Advertisement

Inflammation

, Volume 40, Issue 1, pp 184–194 | Cite as

NPS2143 Inhibits MUC5AC and Proinflammatory Mediators in Cigarette Smoke Extract (CSE)-Stimulated Human Airway Epithelial Cells

  • Jae-Won Lee
  • Ji-Won Park
  • Ok-Kyoung Kwon
  • Hee Jae Lee
  • Hye Gwang Jeong
  • Jae-Hong Kim
  • Sei-Ryang OhEmail author
  • Kyoung-Seop AhnEmail author
ORIGINAL ARTICLE

Abstract

Mucus overproduction is a fundamental hallmark of COPD that is caused by exposure to cigarette smoke. MUC5AC is one of the main mucin genes expressed in the respiratory epithelium, and its transcriptional upregulation often correlates with increased mucus secretion. Calcium-sensing receptor (CaSR) antagonists have been reported to possess anti-inflammatory effects. The purpose of the present study was to investigate the protective role of NPS2143, a selective CaSR antagonist on cigarette smoke extract (CSE)-stimulated NCI-H292 mucoepidermoid human lung cells. Treatment of NPS2143 significantly inhibited the expression of MUC5AC in CSE-stimulated H292 cells. NPS2143 reduced the expression of MMP-9 in CSE-stimulated H292 cells. NPS2143 also decreased the release of proinflammatory cytokines such as IL-6 and TNF-α in CSE-stimulated H292 cells. Furthermore, NPS2143 attenuated the activation of MAPKs (JNK, p38, and ERK) and inhibited the nuclear translocation of NF-κB in CSE-stimulated H292 cells. These results indicate that NPS2143 had a therapeutic potential in COPD.

KEY WORDS

chronic obstructive pulmonary disease cigarette smoke NPS2143 MUC5AC MAPKs NF-κB 

Abbreviations

CaSR

Calcium sensing receptor

COPD

Chronic obstructive pulmonary disease

CSE

Cigarette smoke extract

MUC5AC

Mucin 5AC

MMP-9

Matrix-metalloproteinase 9

IL-6

Interleukin 6

TNF-α

Tumor necrosis factor α

MAPKs

Mitogen-activated protein kinases

NF-κB

Nuclear factor-κB

Notes

Acknowledgments

This work was supported by a grant from the KRIBB Research Initiative Program (KGM 1221622) and the Ministry of Health and Welfare (HI14C1277) of the Republic of Korea.

References

  1. 1.
    Rycroft, C.E., A. Heyes, L. Lanza, and K. Becker. 2012. Epidemiology of chronic obstructive pulmonary disease: A literature review. International Journal of Chronic Obstructive Pulmonary Disease 7: 457–494. doi: 10.2147/COPD.S32330.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Vestbo, J., S.S. Hurd, A.G. Agusti, P.W. Jones, C. Vogelmeier, A. Anzueto, P.J. Barnes, L.M. Fabbri, F.J. Martinez, M. Nishimura, R.A. Stockley, D.D. Sin, and R. Rodriguez-Roisin. 2013. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. American Journal of Respiratory and Critical Care Medicine 187: 347–365. doi: 10.1164/rccm.201204-0596PP.CrossRefPubMedGoogle Scholar
  3. 3.
    Shin, I.S., N.R. Shin, J.W. Park, C.M. Jeon, J.M. Hong, O.K. Kwon, J.S. Kim, I.C. Lee, J.C. Kim, S.R. Oh, and K.S. Ahn. 2015. Melatonin attenuates neutrophil inflammation and mucus secretion in cigarette smoke-induced chronic obstructive pulmonary diseases via the suppression of Erk-Sp1 signaling. Journal of Pineal Research 58: 50–60. doi: 10.1111/jpi.12192.CrossRefPubMedGoogle Scholar
  4. 4.
    Chapman, K.R., D.M. Mannino, J.B. Soriano, P.A. Vermeire, A.S. Buist, M.J. Thun, C. Connell, A. Jemal, T.A. Lee, M. Miravitlles, S. Aldington, and R. Beasley. 2006. Epidemiology and costs of chronic obstructive pulmonary disease. European Respiratory Journal 27: 188–207. doi: 10.1183/09031936.06.00024505.CrossRefPubMedGoogle Scholar
  5. 5.
    Spurzem, J.R., and S.I. Rennard. 2005. Pathogenesis of COPD. Seminars in Respiratory and Critical Care Medicine 26: 142–153. doi: 10.1055/s-2005-869535.CrossRefPubMedGoogle Scholar
  6. 6.
    Gao, W., C. Yuan, J. Zhang, L. Li, L. Yu, C.H. Wiegman, P.J. Barnes, I.M. Adcock, M. Huang, and X. Yao. 2015. Klotho expression is reduced in COPD airway epithelial cells: Effects on inflammation and oxidant injury. Clinical Science (London) 129: 1011–1023. doi: 10.1042/CS20150273.CrossRefGoogle Scholar
  7. 7.
    Ehre, C., E.N. Worthington, R.M. Liesman, B.R. Grubb, D. Barbier, W.K. O’Neal, J.M. Sallenave, R.J. Pickles, and R.C. Boucher. 2012. Overexpressing mouse model demonstrates the protective role of Muc5ac in the lungs. Proceedings of the National Academy of Sciences of the United States of America 109: 16528–16533. doi: 10.1073/pnas.1206552109.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Caramori, G., C. Di Gregorio, I. Carlstedt, P. Casolari, I. Guzzinati, I.M. Adcock, P.J. Barnes, A. Ciaccia, G. Cavallesco, K.F. Chung, and A. Papi. 2004. Mucin expression in peripheral airways of patients with chronic obstructive pulmonary disease. Histopathology 45: 477–484. doi: 10.1111/j.1365-2559.2004.01952.x.CrossRefPubMedGoogle Scholar
  9. 9.
    Shin, I.S., J.W. Park, N.R. Shin, C.M. Jeon, O.K. Kwon, M.Y. Lee, H.S. Kim, J.C. Kim, S.R. Oh, and K.S. Ahn. 2014. Melatonin inhibits MUC5AC production via suppression of MAPK signaling in human airway epithelial cells. Journal of Pineal Research 56: 398–407. doi: 10.1111/jpi.12127.CrossRefPubMedGoogle Scholar
  10. 10.
    Papakonstantinou, E., G. Karakiulakis, S. Batzios, S. Savic, M. Roth, M. Tamm, and D. Stolz. 2015. Acute exacerbations of COPD are associated with significant activation of matrix metalloproteinase 9 irrespectively of airway obstruction, emphysema and infection. Respiratory Research 16: 78. doi: 10.1186/s12931-015-0240-4.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Abd El-Fatah, M.F., M.A. Ghazy, M.S. Mostafa, M.M. El-Attar, and A.O. Egiza. 2015. Identification of MMP-9 as a biomarker for detecting progression of chronic obstructive pulmonary disease. Biochemistry and Cell Biology 1–7. doi: 10.1139/bcb-2015-0073.
  12. 12.
    Chung, K.F. 2001. Cytokines in chronic obstructive pulmonary disease. The European Respiratory Journal Supplement 34: 50s–59s.CrossRefPubMedGoogle Scholar
  13. 13.
    Tanni, S.E., N.R. Pelegrino, A.Y. Angeleli, C. Correa, and I. Godoy. 2010. Smoking status and tumor necrosis factor-alpha mediated systemic inflammation in COPD patients. Journal of Inflammation (London) 7: 29. doi: 10.1186/1476-9255-7-29.CrossRefGoogle Scholar
  14. 14.
    Edwards, M.R., N.W. Bartlett, D. Clarke, M. Birrell, M. Belvisi, and S.L. Johnston. 2009. Targeting the NF-kappaB pathway in asthma and chronic obstructive pulmonary disease. Pharmacology and Therapeutics 121: 1–13. doi: 10.1016/j.pharmthera.2008.09.003.CrossRefPubMedGoogle Scholar
  15. 15.
    Kraft, M., K.B. Adler, J.L. Ingram, A.L. Crews, T.P. Atkinson, C.B. Cairns, D.C. Krause, and H.W. Chu. 2008. Mycoplasma pneumoniae induces airway epithelial cell expression of MUC5AC in asthma. European Respiratory Journal 31: 43–46. doi: 10.1183/09031936.00103307.CrossRefPubMedGoogle Scholar
  16. 16.
    Lee, J.W., N.R. Shin, J.W. Park, S.Y. Park, O.K. Kwon, H.S. Lee, J. Hee Kim, H.J. Lee, J. Lee, Z.Y. Zhang, S.R. Oh, and K.S. Ahn. 2015. Callicarpa japonica Thunb. attenuates cigarette smoke-induced neutrophil inflammation and mucus secretion. Journal of Ethnopharmacology 175: 1–8. doi: 10.1016/j.jep.2015.08.056.CrossRefPubMedGoogle Scholar
  17. 17.
    Nie, Y.C., H. Wu, P.B. Li, Y.L. Luo, C.C. Zhang, J.G. Shen, and W.W. Su. 2012. Characteristic comparison of three rat models induced by cigarette smoke or combined with LPS: to establish a suitable model for study of airway mucus hypersecretion in chronic obstructive pulmonary disease. Pulmonary Pharmacology & Therapeutics 25: 349–356. doi: 10.1016/j.pupt.2012.06.004.CrossRefGoogle Scholar
  18. 18.
    Wang, H.Y., X.Y. Liu, G. Han, Z.Y. Wang, X.X. Li, Z.M. Jiang, and C.M. Jiang. 2013. LPS induces cardiomyocyte injury through calcium-sensing receptor. Molecular and Cellular Biochemistry 379: 153–159. doi: 10.1007/s11010-013-1637-3.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Drueke, T.B. 2004. Modulation and action of the calcium-sensing receptor. Nephrology, Dialysis, Transplantation 19(Suppl 5): V20–V26. doi: 10.1093/ndt/gfh1052.CrossRefPubMedGoogle Scholar
  20. 20.
    Kos, C.H., A.C. Karaplis, J.B. Peng, M.A. Hediger, D. Goltzman, K.S. Mohammad, T.A. Guise, and M.R. Pollak. 2003. The calcium-sensing receptor is required for normal calcium homeostasis independent of parathyroid hormone. Journal of Clinical Investigation 111: 1021–1028. doi: 10.1172/JCI17416.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Lee, G.S., N. Subramanian, A.I. Kim, I. Aksentijevich, R. Goldbach-Mansky, D.B. Sacks, R.N. Germain, D.L. Kastner, and J.J. Chae. 2012. The calcium-sensing receptor regulates the NLRP3 inflammasome through Ca2+ and cAMP. Nature 492: 123–127. doi: 10.1038/nature11588.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Wu, C.L., Q.Y. Wu, J.J. Du, J.Y. Zeng, T.T. Li, C.Q. Xu, and Y.H. Sun. 2015. Calcium-sensing receptor in the T lymphocyte enhanced the apoptosis and cytokine secretion in sepsis. Molecular Immunology 63: 337–342. doi: 10.1016/j.molimm.2014.08.007.CrossRefPubMedGoogle Scholar
  23. 23.
    Tanday, S. 2015. Calcium-sensing receptors linked to development of asthma. The Lancet Respiratory Medicine 3: 428. doi: 10.1016/S2213-2600(15)00193-9.CrossRefPubMedGoogle Scholar
  24. 24.
    Yarova, P.L., A.L. Stewart, V. Sathish, R.D. Britt Jr., A.P.P.L. Thompson MA, M. Freeman, B. Aravamudan, H. Kita, S.C. Brennan, M. Schepelmann, T. Davies, S. Yung, Z. Cholisoh, E.J. Kidd, W.R. Ford, K.J. Broadley, K. Rietdorf, W. Chang, M.E. Bin Khayat, D.T. Ward, J.P.T.W. Corrigan CJ, P.J. Kemp, C.M. Pabelick, Y.S. Prakash, and D. Riccardi. 2015. Calcium-sensing receptor antagonists abrogate airway hyperresponsiveness and inflammation in allergic asthma. Science Translational Medicine 7: 284ra60. doi: 10.1126/scitranslmed.aaa0282.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Park, J.W., O.K. Kwon, J.H. Kim, S.R. Oh, J.H. Kim, J.H. Paik, B. Marwoto, R. Widjhati, F. Juniarti, D. Irawan, and K.S. Ahn. 2015. Rhododendron album Blume inhibits iNOS and COX-2 expression in LPS-stimulated RAW264.7 cells through the downregulation of NF-kappaB signaling. International Journal of Molecular Medicine 35: 987–994. doi: 10.3892/ijmm.2015.2107.PubMedGoogle Scholar
  26. 26.
    Liu, C., D. Weir, P. Busse, N. Yang, Z. Zhou, C. Emala, and X.M. Li. 2015. The flavonoid 7,4′-Dihydroxyflavone inhibits MUC5AC gene expression, production, and secretion via regulation of NF-kappaB, STAT6, and HDAC2. Phytotherapy Research 29: 925–932. doi: 10.1002/ptr.5334.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Caramori, G., P. Casolari, C. Di Gregorio, M. Saetta, S. Baraldo, P. Boschetto, K. Ito, L.M. Fabbri, P.J. Barnes, I.M. Adcock, G. Cavallesco, K.F. Chung, and A. Papi. 2009. MUC5AC expression is increased in bronchial submucosal glands of stable COPD patients. Histopathology 55: 321–331. doi: 10.1111/j.1365-2559.2009.03377.x.CrossRefPubMedGoogle Scholar
  28. 28.
    Cortijo, J., M. Mata, J. Milara, E. Donet, A. Gavalda, M. Miralpeix, and E.J. Morcillo. 2011. Aclidinium inhibits cholinergic and tobacco smoke-induced MUC5AC in human airways. European Respiratory Journal 37: 244–254. doi: 10.1183/09031936.00182009.CrossRefPubMedGoogle Scholar
  29. 29.
    Park, J.W., I.C. Lee, N.R. Shin, C.M. Jeon, O.K. Kwon, J.W. Ko, J.C. Kim, S.R. Oh, I.S. Shin, and K.S. Ahn. 2015. Copper oxide nanoparticles aggravate airway inflammation and mucus production in asthmatic mice via MAPK signaling. Nanotoxicology 1–8. doi: 10.3109/17435390.2015.1078851.
  30. 30.
    Ishikawa, N., N. Hattori, N. Kohno, A. Kobayashi, T. Hayamizu, and M. Johnson. 2015. Airway inflammation in Japanese COPD patients compared with smoking and nonsmoking controls. International Journal of Chronic Obstructive Pulmonary Disease 10: 185–192. doi: 10.2147/COPD.S74557.PubMedPubMedCentralGoogle Scholar
  31. 31.
    Lappalainen, U., J.A. Whitsett, S.E. Wert, J.W. Tichelaar, and K. Bry. 2005. Interleukin-1beta causes pulmonary inflammation, emphysema, and airway remodeling in the adult murine lung. American Journal of Respiratory Cell and Molecular Biology 32: 311–318. doi: 10.1165/rcmb.2004-0309OC.CrossRefPubMedGoogle Scholar
  32. 32.
    Broom, O.J., B. Widjaya, J. Troelsen, J. Olsen, and O.H. Nielsen. 2009. Mitogen activated protein kinases: A role in inflammatory bowel disease? Clinical and Experimental Immunology 158: 272–280. doi: 10.1111/j.1365-2249.2009.04033.x.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Park, J.W., I.S. Shin, U.H. Ha, J.H. Kim, and K.S. Ahn. 2015. Pathophysiological changes induced by pseudomonas aeruginosa infection are involved in MMP-12 and MMP-13 upregulation in human carcinoma epithelial cells and a pneumonia mouse model. Infection and Immunity. doi: 10.1128/IAI.00619-15.Google Scholar
  34. 34.
    Wu, Y.L., A.H. Lin, C.H. Chen, W.C. Huang, H.Y. Wang, M.H. Liu, T.S. Lee, and Y. Ru Kou. 2014. Glucosamine attenuates cigarette smoke-induced lung inflammation by inhibiting ROS-sensitive inflammatory signaling. Free Radical Biology and Medicine 69: 208–218. doi: 10.1016/j.freeradbiomed.2014.01.026.CrossRefPubMedGoogle Scholar
  35. 35.
    Binker, M.G., M.J. Binker-Cosen, D. Richards, A.A. Binker-Cosen, S.D. Freedman, and L.I. Cosen-Binker. 2015. Omega-3 PUFA docosahexaenoic acid decreases LPS-stimulated MUC5AC production by altering EGFR-related signaling in NCI-H292 cells. Biochemical and Biophysical Research Communications 463: 1047–1052. doi: 10.1016/j.bbrc.2015.06.056.CrossRefPubMedGoogle Scholar
  36. 36.
    Pera, T., A.B. Zuidhof, M. Smit, M.H. Menzen, T. Klein, G. Flik, J. Zaagsma, H. Meurs, and H. Maarsingh. 2014. Arginase inhibition prevents inflammation and remodeling in a guinea pig model of chronic obstructive pulmonary disease. Journal of Pharmacology and Experimental Therapeutics 349: 229–238. doi: 10.1124/jpet.113.210138.CrossRefPubMedGoogle Scholar
  37. 37.
    Yu, Q., X. Chen, X. Fang, Q. Chen, and C. Hu. 2015. Caveolin-1 aggravates cigarette smoke extract-induced MUC5AC secretion in human airway epithelial cells. International Journal of Molecular Medicine 35: 1435–1442. doi: 10.3892/ijmm.2015.2133.PubMedGoogle Scholar
  38. 38.
    Montalbano, A.M., G.D. Albano, G. Anzalone, A. Bonanno, L. Riccobono, C. Di Sano, R. Gagliardo, L. Siena, M.P. Pieper, M. Gjomarkaj, and M. Profita. 2014. Cigarette smoke alters non-neuronal cholinergic system components inducing MUC5AC production in the H292 cell line. European Journal of Pharmacology 736: 35–43. doi: 10.1016/j.ejphar.2014.04.022.CrossRefPubMedGoogle Scholar
  39. 39.
    Wang, G., Z. Xu, R. Wang, M. Al-Hijji, J. Salit, Y. Strulovici-Barel, A.E. Tilley, J.G. Mezey, and R.G. Crystal. 2012. Genes associated with MUC5AC expression in small airway epithelium of human smokers and non-smokers. BMC Medical Genomics 5: 21. doi: 10.1186/1755-8794-5-21.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Kanai, K., A. Koarai, Y. Shishikura, H. Sugiura, T. Ichikawa, T. Kikuchi, K. Akamatsu, T. Hirano, M. Nakanishi, K. Matsunaga, Y. Minakata, and M. Ichinose. 2015. Cigarette smoke augments MUC5AC production via the TLR3-EGFR pathway in airway epithelial cells. Respiratory Investigation 53: 137–148. doi: 10.1016/j.resinv.2015.01.007.CrossRefPubMedGoogle Scholar
  41. 41.
    Lee, H.J., H.S. Seo, J. Ryu, Y.P. Yoon, S.H. Park, and C.J. Lee. 2015. Luteolin inhibited the gene expression, production and secretion of MUC5AC mucin via regulation of nuclear factor kappa B signaling pathway in human airway epithelial cells. Pulmonary Pharmacology & Therapeutics 31: 117–122. doi: 10.1016/j.pupt.2014.09.008.CrossRefGoogle Scholar
  42. 42.
    Lee, S.U., M.H. Sung, H.W. Ryu, J. Lee, H.S. Kim, H.J. In, K.S. Ahn, H.J. Lee, H.K. Lee, D.H. Shin, Y. Lee, S.T. Hong, and S.R. Oh. 2015. Verproside inhibits TNF-alpha-induced MUC5AC expression through suppression of the TNF-alpha/NF-kappaB pathway in human airway epithelial cells. Cytokine. doi: 10.1016/j.cyto.2015.08.262.PubMedCentralGoogle Scholar
  43. 43.
    Mata, M., B. Sarria, A. Buenestado, J. Cortijo, M. Cerda, and E.J. Morcillo. 2005. Phosphodiesterase 4 inhibition decreases MUC5AC expression induced by epidermal growth factor in human airway epithelial cells. Thorax 60: 144–152. doi: 10.1136/thx.2004.025692.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Erle, D.J., and D. Sheppard. 2014. The cell biology of asthma. Journal of Cell Biology 205: 621–631. doi: 10.1083/jcb.201401050.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Lai, H., and D.F. Rogers. 2010. New pharmacotherapy for airway mucus hypersecretion in asthma and COPD: targeting intracellular signaling pathways. Journal of Aerosol Medicine and Pulmonary Drug Delivery 23: 219–231. doi: 10.1089/jamp.2009.0802.CrossRefPubMedGoogle Scholar
  46. 46.
    Cane, J.L., B. Mallia-Millanes, D.L. Forrester, A.J. Knox, C.E. Bolton, and S.R. Johnson. 2015. Matrix metalloproteinases -8 and -9 in the airways, blood and urine during exacerbations of COPD. Chronic Obstructive Pulmonary Disease 1–10. doi: 10.3109/15412555.2015.1043522.
  47. 47.
    Abd El-Fatah, M.F., M.A. Ghazy, M.S. Mostafa, M.M. El-Attar, and A. Osman. 2015. Identification of MMP-9 as a biomarker for detecting progression of chronic obstructive pulmonary disease. Biochemistry and Cell Biology 1–7. doi: 10.1139/bcb-2015-0073.
  48. 48.
    Higashimoto, Y., Y. Yamagata, S. Taya, T. Iwata, M. Okada, T. Ishiguchi, H. Sato, and H. Itoh. 2008. Systemic inflammation in chronic obstructive pulmonary disease and asthma: Similarities and differences. Respirology 13: 128–133. doi: 10.1111/j.1440-1843.2007.01170.x.PubMedGoogle Scholar
  49. 49.
    Gan, W.Q., S.F. Man, A. Senthilselvan, and D.D. Sin. 2004. Association between chronic obstructive pulmonary disease and systemic inflammation: A systematic review and a meta-analysis. Thorax 59: 574–580.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Guo, L., T. Wang, Y. Wu, Z. Yuan, J. Dong, X. Li, J. An, Z. Liao, X. Zhang, D. Xu, and F.Q. Wen. 2015. WNT/beta-catenin signaling regulates cigarette smoke-induced airway inflammation via the PPARdelta/p38 pathway. Laboratory Investigation. doi: 10.1038/labinvest.2015.101.Google Scholar
  51. 51.
    Pedroza, M., D.J. Schneider, H. Karmouty-Quintana, J. Coote, S. Shaw, R. Corrigan, J.G. Molina, J.L. Alcorn, D. Galas, R. Gelinas, and M.R. Blackburn. 2011. Interleukin-6 contributes to inflammation and remodeling in a model of adenosine mediated lung injury. PLoS One 6, e22667. doi: 10.1371/journal.pone.0022667.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Liu, W., Y. Liu, Z. Wang, T. Yu, Q. Lu, and H. Chen. 2015. Suppression of MAPK and NF-kappa B pathways by schisandrin B contributes to attenuation of DSS-induced mice model of inflammatory bowel disease. Pharmazie 70: 598–603.PubMedGoogle Scholar
  53. 53.
    Ma, W.J., Y.H. Sun, J.X. Jiang, X.W. Dong, J.Y. Zhou, and Q.M. Xie. 2015. Epoxyeicosatrienoic acids attenuate cigarette smoke extract-induced interleukin-8 production in bronchial epithelial cells. Prostaglandins, Leukotrienes, and Essential Fatty Acids 94: 13–19. doi: 10.1016/j.plefa.2014.10.006.CrossRefPubMedGoogle Scholar
  54. 54.
    Moon, H.G., Y. Zheng, C.H. An, Y.K. Kim, and Y. Jin. 2013. CCN1 secretion induced by cigarette smoking extracts augments IL-8 release from bronchial epithelial cells. PLoS One 8, e68199. doi: 10.1371/journal.pone.0068199.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Ng, D.S., W. Liao, W.S. Tan, T.K. Chan, X.Y. Loh, and W.S. Wong. 2014. Anti-malarial drug artesunate protects against cigarette smoke-induced lung injury in mice. Phytomedicine 21: 1638–1644. doi: 10.1016/j.phymed.2014.07.018.CrossRefPubMedGoogle Scholar
  56. 56.
    Monzon, M.E., R.M. Forteza, and S.M. Casalino-Matsuda. 2011. MCP-1/CCR2B-dependent loop upregulates MUC5AC and MUC5B in human airway epithelium. American Journal of Physiology - Lung Cellular and Molecular Physiology 300: L204–L215. doi: 10.1152/ajplung.00292.2010.CrossRefPubMedGoogle Scholar
  57. 57.
    Lee, H., J.R. Park, E.J. Kim, W.J. Kim, S.H. Hong, S.M. Park, and S.R. Yang. 2016. Cigarette smoke-mediated oxidative stress induces apoptosis via the MAPKs/STAT1 pathway in mouse lung fibroblasts. Toxicology Letters 240: 140–148. doi: 10.1016/j.toxlet.2015.10.030.CrossRefPubMedGoogle Scholar
  58. 58.
    Guo, L., T. Wang, Y. Wu, Z. Yuan, J. Dong, X. Li, J. An, Z. Liao, X. Zhang, D. Xu, and F.Q. Wen. 2016. WNT/beta-catenin signaling regulates cigarette smoke-induced airway inflammation via the PPARdelta/p38 pathway. Laboratory Investigation 96: 218–229. doi: 10.1038/labinvest.2015.101.CrossRefPubMedGoogle Scholar
  59. 59.
    Atkinson, J.J., B.A. Lutey, Y. Suzuki, H.M. Toennies, D.G. Kelley, D.K. Kobayashi, W.G. Ijem, G. Deslee, C.H. Moore, M.E. Jacobs, S.H. Conradi, D.S. Gierada, R.A. Pierce, T. Betsuyaku, and R.M. Senior. 2011. The role of matrix metalloproteinase-9 in cigarette smoke-induced emphysema. American Journal of Respiratory and Critical Care Medicine 183: 876–884. doi: 10.1164/rccm.201005-0718OC.CrossRefPubMedGoogle Scholar
  60. 60.
    Ogata, S., Y. Kubota, S. Satoh, S. Ito, H. Takeuchi, M. Ashizuka, and K. Shirasuna. 2006. Ca2+ stimulates COX-2 expression through calcium-sensing receptor in fibroblasts. Biochemical and Biophysical Research Communications 351: 808–814. doi: 10.1016/j.bbrc.2006.10.098.CrossRefPubMedGoogle Scholar
  61. 61.
    Schuliga, M. 2015. NF-kappaB signaling in chronic inflammatory airway disease. Biomolecules 5: 1266–1283. doi: 10.3390/biom5031266.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Lee, J.W., J.H. Kwon, M.S. Lim, H.J. Lee, S.S. Kim, S.Y. Lim, and W. Chun. 2014. 3,4,5-Trihydroxycinnamic acid increases heme-oxygenase-1 (HO-1) and decreases macrophage infiltration in LPS-induced septic kidney. Molecular and Cellular Biochemistry 397: 109–116. doi: 10.1007/s11010-014-2177-1.CrossRefPubMedGoogle Scholar
  63. 63.
    Shin, I.S., K.S. Ahn, N.R. Shin, H.J. Lee, H.W. Ryu, J.W. Kim, K.Y. Sohn, H.J. Kim, Y.H. Han, and S.R. Oh. 2016. Protective effect of EC-18, a synthetic monoacetyldiglyceride on lung inflammation in a murine model induced by cigarette smoke and lipopolysaccharide. International Immunopharmacology 30: 62–68. doi: 10.1016/j.intimp.2015.11.025.CrossRefPubMedGoogle Scholar
  64. 64.
    Fujisawa, T., S. Velichko, P. Thai, L.Y. Hung, F. Huang, and R. Wu. 2009. Regulation of airway MUC5AC expression by IL-1beta and IL-17A; the NF-kappaB paradigm. Journal of Immunology 183: 6236–6243. doi: 10.4049/jimmunol.0900614.CrossRefGoogle Scholar
  65. 65.
    Syed, D.N., F. Afaq, M.H. Kweon, N. Hadi, N. Bhatia, V.S. Spiegelman, and H. Mukhtar. 2007. Green tea polyphenol EGCG suppresses cigarette smoke condensate-induced NF-kappaB activation in normal human bronchial epithelial cells. Oncogene 26: 673–682. doi: 10.1038/sj.onc.1209829.CrossRefPubMedGoogle Scholar
  66. 66.
    Xue, H., K. Sun, W. Xie, G. Hu, H. Kong, Q. Wang, and H. Wang. 2012. Etanercept attenuates short-term cigarette-smoke-exposure-induced pulmonary arterial remodelling in rats by suppressing the activation of TNF-a/NF-kB signal and the activities of MMP-2 and MMP-9. Pulmonary Pharmacology & Therapeutics 25: 208–215.CrossRefGoogle Scholar
  67. 67.
    Rossol, M., M. Pierer, N. Raulien, D. Quandt, U. Meusch, K. Rothe, K. Schubert, T. Schoneberg, M. Schaefer, U. Krugel, S. Smajilovic, H. Brauner-Osborne, C. Baerwald, and U. Wagner. 2012. Extracellular Ca2+ is a danger signal activating the NLRP3 inflammasome through G protein-coupled calcium sensing receptors. Nature Communications 3: 1329. doi: 10.1038/ncomms2339.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Xi, Y.H., H.Z. Li, W.H. Zhang, L.N. Wang, L. Zhang, Y. Lin, S.Z. Bai, H.X. Li, L.Y. Wu, R. Wang, and C.Q. Xu. 2010. The functional expression of calcium-sensing receptor in the differentiated THP-1 cells. Molecular and Cellular Biochemistry 342: 233–240. doi: 10.1007/s11010-010-0489-3.CrossRefPubMedGoogle Scholar
  69. 69.
    Cifuentes, M., C. Fuentes, N. Tobar, I. Acevedo, E. Villalobos, E. Hugo, N. Ben-Jonathan, and M. Reyes. 2012. Calcium sensing receptor activation elevates proinflammatory factor expression in human adipose cells and adipose tissue. Molecular and Cellular Endocrinology 361: 24–30. doi: 10.1016/j.mce.2012.03.006.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Jae-Won Lee
    • 1
  • Ji-Won Park
    • 1
  • Ok-Kyoung Kwon
    • 1
    • 2
  • Hee Jae Lee
    • 3
  • Hye Gwang Jeong
    • 2
  • Jae-Hong Kim
    • 4
  • Sei-Ryang Oh
    • 1
    Email author
  • Kyoung-Seop Ahn
    • 1
    Email author
  1. 1.Natural Medicine Research Center, Korea Research Institute of Bioscience and BiotechnologyChungju-siRepublic of Korea
  2. 2.Department of Toxicology, College of PharmacyChungnam National UniversityDaejeonRepublic of Korea
  3. 3.Department of Pharmacology, College of MedicineKangwon National UniversityChuncheonRepublic of Korea
  4. 4.Department of Life Sciences and BiotechnologyKorea UniversitySeoulRepublic of Korea

Personalised recommendations