Advertisement

Assessing the Adverse Effects of Two-Dimensional Materials Using Cell Culture-Based Models

  • Lidiane Silva Franqui
  • Luis Augusto Visani de Luna
  • Thomas Loret
  • Diego Stefani Teodoro Martinez
  • Cyrill BussyEmail author
Chapter

Abstract

Two-dimensional materials (2D materials) are a relatively new class of engineered nanomaterials (ENM) defined by their property of being one or two atoms thick, with atoms arranged in a two-dimensional plane. Since 2010, these materials have slowly but consistently progressed from lab bench discoveries to real-life products and have now reached the global market. While this transfer from academia to industry has been relatively fast, there remain some concerns as to their safety profiles, which have not been studied as extensively as their properties and applications [1]. Cell culture-based assays are currently the most accessible and sustainable methods to evaluate the potential of ENMs to cause harm to humans. They have been developed as alternatives to the costly and time-consuming animal-based assays that have been used for decades for safety testing of new chemicals and to allow testing all existing ENMs. While some of these assays have proven to be highly reliable to predict 2D material deleterious impacts (after confirmation of similar outcomes in animal models), some assays were revealed to be not applicable for hazard testing of these flat materials due to interference of the materials with reagents, causing misleading results (Fig. 1.1).

References

  1. 1.
    Novoselov KS et al (2012) A roadmap for graphene. Nature 490:192–200CrossRefGoogle Scholar
  2. 2.
    Oberdorster G, Oberdorster E, Oberdorster J (2005) Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 113:823–839CrossRefGoogle Scholar
  3. 3.
    Nel A, Xia T, Mädler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311(80):622–627CrossRefGoogle Scholar
  4. 4.
    Nel AE et al (2009) Understanding biophysicochemical interactions at the nano–bio interface. Nat Mater 8:543–557CrossRefGoogle Scholar
  5. 5.
    Krug HF, Wick P (2011) Nanotoxicology: an interdisciplinary challenge. Angew Chem Int Ed 50:1260–1278CrossRefGoogle Scholar
  6. 6.
    Stone V et al (2017) Nanomaterials versus ambient ultrafine particles: an opportunity to exchange toxicology knowledge. Environ Health Perspect 125:106002CrossRefGoogle Scholar
  7. 7.
    Krug HF (2014) Nanosafety research-are we on the right track? Angew Chem Int Ed 53:12304–12319Google Scholar
  8. 8.
    Fornara A, Toprak MS, Bhattacharya K (2015) Keeping it real: the importance of material characterization in nanotoxicology. Biochem Biophys Res Commun 468:498–503CrossRefGoogle Scholar
  9. 9.
    Nel A et al (2013) Nanomaterial toxicity testing in the 21st century: use of a predictive toxicological approach and high-throughput screening. Acc Chem Res 46:607–621CrossRefGoogle Scholar
  10. 10.
    Hartung T (2009) Toxicology for the twenty-first century. Nature 460:208–212CrossRefGoogle Scholar
  11. 11.
    Hirsch C, Roesslein M, Krug HF, Wick P (2011) Nanomaterial cell interactions: are current in vitro tests reliable? Nanomedicine 6:837–847CrossRefGoogle Scholar
  12. 12.
    Fadeel B et al (2018) Advanced tools for the safety assessment of nanomaterials. Nat Nanotechnol 13:537–543CrossRefGoogle Scholar
  13. 13.
    Gajewicz A et al (2018) Decision tree models to classify nanomaterials according to the DF4nanoGrouping scheme. Nanotoxicology 12:1–17CrossRefGoogle Scholar
  14. 14.
    Geim AK, Novoselov KS (2007) The rise of graphene. Nat Mater 6:183–191CrossRefGoogle Scholar
  15. 15.
    Novoselov KS, Mishchenko A, Carvalho A, Castro Neto AH (2016) 2D materials and van der Waals heterostructures. Science 353(6298):aac9439Google Scholar
  16. 16.
    Mounet N et al (2018) Two-dimensional materials from high-throughput computational exfoliation of experimentally known compounds. Nat Nanotechnol 13:246–252CrossRefGoogle Scholar
  17. 17.
    Geim AK, Van der Grigorieva IV (2013) Waals heterostructures. Nature 499:419–425CrossRefGoogle Scholar
  18. 18.
    Wick P et al (2014) Classification framework for graphene-based materials. Angew Chem Int Ed 53:7714–7718CrossRefGoogle Scholar
  19. 19.
    Bianco A (2013) Graphene: safe or toxic? The two faces of the medal. Angew Chem Int Ed 52:4986–4997CrossRefGoogle Scholar
  20. 20.
    Fadeel B et al (2018) Safety assessment of graphene-based materials: focus on human health and the environment. ACS Nano 12:10582–10620CrossRefGoogle Scholar
  21. 21.
    Bussy C, Jasim D, Lozano N, Terry D, Kostarelos K (2015) The current graphene safety landscape-a literature mining exercise. Nanoscale 7:6432–6435CrossRefGoogle Scholar
  22. 22.
    Bussy C, Ali-Boucetta H, Kostarelos K (2013) Safety considerations for graphene: lessons learnt from carbon nanotubes. Acc Chem Res 46:692–701CrossRefGoogle Scholar
  23. 23.
    Guiney LM, Wang X, Xia T, Nel AE, Hersam MC (2018) Assessing and mitigating the hazard potential of two-dimensional materials. ACS Nano 12:6360–6377CrossRefGoogle Scholar
  24. 24.
    Bianco A et al (2013) All in the graphene family – a recommended nomenclature for two-dimensional carbon materials. Carbon N Y 65:1–6CrossRefGoogle Scholar
  25. 25.
    Kostarelos K, Novoselov KS (2014) Exploring the interface of graphene and biology. Science 344(80):261–263CrossRefGoogle Scholar
  26. 26.
    Park MVDZ et al (2017) Considerations for safe innovation: the case of graphene. ACS Nano 11:9574–9593CrossRefGoogle Scholar
  27. 27.
    Creighton MA, Rangel-Mendez JR, Huang J, Kane AB, Hurt RH (2013) Graphene-induced adsorptive and optical artifacts during in vitro toxicology assays. Small 9:1921–1927CrossRefGoogle Scholar
  28. 28.
    Monteiro-Riviere NA, Inman AO (2006) Challenges for assessing carbon nanomaterial toxicity to the skin. Carbon 44:1070–1078CrossRefGoogle Scholar
  29. 29.
    Val S, Hussain S, Boland S, Hamel R, Baeza-Squiban A, Marano F (2009) Carbon black and titanium dioxide nanoparticles induce pro-inflammatory responses in bronchial epithelial cells: need for multiparametric evaluation due to adsorption artifacts. Inhal Toxicol 21(Suppl 1):115–122.  https://doi.org/10.1080/08958370902942533
  30. 30.
    Hinderliter PM, Minard KR, Orr G, Chrisler WB, Thrall BD, Pounds JG, Teeguarden JG (2010) ISDD: a computational model of particle sedimentation, diffusion and target cell dosimetry for in vitro toxicity studies. Part Fibre Toxicol. 7(1):36.  https://doi.org/10.1186/1743-8977-7-36
  31. 31.
    Duffin R, Tran L, Brown D, Stone V, Donaldson K (2007) Proinflammogenic effects of low-toxicity and metal nanoparticles in vivo and in vitro: highlighting the role of particle surface area and surface reactivity. Inhal Toxicol 19(10):849–856.  https://doi.org/10.1080/08958370701479323
  32. 32.
    Lacroix G et al (2018) Air–liquid Interface in vitro models for respiratory toxicology research: consensus workshop and recommendations. Appl Vitr Toxicol.  https://doi.org/10.1089/aivt.2017.0034
  33. 33.
    Drasler B, Kucki M, Delhaes F, Buerki-Thurnherr T, Vanhecke D, Korejwo D, … Wick P (2018) Single exposure to aerosolized graphene oxide and graphene nanoplatelets did not initiate an acute biological response in a 3D human lung model. Carbon 37:125–135.  https://doi.org/10.1016/j.carbon.2018.05.012
  34. 34.
    Loret T, Peyret E, Dubreuil M, Aguerre-Chariol O, Bressot C, le Bihan O, Amodeo T, Trouiller B, Braun A, Egles C, Lacroix G (2016) Air-liquid interface exposure to aerosols of poorly soluble nanomaterials induces different biological activation levels compared to exposure to suspensions. Part Fibre Toxicol 13(1):58Google Scholar
  35. 35.
    Loret T, Rogerieux F, Trouiller B, Braun A, Egles C, Lacroix G (2018) Predicting the in vivo pulmonary toxicity induced by acute exposure to poorly soluble nanomaterials by using advanced in vitro methods. Part Fibre Toxicol 15(1):25.  https://doi.org/10.1186/s12989-018-0260-6
  36. 36.
    Liao K-H, Lin Y-S, 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/am200428vCrossRefGoogle Scholar
  37. 37.
    Chng EL, Chua CK, Pumera M (2014) Graphene oxide nanoribbons exhibit significantly greater toxicity than graphene oxide nanoplatelets. Nanoscale 6(18):10792–10797.  https://doi.org/10.1039/c4nr03608e
  38. 38.
    Li Y, Liu Y, Fu Y, Wei T, Le Guyader L, Gao G, Liu RS, Chang YZ, Chen C (2012) The triggering of apoptosis in macrophages by pristine graphene through the MAPK and TGF-beta signaling pathways. Biomaterials 33(2):402–411.  https://doi.org/10.1016/j.biomaterials.2011.09.091
  39. 39.
    Jiao G et al (2015) Limitations of MTT and CCK-8 assay for evaluation of graphene cytotoxicity. RSC Adv 5:53240–53244.  https://doi.org/10.1039/c5ra08958a
  40. 40.
    Mukherjee SP et al (2018) Graphene oxide is degraded by neutrophils and the degradation products are non-genotoxic. Nanoscale 10:1180–1188CrossRefGoogle Scholar
  41. 41.
    Monteiro-Riviere NA, Inman AO, Zhang LW (2009) Limitations and relative utility of screening assays to assess engineered nanoparticle toxicity in a human cell line. Toxicol Appl Pharmacol 234(2):222–235.  https://doi.org/10.1016/j.taap.2008.09.030
  42. 42.
    Vranic S et al (2018) Live imaging of label-free graphene oxide reveals critical factors causing oxidative-stress-mediated cellular responses. ACS Nano 12:1373–1389CrossRefGoogle Scholar
  43. 43.
    Guadagnini R, Halamoda Kenzaoui B, Walker L, Pojana G, Magdolenova Z, Bilanicova D, Saunders M, Juillerat-Jeanneret L, Marcomini A, Huk A, Dusinska M, Fjellsbø LM, Marano F, Boland S (2015) Toxicity screenings of nanomaterials: challenges due to interference with assay processes and components of classic in vitro tests. Nanotoxicology 9(Suppl 1):13–24.  https://doi.org/10.3109/17435390.2013.829590
  44. 44.
    Jasim DA, Lozano N, Kostarelos K (2016) Synthesis of few-layered, high-purity graphene oxide sheets from different graphite sources for biology. 2D Mater 3:14006CrossRefGoogle Scholar
  45. 45.
    McManus D et al (2017) Water-based and biocompatible 2D crystal inks for all-inkjet-printed heterostructures. Nat Nanotechnol 12:343–350CrossRefGoogle Scholar
  46. 46.
    Dekkers S et al (2018) Multi-omics approaches confirm metal ions mediate the main toxicological pathways of metal-bearing nanoparticles in lung epithelial A549 cells. Environ Sci Nano 5:1506–1517CrossRefGoogle Scholar
  47. 47.
    Gioria S et al (2016) A combined proteomics and metabolomics approach to assess the effects of gold nanoparticles in vitro. Nanotoxicology 10:736–748CrossRefGoogle Scholar
  48. 48.
    Hoyle C et al (2018) Small, thin graphene oxide is anti-inflammatory activating nuclear factor erythroid 2-related factor 2 via metabolic reprogramming. ACS Nano 12:11949–11962CrossRefGoogle Scholar
  49. 49.
    Bramini M et al (2016) Graphene oxide nanosheets disrupt lipid composition, ca 2+ homeostasis, and synaptic transmission in primary cortical neurons. ACS Nano 10:7154–7171CrossRefGoogle Scholar
  50. 50.
    Oostingh GJ, Casals E, Italiani P, Colognato R, Stritzinger R, Ponti J, Pfaller T, Kohl Y, Ooms D, Favilli F, Leppens H, Lucchesi D, Rossi F, Nelissen I, Thielecke H, Puntes VF, Duschl A, Boraschi D (2011) Problems and challenges in the development and validation of human cell-based assays to determine nanoparticle-induced immunomodulatory effects. Part Fibre Toxicol 8(1):8.  https://doi.org/10.1186/1743-8977-8-8
  51. 51.
    Gliga AR, Di Bucchianico S, Lindvall J, Fadeel B, Karlsson HL (2018) RNA-sequencing reveals long-term effects of silver nanoparticles on human lung cells. Sci Rep 8:6668CrossRefGoogle Scholar
  52. 52.
    Feliu N et al (2015) Next-generation sequencing reveals low-dose effects of cationic dendrimers in primary human bronchial epithelial cells. ACS Nano 9:146–163CrossRefGoogle Scholar
  53. 53.
    de Lazaro I, Kostarelos K (2019) Exposure to graphene oxide sheets alters the expression of reference genes used for real-time RT-qPCR normalization. Sci Rep 9(1):12520.  https://doi.org/10.1101/469304
  54. 54.
    Orecchioni M et al (2017) Single-cell mass cytometry and transcriptome profiling reveal the impact of graphene on human immune cells. Nat Commun 8:1109CrossRefGoogle Scholar
  55. 55.
    Li Y, Fujita M, Boraschi D (2017) Endotoxin contamination in nanomaterials leads to the misinterpretation of immunosafety results. Front Immunol 8:472CrossRefGoogle Scholar
  56. 56.
    Mukherjee SP, Bottini M, Fadeel B (2017) Graphene and the immune system: a romance of many dimensions. Front Immunol 8:673CrossRefGoogle Scholar
  57. 57.
    Mukherjee SP et al (2016) Detection of endotoxin contamination of graphene based materials using the TNF-α expression test and guidelines for endotoxin-free graphene oxide production. PLoS One 11:1–17Google Scholar
  58. 58.
    Help me understand genetics – genetics home reference – NIH. Available at: https://ghr.nlm.nih.gov/primer. Accessed 31 Dec 2018
  59. 59.
    Guidance document on revisions to OECD genetic toxicology test guidelines. https://www.oecd.org/env/ehs/testing/Draft%20Guidance%20Document%20on%20OECD%20Genetic%20Toxicology%20Test%20Guidelines.pdf. Accessed 13 Oct 2019
  60. 60.
    Joint Meeting of the Chemicals Committee and the Working Party on Chemicals, Pesticides and Biotechnology Overview of the set of OECD Genetic. (2017). http://www.oecd.org/env/ehs/36285973.pdf. Accessed 13 Oct 2019
  61. 61.
    Doak SH, Manshian B, Jenkins GJS, Singh N (2012) In vitro genotoxicity testing strategy for nanomaterials and the adaptation of current OECD guidelines. Mutat Res Toxicol Environ Mutagen 745:104–111CrossRefGoogle Scholar
  62. 62.
    Karlsson HL, Di Bucchianico S, Collins AR, Dusinska M (2015) Can the comet assay be used reliably to detect nanoparticle-induced genotoxicity? Environ Mol Mutagen 56:82–96CrossRefGoogle Scholar
  63. 63.
    Moller P et al (2015) Applications of the comet assay in particle toxicology: air pollution and engineered nanomaterials exposure. Mutagenesis 30:67–83CrossRefGoogle Scholar
  64. 64.
    PetkoviĆ J et al (2011) DNA damage and alterations in expression of DNA damage responsive genes induced by TiO 2 nanoparticles in human hepatoma HepG2 cells. Nanotoxicology 5:341–353CrossRefGoogle Scholar
  65. 65.
    Zerdoumi Y et al (2015) A new genotoxicity assay based on p53 target gene induction. Mutat Res Toxicol Environ Mutagen 789–790:28–35CrossRefGoogle Scholar
  66. 66.
    Tahara Y et al (2018) Potent and selective inhibitors of 8-oxoguanine DNA glycosylase. J Am Chem Soc 140:2105–2114CrossRefGoogle Scholar
  67. 67.
    Harismendy O, Howell S (2018) Ad-Seq, a genome-wide DNA-adduct profiling assay. bioRxiv 364794.  https://doi.org/10.1101/364794
  68. 68.
    Monien BH et al (2015) Simultaneous detection of multiple DNA adducts in human lung samples by isotope-dilution UPLC-MS/MS. Anal Chem 87:641–648CrossRefGoogle Scholar
  69. 69.
    Grob S, Cavalli G (2018) Technical Review: A Hitchhiker’s Guide to Chromosome Conformation Capture. In: Bemer M, Baroux C (eds) Plant Chromatin Dynamics. Methods in Molecular Biology, vol 1675. Humana Press, New York.  https://doi.org/10.1007/978-1-4939-7318-7_14
  70. 70.
    Sati S, Cavalli G (2017) Chromosome conformation capture technologies and their impact in understanding genome function. Chromosoma 126:33–44CrossRefGoogle Scholar
  71. 71.
    Sun Y et al (2018) Graphene oxide regulates cox2 in human embryonic kidney 293T cells via epigenetic mechanisms: dynamic chromosomal interactions. Nanotoxicology 12:117–137CrossRefGoogle Scholar
  72. 72.
    Pietroiusti A, Stockmann-Juvala H, Lucaroni F, Savolainen K (2018) Nanomaterial exposure, toxicity, and impact on human health. Wiley Interdiscip Rev Nanomed Nanobiotechnol 10:e1513CrossRefGoogle Scholar
  73. 73.
    Oh E et al (2016) Meta-analysis of cellular toxicity for cadmium-containing quantum dots. Nat Nanotechnol 11:479–486CrossRefGoogle Scholar
  74. 74.
    Zhao J, Riediker M (2014) Detecting the oxidative reactivity of nanoparticles: a new protocol for reducing artifacts. J Nanopart Res 16:2493CrossRefGoogle Scholar
  75. 75.
    Kalyanaraman B et al (2012) Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med 52:1–6CrossRefGoogle Scholar
  76. 76.
    Alnasser F, Castagnola V, Boselli L, Esquivel-Gaon M, Efeoglu E, McIntyre J, Byrne HJ, Dawson KA (2019) Graphene nanoflakes uptake mediated by scavenger receptors. Nano Lett. 19(2):1260–1268.  https://doi.org/10.1021/acs.nanolett.8b04820
  77. 77.
    Dorney J et al (2012) Identifying and localizing intracellular nanoparticles using Raman spectroscopy. Analyst 137:1111CrossRefGoogle Scholar
  78. 78.
    Ma J et al (2015) Crucial role of lateral size for graphene oxide in activating macrophages and stimulating pro-inflammatory responses in cells and animals. ACS Nano 9:10498–10515CrossRefGoogle Scholar
  79. 79.
    Kucki M et al (2017) Uptake of label-free graphene oxide by Caco-2 cells is dependent on the cell differentiation status. J Nanobiotechnol 15:46CrossRefGoogle Scholar
  80. 80.
    McEvoy L et al (1986) Membrane phospholipid asymmetry as a determinant of erythrocyte recognition by macrophages. Proc Natl Acad Sci U S A 83:3311–3315CrossRefGoogle Scholar
  81. 81.
    Jasim DA et al (2016) The effects of extensive glomerular filtration of thin graphene oxide sheets on kidney physiology. ACS Nano 10:10753–10767CrossRefGoogle Scholar
  82. 82.
    Jasim DA, Menard-Moyon C, Begin D, Bianco A, Kostarelos K (2015) Tissue distribution and urinary excretion of intravenously administered chemically functionalized graphene oxide sheets. Chem Sci 6:3952–3964CrossRefGoogle Scholar
  83. 83.
    Hu W et al (2011) Protein corona-mediated mitigation of cytotoxicity of graphene oxide. ACS Nano 5:3693–3700CrossRefGoogle Scholar
  84. 84.
    Papi M et al (2015) Plasma protein corona reduces the haemolytic activity of graphene oxide nano and micro flakes. RSC Adv 5:81638–81641CrossRefGoogle Scholar
  85. 85.
    Hajipour MJ et al (2015) Personalized disease-specific protein corona influences the therapeutic impact of graphene oxide. Nanoscale 7:8978–8994CrossRefGoogle Scholar
  86. 86.
    Mao H et al (2013) Hard corona composition and cellular toxicities of the graphene sheets. Colloids Surf B Biointerfaces 109:212–218CrossRefGoogle Scholar
  87. 87.
    Mbeh DA, Akhavan O, Javanbakht T, Mahmoudi M, Yahia L (2014) Cytotoxicity of protein corona-graphene oxide nanoribbons on human epithelial cells. Appl Surf Sci 320:596–601CrossRefGoogle Scholar
  88. 88.
    Castagnola V et al (2018) Biological recognition of graphene nanoflakes. Nat Commun 9:1577CrossRefGoogle Scholar
  89. 89.
    Mei K-C et al (2018) Protein-corona-by-design in 2D: a reliable platform to decode bio-nano interactions for the next-generation quality-by-design nanomedicines. Adv Mater 30:1802732CrossRefGoogle Scholar
  90. 90.
    Duan G, Kang SG, Tian X, Garate JA, Zhao L, Ge C, Zhou R (2015) Protein corona mitigates the cytotoxicity of graphene oxide by reducing its physical interaction with cell membrane. Nanoscale 7(37):15214–15224Google Scholar
  91. 91.
    Chong Y et al (2015) Reduced cytotoxicity of graphene nanosheets mediated by blood-protein coating. ACS Nano 9:5713–5724CrossRefGoogle Scholar
  92. 92.
    Rodrigues AF et al (2018) Immunological impact of graphene oxide sheets in the abdominal cavity is governed by surface reactivity. Arch Toxicol 92:3359–3379CrossRefGoogle Scholar
  93. 93.
    Mullick Chowdhury S, Lalwani G, Zhang K, Yang JY, Neville K, Sitharaman B (2013) Cell specific cytotoxicity and uptake of graphene nanoribbons. Biomaterials 34(1):283–293.  https://doi.org/10.1016/j.biomaterials.2012.09.057
  94. 94.
    Li R et al (2018) Surface oxidation of graphene oxide determines membrane damage, lipid peroxidation, and cytotoxicity in macrophages in a pulmonary toxicity model. ACS Nano 12:1390–1402CrossRefGoogle Scholar
  95. 95.
    Oberdorster G et al (2005) Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 113:823–839CrossRefGoogle Scholar
  96. 96.
    Mittal S et al (2016) Physico-chemical properties based differential toxicity of graphene oxide/reduced graphene oxide in human lung cells mediated through oxidative stress. Sci Rep 6:39548CrossRefGoogle Scholar
  97. 97.
    Wang X et al (2015) Use of a pro-fibrogenic mechanism-based predictive toxicological approach for tiered testing and decision analysis of carbonaceous nanomaterials. ACS Nano 9:3032–3043CrossRefGoogle Scholar
  98. 98.
    Sun C et al (2016) Graphene oxide nanosheets stimulate ruffling and shedding of mammalian cell plasma membranes. Chem 1:273–286CrossRefGoogle Scholar
  99. 99.
    Bussy C, Kostarelos K (2017) Culture media critically influence graphene oxide effects on plasma membranes. Chem 2:322–323. (Cell PressCrossRefGoogle Scholar
  100. 100.
    DeLoid GM, Cohen JM, Pyrgiotakis G, Pirela SV, Pal A, Liu J, Srebric J, Demokritou P (2015) Advanced computational modeling for in vitro nanomaterial dosimetry. Part Fibre Toxicol 12:32.  https://doi.org/10.1186/s12989-015-0109-1
  101. 101.
    Orecchioni M, Ménard-Moyon C, Delogu LG, Bianco A (2016) Graphene and the immune system: challenges and potentiality. Adv Drug Deliv Rev 105:163–175CrossRefGoogle Scholar
  102. 102.
    Orecchioni M et al (2016) Molecular and genomic impact of large and small lateral dimension graphene oxide sheets on human immune cells from healthy donors. Adv Healthc Mater 5:276–287CrossRefGoogle Scholar
  103. 103.
    Wibroe PP, Petersen SV, Bovet N, Laursen BW, Moghimi SM (2016) Soluble and immobilized graphene oxide activates complement system differently dependent on surface oxidation state. Biomaterials 78:20–26CrossRefGoogle Scholar
  104. 104.
    Zhi X et al (2013) The immunotoxicity of graphene oxides and the effect of PVP-coating. Biomaterials 34:5254–5261CrossRefGoogle Scholar
  105. 105.
    Zurutuza A, Marinelli C (2014) Challenges and opportunities in graphene commercialization. Nat Nanotechnol 9:730–734CrossRefGoogle Scholar
  106. 106.
    Magdolenova Z et al (2014) Mechanisms of genotoxicity. A review of in vitro and in vivo studies with engineered nanoparticles. Nanotoxicology 8:233–278CrossRefGoogle Scholar
  107. 107.
    Luch A (2005) Nature and nurture – lessons from chemical carcinogenesis. Nat Rev Cancer 5:113–125CrossRefGoogle Scholar
  108. 108.
    Öner D et al (2018) Differences in MWCNT- and SWCNT-induced DNA methylation alterations in association with the nuclear deposition. Part Fibre Toxicol 15:11CrossRefGoogle Scholar
  109. 109.
    Grady WM, Ulrich CM (2007) DNA alkylation and DNA methylation: cooperating mechanisms driving the formation of colorectal adenomas and adenocarcinomas? Gut 56:318–320CrossRefGoogle Scholar
  110. 110.
    Barros SP, Offenbacher S (2009) Epigenetics: connecting environment and genotype to phenotype and disease. J Dent Res 88:400–408CrossRefGoogle Scholar
  111. 111.
    Nelson BC et al (2017) Emerging metrology for high-throughput nanomaterial genotoxicology. Mutagenesis 32:215–232CrossRefGoogle Scholar
  112. 112.
    Chatterjee N, Yang J, Choi J (2016) Differential genotoxic and epigenotoxic effects of graphene family nanomaterials (GFNs) in human bronchial epithelial cells. Mutat Res Toxicol Environ Mutagen 798–799:1–10CrossRefGoogle Scholar
  113. 113.
    Carrow JK et al (2018) Widespread changes in transcriptome profile of human mesenchymal stem cells induced by two-dimensional nanosilicates. Proc Natl Acad Sci U S A 115:E3905–E3913CrossRefGoogle Scholar
  114. 114.
    Petibone DM et al (2017) p53 -competent cells and p53 -deficient cells display different susceptibility to oxygen functionalized graphene cytotoxicity and genotoxicity. J Appl Toxicol 37:1333–1345CrossRefGoogle Scholar
  115. 115.
    Chatterjee N, Eom H-J, Choi J (2014) A systems toxicology approach to the surface functionality control of graphene–cell interactions. Biomaterials 35:1109–1127CrossRefGoogle Scholar
  116. 116.
    Wang A et al (2013) Role of surface charge and oxidative stress in cytotoxicity and genotoxicity of graphene oxide towards human lung fibroblast cells. J Appl Toxicol 33:1156–1164CrossRefGoogle Scholar
  117. 117.
    Akhavan O, Ghaderi E, Akhavan A (2012) Size-dependent genotoxicity of graphene nanoplatelets in human stem cells. Biomaterials 33:8017–8025CrossRefGoogle Scholar
  118. 118.
    Bengtson S et al (2016) No cytotoxicity or genotoxicity of graphene and graphene oxide in murine lung epithelial FE1 cells in vitro. Environ Mol Mutagen 57:469–482CrossRefGoogle Scholar
  119. 119.
    Bengtson S et al (2017) Differences in inflammation and acute phase response but similar genotoxicity in mice following pulmonary exposure to graphene oxide and reduced graphene oxide. PLoS One 12:e0178355CrossRefGoogle Scholar
  120. 120.
    Monopoli MP, Åberg C, Salvati A, Dawson KA (2012) Biomolecular coronas provide the biological identity of nanosized materials. Nat Nanotechnol 7:779–786CrossRefGoogle Scholar
  121. 121.
    Walczyk D, Bombelli FB, Monopoli MP, Lynch I, Dawson KA (2010) What the cell ‘sees’ in bionanoscience. J Am Chem Soc 132:5761–5768CrossRefGoogle Scholar
  122. 122.
    Lundqvist M et al (2017) The nanoparticle protein corona formed in human blood or human blood fractions. PLoS One 12:e0175871CrossRefGoogle Scholar
  123. 123.
    Lesniak A et al (2010) Serum heat inactivation affects protein corona composition and nanoparticle uptake. Biomaterials 31:9511–9518CrossRefGoogle Scholar
  124. 124.
    Hadjidemetriou M, Al-Ahmady Z, Kostarelos K (2016) Time-evolution of in vivo protein corona onto blood-circulating PEGylated liposomal doxorubicin (DOXIL) nanoparticles. Nanoscale 8:6948–6957CrossRefGoogle Scholar
  125. 125.
    Casals E, Pfaller T, Duschl A, Oostingh GJ, Puntes V (2010) Time evolution of the nanoparticle protein corona. ACS Nano 4:3623–3632CrossRefGoogle Scholar
  126. 126.
    Tenzer S et al (2013) Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology. Nat Nanotechnol 8:772–781CrossRefGoogle Scholar
  127. 127.
    Mahmoudi M et al (2013) Temperature: the ‘ignored’ factor at the nanobio interface. ACS Nano 7:6555–6562CrossRefGoogle Scholar
  128. 128.
    Mahmoudi M, Shokrgozar MA, Behzadi S (2013) Slight temperature changes affect protein affinity and cellular uptake/toxicity of nanoparticles. Nanoscale 5:3240CrossRefGoogle Scholar
  129. 129.
    Zhao X, Lu D, Hao F, Liu R (2015) Exploring the diameter and surface dependent conformational changes in carbon nanotube-protein corona and the related cytotoxicity. J Hazard Mater 292:98–107CrossRefGoogle Scholar
  130. 130.
    Mahmoudi M et al (2011) Protein−nanoparticle interactions: opportunities and challenges. Chem Rev 111:5610–5637CrossRefGoogle Scholar
  131. 131.
    Monopoli MP et al (2011) Physical-chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. J Am Chem Soc 133:2525–2534CrossRefGoogle Scholar
  132. 132.
    Winzen S, Schoettler S, Baier G, Rosenauer C, Mailaender V, Landfester K, Mohr K (2015) Complementary analysis of the hard and soft protein corona: sample preparation critically effects corona composition. Nanoscale 7(7):2992–3001Google Scholar
  133. 133.
    Cedervall T et al (2007) Understanding the nanoparticle-protein corona using methods to quantify exchange rates and affinities of proteins for nanoparticles. Proc Natl Acad Sci 104:2050–2055CrossRefGoogle Scholar
  134. 134.
    Ke PC, Lin S, Parak WJ, Davis TP, Caruso F (2017) A decade of the protein corona. ACS Nano 11:11773–11776CrossRefGoogle Scholar
  135. 135.
    Hadjidemetriou M, Kostarelos K (2017) Nanomedicine: evolution of the nanoparticle corona. Nat Nanotechnol 12(4):288–290Google Scholar
  136. 136.
    Hu Q, Bai X, Hu G, Zuo YY (2017) Unveiling the molecular structure of pulmonary surfactant corona on nanoparticles. ACS Nano 11:6832–6842CrossRefGoogle Scholar
  137. 137.
    Kapralova AA, Fenga WH, Andrew A, Amoscatoa N et al (2013) Adsorption of surfactant lipids by single-walled carbon nanotubes in mouse lung upon pharyngeal aspiration: role in uptake by macrophages. ACS Nano 6:4147–4156CrossRefGoogle Scholar
  138. 138.
    Sopotnik M et al (2015) Comparative study of serum protein binding to three different carbon-based nanomaterials. Carbon N Y 95:560–572CrossRefGoogle Scholar
  139. 139.
    Mu Q et al (2012) Size-dependent cell uptake of protein-coated graphene oxide nanosheets. ACS Appl Mater Interfaces 4:2259–2266CrossRefGoogle Scholar
  140. 140.
    Xu M et al (2016) Improved in vitro and in vivo biocompatibility of graphene oxide through surface modification: poly(acrylic acid)-functionalization is superior to PEGylation. ACS Nano 10:3267–3281CrossRefGoogle Scholar
  141. 141.
    Ma N et al (2017) Folic acid-grafted bovine serum albumin decorated graphene oxide: an efficient drug carrier for targeted cancer therapy. J Colloid Interface Sci 490:598–607CrossRefGoogle Scholar
  142. 142.
    Wang Y, Zhang B, Zhai G (2016) The effect of incubation conditions on the hemolytic properties of unmodified graphene oxide with various concentrations. RSC Adv 6:68322–68334CrossRefGoogle Scholar
  143. 143.
    Cheng C et al (2012) General and biomimetic approach to biopolymer-functionalized graphene oxide nanosheet through adhesive dopamine. Biomacromolecules 13:4236–4246CrossRefGoogle Scholar
  144. 144.
    Sasidharan A et al (2012) Hemocompatibility and macrophage response of pristine and functionalized graphene. Small 8:1251–1263CrossRefGoogle Scholar
  145. 145.
    de Sousa M et al (2018) Covalent functionalization of graphene oxide with d -mannose: evaluating the hemolytic effect and protein corona formation. J Mater Chem B 6:2803–2812CrossRefGoogle Scholar
  146. 146.
    Belling JN et al (2016) Stealth immune properties of graphene oxide enabled by surface-bound complement factor H. ACS Nano 10:10161–10172CrossRefGoogle Scholar
  147. 147.
    Tan X et al (2013) Functionalization of graphene oxide generates a unique interface for selective serum protein interactions. ACS Appl Mater Interfaces 5:1370–1377CrossRefGoogle Scholar
  148. 148.
    Rodrigues AF et al (2018) A blueprint for the synthesis and characterisation of thin graphene oxide with controlled lateral dimensions for biomedicine. 2D Mater 5:35020CrossRefGoogle Scholar
  149. 149.
    Bhattacharya K et al (2016) Biological interactions of carbon-based nanomaterials: from coronation to degradation. Nanomed Nanotechnol Biol Med 12:333–351CrossRefGoogle Scholar
  150. 150.
    Lara S et al (2017) Identification of receptor binding to the biomolecular corona of nanoparticles. ACS Nano 11:1884–1893CrossRefGoogle Scholar
  151. 151.
    Digiacomo L et al (2017) An apolipoprotein-enriched biomolecular corona switches the cellular uptake mechanism and trafficking pathway of lipid nanoparticles. Nanoscale 9:17254–17262CrossRefGoogle Scholar
  152. 152.
    Saha K et al (2016) Regulation of macrophage recognition through the interplay of nanoparticle surface functionality and protein corona. ACS Nano 10:4421–4430CrossRefGoogle Scholar
  153. 153.
    Melby ES et al (2017) Cascading effects of nanoparticle coatings: surface functionalization dictates the assemblage of complexed proteins and subsequent interaction with model cell membranes. ACS Nano 11:5489–5499CrossRefGoogle Scholar
  154. 154.
    Corbo C et al (2016) The impact of nanoparticle protein corona on cytotoxicity, immunotoxicity and target drug delivery. Nanomedicine 11:81–100CrossRefGoogle Scholar
  155. 155.
    Kumar A et al (2016) Enrichment of immunoregulatory proteins in the biomolecular corona of nanoparticles within human respiratory tract lining fluid. Nanomed Nanotechnol Biol Med 12:1033–1043CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Lidiane Silva Franqui
    • 1
    • 2
    • 3
    • 4
  • Luis Augusto Visani de Luna
    • 1
    • 2
  • Thomas Loret
    • 1
    • 2
  • Diego Stefani Teodoro Martinez
    • 3
    • 4
  • Cyrill Bussy
    • 1
    • 2
    • 4
    • 5
    • 6
    Email author
  1. 1.Nanomedicine Lab, Nano-Inflammation Team, School of Health Sciences, Faculty of Biology, Medicine and HealthThe University of ManchesterManchesterUK
  2. 2.National Graphene InstituteThe University of ManchesterManchesterUK
  3. 3.Brazilian Nanotechnology National Laboratory (LNNano)Brazilian Center for Research in Energy and Materials (CNPEM)CampinasBrazil
  4. 4.School of TechnologyUniversity of Campinas (UNICAMP)LimeiraBrazil
  5. 5.Lydia Becker Institute of Immunology and Inflammation, Faculty of Biology, Medicine and HealthThe University of ManchesterManchesterUK
  6. 6.Thomas Ashton Institute for Risk and Regulatory ResearchThe University of ManchesterManchesterUK

Personalised recommendations