Korean Journal of Food Science and Technology (한국식품과학회지)

Korean Society of Food Science and Technology (한국식품과학회)
권호 표지
DOI QR코드

DOI QR Code

Inhibitory effect of ethanol extract of Codonopsis lanceolata against oxidative stress and disruption of tight cell junction in NCI-H441 cells after exposure to urban particulate matter

더덕 에탄올 추출물의 도시미세먼지 노출로 인한 폐 세포 산화스트레스 발생과 세포밀착연접 손상 억제 효과

  • So, Hee-Jung (Department of Food Bioscience and Technology, Graduate School of Life and Environmental Science, Korea University) ;
  • Chun, Su-Hyun (Institute of Biomedical Science and Food Safety, Korea University) ;
  • Lee, Jin-Won (Faculty of Health and Food/Medicinal Plant, Suwon Women University) ;
  • Lee, Kwang-Won (Department of Biotechnology, College of Life Sciences and Biotechnology, Korea University)
  • 소희정 (고려대학교 생명환경과학대학원 식품공학과) ;
  • 전수현 (고려대학교 식품생의학안전연구소) ;
  • 이진원 (수원여자대학교 보건식품학부 약용식물과) ;
  • 이광원 (고려대학교 일반대학원 생명공학과)
  • Received : 2021.01.26
  • Accepted : 2021.03.12
  • Published : 2021.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

One of the major sources of air pollution is urban particulate matter (UPM), which causes lung diseases involving oxidative stress, inflammation, and cancer. Codonopsis lanceolata (CL) has been used in East Asia as a traditional oriental medicinal ingredient for lung diseases (e.g., asthma and bronchitis). However, the connection between the impact of CL and UPM in the lungs has rarely been investigated. This study aimed to confirm the inhibitory activity of the ethanol extract of CL (ECL) against oxidative stress and disruption of tight cell junctions in human pulmonary epithelial cells after exposure to UPM. As the lung cells were pre-treated with ECL, the UPM-induced increase in cellular reactive oxygen species production suppressed tight junction proteins (e.g., N-cadherin, fibronectin, occludin, zonula occludens-1, and claudin-4). These results suggest that ECL prevents the possible effects of UPM toxicity on the lungs.

본 연구에서는 UPM에 의해 유발되는 NCI-H441 세포 내 ROS 생성과 그에 따른 tight junction 단백질(N-cadherin, fibronectin, occluding, ZO-1, 및 claudin-4 등)의 발현 억제를 확인하였고 ECL의 전처리로 인하여 해당 ROS 생성 및 tight junction 단백질 발현 억제 현상이 완화되는 보호효과를 확인하였다. 그 결과, 폐 세포에서 UPM에 의해 유발된 산화 스트레스 및 tight junction 단백질의 발현 감소가 ECL을 선 처리함으로써 억제되어 결과적으로 산화 스트레스와 같은 미세먼지에 의한 폐 손상으로부터 보호 효과를 나타내고 tight junction 수준의 유지를 확인하였다. 이러한 결과를 통해 ECL 추출물은 폐와 기관지의 보호효과를 나타내며 폐 관련 질병의 예방효과가 있는 기능성 천연 물질로써 활용이 가능할 것으로 기대된다.

Keywords

References

  1. Ahn JY, Kim JS, Lee MD, Lee SU, Jeon HE, Oh J, Park SM, Jo JG, Seo WH, Lee SJ, Do WS, Lee BW, Lee SW, Ha HS, Yu HJ, Seo KY, Kim SH, Kwon SM, Lee KW. Study on the Composition of PM2.5 in the Yellow Sand and Fine Particle. National Institute of Environmental Research. pp. 1-118 (2008)
  2. Anderson JO, Thundiyil JG, Stolbach A. Clearing the air: a review of the effects of particulate matter air pollution on human health. J. Med. Toxicol. 8: 166-175 (2012) https://doi.org/10.1007/s13181-011-0203-1
  3. Barnes PJ. Chronic obstructive pulmonary disease. N. Engl. J. Med. 343: 269-280 (2000) https://doi.org/10.1056/NEJM200007273430407
  4. Beeman NE, Baumgartner HK, Webb PG, Schaack JB, Neville MC. Disruption of occludin function in polarized epithelial cells activates the extrinsic pathway of apoptosis leading to cell extrusion without loss of transepithelial resistance. BMC Cell Biol. 10: 85 (2009) https://doi.org/10.1186/1471-2121-10-85
  5. Choe SY, Yang KH. Toxicological studies of antioxidants butylated hydroxytoluene (BHT) and butylated hydroxy anisol (BHA). Korean J. Food Sci. Technol. 14:283-288 (1982)
  6. Chosa N, Ishisaki A. Two novel mechanisms for maintenance of stemness in mesenchymal stem cells: SCRG1/BST1 axis and cell-cell adhesion through N-cadherin. Jpn. Dent. Sci. Rev. 54: 37-44 (2018) https://doi.org/10.1016/j.jdsr.2017.10.001
  7. Cunningham KE, Turner JR. Myosin light chain kinase: pulling the strings of epithelial tight junction function. Ann. N. Y. Acad. Sci. 1258: 34-42 (2012) https://doi.org/10.1111/j.1749-6632.2012.06526.x
  8. Donaldson K, Stone V. Current hypotheses on the mechanisms of toxicity of ultrafine particles. Ann. Ist. Super. Sanita. 39: 405-410 (2003)
  9. Ghim YS, Choi Y, Kim S, Bae CH, Park J, Shin HJ. Evaluation of Model Performance for Forecasting Fine Particle Concentrations in Korea. Aerosol Air Qual. Res. 17: 1856-1864 (2017) https://doi.org/10.4209/aaqr.2016.10.0446
  10. Guan L, Rui W, Bai R, Zhang W, Zhang F, Ding W. Effects of Size-Fractionated Particulate Matter on Cellular Oxidant Radical Generation in Human Bronchial Epithelial BEAS-2B Cells. Int. J. Environ. Res. Public Health. 13: 483 (2016) https://doi.org/10.3390/ijerph13050483
  11. Gumbiner B. Structure, biochemistry, and assembly of epithelial tight junctions. Am. J. Physiol. Cell Physiol. 253: 749-758 (1987) https://doi.org/10.1152/ajpcell.1987.253.6.C749
  12. Ha SJ, Jung SK. Functional Food for Particulate Matter, Food Ind. Nutr. 22: 33-37 (2017)
  13. Hagerman A, Harvey MI., Makkar HPS. Quantification of tannins in tree foliage: a laboratory manual for the FAO/IAEA co-ordinated research project on 'The use of nuclear and related techniques to develop simple tannin assays for predicting and improving the safety and efficiency of feeding ruminants on tanninferous tree foliage.' FAO/IAEA Working Document IAEA, Vienna. pp. 4-7 (2000)
  14. Hur GY, Choi GS, Park HJ, Ye YM, Park HS. Anaphylactic shock induced by Codonopsis lanceolata, traditional Chinese medicine in a patient with allergic rhinitis. Allergy 63: 1406-1407 (2008) https://doi.org/10.1111/j.1398-9995.2008.01837.x
  15. International Agency for Research on Cancer (IARC). IARC Monographs on the evaluation of carcinogenic risks to humans, No. 109-Outdoor air pollution. Lyon, France. pp. 135-188 (2015)
  16. Jeon SM, Kim SY, Kim IH, Go JS, Kim HR, Jeong JY, Lee HY, Park DS. Antioxidant Activities of Processed Deoduck (Codonopsis lanceolata) Extract. J. Korean Soc. Food Sci. Nutr. 42: 924-932 (2013) https://doi.org/10.3746/JKFN.2013.42.6.924
  17. Kim TW, Joh EH, Kim B, Kim DH. Ginsenoside Rg5 ameliorates lung inflammation in mice by inhibiting the binding of LPS to toll-like receptor-4 on macrophages. Int. Immunopharmacol. 12: 110-116 (2012) https://doi.org/10.1016/j.intimp.2011.10.023
  18. Kitagaki H, Tsugawa M. 1,1-diphenyl-2-picrylhydrazyl radical (DPPH) scavenging ability of sake during storage. J Biosci. Bioeng. 87: 328-332 (1999) https://doi.org/10.1016/S1389-1723(99)80040-1
  19. Knekt P, Kumpulainen J, Jarvinen R, Rissanen H, Heliovaara M, Reunanen A, Hakulinen T, Aromaa A. Flavonoid intake and risk of chronic diseases. Am. J. Clin. Nutr. 76: 560-568 (2002) https://doi.org/10.1093/ajcn/76.3.560
  20. Korea Institute of Oriental Medicine (KIOM). Korea Oriental Medicine Data Base Mediclassics- Donguibogam (principles and practice of eastern medicine), No. 4.24-Codonopsis lanceolate. Available from: https://mediclassics.kr/books/8/volume/21#content_999 (2014)
  21. Lee DC, Choi H, Oh JM, Lee DH, Kim SW, Kim SW, Kim BG, Cho JH, Lee J. Protective effects of α-lipoic acid on cultured human nasal fibroblasts exposed to urban particulate matter. Int. Forum Allergy Rhinol. 9: 638-647 (2019a) https://doi.org/10.1002/alr.22296
  22. Lee DC, Choi H, Oh JM, Lee J, Lee J, Lee HY, Kang JY. Urban particulate matter regulates tight junction proteins by inducing oxidative stress via the Akt signal pathway in human nasal epithelial cells. Toxicol. Lett. 333: 33-41 (2020) https://doi.org/10.1016/j.toxlet.2020.07.017
  23. Lee KW, Jung HJ, Park HJ, Kim DG, Lee JY, Lee KT. Beta-D-xylopyranosyl-(1→3)-beta-D-glucuronopyranosyl echinocystic acid isolated from the roots of Codonopsis lanceolata induces caspase-dependent apoptosis in human acute promyelocytic leukemia HL-60 cells. Biol. Pharm. Bull. 28: 854-859 (2005a) https://doi.org/10.1248/bpb.28.854
  24. Lee HS, Jung SH, Yun BS, Lee KW. Isolation of chebulic acid from Terminalia chebula Retz. and its antioxidant effect in isolated rat hepatocytes. Arch. Toxicol. 81: 211-218 (2007a) https://doi.org/10.1007/s00204-006-0139-4
  25. Lee YG, Kim JY, Lee JY, Byeon SE, Hong EK, Lee J. Regulatory effects of Codonopsis lanceolata on macrophage-mediated immune responses. J. Ethnopharmacol. 112: 180-188 (2007b) https://doi.org/10.1016/j.jep.2007.02.026
  26. Lee YS, Kim HE, Kim J, Seol GH, Lee KW. Lancemaside A, a major triterpene saponin of Codonopsis lanceolata enhances regulation of nitric oxide synthesis via eNOS activation. BMC Complement Altern. Med. 19: 110 (2019b) https://doi.org/10.1186/s12906-019-2516-6
  27. Lee JH, Lee JY, Kim MJ, Kim HJ, Lee SH, Jeon BG. Cytotoxicity of Particulate Matter in Various Human Cells Lines. J. Life Sci. 29: 724-734 (2019c) https://doi.org/10.5352/JLS.2019.29.6.724
  28. Lee KW, Nam MH, Lee HR, Hong CO, Lee KW. Protective effects of chebulic acid on alveolar epithelial damage induced by urban particulate matter. BMC Complement Altern. Med. 17: 373 (2017) https://doi.org/10.1186/s12906-017-1870-5
  29. Lee HR, Pyo MC, Chae SA, Hong CO, Lee KW. Inhibitory Effect of Chebulic Acid on Alveolar Epithelial to Mesenchymal Transition in Response to Urban Particulate Matter Using Co-treatment and Post-treatment Exposure. Biol. Pharm. Bull. 42: 1322-1331 (2019d) https://doi.org/10.1248/bpb.b19-00061
  30. Lee HS, Won NH, Kim KH, Lee H, Jun W, Lee KW. Antioxidant effects of aqueous extract of Terminalia chebula in vivo and in vitro. Biol. Pharm. Bull. 28: 1639-1644 (2005b) https://doi.org/10.1248/bpb.28.1639
  31. Li HB, Wong CC, Cheng KW, Chen F. Antioxidant properties in vitro and total phenolic contents in methanol extracts from medicinal plants. LWT-Food Sci. Technol. 41: 385-390 (2008) https://doi.org/10.1016/j.lwt.2007.03.011
  32. Ljubimova JY, Braubach O, Patil R, Chiechi A, Tang J, Galstyan A, Shatalova ES, Kleinman MT, Black KL, Holler E. Coarse particulate matter (PM2.5-10) in Los Angeles Basin air induces expression of inflammation and cancer biomarkers in rat brains. Sci. Rep. 8: 5708 (2018) https://doi.org/10.1038/s41598-018-23885-3
  33. Mann EH, Ho TR, Pfeffer PE, Matthews NC, Chevretton E, Mudway I, Kelly FJ, Hawrylowicz CM. Vitamin D Counteracts an IL-23-Dependent IL-17A+IFN-γ+ Response Driven by Urban Particulate Matter. Am. J. Respir. Cell Mol. Biol. 57: 1-12 (2017) https://doi.org/10.1165/rcmb.2017-0070ED
  34. Ministry of Environment (ME). Enforcement Decree of the Clean Air Conservation Act. Ministry of Environment, Sejong, Republic of Korea (2019)
  35. Ministry of Environment (ME). Enforcement Decree of the Framework Act on Environmental Policy Attached Sheet 1-Environmental standards. Ministry of Environment, Sejong, Republic of Korea (2020)
  36. Pankov R, Yamada KM. Fibronectin at a glance. J. Cell Sci. 115: 3861-3863 (2002) https://doi.org/10.1242/jcs.00059
  37. Park KH, Kim JH, Yoon HS, Kim IH, Choi IM, Lee JY, Ju MK. Correlation between Coarse Airborne Particulate Matter and Mortality Rates of Malignant Neoplasm. Korean J. Health Promot. 16: 215-222 (2016) https://doi.org/10.15384/kjhp.2016.16.4.215
  38. Park SK, Kang JY, Kim JM, Yoo SK, Han HJ, Shin EJ, Heo HJ. Cellular protective effect of Ecklonia cava extract on ultra-fine dust (PM2.5)-induced cytoxicity. Korean J. Food Sci. Technol. 51: 503-508 (2019) https://doi.org/10.9721/KJFST.2019.51.5.503
  39. Park KS, Kim YJ, Yoon JY, Kyung SY, An CH, Lee SP, Park JW, Jeong SH. Particulate Matter 10 from Asian Dust Storms Induces the Expression of Reactive Oxygen Species, NF-κB, TGF-β and Fibronectin in WI-26 VA4 Epithelial Cells. Tuberc. Respir. Dis. 65: 504-511 (2008) https://doi.org/10.4046/trd.2008.65.6.504
  40. Park SJ, Song SW, Seong DH, Park DS, Kim SS, Gou J, Ahn JH, Yoon WB, Lee HY. Biological Activities in the Extract of Fermented Codonopsis lanceolata. J. Korean Soc. Food Sci. Nutr. 38: 983-988 (2009) https://doi.org/10.3746/JKFN.2009.38.8.983
  41. Patel, VJ, Roy SB, Mehta HJ, Joo M, Sadikot RT. Alternative and natural therapies for acute lung injury and acute respiratory distress syndrome. BioMed Res. Int. 2018: 1-10 (2018)
  42. Quay JL, Reed W, Samet J, Devlin RB. Air Pollution Particles Induce IL-6 Gene Expression in Human Airway Epithelial Cells via NF-kappa B Activation. Am. J. Respir. Cell Mol. Biol. 19: 98-106 (1998) https://doi.org/10.1165/ajrcmb.19.1.3132
  43. Santana FPR, Pinheiro NM, Mernak MIB, Righetti RF, Martins MA, Lago JHG, dos Santos Lopes FDTQ, Tiberio IFLC, Prado CM. Evidences of Herbal Medicine-Derived Natural Products Effects in Inflammatory Lung Diseases. Mediators Inflamm. 2016: 1-14 (2016)
  44. Seo YS, Kim HS, Lee AY, Chun JM, Kim SB, Moon BC, Kwon BI. Codonopsis lanceolata attenuates allergic lung inflammation by inhibiting Th2 cell activation and augmenting mitochondrial ROS dismutase (SOD2) expression. Sci. Rep. 9: 2312 (2019) https://doi.org/10.1038/s41598-019-38782-6
  45. Shin YK, Han AY, Hsieh YS, Kwon SH, Kim JH, Lee KW, Seol GH. Lancemaside A from Codonopsis lanceolata prevents hypertension by inhibiting NADPH oxidase 2-mediated MAPK signalling and improving NO bioavailability in rats. J. Pharm. Pharmacol. 71: 1458-1468 (2019) https://doi.org/10.1111/jphp.13140
  46. Song CH, Seo YC, Choi WY, Lee CG, Kim DU, Chung JY, Chung HC, Park DS, Ma CJ, Lee HY. Enhancement of Antioxidative Activity of Codonopsis lanceolata by Stepwise Steaming Process. Korean J. Med. Crop Sci. 20: 238-244 (2012) https://doi.org/10.7783/KJMCS.2012.20.4.238
  47. Valavanidis A, Vlachogianni T, Fiotakis K, Loridas S. Pulmonary oxidative stress, inflammation and cancer: respirable particulate matter, fibrous dusts and ozone as major causes of lung carcinogenesis through reactive oxygen species mechanisms. Int. J. Environ. Res. Public Health 10: 3886-3907 (2013) https://doi.org/10.3390/ijerph10093886
  48. Vermette D, Hu P, Canarie MF, Funaro M, Glover J, Pierce RW. Tight junction structure, function, and assessment in the critically ill: a systematic review. Intensive Care Med. Exp. 6: 37 (2018) https://doi.org/10.1186/s40635-018-0203-4
  49. Wang J, Huang J, Wang L, Chen C, Yang D, Jin M, Bai C, Song Y. Urban particulate matter triggers lung inflammation via the ROS-MAPK-NF-κB signaling pathway. J. Thorac. Dis. 9: 4398-4412 (2017) https://doi.org/10.21037/jtd.2017.09.135
  50. Wang M, Yang L, Ji M, Zhao P, Sun P, Bai R, Tian Y, Su L, Li C. Aqueous extract of Terminalia chebula induces apoptosis in lung cancer cells via a mechanism involving mitochondria-mediated pathways. Braz. Arch. Biol. Technol. 58: 208-215 (2015) https://doi.org/10.1590/S1516-8913201400202
  51. World Health Organization (WHO). 3rd Meeting of the Global Platform on Air Quality and Health, Madrid, 7-9 March 2017 - Meeting Report (2017). Available from: https://www.who.int/airpollution/global-platform/Global_Platform_Consultation_Report_3rd_Meeting_DRAFT_30_May_2017.pdf?ua=1. Accessed May (2017)
  52. World Health Organization (WHO). Exposure to ambient air pollution from particulate matter for 2016. Version 2. Available from: https://www.who.int/airpollution/ambient/AAP_exposure_Apr2018_final.pd f?ua=1. Accessed Apr. (2018)
  53. Wray C, Mao Y, Pan J, Chandrasena A, Piasta F, Frank JA. Claudin-4 augments alveolar epithelial barrier function and is induced in acute lung injury. Am. J. Physiol. Lung Cell Mol. Physiol. 297: L219-L227 (2009) https://doi.org/10.1152/ajplung.00043.2009
  54. Xu LP, Wang H, Yuan Z. Triterpenoid saponins with anti-inflammatory activity from Codonopsis lanceolata. Planta Med. 74: 1412-1415 (2008) https://doi.org/10.1055/s-2008-1081318
  55. Yuan Z, Syed MA, Panchal D, Rogers D, Joo M, Sadikot RT. Cur-cumin mediated epigenetic modulation inhibits TREM-1 expression in response to lipopolysaccharide. Int. J. Biochem. Cell Biol. 44: 2032-2043 (2012) https://doi.org/10.1016/j.biocel.2012.08.001
  56. Zhao R, Guo Z, Zhang R, Deng C, Xu J, Dong W, Hong Z, Yu H, Situ H, Liu C, Zhuang G. Nasal epithelial barrier disruption by particulate matter ≤2.5 ㎛ via tight junction protein degradation. J. Appl. Toxicol. 38: 678-687 (2018) https://doi.org/10.1002/jat.3573