Density of surface charge is a more predictive factor of the toxicity of cationic carbon nanoparticles than zeta potential.
Carbon dots
Charge
Lung
Nanoparticle
Surface chemistry
Toxicity
Journal
Journal of nanobiotechnology
ISSN: 1477-3155
Titre abrégé: J Nanobiotechnology
Pays: England
ID NLM: 101152208
Informations de publication
Date de publication:
06 Jan 2021
06 Jan 2021
Historique:
received:
11
09
2020
accepted:
04
12
2020
entrez:
7
1
2021
pubmed:
8
1
2021
medline:
8
9
2021
Statut:
epublish
Résumé
A positive surface charge has been largely associated with nanoparticle (NP) toxicity. However, by screening a carbon NP library in macrophages, we found that a cationic charge does not systematically translate into toxicity. To get deeper insight into this, we carried out a comprehensive study on 5 cationic carbon NPs (NP2 to NP6) exhibiting a similar zeta (ζ) potential value (from + 20.6 to + 26.9 mV) but displaying an increasing surface charge density (electrokinetic charge, Q The 5 cationic NPs induced high (NP6 and NP5, Q Thus, this study clearly reveals that the surface charge density of a cationic carbon NP rather than the absolute value of its ζ-potential is a relevant descriptor of its in vitro and in vivo toxicity.
Sections du résumé
BACKGROUND
BACKGROUND
A positive surface charge has been largely associated with nanoparticle (NP) toxicity. However, by screening a carbon NP library in macrophages, we found that a cationic charge does not systematically translate into toxicity. To get deeper insight into this, we carried out a comprehensive study on 5 cationic carbon NPs (NP2 to NP6) exhibiting a similar zeta (ζ) potential value (from + 20.6 to + 26.9 mV) but displaying an increasing surface charge density (electrokinetic charge, Q
RESULTS
RESULTS
The 5 cationic NPs induced high (NP6 and NP5, Q
CONCLUSIONS
CONCLUSIONS
Thus, this study clearly reveals that the surface charge density of a cationic carbon NP rather than the absolute value of its ζ-potential is a relevant descriptor of its in vitro and in vivo toxicity.
Identifiants
pubmed: 33407567
doi: 10.1186/s12951-020-00747-7
pii: 10.1186/s12951-020-00747-7
pmc: PMC7789233
doi:
Substances chimiques
Cations
0
Cytokines
0
Carbon
7440-44-0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
5Subventions
Organisme : Agence Nationale de Sécurité Sanitaire de l'Alimentation, de l'Environnement et du Travail
ID : EST-2015/1/005
Références
Kessler R. Engineered nanoparticles in consumer products: understanding a new ingredient. Environ Health Perspect. 2011;119:a120–5.
pubmed: 21356630
pmcid: 3060016
Vance ME, Kuiken T, Vejerano EP, McGinnis SP, Hochella MF Jr, Rejeski D, et al. Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory. Beilstein J Nanotechnol. 2015;6:1769–80.
pubmed: 26425429
pmcid: 4578396
Oberdorster G, Oberdorster E, Oberdorster J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect. 2005;113:823–39.
pubmed: 16002369
pmcid: 1257642
Sharifi S, Behzadi S, Laurent S, Forrest ML, Stroeve P, Mahmoudi M. Toxicity of nanomaterials. Chem Soc Rev. 2012;41:2323–43.
pubmed: 22170510
Lanone S, Rogerieux F, Geys J, Dupont A, Maillot-Marechal E, Boczkowski J, et al. Comparative toxicity of 24 manufactured nanoparticles in human alveolar epithelial and macrophage cell lines. Part Fibre Toxicol. 2009;6:14.
pubmed: 19405955
pmcid: 2685765
Guadagnini R, Moreau K, Hussain S, Marano F, Boland S. Toxicity evaluation of engineered nanoparticles for medical applications using pulmonary epithelial cells. Nanotoxicology. 2015;9(Suppl 1):25–32.
pubmed: 24286383
Kaewamatawong T, Kawamura N, Okajima M, Sawada M, Morita T, Shimada A. Acute pulmonary toxicity caused by exposure to colloidal silica: particle size dependent pathological changes in mice. Toxicol Pathol. 2005;33:743–9.
pubmed: 16306027
Muller J, Huaux F, Moreau N, Misson P, Heilier JF, Delos M, et al. Respiratory toxicity of multi-wall carbon nanotubes. Toxicol Appl Pharmacol. 2005;207:221–31.
pubmed: 16129115
Hussain S, Boland S, Baeza-Squiban A, Hamel R, Thomassen LCJ, Martens JA, et al. Oxidative stress and proinflammatory effects of carbon black and titanium dioxide nanoparticles: role of particle surface area and internalized amount. Toxicology. 2009;260:142–9.
pubmed: 19464580
Park EJ, Cho WS, Jeong J, Yi J, Choi K, Park K. Pro-inflammatory and potential allergic responses resulting from B cell activation in mice treated with multi-walled carbon nanotubes by intratracheal instillation. Toxicology. 2009;259:113–21.
pubmed: 19428951
Yazdi AS, Guarda G, Riteau N, Drexler SK, Tardivel A, Couillin I, et al. Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1 alpha and IL-1 beta. PNAS. 2010;107:19449–54.
pubmed: 20974980
Ronzani C, Spiegelhalter C, Vonesch JL, Lebeau L, Pons F. Lung deposition and toxicological responses evoked by multi-walled carbon nanotubes dispersed in a synthetic lung surfactant in the mouse. Arch Toxicol. 2012;86:137–49.
pubmed: 21805258
de Haar C, Hassing I, Bol M, Bleumink R, Pieters R. Ultrafine carbon black particles cause early airway inflammation and have adjuvant activity in a mouse allergic airway disease model. Toxicol Sci. 2005;87:409–18.
pubmed: 16014737
Ryman-Rasmussen JP, Tewksbury EW, Moss OR, Cesta MF, Wong BA, Bonner JC. Inhaled multiwalled carbon nanotubes potentiate airway fibrosis in murine allergic asthma. Am J Respir Cell Mol Biol. 2009;40:349–58.
pubmed: 18787175
Inoue K, Yanagisawa R, Koike E, Nishikawa M, Takano H. Repeated pulmonary exposure to single-walled carbon nanotubes exacerbates allergic inflammation of the airway: possible role of oxidative stress. Free Radical Biol Med. 2010;48:924–34.
Hussain S, Vanoirbeek JAJ, Luyts K, De Vooght V, Verbeken E, Thomassen LCJ, et al. Lung exposure to nanoparticles modulates an asthmatic response in a mouse model. Eur Respir J. 2011;37:299–309.
pubmed: 20530043
Brandenberger C, Rowley NL, Jackson-Humbles DN, Zhang Q, Bramble LA, Lewandowski RP, et al. Engineered silica nanoparticles act as adjuvants to enhance allergic airway disease in mice. Part Fibre Toxicol. 2013;10:26.
pubmed: 23815813
pmcid: 3729411
Chuang HC, Hsiao TC, Wu CK, Chang HH, Lee CH, Chang CC, et al. Allergenicity and toxicology of inhaled silver nanoparticles in allergen-provocation mice models. Int J Nanomedicine. 2013;8:4495–506.
pubmed: 24285922
pmcid: 3841295
Ronzani C, Casset A, Pons F. Exposure to multi-walled carbon nanotubes results in aggravation of airway inflammation and remodeling and in increased production of epithelium-derived innate cytokines in a mouse model of asthma. Arch Toxicol. 2014;88:489–99.
pubmed: 23948970
Luyts K, Napierska D, Nemery B, Hoet PHM. How physico-chemical characteristics of nanoparticles cause their toxicity: complex and unresolved interrelations. Environ Sci Process Impacts. 2013;15:23–38.
pubmed: 24592425
Braakhuis HM, Park MVDZ, Gosens I, De Jong WH, Cassee FR. Physicochemical characteristics of nanomaterials that affect pulmonary inflammation. Part Fibre Toxicol. 2014;11:5.
Lundqvist M, Stigler J, Elia G, Lynch I, Cedervall T, Dawson KA. Nanoparticle size and surface properties determine the protein corona with possible implications for biological impacts. PNAS. 2008;105:14265–70.
pubmed: 18809927
Monopoli MP, Walczyk D, Campbell A, Elia G, Lynch I, Baldelli Bombelli F, et al. Physical–chemical aspects of protein corona: relevance to in vitro and in vivo biological impacts of nanoparticles. J Amer Chem Soc. 2011;133:2525–34.
Frohlich E. The role of surface charge in cellular uptake and cytotoxicity of medical nanoparticles. Int J Nanomedicine. 2012;7:5577–91.
pubmed: 23144561
pmcid: 3493258
Nagy A, Steinbruck A, Gao J, Doggett N, Hollingsworth JA, Iyer R. Comprehensive analysis of the effects of CdSe quantum dot size, surface charge, and functionalization on primary human lung cells. Acs Nano. 2012;6:4748–62.
pubmed: 22587339
Li RB, Wang X, Ji ZX, Sun BB, Zhang HY, Chang CH, et al. Surface charge and cellular processing of covalently functionalized multiwall carbon nanotubes determine pulmonary toxicity. Acs Nano. 2013;7:2352–68.
pubmed: 23414138
pmcid: 4012619
Shahbazi MA, Hamidi M, Makila EM, Zhang HB, Almeida PV, Kaasalainen M, et al. The mechanisms of surface chemistry effects of mesoporous silicon nanoparticles on immunotoxicity and biocompatibility. Biomaterials. 2013;34:7776–89.
pubmed: 23866976
Cho WS, Thielbeer F, Duffin R, Johansson EM, Megson IL, MacNee W, et al. Surface functionalization affects the zeta potential, coronal stability and membranolytic activity of polymeric nanoparticles. Nanotoxicology. 2014;8:202–11.
pubmed: 23379633
Kim J, Chankeshwara SV, Thielbeer F, Jeong J, Donaldson K, Bradley M, et al. Surface charge determines the lung inflammogenicity: a study with polystyrene nanoparticles. Nanotoxicology. 2016;10:94–101.
pubmed: 25946036
Mahmoudi M, Lynch I, Ejtehadi MR, Monopoli MP, Bombelli FB, Laurent S. Protein-nanoparticle interactions: opportunities and challenges. Chem Rev. 2011;111:5610–37.
pubmed: 21688848
Liu Q, Li H, Xia Q, Liu Y, Xiao K. Role of surface charge in determining the biological effects of CdSe/ZnS quantum dots. Int J Nanomedicine. 2015;10:7073–88.
pubmed: 26604757
pmcid: 4655958
Usman M, Zaheer Y, Younis MR, Demirdogen RE, Hussain SZ, Sarwar Y, et al. The effect of surface charge on cellular uptake and inflammatory behavior of carbon dots. Colloid Interfac Sci. 2020;35:12.
Fan J, Claudel M, Ronzani C, Arezki Y, Lebeau L, Pons F. Physicochemical characteristics that affect carbon dot safety: Lessons from a comprehensive study on a nanoparticle library. Int J Pharm. 2019;569:118521.
pubmed: 31323371
Havrdova M, Hola K, Skopalik J, Tomankova K, Martin PA, Cepe K, et al. Toxicity of carbon dots - Effect of surface functionalization on the cell viability, reactive oxygen species generation and cell cycle. Carbon. 2016;99:238–48.
Himaja AL, Karthik PS, Singh SP. Carbon Dots: The newest member of the carbon nanomaterials family. Chem Rec. 2015;15:595–615.
pubmed: 25755070
Sharma A, Das J. Small molecules derived carbon dots: synthesis and applications in sensing, catalysis, imaging, and biomedicine. J Nanobiotechnology. 2019;17:92.
pubmed: 31451110
pmcid: 6709552
Kwon W, Lee G, Do S, Joo T, Rhee SW. Size-controlled soft-template synthesis of carbon nanodots toward versatile photoactive materials. Small. 2014;10:506–13.
pubmed: 24014253
Xia J, Chen S, Zou GY, Yu YL, Wang JH. Synthesis of highly stable red-emissive carbon polymer dots by modulated polymerization: from the mechanism to application in intracellular pH imaging. Nanoscale. 2018;10:22484–92.
pubmed: 30480294
Pierrat P, Wang R, Kereselidze D, Lux M, Didier P, Kichler A, et al. Efficient in vitro and in vivo pulmonary delivery of nucleic acid by carbon dot-based nanocarriers. Biomaterials. 2015;51:290–302.
pubmed: 25771019
Edison TNJI, Atchudan R, Sethuraman MG, Shim JJ, Lee YR. Microwave assisted green synthesis of fluorescent N-doped carbon dots: cytotoxicity and bio-imaging applications. J Photochem Photobiol B. 2016;161:154–61.
pubmed: 27236237
Gomez IJ, Arnaiz B, Cacioppo M, Arcudi F, Prato M. Nitrogen-doped carbon nanodots for bioimaging and delivery of paclitaxel. J Mat Chem B. 2018;6:10.
Bao X, Yuan Y, Chen J, Zhang B, Li D, Zhou D, et al. In vivo theranostics with near-infrared-emitting carbon dots-highly efficient photothermal therapy based on passive targeting after intravenous administration. Light Sci Appl. 2018;7:91.
pubmed: 30479757
pmcid: 6249234
Claudel M, Fan J, Rapp M, Pons F, Lebeau L. Influence of carbonization conditions on luminescence and gene delivery properties of nitrogen-doped carbon dots. RSC Adv. 2019;9:3493.
Abuchowski A, Vanes T, Palczuk NC, Davis FF. Alteration of immunological properties of bovine serum-albumin by covalent attachment of polyethylene-glycol. J Biol Chem. 1977;252:3578–81.
pubmed: 405385
Stark WJ. Nanoparticles in biological systems. Angew Chem Int Ed. 2011;50:1242–58.
Marano F, Hussain S, Rodrigues-Lima F, Baeza-Squiban A, Boland S. Nanoparticles: molecular targets and cell signalling. Arch Toxicol. 2011;85:733–41.
pubmed: 20502881
Madl AK, Plummer LE, Carosino C, Pinkerton KE. Nanoparticles, lung injury, and the role of oxidant stress. Annu Rev Physiol. 2014;76:447–65.
pubmed: 24215442
Ronzani C, Van Belle C, Didier P, Spiegelhalter C, Pierrat P, Lebeau L, et al. Lysosome mediates toxicological effects of polyethyleneimine-based cationic carbon dots. J Nanopart Res. 2019;21:4.
Clift MJ, Gehr P, Rothen-Rutishauser B. Nanotoxicology: a perspective and discussion of whether or not in vitro testing is a valid alternative. Arch Toxicol. 2011;85:723–31.
pubmed: 20499226
Anderson JO, Thundiyil JG, Stolbach A. Clearing the air: a review of the effects of particulate matter air pollution on human health. J Med Toxicol. 2012;8:166–75.
pubmed: 22194192
Wang R, Lu KQ, Tang ZR, Xu YJ. Recent progress in carbon quantum dots: synthesis, properties and applications in photocatalysis. J Mater Chem A. 2017;5:3717–34.
Yao BW, Huang H, Liu Y, Kang ZH. Carbon dots: a small conundrum. Trends Chem. 2019;1:235–46.
Xia CL, Zhu SJ, Feng TL, Yang MX, Yang B. Evolution and synthesis of carbon dots: from carbon dots to carbonized polymer dots. Adv Sci. 2019;190:1316.
Tian XT, Yin XB. Carbon dots, unconventional preparation strategies, and applications beyond photoluminescence. Small. 2019;15:30.
de Medeiros TV, Manioudakis J, Noun F, Macairan JR, Victoria F, Naccache R. Microwave-assisted synthesis of carbon dots and their applications. J Mater Chem C. 2019;7:7175–95.
Fytianos K, Drasler B, Blank F, von Garnier C, Seydoux E, Rodriguez-Lorenzo L, et al. Current in vitro approaches to assess nanoparticle interactions with lung cells. Nanomedicine. 2016;11:2457–69.
pubmed: 27529369
Foldbjerg R, Wang J, Beer C, Thorsen K, Sutherland DS, Autrup H. Biological effects induced by BSA-stabilized silica nanoparticles in mammalian cell lines. Chem Biol Interact. 2013;204:28–38.
pubmed: 23623845
Breznan D, Das DD, O’Brien JS, MacKinnon-Roy C, Nimesh S, Vuong NQ, et al. Differential cytotoxic and inflammatory potency of amorphous silicon dioxide nanoparticles of similar size in multiple cell lines. Nanotoxicology. 2017;11:223–35.
pubmed: 28142331
Mura S, Hillaireau H, Nicolas J, Kerdine-Romer S, Le Droumaguet B, Delomenie C, et al. Biodegradable nanoparticles meet the bronchial airway barrier: how surface properties affect their interaction with mucus and epithelial cells. Biomacromol. 2011;12:4136–43.
Foster KA, Yazdanian M, Audus KL. Microparticulate uptake mechanisms of in-vitro cell culture models of the respiratory epithelium. J Pharm Pharmacol. 2001;53:57–66.
pubmed: 11206193
Paget V, Dekali S, Kortulewski T, Grall R, Gamez C, Blazy K, et al. Specific uptake and genotoxicity induced by polystyrene nanobeads with distinct surface chemistry on human lung epithelial cells and macrophages. Plos One. 2015;10:e0123297.
pubmed: 25875304
pmcid: 4398494
Worle-Knirsch JM, Pulskamp K, Krug HF. Oops they did it again! Carbon nanotubes hoax scientists in viability assays. Nano Lett. 2006;6:1261–8.
pubmed: 16771591
Cho WS, Duffin R, Thielbeer F, Bradley M, Megson IL, Macnee W, et al. Zeta potential and solubility to toxic ions as mechanisms of lung inflammation caused by metal/metal oxide nanoparticles. Toxicol Sci. 2012;126:469–77.
pubmed: 22240982
Mura S, Hillaireau H, Nicolas J, Le Droumaguet B, Gueutin C, Zanna S, et al. Influence of surface charge on the potential toxicity of PLGA nanoparticles towards Calu-3 cells. Int J Nanomed. 2011;6:2591–605.
Schaeublin NM, Braydich-Stolle LK, Schrand AM, Miller JM, Hutchison J, Schlager JJ, et al. Surface charge of gold nanoparticles mediates mechanism of toxicity. Nanoscale. 2011;3:410–20.
pubmed: 21229159
Bhattacharjee S. DLS and zeta potential - what they are and what they are not? J Control Release. 2016;235:337–51.
pubmed: 27297779
Suh J, Paik HJ, Hwang BK. Ionization of poly(ethylenimine) and poly(allylamine) at various pH′s. Bioorg Chem. 1994;22:318–27.
Pierrat P, Lebeau L. Characterization of titratable amphiphiles in lipid membranes by fluorescence spectroscopy. Langmuir. 2015;31:12362–71.
pubmed: 26507074
Borukhov I, Andelman D, Borrega R, Cloitre M, Leibler L, Orland H. Polyelectrolyte titration: theory and experiment. J Phys Chem B. 2000;104:11027–34.
Ritz S, Schottler S, Kotman N, Baier G, Musyanovych A, Kuharev J, et al. Protein corona of nanoparticles: distinct proteins regulate the cellular uptake. Biomacromol. 2015;16:1311–21.
Collot M, Kreder R, Tatarets AL, Patsenker LD, Mely Y, Klymchenko AS. Bright fluorogenic squaraines with tuned cell entry for selective imaging of plasma membrane vs. endoplasmic reticulum. Chem Commun. 2015;51:17136–9.