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Multibiomarker response in the earthworm Eisenia fetida as tool for assessing multi-walled carbon nanotube ecotoxicity

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Abstract

Carbon nanotubes have received a great attention in the last years thanks to their remarkable structural, electrical, and chemical properties. Nowadays carbon nanotubes are increasingly found in terrestrial and aquatic environment and potential harmful impacts of these nanoparticles on humans and wildlife are attracting increasing research and public attention. The effects of carbon nanotubes on aquatic organisms have been explored by several authors, but comparatively the information available on the impact of these particles on soil organisms is much less. Earthworms have traditionally been considered to be convenient indicators of land use impact and soil fertility. The aim of this work was to study the integrated response of a suite of biomarkers covering molecular to whole organism endpoints for the assessment of multi-walled carbon nanotube (MWCNTs) effects on earthworms (Eisenia fetida) exposed to spiked soil. Results showed that cellular and biochemical responses, such as immune cells morphometric alterations and lysosomal membrane destabilization, acetylcholinesterase inhibition and metallothionein tissue concentration changes, showed high sensitivity to MWCNTs exposure. They can improve our understanding and ability to predict chronic toxicity outcomes of MWCNTs exposure such as reproductive alterations. In this context although more investigation is needed to understand the mechanistic pathway relating the biochemical and cellular biomarker analyzed to reproductive alterations, the obtained results give an early contribution to the future development of an adverse outcomes pathways for MWCNTs exposure.

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References

  • Andrews GK (2000) Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem Pharmacol 59:95–104

    Article  CAS  Google Scholar 

  • Aschberger K, Johnston HJ, Stone V, Aitken RJ, Hankin SM, Peters SA, Tran CL, Christensen FM (2010) Review of carbon nanotubes toxicity and exposure–appraisal of human health risk assessment based on open literature. Crit Rev Toxicol 40:759–790

    Article  CAS  Google Scholar 

  • Baun A, Hartmann NB, Grieger K, Kusk KO (2008) Ecotoxicity of engineered nanoparticles to aquatic invertebrates: a brief review and recommendations for future toxicity testing. Ecotoxicology 17:387–395

    Article  CAS  Google Scholar 

  • Buzea C, Pacheco II, Robbie K (2007) Nanomaterials and nanoparticles: sources and toxicity. Biointerphases 2:17–71

    Article  Google Scholar 

  • Calisi A, Lionetto MG, Caricato R, Giordano ME, Schettino T (2008) Morphometric alteration in Mytilus galloprovincialis: a new biomarker. Environ Toxicol Chem 27:1435–1441

    Article  CAS  Google Scholar 

  • Calisi A, Lionetto MG, Schettino T (2009) Pollutant-induced alterations of granulocyte morphology in the earthworm Eisenia foetida. Ecotox Environ Saf 72:1369–1377

    Article  CAS  Google Scholar 

  • Calisi A, Lionetto MG, Schettino T (2011a) Biomarker response in the earthworm Lumbricus terrestris exposed to chemical pollutants. Sci Total Environ 409:4456–4464

    Article  CAS  Google Scholar 

  • Calisi A, Lionetto MG, Sanchez-Hernandez JC, Schettino T (2011b). Effect of heavy metal exposure on blood haemoglobin concentration and methemoglobin percentage in Lumbricus terrestris. Ecotoxicol 20:847–854

  • Calisi A, Zaccarelli N, Lionetto MG, Schettino T (2013) Integrated biomarker analysis in the earthworm Lumbricus terrestris: application to the monitoring of soil heavy metal pollution. Chemosphere 90:2637–2644

    Article  CAS  Google Scholar 

  • Cheng JP, Flahaut E, Cheng SH (2007) Effect of carbon nanotubes on developing zebrafish (Danio rerio) embryos. Environ Toxicol Chem 26:708–716

    Article  CAS  Google Scholar 

  • Cooper EL (2002) The earthworm: a new model with biomedical applications. In: Beschin A, Bilej M, Cooper EL (eds) New model for analyzing antimicrobial peptides with biomedical applications. IOS, Amsterdam, pp 3–26

    Google Scholar 

  • Cooper EL, Roch P (2003) Earthworm immunity: a model of immune competence. Pedobiologia 47:1–13

    Article  Google Scholar 

  • Dondero F, Calisi A (2015) Evaluation of pollution effects in marine organisms: “Old” and “New Generation” biomarkers. In: Sebastià MT (ed) Coastal ecosystems: experiences and recommendations for environmental monitoring programs. Nova Science Publishers, New York, pp 143–192

    Google Scholar 

  • Elmann GL, Cortney KD, Andrea VJ, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  Google Scholar 

  • Engelmann P, Palinkas L, Cooper EL, Nemeth P (2005) Monoclonal antibodies identify four distinct annelid leukocyte markers. Dev Comp Immunol 9:599–614

    Article  Google Scholar 

  • Gastaldi L, Ranzato E, Caprì F, Hankard P, Pérès G, Canesi L et al (2007) Application of a biomarker battery for the evaluation of the sublethal effects of pollutants in the earthworm Eisenia andrei. Comp Biochem Physiol C 146:398–405

    Google Scholar 

  • Hagger JA, Jones MB, Leonard DP, Owen R, Galloway TS (2006) Biomarkers and integrated environmental risk assessment: are there more questions than answers. Int Environ Assess Manag 2:312–329

    Article  CAS  Google Scholar 

  • Hankard PK, Svendsen C, Wright J, Wienberg C, Fishwick SK, Spurgeon DJ et al (2004) Biological assessment of contaminated land using earthworm biomarkers in support of chemical analysis. Sci Total Environ 330:9–20

    Article  CAS  Google Scholar 

  • Hayashi Y, Engelmann P, Foldbjerg R, Szabo M, Somogyi I, Pollak E (2012) Earthworms and humans in vitro: characterizing evolutionarily conserved stress and immune responses to silver nanoparticles. Environ Sci Technol 9:4166–4173

    Article  Google Scholar 

  • Hayashi Y, Heckmann LH, Simonsen V, Scott-Fordsman JJ (2013) Time course profiling of molecular stress responses to silver nanoparticles in the earthworm Eisenia foetida. Ecotoxicol Environ Saf 98:219–226

    Article  CAS  Google Scholar 

  • Hu CW, Zhang LJ, Wang WL, Cui YB, Li M (2014) Evaluation of the combined toxicity of multi-walled carbon nanotubes and sodium pentachlorophenate on the earthworm Eisenia fetida using avoidance bioassay and comet assay. Soil Biol Biochem 70:123–130

    Article  CAS  Google Scholar 

  • ISO (International Standard Organization) (1993) Soil quality—effects of pollutants on earthworms (Eisenia foetida). Part 1: determination of acute toxicity using artificial soil substrate, No. 11268-1. ISO, Geneva, Helvetia

  • ISO (International Standard Organization) (1996) Soil quality—effects of pollutants on earthworms (Eisenia foetida). Part 2: determination of effects on reproduction, No. 11268-2. ISO, Geneva, Helvetia

  • Jackson P, Jacobsen NR, Baun A, Birkedal R, Kühnel D, Jensen KA, Vogel U, Wallin H (2013a) Bioaccumulation and ecotoxicity of carbon nanotubes. Chem Cent J 7:154

    Article  Google Scholar 

  • Jackson P, Jacobsen NR, Baun A, Birkedal R, Kühnel D, Jensen KA, Vogel U, Wallin H (2013b) Bioaccumulation and ecotoxicity of carbon nanotubes. Chem Cent J 7(154):b84

    Google Scholar 

  • Ju-Nam Y, Lead JR (2008) Manufactured nanoparticles: an overview of their chemistry, interactions and potential environmental implications. Sci Total Environ 400:396–414

    Article  CAS  Google Scholar 

  • Kahru A, Dubourguier HC (2010) From ecotoxicology to nanoecotoxicology. Toxicology 20269:105–119

    Article  Google Scholar 

  • Kammenga JE, Dallinger R, Donker MH, Köhler HR, Simonsen V, Triebskorn R, Weeks JM (2000) Biomarkers in terrestrial invertebrates for ecotoxicological soil risk assessment. Rev Environ Contam T 164:93–147

    CAS  Google Scholar 

  • Kang Y, Liu YC, Wang Q, Shen JW, Wu T, Guan WJ (2009) On the spontaneous encapsulation of proteins in carbon nanotubes. Biomaterials 30:2807–2815

    Article  CAS  Google Scholar 

  • Klaine SJ, Alvarez PJJ, Batley GE, Fernandes TF, Handy RD, Lyon DY, Mahendra S, Mc Laughlin MJ, Lead JR (2008) Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ Toxicol Chem 27:1825–1851

    Article  CAS  Google Scholar 

  • Kroemer G, Jaattela M (2005) Lysosomes and autophagy in cell death control. Nat Rev Cancer 5:886–897

    Article  CAS  Google Scholar 

  • Lionetto MG, Caricato R, Calisi A, Schettino T (2011) Acetylcholinesterase inhibition as a relevant biomarker in environmental biomonitoring: new insights and perspectives. In: Visser JE (ed) Ecotoxicology around the globe. Nova Science Publishers, New York, pp 87–115

    Google Scholar 

  • Lionetto MG, Calisi A, Schettino T (2012) Earthworms biomarkers as tools for soil pollution assessment. In: Hernandz-Soriano MC (ed). Soil health and land use management. InTech-Open Access Publisher in Science, Technology and Medicine, Rijeka, p. 305–332

  • Ma X, Wu Y, Jin S, Tian Y, Zhang X, Zhao Y, Yu L, Liang XJ (2011) Gold nanoparticles induce autophagosome accumulation through size-dependent nanoparticle uptake and lysosome impairment. ACS Nano 5:8629–8639

    Article  CAS  Google Scholar 

  • Marino F, Ligero A, Cosin DJD (1992) Heavy metals and earthworms on the border of a road next to Santiago. Soil Biol Biochem 24:1705–1709

    Article  CAS  Google Scholar 

  • Mauter MS, Elimelech M (2008) Environmental applications of carbon-based nanomaterials. Environ Sci Technol 42:5843–5859

    Article  CAS  Google Scholar 

  • Morrison DE, Robertson BK, Alexander M (2000) Bioavailability to earthworms of aged DDT, DDE, DDD, and dieldrin in soil. Environ Sci Technol 34:709–713

    Article  CAS  Google Scholar 

  • Mueller NC, Nowack B (2008) Exposure modeling of engineered nanoparticles in the environment. Environ Sci Technol 42:4447–4453

    Article  CAS  Google Scholar 

  • Mwangi JN, Wang N, Ingersoll CG, Hardesty DK, Brunson EL, Li H, Deng B (2012) Toxicity of carbon nanotubes to freshwater aquatic invertebrates. Environ Toxicol Chem 31:1823–1830

    Article  CAS  Google Scholar 

  • OECD (1984) Guidelines for testing of chemicals: earthworm acute toxicity test. No. 207. Paris, France

  • OECD (2004) Guideline for testing of chemicals: earthworms reproduction test. No. 222. Paris, France

  • OECD (2013) Guidance document on developing and assessing adverse outcome pathways. OECD Environment, Health and Safety Publications, series on Testing and Assessment, No. 184. Paris, France

  • Petersen EJ, Huang QG, Weber WJ (2008) Bioaccumulation of radio-labeled carbon nanotubes by Eisenia foetida. Environ Sci Technol 42:3090–3095

    Article  CAS  Google Scholar 

  • Petersen EJ, Pinto RA, Landrum PF, Weber WJ Jr (2009) Influence of carbon nanotubes on pyrene bioaccumulation from contaminated soils by earthworms. Environ Sci Technol 43:4181–4187

    Article  CAS  Google Scholar 

  • Petersen EJ, Pinto RA, Mai DJ, Landrum PF, Weber WJ Jr (2011) Influence of polyethyleneimine graftings of multi-walled carbon nanotubes on their accumulation and elimination by and toxicity to Daphnia magna. Environ Sci Technol 45:1133–1138

    Article  CAS  Google Scholar 

  • Roberts AP, Mount AS, Seda B, Souther J, Qiao R, Lin S et al (2007) In vivo biomodification of lipid-coated carbon nanotubes by Daphnia magna. Environ Sci Technol 41:3025–3029

    Article  CAS  Google Scholar 

  • Rodriguez-Castellanos L, Sanchez-Hernandez JC (2007) Earthworm biomarkers of pesticide contamination: current status and perspectives. J Pest Sci 32:360–371

    Article  CAS  Google Scholar 

  • Sanchez- Hernandez JC (2006) Earthworms biomarkers in ecological risk assessment. Rev Environ Contam Toxicol 188:85–126

    CAS  Google Scholar 

  • Scott-Fordsmand JJ, Krogh PH, Schaefer M, Johansen A (2008) The toxicity testing of double-walled nanotubes-contaminated food to Eisenia veneta earthworms. Ecotox Environ Saf 71:616–619

    Article  CAS  Google Scholar 

  • Shi XY, Wang SH, Shen MW, Antwerp ME, Chen XS, Li C et al (2009) Multifunctional dendrimer-modified multiwalled carbon nanotubes: synthesis, characterization, and in vitro cancer cell targeting and imaging. Biomacromolecules 10:1744–1750

    Article  CAS  Google Scholar 

  • Sohaebuddin SK, Thevenot PT, Baker D, Eaton JW, Tang L (2010) Nanomaterial cytotoxicity is composition, size, and cell type dependent. Part Fibre Toxicol 7:22

    Article  Google Scholar 

  • Stein EA, Cooper EL (1983) Inflammatory responses in annelids. Am Zool 23:145–156

    Article  Google Scholar 

  • Svendsen C, Meharg AA, Freestone P, Weeks JM (1996) Use of an earthworm lysosomal biomarker for the ecological assessment of pollution from an industrial plastics fire. Appl Soil Ecol 3:99–107

    Article  Google Scholar 

  • Thurnherr T, Brandenberger C, Fischer K, Diener L, Manser P, Maeder-Althaus X et al (2011) A comparison of acute and long-term effects of industrial multiwalled carbon nanotubes on human lung and immune cells in vitro. Toxicol Lett 200:176–186

    Article  CAS  Google Scholar 

  • Van der Ploeg MJ, Baveco JM, Van der Hout A, Bakker R, Rictjens IM, Van den Brink NW (2011) Effect of C60 nanoparticles exposure on earthworms (Lumbricus rubellus) and implications for population dynamics. Environ Pollut 159:198–203

    Article  Google Scholar 

  • Van der Ploeg MJ, Van den Berg JH, Bhattacharjee S, Dehaan LH, Ershov DS, Fokkink RG (2012) In vitro nanoparticle toxicity to rat alveolar cells and coelomocytes from the earthworm Lumbricus rubellus. Nanotoxicology 9:28–37

    Google Scholar 

  • Van der Zande M, Junker R, Walboomers XF, Jansen JA (2011) Carbon nanotubes in animal models: a systematic review on toxic potential. Tissue Eng Part B Rev. 17:57–69

    Article  Google Scholar 

  • Viarengo A, Ponzano E, Dondero F, Fabbri R (1997) A simple spectrophotometric method for metallothionein valuation marine organisms: an application to mediterranean an antartic molluscs. Mar Environ Res 44:69–84

    Article  CAS  Google Scholar 

  • Wang Z, Zhao J, Li F, Gao D, Xing B (2009) Adsorption and inhibition of acetylcholinesterase by different nanoparticles. Chemosphere 77:67–73

    Article  CAS  Google Scholar 

  • Weeks JM, Svendsen C (1996) Neutral red retention by lysosomes from earthworm (Lumbricus rubellus) coelomocytes: a simple biomarker of exposure to soil copper. Environ Toxicol Chem 15:1801–1805

    Article  CAS  Google Scholar 

  • Xia W, Song HM, Wei Q, Wei A (2012) Differential response of macrophages to core-shell Fe3O4@Au nanoparticles and nanostars. Nanoscale 4:7143–7148

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The present study was carried out within the framework of projects funded by MIUR.

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Correspondence to M. G. Lionetto.

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Calisi, A., Grimaldi, A., Leomanni, A. et al. Multibiomarker response in the earthworm Eisenia fetida as tool for assessing multi-walled carbon nanotube ecotoxicity. Ecotoxicology 25, 677–687 (2016). https://doi.org/10.1007/s10646-016-1626-x

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