Differences in allergic inflammatory responses between urban PM2.5 and fine particle derived from desert-dust in murine lungs

https://doi.org/10.1016/j.taap.2016.02.017Get rights and content

Highlights

  • The aggravating effects of urban-PM2.5 and desert-PM2.5 on lung eosinophilia were compared.

  • Both PM2.5 enhanced Th2-immune response along with induced M2 macrophages.

  • The effect is greater in desert-PM2.5 than in organic chemical-rich urban-PM2.5.

  • Desert-PM2.5 may cause greater effects upon human respiratory health than urban-PM2.5.

Abstract

The biological and chemical natures of materials adsorbed onto fine particulate matter (PM2.5) vary by origin and passage routes. The exacerbating effects of the two samples—urban PM2.5 (U-PM2.5) collected during the hazy weather in a Chinese city and fine particles (ASD-PM2.5) collected during Asian sand dust (ASD) storm event days in Japan—on murine lung eosinophilia were compared to clarify the role of toxic materials in PM2.5. The amounts of β-glucan and mineral components were higher in ASD-PM2.5 than in U-PM2.5. On the other hand, organic chemicals, including polycyclic aromatic hydrocarbons (PAHs), were higher in U-PM2.5 than in ASD-PM2.5. When BALB/c mice were intratracheally instilled with U-PM2.5 and ASD-PM2.5 (total 0.4 mg/mouse) with or without ovalbumin (OVA), various biological effects were observed, including enhancement of eosinophil recruitment induced by OVA in the submucosa of the airway, goblet cell proliferation in the bronchial epithelium, synergic increase of OVA-induced eosinophil-relevant cytokines and a chemokine in bronchoalveolar lavage fluid, and increase of serum OVA-specific IgG1 and IgE. Data demonstrate that U-PM2.5 and ASD-PM2.5 induced allergic inflammatory changes and caused lung pathology. U-PM2.5 and ASD-PM2.5 increased F4/80+ CD11b+ cells, indicating that an influx of inflammatory and exudative macrophages in lung tissue had occurred. The ratio of CD206 positive F4/80+ CD11b+ cells (M2 macrophages) in lung tissue was higher in the OVA + ASD-PM2.5 treated mice than in the OVA + U-PM2.5 treated mice. These results suggest that the lung eosinophilia exacerbated by both PM2.5 is due to activation of a Th2-associated immune response along with induced M2 macrophages and the exacerbating effect is greater in microbial element (β-glucan)-rich ASD-PM2.5 than in organic chemical-rich U-PM2.5.

Introduction

Residents in big cities are commonly exposed to high concentrations of particulate matter (PM) due to anthropogenic air pollution caused by exhaust from automobiles, domestic/public incinerators, and industrial activities as well as sand dust storms. Consequently, there is considerable evidence that PM has a tremendous impact on respiratory health. Fine PM (PM2.5, particles less than 2.5 μm in size) are various in nature and may contain a large number of toxic substances; they can, moreover, stay in the atmosphere for a prolonged time, traverse long distances, and readily trigger asthma, bronchitis and other diseases (Bi, 2012). It is well-known that the smaller the particle size, the greater the harm it may cause (Yanran et al., 2015).

PM2.5 has been linked to the development and exacerbation of asthma and related diseases in Europe (Jacquemin et al., 2015), America (Young et al., 2014), Korea (Jeong et al., 2011), Japan (Michikawa et al., 2015) and China (Baccarelli et al., 2014). Epidemiological studies indicate that a PM2.5 level in ambient air is associated with increases in the incidence of asthma-related health problems, including, an uptick in emergency department visits for asthma at lag days 2 and 3 (Mar et al., 2010), worsening wheezing and dyspnea (Vempilly et al., 2013), and hospital admissions for asthma in children aged 0–18 years (Iskandar et al., 2012). A recent report showed that asthma morbidity was positively associated with daily ambient PM2.5 concentrations, both in warm and cool seasons (Delfino et al., 2014). Furthermore, PM2.5 can promote sensitization of common aeroallergens and the development of allergic respiratory diseases (Gavett et al., 2003).

Epidemiologic studies have suggested that the airborne desert-dust—so called PM10 which includes inhalable fine particles (PM2.5)—has various adverse effects to human, including an increase of daily admissions and clinic visits for asthma in Taiwan (Yang et al., 2005), deterioration of pulmonary function in asthmatic patients and aggravation of their symptoms at night in Korea (Park et al., 2005) and exacerbation of both adult asthma (Watanabe et al., 2011) and child asthma in Japan (Kanatani et al., 2010).

Anthropogenic PM2.5 contains large amounts of toxic chemicals formed from fossil fuel combustion, including polycyclic aromatic hydrocarbons (PAHs), sulfates (SO42 ), and nitrates (NO3). On the other hand, desert dust contains silica and large quantities of microbial material (He et al., 2013, Maki et al., 2010). However, there are no comparative studies measuring the relative respiratory health effects of PM2.5 from different origins. Such studies are in order because people in the East Asia region usually receive mixed exposure to anthropogenic PM2.5 and natural origin PM2.5.

In the present study, urban PM2.5 (U-PM2.5) was collected from the hazy weather atmosphere in Shenyang, China and ASD-PM2.5 was collected from the ambient air during Asian sand dust storm event days in Fukuoka, Japan. These PM2.5 samples were administered into the airways of mice to compare the effects of PM2.5 from different origins on allergic lung inflammation. The investigation included examination of pathologic change, cytological alteration in bronchoalveolar lavage fluid (BALF), changes in inflammatory cytokines and chemokines in BALF, and ovalbumin (OVA) specific IgE and IgG1 antibodies in serum. In the context of allergic airway inflammation, the contribution of the alternatively activated M2 macrophage with its specific functionality is of particular interest. The M2 macrophages in the mice lung tissue were also investigated because macrophages reportedly undergo M2 polarization during the acute phase of allergic airway inflammation in mouse models (Winkler et al., 2014).

Section snippets

Sample collections of PM2.5 from two areas

The PM sample was collected at China Medial University, Shenyang, China on March 24th, 2014, when a massive haze event was occurring in China. The air sample was collected with a four-stage multi nozzle cascade impactor (MCI) (Tokyo Dylec Co., Tokyo, Japan). The levels of size-classified mass and the elemental concentrations of PM2.5 were measured by a MCI combined with the 1st, 2nd and 3rd stages with 12-orifice and back-up stage according to a previously reported method (Ma et al., 2010). PM

Components found in PM samples

To clarify the relationship between toxic substances and the aggravation of allergic inflammatory responses by the PM2.5, the components in the two PM samples (U-PM2.5 and ASD-PM2.5) were analyzed.

Table 1 shows the results of major elements analysis. A total of 8 major elements were identified as well as element carbon (EC) and organic carbon (OC). In ASD-PM2.5, the concentration of Si (184 μg/mg) was the highest, followed by Al (58 μg/mg), Fe (40 μg/mg), and Ca (39 μg/mg). In U-PM2.5, the

Discussion

Epidemiologic studies demonstrate that the composition of PM2.5 may contribute to a higher prevalence of allergic diseases (Heinrich et al., 2000, Heinrich et al., 2002). In the present study, the exacerbating effects of PM2.5 (U-PM2.5 and ASD-PM2.5) collected from two different origins on lung eosinophilia were compared in order to investigate the role of PM2.5 components in the increased prevalence and severity of allergic diseases in the East Asian region. The results demonstrate that the

Conclusion

We found that PM2.5 sampled from different sources had differential effects. The lung eosinophilia exacerbated by both types of PM2.5 may be due to activation of a Th2-associated immune response along with induced M2 macrophages. Although the precise mechanism by which PM2.5 exacerbated lung eosinophilia is not fully understood, it might be mediated in part by PM2.5 containing toxic materials. Further studies to understand the mechanisms underlying this exacerbation are in order. The results of

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Conflict of interest disclosure

The authors declare that they have no competing interests.

Acknowledgments

This study was supported by grants from the Global Environment Research Fund (5-1457) of the Ministry of the Environment Japan and National Nature Science Foundation of China (81302403). We appreciate the vital contribution of students at Oita University of Nursing and Health Sciences in this research.

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