Biosafety of multiwalled carbon nanotube in mice: A behavioral toxicological approach

Journal of Toxicological Sciences

Volumn 37, Issue 6, 2012, Pages 1191-1205

  Ivani, Saeed ^a   Karimi, Isaac ^b   Tabatabaei, Seyed Reza Fatemi ^a  

^a SHAHID CHAMRAN UNIVERSITY OF AHVAZ   (Iran)

^b RAZI UNIVERSITY   (Iran)

Author keywords

Anxiety; Carbon nanotubes; Depression; Memory; Neurobehavioral development; Pregnancy

Indexed keywords

CARBON NANOTUBE; DRUG VEHICLE; MULTI WALLED NANOTUBE; PHOSPHATE BUFFERED SALINE;

ANIMAL EXPERIMENT; ANXIETY; ARTICLE; BEHAVIOR; BIOSAFETY; COGNITION; CONTROLLED STUDY; DEPRESSION; DRUG DELIVERY SYSTEM; FEMALE; LIVER WEIGHT; MATING; MOUSE; NEUROTOXICITY; NONHUMAN; ORGAN WEIGHT; PREGNANCY; PRENATAL EXPOSURE; PSYCHOBIOLOGY; SPLEEN WEIGHT; THYMUS;

EID: 84870865464     PISSN: 03881350     EISSN: 18803989     Source Type: Journal    
DOI: 10.2131/jts.37.1191     Document Type: Article

References (64)

1. Amusquivar, E., Rupérez, F.J., Barbas, C. and Herrera, E. (2000): Low arachidonic acid rather than alpha-tocopherol is responsible for the delayed postnatal development in offspring of rats fed fish oil instead of olive oil during pregnancy and lactation. J. Nutr., 130, 2855-2865.
2. Bai, Y., Zhang, Y., Zhang, J., Mu, Q., Zhang, W., Butch, E.R., Snyder, S.E. and Yan, B. (2010): Repeated administrations of carbon nanotubes in male mice cause reversible testis damage without affecting fertility. Nature Nanotechnol., 5, 683-689.
3. Bottini, M., Bruckner, S., Nika, K., Bottini, N., Bellucci, S. and Magrini, A. (2006): Multi-walled carbon nanotubes induce T lymphocyte apoptosis. Toxicol. Lett., 160, 121-126.
4. Brambilla, F., Biggio, G., Pisu, M.G., Purdy, R.H., Gerra, G., Zaimovich, A. and Serra, M. (2004): Plasma concentrations of anxiolytic neurosteroids in men with normal anxiety scores: a correlation analysis. Neuropsychobiology, 50, 6-9.
5. Cadenhead, K.S., Geyer, M.A. and Braff, D.L. (1993): Impaired startle prepulse inhibition and habituation in patients with schizotypal personality disorder. Am. J. Psychiat., 150, 1862-1867.
6. Chou, C.C., Hsiao, H.Y., Hong, Q.S., Chen, C.H., Peng, Y.W., Chen, H.W. and Yang, P.C. (2008): Single-walled carbon nanotubes can induce pulmonary injury in mouse model. Nano. Lett., 8, 437-445.
7. Cui, D., Tian, F., Ozkan, C.S., Wang, M. and Gao, H. (2005): Effect of single wall carbon nanotubes on human HEK293 cells. Toxicol. Lett., 155, 73-85.
8. Cuomo, V., Salvia, M.A.D., Petruzzi, S. and Alleva, E. (1996): Appropriate end points for the characterization of behavioral changes in developmental toxicology. Environ. Health Persp., 104, 307-315.
9. Darke, S. (1988): Anxiety and working memory capacity. Cognition and Emotion., 2, 145-154.
10. Degroot, A., Kashluba, S. and Treit, D. (2001): Septal GABAergic and hippocampal cholinergic systems modulate anxiety in the plus-maze and shock-probe tests. Pharmacol. Biochem. Behav., 69, 391-399.
11. Folkmann, J.K., Risom, L., Jacobsen, N.R., Wallin, H., Loft, S. and Moller, P. (2009): Oxidatively damaged DNA in rats exposed by oral gavage to C60 fullerenes and single-walled carbon nanotubes. Environ. Health Persp., 117, 703-708.
12. Fox, W.M. (1965): Reflex-ontogeny and behavioural development of the mouse. Anim. Behav., 13, 234-241.
13. Fujitani, T., Ohyama, K., Hirose, A., Nishimura, T., Nakae, D. and Ogata, A. (2012): Teratogenicity of multi-wall carbon nanotube (MWCNT) in ICR mice. J. Toxicol. Sci., 37, 81-89.
14. Garza, K.M., Soto, K.F. and Murr, L.Z. (2008): Cytotoxicity and reactive oxygen species generation from aggregated carbon and carbonaceous nanoparticulate materials. Int. J. Nanomed., 3, 83-94.
15. Graeff, F.G., Viana, M.B. and Tomaz, C., (1993): The elevated T maze, a new experimental model of anxiety and memory: effect of diazepam. Braz J. Med. Biol. Res., 26, 67-70.
16. Heller, D., Baik, S., Eurell, T. and Strano, M. (2005): Single-walled carbon nanotube spectroscopy in live cells: towards long-term labels and optical sensors. Adv. Mater., 17, 2793-2799.
17. Hougaard, K.S., Jackson, P., Jensen, K.A., Sloth, J.J., Loschner, K., Larsen, E.H., Birkedal, R.K., Vibenholt, A., Boisen, A.M., Wallin, H. and Vogel, U. (2010): Effects of prenatal exposure to surface-coated nanosized titanium dioxide (UV-Titan). A study in mice. Part Fibre. Toxicol., 7, 16.
18. Jeffrey, A. (2011). Nanotoxicology: Nanoparticles versus the placenta. Nature Nanotechnol., 6, 263-264.
19. Jonakait, G.M. (2007): The effects of maternal inflammation on neuronal development: possible mechanisms. Int. J. Dev. Neurosci., 25, 415-425.
20. Kam, N.W. and Dai, H. (2005): Carbon nanotubes as intracellular protein transporters: generality and biological functionality. J. Am. Chem. Soc., 127, 6021-6026.
21. Karlsson, H.L., Cronholm, P., Gustafsson, J. and Möller, L. (2008): Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res. Toxicol., 21, 1726-1732.
22. Kesner, R.P., Bolland, B.L. and Dakis, M. (1993): Memory for spatial locations, motor responses, and objects: triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex. Exp. Brain Res., 93, 462-470.
23. Kiewert, C., Buchholzer, M.L., Hartmann, J., Chatterjee, S.S. and Klein, J. (2004): Stimulation of hippocampal acetylcholine release by hyperforin, a constituent of St. John's Worth. Neurosci. Lett., 364, 195-198.
24. Kihara, T. (1991): Effects of the prenatal ochratoxin-A exposure on behaviors of rat offspring. Acta Med. Kinki Univ., 16, 1-22.
25. Koren, G., Pastuszak, A. and Ito, S. (1998): Drugs in pregnancy. N. Engl. J. Med., 338, 1128-1137.
26. Kovacic, P. and Somanathan, R. (2006): Mechanism of teratogenesis: electron transfer, reactive oxygen species, and antioxidants. Birth Defects. Res. C Embryo. Today, 78, 308-325.
27. Li, J.G., Li, W.X., Xu, J.Y., Cai, X.Q., Liu, R.L. and Li, Y.J. (2007): Comparative study of pathological lesions induced by Multiwalled carbon nanotubes in lungs of mice by intratracheal instillation and inhalation. Environ. Toxicol., 22, 415-421.
28. Liang, G., Yin, L., Zhang, J., Liu, R., Zhang, T. and Ye, B. (2010): Effects of subchronic exposure to Multi-walled carbon nanotubes on mice. J. Toxicol. Environ. Health, 73, 463-470.
29. Lim, J.H., Kim, S.H., Lee, I.C., Moon, C., Kim, S.H., Shin, D. H, Kim, H.C. and Kim, J.C. (2011): Evaluation of maternal toxicity in rats exposed to Multi-walled carbon nanotubes during pregnancy. Environ Health Toxicol., 26, e2011006.
30. Lim, J.H., Kim, S.H., Shin, I.S., Park, N.H., Moon, C., Kang, S.S., Kim, S.H., Park, S.C. and Kim, J.C. (2011): Maternal exposure to Multi-walled carbon nanotubes does not induce embryofetal developmental toxicity in rats. Birth Defects. Res. B Dev. Reprod. Toxicol., 92, 69-76
31. Longone, P., Rupprecht, R., Manieri, G.A., Bernardi, G., Romeo, E. and Pasini, A. (2008): The complex roles of neurosteroids in depression and anxiety disorders. Neurochem. Int., 52, 596-601.
32. Mahmood, M., Casciano, D. Xu, Y. and Biris, A.S. (2012): Engineered nanostructural materials for application in cancer biology and medicine. J. Appl. Toxicol., 32,10-19.
33. Mattson, M.P., Haddon, R.C. and Rao, A.M. (2001): Molecular functionalization of carbon nanotubes and use as substrates for neuronal growth. J. Mol. Neurosci., 14, 175-182.
34. Meer, P.V. and Raber, J. (2005): Mouse behavioural analysis in systems biology. Biochem J., 389, 593-610.
35. Meyer, U., Feldon, J. and Fatemi, S.H. (2009): In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci. Biobehav. Res., 33, 1061-1079.
36. Mitchell, L.A., Gao, J., Wal, R.V., Gigliotti, A., Burchiel, S.W. and McDonald, J.D. (2007): Pulmonary and systemic immune response to inhaled multiwalled carbon nanotubes. Toxicol. Sci., 100, 203-214.
37. Morris, R.G.M. (1984): Development of water maze procedure for studying spatial learning in the rat. J. Neurosci. Meth., 11, 47-60.
38. Muller, J., Delos, M., Panin, N., Rabolli, V., Huaux, F. and Lison, D. (2009): Absence of carcinogenic response to multi-wall carbon nanotubes in a 2-year bioassay in the peritoneal cavity of the rat. Toxicol. Sci., 110, 442-448.
39. Muller, J., Huaux, F., Moreau, N., Misson, P., Heilier, J.F. and Delos, M. (2005): Respiratory toxicity of Multiwalled carbon nanotubes. Toxicol. Appl. Pharm., 207, 221-231.
40. Oberdorster, G., Oberdörster, E. and Oberdörster, J. (2005): Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ. Health Persp., 113, 823-839.
41. Pacurari, M., Yin, X.J., Zhao, J., Ding, M., Leonard, S.S. and Schwegler-Berry, D. (2008): Raw single-wall carbon nanotubes induce oxidative stress and activate MAPKs, AP-1, NF-kappaB, and Akt in normal and malignant human mesothelial cells. Environ Health Persp., 116, 1211-1217.
42. Patlolla, A., Knighten, B. and Tchounwou, P. (2010): Multi-walled carbon nanotubes induce cytotoxicity, genotoxicity and apoptosis in normal human dermal fibroblast cells. Ethnic Dis., 20, 65-72.
43. Pauluhn, J. (2010): Subchronic 13-week inhalation exposure of rats to multiwalled carbon nanotubes: toxic effects are determined by density of agglomerate structures, not fibrillar structures. Toxicol. Sci., 113, 226-242.
44. Pietroiusti, A., Massimiani, M., Fenoglio, I., Colonna, M., Valentini, F., Palleschi, G., Camaioni, A., Magrini, A., Siracusa, G., Bergamaschi, A., Sgambato, A. and Campagnolo, L. (2011): Low doses of pristine and oxidized single-wall carbon nanotubes affect mammalian embryonic development. J. Am. Chem. Soc., 5, 4624-4633.
45. Ratnasooriya, W.D., Jayakody, J.R.A.C. and Premakumara, G.A.S. (2003): Adverse pregnancy outcome in rats following exposure to a Salacia reticulata (Celastraceae) root extract. Braz. J. Med. Biol. Res., 36, 931-935.
46. Rodgers, R.J. and Johnson, N.J. (1995): Factor analysis of spatiotemporal and ethological measures in the murine elevated plusmaze test of anxiety. Pharmacol. Biochem. Behav., 52, 297-303.
47. Sampson, D.A. and Jansen, G.R. (1984): Measurement of milk yield in the lactating rat from pup weight and weight gain. J. Pediatr. Gastroenterol. Nutr., 3, 613-617.
48. Sato, Y., Yokoyama, A., Shibata, K., Akimoto, Y., Ogino, S. and Nodasaka, Y. (2005): Influence of length on cytotoxicity of Multi-walled carbon nanotubes against human acute monocytic leukemia cell line THP-1 in vitro and subcutaneous tissue of rats in vivo. Mol. Biosyst., 1, 176-182.
49. Shimizu, M., Tainaka, H., Oba, T., Mizuo, K., Umezawa, M. and Takeda, K. (2009): Maternal exposure to nanoparticulate titanium dioxide during the prenatal period alters gene expression related to brain development in the mouse. Part Fibre Toxicol., 6, 20.
50. Shvedova, A.A., Castranova, V., Kisin, E.R., Schwegler-Berry, D., Murray, A.R. and Gandelsman, V.Z. (2003): Exposure to carbon nanotube material: assessment of nanotube cytotoxicity using human keratinocytes cells. J. Toxicol. Env. Health, 66, 1909-1926.
51. Swerdlow, N.R., Benbow, C.H., Zisook, S., Geyer, M.A. and Braff, D.L. (1993): A preliminary assessment of sensorimotor gating in patients with obsessive compulsive disorder. Biol. Psychiat., 33, 298-301.
52. Takeda, K., Suzuki, K., Ishihara, A., Kubo-Irie, M., Fujimoto, R., Tabata, M., Oshio, S., Nihei, Y., Ihara, T. and Sugamata, M. (2009): Nanoparticles transferred from pregnant mice to their offspring can damage the genital and cranial nerve systems. J. Health Sci., 55, 95-102.
53. Tanimura, T. (1992): Update on the activities of the Japanese behavioral teratology meeting. Cong Anom., 32, 7-20.
54. Thurnherr, T., Su, D.S., Diener, L., Weinberg, G., Manser, P., Pfänder, N., Arrigo, R., Schuster M.E., Wick, P. and Krug, H.F. (2009): Comprehensive evaluation of in vitro toxicity of three large-scale produced carbon nanotubes on human Jurkat T cells and a comparison to crocidolite asbestos. Nanotoxicology, 3, 319-338.
55. Vajtai, R., Wei, B.Q. and Ajayan, P.M. (2004): Controlled growth of carbon nanotubes. Phil. Trans. R. Soc. Lond., 362, 2143-2160.
56. Viana, M.B., Tomaz, C. and Graeff, F.G. (1994): The elevated T-maze: a new animal model of anxiety and memory. Pharmacol. Biochem. Behav., 49, 549-554.
57. Wessels, A., Van Berlo, D., Boots, A.W., Gerloff, K., Scherbart, A.M., Cassee, F.R., Gerlofs-Nijland, M.E., Van Schooten, F.J., Albrecht, C. and Schins, R.P. (2011): Oxidative stress and DNA damage responses in rat and mouse lung to inhaled carbon nanoparticles. Nanotoxicology, 5, 66-78.
58. Wick, P., Malek, A., Manser, P., Meili, D., Althaus, X.M., Diener, L., Diener, P.A., Zisch, A., Krug, H.F. and Mandach, U. (2010): Barrier capacity of human placenta for nanosized materials. Environ. Health Persp., 118, 432-436.
59. Wolansky, M.J. and Harrill, J.A. (2008): Neurobehavioral toxicology of pyrethroid insecticides in adult animals: A critical review, neurotoxicology and teratology. Neurotoxicol. Teratol., 30, 55-78.
60. Xia, T., Kovochich, M., Brant, J., Hotze, M., Sempf, J., Oberley, T., Sioutas, C., Yeh, J.I., Wiesner, M.R. and Nel, A.E. (2006): Comparison of the abilities of ambient and manufactured nanoparticles to induce cellular toxicity according to an oxidative stress paradigm. Nano Lett., 6, 1794-1807.
61. Yamashita, K., Yoshioka, Y., Higashisaka, K., Mimura, K., Morishita, Y., Nozaki, M., Yoshida, T., Ogura, T., Nabeshi, H., Nagano, K., Abe, Y., Kamada, H., Monobe, Y., Imazawa, T., Aoshima, H., Shishido, K., Kawai, Y., Mayumi, T., Tsunoda, S., Itoh, N., Yoshikawa, T., Yanagihara, I., Saito, S. and Tsutsumi, Y. (2011): Silica and titanium dioxide nanoparticles cause pregnancy complications in mice. Nature Nanotechnol., 6, 321-328.
62. Yang, Z., Zhang, Y., Yang, Y., Sun, L., Han, D., Li, H. and Wang, C. (2010): Pharmacological and toxicological target organelles and safe use of single-walled carbon nanotubes as drug carriers in treating Alzheimer disease. Nanomed Nanotechnol., 6, 427-441.
63. Yee, B.K., Keist, R., von Boehmer, L., Studer, R., Benke, D., Hagenbuch, N., Dong, Y., Malenka, R.C., Fritschy, J.M., Bluethmann, H., Feldon, J., Möhler, H. and Rudolph, U. (2005): A schizophrenia-related sensorimotor deficit links 3-containing GABA A receptors to dopamine hyperfunction. Proc. Natl. Acad. Sci. USA, 102, 17154-17159.
64. Yousofi, M., Saberivand, A., Becker, L.A. and Karimi, I. (2011): The effects of Cannabis sativa L. seed (hemp seed) on reproductive and neurobehavioral end points in rats. Dev Psychobiol., 53, 402-412.