680

    Article  CAS  Google Scholar 

  • Manyin T, Rowe CL (2009) Bioenergetic effects of aqueous copper and cadmium on the grass shrimp, Palaemonetes pugio. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 150:65–71

    Google Scholar 

  • Murty AS (1986) Toxicity of pesticides to fish, 2. CRC press Boca Raton, FL, USA

    Google Scholar 

  • Özaslan MS, Demir Y, Aksoy M, Küfrevioğlu ÖI, Beydemir Ş (2018) Inhibition effects of pesticides on glutathione-S-transferase enzyme activity of Van Lake fish liver. J Biochem Mol Toxicol 32:e22196

    Article  CAS  Google Scholar 

  • Öztaskın N, Taslimi P, Maraş A, Gülcin İ, Göksu S (2017) Novel antioxidant bromophenols with acetylcholinesterase, butyrylcholinesterase and carbonic anhydrase inhibitory actions. Bioorg Chem 74:104–114

    Article  CAS  Google Scholar 

  • Öztaşkın N, Kaya R, Maraş A, Şahin E, Gülcin İ, Göksu S (2019) Synthesis and characterization of novel Bromophenols: determination of their anticholinergic, Antidiabetic and antioxidant activities. Bioorg Chem

  • Pari L, Karthikeyan A, Karthika P, Rathinam A (2015) Protective effects of hesperidin on oxidative stress, dyslipidaemia and histological changes in iron-induced hepatic and renal toxicity in rats. Toxicol Rep 2:46–55

    Article  CAS  Google Scholar 

  • Peterson RE, Tu C, Linser PJ (1997) Isolation and characterization of a carbonic anhydrase homologue from the zebrafish (Danio rerio). JMolE 44:432–439

    CAS  Google Scholar 

  • Rai PK (2009) Heavy metal phytoremediation from aquatic ecosystems with special reference to macrophytes. Crit Rev Environ Sci Technol 39:697–753

    Article  CAS  Google Scholar 

  • Sağlık BN, Çevik UA, Osmaniye D, Levent S, Çavuşoğlu BK, Demir Y, Ilgın S, Özkay Y, Koparal AS, Beydemir Ş, Kaplancıklı ZA (2019) Synthesis, molecular docking analysis and carbonic anhydrase I-II inhibitory evaluation of new sulfonamide derivatives. Bioorg Chem 91:103153

    Article  CAS  Google Scholar 

  • Sender S, Böttcher K, Cetin Y, Gros G (1999) Carbonic anhydrase in the gills of seawater-and freshwater-acclimated flounders Platichthys flesus: purification, characterization, and immunohistochemical localization. J Histochem Cytochem 47:43–50

    Article  CAS  Google Scholar 

  • Simonsen LO, Harbak H, Bennekou P (2012) Cobalt metabolism and toxicology—a brief update. ScTEn 432:210–215

    CAS  Google Scholar 

  • Sivaperumal P, Sankar T, Nair PV (2007) Heavy metal concentrations in fish, shellfish and fish products from internal markets of India Vis-a-Vis international standards. Food Chem 102:612–620

    Article  CAS  Google Scholar 

  • Soyut H, Beydemir S (2008) Purification and some kinetic properties of carbonic anhydrase from rainbow trout (Oncorhynchus mykiss) liver and metal inhibition. Protein and peptide letters 15:528–535

    Article  CAS  Google Scholar 

  • Söyüt H, Beydemir Ş (2012) The impact of heavy metals on the activity of carbonic anhydrase from rainbow trout (Oncorhynchus mykiss) kidney. Toxicol Ind Health 28:296–305

    Article  CAS  Google Scholar 

  • Söyüt H, Beydemir Ş, Ceyhun SB, Erdoğan O, Kaya ED (2012) 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 36:499–508

    Google Scholar 

  • Taslimi P, Caglayan C, Gulcin İ (2017) The impact of some natural phenolic compounds on carbonic anhydrase, acetylcholinesterase, butyrylcholinesterase, and α-glycosidase enzymes: an antidiabetic, anticholinergic, and antiepileptic study. J Biochem Mol Toxicol 31:e21995

    Article  CAS  Google Scholar 

  • Taslimi P, Caglayan C, Farzaliyev V, Nabiyev O, Sujayev A, Turkan F, Kaya R, Gulçin İ (2018a) Synthesis and discovery of potent carbonic anhydrase, acetylcholinesterase, butyrylcholinesterase, and α-glycosidase enzymes inhibitors: the novel N, N′-bis-cyanomethylamine and alkoxymethylamine derivatives. J Biochem Mol Toxicol 32:e22042

    Article  CAS  Google Scholar 

  • Taslimi P, Osmanova S, Caglayan C, Turkan F, Sardarova S, Farzaliyev V, Sujayev A, Sadeghian N, Gulçin İ (2018b) Novel amides of 1, 1-bis-(carboxymethylthio)-1-arylethanes: synthesis, characterization, acetylcholinesterase, butyrylcholinesterase, and carbonic anhydrase inhibitory properties. J Biochem Mol Toxicol 32:e22191

    Article  CAS  Google Scholar 

  • Taslimi P, Kandemir FM, Demir Y, İleritürk M, Temel Y, Caglayan C, Gulçin İ (2019) The antidiabetic and anticholinergic effects of chrysin on cyclophosphamide-induced multiple organ toxicity in rats: Pharmacological evaluation of some metabolic enzyme activities. J Biochem Mol Toxicol:e22313

  • Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metal toxicity and the environment, molecular, clinical and environmental toxicology. Springer, Berlin, pp 133–164

    Book  Google Scholar 

  • Topal M, Gülçin İ (2014) Rosmarinic acid: a potent carbonic anhydrase isoenzymes inhibitor. Turk J Chem 38:894–902

    Article  CAS  Google Scholar 

  • Turk E, Kandemir FM, Yildirim S, Caglayan C, Kucukler S, Kuzu M (2019) Protective effect of hesperidin on sodium arsenite-induced nephrotoxicity and hepatotoxicity in rats. Biol Trace Elem Res 189:95–108

    Article  CAS  Google Scholar 

  • Turkan F, Cetin A, Taslimi P, Karaman M, Gulçin İ (2019) Synthesis, biological evaluation and molecular docking of novel pyrazole derivatives as potent carbonic anhydrase and acetylcholinesterase inhibitors. Bioorg Chem 86:420–427

    Article  CAS  Google Scholar 

  • Türkeş C, Arslan M, Demir Y, Çoçaj L, Rifati Nixha A, Beydemir Ş (2019) Synthesis, biological evaluation and in silico studies of novel N-substituted phthalazine sulfonamide compounds as potent carbonic anhydrase and acetylcholinesterase inhibitors. Bioorg Chem 89:103004

    Article  CAS  Google Scholar 

  • Vakonaki E, Androutsopoulos VP, Liesivuori J, Tsatsakis AM, Spandidos DA (2013) Pesticides and oncogenic modulation. Toxicology 307:42–45

    Article  CAS  Google Scholar 

  • Walia S, Sharma RK, Parmar BS (2009) Isolation and simultaneous LC analysis of thiram and its less toxic transformation product in DS formulation. Bull Environ Contam Toxicol 83:363–368

    Article  CAS  Google Scholar 

  • Wilbur KM, Anderson NG (1948) Electrometric and colorimetric determination of carbonic anhydrase. J Biol Chem 176:147–154

    CAS  Google Scholar 

  • Ye C, Zhou Q, Wang X (2008) Determination of thiophanate-methyl and chlorotoluron in water samples by improved single-drop microextraction coupled with high-performance liquid chromatography. Int J Environ Anal Chem 88:461–471

    Article  CAS  Google Scholar 

  • Yousef MI, Awad TI, Mohamed EH (2006) Deltamethrin-induced oxidative damage and biochemical alterations in rat and its attenuation by vitamin E. Toxicology 227:240–247

    Article  CAS  Google Scholar 

  • Zengin M, Genc H, Taslimi P, Kestane A, Guclu E, Ogutlu A, Karabay O, Gulçin İ (2018) Novel thymol bearing oxypropanolamine derivatives as potent some metabolic enzyme inhibitors–their antidiabetic, anticholinergic and antibacterial potentials. Bioorg Chem 81:119–126

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Biochemistry, Faculty of Veterinary Medicine, Bingol University, 12000, Bingol, Turkey

    Cuneyt Caglayan

  2. Department of Biotechnology, Faculty of Science, Bartin University, 74100, Bartin, Turkey

    Parham Taslimi

  3. Department of Fisheries, Genç Vocational School, Bingol University, 12500, Bingol, Turkey

    Cebrahil Türk

  4. Department of Chemistry, Faculty of Science, Atatürk University, 25240, Erzurum, Turkey

    İlhami Gulcin

  5. Department of Biochemistry, Faculty of Veterinary Medicine, Atatürk University, 25240, Erzurum, Turkey

    Fatih Mehmet Kandemir

  6. Department of Pharmacy Services, Nihat Delibalta Göle Vocational High School, Ardahan University, 75700, Ardahan, Turkey

    Yeliz Demir

  7. Department of Biochemistry, Faculty of Pharmacy, Anadolu University, 26210, Eskişehir, Turkey

    Şükrü Beydemir

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  1. Cuneyt Caglayan
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Caglayan, C., Taslimi, P., Türk, C. et al. Inhibition effects of some pesticides and heavy metals on carbonic anhydrase enzyme activity purified from horse mackerel (Trachurus trachurus) gill tissues. Environ Sci Pollut Res 27, 10607–10616 (2020). https://doi.org/10.1007/s11356-020-07611-z

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