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Radiolabeling of amide functionalized multi-walled carbon nanotubes for bioaccumulation study in fish bone using whole-body autoradiography

  • Youssouf Djibril SoubanehEmail author
  • Emilien Pelletier
  • Isabelle Desbiens
  • Claude Rouleau
Multi-Stressors in Freshwater and Transitional Environments: from Legacy Pollutants to Emerging Ones

Abstract

Commercial and medicinal applications of functionalized carbon nanotubes (f-CNTs) such as amidated f-CNTs are expanding rapidly with a potential risk exposure to living organisms. The effects of amidated f-CNTs on aquatic species have received a limited attention. In this work, an easy wet method to prepare [14C]-label amide multi-walled carbon nanotubes (MWNTs) is reported. Labeled carbon nanotubes were prepared by successive reactions of carboxylation, chloroacylation, and final amidation using [14C]-labeled ethanolamine. The f-CNTs were characterized using elemental analysis, electron dispersive X-ray, transmission electron microscopy, thermogravimetric analysis, and Raman and FTIR spectroscopy. An uptake experiment was carried out with juvenile Arctic char (Salvelinus alpinus) using water dispersed amidated [14C]-f-CNTs to assess their biodistribution in fish tissues using whole body autoradiography. The radioactivity pattern observed in fish head suggests that f-CNTs were accumulated in head bone canals, possibly involving an interaction with mineral or organic phases of bones such as calcium and collagen. This f-CNTs distribution illustrates how important is to consider the surface charges of functionalized carbon nanotubes in ecotoxicological studies.

Keywords

Carbon nanotubes Amide functionalization Radiolabeling method Fish Canal bones 

Notes

Funding information

This research work was funded by the Natural Sciences and Engineering Research Council of Canada and supported by the Canada Research Chair in Molecular Ecotoxicology (E.P).

Compliance with ethical standards

This research involved experiments on animals, Arctic char, due to the potential impact of f-CNTs on organisms in aquatic environment. This study was performed in strict accordance with Ethical Policy for Animal Experimentation (Publication No. C2-D34, Rev. 2012) approved by the Institutional Animal Care and Use Committee of the Université du Québec à Rimouski. This ethical policy is an application of the Canadian Council on Animal Care. Post-experimental cares of animals were provided including minimizing discomfort and the consequences of any disability resulting from the experiment.

Conflict of interest

The authors declare that they have no conflict of interest (financial or non-financial).

References

  1. Al-Sid-Cheikh M, Pelletier E, Rouleau C (2011) Synthesis and characterization of [110mAg]-nanoparticles with application to whole body autoradiography of aquatic organisms. Appl Radiat Isot 69:1415–1142CrossRefGoogle Scholar
  2. Bacakova L, Kopova I, Stankova L, Liskova J, Vacik J, Lavrentiev V, Alexander Kromka A, Potocky S, Stranska D (2014) Bone cells in cultures on nanocarbonbased materials for potential bone tissue engineering: A review. Phys Status Solidi A 211:2688–2702CrossRefGoogle Scholar
  3. Bjorkland R, Tobias DA, Petersen EJ (2017) Increasing evidence indicates low bioaccumulation of carbon nanotubes. Environ Sci Nano 4:747–766CrossRefGoogle Scholar
  4. Campos-Garcia J, Martinez DS, Rezende KF, da Silva JR, Alves OL, Barbieri E (2016) Histopathological alterations in the gills of Nile tilapia exposed to carbofuran and multiwalled carbon nanotubes. Ecotoxicol Environ Saf 133:481–488CrossRefGoogle Scholar
  5. Chen P, Zhang HB, Lin GD, Hong Q, Tsai KR (1997) Gowth of carbon nanotubes by catalytic decomposition of CH4 or CO on a Ni-MgO catalyst. Carbon 35:1495–1501CrossRefGoogle Scholar
  6. Cui HF, Vashist SK, Al-Rubeaan K, Luong JHT, Sheu FS (2010) Interfacing carbon nanotubes with living mammalian cells and cytotoxicity issues. Chem Res Toxicol 23:1131–1147CrossRefGoogle Scholar
  7. Datsyuk V, Kalyva M, Papagelis K, Parthenios J, Tasis D, Siokou A, Kallitsis I, Galiotis C (2008) Chemical oxidation of multi walled carbon nanotubes. Carbon 46:833–840CrossRefGoogle Scholar
  8. Deng X, Jia G, Wang H, Sun H, Wang X, Yang S, Wang T, Liu Y (2007) Translocation and fate of multi-walled carbon nanotubes in vivo. Carbon 45:1419–1424CrossRefGoogle Scholar
  9. Felix LC, Ede JD, Snell DA, Oliveira TM, Martinez-Rubi Y, Simard B, Luong JHT, Goss GG (2016) Physicochemical properties of functionalized carbon-based nanomaterials and their toxicity to fishes. Carbon 104:78–89CrossRefGoogle Scholar
  10. Forest GA, Alexander AJ (2007) A model for the dependence of carbon nanotube length on acid oxidation time. J Phys Chem C 111:10792–10798CrossRefGoogle Scholar
  11. Genten F, Terwinghe E, Danguy A (2010) Histologie illustrée du poisson. Quae edition, Paris, pp 379–402Google Scholar
  12. Georgin, D., Czarny,B., Botquin, M., L’Hermite, M., Pinault, M., Bouchet-Fabre, B., Carriere, M., Poncy, J.L.; Chau, Q., Maximilien, R., Dive, V., Taran F., 2009. Preparation of the 14C-labeled multi walled carbon nanotubes for the biodistribution investigation. J Am Chem Soc 131, 14658-14659.Google Scholar
  13. Gopalakrishnan R, Balamurugan K, Singam ERA, Sundaraman S, Subramanian V (2011) Adsorption of collagen onto single walled carbon nanotubes: a molecular dynamics investigation. Phys Chem Chem Phys 13:13046–13057CrossRefGoogle Scholar
  14. Grandi, S., Magistis, A., Mustarelli, P., Quarterone, E., Tomasi, C., Meda, L., 2006. Synthesis and characterization of Si-O2-PEG hybrid materials. J Noncryst Sol. 352, 273-280.Google Scholar
  15. Heller DA, Barone PW, Strano MS (2005) Sonication-induced changes in chiral distribution: A complication in the use of single-walled carbon nanotube fluorescence for determining species distribution. Carbon 43:651–673CrossRefGoogle Scholar
  16. Hou P, Liu C, Tong Y, Xu S, Liu M, Cheng H (2001) Purification of single-walled carbon nanotubes synthetized by the hydrogen arc-discharge method. J Mater Res 16:2526–2529CrossRefGoogle Scholar
  17. Iijima S (1991) Helical microtubules of graphitic carbon. Nature 354:56–58CrossRefGoogle Scholar
  18. Jackson P, Jacobsen NR, Baun A, Birkedal R, Kühnel D, Jensen KA, Vogel U, Wallin H (2013) Bioaccumulation and ecotoxicity of carbon nanotubes. Chem Cent J 7:154 A reviewCrossRefGoogle Scholar
  19. Jacoby A (2015) Global Markets and Technologies for Carbon Nanotubes. A BCC Research Nanotechnology Report, Report Code: NAN024F. http://www.bccresearch.com/market-research/nanotechnology/carbon-nantubes-global-markets-technologies-report-nan024f.html Visited 2019-03-15
  20. Jang M-H, Hwang YS (2018) Effects of functionalized multi-walled carbon nanotubes on toxicity and bioaccumulation of lead in Daphnia magna. PLoS One 13(3):e0194935.  https://doi.org/10.1371/journal.pone.0194935 CrossRefGoogle Scholar
  21. Jia G, Wang H, Yan L, Wang X, Pei L, Yan T, Zhao Y, Guo X (2005) Cytotoxicity of carbon nanomaterials: single-wall nanotube, multi-wall nanotube, and fullerene. Environ Sci Technol 39:1378–1383CrossRefGoogle Scholar
  22. Kaempgen M, Lebert M, Haluska M, Nicoloso N, Roth S (2008) Sonochimical optimization of the conductivity of single-wall carbon nanotube networks. Adv Mater 20:616–620CrossRefGoogle Scholar
  23. Karimi M, Solati N, Amiri M, Mirshekari H, Mohamed E, Taheri M, Hashemkhani M, Saeidi A, Estiar MA, Kiani P, Ghasemi A, Basri SMM, Aref AR, Hamblin MR (2015) Carbon nanotubes part I: preparation of a novel and versatile drug-delivery vehicle. Expert Opin Drug Deliv 12:1071–1087CrossRefGoogle Scholar
  24. Kushuawa SKS, Ghoshal S, Rai AK, Singh S (2013) Carbon nanotubes as a novel drug delivery system for anticancer therapy: a review. Brazil. J Pharm Sci 49:629–643Google Scholar
  25. Lekander B (1949) The sensory line system and the canal bones in the head of some Ostariophysi. Acta Zool 30:1–131CrossRefGoogle Scholar
  26. Maes HM, Stibany F, Giefers S, Daniels B, Deutschmann B, Werner Baumgartner W, Schäffer A (2014) Accumulation and distribution of Mmultiwalled carbon nanotubes in Zebrafish (Danio rerio). Environ Sci Technol 48:12256–12264CrossRefGoogle Scholar
  27. Mananghaya M (2015) Modeling of single-walled carbon nanotubes functionalized with carboxylic and amide groups towards its solubilization in water. J Mol Liq 212:592–596CrossRefGoogle Scholar
  28. Martınez MT, Callejas MA, Benito AM, Cochet M, Seeger T, Anson A, Schreiber J, Gordon C, Marhic C, Chauvet O, Fierro JLG, Maser WK (2003) Sensitivity of single wall carbon nanotubes to oxidative processing: structural modification, intercalation and functionalization. Carbon 41:2247–2256CrossRefGoogle Scholar
  29. Petersen EJ, Akkanen J, Kukkonen JVK, Weber WJ (2009) Biological uptake and depuration of carbon nanotubes by Daphnia magna. Environ Sci Technol 43:2969–2975CrossRefGoogle Scholar
  30. Petersen, E.J., Pinto, R.A., Zhang, L., Huang, Q., Landrum, P.F., Weber, Jr. W.J., 2011. Effects of polyethyleneimine-mediated functionalization of multi-walled carbon nanotubes on earthworm bioaccumulation and sorption by soils. Environ Sci Technol 45, 3718–3724.Google Scholar
  31. Riddick JA, Bunger WB, Sakano TK (1986) Organic solvents - physical properties and methods of purification. Ed. A. Weissberger. John Wiley & Sons, New York, NYGoogle Scholar
  32. Saffar KP, JamilPour N, and Rouhi G (2009) Carbon nanotubes in bone tissue engineering. Biomedical Engineering, Carlos Alexandre Barros de Mello (Ed.), 26, 477-498, InTechOpen.Google Scholar
  33. Sajid MI, Jamshaid U, Jamshaid T, Zafar N, Fessi H, Elaissari A (2016) Carbon nanotubes from synthesis to in vivo biomedical applications. Int J Pharm 501:278–299CrossRefGoogle Scholar
  34. Smith MB, March J (2007) March’s Advanced Organic Chemistry: Reactions, Mechanisms, and Structure (6th ed.), John Wiley & Sons, New York.
  35. Sohn EK, Chung YS, Johari SA, Kim TG, Kim JK, Lee JH, Lee YH, Kang SW, Yu IJ (2015) Acute toxicity comparison of single-walled carbon nanotubes in various freshwater organisms. Biomed Res Int:323090 7 pagesGoogle Scholar
  36. Solon EG (2007) Autoradiography: high-resolution molecular imaging in pharmaceutical discovery and development. Expert Opin Drug Discovery 2:503–514CrossRefGoogle Scholar
  37. Tasi D, Tagmatarchis N, Bianco A, Prato M (2006) Chemistry of carbon nanotubes. Chem Rev 106:1105–1136CrossRefGoogle Scholar
  38. Wang J., He C., Cheng N., Yang Q., Chen M., You L., Zhang Q. 2015. Bone marrow stem cells response to collagen/single-wall carbon nanotubes-COOHs nanocompositefFilms with transforming growth factor Beta 1. J Nanosci Nanotechnol 15, 4844-4850, Bone Marrow Stem Cells Response to Collagen/Single-Wall Carbon Nanotubes-COOHs Nanocomposite Films with Transforming Growth Factor Beta 1.Google Scholar
  39. Webb JF (1989) Gross morphology and evolution of the mecanoreceptive lateral-line system in teleost fishes. Brain Behav Evol 33:34–53CrossRefGoogle Scholar
  40. Weiner S, Wagner HD (1998) The material bone: structure-mechanical function relations. Annu Rev Mater Sci 28:271–298CrossRefGoogle Scholar
  41. Widiyarti G, Hanafi M, Isnijah S, Kardono LBS, Ngadiman E, Sundowo A (2009) Preparation of 2-aminoethylsulfonic acid. J Makara 13:55–58Google Scholar
  42. Wijnhoven SWP, Peijnenburg WJGM, Herberts CA, Hagens WI, Oomen AG, Heugens EHW, Roszek B, Bisschops J, Gosens I, Van De Meent D, Dekkers S, de Jong WH, van Zijverden M, Sips AJAM, Geertsma RE (2009) Nano-silver—A review of available data and knowledge gaps in human and environmental risk assessment. Nanotoxicology 3:109–138CrossRefGoogle Scholar
  43. Wu CS, Liao HT (2007) Study on the preparation and characterization of biodegradable polyactide/multi-walled carbon nanotubes nanocomposites. Polymer 48:4449–4458CrossRefGoogle Scholar
  44. Zardini HZ, Davarpanah M, Shanbedi M, Amiri A, Maghrebi M, Ebrahimi L (2014) Microbial toxicity of ethanolamines—Multiwalled carbon nanotubes. J Biomed Mater Res Part A 102A:1774–1781CrossRefGoogle Scholar
  45. Zhai G, Gutowski SM, Walters KS, Yan B, Schnoor JL (2015) Charge, size, and cellular selectivity for multiwall carbon nanotubes by maize and soybean. Environ Sci Technol 49:7380–7390CrossRefGoogle Scholar
  46. Zhang L, Petersen EJ, Zhang W, Chen Y, Cabrera M, Huang Q (2012) Interactions of 14C-labeled multi-walled carbon nanotubes with soil minerals in water. Environ Pollut 166:75–81CrossRefGoogle Scholar
  47. Zhang W, Zhang Z, Zhang Y (2011) The application of carbon nanotubes in target drug delivery systems for cancer therapies. Nanoscale Res Lett 6:555–577CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Youssouf Djibril Soubaneh
    • 1
    Email author
  • Emilien Pelletier
    • 2
  • Isabelle Desbiens
    • 2
  • Claude Rouleau
    • 2
  1. 1.Département de biologie, chimie et géographieUniversité du Québec à RimouskiQCCanada
  2. 2.Institut des sciences de la mer de RimouskiUniversité du Québec à RimouskiQCCanada

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