Journal of Veterinary Science

The Korean Society of Veterinary Science (대한수의학회)
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PM2.5 in poultry houses synergizes with Pseudomonas aeruginosa to aggravate lung inflammation in mice through the NF-κB pathway

  • Li, Meng (College of Life Science, Ludong University) ;
  • Wei, Xiuli (Shandong Provincial Key Laboratory of Quality Safty Monitoring and Risk Assessment for Animal Products) ;
  • Li, Youzhi (Shandong Provincial Key Laboratory of Quality Safty Monitoring and Risk Assessment for Animal Products) ;
  • Feng, Tao (Shandong Provincial Key Laboratory of Quality Safty Monitoring and Risk Assessment for Animal Products) ;
  • Jiang, Linlin (College of Life Science, Ludong University) ;
  • Zhu, Hongwei (College of Life Science, Ludong University) ;
  • Yu, Xin (College of Life Science, Ludong University) ;
  • Tang, Jinxiu (College of Life Science, Ludong University) ;
  • Chen, Guozhong (College of Life Science, Ludong University) ;
  • Zhang, Jianlong (College of Life Science, Ludong University) ;
  • Zhang, Xingxiao (College of Life Science, Ludong University)
  • Received : 2019.12.13
  • Accepted : 2020.03.23
  • Published : 2020.05.31
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Abstract

Background: High concentrations of particulate matter less than 2.5 ㎛ in diameter (PM2.5) in poultry houses is an important cause of respiratory disease in animals and humans. Pseudomonas aeruginosa is an opportunistic pathogen that can induce severe respiratory disease in animals under stress or with abnormal immune functions. When excessively high concentrations of PM2.5 in poultry houses damage the respiratory system and impair host immunity, secondary infections with P. aeruginosa can occur and produce a more intense inflammatory response, resulting in more severe lung injury. Objectives: In this study, we focused on the synergistic induction of inflammatory injury in the respiratory system and the related molecular mechanisms induced by PM2.5 and P. aeruginosa in poultry houses. Methods: High-throughput 16S rDNA sequence analysis was used for characterizing the bacterial diversity and relative abundance of the PM2.5 samples, and the effects of PM2.5 and P. aeruginosa stimulation on inflammation were detected by in vitro and in vivo. Results: Sequencing results indicated that the PM2.5 in poultry houses contained a high abundance of potentially pathogenic genera, such as Pseudomonas (2.94%). The lung tissues of mice had more significant pathological damage when co-stimulated by PM2.5 and P. aeruginosa, and it can increase the expression levels of interleukin (IL)-6, IL-8, and tumor necrosis factor-α through nuclear factor (NF)-κB pathway in vivo and in vitro. Conclusions: The results confirmed that poultry house PM2.5 in combination with P. aeruginosa could aggravate the inflammatory response and cause more severe respiratory system injuries through a process closely related to the activation of the NF-κB pathway.

Keywords

Acknowledgement

This research was financially supported by the National Key Research and Development Program of China (Grant No. 2018YFD0501402), the Key Research and Development Plan of Shandong Province (No. 2017NC210009), the Major Agricultural Applied Technological Innovation Projects of Shandong Province, the Key Research and Development Plan of Yantai (No. 2018XSCC045), and the Innovation Team Project for Modern Agricultural Industrious Technology System of Shandong Province (SDAIT-11-10).

References

  1. Lippmann M. 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. 2014;44(4):299-347. https://doi.org/10.3109/10408444.2013.861796
  2. Xing YF, Xu YH, Shi MH, Lian YX. The impact of PM2.5 on the human respiratory system. J Thorac Dis 2016;8(1):E69-E74.
  3. Zhang J, Wei X, Jiang L, Li Y, Li M, Zhu H, Yu X, Tang J, Chen G, Zhang X. Bacterial Community Diversity in Particulate Matter (PM2.5 and PM10) Within Broiler Houses in Different Broiler Growth Stages Under Intensive Rearing Conditions in Summer. J Appl Poult Res. 2019;28(2):479-489. https://doi.org/10.3382/japr/pfz006
  4. Fiegel J, Clarke R, Edwards DA. Airborne infectious disease and the suppression of pulmonary bioaerosols. Drug Discov Today. 2006;11(1-2):51-57. https://doi.org/10.1016/S1359-6446(05)03687-1
  5. Isiugo K, Jandarov R, Cox J, Ryan P, Newman N, Grinshpun SA, Indugula R, Vesper S, Reponen T. Indoor particulate matter and lung function in children. Sci Total Environ. 2019;663:408-417. https://doi.org/10.1016/j.scitotenv.2019.01.309
  6. Huang Q, Hu D, Wang X, Chen Y, Wu Y, Pan L, Li H, Zhang J, Deng F, Guo X, Shen H. The modification of indoor PM2.5 exposure to chronic obstructive pulmonary disease in Chinese elderly people: A meet-inmetabolite analysis. Environ Int. 2018;121(Pt 2):1243-1252. https://doi.org/10.1016/j.envint.2018.10.046
  7. Chenxu G, Minxuan X, Yuting Q, Tingting G, Jinxiao L, Mingxing W, Sujun W, Yongjie M, Deshuai L, Qiang L, Linfeng H, Jun T. iRhom2 loss alleviates renal injury in long-term PM2.5-exposed mice by suppression of inflammation and oxidative stress. Redox Biol. 2018;19:147-157. https://doi.org/10.1016/j.redox.2018.08.009
  8. Hiraiwa K, van Eeden SF. Contribution of lung macrophages to the inflammatory responses induced by exposure to air pollutants. Mediators Inflamm. 2013;2013:619523. https://doi.org/10.1155/2013/619523
  9. Tang Q, Huang K, Liu J, Wu S, Shen D, Dai P, Li C. Fine particulate matter from pig house induced immune response by activating TLR4/MAPK/NF-κB pathway and NLRP3 inflammasome in alveolar macrophages. Chemosphere. 2019;236:124373. https://doi.org/10.1016/j.chemosphere.2019.124373
  10. Just N, Kirychuk S, Gilbert Y, Letourneau V, Veillette M, Singh B, Duchaine C. Bacterial diversity characterization of bioaerosols from cage-housed and floor-housed poultry operations. Environ Res. 2011;111(4):492-498. https://doi.org/10.1016/j.envres.2011.01.009
  11. Kearney GD, Shaw R, Prentice M, Tutor-Marcom R. Evaluation of respiratory symptoms and respiratory protection behavior among poultry workers in small farming operations. J Agromed. 2014;19(2):162-170. https://doi.org/10.1080/1059924X.2014.886536
  12. Jiang L, Zhang J, Tang J, Li M, Zhao X, Zhu H, Yu X, Li Y, Feng T, Zhang X. Analyses of aerosol concentrations and bacterial community structures for closed cage broiler houses at different broiler growth stages in winter. J Food Prot. 2018;81(9):1557-1564. https://doi.org/10.4315/0362-028x.jfp-17-524
  13. Arteaga V, Mitchell D, Armitage T, Tancredi D, Schenker M, Mitloehner F. Cage versus noncage laying-hen housings: respiratory exposures. J Agromed. 2015;20(3):245-255. https://doi.org/10.1080/1059924X.2015.1044681
  14. Musavi L, Lopez J, Cho R, Siegel N, Seal S, Dorafshar AH, Steinberg JP. Infectious complications after open cranial vault remodeling for craniosynostosis. J Craniofac Surg. Forthcoming 2019.
  15. Rybtke M, Hultqvist LD, Givskov M, Tolker-Nielsen T. Pseudomonas aeruginosa biofilm infections: community structure, antimicrobial tolerance and immune response. J Mol Biol. 2015;427(23):3628-3645. https://doi.org/10.1016/j.jmb.2015.08.016
  16. Walker SE, Sander JE, Cline JL, Helton JS. Characterization of Pseudomonas aeruginosa isolates associated with mortality in broiler chicks. Avian Dis. 2002;46(4):1045-1050. https://doi.org/10.1637/0005-2086(2002)046[1045:COPAIA]2.0.CO;2
  17. Psoter KJ, De Roos AJ, Mayer JD, Kaufman JD, Wakefield J, Rosenfeld M. Fine particulate matter exposure and initial Pseudomonas aeruginosa acquisition in cystic fibrosis. Ann Am Thorac Soc. 2015;12(3):385-391. https://doi.org/10.1513/AnnalsATS.201408-400OC
  18. Tamura N, Hazeki K, Okazaki N, Kametani Y, Murakami H, Takaba Y, Ishikawa Y, Nigorikawa K, Hazeki O. Specific role of phosphoinositide 3-kinase p110alpha in the regulation of phagocytosis and pinocytosis in macrophages. Biochem J. 2009;423(1):99-108. https://doi.org/10.1042/BJ20090687
  19. Franzi LM, Linderholm AL, Rabowsky M, Last JA. Lung toxicity in mice of airborne particulate matter from a modern layer hen facility containing Proposition 2-compliant animal caging. Toxicol Ind Health. 2017;33(3):211-221. https://doi.org/10.1177/0748233716630490
  20. Meng K, Wu B, Gao J, Cai Y, Yao M, Wei L, Chai T. Immunity-related protein expression and pathological lung damage in mice poststimulation with ambient particulate matter from live bird markets. Front Immunol. 2016;7:252.
  21. Ma QY, Huang DY, Zhang HJ, Wang S, Chen XF. Exposure to particulate matter 2.5 (PM2.5) induced macrophage-dependent inflammation, characterized by increased Th1/Th17 cytokine secretion and cytotoxicity. Int Immunopharmacol. 2017;50:139-145. https://doi.org/10.1016/j.intimp.2017.06.019
  22. He M, Ichinose T, Yoshida S, Ito T, He C, Yoshida Y, Arashidani K, Takano H, Sun G, Shibamoto T. PM2.5-induced lung inflammation in mice: differences of inflammatory response in macrophages and type II alveolar cells. J Appl Toxicol. 2017;37(10):1203-1218. https://doi.org/10.1002/jat.3482
  23. Zhou Y, Li P, Goodwin AJ, Cook JA, Halushka PV, Chang E, Zingarelli B, Fan H. Exosomes from endothelial progenitor cells improve outcomes of the lipopolysaccharide-induced acute lung injury. Crit Care. 2019;23(1):44. https://doi.org/10.1186/s13054-019-2339-3
  24. Matute-Bello G, Downey G, Moore BB, Groshong SD, Matthay MA, Slutsky AS, Kuebler WM; Acute Lung Injury in Animals Study Group. An official American Thoracic Society workshop report: features and measurements of experimental acute lung injury in animals. Am J Respir Cell Mol Biol. 2011;44(5):725-738. https://doi.org/10.1165/rcmb.2009-0210ST
  25. Wang S, Chi Q, Hu X, Cong Y, Li S. Hydrogen sulfide-induced oxidative stress leads to excessive mitochondrial fission to activate apoptosis in broiler myocardia. Ecotoxicol Environ Saf. 2019;183:109578-109578. https://doi.org/10.1016/j.ecoenv.2019.109578
  26. Shi Q, Wang W, Chen M, Zhang H, Xu S. Ammonia induces Treg/Th1 imbalance with triggered NF-κB pathway leading to chicken respiratory inflammation response. Sci Total Environ. 2019;659:354-362. https://doi.org/10.1016/j.scitotenv.2018.12.375
  27. Zhang J, Li Y, Xu E, Jiang L, Tang J, Li M, Zhao X, Chen G, Zhu H, Yu X, Zhang X. Bacterial communities in PM2.5 and PM10 in broiler houses at different broiler growth stages in spring. Pol J Vet Sci 2019;22(3):495-504.
  28. Jiang L, Li M, Tang J, Zhao X, Zhang J, Zhu H, Yu X, Li Y, Feng T, Zhang X. Effect of different disinfectants on bacterial aerosol diversity in poultry houses. Front Microbiol. 2018;9:2113. https://doi.org/10.3389/fmicb.2018.02113
  29. Los-Arcos I, Len O, Martin-Gomez MT, Baroja A, Berastegui C, Deu M, Sacanell J, Roman A, Gavalda J. Clinical characteristics and outcome of lung transplant recipients with respiratory isolation of Corynebacterium spp. J Clin Microbiol. 2018;56(8):e00142-e00118.
  30. Gong Q, Ruan MD, Niu MF, Qin CL, Hou Y, Guo JZ. Immune efficacy of DNA vaccines based on oprL and oprF genes of Pseudomonas aeruginosa in chickens. Poult Sci. 2018;97(12):4219-4227. https://doi.org/10.3382/ps/pey307
  31. Azam MW, Khan AU. Updates on the pathogenicity status of Pseudomonas aeruginosa. Drug Discov Today. 2019;24(1):350-359. https://doi.org/10.1016/j.drudis.2018.07.003
  32. Garau J, Gomez L. Pseudomonas aeruginosa pneumonia. Curr Opin Infect Dis. 2003;16(2):135-143. https://doi.org/10.1097/00001432-200304000-00010
  33. Do H, Pyo S, Sohn EH. Suppression of iNOS expression by fucoidan is mediated by regulation of p38 MAPK, JAK/STAT, AP-1 and IRF-1, and depends on up-regulation of scavenger receptor B1 expression in TNF-alpha- and IFN-gamma-stimulated C6 glioma cells. J Nutr Biochem. 2010;21(8):671-679. https://doi.org/10.1016/j.jnutbio.2009.03.013
  34. Li W, Cai ZN, Mehmood S, Liang LL, Liu Y, Zhang HY, Chen Y, Lu YM. Anti-inflammatory effects of Morchella esculenta polysaccharide and its derivatives in fine particulate matter-treated NR8383 cells. Int J Biol Macromol. 2019;129:904-915. https://doi.org/10.1016/j.ijbiomac.2019.02.088
  35. Xu Z, Li Z, Liao Z, Gao S, Hua L, Ye X, Wang Y, Jiang S, Wang N, Zhou D, Deng X. PM2.5 induced pulmonary fibrosis in vivo and in vitro. Ecotoxicol Environ Saf. 2019;171:112-121. https://doi.org/10.1016/j.ecoenv.2018.12.061
  36. Li X, Huang Q, Ong CN, Yang XF, Shen HM. Chrysin sensitizes tumor necrosis factor-alpha-induced apoptosis in human tumor cells via suppression of nuclear factor-kappaB. Cancer Lett. 2010;293(1):109-116. https://doi.org/10.1016/j.canlet.2010.01.002
  37. Al Hanai AH, Antkiewicz DS, Hemming JD, Shafer MM, Lai AM, Arhami M, Hosseini V, Schauer JJ. Seasonal variations in the oxidative stress and inflammatory potential of PM2.5 in Tehran using an alveolar macrophage model; the role of chemical composition and sources. Environ Int. 2019;123:417-427. https://doi.org/10.1016/j.envint.2018.12.023
  38. Ayaub EA, Dubey A, Imani J, Botelho F, Kolb MR, Richards CD, Ask K. Overexpression of OSM and IL-6 impacts the polarization of pro-fibrotic macrophages and the development of bleomycin-induced lung fibrosis. Sci Rep. 2017;7(1):13281-13281. https://doi.org/10.1038/s41598-017-13511-z
  39. Tian G, Wang J, Lu Z, Wang H, Zhang W, Ding W, Zhang F. Indirect effect of PM1 on endothelial cells via inducing the release of respiratory inflammatory cytokines. Toxicol In Vitro. 2019;57:203-210. https://doi.org/10.1016/j.tiv.2019.03.013
  40. Coates BM, Staricha KL, Koch CM, Cheng Y, Shumaker DK, Budinger GR, Perlman H, Misharin AV, Ridge KM. Inflammatory monocytes drive influenza a virus-mediated lung injury in juvenile mice. J Immunol. 2018;200(7):2391-2404. https://doi.org/10.4049/jimmunol.1701543
  41. Stravinskas Durigon T, MacKenzie B, Carneiro Oliveira-Junior M, Santos-Dias A, De Angelis K, Malfitano C, Kelly da Palma R, Moreno Guerra J, Damaceno-Rodrigues NR, Garcia Caldini E, de Almeida FM, Aquino-Santos HC, Rigonato-Oliveira NC, Leal de Oliveira DB, Aimbire F, Ligeiro de Oliveira AP, Franco de Oliveira LV, Durigon EL, Hiemstra PS, Vieira RP. Aerobic Exercise Protects from Pseudomonas aeruginosaInduced Pneumonia in Elderly Mice. J Innate Immun. 2018;10(4):279-290. https://doi.org/10.1159/000488953
  42. Dou C, Zhang J, Qi C. Cooking oil fume-derived PM2.5 induces apoptosis in A549 cells and MAPK/NF-κB/STAT1 pathway activation. Environ Sci Pollut Res Int. 2018;25(10):9940-9948. https://doi.org/10.1007/s11356-018-1262-5
  43. Yoon YK, Woo HJ, Kim Y. Orostachys japonicus inhibits expression of the TLR4, NOD2, iNOS, and COX-2 genes in LPS-stimulated human PMA-differentiated THP-1 cells by inhibiting NF-κB and MAPK activation. Evid Based Complement Alternat Med. 2015;2015:682019.
  44. Valacchi G, Pagnin E, Phung A, Nardini M, Schock BC, Cross CE, van der Vliet A. Inhibition of NFkappaB activation and IL-8 expression in human bronchial epithelial cells by acrolein. Antioxid Redox Signal. 2005;7(1-2):25-31. https://doi.org/10.1089/ars.2005.7.25
  45. Wang J, Wang H, Zhang H, Liu Z, Ma C, Kang W. Immunomodulation of ADPs-1a and ADPs-3a on RAW264.7 cells through NF-κB/MAPK signaling pathway. Int J Biol Macromol. 2019;132:1024-1030. https://doi.org/10.1016/j.ijbiomac.2019.04.031
  46. Hu X, Chi Q, Liu Q, Wang D, Zhang Y, Li S. Atmospheric H2S triggers immune damage by activating the TLR-7/MyD88/NF-κB pathway and NLRP3 inflammasome in broiler thymus. Chemosphere. 2019;237:124427-124427. https://doi.org/10.1016/j.chemosphere.2019.124427