B-esterases activities in several tissues of the marine fish: sea bass and hake, as potential biomarkers of bisphenol A derivatives

Abstract

In the marine environment, a new threat linked to plastic pollution relates to plastic additives. This threat encompasses multiple chemical compound groups with a high bioaccumulation potential for these chemical mixtures. Hence, informative biomarkers are needed to indicate the effects of environmentally realistic mixtures of these additives. This study proposes an in vitro approach using tissue homogenates of two marine fish, the European sea bass and hake, which are both of interest in aquaculture and fisheries. The selected biomarkers are B-esterase activities comprising acetylcholinesterase (AChE) and carboxylesterases (CEs). The physiological role of AChE in brain and muscle is mainly neural transmission, while CEs participate in liver detoxification processes. However, B-esterases are also widely distributed in other tissues/organs, where their role is yet to be determined, but their inhibition may have undesired biological consequences. Here, we compared the interaction of the plastic additives, bisphenol A and some of its derivatives, like tetrabromobisphenol A (TBBPA), with B-esterase activities. We particularly focused not only on the robust and broadly distributed CE enzymes in brain, gonad, liver, kidney, and plasma tissues of two marine fish, but also on the use of two commercial substrates, p-nitrophenyl butyrate and α-naphthyl butyrate, tentatively representing two CE isoforms. The results evidenced specific species and tissue responses that could be due to a diverse isoform composition. They identified sea bass as better protected against neurotoxic exposures, at least in terms of B-esterase composition. The flame retardant TBBPA was the most reactive to B-esterases inhibition, although Bisphenol A bis (2,3-dihydroxy propyl) ether and Bisphenol F bis (3-chloro-2-hydroxypropyl) ether warrant further toxicology assessments.

Keywords

Acetylcholinesterase / carboxylesterase / marine fish in vitro. assessment / plastic additives / bisphenol A analogs

References

[1] Alberghini L,Santonicola S,Giaccone V.Microplastics in fish and fishery products and risks for human health: a review.Int J Environ Res Public Health2022;20:789 PMCID:PMC9819327

[2] Cózar A,González-Gordillo JI.Plastic debris in the open ocean.Proc Natl Acad Sci USA2014;111:10239-44 PMCID:PMC4104848

[3] Cózar A,Martí E.Plastic accumulation in the Mediterranean sea.PLoS One2015;10:e0121762 PMCID:PMC4382178

[4] Chen G,Wang J.Occurrence and ecological impact of microplastics in aquaculture ecosystems.Chemosphere2021;274:129989

[5] Lin L,Wang P.Environmental occurrence and ecotoxicity of aquaculture-derived plastic leachates.J Hazard Mater2023;458:132015

[6] Vandeputte M,Allal F.The European sea bass: a key marine fish model in the wild and in aquaculture.Anim Genet2019;50:195-206 PMCID:PMC6593706

[7] Muns-Pujadas L,Constenla M.Revealing the capability of the European hake to cope with micro-litter environmental exposure and its inferred potential health impact in the NW Mediterranean Sea.Mar Environ Res2023;186:105921

[8] Chenet T,Bono G.Plastic ingestion by Atlantic horse mackerel (Trachurus trachurus) from central Mediterranean Sea: a potential cause for endocrine disruption.Environ Pollut2021;284:117449

[9] Barboza LGA,Oliveira P.Microplastics in wild fish from North East Atlantic Ocean and its potential for causing neurotoxic effects, lipid oxidative damage, and human health risks associated with ingestion exposure.Sci Total Environ2020;717:134625

[10] Barboza LGA,Monteiro C,Guilhermino L.Bisphenol A and its analogs in muscle and liver of fish from the North East Atlantic Ocean in relation to microplastic contamination. Exposure and risk to human consumers.J Hazard Mater2020;393:122419

[11] Barboza LGA,Branco V.Microplastics cause neurotoxicity, oxidative damage and energy-related changes and interact with the bioaccumulation of mercury in the European seabass, Dicentrarchus labrax (Linnaeus, 1758).Aquat Toxicol2018;195:49-57

[12] Brandts I,Gonçalves AP.Immuno-modulatory effects of nanoplastics and humic acids in the European seabass (Dicentrarchus labrax).J Hazard Mater2021;414:125562

[13] Gunaalan K,Capolupo M.The hidden threat of plastic leachates: a critical review on their impacts on aquatic organisms.Water Res2020;184:116170

[14] Lionetto MG,Giordano ME.Pollution biomarkers in the framework of marine biodiversity conservation: state of art and perspectives.Water2021;13:1847

[15] Hermabessiere L,Paul-Pont I.Occurrence and effects of plastic additives on marine environments and organisms: a review.Chemosphere2017;182:781-93

[16] Abdallah M. Environmental occurrence, analysis and human exposure to the flame retardant tetrabromobisphenol-A (TBBP-A)-A review.Environ Int2016;94:235-50

[17] Chen D,Tan H.Bisphenol analogues other than BPA: environmental occurrence, human exposure, and toxicity - a review.Environ Sci Technol2016;50:5438-53

[18] Liu J,Lu G,Yan Z.Occurrence, toxicity and ecological risk of bisphenol A analogues in aquatic environment - a review.Ecotoxicol Environ Saf2021;208:111481

[19] den Braver-Sewradj SP, van Spronsen R, Hessel EVS. Substitution of bisphenol A: a review of the carcinogenicity, reproductive toxicity, and endocrine disruption potential of alternative substances.Crit Rev Toxicol2020;50:128-47

[20] Fabrello J.Bisphenol analogs in aquatic environments and their effects on marine species - a review.J Mar Sci Eng2022;10:1271

[21] Carnevali O,Canuti D,Forner-Piquer I.Diets contaminated with bisphenol A and Di-isononyl phtalate modify skeletal muscle composition: a new target for environmental pollutant action.Sci Total Environ2019;658:250-9

[22] Maradonna F,Dalla Valle L.A developmental hepatotoxicity study of dietary bisphenol A in Sparus aurata juveniles.Comp Biochem Physiol C Toxicol Pharmacol2014;166:1-13

[23] Pérez-Albaladejo E,Bani I.PLHC-1 topminnow liver cells: an alternative model to investigate the toxicity of plastic additives in the aquatic environment.Ecotoxicol Environ Saf2021;208:111746

[24] Pérez-Albaladejo E,Porte C.Plastics and plastic additives as inducers of oxidative stress.Curr Opin Toxicol2020;20-1:69-76

[25] Rios-Fuster B,Paniagua González G.Assessing microplastic ingestion and occurrence of bisphenols and phthalates in bivalves, fish and holothurians from a Mediterranean marine protected area.Environ Res2022;214:114034

[26] Gil-Solsona R,Muñoz-Mas R.A holistic assessment of the sources, prevalence, and distribution of bisphenol A and analogues in water, sediments, biota and plastic litter of the Ebro Delta (Spain).Environ Pollut2022;314:120310

[27] Prokić MD,Gavrić JP.Ecotoxicological effects of microplastics: examination of biomarkers, current state and future perspectives.TrAC Trend Anal Chem2019;111:37-46

[28] Prüst M,Westerink RHS.The plastic brain: neurotoxicity of micro- and nanoplastics.Part Fibre Toxicol2020;17:24 PMCID:PMC7282048

[29] Russo G,Mita DG.Occurrence of bisphenol A and its analogues in some foodstuff marketed in Europe.Food Chem Toxicol2019;131:110575

[30] Lee JG,Kim D,Kang Y.Assessment of tetrabromobisphenol and hexabromocyclododecanes exposure and risk characterization using occurrence data in foods.Food Chem Toxicol2020;137:111121

[31] Akhbarizadeh R,Rossi S.Emerging endocrine disruptors in two edible fish from the Persian Gulf: occurrence, congener profile, and human health risk assessment.Mar Pollut Bull2021;166:112241

[32] Capó X,Compa M.Quantification of differential tissue biomarker responses to microplastic ingestion and plasticizer bioaccumulation in aquaculture reared sea bream Sparus aurata.Environ Res2022;211:113063

[33] Mita L,Viggiano E.Bisphenol A content in fish caught in two different sites of the Tyrrhenian Sea (Italy).Chemosphere2011;82:405-10

[34] Estevez J.Model equations for the kinetics of covalent irreversible enzyme inhibition and spontaneous reactivation: esterases and organophosphorus compounds.Crit Rev Toxicol2009;39:427-48

[35] Fu H,Chen Y.Acetylcholinesterase is a potential biomarker for a broad spectrum of organic environmental pollutants.Environ Sci Technol2018;52:8065-74

[36] Fu J,Leed MGD,Marson L.Interspecies differences in the metabolism of a multiester prodrug by carboxylesterases.J Pharm Sci2016;105:989-95 PMCID:PMC4781669

[37] Tsugoshi Y,Tanikawa Y.Inhibitory effects of organophosphate esters on carboxylesterase activity of rat liver microsomes.Chem Biol Interact2020;327:109148

[38] Wheelock CE,Anderson BS,Miller MJ.Applications of carboxylesterase activity in environmental monitoring and toxicity identification evaluations (TIEs). In: Whitacre DM, editor. Reviews of environmental contamination and toxicology. New York: Springer; 2008. pp. 117-78.

[39] Marcos-López M,Rodger HD,MacCarthy E.Local and systemic humoral immune response in farmed Atlantic salmon (Salmo salar L.) under a natural amoebic gill disease outbreak.Fish Shellfish Immun2017;66:207-16

[40] Satoh T.The mammalian carboxylesterases: from molecules to functions.Annu Rev Pharmacol Toxicol1998;38:257-88

[41] Satoh T.Structure, function and regulation of carboxylesterases.Chem Biol Interact2006;162:195-211

[42] Zou LW,Wang DD.Carboxylesterase inhibitors: an update.Curr Med Chem2018;25:1627-49

[43] Ghodke VM.Environmental role of aromatic carboxylesterases.Environ Microbiol2022;24:2657-68

[44] Zhu G-F.Exposure of bisphenol A (BPA) derivatives affect the metabolic elimination of alzheimer’s diseases treatment drugs.Lat Am J Pharm2017;36:1753-9Available from: https://hero.epa.gov/hero/index.cfm/reference/details/reference_id/5498000 [Last accessed on 29 Feb 2024].

[45] Fukami T,Nakagawa N,Nakajima M.In vitro evaluation of inhibitory effects of antidiabetic and antihyperlipidemic drugs on human carboxylesterase activities.Drug Metab Dispos2010;38:2173-8

[46] Shimizu M,Nakajima M.Screening of specific inhibitors for human carboxylesterases or arylacetamide deacetylase.Drug Metab Dispos2014;42:1103-9

[47] Solé M.An in vitro screening with emerging contaminants reveals inhibition of carboxylesterase activity in aquatic organisms.Aquat Toxicol2015;169:215-22

[48] Liu YZ,Bai Y,Dong PP.Per- and polyfluoroalkyl substances exert strong inhibition towards human carboxylesterases.Environ Pollut2020;263:114463

[49] Nos D,Saiz E,Solé M.Tetrabromobisphenol A inhibits carboxylesterase activity of marine organisms from different trophic levels.Chemosphere2020;238:124592

[50] Albendín MG,Arellano JM.In vivo cholinesterase sensitivity of gilthead seabream (Sparus aurata) exposed to organophosphate compounds: influence of biological factors.Ecol Indic2021;121:107176

[51] Solé M,Mañanós E.Effects of selected xenobiotics on hepatic and plasmatic biomarkers in juveniles of Solea senegalensis.Environ Res2014;135:227-35

[52] Albendín MG,Coello MD.The effects of exposing Solea senegalensis to microbeads with and without pesticides.Water Air Soil Pollut2023;234:132

[53] Araújo MJ,Soares AMVM.Effects of triclosan on early development of Solea senegalensis: from biochemical to individual level.Chemosphere2019;235:885-99

[54] Abdel-Tawwab M.Effect of bisphenol A toxicity on growth performance, biochemical variables, and oxidative stress biomarkers of Nile tilapia, Oreochromis niloticus (L.).J Appl Ichthyol2018;34:1117-25

[55] de Oliveira Ferreira R,da Luz TM.First report on the toxicity of SARS-CoV-2, alone and in combination with polyethylene microplastics in neotropical fish.Sci Total Environ2023;882:163617 PMCID:PMC10122543

[56] Brandts I,Tvarijonaviciute A.Effects of polymethylmethacrylate nanoplastics on Dicentrarchus labrax.Genomics2018;110:435-41

[57] Barría C,Tort L,Teles M.Effect of nanoplastics on fish health and performance: a review.Mar Pollut Bull2020;151:110791

[58] Hemmert AC,Chica RA.Nerve agent hydrolysis activity designed into a human drug metabolism enzyme.PLoS One2011;6:e17441 PMCID:PMC3060870

[59] Hatfield MJ.Carboxylesterase inhibitors.Expert Opin Ther Pat2011;21:1159-71 PMCID:PMC3139797

[60] Sanahuja I,Ibarz A.Multi-organ characterisation of B-esterases in the European sea bass (Dicentrarchus labrax): effects of the insecticide fipronil at two temperatures.Aquat Toxicol2020;228:105617

[61] Salvaggio A,Krasakopoulou E.Biomarkers of exposure to chemical contamination in the commercial fish species Lepidopus caudatus (Euphrasen, 1788): a particular focus on plastic additives.Front Physiol2019;10:905 PMCID:PMC6646597

[62] Sole M,Labrada-Martagón V.Plasmatic B-esterases as potential biomarkers of exposure to marine plastics in loggerhead turtles.Environ Res2022;213:113639

[63] Solé M,Viñas L.Biomarker considerations in monitoring petrogenic pollution using the mussel Mytilus galloprovincialis.Environ Sci Pollut Res Int2020;27:31854-62

[64] Solé M,Mañanós E,García-Párraga D.Characterisation of plasmatic B-esterases in bottlenose dolphins (Tursiops truncatus) and their potential as biomarkers of xenobiotic chemical exposures.Environ Pollut2022;313:120149

[65] Omedes S,Escolar O,Freitas R.B-esterases characterisation in the digestive tract of the common octopus and the European cuttlefish and their in vitro responses to contaminants of environmental concern.Environ Res2022;210:112961

[66] Dallarés S,Sanahuja I.Multibiomarker approach to fipronil exposure in the fish Dicentrarchus labrax under two temperature regimes.Aquat Toxicol2020;219:105378

[67] Ellman GL,Andres V Jr.A new and rapid colorimetric determination of acetylcholinesterase activity.Biochem Pharmacol1961;7:88-95

[68] Hosokawa M.Measurement of carboxylesterase (CES) activities.Curr Protoc Toxicol2002;4:Unit4.7

[69] Mastropaolo W.An ultraviolet spectrophotometric assay for alpha-naphthyl acetate and alpha-naphthyl butyrate esterases.Anal Biochem1981;115:188-93

[70] Bradford MM.A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Anal Biochem1976;72:248-54

[71] Benabent M,Mangas I,Estévez J.Interaction between substrates suggests a relationship between organophosphorus-sensitive phenylvalerate- and acetylcholine-hydrolyzing activities in chicken brain.Toxicol Lett2014;230:132-8

[72] Mangas I,Estévez J.Phenyl valerate esterase activity of human butyrylcholinesterase.Arch Toxicol2017;91:3295-305

[73] Varò I,Amat F.Effect of dichlorvos on cholinesterase activity of the European sea bass (Dicentrarchus labrax).Pestic Biochem Phys2003;75:61-72

[74] Leticia AG.Determination of esterase activity and characterization of cholinesterases in the reef fish Haemulon plumieri.Ecotoxicol Environ Saf2008;71:787-97

[75] Soto-Mancera F,Albendín MG.Carboxylesterase in Sparus aurata: characterisation and sensitivity to organophosphorus pesticides and pharmaceutical products.Ecol Indic2020;109:105603

[76] Valbonesi P,Mattioli M,Fabbri E.Cholinesterase activities and sensitivity to pesticides in different tissues of silver European eel, Anguilla anguilla.Comp Biochem Physiol C2011;154:353-9

[77] Solé M,Varó I.Characterization of type “B” esterases and hepatic CYP450 isoenzimes in Senegalese sole for their further application in monitoring studies.Ecotoxicol Environ Saf2012;78:72-9

[78] Koenig S,Solé M.Comparative xenobiotic metabolism capacities and pesticide sensitivity in adults of Solea solea and Solea senegalensis.Comp Biochem Physiol C2013;157:329-36

[79] Crespo M.The use of juvenile Solea solea as sentinel in the marine platform of the Ebre Delta: in vitro interaction of emerging contaminants with the liver detoxification system.Environ Sci Pollut Res Int2016;23:19229-36

[80] Kristoff G,Cacciatore LC,Cochón AC.In vivo studies on inhibition and recovery of B-esterase activities in Biomphalaria glabrata exposed to azinphos-methyl: analysis of enzyme, substrate and tissue dependence.Aquat Toxicol2012;112-3:19-26

[81] Brandts I,Martins MA.A baseline study on the impact of nanoplastics on the portals of entry of xenobiotics in fish.Mar Pollut Bull2021;173:113018

[82] Balasch JC,Barría C.Short-term exposure to polymethylmethacrylate nanoplastics alters muscle antioxidant response, development and growth in Sparus aurata.Mar Pollut Bull2021;172:112918

[83] Nos D,Solé M.The influence of ecological factors in the modulation of pollution biomarkers of two small pelagic marine fish.Mar Pollut Bull2023;188:114717

[84] Ribalta C,Sole M.Hepatic biotransformation and antioxidant enzyme activities in Mediterranean fish from different habitat depths.Sci Total Environ2015;532:176-83

[85] Schmidt N,Oursel B.Phthalates and organophosphate esters in surface water, sediments and zooplankton of the NW Mediterranean Sea: Exploring links with microplastic abundance and accumulation in the marine food web.Environ Pollut2021;272:115970

[86] Rios-Fuster B,García-Marcos K.Experimental evidence of physiological and behavioral effects of microplastic ingestion in Sparus aurata.Aquat Toxicol2021;231:105737

[87] Alomar C,Compa M.Microplastic ingestion in reared aquaculture fish: biological responses to low-density polyethylene controlled diets in Sparus aurata.Environ Pollut2021;280:116960

[88] Rodríguez-Romeu O,Padrós F.Assessment of the health status of the European anchovy (Engraulis encrasicolus) in the NW Mediterranean Sea from an interdisciplinary approach and implications for food safety.Sci Total Environ2022;841:156539

[89] Wang YQ,Cao J.Exploring the interactions of decabrominateddiphenyl ether and tetrabromobisphenol A with human serum albumin.Environ Toxicol Pharmacol2014;38:595-606