Advertisement

Targeting and non-targeting effects of nanomaterials on DNA: challenges and perspectives

  • Ruixue Huang
  • Yao Zhou
  • Sai Hu
  • Ping-Kun ZhouEmail author
review paper
  • 39 Downloads

Abstract

Due to their large-scale manufacture and widespread application, there have been a number of studies related to toxicological assessment of nanomaterials (NMs) over the past decade. Although there has been extensive research on the cytotoxicity of NMs, concerns have been raised about their possible genotoxicity. The genome is constantly exposed to genotoxic insults that can lead to DNA damage, which in turn can have consequences for health, such as the induction of carcinogenesis. This comprehensive review focuses on the direct and indirect interactions of NMs with DNA. Factors influencing the genotoxicity of NMs, such as their physicochemical characteristics, are also discussed. The mechanisms involved in the direct and indirect interactions of NMs with DNA are also reviewed. Many studies have shown that ENMs have genotoxic effects, such as chromosomal fragmentation, DNA strand breaks, point mutations, oxidative DNA adducts, apoptosis, hypoxic responses, mitochondrial dysfunction, and epigenetic modifications. As the data reported to date are inconsistent, it is difficult to draw definitive conclusions regarding the features of NMs that promote genotoxicity. Therefore, challenges and future research perspectives are discussed. This review provides insights into the genotoxic effects of NMs and their consequences for human health.

Keywords

Nanomaterial DNA Genotoxicity 

Notes

Funding

This study is supported by grants from National Key Basic Research Program (973 Program) of MOST, China (Grant No. 2015CB910601), the National Natural Science Foundations of China (Grant Nos. U1803124, 81530085, 31870847).

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Consent for publication

This work is published under the standard license to publish agreement.

References

  1. Agita A, Alsagaff MT (2017) Inflammation, immunity, and hypertension. Acta Med Indones 49:158–165Google Scholar
  2. Ali D, Alarifi S, Alkahtani S, Almeer RS (2018) Silver-doped graphene oxide nanocomposite triggers cytotoxicity and apoptosis in human hepatic normal and carcinoma cells. Int J Nanomed 13:5685–5699Google Scholar
  3. Almansour M, Sajti L, Melhim W, Jarrar BM (2016) Ultrastructural hepatocytic alterations induced by silver nanoparticle toxicity. Ultrastruct Pathol 40:92–100Google Scholar
  4. Antonoglou O, Lafazanis K, Mourdikoudis S, Vourlias G, Lialiaris T et al (2019) Biological relevance of CuFeO2 nanoparticles: antibacterial and anti-inflammatory activity, genotoxicity, DNA and protein interactions. Mater Sci Eng C Mater Biol Appl 99:264–274Google Scholar
  5. Atha DH, Nagy A, Steinbruck A, Dennis AM, Hollingsworth JA et al (2017) Quantifying engineered nanomaterial toxicity: comparison of common cytotoxicity and gene expression measurements. J Nanobiotechnol 15:79Google Scholar
  6. Avalos A, Haza AI, Morales P (2015) Manufactured silver nanoparticles of different sizes induced DNA strand breaks and oxidative DNA damage in hepatoma and leukaemia cells and in dermal and pulmonary fibroblasts. Folia Biol (Praha) 61:33–42Google Scholar
  7. Aviello G, Knaus UG (2017) ROS in gastrointestinal inflammation: rescue or sabotage? Br J Pharmacol 174:1704–1718Google Scholar
  8. Barreto A, Luis LG, Pinto E, Almeida A, Paiga P et al (2019) Genotoxicity of gold nanoparticles in the gilthead seabream (Sparus aurata) after single exposure and combined with the pharmaceutical gemfibrozil. Chemosphere 220:11–19Google Scholar
  9. Bello-Bello JJ, Spinoso-Castillo JL, Arano-Avalos S, Martinez-Estrada E, Arellano-Garcia ME et al (2018) Cytotoxic, genotoxic, and polymorphism effects on Vanilla planifolia Jacks Ex Andrews after long-term exposure to argovit((R)) silver nanoparticles. Nanomaterials (Basel).  https://doi.org/10.3390/nano8100754 CrossRefGoogle Scholar
  10. Bhabra G, Sood A, Fisher B, Cartwright L, Saunders M et al (2009) Nanoparticles can cause DNA damage across a cellular barrier. Nat Nanotechnol 4:876–883Google Scholar
  11. Bhatia S, Drake DM, Miller L, Wells PG (2019) Oxidative stress and DNA damage in the mechanism of fetal alcohol spectrum disorders. Birth Defects Res 111:714–748Google Scholar
  12. Bhattacharya D, Santra CR, Ghosh AN, Karmakar P (2014) Differential toxicity of rod and spherical zinc oxide nanoparticles on human peripheral blood mononuclear cells. J Biomed Nanotechnol 10:707–716Google Scholar
  13. Blanco J, Lafuente D, Gomez M, Garcia T, Domingo JL, Sanchez DJ (2017) Polyvinyl pyrrolidone-coated silver nanoparticles in a human lung cancer cells: time- and dose-dependent influence over p53 and caspase-3 protein expression and epigenetic effects. Arch Toxicol 91:651–666Google Scholar
  14. Blanco J, Tomas-Hernandez S, Garcia T, Mulero M, Gomez M et al (2018) Oral exposure to silver nanoparticles increases oxidative stress markers in the liver of male rats and deregulates the insulin signalling pathway and p53 and cleaved caspase 3 protein expression. Food Chem Toxicol 115:398–404Google Scholar
  15. Brzoska K, Gradzka I, Kruszewski M (2018) Impact of silver, gold, and iron oxide nanoparticles on cellular response to tumor necrosis factor. Toxicol Appl Pharmacol 356:140–150Google Scholar
  16. Cameron SJ, Hosseinian F, Willmore WG (2018) A current overview of the biological and cellular effects of nanosilver. Int J Mol Sci.  https://doi.org/10.3390/ijms19072030 CrossRefGoogle Scholar
  17. Capasso L, Camatini M, Gualtieri M (2014) Nickel oxide nanoparticles induce inflammation and genotoxic effect in lung epithelial cells. Toxicol Lett 226:28–34Google Scholar
  18. Cardozo TR, De Carli RF, Seeber A, Flores WH, Da RJ et al (2019) Genotoxicity of zinc oxide nanoparticles: an in vivo and in silico study. Toxicol Res (Camb) 8:277–286Google Scholar
  19. Catalan J, Siivola KM, Nymark P, Lindberg H, Suhonen S et al (2016) In vitro and in vivo genotoxic effects of straight versus tangled multi-walled carbon nanotubes. Nanotoxicology 10:794–806Google Scholar
  20. Cavallo D, Fanizza C, Ursini CL, Casciardi S, Paba E et al (2012) Multi-walled carbon nanotubes induce cytotoxicity and genotoxicity in human lung epithelial cells. J Appl Toxicol 32:454–464Google Scholar
  21. Cavallo D, Ciervo A, Fresegna AM, Maiello R, Tassone P et al (2015) Investigation on cobalt-oxide nanoparticles cyto-genotoxicity and inflammatory response in two types of respiratory cells. J Appl Toxicol 35:1102–1113Google Scholar
  22. Chang RM, Kauffman RJ, Kwon Y (2014) Understanding the paradigm shift to computational social science in the presence of big data. Decis Support Syst 63:67–80Google Scholar
  23. Chen Y, Wang M, Zhang T, Du E, Liu Y et al (2018) Autophagic effects and mechanisms of silver nanoparticles in renal cells under low dose exposure. Ecotoxicol Environ Saf 166:71–77Google Scholar
  24. Chernova T, Murphy FA, Galavotti S, Sun XM, Powley IR et al (2017) Long-fiber carbon nanotubes replicate asbestos-induced mesothelioma with disruption of the tumor suppressor gene Cdkn2a (Ink4a/Arf). Curr Biol 27:3302–3314Google Scholar
  25. Cupi D, Baun A (2016) Methodological considerations for using umu assay to assess photo-genotoxicity of engineered nanoparticles. Mutat Res Genet Toxicol Environ Mutagen 796:34–39Google Scholar
  26. Dang Y, Zhang Y, Fan L, Chen H, Roco MC (2010) Trends in worldwide nanotechnology patent applications: 1991 to 2008. J Nanopart Res 12:687–706Google Scholar
  27. Di Bucchianico S, Cappellini F, Le Bihanic F, Zhang Y, Dreij K, Karlsson HL (2017) Genotoxicity of TiO2 nanoparticles assessed by mini-gel comet assay and micronucleus scoring with flow cytometry. Mutagenesis 32:127–137Google Scholar
  28. Di Bucchianico S, Gliga AR, Akerlund E, Skoglund S, Wallinder IO et al (2018) Calcium-dependent cyto- and genotoxicity of nickel metal and nickel oxide nanoparticles in human lung cells. Part Fibre Toxicol 15:32Google Scholar
  29. Durairajanayagam D, Agarwal A, Ong C (2015) Causes, effects and molecular mechanisms of testicular heat stress. Reprod Biomed Online 30:14–27Google Scholar
  30. Ekvall MT, Hedberg J, Odnevall WI, Hansson LA, Cedervall T (2018) Long-term effects of tungsten carbide (WC) nanoparticles in pelagic and benthic aquatic ecosystems. Nanotoxicology 12:79–89Google Scholar
  31. Ema M, Gamo M, Honda K (2017) A review of toxicity studies on graphene-based nanomaterials in laboratory animals. Regul Toxicol Pharmacol 85:7–24Google Scholar
  32. Eom HJ, Chatterjee N, Lee J, Choi J (2014) Integrated mRNA and micro RNA profiling reveals epigenetic mechanism of differential sensitivity of Jurkat T cells to AgNPs and Ag ions. Toxicol Lett 229:311–318Google Scholar
  33. Esmaeilnejad B, Samiei A, Mirzaei Y, Farhang-Pajuh F (2018) Assessment of oxidative/nitrosative stress biomarkers and DNA damage in Haemonchus contortus, following exposure to zinc oxide nanoparticles. Acta Parasitol 63:563–571Google Scholar
  34. Fadda LM, Ali HM, Mohamed AM, Hagar H (2019) Prophylactic administration of carnosine and melatonin abates the incidence of apoptosis, inflammation, and DNA damage induced by titanium dioxide nanoparticles in rat livers. Environ Sci Pollut Res Int 32:e22040Google Scholar
  35. Fadeel B, Farcal L, Hardy B, Vazquez-Campos S, Hristozov D et al (2018) Advanced tools for the safety assessment of nanomaterials. Nat Nanotechnol 13:537–543Google Scholar
  36. Fang H, Cui Y, Wang Z, Wang S (2018) Toxicological assessment of multi-walled carbon nanotubes combined with nonylphenol in male mice. PLoS ONE 13:e200238Google Scholar
  37. Feng L, Yang X, Asweto CO, Wu J, Zhang Y et al (2017) Low-dose combined exposure of nanoparticles and heavy metal compared with PM2.5 in human myocardial AC16 cells. Environ Sci Pollut Res Int 24:27767–27777Google Scholar
  38. Fernandez-Jimenez N, Garcia-Etxebarria K, Plaza-Izurieta L, Romero-Garmendia I, Jauregi-Miguel A et al (2019) The methylome of the celiac intestinal epithelium harbours genotype-independent alterations in the HLA region. Sci Rep 9:1298Google Scholar
  39. Folkmann JK, Risom L, Jacobsen NR, Wallin H, Loft S, Moller P (2009) Oxidatively damaged DNA in rats exposed by oral gavage to C60 fullerenes and single-walled carbon nanotubes. Environ Health Perspect 117:703–708Google Scholar
  40. Fukai E, Sato H, Watanabe M, Nakae D, Totsuka Y (2018) Establishment of an in vivo simulating co-culture assay platform for genotoxicity of multi-walled carbon nanotubes. Cancer Sci 109:1024–1031Google Scholar
  41. Gao M, Lv M, Liu Y, Song Z (2018) Transcriptome analysis of the effects of Cd and nanomaterial-loaded Cd on the liver in zebrafish. Ecotoxicol Environ Saf 164:530–539Google Scholar
  42. Garcia JM, Chen JA, Guillory B, Donehower LA, Smith RG, Lamb DJ (2015) Ghrelin prevents cisplatin-induced testicular damage by facilitating repair of DNA double strand breaks through activation of p53 in mice. Biol Reprod 93:24Google Scholar
  43. Geiser M, Rothen-Rutishauser B, Kapp N, Schurch S, Kreyling W et al (2005) Ultrafine particles cross cellular membranes by nonphagocytic mechanisms in lungs and in cultured cells. Environ Health Perspect 113:1555–1560Google Scholar
  44. Ghosh M, Oner D, Duca RC, Cokic SM, Seys S et al (2017) Cyto-genotoxic and DNA methylation changes induced by different crystal phases of TiO2-np in bronchial epithelial (16-HBE) cells. Mutat Res 796:1–12Google Scholar
  45. Glezeva N, Moran B, Collier P, Moravec CS, Phelan D et al (2019) Targeted DNA methylation profiling of human cardiac tissue reveals novel epigenetic traits and gene deregulation across different heart failure patient subtypes. Circ Heart Fail 12:e5765Google Scholar
  46. Golbamaki A, Golbamaki N, Sizochenko N, Rasulev B, Leszczynski J, Benfenati E (2018) Genotoxicity induced by metal oxide nanoparticles: a weight of evidence study and effect of particle surface and electronic properties. Nanotoxicology 12:1113–1129Google Scholar
  47. Gong N, Ma X, Ye X, Zhou Q, Chen X et al (2019) Carbon-dot-supported atomically dispersed gold as a mitochondrial oxidative stress amplifier for cancer treatment. Nat Nanotechnol 14:379–387Google Scholar
  48. Grigor’Eva A, Saranina I, Tikunova N, Safonov A, Timoshenko N et al (2013) Fine mechanisms of the interaction of silver nanoparticles with the cells of Salmonella typhimurium and Staphylococcus aureus. Biometals 26:479–488Google Scholar
  49. Gudkov SV, Guryev EL, Gapeyev AB, Sharapov MG, Bunkin NF et al (2019) Unmodified hydrated capital ES, Cyrillic60 fullerene molecules exhibit antioxidant properties, prevent damage to DNA and proteins induced by reactive oxygen species and protect mice against injuries caused by radiation-induced oxidative stress. Nanomedicine-UK 15:37–46Google Scholar
  50. Gupta SK, Baweja L, Gurbani D, Pandey AK, Dhawan A (2011) Interaction of C60 fullerene with the proteins involved in DNA mismatch repair pathway. J Biomed Nanotechnol 7:179–180Google Scholar
  51. Gurunathan S, Kang MH, Kim JH (2018) Combination effect of silver nanoparticles and histone deacetylases inhibitor in human alveolar basal epithelial cells. Molecules.  https://doi.org/10.3390/molecules23082046 CrossRefGoogle Scholar
  52. Habrowska-Gorczynska DE, Kowalska K, Urbanek KA, Dominska K, Sakowicz A, Piastowska-Ciesielska AW (2019) Deoxynivalenol modulates the viability, ROS production and apoptosis in prostate cancer cells. Toxins (Basel) 11:265Google Scholar
  53. Hadrup N, Sharma AK, Loeschner K (2018) Toxicity of silver ions, metallic silver, and silver nanoparticle materials after in vivo dermal and mucosal surface exposure: a review. Regul Toxicol Pharmacol 98:257–267Google Scholar
  54. Han X, Kou J, Zheng Y, Liu Z, Jiang Y et al (2019) ROS generated by upconversion nanoparticle-mediated photodynamic therapy induces autophagy via PI3K/AKT/mTOR signaling pathway in M1 peritoneal macrophage. Cell Physiol Biochem 52:1325–1338Google Scholar
  55. Hochella MJ, Mogk DW, Ranville J, Allen IC, Luther GW et al (2019) Natural, incidental, and engineered nanomaterials and their impacts on the Earth system. Science.  https://doi.org/10.1126/science.aau8299 CrossRefGoogle Scholar
  56. Honda K, Naya M, Takehara H, Kataura H, Fujita K, Ema M (2017) A 104-week pulmonary toxicity assessment of long and short single-wall carbon nanotubes after a single intratracheal instillation in rats. Inhal Toxicol 29:471–482Google Scholar
  57. Huk A, Izak-Nau E, El YN, Uggerud H, Vadset M et al (2015) Impact of nanosilver on various DNA lesions and HPRT gene mutations—effects of charge and surface coating. Part Fibre Toxicol 12:25Google Scholar
  58. Ickrath P, Wagner M, Scherzad A, Gehrke T, Burghartz M et al (2017) Time-dependent toxic and genotoxic effects of zinc oxide nanoparticles after long-term and repetitive exposure to human mesenchymal stem cells. Int J Environ Res Public Health.  https://doi.org/10.3390/ijerph14121590 CrossRefGoogle Scholar
  59. Jiang W, Li Q, Zhu Z, Wang Q, Dou J et al (2018) Cancer chemoradiotherapy duo: nano-enabled targeting of DNA lesion formation and DNA damage response. ACS Appl Mater Interfaces 10:35734–35744Google Scholar
  60. Ju L, Wu W, Yu M, Lou J, Wu H et al (2017) Different cellular response of human mesothelial cell MeT-5A to short-term and long-term multiwalled carbon nanotubes exposure. Biomed Res Int 2017:2747215Google Scholar
  61. Kidd J, Bi Y, Hanigan D, Herckes P, Westerhoff P (2019) Yttrium residues in MWCNT enable assessment of MWCNT removal during wastewater treatment. Nanomaterials (Basel) 9:670Google Scholar
  62. Kim YJ, Rahman MM, Lee SM, Kim JM, Park K et al (2019) Assessment of in vivo genotoxicity of citrated-coated silver nanoparticles via transcriptomic analysis of rabbit liver tissue. Int J Nanomed 14:393–405Google Scholar
  63. Ktistakis NT (2017) In praise of M. Anselmier who first used the term “autophagie” in 1859. Autophagy 13:2015–2017Google Scholar
  64. Kuhnel D, Krug HF, Kokalj AJ (2018) environmental impacts of engineered nanomaterials—imbalances in the safety assessment of selected nanomaterials. Materials (Basel) 11:1444Google Scholar
  65. Kwon JY, Koedrith P, Seo YR (2014) Current investigations into the genotoxicity of zinc oxide and silica nanoparticles in mammalian models in vitro and in vivo: carcinogenic/genotoxic potential, relevant mechanisms and biomarkers, artifacts, and limitations. Int J Nanomed 9(Suppl 2):271–286Google Scholar
  66. Laura H, Adrienne E, Herbers R (2019) An evaluation of engineered nanomaterial safety data sheets for safety and health information post implementation of the revised hazard communication standard. J Chem Health Saf 26:12–18Google Scholar
  67. Lewis RW, Bertsch PM, McNear DH (2019) Nanotoxicity of engineered nanomaterials (ENMs) to environmentally relevant beneficial soil bacteria—a critical review. Nanotoxicology 13:392–428Google Scholar
  68. Li PR, Wei JC, Chiu YF, Su HL, Peng FC, Lin JJ (2010) Evaluation on cytotoxicity and genotoxicity of the exfoliated silicate nanoclay. ACS Appl Mater Interfaces 2:1608–1613Google Scholar
  69. Liao W, Yu Z, Lin Z, Lei Z, Ning Z et al (2015) Biofunctionalization of selenium nanoparticle with dictyophoraindusiata polysaccharide and its antiproliferative activity through death-receptor and mitochondria-mediated apoptotic pathways. Sci Rep 5:18629Google Scholar
  70. Madannejad R, Shoaie N, Jahanpeyma F, Darvishi MH, Azimzadeh M, Javadi H (2019) Toxicity of carbon-based nanomaterials: reviewing recent reports in medical and biological systems. Chem Biol Interact 307:206–222Google Scholar
  71. Mahaye N, Thwala M, Cowan DA, Musee N (2017) Genotoxicity of metal based engineered nanoparticles in aquatic organisms: a review. Mutat Res 773:134–160Google Scholar
  72. Mani C, Reddy PH, Palle K (2019) DNA repair fidelity in stem cell maintenance, health, and disease. Biochim Biophys Acta Mol Basis Dis.  https://doi.org/10.1016/j.bbadis.2019.03.017 CrossRefGoogle Scholar
  73. May S, Hirsch C, Rippl A, Bohmer N, Kaiser JP et al (2018) Transient DNA damage following exposure to gold nanoparticles. Nanoscale 10:15723–15735Google Scholar
  74. McShan D, Yu H (2014) DNA damage in human skin keratinocytes caused by multiwalled carbon nanotubes with carboxylate functionalization. Toxicol Ind Health 30:489–498Google Scholar
  75. Minigalieva IA, Katsnelson BA, Privalova LI, Sutunkova MP, Gurvich VB et al (2018) Combined subchronic toxicity of aluminum (III), titanium (IV) and silicon (IV) oxide nanoparticles and its alleviation with a complex of bioprotectors. Int J Mol Sci.  https://doi.org/10.3390/ijms19030837 CrossRefGoogle Scholar
  76. Minten EV, Yu DS (2019) DNA repair: translation to the Clinic. Clin Oncol (R Coll Radiol) 31:303–310Google Scholar
  77. Modrzynska J, Berthing T, Ravn-Haren G, Jacobsen NR, Weydahl IK et al (2018) Primary genotoxicity in the liver following pulmonary exposure to carbon black nanoparticles in mice. Part Fibre Toxicol 15:2Google Scholar
  78. Mondal S, Giri A, Zhang Y, Kumar PS, Zhou W, Wen LP (2017) Caspase mediated beclin-1 dependent autophagy tuning activity and apoptosis promotion by surface modified hausmannite nanoparticle. J Biomed Mater Res A 105:1299–1310Google Scholar
  79. Moridi H, Hosseini SA, Shateri H, Kheiripour N, Kaki A et al (2018) Protective effect of cerium oxide nanoparticle on sperm quality and oxidative damage in malathion-induced testicular toxicity in rats: an experimental study. Int J Reprod Biomed (Yazd) 16:261–266Google Scholar
  80. Mullins EA, Rodriguez AA, Bradley NP, Eichman BF (2019) Emerging roles of DNA glycosylases and the base excision repair pathway. Trends Biochem Sci.  https://doi.org/10.1016/j.tibs.2019.04.006 CrossRefGoogle Scholar
  81. Musee N (2018) Comment on “risk assessments show engineered nanomaterials to be of low environmental concern”. Environ Sci Technol 52:6723–6724Google Scholar
  82. Nallanthighal S, Chan C, Murray TM, Mosier AP, Cady NC, Reliene R (2017) Differential effects of silver nanoparticles on DNA damage and DNA repair gene expression in Ogg1-deficient and wild type mice. Nanotoxicology 11:996–1011Google Scholar
  83. Ng CT, Yong LQ, Hande MP, Ong CN, Yu LE et al (2017) Zinc oxide nanoparticles exhibit cytotoxicity and genotoxicity through oxidative stress responses in human lung fibroblasts and Drosophila melanogaster. Int J Nanomed 12:1621–1637Google Scholar
  84. Nguyen KT, Shukla KP, Moctezuma M, Tang L (2007) Cellular and molecular responses of smooth muscle cells to surface nanotopography. J Nanosci Nanotechnol 7:2823–2832Google Scholar
  85. Nymark P, Catalan J, Suhonen S, Jarventaus H, Birkedal R et al (2013) Genotoxicity of polyvinylpyrrolidone-coated silver nanoparticles in BEAS 2B cells. Toxicology 313:38–48Google Scholar
  86. Oner D, Ghosh M, Bove H, Moisse M, Boeckx B et al (2018) Differences in MWCNT- and SWCNT-induced DNA methylation alterations in association with the nuclear deposition. Part Fibre Toxicol 15:11Google Scholar
  87. Pan Y, Leifert A, Ruau D, Neuss S, Bornemann J et al (2009) Gold nanoparticles of diameter 1.4 nm trigger necrosis by oxidative stress and mitochondrial damage. Small 5:2067–2076Google Scholar
  88. Pirela SV, Miousse IR, Lu X, Castranova V, Thomas T et al (2016) Effects of laser printer-emitted engineered nanoparticles on cytotoxicity, chemokine expression, reactive oxygen species, DNA methylation, and dna damage: a comprehensive in vitro analysis in human small airway epithelial cells, macrophages, and lymphoblasts. Environ Health Perspect 124:210–219Google Scholar
  89. Raghunathan VK, Devey M, Hawkins S, Hails L, Davis SA et al (2013) Influence of particle size and reactive oxygen species on cobalt chrome nanoparticle-mediated genotoxicity. Biomaterials 34:3559–3570Google Scholar
  90. Resnik DB (2019) How should engineered nanomaterials be regulated for public and environmental health? AMA J Ethics 21:E363–E369Google Scholar
  91. Robert D, Aubertin K, Bacri JC, Wilhelm C (2012) Magnetic nanomanipulations inside living cells compared with passive tracking of nanoprobes to get consensus for intracellular mechanics. Phys Rev E Stat Nonlinear Soft Matter Phys 85:11905Google Scholar
  92. Rogers SJ, Puric E, Eberle B, Datta NR, Bodis SB (2019) Radiotherapy for melanoma: more than DNA damage. Dermatol Res Pract 2019:9435389Google Scholar
  93. Roxbury D, Jagota A, Mittal J (2011) Sequence-specific self-stitching motif of short single-stranded DNA on a single-walled carbon nanotube. J Am Chem Soc 133:13545–13550Google Scholar
  94. Roy K, Kanwar RK, Kanwar JR (2015) LNA aptamer based multi-modal, Fe3O4-saturated lactoferrin (Fe3O4-bLf) nanocarriers for triple positive (EpCAM, CD133, CD44) colon tumor targeting and NIR, MRI and CT imaging. Biomaterials 71:84–99Google Scholar
  95. Saitoh T, Kokue E, Shimoda M (1999) The suppressive effects of lipopolysaccharide-induced acute phase response on hepatic cytochrome P450-dependent drug metabolism in rabbits. J Vet Pharmacol Ther 22:87–95Google Scholar
  96. Samanta A, Medintz IL (2016) Nanoparticles and DNA—a powerful and growing functional combination in bionanotechnology. Nanoscale 8:9037–9095Google Scholar
  97. Saquib Q, Faisal M, Alatar AA, Al-Khedhairy AA, Ahmed M et al (2016) Genotoxicity of ferric oxide nanoparticles in Raphanus sativus: deciphering the role of signaling factors, oxidative stress and cell death. J Environ Sci (China) 47:49–62Google Scholar
  98. Schlinkert P, Casals E, Boyles M, Tischler U, Hornig E et al (2015) The oxidative potential of differently charged silver and gold nanoparticles on three human lung epithelial cell types. J Nanobiotechnology 13:1Google Scholar
  99. Schulte PA, Leso V, Niang M, Iavicoli I (2019) Current state of knowledge on the health effects of engineered nanomaterials in workers: a systematic review of human studies and epidemiological investigations. Scand J Work Environ Health 45:217–238Google Scholar
  100. Singh A, Kukreti R, Saso L, Kukreti S (2019) Oxidative stress: a key modulator in neurodegenerative diseases. Molecules.  https://doi.org/10.3390/molecules24081583 CrossRefGoogle Scholar
  101. Sohal IS, O’Fallon KS, Gaines P, Demokritou P, Bello D (2018) Ingested engineered nanomaterials: state of science in nanotoxicity testing and future research needs. Part Fibre Toxicol 15:29Google Scholar
  102. Stoccoro A, Di Bucchianico S, Coppede F, Ponti J, Uboldi C et al (2017) Multiple endpoints to evaluate pristine and remediated titanium dioxide nanoparticles genotoxicity in lung epithelial A549 cells. Toxicol Lett 276:48–61Google Scholar
  103. Thongkumkoon P, Sangwijit K, Chaiwong C, Thongtem S, Singjai P, Yu LD (2014) Direct nanomaterial-DNA contact effects on DNA and mutation induction. Toxicol Lett 226:90–97Google Scholar
  104. Tian B, Li J, Pang R, Dai S, Li T et al (2018) Gold nanoparticles biosynthesized and functionalized using a hydroxylated tetraterpenoid trigger gene expression changes and apoptosis in cancer cells. ACS Appl Mater Interfaces 10:37353–37363Google Scholar
  105. Ursini CL, Cavallo D, Fresegna AM, Ciervo A, Maiello R et al (2014) Differences in cytotoxic, genotoxic, and inflammatory response of bronchial and alveolar human lung epithelial cells to pristine and COOH-functionalized multiwalled carbon nanotubes. Biomed Res Int 2014:359506Google Scholar
  106. Vellampatti S, Chandrasekaran G, Mitta SB, Lakshmanan VK, Park SH (2018) Metallo-curcumin-conjugated DNA complexes induces preferential prostate cancer cells cytotoxicity and pause growth of bacterial cells. Sci Rep 8:14929Google Scholar
  107. Visalli G, Curro M, Iannazzo D, Pistone A, Pruiti CM et al (2017) In vitro assessment of neurotoxicity and neuroinflammation of homemade MWCNTs. Environ Toxicol Pharmacol 56:121–128Google Scholar
  108. Wang X, Cheng W, Yang Q, Niu H, Liu Q et al (2018) Preliminary investigation on cytotoxicity of fluorinated polymer nanoparticles. J Environ Sci (China) 69:217–226Google Scholar
  109. Warheit DB, Donner M, Murli H (2001) p-Aramid RFP do not induce chromosomal aberrations in a standardized in vitro genotoxicity assay using human lymphocytes. Inhal Toxicol 13:1079–1091Google Scholar
  110. Xu B, Mao Z, Ji X, Yao M, Chen M et al (2015) miR-98 and its host gene Huwe1 target Caspase-3 in Silica nanoparticles-treated male germ cells. Sci Rep 5:12938Google Scholar
  111. Xue Y, Wang J, Huang Y, Gao X, Kong L et al (2018) Comparative cytotoxicity and apoptotic pathways induced by nanosilver in human liver HepG2 and L02 cells. Hum Exp Toxicol 37:1293–1309Google Scholar
  112. Yamindago A, Lee N, Woo S, Choi H, Mun JY et al (2018) Acute toxic effects of zinc oxide nanoparticles on Hydra magnipapillata. Aquat Toxicol 205:130–139Google Scholar
  113. Zhang R, Zhang X, Jia C, Pan J, Liu R (2019) Carbon black induced DNA damage and conformational changes to mouse hepatocytes and DNA molecule: a combined study using comet assay and multi-spectra methods. Ecotoxicol Environ Saf 170:732–738Google Scholar
  114. Zhou PK, Huang RX (2018) Targeting of the respiratory chain by toxicants: beyond the toxicities to mitochondrial morphology. Toxicol Res (Camb) 7:1008–1011Google Scholar
  115. Zhou F, Liao F, Chen L, Liu Y, Wang W, Feng S (2019) The size-dependent genotoxicity and oxidative stress of silica nanoparticles on endothelial cells. Environ Sci Pollut Res Int 26:1911–1920Google Scholar
  116. Zhu B, Xia X, Zhang S, Tang Y (2018) Attenuation of bacterial cytotoxicity of carbon nanotubes by riverine suspended solids in water. Environ Pollut 234:581–589Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Occupational and Environmental HealthCentral South UniversityChangshaChina
  2. 2.Department of Radiation Biology, Beijing Key Laboratory for Radiobiology, Beijing Institute of Radiation MedicineAMMSBeijingPeople’s Republic of China
  3. 3.Institute for Chemical Carcinogenesis, State Key Laboratory of RespiratoryGuangzhou Medical UniversityGuangzhouPeople’s Republic of China

Personalised recommendations