Abstract
Epidemiological studies demonstrate a linkage between morbidity and mortality and particulate matter (PM), particularly fine particulate matter (PM2.5) that can readily penetrate into the lungs and are therefore more likely to increase the incidence of respiratory and cardiovascular diseases. The present study investigated the compositions of cooking oil fume (COF)-derived PM2.5, which is the major source of indoor pollution in China. Furthermore, oxidative stress, cytotoxicity, apoptosis, and cell cycle arrest induced by COF-derived PM2.5 in primary fetal alveolar type II epithelial cells (AEC II cells) were also detected. N-acetyl-l-cysteine (NAC), a radical scavenger, was used to identify the role of oxidative stress in the abovementioned processes. Our results suggested that compositions of COF-derived PM2.5 are obviously different to PM2.5 derived from other sources, and COF-derived PM2.5 led to cell death, oxidative stress, apoptosis, and G0/G1 cell arrest in primary fetal AEC II cells. Furthermore, the results also showed that COF-derived PM2.5 induced apoptosis through the endoplasmic reticulum (ER) stress pathway, which is indicated by the increased expression of ER stress-related apoptotic markers, namely GRP78 and caspase-12. Besides, the induction of oxidative stress, cytotoxicity, apoptosis, and cell cycle arrest was reversed by pretreatment with NAC. These findings strongly suggested that COF-derived PM2.5-induced toxicity in primary fetal AEC II cells is mediated by increased oxidative stress, accompanied by ER stress which results in apoptosis.
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References
Astort F, Sittner M, Ferraro SA, et al (2013) Pulmonary inflammation and cell death in mice after acute exposure to air particulate matter from an industrial region of Buenos Aires. Arch Environ Contam Toxicol
Batenburg JJ, Ossendorp BC, Snoek GT et al (1994) Phospholipid-transfer proteins and their mRNAs in developing rat lung and in alveolar type-II cells. Biochem J 298(Pt 1):223–229
Bell ML, Zanobetti A, Dominici F (2013) Evidence on vulnerability and susceptibility to health risks associated with short-term exposure to particulate matter: a systematic review and meta-analysis. Am J Epidemiol 178:865–876
Bezergianni S, Dimitriadis A, Sfetsas T et al (2010) Hydrotreating of waste cooking oil for biodiesel production. Part II: effect of temperature on hydrocarbon composition. Bioresour Technol 101:7658–7660
Brook RD, Franklin B, Cascio W et al (2004) Air pollution and cardiovascular disease: a statement for healthcare professionals from the Expert Panel on Population and Prevention Science of the American Heart Association. Circulation 109:2655–2671
Brook RD, Bard RL, Morishita M, et al (2014) Hemodynamic, autonomic, and vascular effects of exposure to coarse particulate matter air pollution from a rural location. Environ Health Perspect
Cao J, Ding R, Wang Y et al (2013) Toxic effect of cooking oil fumes in primary fetal pulmonary type II-like epithelial cells. Environ Toxicol Pharmacol 36:320–331
Che Z, Liu Y, Chen Y et al (2014) The apoptotic pathways effect of fine particulate from cooking oil fumes in primary fetal alveolar type II epithelial cells. Mutat Res 761:35–43
Chen H, Burnett RT, Kwong JC et al (2013) Risk of incident diabetes in relation to long-term exposure to fine particulate matter in Ontario, Canada. Environ Health Perspect 121:804–810
Chin BY, Choi ME, Burdick MD et al (1998) Induction of apoptosis by particulate matter: role of TNF-alpha and MAPK. Am J Physiol 275:L942–L949
Chuang HC, Jones T, Chen Y et al (2011) Characterisation of airborne particles and associated organic components produced from incense burning. Anal Bioanal Chem 401:3095–3102
Dearth-Wesley T, Gordon-Larsen P, Adair LS et al (2011) Less traditional diets in Chinese mothers and children are similarly linked to socioeconomic and cohort factors but vary with increasing child age. J Nutr 141:1705–1711
Ferecatu I, Borot MC, Bossard C et al (2010) Polycyclic aromatic hydrocarbon components contribute to the mitochondria-antiapoptotic effect of fine particulate matter on human bronchial epithelial cells via the aryl hydrocarbon receptor. Part Fibre Toxicol 7:18
Ge K (2011) The transition of Chinese dietary guidelines and food guide pagoda. Asia Pac J Clin Nutr 20:439–446
Hemmingsen JG, Moller P, Nojgaard JK et al (2011) Oxidative stress, genotoxicity, and vascular cell adhesion molecule expression in cells exposed to particulate matter from combustion of conventional diesel and methyl ester biodiesel blends. Environ Sci Technol 45:8545–8551
Hou L, Zhang X, Dioni L et al (2013) Inhalable particulate matter and mitochondrial DNA copy number in highly exposed individuals in Beijing, China: a repeated-measure study. Part Fibre Toxicol 10:17
Jedrychowski WA, Perera FP, Spengler JD et al (2013) Intrauterine exposure to fine particulate matter as a risk factor for increased susceptibility to acute broncho-pulmonary infections in early childhood. Int J Hyg Environ Health 216:395–401
Kasper J, Hermanns MI, Bantz C et al (2011) Inflammatory and cytotoxic responses of an alveolar-capillary coculture model to silica nanoparticles: comparison with conventional monocultures. Part Fibre Toxicol 8:6
Kim JB, Kim C, Choi E et al (2012) Particulate air pollution induces arrhythmia via oxidative stress and calcium calmodulin kinase II activation. Toxicol Appl Pharmacol 259:66–73
Knothe G, Steidley KR (2009) A comparison of used cooking oils: a very heterogeneous feedstock for biodiesel. Bioresour Technol 100:5796–5801
Laing S, Wang G, Briazova T et al (2010) Airborne particulate matter selectively activates endoplasmic reticulum stress response in the lung and liver tissues. Am J Physiol Cell Physiol 299:C736–C749
Mahadevan B, Parsons H, Musafia T et al (2004) Effect of artificial mixtures of environmental polycyclic aromatic hydrocarbons present in coal tar, urban dust, and diesel exhaust particulates on MCF-7 cells in culture. Environ Mol Mutagen 44:99–107
Mansha M, Ghauri B, Rahman S et al (2012) Characterization and source apportionment of ambient air particulate matter (PM2.5) in Karachi. Sci Total Environ 425:176–183
Michael S, Montag M, Dott W (2013) Pro-inflammatory effects and oxidative stress in lung macrophages and epithelial cells induced by ambient particulate matter. Environ Pollut 183:19–29
Montiel-Davalos A, Sanchez MJ, Gallegos JL et al (2010) Oxidative stress and apoptosis are induced in human endothelial cells exposed to urban particulate matter. Toxicol In Vitro 24:135–141
Nishiwaki Y, Michikawa T, Takebayashi T et al (2013) Long-term exposure to particulate matter in relation to mortality and incidence of cardiovascular disease: the JPHC Study. J Atheroscler Thromb 20:296–309
Pereira G, Belanger K, Ebisu K et al (2014) Fine particulate matter and risk of preterm birth in Connecticut in 2000–2006: a longitudinal study. Am J Epidemiol 179:67–74
Piazzalunga A, Bernardoni V, Fermo P et al (2013) Optimisation of analytical procedures for the quantification of ionic and carbonaceous fractions in the atmospheric aerosol and applications to ambient samples. Anal Bioanal Chem 405:1123–1132
Pires A, de Melo EN, Mauad T et al (2011) Pre- and postnatal exposure to ambient levels of urban particulate matter (PM(2.5)) affects mice spermatogenesis. Inhal Toxicol 23:237–245
Sama P, Long TC, Hester S et al (2007) The cellular and genomic response of an immortalized microglia cell line (BV2) to concentrated ambient particulate matter. Inhal Toxicol 19:1079–1087
Wang T, Chiang ET, Moreno-Vinasco L et al (2010) Particulate matter disrupts human lung endothelial barrier integrity via ROS- and p38 MAPK-dependent pathways. Am J Respir Cell Mol Biol 42:442–449
Williams KM, Franzi LM, Last JA (2013) Cell-specific oxidative stress and cytotoxicity after wildfire coarse particulate matter instillation into mouse lung. Toxicol Appl Pharmacol 266:48–55
Wu M, Che W, Zhang Z (2008) Enhanced sensitivity to DNA damage induced by cooking oil fumes in human OGG1 deficient cells. Environ Mol Mutagen 49:265–275
Yi S, Zhang F, Qu F et al (2014) Water-insoluble fraction of airborne particulate matter (PM10) induces oxidative stress in human lung epithelial A549 cells. Environ Toxicol 29:226–233
Yin L, Niu Z, Chen X et al (2012) Chemical compositions of PM2.5 aerosol during haze periods in the mountainous city of Yong’an, China. J Environ Sci (China) 24:1225–1233
Zhang L, Yu J (2013) Role of apoptosis in colon cancer biology, therapy, and prevention. Curr Colorectal Cancer Rep 9
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This work was supported by the National Basic Research Programme of China (2013CB933900) and the Science Research Fund of Anhui Province (090413265X). The authors declare that they have no interest that could be constructed to have inappropriately influenced this work. We kindly thank the reviewers and editors for their work.
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Liu, Y., Chen, YY., Cao, JY. et al. Oxidative stress, apoptosis, and cell cycle arrest are induced in primary fetal alveolar type II epithelial cells exposed to fine particulate matter from cooking oil fumes. Environ Sci Pollut Res 22, 9728–9741 (2015). https://doi.org/10.1007/s11356-015-4140-4
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DOI: https://doi.org/10.1007/s11356-015-4140-4