Toxicological effects of some antiparasitic drugs on equine liver glutathione S-Transferase enzyme activity

https://doi.org/10.1016/j.jpba.2019.113048Get rights and content

Highlights

  • The inhibitory effects of ricobendazole, thiabendazole, albendazole and oxfendazole on glutathione s-transferase activity.

  • IC50 values were found; ricobendazole (53.31 μM) < oxfendazole (57.75 μM) < albendazole (63.00 μM) < thiabendazole (69.30 μM).

  • Ricobendazole drug showed the best inhibitory effect with the lowest Ki value.

Abstract

Benzimidazoles are antiparasitic drugs having an extensive application field like agriculture, medicine, and especially in veterinary medicine. In this study, we report the effect of some benzimidazole drugs such as ricobendazole (RBZ), thiabendazole (TBZ), albendazole (ALBA) and oxfendazole (OFZ) on glutathione s-transferase (GST) enzyme activity. The kinetics studies, IC50 and Ki values of the tested drugs on GSTs enzyme activity were investigated. The obtained ranking of IC50 values were found to be approximately RBZ (53.31 μM, r2: 0.9778) < OFZ (57.75 μM, r2: 0.9630) < ALBA (63.00 μM, r2: 0.9443) < TBZ (69.30 μM, r2: 0.9491). And the obtained ranking of Ki values of the tested drugs (RBZ, TBZ, ALBA, and OFZ) for GSTs enzyme activity was found to be approximately 26.37 ± 2.96, 44.01 ± 5.74, 39.82 ± 3.98 and 30.14 ± 3.03 μM, respectively. Experimental results showed that tested the benzimidazoles drugs have some significant inhibitory effect on GSTs enzyme activity. And also, it was determined that RBZ, ALBA, OFZ are competitive inhibition, but TBZ is non-competitive inhibitors on GSTs enzyme activity. RBZ drug showed the best inhibitory effect with the lowest Ki value.

Introduction

Glutathione S-transferase (GSTs: E.C.2.5.1.18) as a multifunctional enzyme catalyzes the first step formation of mercapturic acid that occurs as a final product in the detoxification metabolic process [1,2]. The GSTs enzyme is present in the liver of mammals such as humans, rats, and mice [3,4]. Additionally, GSTs presents in plants, fungi, insects, and bacteria [5]. Mitochondrial, cytosolic and microsomal enzymes are GSTs derivatives, and these enzymes metabolize various electrophilic based chemicals by the conjugation of reduced glutathione [6,7]. The formation of mercapturic acid occurs in the first phase of the conjugation reaction in which the organism can eliminate and inactivate the harmful endobiotic and xenobiotics [8,9]. Additionally, GSTs also play an important role in the detoxification of xenobiotics reaction in prokaryotes [10,11]. The GSTs enzyme has been found to be associated with an increase in bacterial resistance to some antibiotics such as rifampicin and tetracycline [12,13].

Various new benzimidazoles derivatives have been developed, which used for the enhancing of antiparasitic activity and for the change of pharmacokinetic properties [[14], [15], [16]]. The drugs in the benzimidazole class are widely used in the prevention and treatment of parasitic diseases in veterinary medicine [[16], [17], [18], [19]].

Ricobendazole is a compound of the benzimidazole drug class, and also called albendazole sulfoxide. Ricobendazole is a broad spectrum compound that is effectively used against lungworms and nematodes. In some Latin American countries, such as Argentina, an aqueous solution of Ricobendazole is being prepared and used in cattle subcutaneous injections by veterans and farmers [20].

Tiabendazole is a post-harvest pesticide used to control diseases caused by fungi, it may cause cell death by apoptosis of hepatocyte and may cause human death by damaging the liver [21].

Albendazole is used in a variety of experimental and clinical chemotherapy trials of various intestinal and systematic parasitoses. Albendazole is a broad-spectrum anthelmintic approved for human use for the first time in 1982. It is generally used against systematic parasites, only used for intestinal absorption due to its low aqueous solubility. So, long treatments and high doses are used at appropriate concentrations [22,23].

Oxfendazole contains methylcarbamate, and it is a benzimidazole compound [24]. Oxfendazole is a highly effective drug for zoonotic diseases such as fasciolosis, echinococcosis, and cysticercosis. It is also very effective in the treatment of pig cysticercosis [25,26]. Also, oxfendazole is an effective drug that is cheap, has no side effects and is suitable for human use after treatment [27]. Some studies have reported that degradation of some antibiotics (sulfathiazole, ampicillin) has been found in microorganisms receiving GSTs enzyme under specified conditions [28,29]. Normally, the binding of inhibitors to active sites in the GSTs enzyme results in slowing or stopping enzyme activity [30,31]. There are many drugs that can inhibit the GSTs enzyme, and herbicides and pesticides also have an inhibitory effect on the GSTs enzyme. The detection of drugs in biochemical studies as an inhibitor is crucial [14,32]. Our most important goal in this study is to emphasize the use of antiparasitics which can inhibit this enzyme which has a vital role in metabolism. Herein, we investigated in vitro the inhibitory effects of benzimidazole drugs such as ricobendazole, thiabendazole, albendazole and oxfendazole compounds on GSTs enzyme activity, using the 1-chloro-2,4-dinitrobenzene (CDNB) solution as a substrate for GSTs enzyme, respectively Fig. 1.

Section snippets

Chemicals

GSTs enzyme obtained from the equine liver (Sigma-Aldrich G6511, USA) was used for inhibition study. Ricobendazole (RBZ), thiabendazole (TBZ), albendazole (ALBA), oxfendazole (OFZ), glutathione (GSH) and 1-chloro-2,4-dinitrobenzene (CDNB) were purchased from Sigma Aldrich. All glassware used in the experiment were cleaned with purified water.

Results

In this paper, the inhibitory effect of RBZ, TBZ, ALBA, OFZ drugs on GSTs enzyme activity was tested. As detailed below, these benzimidazoles derivatives were investigated for their inhibition properties against GSTs enzymes, and the results showed that these drugs have an impressive effect on the GSTs inhibition. The chemical structures of some benzimidazoles derivatives compounds are shown in Fig. 1. Also, these enzyme inhibiting results of benzimidazoles derivatives compounds are seen in

Discussion

Benzimidazoles (BZMs), a group of heterocyclic compounds, have a fused aromatic imidazole [36]. Benzene ring in the imidazole compound can easily interact with active sites in biological systems via weak interactions such as dipole-ion interactions, hydrophobic interactions, hydrogen bonds, and van der Waals bonds [36,37]. Thanks to this feature, BZMs, and its derivatives can easily be combined with many biological systems. BZMs and its derivatives have been shown to have significant effects on

Conclusion

BZM are antiparasitic drugs and commonly used in various fields such as medicine, agriculture and particularly in veterinary medicine. The experimental results of the tested drugs revealed that BZM derivatives have some significant inhibitory effect on GSTs enzyme activity according to IC50 and Ki values at the micromolar level. These findings are very important because GSTs inhibitors emerge as promising therapy factors for managing the formation of resistance amongst anticancer factors.

Declaration of Competing Interest

The authors declare no conflict of interest.

References (62)

  • L.A. Gomez-Puerta et al.

    Oxfendazole as successful treatment of Taenia hydatigena metacestodes in naturally infected pigs

    Asian Pac. J. Trop. Biomed.

    (2015)
  • L. Moreno et al.

    A high oxfendazole dose to control porcine cysticercosis: pharmacokinetics and tissue residue profiles

    Food Chem. Toxicol.

    (2012)
  • H. Göcer et al.

    Carbonic anhydrase inhibitory properties of phenolic sulfonamides derived from dopamine related compounds

    Arab. J. Chem.

    (2017)
  • W.H. Habig et al.

    Glutathione S transferases. The first enzymatic step in mercapturic acid formation

    J. Biol. Chem.

    (1974)
  • D. de Castro Rodrigues et al.

    Avermectin toxicity in bovines less than thirty days old

    Res. Vet. Sci.

    (2018)
  • M. Song et al.

    Research on the differences between 2-(2-Chlorophenyl)benzimidazole and 2-(4-Chlorophenyl)benzimidazole based on terahertz time domain spectroscopy, Spectrochim

    Acta Part A Mol. Biomol. Spectrosc.

    (2018)
  • A. Yıldırım et al.

    N-Acylsulfonamides strongly inhibit human carbonic anhydrase isoenzymes I and II

    Bioorg. Med. Chem.

    (2015)
  • Y. Özkay et al.

    Antimicrobial activity and a SAR study of some novel benzimidazole derivatives bearing hydrazone moiety

    Eur. J. Med. Chem.

    (2010)
  • M.J. Akhtar et al.

    Synthesis of stable benzimidazole derivatives bearing pyrazole as anticancer and EGFR receptor inhibitors

    Bioorg. Chem.

    (2018)
  • K.M. Amin et al.

    Synthesis and biological evaluation of novel coumarin–pyrazoline hybrids endowed with phenylsulfonyl moiety as antitumor agents

    Eur. J. Med. Chem.

    (2013)
  • J.E. Cheong et al.

    Synthesis and anticancer activity of novel water soluble benzimidazole carbamates

    Eur. J. Med. Chem.

    (2018)
  • D.C. Thienpont et al.

    Mebendazole, a New Potent Drug Against Syngamus Trachea in Turkeys

    Poult. Sci.

    (1973)
  • A. Stepniak et al.

    Study of the interaction of β-cyclodextrin with albendazole in aqueous solutions

    J. Mol. Liq.

    (2017)
  • A. Sevastos et al.

    Glutathione transferase-mediated benzimidazole-resistance in Fusarium graminearum

    Pestic. Biochem. Physiol.

    (2017)
  • I. Gulçin et al.

    Antidiabetic and antiparasitic potentials: inhibition effects of some natural antioxidant compounds on α-glycosidase, α-amylase and human glutathione S-transferase enzymes

    Int. J. Biol. Macromol.

    (2018)
  • J.D. Hayes et al.

    Glutathione transferases

    Annu. Rev. Pharmacol. Toxicol.

    (2005)
  • M. Erat et al.

    Effects of some antibiotics on glutathione reductase activities from human erythrocytes in vitro and from rat erythrocytes in vivo

    J. Enzyme Inhib. Med. Chem.

    (2005)
  • F. Türkan et al.

    The in vivo effects of cefazolin, cefuroxime, and cefoperazon on the carbonic anhydrase in different rat tissues

    J. Biochem. Mol. Toxicol.

    (2018)
  • İ. Gülçin et al.

    The effect of caffeic acid phenethyl ester (CAPE) on metabolic enzymes including acetylcholinesterase, butyrylcholinesterase, glutathione S-transferase, lactoperoxidase, and carbonic anhydrase isoenzymes I, II, IX, and XII

    J. Enzyme Inhib. Med. Chem.

    (2016)
  • F. Türkan et al.

    The effects of some antibiotics from cephalosporin groups on the acetylcholinesterase and butyrylcholinesterase enzymes activities in different tissues of rats

    Arch. Physiol. Biochem.

    (2019)
  • F. Turkan et al.

    Purification and characterization of glutathione s-transferase enzyme from karayemis fruit (laurocerasus officinalis roem.) and the inhibition effects of bazipesticites on enzyme activity

    Mus Alparslan Univ. J. Sci.

    (2014)
  • Cited by (0)

    View full text