Modulation of metallothionein, pi-GST and Se-GPx mRNA expression in the freshwater bivalve <em>Dreissena polymorpha</em> transplanted into polluted areas

Périne Doyen; Etienne Morhain; François Rodius; Périne Doyen; Etienne Morhain; François Rodius

doi:10.3934/environsci.2015.2.333

AIMS Environmental Science

2015, Volume 2, Issue 2: 333-344. doi: 10.3934/environsci.2015.2.333

Previous Article Next Article

Research article

Modulation of metallothionein, pi-GST and Se-GPx mRNA expression in the freshwater bivalve Dreissena polymorpha transplanted into polluted areas

1.
Université du Littoral Côte d'Opale, Institut Charles Viollette, Equipe Biochimie des Produits Aquatiques (BPA), Boulevard du Bassin Napoléon, 62327 Boulogne-sur-Mer, France;
2.
Universitéde Lorraine, UMR CNRS 7360 : Laboratoire Interdisciplinaire des Environnements Continentaux (LIEC), Rue Delestraint, 57070 Metz, France

Received: 22 January 2015 Accepted: 23 April 2015 Published: 27 April 2015

Glutathione S-transferases (GST), glutathione peroxidases (GPx) and metallothioneins (MT) are essential components of cellular detoxication systems. We studied the expression of pi-GST, Se-GPx, and MT transcripts in the digestive gland of Dreissena polymorpha exposed to organic and metallic pollutants. Mussels from a control site were transplanted during 3, 15 and 30 days into the Moselle River, upstream and downstream to the confluence with the Fensch River, a tributary highly polluted by polycyclic aromatic hydrocarbons and heavy metals. Se-GPx and pi-GST mRNA expression increased in mussels transplanted into the upstream site, Se-GPx response being the earliest. These genes were also induced after 3-days exposure at the downstream site. These inductions suggest an adaptative response to an alteration of the environment. Moreover, at this site, a significant decrease of the expression of MT, pi-GST and Se-GPx transcripts was observed after 30 days which could correspond to an inefficiency of detoxification mecanisms. The results are in correlation with the levels of pollutants in the sediments and their bioaccumulation in mussels, they confirm the environmental deleterious impact of the pollutants carried by the Fensch River.

Keywords:

Citation: Périne Doyen, Etienne Morhain, François Rodius. Modulation of metallothionein, pi-GST and Se-GPx mRNA expression in the freshwater bivalve Dreissena polymorpha transplanted into polluted areas[J]. AIMS Environmental Science, 2015, 2(2): 333-344. doi: 10.3934/environsci.2015.2.333

Related Papers:

[1]	Fernanda P. Maciel, Joshua M. Peschel . A GIS-based tool for bioaccumulation risk analysis and its application to study polychlorinated biphenyls in the Great Lakes. AIMS Environmental Science, 2018, 5(1): 1-23. doi: 10.3934/environsci.2018.1.1
[2]	Hedi Januar, Dwiyitno, Izhamil Hidayah, Irma Hermana . Seasonal heavy metals accumulation in the soft tissue of Anadara granosa mollusc form Tanjung Balai, Indonesia. AIMS Environmental Science, 2019, 6(5): 356-366. doi: 10.3934/environsci.2019.5.356
[3]	Marcos André dos Santos, Alfredo Jarma-Orozco, Flavio Lozano-Isla, José Nailson S. Barros, Jesús Rivera, Carlos Espitia-Romero, Ángela Castillejo-Morales, Betty Jarma-Arroyo, Marcelo Francisco Pompelli . Leaf area estimation in Jatropha curcas (L.): an update. AIMS Environmental Science, 2018, 5(5): 353-371. doi: 10.3934/environsci.2018.5.353
[4]	Nurul Akhma Zakaria, A.A. Kutty, M.A. Mahazar, Marina Zainal Abidin . Arsenic acute toxicity assessment on select freshwater organism species in Malaysia. AIMS Environmental Science, 2016, 3(4): 804-814. doi: 10.3934/environsci.2016.4.804
[5]	Navid Ahmadi, Mozhgan Ahmadi Nadoushan, Mohammad Hadi Abolhasani, Abbas Hosseini . Investigating the efficiency of biological treatment process of oil pollutants using mix of Scenedesmus obliquus and Chlamydomonas reinhardtii algae: A case study. AIMS Environmental Science, 2021, 8(3): 221-237. doi: 10.3934/environsci.2021015
[6]	Kayla L. Penta, Diego Altomare, Devon L. Shirley, Jennifer F. Nyland . Female immune system is protected from effects of prenatal exposure to mercury. AIMS Environmental Science, 2015, 2(3): 448-463. doi: 10.3934/environsci.2015.3.448
[7]	Alma Sobrino-Figueroa, Sergio H. Álvarez Hernandez, Carlos Álvarez Silva C . Evaluation of the freshwater copepod Acanthocyclops americanus (Marsh, 1983) (Cyclopidae) response to Cd, Cr, Cu, Hg, Mn, Ni and Pb. AIMS Environmental Science, 2020, 7(6): 449-463. doi: 10.3934/environsci.2020029
[8]	B. Ravit, K. Cooper, G. Moreno, B. Buckley, I. Yang, A. Deshpande, S. Meola, D. Jones, A. Hsieh . Microplastics in urban New Jersey freshwaters: distribution, chemical identification, and biological affects. AIMS Environmental Science, 2017, 4(6): 809-826. doi: 10.3934/environsci.2017.6.809
[9]	Muhammad Rendana, Wan Mohd Razi Idris, Sahibin Abdul Rahim . Clustering analysis of PM2.5 concentrations in the South Sumatra Province, Indonesia, using the Merra-2 Satellite Application and Hierarchical Cluster Method. AIMS Environmental Science, 2022, 9(6): 754-770. doi: 10.3934/environsci.2022043
[10]	Xiaojun Liu, Ikbel Souli, Mohamad-Amr Chamaa, Thomas Lendormi, Claire Sabourin, Yves Lemée, Virginie Boy, Nizar Chaira, Ali Ferchichi, Pascal Morançais, Jean-Louis Lanoisellé . Effect of thermal pretreatment at 70 °C for one hour (EU hygienization conditions) of various organic wastes on methane production under mesophilic anaerobic digestion. AIMS Environmental Science, 2018, 5(2): 117-129. doi: 10.3934/environsci.2018.2.117

Abstract

References

[1]	Roméo M, Hoarau P, Garello G, et al. (2003) Mussel transplantation and biomarkers as useful tools for assessing water quality in the NW Mediterranean. Environ Pollut 122: 369-378. doi: 10.1016/S0269-7491(02)00303-2
[2]	Guerlet E, Ledy K, Meyer A, et al. (2007) Towards a validation of a cellular biomarker suite in native and transplanted zebra mussels: A 2-year integrative field study of seasonal and pollution-induced variations. Aquat Toxicol 81: 377-388. doi: 10.1016/j.aquatox.2006.12.016
[3]	Viarengo A, Lowe D, Bolognesi C, et al. (2007) The use of biomarkers in biomonitoring: A 2-tier approach assessing the level of pollutant-induced stress syndrome in sentinel organisms. Comp Biochem Physiol C Toxicol Pharmacol 146: 281-300. doi: 10.1016/j.cbpc.2007.04.011
[4]	Borcherding J (2010) Steps from ecological and ecotoxicological research to the monitoring for water quality using the zebra mussel in a biological warning system, In: Van der Velde G, Rajagopal S and bij de Vaate, A The Zebra Mussel in Europe, Leiden/Margraf, Weikersheim: Backhuys, 279-283.
[5]	Voets J, Bervoets L, Smolders R, et al. (2010) Biomonitoring environmental pollution in freshwater ecosystems using Dreissena polymorpha, In: Van der Velde G, Rajagopal S and bij de Vaate, A The Zebra Mussel in Europe, Leiden/Margraf, Weikersheim: Backhuys, 301-321.
[6]	Chatel A, Faucet-Marquis V, Gourlay-Francé C, et al. (2015) Genotoxicity and activation of cellular defenses in transplanted zebra mussels Dreissena polymorpha along the Seine River. Ecotoxicol Environ Saf 114: 241-249. doi: 10.1016/j.ecoenv.2014.03.023
[7]	Almar M, Otero L, Santos C, et al. (1998) Liver glutathione content and glutathione-dependent enzymes of two species of freshwater fish as bioindicators of chemical pollution. J Environ Sci Health 33: 769-783. doi: 10.1080/03601239809373177
[8]	Viarengo A, Nott JA (1993) Mechanisms of heavy metal cation homeostasis in marine invertebrates. Comp Biochem Physiol C Toxicol Pharmacol 104: 355-372. doi: 10.1016/0742-8413(93)90001-2
[9]	Roesijadi D (1996) Metallothionein and its role in toxic metal regulation. Comp Biochem Physiol C Toxicol Pharmacol 113: 117-123.
[10]	Lemoine S, Laulier M (2003) Potential use of the levels of the mRNA of a specific metallothionein isoform (MT-20) in mussel (Mytilus edulis) as a biomarker of cadmium contamination. Mar Pollut Bull 46: 1450-1455. doi: 10.1016/S0025-326X(03)00283-2
[11]	Mourgaud Y, Martinez E, Geffard A, et al. (2002) Metallothionein concentration in the mussel Mytilus galloprovincialis as a biomarker of response to metal contamination: validation in the field. Biomarkers 7: 479-490. doi: 10.1080/1354750021000034528
[12]	Rodius F, Hammer C, Vasseur P (2002). Use of RNA arbitrarily primed PCR to identify genomic alterations in the digestive gland of the freshwater bivalve Unio tumidus at a contaminated site. Environ Toxicol 17: 538-546. doi: 10.1002/tox.10090
[13]	Engelken J, Hildebrandt A (1999) cDNA cloning and cadmium-induced expression of metallothionein mRNA in the zebra mussel Dreissena polymorpha. Biochem Cell Biol 77: 237-241. doi: 10.1139/bcb-77-3-237
[14]	Doyen P, Bigot A, Vasseur P, et al. (2008) Molecular cloning and expression study of pi-class glutathione S-transferase (pi-GST) and selenium-dependent glutathione peroxidase (Se-GPx) transcripts in the freshwater bivalve Dreissena polymorpha. Comp Biochemi Physiol C Toxicol Pharmacol 147: 69-77. doi: 10.1016/j.cbpc.2007.08.002
[15]	Snell TW, Brogdon SE, Morgan MB (2003) Gene expression profiling in ecotoxicology. Ecotoxicology 12: 475-483. doi: 10.1023/B:ECTX.0000003033.09923.a8
[16]	Sarkar A, Ray D, Shrivastava AN, et al. (2006) Molecular Biomarkers: their significance and application in marine pollution monitoring. Ecotoxicology 15: 333-340. doi: 10.1007/s10646-006-0069-1
[17]	Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2^-∆∆Ctmethod. Methods 25: 402-8. doi: 10.1006/meth.2001.1262
[18]	R, Developement Core Team (2006) R: A 701 language and environment for statistical 702 computing. R foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0
[19]	Mazauer P, Matte JL (2001) Qualité du milieu physique de la Fensch – synthèse. Direction Régionale de l'Environnement de Lorraine, France.
[20]	Agences de l'Eau (2003) Seuils de qualité pour les micropolluants organiques et minéraux dans les eaux superficielles-synthèse, In: Agences de l'Eau, Système d'Evaluation de la Qualité de l'Eau, Paris, France.
[21]	Bigot A, Minguez L, Giamberini L, et al. (2011) Early defense responses in the freshwater bivalve Corbicula fluminea exposed to copper and cadmium: transcriptional and histochemical studies. Environ Toxicol 26: 623-632. doi: 10.1002/tox.20599
[22]	Cossu C, Doyotte A, Jacquin MC, et al. (1997) Glutathione reductase, selenium-dependent glutathione peroxidase, glutathione levels, and lipid peroxidation in freshwater bivalves, Unio tumidus, as biomarkers of aquatic contamination in field studies. Ecotoxicol Environ Saf 38: 122-131. doi: 10.1006/eesa.1997.1582
[23]	Suteau P, Daubeze M, Migaud ML, et al. (1988) PAH metabolising enzymes in whole mussel as biochemical tests for chemical pollution monitoring. Mar Ecol Prog Ser 46: 45-49. doi: 10.3354/meps046045
[24]	Livingstone DR, Martinez PG, Michel X, et al. (1990) Oxyradical production as a pollution-mediated mechanism of toxicity in the common mussel, Mytilus edulis L., and other molluscs. Funct Ecol 4: 415-424. doi: 10.2307/2389604
[25]	Livingstone DR (1998) The fate of organic xenobiotics in aquatic ecosystems: quantitative and qualitative differences in biotransformation by invertebrates and fish. Comp Biochem Physiol A Mol Integr Physiol 120: 43-49. doi: 10.1016/S1095-6433(98)10008-9
[26]	Sole M, Porte C, Albaiges J (1994) Mixed-function oxygenase system components and antioxidant enzymes in different marine bivalves: its relation with contaminants body burdens. Aquat Toxicol 30: 271-283. doi: 10.1016/0166-445X(94)90064-7
[27]	Chatel A, Faucet-Marquis V, Perret M, et al. (2012) Genotoxicity assessement and detoxification induction in Dreissena polymorpha exposed to benzo[a]pyrene. Mutagenesis 27: 703-711. doi: 10.1093/mutage/ges036
[28]	Chatel A, Faucet-Marquis V, Pfohl-Leszkowicz A, et al. (2014) DNA adduct formation and induction of detoxification mechanisms in Dreissena polymorpha exposed to nitro-PAHs. Mutagenesis 29: 457-465. doi: 10.1093/mutage/geu040
[29]	Bebianno MJ, Langston WJ (1992) Cadmium induction of metallothionein synthesis in Mytilus galloprovincialis. Comp Biochem Physiol C Toxicol Pharmacol 103: 79-85. doi: 10.1016/0742-8413(92)90231-U
[30]	Imagawa M, Osada S, Koyama Y, et al. (1991) SF-B that binds to a negative element in glutathions transferase P gene is similar or identical to trans-activator LAP/IL6-DBP. Biochem Biophys Res Commun 179: 293-300. doi: 10.1016/0006-291X(91)91368-M
[31]	Robillard S, Beauchamp G, Laulier M (2003) The role of abiotic factors and pesticide levels on enzymatic activity in the freshwater mussel Anodonta cygnea at three different exposure sites. Comp Biochem Physiol C Toxicol Pharmacol 135: 49-59. doi: 10.1016/S1532-0456(03)00049-8
[32]	Kamel N, Jebali J, Banni M, et al. (2012) Biochemical responses and metals levels in Ruditapes decussatus after exposure to treated municipal effluents. Ecotox Env Saf 82: 40-46. doi: 10.1016/j.ecoenv.2012.05.008
[33]	Radwan MA, El-Gendy KS, Gad AF (2010) Oxidative stress biomarkers in the digestive gland of Theba pisana exposed to heavy metals. Arch Environ Contam Toxicol 58: 828-835. doi: 10.1007/s00244-009-9380-1
[34]	Brown RJ, Galloway TS, Lowe D, et al. (2004) Differential sensitivity of three marine invertebrates to copper assessed using multiple biomarkers. Aquat Toxicol 66: 267-278. doi: 10.1016/j.aquatox.2003.10.001
[35]	Ciacci C, Barmo C, Gallo G, et al. (2012) Effects of sublethal, environmentally relevant concentrations of hexavalent chromium in the gills of Mytilus galloprovincialis. Aquat Toxicol 120: 109-118.
[36]	David E, Tanguy A, Riso R, et al. (2012) Responses of Pacific oyster Crassostrea gigas populations to abiotic stress in environmentally contrasted estuaries along the Atlantic coast of France. Aquat Toxicol 109: 70-79. doi: 10.1016/j.aquatox.2011.11.014
[37]	Geret F, Serafim A, Bebianno J (2003) Antioxidant enzyme activities metallothioneins and lipid peroxidation as biomarkers in Ruditapes decussatus? Ecotoxicology 12: 417-426. doi: 10.1023/A:1026108306755
[38]	Kucuksezgin F, Kayatekin BM, Uluturhan E, et al. (2008) Preliminary investigation of sensitive biomarkers of trace metal pollution in mussel (Mytilus galloprovincialis) from Izmir Bay (Turkey). Environ Monit Assess 141: 339-345. doi: 10.1007/s10661-007-9900-2
[39]	Cheung CCC, Zheng GJ, Li AM, et al. (2001) Relationships between tissue concentrations of polycyclic aromatic hydrocarbons and antioxidative responses of marine mussels, Perna viridis. Aquat Toxicol 52: 189-203. doi: 10.1016/S0166-445X(00)00145-4
[40]	Remacle J, Lambert D, Raes M, et al. (1992) Importance of various antioxidant enzymes for cell stability. Confrontation between theoretical and experimental data. Biochem J 286: 41-46.
[41]	Regoli F (2000) Total oxyradical scavenging capacity (TOSC) in polluted and translocated mussels: a predictive biomarker of oxidative stress. Aquat Toxicol 50: 351-61. doi: 10.1016/S0166-445X(00)00091-6
[42]	Doyotte A, Cossu C, Jacquin MC, et al. (1997) Antioxidant enzymes, glutathione and lipid peroxidation as relevant biomarkers of experimental or field exposure in the gills and the digestive gland of the freshwater bivalve Unio tumidus. Aquatic Toxicol 39: 93-110. doi: 10.1016/S0166-445X(97)00024-6

This article has been cited by:

1.	Neila Drira, John H. Trefry, Robert P. Trocine, Interrelationships among trace metals and metallothionein in digestive glands and gills for field samples of Merceneria merceneria , 2017, 24, 0944-1344, 27897, 10.1007/s11356-017-0368-5
2.	Violetta Aru, Giorgia Sarais, Francesco Savorani, Søren Balling Engelsen, Flaminia Cesare Marincola, Metabolic responses of clams, Ruditapes decussatus and Ruditapes philippinarum , to short-term exposure to lead and zinc, 2016, 107, 0025326X, 292, 10.1016/j.marpolbul.2016.03.054
3.	Amarachi P. Onyena, Cathrine S. Manohar, Joseph A. Nkwoji, Lucian O. Chukwu, Characterization of the molecular differential responses in marine benthic macroinvertebrates exposed to polycyclic aromatic hydrocarbons, 2023, 1386-2588, 10.1007/s10452-023-10064-4
4.	Tetiana Matskiv, Viktoria Martyniuk, Vira Khoma, Kateryna Yunko, Kateryna Orlova-Hudim, Lesya Gnatyshyna, Alain Geffard, Melissa Palos-Ladeiro, Oksana Stoliar, Biochemical basis of resistance to multiple contaminations in the native and invasive populations of Dreissena polymorpha, 2024, 276, 15320456, 109803, 10.1016/j.cbpc.2023.109803

Reader Comments

Your name:*

Email:*
© 2015 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)