Generic placeholder image

Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

General Review Article

The Neurotoxic Mechanisms of Graphene Family Nanomaterials at the Cellular Level: A Solution-based Approach Review

Author(s): Mohammad Mahdi Ghazimoradi, Farhan Vahdat Azad, Fatemeh Jalali and Mahmoud Rafieian-Kopaei*

Volume 28, Issue 44, 2022

Published on: 13 December, 2022

Page: [3572 - 3581] Pages: 10

DOI: 10.2174/1381612829666221202093813

Price: $65

Abstract

The graphene family nanomaterials (GFNs) have been recognized to have potential applications in biomedicine, especially in the rag nostic, drug delivery and neuroimaging. Multiple studies have examined the neurotoxicity of GFNs to assay their toxic effects on organisms and ecosystems. In this article, we reviewed the different neurotoxicity effects of GFNs at intracellular levels, including nucleus-related effects and cytosolic mechanisms, as well as extracellular levels, including effects on enzyme activity, oxidative stress, behavior, neurotransmitters, and central nervous system (CNS). Furthermore, for the sake of the solution, we discussed the reducing ways of graphene toxicity. A schematic description is shown in Fig. (1).

Keywords: Graphene family, nanomaterials, neurotoxicity, molecular, cellular, neurotransmitters, animal models.

« Previous
[1]
Patel TN, Priyanka R, Vashi Y, Bhattacharya P. Toxic impacts and industrial potential of graphene. J Environ Sci Health C Toxicol Carcinog 2020; 38(3): 269-97.
[http://dx.doi.org/10.1080/26896583.2020.1812335]
[2]
Liao C, Li Y, Tjong S. Graphene nanomaterials: Synthesis, biocompatibility, and cytotoxicity. Int J Mol Sci 2018; 19(11): 3564.
[http://dx.doi.org/10.3390/ijms19113564] [PMID: 30424535]
[3]
Bramini M, Rocchi A, Benfenati F, Cesca F. Neuronal cultures and nanomaterials. Adv Neurobiol 2019; 22: 51-79.
[http://dx.doi.org/10.1007/978-3-030-11135-9_3] [PMID: 31073932]
[4]
Perini G, Palmieri V, Ciasca G, De Spirito M, Papi M. Unravelling the potential of graphene quantum dots in biomedicine and neuroscience. Int J Mol Sci 2020; 21(10): 3712.
[http://dx.doi.org/10.3390/ijms21103712]
[5]
Papi M. Graphene-based materials: Biological and biomedical applications. Int J Mol Sci 2021; 22(2): 672.
[http://dx.doi.org/10.3390/ijms22020672] [PMID: 33445419]
[6]
Biomedical applications of plasma-deposited thin films. Plasma Polym Film 2004; (Aug): 325-77.
[7]
Lai JY, Ma DHK, Lai MH, Li YT, Chang RJ, Chen LM. Characterization of cross-linked porous gelatin carriers and their interaction with corneal endothelium: Biopolymer concentration effect. PLoS One 2013; 8(1): e54058.
[http://dx.doi.org/10.1371/journal.pone.0054058] [PMID: 23382866]
[8]
Lee OJ, Ju HW, Khang G, et al. An experimental burn wound-healing study of non-thermal atmospheric pressure microplasma jet arrays. J Tissue Eng Regen Med 2016; 10(4): 348-57.
[http://dx.doi.org/10.1002/term.2074] [PMID: 26227832]
[9]
Wang C, Li YS, Jiang J, Chiang WH. Controllable tailoring graphene nanoribbons with tunable surface functionalities: An effective strategy toward high-performance lithium-ion batteries. ACS Appl Mater Interfaces 2015; 7(31): 17441-9.
[http://dx.doi.org/10.1021/acsami.5b04864] [PMID: 26196904]
[10]
Whang K, Healy KE, Elenz DR, et al. Engineering bone regeneration with bioabsorbable scaffolds with novel microarchitecture. Tissue Eng 1999; 5(1): 35-51.
[http://dx.doi.org/10.1089/ten.1999.5.35] [PMID: 10207188]
[11]
Novoselov KS, Geim AK, Morozov SV, Jiang D, Zhang Y, Dubonos SV. Electric field effect in atomically thin carbon films. Science 2004; 306(5696): 666-9.
[http://dx.doi.org/10.1126/science.1102896]
[12]
Pelin M, Fusco L, Martín C, et al. Graphene and graphene oxide induce ROS production in human HaCaT skin keratinocytes: The role of xanthine oxidase and NADH dehydrogenase. Nanoscale 2018; 10(25): 11820-30.
[http://dx.doi.org/10.1039/C8NR02933D] [PMID: 29920573]
[13]
Duch MC, Budinger GRS, Liang YT, et al. Minimizing oxidation and stable nanoscale dispersion improves the biocompatibility of graphene in the lung. Nano Lett 2011; 11(12): 5201-7.
[http://dx.doi.org/10.1021/nl202515a] [PMID: 22023654]
[14]
Wang X, Duch MC, Mansukhani N, et al. Use of a pro-fibrogenic mechanism-based predictive toxicological approach for tiered testing and decision analysis of carbonaceous nanomaterials. ACS Nano 2015; 9(3): 3032-43.
[http://dx.doi.org/10.1021/nn507243w] [PMID: 25646681]
[15]
Chen Y, Hu X, Sun J, Zhou Q. Specific nanotoxicity of graphene oxide during zebrafish embryogenesis. Nanotoxicology 2015; 10(1): 42-52.
[http://dx.doi.org/10.3109/17435390.2015.1005032]
[16]
Sasidharan A, Panchakarla LS, Sadanandan AR, et al. Hemocompatibility and macrophage response of pristine and functionalized graphene. Small 2012; 8(8): 1251-63.
[http://dx.doi.org/10.1002/smll.201102393] [PMID: 22334378]
[17]
Ou L, Song B, Liang H, Liu J, Feng X, Deng B. Toxicity of graphene-family nanoparticles: A general review of the origins and mechanisms. Particle and Fibre Toxicology 2016; 13(1)
[http://dx.doi.org/10.1186/s12989-016-0168-y]
[18]
Kim M, Eom HJ, Choi I, Hong J, Choi J. Graphene oxide-induced neurotoxicity on neurotransmitters, AFD neurons and locomotive behavior in Caenorhabditis elegans. Neurotoxicology 2020; 77: 30-9.
[http://dx.doi.org/10.1016/j.neuro.2019.12.011] [PMID: 31862286]
[19]
Cao Z, Su M, Wang H, et al. Carboxyl graphene oxide nanoparticles induce neurodevelopmental defects and locomotor disorders in zebrafish larvae. Chemosphere 2021; 270: 128611.
[http://dx.doi.org/10.1016/j.chemosphere.2020.128611] [PMID: 33092822]
[20]
Chen H, Li H, Wang D. Graphene oxide dysregulates neuroligin/NLG-1-mediated molecular signaling in interneurons in Caenorhabditis elegans. Sci Rep 2017; 7(1): 41655.
[http://dx.doi.org/10.1038/srep41655] [PMID: 28128356]
[21]
Soares JC, Pereira TCB, Costa KM, Maraschin T, Basso NR, Bogo MR. Developmental neurotoxic effects of graphene oxide exposure in zebrafish larvae (Danio rerio). Colloids Surf B Biointerfaces 2017; 157: 335-46.
[http://dx.doi.org/10.1016/j.colsurfb.2017.05.078] [PMID: 28618356]
[22]
Xu H, Wang X, Zhang X, et al. A deep learning analysis reveals nitrogen-doped graphene quantum dots damage neurons of nematode Caenorhabditis elegans. Nanomaterials 2021; 11(12): 3314.
[http://dx.doi.org/10.3390/nano11123314] [PMID: 34947663]
[23]
Ahmadian H, Hashemi E, Akhavan O, et al. Apoptotic and anti-apoptotic genes transcripts patterns of graphene in mice. Mater Sci Eng C 2017; 71: 460-4.
[http://dx.doi.org/10.1016/j.msec.2016.09.073] [PMID: 27987732]
[24]
Demir E, Marcos R. Toxic and genotoxic effects of graphene and multi-walled carbon nanotubes. J Toxicol Environ Health A 2018; 81(14): 645-60.
[http://dx.doi.org/10.1080/15287394.2018.1477314] [PMID: 29873610]
[25]
Ricci R, Leite NCS, da-Silva NS, et al. Graphene oxide nanoribbons as nanomaterial for bone regeneration: Effects on cytotoxicity, gene expression and bactericidal effect. Mater Sci Eng C 2017; 78: 341-8.
[http://dx.doi.org/10.1016/j.msec.2017.03.278] [PMID: 28575993]
[26]
Fujita K, Take S, Tani R, Maru J, Obara S, Endoh S. Assessment of cytotoxicity and mutagenicity of exfoliated graphene. Toxicol In Vitro 2018; 52(May): 195-202.
[http://dx.doi.org/10.1016/j.tiv.2018.06.016] [PMID: 29933104]
[27]
Yuan YG, Cai HQ, Wang JL, et al. Graphene oxide-silver nanoparticle nanocomposites induce oxidative stress and aberrant methylation in caprine fetal fibroblast cells. Cells 2021; 10(3): 682.
[http://dx.doi.org/10.3390/cells10030682] [PMID: 33808775]
[28]
Yang X, Yang Q, Zheng G, et al. Developmental neurotoxicity and immunotoxicity induced by graphene oxide in zebrafish embryos. Environ Toxicol 2019; 34(4): 415-23.
[PMID: 30549182]
[29]
Zhao S, Wang Y, Duo L. Biochemical toxicity, lysosomal membrane stability and DNA damage induced by graphene oxide in earthworms. Environ Pollut 2021; 269: 116225.
[http://dx.doi.org/10.1016/j.envpol.2020.116225] [PMID: 33316493]
[30]
Manjunatha B, Seo E, Park SH, Kundapur RR, Lee SJ. Pristine graphene and graphene oxide induce multi-organ defects in zebrafish (Danio rerio) larvae/juvenile: An in vivo study. Environ Sci Pollut Res Int 2021; 28(26): 34664-75.
[http://dx.doi.org/10.1007/s11356-021-13058-7] [PMID: 33656705]
[31]
Wu T, Liang X, Liu X, et al. Induction of ferroptosis in response to graphene quantum dots through mitochondrial oxidative stress in microglia. Part Fibre Toxicol 2020; 17(1): 30.
[http://dx.doi.org/10.1186/s12989-020-00363-1] [PMID: 32652997]
[32]
Hu X, Wei Z, Mu L. Graphene oxide nanosheets at trace concentrations elicit neurotoxicity in the offspring of zebrafish. Carbon 2017; 117: 182-91.
[http://dx.doi.org/10.1016/j.carbon.2017.02.092]
[33]
Audira G, Lee JS, Siregar P, et al. Comparison of the chronic toxicities of graphene and graphene oxide toward adult zebrafish by using biochemical and phenomic approaches. Environ Pollut 2021; 278: 116907.
[http://dx.doi.org/10.1016/j.envpol.2021.116907] [PMID: 33744786]
[34]
Wu Q, Yin L, Li X, Tang M, Zhang T, Wang D. Contributions of altered permeability of intestinal barrier and defecation behavior to toxicity formation from graphene oxide in nematode Caenorhabditis elegans. Nanoscale 2013; 5(20): 9934-43.
[http://dx.doi.org/10.1039/c3nr02084c] [PMID: 23986404]
[35]
Martínez-Álvarez I, Le Menach K, Devier MH, et al. Uptake and effects of graphene oxide nanomaterials alone and in combination with polycyclic aromatic hydrocarbons in zebrafish. Sci Total Environ 2021; 775: 145669.
[http://dx.doi.org/10.1016/j.scitotenv.2021.145669] [PMID: 33618313]
[36]
Li P, Xu T, Wu S, Lei L, He D. Chronic exposure to graphene-based nanomaterials induces behavioral deficits and neural damage in Caenorhabditis elegans. J Appl Toxicol 2017; 37(10): 1140-50.
[http://dx.doi.org/10.1002/jat.3468] [PMID: 28418071]
[37]
Xiao G, Chen H, Krasteva N, Liu Q, Wang D. Identification of interneurons required for the aversive response of Caenorhabditis elegans to graphene oxide. J Nanobiotechnology 2018; 16(1): 45.
[http://dx.doi.org/10.1186/s12951-018-0373-y] [PMID: 29703212]
[38]
Di Mauro G, Rauti R, Casani R, et al. Tuning the reduction of graphene oxide nanoflakes differently affects neuronal networks in the zebrafish. Nanomaterials (Basel) 2021; 11(9): 2161.
[http://dx.doi.org/10.3390/nano11092161] [PMID: 34578477]
[39]
Chen Y, Ren C, Ouyang S, Hu X, Zhou Q. Mitigation in multiple effects of graphene oxide toxicity in zebrafish embryogenesis driven by humic acid. Environ Sci Technol 2015; 49(16): 10147-54.
[http://dx.doi.org/10.1021/acs.est.5b02220] [PMID: 26171725]
[40]
Hu X, Mu L, Kang J, Lu K, Zhou R, Zhou Q. Humic acid acts as a natural antidote of graphene by regulating nanomaterial translocation and metabolic fluxes in vivo. Environ Sci Technol 2014; 48(12): 6919-27.
[http://dx.doi.org/10.1021/es5012548] [PMID: 24857237]
[41]
Zhang Y, Meng T, Shi L, et al. The effects of humic acid on the toxicity of graphene oxide to Scenedesmus obliquus and Daphnia magna. Sci Total Environ 2019; 649: 163-71.
[http://dx.doi.org/10.1016/j.scitotenv.2018.08.280] [PMID: 30173026]
[42]
Zhang S, Yang K, Feng L, Liu Z. In vitro and in vivo behaviors of dextran functionalized graphene. Carbon 2011; 49(12): 4040-9.
[http://dx.doi.org/10.1016/j.carbon.2011.05.056]
[43]
Guo Z, Zhang P, Chetwynd AJ, et al. Elucidating the mechanism of the surface functionalization dependent neurotoxicity of graphene family nanomaterials. Nanoscale 2020; 12(36): 18600-5.
[http://dx.doi.org/10.1039/D0NR04179C] [PMID: 32914812]
[44]
Guo Z, Chakraborty S, Monikh FA, et al. Surface functionalization of graphene-based materials: Biological behavior, toxicology, and safe-by-design aspects. Adv Biol 2021; 5(9): 2100637.
[http://dx.doi.org/10.1002/adbi.202100637] [PMID: 34288601]
[45]
Lovén K, Franzén SM, Isaxon C, Messing ME, Martinsson J, Gudmundsson A. Emissions and exposures of graphene nanomaterials, titanium dioxide nanofibers, and nanoparticles during down-stream industrial handling. J Expo Sci Environ Epidemiol 2020; 31(4): 736-52.
[46]
Lee JH, Han JH, Kim JH, et al. Exposure monitoring of graphene nanoplatelets manufacturing workplaces. Inhal Toxicol 2016; 28(6): 281-91.
[http://dx.doi.org/10.3109/08958378.2016.1163442] [PMID: 27055369]
[47]
Vaquero C, Wendelbo R, Egizabal A, Gutierrez-Cañas C, López de Ipiña J. Exposure to graphene in a pilot production plant. J Phys Conf Ser 2019; 1323(1): 012005. [Internet].
[http://dx.doi.org/10.1088/1742-6596/1323/1/012005]
[48]
Zhang C, Chen X, Ho SH. Wastewater treatment nexus: Carbon nanomaterials towards potential aquatic ecotoxicity. J Hazard Mater 2021; 417: 125959.
[http://dx.doi.org/10.1016/j.jhazmat.2021.125959] [PMID: 33990041]
[49]
Bu S, Yao N, Hunter MA, Searles DJ, Yuan Q. Design of two-dimensional carbon-nitride structures by tuning the nitrogen concentration. Npj Comput Mater 2020; 6(128)
[50]
Sharif F, Gagnon LR, Mulmi S, Roberts EPL. Electrochemical regeneration of a reduced graphene oxide/magnetite composite adsorbent loaded with methylene blue. Water Res 2017; 114: 237-45.
[http://dx.doi.org/10.1016/j.watres.2017.02.042] [PMID: 28249215]
[51]
Ouyang S, Li K, Zhou Q, Hu X. Widely distributed nanocolloids in water regulate the fate and risk of graphene oxide. Water Res 2019; 165: 114987.
[http://dx.doi.org/10.1016/j.watres.2019.114987] [PMID: 31450222]
[52]
Souza JP, Mansano AS, Venturini FP, Santos F, Zucolotto V. Antioxidant metabolism of zebrafish after sub-lethal exposure to graphene oxide and recovery. Fish Physiol Biochem 2019; 45(4): 1289-97.
[http://dx.doi.org/10.1007/s10695-019-00678-7] [PMID: 31278452]
[53]
Malina T, Maršálková E, Holá K, et al. Toxicity of graphene oxide against algae and cyanobacteria: Nanoblade-morphology-induced mechanical injury and self-protection mechanism. Carbon 2019; 155: 386-96.
[http://dx.doi.org/10.1016/j.carbon.2019.08.086]
[54]
Zhao Y, Liu Y, Zhang X, Liao W. Environmental transformation of graphene oxide in the aquatic environment. Chemosphere 2021; 262: 127885.
[http://dx.doi.org/10.1016/j.chemosphere.2020.127885] [PMID: 32805658]
[55]
Du T, Adeleye AS, Zhang T, et al. Influence of light wavelength on the photoactivity, physicochemical transformation, and fate of graphene oxide in aqueous media. Environ Sci Nano 2018; 5(11): 2590-603.
[http://dx.doi.org/10.1039/C8EN00593A]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy