368
Views
24
CrossRef citations to date
0
Altmetric
Articles

Toxic and genotoxic effects of graphene and multi-walled carbon nanotubes

ORCID Icon &
Pages 645-660 | Received 31 Mar 2018, Accepted 02 May 2018, Published online: 06 Jun 2018

References

  • Ai, J., E. Biazar, M. Jafarpour, M. Montazeri, A. Majdi, S. Aminifard, M. Zafari, H. R. Akbari, and H. G. Rad. 2011. Nanotoxicology and nanoparticle safety in biomedical designs. International Journal Nanomedicine 6:1117–27.
  • Alaraby, M., B. Annangi, R. Marcos, and A. Hernández. 2016. Drosophila Melanogaster as a suitable in vivo model to determine potential side effects of nanomaterials: A review. Journal Toxicogical Environment Health B 19:65–104.
  • Aqel, A., K. M. M. A. El-Nour, R. A. A. Ammar, and A. Al-Warthan. 2012. Carbon nanotubes, science and technology part (I) structure, synthesis and characterisation. Arab Journal Chemical 5:1–23.
  • Arul Prakash, F., G. J. Dushendra Babu, M. Lavanya, K. Shenbaga Vidhya, and T. Devasena. 2011. Toxicity studies of aluminium oxide nanoparticles in cell lines. International Journal Nanotechnol Appications 5:99–107.
  • Bengtson, S., K. Kling, A. M. Madsen, A. W. Noergaard, N. R. Jacobsen, P. A. Clausen, B. Alonso, A. Pesquera, A. Zurutuza, R. Ramos, H. Okuno, J. Dijon, H. Wallin, and U. Vogel. 2016. No cytotoxicity or genotoxicity of graphene and graphene oxide in murine lung epithelial FE1 cells. In Vitro Environment Molecular Mutagen 57:469–82.
  • Bianco, A., H. M. Cheng, T. Enoki, Y. Gogots, R. H. Hurt, N. Koratkar, T. Kyotani, M. Monthioux, C. R. Park, J. M. D. Tascon, and J. Zhang. 2013. All in the graphene family GÇô A recommended nomenclature for two-dimensional carbon materials. Carbon 65:1–6.
  • Bunderson-Schelvan, M., A. Holian, and R. F. Hamilton. 2017. Engineered nanomaterial-induced lysosomal membrane permeabilization and anti-cathepsin agents. Journal Toxicogical Environment Health B 20:230–48.
  • Carneiro, M. F. H., and F. Barbosa, Jr. 2016. Gold nanoparticles: A critical review of therapeutic applications and toxicological aspects. Journal Toxicogical Environment Health B 19:129–48.
  • Cavallo, D., C. Fanizza, C. L. Ursini, S. Casciardi, E. Paba, A. Ciervo, A. M. Fresegna, R. Maiello, A. M. Marcelloni, G. Buresti, F. Tombolini, S. Bellucci, and S. Iavicoli. 2012. Multi-walled carbon nanotubes induce cytotoxicity and genotoxicity in human lung epithelial cells. Journal Applications Toxicogical 32:454–64.
  • Chatterjee, N., J. Yang, and J. Choi. 2016. Differential genotoxic and epigenotoxic effects of graphene family nanomaterials (GFNs) in human bronchial epithelial cells. Mutat Res-Genet Toxicogical Environment Mutagen 798-799:1–10.
  • Chen, T., K. Harrington-Brock, and M. M. Moore. 2002. Mutant frequencies and loss of heterozygosity induced by N-ethyl-N-nitrosourea in the thymidine kinase gene of L5178Y/TK+/−-3.7.2C mouse lymphoma cells. Mutagenesis 17:105–09.
  • Chen, T., and M. M. Moore. 2004. Screening for chemical mutagens using the mouse lymphoma assay. In Optimization in Drug Discovery: In-vitro Methods, editors., 337–52. Totowa, NJ: Humana Press.
  • Clark, L. S., K. Harrington-Brock, J. Wang, L. Sargent, D. Lowry, S. H. Reynolds, and M. M. Moore. 2004. Loss of P53 heterozygosity is not responsible for the small colony thymidine kinase mutant phenotype in L5178Y mouse lymphoma cells. Mutagenesis 19:263–68.
  • Committee for Review of the Federal Strategy to Address Environmental, Health and Safety Research Needs for Engineered Nanoscale Materials, Committee on Toxicology, National Research Council. 2009. Review of federal strategy for nanotechnology-related environmental. Health, and Safety Research. Washington (DC), USA: National Academies Press.
  • Demir, E., and V. Castranova. 2016. Genotoxic effects of synthetic amorphous silica nanoparticles in the mouse lymphoma assay. Toxicogical Reports 3:807–15.
  • Demir, E., A. Creus, and R. Marcos. 2017. Titanium dioxide and zinc oxide nanoparticles are not mutagenic in the mouse lymphoma assay but modulate the mutagenic effect of UV-C-light post-treatment. Fresen Environment Bulletin 26:1001–16.
  • Demir, E., B. Kaya, C. Soriano, A. Creus, and R. Marcos. 2011. Genotoxic analysis of four lipid peroxidation products in the mouse lymphoma assay. Mutation Research 726:98–103.
  • Ding, L., J. Stilwel, T. Zhang, O. Elboudwarej, H. Jiang, J. P. Seleque, P. A. Cooke, J. W. Gray, and F. F. Chen. 2005. Molecular characterization of the cytotoxic mechanism of multiwall carbon nanotubes and nano-onions on human skin fibroblast. Nano Letters 5:2448–64.
  • Dreher, K. L. 2004. Health and environmental impact of nanotechnology: Toxicological assessment of manufactured nanoparticles. Toxicological Sciences : an Official Journal of the Society of Toxicology 77:3–5.
  • Durga, M., F. Arul Prakash, A. Rajasekar, and T. Devasena. 2012. Potential cell line toxicity of environmental nanoparticles. International Researcher Journal Pharmaceutical 3:145–49.
  • Ema, M., M. Gamo, and K. Honda. 2017. A review of toxicity studies on graphene-based nanomaterials in laboratory animals. Reg Toxicogical Pharmacology 85:724.
  • Ema, M., T. Imamura, H. Suzuki, N. Kobayashi, M. Naya, and J. Nakanishi. 2012. Evaluation of genotoxicity of multi-walled carbon nanotubes in a battery of in vitro and in vivo assays. Reg Toxicogical Pharmacology 63:188–95.
  • Fenoglio, I., M. Tomatis, D. Lison, J. Muller, A. Fonseca, J. B. Nagy, and B. Fubini. 2006. Reactivity of carbon nanotubes: Free radical generation or scavenging activity? Free Radical Biology & Medicine 40:1227–33.
  • Ghosh, M., A. Chakraborty, M. Bandyopadhyay, and A. Mukherjee. 2011. Multi-walled carbon nanotubes (MWCNT): Induction of DNA damage in plant and mammalian cells. Journal of Hazardous Materials 197:327–36.
  • Guo, N. L., Y. W. Wan, J. Denvir, D. W. Porter, M. Pacurari, M. G. Wolfarth, V. Castranova, and Y. Qian. 2012. Multi-walled carbon nanotube-induced gene signatures in the mouse lung: Potential predictive value for human lung cancer risk and prognosis. Journal Toxicogical Environment Health A 75:1129–53.
  • Hartmann, N. B., K. A. Jensen, A. Baun, K. Rasmussen, H. Rauscher, R. Tantra, D. Cupi, D. Gilliland, F. Pianella, and J. M. Riego Sintes. 2015. Techniques and protocols for dispersing nanoparticle powders in aqueous media- Is there a rationale for harmonization? Journal Toxicogical Environment Health B 18:299–326.
  • Hashemi, E., O. Akhavan, M. Shamsara, M. Daliri, M. Dashtizad, and A. Farmany. 2016. Synthesis and cyto-genotoxicity evaluation of graphene on mice spermatogonial stem cells. Colloids Surf. B Biointerfaces 146:770–76.
  • Horibata, K., A. Ukai, A. Ogata, D. Nakae, H. Ando, Y. Kubo, A. Nagasawa, K. Yuzawa, and M. Honma. 2017. Absence of in vivo mutagenicity of multi-walled carbon nanotubes in single intratracheal instillation study using F344 gpt delta rats. Genes Environment 39:4.
  • Hu, X., and Q. Zhou. 2013. Health and ecosystem risks of graphene. Chemical Reviews 113:3815–35.
  • ICH. 2008. International Conference on Harmonization, Guidance on genotoxicity testing and data interpretation for pharmaceuticals intended for human use. http://www.ich.org/cache/compo/502-272-1.html.
  • Ji, W., H. Liang, W. Zhou, and X. Zhang. 2011. Apoptotic responses of zebrafish (Danio rerio) after exposure with microcystin-LR under different ambient temperatures. Journal Applications Toxicogical 33:799–806.
  • Kato, T., Y. Totsuka, K. Ishino, Y. Matsumoto, Y. Tada, D. Nakae, S. Goto, S. Masuda, S. Ogo, M. Kawanishi, T. Yagi, T. Matsuda, M. Watanabe, and K. Wakabayashi. 2013. Genotoxicity of multi-walled carbon nanotubes in both in vitro and in vivo assay systems. Nanotoxicology 7:452–61.
  • Kermanizadeh, A., I. Gosens, L. MacCalman, H. Johnston, P. H. Danielsen, N. R. Jacobsen, A. G. Lenz, T. Fernandes, R. P. Schins, F. R. Cassee, H. Wallin, W. Kreyling, T. Stoeger, S. Loft, P. Moller, L. Tran, and V. Stone. 2016. A Multilaboratory toxicological assessment of a panel of 10 engineered nanomaterials to human health–ENPRA Project–The Highlights, limitations, and current and future challenges. Journal Toxicogical Environment Health Particle B 19:1–28.
  • Kisin, E. R., A. R. Murray, M. J. Keane, X. C. Shi, D. Schwegler-Berry, O. Gorelik, S. Arepalli, V. Castranova, W. E. Wallace, V. E. Kagan, and A. A. Shvedova. 2007. Single-walled carbon nanotubes: Geno- and cytotoxic effects in lung fibroblast V79 cells. Journal Toxicogical Environment Health Particle A 70:2071–79.
  • Kroll, A., M. H. Pillukat, D. Hahn, and J. Schnekenburger. 2012. Interference of engineered nanoparticles with in vitro toxicity assays. Archives of Toxicology 86:1123–36.
  • Landsiedel, R., M. D. Kapp, M. Schulz, K. Wiench, and F. Oesch. 2009. Genotoxicity investigations on nanomaterials: Methods, preparation and characterization of test material, potential artifacts and limitations -many questions, some answers. Mutation Research 681:241–58.
  • Lankoff, A., M. Arabski, A. Wegierek-Ciuk, M. Kruszewski, H. Lisowska, A. Banasik-Nowak, K. Rozga-Wijas, M. Wojewodzka, and S. Slomkowski. 2013. Effect of surface modification of silica nanoparticles on toxicity and cellular uptake by human peripheral blood lymphocytes. In Vitro. Nanotoxicology 7:235–50.
  • Lanone, S., F. Rogerieux, J. Geys, A. Dupont, E. Maillot-Marechal, J. Boczkowski, G. Lacroix, and P. Hoet. 2009. Comparative toxicity of 24 manufactured nanoparticles in human alveolar epithelial and macrophage cell lines. Particle Fibre Toxicogical 6:14.
  • Li, X. L., Y. S. Wong, G. Xu, and J. C. N. Chan. 2015. Selenium-enriched Spirulina protects INS-1E pancreatic beta cells from human islet amyloid polypeptide-induced apoptosis through suppression of ROS-mediated mitochondrial dysfunction and PI3/AKT pathway. European Journal Nutritional 54:509–22.
  • Lindberg, H. K., G. C. Falck, R. Singh, S. Suhonen, H. Järventaus, E. Vanhala, J. Catalán, P. B. Farmer, K. M. Savolainen, and H. Norppa. 2013. Genotoxicity of short single-wall and multi-wall carbon nanotubes in human bronchial epithelial and mesothelial cells in vitro. Toxicology 313:24–37.
  • Maisanaba, S., A. I. Prieto, M. Puerto, D. Gutiérrez-Praena, E. Demir, R. Marcos, and A. M. Cameán. 2015. In vitro genotoxicity testing of carvacrol and thymol using the micronucleus and mouse lymphoma assays. Mutat Res-Genet Toxicogical Environment Mutagen 784-785:37–44.
  • Martinez Paino, I. M., F. Santos, and V. Zucolotto. 2017. Biocompatibility and toxicology effects of graphene oxide in cancer, normal, and primary immune cells. Journal Biomedical MaterRes A 105A:728–36.
  • Martins, A. D. C., Jr., L. F. Azevedo, C. C. De Souza Rocha, M. F. H. Carneiro, V. P. Venancio, M. R. De Almeida, L. M. G. Antunes, R. De CarvalhoHott, J. L. Rodrigues, A. T. Ogunjimi, J. A. Adeyemi, and F. Barbosa, Jr. 2017. Evaluation of distribution, redox parameters, and genotoxicity in Wistar rats co-exposed to silver and titanium dioxide nanoparticles. Journal Toxicogical Environment Health A 80:1156–65.
  • Maynard, A. D., R. J. Aitken, T. Butz, V. Colvin, K. Donaldson, G. Oberdörster, M. A. Philbert, J. Ryan, A. Seaton, V. Stone, S. S. Tinkle, L. Tran, N. J. Walker, and D. B. Warheit. 2006. Safe handling of nanotechnology. Nature 444:267–69.
  • Mei, N., X. Guo, and M. M. Moore. 2014. Methods for using the mouse lymphoma assay to screen for chemical mutagenicity and photo-mutagenicity. In Optimization in Drug Discovery: In Vitro Methods, Methods in Pharmacology and Toxicology, eds. 561–92. New York: Springer Science+Business Media.
  • Monteiro-Riviere, N. A., and A. O. Inman. 2006. Challenges for assessing carbon nanomaterial toxicity to the skin. Carbon 44:1070–78.
  • Monteiro-Riviere, N. A., A. O. Inman, Y. Y. Wang, and R. J. Nemanich. 2005a. Surfactant effects on carbon nanotube interactions with human keratinocytes. Nanomed-Nanotechnol 1:293–99.
  • Monteiro-Riviere, N. A., R. J. Nemanich, A. O. Inman, Y. Y. Wang, and J. E. Riviere. 2005b. Multi-walled carbon nanotube interactions with human epidermal keratinocytes. Toxicology Letters 155:377–84.
  • Moore, M. M., M. Honma, J. Clements, G. Bolcsfoldi, B. Burlinson, M. Cifone, J. Clarke, P. Clay, R. Doppalapudi, M. Fellows, B. Gollapudi, S. Hou, P. Jenkinson, W. Muster, K. Pant, D. A. Kidd, E. Lorge, M. Lloyd, B. Myhr, M. O’Donovan, C. Riach, L. F. Stankowski, Jr., A. K. Thakur, and F. Van Goethem. 2007. Mouse lymphoma thymidine kinase gene mutation assay: Meeting of the International Workshop on Genotoxicity Testing, San Francisco, 2005, recommendations for 24-h treatment. Mutation Research 627:36–40.
  • Moore, M. M., M. Honma, J. Clements, G. Bolcsfoldi, B. Burlinson, M. Cifone, J. Clarke, R. Delongchamp, R. Durward, M. Fellows, B. Gollapudi, S. Hou, P. Jenkinson, M. Lloyd, J. Majeska, B. Myhr, M. O’Donovan, T. Omori, C. S. Riach, R. An, L. F. Stankowski, Jr., A. K. Thakur, F. VanGoethem, S. Wakuri, and I. Yoshimura. 2006. Mouse lymphoma thymidine kinase gene mutation assay: Follow up meeting of the International Workshop on Genotoxicity Testing-Aberdeen, Scotland, 2003-Assay acceptance criteria, positive controls, and data evaluation. Environment Molecular Mutagen 47:1–5.
  • Moore, M. M., M. Honma, J. Clements, G. Bolcsfoldi, M. Cifone, R. Delongchamp, M. Fellows, B. Gollapudi, P. Jenkinson, P. Kirby, S. Kirchner, W. Muster, B. Myhr, M. O’Donovan, J. Oliver, T. Omori, M. C. Ouldelhkim, K. Pant, R. Preston, C. Riach, R. San, L. F. Stankowski, Jr., A. Thakur, S. Wakuri, and I. Yoshimura. 2003. Mouse lymphoma thymidine kinase gene mutation assay: Workshop on Genotoxicity TestingWorkgroup Report-Plymouth, UK, 2002. Mutation Research 540:127–40.
  • Nanogenotox. 2011. http://www.nanogenotox.eu/files/PDF/Deliverables/nanogenotox%20delivera-ble%203_wp4_%20dispersion%20protocol.pdf.
  • Niitsuya, M., M. Watanabe, M. Okada, H. Shinji, T. Satoh, Y. Aizawa, Y. C. Cho, and M. Kotani. 2003. Magnetometricevaluation of cadmium oxide-induced toxicity to pulmonary alveolar macrophages of Syrian golden hamsters. Journal Toxicol Environment Health A 66:365–78.
  • Oberdörster, G., V. Castranova, B. Asgharian, and P. Sayre. 2015. Inhalation exposure to carbon nanotubes (CNT) and carbon nanofibers (CNF): Methodology and dosimetry. Journal Toxicogical Environment Health B 18:121–212.
  • OECD. 2015. OECD guidelines for the testing of chemicals, section 4: Health effects. Test No. 490: In Vitro Mammalian Cell Gene Mutation Tests Using the Thymidine Kinase Gene. Published 28 July, 2015.
  • Petibone, D. M., T. Mustafa, S. E. Bourdo, A. Lafont, W. Ding, A. Karmakar, Z. A. Nima, F. Watanabe, D. Casciano, S. M. Morris, V. N. Dobrovolsky, and A. S. Biris. 2017. p53-competent cells and p53-deficient cells display different susceptibility to oxygen functionalized graphene cytotoxicity and genotoxicity. Journal Applications Toxicogical 37:1333–45.
  • Platel, A., R. Carpentier, E. Becart, G. Mordacq, D. Betbeder, and F. Nesslany. 2016. Influence of the surface charge of PLGA nanoparticles on their in vitro genotoxicity, cytotoxicity, ROS production and endocytosis. Journal Applications Toxicogical 36:434–44.
  • Rubio, L., N. El Yamani, A. Kazimirova, M. Dusinska, and R. Marcos. 2016. Multi-walled carbon nanotubes (NM401) induce ROS-mediated HPRT mutations in Chinese hamster lung fibroblasts. Environmental Research 146:185–90.
  • Sargent, L. M., A. F. Hubbs, S. H. Young, M. L. Kashon, C. Z. Dinu, J. L. Salisbury, S. A. Enkovic, D. T. Lowry, A. R. Murray, E. R. Kisin, K. J. Siegrist, L. Battelli, J. Mastovich, J. L. Sturgeon, K. L. Bunker, A. A. Shvedova, and S. H. Reynolds. 2012. Single-walled carbon nanotube-induced mitotic disruption. Mutation Research 745:28–37.
  • Sarkar, B., S. Mandal, Y. F. Tsang, P. Kumar, K. H. Kim, and Y. S. Ok. 2018. Designer carbon nanotubes for contaminant removal in water and wastewater: A critical review. The Science of the Total Environment 612:561–81.
  • Shen, H., L. Zhang, M. Liu, and Z. Zhang. 2012. Biomedical applications of graphene. Theranostics 2:283–94.
  • Siegrist, K. J., S. H. Reynolds, M. I. Kashon, D. T. Lowry, C. Dong, A. F. Hubbs, S. H. Young, J. L. Salisbury, D. W. Porter, S. A. Benkovik, M. McCawley, M. J. Keane, J. T. Mastovich, K. L. Bunker, L. G. Cena, M. C. Sparrow, J. L. Sturgeon, C. Z. Dinu, and L. M. Sargent. 2014. Genotoxicity of multi-walled carbon nanotubes at occupationally relevant doses. Particle Fibre Toxicogical 11:6.
  • Simon-Deckers, A., B. Gouget, M. Mayne-L’hermite, N. Herlin-Boime, C. Reynaud, and M. Carrière. 2008. In vitro investigation of oxide nanoparticle and carbon nanotube toxicity and intracellular accumulation in A549 human pneumocytes. Toxicology 253:137–46.
  • Singh, N., B. Manshian, G. J. Jenkins, S. M. Griffiths, P. M. Williams, T. G. Maffeis, C. J. Wright, and S. H. Doak. 2009. NanoGenotoxicology: The DNA damaging potential of engineered nanomaterials. Biomaterials 30:3891–914.
  • Soriano, C., A. Creus, and R. Marcos. 2007. Gene-mutation induction by arsenic compounds in the mouse lymphoma assay. Mutation Research 634:40–50.
  • Souza, J. P., J. F. Baretta, F. Santos, I. M. M. Paino, and V. Zucolotto. 2017. Toxicological effects of graphene oxide on adult zebrafish (Danio rerio). Aquatic Toxicology (Amsterdam, Netherlands) 186:11–18.
  • Toduka, Y., T. Toyooka, and Y. Ibuki. 2012. Flow cytometric evaluation of nanoparticles using side-scattered light and reactive oxygen species-mediated fluorescence-correlation with genotoxicity. Environmental Science & Technology 46:7629–36.
  • Ursini, C. L., D. Cavallo, A. M. Fresegna, A. Ciervo, R. Maiello, G. Buresti, S. Casciardi, F. Tombolini, S. Bellucci, and S. Iavicoli. 2012. Comparative cyto-genotoxicity assessment of functionalized and pristine multiwalled carbon nanotubes on human lung epithelial cells. Toxicogical In Vitro 26:831–40.
  • Ursini, C. L., R. Maiello, A. Ciervo, A. M. Fresegna, G. Buresti, F. Superti, M. Marchetti, S. Iavicoli, and D. Cavallo. 2016. Evaluation of uptake, cytotoxicity and inflammatory effects in respiratory cells exposed to pristine and -OH and -COOH functionalized multi-wall carbon nanotubes. Journal Applications Toxicogical 36:394–403.
  • Vales, G., L. Rubio, and R. Marcos. 2016. Genotoxic and cell-transformation effects of multiwalled carbon nanotubes (MWCNT) following in vitro sub-chronic exposures. Journal of Hazardous Materials 306:193–202.
  • Wang, J., Y. Chen, C. Lin, J. Jia, L. Tian, K. Yang, L. Zhao, N. Lai, Q. J Iang, Y. Sun, N. Zhong, P. Ran, and W. Lu. 2014. Effects of chronic exposure to cigarette smoke on canonical transient receptor potential expression in rat pulmonary arterial smooth muscle. American Journal Physiological Cellular Physiological 306:364–73.
  • Wick, P., P. Manser, L. K. Limbach, U. Dettlaff-Weglikowska, F. Krumeich, S. Roth, W. J. Stark, and A. Bruinink. 2007. The degree and kind of agglomeration affect carbon nanotube cytotoxicity. Toxicology Letters 168:121–31.
  • Xia, T., R. F. Hamilton, J. C. Bonner, E. D. Crandall, A. Elder, F. Fazlollahi, T. A. Girtsman, K. Kim, S. Mitra, S. A. Ntim, G. Orr, M. Tagmount, A. J. Taylor, D. Telesca, A. Tolic, C. D. Vulpe, A. J. Walker, X. Wang, F. A. Witzmann, N. Wu, Y. Xie, J. I. Zink, A. Nel, and A. Holian. 2013. Interlaboratory evaluation of in vitro cytotoxicity and inflammatory responses to engineered nanomaterials: The NIEHS Nano GO Consortium. Environment Health Persp 121:683–90.
  • Xu, L., Q. L. Zhang, F. P. Gao, J. S. Nie, and Q. Niu. 2010. Cell toxicity assessment methodologies applied in the study of the toxicity of nano-alumina to nerve cells. Zhonghua Yu Fang Yi XueZaZhi 44:785–89.
  • Zhao, J., and V. Castranova. 2011. Toxicology of nanomaterials used in nanomedicine. Journal Toxicogical Environment Health B 14:593–632.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.