Review Article

 

Bird Glutathione S-transferases: Endogenous and Exogenous Toxic Insults

 

Sreenivasulu Dasari*, Muni Swamy Ganjayi, Balaji Meriga

Department of Biochemistry, Sri Venkateswara University, Tirupati 517502, Andhra Pradesh, India.

 

Editor | Kuldeep Dhama, Indian Veterinary Research Institute, Uttar Pradesh, India.

Received | May 24, 2017; Accepted | July 19, 2017; Published | September 11, 2017

*Correspondence | Sreenivasulu Dasari, Department of Biochemistry, Sri Venkateswara University Tirupati, 517502, Andhra Pradesh, India; Email: dasarisreenivaasulu@gmail.com

Citation | Dasari S, Ganjayi MS, Meriga B (2017). Bird glutathione s-transferases: endogenous and exogenous toxic insults. Adv. Anim. Vet. Sci. 5(9): 388-394.

DOI | http://dx.doi.org/10.17582/journal.aavs/2017/5.9.388.394

ISSN (Online) | 2307-8316; ISSN (Print) | 2309-3331

Copyright © 2017 Dasari et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

 

Introduction

 

That the xenobiotic metabolism is the biochemical modification by living organisms through the action of specialized enzymatic system. At the time of xenobiotic metabolism lipophilic chemical compounds are converts into hydrophilic compounds which are ready to excrete. That the xenobiotic metabolism which is divided as three phases. The glutathione S-transferases (GST) are most important xenobiotic metabolizing enzymes in phase II defence enzymes. Glutathione S-transferases (GSTs) (EC. 2.5.2.18) are belongs to a family of multifunctional enzymes which conjugate electrophilic intermediates with the endogenous tripeptide glutathione (GSH) (Hayes et al., 2005).Based on both functional and sequence similarities that the cytosolic GSTs are classified, which composed of two sub units (dimers) within the same class (Wilce and Parker, 1994). There are cytosolic, mitochondrial and membrane associated GSTs, but detoxification is the key function of cytosolic GSTs (Hayes et al., 2005). Mammalian cytosolic GSTs are extensively studied (Frova, 2006). GSTs play a key role in cellular detoxification, protection of macromolecules from reactive electrophiles, environmental carcinogens, reactive oxygen species and chemotherapeutic agents (Strange et al., 2000), which catalyse the nucleophilic addition of glutathione to several xenobiotics that including phase I electrophilic and carcinogenic metabolites (Senhaji et al., 2015; Nebert and Vasilou, 2004; Hayes and Strange, 2000). The GSTs can serve as peroxidases, isomerases and thiol transferases (Board et al., 2000).

 

Kumar et al. (1980) said that the relative specific activities of GSTs in various tissues of pigeon are as follows: kidney > liver > testes > brain > lung > heart. Quail liver cytosolic GSTs were purified by using S-hexylglutathione affinity column in tandem by a glutathione (GSH) affinity column and designated as QL 1, QL 2, QL 3a, QL 3b and QL 4 (Dai et al., 1996). Based on immunochemical studies, it was reported that the QL 1 and QL 2 are similar to the rat mu (μ) class GSTs, QL 3a and QL 3b are related to the rat and mouse alpha (α) class GSTs (Dai et al., 1996). N-terminal sequence of QL 2 is identical to the chicken mu (μ) class GST i.e CL 2 (Dai et al., 1996). The two initial valine residues which are on the N-terminus are unique character of bird mu (μ) class GSTs when compared the mammals (Dai et al., 1996).

 

Chang et al. (1990) was purified CL1, CL2, CL3, CL4 and CL5 GSTs from chicken liver by using S-hexylglutaathione and glutathione (GSH) combination affinity column. Chang et al. (1992), Liu et al. (1993), alpha (α) class GST, Liu and Tam (1991) mu (μ) class GST, Hsiao et al. (1995) theta (θ) class GST and Thomson et al. (1998) sigma (σ) class GST cDNAs isolated by both cloning experiments and Expressed Sequence Tag (EST) database search from domestic chicken. It was reported that the CL1 (θ GST) and CL5 (σ GST) are not detected chick liver purified fraction by glutathione (GSH) affinity column (Hsieh et al., 1999). Chicken GSTs protein structure and DNA sequence are elucidated (Chang et al., 1990; Liu and Tam, 1991; Liu et al., 1993). Chick embryo brain GSTs were purified by using glutathione CL-agarose affinity column and designated them as CBI and CBII (Dasari et al., 2016). Based on biochemical characterization, CBI and CBII GSTs which related alpha (α) and mu (μ) class GSTs (Dasari et al., 2016).

 

Kim et al. (2011) was cloned six alpha (α) class GST subunits of turkey were cloned and expressed in E. coli. It was reported that the molecular weights of expressed tGSTA subunits were similar to the alpha (α) class GSTs (Kim et al., 2010). GSTs are ubiquitous multifunctional enzymes and they play an important role in detoxification of pesticides (Ezemonye and Tongo, 2010); carcinogens like mycotoxin aflatoxin B1(AFB1) (Eaton and Bammler, 1999). GST has catalyses the addition of glutathione (GSH) to endogenous xenobiotics (Satheesh et al., 2010).

 

Environmental Toxic Agents and Oxidative Stress

 

That the environment is whether intentionally or unintentionally loading with foreign chemical compounds (xenobitics) which released by industries. But thousands of organic pollutants have been produced which released into environment from twentieth century (Helm et al., 2011). Many of such chemical agents are extremely stable, which hazard to the living organisms. That the stable organic pollutants which accumulate in all ecosystems and they are transported by air, water and migratory species and deposited in too distance from the place of their production (Choi and Wania, 2011).

 

That the oxidative stress can be characterized by either an oxidative burst or rapid and transient production of high levels of reactive oxygen species (ROS). That the oxidative burst can be inducing either directly by various pollutants or indirectly by their metabolism (Droege, 2002). Several mechanisms are there that the formation of oxidative stress by xenobiotics. That the free radicals which can readily react with biomolecules.The cells have developed protection mechanism against oxidative stress, due to the inefficiency of protection mechanism, oxidative stress can damage biomolecules (Zhang et al., 2004). That the biochemical markers which can provide information about the health status of an organism and this can be used as early warning signals of particular stress (Korte et al., 2000).

 

Detoxification of Exogenous Hazardous Agents by Gst

 

Glutathione S-transferases (GSTs) are detoxifying a large number of exogeneous toxic agents like carcinogens, drugs and environmental pollutants as shown in Figure 1. That the chemotherapeutic agents of cancer such as adriamycin, 1, 3-bis (2-chloroethyl)-1-nitrosourea (BCNU), busulfan, carmustine, chlorambucil, cis-platin, crotonyloxymethyl-2-cyclohexenone (COMC-6), melphalan, mitozantrone, thiotepa, cyclophosphamide and ethacrynic acid are detoxified by GSTs (Hamilton et al., 2003). Environmental chemicals and their metabolites like acrolein, atrazine, DDT, inorganic arsenic, lindane, Malathion, methyl parathion, muconaldehyde and tridiphane are detoxified by GST isoenzymes (Abel et al., 2004a, 2004b). A large number of epoxides like fosfomycin and those derived from environmental carcinogens, polycyclic aromatic hydrocarbons (PAHs) are detoxified by GST. Activated metabolites N-acetoxy-PhIP of heterocyclic amine, 2-amino-1-methyl-6-phennylimidazo [4, 5-b] pyridine (PhIP) which produced by cooking protein-rich food is also detoxified by cytosolic GST isoenzymes.

 

Activation of Xenobiotics by GST

 

The conjugation reaction catalysed by GST can form less reactive and readily excreted products. But in some cases that the glutathione (GSH) conjugate is more reactive than the parent compound like short chain alkyl halides that contain two functional groups and 1, 2-dihaloethanes, where the GSH conjugate rearranges to form an episulfonium intermediate which responsible for DNA modification (Guengerich et al., 2003). The conjugation of GSH with the solvent dichloromethane facilitate formation of the highly unstable Schloromethlglutathione which capable to modify DNA (Guengerich et al., 2003; Wheeler et al., 2001).

 

That the moderately toxic compounds like allyl-, benzyl-, phenethyl-isothiocyanates and sulforaphane are reversibly conjugated with GSH by GST to form thiocarbamates which spontaneously degrade to their isothiocyanates by releasing GSH. Again that the isothiocyanates may be taken up by the cell and re-conjugated with GSH and then form thiocarbamate and then revert to the isothiocyanate. Due to this cyclic process, intracellular GSH levels are decreased and facilitate the distribution of isothiocyanates entire the body. Such isothiocyanate either low GSH content or not conjugated with GSH, but rather are more likely to thiocarbalate proteins, which result in cell death (Xu and Thornalley, 2001).

 

Detoxification of Endogenous Hazardous Agents by Gst

 

The GST isoenzymes are exhibits moderate role in lipid peroxidation in biological membranes. The GSTs exhibit non selenium glutathione peroxidase (GPx) activity with 1-palmitoyl-2-(13-hydroperoxy-cic-9, trans-11-octadecadienoyl)-L-3-phosphadylcholine, phospatidylcholine hydroperoxide and redusing lipid hydroperoxides which are in membranes (Yang et al., 2002; Li et al., 2005; Prabhu et al., 2004). The transferases can reduce cholesteryl hydroperoxides (Hamdy et al., 2003), fatty acid hydroperoxides, (S)-9-hydroproxy-10, 12-octodecadieonic acid and (S)-13-hydroperoxy-9, 11-octadecadieonic acid (Liang et al., 2004). That the lipid peroxidation end products like 2-alkenals acrolein, crotonaldedyde and 4-hydroxy-2-alkenals are conjugate with GSH by GSTs (Liang et al., 2004). GSTs catalyze the GSH conjugation with cholesterol-5, 6-oxide, epoxyeicosatrienoic acid and 9, 10-epoxystearic acid, which indicating its role in cellular protection against oxidative stress harmful electrophiles (Hayes et al., 2005).

 

Birds in Polluted Environments

 

As shown in Figure 1, birds are victimizing to toxic agents by air, water and territory. It was reported that the effects of indirect pollution may be very common in nature than the direct pollution and which may affect even at lower contaminant levels (Eeva et al., 2003). In addition to normal metabolism during the processing of many toxic compounds produce several reactive oxygen species and they may increase the oxidative stress in species which are live in polluted environments (Valko et al., 2005). Great tits are showed lower breeding performance with poor quality diet in polluted environment which suggests the importance of secondary environmental changes including food quality (Eeva et al., 2005; 2009). That the individuals which are living in polluted environments can exposed to a mixture of pollutants at sub lethal concentrations which shows synergistic, antagonistic effects. Based on oxidative potential and reactivity with biomolecules the hydroxyl radicals are the most important in biological and toxicological terms (Ercal et al., 2001). Little attention was paid on the function of antioxidant enzymatic system and it’s levels in different bird species as an indicators of oxidative stress in polluted environments (Berglund et al., 2007; Norte et al., 2009; Hegseth et al., 2011). It was reported that the oxidative stress may be a physiological challenge and which is a factor potentially affecting bird migration strategies, but it is not yet recognized (Jenni-Eiermann et al., 2014).

 

Defensive System in Birds

 

Especially in birds that the detoxification efficiency is depend on with diet composition (Ronis and Walker, 1989; Fossi et al., 1995) and sometimes it is associated with the metabolic rate (Ronis and Walker, 1989). Low rates of mitochondrial oxygen radical production and high blood glucose levels, which are the unique molecular mechanisms in birds than the other vertebrates and due to these unique character birds can easily defend free radicals and oxidative stress (Pamplona and Costantini, 2011). Recognizable attention is increasing that the balancing investment in antioxidant defences to sustain to oxidative damage has possibly influence life history traits (Monaghan et al., 2009). It is suggests that the up regulation of antioxidant system in free flying migrants which adapt their antioxidant system to the sustainability to extraordinary exercise at very high metabolic rate (Jenni-Eiermann et al., 2014).

 

Gst is a Biomarker in Birds

 

GSTs are useful as biomarker in ecological risk assessment of pesticide contaminated environment (Ezeji et al., 2012). It was reported that the presence of glutathione S-trnsferases (GSTs) activity in wild birds (Witt and Snell, 1968). Mukthar and Bresnick (1976) said that the GST is an inducible enzyme. It have been identified that the species differences in conjugation reactions, some birds use ornithine instead of glycine for conjugation with xenobiotics (Baldwin et al., 1960), it may be due to difference in evolutionary scale of avian species. That the significant level of GST activity in hepatic and extra hepatic tissues of pigeons are similar to the tissues of rodent. Pigeon hepatic GSTs were inducted with 3-methylcholanthrene (3-MC) (Kumar et al., 1980). It was reported that the various biomarkers are measure different aspects of redox balance, which suggests the careful planning is need at the level of designing certain study set up (Horak and Cohan, 2010). Glutathione related enzymes like GPx and GST are most prominent biomarkers in birds (Isaksson, 2010) and elevation of those enzyme activities was reported in white stork (Ciconia ciconia) (Kaminski et al., 2009), the pied flycatcher (Berglund et al., 2007), the great tit (Isaksson et al., 2005; Norte et al., 2010). It was reported that the GST activity induction is an evolutionary response of cells to protect against metabolites and degenerative disorders which related to oxidative stress (Hayes et al., 2005; Raza, 2011). In Avian species, tissue distribution of GST is not similar to mammals; high renal specific activity is the most distinctive feature of Avian GST (Maurice et al., 1991). As shown in Figure 1, GST is expressed in response to both endogenous and exogenous toxic agents.

 

 

Usually, as shown in Figure 1, in normal metabolism toxic agents like reactive oxygen species (ROS) and reactive nitrogen species (RNS) are formed in cellular system. In addition to that, environments are loading with toxic chemical agents in the form of pesticides, insecticides, agriculture related chemical formulas, industrial effluents and motor vehicle pollutants etc. Because of highly mobile nature, birds are victimizing to these exogenous (xenobiotic) toxic agents by air, water and terrestrial. When the toxic agents enter into cellular system, they cause to oxidative stress in addition to deleterious effect of them. Glutathione S-transferse (GST) is expressed more and more to detoxify both endogenous and exogenous toxic insults.

 

Susceptibility of Birds

 

Poultry birds (domestic fowls) are victimizing to pesticide poisoning due to their tendency to eat pesticide contaminated food and other items in the environment (Ezeji et al., 2011). Domestic turkeys (Meleagris gallopavo) are one of the most susceptible species known to AFB1 (Klein et al., 2000; Rawal et al., 2010). The efficiency of GST conjugation is a principal ‘‘rate-limiting’’ determinant for AFB1 action in individuals and species (Ilic et al., 2010). Numerous studies have demonstrated that individual and species susceptibility to AFB1-induced toxicity and hepatocarcinogenicity is strongly associated with GST-mediated detoxification of AFBO (Monroe and Eaton, 1988). Acute and chronic toxic effects of AFB1, apparently because of the extremely high affinity toward AFBO exhibited by their hepatic Alpha-class A3 subunit (Buetler et al., 1992; Hayes et al., 1992).

 

Comparative toxicology studies have shown that wild turkeys are substantially more resistant to AFB1 compared to domestic turkeys (Quist et al., 2000). But GSTs of the domestic turkeys have little or no AFBO affinity activity with AFB1 (Klein et al., 2002; 2003). Wild and heritage turkeys might contain potentially useful GST alleles not found in domestic birds (Kim et al., 2013).

 

Bird Gsts Specific Activity and Mutations

 

In pigeon, GST activity with 1-chloro-2, 4-dinitobenezene (CDNB) is higher in 40 to 44 times in liver and kidney than with 1, 2-dichloro-4-nitrobenezene (DCNB) (Kumar et al., 1980). In Japanese quail, GST activity with CDNB and cumene hydroperoxide (CHP) elevated in kidney and liver than brain and lung (Dai et al., 1996). Dai et al. (1996) reported that both GST activity with multiple substrates and glutathione peroxidase (Gpx) activity with CHP are higher in kidney than in liver of Japanese quail and also Gpx activity is higher than GST activity in lung.All recombinant GSTA and GSTM of turkey have activity with prototype substrates (Kim et al., 2010, 2011, 2013). In turkeys, GST A1-2 and GST A1-3 shows the highest activity with CDNB, ethacrynic acid (ECA) and CHP but GST A1-1 shows highest activity with DCNB (Kim et al., 2011). Turkey hepatic cytosol GSTAs, shows catalytic activities with the GST substrates such as CDNB, DCNB, ECA and CHP, but with CDNB and CHP which appeared to be the much more (Kim et al., 2011). Turkey hepatic cytosol GSTA shows the least activity with 1, 2-dichloro-4-nitrobenzene (DCNB), which is a specific substrate of mu (µ) class GST (Vanhaecke et al., 2000).

 

Numerous studies have proved that the single amino acid site change can influence catalytic properties, substrate specificity and stereoselectivity of GSTs (Bammler et al., 1995). In chickens, Lys 15 and Ser 208 of GSTA 1 are responsible for high specific activity and selectivity with ethacrynic acid (ECA) (Liu et al., 1997). Kim et al. (2011) suggested that the site-directed mutagenesis with molecular modeling may be useful to elucidate the relative contributions of specific amino acid residues to the catalytic function of GSTAs of turkey.

 

Conclusion

 

That the endogenous and exogenous toxic agents which are not benefit to the body. In addition to that they injure to the body if they stayed long period in the living system. Therefore, they should be remove by set of metabolic pathways which mediated by antioxidant enzymatic system. Birds are frequently encountering environmental xenobiotic substances which have hazardous biological activity. GSTs are the versatile toxic agents metabolizing enzymes among antioxidant enzymatic system. In birds, GSTs are playing major role in detoxification of toxic agents and also act as biomarker to evaluate the health condition of birds. The single amino acid change can alter the GST antioxidant activity. It is concluding that the GST can detoxify toxic agents in birds and an amino acid can change GST activity which leads to susceptibility of birds to various environmental toxic agents and endogenous toxic species.

 

Acknowledgements

 

Authors are thankful to University Grants Commission, New Delhi, India (Grant No: 20601/UGC-I (2)/RGNF/2007) for providing Financial Assistance.

 

Conflict of interest

 

Authors do not have any potential conflict of interest.

 

AUTHORS Contribution

 

This review was written by DS, quality checked by GMS and technical guidance given by BM.

 

References

 

Abel EL, Bammler TK, Eaton DL (2004a). Biotransformation of methyl parathion by glutathione S-transferases. Toxicol. Sci. 79 (2): 224-232. https://doi.org/10.1093/toxsci/kfh118

Abel EL, Opp SM, Verlinde CL, Bammler TK, Eaton DL (2004b). Characterization of atrazine biotransformation by human and murine glutathione S-transferases. Toxicol. Sci. 80 (2): 230-238. https://doi.org/10.1093/toxsci/kfh152

Baldwin BC, Robinson D, Williams RT (1960). Studies in detoxication. 82. The fate of benzoic acid in some domestic and other birds. Biochem. J. 76(3): 595-600. https://doi.org/10.1042/bj0760595

Bammler TK, Driessen H, Finnstrom N, Wolf CR (1995). Amino acid differences at positions 10, 11, and 104 explain the profound catalytic differences between two murine pi-class glutathione S-transferases. Biochemistry. 34(28): 9000-9008. https://doi.org/10.1021/bi00028a008

Berglund ÅM, Sturve J, Förlin L, Nyholm NE (2007). Oxidative stress in pied flycatcher (Ficedula hypoleuca) nestlings from metal contaminated environments in northern Sweden. Environ. Res. 105(3): 330-339. https://doi.org/10.1016/j.envres.2007.06.002

Board PG, Coggan M, Chelvanayagam G, Easteal S, Jermiin LS, Schulte GK, Danley DE, Hoth LR, Griffor MC, Kamath AV, Rosner MH (2000). Identification, characterization, and crystal structure of the Omega class glutathione transferases. J. Biol. Chem. 275(32): 24798-24806. https://doi.org/10.1074/jbc.M001706200

Buetler TM, Eaton DL (1992). Glutathione S‐transferases: Amino acid sequence comparison, classification and phylogenetic relationship. J. Environ. Sci. Health. C. 10(2):181-203. https://doi.org/10.1080/10590509209373416

Chang LH, Chuang LF, Tsai CP, Tu CP, Tam MF (1990). Characterization of glutathione S-transferases from day-old chick livers. Biochemistry. 29(3):744-750. https://doi.org/10.1021/bi00455a022

Chang LH, Fan JY, Liu LF, Tsai SP, Tam MF (1992). Cloning and expression of a chick liver glutathione S-transferase CL 3 subunit with the use of a baculovirus expression system. Biochem. J. 281(2):545-51. https://doi.org/10.1042/bj2810545

Choi SD, Wania F (2011). On the Reversibility of Environmental Contamination with Persistent Organic Pollutants. Environ. Sci. Technol. 45(20): 8834-8841. https://doi.org/10.1021/es2017544

Dai H, Edens FW, Roe RM (1996). Glutathione S‐transferases in the Japanese quail: Tissue distribution and purification of the liver isozymes. J. Biochem. Mol. Toxicol. 11(2): 85-96.

Dasari S, Gonuguntla S, Ganjayi M, Meriga B, Kedam T. (2016) Biochemical characterization of glutathione S-transferases purified from chick embryo brain. J. Anim. Poult. Sci. 5(4): 42-51.https://doi.org/10.1002/(SICI)1522-7146(1996)11:2%3C85::AID-JBT6%3E3.0.CO;2-Q.

Droege W (2002). Free radicals in the physiological control of cell function. Physiol. Rev. 82(1): 47-95. https://doi.org/10.1152/physrev.00018.2001

Eaton DL, Bammler TK (1999). Concise review of the glutathione S-transferases and their significance to toxicology. Toxicol. Sci. 49(2):156-164. https://doi.org/10.1093/toxsci/49.2.156

Eeva T, Lehikoinen E, Nikinmaa M (2003). Pollution‐induced nutritional stress in birds: an experimental study of direct and indirect effects. Ecolog. Appl. 13(5):1242-1249. https://doi.org/10.1890/01-5375

Eeva T, Hasselquist D, Langefors Å, Tummeleht L, Nikinmaa M, Ilmonen P (2005). Pollution related effects on immune function and stress in a free‐living population of pied flycatcher Ficedula hypoleuca. J. Avian Biol. 36(5): 405-412 https://doi.org/10.1111/j.0908-8857.2005.03449.x.

Eeva T, Sillanpää S, Salminen JP (2009). The effects of diet quality and quantity on plumage colour and growth of great tit Parus major nestlings: a food manipulation experiment along a pollution gradient. J. Avian Biol. 40(5):491-199. https://doi.org/10.1111/j.1600-048X.2008.04535.x

Ercal N, Gurer-Orhan H, Aykin-Burns N (2001). Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Current Topics Medic. Chem. 1(6): 529-539. https://doi.org/10.2174/1568026013394831

Ezemonye L, Tongo I (2010). Sublethal effects of endosulfan and diazinon pesticides on glutathione-S-transferase (GST) in various tissues of adult amphibians (Bufo regularis). Chemosphere. 81(2): 214-217. https://doi.org/10.1016/j.chemosphere.2010.06.039

Ezeji EU, Anyalogbu EA, Duru CM (2011). Use of biochemical biomarkers in the ecological risk assessment of permetrin pesticide exposure. J. Toxicol. Environ. Health Sci. 3(1):14-17.

Ezeji EU, Anyalogbu EA, Ezejiofor TN, Udensi JU (2012). Determination of reduced glutathione and glutathione S-transferase of poultry birds exposed to permethrin insecticide. Am. J. Biochem. 2(3): 21-24.

Fossi MC, Massi A, Lari L, Marsili L, Focardi S, Leonzio C, Renzoni A (1995). Interspecies differences in mixed function oxidase activity in birds: relationship between feeding habits, detoxication activities and organochlorine accumulation. Environ. Poll. 90 (1):15-24. https://doi.org/10.1016/0269-7491(94)00098-X

Frova C (2006). Glutathione transferases in the genomics era: new insights and perspectives. Biomol. Engg. 23(4):149-69. https://doi.org/10.1016/j.bioeng.2006.05.020

Guengerich FP, McCormick WA, Wheeler JB (2003). Analysis of the kinetic mechanism of haloalkane conjugation by mammalian θ-class glutathione transferases. Chem. Res. Toxicol. 16 (11): 1493-1499. https://doi.org/10.1021/tx034157r

Hayes JD, Flanagan JU, Jowsey IR (2005). Glutathione transferases. Annu. Rev. Pharmacol. Toxicol. 45: 51-88. https://doi.org/10.1146/annurev.pharmtox.45.120403.095857

Hayes JD, Strange RC (2000) Glutathione S-transferase polymorphisms and their biological consequences. Pharmacology. 61(3): 154-66. https://doi.org/10.1159/000028396

Hayes JD, Judah DJ, Neal GE, Nguyen T (1992). Molecular cloning and heterologous expression of a cDNA encoding a mouse glutathione S-transferase Yc subunit possessing high catalytic activity for aflatoxin B1-8, 9-epoxide. Biochem. J. 285 (1): 173-180. https://doi.org/10.1042/bj2850173

Hamdy SI, Hiratsuka M, Narahara K, Endo N, El‐Enany M, Moursi N, Ahmed MS, Mizugaki M (2003). Genotype and allele frequencies of TPMT, NAT2, GST, SULT1A1 and MDR‐1 in the Egyptian population. Br. J. Clin. Pharmacol. 55 (6): 560-569.

Hamilton DS, Zhang X, Ding Z, Hubatsch I, Mannervik B, Houk KN, Ganem B, Creighton DJ (2003). Mechanism of the glutathione transferase-catalyzed conversion of antitumor 2-crotonyloxymethyl-2-cycloalkenones to GSH adducts. J. Am. Chem. Soc. 125 (49):15049-15058.

Hegseth MN, Camus L, Helgason LB, Bocchetti R, Gabrielsen GW, Regoli F (2011). Hepatic antioxidant responses related to levels of PCBs and metals in chicks of three Arctic seabird species. Comparative Biochemistry and Physiology Part C: Toxicol. Pharmacol. 154 (1):28-35.

Helm PA, Milne J, Hiriart-Baer V, Crozier P, Kolic T, Lega R, Chen T, MacPherson K, Gewurtz S, Winter J, Myers A (2011). Lake-wide distribution and depositional history of current-and past-use persistent organic pollutants in Lake Simcoe, Ontario, Canada. J. Great Lakes Res. 37:132-141. https://doi.org/10.1016/j.jglr.2011.03.016

Horak P, Cohen A (2010). How to measure oxidative stress in an ecological context: methodological and statistical issues. Function. Ecol. 24 (5): 960-970. https://doi.org/10.1111/j.1365-2435.2010.01755.x

Hsieh CH, Li-Fan LI, Shu-Ping TS (1999). Characterization and cloning of avian-hepatic glutathione S-transferases. Biochem. J. 343(1): 87-93. https://doi.org/10.1042/bj3430087

Hsiao CD, Martsen EO, Lee JY, Tsai SP, Tam MF (1995). Amino acid sequencing, molecular cloning and modelling of the chick liver class-theta glutathione S-transferase CL1. Biochem. J. 312(1):91-98 https://doi.org/10.1042/bj3120091

Ilic Z, Crawford D, Egner PA, Sell S (2010). Glutathione-S-transferase A3 knockout mice are sensitive to acute cytotoxic and genotoxic effects of aflatoxin B1. Toxicol. Appl. Pharmacol. 242 (3): 241-246. https://doi.org/10.1016/j.taap.2009.10.008

Isaksson C (2010). Pollution and its impact on wild animals: a meta-analysis on oxidative stress. EcoHealth. 7 (3):342-350 https://doi.org/10.1007/s10393-010-0345-7.

Isaksson C, Örnborg J, Stephensen E, Andersson S (2005). Plasma glutathione and carotenoid coloration as potential biomarkers of environmental stress in great tits. EcoHealth. 2 (2):138-146 https://doi.org/10.1007/s10393-005-3869-5

Jenni-Eiermann S, Jenni L, Smith S, Costantini D (2014). Oxidative stress in endurance flight: an unconsidered factor in bird migration. PLoS One. 9 (5): e97650. https://doi.org/10.1371/journal.pone.0097650

Kamiński P, Kurhalyuk N, Jerzak L, Kasprzak M, Tkachenko H, Klawe JJ, Szady-Grad M, Koim B, Wiśniewska E (2009). Ecophysiological determinations of antioxidant enzymes and lipoperoxidation in the blood of White Stork Ciconia ciconia from Poland. Environ. Res. 109 (1): 29-39. https://doi.org/10.1016/j.envres.2008.07.013

Kim JE, Bunderson BR, Croasdell A, Coulombe RA (2011). Functional characterization of alpha-class glutathione s-transferases from the Turkey (Meleagris gallopavo). Toxicol. Sci. 124: 45–53. https://doi.org/10.1093/toxsci/kfr212

Kim JE, Bauer MM, Mendoza KM, Reed KM, Coulombe RA (2010). Comparative genomics identifies new alpha class genes within the avian glutathione S-transferase gene cluster. Gene. 452 (2): 45-53. https://doi.org/10.1016/j.gene.2009.11.001

Kim JE, Bunderson BR, Croasdell A, Reed KM, Coulombe Jr RA (2013). Alpha-class glutathione S-transferases in wild turkeys (Meleagris gallopavo): Characterization and role in resistance to the carcinogenic mycotoxin aflatoxin B 1. PloS one. 8 (4): e60662. https://doi.org/10.1371/journal.pone.0060662

Klein PJ, Van Vleet TR, Hall JO, Coulombe RA (2002). Dietary butylated hydroxytoluene protects against aflatoxicosis in turkeys. Toxicol. Appl. Pharmacol. 182 (1): 11-19. https://doi.org/10.1006/taap.2002.9433

Klein PJ, Van Vleet TR, Hall JO, Coulombe Jr RA (2003). Effects of dietary butylated hydroxytoluene on aflatoxin B 1-relevant metabolic enzymes in turkeys. Food Chem. Toxicol. 41 (5): 671-678. https://doi.org/10.1016/S0278-6915(02)00332-0

Klein PJ, Buckner R, Kelly J, Coulombe RA (2000). Biochemical basis for the extreme sensitivity of turkeys to aflatoxin B1. Toxicol. Appl. Pharmacol. 165 (1): 45-52. https://doi.org/10.1006/taap.2000.8926

Korte F, Kvesitadze G, Ugrekhelidze D, Gordeziani M, Khatisashvili G, Buadze O, Zaalishvili G, Coulston F (2000). Organic toxicants and plants. Ecotoxicol. Environ. Safety. 47(1):1-26. https://doi.org/10.1006/eesa.2000.1929

Kumar A, Husain MM, Mukhtar H, Murti CK (1980). Hepatic and extra-hepatic glutathione-S-transferase activity in wild pigeons (Columba livia). J. Biosci. 2(3): 181-189. https://doi.org/10.1007/BF02703244

Li J, Xia Z, Ding J (2005). Thioredoxin‐like domain of human κ class glutathione transferase reveals sequence homology and structure similarity to the θ class enzyme. Protein Sci. 14 (9): 2361-2369. https://doi.org/10.1110/ps.051463905

Liang T, Habegger K, Spence JP, Foroud T, Ellison JA, Lumeng L, Li TK, Carr LG (2004). Glutathione S‐Transferase 8‐8 Expression Is Lower in Alcohol‐Preferring Than in Alcohol‐Nonpreferring Rats. Alcoholism: Clin. Exp. Res. 28 (11):1622-1628. https://doi.org/10.1097/01.ALC.0000145686.79141.57

Liu LF, Wu SH, Tam MF (1993). Nucleotide sequence of class-α glutathione S-transferases from chicken liver. Biochim. Biophys. Acta -Gene Structure Expression. 1216 (2): 332-334.

Liu LF, Tam MF (1991). Nucleotide sequence of a class μ glutathione S-transferase from chicken liver. Biochim Biophys Acta-Gene Structure and Expression. 1090 (3):343-344. https://doi.org/10.1016/0167-4781(91)90199-V

Liu LF, Liaw YC, Tam MF (1997). Characterization of chickenliver glutathione S-transferase (GST) A1-1 and A2-2 isoenzymes and their site-directed mutants heterologously expressed in Escherichia coli: identification of Lys-15 and Ser-208 on cGSTA1-1 as residues interacting with ethacrynic acid. Biochem. J. 327: 593–600. https://doi.org/10.1042/bj3270593

Maurice DV, Lightsey SF, Kuo-Tung H, Rhoades JF (1991). Comparison of glutathione S-transferase activity in the rat and birds: tissue distribution and rhythmicity in chicken (Gallus domesticus) liver. Comparative Biochemistry and Physiology Part B: Comp. Biochem. 100 (3): 471-474.

Monaghan P, Metcalfe NB, Torres R (2009). Oxidative stress as a mediator of life history trade‐offs: mechanisms, measurements and interpretation. Ecology letters. 12 (1):75-92. https://doi.org/10.1111/j.1461-0248.2008.01258.x

Monroe DH, Eaton DL (1988). Effects of modulation of hepatic glutathione on biotransformation and covalent binding of aflatoxin B1 to DNA in the mouse. Toxicol. Appl. Pharmacol. 94 (1): 118-127. https://doi.org/10.1016/0041-008X(88)90342-0

Mukhtar H, Bresnick E (1976). Effects of phenobarbital and 3-methylcholanthrene administration on glutathione-S-epoxide transferase activity in rat liver. Biochem. Pharmacol. 25 (9): 1081-1084. https://doi.org/10.1016/0006-2952(76)90501-3

Nebert DW, Vasiliou V (2004). Analysis of the glutathione S-transferase (GST) gene family. Human genomics. 1 (6):460-464. https://doi.org/10.1186/1479-7364-1-6-460

Norte AC, Ramos JA, Sousa JP, Sheldon BC (2009). Variation of adult great tit Parus major body condition and blood parameters in relation to sex, age, year and season. J. Ornithol. 150 (3): 651-660. https://doi.org/10.1007/s10336-009-0387-1

Norte AC, Sheldon BC, Sousa JP, Tavares PC, Pereira ME, Duarte AC, Ramos JA (2010). Are Great Tits (Parus major) inhabiting the vicinity of a pulp mill healthy? Impacts on physiology and breeding performance. Archives Environ. Contamin. Toxicol. 59 (3): 502-512.

Pamplona R, Costantini D (2011). Molecular and structural antioxidant defenses against oxidative stress in animals. American J. Physiol.-Regul. Integrat. Comp. Physiol. 301(4): R843-863. https://doi.org/10.1152/ajpregu.00034.2011

Prabhu KS, Reddy PV, Jones EC, Liken AD, Reddy CC (2004). Characterization of a class alpha glutathione-S-transferase with glutathione peroxidase activity in human liver microsomes. Arch. Biochem. Biophys. 424 (1):72-80. https://doi.org/10.1016/j.abb.2004.02.002

Quist CF, Bounous DI, Kilburn JV, Nettles VF, Wyatt RD (2000). The effect of dietary aflatoxin on wild turkey poults. J. Wildl. Dis. 36 (3): 436–444. https://doi.org/10.7589/0090-3558-36.3.436

Rawal S, Kim JE, Coulombe R (2010). Aflatoxin B 1 in poultry: toxicology, metabolism and prevention. Res. Vet. Sci. 89 (3): 325-331. https://doi.org/10.1016/j.rvsc.2010.04.011

Raza H (2011). Dual localization of glutathione S‐transferase in the cytosol and mitochondria: implications in oxidative stress, toxicity and disease. The FEBS J. 278 (22): 4243-4251 https://doi.org/10.1111/j.1742-4658.2011.08358.x.

Ronis MJ, Walker CH (1989). The microsomal monooxygenase of birds. Reviews in biochemical toxicology (USA). Rev. Biochem. Toxicol. 10: 301-384.

Satheesh P, Rao AA, Sridhar GR, Srinivas K, Akula CS. 2010. Sequence analysis and homology modeling Gallus gallus glutathione s-transferase. Adv. Exp. Med. Biol. 680: 405-410. doi: 10.1007/978-1-4419-5913-3_46. https://doi.org/10.1007/978-1-4419-5913-3_46

Senhaji N, Kassogue Y, Fahimi M, Serbati N, Badre W, Nadifi S (2015). Genetic polymorphisms of multidrug resistance gene-1 (MDR1/ABCB1) and glutathione S-transferase gene and the risk of inflammatory bowel disease among Moroccan patients. Mediators of inflammation. 2015 (24): 1-8. http://dx.doi.org/10.1155/2015/248060

Strange RC, Jones PW, Fryer AA (200). Glutathione S-transferase: genetics and role in toxicology. Toxicol. Lett. 112: 357-363.

Thomson AM, Meyer DJ, Hayes JD (1998). Sequence, catalytic properties and expression of chicken glutathione-dependent prostaglandin D2 synthase, a novel class Sigma glutathione S-transferase. Biochem. J. 333(2): 317-325. https://doi.org/10.1042/bj3330317

Valko MM, Morris H, Cronin MT (2005). Metals, toxicity and oxidative stress. Current Medicin. Chem. 12 (10):1161-11208. https://doi.org/10.2174/0929867053764635

Vanhaecke T, Lindros KO, Oinonen T, Vercruysse A, Rogiers V (2000). Effect of long-term ethanol exposure on the acinar distribution of hepatic glutathione S-transferase. Drug Metab. Dispos. 28 (12): 1470-1474.

Wheeler JB, Stourman NV, Thier R, Dommermuth A, Vuilleumier S, Rose JA, Armstrong RN, Guengerich FP (2001). Conjugation of haloalkanes by bacterial and mammalian glutathione transferases: mono-and dihalomethanes. Chem. Res. Toxicol. 14(8):1118-1127. https://doi.org/10.1021/tx010019v

Wilce MC, Parker MW (1994). Structure and function of glutathione S-transferases. Biochimica. et Biophysica. Acta. (BBA)-Protein Structure Mol. Enzymol. 1205 (1):1-8. https://doi.org/10.1016/0167-4838(94)90086-8

Wit JG, Snel J (1968). Enzymatic glutathione conjugations with 2, 3-epoxyphenylpropylether and diethylmaleate by wild bird liver supernatant. European J. Pharmacol. 3(4):370-373 https://doi.org/10.1016/0014-2999(68)90125-8.

Xu K, Thornalley PJ (2001). Involvement of glutathione metabolism in the cytotoxicity of the phenethylisothiocyanate and its cysteine conjugate to human leukaemia cells in vitro. Biochem. Pharmacol. 61: 165–177. https://doi.org/10.1016/S0006-2952(00)00526-8

Yang Y, Sharma R, Zimniak P, Awasthi YC. (2002). Role of α class glutathione S-transferases as antioxidant enzymes in rodent tissues. Toxicol. Appl. Pharmacol. 182 (2):105-115. https://doi.org/10.1006/taap.2002.9450

Zhang X, Sharma RK, Agarwal A, Falcone T (2004). Antioxidant effect of pentoxifylline in reducing oxidative stress induced embryotoxicity. Fertil. Steril. 82: S324-325. https://doi.org/10.1016/j.fertnstert.2004.07.878