Abstract
Introduction
This study aimed to analyze antioxidant responses and oxidative damage induced by two inorganic forms of arsenic (As; AsIII and AsV) in an estuarine polychaete species, Laeonereis acuta (Nereididae). The capacity of arsenic biotransformation was also evaluated through the methylation process considering the activity of a key enzyme involved in the metabolization process.
Materials and methods
Worms were exposed to 50 μg (AsIII or AsV)/l during 2 or 7 days, plus a control group. Endpoints analyzed included concentration of reactive oxygen species (ROS), activities of antioxidant enzymes such as glutathione reductase (GR), total glutathione-S-transferase (GST), and omega isoform (GST Ω), glucose-6-phosphate deshydrogenase (G6PDH), levels of the antioxidant glutathione (GSH), and lipid peroxides concentration (TBARS).
Results and discussion
Results showed: (1) GR inhibition after 2-day exposure to both As forms (p < 0.05); (2) GST Ω inhibition after 7-day exposure to AsIII paralleled by an increase in total GST activity (p < 0.05); (3) augmented G6PDH activity after 7-day exposure to both As forms (p < 0.05); (4) no differences in terms of ROS and TBARS; and (5) inhibition of GST Ω activity in AsIII exposed worms, which was concomitant with a lowering of mono- and dymethylated arsenic species.
Conclusion
These results confirm the reactivity of some biochemical variables of L. acuta to As and indicates its importance as a sentinel species in estuarine regions with presence of arsenic.
Similar content being viewed by others
References
Agusa T, Takagi K, Kubota R, Anan Y, Iwata H, Tanabe S (2008) Specific accumulation of arsenic compounds in green turtles (Chelonia mydas) and hawksbill turtles (Eretmochelys imbricata) from Ishigaki Island, Japan. Environ Pollut 153:127–136
Akter KF, Owens G, Davey DE, Naidu R (2005) Arsenic speciation and toxicity in biological systems. Environ Contam Toxicol 184:97–149
Amado LL, Longaray Garcia M, Ramos PB, Freitas RF, Zafalon B, Ribas Ferreira JL, Yunes JS, Monserrat JM (2009) A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity. Sci Total Environ 407:2115–2123
Aposhian HV, Zakharyan RA, Avran MD, Sampayo-Reyes A, Wollenberg ML (2004) A review of the enzymology of arsenic metabolism and new potential role of hydrogen peroxide in the detoxication of the trivalent species. Toxicol Appl Pharmacol 198:319–326
Bagnyukova TV, Luzhna LI, Pogribny IP, Lushchak VI (2007) Oxidative stress and antioxidant defenses in goldfish liver in response to short-term exposure to arsenite. Environ Mol Mutagen 48:658–665
Bhattacharya A, Bhattacharya S (2007) Induction of oxidative stress by arsenic in Clarias batrachus: involvement of peroxisomes. Ecotoxicol Environ Saf 68:178–187
Carvalho CS, Fernandes MN (2007) Effect of copper on liver key enzymes of anaerobic glucose metabolism from freshwater tropical fish Prochilus lineatus. Comp Biochem Physiol 151:437–442
Chowdhury UK, Zakharyan RA, Hernandez A, Avran MD, Koplin MJ, Aposhian HV (2006) Glutathione-S-transferase-omega [MMA(V) reductase] knockout mice: enzyme and arsenic species concentrations in tissues after arsenate administration. Toxicol Appl Pharmacol 216:446–457
Culioli J, Calendini S, Mori C, Orsini A (2009) Arsenic accumulation in a freshwater fish living in a contaminated river of Corsica, France. Ecotoxicol Environ Saf 72:1440–1445
Fattorini D, Regoli F (2004) Arsenic speciation in tissues of the Mediterranean polychaete Sabella spallanzanii. Environ Toxicol Chem 23:1881–1887
Fattorini D, Notti A, Halt MN, Gambi MC, Regoli F (2005) Levels and chemical speciation of arsenic in polychaetes: a review. Mar Ecol 26:255–264
Fattorini D, Notti A, Regoli F (2006) Characterization of arsenic content in marine organisms from temperate, tropical, and polar environments. Chem Ecol 22:405–414
Fattorini D, Notti A, Mento R, Cicero AM, Gabellini M, Russo A, Regoli F (2008) Seasonal, spatial and inter-annual variations of trace metals in mussels from the Adriatic Sea: a regional gradient for arsenic and implications for monitoring the impact of off-shore activities. Chemosphere 72:1524–1533
Ferreira-Cravo M, Reinhardt Piedras F, Moraes TB, Ferreira JLR, Salomão DPF, Dornelles Machado M, Geracitano LA, Monserrat JM (2007) Antioxidant responses and reactive oxygen species generation in different body regions of the estuarine polychaeta Laeonereis acuta (Nereididae). Chemosphere 66:1367–1374
Ferreira-Cravo M, Ventura-Lima J, Sandrini JZ, Amado LL, Geracitano LA, Rebelo M, Bianchini A, Monserrat JM (2009) Antioxidant responses in different body regions of the polychaeta Laeonereis acuta (Nereididae) exposed to copper. Ecotoxicol Environ Saf 72:388–393
Francesconi KA, Edmonds JS (1997) Arsenic and marine organisms. Adv Inorg Chem 31:111–151
Franco JL, Trivella DBB, Trevisan R, Dinslaken DF, Marques MRF, Bainy ACD, Dafre AL (2006) Antioxidant status and stress proteins in the gills of the brown mussel Perna perna exposed to zinc. Chem Biol Int 160:232–240
Geiszinger AE, Goesslerb W, Francesconia KA (2002) The marine polychaete Arenicola marina: its unusual arsenic compound pattern and its uptake of arsenate from seawater. Mar Environ Res 53:37–50
Geracitano LA, Bocchetti R, Monserrat JM, Regoli F, Bianchini A (2004) Oxidative stress responses in two populations of Laeonereis acuta (Polychaeta, Nereididae) after acute and chronic exposure to copper. Mar Environ Res 58:1–17
Habig NH, Jakoby WB (1981) Assays for differentiation of glutathione-S-transferase. Meth Enzymol 77:398–405
Habuda-Stanić M, Kuleš M, Kalajdžić B, Romić Ž (2007) Quality of groundwater in eastern Croatia. The problem of arsenic pollution. Desalination 210:157–162
Hornhardt S, Gomolka M, Walsh L, Jung T (2006) Comparative investigation of sodium arsenite, arsenic trioxide and cadmium sulphate in combination with gamma-radiation on apoptosis, micronuclei induction and DNA damage in human lymphoblastoid cell line. Fund Mol Mechan Mut 600:165–172
Kitchin KT (2001) Recent advances in As carcinogenesis: modes of action, animal models systems and methylated As metabolites. Toxicol Appl Pharmacol 172:249–261
Mrak T, Slejkovec Z, Jeran Z, Jacimovic R, Kastelec D (2008) Uptake and biotransformation of arsenate in the lichen Hypogymnia physodes (L.) Nyl. Environ Pollut 151:300–307
Mirlean N, Roseiberg A (2006) The effect of emissions of fertilizer production on the environment contamination by cadmium and arsenic in southern Brazil. Environ Pollut 143:335–340
Mirlean N, Andrus VE, Baisch P, Griep G, Casartelli MR (2003) Arsenic pollution in Patos Lagoon estuarine sediments, Brazil. Mar Pollut Bull 46:1480–1484
Notti A, Fattorini D, Razzetti EM, Regoli F (2007) Bioaccumulation and biotransformation of arsenic in the Mediterranean polychaete Sabella spallanzanii: experimental observations. Environ Toxicol Chem 26:1186–1191
Oakes KD, Kraak GJV (2003) Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquat Toxicol 63:447–460
O’Connor TP, Lauenstein GG (2006) Trends in chemical concentrations in mussels and oysters collected along the US coast: update to 2003. Mar Environ Res 62:261–285
Ramanathan K, Shila S, Kumaran S, Panneerselvan C (2003) Ascorbic acid and α-tocopherol as potent modulators on As induced toxicity in mitochondria. J Nutr Biochem 14:416–420
Regoli F, Winston GW (1999) Quantification of total oxidant scavenging capacity of antioxidants for peroxynitrite, peroxyl radicals, and hydroxyl radicals. Toxicol Appl Pharmacol 156:96–105
Sampayo-Reyes A, Zakharyan RA (2006) Inhibition of human glutathione S-transferase omega by tocopherol succinate. Biomed Pharmacother 60:238–244
Sandrini JZ, Ventura-Lima J, Regoli F, Fattorini D, Notti A, Marins LF, Monserrat JM (2008) Antioxidant responses in the nereidid Laeonereis acuta (Annelida, Polychaeta) after cadmium exposure. Ecotoxicol Environ Saf 70:115–120
Thomas DJ (2007) Molecular process in cellular arsenic metabolism. Toxicol Appl Pharmacol 222:365–393
Tseng C (2004) The potential biological mechanism of arsenic-induced diabetes mellitus. Toxicol Appl Pharmacol 197:67–83
Vahter M (2002) Mechanisms of arsenic biotransformation. Toxicology 181:211–217
Ventura-Lima J, Sandrini JZ, Ferreira-Crav M, Piedras FR, Moraes TB, Fattorini D, Notti A, Regoli F, Geracitano LA, Marins LF, Monserrat JM (2007) Toxicological responses in Laeonereis acuta (Annelida, Polychaeta) after arsenic exposure. Environ Int 33:559–564
Ventura-Lima J, Fattorini D, Regoli F, Monserrat JM (2009a) Effects of different inorganic arsenic species in Cyprinus carpio (Cyprinidae) tissues after short-time exposure: bioaccumulation, biotransformation and biological responses. Environ Pollut 157:3479–3484
Ventura-Lima J, Castro MR, Acosta D, Fattorini D, Regoli F, Carvalho LM, Bohrer D, Geracitano LA, Barros DM, Silva RS, Bonan CD, Bogo MR, Monserrat JM (2009b) Effects of arsenic (As) exposure on the antioxidant status of gills of the zebrafish Danio rerio (Cyprinidae). Comp Biochem Physiol C149:538–543
White CC, Viernes H, Krejsa CM, Botta D, Kavanagh TJ (2003) Fluorescence-based microtiter plate assay for glutamate–cysteine ligase activity. Anal Biochem 318:175–180
Winston GW, Regoli F, Dugas AJ Jr, Fong JH, Blanchard KA (1998) A rapid gas chromatographic assay for determining oxyradical scavenging capacity of antioxidants and biological fluids. Free Radic Biol Med 24:480–493
Zar J (1984) Biostatistical analysis. Prentice Hall, New Jersey
Grants, sponsors, and funding sources
The authors wish to thank the Brazilian Agency CNPq that funded a short-time fellowship to J. Ventura-Lima to stay in Dr. Regoli lab. (process 200603/2008-6, SWE program). J.M. Monserrat is a research fellow funded by CNPq (process 304917/2006-0). J. Ventura-Lima is a graduate fellow from the Brazilian Agency CAPES. J. Ventura-Lima acknowledges the post-doctoral fellow from Programa Ciências do Mar - Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brasília, DF, Brasil.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Vera Slaveykova
Rights and permissions
About this article
Cite this article
Ventura-Lima, J., Ramos, P.B., Fattorini, D. et al. Accumulation, biotransformation, and biochemical responses after exposure to arsenite and arsenate in the estuarine polychaete Laeonereis acuta (Nereididae). Environ Sci Pollut Res 18, 1270–1278 (2011). https://doi.org/10.1007/s11356-011-0478-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-011-0478-4