Evaluation of the impact of industrial single-walled and multi-walled carbon nanotubes on human respiratory tract epithelial cells

Мұқаба

Дәйексөз келтіру

Толық мәтін

Аннотация

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

Авторлар туралы

Gulnaz Gabidinova

Kazan State Medical University

Хат алмасуға жауапты Автор.
Email: noemail@neicon.ru
ORCID iD: 0000-0003-2616-5017
Ресей

Gyuzel 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
Ресей

Amina Daminova

Kazan Federal University

Email: noemail@neicon.ru
ORCID iD: 0000-0002-7672-4430
Ресей

Shamil Galyaltdinov

Kazan Federal University

Email: noemail@neicon.ru
ORCID iD: 0000-0002-9494-5288
Ресей

Ayrat Dimiev

Kazan Federal University

Email: noemail@neicon.ru
ORCID iD: 0000-0001-7497-1211
Ресей

Marina Kryuchkova

Kazan Federal University

Email: noemail@neicon.ru
ORCID iD: 0000-0002-6946-0553
Ресей

Rawil Fakhrullin

Kazan Federal University

Email: noemail@neicon.ru
ORCID iD: 0000-0003-2015-7649
Ресей

Liliya 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

Ресей

Әдебиет тізімі

  1. 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
  2. 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
  3. 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
  4. 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
  5. 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
  6. 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
  7. 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
  8. 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
  9. 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
  10. 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)
  11. 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
  12. 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
  13. 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
  14. 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.
  15. 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
  16. 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
  17. 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
  18. 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
  19. 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
  20. 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
  21. 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
  22. 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
  23. 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
  24. 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
  25. 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
  26. 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
  27. Multiple-Path Particle Dosimetry Model (MPPD v 3.04). Available at: https://www.ara.com/products/multiple-path-particle-dosimetry-model-mppd-v-304
  28. 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)
  29. 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
  30. 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)
  31. 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
  32. 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
  33. 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
  34. 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
  35. 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
  36. 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

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© Gabidinova G.F., Timerbulatova G.A., Daminova A.G., Galyaltdinov S.F., Dimiev A.M., Kryuchkova M.A., Fakhrullin R.F., Fatkhutdinova L.M., 2023


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