Abstract
This study aimed to assess the mechanisms of innate immune function responses to silica-coated iron oxide nanoparticle functionalized with dithiocarbamate groups (IONP) exposure alone and its associated mercury (Hg) in European eel (Anguilla anguilla L.) phagocytes isolated from peritoneum (P-phagocytes), gill (G-phagocytes), head kidney (HK-phagocytes) and spleen (S-phagocytes). The study evaluated viability, phagocytosis, oxidative burst activity (OBA) and lipid peroxidation (LPO). Four groups were made: (1) 2 × 106 phagocytes + RPMI-1640 (control), (2) 2 × 106 phagocytes + IONP (2.5 mg L−1), (3) 2 × 106 phagocytes + Hg (50 μg L−1) and (4) 2 × 106 phagocytes + IONP + Hg. Samplings were performed at 0, 2, 4, 8, 16, 24, 48 and 72 h of exposure. A. anguilla P-, G-, HK- and S-phagocytes in vitro exposure to IONP alone revealed either increased (except HK-phagocytes at 16 h) or no change in viability, suggesting that the cells are metabolically active and resistant to IONP exposure alone. In terms of phagocytes overactivation and reactive oxygen species (ROS) production as an indirect mechanism of immunotoxicity, the phagocytes responded in the following manner: P- > S- > HK- = G-phagocytes for IONP exposure alone, S- > HK- > P- = G-phagocytes for Hg exposure alone and HK- > G- = S- > P-phagocytes for concomitant exposure. Overall, considering Hg as a surrogate for metals and its association with IONP, as well as the likelihood that it could pose a serious threat to aquatic organisms by modulating their immune defense mechanisms if accidentally discharged into the aquatic environment, current results suggest that the step of IONP–metal complex removal must not be underrated and should be processed without any more ado.
Similar content being viewed by others
References
Ahmad I, Fatima M, Athar M, Khan NZ, Raisuddin S (1998) Responses of circulating fish phagocytes to paper mill effluent exposure. Bull Environ Contam Toxicol 61:746–753
Ahmad I, Hamid T, Fatima M, Chand HS, Jain SK, Athar M, Raisuddin S (2000) Induction of hepatic antioxidants in freshwater catfish (Channa punctatus Bloch) is a biomarker of paper mill effluent exposure. Biochim Biophys Acta (BBA) 1523:37–48
Ahmad I, Pacheco M, Santos MA (2003) Naphthalene-induced differential tissue damage association with circulating fish phagocyte induction. Ecotoxicol Environ Saf 54:7–15
Ahmad I, Pacheco M, Santos MA (2004) Enzymatic and nonenzymatic antioxidants as an adaptation to phagocyte-induced damage in Anguilla anguilla L. following in situ harbor water exposure. Ecotoxicol Environ Saf 57:290–302
Ahmad I, Coelho JP, Mohmood I, Pacheco M, Santos MA, Duarte AC, Pereira E (2011a) Immunosuppression in the infaunal bivalve Scrobicularia plana environmentally exposed to mercury and association with its accumulation. Chemosphere 82:1541–1546
Ahmad I, Mohmood I, Mieiro CL, Coelho JP, Pacheco M, Santos MA, Duarte AC, Pereira E (2011b) Lipid peroxidation versus antioxidant modulation in the bivalve Scrobicularia plana in response to environmental mercury—organ specificities and age effect. Aquat Toxicol 103:150–158
Ahmad I, Coelho J, Mohmood I, Anjum NA, Pacheco M, Santos MA, Duarte AC, Pereira E (2012) Mercury contaminated systems under recovery can represent an increased risk to seafood human consumers—a paradox depicted in bivalves’ body burdens. Food Chem 133:665–670
Ambashta RD, Sillanpaa M (2010) Water purification using magnetic assistance: a review. J Hazard Mater 180:38–49
Bartneck M, Keul HA, Singh S, Czaja K, Bornemann J, Bockstaller M, Moeller M, Zwadlo-Klarwasser G, Groll J (2010) Rapid uptake of gold nanorods by primary human blood phagocytes and immunomodulatory effects of surface chemistry. ACS Nano 4:3073–3086
Berry CC, Wells S, Charles S, Curtis AS (2003) Dextran and albumin derivatised iron oxide nanoparticles: influence on fibroblasts in vitro. Biomaterials 24:4551–4557
Berry CC, Wells S, Charles S, Aitchison G, Curtis AS (2004) Cell response to dextran-derivatised iron oxide nanoparticles post internalisation. Biomaterials 25:5405–5413
Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254
Bulte JM, Kraitchman DL (2004a) Monitoring cell therapy using iron oxide MR contrast agents. Curr Pharm Biotechnol 5:567–584
Bulte JW, Kraitchman DL (2004b) Iron oxide MR contrast agents for molecular and cellular imaging. NMR Biomed 17:484–499
Dobrovolskaia MA, McNeil SE (2007) Immunological properties of engineered nanomaterials. Nat Nanotechnol 2:469–478
Fatima M, Ahmad I, Sayeed I, Athar M, Raisuddin S (2000) Pollutant-induced over-activation of phagocytes is concomitantly associated with peroxidative damage in fish tissues. Aquat Toxicol 49:243–250
Feng X, Deng T, Zhang Y, Su S, Wei C, Han D (2011) Lipopolysaccharide inhibits macrophage phagocytosis of apoptotic neutrophils by regulating the production of tumour necrosis factor alpha and growth arrest-specific gene 6. Immunology 132:287–295
Fournier M, Pellerin J, Clermont Y, Morin Y, Brousseau P (2001) Effects of in vivo exposure of Mya arenaria to organic and inorganic mercury on phagocytic activity of hemocytes. Toxicology 161:201–211
Fraga CG, Oteiza PI (2002) Iron toxicity and antioxidant nutrients. Toxicology 180:23–32
Fujiki K, Yano T (1997) Effects of sodium alginate on the non-specific defence system of the common carp (Cyprinus carpio L.). Fish Shellfish Immunol 7:417–427
Geeraerts C, Belpaire C (2010) The effects of contaminants in European eel: a review. Ecotoxicology 19:239–266
Girginova PI, Daniel-da-Silva AL, Lopes CB, Figueira P, Otero M, Amaral VS, Pereira E, Trindade T (2010) Silica coated magnetite particles for magnetic removal of Hg2+ from water. J Colloid Interface Sci 345:234–240
Gordon S (1998) The role of the macrophage in immune regulation. Immunol Res 149:685–688
Handy R, Henry T, Scown T, Johnston B, Tyler C (2008a) Manufactured nanoparticles: their uptake and effects on fish—a mechanistic analysis. Ecotoxicology 17:396–409
Handy R, Owen R, Valsami-Jones E (2008b) The ecotoxicology of nanoparticles and nanomaterials: current status, knowledge gaps, challenges, and future needs. Ecotoxicology 17:315–325
Handy R, von der Kammer F, Lead J, Hassellöv M, Owen R, Crane M (2008c) The ecotoxicology and chemistry of manufactured nanoparticles. Ecotoxicology 17:287–314
Isani G, Falcioni ML, Barucca G, Sekar D, Andreani G, Carpenè E, Falcioni G (2013) Comparative toxicity of CuO nanoparticles and CuSO4 in rainbow trout. Ecotoxicol Environ Saf 97:40–46
Jain TK, Reddy MK, Morales MA, Leslie-Pelecky DL, Labhasetwar V (2007) Biodistribution, clearance and biocompatibility of iron oxide magnetic nanoparticles in rats. Mol Pharm 5:316–327
Jovanović B, Palić D (2012) Immunotoxicology of non-functionalized engineered nanoparticles in aquatic organisms with special emphasis on fish—review of current knowledge, gap identification, and call for further research. Aquat Toxicol 118–119:141–151
Jovanovic B, Whitley EM, Palic D (2014) Histopathology of fathead minnow (Pimephales promelas) exposed to hydroxylated fullerenes. Nanotoxicology 8:755–763
Karlsson HL, Holgersson A, Moller L (2008) Mechanisms related to the genotoxicity of particles in the subway and from other sources. Chem Res Toxicol 21:726–731
Karlsson HL, Gustafsson J, Cronholm P, Moller L (2009) Size dependent toxicity of metal oxide particles—a comparison between nano- and micrometer size. Toxicol Lett 188:112–118
Kim BC, Lee J, Um W, Kim J, Joo J, Lee JH, Kwak JH, Kim JH, Lee C, Lee H, Addleman RS, Hyeon T, Gu MB, Kim J (2011) Magnetic mesoporous materials for removal of environmental wastes. J Hazard Mater 192:1140–1147
Klaine SJ, Alvarez PJ, Batley GE, Fernandes TF, Handy RD, Lyon DY, Mahendra S, McLaughlin MJ, Lead JR (2008) Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ Toxicol Chem 27:1825–1851
Krpetic Z, Porta F, Caneva E, Dal Santo V, Scari G (2010) Phagocytosis of biocompatible gold nanoparticles. Langmuir 26:14799–14805
Lima R, Espirito AP, Porto R, Fraceto L (2011) Evaluation of cyto- and genotoxicity of poly(lactide-co-glycolide) nanoparticles. J Polym Environ 19:196–202
Lloyd RV, Hanna PM, Mason RP (1997) The origin of the hydroxyl radical oxygen in the Fenton reaction. Free Radic Biol Med 22:885–888
Mahmoudi M, Simchi A, Imani M, Milani AS, Stroeve P (2009) An in vitro study of bare and poly(ethylene glycol)-co-fumarate coated superparamagnetic iron oxide nanoparticles: a new toxicity identification procedure. Nanotechnology 20:225104–22512
Mahmoudi M, Simchi A, Imani M, Shokrgozar MA, Milani AS, Hafeli UO, Stroeve P (2010) A new approach for the in vitro identification of the cytotoxicity of superparamagnetic iron oxide nanoparticles. Colloids Surf B: Biointerfaces 75:300–309
Manibusan MK, Odin M, Eastmond DA (2007) Postulated carbon tetrachloride mode of action: a review. J Environ Sci Health Part C 25:185–209
Matranga V, Corsi I (2012) Toxic effects of engineered nanoparticles in the marine environment: model organisms and molecular approaches. Mar Environ Res 76:32–40
Moeller S, Kegler R, Sternberg K, Mundkowski RG (2012) Influence of sirolimus-loaded nanoparticles on physiological functions of native human polymorphonuclear neutrophils. Nanomed: Nanotechnol, Biol Med 8:1293–1300
Mohmood I, Ahmad I, Asim M, Costa L, Lopes CB, Trindade T, Duarte AC, Pereira E (2015) Interference of the co-exposure of mercury with silica-coated iron oxide nanoparticles can modulate genotoxicity induced by their individual exposures—a paradox depicted in fish under in vitro conditions. Environ Sci Pollut Res 22:3687–3696
Moore MN (2006) Do nanoparticles present ecotoxicological risks for the health of the aquatic environment? Environ Int 32:967–976
Mukherjee SP, Lyng FM, Garcia A, Davoren M, Byrne HJ (2010) Mechanistic studies of in vitro cytotoxicity of poly(amidoamine) dendrimers in mammalian cells. Toxicol Appl Pharmacol 248:259–268
Parra D, Rieger A, Li J, Zhang YA, Randall LM, Hunter CA, Barreda DR, Sunyer JO (2012) Pivotal advance: peritoneal cavity B-1 B cells have phagocytic and microbicidal capacities and present phagocytosed antigen to CD4+ T cells. J Leukoc Biol 91:525–536
Paul N, Sengupta M (2013) Lead induced overactivation of phagocytes and variation in enzymatic and non-enzymatic antioxidant defenses in intestinal macrophages of Channa punctatus. Modern Res Inflamm 2:28–35
Perreault F, Melegari SP, Costa CH, Oliveira AL, Popovic R, Matias WG (2012) Genotoxic effects of copper oxide nanoparticles in Neuro 2A cell cultures. Sci Total Environ 441:117–124
Planque MR, Aghdaei S, Roose T, Morgan H (2011) Electrophysiological characterization of membrane disruption by nanoparticles. ACS Nano 5:3599–3606
Raisuddin S, Singh KP, Zaidi SI, Paul BN, Ray PK (1993) Immunosuppressive effects of aflatoxin in growing rats. Mycopathologia 124:189–194
Roesslein M, Hirsch C, Kaiser JP, Krug HF, Wick P (2013) Comparability of in vitro tests for bioactive nanoparticles: a common assay to detect reactive oxygen species as an example. Int J Mol Sci 14:24320–24337
Rousselet E, Levin M, Gebhard E, Higgins BM, DeGuise S, Godard-Codding CJ (2013) Evaluation of immune functions in captive immature loggerhead sea turtles (Caretta caretta). Vet Immunol Immunopathol 156:43–53
Santos MA, Pacheco M (1996) Anguilla anguilla L. stress biomarkers recovery in clean water and secondary-treated pulp mill effluent. Ecotoxicol Environ Saf 35:96–100
Santos MA, Pacheco M, Ahmad I (2004) Anguilla anguilla L. antioxidants responses to in situ bleached kraft pulp mill effluent outlet exposure. Environ Int 30:301–308
Santos MA, Pacheco M, Ahmad I (2006) Responses of European eel (Anguilla anguilla L.) circulating phagocytes to an in situ closed pulp mill effluent exposure and its association with organ-specific peroxidative damage. Chemosphere 63:794–801
Sauvé S, Brousseau P, Pellerin J, Morin Y, Senecal L, Goudreau P, Fournier M (2002) Phagocytic activity of marine and freshwater bivalves: in vitro exposure of hemocytes to metals (Ag, Cd, Hg and Zn). Aquat Toxicol 58:189–200
Semete B, Booysen L, Lemmer Y, Kalombo L, Katata L, Verschoor J, Swai HS (2010) In vivo evaluation of the biodistribution and safety of PLGA nanoparticles as drug delivery systems. Nanomed: Nanotechnol, Biol Med 6:662–671
Shaw BJ, Handy RD (2011) Physiological effects of nanoparticles on fish: a comparison of nanometals versus metal ions. Environ Int 37:1083–1097
Singh N, Gareth JS, Asadi R, Doak S (2010) Potential toxicity of superparamagnetic iron oxide nanoparticles (SPION). Nano Reviews 1. 10.3402/nano.v1i0.5358
Tavares DS, Daniel-da-Silva AL, Lopes CB, Silva NJ, Amaral VS, Rocha J, Pereira E, Trindade T (2013) Efficient sorbents based on magnetite coated with siliceous hybrid shells for removal of mercury ions. J Mater Chem A 1:8134–8143
Tavares DS, Lopes CB, Daniel-da-Silva AL, Duarte AC, Trindade T, Pereira E (2014) The role of operational parameters on the uptake of mercury by dithiocarbamate functionalized particles. Chem Eng J 254:559–570
Tellez-Bañuelos MC, Santerre A, Casas-Solis J, Bravo-Cuellar A, Zaitseva G (2009) Oxidative stress in macrophages from spleen of Nile tilapia (Oreochromis niloticus) exposed to sublethal concentration of endosulfan. Fish Shellfish Immunol 27:105–111
Valko M, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12:1161–1208
Wang C, Yu X, Cao Q, Wang Y, Zheng G, Tan TK, Zhao H, Zhao Y, Wang Y, Harris D (2013) Characterization of murine macrophages from bone marrow, spleen and peritoneum. BMC Immunol 14:1–10
Zhu X, Tian S, Cai Z (2012) Toxicity assessment of iron oxide nanoparticles in zebrafish (Danio rerio) early life stages. PLoS One 7:1–6
Acknowledgments
Leonor Costa, Iram Mohmood (SFRH/BD/74410/2010), Iqbal Ahmad, Armando Duarte and Eduarda Pereira are grateful to European Funds through COMPETE and by National Funds through the Portuguese Science Foundation (FCT) (PEst-C/MAR/LA0017/2013, PTDC/MAR-BIO/3533/2012) and the Aveiro University Research Institute/Centre for Environmental and Marine Studies (CESAM) for partial financial supports.
Conflict of interest
The athors declare no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Henner Hollert
Rights and permissions
About this article
Cite this article
Costa, L.C., Mohmood, I., Trindade, T. et al. Rescheduling the process of nanoparticle removal used for water mercury remediation can increase the risk to aquatic organism: evidence of innate immune functions modulation in European eel (Anguilla anguilla L.). Environ Sci Pollut Res 22, 18574–18589 (2015). https://doi.org/10.1007/s11356-015-5375-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-015-5375-9