Korean Journal of Medicinal Crop Science (한국약용작물학회지)

The Korean Society of Medicinal Crop Science (한국약용작물학회)
권호 표지
DOI QR코드

DOI QR Code

Respiratory Protective Effect of Salvia plebeia R. Br. Extracts against Ambient Particulate Matter-induced Airway Inflammation

미세먼지 유도 기도염증에 대한 배암차즈기 추출물의 호흡기 보호 효과

  • Song, Hyeongwoo (School of Biological Sciences and Technology, Chonnam National University) ;
  • Ji, Kon Young (School of Biological Sciences and Technology, Chonnam National University) ;
  • Kim, Bok Kyu (Institute of Traditional Medicine and Bioscience, Daejeon University) ;
  • Yang, Won Kyung (Institute of Traditional Medicine and Bioscience, Daejeon University) ;
  • Han, Chang Kyun (KT&G Research Institute) ;
  • Shin, Han Jae (KGC Research Institute) ;
  • Park, Yang Chun (Division of Respiratory System, Department of Internal Medicine, Daejeon University) ;
  • Hwang, Ji Sook (KOC Biotech) ;
  • Kang, Hyung Sik (School of Biological Sciences and Technology, Chonnam National University) ;
  • Kim, Seung Hyung (Institute of Traditional Medicine and Bioscience, Daejeon University)
  • 송형우 (전남대학교 생물과학.생명기술학부) ;
  • 지건영 (전남대학교 생물과학.생명기술학부) ;
  • 김복규 (대전대학교 동서생명과학연구원) ;
  • 양원경 (대전대학교 동서생명과학연구원) ;
  • 한창균 (KT&G 중앙연구원) ;
  • 신한재 (KGC 중앙연구원) ;
  • 박양춘 (대전대학교 폐계내과학교실) ;
  • 황지숙 (케이오씨바이오텍) ;
  • 강형식 (전남대학교 생물과학.생명기술학부) ;
  • 김승형 (대전대학교 동서생명과학연구원)
  • Received : 2017.08.18
  • Accepted : 2017.10.16
  • Published : 2017.10.30
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Small particles increase airway inflammation upon reaching the alveoli. Here, we investigated the protective or therapeutic effects of Salvia plebeia R. Br. (SP_R) extracts on airway inflammation. Methods and Results: To investigate the anti-inflammatory activity of SP_R extracts, we measured their inhibitory effect on the production of reactive oxygen species (ROS) expression of inflammatory mediators, and immune cell infiltration in MH-S alveolar macrophage cells and in the ambient particulate matter (APM)-exposed airway inflammation mice model. The SP_R extracts inhibited the production of ROS and expression of IL-4, IL-10, IL-15, and IL-17A mRNA in APM-stimulated MH-S cells. Oral administration of SP_R extracts suppressed APM-induced inflammatory symptoms, such as high alveolar wall thickness, excess collagen fibers, decreased mRNA expression of chemokines (Ccr9, Ccl5, Ccr3), inflammatory cytokines (IL-15, TNF-${\alpha}$), and IL-4 Th2 cytokine in the lung. The SP_R extracts also inhibited ROS production, granulocyte ($CD11b^+Gr-1^+$) infiltration, IL-17A, TNF-${\alpha}$, macrophage inflammatory protein (Mip-2), and chemokine (C-X-C motif) ligand 1 (Cxcl-1) production in the airway. The specific compounds in the SR-R extracts that mediate the anti-inflammatory effects were identified. Conclusions: In this study, SP_R extracts effectively inhibited airway inflammatory responses, such as ROS production and granulocyte infiltration into the airway, by regulating the expression of chemokines and inflammatory cytokines.

Keywords

References

  1. Ajuebor MN, Das AM, Virag L, Flower RJ, Szabo C and Perretti M. (1999). Role of resident peritoneal macrophages and mast cells in chemokine production and neutrophil migration in acute inflammation: Evidence for an inhibitory loop involving endogenous IL-10. The Journal of Immunology. 162:1685-1691.
  2. Akram M, Syed AS, Kim KA, Lee JS, Chang SY, Kim CY and Bae ON. (2015). Heme oxygenase 1-mediated novel antiinflammatory activities of Salvia plebeia and its active components. Journal of Ethnopharmacology. 174:322-330. https://doi.org/10.1016/j.jep.2015.08.028
  3. Amulic B, Cazalet C, Hayes GL, Metzler KD and Zychlinsky A. (2012). Neutrophil function: From mechanisms to disease. Annual Review of Immunology. 30:459-489. https://doi.org/10.1146/annurev-immunol-020711-074942
  4. Barnes PJ. (1994). Cytokines as mediators of chronic asthma. American Journal of Respiratory and Critical Care Medicine. 150:S42-S49. https://doi.org/10.1164/ajrccm/150.5_Pt_2.S42
  5. Bohadana AB, Massin N, Wild P, Toamain JP, Engel S and Goutet P. (2000). Symptoms, airway responsiveness, and exposure to dust in beech and oak wood workers. Occupational and Environmental Medicine. 57:268-273. https://doi.org/10.1136/oem.57.4.268
  6. Brandt EB, Kovacic MB, Lee GB, Gibson AM, Acciani TH, Le Cras TD, Ryan PH, Budelsky AL and Hershey GKK. (2013). Diesel exhaust particle induction of IL-17A contributes to severe asthma. Journal of Allergy and Clinical Immunology. 132:1194-1204. https://doi.org/10.1016/j.jaci.2013.06.048
  7. Choi BO, Yin HH, Fang CZ, Ha HO, Kim SJ, Jeong SJ and Jang SI. (2015). Synergistic anti-inflammatory effect of rosmarinic acid and luteolin in lipopolysaccharide-stimulated RAW264.7 macrophage cells. Korean Journal of Food Science and Technology. 47:119-125. https://doi.org/10.9721/KJFST.2015.47.1.119
  8. Choi JK, Oh HM, Lee S, Kwon TK, Shin TY, Rho MC and Kim SH. (2014). Salvia plebeia suppresses atopic dermatitislike skin lesions. The American Journal of Chinese Medicine. 42:967-985. https://doi.org/10.1142/S0192415X1450061X
  9. Choi SI, Cho IH, Han SH, Jeon YJ, Choi JG, Kim JS and Lee JH. (2016). Antiobesity effects of Salvia plebeia R. Br. extract in high-fat diet-induced obese mice. Journal of Medicinal Food. 19:1048-1056. https://doi.org/10.1089/jmf.2016.3763
  10. Costa RS, Carneiro TCB, Cerqueira-Lima AT, Queiroz NV, Alcantara-Neves NM, Pontes-de-Carvalho LC, Velozo Eda S, Oliveira EJ and Figueiredo CA. (2012). Ocimum gratissimum Linn. and rosmarinic acid, attenuate eosinophilic airway inflammation in an experimental model of respiratory allergy to Blomia tropicalis. International Immunopharmacology. 13:126-134. https://doi.org/10.1016/j.intimp.2012.03.012
  11. De Filippo K, Dudeck A, Hasenberg M, Nye E, van Rooijen N, Hartmann K, Gunzer M, Roers A and Hogg N. (2013). Mast cell and macrophage chemokines CXCL1/CXCL2 control the early stage of neutrophil recruitment during tissue inflammation. Blood. 121:4930-4937. https://doi.org/10.1182/blood-2013-02-486217
  12. Doeing DC and Solway J. (2013). Airway smooth muscle in the pathophysiology and treatment of asthma. Journal of Applied Physiology. 114:834-843. https://doi.org/10.1152/japplphysiol.00950.2012
  13. Fuks K, Moebus S, Hertel S, Viehmann A, Nonnemacher M, Dragano N, Mohlenkamp S, Jakobs H, Kessler C, Erbel R and Hoffmann B. (2011). Long-term urban particulate air pollution, traffic, noise and arterial blood pressure. Environmental Health Perspectives. 119:1706-1711. https://doi.org/10.1289/ehp.1103564
  14. Ghio AJ, Smith CB and Madden MC. (2012). Diesel exhaust particles and airway inflammation. Current Opinion in Pulmonary Medicine. 18:144-150. https://doi.org/10.1097/MCP.0b013e32834f0e2a
  15. Gu L and Weng X. (2001). Antioxidant activity and components of Salvia plebeia R. Br. a Chinese Herb. Food Chemistry. 73:299-305. https://doi.org/10.1016/S0308-8146(00)00300-9
  16. Hoffmann B, Weinmayr G, Hennig F, Fuks K, Moebus S, Weimar C, Dragano N, Hermann DM, Kalsch H, Mahabadi AA, Erbel R and Jockel KH. (2015). Air quality, stroke, and coronary events: Results of the heinz nixdorf recall study from the ruhr region. Deutsches Arzteblatt International. 112:195-201.
  17. Jang HH, Cho SY, Kim MJ, Kim JB, Lee SH, Lee MY and Lee YM. (2016). Anti-inflammatory effects of Salvia plebeia R. Br extract in vitro and in ovalbumin-induced mouse model. Biological Research. 49:41-51. https://doi.org/10.1186/s40659-016-0102-7
  18. Jang TY, Jung AY, Kyung TS, Kim DY, Hwang JH and Kim YH. (2017). Anti-allergic effect of luteolin in mice with allergic asthma and rhinitis. Central European Journal of Immunology. 42:24-29.
  19. Jin XF, Qian J and Lu YH. (2011). The role of hepatoprotective effect of a flavonoid-rich extracts of Salvia plebeia R. Br. on carbon tetrachloride-induced acute hepatic injury in mice. Journal of Medicinal Plants Research. 5:1558-1563.
  20. Jung JY, Jung SK, Jung HJ and Rhee HK. (2008). Microarray analysis of gene expression profile by treatment of Schizandrae fructus extract in inflammation-induced human epithelial A549 Cells. The Journal of Korean Oriental Internal Medicine. 29:543-553.
  21. Kim MH, Jung K, Nam KH, Jang HJ, Lee SW, Kim Y, Park CS, Lee TH, Park JH, Choi JH, Rho MC and Oh HM. (2016). Salvia plebeia R.Br. inhibits signal transduction of IL-6 and prevents ovariectomy-induced bone loss by suppressing osteoclastogenesis. Archives of Pharmacal Research. 39:1671-1681. https://doi.org/10.1007/s12272-016-0810-0
  22. Kim YJ, Jeong JS, Park NJ, Go GB and Son BG. (2014). Active ingredients and antioxidant activities of Salvia plebeia R. Br. according to pretreatment conditions. Journal of the Korean Society of Food Science and Nutrition. 43:1948-1953. https://doi.org/10.3746/jkfn.2014.43.12.1948
  23. Kolaczkowska E and Kubes P. (2013). Neutrophil recruitment and function in health and inflammation. Nature Reviews Immunology. 13:159-175. https://doi.org/10.1038/nri3399
  24. Korzh EV, Valutsina VM and Protsiuk RG. (1993). State of pulmonary surfactant and hemodynamics of lesser blood circulation in Donets Basin coal miners during development of dust-induced respiratory tract diseases. Meditsina Truda i Promyshlennaia Ekologiia. 3:26-28.
  25. Kyung SY, Kim YS, Kim WJ, Park MS, Song JW, Yum H, Yoon HK, Rhee CK and Jeong SH. (2015). Guideline for the prevention and management of particulate matter/Asian dust particle-induced adverse health effect on the patients with pulmonary diseases. Journal of the Korean Medical Association. 58:1060-1069. https://doi.org/10.5124/jkma.2015.58.11.1060
  26. Lee WC, Jung HA, Choi JS, Kim YS and Lee SM. (2011). Protective effects of luteolin against apoptotic liver damage induced by D-galactosamine/lipopolysaccharide in mice. Journal of Natural Productions. 74:1916-1921. https://doi.org/10.1021/np2003935
  27. Liang Z, Nie H, Xu Y, Peng J, Zeng Y, Wei Y, Wen X, Qiu J, Zhong W, Deng X and He J. (2016). Therapeutic effects of rosmarinic acid on airway responses in a murine model of asthma. International Immunopharmacology. 41:90-97. https://doi.org/10.1016/j.intimp.2016.10.010
  28. Lim HB and Kim SH. (2009). The effect of crude saponins of Korean red ginseng against airway inflammation and airway hyperresponsiveness induced by diesel exhaust particles in mice. Korean Journal of Medicinal Crop Science. 17:90-96.
  29. Lopez-Pacheco C, Soldevila G, Du Pont G, Hernandez-Pando R and Garcia-Zepeda EA. (2016). CCR9 is a key regulator of early phases of allergic airway inflammation. mediators of inflammation. 2016:3635809. http://dx.doi.org/10.1155/2016/3635809 (cited by 2016 Aug 8).
  30. Lu Y and Foo LY. (2002). Polyphenolics of salvia-a review. Phytochemistry. 59:117-140. https://doi.org/10.1016/S0031-9422(01)00415-0
  31. Manners S, Alam R, Schwartz DA and Gorska MM. (2014) A mouse model links asthma susceptibility to prenatal exposure to diesel exhaust. Journal of Allergy Clinical Immunology. 134:63-72. https://doi.org/10.1016/j.jaci.2013.10.047
  32. Nials AT and Uddin S. (2008). Mouse models of allergic asthma: Acute and chronic allergen challenge. Disease Models and Mechanisms. 1:213-220. https://doi.org/10.1242/dmm.000323
  33. Peters S, Reid A, Fritschi L, de Klerk N and Musk AW. (2013). Long-term effects of aluminium dust inhalation. Occupational and Environmental Medicine. 70:864-868. https://doi.org/10.1136/oemed-2013-101487
  34. Quinton LJ, Nelson S, Zhang P, Boe DM, Happel KI, Pan W and Bagby GJ. (2004). Selective transport of cytokine-induced neutrophil chemoattractant from the lung to the blood facilitates pulmonary neutrophil recruitment. American journal of physiology. Lung Cellular and Molecular Physiology. 286:L465-L472. https://doi.org/10.1152/ajplung.00153.2003
  35. Shin HJ, Gwak HM, Jang M, Park SH, Min HJ, Lee JM, Lee MY, Kim JH, Kim SW, Han CK and Kim SH. (2016). Antiinflammatory activity of three kinds of Salvia and its active compounds. Korean Journal of Medicinal Crop Science. 24:401-407. https://doi.org/10.7783/KJMCS.2016.24.5.401
  36. Talib WH, Zarga MH and Mahasneh AM. (2012). Antiproliferative, antimicrobial and apoptosis inducing effects of compounds isolated from Inula viscosa. Molecules. 17:3291-3303. https://doi.org/10.3390/molecules17033291
  37. Tosello Boari J, Amezcua Vesely MC, Bermejo DA, Ramello MC, Montes CL, Cejas H, Gruppi A and Acosta Rodriguez EV. (2012). IL-17RA signaling reduces inflammation and mortality during Trypanosoma cruzi infection by recruiting suppressive IL-10-producing neutrophils. PLoS Pathogens, 8: e1002658. http://doi.org/10.1371/journal.ppat.1002658 (cited by 2017 Sep 11).
  38. Yang JM, Hung CM, Fu CN, Lee JC, Huang CH, Yang MH, Lin CL, Kao JY and Way TD. (2010). Hispidulin sensitizes human ovarian cancer cells to TRAIL-induced apoptosis by AMPK activation leading to Mcl-1 block in translation. Journal of Agricultural and Food Chemistry. 58:10020-10026. https://doi.org/10.1021/jf102304g
  39. Yang SN, Hsieh CC, Kuo HF, Lee MS, Huang MY, Kuo CH and Hung CH. (2014). The effects of environmental toxins on allergic inflammation. Allergy Asthma Immunology Research. 6:478-484. https://doi.org/10.4168/aair.2014.6.6.478
  40. Yin Y, Gong FY, Wu XX, Sun Y, Li YH, Chen T and Xu Q. (2008). Anti-inflammatory and immunosuppressive effect of flavones isolated from Artemisia vestita. Journal of Ethnopharmacology. 120:1-6. https://doi.org/10.1016/j.jep.2008.07.029
  41. Yoshitaka I. (2007). Research on the quality distribution of JIS type-II fly ash in Japan. World of Coal Ash. www.flyash.info/2007/67ishikawa.pdf (cited by 2007 May 7).