, such as asthma and chronic obstructive pulmonary disease (COPD), and lung cancer, 60 on the other hand, 2013.
, , p.61, 2019.
To date, fine (i.e., PM 2.5 ) 62 and mainly ultrafine (i.e., PM 0.1 ) particles, generally corresponding to a very complex and 63 heterogeneous chemical mixtures, from natural and anthropogenic sources are reported as having 64 the greatest effects on human health, 2014. ,
, Leclercq et al, vol.69, 2006.
, To date, a great deal of effort has been done to identify some typical features of in vitro ambient PM. However, the fact that ambient PM is a complex and heterogeneous, 73 regrettably often poorly described
To this 79 end, polycyclic aromatic hydrocarbons (PAH) within fine and quasi-ultrafine particles have been 80 already identified as the major redox-active components, and subsequently, inducers of critical of 81 underlying mechanisms of toxicity. Ambient PM contains a wide variety of organic chemicals, 82 which could, directly or indirectly, through their metabolic activation, possibly participate to the 83 induction of oxidative stress and inflammation oxidative and/or pro-inflammatory events in human 84 bronchial epithelial cell models, 2010. ,
, , 2011.
, residual PM 2.involved. Hence, in this work, using a relevant normal human epithelial bronchial BEAS-102 2B cell model, we sought to better investigate: (i) the toxicological effects of both OEM 2.5-0.3 and 103 NEM 2.5-0.3 in terms of oxidative stress, autophagy and apoptosis, Further toxicological researches are therefore urgently requested to gain more knowledge , and the toxicity of non-extractable matter (NEM 2.5-0.3 , i.e
, BEAS-2B cells and all the chemical reagents were purchased from Sigma-Aldrich
All the cell culture and molecular biology reagents, dihydroethidium 112 (DHE), 6-carboxy-2',7'-dichlorodihydrofluorescein diacetate (carboxy-H2DCFDA), High 113 Capacity cDNA Reverse Transcription Kit, Taqman fast advanced Master Mix, Taqman gene 114 expression assays, Pierce? BCA Protein Assay Kit, and Single-Channel Dead Cell Apoptosis Kit 115 with Annexin V Alexa Fluor? 488 and SYTOX? Green Dyes were provided by ThermoFisher 116 scientific ,
CellTiter-Glo® Luminescent Cell Viability, Caspase Glo® 3/7 Assay, Caspase Glo®, vol.8 ,
Highly 119 Sensitive 8-OHdG Check kit was from Gentaur France SARL ,
, Nuclear 121 extract kit and TransAM® NRF2 kit were from Active Motif, MILLIPLEX® 122 MAP Human Cytokine/Chemokine Magnetic Bead Panel-Immunology Multiplex Assays were 123 from Merck-Millipore
TACS® TdT in situ -Fluorescein System and mouse monoclonal anti-human 125 actin antibody (MAB8929), Cell Signaling Technology ,
, France) provided rabbit monoclonal anti-mouse IgG, HRP-linked antibody (S7076)
, 128 rabbit polyclonal anti-human LC3-B antibody (NB100-2220), rabbit polyclonal anti-human beclin 8, pp.110-53818
, mouse monoclonal anti-human p62/SQSTM1 antibody (H00008878, pp.500-249
, M01), and goat polyclonal anti-rabbit IgG, HRP-linked antibody (NB7160)
133 and PM fraction preparation 134 Sampling site description, sampling methods for PM 2.5-0.3 and PM 0.3 , methods for the 135 determination of the physical and chemical characteristics of PM samples, and methods for the 136 preparation of PM fractions, PM sampling methods, PM physicochemical characterization, 2019. ,
, BEAS-2B cell line
, Cell culture methods have been published elsewhere, 2017.
, PM/cm 2 , 156 with DMSO ? 0.5% v/v). The ?g Eq. PM/mL unit is in relation with the mass of PM extracted and 157 the final volume of DMSO. Defined volumes of these OEM stock solutions were diluted in the 158 LHC-9 culture medium to expose BEAS-2B cells to the desired concentrations of OEM (also 159 expressed in ?g Eq. PM/cm 2 ). After 6, 24 and/or 48 h, aliquots of cell-free culture supernatants, 160 also dedicated to cytotoxicity and inflammatory endpoints, were collected and quickly frozen at -161 80°C. Adherent cells, also dedicated to for immunofluorescence labelling and flow cytometry 162 analysis, were washed twice with 1mL-aliquots of cold sterile PBS, and immediately fixed. Other 163 adherent cells, also dedicated to oxidative stress, inflammation, autophagy
, NEM 2.5-0.3 OEM 2.5-0.3 , or OEM 0.3 ) was evaluated 168 after cell exposure to increasing concentrations, Cytotoxicity of the PM fractions
, Luminescent Cell Viability, Promega)
, Oxidative stress was evaluated in BEAS-2B cells, 6 and 24 h after their incubation as controls 174 or their exposure either to PM 2, vol.10
, In addition, DNA binding activity of nuclear 176 factor erythroid 2-related factor 2 (NRF2) and the associated gene expression of NRF2, intracellular ROS (HE and carboxy-H2DCFDA)
, NAD(P)H quinone 178 dehydrogenase 1 (NQO1), and superoxide dismutase (SOD), one the one hand, and the occurrence 179 of oxidative damage to macromolecules, ECH-associated protein 1 (KEAP-1), heme oxygenase 1 (HMOX), p.8
, BEAS-2B 181 cells treated with Menadione (2.5 mM) served as positive controls. Briefly, either HE (1 ?M) or 182 carboxy-H2DCFDA (1 ?M) was added to control or exposed BEAS-2B cells and incubated at, Isop), and 8-hydroxy-2'-deoxyguanosine (8-OHdG), on the other hand, were studied
Gene expressions of HMOX, NQO1 186 and SOD were evaluated using quantitative RT-PCR. Briefly, after the total RNA isolation using 187 the RNeasy Kit (Qiagen), the reverse transcription of 1 ?g of total RNA in single-stranded cDNA 188 was performed using the High Capacity cDNA Reverse Transcription Kit. Thereafter, the relative 189 quantitation of the target gene expression was determined using specific Taqman? gene 190 expression assays, TransAM® NRF2 from Active Motif, 2018. ,
, The relative 193 change in gene expression was calculated by the ??CT method, normalized against endogenous 194 ribosomal 18S, Real-Time PCR System, and the Expression Suite Software (ThermoFisher scientific)
Oxidative DNA adduct 8-OHdG concentrations were studied using a commercially 11 197 available enzyme immunoassay (Highly Sensitive 8-OHdG Check, 2016. ,
, IL-6), were determined in cell-free culture 201 supernatants of BEAS-2B cells, Tumor necrosis factor (TNF-?) and interleukin-6, vol.6
, Cytokine/Chemokine Magnetic Bead Panel-Immunology Multiplex Assay (Merck-Millipore) 204 according to the manufacturer's instruction, 2017.
, currently described as 209 critical hallmarks of autophagosome formation, were considered to study authophagy in BEAS-210 2B cells, 24 and 48 h after their incubation as controls or their exposure either to PM 2.5-0.3 , NEM 2.5-211 0.3 OEM 2.5-0.3 , or OEM 0.3 through. BEAS-2B cells treated with Rapamycine (10 ?M) served as 212 positive controls. Protein extracts (20 ?g) were prepared from BEAS-2B cells using protease and 213 phosphatase inhibitor cocktail (Sigma-Aldrich)-supplemented RIPA lysis and extraction buffer 214 (ThermoFisher scientific), Autophagy 207 Relevant molecules including ATG5, BECN1/Beclin 1, SQSTM1/p62 protein, and 208 microtubule-associated protein 1 light chain 3 b (MAP1LC3B/LC3B)
, Novus Biologicals); mouse 219 monoclonal anti-human actin antibody (R&D Systems) overnight at 4°C, secondly for 1 h with 12 220 secondary antibodies (rabbit monoclonal anti-mouse IgG, HRP-linked antibody (Cell Signaling 221 Technology); goat polyclonal anti-rabbit IgG, HRP-linked antibody, ATG5, rabbit polyclonal anti-human LC3-B antibody, rabbit polyclonal anti-human Beclin 218 antibody, mouse monoclonal anti-human p62/SQSTM1 antibody
, Chemiluminescence was recorded by Fusion FX Spectra (Vilbert-Lourmat
, Apoptosis
BEAS-2B cells treated with Staurosporine 231 (1 µM) served as positive controls, BEAS-2B cells were studied 232 using commercially available luminescent assays (i.e., CellTiter-Glo® Luminescent Cell Viability, vol.9 ,
, Caspase Glo® 8 Assay, and Caspase Glo® 9 Assay, Promega) according 234 to the manufacturer's recommendations (Leclercq et al, TACS® TdT in situ -Fluorescein, 2018.
, System (R&D systems), a classic TUNEL assay, was used according to the manufacturer's 236 recommendations before cell observation using an EVOS® FL Cell Imaging System 237 (ThermoFisher scientific), Single-Channel Dead Cell Apoptosis Kit with Annexin V Alexa
, ThermoFisher scientific), based on 5-ethynyl-2'-deoxyuridine (EdU) as a nucleoside analog to 244 thymidine and to be incorporated into DNA during active DNA synthesis, was used to measure 245 the cell ability to proliferate as a fundamental method for assessing cell health. Detection is based 246 on a click reaction, a copper catalyzed covalent reaction between a picolyl azide and an alkyne, Fluor? 488 and SYTOX? Green Dyes (ThermoFisher scientific) SYTOX?, before cell analysis using an Attune? NxT Acoustic Focusing Cytometer, vol.242, p.243
,
, For each incubation time, 253 results from BEAS-2B cells exposed either to PM 2.5-0.3 , NEM 2.5-0.3 OEM 2.5-0.3 , or OEM 0.3 at their 254 different concentrations or to positive controls were compared to those obtained from negative 255 controls (i.e., non-exposed). Thereafter, significant difference between results from BEAS-2B 256 cells exposed either to NEM 2, Results were expressed as mean values and standard deviations
Indeed, there is still a lack of knowledge about the specific chemical fraction 267 within ambient PM, which could be mainly responsible of its adverse effects on human health, p.266, 2016. ,
, significant decreases of intracellular ATP concentration in to NEM 2.5-0.3 . In contrast, both OEM 2.5-0.3 and particularly OEM 0.3 significantly altered 276 intracellular ATP concentration in BEAS-2B cells only for the highest doses, As shown in Figure S2
The dose-and/or time-dependent cytotoxicity of PM 2 ,
PM/cm²) among the lowest reported to give harmful effects whilst limiting a massive regulated 280 cell death, and the kinetic (from 6 to 48 h) to apply for the further study of toxicological endpoints 281, Leclercq et al, vol.282, 2010. ,
, Figure 1 showed the intracellular overproduction of ROS in BEAS-287 2B cells 6 and 24 h after their exposure to either PM 2.5-0.3 , NEM 2.5-0.3 , OEM 2.5-0.3 , and OEM 0.3 . HE 288 fluorescence intensity significantly increased in a dose-dependent manner in BEAS-2B cells after 289 their exposure to NEM 2.5-0.3 and OEM 2.5-0.3 , and more markedly PM 2.5-0.3 and OEM 0.3 . Because of 290 its desirable quality of passive diffusion into cells, as well as its high reactivity, Oxidative stress is often considered to be the primary critical underlying mechanism induced 286 by ambient PM. Accordingly, 2013.
Almost similar results were observed for the intensity of fluorescence emitted 293 by carboxy-H2DCFDA, with the highest intensity detected in BEAS-2B cells 24 hours after of ROS detected by this probe is much broader, 2014. ,
Zn are generally associated with redox reactions. In addition, the 299 overproduction of ROS could be related to the organic species, vol.300, 2019. ,
, AhR signaling pathway, thereby triggering transcription levels of CYP1A1 and 1B1 genes, which 303 are poorly or not at all expressed in BEAS-2B cells. Although metabolic activation is generally 304 beneficial in helping lung cells to reduce the potential toxicity of inhaled pollutants, it sometimes 305 converts harmless substances into highly biologically reactive electrophilic metabolites, thereby 306 contributing to the overproduction of ROS, p.16
the cell (Wardyn et al. 2015). In response to the exposure to oxidants or electrophiles, 323 NRF2 accumulates in the nucleus, where it binds to the ARE in upstream regulatory regions of 324 genes encoding NRF2 targets. Among them, antioxidant enzymes, proteins involved in the 325 metabolism and clearance of xenobiotics, protection against metal toxicity, inhibition of 326 inflammation, PM 10 and PM 2 5 , representative of urban background air pollution, diesel exhaust PM 308 and wood smoke, because of their relatively high levels of PAH, were all able to significantly 309 activate the AHR signaling pathway and/or generate oxidative stress conditions in BEAS-2B cells 310, 2011. ,
Oxidative damage to DNA, proteins and/or lipids can 339 significantly disrupt the cell homeostasis through the inorganic-and organic chemical-catalyzed 340 overproduction of ROS and cellular internalization, contributing to the modulation of gene 341 expression or DNA mutation, protein alteration with loss of function, and oxidative degradation 342 of the lipid membrane with loss of integrity and fluidity, Remarkably, the highest concentrations of oxidative 333 damage in BEAS-2B cells were generally reported after their exposure to, vol.343, 2006. ,
Accordingly, as shown in Figure S3, only TNF-? and IL-6 were significantly secreted 351 by BEAS-2B cells 6 and 24 h after their exposure to PM 2.5-0.3 , and mainly 6 h after their exposure 352 to NEM 2.5-0.3 , OEM 2.5-0.3 , and OEM 0.3 . However, it is noteworthy that there was only limited 18 353 secretion of TNF-? and IL-6 by exposed BEAS-2B cells, as compared with other results, While NRF2, as an anti-inflammatory, can modulate NF-?B binding activity, NF-?B can, as 348 a self-starter, modulate NRF2 transcription and activity having thereby positive or negative effects 349 on the expression of its target gene expression, vol.357, 2006. ,
, , p.360, 2006.
A remarkable relationship has 362 been reported between the contents of redox-active compounds (e.g., metals, PAH) within ambient 363 PM and the proinflammatory response occurring within lung cells, which might closely rely on 364 the regulation of NF-?B, addition, the activation of the NF-?B the NRF2 and NF-?B signaling pathways, p.361, 2011. ,
NEM 2.5-0.3 , OEM 2.5-0.3 , and OEM 0.3 -induced autophagy 374 To go further in this original work and to contribute to fill the knowledge about the harmful 375 effects of the exposure to PM 2.5-0.3 , NEM 2.5-0.3 , OEM 2.5-0.3 , and OEM 0.3 on BEAS-2B cell 19 376 homeostasis and functionality, autophagy was thereafter studied. Indeed, mounting evidences 377 further suggest that long-lasting oxidative stress may help to cell adaptation to the stress by limiting 378 the oxidative damage, and although the molecular mechanisms underlying these changes remain 379 unknown, autophagy is part of the adaptive response (Deng et al 2017lung diseases, including asthma and COPD, and several, if not all forms of regulated 384 cell death (RCD), either by hyperactivation or by inhibition of the autophagy flow, Other authors contributing to decipher the underlying mechanisms of toxicity of PM 10 and PM 2.5 370 in BEAS-2B cells reported that PM 2.5 -induced IL-6 secretion appeared to be activated before IL-371 8 secretion, and did not increase beyond 24 h in contrast to PM 10 -induced IL-6 secretion. 372 373, vol.385, p.3, 2016. ,
) further the inhibition of NF-?B signaling pathway. Taken together, our 414 results also supported the intriguing occurrence of a specific autophagy-impairment as a critical or 415 even beneficial mechanism triggered during OEM-mediated toxicity, Overall, the study of autophagy closely supported differential responses of whole PM or NEM 398 towards organic enriched fractions (i.e., OEM 2.5-0.3 and rather OEM 0.3 ), 2013. ,
To go 424 further, apoptosis was also investigated. Figure 5 shows the specific activities of some of the 425 critical caspases closely involved in both the cell death receptor (extrinsic) and the mitochondrial 426 (intrinsic) pathways of apoptosis. The activities of the initiator caspases, vol.8, 2017. ,
on the one hand, and cell 431 cycle phases of these cells, on the other hand, indicated rather no clear morphological 432 characteristics of a regulated cell death by apoptosis, even after 48 h of exposure. However, An et 433 al. (2019), studying the critical interplays between oxidative stress, autophagy and apoptosis cell models, including BEAS-2B cells, according to the specific 437 exposure conditions, thereby 429 supporting the progressive occurrence of apoptotic events. However, as shown by Figures 6 and 430 7, both TUNEL and Annexin-V immunostaining of BEAS-2B cells, vol.438, 2011. ,
, , p.605
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, The research described in this article benefited from grants from the National Council for
, Ref: 04-06-2014). The "Unité de
UCEIV-EA4492) and the "IMPacts de 672 l'Environnement Chimique sur la Santé" (IMPECS-EA4483) both participate in the CLIMIBIO 673 project, which is financially supported by the Hauts-de-France Region Council, the French 674 Ministry of Higher Education and Research, and the European Regional Development Funds ,
, Figure 1: Fluorescence intensity of dihydroethidium (HE) and 6-carboxy-2',7'-681 dichlorodihydrofluorescein diacetate (carboxy-H2DCFDA), and gene expression and/or protein 682 binding activity of nuclear factor erythroid 2-related factor 2 (NRF-2) in BEAS-2B cells, vol.6, p.24
, Menadione (100 µM, 4 h) has been used as positive control for ROS generation
normalized to control, are described by their means and their standard deviations (3 687 replicates for controls, and 3 replicates for exposed cells ,
,
, Gene expression of Kelch-like ECH-associated protein 1 (KEAP-1), heme oxygenase 1 693 (HMOX), NAD(P)H quinone dehydrogenase 1 (NQO1), and superoxide dismutase, vol.2
, Results, normalized to control, are described 697 by their means and their standard deviations (3 replicates for controls, and 3 replicates for exposed 698 cells, BEAS-2B cells, 6 and 24 h after their exposure to the fine particles and their extractable and non-695 extractable fractions
, CO-protein), and 8-703 isoprostane (8-Isop) in BEAS-2B cells, 6 and 24 h after their exposure to the fine particles and 704 their extractable and non-extractable fractions
U-test ,
, Protein expression of autophagy-related 5, BECN1/Beclin 1, SQSTM1/p62 protein, and, Figure, vol.4
, NEM 2.5-0.3 , and OEM 2.5-0.3 , respectively) and to the extractable fraction (OEM 0.3 ) of the 715 ultrafine particles (PM 0.3 ) at 12 ?g Eq. PM/cm 2 . Results, normalized to control, are described by 716 their means and their standard deviations (3 replicates for controls, and 3 replicates for exposed 717 cells
, or 48h) has been used as positive control for 725 apoptosis. Results, normalized to control, are described by their means and their standard 726 deviations (3 replicates for controls, Activities of caspases 3/7, 8, and 9 in BEAS-2B cells 24 and 48 h after their exposure to 722 the fine particles and their extractable and non-extractable fractions, vol.5
, Immunofluorescence labelling of apoptotic cells using the TdT-mediated dUTP Nick, vol.6
, End Labeling (TUNEL) method in BEAS-2B cells 24 and 48 h after their exposure to the fine 733 particles and their extractable and non-extractable fractions
, PM/cm 2 . Endonuclease and staurosporine (2.5 ?M) served as positive controls
, Figure 7: Detection of apoptotic cells using the Single-Channel Dead Cell Apoptosis Kit with
Fluor? 488 and SYTOX? Green Dyes (ThermoFisher scientific) and cell cycle 741 analysis using Click-iT? Plus EdU Alexa Fluor? 647 Flow Cytometry Assay Kit of BEAS-2B ,
U-test ,
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Résumé La pollution de l'air et les particules fines (PM 2.5 ) ont été classées cancérogènes (groupe 1) par le Centre International de Recherche sur le Cancer en 2013. Cette fraction particulaire représente un mélange complexe dont la composition, très variable, influe sur la toxicité. Cependant, peu d'études ont déterminé l'implication respective des différentes fractions chimiques constitutives des PM dans leurs effets toxiques, Environ. Sci. Technol, vol.47, pp.8434-8442, 2013. ,
, la fraction organique extractible (EOM 2.5-0.3 ) et la fraction non-extractible par le dichlorométhane (NEM 2.5-0.3 ). De plus, les effets spécifiques de la fraction organique extraite des particules quasi-ultrafines (EOM 0.3 ) ont été comparés à ceux de la fraction organique extraite des particules fines (EOM 2.5-0.3 ). Nos résultats montrent que chacune des fractions considérées a été capable d'activer au moins un des mécanismes étudiés. Les PM 2.5-0.3 ont induit des effets toxiques généralement plus marqués que les EOM 2.5-0.3 et NEM 2.5-0.3 . La fraction organique des particules quasi-ultrafines (EOM 0.3 ), plus riche en composés organiques et notamment en HAP et autres congénères, est apparue responsable d'effets délétères globalement plus importants que celle extraite des particules fines (EOM 2.5-0.3 ). Les résultats de ce travail ont apporté des éléments nouveaux sur la toxicité relative des différentes fractions extractibles et non extractibles des particules fines et soulignent le rôle crucial joué par les particules ultrafines, encore trop peu étudiées. Abstract Air pollution and particulate matter (PM 2.5 ) were classified as carcinogens (group 1) by the International Agency for Research on Cancer in 2013. This particulate fraction represents a complex mixture with a highly variable composition influencing the toxicity. However, few studies have determined the respective involvement of the different chemical fractions of PM in their toxic effects. In this work, fine particles (PM 2.5-0.3 ) and quasi-ultrafine particles (PM 0.3 ) were sampled in an urban site located in Beirut (Lebanon), Après avoir réalisé la caractérisation physico-chimique de ces deux types de particules, leurs effets toxiques (cytotoxicité globale, activation métabolique, génotoxicité, inflammation, stress oxydant, autophagie et apoptose) ont été étudiés sur une lignée de cellules épithéliales bronchiques humaines (BEAS-2B). L'analyse des fractions organiques a révélé des différences entre les teneurs en hydrocarbures aromatiques polycycliques (HAP), de même qu'en congénères oxygénés (O-HAP) et nitrés (N-HAP), respectivement 43, 17 et 4 fois plus élevées dans les PM 0.3 que dans les PM 2.5-0.3 . L'étude toxicologique a porté sur les particules fines considérées dans leur entièreté