Механизмы канцерогенного действия наноматериалов
https://doi.org/10.17650/2313-805X-2022-9-4-8-23
Аннотация
Наноматериалы получают все большее распространение во многих областях жизни человека, формируя новую философию техносферы и, в частности, новые подходы к получению и использованию материалов в бытовых процессах, производстве, медицине и пр. Физико-химические характеристики наноматериалов существенно отличаются от соответствующих показателей агрегатных материалов и, по крайней мере, некоторые из них – высокой реакционноспособностью и / или повышенной каталитической активностью. Это позволяет предположить их агрессивность по отношению к биологическим системам, включая участие в процессах канцерогенеза.
В обзоре рассмотрены сферы использования современных наноматериалов, при этом особое внимание уделено описанию лекарственных препаратов, произведенных с использованием нанотехнологий, приведен анализ механизмов действия тех из них, которые уже признаны канцерогенными, а также представлены имеющиеся экспериментальные и механистические данные, полученные при изучении канцерогенного / проканцерогенного действия различных групп наноматериалов, не классифицируемых в настоящее время как представляющие канцерогенную опасность для человека.
При подготовке обзора был проведен анализ публикаций информационных баз биомедицинской литературы Scopus (507), PubMed (561), Web of Science (268), eLibrary.ru (190). Для получения полнотекстовых документов использованы электронные ресурсы PubMed Central (PMC), Science Direct, Research Gate, базы данных Sci-Hub и eLibrary.ru.
Ключевые слова
Об авторах
Г. А. БелицкийРоссия
115522 Москва, Каширское шоссе, 24
К. И. Кирсанов
Россия
115522 Москва, Каширское шоссе, 24
117198 Москва, ул. Миклухо-Маклая, 6
Е. А. Лесовая
Россия
115522 Москва, Каширское шоссе, 24
390026 Рязань, ул. Высоковольтная, 9
М. Г. Якубовская
Россия
Марианна Геннадиевна Якубовская
115522 Москва, Каширское шоссе, 24
Список литературы
1. Feynman R.P. There’s plenty of room at the bottom. Engineering Sci 1960;23(5):22–36.
2. Карпов Д.А., Литуновский В.Н. Наноматериалы. СПб.: ФГУП «НИИЭФА им. Д.В. Ефремова», 2007. 82 с.
3. Karthik P.S., Himaja A.L., Singh S.P. Carbon-allotropes: synthesis methods, applications and future perspectives. Carbon Letters 2014;15(4):219–37.
4. Кирчанов В.С. Наноматериалы и нанотехнологии. Пермь, 2016. 193 с.
5. Menezes de B.R.C., Rodrigues K.F., Fonseca da Silva B.C. Recent advances in the use of carbon nanotubes as smart biomaterials. J Mater Chem B 2019;7:1343–60. DOI: 10.1039/c8tb02419g
6. Janković N., Plata D. Engineered nanomaterials in the context of global element cycles. Environmental Science: Nano 2019;6(9):2697–711. DOI: 10.1039/c9en00322c
7. Chemical accidents involving nanomaterials: potential risks and review of prevention, preparedness and response measures – project report. Series on chemical accidents. OECD 2022;34:50.
8. Выявление наноматериалов, представляющих потенциальную опасность для здоровья человека: Методические рекомендации. М.: Федеральный центр гигиены и эпидемиологии Роспотребнадзора, 2009. 35 с.
9. Hu C.M., Zhang L. Nanoparticle-based combination therapy toward overcoming drug resistance in cancer. Biochem Pharmacol 2012;83(8):1104–11. DOI: 10.1016/j.bcp.2012.01.008
10. Davatgaran-Taghipour Y., Masoomzadeh S., Farzaei M.H. et al. Polyphenol nanoformulations for cancer therapy: experimental evidence and clinical perspective. Int J Nanomedicine 2017;12:2689–702. DOI: 10.2147/IJN.S131973
11. Бовина Е.М., Романов Б.К., Казаков А.С. и др. Наноразмерные лекарственные средства: особенности оценки безопасности. Безопасность и риск фармакотерапии 2019;7(3):127–38. DOI: 10.30895/2312-7821-2019-7-3-127-138
12. Halwani A. Development of pharmaceutical nanomedicines: from the bench to the market. Pharmaceutics 2022;106:1–21. DOI: 10.3390/pharmaceutics14010106
13. Rajora A.K., Ravishankar D., Zhang H. et al. Recent advances and impact of chemotherapeutic and antiangiogenic nanoformulations for combination cancer therapy. Pharmaceutics 2020;12(6):592. DOI: 10.3390/pharmaceutics12060592
14. Allemailem K.S., Almatroudi A., Alsahli M.A. et al. Novel strategies for disrupting cancer-cell functions with mitochondria-targeted antitumor drug-loaded nanoformulations. Int J Nanomedicine 2021;16:3907–36. DOI: 10.2147/IJN.S303832
15. Thambiraj S., Vijayalakshmi R., Ravi Shankaran D. An effective strategy for development of docetaxel encapsulated gold nanoformulations for treatment of prostate cancer. Sci Rep 2021;11:2808. DOI: 10.1038/s41598-020-80529-1
16. Mirjolet C., Boudon J., Loiseau A. Docetaxel-titanate nanotubes enhance radiosensitivity in an androgen-independent prostate cancer model. Int J Nanomedicine 2017;2:6357–64. DOI: 10.2147/IJN.S139167.12
17. Ganju A., Khan S., Hafeez B.B. et al. miRNA nanotherapeutics for cancer. Drug Discov Today 2017;22(2):424–32. DOI: 10.1016/j.drudis.2016.10.014
18. IARC monographs on the evaluation of carcinogenic risks to humans. Volume 100C. Arsenic, metals, fibres, and dusts, 2009. International Agency for Research on Cancer. II Series. Available at: https://monographs.iarc.who.int/wp-content/uploads/2018/06/mono100C.pdf.
19. IARC monographs on the evaluation of carcinogenic risks to humans. Volume 111. Some nanomaterials and some fibres. 2017. International Agency for Research on Cancer. II Series. Available at: https://monographs.iarc.who.int/wp-content/uploads/2018/06/mono111.pdf.
20. IARC monographs on the evaluation of carcinogenic risks to humans. Volume 131. Cobalt Metal (without Tungsten Carbide or Other Metal Alloys) and Cobalt (II) Salts, Trivalent and Pentavalent Antimony, and Weapons-grade Tungsten (with Nickel and Cobalt) Alloy. 2022. International Agency for Research on Cancer. II Series. Available at: https://www.iarc.who.int/news-events/iarcmonographs-vol-131/.
21. Бычков М.Б., Абдуллаев А.Г., Багрова С.Г. и др. Практические рекомендации по лечению мезотелиомы плевры, брюшины и других локализаций. Злокачественные опухоли. RUSSCO 2019 (#3s2):55–67. DOI: 10.18027 / 2224-5057-2019-9-3s2-55-67
22. Beard J.D., Erdely A., Dahm M.M. Carbon nanotube and nanofiber exposure and sputum and blood biomarkers of early effect among U.S. workers. Environ Int 2018;116:214–28. DOI: 10.1016/j.envint.2018.04.004
23. Vlaanderen J., Pronk A., Rothman N. A cross-sectional study of changes in markers of immunological effects and lung health due to exposure to multi-walled carbon nanotubes. Nanotoxicology 2017;11(3):395–404. DOI: 10.1080/17435390.2017.1308031
24. Fatkhutdinova L.M., Khaliullin T.O., Vasil’yeva O.L. et al. Fibrosis biomarkers in workers exposed to MWCNTs. Toxicol Appl Pharmacol 2016;299:125–31. DOI: 10.1016/j.taap.2016.02.016
25. Liou S.-H., Wu W.-T., Liao H.-Y. et al. Global DNA methylation and oxidative stress biomarkers in workers exposed to metal oxide nanoparticles. J Hazard Mater 2017;331:329–35. DOI: 10.1016/j.jhazmat.2017.02.042
26. Rossnerova A., Honkova K., Pelclova D. et al. DNA Methylation profiles in a group of workers occupationally exposed to nanoparticles. Int J Mol Sci 2020;21(7):2420. DOI: 10.3390/ijms21072420
27. Pogribna M., Hammons G. Epigenetic effects of nanomaterials and nanoparticles. J Nanobiotechnology 2021;19(1):2. DOI: 10.1186/s12951-020-00740-0
28. Pilger A., Rüdiger H.W. 8-Hydroxy-2’-deoxyguanosine as a marker of oxidative DNA damage related to occupational and environmental exposures. Int Arch Occup Environ Health 2006;80:1–15. DOI: 10.1007/s00420-006-0106-7
29. Gupta S.S., Singh K.P., Gupta S. et al. Do carbon nanotubes and asbestos fibers exhibit common toxicity mechanisms? Nanomaterials (Basel) 2022;12(10):1708. DOI: 10.3390/nano12101708
30. Fraser K., Kodali V., Yanamala N. et al. Physicochemical characterization and genotoxicity of the broad class of carbon nanotubes and nanofibers used or produced in US facilities. Part Fibre Toxicol 2020;17(1):62. DOI: 10.1186/s12989-020-00392-w
31. Kane A.B., Hurt R.H., Gao H. The asbestos-carbon nanotube analogy: an update. Toxicol Appl Pharmacol 2018;361:68–80. DOI: 10.1016/j.taap.2018.06.027
32. Guo L., Morris D.G., Liu X. et al. Iron bioavailability and redox activity in diverse carbon nanotube samples. Chem Mater 2007;19:3472–8. DOI: 10.1021/cm062691p
33. Fukushima S., Kasai T., Umeda Y. et al. Carcinogenicity of multiwalled carbon nanotubes: challenging issue on hazard assessment. J Occup Health 2018;60:10–30. DOI: 10.1539/joh.17-0102-RA
34. Numano T., Higuchi H., Alexander D.B. et al. MWCNT-7 administered to the lung by intratracheal instillation induces development of pleural mesothelioma in F344 rats. Cancer Sci 2019;110(8):2485–92. DOI: 10.1111/cas.14121
35. Takagi A., Hirose A., Futakuchi M. et al. Dose-dependent mesothelioma induction by intraperitoneal administration of multiwall carbon nanotubes in p53 heterozygous mice. Cancer Sci 2012;103(8):1440–4. DOI: 10.1111/j.1349-7006.2012.02318.x
36. Muller J., Decordier I., Hoet P.H. et al. Clastogenic and aneugenic effects of multi-wall carbon nanotubes in epithelial cells. Carcinogenesis 2008;29(2):427–33. DOI: 10.1093/carcin/bgm243
37. Magaye R., Zhao J., Bowman L., Ding M. Genotoxicity and carcinogenicity of cobalt-, nickel- and copper-based nanoparticles. Exp Ther Med 2012;4(4):551–61. DOI: 10.3892/etm.2012.656
38. Bouchard L., Anwar M., Liu L. et al. Picomolar sensitivity MRI and photoacoustic imaging of cobalt nanoparticles. Proc Natl Acad Sci USA 2009;106(11):4085–89. DOI: 10.1073/pnas.0813019106
39. Li Y., Ye F., Zhang S. et al. Carbon-coated magnetic nanoparticle dedicated to MRI/photoacoustic Imaging of tumor in living mice. Front Bioeng Biotechnol 2021;2;9:800744. DOI: 10.3389/fbioe.2021.800744
40. Carbon black, titanium dioxide, and talc. IARC monographs on the evaluation of carcinogenic risks to humans. Vol. 93. Lyon (FR): International Agency for Research on Cancer, 2010. 466 p.
41. Proquin H., Jonkhout M., Jetten M. et al. Transcriptome changes in undifferentiated Caco-2 cells exposed to food-grade titanium dioxide (E171): contribution of the nano- and micro- sized particles. Sci Rep 2019;9(1):18287. DOI: 10.1038/s41598-019-54675-0
42. Shi J., Han S., Zhang J. et al. Advances in genotoxicity of titanium dioxide nanoparticles in vivo and in vitro. NanoImpact 2022;100377. DOI: 10.1016/j.impact.2021.100377
43. Xia Q., Li H., Liu Y. et al. The effect of particle size on the genotoxicity of gold nanoparticles. J Biomed Mater Res A 2017; 105(3):710–9. DOI: 10.1002/jbm.a.35944
44. Sighinolfi G.L., Artoni E., Gatti A.M., Corsi L. Carcinogenic potential of metal nanoparticles in BALB/3T3 cell transformation assay. Environ Toxicol 2016;31(5):509–19. DOI: 10.1002/tox.22063
45. Rodriguez-Garraus A., Azqueta A., Vettorazzi A. et al. Genotoxicity of silver nanoparticles. Nanomater (Basel, Switzerland) 2020;10(2):251. DOI: 10.3390/nano10020251
46. Liu L., Kong L. Research progress on the carcinogenicity of metal nanomaterials. Appl Toxicol 2021;41(9):1334–44. DOI: 10.1002/jat.4145
47. Yazdimamaghani M., Moos P.J., Dobrovolskaia M.A., Ghandehari H. Genotoxicity of amorphous silica nanoparticles: status and prospects. Nanomedicine 2019;16:106–25. DOI: 10.1016/j.nano.2018.11.013
48. Downs T., Crosby M., Hu T. et al. Silica nanoparticles administered at the maximum tolerated dose induce genotoxic effects through an inflammatory reaction while gold nanoparticles do not. Mutat Res 2012;745(1–2):38–50. DOI: 10.1016/j.mrgentox.2012.03.012
49. Xi W., Tang H., Liu Y. et al. Cytotoxicity of vanadium oxide nanoparticles and titanium dioxide-coated vanadium oxide nanoparticles to human lung cells. J Appl Toxicol 2020;40(5): 567–77. DOI: 10.1002/jat.3926
50. Sighinolfi G., Artoni E., Gatti A., Corsi L. Carcinogenic potential of metal anoparticles in BALB/3T3 cell transformation assay. Environ Toxicol 2016;31(5):509–19. DOI: 10.1002/tox.22063
51. Ахальцева Л.В., Журков В.С., Ингель Ф.И. Мутагенная активность наноматериалов в тесте Эймса. Гигиена и санитария 2019;98(11):1309–20.
52. Zhou F., Liao F., Chen L. et al. The size-dependent genotoxicity and oxidative stress of silica nanoparticles on endothelial cells. Environ Sci Pollut Res Int 2019;26:1911–20. DOI: 10.1007/s11356-018-3695-2
53. Murphy F.A., Poland C.A., Duffin R. et al. Length-dependent retention of carbon nanotubes in the pleural space of mice initiates sustained inflammation and progressive fibrosis on the parietal pleura. Am J Pathol 2011;178(6):2587–600. DOI: 10.1016/j.ajpath.2011.02.040
54. Murphy F.A., Schinwald A., Poland C.A. The mechanism of pleural inflammation by long carbon nanotubes: interaction of long fibres with macrophages stimulates them to amplify pro-inflammatory responses in mesothelial cells. Part Fibre Toxicol 2012;9:8. DOI: 10.1186/1743-8977-9-8
55. Magdolenova Z., Drlickova M., Henjum K. et al. Coatingdependent induction of cytotoxicity and genotoxicity of iron oxide nanoparticles. Nanotoxicology 2015;9(1):44–56. DOI: 10.3109/17435390.2013.847505
56. Kohl Y., Rundén-Pran E., Mariussen E. et al. Genotoxicity of nanomaterials: advanced in vitro models and high throughput methods for human hazard assessment – a review. Nanomater (Basel, Switzerland) 2020;10(10):1911. DOI: 10.3390/nano10101911
57. Evans S.J., Clift M.J.D., Singh N. et al. Critical review of the current and future challenges associated with advanced in vitro systems towards the study of nanoparticle (secondary) genotoxicity. Mutagenesis 2017;32(1):233–41. DOI: 10.1093/mutage/gew054
58. Hanot-Roy M., Tubeuf E., Guilbert A. et al. Oxidative stress pathways involved in cytotoxicity and genotoxicity of titanium dioxide (TiO2) nanoparticles on cells constitutive of alveolocapillary barrier in vitro. Toxicol In Vitro 2016;33:125–35. DOI: 10.1016/j.tiv.2016.01.013
59. Wan R., Mo Y., Feng L. et al. DNA damage caused by metal nanoparticles: involvement of oxidative stress and activation of ATM. Chem Res Toxicol 2012;25(7):1402–11. DOI: 10.1021/tx200513t
60. Brown T.A., Lee J.W., Holian A. et al. Alterations in DNA methylation corresponding with lung inflammation and as a biomarker for disease development after MWCNT exposure. Nanotoxicology 2016;10(4):453–61. DOI: 10.3109/17435390.2015.1078852
61. Yu J., Loh X.J., Luo Y. et al. Insights into the epigenetic effects of nanomaterials on cells. Biomater Sci 2020;8(3):763–75. DOI: 10.1039/c9bm01526d
62. Öner D., Ghosh M., Bové H. et al. Differences in MWCNTand SWCNT-induced DNA methylation alterations in association with the nuclear deposition. Part Fibre Toxicol 2018;15(1):11. DOI: 10.1186/s12989-018-0244-6
63. Öner D., Ghosh M., Coorens R. et al. Induction and recovery of CpG site specific methylation changes in human bronchial cells after long-term exposure to carbon nanotubes and asbestos. Environ Int 2020;137:105530. DOI: 10.1016/j.envint.2020.105530
64. Ghosh M., Öner D., Duca R.C. et al. Single-walled and multiwalled carbon nanotubes induce sequence-specific epigenetic alterations in 16 HBE cells. Oncotarget 2018;9(29):20351–65. DOI: 10.18632/oncotarget.24866
65. Sierra M.I., Rubio L., Bayón G.F. et al. DNA methylation changes in human lung epithelia cells exposed to multi-walled carbon nanotubes. Nanotoxicology 2017;11(7):857–70. DOI: 10.1080/17435390.2017.1371350
66. Valinluck V., Sowers L.C. Inflammation-mediated cytosine damage: a mechanistic link between inflammation and the epigenetic alterations in human cancers. Cancer Res 2007;67(12):5583–6. DOI: 10.1158/0008-5472.CAN-07-0846
67. Jiang Z., Lai Y., Beaver J.M. et al. Oxidative DNA damage modulates DNA methylation pattern in Human Breast Cancer 1 (BRCA1) gene via the crosstalk between DNA polymerase β and a de novo DNA methyltransferase. Cells 2020;9(1):225. DOI: 10.3390/cells9010225
68. Sima M., Vrbova K., Zavodna T. et al. The differential effect of carbon dots on gene expression and DNA methylation of human embryonic lung fibroblasts as a function of surface charge and dose. Int J Mol Sci 2020;21(13):4763. DOI: 10.3390/ijms21134763
69. Kopp B., Dario M., Zalko D. et al. Assessment of a panel of cellular biomarkers and the kinetics of their induction in comparing genotoxic modes of action in HepG2 cells. Environ Mol Mutagen 2018;59(6):516–28. DOI: 10.1002/em.22197
70. Seidel C., Kirsch A., Fontana C. et al. Epigenetic changes in the early stage of silica-induced cell transformation. Nanotoxicology 2017;11(7):923–35. DOI: 10.1080/17435390.2017.1382599
71. Shyamasundar S., Ng C.T., Yung L.Y.L. et al. Epigenetic mechanisms in nanomaterial-induced toxicity. Epigenomics 2015;7(3):395–411. DOI: 10.2217/epi.15.3
72. Halappanavar S., Jackson P., Williams A. et al. Pulmonary response to surface-coated nanotitanium dioxide particles includes induction of acute phase response genes, inflammatory cascades, and changes in microRNAs: a toxicogenomic study. Environ Mol Mutagen 2011;52(6):425–39. DOI: 10.1002/em.20639
73. Shukla R.K., Badiye A., Vajpayee K. et al. Genotoxic potential of nanoparticles: structural and functional modifications in DNA. Front Genet. 2021;12:728250. DOI: 10.3389/fgene.2021.728250
74. Brzóska K., Grądzka I., Kruszewski M. Silver, gold, and iron oxide nanoparticles alter miRNA expression but do not affect DNA methylation in HepG2 cells. Mater (Basel, Switzerland) 2019;12(7):1038. DOI: 10.3390/ma12071038
75. Snyder-Talkington B.N., Dong C., Sargent L.M. et al. mRNAs and miRNAs in whole blood associated with lung hyperplasia, fibrosis, and bronchiolo-alveolar adenoma and adenocarcinoma after multiwalled carbon nanotube inhalation exposure in mice. J Appl Toxicol 2016;36(1):161–74. DOI: 10.1002/jat.3157
76. Yang K., Zhu L., Xing B. Adsorption of polycyclic aromatic hydrocarbons by carbon nanomaterials. Environ Sci Technol 2006;40(6):1855–61. DOI: 10.1021/es052208w
77. Yang K., Xing B. Desorption of polycyclic aromatic hydrocarbons from carbon nanomaterials in water. Environ Pollut 2007;145:529–37. DOI: 10.1016/j.envpol.2006.04.020
78. Birch M.E. Exposure and emissions monitoring during carbon nanofiber production. Part II: polycyclic aromatic hydrocarbons. Ann Occup Hyg 2011;55:1037–47. DOI: 10.1093/annhyg/mer070
79. Samburova V., Zielinska B., Khlystov A. Do 16 polycyclic aromatic hydrocarbons represent PAH air toxicity? Toxics 2017;5. DOI: 10.3390/toxics5030017
80. Chalbot M.-C.G., Pirela S.V., Schifman L. et al. Synergistic effects of engineered nanoparticles and organics released from laser printers using nano-enabled toners: potential health implications from exposures to the emitted organic aerosol. Environ Sci Nano 2017;4:2144–56. DOI: 10.1039/C7EN00573C
Рецензия
Для цитирования:
Белицкий Г.А., Кирсанов К.И., Лесовая Е.А., Якубовская М.Г. Механизмы канцерогенного действия наноматериалов. Успехи молекулярной онкологии. 2022;9(4):8‑23. https://doi.org/10.17650/2313-805X-2022-9-4-8-23
For citation:
Belitsky G.A., Kirsanov K.I., Lesovaya E.A., Yakubovskaya M.G. Mechanisms of the carcinogenicity of nanomaterials. Advances in Molecular Oncology. 2022;9(4):8‑23. (In Russ.) https://doi.org/10.17650/2313-805X-2022-9-4-8-23