Interaction of graphene oxide nanoparticles with cells of the immune system



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Abstract

Graphene-based preparations are the most promising materials in biomedicine. This review is aimed at analyzing data on the interaction of graphene oxide nanoparticles with different types of cells of the immune system: neutrophils, monocytes, macrophages, dendritic cells, T- and B-lymphocytes, NK and iNKT cells. Scopus publications from 2011 to May 2020 were analyzed. The primary vector of the graphene oxide nanoparticles' effects is associated with cell activation and the formation of a proinflamma-tory profile of the immune response. At the same time, the functionalization of the graphene oxide surface with the biocompatible polymers leads to a decrease in its cytotoxicity, and in some cases, to suppression of cell activation. The interaction of graphene oxide nanoparticles with cells depends on numerous factors, such as direct and lateral sizes, oxidation state, functionalization, number of layers, 3D configuration, as well as the microbiological purity and pyrogenicity of graphene. Together, these characteristics determine whether graphene oxide nanoparticles must stimulate or suppress the immune system. These multidirectional possibilities of graphene oxide can be useful in the development of adjuvants, new drug delivery mechanisms, and modern biosensors.

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About the authors

P. V Khramtsov

Institute of Ecology and Genetics of Microorganisms, UB of the RAS - Branch of the Perm State Research Cente, UB of the RAS

M. B Rayev

Institute of Ecology and Genetics of Microorganisms, UB of the RAS - Branch of the Perm State Research Cente, UB of the RAS

V. P Timganova

Institute of Ecology and Genetics of Microorganisms, UB of the RAS - Branch of the Perm State Research Cente, UB of the RAS

M. S Bochkova

Institute of Ecology and Genetics of Microorganisms, UB of the RAS - Branch of the Perm State Research Cente, UB of the RAS

S. A Zamorina

Institute of Ecology and Genetics of Microorganisms, UB of the RAS - Branch of the Perm State Research Cente, UB of the RAS

References

  1. Разумов В.Ф. Г. рафен - новый прорыв в области нанотехнологий. Российские нанотехнологии 2010; 5: 17-22.
  2. Панкратов Д.В., Г. онзалез-Аррибас Е., Парунова Ю.М. и др. Новые нанобиокомпозитные материалы для биоэлектронных устройств. Acta Naturae 2015; 7: 103-7.
  3. Dasari Shareena T.P., McShan D., Dasmahapatra A.K. et al. Review on graphene-based nanomaterials in biomedical applications and risks in environment and health. Nanomicro Lett. 2018; 10: 53.
  4. Zhang H., Yan T., Xu S. et al. Graphene oxide-chitosan nanocomposites for intracellular delivery of immunostimulatory CpG oligodeoxynucleotides. Mater. Sci. Eng. C. Mater. Biol. Appl. 2017; 73: 144-51.
  5. Park M.V.D.Z., Bleeker E.A.J., Brand W. et al. Considerations for Safe Innovation: The Case of Graphene. ACS Nano 2017; 11: 9574-93.
  6. Makharza S., Cirillo G., Bachmatiuk A. et al. Graphene oxide-based drug delivery vehicles: functionalization, characterization, and cytotoxicity evaluation. J. Nanoparticle Research 2013; 15: 2099.
  7. Ou L., Lin S., Song B. et al. The mechanisms of graphene-based materials-induced programmed cell death: a review of apoptosis, autophagy, and programmed necrosis. Int. J. Nanomedicine 2017; 12: 6633-46.
  8. Tang Z., Zhao L., Yang Z. et al. Mechanisms of oxidative stress, apoptosis, and autophagy involved in graphene oxide nanomaterial antiosteosarcoma effect. Int. J. Nanomedicine 2018; 13: 2907-19.
  9. Dudek I., Skoda M., Jarosz A. et al. The molecular influence of graphene and graphene oxide on the immune system under in vitro and in vivo conditions. Arch. Immunol. Ther. Exp. (Warsz) 2016; 64(3): 195-215.
  10. Orecchioni M., Bedognetti D., Newman L. et al. Single-cell mass cytometry and transcriptome profiling reveal the impact of graphene on human immune cells. Nat. Commun. 2017; 8(1): 1109.
  11. Dreyer D.R., Park S., Bielawski C.W. et al. The chemistry of graphene oxide. Chem. Soc. Rev. 2010; 39(1): 228-40.
  12. Singh D.P., Herrera C.E., Singh B. et al. Graphene oxide: An efficient material and recent approach for biotechnological and biomedical applications. Mater. Sci. Eng. 2018; 86: 173-97.
  13. Orecchioni M., Jasim D.A., Pescatori M. et al. Molecular and genomic impact of large and small lateral dimension graphene oxide sheets on human immune cells from healthy donors. Adv. Healthcare Mater. 2016; 5: 276-87.
  14. Kiew S.F., Kiew L.V., Lee H.B. et al. Assessing biocompatibility of graphene oxide-based nanocarriers: A review. J. Controlled Release 2016; 226: 217-28.
  15. McCallion C., Burthem J., Rees-Unwin K. et al. Graphene in therapeutics delivery: Problems, solutions and future opportunities. J. Pharmaceutics and Biopharmaceutics 2016; 104: 235-50.
  16. Ishida T., Ichihara M., Wang X. et al. Injection of PEGylated liposomes in rats elicits PEG-specific IgM, which is responsible for rapid elimination of a second dose of PEGylated liposomes. J. Controlled Release 2006; 112(1): 15-25.
  17. Kurapati R., Russier J., Squillaci M.A. et al. Dispersibility-dependent biodegradation of graphene oxide by myeloperoxidase. Small 2016; 11: 3985-94.
  18. Mukherjee S.P., Gliga A.R., Lazzaretto B. et al. Graphene oxide is degraded by neutrophils and the degradation products are non-genotoxic. Nanoscale 2018; 10(3): 1180-8.
  19. Paino I.M., Santos F., Zucolotto V. Biocompatibility and toxicology effects of graphene oxide in cancer, normal, and primary immune cells. J. Biomedical Materials Research - Part A 2017; 105(3): 728-36.
  20. Mukherjee S.P., Lazzaretto B., Hultenby K. et al. Graphene oxide elicits membrane lipid changes and neutrophil extracellular trap formation. Chem. 2018; 4(2): 334-58.
  21. Li Y., Feng L., Shi X. et al. Surface coating-dependent cytotoxicity and degradation of graphene derivatives: towards the design of non-toxic, degradable nano-graphene. Small 2014; 10(8): 1544-54.
  22. Yan J., Chen L., Huang C.C. et al. Consecutive evaluation of graphene oxide and reduced graphene oxide nanoplatelets immunotoxicity on monocytes. Colloids and Surfaces B: Biointerfaces 2017; 153: 300-9.
  23. Orecchioni M., Bordoni V., Fuoco C. et al. Toward high-dimensional single-cell analysis of graphene oxide biological impact: tracking on immune cells by single-cell mass cytometry. Small 2020; 16(21): е2000123.
  24. Chen G.Y., Chen C.L., Tuan H.Y. et al. Graphene oxide triggers Toll-like receptors/autophagy responses in vitro and inhibits tumor growth in vivo. Adv. Healthcare Mater. 2014; 3: 1486-95.
  25. Chen G.Y., Yang H., Lu C.H. et al. Simultaneous induction of autophagy and toll-like receptor signaling pathways by graphene oxide. Biomaterials 2012; 33(27): 6559-69.
  26. Duch M.C., Budinger G.R., Liang Y.T. et al. Minimizing oxidation and stable nanoscale dispersion improves the biocompatibility of graphene in the lung. Nano Lett. 2011; 11(12): 5201-7.
  27. Wang X., Podila R., Shannahan J.H. et al. Intravenously delivered graphene nanosheets and multiwalled carbon nanotubes induce site-specific Th2 inflammatory responses via the IL-33/ST2 axis. Int. J. Nanomedicine 2013; 8: 1733-48.
  28. Chang Y., Yang S.T., Liu J.H. et al. In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol. Lett. 2011; 200(3): 201-10.
  29. Feito M.J., Vila M., Matesanz M.C. et al. In vitro evaluation of graphene oxide nanosheets on immune function. J. Colloid and Interface Science 2014; 432: 221-8.
  30. Diez-Orejas R., Feito M.J., Cicuendez M. et al. Differential effects of graphene oxide nanosheets on Candida albicans phagocytosis by murine peritoneal macrophages. J. Colloid and Interface Science 2018; 512: 665-73.
  31. Zhi X., Fang H., Bao C. et al. The immunotoxicity of graphene oxides and the effect of PVP-coating. Biomaterials 2013; 34: 5254-61.
  32. Mendes R.G., Koch B., Bachmatiuk A. et al. A size dependent evaluation of the cytotoxicity and uptake of nanographene oxide. J. Mater. Chem. 2015; 3: 2522.
  33. Yue H., Wei W., Gu Z. et al. Exploration of graphene oxide as an intelligent platform for cancer vaccines. Nanoscale 2015; 7: 19949-57.
  34. Russier J., Treossi E., Scarsi A. et al. Evidencing the mask effect of graphene oxide: a comparative study on primary human and murine phagocytic cells. Nanoscale 2013; 5: 11234-47.
  35. Feito M.J., Orejas R.D., Cicuendez M. et al. Characterization of M1 and M2 polarization phenotypes in peritoneal macrophages after treatment with graphene oxide nanosheets. Colloids and Surfaces B: Biointerfaces 2019; 176: 96-105.
  36. Lategan K., Alghadi H., Bayati M. et al. Effects of graphene oxide nanoparticles on the immune system biomarkers produced by RAW 264.7 and human whole blood cell cultures. Nanomaterials (Basel) 2018; 8(2): 125.
  37. Mukherjee S. P., Kostarelos K., Fadeel B. Cytokine profiling of primary human macrophages exposed to endotoxin-free graphene oxide: size-independent NLRP3 inflammasome activation. Adv. Healthcare Mater. 2018; 7: 1700815.
  38. Orecchioni D. Bedognetti F. Sgarrella F.M. et al. Impact of carbon nanotubes and graphene on immune cells. J. Transl. Med. 2014; 12: 138.
  39. Schreibelt G., Tel J., Sliepen K.H.E.W.J. et al. Toll-like receptor expression and function in human dendritic cell subsets: implications for dendritic cell-based anti-cancer immunotherapy. Cancer Immunology, Immunotherapy 2010; 59(10): 1573-82.
  40. Tomic S., Janjetovic K., Mihajlovic D. et al. Graphene quantum dots suppress proinflammatory T cell responses via autophagy-dependent induction of tolerogenic dendritic cells. Biomaterials 2017; 146: 13-28.
  41. Tkach A.V., Yanamala N., Stanley S. et al. Graphene oxide, but not fullerenes, targets immunoproteasomes and suppresses antigen presentation by dendritic cells. Small 2013; 9(9-10): 1686-90.
  42. Xu L., Xiang J., Liu Y. et al. Functionalized graphene oxide serves as a novel vaccine nano-adjuvant for robust stimulation of cellular immunity. Nanoscale 2016; 8(6): 3785-95.
  43. Wang W., Li Z., Duan J. et al. In vitro enhancement of dendritic cell-mediated anti-glioma immune response by graphene oxide. Nanoscale Res. Lett. 2014; 9(1): 311.
  44. Schinwald A., Murphy F.A., Jones A. et al. Graphene-based nanoplatelets: a new risk to the respiratory system as a consequence of their unusual aerodynamic properties. ACS Nano 2012; 6(1): 736-46.
  45. Mu Q., Su G., Li L. et al. Size-Dependent cell uptake of protein-coated graphene oxide nanosheets. ACS Appl. Mater. Interfaces 2012; 4(4): 2259-66.
  46. Meng C., Zhi X., Li C. et al. Graphene oxides decorated with carnosine as an adjuvant to modulate innate immune and improve adaptive immunity in vivo. ACS Nano 2016; 10(2): 2203-13.
  47. Ni G., Wang Y., Wu X. et al. Graphene oxide absorbed anti-IL10R antibodies enhance LPS induced immune responses in vitro and in vivo. Immunol. Lett. 2012; 148: 126-32.
  48. Zhang M., Mao X., Wang C. et al. The effect of graphene oxide on conformation change, aggregation and cytotoxicity of HIV-1 regulatory protein (Vpr). Biomaterials 2013; 34: 1383-90.
  49. Lee S.W., Park H.J., Van Kaer L. et al. Graphene oxide polarizes iNKT cells for production of TGFp and attenuates inflammation in an iNKT cell-mediated sepsis model. Sci. Rep. 2018; 8(1): 810081.
  50. Xu S., Xu S., Chen S. et al. Graphene oxide modulates B cell surface phenotype and impairs immunoglobulin secretion in plasma cell. J. Nanosci. Nanotechnol. 2016; 16(4): 4205-15.
  51. Luo C., Deng Z., Li L. et al. Association of rituximab with graphene oxide confers direct cytotoxicity for CD20-positive lymphoma cells. Oncotarget 2016; 7(11): 12806-22.
  52. Loftus C., Saeed M., Davis D.M. et al. Activation of human natural killer cells by graphene oxide-templated antibody nanoclusters. Nano Lett. 2018; 18(5): 3282-9.
  53. Shissler S.C., Webb T.J. The ins and outs of type I iNKT cell development. Mol. Immunol. 2019; 105: 116-30.
  54. Yan M., Liu Y., Zhu X. et al. Nanoscale reduced graphene oxide-mediated photothermal therapy together with IDO inhibition and PD-L1 blockade synergistically promote antitumor immunity. ACS Appl. Interfaces 2019; 11: 1876-85.
  55. Ding Z., Luo N., Yue H. et al. In vivo immunological response of exposure to PEGylated graphene oxide via intraperitoneal injection. J. Mater. Chem. B 2020; 8: 10081.

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