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Original article
10 (
3
); 398-402
doi:
10.1016/j.arabjc.2014.08.005

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

, , ,
a Department of Chemistry, Faculty of Science, Atatürk University, 25240-Erzurum, Turkey
b Agri Ibrahim Cecen University, Central Researching Laboratory, 04100-Agri, Turkey
c Department of Zoology, College of Science, King Saud University, Riyadh, Saudi Arabia

⁎Corresponding author. Address: Atatürk University, Faculty of Sciences, Department of Chemistry, TR-25240-Erzurum, Turkey. Tel.: +90 442 2314375; fax: +90 442 2360948. igulcin@atauni.edu.tr (İlhami Gülçin) igulcin@yahoo.com (İlhami Gülçin)

Received: , Accepted: ,
© The Author(s) 2014
Disclaimer:
This article was originally published by Elsevier and was migrated to Scientific Scholar after the change of Publisher.

Peer review under responsibility of King Saud University.

Abstract

The effects of some phenolic sulfonamides were determined on the cytosolic carbonic anhydrase isoenzyme I and II (hCA I and II). Both isoenzymes were purified separately from human erythrocytes, using the Sepharose-4B-l-tyrosine-sulfanilamide affinity column chromatography method. In continuation of the study, we identified the inhibitory effects of phenolic sulfonamides 1–4 on the esterase activity of hCA I, and II. The inhibitory effects of phenolic sulfonamides 1–4 were tested on human carbonic anhydrase isoenzymes hCA I, and II. Among the compounds 1–4, compound 1 was concluded to show the best inhibitory effects. According to our data, IC50 values of compound 1 were found as 3.55 and 2.94 μM for hCA I, and hCA II, respectively. On the other hand, Ki values of this compound were found as 0.827 and 0.745 μM for both isoenzymes, respectively.

Keywords

Phenolic sulfonamides
Carbonic anhydrase
Enzyme inhibition
Carbonic anhydrase
1

1 Introduction

Carbonic anhydrase (CA: EC 4.2.1.1.) is a metalloenzyme containing a Zn2+ ion. CA is a very important enzyme, which regulates CO2 levels in living organisms. CA was first isolated from mammalian erythrocyte (Gülçin et al., 2004; Güney et al., 2014). It was reported that CA was isolated, purified and characterized from many different plant and animal tissues (Gülçin et al., 2004; Topal and Gülçin, 2014). All these enzymes catalyze the reactions as shown below: CO 2 + H 2 O ⇌ H 2 CO 3 ⇌ HCO 3 - + H +

CA has active properties in the kidney, gastric mucosa, eye lens, salivary glands, brain, nerve myelin sheath, pancreas, prostate and uterus (Gülçin and Beydemir, 2013; Arabaci et al., 2014). CA isoforms participate in several important biological processes and they are found in a variety of tissues. Studies demonstrated important roles of CAs in a variety of physiological procedures, and showed that extraordinary levels or activities of these enzymes have been often related with different human diseases (Innocenti et al., 2010a; Göçer et al, 2014).

CA inhibitors (CAIs) are classified into two main groups, the metal complexing anions and the unsubstituted sulfonamides. Sulfonamides are very important CAIs. Anions may bind either in a tetrahedral geometry with the metal ions or as a trigonal-bipyramidal adduct. Sulfonamides bind in a tetrahedral geometry with the Zn2+ ions (Bertini et al., 1982; Lindahl et al., 1990; Briganti et al., 1996; Supuran and Scozzafava, 2000; Kim et al., 2000). E ∼ Zn 2 + ∼ OH 2 + I ↔ E ∼ Zn 2 + ∼ I + H 2 O E ∼ Zn 2 + ∼ OH 2 + I ↔ E ∼ Zn 2 + ∼ H 2 O ( I )

The discovery of CA inhibition with sulfanilamide by Mann and Keilin (1940) was the beginning of many scientific discoveries and applications. Important drugs, such as antihypertensives of benzothiadiazine and high-ceiling diuretics were prepared following the discovery (Maren, 1967). More than 100 sulfonamides were investigated by means of kinetic, physiological and pharmacological studies. Following these, many studies were performed for preparing aromatic sulfonamides, which were investigated for their CA inhibitory action. Among the aromatic sulfonamides, benzene sulfonamides have shown the best CA inhibitory action (Supuran et al., 2004). Over the years many different sulfonamides have been reported to act as CAIs. One of the most investigated compounds is phenol (Göksu et al., 2014).

After many studies, excellent results have been achieved, especially associated with sulfonamides and their derivatives. In 1982 Lindskog’s group reported that phenols act as competitive inhibitors against human cytosolic CA II (Tibell et al., 1985; Simonsson et al., 1982). Also, extra structural description on the binding mode of phenolic compounds or derivatives to the CA active site has been clarified (Supuran and Scozzafava 2002).

In this context, we aimed to extend our study on the CA inhibitory properties of some phenolic sulfonamides.

2

2 Result and discussion

2.1

2.1 CA purification and activity assay

In this study, hCA I, and II isoenzymes were purified separately from human fresh erythrocytes, using a simple one-step chromatographic method using Sepharose-4B-l-tyrosine-sulfanilamide column material. In the first part of our study, we have identified the inhibitory effects of phenolic sulfonamides 1–4 on the esterase activity of both isoenzymes (Table 1). In one of our early studies we have reported the synthesis, acetylcholinesterase inhibitory and antioxidant activity of compounds 1–4 (Göçer et al., 2013).

Table 1 The chemical structure of phenolic sulfonamides 1–4.
Compounds R1 R2 R3 R4 R5
1 OH H H H H
2 H OH OH H H
3 H OH H OH H
4 OH OH H H H

The inhibition measurements were performed with esterase activity methods described by Akincioglu et al. (2013a,b). The base of this method is based on the destruction of CA ester bonds. In this process, the CA enzyme hydrolyzes the phenyl acetate and the resulting product showed absorption at 348 nm. In our study, this method was preferred due to its high sensitivity compared to methods of Wilbur and Anderson (1948).

2.2

2.2 CA isoenzymes inhibitory effects

CAIs have been essentially used as diuretics and antiglaucoma agents (Winum et al., 2006; Supuran 2007, 2008; De Simone et al, 2008; Hen et al., 2011). In recent studies for the synthesis of CAIs, the sulfonamide compounds (R-SO2NH2) are very important and widely used in zinc binding functions (Akıncıoğlu et al., 2013a; Akbaba et al., 2013a; Çetinkaya et al., 2013; Aksu et al., 2013). They are designed and synthesized according to these characteristics. We firstly reported the study on the inhibitory effects of synthesized novel sulfonamides 1–4 and on the esterase activity of hCA I, and II. In this study inhibitory effects of compounds on the CA isoenzymes were investigated. Results were determined for hCA I, and II by drawing Lineweaver-Burk graphs (1934). After hCA I, and II inhibitory effects of the novel phenolic sulfonamides 1–4 the IC50 and average Ki values were calculated. The results given in Table 2 show the following regarding the inhibitory effects of hCA I, and II by novel phenolic sulfonamides 1–4.

Table 2 Human carbonic anhydrase isoenzyme (hCA I and hCA II) inhibition value with some phenolic sulfonamide derivatives (1–4) by an esterase assay with 4-nitrophenylacetate as substrate.
Compounds IC50 (μM) KI (μM)
hCA I R2 hCA II R2 hCA I hCA II
1 3.55 0.997 2.94 0.985 0.827 ± 0.096 0.745 ± 0.173
2 3.60 0.995 2.42 0.989 2.508 ± 0.099 0.919 ± 0.019
3 3.43 0.961 3.43 0.9632 1.884 ± 0.098 0.867 ± 0.034
4 5.41 0.985 4.07 0.994 1.592 ± 0.033 1.046 ± 0.008

CA isoenzyme inhibitors block the active site of CA isoenzymes and in this way the actual metabolism of the substrate is inhibited and the body functions remain normal (Shahwar et al., 2012). In the current study, we demonstrated strong inhibitory effects of newly synthesized phenolic sulfonamide compounds (1–4) on both cytosolic isoenzymes. The arithmetic average Ki values of sulfonamides compounds (1−4) are in the range of 0.827–2.508 μM for hCA I, and 0.745–1.046 μM for hCA II (Table 2). Half-maximum inhibitory concentration (IC50) measures the effectiveness of novel phenolic sulfonamides 1–4 in inhibiting CA isoenzyme function. Lower IC50 and Ki values show strong CA isoenzyme inhibitory effects of sulfonamides. These data are very important for biologically active compounds. In the last years, a lot of sulfonamide drug groups have been developed in the drug markets (Supuran and Scozzafava 2000). At first, Lindskog’s group (Simonsson et al., 1982) reported phenols as inhibitors against human CA II and extra structural definition on the binding mode of phenolic derivatives to the CA active site was obtained (Supuran and Scozzafava 2002). CA inhibitory effects of a large spectrum of phenolic compounds including melatonin (Beydemir and Gülçin, 2004), morphine (Çoban et al., 2007), vitamin E (ArasHisar et al., 2004), caffeic acid phenethyl ester (Göçer and Gülçin, 2013), a series of antioxidant phenols (Sentürk et al., 2009), a series of phenolic acids (Ozturk Sarikaya et al., 2010), a series of natural product polyphenols and phenolic acids (Innocenti et al., 2010a,b), two different series of natural phenolic compounds (Sentürk et al., 2011; Ozturk Sarikaya et al., 2011; Gülçin and Beydemir, 2013), antioxidant polyphenol natural products (Innocenti et al., 2010b), (3,4-dihydroxyphenyl)(2,3,4-trihydroxyphenyl)methanone and its derivatives (Nar et al., 2013), natural and synthetic bromophenols (Akbaba et al. 2013b; Balaydın et al. 2012a,b), novel phenolic sulfonamides (Akıncıoğlu et al., 2013b), novel sulfonamide derivatives of aminoindanes and aminotetralins (Akbaba et al., 2013b), novel phenolic benzylamine derivatives (Çetinkaya et al., 2013), sulfonamide analogs of dopamine related compounds (Aksu et al., 2013), new benzotropons (Güney et al., 2014) and novel sulfonamides incorporating tetralin scaffold (Akıncıoğlu et al., 2013b) have been reported. These extensive studies indicate the importance of CA enzyme inhibitors. The results obtained from Table 2 clearly show that the physiologically dominant cytosolic isozymes hCA I, and II were effectively inhibited by sulfonamide compounds 1–4. The reason for this is that both cytosolic isoenzymes have a high sequence of amino acid homology within their active sites (Xue et al., 1993; Brzozowski et al., 2012).

Sulfonamides 1–4 have one aromatic ring and –OH groups. Here, compounds 1–4 have been studied as hCA isoenzymes inhibitors. The logic of working these sulfonamides as potent CA inhibitors exists in the fact that the compounds with aromatic rings have been identified to be the inhibitor with CO2 as the substrate for the main isoform of CA.

3

3 Conclusion

In conclusion, acetylcholine esterase inhibitors and antioxidant sulfonamides 1–4 were evaluated for CA inhibitory properties. In this study, micromolar levels of Ki and IC50 values were observed. We show by this study that compounds 1–4 are both selective cytosolic CA isoenzyme inhibitors with selectivity ratios in the range of 0.745–2.508 μM. These results clearly indicate that phenolic sulfonamides 1–4 may be used as leads for generating both powerful cytosolic CA inhibitors eventually targeting other isoforms.

4

4 Experimental

4.1

4.1 General information

The chemicals and solvents used in this study are commercially available. All solvents were purified according to standard procedures. CA inhibitory properties of samples were determined using a spectrophotometer (UV-1208, Shimadzu, Japan). Compounds 1–4 were synthesized according to our previous procedure (Göçer et al., 2013).

4.2

4.2 Purification of CA isoenzymes

CA isoenzymes were purified via a simple single-step method Sepharose-4B-l-tyrosine-sulfanilamide affinity gel chromatography (Atasaver et al., 2013), as defined previously (Ozturk Sarikaya et al., 2010; Sentürk et al., 2011). Fresh human erythrocyte samples were centrifuged at 10,000g for 30 min and then removed and the serum isolated. The pH was adjusted to 8.7 with solid Tris. Sepharose-4B-l-tyrosine-sulfanilamide affinity column equilibrated with Tris–HCl (25 mM)/Na2SO4 (0.1 M; pH 8.7). The Sepharose-4B-l-tyrosine-sulfanilamide affinity gel was washed with Tris–HCl (25 mM)/Na2SO4 (22 mM) at pH 8.7. Both CA isozymes were eluted with NaCl (1.0 M)/Na2HPO4 (25 m) at pH 6.3 and NaCH3COO (0.1 M)/NaClO4 (0.5 M) at pH 5.6, respectively. During both isozymes purification procedures, proteins stream was monitored at 280 nm (Beydemir and Gülçin 2004; Göçer and Gülçin, 2013).

4.3

4.3 Esterase activity assay and protein determination

A spectrophotometric method (SHIMADZU, UVmini-1240 UV–VIS Spectrophotometer) was used for the determination of carbonic anhydrase activities (Verpoorte et al. 1967). This method was previously described (Hisar et al., 2005a; Gülçin and Beydemir, 2013). The change in absorbance at 348 nm of 4-nitrophenylacetate (NPA) to 4-nitrophenylate was recorded for 3 min at 25 °C. The control medium contained 1.4 mL Tris-SO4 buffer (0.05 M, pH 7.4), 4-nitrophenylacetate (1 mL, 3 mM), H2O (0.5 mL) and enzyme solution (0.1 mL). Final volume reached 3.0 mL. The control was obtained by preparing the mixture without the enzyme solution. All measurements were recorded as triplicate. The Ki values were determined from a series of experiments using three different phenolic sulfonamide compound (1–4) concentrations and NPA as the substrate at five different concentrations for the construction of Lineweaver-Burk curves (1934) described previously (Hisar et al., 2005b; Sentürk et al., 2008). Furthermore the quantity of protein during every purification step was determined spectrophotometrically at 595 nm according to the Bradford method (1976). As in other studies, bovine serum albumin was used as standard protein in this study (Gülçin et al., 2005).

4.4

4.4 SDS–polyacrylamide gel electrophoresis

The purity of the enzymes was confirmed using SDS–polyacrylamide gel electrophoresis (SDS–PAGE). The running and stacking gels contained 10% and 3% acrylamide, respectively, and 0.1% SDS, according to the Laemmli procedure (1970) described previously (Sişecioğlu et al., 2009, 2010). To each electrophoresis medium a 20 mg sample aliquot was applied. SDS–polyacrylamide gel was painted with Coomassie brilliant blue R-250 reagent over night. Then, the electrophoretic zymogram was photographed (Köksal et al., 2012).

Acknowledgments

The authors would like to extend their sincere appreciation to the Deanship of Scientific Research at the King Saud University for funding this research through the Research Group Project no. RGP-VPP-254.

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