Biodistribution and toxicological study of PEGylated single-wall carbon nanotubes in the zebrafish (Danio rerio) nervous system

Toxicology and Applied Pharmacology

Volumn 280, Issue 3, 2014, Pages 484-492

  Weber, Gisele E B ^a   Dal Bosco, Lidiane ^a   Gonçalves, Carla O F ^b   Santos, Adelina P ^b   Fantini, Cristiano ^c   Furtado, Clascídia A ^b   Parfitt, Gustavo M ^a   Peixoto, Carolina ^a   Romano, Luis Alberto ^a   Vaz, Bernardo S ^a   Barros, Daniela M ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE   (Brazil)

^b CENTRO DE DESENVOLVIMENTO DA TECNOLOGIA NUCLEAR   (Brazil)

^c Departamento de Fisica   (Brazil)

Author keywords

Behavioral; Biocompatibility; Biodistribution; Oxidative stress; SWNT PEG; Toxicity

Indexed keywords

GLUTATHIONE; MACROGOL; SINGLE WALLED NANOTUBE; CARBON NANOTUBE; MACROGOL DERIVATIVE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BIOACCUMULATION; BIOCOMPATIBILITY; BRAIN HOMOGENATE; CHEMICAL ANALYSIS; CONTROLLED STUDY; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LIPID PEROXIDATION; MALE; NANOTOXICOLOGY; NERVOUS SYSTEM; NEUROTOXICITY; NONHUMAN; OPEN FIELD BEHAVIOR; OPEN FIELD TEST; RAMAN SPECTROMETRY; ZEBRA FISH; ANIMAL; ANIMAL BEHAVIOR; BRAIN; CYTOCHEMISTRY; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; TISSUE DISTRIBUTION; TOXICITY; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; GLUTATHIONE; HISTOCYTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; NANOTUBES, CARBON; POLYETHYLENE GLYCOLS; SPECTRUM ANALYSIS, RAMAN; THIOBARBITURIC ACID REACTIVE SUBSTANCES; TISSUE DISTRIBUTION; ZEBRAFISH;

EID: 84908299326     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2014.08.018     Document Type: Article

References (56)

1. Ajayan P.M. Nanotubes from carbon. Chem. Rev. 1999, 99(7):1787-1800.
2. Amado L.L., Garcia M.L., Ramos P.B., Freitas R.F., Zafalon B., Ferreira J.L.R., Yunes J.S., Monserrat J.M. A method to measure total antioxidant capacity against peroxyl radicals in aquatic organisms: application to evaluate microcystins toxicity. Sci. Total Environ. 2009, 407:2115-2123.
3. Barros T.P., Alderton W.K., Reynolds H.M., Roach A.G., Berghmans S. Zebrafish: an emerging technology for in vivo pharmacological assessment to identify potential safety liabilities in early drug discovery. Br. J. Pharmacol. 2008, 154(7):1400-1413.
4. Bekyarova E., Ni Y., Malarkey E.B., Montana V., McWilliams J.L., Haddon R.C., Parpura V. Applications of carbon nanotubes in biotechnology and biomedicine. J. Biomed. Nanotechnol. 2005, 1(1):3-17.
5. Cheng J., Chan C.M., Veca L.M., Poon W.L., Chan P.K., Qu L., Sun Y.P., Cheng S.H. Acute and long-term effects after single loading of functionalized multi-walled carbon nanotubes into zebrafish (Danio rerio). Toxicol. Appl. Pharmacol. 2009, 235(2):216-225.
6. Cheung W., Pontoriero F., Taratula O., Chen A.M., He H. DNA and carbon nanotubes as medicine. Adv. Drug Deliv. Rev. 2010, 62(6):633-649. (Review).
7. de Castro M.R., Lima J.V., de Freitas D.P., Valente Rde S., Dummer N.S., de Aguiar R.B., dos Santos L.C., Marins L.F., Geracitano L.A., Monserrat J.M., Barros D.M. Behavioral and neurotoxic effects of arsenic exposure in zebrafish (Danio rerio, Teleostei: Cyprinidae). Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 2009, 150(3):337-342.
8. Fako V.E., Furgeson D.Y. Zebrafish as a correlative and predictive model for assessing biomaterial nanotoxicity. Adv. Drug Deliv. Rev. 2009, 61(6):478-486.
9. Ferreira J.L.R., Barros D.M., Geracitano L.A., Fillmann G., Fossa C.E., Almeida E.A., Prado M.C., Neves B.R.A., Pinheiro M.V.B., Monserrat J.M. In vitro exposure to fullerene c60 influences redox state and lipid peroxidation in brain and gills from cyprinus carpio (cyprinidae). Environ. Toxicol. Chem. 2012, 31(5):961-967.
10. Firme C.P., Bandaru P.R. Toxicity issues in the application of carbon nanotubes to biological systems. Nanomedicine: NBM 2010, 6:245-256.
11. Foldvari M., Bagonluri M. Carbon nanotubes as functional excipients for nanomedicines: II. Drug delivery and biocompatibility issues. Nanomedicine 2008, 4(3):183-200.
12. Galvan-Garcia P., Keefer E.W., Yang F., Zhang M., Fang S., Zakhidov A.A., Baughman R.H., Romero M.I. Robust cell migration and neuronal growth on pristine carbon nanotube sheets and yarns. J. Biomater. Sci. Polym. Ed. 2007, 18(10):1245-1261.
13. Gilmore J.L., Yi X., Quan L., Kabanov A.V. Novel nanomaterials for clinical neuroscience. J. NeuroImmune Pharmacol. 2008, 3:83-94. (Review).
14. Halliwell B., Gutteridge J.M.C. Role of free radicals in the neurodegenerative disease: therapeutic implications for antioxidant treatment. Drugs Aging 2001, 18:685-716.
15. Heister E., Lamprecht C., Neves V., Tilmaciu C., Datas L., Flahaut E., Soula B., Hinterdorfer P., Coley H.M., Silva S.R.P., McFadden J. Higher dispersion efficacy of functionalized carbon nanotubes in chemical and biological environments. ACS Nano 2010, 4(5):2615-2626.
16. Ilbasmiş-Tamer S., Yilmaz S., Banoğlu E., Değim I.T. Carbon nanotubes to deliver drug molecules. J. Biomed. Nanotechnol. 2010, 6(1):20-27.
17. Jain S., Thakare V.S., Das M., Godugu C., Jain A.K., Mathur R., Chuttani K., Mishra A.K. Toxicity of multiwalled carbon nanotubes with end defects critically depends on their functionalization density. Chem. Res. Toxicol. 2011, 24(11):2028-2039.
18. Jakubek L., Marangoudakis S., Raingo J., Liu X., Lipscombe D., Hurt R. The inhibition of neuronal calcium ion channels by trace levels of yttrium released from carbon nanotubes. Biomaterials 2009, 30(31):6351-6357.
19. Janovic B., Whitley E.M., Palic D. Histopathology of feathed minnow(Pimephales promelas) exposed to hidroxyated fulerenes. Nanotoxicol. 2014, 8(7):755-763.
20. Johnston H.J., Hutchison G.R., Christensen F.M., Peters S., Hankin S., Aschberger K., Stone V. A critical review of the biological mechanisms underlying the in vivo and in vitro toxicity of carbon nanotubes: the contribution of physico-chemical characteristics. Nanotoxicology 2010, 4(2):207-246.
21. Jones D.P. Redefining oxidative stress. Antioxid. Redox Signal. 2006, 8:1865-1879.
22. Kalinina I., Worsley K., Lugo C., Mandal S., Bekyarova E., Haddon R.C. Synthesis, dispersion, and viscosity of poly(ethylene glycol)-functionalized water-soluble single-walled carbon nanotubes. Chem. Mater. 2011, 23:1246-1253.
23. Kam N.W., O'Connell M., Wisdom J.A., Dai H. Carbon nanotubes as multifunctional biological transporters and near-infrared agents for selective cancer cell destruction. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(33):11600-11605.
24. Kang B., Yu D., Dai Y., Chang S., Chen D., Ding Y. Biodistribution and accumulation of intravenously administered carbon nanotubes in mice prprobed by Raman spectroscopy and fluorescent labeling. Carbon 2009, 47(4):1189-1192.
25. Liang F., Chen B. A review on biomedical applications of single-walled carbon nanotubes. Curr. Med. Chem. 2010, 17(1):10-24.
26. Linney E., Upchurch L., Donerly S. Zebrafish as a neurotoxicological model. Neurotoxicol. Teratol. 2004, 27(1):709-718.
27. Liopo A.V., Stewart M.P., Hudson J., Tour J.M., Pappas T.C. Biocompatibility of native and functionalized single-walled carbon nanotubes for neuronal interface. J. Nanosci. Nanotechnol. 2006, 6(5):1365-1374.
28. Liu Z., Davis C., Cai W., He L., Chen X., Dai H. Circulation and long-term fate of functionalized, biocompatible single-walled carbon nanotubes in mice probed by Raman spectroscopy. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(5):1410-1415.
29. Liu Z., Tabakman S.M., Chen Z., Dai H. Preparation of carbon nanotube bioconjugates for biomedical applications. Nat. Protoc. 2009, 4(9):1372-1382.
30. Maher P. Redox control of neural function: background, mechanisms, and significance. Antioxid. Redox Signal. 2006, 8(11-12):1941-1970.
31. Mattson M.P., Haddon R.C., Rao A.M. Molecular functionalization of carbon nanotubes and use as substrates for neuronal growth. J. Mol. Neurosci. 2000, 14(3):175-182.
32. Medina C., Santos-Martinez M.J., Radomski A., Corrigan O.I., Radomski M.W. Nanoparticles: pharmacological and toxicological significance. Br. J. Pharmacol. 2007, 50(5):552-558.
33. Meng L., Zhang X., Lu Q., Fei Z., Dyson P.J. Single walled carbon nanotubes as drug delivery vehicles: targeting doxorubicin to tumors. Biomaterials 2012, 33(6):1689-1698.
34. Naderi N., Madani S.Y., Mosahebi A., Seifalian A.M. Carbon nanotubes in the diagnosis and treatment of malignant melanoma. Anticancer Agents Med. Chem. 2013, 13(1):171-185.
35. Nance E.A., Woodworth G.F., Sailor K.A., Shih T., Xu Q., Swaminathan G., Xiang D., Eberhart C., Hanes J. Penetration of large polymeric nanoparticles within brain tissue. Nanomedicine 2012, 149(4):149ra119.
36. Nel A., Xia T., Mädler L., Li N. Toxic potential of materials at the nanolevel. Science 2006, 311(5761):622-627. (Review).
37. Oakes K.D., Van Der Kraak G.J. Utility of the TBARS assay in detecting oxidative stress in white sucker (Catostomus commersoni) populations exposed to pulp mill effluent. Aquat. Toxicol. 2003, 63(4):447-463.
38. Oberdörster G., Oberdörster E., Oberdörster J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ. Health Perspect. 2005, 113:823-839.
39. Oberdörster G., Elder A., Rinderknecht A. Nanoparticles and the brain: cause for concern?. J. Nanosci. Nanotechnol. 2009, 9(8):4996-5007.
40. Porter A., Gass M., Muller K., Skepper J., Midgley P., Welland M. Direct imaging of single-walled carbon nanotubes in cells. Nat. Nanotechnol. 2007, 2:713-717.
41. Roman J.A., Niedzielko T.L., Haddon R.C., Parpura V., Floyd C.L. Single-walled carbon nanotubes chemically functionalized with polyethylene glycol promote tissue repair in a rat model of spinal cord injury. J. Neurotrauma 2011, 28(11):2349-2362.
42. Smith D.M., Mizumori S.J. Learning-related development of context-specific neuronal responses to places and events: the hippocampal role in context processing. J. Neurosci. 2006, 26(12):3154-3163.
43. Stewart A.M., Gaikwad S., Kyzar E., Kalueff A.V. Understanding spatio-temporal strategies of adult zebrafish exploration in the open field test. Brain Res. 2012, 1451:44-52.
44. Sucapane A., Cellot G., Prato M., Giugliano M., Parpura V., Ballerini L. Interactions between cultured neurons and carbon nanotubes: a nanoneuroscience vignette. J. Nanoneurosci. 2009, 1(1):10-16.
45. Suh W.H., Suslick K.S., Stucky G.D., Suh Y.H. Nanotechnology, nanotoxicology, and neuroscience. Prog. Neurobiol. 2009, 87:133-170.
46. Truong L., Saili K.S., Miller J.M., Hutchison J.E., Tanguay R.L. Persistent adult zebrafish behavioral deficits results from acute embryonic exposure to gold nanoparticles. Comp. Biochem. Physiol. C 2012, 155:269-274.
47. Valko M., Leibfritz D., Moncol J., Cronin M.T., Mazur M., Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol. 2007, 39(1):44-84.
48. Vashist S.K., Zheng D., Pastorin G., Al-Rubeaan K., Luong J.H., Sheu F.S. Delivery of drugs and biomolecules using carbon nanotubes. Carbon 2011, 49:4077-4097.
49. Wang J., Sun P., Bao Y., Liu J., An L. Cytotoxicity of single-walled carbon nanotubes on PC12 cells. Toxicol. in Vitro 2011, 25:242-250.
50. Warheit D.B. How meaningful are the results of nanotoxicity studies in the absence of adequate material characterization?. J. Toxicol. Sci. 2008, 101:183-185.
51. White C.C., Viernes H., Krejsa C.M., Botta D., Kavanagh T.J. Fluorescence-based microtiter plate assay for glutamate-cysteine ligase activity. Anal. Biochem. 2003, 318:175-180.
52. Yang S.T., Fernando K.A., Liu J.H., Wang J., Sun H.F., Liu Y., Chen M., Huang Y., Wang X., Wang H., Sun Y.P. Covalently Pegylated carbon nanotubes with stealth character in vivo. Small 2008, 4(7):940-944.
53. Yang S.T., Wang X., Jia G., Gu Y., Wang T., Nie H., Ge C., Wang H., Liu Y. Long-term acumulation and low toxicity of single wall carbon nanotubes in intravenously exposed mice. Toxicol. Lett. 2008, 181(3):182-189.
54. Zhang Y., Bai Y., Yan B. Functionalized carbon nanotubes for potential medicinal applications. Drug Discov. Today 2010, 15:428-435.
55. Zhang Y., Xu Y., Li Z., Chen T., Lantz S.M., Howard P.C., Paule M.G. Mechanistic toxicity evaluation of uncoated and pegylated single-walled carbon nanotubes in neuronal PC12 cells. ACS Nano 2011, 5(9):7020-7033.
56. Zhao W., Karp J.M., Ferrari M., Serda R. Bioengineering nanotechnology: towards the clinic. Nanotechnology 2011, 22(49):490201.