Special Issue on Pulmonary and Neurological Health Impacts from Airborne Particulate Matter

Juan Li, Yingying Liu, Zhen An, Wen Li, Xiang Zeng, Huijun Li, Jing Jiang, Jie Song, Weidong Wu This email address is being protected from spambots. You need JavaScript enabled to view it.

International Collaborative Laboratory for Air Pollution Health Effects and Intervention, School of Public Health, Xinxiang Medical University, Xinxiang, Henan 453003, China


 

Received: August 5, 2019
Revised: November 18, 2019
Accepted: November 30, 2019

 Copyright The Author(s). This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are cited.


Download Citation: ||https://doi.org/10.4209/aaqr.2019.06.0288  

  • Download: PDF


Cite this article:

Li, J., Liu, Y., An, Z., Li, W., Zeng, X., Li, H., Jiang, J., Song, J. and Wu, W. (2020). Seasonal Variations in PM2.5-induced Oxidative Stress and Up-regulation of Pro-inflammatory Mediators. Aerosol Air Qual. Res. 20: 1686–1694. https://doi.org/10.4209/aaqr.2019.06.0288


HIGHLIGHTS

  • PM2.5 from different seasons own distinct composition.
  • The water-soluble composition of PM2.5 showed seasonal variations.
  • PM2.5 -induced oxidative stress and subsequent production of pro-inflammatory mediators varies with season.
 

ABSTRACT


Inhaling particulate matter with an aerodynamic diameter of ≤ 2.5 µm (PM2.5) has been demonstrated to induce season-dependent adverse health effects. As inflammation and oxidative stress play a critical role in PM2.5-induced health effects, this study used a human monocytic cell line, THP-1, to investigate whether the PM2.5-induced oxidative stress and pro-inflammatory response varied by season. PM2.5 was collected during April (spring), July (summer), September (fall) and December (winter) of 2014. The cytotoxicity was assessed with a lactate dehydrogenase (LDH) release assay. The levels of pro-inflammatory mediators, including tumor necrosis factor (TNF-α) and interleukin-1β (IL-1β), were measured with ELISA, and the reactive oxygen species (ROS) were identified with flow cytometry. Sulforaphane (SFN), an antioxidant, was used to determine whether ROS regulated the PM2.5-induced expression of pro-inflammatory mediators. The PM2.5 from winter exhibited the highest potency in inducing cytotoxicity as well as the production of TNF-α and IL-1β from THP-1 cells; the same was true for ROS production. Further experiments demonstrated that pretreating THP-1 cells with SFN markedly mitigated the winter-PM2.5-induced release of TNF-α and IL-1β. Composition analysis revealed that the PM2.5 contained higher levels of anions (NO3 and SO42–) and water-soluble metals (Al, Ca, Mg, Zn and Cr) during summer and winter than spring and fall. In summary, PM2.5-induced oxidative stress and the subsequent production of pro-inflammatory mediators vary by season.


Keywords: PM2.5; THP-1 cells; Cytotoxicity; Oxidative stress; Inflammation.


INTRODUCTION


Air pollution has become a major global public health concern. PM2.5 is the primary component of urban air pollutants in China (van Donkelaar et al., 2015). Epidemiological studies revealed that exposure to PM2.5 increases cardiopulmonary mortality and morbidity (Schwarze et al., 2006; Lippmann, 2014). A survey carried out in 2015 indicated that ambient PM2.5 was the fifth-ranking mortality risk factor. The report also pointed out that deaths which is attributable to long-term exposure to PM2.5 varied with country (Cohen et al., 2017). Additionally, previous studies have shown that adverse health effects exposed to PM2.5 vary with season (Becker et al., 2005; Peng et al., 2005).

PM2.5, a heterogeneous mixture of constituents, includes diverse organics, metals and biological components. The constituents of PM2.5 vary with origin and season (Becker et al., 2005; Pardo et al., 2018). Previous report has demonstrated that the PM2.5 from different seasons presented different toxicity profiles (Hetland et al., 2005). There is evidence that PM-induced increase in mortality is higher in the warm seasons compared with the cold seasons (Smith et al., 2000; Danielsen et al., 2011). These observations were further supported by an in vivo study showing that particles from warm/sunny days had greater inflammatory and cytotoxic activities in mouse lung than the particles from cold/wet seasons (Happo et al., 2008). However, inconsistent results were also observed. For example, previous epidemiological and toxicological studies demonstrated that winter PM have more potency in cytotoxicity, especially in Asian countries (Chen et al., 2013; Kurai et al., 2016).

Oxidative stress as well as inflammation is regarded as critical events in PM-induced adverse health risk (Mazzoli-Rocha et al., 2010). It is an effective way to evaluate PM2.5-induced oxidative stress and inflammatory response by establishing a cell system. Assays of oxidative stress and inflammatory responses in PM-exposed cell systems, for example, could be used to provide an integrative assessment of biological activity of the PM mixture at modest cost. Assays reflecting different biological pathways of effect could be used to examine the mechanisms underlying epidemiological associations of PM with both acute and chronic disease. Associations in plausible pathways would also help reduce uncertainty in the causal interpretation of epidemiological findings (Manzano-Leon et al., 2016).

Our previous studies have shown that PM2.5 exposure can induce oxidative stress and inflammation in rats or BEAS-2B cells (Yan et al., 2016; Li et al., 2019). Alveolar macrophages (AMs) are regarded as the initial cells which can phagocytose inhaled particulates. PM deposited in lung could activate AMs via binding of ligands to receptors. Subsequently activate signaling pathways and potentially mediate inflammatory or cytotoxic outcomes (Wu et al., 2014). AMs are a critical type of airway cells derived from blood monocytes (Hocking and Golde, 1979). The present study in vitro was to explore whether PM2.5-induced oxidative stress and inflammatory effects exhibited seasonal variations using a human acute monocytic leukemia cell line (THP-1), which is an economical, high-throughput system associated to airway monocytes and AMs (Tsuchiya et al., 1980).


MATERIALS AND METHODS



Reagents

IL-1β and TNF-α ELISA kits were purchased from Boster Biological Technology Co., Ltd. (Wuhan, China). Lactate dehydrogenase (LDH) and superoxide dismutase (SOD) assay kits were obtained from Nanjing Jiancheng Bioengineering Institute (Nanjing, China). The 5(6)-carboxy-2ʹ,7ʹ-dichlorodihydrofluorescein diacetate (carboxy-H2DCFDA) was procured from Beyotime Biotechnology (Shanghai, China). Sulforaphane (SFN) was purchased from Sigma-Aldrich (St. Louis, MO, USA).


PM2.5 Collection

The PM2.5 samples were provided by Dr. Ruiqin Zhang from Zhengzhou University, China. They were collected onto quartz microfiber filters (20.3 × 25.4 cm; PALL, USA) for a continuous 24 h using a PM2.5 high-volume air sampler (KC-1000; Laoshan Mountain Electronic Instrument Factory Company, Qingdao, China) from April 2015 and December 2015 on non-rainy days, with proximity to a variety of small- and medium-size factories including machinery, chemical manufacturing, boiler industry, and power plant, indicating a characteristic mixed pollutant area. Before and after PM extraction, the quartz filters were equilibrated in a conditioning room at 22°C and at 33% relative humidity for 48 h (XS205; Mettler Toledo, Switzerland). Each filter was weighed twice, and the difference of the weights was less than or equal to 0.03 mg. The PM2.5 was extracted from the filters by a 15 min sonication for three times with 2 min intervals. The extraction rate of PM2.5-loaded quartz filters was between 87–92%. The PM2.5 was recovered through a vacuum freeze-drying procedure and used for the following in vitro exposure studies.


PM2.5 Constituent Analysis

To specify the physicochemical properties of PM2.5, anions in PM2.5 were determined with ion chromatography (ICS-90; Dionex, USA) using 8 mM Na2CO3/1 mM NaHCO3 as eluent at 0.5 mL min1. Particles were digested by nitric acid and hydrogen peroxide. The metal elements analysis was carried out using an inductively coupled plasma mass spectrometry (ICP-MS; Thermo Fisher, USA).


Cell Culture and PM2.5 Exposure

THP-1 cells were purchased from American Type Tissue Culture Collection (ATCC, Rockville, MD, USA). The cells were cultured in RPMI 1640 medium supplemented with 10% fetal bovine serum (FBS) and maintained at 37°C, 5% CO2 in a humidified incubator. For determination of cytotoxicity and inflammatory response, the cells were seeded in 96-well plates (2 × 104 cells per well). After 24 h incubation, the cells were exposed to different doses of PM2.5 from different seasons (0, 12.5, 25, 50, 100 µg mL–1) for 24 h. Diesel exhaust particles (DEP) were used as the positive control. The rationale for using DEP as the positive control is that the associations of air pollution with cardiopulmonary diseases are strongest for PM2.5, of which the combustion-derived ultrafine particles from diesel exhaust are an important component (Laden et al., 2000). The final concentration for oxidative stress assay was 100 µg mL–1.


Evaluation of Cytotoxicity

LDH is a stable cytoplasmic enzyme that is present in all kinds of cells. Once plasma membrane of cell is damaged, the LDH will instantly be released to the outside of the cells. The cytotoxicity was evaluated with LDH assay kit following the manufacturer’s instructions.


Determination of Inflammatory Cytokines with ELISA

TNF-α and IL-1β are bio-markers of pro-inflammatory response. After the exposure of THP-1 cells to PM2.5 for 24 h, the cell culture media were collected and the supernatants obtained through centrifugation at 300 g for 10 min. Levels of TNF-α and IL-1β were determined with ELISA according to the manufacturer’s instructions.


Determination of Oxidative Stress

Levels of intracellular ROS were measured with flow cytometry. Briefly, the cells were incubated with 10 µM carboxy-H2DCFDA in a 37°C, 5% CO2 humidified incubator for 30 min before exposed to PM2.5 for 4 h. Then the cells were washed three times with PBS. Mean fluorescence (MFI) was measured by using BD Flow Cytometer (Becton Dickinson, NY, USA).


Effect of SFN on PM2.5-induced Production of ROS and Over-expression of Pro-inflammatory Mediators

THP-1 cells were incubated with 5 µM SFN for 8 h before further exposure to 100 µg mL–1 PM2.5 for 4 h and 24 h, respectively. The supernatants of cell media were collected for measurement of TNF-α, IL-1β and ROS as described above.


Statistical Analysis

Analysis of variance (ANOVA) was used to make multiple comparisons followed by LSD analysis. Student’s t-test was used to compare two comparisons. Data were presented as mean ± standard deviation (SD) and P-value less than 0.05 was considered statistically significant. Statistical analysis was performed using SPSS 21.0.


RESULTS



Water-soluble Chemical Composition of PM2.5

April, July, September and December in 2015 were chosen to represent spring, summer, fall and winter, respectively. The elemental and water-soluble ions of PM2.5 from these four months are shown in Table 1. The water-soluble metal analysis uncovered twelve metals (Fe, Al, Ca, Mg, Cr, Mn, Ni, Cu, Zn, As, Pb, Cd) in the PM2.5 samples. Mg, Ca, and Zn were the most abundant metals presented in fall and winter PM2.5. The PM2.5 from summer contained more Cr. As shown in Table 2, PM2.5 from summer contained more NO3 and SO42–, while those from spring and winter contained more Cl




Seasonal Variation of PM2.5 Cytotoxicity

Fig. 1(d) indicated that the PM2.5 from winter induced a dose-dependent increase in cytotoxicity in THP-1 cells. In comparison with the PM2.5 from winter, the PM2.5 from other three seasons showed less cytotoxicity at a concentration of 50 µg mL–1 (Figs. 1(a), 1(b) and 1(c)). 


Fig. 1. Cytotoxicity of THP-1 cells exposed to PM2.5. THP-1 cells were stimulated with PM2.5 from (a) spring, (b) summer, (c) fall and (d) winter or (e) DEP at an indicative concentration for 24 h, separately. Cell viability was evaluated by using an LDH assay kit. LDH levels were represented by fold over control. All values represent the mean ± SD in three independent experiments. *p < 0.05, compared with control.Fig. 1. Cytotoxicity of THP-1 cells exposed to PM2.5. THP-1 cells were stimulated with PM2.5 from (a) spring, (b) summer, (c) fall and (d) winter or (e) DEP at an indicative concentration for 24 h, separately. Cell viability was evaluated by using an LDH assay kit. LDH levels were represented by fold over control. All values represent the mean ± SD in three independent experiments. *p < 0.05, compared with control.


Seasonal Variation of PM2.5-induced Over-expression of Pro-inflammatory Mediators

As shown in Figs. 2(a), 2(b), 2(c) and 2(d), PM2.5 (100 µg mL–1) from different seasons all induced significant increases in the expression of TNF-α. Of them, winter PM2.5 was the most potent in inducing the expression of TNF-α. As shown in Fig. 3, all the PM2.5 samples increased the release of IL-1β compared with the control. 


Fig. 2. Effect of PM2.5 on TNF-α expression in THP-1 cells supernatant. THP-1 cells were exposed to PM2.5 from (a) spring, (b) summer, (c) fall and (d) winter at an indicative concentration for 24 h, separately. The production of TNF-α was determined by using ELISA. TNF-α levels were represented by fold over control. All values represent the mean ± SD in three independent experiments. *p < 0.05, compared with control group.Fig. 2. Effect of PM2.5 on TNF-α expression in THP-1 cells supernatant. THP-1 cells were exposed to PM2.5 from (a) spring, (b) summer, (c) fall and (d) winter at an indicative concentration for 24 h, separately. The production of TNF-α was determined by using ELISA. TNF-α levels were represented by fold over control. All values represent the mean ± SD in three independent experiments. *p < 0.05, compared with control group.

Fig. 3. Effect of PM2.5 on IL-1β expression in culture medium of THP-1 cells. THP-1 cells were exposed to PM2.5 from (a) spring, (b) summer, (c) fall and (d) winter at an indicative concentration for 24 h, separately. The production of IL-1β was determined by using ELISA. IL-1β levels were represented by fold over control. All values represent the mean ± SD in three independent experiments. *p < 0.05, compared with control group.Fig. 3. Effect of PM2.5 on IL-1β expression in culture medium of THP-1 cells. THP-1 cells were exposed to PM2.5 from (a) spring, (b) summer, (c) fall and (d) winter at an indicative concentration for 24 h, separately. The production of IL-1β was determined by using ELISA. IL-1β levels were represented by fold over control. All values represent the mean ± SD in three independent experiments. *p < 0.05, compared with control group.


Seasonal Variation of ROS Production Induced by PM2.5

ROS production was measured by MFI using flow cytometry in THP-1 cells. Intracellular levels of ROS were obviously increased when exposure of THP-1 cells to PM2.5 (100 µg mL–1) compared with control, especially from winter (Fig. 4(a)). 


Fig. 4. Production of ROS triggered by PM2.5 exposure in THP-1 cells. (a) THP-1 cells were exposed to 100 µg mL–1 PM2.5 from different seasons for 4 h after incubated with carboxy-H2DCFDA for 30 min. ROS generation was determined by flow cytometry. ROS levels were represented by fold over control. (b) Before exposure to 100 µg mL–1 PM2.5, 5 µM SFN was supplied to inhibit the production of ROS. All values represent the mean ± SD in three independent experiments. *p < 0.05, compared with Apr group; #p < 0.05, compared with Jul group; △p < 0.05, compared with Sep group; ▲p < 0.05, compared with Dec group.Fig. 4. Production of ROS triggered by PM2.5 exposure in THP-1 cells. (a) THP-1 cells were exposed to 100 µg mL–1 PM2.5 from different seasons for 4 h after incubated with carboxy-H2DCFDA for 30 min. ROS generation was determined by flow cytometry. ROS levels were represented by fold over control. (b) Before exposure to 100 µg mL–1 PM2.5, 5 µM SFN was supplied to inhibit the production of ROS. All values represent the mean ± SD in three independent experiments. *p < 0.05, compared with Apr group; #p < 0.05, compared with Jul group; p < 0.05, compared with Sep group; p < 0.05, compared with Dec group.


Inhibition of SFN on PM2.5-induced ROS Production and Expression of Pro-inflammatory Mediators

ROS is regarded as a key factor in inducing the release of inflammatory mediators (Mazzoli-Rocha et al., 2010). As expected, the release of ROS was significantly inhibited by pretreatment of THP-1 cells with SFN (Fig. 4(b)). Importantly, the TNF-α and IL-1β release were decreased by the pretreatment with SFN in THP-1 cells exposed to 100 µg mL–1 PM2.5 from winter (Fig. 5(a) and 5(b)), indicating that ROS were required for winter-PM2.5-induced pro-inflammatory response. 


Fig. 5. Effect of SFN treatment on TNF-α and IL-1β expression induced by PM2.5 exposure in THP-1 cells. TNF-α and IL-1β levels were represented by fold over control. All values represent the mean ± SD in three independent experiments. *p < 0.05, compared with PM2.5 group.Fig. 5. Effect of SFN treatment on TNF-α and IL-1β expression induced by PM2.5 exposure in THP-1 cells. TNF-α and IL-1β levels were represented by fold over control. All values represent the mean ± SD in three independent experiments. *p < 0.05, compared with PM2.5 group.


DISCUSSION


PM2.5 has been considered to be a key contributor to the formation of haze in most parts of China. Although the association between PM2.5 exposure and adverse human health effects is well known (Lawal, 2017; Mukherjee and Agrawal, 2018), the mechanisms of adverse effects caused by PM2.5 is still unclear. Thus far, oxidative stress and inflammation have been recognized to play vital roles in PM2.5-induced adverse effects. Season is an important modifying factor when investigating the acute health effects of air pollution. Documented studies have shown season-associated short-term health effects of PM (Roosli et al., 2000). However, the evidence of seasonal variation in these associations is inconsistent (Hetland et al., 2004; Molinelli et al., 2006). A previous epidemiological study in China indicated that the acute effect of PM air pollution varied by seasons with the largest effect in winter and summer (Roosli et al., 2000). In contrast, a recent in vitro study employed human lung epithelial carcinoma cells (A549), hepatocellular liver carcinoma cells (HepG2), and neuroblastoma cells (Sh-Sy5y) to evaluate the toxicological properties of the collected PM2.5 in Nanjing, China, showing that the viability inhibition in A549, Sh-Sy5y, and HepG2 cells was more prominent in summer, and the induction of ROS in A549 and Sh-Sy5y cells was also more evident in summer (Zhang et al., 2019).

In the present study with human blood monocytic cells, we showed that PM2.5 from different seasons presented variable potencies in oxidative stress and inflammation, with the strongest potency for PM2.5 from winter. Uniquely, this study found that oxidative stress was involved in PM2.5-induced pro-inflammatory response since SFN, a naturally occurring potent inducer of antioxidant Phase II enzymes, from broccoli sprouts, significantly block PM2.5-induced ROS production and subsequent expression of pro-inflammatory mediators (Riedl et al., 2009).

TNF-α and IL-1α/β are regarded as key mediators in lung, which will up-regulate the induction of secondary mediators including IL-6 and TGF-β1 and initiate the following inflammation cascade (Becker et al., 1996; Grivennikov et al., 2006; Barksby et al., 2007). Previous studies have shown that PM2.5 is capable of inducing TNF-α and IL-1β release (Ovrevik et al., 2009; Dieme et al., 2012). Chen et al. (2018) found cytotoxicity of PM2.5 from winter was more potent than PM2.5 from summer in Nanjing, China. The observation from Chen and his colleagues is supported by the present study, showing that PM2.5, especially from winter, induces the release of inflammatory cytokines. Remarkably, several studies have indicated that PM from warmer seasons has a greater cell toxicity and pro-inflammatory response (Becker et al., 2005; Happo et al., 2008). The inconsistent findings suggest that mixture of components may participate in PM-induced heterogeneous health outcomes. The pathways regulating PM-induced inflammatory effect were not elucidated. Previous studies have shown inflammatory mediators induced by PM exposure through activating transcription factors including NF-kB and AP-1 (Donaldson and Stone, 2003; Ohyama et al., 2007). In addition, the release of IL-6 or TNF-α induced by PM exposure was associated with Cu and Zn content (Becker et al., 2005). Our previous study found 20% of IL-8 production was reduced after chelating of zinc of PM2.5 (Yan et al., 2016). In our study, Zn (varied in different seasons) is the highest metal in all the samples, especially winter ones. PM2.5 from winter can obviously induce ROS release and up-regulation of TNF-α and IL-1β. 

Although mechanisms of PM2.5-induced health effects are not fully understood, ROS production has been well recognized to involve in inflammatory response upon exposure to PM (Nel, 2005). ROS is regarded as an important messenger to activate several cell signal transduction pathways which can initiate inflammatory gene expression (Dagher et al., 2007). We found that PM2.5 can lead to the generation of ROS which is in line with other studies (Becker et al., 2005). Moreover, PM2.5-induced TNF-α and IL-1β expression was significantly inhibited by the antioxidant SFN, implying that oxidative stress is required for release of pro-inflammatory cytokines in THP-1 cells. However, how PM induces oxidative stress is still to be investigated. A plethora of studies pointed out that PM components may account for oxidative stress. Metals, especially transition metals, which are present on PM are related to PM2.5-induced airway injury, inflammation and oxidative stress (Hetland et al., 2000; Steenhof et al., 2011). Our present study found that Zn and Cr are enriched in PM2.5 from Zhengzhou. Zinc is an important metal element detected in traffic-derived PM2.5, and it could mediate ROS generation (Chen and Lippmann, 2009; Donadelli et al., 2009). In conclusion, these studies indicate that differential cytotoxicity, inflammation and oxidative stress may be related to water-soluble metals.

It should be noted that although quartz filter is recommended for air sampling and chemical analyses, its highest efficiency of absorption and promotion of on-filter degradation of air pollutant components poses potential limitations on evaluation of PM toxicity (Grosjean, 1983; Parshintsev et al., 2011).


CONCLUSIONS


In summary, the present study uses THP-1 cells to demonstrate that the ability of PM2.5 to induce oxidative stress and inflammation differs by season. Our findings, which suggest that PM during winter in Zhengzhou (China) produces stronger toxic effects, support the conclusions of previous epidemiological studies. The variation in the PM2.5 composition across different seasons must be considered in future toxicological and epidemiological research.


ACKNOWLEDGMENTS


This work was supported by grants from the National Natural Science Foundation of China (81573112 and 81373030).


REFERENCES


  1. Barksby, H.E., Lea, S.R., Preshaw, P.M. and Taylor, J.J. (2007). The expanding family of interleukin-1 cytokines and their role in destructive inflammatory disorders. Clin. Exp. Immunol. 149: 217–225. [Publisher Site]

  2. Becker, S., Soukup, J.M., Gilmour, M.I. and Devlin, R.B. (1996). Stimulation of human and rat alveolar macrophages by urban air particulates: Effects on oxidant radical generation and cytokine production. Toxicol. Appl. Pharmacol. 141: 637–648. [Publisher Site]

  3. Becker, S., Dailey, L.A., Soukup, J.M., Grambow, S.C., Devlin, R.B. and Huang, Y.C. (2005). Seasonal variations in air pollution particle-induced inflammatory mediator release and oxidative stress. Environ. Health Perspect. 113: 1032–1038. [Publisher Site]

  4. Chen, L.C. and Lippmann, M. (2009). Effects of metals within ambient air particulate matter (PM) on human health. Inhalation Toxicol. 21: 1–31. [Publisher Site]

  5. Chen, R., Peng, R.D., Meng, X., Zhou, Z., Chen, B. and Kan, H. (2013). Seasonal variation in the acute effect of particulate air pollution on mortality in the China Air Pollution and Health Effects Study (CAPES). Sci. Total Environ. 450–451: 259–265. [Publisher Site]

  6. Chen, Y., Luo, X.S., Zhao, Z., Chen, Q., Wu, D., Sun, X., Wu, L. and Jin, L. (2018). Summer–winter differences of PM2.5 toxicity to human alveolar epithelial cells (A549) and the roles of transition metals. Ecotoxicol. Environ. Saf. 165: 505–509. [Publisher Site]

  7. Cohen, A.J., Brauer, M., Burnett, R., Anderson, H.R., Frostad, J., Estep, K., Balakrishnan, K., Brunekreef, B., Dandona, L., Dandona, R., Feigin, V., Freedman, G., Hubbell, B., Jobling, A., Kan, H., Knibbs, L., Liu, Y., Martin, R., Morawska, L., ... Forouzanfar, M.H. (2017). Estimates and 25-year trends of the global burden of disease attributable to ambient air pollution: An analysis of data from the Global Burden of Diseases Study 2015. Lancet 389: 1907–1918. [Publisher Site]

  8. Dagher, Z., Garcon, G., Billet, S., Verdin, A., Ledoux, F., Courcot, D., Aboukais, A. and Shirali, P. (2007). Role of nuclear factor-kappa B activation in the adverse effects induced by air pollution particulate matter (PM2.5) in human epithelial lung cells (L132) in culture. J. Appl. Toxicol. 27: 284–290. [Publisher Site]

  9. Danielsen, P.H., Moller, P., Jensen, K.A., Sharma, A.K., Wallin, H., Bossi, R., Autrup, H., Molhave, L., Ravanat, J.L., Briede, J.J., de Kok, T.M. and Loft, S. (2011). Oxidative stress, DNA damage, and inflammation induced by ambient air and wood smoke particulate matter in human A549 and THP-1 cell lines. Chem. Res. Toxicol. 24: 168–184. [Publisher Site]

  10. Dieme, D., Cabral-Ndior, M., Garcon, G., Verdin, A., Billet, S., Cazier, F., Courcot, D., Diouf, A. and Shirali, P. (2012). Relationship between physicochemical characterization and toxicity of fine particulate matter (PM2.5) collected in Dakar city (Senegal). Environ. Res. 113: 1–13. [Publisher Site]

  11. Donadelli, M., Dalla Pozza, E., Scupoli, M.T., Costanzo, C., Scarpa, A. and Palmieri, M. (2009). Intracellular zinc increase inhibits p53(-/-) pancreatic adenocarcinoma cell growth by ROS/AIF-mediated apoptosis. Biochim. Biophys. Acta 1793: 273–280. [Publisher Site]

  12. Donaldson, K. and Stone, V. (2003). Current hypotheses on the mechanisms of toxicity of ultrafine particles. Ann. Ist. Super. Sanita. 39: 405–410.

  13. Grivennikov, S.I., Kuprash, D.V., Liu, Z.G. and Nedospasov, S.A. (2006). Intracellular signals and events activated by cytokines of the tumor necrosis factor superfamily: From simple paradigms to complex mechanisms. Int. Rev. Cytol. 252: 129–161. [Publisher Site]

  14. Grosjean, D. (1983). Polycyclic aromatic hydrocarbons in Los Angeles air from samples collected on teflon, glass and quartz filters. Atmos. Environ. 17: 2565–2573. [Publisher Site]

  15. Happo, M.S., Hirvonen, M.R., Halinen, A.I., Jalava, P.I., Pennanen, A.S., Sillanpaa, M., Hillamo, R. and Salonen, R.O. (2008). Chemical compositions responsible for inflammation and tissue damage in the mouse lung by coarse and fine particulate samples from contrasting air pollution in Europe. Inhalation Toxicol. 20: 1215–1231. [Publisher Site]

  16. Hetland, R.B., Refsnes, M., Myran, T., Johansen, B.V., Uthus, N. and Schwarze, P.E. (2000). Mineral and/or metal content as critical determinants of particle-induced release of IL-6 and IL-8 from A549 cells. J. Toxicol. Environ. Health Part A 60: 47–65. [Publisher Site]

  17. Hetland, R.B., Cassee, F.R., Refsnes, M., Schwarze, P.E., Lag, M., Boere, A.J. and Dybing, E. (2004). Release of inflammatory cytokines, cell toxicity and apoptosis in epithelial lung cells after exposure to ambient air particles of different size fractions. Toxicol. in Vitro 18: 203–212. [Publisher Site]

  18. Hetland, R.B., Cassee, F.R., Lag, M., Refsnes, M., Dybing, E. and Schwarze, P.E. (2005). Cytokine release from alveolar macrophages exposed to ambient particulate matter: Heterogeneity in relation to size, city and season. Part. Fibre Toxicol. 2: 4. [Publisher Site]

  19. Hocking, W.G. and Golde, D.W. (1979). The pulmonary-alveolar macrophage (first of two parts). N. Engl. J. Med. 301: 580–587. [Publisher Site]

  20. Kurai, J., Watanabe, M., Sano, H., Hantan, D. and Shimizu, E. (2016). The Effect of seasonal variations in airborne particulate matter on asthma-related airway inflammation in mice. Int. J. Environ. Res. Public Health 13: 579. [Publisher Site]

  21. Laden, F., Neas, L.M., Dockery, D.W. and Schwartz, J. (2000). Association of fine particulate matter from different sources with daily mortality in six U.S. cities. Environ. Health Perspect. 108: 941–947. [Publisher Site]

  22. Lawal, A.O. (2017). Air particulate matter induced oxidative stress and inflammation in cardiovascular disease and atherosclerosis: The role of Nrf2 and AhR-mediated pathways. Toxicol. Lett. 270: 88–95. [Publisher Site]

  23. Li, J., Li, H., Li, H., Guo, W., An, Z., Zeng, X., Li, W., Li, H., Song, J. and Wu, W. (2019). Amelioration of PM2.5-induced lung toxicity in rats by nutritional supplementation with fish oil and Vitamin E. Respir. Res. 20: 76. [Publisher Site]

  24. Lippmann, M. (2014). Toxicological and epidemiological studies of cardiovascular effects of ambient air fine particulate matter (PM2.5) and its chemical components: Coherence and public health implications. Crit. Rev. Toxicol. 44: 299–347. [Publisher Site]

  25. Manzano-Leon, N., Serrano-Lomelin, J., Sanchez, B.N., Quintana-Belmares, R., Vega, E., Vazquez-Lopez, I., Rojas-Bracho, L., Lopez-Villegas, M.T., Vadillo-Ortega, F., De Vizcaya-Ruiz, A., Perez, I.R., O'Neill, M.S. and Osornio-Vargas, A.R. (2016). TNFα and IL-6 responses to particulate matter in vitro: Variation according to PM size, season, and polycyclic aromatic hydrocarbon and soil content. Environ. Health Perspect. 124: 406–412. [Publisher Site]

  26. Mazzoli-Rocha, F., Fernandes, S., Einicker-Lamas, M. and Zin, W.A. (2010). Roles of oxidative stress in signaling and inflammation induced by particulate matter. Cell Biol. Toxicol. 26: 481–498. [Publisher Site]

  27. Molinelli, A.R., Santacana, G.E., Madden, M.C. and Jimenez, B.D. (2006). Toxicity and metal content of organic solvent extracts from airborne particulate matter in Puerto Rico. Environ. Res. 102: 314–325. [Publisher Site]

  28. Mukherjee, A. and Agrawal, M. (2018). A global perspective of fine particulate matter pollution and its health effects. Rev. Environ. Contam. Toxicol. 244: 5–51. [Publisher Site]

  29. Nel, A. (2005). Atmosphere. Air pollution-related illness: Effects of particles. Science 308: 804–806. [Publisher Site]

  30. Ohyama, M., Otake, T., Adachi, S., Kobayashi, T. and Morinaga, K. (2007). A comparison of the production of reactive oxygen species by suspended particulate matter and diesel exhaust particles with macrophages. Inhalation Toxicol. 19: 157–160. [Publisher Site]

  31. Ovrevik, J., Lag, M., Holme, J.A., Schwarze, P.E. and Refsnes, M. (2009). Cytokine and chemokine expression patterns in lung epithelial cells exposed to components characteristic of particulate air pollution. Toxicology 259: 46–53. [Publisher Site]

  32. Pardo, M., Xu, F., Qiu, X., Zhu, T. and Rudich, Y. (2018). Seasonal variations in fine particle composition from Beijing prompt oxidative stress response in mouse lung and liver. Sci. Total Environ. 626: 147–155. [Publisher Site]

  33. Parshintsev, J., Ruiz-Jimenez, J., Petäjä, T., Hartonen, K., Kulmala, M. and Riekkola, M.L. (2011). Comparison of quartz and Teflon filters for simultaneous collection of size-separated ultrafine aerosol particles and gas-phase zero samples. Anal. Bioanal.Chem. 400: 3527–3535.[Publisher Site]

  34. Peng, R.D., Dominici, F., Pastor-Barriuso, R., Zeger, S.L. and Samet, J.M. (2005). Seasonal analyses of air pollution and mortality in 100 US cities. Am. J. Epidemiol. 161: 585–594. [Publisher Site]

  35. Riedl, M.A., Saxon, A. and Diaz-Sanchez, D. (2009). Oral sulforaphane increases Phase II antioxidant enzymes in the human upper airway. Clin. Immunol. 130: 244–251. [Publisher Site]

  36. Roosli, M., Braun-Fahrlander, C., Kunzli, N., Oglesby, L., Theis, G., Camenzind, M., Mathys, P. and Staehelin, J. (2000). Spatial variability of different fractions of particulate matter within an urban environment and between urban and rural sites. J. Air Waste Manage. Assoc. 50: 1115–1124. [Publisher Site]

  37. Schwarze, P.E., Ovrevik, J., Lag, M., Refsnes, M., Nafstad, P., Hetland, R.B. and Dybing, E. (2006). Particulate matter properties and health effects: Consistency of epidemiological and toxicological studies. Hum. Exp. Toxicol. 25: 559–579.|

  38. Smith, R.L., Spitzner, D., Kim, Y. and Fuentes, M. (2000). Threshold dependence of mortality effects for fine and coarse particles in Phoenix, Arizona. J. Air Waste Manage. Assoc. 50: 1367–1379. [Publisher Site]

  39. Steenhof, M., Gosens, I., Strak, M., Godri, K.J., Hoek, G., Cassee, F.R., Mudway, I.S., Kelly, F.J., Harrison, R.M., Lebret, E., Brunekreef, B., Janssen, N.A. and Pieters, R.H. (2011). In vitro toxicity of particulate matter (PM) collected at different sites in the Netherlands is associated with PM composition, size fraction and oxidative potential - The RAPTES project. Part. Fibre Toxicol. 8: 26. [Publisher Site]

  40. Tsuchiya, S., Yamabe, M., Yamaguchi, Y., Kobayashi, Y., Konno, T. and Tada, K. (1980). Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). Int. J. Cancer 26: 171–176. [Publisher Site]

  41. van Donkelaar, A., Martin, R.V., Brauer, M. and Boys, B.L. (2015). Use of satellite observations for long-term exposure assessment of global concentrations of fine particulate matter. Environ. Health Perspect. 123: 135–143. [Publisher Site]

  42. Wu, W., Muller, R., Berhane, K., Fruin, S., Liu, F., Jaspers, I., Diaz-Sanchez, D., Peden, D.B. and McConnell, R. (2014). Inflammatory response of monocytes to ambient particles varies by highway proximity. Am. J. Respir. Cell Mol. Biol. 51: 802–809. [Publisher Site]

  43. Yan, Z., Wang, J., Li, J., Jiang, N., Zhang, R., Yang, W., Yao, W. and Wu, W. (2016). Oxidative stress and endocytosis are involved in upregulation of interleukin-8 expression in airway cells exposed to PM2.5. Environ. Toxicol. 31: 1869–1878. [Publisher Site]

  44. Zhang, K., Nie, D., Chen, M., Wu, Y., Ge, X., Hu, J., Ge, P., Li, W., Huang, B., Yuan, Y., Li, Z. and Ma, X. (2019). Chemical characterization of two seasonal PM2.5 samples in Nanjing and its toxicological properties in three human cell lines. Environments 6: 42. [Publisher Site]

Aerosol Air Qual. Res. 20 :1686 -1694 . https://doi.org/10.4209/aaqr.2019.06.0288  


Don't forget to share this article 

 

Subscribe to our Newsletter 

Aerosol and Air Quality Research has published over 2,000 peer-reviewed articles. Enter your email address to receive latest updates and research articles to your inbox every second week.

Latest coronavirus research from Aerosol and Air Quality Research

2018 Impact Factor: 2.735

5-Year Impact Factor: 2.827


SCImago Journal & Country Rank