Evaluation of the impact of industrial single-walled and multi-walled carbon nanotubes on human respiratory tract epithelial cells
- Authors: Gabidinova G.F.1, Timerbulatova G.A.1,2, Daminova A.G.3, Galyaltdinov S.F.3, Dimiev A.M.3, Kryuchkova M.A.3, Fakhrullin R.F.3, Fatkhutdinova L.M.1
-
Affiliations:
- Kazan State Medical University
- Center of Hygiene and Epidemiology in the Republic of Tatarstan
- Kazan Federal University
- Issue: Vol 101, No 12 (2022)
- Pages: 1509-1520
- Section: OCCUPATIONAL HEALTH
- Published: 13.01.2023
- URL: https://rjpbr.com/0016-9900/article/view/638663
- DOI: https://doi.org/10.47470/0016-9900-2022-101-12-1509-1520
- ID: 638663
Cite item
Full Text
Abstract
Introduction. In the present study, a comparative assessment of the toxic effects of industrial single-walled and multi-walled carbon nanotubes (SWCNT and MWCNT) at doses corresponding to industrial exposures on BEAS-2B and A549 cells was carried out.
Materials and methods. The size distribution of SWCNT and MWCNT agglomerates in dispersions was estimated by dynamic light scattering and transmission electron microscopy. Cytotoxicity was assessed using a MTS test and LDH assay. The interaction of CNTs with cells was visualized using dark-field and transmission electron microscopy.
Results. Cytotoxic effects of pristine SWCNT and MWCNT in concentrations of 50–200 μg/ml and purified SWCNT in the range of 25–200 μg/ml were found in BEAS-2B cells. SWCNT and MWCNT were found to penetrate into the cytoplasm of both BEAS-2B and A549 cells, while MWCNT are more often revealed in the intracellular content as vacuolized clusters, and single SWCNT and agglomerates are visualized in the cytoplasm without a tendency to vacuolization.
Limitations. CNT were introduced into cells in the form of dispersions, where both single nanotubes and their agglomerates were found. The calculation of CNT concentrations for introduction into cells was based on computer simulation.
Conclusion. Further study of the mechanisms of cytotoxic and genotoxic effects of different types of carbon nanotubes (CNT) may contribute to the identification of MWCNT and SWCNT specific effects on the cells of the respiratory system to develop methodological approaches to the safe use of CNT.
Compliance with ethical standards. The study does not require submission of the opinion of the biomedical ethics committee or other documents.
Contribution:
Gabidinova G.F. — literature review on the topic of research, cell cultivation, tests (LDH) on cells, statistical data processing, preparation of pictures, generalization of the results;
Timerbulatova G.A. — literature review on the topic of research, cell cultivation, tests (MTS) on cells, preparation of pictures, generalization of the results;
Daminova A.G. — transmission electron microscopy, suspension morphometry, generalization of the obtained results;
Galyaltdinov Sh.F. — preparation of suspensions of materials for introduction into cells;
Dimiev A.M. — development of methods for preparing suspensions of materials for introduction into cells;
Kryuchkova M.A. — visualization of nanomaterials in cells (dark field microscopy);
Fakhrullin R.F. — visualization of nanomaterials in cells (dark field microscopy);
Fatkhutdinova L.M. — material analysis; editing; preparing an article for publication.
All authors are responsible for the integrity of all parts of the manuscript and approval of the manuscript final version.
Conflict of interest. The authors declare no conflict of interest.
Acknowledgment. The study was supported by the Russian Science Foundation grant № 22-25-00512, https://rscf.ru/project/22-25-00512/
Received: October 27, 2022 / Accepted: December 8, 2022 / Published: January 12, 2023
About the authors
Gulnaz F. Gabidinova
Kazan State Medical University
Author for correspondence.
Email: noemail@neicon.ru
ORCID iD: 0000-0003-2616-5017
Russian Federation
Gyuzel A. Timerbulatova
Kazan State Medical University; Center of Hygiene and Epidemiology in the Republic of Tatarstan
Email: noemail@neicon.ru
ORCID iD: 0000-0002-2479-2474
Russian Federation
Amina G. Daminova
Kazan Federal University
Email: noemail@neicon.ru
ORCID iD: 0000-0002-7672-4430
Russian Federation
Shamil F. Galyaltdinov
Kazan Federal University
Email: noemail@neicon.ru
ORCID iD: 0000-0002-9494-5288
Russian Federation
Ayrat M. Dimiev
Kazan Federal University
Email: noemail@neicon.ru
ORCID iD: 0000-0001-7497-1211
Russian Federation
Marina A. Kryuchkova
Kazan Federal University
Email: noemail@neicon.ru
ORCID iD: 0000-0002-6946-0553
Russian Federation
Rawil F. Fakhrullin
Kazan Federal University
Email: noemail@neicon.ru
ORCID iD: 0000-0003-2015-7649
Russian Federation
Liliya M. Fatkhutdinova
Kazan State Medical University
Email: liliya.fatkhutdinova@kazangmu.ru
ORCID iD: 0000-0001-9506-563X
MD, PhD, head of the Department of Hygiene and Occupational Medicine, Kazan, 420012, Russian Federation.
e-mail: liliya.fatkhutdinova@kazangmu.ru
Russian FederationReferences
- Venkataraman A., Amadi E.V., Chen Y., Papadopoulos C. Carbon nanotube assembly and integration for applications. Nanoscale Res. Lett. 2019; 14(1): 220. https://doi.org/10.1186/s11671-019-3046-3
- Chetyrkina M.R., Fedorov F.S., Nasibulin A.G. In vitro toxicity of carbon nanotubes: a systematic review. RSC Adv. 2022; 12(25): 16235–56. https://doi.org/10.1039/d2ra02519a
- Alshehri R., Ilyas A.M., Hasan A., Arnaout A., Ahmed F., Memic A. Carbon Nanotubes in Biomedical Applications: Factors, Mechanisms, and Remedies of Toxicity. J. Med. Chem. 2016; 59(18): 8149–67. https://doi.org/10.1021/acs.jmedchem.5b01770
- Pietroiusti A., Stockmann-Juvala H., Lucaroni F., Savolainen K. Nanomaterial exposure, toxicity, and impact on human health. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2018; 10(5): e1513. https://doi.org/10.1002/wnan.1513
- Luanpitpong S., Wang L., Rojanasakul Y. The effects of carbon nanotubes on lung and dermal cellular behaviors. Nanomedicine (Lond). 2014; 9(6): 895–912. https://doi.org/10.2217/nnm.14.42
- Siegrist K.J., Reynolds S.H., Porter D.W., Mercer R.R., Bauer A.K., Lowry D., et al. Mitsui-7, heat-treated, and nitrogen-doped multi-walled carbon nanotubes elicit genotoxicity in human lung epithelial cells. Part. Fibre Toxicol. 2019; 16(1): 36. https://doi.org/10.1186/s12989-019-0318-0
- Lindberg H.K., Falck G.C., Singh R., Suhonen S., Järventaus H., Vanhala E., et al. Genotoxicity of short single-wall and multi-wall carbon nanotubes in human bronchial epithelial and mesothelial cells in vitro. Toxicol. 2013; 313(1): 24–37. https://doi.org/10.1016/j.tox.2012.12.008
- Haniu H., Saito N., Matsuda Y., Tsukahara T., Usui Y., Maruyama K., et al. Biological responses according to the shape and size of carbon nanotubes in BEAS-2B and MESO-1 cells. Int. J. Nanomed. 2014; 9: 1979–90. https://doi.org/10.2147/IJN.S58661
- Jia G., Wang H., Yan L., Wang X., Pei R., Yan T., et al. Cytotoxicity of carbon nanomaterials: single-wall nanotube, multi-wall nanotube, and fullerene. Environ. Sci. Technol. 2005; 39(5): 1378–83. https://doi.org/10.1021/es048729l
- Khaliullin T.O., Kisin E.R., Myurrey R.E., Zalyalov R.R., Shvedova A.A., Fatkhutdinova L.M. Toxic effects of carbon nanotubes in macrophage and bronchial epithelium cell cultures. Vestnik Tomskogo gosudarstvennogo universiteta. Biologiya. 2014; (1): 199–210. (in Russian)
- Hu X., Cook S., Wang P., Hwang H.M., Liu X., Williams Q.L. In vitro evaluation of cytotoxicity of engineered carbon nanotubes in selected human cell lines. Sci. Total Environ. 2010; 408(8): 1812–7. https://doi.org/10.1016/j.scitotenv.2010.01.035
- Murr L.E., Garza K.M., Soto K.F., Carrasco A., Powell T.G., Ramirez D.A., et al. Cytotoxicity assessment of some carbon nanotubes and related carbon nanoparticle aggregates and the implications for anthropogenic carbon nanotube aggregates in the environment. Int. J. Environ. Res. Public Health. 2005; 2(1): 31–42. https://doi.org/10.3390/ijerph2005010031
- Palomäki J., Karisola P., Pylkkänen L., Savolainen K., Alenius H. Engineered nanomaterials cause cytotoxicity and activation on mouse antigen presenting cells. Toxicol. 2010; 267(1–3): 125–31. https://doi.org/10.1016/j.tox.2009.10.034
- Timerbulatova G.A., Fatkhutdinova L.M. Assessment of the toxicity of single-wall carbon nanotubes using different types of cell cultures: review of the current state of knowledge. Rossiyskie nanotekhnologii. 2018; 13(5–6): 240–5.
- Grosse Y., Loomis D., kio Guyton K.Z., Lauby-Secretan B., El Ghissassi F., Bouvard V., et al. International Agency for Research on Cancer Monograph Working Group. Carcinogenicity of fluoro-edenite, silicon carbide fibres and whiskers, and carbon nanotubes. Lancet Oncol. 2014; 15(13): 1427–8. https://doi.org/10.1016/S1470-2045(14)71109-X
- Ghosh M., Murugadoss S., Janssen L., Cokic S., Mathyssen C., Van Landuyt K., et al. Distinct autophagy-apoptosis related pathways activated by Multi-walled (NM 400) and Single-walled carbon nanotubes (NIST-SRM2483) in human bronchial epithelial (16HBE14o-) cells. J. Hazard. Mater. 2020; 387: 121691. https://doi.org/10.1016/j.jhazmat.2019.121691
- Caoduro C., Hervouet E., Girard-Thernier C., Gharbi T., Boulahdour H., Delage-Mourroux R., et al. Carbon nanotubes as gene carriers: Focus on internalization pathways related to functionalization and properties. Acta Biomater. 2017; 49: 36–44. https://doi.org/10.1016/j.actbio.2016.11.013
- Kang B., Chang S., Dai Y., Yu D., Chen D. Cell response to carbon nanotubes: size-dependent intracellular uptake mechanism and subcellular fate. Small. 2010; 6(21): 2362–6. https://doi.org/10.1002/smll.201001260
- Raffa V., Ciofani G., Nitodas S., Karachalios T., D’Alessandro D., Masini M., et al. Can the properties of carbon nanotubes influence their internalization by living cells? Carbon. 2008; 46: 1600–10. https://doi.org/10.1016/j.carbon.2008.06.053
- Han Y.G., Xu J., Li Z.G., Ren G.G., Yang Z. In vitro toxicity of multi-walled carbon nanotubes in C6 rat glioma cells. Neurotoxicol. 2012; 33(5): 1128–34. https://doi.org/10.1016/j.neuro.2012.06.004
- Ema M., Takehara H., Naya M., Kataura H., Fujita K., Honda K. Length effects of single-walled carbon nanotubes on pulmonary toxicity after intratracheal instillation in rats. J. Toxicol. Sci. 2017; 42(3): 367–78. https://doi.org/10.2131/jts.42.367
- Migliore L., Saracino D., Bonelli A., Colognato R., D’Errico M.R., Magrini A., et al. Carbon nanotubes induce oxidative DNA damage in RAW 264.7 cells. Environ. Mol. Mutagen. 2010; 51(4): 294–303. https://doi.org/10.1002/em.20545
- Ursini C.L., Cavallo D., Fresegna A.M., Ciervo A., Maiello R., Buresti G., et al. 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; 2014: 359506. https://doi.org/10.1155/2014/359506
- Eldawud R., Wagner A., Dong C., Stueckle T.A., Rojanasakul Y., Dinu C.Z. Carbon nanotubes physicochemical properties influence the overall cellular behavior and fate. NanoImpact. 2018; 9: 72–84. https://doi.org/10.1016/j.impact.2017.10.006
- Guseva Canu I., Bateson T.F., Bouvard V., Debia M., Dion C., Savolainen K., et al. Human exposure to carbon-based fibrous nanomaterials: A review. Int. J. Hyg. Environ. Health. 2016; 219(2): 166–75. https://doi.org/10.1016/j.ijheh.2015.12.005
- Donaldson K., Aitken R., Tran L., Stone V., Duffin R., Forrest G., et al. Carbon nanotubes: a review of their properties in relation to pulmonary toxicology and workplace safety. Toxicol. Sci. 2006; 92(1): 5–22. https://doi.org/10.1093/toxsci/kfj130
- Multiple-Path Particle Dosimetry Model (MPPD v 3.04). Available at: https://www.ara.com/products/multiple-path-particle-dosimetry-model-mppd-v-304
- Timerbulatova G.A., Dimiev A.M., Khamidullin T.L., Boychuk S.V., Dunaev P.D., Fakhrullin R.F., et al. Dispersion of single-walled carbon nanotubes in biocompatible media. Rossiyskie nanotekhnologii. 2020; 15(4): 461–9. https://doi.org/10.1134/S1992722320040160 (in Russian)
- Davoren M., Herzog E., Casey A., Cottineau B., Li Y., Boraschi D. Endotoxin contamination: a key element in the interpretation of nanosafety studies. Nanomed. Lond. 2016; 11(3): 269. https://doi.org/10.221/nnm.15.19619
- Cherednichenko Yu.V., Evtyugin V.G., Nigamatzyanova L.R., Akhatova F.S., Rozhina E.V., Fakhrullin R.F. Silver nanoparticle synthesis using ultrasound and halloysite to create a nanocomposite with antibacterial properties. Rossiyskie nanotekhnologii. 2019; 14 (9–10): 64–70. https://doi.org/10.21517/1992-7223-2019-9-10-64-70 (in Russian)
- Fakhrullin R., Nigamatzyanova L., Fakhrullina G. Dark-field/hyperspectral microscopy for detecting nanoscale particles in environmental nanotoxicology research. Sci. Total Environment. 2021; 772: 145478. https://doi.org/10.1016/j.scitotenv.2021.145478
- Mohd Nurazzi N., Asyraf M.R.M., Khalina A., Abdullah N., Sabaruddin F.A., Kamarudin S.H., et al. Fabrication, functionalization, and application of carbon nanotube-reinforced polymer composite: an overview. Polymers (Basel). 2021; 13(7): 1047. https://doi.org/10.3390/polym13071047
- Dong J., Ma Q. Suppression of basal and carbon nanotube-induced oxidative stress, inflammation and fibrosis in mouse lungs by Nrf2. Nanotoxicol. 2016; 10(6): 699–709. https://doi.org/10.3109/17435390.2015.1110758
- Gupta S.S., Singh K.P., Gupta S., Dusinska M., Rahman Q. Do carbon nanotubes and asbestos fibers exhibit common toxicity mechanisms? Nanomaterials (Basel). 2022; 12(10): 1708. https://doi.org/10.3390/nano12101708
- Ursini C.L., Maiello R., Ciervo A., Fresegna A.M., Buresti G., Superti F., et al. Evaluation of uptake, cytotoxicity and inflammatory effects in respiratory cells exposed to pristine and -OH and -COOH functionalized multi-wall carbon nanotubes. J. Appl. Toxicol. 2016; 36(3): 394–403. https://doi.org/10.1002/jat.3228
- Davoren M., Herzog E., Casey A., Cottineau B., Chambers G., Byrne H.J., et al. In vitro toxicity evaluation of single walled carbon nanotubes on human A549 lung cells. Toxicol. In Vitro. 2007; 21(3): 438–48. https://doi.org/10.1016/j.tiv.2006.10.007
Supplementary files
