Carbon-Based Nanomaterials Increase Reactivity of Primary Monocytes towards Various Bacteria and Modulate Their Differentiation into Macrophages

. 2021 Sep 27 ; 11 (10) : . [epub] 20210927

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid34684950

Grantová podpora
CZ.02.1.01/0.0/0.0/17_048/0007421 Ministerstvo Školství, Mládeže a Tělovýchovy
CZ.02.1.01/0.0/0.0/16_019/0000760 Ministerstvo Školství, Mládeže a Tělovýchovy
PROGRES Q40/10 Univerzita Karlova v Praze
PROGRES Q40/09 Univerzita Karlova v Praze

The evaluation of carbon-based nanomaterials' (C-BNMs') interactions with the immune system, notably their ability to cause inflammation, is a critical step in C-BNM health risk assessment. Particular attention should be given to those C-BNMs that do not cause direct cytotoxicity or inflammation on their own. However, the intracellular presence of these non-biodegradable nanomaterials could dysregulate additional cell functions. This is even more crucial in the case of phagocytes, which are the main mediators of defensive inflammation towards pathogens. Hence, our study was focused on multi-walled carbon nanotubes (MWCNTs) and two different types of graphene platelets (GPs) and whether their intracellular presence modulates a proinflammatory response from human primary monocytes towards common pathogens. Firstly, we confirmed that all tested C-BNMs caused neither direct cytotoxicity nor the release of tumour necrosis factor α (TNF-α), interleukin (IL)-6 or IL-10. However, such pre-exposed monocytes showed increased responsiveness to additional bacterial stimuli. In response to several types of bacteria, monocytes pre-treated with GP1 produced a significantly higher quantity of TNF-α, IL-6 and IL-10. Monocytes pre-treated with MWCNTs produced increased levels of IL-10. All the tested C-BNMs enhanced monocyte phagocytosis and accelerated their differentiation towards macrophages. This study confirms the immunomodulatory potential of C-BNMs.

Zobrazit více v PubMed

Bei H.P., Yang Y., Zhang Q., Tian Y., Luo X., Yang M., Zhao X. Graphene-based nanocomposites for neural tissue engineering. Molecules. 2019;24:658. doi: 10.3390/molecules24040658. PubMed DOI PMC

Li Q., Wen J., Liu C., Jia Y., Wu Y., Shan Y., Qian Z., Liao J. Graphene-nanoparticle-based self-healing hydrogel in preventing postoperative recurrence of breast cancer. ACS Biomater. Sci. Eng. 2019;5:768–779. doi: 10.1021/acsbiomaterials.8b01475. PubMed DOI

Raphey V.R., Henna T.K., Nivitha K.P., Mufeedha P., Sabu C., Pramod K. Advanced biomedical applications of carbon nanotube. Mater. Sci. Eng. C. 2019;100:616–630. doi: 10.1016/j.msec.2019.03.043. PubMed DOI

Gonzalez-Carter D., Goode A.E., Kiryushko D., Masuda S., Hu S., Lopes-Rodrigues R., Dexter D.T., Shaffer M.S.P., Porter A.E. Quantification of blood–brain barrier transport and neuronal toxicity of unlabelled multiwalled carbon nanotubes as a function of surface charge. Nanoscale. 2019;11:22054–22069. doi: 10.1039/C9NR02866H. PubMed DOI

Yang K., Gong H., Shi X., Wan J., Zhang Y., Liu Z. In vivo biodistribution and toxicology of functionalized nano-graphene oxide in mice after oral and intraperitoneal administration. Biomaterials. 2013;34:2787–2795. doi: 10.1016/j.biomaterials.2013.01.001. PubMed DOI

Li J., Zhang X., Jiang J., Wang Y., Jiang H., Zhang J., Nie X., Liu B. Systematic assessment of the toxicity and potential mechanism of graphene derivatives in vitro and in vivo. Toxicol. Sci. 2019;167:269–281. doi: 10.1093/toxsci/kfy235. PubMed DOI

Barosova H., Karakocak B.B., Septiadi D., Petri-Fink A., Stone V., Rothen-Rutishauser B. An in vitro lung system to assess the proinflammatory hazard of carbon nanotube aerosols. Int. J. Mol. Sci. 2020;21:5335. doi: 10.3390/ijms21155335. PubMed DOI PMC

Yuan X., Zhang X., Sun L., Wei Y., Wei X. Cellular toxicity and immunological effects of carbon-based nanomaterials. Part. Fibre Toxicol. 2019;16:18. doi: 10.1186/s12989-019-0299-z. PubMed DOI PMC

Ghanbari F., Nasarzadeh P., Seydi E., Ghasemi A., Taghi Joghataei M., Ashtari K., Akbari M. Mitochondrial oxidative stress and dysfunction induced by single- and multiwall carbon nanotubes: A comparative study. J. Biomed. Mater. Res. Part A. 2017;105:2047–2055. doi: 10.1002/jbm.a.36063. PubMed DOI

Wan B., Wang Z.X., Lv Q.Y., Dong P.X., Zhao L.X., Yang Y., Guo L.H. Single-walled carbon nanotubes and graphene oxides induce autophagosome accumulation and lysosome impairment in primarily cultured murine peritoneal macrophages. Toxicol. Lett. 2013;221:118–127. doi: 10.1016/j.toxlet.2013.06.208. PubMed DOI

Svadlakova T., Hubatka F., Turanek Knotigova P., Kulich P., Masek J., Kotoucek J., Macak J., Motola M., Kalbac M., Kolackova M., et al. Proinflammatory effect of carbon-based nanomaterials: In vitro study on stimulation of inflammasome NLRP3 via destabilisation of lysosomes. Nanomaterials. 2020;10:418. doi: 10.3390/nano10030418. PubMed DOI PMC

Drasler B., Kucki M., Delhaes F., Buerki-Thurnherr T., Vanhecke D., Korejwo D., Chortarea S., Barosova H., Hirsch C., Petri-Fink A., et al. Single exposure to aerosolized graphene oxide and graphene nanoplatelets did not initiate an acute biological response in a 3D human lung model. Carbon. 2018;137:125–135. doi: 10.1016/j.carbon.2018.05.012. DOI

Park E.J., Lee S.J., Lee K., Choi Y.C., Lee B.S., Lee G.H., Kim D.W. Pulmonary persistence of graphene nanoplatelets may disturb physiological and immunological homeostasis. J. Appl. Toxicol. 2017;37:296–309. doi: 10.1002/jat.3361. PubMed DOI

Jaworski S., Sawosz E., Grodzik M., Winnicka A., Prasek M., Wierzbicki M., Chwalibog A. In vitro evaluation of the effects of graphene platelets on glioblastoma multiforme cells. Int. J. Nanomed. 2013;8:413–420. PubMed PMC

Malanagahalli S., Murera D., Martín C., Lin H., Wadier N., Dumortier H., Vázquez E., Bianco A. Few layer graphene does not affect cellular homeostasis of mouse macrophages. Nanomaterials. 2020;10:228. doi: 10.3390/nano10020228. PubMed DOI PMC

Mao L., Hu M., Pan B., Xie Y., Petersen E.J. Biodistribution and toxicity of radio-labeled few layer graphene in mice after intratracheal instillation. Part. Fibre Toxicol. 2016;13:7. doi: 10.1186/s12989-016-0120-1. PubMed DOI PMC

Sasidharan A., Swaroop S., Koduri C.K., Girish C.M., Chandran P., Panchakarla L.S., Somasundaram V.H., Gowd G.S., Nair S., Koyakutty M. Comparative in vivo toxicity, organ biodistribution and immune response of pristine, carboxylated and PEGylated few-layer graphene sheets in Swiss albino mice: A three month study. Carbon. 2015;95:511–524. doi: 10.1016/j.carbon.2015.08.074. DOI

Jacobsen N.R., Møller P., Clausen P.A., Saber A.T., Micheletti C., Jensen K.A., Wallin H., Vogel U. Biodistribution of carbon nanotubes in animal models. Basic Clin. Pharmacol. Toxicol. 2017;121:30–43. doi: 10.1111/bcpt.12705. PubMed DOI

Cao Y., Luo Y. Pharmacological and toxicological aspects of carbon nanotubes (CNTs) to vascular system: A review. Toxicol. Appl. Pharmacol. 2019;385:114801. doi: 10.1016/j.taap.2019.114801. PubMed DOI

Tadyszak K., Wychowaniec J.K., Litowczenko J. Biomedical applications of graphene-based structures. Nanomaterials. 2018;8:944. doi: 10.3390/nano8110944. PubMed DOI PMC

Dale D.C., Boxer L., Liles W.C. The phagocytes: Neutrophils and monocytes. Blood. 2008;112:935–945. doi: 10.1182/blood-2007-12-077917. PubMed DOI

Meunier E., Coste A., Olagnier D., Authier H., Lefevre L., Dardenne C., Bernad J., Beraud M., Flahaut E., Pipy B. Double-walled carbon nanotubes trigger IL-1beta release in human monocytes through Nlrp3 inflammasome activation. Nanomedicine. 2012;8:987–995. doi: 10.1016/j.nano.2011.11.004. PubMed DOI

Delogu L.G., Venturelli E., Manetti R., Pinna G.A., Carru C., Madeddu R., Murgia L., Sgarrella F., Dumortier H., Bianco A. Ex vivo impact of functionalized carbon nanotubes on human immune cells. Nanomedicine. 2012;7:231–243. doi: 10.2217/nnm.11.101. PubMed DOI

David C.A.W., Barrow M., Murray P., Rosseinsky M.J., Owen A., Liptrott N.J. In vitro determination of the immunogenic impact of nanomaterials on primary peripheral blood mononuclear cells. Int. J. Mol. Sci. 2020;21:5610. doi: 10.3390/ijms21165610. PubMed DOI PMC

Grosse S., Stenvik J., Nilsen A.M. Iron oxide nanoparticles modulate lipopolysaccharide-induced inflammatory responses in primary human monocytes. Int. J. Nanomed. 2016;11:4625–4642. doi: 10.2147/IJN.S113425. PubMed DOI PMC

Laverny G., Casset A., Purohit A., Schaeffer E., Spiegelhalter C., de Blay F., Pons F. Immunomodulatory properties of multi-walled carbon nanotubes in peripheral blood mononuclear cells from healthy subjects and allergic patients. Toxicol. Lett. 2013;217:91–101. doi: 10.1016/j.toxlet.2012.12.008. PubMed DOI

Lebre F., Boland J.B., Gouveia P., Gorman A.L., Lundahl M.L.E., Lynch R.I., O’Brien F.J., Coleman J., Lavelle E.C. Pristine graphene induces innate immune training. Nanoscale. 2020;12:11192–11200. doi: 10.1039/C9NR09661B. PubMed DOI

Kinaret P.A.S., Scala G., Federico A., Sund J., Greco D. Carbon nanomaterials promote M1/M2 macrophage activation. Small. 2020;16:1907609. doi: 10.1002/smll.201907609. PubMed DOI

Öner D., Moisse M., Ghosh M., Duca R.C., Poels K., Luyts K., Putzeys E., Cokic S.M., Van Landuyt K., Vanoirbeek J., et al. Epigenetic effects of carbon nanotubes in human monocytic cells. Mutagenesis. 2017;32:181–191. doi: 10.1093/mutage/gew053. PubMed DOI

Yan J., Chen L., Huang C.-C., Lung S.-C.C., Yang L., Wang W.-C., Lin P.-H., Suo G., Lin C.-H. Consecutive evaluation of graphene oxide and reduced graphene oxide nanoplatelets immunotoxicity on monocytes. Colloids Surf. B Biointerfaces. 2017;153:300–309. doi: 10.1016/j.colsurfb.2017.02.036. PubMed DOI

Farrera C., Fadeel B. It takes two to tango: Understanding the interactions between engineered nanomaterials and the immune system. Eur. J. Pharm. Biopharm. 2015;95:3–12. doi: 10.1016/j.ejpb.2015.03.007. PubMed DOI

Knötigová P.T., Mašek J., Hubatka F., Kotouček J., Kulich P., Šimečková P., Bartheldyová E., Machala M., Švadláková T., Krejsek J., et al. Application of advanced microscopic methods to study the interaction of carboxylated fluorescent nanodiamonds with membrane structures in THP-1 cells: Activation of inflammasome NLRP3 as the result of lysosome destabilization. Mol. Pharm. 2019;16:3441–3451. doi: 10.1021/acs.molpharmaceut.9b00225. PubMed DOI

Brown D.M., Kinloch I.A., Bangert U., Windle A.H., Walter D.M., Walker G.S., Scotchford C.A., Donaldson K., Stone V. An in vitro study of the potential of carbon nanotubes and nanofibres to induce inflammatory mediators and frustrated phagocytosis. Carbon. 2007;45:1743–1756. doi: 10.1016/j.carbon.2007.05.011. DOI

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. Healthc. Mater. 2018;7:1700815. doi: 10.1002/adhm.201700815. PubMed DOI

Sun B., Wang X., Ji Z., Wang M., Liao Y.-P., Chang C.H., Li R., Zhang H., Nel A.E., Xia T. NADPH oxidase-dependent NLRP3 inflammasome activation and its important role in lung fibrosis by multiwalled carbon nanotubes. Small. 2015;11:2087–2097. doi: 10.1002/smll.201402859. PubMed DOI PMC

Katsumiti A., Tomovska R., Cajaraville M.P. Intracellular localization and toxicity of graphene oxide and reduced graphene oxide nanoplatelets to mussel hemocytes in vitro. Aquat. Toxicol. 2017;188:138–147. doi: 10.1016/j.aquatox.2017.04.016. PubMed DOI

Kim J.K., Shin J.H., Lee J.S., Hwang J.H., Lee J.H., Baek J.E., Kim T.G., Kim B.W., Kim J.S., Lee G.H., et al. 28-Day inhalation toxicity of graphene nanoplatelets in Sprague-Dawley rats. Nanotoxicology. 2016;10:891–901. doi: 10.3109/17435390.2015.1133865. PubMed DOI

Schinwald A., Murphy F., Askounis A., Koutsos V., Sefiane K., Donaldson K., Campbell C.J. Minimal oxidation and inflammogenicity of pristine graphene with residence in the lung. Nanotoxicology. 2014;8:824–832. doi: 10.3109/17435390.2013.831502. PubMed DOI

Schinwald A., Murphy F.A., Jones A., MacNee W., Donaldson K. Graphene-based nanoplatelets: A new risk to the respiratory system as a consequence of their unusual aerodynamic properties. ACS Nano. 2012;6:736–746. doi: 10.1021/nn204229f. PubMed DOI

Vallhov H., Qin J., Johansson S.M., Ahlborg N., Muhammed M.A., Scheynius A., Gabrielsson S. The importance of an endotoxin-free environment during the production of nanoparticles used in medical applications. Nano Lett. 2006;6:1682–1686. doi: 10.1021/nl060860z. PubMed DOI

Oostingh G.J., Casals E., Italiani P., Colognato R., Stritzinger R., Ponti J., Pfaller T., Kohl Y., Ooms D., Favilli F., et al. Problems and challenges in the development and validation of human cell-based assays to determine nanoparticle-induced immunomodulatory effects. Part. Fibre Toxicol. 2011;8:8. doi: 10.1186/1743-8977-8-8. PubMed DOI PMC

Smulders S., Kaiser J.P., Zuin S., Van Landuyt K.L., Golanski L., Vanoirbeek J., Wick P., Hoet P.H. Contamination of nanoparticles by endotoxin: Evaluation of different test methods. Part. Fibre Toxicol. 2012;9:41. doi: 10.1186/1743-8977-9-41. PubMed DOI PMC

Pellegrini C., Antonioli L., Lopez-Castejon G., Blandizzi C., Fornai M. Canonical and non-canonical activation of NLRP3 inflammasome at the crossroad between immune tolerance and intestinal inflammation. Front. Immunol. 2017;8:36. doi: 10.3389/fimmu.2017.00036. PubMed DOI PMC

Sun B., Wang X., Ji Z., Li R., Xia T. NLRP3 inflammasome activation induced by engineered nanomaterials. Small. 2013;9:1595–1607. doi: 10.1002/smll.201201962. PubMed DOI PMC

Yimin, Kohanawa M. A regulatory effect of the balance between TNF-α and IL-6 in the granulomatous and inflammatory response to Rhodococcus aurantiacus infection in mice. J. Immunol. 2006;177:642–650. doi: 10.4049/jimmunol.177.1.642. PubMed DOI

Mukherjee S.P., Bottini M., Fadeel B. Graphene and the Immune System: A romance of many dimensions. Front. Immunol. 2017;8:673. doi: 10.3389/fimmu.2017.00673. PubMed DOI PMC

Li Y., Yuan H., von dem Bussche A., Creighton M., Hurt R.H., Kane A.B., Gao H. Graphene microsheets enter cells through spontaneous membrane penetration at edge asperities and corner sites. Proc. Natl. Acad. Sci. USA. 2013;110:12295–12300. doi: 10.1073/pnas.1222276110. PubMed DOI PMC

Park E.-J., Lee G.-H., Han B.S., Lee B.-S., Lee S., Cho M.-H., Kim J.-H., Kim D.-W. Toxic response of graphene nanoplatelets in vivo and in vitro. Arch. Toxicol. 2015;89:1557–1568. doi: 10.1007/s00204-014-1303-x. PubMed DOI

Di Cristo L., Mc Carthy S., Paton K., Movia D., Prina-Mello A. Interplay between oxidative stress and endoplasmic reticulum stress mediated- autophagy in unfunctionalised few-layer graphene-exposed macrophages. 2D Mater. 2018;5:045033. doi: 10.1088/2053-1583/aadf45. DOI

Boyles M.S., Young L., Brown D.M., MacCalman L., Cowie H., Moisala A., Smail F., Smith P.J., Proudfoot L., Windle A.H., et al. Multi-walled carbon nanotube induced frustrated phagocytosis, cytotoxicity and pro-inflammatory conditions in macrophages are length dependent and greater than that of asbestos. Toxicol. Vitr. 2015;29:1513–1528. doi: 10.1016/j.tiv.2015.06.012. PubMed DOI

Moujaber O., Stochaj U. The cytoskeleton as regulator of cell signaling pathways. Trends Biochem. Sci. 2020;45:96–107. doi: 10.1016/j.tibs.2019.11.003. PubMed DOI

Hohmann T., Dehghani F. The cytoskeleton-a complex interacting meshwork. Cells. 2019;8:362. doi: 10.3390/cells8040362. PubMed DOI PMC

Bekkering S., Blok B.A., Joosten L.A., Riksen N.P., van Crevel R., Netea M.G. In vitro experimental model of trained innate immunity in human primary monocytes. Clin. Vaccine Immunol. 2016;23:926–933. doi: 10.1128/CVI.00349-16. PubMed DOI PMC

Cheng S.C., Quintin J., Cramer R.A., Shepardson K.M., Saeed S., Kumar V., Giamarellos-Bourboulis E.J., Martens J.H., Rao N.A., Aghajanirefah A., et al. mTOR- and HIF-1α-mediated aerobic glycolysis as metabolic basis for trained immunity. Science. 2014;345:1250684. doi: 10.1126/science.1250684. PubMed DOI PMC

Zhang Y., Morgan M.J., Chen K., Choksi S., Liu Z.G. Induction of autophagy is essential for monocyte-macrophage differentiation. Blood. 2012;119:2895–2905. doi: 10.1182/blood-2011-08-372383. PubMed DOI PMC

Murray P.J., Allen J.E., Biswas S.K., Fisher E.A., Gilroy D.W., Goerdt S., Gordon S., Hamilton J.A., Ivashkiv L.B., Lawrence T., et al. Macrophage activation and polarization: Nomenclature and experimental guidelines. Immunity. 2014;41:14–20. doi: 10.1016/j.immuni.2014.06.008. PubMed DOI PMC

Perrotta C., Cattaneo M.G., Molteni R., De Palma C. Autophagy in the regulation of tissue differentiation and homeostasis. Front. Cell Dev. Biol. 2020;8:1563. doi: 10.3389/fcell.2020.602901. PubMed DOI PMC

Clarke A.J., Simon A.K. Autophagy in the renewal, differentiation and homeostasis of immune cells. Nat. Rev. Immunol. 2019;19:170–183. doi: 10.1038/s41577-018-0095-2. PubMed DOI

Zhong C., Yang X., Feng Y., Yu J. Trained immunity: An underlying driver of inflammatory atherosclerosis. Front. Immunol. 2020;11:284. doi: 10.3389/fimmu.2020.00284. PubMed DOI PMC

Kobayashi M., Usui F., Karasawa T., Kawashima A., Kimura H., Mizushina Y., Shirasuna K., Mizukami H., Kasahara T., Hasebe N., et al. NLRP3 deficiency reduces macrophage interleukin-10 production and enhances the susceptibility to doxorubicin-induced cardiotoxicity. Sci. Rep. 2016;6:26489. doi: 10.1038/srep26489. PubMed DOI PMC

Sun Y., Ma J., Li D., Li P., Zhou X., Li Y., He Z., Qin L., Liang L., Luo X. Interleukin-10 inhibits interleukin-1β production and inflammasome activation of microglia in epileptic seizures. J. Neuroinflamm. 2019;16:66. doi: 10.1186/s12974-019-1452-1. PubMed DOI PMC

Butcher S.K., O’Carroll C.E., Wells C.A., Carmody R.J. Toll-like receptors drive specific patterns of tolerance and training on restimulation of macrophages. Front. Immunol. 2018;9:933. doi: 10.3389/fimmu.2018.00933. PubMed DOI PMC

Kwiecień I., Polubiec-Kownacka M., Dziedzic D., Wołosz D., Rzepecki P., Domagała-Kulawik J. CD163 and CCR7 as markers for macrophage polarization in lung cancer microenvironment. Cent.-Eur. J. Immunol. 2019;44:395–402. doi: 10.5114/ceji.2019.92795. PubMed DOI PMC

Tian X., Yang Z., Duan G., Wu A., Gu Z., Zhang L., Chen C., Chai Z., Ge C., Zhou R. Graphene oxide nanosheets retard cellular migration via disruption of actin cytoskeleton. Small. 2017;13:1602133. doi: 10.1002/smll.201602133. PubMed DOI

Wang J., Wang P., He Y., Liu X., Wang S., Ma C., Tian X., Wang J., Wu X. Graphene oxide inhibits cell migration and invasion by destroying actin cytoskeleton in cervical cancer cells. Aging. 2020;12:17625–17633. doi: 10.18632/aging.103821. PubMed DOI PMC

Malkova A., Svadlakova T., Singh A., Kolackova M., Vankova R., Borsky P., Holmannova D., Karas A., Borska L., Fiala Z. In vitro assessment of the genotoxic potential of pristine graphene platelets. Nanomaterials. 2021;11:2210. doi: 10.3390/nano11092210. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...