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Environmental Science and Pollution Research

, Volume 25, Issue 23, pp 22356–22367 | Cite as

In vitro genotoxicity of asbestos substitutes induced by coupled stimulation of dissolved high-valence ions and oxide radicals

  • Tingting Huo
  • Faqin Dong
  • Jianjun Deng
  • Qingbi Zhang
  • Wei Ye
  • Wei Zhang
  • Pingping Wang
  • Dongping Sun
Interface Effect of Ultrafine Mineral Particles and Microorganisms
  • 120 Downloads

Abstract

The wide use of asbestos and its substitutes has given rise to studies on their possible harmful effects on human health and environment. However, their toxic effects remain unclear. The present study was aimed to disclose the coupled effects of dissolved high-valence ions and oxide radicals using the in vitro cytotoxicity and genotoxicity of chrysotile (CA), nano-SiO2 (NS), ceramic fiber (CF), glass fiber (GF), and rock wool (RW) on Chinese hamster lung cells V79. All samples induced cell mortality correlated well with the chemical SiO2 content of asbestos substitutes and the amount of dissolved Si. Alkali or alkaline earth metal elements relieved mortality of V79 cells; Al2O3 reinforced toxicity of materials. Asbestos substitutes generated lasting, increasing amount of acellular ·OH which formed at the fiber surface at sites with loose/unsaturated bonds, as well as by catalytic reaction through dissolved iron. Accumulated mechanical and radical stimulation induced the intracellular reactive oxygen species (ROS) elevation, morphology change, and deviating trans-membrane ion flux. The cellular ROS appeared as NS > GF > CF ≈ CA > RW, consistent with cell mortality rather than with acellular ·OH generation. Chromosomal and DNA lesions in V79 cells were not directly associated with the cellular ROS, while influenced by dissolved high-valence irons in the co-culture medium. In conclusion, ions from short-time dissolution of dust samples and the generation of extracellular ·OH presented combined effects in the elevation of intracellular ROS, which further synergistically induced cytotoxicity and genotoxicity.

Keywords

Chrysotile Asbestos substitutes Dissolved ions Hydroxyl radical Reactive oxygen species Cytotoxicity and genotoxicity 

Notes

Acknowledgements

This study was founded by projects of the National Natural Science Foundation of China (41130746, 41602033 and 41472046). The authors would like to thank the preclinical medicine laboratory of Southwest Medical University for its support in the experiment. Specially, the authors would like to express heartfelt gratitude to Dr. Maarten A.T.M. Broekmans for his kind, patient, and valuable suggestions for this manuscript’s improvement.

Author contributions

All authors contributed to this manuscript. Faqin Dong and Jianjun Deng conceived and designed the study. Tingting Huo, Wei Ye, and Pingping Wang performed the experiments. Wei Zhang performed the data analysis. Tingting Huo wrote this manuscript. Faqin Dong, Qingbi Zhang, and Dongping Sun guided the structure and contents of the paper and improved earlier drafts.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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Fig. S1 (DOCX 136 kb)
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Table S1 (DOCX 15 kb)

References

  1. Anonymous (1986) Environmental health criteria 53: asbestos and other natural mineral fibers, international programme on chemical safety. World Health Organization, GenevaGoogle Scholar
  2. Anonymous (2002) Man-made vitreous fibres, IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. World Health Organization International Agency for Research on Cancer Google Scholar
  3. Armand L, Tarantini A, Beal D, Biola-Clier M, Bobyk L, Sorieul S, Pernet-Gallay K, Marie-Desvergne C, Lynch I, Herlin-Boime N (2016) Long-term exposure of A549 cells to titanium dioxide nanoparticles induces DNA damage and sensitizes cells towards genotoxic agents. Nanotoxicology 10:913–923CrossRefGoogle Scholar
  4. Aust AE, Cook PM, Dodson RF (2011) Morphological and chemical mechanisms of elongated mineral particle toxicities. J Toxicol Environ Health, Pt. B Crit Rev 14:40–75CrossRefGoogle Scholar
  5. Baur X, Soskolne CL, Lemen RA, Schneider J, Woitowitz H-J, Budnik LT (2015) How conflicted authors undermine the World Health Organization (WHO) campaign to stop all use of asbestos: spotlight on studies showing that chrysotile is carcinogenic and facilitates other non-cancer asbestos-related diseases. Int J Occup Environ Health 21:176–179CrossRefGoogle Scholar
  6. Benjamin H, Lebanony D, Rosenwald S, Cohen L, Gibori H, Barabash N, Ashkenazi K, Goren E, Meiri E, Morgenstern S (2010) A diagnostic assay based on microRNA expression accurately identifies malignant pleural mesothelioma. J Mol Diagn 12:771–779CrossRefGoogle Scholar
  7. Berlo DV, Clift MJ, Albrecht C, Schins RP (2012) Carbon nanotubes: an insight into the mechanisms of their potential genotoxicity. Swiss Med Wkly 142:w13698Google Scholar
  8. Bernareggi A, Ren E, Borelli V, Vita F, Constanti A, Zabucchi G (2015): Xenopus laevis oocytes as a model system for studying the interaction between asbestos fibres and cell membranes. Toxicol. Sci., kfv050Google Scholar
  9. Bernstein D, Dunnigan J, Hesterberg T, Brown R, Velasco JAL, Barrera R, Hoskins J, Gibbs A (2013) Health risk of chrysotile revisited. Crit Rev Toxicol 43:154–183CrossRefGoogle Scholar
  10. Bernstein DM, Riego Sintes JM, Bjarne KE, Kunert J (2001) Biopersistence of synthetic mineral fibers as a predictor of chronic inhalation toxicity in rats. Inhal Toxicol 13:823–849CrossRefGoogle Scholar
  11. Bernstein DM, Rogers RA, Sepulveda R, Kunzendorf P, Bellmann B, Ernst H, Creutzenberg O, Phillips JI (2015) Evaluation of the fate and pathological response in the lung and pleura of brake dust alone and in combination with added chrysotile compared to crocidolite asbestos following short-term inhalation exposure. Toxicol Appl Pharmacol 283:20–34CrossRefGoogle Scholar
  12. Bhattacharjee P, Paul S (2016) Risk of occupational exposure to asbestos, silicon and arsenic on pulmonary disorders: understanding the genetic-epigenetic interplay and future prospects. Environ Res 147:425–434CrossRefGoogle Scholar
  13. Boulanger G, Andujar P, Pairon JC, Billon-Galland MA, Dion C, Dumortier P, Brochard P, Sobaszek A, Bartsch P, Paris C (2014) Quantification of short and long asbestos fibers to assess asbestos exposure: a review of fiber size toxicity. Environ Health 13:1CrossRefGoogle Scholar
  14. Cardile V, Renis M, Scifo C, Lombardo L, Gulino R, Mancari B, Panico A (2004) Behaviour of the new asbestos amphibole fluoro-edenite in different lung cell systems. Int J Biochem Cell Biol 36:849–860CrossRefGoogle Scholar
  15. Cavallo D, Campopiano A, Cardinali G, Casciardi S, De Simone P, Kovacs D, Perniconi B, Spagnoli G, Ursini CL, Fanizza C (2004) Cytotoxic and oxidative effects induced by man-made vitreous fibers (MMVFs) in a human mesothelial cell line. Toxicology 201:219–229CrossRefGoogle Scholar
  16. Cely-Garcia MF, Torres-Duque CA, Duran M, Parada P, Sarmiento OL, Breysse PN, Ramos-Bonilla JP (2015) Personal exposure to asbestos and respiratory health of heavy vehicle brake mechanics. J Expo Sci Environ Epidemiol 25:26–36CrossRefGoogle Scholar
  17. Darcey DJ, Feltner C (2014) Occupational and environmental exposure to asbestos, pathology of asbestos-associated diseases. Springer, Berlin, Heidelberg, pp 11–24Google Scholar
  18. Donaldson K, Murphy F, Schinwald A, Duffin R, Poland CA (2011) Identifying the pulmonary hazard of high aspect ratio nanoparticles to enable their safety-by-design. Nanomedicine 6:143–156CrossRefGoogle Scholar
  19. Fröhlich E (2012) The role of surface charge in cellular uptake and cytotoxicity of medical nanoparticles. Int J Nanomedicine 7:5577–5591CrossRefGoogle Scholar
  20. Fubini B, Mollo L, Giamello E (1995) Free radical generation at the solid/liquid interface in iron containing minerals. Free Radic Res 23:593–614CrossRefGoogle Scholar
  21. Funahashi S, Okazaki Y, Ito D, Asakawa A, Nagai H, Tajima M, Toyokuni S (2015) Asbestos and multi-walled carbon nanotubes generate distinct oxidative responses in inflammatory cells. J Clin Biochem Nutr 56:111–117CrossRefGoogle Scholar
  22. Gilmour PS, Brown DM, Beswick PH, MacNee W, Rahman I, Donaldson K (1997) Free radical activity of industrial fibers: role of iron in oxidative stress and activation of transcription factors. Environ Health Perspect 105:1313CrossRefGoogle Scholar
  23. Goodman JE, Peterson MK, Bailey LA, Kerper LE, Dodge DG (2014) Electricians’ chrysotile asbestos exposure from electrical products and risks of mesothelioma and lung cancer. Regul Toxicol Pharmacol 68:8–15CrossRefGoogle Scholar
  24. Guldberg M, Jensen SL, Knudsen T, Steenberg T, Kamstrup O (2002) High-alumina low-silica HT stone wool fibers: a chemical compositional range with high biosolubility. Regul Toxicol Pharmacol 35:217–226CrossRefGoogle Scholar
  25. Gulino GR, Polimeni M, Prato M, Gazzano E, Kopecka J, Colombatto S, Ghigo D, Aldieri E (2016) Effects of chrysotile exposure in human bronchial epithelial cells: insights into the pathogenic mechanisms of asbestos-related diseases. Environ Health Perspect 124:776Google Scholar
  26. Guo H, Zhang J, Boudreau M, Meng J, Yin J, Liu J, Xu H (2016) Intravenous administration of silver nanoparticles causes organ toxicity through intracellular ROS-related loss of inter-endothelial junction. Part Fibre Toxicol 13:1Google Scholar
  27. Hoppe A, Güldal NS, Boccaccini AR (2011) A review of the biological response to ionic dissolution products from bioactive glasses and glass-ceramics. Biomaterials 32:2757–2774CrossRefGoogle Scholar
  28. Jargin SV (2015) Asbestos and its substitutes: international coordination and independent research needed. J Environ Occup Sci 4:1CrossRefGoogle Scholar
  29. Jiang L, Nagai H, Ohara H, Hara S, Tachibana M, Hirano S, Shinohara Y, Kohyama N, Akatsuka S, Toyokuni S (2008) Characteristics and modifying factors of asbestos-induced oxidative DNA damage. Cancer Sci 99:2142–2151CrossRefGoogle Scholar
  30. Ken DMBCF (1998) Free radical activity of synthetic vitreous fibers: iron chelation inhibits hydroxyl radical generation by refractory ceramic fiber. J Toxicol Environ Health Part A 53:545–561CrossRefGoogle Scholar
  31. Kim SY, Kim YC, Kim Y, Hong WH (2016) Predicting the mortality from asbestos-related diseases based on the amount of asbestos used and the effects of slate buildings in Korea. Sci Total Environ 542:1–11CrossRefGoogle Scholar
  32. Konecny R, Leonard S, Shi X, Robinson V, Castranova V (2001) Reactivity of free radicals on hydroxylated quartz surface and its implications for pathogenicity: experimental and quantum mechanical study. J Environ Pathol Toxicol Oncol Off Organ Int Soc Environ Toxicol Cancer 20(suppl 1):521–532Google Scholar
  33. Kusiorowski R, Zaremba T, Piotrowski J, Podwórny J (2015) Utilisation of cement-asbestos wastes by thermal treatment and the potential possibility use of obtained product for the clinker bricks manufacture. J Mater Sci 50:6757–6767CrossRefGoogle Scholar
  34. Lemos AT, Lemos CTD, Flores AN, Pantoja EO, Rocha JAV, Vargas VMF (2016) Genotoxicity biomarkers for airborne particulate matter (PM2.5) in an area under petrochemical influence. Chemosphere 159:610–618CrossRefGoogle Scholar
  35. Miozzi E, Rapisarda V, Marconi A, Costa C, Polito I, Spandidos DA, Libra M, Fenga C (2016) Fluoro-edenite and carbon nanotubes: the health impact of ‘asbestos-like’ fibres. Exp Ther Med 11:21–27CrossRefGoogle Scholar
  36. Murayama T, Takahashi K, Natori Y, Kurumatani N (2006) Estimation of future mortality from pleural malignant mesothelioma in Japan based on an age-cohort model. Am J Ind Med 49:1–7CrossRefGoogle Scholar
  37. Nagai H, Toyokuni S (2012) Differences and similarities between carbon nanotubes and asbestos fibers during mesothelial carcinogenesis: shedding light on fiber entry mechanism. Cancer Sci 103:1378–1390CrossRefGoogle Scholar
  38. Pacella A, Fantauzzi M, Turci F, Cremisini C, Montereali MR, Nardi E, Atzei D, Rossi A, Andreozzi GB (2015) Surface alteration mechanism and topochemistry of iron in tremolite asbestos: a step toward understanding the potential hazard of amphibole asbestos. Chem Geol 405:28–38CrossRefGoogle Scholar
  39. Pavan C, Tomatis M, Ghiazza M, Rabolli V, Bolis V, Lison D, Fubini B (2013) In search of the chemical basis of the hemolytic potential of silicas. Chem Res Toxicol 26:1188–1198CrossRefGoogle Scholar
  40. Pietrofesa RA, Velalopoulou A, Albelda SM, Christofidou-Solomidou M (2016) Asbestos induces oxidative stress and activation of Nrf2 signaling in murine macrophages: chemopreventive role of the synthetic lignan secoisolariciresinol diglucoside (LGM2605). Int J Mol Sci 17:322CrossRefGoogle Scholar
  41. Rapisarda V, Loreto C, Ledda C, Musumeci G, Bracci M, Santarelli L, Renis M, Ferrante M, Cardile V (2015) Cytotoxicity, oxidative stress and genotoxicity induced by glass fibers on human alveolar epithelial cell line A549. Toxicol In Vitro 29:551–557CrossRefGoogle Scholar
  42. Sadual RR, Badamali SK, Dapurkar SE, Singh RK (2015) Unusual oxidation behaviour of mesoporous silicates towards lignin model phenolic monomer. World J Nano Sci Eng 05:88–95CrossRefGoogle Scholar
  43. Sahmel J, Barlow CA, Gaffney S, Avens HJ, Madl AK, Henshaw J, Unice K, Galbraith D, DeRose G, Lee RJ (2016) Airborne asbestos take-home exposures during handling of chrysotile-contaminated clothing following simulated full shift workplace exposures. J Expo Sci Env Epid 26:48–62CrossRefGoogle Scholar
  44. Scarselli A, Corfiati M, Di Marzio D (2016) Occupational exposure in the removal and disposal of asbestos-containing materials in Italy. Int Arch Occup Environ Health 89:857–865CrossRefGoogle Scholar
  45. Schinwald A, Murphy F, Prina-Mello A, Poland C, Byrne F, Glass J, Dickerson J, Schultz D, Movia D, Jeffree C (2012) The threshold length for fibre-induced acute pleural inflammation: shedding light on the early events in asbestos-induced mesothelioma. Toxicol Sci 128:461–470Google Scholar
  46. Sen S, Chakraborty R (2011) The role of antioxidants in human health. Oxidative stress: diagnostics, prevention, and therapy 1083, 1–37Google Scholar
  47. Shukla A, Gulumian M, Hei TK, Kamp D, Rahman Q, Mossman BT (2003) Multiple roles of oxidants in the pathogenesis of asbestos-induced diseases. Free Radic Biol Med 34:1117–1129CrossRefGoogle Scholar
  48. Toyokuni S (1996) Iron-induced carcinogenesis: the role of redox regulation. Free Radic Biol Med 20(4):553–556Google Scholar
  49. Toyokuni S (2014) Iron overload as a major targetable pathogenesis of asbestos-induced mesothelial carcinogenesis. Redox Rep 19:1–7Google Scholar
  50. Utembe W, Potgieter K, Stefaniak AB, Gulumian M (2015) Dissolution and biodurability: important parameters needed for risk assessment of nanomaterials. Part Fibre Toxicol 12:1CrossRefGoogle Scholar
  51. Wang M, Dong F, Wang B, He X, Liu L, Sun S, Huo T (2015) Free radical generation at the solid/liquid interface in iron containing minerals. J Central South Univ (Science and Technology) 46:1967–1972Google Scholar
  52. Yu J, Liu S, Wu B, Shen Z, Cherr GN, Zhang X, Li M (2016) Comparison of cytotoxicity and inhibition of membrane ABC transporters induced by MWCNTs with different length and functional groups. Environ Sci Technol 50:3985–3994CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Tingting Huo
    • 1
    • 2
  • Faqin Dong
    • 1
  • Jianjun Deng
    • 3
    • 4
  • Qingbi Zhang
    • 4
  • Wei Ye
    • 4
  • Wei Zhang
    • 1
  • Pingping Wang
    • 1
  • Dongping Sun
    • 2
  1. 1.Key Laboratory of Solid Waste Treatment and Resource Recycle, Ministry of EducationSouthwest University of Science and TechnologyMianyangChina
  2. 2.Institute of Chemical EngineeringNanjing University of Science and TechnologyNanjingChina
  3. 3.Clinical LaboratoryMianyang 404 HospitalMianyangChina
  4. 4.School of Public HealthSouthwest Medical UniversityLuzhouChina

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