Abstract
Graphene possesses wider biomedical applications including drug delivery, photothermal ablation of tumors, biosensors, and also in the disease diagnosis. The accidental or intentional exposure of the environment including plants, ecosystem, and humans toward graphene is gradually increasing. Therefore, graphene toxicity becomes a critical issue to be addressed despite their diverse applications in multiple fields. In this situation, the scientific community as well as the general public must get awareness about the toxicity of graphene. This article, therefore, reviews the investigations on graphene toxicity. This review reveals the toxicity of graphene in vitro, in vivo models along with the environmental toxicity. The advantages of graphene toxicity in bacterial cells and cancer cells were also reviewed.
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References
Agarwal S, Zhou X, Ye F et al (2010) Interfacing live cells with nanocarbon substrates. Langmuir 26:2244–2247. https://doi.org/10.1021/la9048743
Akhavan O, Ghaderi E (2010) Toxicity of graphene and graphene oxide nanowalls against bacteria. ACS Nano 4:5731–5736. https://doi.org/10.1021/nn101390x
Anirudhan TS, Chithra Sekhar V, Athira VS (2020) Graphene oxide based functionalized chitosan polyelectrolyte nanocomposite for targeted and pH responsive drug delivery. Int J Biol Macromol 150:468–479. https://doi.org/10.1016/j.ijbiomac.2020.02.053
Antony J, Grimme S (2008) Structures and interaction energies of stacked graphene-nucleobase complexes. Phys Chem Chem Phys 10:2722–2729. https://doi.org/10.1039/b718788b
Balapanuru J, Yang JX, Xiao S et al (2010) A graphene oxide-organic dye ionic complex with DNA-sensing and optical-limiting properties. Angew Chemie Int Ed 49:6549–6553. https://doi.org/10.1002/anie.201001004
Baldrighi M, Trusel M, Tonini R, Giordani S (2016) Carbon nanomaterials interfacing with neurons: an in vivo perspective. Front Neurosci 10:250. https://doi.org/10.3389/fnins.2016.00250
Bartlem DG, Jones MGK, Hammes UZ et al (2015) Graphene oxide amplifies the phytotoxicity of arsenic in wheat. Sci Rep 4:1–10. https://doi.org/10.1016/j.etap.2014.11.014
Begum P, Fugetsu B (2013) Induction of cell death by graphene in Arabidopsis thaliana (Columbia ecotype) T87 cell suspensions. J Hazard Mater 260:1032–1041. https://doi.org/10.1016/j.jhazmat.2013.06.063
Begum P, Ikhtiari R, Fugetsu B (2011) Graphene phytotoxicity in the seedling stage of cabbage, tomato, red spinach, and lettuce. Carbon N Y 49:3907–3919. https://doi.org/10.1016/j.carbon.2011.05.029
Burton GJ, Jauniaux E (2011) Oxidative stress. Best Pract Res Clin Obstet Gynaecol 25:287–299. https://doi.org/10.1016/j.bpobgyn.2010.10.016
Bussy C, Ali-Boucetta H, Kostarelos K (2013) Safety considerations for graphene: lessons learnt from carbon nanotubes. Acc Chem Res 46:692–701. https://doi.org/10.1021/ar300199e
Campbell E, Hasan MT, Pho C et al (2019) Graphene oxide as a multifunctional platform for intracellular delivery, imaging, and cancer sensing. Sci Rep 9:1–9. https://doi.org/10.1038/s41598-018-36617-4
Chang Y, Yang ST, Liu JH et al (2011) In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol Lett 200:201–210. https://doi.org/10.1016/j.toxlet.2010.11.016
Chatterjee N, Eom HJ, Choi J (2014) A systems toxicology approach to the surface functionality control of graphene-cell interactions. Biomaterials 35:1109–1127. https://doi.org/10.1016/j.biomaterials.2013.09.108
Das S, Singh S, Singh V et al (2013) Oxygenated functional group density on graphene oxide: its effect on cell toxicity. Part Part Syst Charact 30:148–157. https://doi.org/10.1002/ppsc.201200066
Deb A, Andrews NG, Raghavan V (2018) Natural polymer functionalized graphene oxide for co-delivery of anticancer drugs: in-vitro and in-vivo. Int J Biol Macromol 113:515–525. https://doi.org/10.1016/j.ijbiomac.2018.02.153
Donaldson K, Stone V, Gilmour PS et al (2000) Ultrafine particles: mechanisms of lung injury. Philos Trans Math Phys Eng Sci 358:2741–2749
Dreyer DR, Park S, Bielawski CW, Ruoff RS (2010) The chemistry of graphene oxide. Chem Soc Rev 39:228–240
Du S, Zhang P, Zhang R et al (2016) Reduced graphene oxide induces cytotoxicity and inhibits photosynthetic performance of the green alga Scenedesmus obliquus. Chemosphere 164:499–507. https://doi.org/10.1016/j.chemosphere.2016.08.138
Duch MC, Budinger GRS, Liang YT et al (2011) Minimizing oxidation and stable nanoscale dispersion improves the biocompatibility of graphene in the lung. Nano Lett 11:5201–5207. https://doi.org/10.1021/nl202515a
Efremova LV, Vasilchenko AS, Rakov EG, Deryabin DG (2015) Toxicity of graphene shells, graphene oxide, and graphene oxide paper evaluated with escherichia coli biotests. Biomed Res Int 2015. https://doi.org/10.1155/2015/869361
Ema M, Gamo, M, Honda K (2017) A review of toxicity studies on graphene-based nanomaterials in laboratory animals. Regul Toxicol Pharmaco 85:7–24. https://doi.org/10.1016/j.yrtph.2017.01.011
Fadeel B, Bussy C, Merino S et al (2018) Safety assessment of graphene-based materials: focus on human health and the environment. ACS Nano 12:10582–10620
Farid MU, Jeong S, Seo DH et al (2018) Mechanistic insight into the in vitro toxicity of graphene oxide against biofilm forming bacteria using laser-induced breakdown spectroscopy. Nanoscale 10:4475–4487. https://doi.org/10.1039/c8nr00189h
Fischer HC, Chan WC (2007) Nanotoxicity: the growing need for in vivo study. Curr Opin Biotechnol 18:565–571
Francis AP, Murthy PB, Devasena T (2014) Bis-demethoxy curcumin analog nanoparticles: synthesis, characterization, and anticancer activity in vitro. J Nanosci Nanotechnol 14:4865–4873
Francis AP, Ganapathy S, Palla VR et al (2015) Future of nano bisdemethoxy curcumin analog: guaranteeing safer intravenous delivery. Environ Toxicol Pharmacol 39:467–474. https://doi.org/10.1016/j.etap.2014.12.018
Geim AK (2009) Graphene: status and prospects. Science 324:1530–1534
Guo X, Dong S, Petersen EJ et al (2013) Biological uptake and depuration of radio-labeled graphene by Daphnia magna. Environ Sci Technol 47:12524–12531. https://doi.org/10.1021/es403230u
Hillyer JF, Albrecht RM (2001) Gastrointestinal persorption and tissue distribution of differently sized colloidal gold nanoparticles. J Pharm Sci 90:1927–1936. https://doi.org/10.1002/jps.1143
Hodges GM, Carr EA, Hazzard RA et al (1995) A commentary on morphological and quantitative aspects of microparticle translocation across the gastrointestinal mucosa. J Drug Target 3:57–60. https://doi.org/10.3109/10611869509015934
Hu W, Peng C, Luo W et al (2010) Graphene-based antibacterial paper. ACS Nano 4:4317–4323. https://doi.org/10.1021/nn101097v
Jastrzębska AM, Olszyna AR (2015) The ecotoxicity of graphene family materials: current status, knowledge gaps and future needs. J Nanopart Res 17:1–21
Jaworski S, Sawosz E, Grodzik M et al (2013) In vitro evaluation of the effects of graphene platelets on glioblastoma multiforme cells. Int J Nanomedicine 8:413–420. https://doi.org/10.2147/IJN.S39456
Jaworski S, Hinzmann M, Sawosz E et al (2017) Interaction of different forms of graphene with chicken embryo red blood cells. Environ Sci Pollut Res 24:21671–21679. https://doi.org/10.1007/s11356-017-9788-5
Jaworski S, Wierzbicki M, Sawosz E et al (2018) Graphene oxide-based nanocomposites decorated with silver nanoparticles as an antibacterial agent. Nanoscale Res Lett 13:116. https://doi.org/10.1186/s11671-018-2533-2
Jaworski S, Strojny B, Sawosz E et al (2019) Degradation of mitochondria and oxidative stress as the main mechanism of toxicity of pristine graphene on U87 glioblastoma cells and tumors and HS-5 cells. Int J Mol Sci 20:650. https://doi.org/10.3390/ijms20030650
Jo BC, Yoon HJ, Ok M-R, Wu S (2017) Molecular dynamics simulation of cytotoxicity of graphene nanosheets to blood-coagulation protein. Biointerphases 12:01A403. https://doi.org/10.1116/1.4977076
Jung HS, Kong WH, Sung DK et al (2014) Nanographene oxide-hyaluronic acid conjugate for photothermal ablation therapy of skin cancer. ACS Nano 8:260–268. https://doi.org/10.1021/nn405383a
Jung SK, Qu X, Aleman-Meza B et al (2015) Multi-endpoint, high-throughput study of nanomaterial toxicity in Caenorhabditis elegans. Environ Sci Technol 49:2477–2485. https://doi.org/10.1021/es5056462
Kang Y, Liu J, Wu J et al (2017) Graphene oxide and reduced graphene oxide induced neural pheochromocytoma-derived PC12 cell lines apoptosis and cell cycle alterations via the ERK signaling pathways. Int J Nanomedicine 12:5511–5523. https://doi.org/10.2147/IJN.S141032
Khim Chng EL, Chua CK, Pumera M (2014) Graphene oxide nanoribbons exhibit significantly greater toxicity than graphene oxide nanoplatelets. Nanoscale 6:10792–10797. https://doi.org/10.1039/c4nr03608e
Kim SN, Kuang Z, Slocik JM et al (2011) Preferential binding of peptides to graphene edges and planes. J Am Chem Soc 133:14480–14483. https://doi.org/10.1021/ja2042832
Kim JK, Shin JH, Lee JS et al (2016) 28-Day inhalation toxicity of graphene nanoplatelets in Sprague-Dawley rats. Nanotoxicology 10:891–901. https://doi.org/10.3109/17435390.2015.1133865
Kim J, Leem J, Kim HN et al (2019) Uniaxially crumpled graphene as a platform for guided myotube formation. Microsyst Nanoeng 5:1–10. https://doi.org/10.1038/s41378-019-0098-6
Koenig SP, Boddeti NG, Dunn ML, Bunch JS (2011) Ultrastrong adhesion of graphene membranes. Nat Nanotechnol 6:543–546. https://doi.org/10.1038/nnano.2011.123
Kotchey GP, Allen BL, Vedala H et al (2011) The enzymatic oxidation of graphene oxide. ACS Nano 5:2098–2108. https://doi.org/10.1021/nn103265h
Krasteva N, Keremidarska-Markova M, Hristova-Panusheva K et al (2019) Aminated graphene oxide as a potential new therapy for colorectal cancer. Oxidative Med Cell Longev 2019. https://doi.org/10.1155/2019/3738980
Krewski D, Acosta D, Andersen M et al (2010) Toxicity testing in the 21st century: a vision and a strategy. J Toxicol Environ Heal Part B Crit Rev 13:51–138
Kurantowicz N, Sawosz E, Jaworski S et al (2015a) Interaction of graphene family materials with listeria monocytogenes and Salmonella enterica. Nanoscale Res Lett 10:1–12. https://doi.org/10.1186/s11671-015-0749-y
Kurantowicz N, Strojny B, Sawosz E et al (2015b) Biodistribution of a high dose of diamond, graphite, and graphene oxide nanoparticles after multiple intraperitoneal injections in rats. Nanoscale Res Lett 10:398. https://doi.org/10.1186/s11671-015-1107-9
Lammel T, Boisseaux P, Fernández-Cruz ML, Navas JM (2013) Internalization and cytotoxicity of graphene oxide and carboxyl graphene nanoplatelets in the human hepatocellular carcinoma cell line Hep G2. Part Fibre Toxicol 10:27. https://doi.org/10.1186/1743-8977-10-27
Lei H, Mi L, Zhou X et al (2011) Adsorption of double-stranded DNA to graphene oxide preventing enzymatic digestion. Nanoscale 3:3888–3892. https://doi.org/10.1039/c1nr10617a
Li N, Zhang X, Song Q et al (2011) The promotion of neurite sprouting and outgrowth of mouse hippocampal cells in culture by graphene substrates. Biomaterials 32:9374–9382. https://doi.org/10.1016/j.biomaterials.2011.08.065
Li Y, Yuan H, Von Dem Bussche A et al (2013) Graphene microsheets enter cells through spontaneous membrane penetration at edge asperities and corner sites. Proc Natl Acad Sci U S A 110:12295–12300. https://doi.org/10.1073/pnas.1222276110
Li R, Mansukhani ND, Guiney LM et al (2016) Identification and optimization of carbon radicals on hydrated graphene oxide for ubiquitous antibacterial coatings. ACS Nano 10:10966–10980. https://doi.org/10.1021/acsnano.6b05692
Li J, Zhou C, Luo C et al (2019) N-acetyl cysteine-loaded graphene oxide-collagen hybrid membrane for scarless wound healing. Theranostics 9:5839–5853. https://doi.org/10.7150/thno.34480
Liang S, Xu S, Zhang D et al (2015) Reproductive toxicity of nanoscale graphene oxide in male mice. Nanotoxicology 9:92–105. https://doi.org/10.3109/17435390.2014.893380
Liao KH, Lin YS, MacOsko CW, Haynes CL (2011) Cytotoxicity of graphene oxide and graphene in human erythrocytes and skin fibroblasts. ACS Appl Mater Interfaces 3:2607–2615. https://doi.org/10.1021/am200428v
Liu Z, Robinson JT, Sun X, Dai H (2008) PEGylated nanographene oxide for delivery of water-insoluble cancer drugs. J Am Chem Soc 130:10876–10877. https://doi.org/10.1021/ja803688x
Liu S, Zeng TH, Hofmann M et al (2011) Antibacterial activity of graphite, graphite oxide, graphene oxide, and reduced graphene oxide: membrane and oxidative stress. ACS Nano 5:6971–6980. https://doi.org/10.1021/nn202451x
Liu XT, Mu XY, Wu XL et al (2014) Toxicity of multi-walled carbon nanotubes, graphene oxide, and reduced graphene oxide to zebrafish embryos. Biomed Environ Sci 27:676–683. https://doi.org/10.3967/bes2014.103
Liu CC, Zhao JJ, Zhang R et al (2017) Multifunctionalization of graphene and graphene oxide for controlled release and targeted delivery of anticancer drugs. Am J Transl Res 9:5197–5219
Ma S, Lin D (2013) The biophysicochemical interactions at the interfaces between nanoparticles and aquatic organisms: adsorption and internalization. Environ Sci Process Impacts 15:145–160
Ma-Hock L, Strauss V, Treumann S et al (2013) Comparative inhalation toxicity of multi-wall carbon nanotubes, graphene, graphite nanoplatelets and low surface carbon black. Part Fibre Toxicol 10:23. https://doi.org/10.1186/1743-8977-10-23
Mendes RG, Koch B, Bachmatiuk A et al (2015) A size dependent evaluation of the cytotoxicity and uptake of nanographene oxide. J Mater Chem B 3:2522–2529. https://doi.org/10.1039/c5tb00180c
Meyer JC, Geim AK, Katsnelson MI et al (2007) The structure of suspended graphene sheets. Nature 446:60–63. https://doi.org/10.1038/nature05545
Mohammadi Gazestani A, Khoei S, Khoee S et al (2018) In vivo evaluation of the combination effect of near-infrared laser and 5-fluorouracil-loaded PLGA-coated magnetite nanographene oxide. Artif Cells Nanomed Biotechnol 46:25–33. https://doi.org/10.1080/21691401.2018.1450265
Mohanty N, Fahrenholtz M, Nagaraja A et al (2011) Impermeable graphenic encasement of bacteria. Nano Lett 11:1270–1275. https://doi.org/10.1021/nl104292k
Navarro E, Baun A, Behra R et al (2008) Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi. Ecotoxicology 17:372–386
Nirmal NK, Awasthi KK, John PJ (2017) Effects of nano-graphene oxide on testis, epididymis and fertility of Wistar rats. Basic Clin Pharmacol Toxicol 121:202–210. https://doi.org/10.1111/bcpt.12782
Novoselov KS, Geim AK, Morozov SV et al (2004) Electric field in atomically thin carbon films. Science 306:666–669. https://doi.org/10.1126/science.1102896
Novoselov KS, Fal’Ko VI, Colombo L et al (2012) A roadmap for graphene. Nature 490:192–200
Orecchioni M, Bedognetti D, Newman L et al (2017) Single-cell mass cytometry and transcriptome profiling reveal the impact of graphene on human immune cells. Nat Commun 8. https://doi.org/10.1038/s41467-017-01015-3
Ou L, Song B, Liang H et al (2016) Toxicity of graphene-family nanoparticles: a general review of the origins and mechanisms. Part Fibre Toxicol 13:1–24. https://doi.org/10.1186/s12989-016-0168-y
Parasuraman S (2011) Toxicological screening. J Pharmacol Pharmacother 2:74–79. https://doi.org/10.4103/0976-500X.81895
Park S, Mohanty N, Suk JW et al (2010) Biocompatible, robust free-standing paper composed of a TWEEN/graphene composite. Adv Mater 22:1736–1740. https://doi.org/10.1002/adma.200903611
Peralta-Videa JR, Zhao L, Lopez-Moreno ML et al (2011) Nanomaterials and the environment: a review for the biennium 2008-2010. J Hazard Mater 186:1–15
Puigpelat E, Ignés-Mullol J, Sagués F, Reigada R (2019) Interaction of graphene nanoparticles and lipid membranes displaying different liquid orderings: a molecular dynamics study. Langmuir 35:16661–16668. https://doi.org/10.1021/acs.langmuir.9b03008
Qiu Z, Hu J, Li Z et al (2020) Graphene oxide-based nanocomposite enabled highly efficient targeted synergistic therapy for colorectal cancer. Colloids Surf A Physicochem Eng Asp 593:124585. https://doi.org/10.1016/j.colsurfa.2020.124585
Qu G, Wang X, Wang Z et al (2013) Cytotoxicity of quantum dots and graphene oxide to erythroid cells and macrophages. Nanoscale Res Lett 8:1–9. https://doi.org/10.1186/1556-276X-8-198
Rajasekar A, Devasena T (2015) Facile synthesis of curcumin nanocrystals and validation of its antioxidant activity against circulatory toxicity in wistar rats. J Nanosci Nanotechnol 15:4119–4125. https://doi.org/10.1166/jnn.2015.9600
Ren H, Wang C, Zhang J et al (2010) DNA cleavage system of nanosized graphene oxide sheets and copper ions. ACS Nano 4:7169–7174. https://doi.org/10.1021/nn101696r
Rive C, Reina G, Wagle P et al (2019) Improved biocompatibility of amino-functionalized graphene oxide in Caenorhabditis elegans. Small 15:1902699. https://doi.org/10.1002/smll.201902699
Ruiz ON, Fernando KAS, Wang B et al (2011) Graphene oxide: a nonspecific enhancer of cellular growth. ACS Nano 5:8100–8107. https://doi.org/10.1021/nn202699t
Ryoo SR, Kim YK, Kim MH, Min DH (2010) Behaviors of NIH-3T3 fibroblasts on graphene/carbon nanotubes: proliferation, focal adhesion, and gene transfection studies. ACS Nano 4:6587–6598. https://doi.org/10.1021/nn1018279
Sawosz E, Jaworski S, Kutwin M et al (2014) Toxicity of pristine graphene in experiments in a chicken embryo model. Int J Nanomedicine 9:3913–3922. https://doi.org/10.2147/IJN.S65633
Schinwald A, Murphy FA, Jones A et al (2012) Graphene-based nanoplatelets: a new risk to the respiratory system as a consequence of their unusual aerodynamic properties. ACS Nano 6:736–746. https://doi.org/10.1021/nn204229f
Shamsipur M, Barati A, Nematifar Z (2019) Fluorescent pH nanosensors: design strategies and applications. J Photochem Photobiol C: Photochem Rev 39:76–141. https://doi.org/10.1016/j.jphotochemrev.2019.03.001
Sharifi S, Behzadi S, Laurent S et al (2012) Toxicity of nanomaterials. Chem Soc Rev 41:2323–2343
Shi T, Hou X, Guo S et al (2021) Nanohole-boosted electron transport between nanomaterials and bacteria as a concept for nano–bio interactions. Nat Commun 12:1–15. https://doi.org/10.1038/s41467-020-20547-9
Siddique YH, Khan W, Khanam S et al (2014) Toxic potential of synthesized graphene zinc oxide nanocomposite in the third instar larvae of transgenic Drosophila melanogaster (hsp70-lacZ)Bg 9. Biomed Res Int 2014:382124. https://doi.org/10.1155/2014/382124
Singh SK, Singh MK, Nayak MK et al (2011) Thrombus inducing property of atomically thin graphene oxide sheets. ACS Nano 5:4987–4996. https://doi.org/10.1021/nn201092p
Singh SK, Singh MK, Kulkarni PP et al (2012) Amine-modified graphene: Thrombo-protective safer alternative to graphene oxide for biomedical applications. ACS Nano 6:2731–2740. https://doi.org/10.1021/nn300172t
Souza JP, Venturini FP, Santos F, Zucolotto V (2018) Chronic toxicity in Ceriodaphnia dubia induced by graphene oxide. Chemosphere 190:218–224. https://doi.org/10.1016/j.chemosphere.2017.10.018
Strojny B, Kurantowicz N, Sawosz E et al (2015) Long term influence of carbon nanoparticles on health and liver status in rats. PLoS One 10. https://doi.org/10.1371/journal.pone.0144821
Suganya TR, Devasena T (2015) Green synthesis of silver nanorods and optimization of its therapeutic cum toxic dose. J Nanosci Nanotechnol 15:9565–9570. https://doi.org/10.1166/jnn.2015.10326
Sun X, Liu Z, Welsher K et al (2008) Nano-graphene oxide for cellular imaging and drug delivery. Nano Res 1:203–212. https://doi.org/10.1007/s12274-008-8021-8
Sun J, Zhang Q, Wang Z, Yan B (2013) Effects of nanotoxicity on female reproductivity and fetal development in animal models. Int J Mol Sci 14:9319–9337
Szczepaniak J, Strojny B, Chwalibog ES et al (2018) Effects of reduced graphene oxides on apoptosis and cell cycle of glioblastoma multiforme. Int J Mol Sci 19:3939. https://doi.org/10.3390/ijms19123939
Szmidt M, Stankiewicz A, Urbańska K et al (2019) Graphene oxide down-regulates genes of the oxidative phosphorylation complexes in a glioblastoma. BMC Mol Biol 20:2. https://doi.org/10.1186/s12867-018-0119-2
Tang Y, Tian J, Li S et al (2015) Combined effects of graphene oxide and Cd on the photosynthetic capacity and survival of Microcystis aeruginosa. Sci Total Environ 532:154–161. https://doi.org/10.1016/j.scitotenv.2015.05.081
Tu Y, Lv M, Xiu P et al (2013) Destructive extraction of phospholipids from Escherichia coli membranes by graphene nanosheets. Nat Nanotechnol 8:594–601. https://doi.org/10.1038/nnano.2013.125
Valentini F, Calcaterra A, Ruggiero V et al (2019) Functionalized graphene derivatives: antibacterial properties and cytotoxicity. J Nanomater 2019:2752539. https://doi.org/10.1155/2019/2752539
Varghese N, Mogera U, Govindaraj A et al (2009) Binding of DNA nucleobases and nucleosides with graphene. ChemPhysChem 10:206–210. https://doi.org/10.1002/cphc.200800459
Wan B, Wang ZX, Lv QY et al (2013) Single-walled carbon nanotubes and graphene oxides induce autophagosome accumulation and lysosome impairment in primarily cultured murine peritoneal macrophages. Toxicol Lett 221:118–127. https://doi.org/10.1016/j.toxlet.2013.06.208
Wang K, Ruan J, Song H et al (2011) Biocompatibility of graphene oxide. Nanoscale Res Lett 6:1–8. https://doi.org/10.1007/s11671-010-9751-6
Wang Q, Masud A, Aich N, Wu Y (2018) In vitro pulmonary toxicity of reduced graphene oxide-nano zero valent iron nanohybrids and comparison with parent nanomaterial attributes. ACS Sustain Chem Eng 6:12797–12806. https://doi.org/10.1021/acssuschemeng.8b02004
Wierzbicki M, Sawosz E, Strojny B et al (2018) NF-κB-related decrease of glioma angiogenic potential by graphite nanoparticles and graphene oxide nanoplatelets. Sci Rep 8:14733. https://doi.org/10.1038/s41598-018-33179-3
Wu M, Kempaiah R, Huang PJJ et al (2011) Adsorption and desorption of DNA on graphene oxide studied by fluorescently labeled oligonucleotides. Langmuir 27:2731–2738. https://doi.org/10.1021/la1037926
Xiaoli F, Qiyue C, Weihong G et al (2020) Toxicology data of graphene-family nanomaterials: an update. Arch Toxicol 94:1915–1939. https://doi.org/10.1007/s00204-020-02717-2
Xu S, Zhang Z, Chu M (2015) Long-term toxicity of reduced graphene oxide nanosheets: effects on female mouse reproductive ability and offspring development. Biomaterials 54:188–200. https://doi.org/10.1016/j.biomaterials.2015.03.015
Yang X, Zhang X, Liu Z et al (2008) High-efficiency loading and controlled release of doxorubicin hydrochloride on graphene oxide. J Phys Chem C 112:17554–17558. https://doi.org/10.1021/jp806751k
Yang K, Zhang S, Zhang G et al (2010) Graphene in mice: ultrahigh in vivo tumor uptake. Nano Lett 10:3318–3323. https://doi.org/10.1021/nl100996u
Yang K, Wan J, Zhang S et al (2012) The influence of surface chemistry and size of nanoscale graphene oxide on photothermal therapy of cancer using ultra-low laser power. Biomaterials 33:2206–2214. https://doi.org/10.1016/j.biomaterials.2011.11.064
Zhang L, Xia J, Zhao Q et al (2010a) Functional graphene oxide as a nanocarrier for controlled loading and targeted delivery of mixed anticancer drugs. Small 6:537–544. https://doi.org/10.1002/smll.200901680
Zhang Y, Ali SF, Dervishi E et al (2010b) Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytoma-derived pc12 cells. ACS Nano 4:3181–3186. https://doi.org/10.1021/nn1007176
Zhang X, Yin J, Peng C et al (2011) Distribution and biocompatibility studies of graphene oxide in mice after intravenous administration. Carbon N Y 49:986–995. https://doi.org/10.1016/j.carbon.2010.11.005
Zhang W, Wang C, Li Z et al (2012) Unraveling stress-induced toxicity properties of graphene oxide and the underlying mechanism. Adv Mater 24:5391–5397. https://doi.org/10.1002/adma.201202678
Zhang H, Peng C, Yang J et al (2013) Uniform ultrasmall graphene oxide nanosheets with low cytotoxicity and high cellular uptake. ACS Appl Mater Interfaces 5:1761–1767. https://doi.org/10.1021/am303005j
Zhang D, Zhang Z, Liu Y et al (2015) The short- and long-term effects of orally administered high-dose reduced graphene oxide nanosheets on mouse behaviors. Biomaterials 68:100–113. https://doi.org/10.1016/j.biomaterials.2015.07.060
Zhao X (2011) Self-assembly of DNA segments on graphene and carbon nanotube arrays in aqueous solution: a molecular simulation study. J Phys Chem C 115:6181–6189. https://doi.org/10.1021/jp110013r
Zhao J, Wang Z, White JC, Xing B (2014) Graphene in the aquatic environment: adsorption, dispersion, toxicity and transformation. Environ Sci Technol 48:9995–10009. https://doi.org/10.1021/es5022679
Zhao Y, Wu Q, Wang D (2016) An epigenetic signal encoded protection mechanism is activated by graphene oxide to inhibit its induced reproductive toxicity in Caenorhabditis elegans. Biomaterials 79:15–24. https://doi.org/10.1016/j.biomaterials.2015.11.052
Zhao J, Cao X, Wang Z et al (2017) Mechanistic understanding toward the toxicity of graphene-family materials to freshwater algae. Water Res 111:18–27. https://doi.org/10.1016/j.watres.2016.12.037
Zhi X, Fang H, Bao C et al (2013) The immunotoxicity of graphene oxides and the effect of PVP-coating. Biomaterials 34:5254–5261. https://doi.org/10.1016/j.biomaterials.2013.03.024
Zhou M, Zhai Y, Dong S (2009) Electrochemical sensing and biosensing platform based on chemically reduced graphene oxide. Anal Chem 81:5603–5613. https://doi.org/10.1021/ac900136z
Zielińska-Górska M, Hotowy A, Wierzbicki M et al (2020) Graphene oxide nanofilm and the addition of L-glutamine can promote development of embryonic muscle cells. J Nanobiotechnol 18:76. https://doi.org/10.1186/s12951-020-00636-z
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Devasena, T., Francis, A.P., Ramaprabhu, S. (2021). Toxicity of Graphene: An Update. In: de Voogt, P. (eds) Reviews of Environmental Contamination and Toxicology Volume 259. Reviews of Environmental Contamination and Toxicology, vol 259. Springer, Cham. https://doi.org/10.1007/398_2021_78
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DOI: https://doi.org/10.1007/398_2021_78
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