Advertisement

Environmental Science and Pollution Research

, Volume 25, Issue 36, pp 36136–36146 | Cite as

Effect of PM2.5 environmental pollution on rat lung

  • Biao Yang
  • Jie Guo
  • Chunling Xiao
Research Article
  • 105 Downloads

Abstract

Particulate matter smaller than 2.5 μm (PM2.5) is a continuing challenge to pulmonary health. Here, we investigated the mechanisms involved in PM2.5 exposure-induced acute lung injury in rats. We analyzed biochemical and morphological changes following a 2-week “real-world” exposure. And then we found that PM2.5 exposure increased the concentrations of total protein, malondialdehyde, hydrogen peroxide, nitric oxide, and soluble elastin in bronchoalveolar lavage fluid, levels of cytokines in blood, and expression of MMP-9 in airways. Further, alveolar macrophage and neutrophil counts increased following PM2.5 exposure, and edema and lung lesions were observed. Our results suggest that PM2.5 exposure can induce oxidative stress and acute inflammatory responses, which can damage the micro-environment and decrease the repair ability of the lung, resulting in tissue damage.

Keywords

PM2.5 Lung Injury Inflammation Oxidative stress Extracellular matrix 

Abbreviations

PM2.5

particulate matter with an aerodynamic diameter less than 2.5 μm

NS

neutral saline

MDA

malondialdehyde

H2O2

hydrogen peroxide

BALF

bronchoalveolar Lavage (BAL) fluid

AMs

alveolar macrophages

H&E

hematoxylin and eosin

ROS

reactive oxygen species

EDTA

ethylene diamine tetraacetic acid

PBS

phosphate buffer sulfate

BCA

bicinchoninic acid

ELISA

enzyme-linked immunosorbent assay

DAPI

DNA-binding dye propidium iodide

EBD

Evans blue dye

ALI

acute lung injury

ANOVA

analysis of variance

CNTF

cholinergic neurotrophic factor

IL

interleukin

MCP-1

monocyte chemotactic protein 1

MMP

metalloproteinases

RAGE

receptor for advanced glycation endproducts

TIMP-1

tissue inhibitor of metalloproteinase-1

DNA

deoxyribonucleic acid

TEM

transmission electron microscopy

Notes

Funding information

This study was financially supported by the National Natural Science Foundation of China (30872083) and Shenyang Nonprofit Science and Technology Project.

Compliance with ethical standards

All studies were performed according to protocols reviewed and approved by the Ethics Committee of Animal Care and Experimentation of the National Institute for Environmental Studies, China.

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

11356_2018_3492_MOESM1_ESM.docx (38 kb)
Table S1 (DOCX 38 kb)
11356_2018_3492_MOESM2_ESM.jpg (620 kb)
ESM 1 (JPG 619 kb)

References

  1. Barnes PJ (2004) Alveolar macrophages as orchestrators of COPD. COPD 1:59–70CrossRefGoogle Scholar
  2. Beelen R, Hoek G, Raaschou-Nielsen O, Stafoggia M, Andersen ZJ, Weinmayr G, Hoffmann B, Wolf K, Samoli E, Fischer PH, Nieuwenhuijsen MJ, Xun WW, Katsouyanni K, Dimakopoulou K, Marcon A, Vartiainen E, Lanki T, Yli-Tuomi T, Oftedal B, Schwarze PE, Nafstad P, De Faire U, Pedersen NL, Östenson CG, Fratiglioni L, Penell J, Korek M, Pershagen G, Eriksen KT, Overvad K, Sørensen M, Eeftens M, Peeters PH, Meliefste K, Wang M, Bueno-de-Mesquita HB, Sugiri D, Krämer U, Heinrich J, de Hoogh K, Key T, Peters A, Hampel R, Concin H, Nagel G, Jaensch A, Ineichen A, Tsai MY, Schaffner E, Probst-Hensch NM, Schindler C, Ragettli MS, Vilier A, Clavel-Chapelon F, Declercq C, Ricceri F, Sacerdote C, Galassi C, Migliore E, Ranzi A, Cesaroni G, Badaloni C, Forastiere F, Katsoulis M, Trichopoulou A, Keuken M, Jedynska A, Kooter IM, Kukkonen J, Sokhi RS, Vineis P, Brunekreef B (2015) Natural-cause mortality and long-term exposure to particle components: an analysis of 19 European cohorts within the multi-center ESCAPE project. Environ Health Perspect 123:525–533CrossRefGoogle Scholar
  3. Bihlet AR, Karsdal MA, Sand JM, Leeming DJ, Roberts M, White W, Bowler R (2017) Biomarkers of extracellular matrix turnover are associated with emphysema and eosinophilic-bronchitis in COPD. Respir Res 18:22CrossRefGoogle Scholar
  4. Butt Y, Kurdowska A, Allen TC (2016) Acute lung injury: a clinical and molecular review. Arch Pathol Lab Med 140:345–350CrossRefGoogle Scholar
  5. Chuturgoon AA, Phulukdaree A, Moodley D (2015) Fumonisin B1 inhibits apoptosis in HepG2 cells by inducing Birc-8/ILP-2. Toxicol Lett 235:67–74CrossRefGoogle Scholar
  6. Fubini B, Hubbard A (2003) Reactive oxygen species (ROS) and reactive nitrogen species (RNS) generation by silica in inflammation and fibrosis. Free Radic Biol Med 34:1507–1516CrossRefGoogle Scholar
  7. Goodman RB, Pugin J, Lee JS, Matthay MA (2003) Cytokine-mediated inflammation in acute lung injury. Cytokine Growth Factor Rev 14:523–535CrossRefGoogle Scholar
  8. Grommes J, Soehnlein O (2011) Contribution of neutrophils to acute lung injury. Mol Med 17:293–307CrossRefGoogle Scholar
  9. Gupta I, Ganguly S, Rozanas CR, Stuehr DJ, Panda K (2016) Ascorbate attenuates pulmonary emphysema by inhibiting tobacco smoke and Rtp801-triggered lung protein modification and proteolysis. Proc Natl Acad Sci U S A 113:E4208–E4217CrossRefGoogle Scholar
  10. He J, Turino GM, Lin YY (2010) Characterization of peptide fragments from lung elastin degradation in chronic obstructive pulmonary disease. Exp Lung Res 36:548–557CrossRefGoogle Scholar
  11. Hodge SJ, Hodge GL, Reynolds PN, Scicchitano R, Holmes M (2003) Increased production of TGF-beta and apoptosis of T lymphocytes isolated from peripheral blood in COPD. Am J Physiol Lung Cell Mol Physiol 285:L492–L499CrossRefGoogle Scholar
  12. Hu S, Li J, Xu X, Liu A, He H, Xu J, Chen Q, Liu S, Liu L, Qiu H, Yang Y (2016) The hepatocyte growth factor-expressing character is required for mesenchymal stem cells to protect the lung injured by lipopolysaccharide in vivo. Stem Cell Res Ther 7:66CrossRefGoogle Scholar
  13. Jeyaseelan S, Chu HW, Young SK, Worthen GS (2004) Transcriptional profiling of lipopolysaccharide-induced acute lung injury. Infect Immun 72:7247–7256CrossRefGoogle Scholar
  14. Jones VC, Birrell MA, Maher SA, Griffiths M, Grace M, O’Donnell VB, Clark SR, Belvisi MG (2016) Role of EP2 and EP4 receptors in airway microvascular leak induced by prostaglandin E2. Br J Pharmacol 173:992–1004CrossRefGoogle Scholar
  15. Kawabata K, Hagio T, Matsuoka S (2002) The role of neutrophil elastase in acute lung injury. Eur J Pharmacol 451:1–10CrossRefGoogle Scholar
  16. Kim HJ, Choi MG, Park MK, Seo YR (2017) Predictive and prognostic biomarkers of respiratory diseases due to particulate matter exposure. J Cancer Prev 22:6–15CrossRefGoogle Scholar
  17. Kristensen JH, Karsdal MA, Sand JM, Willumsen N, Diefenbach C, Svensson B, Hägglund P, Oersnes-Leeming DJ (2015) Serological assessment of neutrophil elastase activity on elastin during ECM remodeling. BMC Pulm Med 15:53CrossRefGoogle Scholar
  18. Kumar RK, Shadie AM, Bucknall MP, Rutlidge H, Garthwaite L, Herbert C, Halliburton B, Parsons KS, Wark PA (2015) Differential injurious effects of ambient and traffic-derived particulate matter on airway epithelial cells. Respirology 20:73–79CrossRefGoogle Scholar
  19. Li R, Kou X, Xie L, Cheng F, Geng H (2015) Effects of ambient PM2.5 on pathological injury, inflammation, oxidative stress, metabolic enzyme activity, and expression of c-fos and c-jun in lungs of rats. Environ Sci Pollut Res Int 22:20167–20176CrossRefGoogle Scholar
  20. Líbalová H, Krčková S, Uhlířová K, Milcová A, Schmuczerová J, Ciganek M, Kléma J, Machala M, Šrám RJ, Topinka J (2014) Genotoxicity but not the AhR-mediated activity of PAHs is inhibited by other components of complex mixtures of ambient air pollutants. Toxicol Lett 225:350–357CrossRefGoogle Scholar
  21. Liu Y, Zhuang J, Zhang X, Yue C, Zhu N, Yang L, Wang Y, Chen T, Wang Y, Zhang LW (2017) Autophagy associated cytotoxicity and cellular uptake mechanisms of bismuth nanoparticles in human kidney cells. Toxicol Lett 275:39–48CrossRefGoogle Scholar
  22. Lubos E, Handy DE, Loscalzo J (2008) Role of oxidative stress and nitric oxide in atherothrombosis. Front Biosci 13:5323–5344CrossRefGoogle Scholar
  23. Ma M, Li S, Jin H, Zhang Y, Xu J, Chen D, Kuimin C, Yuan Z, Xiao C (2015) Characteristics and oxidative stress on rats and traffic policemen of ambient fine particulate matter from Shenyang. Sci Total Environ 526:110–115CrossRefGoogle Scholar
  24. Mokra D, Kosutova P (2015) Biomarkers in acute lung injury. Respir Physiol Neurobiol 209:52–58CrossRefGoogle Scholar
  25. Murakami A, Ohigashi H (2007) Targeting NOX, INOS and COX-2 in inflammatory cells: chemoprevention using food phytochemicals. Int J Cancer 121:2357–2363CrossRefGoogle Scholar
  26. Okada S, Kita H, George TJ, Gleich GJ, Leiferman KM (1997) Migration of eosinophils through basement membrane components in vitro: role of matrixmetalloproteinase-9. Am J Respir Cell Mol Biol 17:519–528CrossRefGoogle Scholar
  27. Pope CA 3rd, Ezzati M, Dockery DW (2009) Fine-particulate air pollution and life expectancy in the United States. N Engl J Med 360:376–386CrossRefGoogle Scholar
  28. Porter DW, Millecchia LL, Willard P, Robinson VA, Ramsey D, McLaurin J, Khan A, Brumbaugh K, Beighley CM, Teass A, Castranova V (2006) Nitric oxide and reactive oxygen species production causes progressive damage in rats after cessation of silica inhalation. Toxicol Sci 90:188–197CrossRefGoogle Scholar
  29. Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24:981–990CrossRefGoogle Scholar
  30. Reddy AT, Lakshmi SP, Reddy RC (2012) The nitrated fatty acid 10-nitro-oleate diminishes severity of lps-induced acute lung injury in mice. PPAR Res 2012:617063Google Scholar
  31. Riva DR, Magalhães CB, Lopes AA, Lanças T, Mauad T, Malm O, Valença SS, Saldiva PH, Faffe DS, Zin WA (2011) Low dose of fine particulate matter (PM2.5) can induce acute oxidative stress, inflammation and pulmonary impairment in healthy mice. Inhal Toxicol 23:257–267CrossRefGoogle Scholar
  32. Rückerl D, Allen JE (2014) Macrophage proliferation, provenance, and plasticity in macroparasite infection. Immunol Rev 262:113–133CrossRefGoogle Scholar
  33. Saetta M, Turato G, Maestrelli P, Mapp CE, Fabbri LM (2001) Cellular and structural bases of chronic obstructive pulmonary disease. Am J Respir Crit Care Med 163:1304–1309CrossRefGoogle Scholar
  34. Sand JM, Knox AJ, Lange P, Sun S, Kristensen JH, Leeming DJ, Karsdal MA, Bolton CE, Johnson SR (2015) Accelerated extracellular matrix turnover during exacerbations of COPD. Respir Res 16:69CrossRefGoogle Scholar
  35. Shah AS, Langrish JP, Nair H, McAllister DA, Hunter AL, Donaldson K, Newby DE, Mills NL (2013) Global association of air pollution and heart failure: a systematic review and meta-analysis. Lancet 382:1039–1048CrossRefGoogle Scholar
  36. Shannahan JH, Schladweiler MC, Thomas RF, Ward WO, Ghio AJ, Gavett SH, Kodavanti UP (2012) Vascular and thrombogenic effects of pulmonary exposure to Libby amphibole. J Toxicol Environ Health A 75:213–231CrossRefGoogle Scholar
  37. Su ZQ, Mo ZZ, Liao JB, Feng XX, Liang YZ, Zhang X, Liu YH, Chen XY, Chen ZW, Su ZR, Lai XP (2014) Usnic acid protects LPS-induced acute lung injury in mice through attenuating inflammatory responses and oxidative stress. Int Immunopharmacol 22:371–378CrossRefGoogle Scholar
  38. Tasaka S, Amaya F, Hashimoto S, Ishizaka A (2008) Roles of oxidants and redox signaling in the pathogenesis of acute respiratory distress syndrome. Antioxid Redox Signal 10:739–753CrossRefGoogle Scholar
  39. Valyi-Nagy T, Olson SJ, Valyi-Nagy K, Montine TJ, Dermody TS (2000) Herpes simplex virus type 1 latency in the murine nervous system is associated with oxidative damage to neurons. Virology 278:309–321CrossRefGoogle Scholar
  40. Wang G, Zhao J, Jiang R, Song W (2013) Rat lung response to ozone and fine particulate matter (PM2.5) exposures. Environ Toxicol 30:343–356CrossRefGoogle Scholar
  41. Wang X, Chen M, Zhong M, Hu Z, Qiu L, Rajagopalan S, Fossett NG, Chen LC, Ying Z (2017) Exposure to concentrated ambient pm2.5 shortens lifespan and induces inflammation-associated signaling and oxidative stress in drosophila. Toxicol Sci 156:199–207Google Scholar
  42. Xu MX, Zhu YF, Chang HF, Liang Y (2016) Nanoceria restrains PM2.5-induced metabolic disorder and hypothalamus inflammation by inhibition of astrocytes activation related NF-κB pathway in Nrf2 deficient mice. Free Radic Biol Med 99:259–272CrossRefGoogle Scholar
  43. Zhang X, Huang H, Yang T, Ye Y, Shan J, Yin Z, Luo L (2010) Chlorogenic acid protects mice against lipopolysaccharide-induced acute lung injury. Injury 41:746–752CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Lab of Environmental Pollution and Microecology of Liaoning ProvinceShenyang Medical CollegeShenyangPeople’s Republic of China

Personalised recommendations